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Cell and Tissue Research

, Volume 377, Issue 3, pp 505–525 | Cite as

The amazing complexity of insect midgut cells: types, peculiarities, and functions

  • Silvia Caccia
  • Morena Casartelli
  • Gianluca TettamantiEmail author
Review

Abstract

The insect midgut epithelium represents an interface between the internal and the external environment and it is the almost unique epithelial tissue by which these arthropods acquire nutrients. This epithelium is indeed able to produce digestive enzymes and to support vectorial transport of small organic nutrients, ions, and water. Moreover, it plays a key role in the defense against pathogenic microorganisms and in shaping gut microbiota. Another important midgut function is the ability to produce signaling molecules that regulate its own physiology and the activity of other organs. The two main mature cell types present in the midgut of all insects, i.e., columnar and endocrine cells, are responsible for these functions. In addition, stem cells, located at the base of the midgut epithelium, ensure the growth and renewal of the midgut during development and after injury. In insects belonging to specific orders, midgut physiology is deeply conditioned by the presence of unique cell types, i.e., goblet and copper cells, which confer peculiar features to this organ. This review reports current knowledge on the cells that form the insect midgut epithelium, focusing attention on their morphological and functional features. Notwithstanding the apparent structural simplicity of this organ, the properties of the cells make the midgut a key player in insect development and homeostasis.

Keywords

Insect midgut Midgut lumen pH Columnar cell Stem cell Endocrine cell Goblet cell Copper cell 

Notes

Acknowledgments

The authors apologize to colleagues whose work could not be cited due to space limitation. We are thankful to Daniele Bruno and Aurora Montali for figure preparation.

Funding

This work was financially supported by Fondazione Cariplo (grant no. 2014-0550) and by Ministero dell’Istruzione, dell’Università e della Ricerca (MIUR) (grant nos. 2017J8JR57 and 2017JLN833).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.

References

  1. Amcheslavsky A, Song W, Li Q, Nie Y, Bragatto I, Ferrandon D, Perrimon N, Ip YT (2014) Enteroendocrine cells support intestinal stem-cell-mediated homeostasis in Drosophila. Cell Rep 9:32–39Google Scholar
  2. Andriès JC, Tramu G (1985) Ultrastructural and immunohistochemical study of endocrine cells in the midgut of the cockroach Blaberus craniifer (Insecta, Dictyoptera). Cell Tissue Res 240:323–332Google Scholar
  3. Azevedo DO, Neves CA, dos Santos Mallet JR, Monte Gonçalves TC, Zanuncio JC, Serrão JE (2009) Notes on midgut ultrastructure of Cimex hemipterus (Hemiptera: Cimicidae). J Med Entomol 46:435–441Google Scholar
  4. Azuma M, Harvey WR, Wieczorek H (1995) Stoichiometry of K+/H+ antiport helps to explain extracellular pH 11 in a model epithelium. FEBS Lett 361:153–156Google Scholar
  5. Baines D, Brownwright A, Schwartz JL (1994) Establishment of primary and continuous cultures of epithelial cells from larval lepidopteran midguts. J Insect Physiol 40:347–357Google Scholar
  6. Baldwin KM, Hakim RS (1987) Change of form of septate and gap junctions during development of the insect midgut. Tissue Cell 19:549–558Google Scholar
  7. Baldwin KM, Hakim R (1991) Growth and differentiation of the larval midgut epithelium during molting in the moth, Manduca sexta. Tissue Cell 23:411–422Google Scholar
  8. Baton LA, Ranford-Cartwright LC (2007) Morphological evidence for proliferative regeneration of the Anopheles stephensi midgut epithelium following Plasmodium falciparum ookinete invasion. J Invertebr Pathol 96:244–254Google Scholar
  9. Billingsley PF (1990) The midgut ultrastructure of hematophagous insects. Annu Rev Entomol 35:219–248Google Scholar
  10. Billingsley PF, Lehane MJ (1996) Structure and ultrastructure of the insect midgut. In: Lehane MJ, Billingsley PF (eds) Biology of the insect midgut. Chapman & Hall, London, pp 3–30Google Scholar
  11. Biteau B, Hochmuth CE, Jasper H (2008) JNK activity in somatic stem cells causes loss of tissue homeostasis in the aging Drosophila gut. Cell Stem Cell 3:442–455Google Scholar
  12. Bonelli M, Bruno D, Caccia S, Sgambetterra G, Cappellozza S, Jucker C, Tettamanti G, Casartelli M (2019) Structural and functional characterization of Hermetia illucens larval midgut. Front Physiol 10:204.  https://doi.org/10.3389/fphys.2019.00204 Google Scholar
  13. Bonfanti P, Colombo A, Heintzelman MB, Mooseker MS, Camatini M (1992) The molecular architecture of an insect midgut brush border cytoskeleton. Eur J Cell Biol 57:298–307Google Scholar
  14. Bonfini A, Liu X, Buchon N (2016) From pathogens to microbiota: how Drosophila intestinal stem cells react to gut microbes. Dev Comp Immunol 64:22–38.  https://doi.org/10.1016/j.dci.2016.02.008 Google Scholar
  15. Bonning BC, Chougule NP (2014) Delivery of intrahemocoelic peptides for insect pest management. Trends Biotechnol 32:91–98Google Scholar
  16. Broderick NA (2016) Friend, foe or food? Recognition and the role of antimicrobial peptides in gut immunity and Drosophila-microbe interactions. Philos Trans R Soc B 371:20150295.  https://doi.org/10.1098/rstb.2015.0295 Google Scholar
  17. Broderick NA, Buchon N, Lemaitre B (2014) Microbiota-induced changes in Drosophila melanogaster host gene expression and gut morphology. mBio 5:e01117–e01114.  https://doi.org/10.1128/mBio.01117-14 Google Scholar
  18. Bruno D, Bonelli M, De Filippis F, Di Lelio I, Tettamanti G, Casartelli M, Ercolini D, Caccia S (2019a) The intestinal microbiota of Hemetia illucens larvae is affected by diet and shows a diverse composition in different midgut regions. Appl Environ Microbiol 85:e1864–e1818.  https://doi.org/10.1128/AEM.01864-18 Google Scholar
  19. Bruno D, Bonelli M, Cadamuro AG, Reguzzoni M, Grimaldi A, Casartelli M, Tettamanti G (2019b) The digestive system of the adult Hermetia illucens (Diptera: Stratiomyidae): morphological features and functional properties. Cell Tissue Res in press.  https://doi.org/10.1007/s00441-019-03025-7
  20. Buchon N, Osman D (2015) All for one and one for all: regionalization of the Drosophila intestine. Insect Biochem Mol Biol 67:2–8Google Scholar
  21. Buchon N, Broderick NA, Lemaitre B (2013a) Gut homeostasis in a microbial world: insights from Drosophila melanogaster. Nat Rev Microbiol 11:615–626Google Scholar
  22. Buchon N, Osman D, David FPA, Fang HY, Boquete JP, Deplancke B, Lemaitre B (2013b) Morphological and molecular characterization of adult midgut compartmentalization in Drosophila. Cell Rep 3:1725–1738Google Scholar
  23. Caccia S, Leonardi MG, Casartelli M, Grimaldi A, de Eguileor PF, Giordana B (2005) Nutrient absorption by Aphidius ervi larvae. J Insect Physiol 51:1183–1192Google Scholar
  24. Caccia S, Casartelli M, Grimaldi A, Losa E, de Eguileor M, Pennacchio F, Giordana B (2007) Unexpected similarity of intestinal sugar absorption by SGLT1 and apical GLUT2 in an insect (Aphidius ervi, Hymenoptera) and mammals. Am J Physiol Regul Integr Comp Physiol 292:R2284–R2291Google Scholar
  25. Casartelli M, Leonardi MG, Fiandra L, Parenti P, Giordana B (2001) Multiple transport pathways for dibasic amino acids in the larval midgut of the silkworm Bombyx mori. Insect Biochem Mol Biol 31:621–632Google Scholar
  26. Casartelli M, Corti P, Cermenati G, Grimaldi A, Fiandra L, Santo N, Pennacchio F, Giordana B (2005) Absorption of albumin by the midgut of a lepidopteran larva. J Insect Physiol 51:933–940Google Scholar
  27. Casartelli M, Corti P, Giovanna Leonardi M, Fiandra L, Burlini N, Pennacchio F, Giordana B (2007) Absorption of horseradish peroxidase in Bombyx mori larval midgut. J Insect Physiol 53:517–525Google Scholar
  28. Casartelli M, Cermenati G, Rodighiero S, Pennacchio F, Giordana B (2008) A megalin-like receptor is involved in protein endocytosis in the midgut of an insect (Bombyx mori, Lepidoptera). Am J Physiol Regul Integr Comp Physiol 295:R1290–R1300Google Scholar
  29. Castagnola A, Jurat-Fuentes JL (2016) Intestinal regeneration as an insect resistance mechanism to entomopathogenic bacteria. Curr Opin Insect Sci 15:104–110Google Scholar
  30. Cermenati G, Terracciano I, Castelli I, Giordana B, Rao R, Pennacchio F, Casartelli M (2011) The CPP Tat enhances eGFP cell internalization and transepithelial transport by the larval midgut of Bombyx mori (Lepidoptera, Bombycidae). J Insect Physiol 57:1689–1697Google Scholar
  31. Chapman RF (2013) The insects: structure and function. Simpson SJ, Douglas AE (eds) Cambridge University Press, CambridgeGoogle Scholar
  32. Chen J, Kim S, Kwon JY (2016) A systematic analysis of Drosophila regulatory peptide expression in enteroendocrine cells. Mol Cells 39:358–366Google Scholar
  33. Chng WB, Bou Sleiman MS, Schupfer F, Lemaitre B (2014) Transforming growth factor β/activin signaling functions as a sugar-sensing feedback loop to regulate digestive enzyme expression. Cell Rep 9:336–348Google Scholar
  34. Cioffi M (1979) The morphology and fine structure of the larval midgut of a moth (Manduca sexta) in relation to active ion transport. Tissue Cell 11:467–479Google Scholar
  35. Cioffi M (1984) Comparative ultrastructure of arthropod transporting epithelia. Amer Zool 24:139–156Google Scholar
  36. Clark TM (1999) Evolution and adaptive significance of larval midgut alkalinization in the insect superorder mecopterida. J Chem Ecol 25:1945–1960Google Scholar
  37. Clem RJ, Passarelli AL (2013) Baculoviruses: sophisticated pathogens of insects. PLoS Pathog 9(11):e1003729.  https://doi.org/10.1371/journal.ppat.1003729 Google Scholar
  38. Clissold FJ, Tedder BJ, Conigrave AD, Simpson SJ (2010) The gastrointestinal tract as a nutrient-balancing organ. Proc Biol Sci 277:1751–1759Google Scholar
  39. Colombani J, Bianchini L, Layalle S, Pondeville E, DauphinVillemant C, Antoniewski C, Carré C, Noselli S, Léopold P (2005) Antagonistic actions of ecdysone and insulins determine final size in Drosophila. Science 310:667–670Google Scholar
  40. Cotter K, Stransky L, McGuire C, Forgac M (2015) Recent insights into the structure, regulation, and function of the V-ATPases. Trends Biochem Sci 40:611–622Google Scholar
  41. de Eguileor M, Grimaldi A, Tettamanti G, Valvassori R, Leonardi MG, Giordana B, Tremblay E, Digilio MG, Pennacchio F (2001) Larval anatomy and structure of absorbing epithelia in the aphid parasitoid Aphidius ervi Haliday (Hymenoptera, Braconidae). Arthropod Struct Dev 30:27–37Google Scholar
  42. de Sousa G, Conte H (2013) Midgut morphophysiology in Sitophilus zeamais Motschulsky, 1855 (Coleoptera: Curculionidae). Micron 51:1–8Google Scholar
  43. Delanoue R, Slaidina M, Léopold P (2010) The steroid hormone ecdysone controls systemic growth by repressing dMyc function in Drosophila fat cells. Dev Cell 18:1012–1102Google Scholar
  44. Docampo R (2016) The origin and evolution of the acidocalcisome and its interactions with other organelles. Mol Biochem Parasitol 209:3–9Google Scholar
  45. Douglas AE (2015) Multiorganismal insects: diversity and function of resident microorganisms. Annu Rev Entomol 60:17–34Google Scholar
  46. Dow JAT (1986) Insect midgut function. Adv Insect Physiol 19:187–328Google Scholar
  47. Dow JAT (1992) pH gradients in lepidopteran midgut. J Exp Biol 172:355–375Google Scholar
  48. Dubovskiy IM, Grizanova EV, Whitten MM, Mukherjee K, Greig C, Alikina T, Kabilov M, Vilcinskas A, Glupov VV, Butt TM (2016) Immuno-physiological adaptations confer wax moth Galleria mellonella resistance to Bacillus thuringiensis. Virulence 7:860–870Google Scholar
  49. Dubreuil RR (2004) Copper cells and stomach acid secretion in the Drosophila midgut. Int J Biochem Cell Biol 36:742–752Google Scholar
  50. Dubreuil RR, Frankel J, Wang P, Howrylak J, Kappil M, Grushko T (1998) Mutations of α spectrin and labial block cuprophilic cell differentiation and acid secretion in the middle midgut of Drosophila larvae. Dev Biol 194:1–11Google Scholar
  51. Dubreuil RR, Grushko T, Baumann O (2001) Differential effects of a labial mutation on the development, structure, and function of stomach acid secreting cells in Drosophila larvae and adults. Cell Tissue Res 306:167–178Google Scholar
  52. Dunkov BC, Georgieva T, Yoshiga T, Hall M, Law JH (2002) Aedes aegypti ferritin heavy chain homologue: feeding of iron or blood influences message levels, lengths and subunit abundance. J Insect Sci 2:7 insectscience.org/2.7Google Scholar
  53. Erkosar B, Defaye A, Bozonnet N, Puthier D, Royet J, Leulieret F (2014) Drosophila microbiota modulates host metabolic gene expression via IMD/NF-kB signaling. PLoS One 9(4):e94729.  https://doi.org/10.1371/journal.pone.0094729 Google Scholar
  54. Fernandes KM, Neves CA, Serrão JE, Martins GF (2014) Aedes aegypti midgut remodeling during metamorphosis. Parasitol Int 63:506–512Google Scholar
  55. Fiandra L, Caccia S, Giordana B, Casartelli M (2010) Leucine transport by the larval midgut of the parasitoid Aphidius ervi (Hymenoptera). J Insect Physiol 56:165–169Google Scholar
  56. Filshie BK, Poulson DF, Waterhouse DF (1971) Ultrastructure of the copper-accumulating region of the Drosophila larval midgut. Tissue Cell 3:77–102Google Scholar
  57. Franzetti E, Huang ZJ, Shi YX, Xie K, Deng XJ, Li JP, Li QR, Yang WY, Zeng WN, Casartelli M, Deng HM, Cappellozza S, Grimaldi A, Xia Q, Feng Q, Cao Y, Tettamanti G (2012) Autophagy precedes apoptosis during the remodeling of silkworm larval midgut. Apoptosis 17:305–324Google Scholar
  58. Franzetti E, Romanelli D, Caccia S, Cappellozza S, Congiu T, Rajagopalan M, Grimaldi A, de Eguileor M, Casartelli M, Tettamanti G (2015) The midgut of the silkmoth Bombyx mori is able to recycle molecules derived from degeneration of the larval midgut epithelium. Cell Tissue Res 361:509–528Google Scholar
  59. Franzetti E, Casartelli M, D’Antona P, Montali A, Romanelli D, Cappellozza S, Caccia S, Grimaldi A, de Eguileor M, Tettamanti G (2016) Midgut epithelium in molting silkworm: a fine balance among cell growth, differentiation, and survival. Arthropod Struct Dev 45:368–379Google Scholar
  60. Fujita T, Yui R, Iwanaga T, Nishiitsutsuji-Uwo J, Endo Y, Yanaihara N (1981) Evolutionary aspects of “brain-gut peptides”: an immunohistochemical study. Peptides 2:123–131Google Scholar
  61. Furuse M, Izumi Y (2017) Molecular dissection of smooth septate junctions: understanding their roles in arthropod physiology. Ann N Y Acad Sci 1397:17–24Google Scholar
  62. Geminard C, Rulifson EJ, Léopold P (2009) Remote control of insulin secretion by fat cells in Drosophila. Cell Metab 10:199–207Google Scholar
  63. Gervais L, Bardin AJ (2017) Tissue homeostasis and aging: new insight from the fly intestine. Curr Opin Cell Biol 48:97–105Google Scholar
  64. Giordana B, Sacchi VF, Hanozet GM (1982) Intestinal amino acid absorption in lepidopteran larvae. Biochim Biophys Acta 692:81–88Google Scholar
  65. Giordana B, Sacchi VF, Parenti P, Hanozet GM (1989) Amino acid transport systems in intestinal brush-border membranes from lepidopteran larvae. Am J Physiol Regul Integr Comp Physiol 257:R494–R500Google Scholar
  66. Giordana B, Leonardi MG, Tasca M, Villa M, Parenti P (1994) The amino acid/K+ symporters for neutral amino acids along the midgut of lepidopteran larvae: functional differentiations. J Insect Physiol 40:1059–1068Google Scholar
  67. Giordana B, Leonardi MG, Casartelli M, Consonni P, Parenti P (1998) K+-neutral amino acid symport of Bombyx mori larval midgut: a system operative in extreme conditions. Am J Physiol Regul Integr Comp Physiol 274:R1361–R1371Google Scholar
  68. Godoy RS, Fernandes KM, Martins GF (2015) Midgut of the non-hematophagous mosquito Toxorhynchites theobaldi (Diptera, Culicidae). Sci Rep 5:15836.  https://doi.org/10.1038/srep15836 Google Scholar
  69. Gomes FM, Carvalho DB, Peron AC, Saito K, Miranda K, Machado EA (2012) Inorganic polyphosphates are stored in spherites within the midgut of Anticarsia gemmatalis and play a role in copper detoxification. J Insect Physiol 58:211–219Google Scholar
  70. Gomes FM, Carvalho DB, Machado EA, Miranda K (2013) Ultrastructural and functional analysis of secretory goblet cells in the midgut of the lepidopteran Anticarsia gemmatalis. Cell Tissue Res 352:313–326Google Scholar
  71. Goto S, Loeb MJ, Takeda M (2005) Bombyxin stimulates proliferation of cultured stem cells derived from Heliothis virescens and Mamestra brassicae larvae. In Vitro Cell Dev Biol Anim 41:38–42Google Scholar
  72. Guo Z, Lucchetta E, Rafel N, Ohlstein B (2016) Maintenance of the adult Drosophila intestine: all roads lead to homeostasis. Curr Opin Genet Dev 40:81–86Google Scholar
  73. Ha EM, Oh CT, Bae YS, Lee WJ (2005) A direct role for dual oxidase in Drosophila gut immunity. Science 310:847–850Google Scholar
  74. Hakim RS, Blackburn MB, Corti P, Gelman DB, Goodman C, Elsen K, Loeb MJ, Lynn D, Soin T, Smagghe G (2007) Growth and mitogenic effects of arylphorin in vivo and in vitro. Arch Insect Biochem Physiol 64:63–73Google Scholar
  75. Hakim RS, Baldwin K, Smagghe G (2010) Regulation of midgut growth, development, and metamorphosis. Annu Rev Entomol 55:593–608Google Scholar
  76. Hartenstein V (1997) Development of the insect stomatogastric nervous system. Trends Neurosci 20:421–427Google Scholar
  77. Harvey WR (1980) Water and ions in the gut. In: Locke M, Smith DS (eds) Insect biology in the future. “VBW 80” Academic Press, New York, pp 105–119Google Scholar
  78. Harvey WR, Cioffi M, Wolfersberger MG (1981) Portasomes as coupling factors in active ion transport and oxidative phosphorylation. Am Zool 21:775–791Google Scholar
  79. Hegedus D, Erlandson M, Gillott C, Toprak U (2009) New insights into peritrophic matrix synthesis, architecture, and function. Annu Rev Entomol 54:285–302Google Scholar
  80. Holtof M, Lenaerts C, Cullen D, Vanden Broeck J (2019) Extracellular nutrient digestion and absorption in the insect gut. Cell Tissue Res in press.  https://doi.org/10.1007/s00441-019-03031-9
  81. Huang JH, Jing X, Douglas AE (2015) The multi-tasking gut epithelium of insects. Insect Biochem Mol Biol 67:15–20Google Scholar
  82. Hubert JF, Thomas D, Cavalier A, Gouranton J (1989) Structural and biochemical observations on specialized membranes of the “filter chamber”, a water-shunting complex in sap-sucking homopteran insects. Biol Cell 66:155–163Google Scholar
  83. Hudry B, Khadayate S, Miguel-Aliaga I (2016) The sexual identity of adult intestinal stem cells controls organ size and plasticity. Nature 530:344–348Google Scholar
  84. Hughes SR, Dowd PF, Johnson ET (2012) Cell-penetrating recombinant peptides for potential use in agricultural pest control applications. Pharmaceuticals 5:1054–1063Google Scholar
  85. Illa-Bochaca I, Montuenga LM (2006) The regenerative nidi of the locust midgut as a model to study epithelial cell differentiation from stem cells. J Exp Biol 209:2215–2223Google Scholar
  86. Iwanaga T, Fujita T, Nishiitsutsuji-Uwo J, Endo Y (1981) Immunohistochemical demonstration of PP-, somatostatin-, enteroglucagon- and VIP-like immunoreactivities in the cockroach midgut. Biomed Res 2:202–207Google Scholar
  87. Janeh M, Osman D, Kambris Z (2017) Damage-induced cell regeneration in the midgut of Aedes albopictus mosquitoes. Sci Rep 7:44594.  https://doi.org/10.1038/srep44594 Google Scholar
  88. Jeffers LA, Roe MR (2008) The movement of proteins across the insect and tick digestive system. J Insect Physiol 54:319–332Google Scholar
  89. Jiang H, Tian A, Jiang J (2016) Intestinal stem cell response to injury: lessons from Drosophila. Cell Mol Life Sci 73:3337–3349Google Scholar
  90. Jura CZ (1958) The alimentary canal of Tetrodontophora bielanensis (Waga) (Collembola). Pol Pismo Entomol 27:85–89Google Scholar
  91. Kane PM (1995) Disassembly and reassembly of the yeast vacuolar H+-ATPase in vivo. J Biol Chem 270:17025–17032Google Scholar
  92. Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M, Goettel MS (2015) Insect pathogens as biological control agents: back to the future. J Invertebr Pathol 132:1–41Google Scholar
  93. LaJeunesse DR, Johnson B, Presnell JS, Catignas KK, Zapotoczny G (2010) Peristalsis in the junction region of the Drosophila larval midgut is modulated by DH31 expressing enteroendocrine cells. BMC Physiol 10:14.  https://doi.org/10.1186/1472-6793-10-14 Google Scholar
  94. Le Caherec F, Guillam MT, Beuron F, Cavalier A, Thomas D, Gouranton J, Hubert JF (1997) Aquaporin-related proteins in the filter chamber of homopteran insects. Cell Tissue Res 290:143–151Google Scholar
  95. Lehane MJ (1997) Peritrophic matrix structure and function. Annu Rev Entomol 42:525–550Google Scholar
  96. Lemaitre B, Miguel-Aliaga I (2013) The digestive tract of Drosophila melanogaster. Annu Rev Genet 47:377–404Google Scholar
  97. Lemos FJ, Terra WR (1991) Digestion of bacteria and the role of midgut lysozyme in some insect larvae. Comp Biochem Physiol 100:265–268Google Scholar
  98. Lemos FJ, Ribeiro A, Terra WR (1993) A bacteria-digesting midgut lysozyme from Musca domestica (Diptera) larvae. Purification, properties and secretory mechanism. Insect Biochem Mol Biol 23:533–541Google Scholar
  99. Leonardi MG, Casartelli M, Parenti P, Giordana B (1998) Evidence for a low-affinity, high-capacity uniport for amino acids in Bombyx mori larval midgut. Am J Physiol Regul Integr Comp Physiol 274:R1372–R1375Google Scholar
  100. Leonardi MG, Caccia S, González-Cabrera J, Ferré J, Giordana B (2006) Leucine transport is affected by Bacillus thuringiensis Cry1 toxins in brush border membrane vesicles from Ostrinia nubilalis Hb (Lepidoptera: Pyralidae) and Sesamia nonagrioides Lefebvre (Lepidoptera: Noctuidae) midgut. J Membr Biol 214:157–164Google Scholar
  101. Li S, Torre-Muruzabal T, Sogaard KC, Ren GR, Hauser F, Engelsen SM, Podenphanth MD, Desjardins A, Grimmelikhuijzen CJ (2013) Expression patterns of the Drosophila neuropeptide CCHamide-2 and its receptor may suggest hormonal signaling from the gut to the brain. PLoS One 8:e76131.  https://doi.org/10.1371/journal.pone.0076131 Google Scholar
  102. Li H, Qi Y, Jasper H (2016) Ubx dynamically regulates Dpp signaling by repressing Dad expression during copper cell regeneration in the adult Drosophila midgut. Dev Biol 419:373–381Google Scholar
  103. Lin G, Xu N, Xi R (2008) Paracrine wingless signalling controls self-renewal of Drosophila intestinal stem cells. Nature 455:1119–1123Google Scholar
  104. Loeb MJ, Coronel N, Natsukawa D, Takeda M (2004) Implications for the functions of the four known midgut differentiation factors: an immunohistologic study of Heliothis virescens midgut. Arch Insect Biochem Physiol 56:7–20Google Scholar
  105. Lucchetta EM, Ohlstein B (2012) The Drosophila midgut: a model for stem cell driven tissue regeneration. Wiley Interdiscip Rev Dev Biol 1:781–788Google Scholar
  106. Malta J, Heerman M, Weng JL, Fernandes KM, Martins GF, Ramalho-Ortigão M (2017) Midgut morphological changes and autophagy during metamorphosis in sand flies. Cell Tissue Res 368:513–529Google Scholar
  107. Marianes A, Spradling AC (2013) Physiological and stem cell compartmentalization within the Drosophila midgut. Elife 2:e00886.  https://doi.org/10.7554/eLife.00886 Google Scholar
  108. Martins GF, Neves CA, Campos LA, Serrão JE (2006) The regenerative cells during the metamorphosis in the midgut of bees. Micron 37:161–168Google Scholar
  109. Mattila J, Kokki K, Hietakangas V, Boutros M (2018) Stem cell intrinsic hexosamine metabolism regulates intestinal adaptation to nutrient content. Dev Cell 47:112–121Google Scholar
  110. McLeod CJ, Wang L, Wong C, Jones DL (2010) Stem cell dynamics in response to nutrient availability. Curr Biol 20:2100–2105Google Scholar
  111. McNulty M, Puljung M, Jefford G, Dubreuil RR (2001) Evidence that a copper-metallothionein complex is responsible for fluorescence in acid secreting cells of the Drosophila stomach. Cell Tissue Res 304:383–389Google Scholar
  112. Miguel-Aliaga I, Jasper H, Lemaitre B (2018) Anatomy and physiology of the digestive tract of Drosophila melanogaster. Genetics 210:357–396Google Scholar
  113. Mirth C, Truman JW, Riddiford LM (2005) The role of the prothoracic gland in determining critical weight for metamorphosis in Drosophila melanogaster. Curr Biol 15:1796–1807Google Scholar
  114. Moffett DF, Koch A (1992) Driving forces and pathways for H+ and K+ transport in insect midgut cells. J Exp Biol 172:403–415Google Scholar
  115. Moffett DF, Koch A, Woods R (1995) Electrophysiology of K+ transport by midgut epithelium of lepidopteran insect larvae. III Goblet valve patency. J Exp Biol 198:2103–2113Google Scholar
  116. Monteiro EC, Tamaki FK, Terra WR, Ribeiro AF (2014) The digestive system of the “stick bug” Cladomorphus phyllinus (Phasmida, Phasmatidae): a morphological, physiological and biochemical analysis. Arthropod Struct Dev 43:123–134Google Scholar
  117. Mylonakis E, Podsiadlowski L, Muhammed M, Vilcinskas A (2016) Diversity, evolution and medical applications of insect antimicrobial peptides. Phil Trans R Soc B 371:20150290.  https://doi.org/10.1098/rstb.2015.0290 Google Scholar
  118. Nardi JB, Bee CM (2012) Regenerative cells and the architecture of beetle midgut epithelia. J Morphol 273:1010–1020Google Scholar
  119. Nardi JB, Bee CM, Miller LA (2010) Stem cells of the beetle midgut epithelium. J Insect Physiol 56:296–303Google Scholar
  120. Nászai M, Carroll LR, Cordero JB (2015) Intestinal stem cell proliferation and epithelial homeostasis in the adult Drosophila midgut. Insect Biochem Mol Biol 67:9–14Google Scholar
  121. Nation JL (2008) Insect physiology and biochemistry. CRC Press, Boca RatonGoogle Scholar
  122. Nijhout HF, Smith WA, Schachar I, Subramanian S, Tobler A, Grunert LW (2007) The control of growth and differentiation of the wing imaginal disks of Manduca sexta. Dev Biol 302:569–576Google Scholar
  123. Nishiitsutsuji-Uwo J, Endo Y (1981) Gut endocrine cells in insects: the ultrastructure of the endocrine cells in the cockroach midgut. Biomed Res 2:30–44Google Scholar
  124. O’Brien LE, Soliman SS, Li X, Bilder D (2011) Altered modes of stem cell division drive adaptive intestinal growth. Cell 147:603–614Google Scholar
  125. Obniski R, Sieber M, Spradling AC (2018) Dietary lipids modulate Notch signaling and influence adult intestinal development and metabolism in Drosophila. Dev Cell 47:98–111Google Scholar
  126. Ohlstein B, Spradling A (2006) The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439:470–474Google Scholar
  127. Okuda K, de Almeida F, Mortara RA, Krieger H, Marinotti O, Bijovsky AT (2007) Cell death and regeneration in the midgut of the mosquito, Culex quinquefasciatus. J Insect Physiol 53:1307–1315Google Scholar
  128. Overend G, Luo Y, Henderson L, Douglas AE, Davies SA, Dow JAT (2016) Molecular mechanism and functional significance of acid generation in the Drosophila midgut. Sci Rep 6:27242.  https://doi.org/10.1038/srep27242 Google Scholar
  129. Pabla N, Lange AB (1999) The distribution and myotropic activity of locustatachykinin-like peptides in locust midgut. Peptides 20:1159–1167Google Scholar
  130. Padilha MHP, Pimentel AC, Ribeiro AF, Terra WR (2009) Sequence and function of lysosomal and digestive cathepsine D-like proteinases of Musca domestica midgut. Insect Biochem Mol Biol 39:782–791Google Scholar
  131. Pardo-López L, Soberón M, Bravo A (2013) Bacillus thuringiensis insecticidal three-domain cry toxins: mode of action, insect resistance and consequences for crop protection. FEMS Microbiol Rev 37:3–22Google Scholar
  132. Parenti P, Villa M, Hanozet GM (1992) Kinetics of leucine transport in brush border membrane vesicles from lepidopteran larvae midgut. J Biol Chem 267:15391–15397Google Scholar
  133. Park JH, Kwon JY (2011) Heterogeneous expression of Drosophila gustatory receptors in enteroendocrine cells. PLoS One 6:e29022.  https://doi.org/10.1371/journal.pone.0029022 Google Scholar
  134. Park MS, Takeda M (2008) Starvation suppresses cell proliferation that rebounds after refeeding in the midgut of the American cockroach, Periplaneta americana. J Insect Physiol 54:386–392Google Scholar
  135. Park MS, Park P, Takeda M (2009) Starvation induces apoptosis in the midgut nidi of Periplaneta americana: a histochemical and ultrastructural study. Cell Tissue Res 335:631–638Google Scholar
  136. Park JH, Chen J, Jang S, Ahn TJ, Kang K, Choi MS, Kwon JY (2016) A subset of enteroendocrine cells is activated by amino acids in the Drosophila midgut. FEBS Lett 590:493–500Google Scholar
  137. Parthasarathy R, Palli SR (2008) Proliferation and differentiation of intestinal stem cells during metamorphosis of the red flour beetle, Tribolium castaneum. Dev Dyn 237:893–908Google Scholar
  138. 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 32:517–523Google Scholar
  139. Pimentel AC, Barroso IG, Ferreira JM, Dias RO, Ferreira C, Terra WR (2018) Molecular machinery of starch digestion and glucose absorption along the midgut of Musca domestica. J Insect Physiol 109:11–20Google Scholar
  140. Predel R (2001) Peptidergic neurohemal system of an insect: mass spectrometric morphology. J Comp Neurol 436:363–375Google Scholar
  141. Predel R, Neupert S, Garczynski SF, Crim JW, Brown MR, Russell WK, Kahnt J, Russell DH, Nachman RJ (2010) Neuropeptidomics of the mosquito Aedes aegypti. J Proteome Res 9:2006–2015Google Scholar
  142. Raes H, Verbeke M, Meulemans W, Coster WD (1994) Organisation and ultrastructure of the regenerative crypts in the midgut of the adult worker honeybee (L. Apis mellifera). Tissue Cell 26:231–238Google Scholar
  143. Ray K, Mercedes M, Chan D, Choi CY, Nishiura JT (2009) Growth and differentiation of the larval mosquito midgut. J Insect Sci 9:1–13Google Scholar
  144. Regan JC, Khericha M, Dobson AJ, Bolukbasi E, Rattanavirotkul N, Partridge L (2016) Sex difference in pathology of the ageing gut mediates the greater response of female lifespan to dietary restriction. Elife 5:e10956.  https://doi.org/10.7554/eLife.10956 Google Scholar
  145. Reiher W, Shirras C, Kahnt J, Baumeister S, Elwyn Isaac R, Wegener C (2011) Peptidomics and peptide hormone processing in the Drosophila midgut. J Proteome Res 10:1881–1892Google Scholar
  146. Reineke S, Wieczorek H, Merzendorfer H (2002) Expression of Manduca sexta V-ATPase genes mvB, mvG and mvd is regulated by ecdysteroids. J Exp Biol 205:1059–1067Google Scholar
  147. Rodenfels J, Lavrynenko O, Ayciriex S, Sampaio JL, Carvalho M, Shevchenko A, Eaton S (2014) Production of systemically circulating Hedgehog by the intestine couples nutrition to growth and development. Genes Dev 28:2636–2651Google Scholar
  148. Romanelli D, Casartelli M, Cappellozza S, de Eguileor M, Tettamanti G (2016) Roles and regulation of autophagy and apoptosis in the remodelling of the lepidopteran midgut epithelium during metamorphosis. Sci Rep 6:32939.  https://doi.org/10.1038/srep32939 Google Scholar
  149. Rost MM, Kuczera M, Malinowska J, Polak M, Sidor B (2005) Midgut epithelium formation in Thermobia domestica (Packard) (Insecta, Zygentoma). Tissue Cell 37:135–143Google Scholar
  150. Rost-Roszkowska MM (2006a) Comparative studies on the regeneration of the midgut epithelium in Lepisma saccharina L. and Thermobia domestica Packard (Insecta, Zygentoma). Ann Entomol Soc Am 99:910–916Google Scholar
  151. Rost-Roszkowska MM (2006b) Ultrastructural changes in the midgut epithelium in Podura aquatic L. (Insecta, Collembola, Arthropleona) during regeneration. Arthropod Struct Dev 35:69–76Google Scholar
  152. Rost-Roszkowska MM (2008) Ultrastructural changes in the midgut epithelium of Acheta domesticus (Orthoptera: Gryllidae) during degeneration and regeneration. Ann Entomol Soc Am 101:151–158Google Scholar
  153. Rost-Roszkowska MM, Undrul A (2008) Fine structure and differentiation of the midgut epithelium of Allacma fusca (Insecta: Collembola: Symphypleona). Zool Stud 47:200–206Google Scholar
  154. Rost-Roszkowska MM, Pilka M, Szymska R, Klag J (2007) Ultrastructural studies of midgut epithelium formation in Lepisma saccharina L. (Insecta, Zygentoma). J Morphol 268:224–231Google Scholar
  155. Rost-Roszkowska MM, Poprawa I, Klag J, Migula P, Mesjasz-Przybyłowicz J, Przybyłowicz W (2010a) Differentiation of regenerative cells in the midgut epithelium of Epilachna cf nylanderi (Mulsant 1850) (Insecta, Coleoptera, Coccinellidae). Folia Biol (Kraków) 58:209–216Google Scholar
  156. Rost-Roszkowska MM, Jansta P, Vilimova J (2010b) Fine structure of the midgut epithelium in two Archaeognatha, Lepismachilis notata and Machilis hrabei (Insecta), in relation to its degeneration and regeneration. Protoplasma 247:91–101Google Scholar
  157. Rost-Roszkowska MM, Vilimova J, Chajec L (2010c) Fine structure of the midgut epithelium of Nicoletia phytophila Gervais, 1844 (Zygentoma: Nicoletiidae: Nicoletiinae) with special emphasis on its degeneration. Folia Biol (Kraków) 58:217–227Google Scholar
  158. Rost-Roszkowska MM, Machida R, Fukui M (2010d) The role of cell death in the midgut epithelium in Filientomon takanawanum (Protura). Tissue Cell 42:24–31Google Scholar
  159. Rost-Roszkowska MM, Vilimova J, Chajec L (2010e) Fine structure of the midgut epithelium in Atelura formicaria (Hexapoda, Zygentoma, Ateluridae), with special reference to its regeneration and degeneration. Zool Stud 49:10–18Google Scholar
  160. Rost-Roszkowska MM, Vilimova J, Włodarczyk A, Sonakowska L, Kamińska K, Kaszuba F, Marchewka A, Sadílek D (2017) Investigation of the midgut structure and ultrastructure in Cimex lectularius and Cimex pipistrelli (Hemiptera: Cimicidae). Neotrop Entomol 46:45–57Google Scholar
  161. Russell VW, Dunn PE (1991) Lysozyme in the midgut of Manduca sexta during metamorphosis. Arch Insect Biochem Physiol 17:67–80Google Scholar
  162. Ryu JH, Ha EM, Lee WJ (2010) Innate immunity and gut-microbe mutualism in Drosophila. Dev Comp Immunol 34:369–376Google Scholar
  163. Sadrud-Din S, Hakim R, Loeb M (1994) Proliferation and differentiation of midgut cells from Manduca sexta, in vitro. Invertebr Reprod Dev 26:197–204Google Scholar
  164. Sakai T, Satake H, Takeda M (2006) Nutrient-induced α-amylase and protease activity is regulated by crustacean cardioactive peptide (CCAP) in the cockroach midgut. Peptides 27:157–2164Google Scholar
  165. Sano H, Nakamura A, Texada MJ, Truman JW, Ishimoto H, Kamikouchi A, Nibu Y, Kume K, Ida T, Kojima M (2015) The nutrient-responsive hormone CCHamide-2 controls growth by regulating insulin-like peptides in the brain of Drosophila melanogaster. PLoS Genet 11(5):e1005209.  https://doi.org/10.1371/journal.pgen.1005209 Google Scholar
  166. Santos HP, Rost-Roszkowska M, Vilimova J, Serrão JE (2017) Ultrastructure of the midgut in Heteroptera (Hemiptera) with different feeding habits. Protoplasma 254:1743–1753Google Scholar
  167. Schols D, Verhaert P, Huybrecht R, Vaudry H, Jégou S, De Loof A (1987) Immunocytochemical demonstration of proopiomelanocortin- and other opioid related substances and a CRF-like peptide in the gut of the american cockroach, Periplaneta americana L. Histochemistry 86:345–351Google Scholar
  168. Scopelliti A, Cordero JB, Diao F, Strathdee K, White BH, Sansom OJ, Vidal M (2014) Local control of intestinal stem cell homeostasis by enteroendocrine cells in the adult Drosophila midgut. Curr Biol 24:1199–1211Google Scholar
  169. Sehnal F, Žitňan D (1996) Midgut endocrine cells. In: Lehane MJ, Billingsley PF (eds) Biology of the insect midgut. Chapman & Hall, London, pp 55–85Google Scholar
  170. Shanbhag S, Tripathi S (2009) Epithelial ultrastructure and cellular mechanisms of acid and base transport in the Drosophila midgut. J Exp Biol 212:1731–1744Google Scholar
  171. Shen P, Cai HN (2001) Drosophila neuropeptide F mediates integration of chemosensory stimulation and conditioning of the nervous system by food. J Neurobiol 47:16–25Google Scholar
  172. Shim J, Gururaja-Rao S, Banerjee U (2013) Nutritional regulation of stem and progenitor cells in Drosophila. Development 140:4647–4656Google Scholar
  173. Silva CP, Silva JR, Vasconcelos FF, Petretski MDA, 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 Dev 33:139–148Google Scholar
  174. Smagghe G, Vanhassel W, Moeremans C, De Wilde D, Goto S, Loeb MJ, Blackburn MB, Hakim RS (2005) Stimulation of midgut stem cell proliferation and differentiation by insect hormones and peptides. Ann N Y Acad Sci 1040:472–475Google Scholar
  175. Song W, Veenstra JA, Perrimon N (2014) Control of lipid metabolism by tachykinin in Drosophila. Cell Rep 9:40–47Google Scholar
  176. Song W, Cheng D, Hong S, Sappe B, Hu Y, Wei N, Zhu C, O’Connor MB, Pissios P, Perrimon N (2017) Midgut-derived activin regulates glucagon-like action in the fat body and glycemic control. Cell Metab 25:386–399Google Scholar
  177. Sumner JP, Dow JAT, Earley FG, Klein U, Jäger D, Wieczorek H (1995) Regulation of plasma membrane V-ATPase activity by dissociation of peripheral subunits. J Biol Chem 270:5649–5653Google Scholar
  178. Takashima S, Younossi-Hartenstein A, Ortiz PA, Hartenstein V (2011) A novel tissue in an established model system: the Drosophila pupal midgut. Dev Genes Evol 221:69–81Google Scholar
  179. Takashima S, Gold D, Hartenstein V (2013) Stem cells and lineages of the intestine: a developmental and evolutionary perspective. Dev Genes Evol 223:85–102Google Scholar
  180. Taracena ML, Bottino-Rojas V, Talyuli OAC, Walter-Nuno AB, Oliveira JHM, Angleró-Rodriguez YI, Wells MB, Dimopoulos G, Oliveira PL, Paiva-Silva GO (2018) Regulation of midgut cell proliferation impacts Aedes aegypti susceptibility to dengue virus. PLoS Negl Trop Dis 12:e0006498.  https://doi.org/10.1371/journal.pntd.0006498 Google Scholar
  181. Teixeira A, Fialho Mdo C, Zanuncio JC, Ramalho Fde S, Serrão JE (2013) Degeneration and cell regeneration in the midgut of Podisus nigrispinus (Heteroptera: Pentatomidae) during post-embryonic development. Arthropod Struct Dev 42:237–246Google Scholar
  182. Terra WR (1988) Physiology and biochemistry of insect digestion: an evolutionary perspective. Braz J Med Biol Res 21:675–734Google Scholar
  183. Terra WR, Ferreira C (1994) Insect digestive enzymes: properties, compartmentalization and function. Comp Biochem Physiol 109:1–62Google Scholar
  184. 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 34:463–472Google Scholar
  185. Terra WR, Ferreira C, Baker JE (1996) Compartmentalization of digestion. In: Lehane MJ, Billingsley PF (eds) Biology of the insect midgut. Chapman & Hall, London, pp 206–235Google Scholar
  186. Tettamanti G, Casartelli M (2019) Cell death during complete metamorphosis. Philos Trans R Soc Lond B:20190065.  https://doi.org/10.1098/rstb.2019.0065
  187. Tettamanti G, Grimaldi A, Casartelli M, Ambrosetti E, Ponti B, Congiu T, Ferrarese R, Rivas-Pena ML, Pennacchio F, de Eguileor M (2007) Programmed cell death and stem cell differentiation are responsible for midgut replacement in Heliothis virescens during prepupal instar. Cell Tissue Res 330:345–359Google Scholar
  188. Tettamanti G, Carata E, Montali A, Dini L, Fimia GM (2019) Autophagy in development and regeneration: role in tissue remodelling and cell survival. Eur Zool J 86:113–131Google Scholar
  189. Turbeck BO, Foder B (1970) Studies on a carbonic anhydrase from the midgut epithelium of larvae of lepidoptera. Biochim Biophys Acta 212:134–138Google Scholar
  190. Ursic-Bedoya R, Buchhop J, Joy JB, Durvasula R, Lowenberger C (2011) Prolixicin: a novel antimicrobial peptide isolated from Rhodnius prolixus with differential activity against bacteria and Trypanosoma cruzi. Insect Mol Biol 20:775–786Google Scholar
  191. Veenstra JA (2009) Peptidergic paracrine and endocrine cells in the midgut of the fruit fly maggot. Cell Tissue Res 336:309–323Google Scholar
  192. Veenstra JA, Ida T (2014) More Drosophila enteroendocrine peptides: orcokinin B and the CCHamides 1 and 2. Cell Tissue Res 357:607–621Google Scholar
  193. Veenstra JA, Agricola HJ, Sellami A (2008) Peptidergic paracrine and endocrine cells in the midgut of the fruit fly maggot. Cell Tissue Res 336:309–323Google Scholar
  194. Vizioli J, Bulet P, Hoffmann JA, Kafatos FC, Müller HM, Dimopoulos G (2001) Gambicin: a novel immune responsive antimicrobial peptide from the malaria vector Anopheles gambiae. Proc Natl Acad Sci U S A 98:12630–12635Google Scholar
  195. Vogel H, Müller A, Heckel DG, Gutzeit H, Vilcinskas A (2018) Nutritional immunology: diversification and diet-dependent expression of antimicrobial peptides in the black soldier fly Hermetia illucens. Dev Comp Immunol 78:141–148Google Scholar
  196. Voss M, Vitavska O, Walz B, Wieczorek H, Baumann O (2007) Stimulus induced phosphorylation of plasma membrane V-ATPase by protein kinase A. J Biol Chem 282:33735–33742Google Scholar
  197. Wegener C, Veenstra JA (2015) Chemical identity, function and regulation of enteroendocrine peptides in insects. Curr Opin Insect Sci 11:8–13Google Scholar
  198. Whetstone PA, Hammock BD (2007) Delivery methods for peptide and protein toxins in insect control. Toxicon 49:576–596Google Scholar
  199. Wieczorek H, Weerth S, Schindlbeck M, Klein U (1989) A vacuolar-type proton pump in a vesicle fraction enriched with potassium transporting plasma membranes from tobacco hornworm midgut. J Biol Chem 264:11143–11148Google Scholar
  200. Wieczorek H, Putzenlechner M, Zeiske W, Klein U (1991) A vacuolar-type proton pump energizes H+/K+-antiport in an animal plasma membrane. J Biol Chem 266:15340–15347Google Scholar
  201. Wieczorek H, Grüber G, Harvey WR, Huss M, Merzendorfer H, Zeiske W (2000) Structure and regulation of insect plasma membrane H+ V-ATPase. J Exp Biol 203:127–135Google Scholar
  202. Wieczorek H, Beyenbach KW, Huss M, Vitavska O (2009) Vacuolar-type proton pumps in insect epithelia. J Exp Biol 212:1611–1619Google Scholar
  203. Wigglesworth VB (1972) Digestion and nutrition. In: The principles of insect physiology. Chapman & Hall, London, pp 476–552Google Scholar
  204. Winther AM, Nässel DR (2001) Intestinal peptides as circulating hormones: release of tachykinin-related peptide from the locust and cockroach midgut. J Exp Biol 204:1269–1280Google Scholar
  205. Wolfersberger MG (1996) Localization of amino acid absorption systems in the larval midgut of the tobacco hornworm Manduca sexta. J Insect Physiol 42:975–982Google Scholar
  206. Wu Q, Patočka J, Kuča K (2018) Insect antimicrobial peptides, a mini review. Toxins 10:461.  https://doi.org/10.3390/toxins10110461 Google Scholar
  207. Zielke N, Edgar BA, DePamphilis ML (2013) Endoreplication. Cold Spring Harb Perspect Biol 5(1):a012948.  https://doi.org/10.1101/cshperspect.a012948 Google Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Agricultural SciencesUniversity of Naples “Federico II”PorticiItaly
  2. 2.Department of BiosciencesUniversity of MilanMilanItaly
  3. 3.Department of Biotechnology and Life SciencesUniversity of InsubriaVareseItaly

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