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Chitin in Arthropods: Biosynthesis, Modification, and Metabolism

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Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1142))

Abstract

Chitin is a structural constituent of extracellular matrices including the cuticle of the exoskeleton and the peritrophic matrix (PM) of the midgut in arthropods. Chitin chains are synthesized through multiple biochemical reactions, organized in several hierarchical levels and associated with various proteins that give their unique physicochemical characteristics of the cuticle and PM. Because, arthropod growth and morphogenesis are dependent on the capability of remodeling chitin-containing structures, chitin biosynthesis and degradation are highly regulated, allowing ecdysis and regeneration of the cuticle and PM. Over the past 20 years, much progress has been made in understanding the physiological functions of chitinous matrices. In this chapter, we mainly discussed the biochemical processes of chitin biosynthesis, modification and degradation, and various enzymes involved in these processes. We also discussed cuticular proteins and PM proteins, which largely determine the physicochemical properties of the cuticle and PM. Although rapid advances in genomics, proteomics, RNA interference, and other technologies have considerably facilitated our research in chitin biosynthesis, modification, and metabolism in recent years, many aspects of these processes are still partially understood. Further research is needed in understanding how the structural organization of chitin synthase in plasma membrane accommodate chitin biosynthesis, transport of chitin chain across the plasma membrane, and release of the chitin chain from the enzyme. Other research is also needed in elucidating the roles of chitin deacetylases in chitin organization and the mechanism controlling the formation of different types of chitin in arthropods.

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References

  • Agrawal S, Kelkenberg M, Begum K, Steinfeld L, Williams CE, Kramer KJ et al (2014) Two essential peritrophic matrix proteins mediate matrix barrier functions in the insect midgut. Insect Biochem Mol Biol 49:24–34

    Article  CAS  PubMed  Google Scholar 

  • Alvarenga ES, Mansur JF, Justi SA, Figueira-Mansur J, Dos Santos VM, Lopez SG et al (2016) Chitin is a component of the Rhodnius prolixus midgut. Insect Biochem Mol Biol 69:61–70

    Article  CAS  PubMed  Google Scholar 

  • Ampasala DR, Zheng SC, Zhang DY, Ladd T, Doucet D, Krell PJ et al (2011) An epidermis-specific chitin synthase cDNA in Choristoneura fumiferana: cloning, characterization, developmental and hormonal-regulated expression. Arch Insect Biochem 76:83–96

    Article  CAS  Google Scholar 

  • Andersen SO (1979) Insect cuticle. Annu Rev Entomol 24:29–61

    Article  CAS  Google Scholar 

  • Andersen SO (1998) Amino acid sequence studies on endocuticular proteins from the desert locust, Schistocerca gregaria. Insect Biochem Mol Biol 28:421–434

    Article  CAS  PubMed  Google Scholar 

  • Andersen SO (2000) Studies on proteins in post-ecdysial nymphal cuticle of locust, Locusta migratoria, and cockroach, Blaberus craniifer. Insect Biochem Mol Biol 30:569–577

    Article  CAS  PubMed  Google Scholar 

  • Andersen SO, Rafn K, Roepstorff P (1997) Sequence studies of proteins from larval and pupal cuticle of the yellow mealworm, Tenebrio moliter. Insect Biochem Mol Biol 27:121–131

    Article  CAS  PubMed  Google Scholar 

  • Arakane Y, Baguinon M, Jasrapuria S, Chaudhari S, Doyungan A, Kramer KJ et al (2011) Both UDP N-acetylglucosamine pyrophosphorylases of Tribolium castaneum are critical for molting, survival and fecundity. Insect Biochem Mol Biol 41:42–50

    Article  CAS  PubMed  Google Scholar 

  • Arakane Y, Dixit R, Begum K, Park Y, Specht CA, Merzendorfer H et al (2009) Analysis of functions of the chitin deacetylase gene family in Tribolium castaneum. Insect Biochem Mol Biol 39:355–365

    Article  CAS  PubMed  Google Scholar 

  • Arakane Y, Hogenkamp DG, Zhu YC, Kramer KJ, Specht CA, Beeman RW et al (2004) Characterization of two chitin synthase genes of the red fl our beetle, Tribolium castaneum, and alternate exon usage in one of the genes during development. Insect Biochem Mol Biol 34:291–304

    Article  CAS  PubMed  Google Scholar 

  • Arakane Y, Lomakin J, Gehrke SH, Hiromasa Y, Tomich JM, Muthukrishnan S et al (2012) Formation of rigid, non-flight forewings (elytra) of a beetle requires two major cuticular proteins. PLoS Genet 8:e1002682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arakane Y, Muthukrishnan S (2010) Insect chitinase and chitinase-like proteins. Cell Mol Life Sci 67:201–216

    Article  CAS  PubMed  Google Scholar 

  • Arakane Y, Muthukrishnan S, Kramer KJ, Specht CA, Tomoyasu Y, Lorenzen MD et al (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

    Article  CAS  PubMed  Google Scholar 

  • Arakane Y, Specht CA, Kramer KJ, Muthukrishnan S, Beeman RW (2008) Chitin synthases are required for survival, fecundity and egg hatch in the red fl our beetle, Tribolium castaneum. Insect Biochem Mol Biol 38:959–962

    Article  CAS  PubMed  Google Scholar 

  • Araújo SJ, Aslam H, Tear G, Casanova J (2005) mummy/cystic encodes an enzyme required for chitin and glycan synthesis, involved in trachea, embryonic cuticle and CNS development analysis of its role in Drosophila tracheal morphogenesis. Dev Biol 288:179–193

    Article  CAS  PubMed  Google Scholar 

  • Asano T, Taoka M, Shinkawa T, Yamauchi Y, Isobe T, Sato D (2013) Identification of a cuticle protein with unique repeated motifs in the silkworm, Bombyx mori. Insect Biochem Mol Biol 43:344–351

    Article  CAS  PubMed  Google Scholar 

  • Ashfaq M, Sonoda S, Tsumuki H (2007) Developmental and tissue-specifi c expression of CHS1 from Plutella xylostella and its response to chlorfluazuron. Pestic Biochem Physiol 89:20–30

    Google Scholar 

  • Balbiani EG (1890) E’tudes anatomiques et histologiques sur le tube digestif des Crytops. Arch Zool Exp Gen 8:1–82

    Google Scholar 

  • Bansal R, Mian MA, Mittapalli O, Michel AP (2012) Characterization of a chitin synthase encoding gene and effect of diflubenzuron in soybean aphid, Aphis glycines. Int J Biol Sci 8:1323–1334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbakadze N, Enders S, Gorb S, Arzt E (2006) Local mechanical properties of the head articulation cuticle in the beetle Pachnoda marginata (Coleoptera, Scarabaeidae). J Exp Biol 209:722–730

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Becker A, Schloder P, Steele JE, Wegener G (1996) The regulation of trehalose metabolism in insects. Experientia 52:433–439

    Article  CAS  PubMed  Google Scholar 

  • Becker B (1980) Effects of polyoxin D on in vitro synthesis of peritrophic membranes in Calliphora erythrocephala. Insect Biochem 10:101–106

    Article  CAS  Google Scholar 

  • Behr M, Hoch M (2005) Identification of the novel evolutionary conserved obstructor multigene family in invertebrates. FEBS Lett 579:6827–6833

    Article  CAS  PubMed  Google Scholar 

  • Belles X, Cristino AS, Tanaka ED, Rubio M, Piulachs MD (2012) Insect MicroRNAs: from molecular mechanisms to biological roles. In: Gilbert LI (ed) Insect molecular biology and biochemistry. Academic, New York, pp 30–56

    Chapter  Google Scholar 

  • Bentov S, Aflalo ED, Tynyakov J, Glazer L, Sagi A (2016) Calcium phosphate mineralization is widely applied in crustacean mandibles. Sci Rep 6:22118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berger M, Chen H, Reutter W, Hinderlich S (2002) Structure and function of N-acetylglucosamine kinase. Eur J Biochem 269:4212–4218

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bouligand Y (1965) On a twisted fibrillar arrangement common to several biologic structures. Comptes Rendus Hebdomadaires des Seances de l’Academie des Sciences, Serie D 261:4864–4867

    CAS  Google Scholar 

  • Bouligand Y (1972) Twisted fibrous arrangements in biological-materials and cholesteric mesophases. Tissue Cell 4:189–217

    Article  CAS  PubMed  Google Scholar 

  • Brameld KA, Shrader WD, Imperiali B, Gddard WA III (1998) Substrate assistance in the mechanism of family 18 chitinases: theoretical studies of potential intermediates and inhibitors. J Mol Biol 280:913–923

    Article  CAS  PubMed  Google Scholar 

  • Brusca RC (2000) Unrevealing the history of arthropod diversification. Ann Mo Bot Gard 87:13–25

    Google Scholar 

  • Campbell PM, Cao AT, Hines ER, East PD, Gordon KHJ (2008) Proteomic analysis of the peritrophic matrix from the gut of the caterpillar, Helicoverpa armigera. Insect Biochem Mol Biol 38:950–958

    Article  CAS  PubMed  Google Scholar 

  • Candy DJ, Kilby BA (1962) Studies on chitin synthesis in the desert locust. J Exp Biol 39:129–140

    CAS  Google Scholar 

  • Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301:336–338

    Article  CAS  Google Scholar 

  • Cattaneo F, Pasini ME, Intra J, Matsumoto M, Briani F, Hoshi M et al (2006) Identification and expression analysis of Drosophila melanogaster genes encoding β-hexosaminidases of the sperm plasma membrane. Glycobiology 16:786–800

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Liang ZK, Liang YK, Pang R, Zhang WQ (2013) Conserved microRNAs miR-8-5p and miR-2a-3p modulate chitin biosynthesis in response to 20-hydroxyecdysone signaling in the brown planthopper, Nilaparvata lugens. Insect Biochem Mol Biol 43:839–848

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Tang B, Chen H, Yao Q, Huang X, Chen J et al (2010) Different functions of the insect soluble and membrane-bound trehalase genes in chitin biosynthesis revealed by RNA interference. PLoS ONE 5:e10133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Q, Ma E, Behar KL, Xu T, Haddad GG (2002) Role of trehalose phosphate synthase in anoxia tolerance and development in Drosophila melanogaster. J Biol Chem 277:3274–3279

    Article  CAS  PubMed  Google Scholar 

  • 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 Physi 23:241–246

    Article  CAS  Google Scholar 

  • Cohen E (1987) Chitin biochemistry: synthesis and inhibition. Annu Rev Entomol 32:71–93

    Article  CAS  Google Scholar 

  • Cohen E (2010) Chitin biochemistry: synthesis, hydrolysis and inhibition. Adv Insect Physiol 38:5–74

    Article  Google Scholar 

  • Cornman RS (2009) Molecular evolution of Drosophila cuticular protein genes. PLoS ONE 4:e8345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cornman RS, Togawa T, Dunn WA, He N, Emmons AC, Willis JH (2008) Annotation and analysis of a large cuticular protein family with the R&R Consensus in Anopheles gambiae. BMC Genom 18:9–22

    Google Scholar 

  • Cornman RS, Willis JH (2009) Annotation and analysis of low-complexity protein families of Anopheles gambiae that are associated with cuticle. Insect Mol Biol 18:607–622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coutinho PM, Deleury E, Davies GJ, Henrissat B (2003) An evolving hierarchical family classification for glycosyltransferases. J Mol Bio 328:307–317

    Article  CAS  Google Scholar 

  • Culliney TW (2014) Chapter 8: Crop losses to arthropods. In: Pimentel D, Peshin R (eds) Integrated pest management: pesticide problems, vol. 3, Springer, pp 201–225

    Google Scholar 

  • De Mets R, Jeuniaux C (1962) Composition of peritrophic membrane. Arch Int Physiol Biochim 70:93–96

    CAS  Google Scholar 

  • Dixit R, Arakane Y, Specht CA, Richard C, Kramer KJ, Beeman RW et al (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

    Article  CAS  PubMed  Google Scholar 

  • Dong Z, Zhang W, Zhang Y, Zhang X, Zhao P, Xia Q (2016) Identification and characterization of novel chitin-binding proteins from the larval cuticle of silkworm, Bombyx mori. J Proteome Res 15:1435

    Google Scholar 

  • Dorfmueller HC, Ferenbach AT, Borodkin VS, van Aalten DM (2014) A structural and biochemical model of processive chitin synthesis. J Biol Chem 289:23020–23028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eisenhaber B, Maurer-Stroh S, Novatchkova M, Schneider G, Eisenhaber F (2003) Enzymes and auxiliary factors for GPI lipid anchor biosynthesis and posttranslational transfer to proteins. BioEssays 25:367–385

    Article  CAS  PubMed  Google Scholar 

  • Elvin CM, Vuocolo T, Pearson RD, East IJ, Riding GA, Eisemann CH et al (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

    Article  CAS  PubMed  Google Scholar 

  • Fabritius HO, Sachs C, Triguero PR, Raabe D (2009) Influence of structural principles on the mechanics of a biological fiber-based composite material with hierarchical organization: the exoskeleton of the lobster Homarus americanus. Adv Mater Sci 21:391–400

    CAS  Google Scholar 

  • Filho BP, Lemos FJ, Secundino NF, Pascoa V, Pereira ST, Pimenta PF (2002) Presence of chitinase and beta-N-acetylglucosaminidase in the Aedes aegypti: a chitinolytic system involving peritrophic matrix formation and degradation. Insect Biochem Mol Biol 32:1723–1729

    Article  CAS  PubMed  Google Scholar 

  • Fukamizo T, Kramer KJ (1985) Mechanism of chitin oligosaccharide hydrolysis by the binary enzyme chitinase system in insect moulting fluid. Insect Biochem 15:1–7

    Article  CAS  Google Scholar 

  • Futahashi R, Okamoto S, Kawasaki H, Zhong YS, Iwanaga M, Mita K et al (2008) Genome-wide identification of cuticular protein genes in the silkworm, Bombyx mori. Insect Biochem Mol Biol 38:1138–1146

    Article  CAS  PubMed  Google Scholar 

  • Gagou ME, Kapsetaki M, Turberg A, Kafetzopoulos D (2002) Stage-specific expression of the chitin synthase DmeChSA and DmeChSB genes during the onset of Drosophila metamorphosis. Insect Biochem Mol Biol 32:141–146

    Article  CAS  PubMed  Google Scholar 

  • Gallai N, Salles J-M, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68:810–821

    Article  Google Scholar 

  • Guan X, Middlebrooks BW, Alexander S, Wasserman SA (2006) Mutation of TweedleD, a member of an unconventional cuticle protein family, alters body shape in Drosophila. Proc Natl Acad Sci USA 103:16794–16799

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Harper MS, Hopkins TL (1997) Peritrophic membrane structure and secretion in European corn borer larvae (Ostrinia nubilalis). Tissue Cell 29:463–475

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • He N, Botelho JM, Mcnall RJ, Belozerov V, Dunn WA, Mize T et al (2007) Proteomic analysis of cast cuticles from Anopheles gambiae by tandem mass spectrometry. Insect Biochem Mol Biol 37:135–146

    Article  CAS  PubMed  Google Scholar 

  • Hegedus D, Erlandson M, Gillott C, Toprak U (2009) New insights into peritrophic matrix synthesis, architecture, and function. Annu Rev Entomol 54:285–302

    Article  CAS  PubMed  Google Scholar 

  • Hinderlich S, Berger M, Schwarzkopf M, Effertz K, Reutter W (2000) Molecular cloning and characterization of murine and human N-acetylglucosamine kinase. Eur J Biochem 267:3301–3308

    Article  CAS  PubMed  Google Scholar 

  • Hogenkamp DG, Arakane Y, Kramer KJ, Muthukrishnan S, Beeman RW (2008) Characterization and expression of the β-N-acetylhexosaminidase gene family of Tribolium castaneum. Insect Biochem Mol Biol 38:478–489

    Article  CAS  PubMed  Google Scholar 

  • Hogenkamp DG, Arakane Y, Zimoch L, Merzendorfer H, Kramer KJ, Beeman RW et al (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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Huang X, Tsuji N, Miyoshi T, Motobu M, Islam MK, Alim MA et al (2007) Characterization of glutamine: fructose-6-phosphate aminotransferase from the ixodid tick, Haemaphysalis longicornis, and its critical role in host blood feeding. Int J Parasitol 37:383–392

    Article  CAS  PubMed  Google Scholar 

  • Ianiro A, Giosia MD, Fermani S, Samor C, Barbalinardo M, Valle F et al (2014) Customizing properties of β-chitin in squid pen (gladius) by chemical treatments. Marine Drugs 12:5979–5992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iconomidou VA, Willis JH, Hamodrakas SJ (2005) Unique features of the structural model of ‘hard’ cuticle proteins: implications for chitin-protein interactions and cross-linking in cuticle. Insect Biochem Mol Biol 35:553–560

    Article  CAS  PubMed  Google Scholar 

  • Ioannidou ZS, Theodoropoulou MC, Papandreou NC, Willis JH, Hamodrakas SJ (2014) CutProtFam-Pred: detection and classification of putative structural cuticular proteins from sequence alone, based on profile hidden Markov models. Insect Biochem Mol Biol 52:51–59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Jasrapuria S, Specht CA, Kramer KJ, Beeman RW, Muthukrishnan S (2012) Gene families of cuticular proteins analogous to peritrophins (CPAPs) in Tribolium castaneum have diverse functions. PLoS ONE 7:e49844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaworski E, Wang L, Margo G (1963) Synthesis of chitin in cell-free extracts of Prodenia eridania. Nature 198:790

    Article  CAS  Google Scholar 

  • Jensen UG, Rothmann A, Skou L, Andersen SO, Roepstorff P, Højrup P (1997) Cuticular proteins from the giant cockroach, Blaberus craniifer. Insect Biochem Mol Biol 27:109–120

    Article  CAS  PubMed  Google Scholar 

  • Kanost MR, Zepp MK, Ladendorff NE, Andersson LA (1994) Isolation and characterization of a hemocyte aggregation inhibitor from hemolymph of Manduca sexta larvae. Arch Insect Biochem Physiol 27:123–136

    Article  CAS  PubMed  Google Scholar 

  • Karouzou MV, Spyropoulos Y, Iconomidou VA, Cornman RS, Hamodrakas SJ, Willis JH (2007) Drosophila cuticular proteins with the R&R Consensus: annotation and classification with a new tool for discriminating RR-1 and RR-2 sequences. Insect Biochem Mol Biol 37:754–760

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kato N, Mueller CR, Wessely V, Lan Q, Christensen BM (2005) Mosquito glucosamine-6-phosphate N-acetyltransferase: cDNA, gene structure and enzyme kinetics. Insect Biochem Mol Biol 35:637–646

    Article  CAS  PubMed  Google Scholar 

  • Kawamura K, Shibata T, Saget O, Peel D, Bryant PJ (1999) A new family of growth factors produced by the fat body and active on Drosophila imaginal disc cells. Development 126:211–219

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • King-Jones K, Thummel CS (2005) Nuclear receptors-a perspective from Drosophila. Nat Rev Genet 6:311–323

    Article  CAS  PubMed  Google Scholar 

  • Koga D, Funakoshi T, Mizuki K, Ide A, Kramer KJ, Zen KC et al (1992) Immunoblot analysis of chitinolytic enzymes in integument and molting fluid of the silkworm, Bombyx mori, and the tobacco hornworm, Manduca sexta. Insect Biochem Mol Biol 22:305–311

    Article  CAS  Google Scholar 

  • Koga D, Mai MS, Dziadik-Turner C, Kramer KJ (1982) Kinetics and mechanism of exochitinase and β-N-acetylhexosaminidase from the tobacco hornworm, Manduca sexta L. (Lepidoptera: Sphingidae). Insect Biochem 12:493–499

    Article  CAS  Google Scholar 

  • Kokuho T, Yasukochi Y, Watanabe S, Inumuru S (2007) Molecular cloning and expression of two novel β-N-acetylglucosaminidases from silkworm Bombyx mori. Biosci Biotechnol Biochem 71:1626–1635

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Kramer KJ, Hopkins TL, Schaefer J (1995) Applications of solids NMR to the analysis of insect sclerotized structures. Insect Biochem Mol Biol 25:1067–1080

    Article  CAS  Google Scholar 

  • Kramer KJ, Koga D (1986) Insect chitin: physical state, synthesis, degradation and metabolic regulation. Insect Biochem 16:851–877

    Article  CAS  Google Scholar 

  • Kucharski R, Maleszka J, Maleszka R (2007) Novel cuticular proteins revealed by the honey bee genome. Insect Biochem Mol Biol 37:128–134

    Article  CAS  PubMed  Google Scholar 

  • Lehane MJ (1997) Peritrophic matrix structure and function. Annu Rev Entomol 42:525–550

    Article  CAS  PubMed  Google Scholar 

  • Leonard R, Rendic D, Rabouille C, Wilson IB, Preat T, Altmann F (2006) The Drosophila fused lobes gene encodes an N-acetylglucosaminidase involved in N-glycan processing. J Biol Chem 281:4867–4875

    Article  CAS  PubMed  Google Scholar 

  • Li D, Zhang J, Wang Y, Liu X, Ma E, Sun Y et al (2015) Two chitinase 5 genes from Locusta migratoria: molecular characteristics and functional differentiation. Insect Biochem Mol Biol 58:46–54

    Article  CAS  PubMed  Google Scholar 

  • Liu T, Zhang HT, Liu FY, Wu QY, Shen X, Yang Q (2011) Structural determinants of an insect β-N-acetyl-D-hexosaminidase specialized as a chitinolytic enzyme. J Biol Chem 286:4049–4058

    Google Scholar 

  • Liu XJ, Zhang HH, Li S, Zhu KY, Ma EB, Zhang JZ (2012) Characterization of a midgut-specific chitin synthase gene (LmCHS2) responsible for biosynthesis of chitin of peritrophic matrix in Locusta migratoria. Insect Biochem Mol Biol 42:902–910

    Article  CAS  PubMed  Google Scholar 

  • Liu XJ, Li F, Li DQ, Ma EB, Zhang WQ, Zhu KY et al (2013) Molecular and functional analysis of UDP-N-acetylglucosamine pyrophosphorylases from the migratory locust, Locusta migratoria. PLoS One 8:e71970

    Google Scholar 

  • Liu XJ, Sun YW, Cui M, Ma EB, Zhang JZ (2016) Molecular characteristics and functional analysis of trehalase genes in Locusta migratoria. Scientia Agricultura Sinica 49:4375–4386

    Google Scholar 

  • Liu XJ, Sun YW, Li DQ, Li S, Ma EB, Zhang JZ (2018) Identification of LmUAP1 as a 20-hydroxyecdysone response gene in the chitin biosynthesis pathway from the migratory locust, Locusta migratoria. Insect Sci 25:211–221

    Article  CAS  PubMed  Google Scholar 

  • Locke M (2001) The Wigglesworth lecture: insects for studying fundamental problems in biology. J Insect Physiol 47:495–507

    Article  CAS  PubMed  Google Scholar 

  • Locke M, Huie P (1979) Apolysis and the turnover of plasma membrane plaques during cuticle formation in an insect. Tissue Cell 11:277–291

    Article  CAS  PubMed  Google Scholar 

  • Lu JB, Luo XM, Zhang XY, Pan PL, Zhang CX (2018) An ungrouped cuticular protein is essential for normal endocuticle formation in the brown planthopper. Insect Biochem Mol Biol 100:1–9

    Article  CAS  PubMed  Google Scholar 

  • Luschnig S, Batz T, Armbruster K, Krasnow MA (2006) Serpentine and vermiform encode matrix proteins with chitin binding and deacetylation domains that limit tracheal tube length in Drosophila. Curr Biol 16:186–194

    Article  CAS  PubMed  Google Scholar 

  • Lyonet P (1762) Trait’e Anatomique de la Chenille qui ronge le bois de Saule. Haye, Holland, La

    Google Scholar 

  • Makki R, Cinnamon E, Gould AP (2014) The development and functions of oenocytes. Annu Rev Entomol 59:405–425

    Article  CAS  PubMed  Google Scholar 

  • Mansur JF, Alvarenga ES, Figueira-Mansur J, Franco TA, Ramos IB, Masuda H et al (2014) Effects of chitin synthase double-stranded RNA on molting and oogenesis in the Chagas disease vector Rhodnius prolixus. Insect Biochem Mol Biol 51:110–121

    Article  CAS  PubMed  Google Scholar 

  • Marschall HU, Matern H, Wietholtz H, Egestad B, Matern S, Sjövall J (1992) Bile acid N-acetylglucosaminidation in vivo and in vitro evidence for a selective conjugation reaction of 7 beta-hydroxylated bile acids in humans. J Clin Invest 89:1981–1987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martins GF, Ramalho-Ortiago JM (2012) Oenocytes in insects. Inverteb Surviv J 9:139–152

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Merzendorfer H (2006) Insect chitin synthases: a review. J Comput Physiol B 176:1–15

    Article  CAS  Google Scholar 

  • Merzendorfer H (2013) Chitin synthesis inhibitors: old molecules and new developments. Insect Sci 20:121–138

    Article  CAS  PubMed  Google Scholar 

  • Merzendorfer H, Zimoch L (2003) Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases. J Exp Biol 206:4393–4412

    Article  CAS  PubMed  Google Scholar 

  • Mitsumasu K, Azuma M, Niimi T, Yamashita O, Yaginuma T (2005) Membrane-penetrating trehalase from silkworm Bombyx mori: molecular cloning and localization in larval midgut. Insect Mol Biol 14:501–508

    Article  CAS  PubMed  Google Scholar 

  • Moussian B, Schwarz H, Bartoszewski S, Nüsslein-Volhard C (2005) Involvement of chitin in exoskeleton morphogenesis in Drosophila melanogaster. J Morphol 264:117–130

    Article  CAS  PubMed  Google Scholar 

  • Moussian B, Tång E, Tonning A, Helms S, Schwarz H, Nüsslein-Volhard C et al (2006) Drosophila Knickkopf and Retroactive are needed for epithelial tube growth and cuticle differentiation through their specific requirement for chitin filament organization. Development 133:163–171

    Article  CAS  PubMed  Google Scholar 

  • Munro CA, Gow NA (2001) Chitin synthesis in human pathogenic fungi. Med Mycol 39(Suppl. 1):41–53

    Article  CAS  PubMed  Google Scholar 

  • Muthukrishnan S, Arakane Y, Yang Q, Zhang C-X, Zhang J, Zhang W et al (2018) Future questions in insect chitin biology: a microreview. Arch Insect Biochem Physiol 98:e21454. https://doi.org/10.1002/arch.21454

    Article  CAS  PubMed  Google Scholar 

  • Muthukrishnan S, Merzendorfer H, Arakane Y, Kramer KJ (2012) Chitin metabolism in insects. In: Biol Insect Biochem Mol (ed) Gilbert LI. Elsevier, San Diego, pp 193–235

    Google Scholar 

  • Nagamatsu Y, Yanagisawa I, Kimoto M, Okamoto E, Koga D (1995) Purification of a chitooligosaccharidolytic β-N-acetylglucosaminidase from Bombyx mori larvae during metamorphosis and the nucleotide sequence of its cDNA. Biosci Biotechnol Biochem 59:219–225

    Article  CAS  PubMed  Google Scholar 

  • Nakabachi A, Shigenobu S, Miyagishima S (2010) Chitinase-like proteins encoded in the genome of the pea aphid, Acyrthosiphon pisum. Insect Mol Biol 19:175–185

    Article  CAS  PubMed  Google Scholar 

  • Neville AC (1975) Biology of the arthropod cuticle. Springer, Berlin

    Book  Google Scholar 

  • Neville AC, Luke BM (1969) A two-system model for chitin-protein complexes in insect cuticles. Tissue Cell 1:689–707

    Article  CAS  PubMed  Google Scholar 

  • Noble-Nesbitt J (1991) Cuticular permeability and its control. In: Binnington K, Retnakaran A (eds) Physiology of the insect epidermis Melbourne. CSIRO, Australia, pp 240–251

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Ostrowski S, Dierick HA, Bejsovec A (2002) Genetic control of cuticle formation during embryonic development of Drosophila melanogaster. Genetics 161:171–182

    CAS  PubMed  PubMed Central  Google Scholar 

  • Palaka BK, Sapam TD, Ilavarasi AV, Chowdhury S, Sk Rajendiran, Khan MB et al (2017) Molecular cloning and characterization of phosphoacetylglucosamine mutase from Bombyx mori. J Entomol Zool Studies 5:1166–1178

    Google Scholar 

  • Pan PL, Ye YX, Lou YH, Lu JB, Cheng C, Shen Y, Moussian B, Zhang CX (2018) A comprehensive omics analysis and functional survey of cuticular proteins in the brown planthopper. Proc Natl Acad Sci USA 115:5175–5180

    Article  CAS  PubMed  Google Scholar 

  • Pan Y, Lu P, Wang Y, Yin L, Ma H, Ma G et al (2012) In silico identification of novel chitinase-like proteins in the silkworm, Bombyx mori, genome. J Insect Sci 12:150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park JT (2001) Identification of a dedicated recycling pathway for an hydro-N-acetylmuramic acid and N-acetylglucosamine derived from Escherichia coli cell wall murein. J Bacteriol 183:3842–3847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peneff C, Ferrari P, Charrier V, Taburet Y, Monnier C, Zamboni V et al (2001) Crystal structures of two human pyrophosphorylase isoforms in complexes with UDPGlc(Gal)NAc: role of the alternatively spliced insert in the enzyme oligomeric assembly and active site architecture. EMBO J 20:6191–6202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pesch YY, Riedel D, Behr M (2015) Obstructor A organizes matrix assembly at the apical cell surface to promote enzymatic cuticle maturation in Drosophila. J Biol Chem 290:10071–10082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peters W (1992) Peritrophic membranes, vol 30. Zoophysiology. Springer, Berlin

    Google Scholar 

  • Peters W, Latka I (1986) Electron microscopic localization of chitin using colloidal gold labelled with wheat germ agglutinin. Histochemistry 84:155–160

    Article  CAS  PubMed  Google Scholar 

  • Petkau G, Wingen C, Jussen LC, Radtke T, Behr M (2012) Obstructor-A is required for epithelial extracellular matrix dynamics, exoskeleton function, and tubulogenesis. J Biol Chem 287:21396–21405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qu M, Ma L, Chen P, Yang Q (2014) Proteomic analysis of insect molting fluid with a focus on enzymes involved in chitin degradation. J Proteome Res 13:2931–2940

    Article  CAS  PubMed  Google Scholar 

  • Qu M, Yang Q (2011) A novel alternative splicing site of class A chitin synthase from the insect Ostrinia furnacalis - Gene organization, expression pattern and physiological significance. Insect Biochem Mol Biol 41:923–931

    Article  CAS  PubMed  Google Scholar 

  • Qu M, Yang Q (2012) Physiological significance of alternatively spliced exon combinations of the single-copy gene class A chitin synthase in the insect Ostrinia furnacalis (Lepidoptera). Insect Mol Biol 21:395–404

    Article  CAS  PubMed  Google Scholar 

  • Raabe D, Al-Sawalmih A, Romano P, Sachs C, Brokmeier HG, Yi SB et al. (2005a) Structure and crystallographic texture of arthropod bio-composites. Icotom 14: Texture of Materials, Pts 1 and 2: 495–497 and 1665–1674

    Google Scholar 

  • Raabe D, Romano P, Sachs C (2005b) The crustacean exoskeleton as an example of a structurally and mechanically graded biological nanocomposite material. Acta Mater 53:4281–4292

    Article  CAS  Google Scholar 

  • Raabe D, Romano P, Sachs C, Al-Sawalmih A, Brokmeier HG, Yi SB et al (2005c) Discovery of a honeycomb structure in the twisted plywood patterns of fibrous biological nanocomposite tissue. J Cryst Growth 283:1–7

    Article  CAS  Google Scholar 

  • Raabe D, Romano P, Sachs C, Fabritius H, Al-Sawalmih A, Yi S-B et al (2006) Microstructure and crystallographic texture of the chitin-protein network in the biological composite material of the exoskeleton of the lobster Homarus americanus. Mater Sci Eng, A 421:143–153

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Rebers JE, Riddiford LI (1988) Structure and expression of a Manduca sexta larval cuticle gene homologous to Drosophila cuticle genes. J Mol Biol 203:411–423

    Article  CAS  PubMed  Google Scholar 

  • Rebers JE, Willis JH (2001a) A conserved domain in arthropod cuticular proteins binds chitin. Insect Biochem Mol Biol 31:1083–1094

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Regier JC, Shultz JW, Zwick A, Hussey A, Ball B, Wetzer R et al (2010) Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 463:1079–1083

    Article  CAS  PubMed  Google Scholar 

  • Rebers JE, Willis JH (2001b) A conserved domain in arthropod cuticular proteins binds chitin. Insect Biochem Mol Biol 31:1083–1094

    Article  CAS  PubMed  Google Scholar 

  • Reynolds SE, Samuels RI (1996) Physiology and biochemistry of insect moulting fluid. Adv Insect Physiol 26:157–232

    Article  CAS  Google Scholar 

  • Richards AG, Richards PA (1977) The peritrophic membranes of insects. Annu Rev Entomol 22:219–240

    Article  PubMed  Google Scholar 

  • Riddiford L, Cherbas P, Truman JW (2001) Ecdysone receptors and their biological actions. Vitam Horm 60:1–73

    CAS  Google Scholar 

  • Rong S, Li D, Zhang X, Li S, Zhu KY et al (2013) β-N-acetylglucosaminidase gene is essential for larval-larval and larval-adult molting in Locusta migratoria. Insect Sci 20:109–119

    Article  CAS  PubMed  Google Scholar 

  • Ruddal KM (1963) The chitin–protein complexes of insect cuticles. Adv Insect Physiol 1:257–313

    Article  Google Scholar 

  • Rudall KM, Kenchington W (1973) The chitin system. Biol Rev 48:597–636

    Article  CAS  Google Scholar 

  • Schimmelpfeng K, Strunk M, Stork T, Klambt C (2006) Mummy encodes an UDP-N-acetylglucosamine-dipohosphorylase and is required during Drosophila dorsal closure and nervous system development. Mech Dev 123:487–499

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Sempere LF, Sokol NS, Dubrovsky EB, Berger EM, Ambros V (2003) Temporal regulation of microRNA expression in Drosophila melanogaster mediated by hormonal signals and Broad-Complex gene activity. Dev Biol 259:9–18

    Article  CAS  PubMed  Google Scholar 

  • Shao L, Devenport M, Jacobs-Lorena M (2001) The peritrophic matrix of hematophagous insects. Arch Insect Biochem Physiol 47:119–125

    Article  CAS  PubMed  Google Scholar 

  • Shi X, Chamankhah M, Visal-Shah S, Hemmingsen SM, Erlandson M, Braun L et al (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

    Article  CAS  PubMed  Google Scholar 

  • Shi JF, Fu J, Mu LL, Guo WC, Li GQ (2016a) Two Leptinotarsa uridine diphosphate N-acetylglucosamine pyrophosphorylases are specialized for chitin synthesis in larval epidermal cuticle and midgut peritrophic matrix. Insect Biochem Mol Biol 68:1–12

    Article  CAS  PubMed  Google Scholar 

  • Shi ZK, Liu X, Xu Q, Qin Z, Wang S, Zhang F et al (2016b) Two novel soluble trehalase genes cloned from Harmonia axyridis and regulation of the enzyme in a rapid changing temperature. Comput Biochem Physiol 198:10–18

    Article  CAS  Google Scholar 

  • Shirk PD, Perera OP, Shelby KS, Furlong RB, LoVullo ED, Popham HJR (2015) Unique synteny and alternate splicing of the chitin synthases in closely related heliothine moths. Gene 574:121–139

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Smibert P, Lai EC (2008) Lessons from microRNA mutants in worms, flies and mice. Cell Cycle 7:2500–2508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song TQ, Yang ML, Wang YL, Liu Q, Wang HM, Zhang J et al (2016) Cuticular protein LmTwdl1 is involved in molt development of the migratory locust. Insect Sci 23:520–530

    Article  CAS  PubMed  Google Scholar 

  • Specht CA, Liu Y, Robbins PW, Bulawa CE, Iartchouk N, Winter KR et al (1996) The chsD and chsE genes of Aspergillus nidulans and their roles in chitin synthesis. Funfal Genet Bio 20:153–167

    Article  CAS  Google Scholar 

  • Takiguchi M, Niimi T, Su ZH, Yaginuma T (1992) Trehalase from male accessory gland of an insect, Tenebrio molitor, cDNA sequencing and developmental profile of the gene expression. Biochem J 288:19–22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang B, Wei P, Zhao L, Shi Z, Shen Q, Yang M et al (2016) Knockdown of five trehalase genes using RNA interference regulates the gene expression of the chitin biosynthesis pathway in Tribolium castaneum. BMC Biotechnol 16:67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tellam RL, Vuocolo T, Johnson SE, Jarmey J, Pearson RD (2000) Insect chitin synthase cDNA sequence, gene organization and expression. Eur J Biochem 267:6025–6043

    Article  CAS  PubMed  Google Scholar 

  • Tellam RL, Wijffels G, Willadsen P (1999) Peritrophic matrix proteins. Insect Biochem Mol Biol 29:87–101

    Article  CAS  PubMed  Google Scholar 

  • Terra WR (2001) The origin and functions of the insect peritrophic membrane and peritrophic gel. Arch Insect Biochem Physiol 47:47–61

    Article  CAS  PubMed  Google Scholar 

  • Tetreau G, Cao XL, Chen YR, Muthukrishnan S, Jiang H, Blissard GW et al (2015a) Overview of chitin metabolism enzymes in Manduca sexta: identification, domain organization, phylogenetic analysis and gene expression. Insect Biochem Mol Biol 62:114–126

    Article  CAS  PubMed  Google Scholar 

  • Tetreau G, Dittmer NT, Cao X, Agrawal S, Chen YR, Muthukrishnan S et al (2015b) Analysis of chitin-1 binding proteins from Manduca sexta provides new insights into evolution of peritrophin A type chitin-binding domains in insects. Insect Biochem Mol Biol 62:27–41

    Google Scholar 

  • Thompson SN (2002) Trehalose – the insect ‘blood’ sugar. Adv Insect Physiol 31:205–285

    Article  CAS  Google Scholar 

  • Thummel CS (2002) Ecdysone-regulated puff genes 2000. Insect Biochem Mol Biol 32:113–120

    Article  CAS  PubMed  Google Scholar 

  • Togawa T, Dunn WA, Emmons AC, Willis JH (2007) CPF and CPFL, two related gene families encoding cuticular proteins of Anopheles gambiae and other insects. Insect Biochem Mol Biol 37:675–688

    Article  CAS  PubMed  Google Scholar 

  • Togawa T, Natkato H, Izumi S (2004) Analysis of the chitin recognition mechanim of cuticle proteins from the soft cuticle of the silkworm, Bombyx mori. Insect Biochem Mol Biol 34:1059–1067

    Article  CAS  PubMed  Google Scholar 

  • Tomiya N, Narang S, Park J, Abdul-Rahman B, Choi O, Singh S et al (2006) Purification, characterization, and cloning of a Spodoptera frugiperda Sf9 β-N-acetylhexosaminidase that hydrolyzes terminal N-acetylglucosamine on the N-glycan core. J Biol Chem 281:19545–19560

    Article  CAS  PubMed  Google Scholar 

  • Tonning A, Helms S, Schwarz H, Uv AE, Moussian B (2006) Hormonal regulation of mummy is needed for apical extracellular matrix formation and epithelial morphogenesis in Drosophila. Development 133:331–341

    Article  CAS  PubMed  Google Scholar 

  • Toprak U, Erlandson M, Baldwin D, Karcz S, Wan L, Coutu C et al (2016) Identification of the Mamestra configurata (Lepidoptera: Noctuidae) peritrophic matrix proteins and enzymes involved in peritrophic matrix chitin metabolism. Insect Sci 23:656–674

    Article  CAS  PubMed  Google Scholar 

  • Tsigos I, Martinou A, Kafetzopoulos D, Bouriotis V (2000) Chitin deacetylases: new, versatile tools in biotechnology. Trends Biotechnol 18:305–312

    Article  CAS  PubMed  Google Scholar 

  • Valdivieso MH, Duran A, Roncero C (1999) Chitin synthases in yeast and fungi. Experientia Supplementrum 87:55–69

    CAS  Google Scholar 

  • Vannini L, Bowen JH, Reed TW, Willis JH (2015) The CPCFC cuticular protein family: Anatomical and cuticular locations in Anopheles gambiae and distribution throughout Pancrustacea. Insect Biochem Mol Biol 65:57–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vincent JF, Wegst UG (2004) Design and mechanical properties of insect cuticle. Arthropod Struct Dev 33:187–199

    Article  PubMed  Google Scholar 

  • Wang P, Granados RR (1997) An intestinal mucin is the target substrate for a baculovirus enhancin. Proc Natl Acad Sci USA 94:6977–6982

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Granados RR (2000) Calcofluor disrupts the midgut defense system in insects. Insect Biochem Mol Biol 30:135–143

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Jayaram SA, Hemphala J, Senti KA, Tsarouhas V, Jin H et al (2006) Septatejunction- dependent luminal deposition of chitin deacetylases restricts tube elongation in the Drosophila trachea. Curr Biol 16:180–185

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Fan HW, Huang HJ, Xue J, Wu WJ, Bao YY et al (2012) Chitin synthase 1 gene and its two alternative splicing variants from two sap-sucking insects, Nilaparvata lugens and Laodelphax striatellus (Hemiptera: Delphacidae). Insect Biochem Mol Biol 42:637–646

    Article  CAS  PubMed  Google Scholar 

  • Wienholds E, Plasterk RH (2005) MicroRNA function in animal development. FEBS Lett 579:5911–5922

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Willis JH (2010) Structural cuticular proteins from arthropods: annotation, nomenclature, and sequence characteristics in the genomics era. Insect Biochem Mol Biol 40:189–204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willis JH, Papandreou NC, Iconomidou VA, Hamodrakas SJ (2012) Cuticular proteins. In: Li Gilbert (ed) Insect molecular biology and biochemistry. Academic, San Diego, pp 134–166

    Chapter  Google Scholar 

  • World Health Organization (2017) World malaria report 2017. Switzerland, World Health Organization, Geneva, p 160

    Book  Google Scholar 

  • Xi Y, Pan PL, Ye YX, Yu B, Zhang CX (2014) Chitin deacetylase family genes in the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). Insect Mol Biol 23:695–705

    Article  CAS  PubMed  Google Scholar 

  • Xi Y, Pan PL, Ye YX, Yu B, Xu HJ, Zhang CX (2015) Chitinase-like gene family in the brown planthopper, Nilaparvata lugens. Insect Biochem Mol Biol 24:29–40

    Article  CAS  Google Scholar 

  • Yang ML, Wang YL, Jiang F, Song TQ, Wang HM, Liu Q et al (2016) miR-71 and miR-263 Jointly regulate target genes chitin synthase and chitinase to control locust molting. PLoS Genet 12:e1006257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Q, Liu T, Liu FY, Qu MB, Qian XH (2008) A novel β-N-acetyl-D-hexosaminidase from the insect Ostrinia furnacalis (Guenée). FEBS J 275:5690–5702

    Article  CAS  PubMed  Google Scholar 

  • Yang WJ, Wu YB, Chen L, Xu KK, Xie YF, Wang JJ (2015) Two chitin biosynthesis pathway genes in Bactrocera dorsalis (Diptera: Tephritidae): molecular characteristics, expression patterns, and roles in larval-pupal transition. J Econ Entomol 108:2433–2442

    Article  CAS  PubMed  Google Scholar 

  • Yang WJ, Xu KK, Cong L, Wang JJ (2013) Identification, mRNA expression, and functional analysis of chitin synthase 1 gene and its two alternative splicing variants in oriental fruit fly, Bactrocera dorsalis. Int J Biol Sci 9:331–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao Q, Zhang DW, Tang B, Chen J, Chen J, Lu L et al (2010) Identification of 20-hydroxyecdysone late-response genes in the chitin biosynthesis pathway. PLoS ONE 5:e14058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao TP, Forman BM, Jiang Z, Cherbas L, Chen JD, McKeown M et al (1993) Functional ecdysone receptor is the product of EcR and Ultraspiracle genes. Nature 366:476–479

    Article  CAS  PubMed  Google Scholar 

  • Yu RR, Liu WM, Li DQ, Zhao XM, Ding GW, Zhang M et al (2016) Helicoidal organization of chitin in the cuticle of the migratory locust requires the function of the chitin deacetylase2 enzyme (LmCDA2). J Biol Chem 291:24352–24363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu X, Zhou Q, Li SC, Luo Q, Cai Y, Lin WC et al (2008) The silkworm (Bombyx mori) microRNAs and their expressions in multiple developmental stages. PLoS ONE 3:e2997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zen KC, Choi HK, Nandigama K, Muthukrishnan S, Kramer KJ (1996) Cloning, expression and hormonal regulation of an insect β-N-acetylglucosaminidase gene. Insect Biochem Mol Biol 26:435–444

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Liu X, Li D, Sun Y, Guo Y, Ma E et al (2010) Silencing of two alternative splicing derived mRNA variants of chitin synthase 1 gene by RNAi is lethal to the oriental migratory locust, Locusta migratoria manilensis (Meyen). Insect Biochem Mol Biol 40:824–833

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Zhang X, Arakane Y, Muthukrishnan S, Kramer KJ, Ma E et al (2011) Comparative genomic analysis of chitinase and chitinase-like genes in the African malaria mosquito (Anopheles gambiae). PLoS ONE 6:e19899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang D, Chen J, Yao Q, Pan Z, Chen J, Zhang W (2012a) Functional analysis of two chitinase genes during the pupation and eclosion stages of the beet armyworm Spodoptera exigua by RNA interference. Arch Insect Biochem Physiol 79:220–234

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Zhang J, Park Y, Zhu KY (2012b) Identification and characterization of two chitin synthase genes in African malaria mosquito, Anopheles gambiae. Insect Biochem Mol Biol 42:674–682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao LN, Yang MM, Shen QD, Shi ZK, Wang SG, Tang B (2016) Knockdown of three trehalases regulating trehalose and chitin metabolism in the rice brown planthopper Nilaparvata lugens. Sci Rep 6:27841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao XM, Gou X, Qin ZY, Li DQ, Wang Y, Ma EB et al (2017) Identification and expression of cuticular protein genes based on Locusta migratoria transcriptome. Sci Rep 7:45462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng YP, Retnakaran A, Krell PJ, Arif BM, Primavera M, Feng QL (2003) Temporal, spatial and induced expression of chitinase in the spruce budworm, Choristoneura fumiferana. J Insect Physiol 49:241–247

    Article  CAS  PubMed  Google Scholar 

  • Zhong Y-S, Mita K, Shimada T, Kawasaki H (2006) Glycine-rich protein genes, which encode a major component of the cuticle protein genes in Bombyx mori. Insect Biochem Mol Biol 36:99–110

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Badgett MJ, Orlando R, Willis JH (2019) Proteomics reveals localization of cuticular proteins in Anopheles gambiae. Insect Biochem Mol Biol 104:91–105

    Google Scholar 

  • Zhu KY, Merzendorfer H, Zhang W, Zhang J, Muthukrishnan S (2016) Biosynthesis, turnover, and functions of chitin in insects. Annu Rev Entomol 61:177–196

    Article  CAS  PubMed  Google Scholar 

  • Zhu Q, Arakane Y, Banerjee D, Beeman RW, Kramer KJ, Muthukrishnan S (2008a) Domain organization and phylogenetic analysis of the chitinase-like family of proteins in three species of insects. Insect Biochem Mol Biol 38:452–466

    Article  CAS  PubMed  Google Scholar 

  • Zhu Q, Arakane Y, Beeman RW, Kramer KJ, Muthukrishnan S (2008b) Functional specialization among insect chitinase family genes revealed by RNA interference. Proc Natl Acad Sci USA 105:6650–6655

    Article  PubMed  Google Scholar 

  • Zhu Q, Deng Y, Vanka P, Brown SJ, Muthukrishnan S, Kramer KJ (2004) Computational identification of novel chitinase-like proteins in the Drosophila melanogaster genome. Bioinformatics 20:161–169

    Article  CAS  PubMed  Google Scholar 

  • Zhu YC, Specht CA, Dittmer NT, Muthukrishnan S, Kanost MR, Kramer KJ (2002) Sequence of a cDNA and expression of the gene encoding a putative epidermal chitin synthase of Manduca sexta. Insect Biochem Mol Biol 32:1497–1506

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

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Acknowledgements

We acknowledge that many relevant studies could not be cited due to space restrictions. We thank Dr. Qing Yang for her invitation to write this chapter. Relevant research conducted in the authors’ laboratories was supported by the grants from the National Natural Science Foundation of China (Grant Nos. 31730074, 31672364) and the Kansas Agricultural Experiment Station, Manhattan, Kansas (KS 362, KS471). This manuscript has contribution no. 19-139-B from the Kansas Agricultural Experiment Station, Kansas State University, Manhattan, Kansas, USA.

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Liu, X., Zhang, J., Zhu, K.Y. (2019). Chitin in Arthropods: Biosynthesis, Modification, and Metabolism. In: Yang, Q., Fukamizo, T. (eds) Targeting Chitin-containing Organisms. Advances in Experimental Medicine and Biology, vol 1142. Springer, Singapore. https://doi.org/10.1007/978-981-13-7318-3_9

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