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Abstract

Chitin is a major component of the exoskeleton and the peritrophic matrix of insects. It forms complex structures in association with different assortments of cuticle and peritrophic matrix proteins to yield biocomposites with a wide range of physicochemical and mechanical properties. The growth and development of insects are intimately coupled with the biosynthesis, turnover, and modification of chitin. The genes encoding numerous enzymes of chitin metabolism and proteins that associate with and organize chitin have been uncovered by bioinformatics analyses. Many of these proteins are encoded by sets of large gene families. There is specialization among members within each family, which function in particular tissues or developmental stages. Chitin-containing matrices are dynamically modified at every developmental stage and are under developmental and/or physiological control. A thorough understanding of the diverse processes associated with the assembly and turnover of these chitinous matrices offers many strategies to achieve selective pest control.

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2016-03-11
2024-04-16
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Literature Cited

  1. Abo-Elghar GE, Fujiyoshi P, Matsumura F. 1.  2004. Significance of the sulfonylurea receptor (SUR) as the target of diflubenzuron in chitin synthesis inhibition in Drosophila melanogaster and Blattella germanica. Insect Biochem. Mol. Biol. 34:743–52 [Google Scholar]
  2. Agrawal S, Kelkenberg M, Begum K, Steinfeld L, Williams CE. 2.  et al. 2014. Two essential peritrophic matrix proteins mediate matrix barrier functions in the insect midgut. Insect Biochem. Mol. Biol. 49:24–34 [Google Scholar]
  3. Ampasala DR, Zheng SC, Zhang DY, Ladd T, Doucet D. 3.  et al. 2011. An epidermis-specific chitin synthase cDNA in Choristoneura fumiferana: cloning, characterization, developmental and hormonal-regulated expression. Arch. Insect Biochem. Physiol. 76:83–96 [Google Scholar]
  4. Arakane Y, Dixit R, Begum K, Park Y, Specht CA. 4.  et al. 2009. Analysis of functions of the chitin deacetylase gene family in Tribolium castaneum. Insect Biochem. Mol. Biol. 39:355–65 [Google Scholar]
  5. Arakane Y, Hogenkamp DG, Zhu YC, Kramer KJ, Specht CA. 5.  et al. 2004. Characterization of two chitin synthase genes of the red flour beetle, Tribolium castaneum, and alternate exon usage in one of the genes during development. Insect Biochem. Mol. Biol. 34:291–304 [Google Scholar]
  6. Arakane Y, Muthukrishnan S. 6.  2010. Insect chitinase and chitinase-like proteins. Cell. Mol. Life Sci. 67:201–16 [Google Scholar]
  7. Arakane Y, Muthukrishnan S, Beeman RW, Kanost MR, Kramer KJ. 7.  2005. Laccase 2 is the phenoloxidase gene required for beetle cuticle tanning. PNAS 102:11337–42 [Google Scholar]
  8. Arakane Y, Muthukrishnan S, Kramer KJ, Specht CA, Tomoyasu Y. 8.  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. 14:453–63 [Google Scholar]
  9. Arakane Y, Specht CA, Kramer KJ, Muthukrishnan S, Beeman RW. 9.  2008. Chitin synthases are required for survival, fecundity and egg hatch in the red flour beetle, Tribolium castaneum. Insect Biochem. Mol. Biol. 38:959–62 [Google Scholar]
  10. Arakane Y, Zhu Q, Matsumiya M, Muthukrishnan S, Kramer KJ. 10.  2003. Properties of catalytic, linker and chitin-binding domains of insect chitinase. Insect Biochem. Mol. Biol. 33:631–48 [Google Scholar]
  11. Ashfaq M, Sonoda S, Tsumuki H. 11.  2007. Developmental and tissue-specific expression of CHS1 from Plutella xylostella and its response to chlorfluazuron. Pestic. Biochem. Physiol. 89:20–30 [Google Scholar]
  12. Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P. 12.  et al. 2007. Control of coleopteran insect pests through RNA interference. Nat. Biotechnol. 25:1322–26 [Google Scholar]
  13. Broehan G, Zimoch L, Wessels A, Ertas B, Merzendorfer H. 13.  2007. A chymotrypsin-like serine protease interacts with the chitin synthase from the midgut of the tobacco hornworm. J. Exp. Biol. 210:3636–43 [Google Scholar]
  14. Campbell PM, Cao AT, Hines ER, East PD, Gordon KH. 14.  2008. Proteomic analysis of the peritrophic matrix from the gut of the caterpillar, Helicoverpa armigera. Insect Biochem. Mol. Biol. 38:950–58 [Google Scholar]
  15. Chaudhari SS, Arakane Y, Specht CA, Moussian B, Boyle DL. 15.  et al. 2011. Knickkopf protein protects and organizes chitin in the newly synthesized insect exoskeleton. PNAS 108:17028–33 [Google Scholar]
  16. Chaudhari SS, Moussian B, Specht CA, Arakane Y, Kramer KJ. 16.  et al. 2014. Functional specialization among members of Knickkopf family of proteins in insect cuticle organization. PLOS Genet. 10:e1004537 [Google Scholar]
  17. Chaudhari SS, Noh MY, Moussian B, Specht CA, Kramer KJ. 17.  et al. 2015. Knickkopf and Retroactive proteins are required for formation of laminar serosal procuticle during embryonic development of Tribolium castaneum. Insect Biochem. Mol. Biol. 60:1–6 [Google Scholar]
  18. Chen J, Liang ZK, Liang YK, Pang R, Zhang WQ. 18.  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. 43:839–48 [Google Scholar]
  19. Chen J, Tang B, Chen H, Yao Q, Huang X. 19.  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 [Google Scholar]
  20. Chen X, Yang X, Senthil Kumar N, Tang B, Sun X. 20.  et al. 2007. The class A chitin synthase gene of Spodoptera exigua: molecular cloning and expression patterns. Insect Biochem. Mol. Biol. 37:409–17 [Google Scholar]
  21. Ding X, Gopalakrishnan B, Johnson LB, White FF, Wang X. 21.  et al. 1998. Insect resistance of transgenic tobacco expressing an insect chitinase gene. Transgenic Res. 7:77–84 [Google Scholar]
  22. Dinglasan RR, Devenport M, Florens L, Johnson JR, McHugh CA. 22.  et al. 2009. The Anopheles gambiae adult midgut peritrophic matrix proteome. Insect Biochem. Mol. Biol. 39:125–34 [Google Scholar]
  23. Dixit R, Arakane Y, Specht CA, Richard C, Kramer KJ. 23.  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. 38:440–51 [Google Scholar]
  24. Doblin MS, Kurek I, Jacob-Wilk D, Delmer DP. 24.  2002. Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol. 43:1407–20 [Google Scholar]
  25. Dorfmueller HC, Ferenbach AT, Borodkin VS, van Aalten DM. 25.  2014. A structural and biochemical model of processive chitin synthesis. J. Biol. Chem. 289:23020–28 [Google Scholar]
  26. Dziadik-Turner C, Mai MS, Kramer KJ. 26.  1981. Purification and characterization of two N-acetylglucosaminidases from the tobacco hornworm, Manduca sexta L. (Lepidoptera: Sphingidae). Arch. Biochem. Biophys. 212:546–60 [Google Scholar]
  27. Elvin CM, Vuocolo T, Pearson RD, East IJ, Riding GA. 27.  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. 271:8925–35 [Google Scholar]
  28. Fukamizo T, Kramer KJ. 28.  1985. Mechanism of chitin hydrolysis by the binary chitinase system in insect molting fluid. Insect Biochem. 15:141–45 [Google Scholar]
  29. Gagou ME, Kapsetaki M, Turberg A, Kafetzopoulos D. 29.  2002. Stage-specific expression of the chitin synthase DmeChSA and DmeChSB genes during the onset of Drosophila metamorphosis. Insect Biochem. Mol. Biol. 32:141–46 [Google Scholar]
  30. Gorman MJ, Arakane Y. 30.  2010. Tyrosine hydroxylase is required for cuticle sclerotization and pigmentation in Tribolium castaneum. Insect Biochem. Mol. Biol. 40:267–73 [Google Scholar]
  31. Harper MS, Hopkins TL. 31.  1997. Peritrophic membrane structure and secretion in European corn borer larvae (Ostrinia nubilalis). Tissue Cell 29:463–75 [Google Scholar]
  32. Harper MS, Hopkins TL, Czapla TH. 32.  1998. Effect of wheat germ agglutinin on formation and structure of the peritrophic membrane in European corn borer (Ostrinia nubilalis) larvae. Tissue Cell 30:166–76 [Google Scholar]
  33. Hegedus D, Erlandson M, Gillott C, Toprak U. 33.  2009. New insights into peritrophic matrix synthesis, architecture, and function. Annu. Rev. Entomol. 54:285–302 [Google Scholar]
  34. Hogenkamp DG, Arakane Y, Kramer KJ, Muthukrishnan S, Beeman RW. 34.  2008. Characterization and expression of the β-N-acetylhexosaminidase gene family of Tribolium castaneum. Insect Biochem. Mol. Biol 38:478–89 [Google Scholar]
  35. Hogenkamp DG, Arakane Y, Zimoch L, Merzendorfer H, Kramer KJ. 35.  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. 35:529–40 [Google Scholar]
  36. Huang X, Tsuji N, Miyoshi T, Motobu M, Islam MK. 36.  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. 37:383–92 [Google Scholar]
  37. Hubbard C, McNamara JT, Azumaya C, Patel MS, Zimmer J. 37.  2012. The hyaluronan synthase catalyzes the synthesis and membrane translocation of hyaluronan. J. Mol. Biol. 418:21–31 [Google Scholar]
  38. Ianiro A, Giosia MD, Fermani S, Samorì C, Barbalinardo M. 38.  et al. 2014. Customizing properties of β-chitin in squid pen (gladius) by chemical treatments. Marine Drugs 12:5979–92 [Google Scholar]
  39. Jacobs CGC, Braak N, Lamers GEM, van der Zee M. 39.  2015. Elucidation of the serosal cuticle machinery in the beetle Tribolium by RNA sequencing and functional analysis of Knickkopf1, Retroactive and Laccase2. Insect Biochem. Mol. Biol 60:7–12 [Google Scholar]
  40. Jakubowska AK, Caccia S, Gordon KH, Ferre J, Herrero S. 40.  2010. Downregulation of a chitin deacetylase-like protein in response to baculovirus infection and its application for improving baculovirus infectivity. J. Virol. 84:2547–55 [Google Scholar]
  41. Jasrapuria S, Arakane Y, Osman G, Kramer KJ, Beeman RW, Muthukrishnan S. 41.  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. 40:214–27 [Google Scholar]
  42. Kanost MR, Zepp MK, Ladendorff NE, Andersson LA. 42.  1994. Isolation and characterization of a hemocyte aggregation inhibitor from hemolymph of Manduca sexta larvae. Arch. Insect Biochem. Physiol. 27:123–36 [Google Scholar]
  43. Kariu T, Smith A, Yang X, Pal U. 43.  2013. A chitin deacetylase-like protein is a predominant constituent of tick peritrophic membrane that influences the persistence of Lyme disease pathogens within the vector. PLOS ONE 8:e78376 [Google Scholar]
  44. Kato N, Mueller CR, Fuchs JF, Wessely V, Lan Q, Christensen BM. 44.  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 [Google Scholar]
  45. Kawamura K, Shibata T, Saget O, Peel D, Bryant PJ. 45.  1999. A new family of growth factors produced by the fat body and active on Drosophila imaginal disc cells. Development 126:211–19 [Google Scholar]
  46. Kaya M, Baran T, Erdoğan S, Menteş A, Aşan Özüsağlam M. 46.  et al. 2014. Physicochemical comparison of chitin and chitosan obtained from larvae and adult Colorado potato beetle (Leptinotarsa decemlineata). Mater. Sci. Eng. C 45:72–81 [Google Scholar]
  47. Kaya M, Erdogan S, Mol A, Baran T. 47.  2015. Comparison of chitin structures isolated from seven Orthoptera species. Int. J. Biol. Macromol. 72:797–805 [Google Scholar]
  48. Kelkenberg M, Odman-Naresh J, Muthukrishnan S, Merzendorfer H. 48.  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 [Google Scholar]
  49. Kelley LA, Sternberg MJE. 49.  2009. Protein structure prediction on the web: a case study using the Phyre server. Nat. Protoc. 4:363–71 [Google Scholar]
  50. Khajuria C, Buschman LL, Chen MS, Muthukrishnan S, Zhu KY. 50.  2010. A gut-specific chitinase gene essential for regulation of chitin content of peritrophic matrix and growth of Ostrinia nubilalis larvae. Insect Biochem. Mol. Biol. 40:621–29 [Google Scholar]
  51. Kim YH, Soumaila Issa M, Cooper AMW, Zhu KY. 51.  2015. RNA interference: applications and advances in insect toxicology and insect pest management. Pestic. Biochem. Physiol. 120:109–17 [Google Scholar]
  52. Koga D, Funakoshi T, Mizuki K, Ide A, Kramer KJ. 52.  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. 22:305–11 [Google Scholar]
  53. Kramer KJ, Corpuz L, Choi HK, Muthukrishnan S. 53.  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 [Google Scholar]
  54. Leonard R, Rendic D, Rabouille C, Wilson IB, Preat T. 54.  et al. 2006. The Drosophila fused lobes gene encodes an N-acetylglucosaminidase involved in N-glycan processing. J. Biol. Chem. 281:4867–75 [Google Scholar]
  55. Li D, Zhang J, Wang Y, Liu X, Ma E. 55.  et al. 2015. Two chitinase 5 genes from Locusta migratoria: molecular characteristics and functional differentiation. Insect Biochem. Mol. Biol. 58:46–54 [Google Scholar]
  56. Liu S, Sun J, Yu L, Zhang C, Bi J. 56.  et al. 2012. Extraction and characterization of chitin from the beetle Holotrichia parallela Motschulsky. Molecules 17:4604–11 [Google Scholar]
  57. Liu T, Zhang HT, Liu FY, Wu QY, Shen X. 57.  et al. 2011. Structural determinants of an insect β-N-acetyl-d-hexosaminidase specialized as a chitinolytic enzyme. J. Biol. Chem. 286:4049–58 [Google Scholar]
  58. Liu X, Li F, Li D, Ma E, Zhang W. 58.  et al. 2013. Molecular and functional analysis of UDP-N-acetylglucosamine pyrophosphorylases from the migratory locust, Locusta migratoria. PLOS ONE 8:e71970 [Google Scholar]
  59. Liu X, Zhang H, Li S, Zhu KY, Ma E. 59.  et al. 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. 42:902–10 [Google Scholar]
  60. Locke M, Kiss A, Sass M. 60.  1994. The cuticular localization of integument peptides from particular routing categories. Tissue Cell 26:707–34 [Google Scholar]
  61. Luschnig S, Batz T, Armbruster K, Krasnow MA. 61.  2006. serpentine and vermiform encode matrix proteins with chitin binding and deacetylation domains that limit tracheal tube length in Drosophila. Curr. Biol. 16:186–94 [Google Scholar]
  62. Mansur JF, Alvarenga ES, Figueira-Mansur J, Franco TA, Ramos IB. 62.  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. 51:110–21 [Google Scholar]
  63. Maue L, Meissner D, Merzendorfer H. 63.  2009. Purification of an active, oligomeric chitin synthase complex from the midgut of the tobacco hornworm. Insect Biochem. Mol. Biol. 39:654–59 [Google Scholar]
  64. McCafferty H, Moore P, Zhu Y. 64.  2006. Improved Carica papaya tolerance to carmine spider mite by the expression of Manduca sexta chitinase transgene. Transgenic Res. 15:337–47 [Google Scholar]
  65. McFarlane HE, Doring A, Persson S. 65.  2014. The cell biology of cellulose synthesis. Annu. Rev. Plant Biol. 65:69–94 [Google Scholar]
  66. Merzendorfer H. 66.  2006. Insect chitin synthases: a review. J. Comp. Physiol. B 176:1–15 [Google Scholar]
  67. Merzendorfer H. 67.  2011. The cellular basis of chitin synthesis in fungi and insects: common principles and differences. Eur. J. Cell Biol. 90:759–69 [Google Scholar]
  68. Merzendorfer H. 68.  2013. Chitin synthesis inhibitors: old molecules and new developments. Insect Sci. 20:121–38 [Google Scholar]
  69. Meyer F, Flötenmeyer M, Moussian B. 69.  2013. The sulfonylurea receptor SUR is dispensable for chitin synthesis in Drosophila melanogaster embryos. Pest Manag. Sci. 69:1136–40 [Google Scholar]
  70. Morgan JL, Strumillo J, Zimmer J. 70.  2013. Crystallographic snapshot of cellulose synthesis and membrane translocation. Nature 493:181–86 [Google Scholar]
  71. Moussian B. 71.  2013. The apical plasma membrane of chitin-synthesizing epithelia. Insect Sci. 20:139–46 [Google Scholar]
  72. Moussian B, Tång E, Tonning A, Helms S, Schwarz H. 72.  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 133:163–71 [Google Scholar]
  73. Mun S, Noh MY, Dittmer NT, Muthukrishnan S, Kramer KJ. 73.  et al. 2015. Cuticular protein with a low complexity sequence becomes cross-linked during insect cuticle sclerotization and is required for the adult molt. Sci. Rep. 5:10484 [Google Scholar]
  74. Muthukrishnan S, Merzendorfer H, Arakane Y, Kramer KJ. 74.  2012. Chitin metabolism in insects. Insect Molecular Biology and Biochemistry LI Gilbert 193–235 London: Academic [Google Scholar]
  75. Nagamatsu Y, Yanagisawa I, Kimoto M, Okamoto E, Koga D. 75.  1995. Purification of a chitooligosaccharidolytic β-N-acetylhexosaminidase from Bombyx mori larvae during metamorphosis and the nucleotide sequence of its cDNA. Biosci. Biotechnol. Biochem. 59:219–25 [Google Scholar]
  76. Nakabachi A, Shigenobu S, Miyagishima S. 76.  2010. Chitinase-like proteins encoded in the genome of the pea aphid, Acyrthosiphon pisum. Insect Mol. Biol. 19:Suppl. 2175–85 [Google Scholar]
  77. Noh MY, Kramer KJ, Muthukrishnan S, Kanost MR, Beeman RW, Arakane Y. 77.  2014. Two major cuticular proteins are required for assembly of horizontal laminae and vertical pore canals in rigid cuticle of Tribolium castaneum. Insect Biochem. Mol. Biol. 53:22–29 [Google Scholar]
  78. Noh MY, Muthukrishnan S, Kramer KJ, Arakane Y. 78.  2015. Tribolium castaneum RR-1 cuticular protein TcCPR4 is required for formation of pore canals in rigid cuticle. PLOS Genet. 11:e1004963 [Google Scholar]
  79. Odman-Naresh J, Duevel M, Muthukrishnan S, Merzendorfer H. 79.  2013. A lepidopteran-specific gene family encoding valine-rich midgut proteins. PLOS ONE 8:e82015 [Google Scholar]
  80. Pan Y, P, Wang Y, Yin L, Ma H. 80.  et al. 2012. In silico identification of novel chitinase-like proteins in the silkworm, Bombyx mori, genome. J. Insect Sci. 12:150 [Google Scholar]
  81. Pesch YY, Riedel D, Behr M. 81.  2015. Obstructor A organizes matrix assembly at the apical cell surface to promote enzymatic cuticle maturation in Drosophila. J. Biol. Chem. 290:10071–82 [Google Scholar]
  82. Peters W. 82.  1992. Peritrophic Membranes Berlin: Springer
  83. Petkau G, Wingen C, Jussen LC, Radtke T, Behr M. 83.  2012. Obstructor-A is required for epithelial extracellular matrix dynamics, exoskeleton function, and tubulogenesis. J. Biol. Chem. 287:21396–405 [Google Scholar]
  84. Qiao L, Li Y, Xiong G, Liu X, He S. 84.  et al. 2012. Effects of altered catecholamine metabolism on pigmentation and physical properties of sclerotized regions in the silkworm melanism mutant. PLOS ONE 7:e42968 [Google Scholar]
  85. Qu M, Yang Q. 85.  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. 41:923–31 [Google Scholar]
  86. Qu M, Yang Q. 86.  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 [Google Scholar]
  87. Rezende GL, Martins AJ, Gentile C, Farnesi LC, Pelajo-Machado M. 87.  et al. 2008. Embryonic desiccation resistance in Aedes aegypti: presumptive role of the chitinized serosal cuticle. BMC Dev. Biol. 8:182–95 [Google Scholar]
  88. Rong S, Li D, Zhang X, Li S, Zhu KY. 88.  et al. 2013. β-N-acetylglucosaminidase gene is essential for larval-larval and larval-adult molting in Locusta migratoria. Insect Sci. 20:109–19 [Google Scholar]
  89. Rose C, Belmonte R, Armstrong SD, Molyneux G, Haines LR. 89.  et al. 2014. An investigation into the protein composition of the teneral Glossina morsitans morsitans peritrophic matrix. PLOS Negl. Trop. Dis. 8:e2691 [Google Scholar]
  90. Sacristan C, Manzano-Lopez J, Reyes A, Spang A, Muniz M, Roncero C. 90.  2013. Oligomerization of the chitin synthase Chs3 is monitored at the Golgi and affects its endocytic recycling. Mol. Microbiol. 90:252–66 [Google Scholar]
  91. Sawada D, Nishiyama Y, Langan P, Forsyth VT, Kimura S. 91.  et al. 2012. Direct determination of the hydrogen bonding arrangement in anhydrous β-chitin by neutron fiber diffraction. Biomacromolecules 13:288–91 [Google Scholar]
  92. Sempere LF, Sokol NS, Dubrovsky EB, Berger EM, Ambros V. 92.  2003. Temporal regulation of microRNA expression in Drosophila melanogaster mediated by hormonal signals and Broad-Complex gene activity. Dev. Biol. 259:9–18 [Google Scholar]
  93. Shao L, Devenport M, Fujioka H, Ghosh A, Jacobs-Lorena M. 93.  2005. Identification and characterization of a novel peritrophic matrix protein, Ae-Aper50, and the microvillar membrane protein, AEG12, from the mosquito, Aedes aegypti. Insect Biochem. Mol. Biol. 35:947–59 [Google Scholar]
  94. Shen Z, Jacobs-Lorena M. 94.  1998. A type I peritrophic matrix protein from the malaria vector Anopheles gambiae binds to chitin. Cloning, expression, and characterization. J. Biol. Chem. 273:17665–70 [Google Scholar]
  95. Shi X, Chamankhah M, Visal-Shah S, Hemmingsen SM, Erlandson M. 95.  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. 34:1101–15 [Google Scholar]
  96. Singtripop T, Oda Y, Wanichacheewa S, Sakurai S. 96.  2002. Sensitivities to juvenile hormone and ecdysteroid in the diapause larvae of Omphisa fuscidentalis based on the hemolymph trehalose dynamics index. J. Insect Physiol. 48:817–24 [Google Scholar]
  97. Snelling EP, Seymour RS, Runciman S. 97.  2011. Molting of insect tracheae captured by light and electron-microscopy in the metathoracic femur of a third instar locust Locusta migratoria. J. Insect Physiol. 57:1312–16 [Google Scholar]
  98. Souza-Ferreira PS, Mansur JF, Berni M, Moreira MF, dos Santos RE. 98.  et al. 2014. Chitin deposition on the embryonic cuticle of Rhodnius prolixus: the reduction of CHS transcripts by CHS-dsRNA injection in females affects chitin deposition and eclosion of the first instar nymph. Insect Biochem. Mol. Biol. 51:101–9 [Google Scholar]
  99. Sparks TC, Nauen R. 99.  2015. IRAC: mode of action classification and insecticide resistance management. Pestic. Biochem. Physiol. 121:122–28 [Google Scholar]
  100. Suderman RJ, Dittmer NT, Kramer KJ, Kanost MR. 100.  2010. Model reactions for insect cuticle sclerotization: participation of amino groups in the cross-linking of Manduca sexta cuticle protein MsCP36. Insect Biochem. Mol. Biol. 40:252–58 [Google Scholar]
  101. Tellam RL, Wijffels G, Willadsen P. 101.  1999. Peritrophic matrix proteins. Insect Biochem. Mol. Biol. 29:87–101 [Google Scholar]
  102. Tetreau G, Cao XL, Chen YR, Muthukrishnan S, Jiang HB. 102.  et al. 2015. Overview of chitin metabolism enzymes in Manduca sexta: identification, domain organization, phylogenetic analysis and gene expression. Insect Biochem. Mol. Biol. 62:114–26 [Google Scholar]
  103. Tetreau G, Dittmer NT, Caoc X, Agrawal S, Chen Y-R. 103.  et al. 2015. 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. 62:127–41 [Google Scholar]
  104. Tian H, Peng H, Yao Q, Chen H, Xie Q. 104.  et al. 2009. Developmental control of a lepidopteran pest Spodoptera exigua by ingestion of bacteria expressing dsRNA of a non-midgut gene. PLOS ONE 4:e6225 [Google Scholar]
  105. Tonning A, Helms S, Schwarz H, Uv AE, Moussian B. 105.  2006. Hormonal regulation of mummy is needed for apical extracellular matrix formation and epithelial morphogenesis in Drosophila. Development 133:331–41 [Google Scholar]
  106. Toprak U, Hegedus DD, Baldwin D, Coutu C, Erlandson M. 106.  2014. Spatial and temporal synthesis of Mamestra configurata peritrophic matrix through a larval stadium. Insect Biochem. Mol. Biol. 54:89–97 [Google Scholar]
  107. van Leeuwen T, Demaeght P, Osborne EJ, Dermauw W, Gohlke S. 107.  et al. 2012. Population bulk segregant mapping uncovers resistance mutations and the mode of action of a chitin synthesis inhibitor in arthropods. PNAS 109:4407–12 [Google Scholar]
  108. Venancio TM, Cristofoletti PT, Ferreira C, Verjovski-Almeida S, Terra WR. 108.  2009. The Aedes aegypti larval transcriptome: a comparative perspective with emphasis on trypsins and the domain structure of peritrophins. Insect Mol. Biol. 18:33–44 [Google Scholar]
  109. Vincent JF, Wengst UG. 109.  2004. Design and mechanical properties of insect cuticle. Arthropod Struct. Dev. 33:187–99 [Google Scholar]
  110. Wang J, Chen Z, Du J, Sun Y, Liang A. 110.  2005. Novel insect resistance in Brassica napus developed by transformation of chitinase and scorpion toxin genes. Plant Cell Rep. 24:549–55 [Google Scholar]
  111. Wang P, Granados RR. 111.  1997. Molecular cloning and sequencing of a novel invertebrate intestinal mucin cDNA. J. Biol. Chem. 272:16663–69 [Google Scholar]
  112. Wang P, Granados RR. 112.  2000. Calcofluor disrupts the midgut defense system in insects. Insect Biochem. Mol. Biol. 30:135–43 [Google Scholar]
  113. Wang P, Li G, Granados RR. 113.  2004. Identification of two new peritrophic membrane proteins from larval Trichoplusia ni: structural characteristics and their functions in the protease rich insect gut. Insect Biochem. Mol. Biol. 34:215–27 [Google Scholar]
  114. Wang S, Jayaram SA, Hemphala J, Senti KA, Tsarouhas V. 114.  et al. 2006. Septate-junction-dependent luminal deposition of chitin deacetylases restricts tube elongation in the Drosophila trachea. Curr. Biol. 16:180–85 [Google Scholar]
  115. Wang Y, Fan HW, Huang HJ, Xue J, Wu WJ. 115.  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. 42:637–46 [Google Scholar]
  116. Weiss BL, Savage AF, Griffith BC, Wu Y, Aksoy S. 116.  2014. The peritrophic matrix mediates differential infection outcomes in the tsetse fly gut following challenge with commensal, pathogenic, and parasitic microbes. J. Immunol. 193:773–82 [Google Scholar]
  117. Wigglesworth VB. 117.  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]
  118. Willis JH, Papandreou NC, Iconomidou VA, Hamodrakas SJ. 118.  2012. Cuticular proteins. Insect Molecular Biology and Biochemistry LI Gilbert 134–66 London: Academic [Google Scholar]
  119. Wu QY, Liu T, Yang Q. 119.  2013. Cloning, expression and biocharacterization of OfCht5, the chitinase from the insect Ostrinia furnacalis. Insect Sci. 20:147–57 [Google Scholar]
  120. Xi Y, Pan PL, Ye YX, Yu B, Xu HJ. 120.  et al. 2015. Chitinase-like gene family in the brown planthopper, Nilaparvata lugens. Insect Biochem. Mol. Biol. 24:29–40 [Google Scholar]
  121. Xi Y, Pan PL, Ye YX, Yu B, Zhang CX. 121.  2014. Chitin deacetylase family genes in the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). Insect Mol. Biol. 23:695–705 [Google Scholar]
  122. Yang Q, Liu T, Liu FY, Qu MB, Qian XH. 122.  2008. A novel β-N-acetyl-d-hexosaminidase from the insect Ostrinia furnacalis (Guenée). FEBS J. 275:5690–702 [Google Scholar]
  123. Yang WJ, Xu KK, Cong L, Wang JJ. 123.  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. 9:331–42 [Google Scholar]
  124. Yao Q, Zhang DW, Tang B, Chen J, Chen J. 124.  et al. 2010. Identification of 20-hydroxyecdysone late-response genes in the chitin biosynthesis pathway. PLOS ONE 5:e14058 [Google Scholar]
  125. Yu X, Zhou Q, Li SC, Luo Q, Cai Y. 125.  et al. 2008. The silkworm (Bombyx mori) microRNAs and their expressions in multiple developmental stages. PLOS ONE 3:e2997 [Google Scholar]
  126. Zhang D, Chen J, Yao Q, Pan Z, Chen J. 126.  et al. 2012. 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. 79:220–34 [Google Scholar]
  127. Zhang J, Liu X, Li D, Sun Y, Guo Y. 127.  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. 40:824–33 [Google Scholar]
  128. Zhang J, Zhang X, Arakane Y, Muthukrishnan S, Kramer KJ. 128.  et al. 2011. Comparative genomic analysis of chitinase and chitinase-like family in the African malaria mosquito (Anopheles gambiae). PLOS ONE 6:e19899 [Google Scholar]
  129. Zhang J, Zhang X, Arakane Y, Muthukrishnan S, Kramer KJ. 129.  et al. 2011. Identification and characterization of a novel chitinase gene cluster (AgCht5) possibly derived from tandem duplications in the African malaria mosquito, Anopheles gambiae. Insect Biochem. Mol. Biol. 41:521–28 [Google Scholar]
  130. Zhang X, Zhang J, Park Y, Zhu KY. 130.  2012. Identification and characterization of two chitin synthase genes in African malaria mosquito, Anopheles gambiae. Insect Biochem. Mol. Biol. 42:674–82 [Google Scholar]
  131. Zhang X, Zhang J, Zhu KY. 131.  2010. Chitosan/double-stranded RNA nanoparticle-mediated RNA interference to silence chitin synthase genes through larval feeding in the African malaria mosquito (Anopheles gambiae). Insect Mol. Biol. 19:683–93 [Google Scholar]
  132. Zheng YP, Retnakaran A, Krell PJ, Arif BM, Primavera M. 132.  et al. 2003. Temporal, spatial and induced expression of chitinase in the spruce budworm, Choristoneura fumiferana. J. Insect Physiol. 49:241–47 [Google Scholar]
  133. Zhong HY, Wei C, Zhang YL. 133.  2013. Gross morphology and ultrastructure of salivary glands of the mute cicada Karenia caelatata Distant (Hemiptera: Cicadoidea). Micron 45:83–91 [Google Scholar]
  134. Zhong X, Zhang L, Zou Y, Yi Q, Zhao P. 134.  et al. 2012. Shotgun analysis on the peritrophic membrane of the silkworm Bombyx mori. BMB Rep. 45:665–70 [Google Scholar]
  135. Zhong XW, Wang XH, Tan X, Xia QY, Xiang ZH. 135.  et al. 2014. Identification and molecular characterization of a chitin deacetylase from Bombyx mori peritrophic membrane. Int. J. Mol. Sci. 15:1946–61 [Google Scholar]
  136. Zhu Q, Arakane Y, Beeman RW, Kramer KJ, Muthukrishnan S. 136.  2008. Characterization of recombinant chitinase-like proteins of Drosophila melanogaster and Tribolium castaneum. Insect Biochem. Mol. Biol. 38:467–77 [Google Scholar]
  137. Zhu Q, Arakane Y, Beeman RW, Kramer KJ, Muthukrishnan S. 137.  2008. Functional specialization among insect chitinase family genes revealed by RNA interference. PNAS 105:6650–55 [Google Scholar]
  138. Zhu Q, Deng Y, Vanka P, Brown SJ, Muthukrishnan S. 138.  et al. 2004. Computational identification of novel chitinase-like proteins in the Drosophila melanogaster genome. Bioinformatics 20:161–69 [Google Scholar]
  139. Zhu R, Liu K, Peng J, Yang H, Hong H. 139.  2007. Optical brightener M2R destroys the peritrophic membrane of Spodoptera exigua (Lepidoptera: Noctuidae) larvae. Pest Manag. Sci. 63:296–300 [Google Scholar]
  140. Zhuo W, Fang Y, Kong L, Li X, Sima Y. 140.  et al. 2014. Chitin synthase A: a novel epidermal development regulation gene in the larvae of Bombyx mori. Mol. Biol. Rep. 41:4177–86 [Google Scholar]
  141. Zimoch L, Hogenkamp DG, Kramer KJ, Muthukrishnan S, Merzendorfer H. 141.  2005. Regulation of chitin synthesis in the larval midgut of Manduca sexta. Insect Biochem. Mol. Biol. 35:515–27 [Google Scholar]
  142. Zimoch L, Merzendorfer H. 142.  2002. Immunolocalization of chitin synthase in the tobacco hornworm. Cell Tissue Res. 308:287–97 [Google Scholar]
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