Abstract
The peritrophic matrix (PM) is an invertebrate intestinal lining, which partitions the midgut lumen into separate digestive compartments, lubricates the lumenal surface to protect from food abrasion, shields from invasion by pathogenic microorganisms and regulates immune responses. It is composed of chitin fibers cross-linked by chitin-binding PM proteins (PMPs) to form a three-dimensional meshwork with water-filled pores of distinct diameters. Various PMPs and other PM-associated proteins have been identified and several of them appear to be essential for maintaining the structural integrity and physiological function of the PM. The PMPs have chitin-binding domains (mostly ChtBD2) and frequently mucin-like linker domains that are more or less extensively O-glycosylated. The composition of PMPs largely determines the physicochemical properties of the PM, and the O-glycans of the mucin-like PMPs (also known as invertebrate intestinal mucins, IIMs) appear to be essential for lubrication and the control of exclusion sizes. Over the past years, much progress has been made in understanding the physiological function of the PM in digestion and innate immunity. This review aims to provide an overview on the insect PM with a particular focus on structure-function-relationships of the PM components.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abedi ZH, Brown AWA (1961) Peritrophic membrane as vehicle for DDT and DDE excretion in Aedes aegypti larvae. Ann Entomol Soc Am 54:539–542
Abraham EG, Jacobs-Lorena M (2004) Mosquito midgut barriers to malaria parasite development. Insect Biochem Mol Biol 34:667–671
Adang MJ, Spence KD (1983) Permeability of the peritrophic membrane of the Douglas fir tussock moth (Orgyia pseudotsugata). Comp Biochem Phys A 75:233–238
Agrawal S, Kelkenberg M, Begum K, Steinfeld L, Williams CE, Kramer KJ, Beeman RW, Park Y, Muthukrishnan S, Merzendorfer H (2014) Two essential peritrophic matrix proteins mediate matrix barrier functions in the insect midgut. Insect Biochem Mol Biol 49:24–34
Allahyari M, Bandani AR, Habibi-Rezaei M (2010) Subcellular fractionation of midgut cells of the sunn pest Eurygaster integriceps (Hemiptera: Scutelleridae): enzyme markers of microvillar and perimicrovillar membranes. J Insect Physiol 56:710–717
Alvarenga ES, Mansur JF, Justi SA, Figueira-Mansur J, Dos Santos VM, Lopez SG, Masuda H, Lara FA, Melo AC, Moreira MF (2015) Chitin is a component of the Rhodnius prolixus midgut. Insect Biochem Mol Biol. pii: S0965-1748(15)00070-3
Alves CR, Albuquerque-Cunha JM, Mello CB, Garcia ES, Nogueira NF, Bourguingnon SC, de Souza W, Azambuja P, Gonzalez MS (2007) Trypanosoma cruzi: attachment to perimicrovillar membrane glycoproteins of Rhodnius prolixus. Exp Parasitol 116:44–52
Arakane Y, Muthukrishnan S, Kramer KJ, Specht CA, Tomoyasu Y, Lorenzen MD, Kanost M, Beeman RW (2005) The Tribolium chitin synthase genes TcCHS1 and TcCHS2 are specialized for synthesis of epidermal cuticle and midgut peritrophic matrix. Insect Mol Biol 14:453–463
Arakane Y, Baguinon M, Jasrapuria S, Chaudhari S, Doyungan A, Kramer KJ, Muthukrishnan S, Beeman RW (2011) Two uridine-diphosphate N-acetylglucosamine pyrophosphorylases are critical for Tribolium castaneum molting, survival and fecundity. Insect Biochem Mol Biol 41:42–50
Asensio JL, Canada FJ, Bruix M, Gonzalez C, Khiar N, Rodriguez-Romero A, Jimenez-Barbero J (1998) NMR investigations of protein-carbohydrate interactions: refined three-dimensional structure of the complex between hevein and methyl beta-chitobioside. Glycobiology 8:569–577
Audsley N, Weaver RJ, Edwards JP (2001) In vivo effects of Manduca sexta allatostatin and allatotropin on larvae of the tomato moth, Lacanobia oleracea. Physiol Entomol 26:181–188
Azuma M, Harvey WR, Wieczorek H (1995) Stoichiometry of K+/H+ antiport helps to explain extracellular pH 11 in a model epithelium. FEBS Lett 361:153–156
Balbiani EG (1890) E’tudes anatomiques et histologiques sur le tube digestif des Crytops. Arch Zool Exp Gen 8:1–82
Barbehenn RV (2001) Roles of peritrophic membranes in protecting herbivorous insects from ingested plant allelochemicals. Arch Insect Biochem Physiol 47:86–99
Barbehenn RV, Martin MM (1995) Peritrophic envelope permeability in herbivorous insects. J Insect Physiol 41:303–311
Barbehenn RV, Stannard J (2004) Antioxidant defense of the midgut epithelium by the peritrophic envelope in caterpillars. J Insect Physiol 50:783–790
Barry MK, Triplett AA, Christensen AC (1999) A peritrophin-like protein expressed in the embryonic tracheae of Drosophila melanogaster. Insect Biochem Mol Biol 29:319–327
Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P, Ilagan O, Johnson S, Plaetinck G, Munyikwa T, Pleau M, Vaughn T, Roberts J (2007) Control of coleopteran insect pests through RNA interference. Nat Biotechnol 25:1322–1326
Becker B (1980) Effects of polyoxin D on in vitro synthesis of peritrophic membranes in Calliphora erythrocephala. Insect Biochem 10:101–106
Behr M, Hoch M (2005) Identification of the novel evolutionary conserved obstructor multigene family in invertebrates. FEBS Lett 579:6827–6833
Belles X (2010) Beyond Drosophila: RNAi in vivo and functional genomics in insects. Annu Rev Entomol 55:111–128
Berridge MJ (1970) A structural analysis of intestinal absorption. Symp R Entomol Soc Lond 5:135–150
Binnington KC (1988) Ultrastructure of the peritrophic membrane-secreting cells in the cardia of the blowfly, Lucilia cuprina. Tissue Cell 20:269–281
Bischoff DS, Slavicek JM (1997) Molecular analysis of an enhancin gene in the Lymantria dispar nuclear polyhedrosis virus. J Virol 71:8133–8140
Bolognesi R, Ribeiro AF, Terra WR, Ferreira C (2001) The peritrophic membrane of Spodoptera frugiperda: secretion of peritrophins and role in immobilization and recycling digestive enzymes. Arch Insect Biochem Physiol 47:62–75
Bolognesi R, Arakane Y, Muthukrishnan S, Kramer KJ, Terra WR, Ferreira C (2005) Sequences of cDNAs and expression of genes encoding chitin synthase and chitinase in the midgut of Spodoptera frugiperda. Insect Biochem Mol Biol 35:1249–1259
Bolognesi R, Terra WR, Ferreira C (2008) Peritrophic membrane role in enhancing digestive efficiency. Theoretical and experimental models. J Insect Physiol 54:1413–1422
Boucias D, Baniszewski J, Prompiboon P, Lietze V, Geden C (2015) Enhancement of the Musca domestica hytrosavirus infection with orally delivered reducing agents. J Invertebr Pathol 124:35–43
Boudko DY, Moroz LL, Harvey WR, Linser PJ (2001) Alkalinization by chloride/bicarbonate pathway in larval mosquito midgut. Proc Natl Acad Sci U S A 98:15354–15359
Boulter D, Edwards GA, Gatehouse AMR, Gatehouse JA, Hilder VA (1990) Additive protective effects of different plant-derived insect resistance genes in transgenic tobacco plants. Crop Prot 9:351–354
Brown SJ, Mahaffey JP, Lorenzen MD, Denell RE, Mahaffey JW (1999) Using RNAi to investigate orthologous homeotic gene function during development of distantly related insects. Evol Dev 1:11–15
Brown SJ, Denell RE, Beeman RW (2003) Beetling around the genome. Genet Res 82:155–161
Bucher G, Scholten J, Klingler M (2002) Parental RNAi in Tribolium (Coleoptera). Curr Biol 12:R85–R86
Burgos MH, Gutierrez LS (1976) The intestine of Triatoma infestans. I Cytology of the midgut. J Ultrastruct Res 57:1–9
Caldeira W, Dias AB, Terra WR, Ribeiro AF (2007) Digestive enzyme compartmentalization and recycling and sites of absorption and secretion along the midgut of Dermestes maculatus (Coleoptera) larvae. Arch Insect Biochem Physiol 64:1–18
Campbell PM, Cao AT, Hines ER, East PD, Gordon KH (2008) Proteomic analysis of the peritrophic matrix from the gut of the caterpillar, Helicoverpa armigera. Insect Biochem Mol Biol 38:950–958
Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active Enzymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37(Database issue):D233–D238
Cao J, Ibrahim H, Garcia J, Mason H, Granados R, Earle E (2002) Transgenic tobacco plants carrying a baculovirus enhancin gene slow the development and increase the mortality of Trichoplusia ni larvae. Plant Cell Rep 21:244–250
Casu R, Eisemann C, Pearson R, Riding G, East I, Donaldson A, Cadogan L, Tellam R (1997) Antibody-mediated inhibition of the growth of larvae from an insect causing cutaneous myiasis in a mammalian host. Proc Natl Acad Sci U S A 94:8939–8944
Ceasar SA, Ignacimuthu S (2012) Genetic engineering of crop plants for fungal resistance: role of antifungal genes. Biotechnol Lett 34:995–1002
Chaudhari SS, Arakane Y, Specht CA, Moussian B, Boyle DL, Park Y, Kramer KJ, Beeman RW, Muthukrishnan S (2011) Knickkopf protein protects and organizes chitin in the newly synthesized insect exoskeleton. Proc Natl Acad Sci U S A 108:17028–17033
Chen SJ, Chen NT, Wang SH, Hsu JC, Ding WH, Kuo-Huang LL, Huang RN (2009) Insecticidal action of mammalian galectin-1 against diamondback moth (Plutella xylostella). Pest Manag Sci 65:923–930
Clarke L, Temple GH, Vincent JF (1977) The effects of a chitin inhibitor-dimilin- on the production of peritrophic membrane in the locust, Locusta migratoria. J Insect Physiol 23:241–246
Cletus J, Balasubramanian V, Vashisht D, Sakthivel N (2013) Transgenic expression of plant chitinases to enhance disease resistance. Biotechnol Lett 35:1719–1732
Comper WD, Laurent TC (1978) Physiological functions of connective tissue polysaccharides. Physiol Rev 58:255–315
Corsaro BG, Gijzen M, Wang P, Granados RR (1993) Baculovirus enhancing proteins as determinants of viral pathogenesis. In: Beckage NE, Thompson SN, Federici BA (eds) Parasites and pathogens of insects, vol 2. Pathogens. Academic Press, New York, pp 127–145.
Coutinho-Abreu IV, Sharma NK, Robles-Murguia M, Ramalho-Ortigao M (2010) Targeting the midgut secreted PpChit1 reduces Leishmania major development in its natural vector, the sand fly Phlebotomus papatasi. PLoS Negl Trop Dis 4:e901
Cristofoletti PT, Ribeiro AF, Terra WR (2001) Apocrine secretion of amylase and exocytosis of trypsin along the midgut of Tenebrio molitor larvae. J Insect Physiol 47:143–155
Cristofoletti PT, Ribeiro AF, Deraison C, Rahbe Y, Terra WR (2003) Midgut adaptation and digestive enzyme distribution in a phloem feeding insect, the pea aphid Acyrthosiphon pisum. J Insect Physiol 49:11–24
D’Amico V, Slavicek J, Podgwaite JD, Webb R, Fuester R, Peiffer RA (2013) Deletion of v-chiA from a baculovirus reduces horizontal transmission in the field. Appl Environ Microbiol 79:4056–4064
Daimon T, Hamada K, Mita K, Okano K, Suzuki MG, Kobayashi M, Shimada T (2003) A Bombyx mori gene, BmChi-h, encodes a protein homologous to bacterial and baculovirus chitinases. Insect Biochem Mol Biol 33:749–759
de Maagd RA, Bravo A, Berry C, Crickmore N, Schnepf HE (2003) Structure, diversity, and evolution of protein toxins from spore-forming entomopathogenic bacteria. Annu Rev Genet 37:409–433
De Mets R, Jeuniaux C (1962) Composition of peritrophic membrane. Arch Int Physiol Biochim 70:93–96
Del Bene G, Dallai R, Marchini D (1991) Ultrastructure of the midgut and the adhering tubular salivary glands of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Int J Insect Morph Embryol 20:15–24
Derksen AC, Granados RR (1988) Alteration of a lepidopteran peritrophic membrane by baculoviruses and enhancement of viral infectivity. Virology 167:242–250
Dessens JT, Mendoza J, Claudianos C, Vinetz JM, Khater E, Hassard S, Ranawaka GR, Sinden RE (2001) Knockout of the rodent malaria parasite chitinase pbCHT1 reduces infectivity to mosquitoes. Infect Immun 69:4041–4047
Devenport M, Fujioka H, Donnelly-Doman M, Shen Z, Jacobs-Lorena M (2005) Storage and secretion of Ag-Aper14, a novel peritrophic matrix protein, and Ag-Muc1 from the mosquito Anopheles gambiae. Cell Tissue Res 320:175–185
Devenport M, Alvarenga PH, Shao L, Fujioka H, Bianconi ML, Oliveira PL, Jacobs-Lorena M (2006) Identification of the Aedes aegypti peritrophic matrix protein AeIMUCI as a heme-binding protein. Biochemistry 45:9540–9549
Di Maro A, Terracciano I, Sticco L, Fiandra L, Ruocco M, Corrado G, Parente A, Rao R (2010) Purification and characterization of a viral chitinase active against plant pathogens and herbivores from transgenic tobacco. J Biotechnol 147:1–6
Ding X, Gopalakrishnan B, Johnson LB, White FF, Wang X, Morgan TD, Kramer KJ, Muthukrishnan S (1998) Insect resistance of transgenic tobacco expressing an insect chitinase gene. Transgenic Res 7:77–84
Dinglasan RR, Devenport M, Florens L, Johnson JR, McHugh CA, Donnelly-Doman M, Carucci DJ, Yates JR 3rd, Jacobs-Lorena M (2009) The Anopheles gambiae adult midgut peritrophic matrix proteome. Insect Biochem Mol Biol 39:125–134
Dixit R, Arakane Y, Specht CA, Richard C, Kramer KJ, Beeman RW, Muthukrishnan S (2008) Domain organization and phylogenetic analysis of proteins from the chitin deacetylase gene family of Tribolium castaneum and three other species of insects. Insect Biochem Mol Biol 38:440–451
Dorner R, Peters W (1988) Localization of sugar components of glycoproteins in peritrophic membranes of larvae of Diptera (Culicidae, Simuliidae). Entomol Gen 14:11–24
Dow JAT (1981) Countercurrent flows, water movements and nutrient absorption in the locust midgut. J Insect Physiol 27:579–585
Dow JAT (1986) Insect midgut function. Adv Insect Physiol 19:188–328
Dow JAT (1992) pH gradients in lepidopteran midgut. J Exp Biol 172(Pt 1):355–375
Down RE, Gatehouse AMR, Hamilton WDO, Gatehouse JA (1996) Snowdrop lectin inhibits development and decreases fecundity of the Glasshouse Potato Aphid (Aulacorthum solani) when administered in vitro and via transgenic plants both in laboratory and glasshouse trials. J Insect Physiol 42:1035–1045
Drioli E, Gianfreda L, Palescandolo R, Scardi V (1976) The kinetic behaviour of enzymes gelified on ultrafiltration membranes. In: Thomas D, Kernevez JP (eds) Analysis and control of immobilised enzyme systems. North Holland Publications, Amsterdam
Edwards MJ, Jacobs-Lorena M (2000) Permeability and disruption of the peritrophic matrix and caecal membrane from Aedes aegypti and Anopheles gambiae mosquito larvae. J Insect Physiol 46:1313–1320
Eisemann CH, Donaldson RA, Pearson RD, Cadogan LC, Vuocolo T, Tellam RL (1994) Larvicidal activity of lectins on Lucilia cuprina: Mechanism of action. Ent Exp Appl 72:1–10
Eisemann C, Wijffels G, Tellam RL (2001) Secretion of the type 2 peritrophic matrix protein, peritrophin-15, from the cardia. Arch Insect Biochem Physiol 47:76–85
Elvin CM, Vuocolo T, Pearson RD, East IJ, Riding GA, Eisemann CH, Tellam RL (1996) Characterization of a major peritrophic membrane protein, peritrophin-44, from the larvae of Lucilia cuprina. cDNA and deduced amino acid sequences. J Biol Chem 271:8925–8935
Espinosa-Marzal RM, Fontani G, Reusch FB, Roba M, Spencer ND, Crockett R (2013) Sugars communicate through water: oriented glycans induce water structuring. Biophys J 104:2686–2694
Espinoza-Fuentes FP, Terra WR (1987) Physiological adaptations for digesting bacteria. Water fluxes and distribution of digestive enzymes in Musca domestica larval midgut. Insect Biochem 17:809–817
Espinoza-Fuentes FP, Ferreira C, Terra WR (1984) Spatial organization of digestion in the larval and imaginal stages of the sciarid fly Trichosia pubescens. Insect Biochem 14:631–638
Fang S, Wang L, Guo W, Zhang X, Peng D, Luo C, Yu Z, Sun M (2009) Bacillus thuringiensis bel protein enhances the toxicity of Cry1Ac protein to Helicoverpa armigera larvae by degrading insect intestinal mucin. Appl Environ Microbiol 75:5237–5243
Fazito do Vale V, Pereira MH, Gontijo NF (2007) Midgut pH profile and protein digestion in the larvae of Lutzomyia longipalpis (Diptera: Psychodidae). J Insect Physiol 53:1151–1159
Feng D, Chen Z, Wang Z, Zhang C, He K, Guo S (2015) Domain III of Bacillus thuringiensis Cry1Ie ioxin plays an important role in binding to peritrophic membrane of Asian corn borer. PLoS One 10:e0136430
Ferreira C, Terra WR (1989) Spatial organization of digestion, secretory mechanisms and digestive enzyme properties in Pheropsophus aequinoctialis (Coleoptera: Carabidae). Insect Biochem 19:383–391
Ferreira C, Ribeiro AF, Garcia ES, Terra WR (1988) Digestive enzymes trapped between and associated with the double plasma membranes of Rhodnius prolixus posterior midgut cells. Insect Biochem 18:521–530
Ferreira C, Capella AN, Sitnik R, Terra WR (1994a) Digestive enzymes in midgut cells, endo-and ectoperitrophic contents, and peritrophic membranes of Spodoptera frugiperda (lepidoptera) larvae. Arch Insect Biochem Physiol 26:299–313
Ferreira C, Capella AN, Sitnik R, Terra WR (1994b) Properties of the digestive enzymes and the permeability of the peritrophic membrane of Spodoptera frugiperda (Lepidoptera) larvae. Comp Biochem Physiol 107A:631–640
Ferreira AH, Cristofoletti PT, Lorenzini DM, Guerra LO, Paiva PB, Briones MR, Terra WR, Ferreira C (2007) Identification of midgut microvillar proteins from Tenebrio molitor and Spodoptera frugiperda by cDNA library screenings with antibodies. J Insect Physiol 53:1112–1124
Ferreira AH, Cristofoletti PT, Pimenta DC, Ribeiro AF, Terra WR, Ferreira C (2008) Structure, processing and midgut secretion of putative peritrophic membrane ancillary protein (PMAP) from Tenebrio molitor larvae. Insect Biochem Mol Biol 38:233–243
Fescemyer HW, Sandoya GV, Gill TA, Ozkan S, Marden JH, Luthe DS (2013) Maize toxin degrades peritrophic matrix proteins and stimulates compensatory transcriptome responses in fall armyworm midgut. Insect Biochem Mol Biol 43:280–291
Fitches E, Gatehouse JA (1998) A comparison of the short and long term effects of insecticidal lectins on the activities of soluble and brush border enzymes of tomato moth larvae (Lacanobia oleracea). J Insect Physiol 44:1213–1224
Fitches E, Audsley N, Gatehouse JA, Edwards JP (2002) Fusion proteins containing neuropeptides as novel insect contol agents: snowdrop lectin delivers fused allatostatin to insect haemolymph following oral ingestion. Insect Biochem Mol Biol 32:1653–1661
Fitches E, Wilkinson H, Bell H, Bown DP, Gatehouse JA, Edwards JP (2004) Cloning, expression and functional characterisation of chitinase from larvae of tomato moth (Lacanobia oleracea): a demonstration of the insecticidal activity of insect chitinase. Insect Biochem Mol Biol 34:1037–1050
Fitches EC, Bell HA, Powell ME, Back E, Sargiotti C, Weaver RJ, Gatehouse JA (2010) Insecticidal activity of scorpion toxin (ButaIT) and snowdrop lectin (GNA) containing fusion proteins towards pest species of different orders. Pest Manag Sci 66:74–83
Fitches EC, Pyati P, King GF, Gatehouse JA (2012) Fusion to snowdrop lectin magnifies the oral activity of insecticidal omega-Hexatoxin-Hv1a peptide by enabling its delivery to the central nervous system. PLoS One 7:e39389
Fonseca FV, Silva JR, Samuels RI, DaMatta RA, Terra WR, Silva CP (2010) Purification and partial characterization of a midgut membrane-bound alpha-glucosidase from Quesada gigas (Hemiptera: Cicadidae). Comp Biochem Phys B 155:20–25
Gaines PJ, Walmsley SJ, Wisnewski N (2003) Cloning and characterization of five cDNAs encoding peritrophin-A domains from the cat flea, Ctenocephalides felis. Insect Biochem Mol Biol 33:1061–1073
Gallo LG, Corsaro BG, Hughes PR, Granados RR (1991) In vivo enhancement of baculovirus infections by the viral enhancing factor of a granulosis virus of the cabbage looper, Trichoplusia ni (Lepidoptera: Noctuidae). J Invertebr Pathol 58:203–210
Galloway CS, Wang P, Winstanley D, Jones IM (2005) Comparison of the bacterial Enhancin-like proteins from Yersinia and Bacillus spp. with a baculovirus Enhancin. J Invertebr Pathol 90:134–137
Garbutt JS, Belles X, Richards EH, Reynolds SE (2013) Persistence of double-stranded RNA in insect hemolymph as a potential determiner of RNA interference success: evidence from Manduca sexta and Blattella germanica. J Insect Physiol 59:171–178
Garcia-Longoria L, Hellgren O, Bensch S (2014) Molecular identification of the chitinase genes in Plasmodium relictum. Malar J 13:239
Gatehouse AMR, Dewey FM, Dove J, Fenton KA, Pusztai A (1984) Effect of seed lectin from Phaeolus vulgaris on the development of larvae of Callosobruchus maculatus; mechanism of toxicity. J Sci Food Agric 35:373–380
Goto C (1990) Enhancement of a nuclear polyhedrosis virus (NPV) infection by a granulosis virus (GV) isolated from the spotted cutworm, Xestia c-nigrum L. (Lepidoptera: Noctuidae). Appl Entomol Zool 25:135–137
Granados RR, Corsaro BG (1990) Baculovirus enhancing proteins and their implication for insect control. In: Proceedings of the 5th international colloquium invertebrate pathology and microbial control, Adelaide, Australia, pp 174–178
Granados RR, Fu Y, Corsaro B, Hughes PR (2001) Enhancement of Bacillus thuringiensis Toxicity to Lepidopterous Species with the Enhancin from Trichoplusia ni Granulovirus. Biol Control 20:153–159
Guo W, Li G, Pang Y, Wang P (2005) A novel chitin-binding protein identified from the peritrophic membrane of the cabbage looper, Trichoplusia ni. Insect Biochem Mol Biol 35:1224–1234
Guo HF, Fang JC, Liu BS, Wang JP, Zhong WF, Wan FH (2007a) Enhancement of the biological activity of nucleopolyhedrovirus through disruption of the peritrophic matrix of insect larvae by chlorfluazuron. Pest Manag Sci 63:68–74
Guo HF, Fang JC, Wang JP, Zhong WF, Liu BS (2007b) Interaction of Xestia c-nigrum granulovirus with peritrophic matrix and Spodoptera litura nucleopolyhedrovirus in Spodoptera litura. J Econ Entomol 100:20–25
Hajaij-Ellouze M, Fedhila S, Lereclus D, Nielsen-LeRoux C (2006) The enhancin-like metalloprotease from the Bacillus cereus group is regulated by the pleiotropic transcriptional activator PlcR but is not essential for larvicidal activity. FEMS Microbiol Lett 260:9–16
Hao Z, Aksoy S (2002) Proventriculus-specific cDNAs characterized from the tsetse, Glossina morsitans morsitans. Insect Biochem Mol Biol 32:1663–1671
Hardingham TE, Fosang AJ (1992) Proteoglycans: many forms and many functions. FASEB J 6:861–870
Hardingham TE, Fosang AJ, Dudhia J (1990) Domain structure in aggregating proteoglycans from cartilage. Biochem Soc Trans 18:794–796
Harper MS, Granados RR (1999) Peritrophic membrane structure and formation of larval Trichoplusia ni with an investigation on the secretion patterns of a PM mucin. Tissue Cell 31:202–211
Harper MS, Hopkins TL (1997) Peritrophic membrane structure and secretion in European corn borer larvae (Ostrinia nubilalis). Tissue Cell 29:463–475
Harper MS, Hopkins TL, Czapla TH (1998) Effect of wheat germ agglutinin on formation and structure of the peritrophic membrane in European corn borer (Ostrinia nubilalis) larvae. Tissue Cell 30:166–176
Hawtin RE, Arnold K, Ayres MD, Zanotto PM, Howard SC, Gooday GW, Chappell LH, Kitts PA, King LA, Possee RD (1995) Identification and preliminary characterization of a chitinase gene in the Autographa californica nuclear polyhedrosis virus genome. Virology 212:673–685
Hawtin RE, Zarkowska T, Arnold K, Thomas CJ, Gooday GW, King LA, Kuzio JA, Possee RD (1997) Liquefaction of Autographa californica nucleopolyhedrovirus-infected insects is dependent on the integrity of virus-encoded chitinase and cathepsin genes. Virology 238:243–253
Hayakawa T, Shitomi Y, Miyamoto K, Hori H (2004) GalNAc pretreatment inhibits trapping of Bacillus thuringiensis Cry1Ac on the peritrophic membrane of Bombyx mori. FEBS Lett 576:331–335
Hegedus D, Baldwin D, O’Grady M, Braun L, Gleddie S, Sharpe A, Lydiate D, Erlandson M (2003) Midgut proteases from Mamestra configurata (Lepidoptera: Noctuidae) larvae: characterization, cDNA cloning, and expressed sequence tag analysis. Arch Insect Biochem Physiol 53:30–47
Hegedus D, Erlandson M, Gillott C, Toprak U (2009) New insights into peritrophic matrix synthesis, architecture, and function. Annu Rev Entomol 54:285–302
Herth W (1980) Calcofluor white and Congo red inhibit chitin microfibril assembly of Poterioochromonas: evidence for a gap between polymerization and microfibril formation. J Cell Biol 87:442–450
Hiramatsu S, Ishihara M, Fujie M, Usami S, Yamada T (1999) Expression of a chitinase gene and lysis of the host cell wall during Chlorella virus CVK2 infection. Virology 260:308–315
Hogenkamp DG, Arakane Y, Zimoch L, Merzendorfer H, Kramer KJ, Beeman RW, Kanost MR, Specht CA, Muthukrishnan S (2005) Chitin synthase genes in Manduca sexta: characterization of a gut-specific transcript and differential tissue expression of alternately spliced mRNAs during development. Insect Biochem Mol Biol 35:529–540
Hoover K, Humphries MA, Gendron AR, Slavicek JM (2010) Impact of viral enhancin genes on potency of Lymantria dispar multiple nucleopolyhedrovirus in L. dispar following disruption of the peritrophic matrix. J Invertebr Pathol 104:150–152
Hopkins TL, Harper MS (2001) Lepidopteran peritrophic membranes and effects of dietary wheat germ agglutinin on their formation and structure. Arch Insect Biochem Physiol 47:100–109
Hu X, Chen L, Xiang X, Yang R, Yu S, Wu X (2012) Proteomic analysis of peritrophic membrane (PM) from the midgut of fifth-instar larvae, Bombyx mori. Mol Biol Rep 39:3427–3434
Huber M, Cabib E, Miller LH (1991) Malaria parasite chitinase and penetration of the mosquito peritrophic membrane. Proc Natl Acad Sci U S A 88:2807–2810
Hukuhara T, Hayakawa T, Wijonarko A (1999) Increased baculovirus susceptibility of armyworm larvae feeding on transgenic rice plants expressing an entomopoxvirus gene. Nat Biotechnol 17:1122–1124
Ishimwe E, Hodgson JJ, Passarelli AL (2015) Expression of the Cydia pomonella granulovirus matrix metalloprotease enhances Autographa californica multiple nucleopolyhedrovirus virulence and can partially substitute for viral cathepsin. Virology 481:166–178
Ivanova N, Sorokin A, Anderson I, Galleron N, Candelon B, Kapatral V, Bhattacharyya A, Reznik G, Mikhailova N, Lapidus A, Chu L, Mazur M, Goltsman E, Larsen N, D’Souza M, Walunas T, Grechkin Y, Pusch G, Haselkorn R, Fonstein M, Ehrlich SD, Overbeek R, Kyrpides N (2003) Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature 423(6935):87–91
Jackson RL, Busch SJ, Cardin AD (1991) Glycosaminoglycans: molecular properties, protein interactions, and role in physiological processes. Physiol Rev 71:481–539
Jacobs-Lorena M, Oo M-M (1996) The peritrophic matrix of insects. In: Beaty BJ, Marquardt WC (eds) The biology of disease vectors. University Press of Colorado, Niwot, pp 318–332
Jang M-K, Kong B-G, Jeong Y-I, Lee CH, Nah JW (2004) Physicochemical characterization of α-chitin, β-chitin, and γ-chitin separated from natural resources. J Polym Sci A1(42):3423–3432
Jasrapuria S, Arakane Y, Osman G, Kramer KJ, Beeman RW, Muthukrishnan S (2010) Genes encoding proteins with peritrophin A-type chitin-binding domains in Tribolium castaneum are grouped into three distinct families based on phylogeny, expression and function. Insect Biochem Mol Biol 40:214–227
Jin S, Singh ND, Li L, Zhang X, Daniell H (2015) Engineered chloroplast dsRNA silences cytochrome p450 monooxygenase, V-ATPase and chitin synthase genes in the insect gut and disrupts Helicoverpa armigera larval development and pupation. Plant Biotechnol J 13:435–446
Johnson KS, Felton GW (1996) Physiological and dietary influences on midgut redox conditions in generalist lepidopteran larvae. J Insect Physiol 42:191–198
Jollès P, Muzzarelli RAA (1999) Chitin and Chitinases. Birkhauser Verlag, Basel
Jordao BP, Terra WR (1991) Regional distribution and substrate specificity of digestive enzymes involved in terminal digestion in Musca domestica hind-midguts. Arch Insect Biochem Physiol 17:157–168
Jordao BP, Lehane MJ, Terra WR, Ribeiro AF, Ferreira C (1996) An immunocytochemical investigation of trypsin secretion in the midgut of the stablefly, Stomoxys calcitrans. Insect Biochem Mol Biol 26:445–453
Jordao BP, Capella AN, Terra WR, Ribeiro AF, Ferreira C (1999) Nature of the anchors of membrane-bound aminopeptidase, amylase, and trypsin and secretory mechanisms in Spodoptera frugiperda (Lepidoptera) midgut cells. J Insect Physiol 45:29–37
Kabir KE, Sugimoto H, Tado H, Endo K, Yamanaka A, Tanaka S, Koga D (2006) Effect of Bombyx mori chitinase against Japanese pine sawyer (Monochamus alternatus) adults as a biopesticide. Biosci Biotechnol Biochem 70:219–229
Kang W, Tristem M, Maeda S, Crook NE, O’Reilly DR (1998) Identification and characterization of the Cydia pomonella granulovirus cathepsin and chitinase genes. J Gen Virol 79:2283–2292
Kato N, Mueller CR, Fuchs JF, Wessely V, Lan Q, Christensen BM (2006) Regulatory mechanisms of chitin biosynthesis and roles of chitin in peritrophic matrix formation in the midgut of adult Aedes aegypti. Insect Biochem Mol Biol 36:1–9
Kelkenberg M, Odman-Naresh J, Muthukrishnan S, Merzendorfer H (2015) Chitin is a necessary component to maintain the barrier function of the peritrophic matrix in the insect midgut. Insect Biochem Mol Biol 56:21–28
Khajuria C, Buschman LL, Chen M-S, Muthukrishnan S, Zhu KY (2010) A gut-specific chitinase gene essential for regulation of chitin content of peritrophic matrix and growth of Ostrinia nubilalis larvae. Insect Biochem Mol Biol 40:621–629
Kitajima EW (1975) A peculiar type of glycocalyx on the microvilli of the midgut epithelial cells of the thrips Frankliniella sp. (Thysanoptera: Thripidae). Cytobiologie 11:299–303
Kjellen L, Lindahl U (1991) Proteoglycans: structures and interactions. Annu Rev Biochem 60:443–475
Konno K, Hirayama C, Nakamura M, Tateishi K, Tamura Y, Hattori M, Kohno K (2004) Papain protects papaya trees from herbivorous insects: role of cysteine proteases in latex. Plant J 37:370–378
Kornfeld R, Kornfeld S (1985) Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem 54:631–664
Kramer KJ, Dziadik-Turner C, Koga D (1985) Chitin metabolism in insects. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry, and pharmacology, vol 3. Pergamon Press, Oxford, pp 75–115
Kramer KJ, Corpuz L, Choi HK, Muthukrishnan S (1993) Sequence of a cDNA and expression of the gene encoding epidermal and gut chitinases of Manduca sexta. Insect Biochem Mol Biol 23:691–701
Krishnan N, Kodrik D, Turanli F, Sehnal F (2007) Stage-specific distribution of oxidative radicals and antioxidant enzymes in the midgut of Leptinotarsa decemlineata. J Insect Physiol 53:67–74
Kuraishi T, Binggeli O, Opota O, Buchon N, Lemaitre B (2011) Genetic evidence for a protective role of the peritrophic matrix against intestinal bacterial infection in Drosophila melanogaster. Proc Natl Acad Sci U S A 108:15966–15971
Lane NJ, Harrison JB (1979) An unusual cell surface modification: a double plasma membrane. J Cell Sci 39:355–372
Lang M, Kanost MR, Gorman MJ (2012) Multicopper oxidase-3 is a laccase associated with the peritrophic matrix of Anopheles gambiae. PLoS One 7:e33985
Laurent TC (1964) The interaction between polysaccharides and other macromolecules. 9. The exclusion of molecules from hyaluronic acid gels and solutions. Biochem J 93:106–112
Laurent TC (1970) The structure and function of intercellular polysaccharides in connective tissue. In: Crone C, Lassen NA (eds) Capillary permeability. Copenhagen, p 681
Lawrence SD, Novak NG (2006) Expression of poplar chitinase in tomato leads to inhibition of development in colorado potato beetle. Biotechnol Lett 28:593–599
Lee RF (1968) The histology and histochemistry of the anterior midgut of Periplaneta americana (Dictyoptera: Blattidae) with reference to the formation of the peritrophic membrane. Proc R Entomol Soc Lond Ser 43A:122–134
Leetachewa S, Moonsom S, Chaisri U, Khomkhum N, Yoonim N, Wang P, Angsuthanasombat C (2013) Functional characterizations of residues Arg-158 and Tyr-170 of the mosquito-larvicidal toxic Bacillus thuringiensis Cry4Ba. BMB Rep 47(10):546–551
Lehane MJ (1976) Formation and histochemical structure of the peritrophic membrane in the stablefly, Stomoxys calcitrans. J Insect Physiol 22:1551–1557
Lehane MJ (1997) Peritrophic matrix structure and function. Annu Rev Entomol 42:525–550
Lehane MJ, Allingham PG, Weglicki P (1996) Composition of the peritrophic matrix of the tsetse fly, Glossina morsitans morsitans. Cell Tissue Res 283:375–384
Lepore LS, Roelvink PR, Granados RR (1996) Enhancin, the granulosis virus protein that facilitates nucleopolyhedrovirus (NPV) infections, is a metalloprotease. J Invertebr Pathol 68:131–140
Levy SM, Falleiros AM, Moscardi F, Gregorio EA (2011) The role of peritrophic membrane in the resistance of Anticarsia gemmatalis larvae (Lepidoptera: Noctuidae) during the infection by its nucleopolyhedrovirus (AgMNPV). Arthropod Struct Dev 40:429–434
Li F, Patra KP, Vinetz JM (2005) An anti-Chitinase malaria transmission-blocking single-chain antibody as an effector molecule for creating a Plasmodium falciparum-refractory mosquito. J Infect Dis 192:878–887
Li C, Song X, Li G, Wang P (2009) Midgut cysteine protease-inhibiting activity in Trichoplusia ni protects the peritrophic membrane from degradation by plant cysteine proteases. Insect Biochem Mol Biol 39:726–734
Lindsay KC, Marshall AT (1980) Ultrastructure of the filter chamber complex in the alimentary canal of Eurymela distincta Signoret (Homoptera: Eurymelydae). Int J Insect Morphol Embryol 15:211–224
Little D, Gouhier-Darimont C, Bruessow F, Reymond P (2007) Oviposition by pierid butterflies triggers defense responses in Arabidopsis. Plant Physiol 143:784–800
Liu M, Cai QX, Liu HZ, Zhang BH, Yan JP, Yuan ZM (2002) Chitinolytic activities in Bacillus thuringiensis and their synergistic effects on larvicidal activity. J Appl Microbiol 93:374–379
Lyonet P (1762) Trait’e Anatomique de la Chenille qui ronge le bois de Saule. La Haye, Holland
Macedo MLR, Damico DCS, Freire MDGM, Toyama MH, Marangoni S et al (2003) Purification and characterization of an N-acetylglucosamine-binding lectin from Koelreuteria paniculata seeds and its effect on the larval development of Callosobruchus maculatus (Coleoptera: Bruchidae) and Anagasta kuehniella (Lepidoptera: Pyralidae). J Agric Food Chem 51:2980–2986
Magalhaes T (2014) What is the association of heme aggregates with the peritrophic matrix of adult female mosquitoes? Parasit Vectors 7:362
Mantle M, Husar SD (1994) Binding of Yersinia enterocolitica to purified, native small intestinal mucins from rabbits and humans involves interactions with the mucin carbohydrate moiety. Infect Immun 62:1219–1227
Mao YB, Cai WJ, Wang JW, Hong GJ, Tao XY, Wang LJ, Huang YP, Chen XY (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat Biotechnol 25:1307–1313
Mao YB, Xue XY, Tao XY, Yang CQ, Wang LJ, Chen XY (2013) Cysteine protease enhances plant-mediated bollworm RNA interference. Plant Mol Biol 83:119–129
Marshall AT, Cheung WW (1970) Ultrastructure and cytochemistry of an extensive plexiform surface coat on the midgut cells of a fulgorid insect. J Ultrastruct Res 33:161–172
Marshall AT, Cheung WW (1974) Studies on water and ion transport in homopteran insects: ultrastructure and cytochemistry of the cicadoid and cercopoid Malpighian tubules and filter chamber. Tissue Cell 6:153–171
Martinez DS, Freire M, Mazzafera P, Araujo-Junior RT, Bueno RD, Macedo ML (2012) Insecticidal effect of labramin, a lectin-like protein isolated from seeds of the beach apricot tree, Labramia bojeri, on the Mediterranean flour moth, Ephestia kuehniella. J Insect Sci 12:62
Maue L, Meissner D, Merzendorfer H (2009) Purification of an active, oligomeric chitin synthase complex from the midgut of the tobacco hornworm. Insect Biochem Mol Biol 39:654–659
Mercer EH, Day MF (1952) The fine structure of the peritrophic membrane of certain insects. Biol Bull 103:384–394
Merzendorfer H (2006) Insect chitin synthases: a review. J Comp Physiol 176B:1–15
Merzendorfer H (2013) Chitin synthesis inhibitors: old molecules and new developments. Insect Sci 20:121–138
Merzendorfer H, Zimoch L (2003) Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases. J Exp Biol 206:4393–4412
Merzendorfer H, Kim HS, Chaudhari SS, Kumari M, Specht CA, Butcher S, Brown SJ, Robert Manak J, Beeman RW, Kramer KJ, Muthukrishnan S (2012) Genomic and proteomic studies on the effects of the insect growth regulator diflubenzuron in the model beetle species Tribolium castaneum. Insect Biochem Mol Biol 42:264–276
Miller N, Lehane MJ (1990) In vitro perfusion studies on the peritrophic membrane of the tsetse fly Glossina morsitans morsitans (Diptera, Glossinidae). J Insect Physiol 36:813–818
Miller N, Lehane MJ (1993) Ionic environment and the permeability properties of the peritrophic membrane of Glossina morsitans morsitans. J Insect Physiol 631:139–144
Mitsuhashi W, Miyamoto K (2003) Disintegration of the peritrophic membrane of silkworm larvae due to spindles of an entomopoxvirus. J Invertebr Pathol 82:34–40
Mitsuhashi W, Furuta Y, Sato M (1998) The spindles of an entomopoxvirus of coleoptera (Anomala cuprea) strongly enhance the infectivity of a nucleopolyhedrovirus in lepidoptera. J Invertebr Pathol 71:186–188
Mitsuhashi W, Kawakita H, Murakami R, Takemoto Y, Saiki T, Miyamoto K, Wada S (2007) Spindles of an entomopoxvirus facilitate its infection of the host insect by disrupting the peritrophic membrane. J Virol 81:4235–4243
Mitsuhashi W, Asano S, Miyamoto K, Wada S (2014) Further research on the biological function of inclusion bodies of Anomala cuprea entomopoxvirus, with special reference to the effect on the insecticidal activity of a Bacillus thuringiensis formulation. Pest Manag Sci 70:46–54
Moffatt MR, Blakemore D, Lehane MJ (1995) Studies on the synthesis and secretion of digestive trypsin in Stomoxys calcitrans (Insects, Diptera). Comp Biochem Physiol 110B:291–300
Mohan S, Ma PW, Pechan T, Bassford ER, Williams WP, Luthe DS (2006) Degradation of the S. frugiperda peritrophic matrix by an inducible maize cysteine protease. J Insect Physiol 52:21–28
Mohan S, Ma PW, Williams WP, Luthe DS (2008) A naturally occurring plant cysteine protease possesses remarkable toxicity against insect pests and synergizes Bacillus thuringiensis toxin. PLoS One 3:e1786
Moncayo AC, Lerdthusnee K, Leon R, Robich RM, Romoser WS (2005) Meconial peritrophic matrix structure, formation, and meconial degeneration in mosquito pupae/pharate adults: histological and ultrastructural aspects. J Med Entomol 42:939–944
Mooser H, Castaneda MR (1932) The multiplication of the virus of Mexican typhus fever in fleas. J Exp Med 55:307–323
Mori M, Kitamura H, Kondo A, Dohi K, Mori M, Kaido M, Mise K, Shimojyo E, Hashimoto Y (2006) Expression of an enhancin gene from the Trichoplusia ni granulosis virus confers resistance to lepidopterous insect pests to rice. Plant Biotechnol 23:55–61
Mury FB, da Silva JR, Ferreira LS, dos Santos FB, de Souza-Filho GA, de Souza-Neto JA, Ribolla PE, Silva CP, de Nascimento VV, Machado OL, Berbert-Molina MA, Dansa-Petretski M (2009) Alpha-glucosidase promotes hemozoin formation in a blood-sucking bug: an evolutionary history. PloS One 4:e6966
Nagadhara D, Ramesh S, Pasalu IC, Rao YK, Sarma NP, Reddy VD, Rao KV (2004) Transgenic rice plants expressing the snowdrop lectin gene (gna) exhibit high-level resistance to the whitebacked planthopper (Sogatella furcifera). Theor Appl Genet 109:1399–1405
Nakasu EY, Williamson SM, Edwards MG, Fitches EC, Gatehouse JA, Wright GA, Gatehouse AM (2014) Novel biopesticide based on a spider venom peptide shows no adverse effects on honeybees. Proc Biol Sci 281(1787):20140619
Neira Oviedo M, Vanekeris L, Corena-McLeod MD, Linser PJ (2008) A microarray-based analysis of transcriptional compartmentalization in the alimentary canal of Anopheles gambiae (Diptera: Culicidae) larvae. Insect Mol Biol 17:61–72
Nisizawa K, Yamaguchi T, Handa N, Maeda M, Yamazaki H (1963) Chemical nature of a uronic acid-containing polysaccharide in the peritrophic membrane of the silkworm. J Biochem 54:419–426
O’Loughlin GT, Chambers TC (1972) Extracellular microtubules in the aphid gut. J Cell Biol 53:575–578
Ohizumi Y, Gaidamashvili M, Ohwada S, Matsuda K, Kominami J, Nakamura-Tsuruta S, Hirabayashi J, Naganuma T, Ogawa T, Muramoto K (2009) Mannose-binding lectin from yam (Dioscorea batatas) tubers with insecticidal properties against Helicoverpa armigera (Lepidoptera: Noctuidae). J Agric Food Chem 57:2896–2902
Okolo CJ, Molyneux DH, Wallbanks KR, Maudlin I (1988) Fluorescein conjugated lectins identify different carbohydrate residues on Glossina peritrophic membranes. Trop Med Parasitol 39:208–210
Oliveira MF, Silva JR, Dansa-Petretski M, de Souza W, Lins U, Braga CM, Masuda H, Oliveira PL (1999) Haem detoxification by an insect. Nature 400:517–518
Oliveira MF, Gandara AC, Braga CM, Silva JR, Mury FB, Dansa-Petretski M, Menezes D, Vannier-Santos MA, Oliveira PL (2007) Heme crystallization in the midgut of triatomine insects. Comp Biochem Physiol 146:168–174
Oliveira CD, Tadei WP, Abdalla FC (2009) Occurrence of apocrine secretion in the larval gut epithelial cells of Aedes aegypti L., Anopheles albitarsis Lynch-Arribalzaga and Culex quinquefasciatus say (Diptera: Culicidae): a defense strategy against infection by Bacillus sphaericus Neide? Neotrop Entomol 38:624–631
Ono M, Kato S (1968) Amino acid composition of the peritrophic membrane in the silkworm, Bombyx mori L. Bull Sericult Exp Stn Jpn 23:1–8
Otsu Y, Mori H, Komuta K, Shimizu H, Nogawa S, Matsuda Y, Nonomura T, Sakuratani Y, Tosa Y, Mayama S, Toyoda H (2003) Suppression of leaf feeding and oviposition of phytophagous ladybird beetles (Coleoptera: Coccinellidae) by chitinase gene-transformed phylloplane bacteria and their specific bacteriophages entrapped in alginate gel beads. J Econ Entomol 96:555–563
Pascoa V, Oliveira PL, Dansa-Petretski M, Silva JR, Alvarenga PH, Jacobs-Lorena M, Lemos FJ (2002) Aedes aegypti peritrophic matrix and its interaction with heme during blood digestion. Insect Biochem Mol Biol 32:517–523
Pechan T, Cohen A, Williams WP, Luthe DS (2002) Insect feeding mobilizes a unique plant defense protease that disrupts the peritrophic matrix of caterpillars. Proc Natl Acad Sci U S A 99:13319–13323
Peel AD (2008) The evolution of developmental gene networks: lessons from comparative studies on holometabolous insects. Philos Trans R Soc Lond B Biol Sci 363:1539–1547
Peng J, Zhong J, Granados RR (1999) A baculovirus enhancin alters the permeability of a mucosal midgut peritrophic matrix from lepidopteran larvae. J Insect Physiol 45:159–166
Perez-Hedo M, Lopez C, Albajes R, Eizaguirre M (2012) Low susceptibility of non-target Lepidopteran maize pests to the Bt protein Cry1Ab. Bull Entomol Res 102:737–743
Perez-Vilar J, Hill RL (1999) The structure and assembly of secreted mucins. J Biol Chem 274:31751–31754
Perrone JB, Spielman A (1986) Microfilarial perforation of the midgut of a mosquito. J Parasitol 72:723–727
Peters W (1969) Vergleichende Untersuchungen der Feinstruktur peritrophischer Membranen von Insekten. Z Morphol Okol Tiere 64:21–58
Peters W (1992) Peritrophic membranes. vol 30. Zoophysiology. Springer, Berlin
Peters W, Kalnins M (1985) Aminopeptidases as immobilized enzymes on the peritrophic membranes of insects. Entomol Gener 11:25–32
Peters W, Latka I (1986) Electron microscopic localization of chitin using colloidal gold labelled with wheat germ agglutinin. Histochemistry 84:155–160
Peters W, Wiese B (1986) Permeability of the peritrophic membranes of some Diptera to labelled dextrans. J Insect Physiol 32:43–49
Peters W, Heitmann S, D’Haese J (1979) Formation and fine structure of peritrophic membranes in the earwig, Forficula auricularia. Entomol Gen 5:241–254
Pimenta PF, Modi GB, Pereira ST, Shahabuddin M, Sacks DL (1997) A novel role for the peritrophic matrix in protecting Leishmania from the hydrolytic activities of the sand fly midgut. Parasitology 115:359–369
Platzer-Schultz I, Welsch U (1969) Zur Entstehung und Feinstruktur der peritrophischen Membran der Larven von Chironomus strenzkei Fittkau (Diptera). Z Zellforsch Mikrosk Anat 100:594–605
Ponnudurai T, Billingsley PF, Rudin W (1988) Differential infectivity of Plasmodium for mosquitoes. Parasitol Today 4:319–321
Popham HJ, Bischoff DS, Slavicek JM (2001) Both Lymantria dispar nucleopolyhedrovirus enhancin genes contribute to viral potency. J Virol 75:8639–8648
Powell KS, Gatehouse AMR, Hilder VA, Gatehouse JA (1993) Antimetabolic effects of plants lectins and fungal enzymes on the nymphal stages of two important rice pests, Nilaparvata lugens and Nephotettix cinciteps. Entomol Exp Appl 66:119–126
Puchta O, Wille H (1956) A parasitic bacterium in the mid-intestine of Solenobia triquetrella. Zeitschrift fur Parasitenkunde 17:400–418
Pusztai A (1991) Plant lectins. Chemistry and pharmacology of natural products. Cambridge University Press, Cambridge
Quan G, Ladd T, Duan J, Wen F, Doucet D, Cusson M, Krell PJ (2013) Characterization of a spruce budworm chitin deacetylase gene: stage- and tissue-specific expression, and inhibition using RNA interference. Insect Biochem Mol Biol 43:683–691
Ramasamy MS, Kulasekera R, Wanniarachchi IC, Srikrishnaraj KA, Ramasamy R (1997) Interactions of human malaria parasites, Plasmodium vivax and P.falciparum, with the midgut of Anopheles mosquitoes. Med Vet Entomol 11:290–296
Ramos A, Mahowald A, Jacobs-Lorena M (1994) Peritrophic matrix of the black fly Simulium vittatum: formation, structure, and analysis of its protein components. J Exp Zool 268:269–281
Rao KV, Rathore KS, Hodges TK, Fu X, Stoger E, Sudhakar D, Williams S, Christou P, Bharathi M, Bown DP, Powell KS, Spence J, Gatehouse AM, Gatehouse JA (1998) Expression of snowdrop lectin (GNA) in transgenic rice plants confers resistance to rice brown planthopper. Plant J 15:469–477
Rao R, Fiandra L, Giordana B, de Eguileor M, Congiu T, Burlini N, Arciello S, Corrado G, Pennacchio F (2004) AcMNPV ChiA protein disrupts the peritrophic membrane and alters midgut physiology of Bombyx mori larvae. Insect Biochem Mol Biol 34:1205–1213
Rayms-Keller A, McGaw M, Oray C, Carlson JO, Beaty BJ (2000) Molecular cloning and characterization of a metal responsive Aedes aegypti intestinal mucin cDNA. Insect Mol Biol 9:419–426
Razek-Desouky A, Specht CA, Soong L, Vinetz JM (2001) Leishmania donovani: expression and characterization of Escherichia coli-expressed recombinant chitinase LdCHT1. Exp Parasitol 99:220–225
Read TD, Peterson SN, Tourasse N, Baillie LW, Paulsen IT, Nelson KE, Tettelin H, Fouts DE, Eisen JA, Gill SR, Holtzapple EK, Okstad OA, Helgason E, Rilstone J, Wu M, Kolonay JF, Beanan MJ, Dodson RJ, Brinkac LM, Gwinn M, DeBoy RT, Madpu R, Daugherty SC, Durkin AS, Haft DH, Nelson WC, Peterson JD, Pop M, Khouri HM, Radune D, Benton JL, Mahamoud Y, Jiang L, Hance IR, Weidman JF, Berry KJ, Plaut RD, Wolf AM, Watkins KL, Nierman WC, Hazen A, Cline R, Redmond C, Thwaite JE, White O, Salzberg SL, Thomason B, Friedlander AM, Koehler TM, Hanna PC, Kolsto AB, Fraser CM (2003) The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria. Nature 423(6935):81–86
Rees JS, Jarrett P, Ellar DJ (2009) Peritrophic membrane contribution to Bt Cry delta-endotoxin susceptibility in Lepidoptera and the effect of Calcofluor. J Invertebr Pathol 100:139–146
Reger JF (1971) Fine structure of the surface coat of midgut epithelial cells in the homopteran Phyllosclis atra (Fulgorid). J Submicrosc Cytol 3:353–358
Regev A, Keller M, Strizhov N, Sneh B, Prudovsky E, Chet I, Ginzberg I, Koncz-Kalman Z, Koncz C, Schell J, Zilberstein A (1996) Synergistic activity of a Bacillus thuringiensis delta-endotoxin and a bacterial endochitinase against Spodoptera littoralis larvae. Appl Environ Microbiol 62:3581–3586
Reymond P, Bodenhausen N, Van Poecke RM, Krishnamurthy V, Dicke M, Farmer EE (2004) A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16:3132–3147
Richards AG, Richards PA (1971) Origin and composition of the peritrophic membrane of the mosquito, Aedes aegypti. J Insect Physiol 17:2253–2275
Richards AG, Richards PA (1977) The peritrophic membranes of insects. Annu Rev Entomol 22:219–240
Robles-Murguia M, Bloedow N, Murray L, Ramalho-Ortigao M (2014) Effect of mouse antisera targeting the Phlebotomus papatasi midgut chitinase PpChit1 on sandfly physiology and fitness. Mem Inst Oswaldo Cruz 109:1064–1069
Rose C, Belmonte R, Armstrong SD, Molyneux G, Haines LR, Lehane MJ, Wastling J, Acosta-Serrano A (2014) An investigation into the protein composition of the teneral Glossina morsitans morsitans peritrophic matrix. PLoS Negl Trop Dis 8:e2691
Rudall KM, Kenchington W (1973) The chitin system. Biol Rev 48:597–636
Rudin W, Hecker H (1989) Lectin-binding sites in the midgut of the mosquitoes Anopheles stephensi Liston and Aedes aegypti L. (Diptera: Culicidae). Parasitol Res 75:268–279
Ryerse JS, Purcell JP, Sammons RD, Lavrik PB (1992) Peritrophic membrane structure and formation in the larva of a moth, Heliothis. Tissue Cell 24:751–771
Ryter SW, Tyrrell RM (2000) The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties. Free Radic Biol Med 28:289–309
Salvador R, Ferrelli ML, Sciocco-Cap A, Romanowski V (2014) Analysis of a chitinase from EpapGV, a fast killing betabaculovirus. Virus Genes 48:406–409
Sampson MN, Gooday GW (1998) Involvement of chitinases of Bacillus thuringiensis during pathogenesis in insects. Microbiology 144:2189–2194
Santos C, Terra WR (1986) Distribution and characterization of oligomeric digestive enzymes from Erinnyis ello larvae and inferences concerning secretory mechanisms and the permeability of the peritrophic membrane. Insect Biochem 16:691–700
Santos CD, Ribeiro AF, Ferreira C, Terra WR (1984) The larval midgut of the cassava hornworm (Erinnyis ello). Cell Tissue Res 237:565–574
Sarauer BL, Gillott C, Hegedus D (2003) Characterization of an intestinal mucin from the peritrophic matrix of the diamondback moth, Plutella xylostella. Insect Mol Biol 12:333–343
Sauvion N, Rahbé Y, Peumans WJ, Van Damme EJM, Gatehouse JA, Gatehouse AMR (1996) Effects of GNA and other mannose binding lectins on development and fecundity of the peach-potato aphid Myzus persicae. Entomol Exp Appl 79:285–293
Sauvion N, Nardon C, Febvay G, Gatehouse AM, Rahbe Y (2004) Binding of the insecticidal lectin Concanavalin A in pea aphid, Acyrthosiphon pisum (Harris) and induced effects on the structure of midgut epithelial cells. J Insect Physiol 50:1137–1150
Schlecht F (1979) Elektronenoptische Untersucghungen des Darmtraktes und der peritrophischen Membran von Cladoceren und Conchostracen (Phyllopoda, Crustacea). Zoomorphologie 92:161–181
Schlein Y, Jacobson RL, Shlomai J (1991) Chitinase secreted by Leishmania functions in the sandfly vector. Proc Biol Sci 245:121–126
Schmidt DD, Voelckel C, Hartl M, Schmidt S, Baldwin IT (2005) Specificity in ecological interactions: attack from the same lepidopteran herbivore results in species-specific transcriptional responses in two solanaceous host plants. Plant Physiol 138:1763–1773
Schorderet S, Pearson RD, Vuocolo T, Eisemann C, Riding GA, Tellam RL (1998) cDNA and deduced amino acid sequences of a peritrophic membrane glycoprotein, ‘peritrophin-48’, from the larvae of Lucilia cuprina. Insect Biochem Mol Biol 28:99–111
Selegny E (1974) Some systems coupling enzymic reactions and other phenomena: energy conversions. In: Selegny E (ed) Polyelectrolytes. Reidel Publ, Dordrecht, p 533
Shahabuddin M, Toyoshima T, Aikawa M, Kaslow DC (1993) Transmission-blocking activity of a chitinase inhibitor and activation of malarial parasite chitinase by mosquito protease. Proc Natl Acad Sci U S A 90:4266–4270
Shao L, Devenport M, Jacobs-Lorena M (2001) The peritrophic matrix of hematophagous insects. Arch Insect Biochem Physiol 47:119–125
Shao L, Devenport M, Fujioka H, Ghosh A, Jacobs-Lorena M (2005) Identification and characterization of a novel peritrophic matrix protein, Ae-Aper50, and the microvillar membrane protein, AEG12, from the mosquito, Aedes aegypti. Insect Biochem Mol Biol 35:947–959
Shen Z, Jacobs-Lorena M (1997) Characterization of a novel gut-specific chitinase gene from the human malaria vector Anopheles gambiae. J Biol Chem 272:28895–28900
Shen Z, Jacobs-Lorena M (1998) A type I peritrophic matrix protein from the malaria vector Anopheles gambiae binds to chitin. Cloning, expression, and characterization. J Biol Chem 273:17665–17670
Shen Z, Jacobs-Lorena M (1999) Evolution of chitin-binding proteins in invertebrates. J Mol Evol 48:341–347
Shi X, Chamankhah M, Visal-Shah S, Hemmingsen SM, Erlandson M, Braun L, Alting-Mees M, Khachatourians GG, O’Grady M, Hegedus DD (2004) Modeling the structure of the type I peritrophic matrix: characterization of a Mamestra configurata intestinal mucin and a novel peritrophin containing 19 chitin binding domains. Insect Biochem Mol Biol 34:1101–1115
Shibata T, Maki K, Hadano J, Fujikawa T, Kitazaki K, Koshiba T, Kawabata S (2015) Crosslinking of a peritrophic matrix protein protects gut epithelia from bacterial exotoxins. PLoS Pathog 11:e1005244
Silva CP, Terra WR (1995) An α-glucosidase from perimicrovillar membranes of Dysdercus peruvianus (Hemiptera: Pyrrhocoridae) midgut cells. Purification and properties. Insect Biochem Mol Biol 25:487–494
Silva CP, Ribeiro AF, Terra WR (1996) Enzyme markers and isolation of the microvillar and perimicrovillar membranes of Dysdercus peruvianus (Hemiptera: Pyrrhocoridae) midgut cells. Insect Biochem Mol Biol 26:1011–1018
Silva CP, Silva JR, Vasconcelos FF, Petretski MD, Damatta RA, Ribeiro AF, Terra WR (2004) Occurrence of midgut perimicrovillar membranes in paraneopteran insect orders with comments on their function and evolutionary significance. Arthropod Struct Develop 33:139–148
Silva JR, Mury FB, Oliveira MF, Oliveira PL, Silva CP, Dansa-Petretski M (2007) Perimicrovillar membranes promote hemozoin formation into Rhodnius prolixus midgut. Insect Biochem Mol Biol 37:523–531
Silva W, Cardoso C, Ribeiro AF, Terra WR, Ferreira C (2013) Midgut proteins released by microapocrine secretion in Spodoptera frugiperda. J Insect Physiol 59:70–80
Slavicek JM, Popham HJ (2005) The Lymantria dispar nucleopolyhedrovirus enhancins are components of occlusion-derived virus. J Virol 79:10578–10588
Smith CJ, Kaper JB, Mack DR (1995) Intestinal mucin inhibits adhesion of human enteropathogenic Escherichia coli to HEp-2 cells. J Pediatr Gastroenterol Nutr 21:269–276
Sneh B, Schuster S, Gross S (1983) Improvement of the insecticidal activity of Bacillus thuringiensis var. entomocidus on larvae of Spodoptera littoralis (Lepidoptera, Noctuidae) by addition of chitinolytic bacteria, a phagostimulant and a UV-protectant. Z Angew Entomol 96:77–83
Sola RJ, Griebenow K (2009) Effects of glycosylation on the stability of protein pharmaceuticals. J Pharm Sci 98:1223–1245
Stamm B, D’Haese J, Peters W (1978) SDS gel electrophoresis of proteins and glycoproteins from peritrophic membranes of some Diptera. J Insect Physiol 24:1–8
Stoltz DB, Summers MD (1971) Pathway of infection of mosquito iridescent virus. I. Preliminary observations on the fate of ingested virus. J Virol 8:900–909
Sudha PM, Muthu SP (1988) Damage to the midgut epithelium caused by food in the absence of peritrophic membrane. Curr Sci 57:624–625
Summers CB, Felton GW (1996) Peritrophic envelope as a functional antioxidant. Arch Insect Biochem Physiol 32:131–142
Sutherland DR, Christensen BM, Lasee BA (1986) Midgut barrier as a possible factor in filarial worm vector competency in Aedes trivittatus. J Invertebr Pathol 47:1–7
Tajne S, Boddupally D, Sadumpati V, Vudem DR, Khareedu VR (2014) Synthetic fusion-protein containing domains of Bt Cry1Ac and Allium sativum lectin (ASAL) conferred enhanced insecticidal activity against major lepidopteran pests. J Biotechnol 171:71–75
Takemoto Y, Mitsuhashi W, Murakami R, Konishi H, Miyamoto K (2008) The N-terminal region of an entomopoxvirus fusolin is essential for the enhancement of peroral infection, whereas the C-terminal region is eliminated in digestive juice. J Virol 82:12406–12415
Takesue Y, Yokota K, Miyajima S, Taguchi R, Ikezawa H (1989) Membrane anchors of alkaline phosphatase and trehalase associated with the plasma membrane of larval midgut epithelial cells of the silkworm, Bombyx mori. J Biochem 105:998–1001
Tanada Y (1959) Synergism between two viruses of the armyworm Pseudaletia unipuncta (Haworth) (Lepidoptera, Noctuidae). J Insect Pathol:215–231
Tellam RL, Eisemann C (2000) Chitin is only a minor component of the peritrophic matrix from larvae of Lucilia cuprina. Insect Biochem Mol Biol 30:1189–1201
Tellam RL, Wijffels G, Willadsen P (1999) Peritrophic matrix proteins. Insect Biochem Mol Biol 29:87–101
Tellam RL, Vuocolo T, Eisemann C, Briscoe S, Riding G, Elvin C, Pearson R (2003) Identification of an immuno-protective mucin-like protein, peritrophin-55, from the peritrophic matrix of Lucilia cuprina larvae. Insect Biochem Mol Biol 33:239–252
Terenius O, Papanicolaou A, Garbutt JS, Eleftherianos I, Huvenne H, Kanginakudru S, Albrechtsen M, An C, Aymeric JL, Barthel A, Bebas P, Bitra K, Bravo A, Chevalier F, Collinge DP, Crava CM, de Maagd RA, Duvic B, Erlandson M, Faye I, Felfoldi G, Fujiwara H, Futahashi R, Gandhe AS, Gatehouse HS, Gatehouse LN, Giebultowicz JM, Gomez I, Grimmelikhuijzen CJ, Groot AT, Hauser F, Heckel DG, Hegedus DD, Hrycaj S, Huang L, Hull JJ, Iatrou K, Iga M, Kanost MR, Kotwica J, Li C, Li J, Liu J, Lundmark M, Matsumoto S, Meyering-Vos M, Millichap PJ, Monteiro A, Mrinal N, Niimi T, Nowara D, Ohnishi A, Oostra V, Ozaki K, Papakonstantinou M, Popadic A, Rajam MV, Saenko S, Simpson RM, Soberon M, Strand MR, Tomita S, Toprak U, Wang P, Wee CW, Whyard S, Zhang W, Nagaraju J, Ffrench-Constant RH, Herrero S, Gordon K, Swevers L, Smagghe G (2011) RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. J Insect Physiol 57:231–245
Terra WR (1988) Physiology and biochemistry of insect digestion: an evolutionary perspective. Braz J Med Biol Res 21:675–734
Terra WR (1990) Evolution of digestive systems of insects. Annu Rev Entomol 35:181–200
Terra WR (2001) The origin and functions of the insect peritrophic membrane and peritrophic gel. Arch Insect Biochem Physiol 47:47–61
Terra WR, Ferreira C (1981) The physiological role of the peritrophic membrane and trehalase: Digestive enzymes in the midgut and excreta of starved larvae of Rhynchosciara. J Insect Physiol 27:325–331
Terra WR, Ferreira C (1983) Further evidence that enzymes involved in the final stages of digestion by Rhynchosciara do not enter the endoperitrophic space. Insect Biochem 13:143–150
Terra WR, Ferreira C, De Bianchi AG (1979) Distribution of digestive enzymes among the endo- and ectoperitrophic spaces and midgut cells of Rhynchosciara and its physiological significance. J Insect Physiol 25:487–494
Terra WR, Espinoza-Fuentes FP, Ribeiro AF, Ferreira C (1988) The larval midgut of the housefly (Musca domestica): Ultrastructure, fluid fluxes and ion secretion in relation to the organization of digestion. J Insect Physiol 34:463–472
Terra WR, Costa RH, Ferreira C (2006) Plasma membranes from insect midgut cells. An Acad Bras Cienc 78:255–269
Tetreau G, Dittmer NT, Cao X, Agrawal S, Chen YR, Muthukrishnan S, Haobo J, Blissard GW, Kanost MR, Wang P (2015) Analysis of chitin-binding proteins from Manduca sexta provides new insights into evolution of peritrophin A-type chitin-binding domains in insects. Insect Biochem Mol Biol 62:127–141
Thamthiankul S, Moar WJ, Miller ME, Panbangred W (2004) Improving the insecticidal activity of Bacillus thuringiensis subsp. aizawai against Spodoptera exigua by chromosomal expression of a chitinase gene. Appl Microbiol Biotechnol 65:183–192
Toprak U, Baldwin D, Erlandson M, Gillott C, Hou X, Coutu C, Hegedus DD (2008) A chitin deacetylase and putative insect intestinal lipases are components of the Mamestra configurata (Lepidoptera: Noctuidae) peritrophic matrix. Insect Mol Biol 17:573–585
Toprak U, Baldwin D, Erlandson M, Gillott C, Hegedus DD (2010) Insect intestinal mucins and serine proteases associated with the peritrophic matrix from feeding, starved and moulting Mamestra configurata larvae. Insect Mol Biol 19:163–175
Toprak U, Harris S, Baldwin D, Theilmann D, Gillott C, Hegedus DD, Erlandson MA (2012) Role of enhancin in Mamestra configurata nucleopolyhedrovirus virulence: selective degradation of host peritrophic matrix proteins. J Gen Virol 93:744–753
Toprak U, Baldwin D, Erlandson M, Gillott C, Harris S, Hegedus DD (2013) In vitro and in vivo application of RNA interference for targeting genes involved in peritrophic matrix synthesis in a lepidopteran system. Insect Sci 20:92–100
Toprak U, Hegedus DD, Baldwin D, Coutu C, Erlandson M (2014) Spatial and temporal synthesis of Mamestra configurata peritrophic matrix through a larval stadium. Insect Biochem Mol Biol 54:89–97
Toprak U, Erlandson M, Baldwin D, Karcz S, Wan L, Coutu C, Gillott C, Hegedus DD (2015) Identification of the Mamestra configurata (Lepidoptera: Noctuidae) peritrophic matrix proteins and enzymes involved in peritrophic matrix chitin metabolism. Insect Sci. doi:10.1111/1744-7917.12225
Tristram JN (1977) Normal and cocoon-forming peritrophic membrane in larvae of the beetle Gibbium psylloides. J Insect Physiol 23:79–87
Tristram JN (1978) The peritrophic membrane and cocoon ribbons in larvae of Cionus scrophulariae. J Insect Physiol 24:391–398
Tsai YL, Hayward RE, Langer RC, Fidock DA, Vinetz JM (2001) Disruption of Plasmodium falciparum chitinase markedly impairs parasite invasion of mosquito midgut. Infect Immun 69:4048–4054
Tse SK, Chadee K (1991) The interaction between intestinal mucus glycoproteins and enteric infections. Parasitol Today 7:163–172
Vandenborre G, Groten K, Smagghe G, Lannoo N, Baldwin IT, Van Damme EJ (2010) Nicotiana tabacum agglutinin is active against Lepidopteran pest insects. J Exp Bot 61:1003–1014
Venancio TM, Cristofoletti PT, Ferreira C, Verjovski-Almeida S, Terra WR (2009) The Aedes aegypti larval transcriptome: a comparative perspective with emphasis on trypsins and the domain structure of peritrophins. Insect Mol Biol 18:33–44
Vieira CM, Tuelher ES, Valicente FH, Wolff JL (2012) Characterization of a Spodoptera frugiperda multiple nucleopolyhedrovirus isolate that does not liquefy the integument of infected larvae. J Invertebr Pathol 111:189–192
Vinetz JM (2005) Plasmodium ookinete invasion of the mosquito midgut. Curr Top Microbiol Immunol 295:357–382
Vinokurov KS, Elpidina EN, Zhuzhikov DP, Oppert B, Kodrik D, Sehnal F (2009) Digestive proteolysis organization in two closely related Tenebrionid beetles: red flour beetle (Tribolium castaneum) and confused flour beetle (Tribolium confusum). Arch Insect Biochem Physiol 70:254–279
Vuocolo T, Eisemann CH, Pearson RD, Willadsen P, Tellam RL (2001) Identification and molecular characterisation of a peritrophin gene, peritrophin-48, from the myiasis fly Chrysomya bezziana. Insect Biochem Mol Biol 31:919–932
Walker VK, Geer W, Williamson JH (1980) Dietary modulation and histochemical localisation of leucine aminopeptidase activity in Drosophila melanogaster. Insect Biochem 10:543–548
Walski T, Van Damme EJ, Smagghe G (2014) Penetration through the peritrophic matrix is a key to lectin toxicity against Tribolium castaneum. J Insect Physiol 70:94–101
Wang P, Granados RR (1997a) An intestinal mucin is the target substrate for a baculovirus enhancin. Proc Natl Acad Sci U S A 94:6977–6982
Wang P, Granados RR (1997b) Molecular cloning and sequencing of a novel invertebrate intestinal mucin cDNA. J Biol Chem 272:16663–16669
Wang P, Granados RR (1998) Observations on the presence of the peritrophic membrane in larval Trichoplusia ni and its role in limiting baculovirus infection. J Invertebr Pathol 72:57–62
Wang P, Granados RR (2000) Calcofluor disrupts the midgut defense system in insects. Insect Biochem Mol Biol 30:135–143
Wang P, Hammer DA, Granados RR (1994) Interaction of Trichoplusia ni granulosis virus-encoded enhancin with the midgut epithelium and peritrophic membrane of four lepidopteran insects. J Gen Virol 75:1961–1967
Wang P, Li G, Granados RR (2004) Identification of two new peritrophic membrane proteins from larval Trichoplusia ni: structural characteristics and their functions in the protease rich insect gut. Insect Biochem Mol Biol 34:215–227
Washburn JO, Kirkpatrick BA, Volkman LE (1995) Comparative pathogenesis of Autographa californica M nuclear polyhedrosis virus in larvae of Trichoplusia ni and Heliothis virescens. Virology 209:561–568
Waterhouse DF (1953) Occurrence and endodermal origin of the peritrophic membrane in some insects. Nature 172(4380):676–677
Waterhouse DF (1957) Digestion in insects. Annu Rev Entomol 2:1–18
Weiss BL, Savage AF, Griffith BC, Wu Y, Aksoy S (2014) The peritrophic matrix mediates differential infection outcomes in the tsetse fly gut following challenge with commensal, pathogenic, and parasitic microbes. J Immunol 193:773–782
Welburn SC, Arnold K, Maudlin I, Gooday GW (1993) Rickettsia-like organisms and chitinase production in relation to transmission of trypanosomes by tsetse flies. Parasitology 107:141–145
Whyard S, Singh AD, Wong S (2009) Ingested double-stranded RNAs can act as species-specific insecticides. Insect Biochem Mol Biol 39:824–832
Wigglesworth VB (1929) Digestion in the tsetse-fly: a study of structure and function. Parasitology 21:288–321
Wigglesworth VB (1930) The formation of the peritrophic membrane in insects, with special reference to the larvae of mosquitoes. Q J Microsc Sci 73:593–616
Wijffels G, Eisemann C, Riding G, Pearson R, Jones A, Willadsen P, Tellam R (2001) A novel family of chitin-binding proteins from insect type 2 peritrophic matrix. cDNA sequences, chitin binding activity, and cellular localization. J Biol Chem 276:15527–15536
Wiwat C, Thaithanun S, Pantuwatana S, Bhumiratana A (2000) Toxicity of chitinase-producing Bacillus thuringiensis ssp. kurstaki HD-1 toward Plutella xylostella. J Invertebr Pathol 76:270–277
Wu H, de Graaf B, Mariani C, Cheung AY (2001) Hydroxyproline-rich glycoproteins in plant reproductive tissues: structure, functions and regulation. Cell Mol Life Sci 58:1418–1429
Yang S, Pyati P, Fitches E, Gatehouse JA (2014) A recombinant fusion protein containing a spider toxin specific for the insect voltage-gated sodium ion channel shows oral toxicity towards insects of different orders. Insect Biochem Mol Biol 47:1–11
Yunovitz H, Sneh B, Schuster S, Oron U, Broza M, Yawetz A (1986) A new sensitive method for determining the toxicity of a highly purified fraction from δ-endotoxin produced by Bacillus thuringiensis var. entomocidus on isolated larval midgut of Spodoptera littoralis (Lepidoptera, Noctuidae). J Invertebr Pathol 48:223–231
Zhang X, Guo W (2011) Isolation and identification of insect intestinal mucin HaIIM86--the new target for Helicoverpa armigera biocontrol. Int J Biol Sci 7:286–296
Zhang S, Sherwood RW, Yang Y, Fish T, Chen W, McCardle JA, Jones RM, Yusibov V, May ER, Rose JK, Thannhauser TW (2012) Comparative characterization of the glycosylation profiles of an influenza hemagglutinin produced in plant and insect hosts. Proteomics 12:1269–1288
Zhu Q, Arakane Y, Banerjee D, Beeman RW, Kramer KJ, Muthukrishnan S (2008) Domain organization and phylogenetic analysis of the chitinase-like family of proteins in three species of insects. Insect Biochem Mol Biol 38:452–466
Zhu-Salzman K, Koiwa H, Salzman RA, Shade RE, Ahn JE (2003) Cowpea bruchid Callosobruchus maculatus uses a three-component strategy to overcome a plant defensive cysteine protease inhibitor. Insect Mol Biol 12:135–145
Zhuzhikov DP (1964) Function of the peritrophic membrane in Musca domestica L. and Calliphora erythrocephala Meig. J Insect Physiol 10:273–278
Zhuzhikov DP (1970) Permeability of the peritrophic membrane in the larvae of Aedes aegypti. J Insect Physiol 16:1193–1202
Zimmermann U, Mehlan D (1976) Water transport across peritrophic membranes of Calliphora erythrocephala. Comp Biochem Physiol 55A:119–126
Zimmermann D, Peters W (1987) Fine structure and permeability of peritrophic membranes of Calliphora erythrocephala (Meigen) (Insecta: Diptera) after inhibition of chitin and protein synthesis. Comp Biochem Physiol 86B:353–360
Zimmermann U, Mehlan D, Peters W (1975) Investigations on the transport function and structure of peritrophic membranes; V – Amino acid analysis and electron microscopic investigations of the peritophic membranes of the blowfly Calliphora erythrocephala Mg. Comp Biochem Physiol 51B:181–186
Zimoch L, Merzendorfer H (2002) Immunolocalization of chitin synthase in the tobacco hornworm. Cell Tissue Res 308:287–297
Zimoch L, Hogenkamp DG, Kramer KJ, Muthukrishnan S, Merzendorfer H (2005) Regulation of chitin synthesis in the larval midgut of Manduca sexta. Insect Biochem Mol Biol 35:515–527
Acknowledgements
This work was supported by the NSF Grant IOS-1022227 to S.M. and the DFG Grant Me2210/3-1 to H.M. M.K. was supported by a Lichtenberg fellowship by the Government of the State of Lower Saxonia, Germany.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Merzendorfer, H., Kelkenberg, M., Muthukrishnan, S. (2016). Peritrophic Matrices. In: Cohen, E., Moussian, B. (eds) Extracellular Composite Matrices in Arthropods. Springer, Cham. https://doi.org/10.1007/978-3-319-40740-1_8
Download citation
DOI: https://doi.org/10.1007/978-3-319-40740-1_8
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-40738-8
Online ISBN: 978-3-319-40740-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)