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Chitinous Structures as Potential Targets for Insect Pest Control

  • Guillaume Tetreau
  • Ping WangEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1142)

Abstract

Chitinous structures are physiologically fundamental in insects. They form the insect exoskeleton, play important roles in physiological systems and provide physical, chemical and biological protections in insects. As critically important structures in insects, chitinous structures are attractive target sites for the development of new insect-pest-control strategies. Chitinous structures in insects are complex and their formation and maintenance are dynamically regulated with the growth and development of insects. In the past few decades, studies on insect chitinous structures have shed lights on the physiological functions, compositions, structural formation, and regulation of the chitinous structures. Current understanding of the chitinous structures has indicated opportunities for exploring new target sites for insect control. Mechanisms to disrupt chitinous structures in insects have been studied and strategies for the potential development of new means of insect control by targeting chitinous structures have been proposed and are practically to be explored.

Keywords

Insect chitinous structure Cuticle Peritrophic membrane Chitin-binding proteins Chitin synthase Chitin deacetylase Chitinase N-acetylglucosaminidases 

Notes

Acknowledgements

This work was supported in part the USDA AFRI Foundational Program competitive grant no. 2016-67013-24754 and USDA NIFA Hatch Project.

References

  1. Adrangi S, Faramarzi MA (2013) From bacteria to human: a journey into the world of chitinases. Biotechnol Adv 31(8):1786–1795CrossRefPubMedGoogle Scholar
  2. Agrawal A, Rajamani V, Reddy VS, Mukherjee SK, Bhatnagar RK (2015) Transgenic plants over-expressing insect-specific microRNA acquire insecticidal activity against Helicoverpa armigera: an alternative to Bt-toxin technology. Transgenic Res 24(5):791–801CrossRefPubMedGoogle Scholar
  3. 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 49:24–34CrossRefPubMedGoogle Scholar
  4. Andersen OA, Dixon MJ, Eggleston IM, van Aalten DM (2005) Natural product family 18 chitinase inhibitors. Nat Prod Rep 22(5):563–579CrossRefPubMedGoogle Scholar
  5. Arai N, Shiomi K, Iwai Y, Omura S (2000a). Argifin, a new chitinase inhibitor, produced by Gliocladium sp. FTD-0668. II. Isolation, physico-chemical properties, and structure elucidation. J Antibiot (Tokyo) 53(6): 609–614Google Scholar
  6. Arai N, Shiomi K, Yamaguchi Y, Masuma R, Iwai Y, Turberg A et al (2000b) Argadin, a new chitinase inhibitor, produced by Clonostachys sp. FO-7314. Chem Pharm Bull (Tokyo) 48(10):1442–1446CrossRefGoogle Scholar
  7. 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(5–6):355–365CrossRefPubMedGoogle Scholar
  8. Arakawa T, Furuta Y, Miyazawa M, Kato M (2002) Flufenoxuron, an insect growth regulator, promotes peroral infection by nucleopolyhedrovirus (BmNPV) budded particles in the silkworm, Bombyx mori L. J Virol Methods 100:141–147CrossRefPubMedGoogle Scholar
  9. Bao W, Cao B, Zhang Y, Wuriyanghan H (2016) Silencing of Mythimna separata chitinase genes via oral delivery of in planta-expressed RNAi effectors from a recombinant plant virus. Biotech Lett 38(11):1961–1966CrossRefGoogle Scholar
  10. Blattner R, Furneaux RH, Kemmitt T, Tyler PC, Ferrier RJ, Tidén A-K (1994) Syntheses of the fungicide/insecticide allosamidin and a structural isomer. J Chem Soc Perkin Trans 1(23):3411–3421CrossRefGoogle Scholar
  11. Casida JE, Durkin KA (2017) Pesticide chemical research in toxicology: lessons from nature. Chem Res Toxicol 30(1):94–104CrossRefPubMedGoogle Scholar
  12. Casu R, Eisemann C, Pearson R, Riding G, East I, Donaldson A et al (1997) Antibody-mediated inhibition of the growth of larvae from an insect causing cutaneous myiasis in a mammalian host. Proc Natl Acad Sci USA 94(17):8939–8944CrossRefPubMedGoogle Scholar
  13. Chen C, Yang H, Tang B, Yang W-J, Jin D-C (2017a) Identification and functional analysis of chitinase 7 gene in white-backed planthopper, Sogatella furcifera. Comp Biochem Physiol B Biochem Mol Biol 208–209:19–28CrossRefPubMedGoogle Scholar
  14. Chen L, Liu T, Duan Y, Lu X, Yang Q (2017b) Microbial secondary metabolite, Phlegmacin B1, as a novel inhibitor of insect chitinolytic enzymes. J Agric Food Chem 65(19):3851–3857CrossRefPubMedGoogle Scholar
  15. Chen P-J, Senthilkumar R, Jane W-N, He Y, Tian Z, Yeh K-W (2014) Transplastomic Nicotiana benthamiana plants expressing multiple defence genes encoding protease inhibitors and chitinase display broad-spectrum resistance against insects, pathogens and abiotic stresses. Plant Biotechnol J 12(4):503–515CrossRefPubMedGoogle Scholar
  16. Chen X, Tian H, Zou L, Tang B, Hu J, Zhang W (2008) Disruption of Spodoptera exigua larval development by silencing chitin synthase gene A with RNA interference. Bull Entomol Res 98(6):613–619CrossRefPubMedGoogle Scholar
  17. Chikate YR, Dawkar VV, Barbole RS, Tilak PV, Gupta VS, Giri AP (2016) RNAi of selected candidate genes interrupts growth and development of Helicoverpa armigera. Pestic Biochem Physiol 133:44–51CrossRefPubMedGoogle Scholar
  18. Cillo F, Palukaitis P (2014) Transgenic resistance. Adv Virus Res 90:35–146CrossRefPubMedGoogle Scholar
  19. Cohen E (1982) Chitin synthetase activity and inhibition in different insect microsomal preparations. EXS 41:470–472Google Scholar
  20. Cohen E (2010) Chitin biochemistry: synthesis, hydrolysis and inhibition. In: Casas J, Simpson SJ (eds) Advances in insect physiology: insect integument and colour, vol 38, pp 5–74Google Scholar
  21. Cornman RS, Willis JH (2008) Extensive gene amplification and concerted evolution within the CPR family of cuticular proteins in mosquitoes. Insect Biochem Mol Biol 38(6):661–676CrossRefPubMedPubMedCentralGoogle Scholar
  22. Corrado G, Arciello S, Fanti P, Fiandra L, Garonna A, Digilio MC et al (2007) The Chitinase A from the baculovirus AcMNPV enhances resistance to both fungi and herbivorous pests in tobacco. Transgenic Res 17(4):557–571CrossRefPubMedGoogle Scholar
  23. da Silva MV, Santi L, Staats CC, da Costa AM, Colodel EM, Driemeier D et al (2005) Cuticle-induced endo/exoacting chitinase CHIT30 from Metarhizium anisopliae is encoded by an ortholog of the chi3 gene. Res Microbiol 156(3):382–392CrossRefPubMedGoogle Scholar
  24. Datta K, Baisakh N, Maung Thet K, Tu J, Datta S (2002) Pyramiding transgenes for multiple resistance in rice against bacterial blight, yellow stem borer and sheath blight. Theor Appl Genet 106(1):1–8CrossRefPubMedGoogle Scholar
  25. de la Vega H, Specht CA, Liu Y, Robbins PW (1998) Chitinases are a multi-gene family in Aedes, Anopheles and Drosophila. Insect Mol Biol 7(3):233–239CrossRefPubMedGoogle Scholar
  26. Derksen AC, Granados RR (1988) Alteration of a lepidopteran peritrophic membrane by baculoviruses and enhancement of viral infectivity. Virology 167(1):242–250CrossRefPubMedGoogle Scholar
  27. Despres L, Stalinski R, Faucon F, Navratil V, Viari A, Paris M et al (2014a) Chemical and biological insecticides select distinct gene expression patterns in Aedes aegypti mosquito. Biol Lett 10(12):20140716CrossRefPubMedPubMedCentralGoogle Scholar
  28. Despres L, Stalinski R, Tetreau G, Paris M, Bonin A, Navratil V et al (2014b). Gene expression patterns and sequence polymorphisms associated with mosquito resistance to Bacillus thuringiensis israelensis toxins. BMC Genom 15:926Google Scholar
  29. Ding X, Gopalakrishnan B, Johnson LB, White FF, Wang X, Morgan TD et al (1998) Insect resistance of transgenic tobacco expressing an insect chitinase gene. Transgenic Res 7:77–84CrossRefPubMedGoogle Scholar
  30. Ding X, Luo Z, Xia L, Gao B, Sun Y, Zhang Y (2008) Improving the insecticidal activity by expression of a recombinant cry1Ac gene with chitinase-encoding gene in acrystalliferous Bacillus thuringiensis. Curr Microbiol 56(5):442–446CrossRefPubMedGoogle Scholar
  31. Dittmer NT, Tetreau G, Cao X, Jiang H, Wang P, Kanost MR (2015) Annotation and expression analysis of cuticular proteins from the tobacco hornworm, Manduca sexta. Insect Biochem Mol Biol 62:100–113CrossRefPubMedPubMedCentralGoogle Scholar
  32. 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(4):440–451CrossRefPubMedGoogle Scholar
  33. Dong B, Miao G, Hayashi S (2014) A fat body-derived apical extracellular matrix enzyme is transported to the tracheal lumen and is required for tube morphogenesis in Drosophila. Development 141(21):4104–4109CrossRefPubMedPubMedCentralGoogle Scholar
  34. Douris V, Steinbach D, Panteleri R, Livadaras I, Pickett JA, van Leeuwen T et al (2016) Resistance mutation conserved between insects and mites unravels the benzoylurea insecticide mode of action on chitin biosynthesis. Proc Natl Acad Sci 113(51):14692–14697CrossRefPubMedGoogle Scholar
  35. Duan Y, Liu T, Zhou Y, Dou T, Yang Q (2018) Glycoside hydrolase family 18 and 20 enzymes are novel targets of the traditional medicine berberine. J Biol Chem 293(40):15429–15438CrossRefPubMedGoogle Scholar
  36. East IJ, Fitzgerald CJ, Pearson RD, Donaldson RA, Vuocolo T, Cadogan LC et al (1993) Lucilia cuprina: inhibition of larval growth induced by immunization of host sheep with extracts of larval peritrophic membrane. Int J Parasitol 23(2):221–229CrossRefPubMedGoogle Scholar
  37. Ganbaatar O, Cao B, Zhang Y, Bao D, Bao W, Wuriyanghan H (2017) Knockdown of Mythimna separata chitinase genes via bacterial expression and oral delivery of RNAi effectors. BMC Biotechnol 17(1):9Google Scholar
  38. Gatehouse AMR, Davison GM, Newell CA, Merryweather A, Hamilton WDO, Burgess EPJ et al (1997) Transgenic potato plants with enhanced resistance to the tomato moth, Lacanobia oleracea: growth room trials. Mol Breeding 3(1):49–63CrossRefGoogle Scholar
  39. Gatehouse AMR, Down RE, Powell KS, Sauvion N, Rahbé Y, Newell CA et al (1996) Transgenic potato plants with enhanced resistance to the peach-potato aphid Myzus persicae. Entomologia Experimentalis Et Applicata 79:295–307Google Scholar
  40. Grover A (2012) Plant chitinases: genetic diversity and physiological roles. Crit Rev Plant Sci 31(1):57–73CrossRefGoogle Scholar
  41. 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 103(45):16794–16799CrossRefPubMedGoogle Scholar
  42. Guo W, Li GX, 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(11):1224–1234CrossRefPubMedGoogle Scholar
  43. Hansen IA, Tian H, Peng H, Yao Q, Chen H, Xie Q 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(7):e6225CrossRefGoogle Scholar
  44. 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(2):166–176CrossRefPubMedGoogle Scholar
  45. Hartl L, Zach S, Seidl-Seiboth V (2012) Fungal chitinases: diversity, mechanistic properties and biotechnological potential. Appl Microbiol Biotechnol 93(2):533–543CrossRefPubMedGoogle Scholar
  46. Hashimoto Y, Corsaro BG, Granados RR (1991) Location and nucleotide sequence of the gene encoding the viral enhancing factor of the Trichoplusia ni granulosis virus. J Gen Virol 72(Pt 11):2645–2651CrossRefPubMedGoogle Scholar
  47. Hegedus D, Erlandson M, Gillott C, Toprak U (2009) New insights into peritrophic matrix synthesis, architecture, and function. Annu Rev Entomol 54:285–302CrossRefPubMedGoogle Scholar
  48. Hogenkamp DG, Arakane Y, Kramer KJ, Muthukrishnan S, Beeman RW (2008) Characterization and expression of the beta-N-acetylhexosaminidase gene family of Tribolium castaneum. Insect Biochem Mol Biol 38(4):478–489CrossRefPubMedGoogle Scholar
  49. Hopkins TL, Harper MS (2001) Lepidopteran peritrophic membranes and effects of dietary wheat germ agglutinin on their formation and structure. Arch Insect Biochem Physiol 47(2):100–109CrossRefPubMedGoogle Scholar
  50. 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 52:51–59CrossRefPubMedPubMedCentralGoogle Scholar
  51. Izumida H, Imamura N, Sano H (1996) A novel chitinase inhibitor from a marine bacterium, Pseudomonas sp. J Antibiot (Tokyo) 49(1):76–80CrossRefGoogle Scholar
  52. Jalil SU, Mishra M, Ansari MI (2015) Current view on chitinase for plant defence. Trends in Biosciences 8(24):6733–6743Google Scholar
  53. 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(3):214–227CrossRefPubMedGoogle Scholar
  54. 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(11):e49844CrossRefPubMedPubMedCentralGoogle Scholar
  55. Jin S, Singh ND, Li L, Zhang X, Daniell H (2015) Engineered chloroplast dsRNA silences cytochrome p450 monooxygenase, V-ATPase and chitin synthase genes in the insect gut and disrupts Helicoverpa armigera larval development and pupation. Plant Biotechnol J 13(3):435–446CrossRefPubMedPubMedCentralGoogle Scholar
  56. 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):1–9CrossRefPubMedGoogle Scholar
  57. Kato T, Shizuri Y, Izumida H, Yokoyama A, Endo M (1995) Styloguanidines, new chitinase inhibitors from the marine sponge Stylotella aurantium. Tetrahedron Lett 36:2133–2136CrossRefGoogle Scholar
  58. 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 56:21–28CrossRefPubMedGoogle Scholar
  59. Khajuria C, Buschman LL, Chen MS, Muthukrishnan S, Zhu KY (2010) A gut-specific chitinase gene essential for regulation of chitin content of peritrophic matrix and growth of Ostrinia nubilalis larvae. Insect Biochem Mol Biol 40(8):621–629CrossRefPubMedGoogle Scholar
  60. Koganemaru R, Miller DM, Adelman ZN (2013) Robust cuticular penetration resistance in the common bed bug (Cimex lectularius L.) correlates with increased steady-state transcript levels of CPR-type cuticle protein genes. Pestic Biochem Physiol 106(3):190–197CrossRefGoogle Scholar
  61. Kramer KJ, Muthukrishnan S (1997) Insect chitinases: Molecular biology and potential use as biopesticides. Insect Biochem Mol Biol 27(11):887–900CrossRefPubMedGoogle Scholar
  62. Kuraishi T, Binggeli O, Opota O, Buchon N, Lemaitre B (2011) Genetic evidence for a protective role of the peritrophic matrix against intestinal bacterial infection in Drosophila melanogaster. Proc Natl Acad Sci 108(38):15966–15971CrossRefPubMedGoogle Scholar
  63. Kuraishi T, Hori A, Kurata S (2013) Host-microbe interactions in the gut of Drosophila melanogaster. Front Physiol 4:375CrossRefPubMedPubMedCentralGoogle Scholar
  64. 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
  65. Lawrence SD, Novak NG (2006) Expression of poplar chitinase in tomato leads to inhibition of development in colorado potato beetle. Biotech Lett 28(8):593–599CrossRefGoogle Scholar
  66. Lee J-B, Kim HS, Park Y (2017) Down-regulation of a chitin synthase a gene by RNA interference enhances pathogenicity of Beauveria bassiana ANU1 against Spodoptera exigua (HÜBNER). Arch Insect Biochem Physiol 94(2):e21371CrossRefGoogle Scholar
  67. Lepore LS, Roelvink PR, Granados RR (1996) Enhancin, the granulosis virus protein that facilitates nucleopolyhedrovirus (NPV) infections, is a metalloprotease. J Invertebr Pathol 68(2):131–140CrossRefPubMedGoogle Scholar
  68. Lertcanawanichakul M, Wiwat C, Bhumiratana A, Dean DH (2004) Expression of chitinase-encoding genes in Bacillus thuringiensis and toxicity of engineered B. thuringiensis subsp. aizawai toward Lymantria dispar larvae. Curr Microbiol 48(3):175–181CrossRefPubMedGoogle Scholar
  69. 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 58:46–54CrossRefPubMedGoogle Scholar
  70. 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(2):186–194CrossRefPubMedGoogle Scholar
  71. Macedo LLP, de Souza Antonino, Junior JD, Coelho RR, Fonseca FCA, Firmino AAP, Silva MCM et al (2017) Knocking down chitin synthase 2 by RNAi is lethal to the cotton boll weevil. Biotechnol Res Innovat 1(1):72–86CrossRefGoogle Scholar
  72. Mamta Reddy KRK, Rajam MV (2015) Targeting chitinase gene of Helicoverpa armigera by host-induced RNA interference confers insect resistance in tobacco and tomato. Plant Mol Biol 90(3):281–292CrossRefPubMedGoogle Scholar
  73. Marx JL (1977) Chitin synthesis inhibitors: new class of insecticides. Science 197(4309):1170–1172CrossRefPubMedGoogle Scholar
  74. Merzendorfer H (2006) Insect chitin synthases: a review. J Comparat Physiol B-Biochem Syst Environ Physiol 176(1):1–15CrossRefGoogle Scholar
  75. Merzendorfer H (2013) Chitin synthesis inhibitors: old molecules and new developments. Insect Sci 20(2):121–138CrossRefPubMedGoogle Scholar
  76. Merzendorfer H, Kim HS, Chaudhari SS, Kumari M, Specht CA, Butcher S et al (2012) Genomic and proteomic studies on the effects of the insect growth regulator diflubenzuron in the model beetle species Tribolium castaneum. Insect Biochem Mol Biol 42(4):264–276CrossRefPubMedGoogle Scholar
  77. Merzendorfer H, Zimoch L (2003) Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases. J Exp Biol 206(24):4393–4412CrossRefPubMedGoogle Scholar
  78. Mohammed AMA, Diab MR, Abdelsattar M, Khalil SMS (2017) Characterization and RNAi-mediated knockdown of chitin synthase A in the potato tuber moth, Phthorimaea operculella. Sci Rep 7(1):9502Google Scholar
  79. Muthukrishnan S, Merzendorfer H, Arakane Y, Kramer KJ (2012) 7 - Chitin Metabolism in Insects. In: Gilbert LI (ed) Insect molecular biology and biochemistry. Academic Press, San Diego, pp 193–235CrossRefGoogle Scholar
  80. Nauen R, Smagghe G (2006) Mode of action of etoxazole. Pest Manag Sci 62(5):379–382CrossRefPubMedGoogle Scholar
  81. Noh MY, Kramer KJ, Muthukrishnan S, Kanost MR, Beeman RW, Arakane Y (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 53:22–29CrossRefPubMedGoogle Scholar
  82. Noh MY, Muthukrishnan S, Kramer KJ, Arakane Y (2015) Tribolium castaneum RR-1 cuticular protein TcCPR4 Is required for formation of pore canals in rigid cuticle. PLoS Genet 11(2):e1004963CrossRefPubMedPubMedCentralGoogle Scholar
  83. Noh MY, Muthukrishnan S, Kramer KJ, Arakane Y (2018) A chitinase with two catalytic domains is required for organization of the cuticular extracellular matrix of a beetle. PLoS Genet 14(3):e1007307CrossRefPubMedPubMedCentralGoogle Scholar
  84. Okay S, Tefon BE, Özkan M, Özcengiz G (2007). Expression of chitinase A (chiA) gene from a local isolate of Serratia marcescens in Coleoptera-specific Bacillus thuringiensis. J Appl Microbiol 104(1):161–170Google Scholar
  85. Omura S, Arai N, Yamaguchi Y, Masuma R, Iwai Y, Namikoshi M et al (2000) Argifin, a new chitinase inhibitor, produced by Gliocladium sp. FTD-0668. I. Taxonomy, fermentation, and biological activities. J Antibiot (Tokyo) 53(6):603–608CrossRefGoogle Scholar
  86. Osman GH, Assem SK, Alreedy RM, El-Ghareeb DK, Basry MA, Rastogi A et al (2015). Development of insect resistant maize plants expressing a chitinase gene from the cotton leaf worm, Spodoptera littoralis. Sci Rep 5(1):18067Google Scholar
  87. Oyeleye A, Normi YM (2018). Chitinase: Diversity, limitations and trends in engineering for suitable applications. Biosci Rep BSR20180323Google Scholar
  88. Pesch Y-Y, Riedel D, Patil KR, Loch G, Behr M (2016) Chitinases and imaginal disc growth factors organize the extracellular matrix formation at barrier tissues in insects. Sci Rep 6(1)Google Scholar
  89. Petkau G, Wingen C, Jussen LCA, Radtke T, Behr M (2012) Obstructor-A is required for epithelial extracellular matrix dynamics, exoskeleton function, and tubulogenesis. J Biol Chem 287(25):21396–21405CrossRefPubMedPubMedCentralGoogle Scholar
  90. Popp J, Pető K, Nagy J (2012) Pesticide productivity and food security: a review. Agronom Sustain Develop 33(1):243–255CrossRefGoogle Scholar
  91. Qiao L, Xiong G, R-x Wang, S-z He, Chen J, X-l Tong et al (2014) Mutation of a cuticular protein, BmorCPR2, alters larval body shape and adaptability in silkworm, Bombyx mori. Genet 196(4):1103–1115Google Scholar
  92. Quan G, Ladd T, Duan J, Wen F, Doucet D, Cusson M et al (2013) Characterization of a spruce budworm chitin deacetylase gene: Stage- and tissue-specific expression, and inhibition using RNA interference. Insect Biochem Molecul BiolGoogle Scholar
  93. Rao FV, Andersen OA, Vora KA, Demartino JA, van Aalten DM (2005) Methylxanthine drugs are chitinase inhibitors: investigation of inhibition and binding modes. Chem Biol 12(9):973–980CrossRefPubMedGoogle Scholar
  94. Regev A, Keller M, Strizhov N, Sneh B, Prudovsky E, Chet I et al (1996) Synergistic Activity of a Bacillus thuringiensis delta-endotoxin and a bacterial endochitinase against Spodoptera littoralis larvae. Appl Environ Microbiol 62(10):3581–3586PubMedPubMedCentralGoogle Scholar
  95. Roelvink PW, Corsaro BG, Granados RR (1995) Characterization of the Helicoverpa armigera and Pseudaletia unipuncta granulovirus enhancin genes. J Gen Virol 76(11):2693–2705CrossRefPubMedGoogle Scholar
  96. Rohrbough J, Rushton E, Woodruff E, Fergestad T, Vigneswaran K, Broadie K (2007) Presynaptic establishment of the synaptic cleft extracellular matrix is required for post-synaptic differentiation. Genes Dev 21(20):2607–2628CrossRefPubMedPubMedCentralGoogle Scholar
  97. Rushton E, Rohrbough J, Deutsch K, Broadie K (2012) Structure-function analysis of endogenous lectin mind-the-gap in synaptogenesis. Develop Neurobiol 72(8):1161–1179CrossRefGoogle Scholar
  98. Saguez J, Vincent C, Giordanengo P (2008) Chitinase inhibitors and chitin mimetics for crop protection. Pest Technol 2(2):81–86Google Scholar
  99. Sakuda S, Isogai A, Matsumoto S, Suzuki A (1987) Search for microbial insect growth regulators. II. Allosamidin, a novel insect chitinase inhibitor. J Antibiot (Tokyo) 40(3):296–300Google Scholar
  100. Sakuda S, Isogai A, Matsumoto S, Suzuki A, Koseki K (1986) The structure of allosamidin, a novel insect chitinase inhibitor, produced by Streptomyces Sp. Tetrahedron Lett 27(22):2475–2478CrossRefGoogle Scholar
  101. Shapiro M, Robertson JL (1992) Enhancement of gypsy moth Lepidoptera Lymantriidae baculovirus activity by optical brighteners. J Econ Entomol 85:1120–1124CrossRefGoogle Scholar
  102. Shen Z, Jacobs-Lorena M (1998) A type I peritrophic matrix protein from the malaria vector Anopheles gambiae binds to chitin. Cloning, expression, and characterization. J Biol Chem 273(28):17665–17670CrossRefPubMedGoogle Scholar
  103. Shi J-F, Mu L-L, Chen X, Guo W-C, Li G-Q (2016) RNA interference of chitin synthase genes inhibits chitin biosynthesis and affects larval performance in Leptinotarsa decemlineata (Say). Int J Biol Sci 12(11):1319–1331CrossRefPubMedPubMedCentralGoogle Scholar
  104. Shiomi K, Arai N, Iwai Y, Turberg A, Kolbl H, Omura S (2000) The structure of argifin, a new chitinase inhibitor, produced by Gliocladium sp. Tetrahedron Lett 41:2141–2143CrossRefGoogle Scholar
  105. Song T-Q, Yang M-L, Wang Y-L, Liu Q, Wang H-M, Zhang J et al (2016) Cuticular protein LmTwdl1 is involved in molt development of the migratory locust. Insect Sci 23(4):520–530CrossRefPubMedGoogle Scholar
  106. St. Leger RJ, Cooper RM, Charnley AK (1986) Cuticle-degrading enzymes of entomopathogenic fungi: Cuticle degradation in vitro by enzymes from entomopathogens. J Inverteb Pathol 47(2):167–177Google Scholar
  107. Sun R, Liu C, Zhang H, Wang Q (2015) Benzoylurea chitin synthesis inhibitors. J Agric Food Chem 63(31):6847–6865CrossRefPubMedGoogle Scholar
  108. Tabudravu JN, Eijsink VG, Gooday GW, Jaspars M, Komander D, Legg M et al (2002) Psammaplin A, a chitinase inhibitor isolated from the Fijian marine sponge Aplysinella rhax. Bioorg Med Chem 10(4):1123–1128CrossRefPubMedGoogle Scholar
  109. Tang L, Liang J, Zhan Z, Xiang Z, He N (2010) Identification of the chitin-binding proteins from the larval proteins of silkworm, Bombyx mori. Insect Biochem Mol Biol 40(3):228–234CrossRefPubMedGoogle Scholar
  110. Tantimavanich S, Pantuwatana S, Bhumiratana A, Panbangred W (1997) Cloning of a chitinase gene into Bacillus thuringiensis subsp. aizawai for enhanced insecticidal activity. J Gen Appl Microbiol 43:341–347CrossRefPubMedGoogle Scholar
  111. Tellam RL, Wijffels G, Willadsen P (1999) Peritrophic matrix proteins. Insect Biochem Mol Biol 29(2):87–101CrossRefPubMedGoogle Scholar
  112. Terra WR (2001) The origin and functions of the insect peritrophic membrane and peritrophic gel. Arch Insect Biochem Physiol 47(2):47–61CrossRefPubMedGoogle Scholar
  113. Terra WR, Ferreira C (2005) Biochemistry of digestion. In: Gilbert LI, Iatrou K and Gill SS (eds) Comprehensive molecular insect science. Elseviers B.V., Amsterdam: New York. vol. 4, pp 171–224Google Scholar
  114. Tetreau G, Cao X, Chen Y-R, 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 Molecul Biol 62:114–126Google Scholar
  115. Tetreau G, Dittmer NT, Cao X, Jasrapuria S, Chen Y-R, Muthukrishnan S et al (2015b). Analysis of chitin-binding proteins from Manduca sexta provides new insights into evolution of peritrophin A-type chitin-binding domains in insects. Insect Biochem Molecul Biol 62:127–141Google Scholar
  116. Tiklova K, Tsarouhas V, Samakovlis C (2013) Control of airway tube diameter and integrity by secreted chitin-binding proteins in Drosophila. PLoS One 8(6):e67415Google Scholar
  117. Tsirilakis K, Kim C, Vicencio AG, Andrade C, Casadevall A, Goldman DL (2012) Methylxanthine inhibit fungal chitinases and exhibit antifungal activity. Mycopathologia 173(2–3):83–91CrossRefPubMedGoogle Scholar
  118. Van Leeuwen T, Demaeght P, Osborne EJ, Dermauw W, Gohlke S, Nauen R et al (2012) Population bulk segregant mapping uncovers resistance mutations and the mode of action of a chitin synthesis inhibitor in arthropods. Proc Natl Acad Sci 109(12):4407–4412CrossRefPubMedGoogle Scholar
  119. Wang J, Chen Z, Du J, Sun Y, Liang A (2005) Novel insect resistance in Brassica napus developed by transformation of chitinase and scorpion toxin genes. Plant Cell Rep 24:549–555CrossRefPubMedGoogle Scholar
  120. Wang P, Granados RR (1997a) An intestinal mucin is the target substrate for a baculovirus enhancin. Proc Natl Acad Sci USA 94(13):6977–6982CrossRefPubMedGoogle Scholar
  121. Wang P, Granados RR (1997b) Molecular cloning and sequencing of a novel invertebrate intestinal mucin cDNA. J Biol Chem 272(26):16663–16669CrossRefPubMedGoogle Scholar
  122. Wang P, Granados RR (1998) Observations on the presence of the peritrophic membrane in larval Trichoplusia ni and its role in limiting baculovirus infection. J Invertebr Pathol 72(1):57–62CrossRefPubMedGoogle Scholar
  123. Wang P, Granados RR (2000) Calcofluor disrupts the midgut defense system in insects. Insect Biochem Mol Biol 30:135–143CrossRefPubMedGoogle Scholar
  124. Wang P, Granados RR (2001) Molecular structure of the peritrophic membrane (PM): identification of potential PM target sites for insect control. Arch Insect Biochem Physiol 47(2):110–118CrossRefPubMedGoogle Scholar
  125. Wang P, Hammer DA, Granados RR (1994) Interaction of Trichoplusia ni granulosis virus-encoded enhancin with the midgut epithelium and peritrophic membrane of four lepidopteran insects. J Gen Virol 75(Pt 8):1961–1967CrossRefPubMedGoogle Scholar
  126. Wang P, Li GX, Granados RR (2004) Identification of two new peritrophic membrane proteins from larval Trichoplusia ni: structural characteristics and their functions in the protease rich insect gut. Insect Biochem Mol Biol 34(3):215–227CrossRefPubMedGoogle Scholar
  127. Wang X, Ding X, Gopalakrishnan B, Morgan TD, Johnson L, White FF et al (1996) Characterization of a 46 kDa insect chitinase from transgenic tobacco. Insect Biochem Mol Biol 26(10):1055–1064CrossRefGoogle Scholar
  128. Willis JH, Iconomidou VA, Smith RF, Hamodrakas SJ (2005) Cuticular proteins. In: Gilbert LI, Iatrou K and Gill SS (eds) Comprehensive molecular insect science. Elseviers B.V., Amsterdam: New York. vol 4, pp 79–109Google Scholar
  129. Willis JH, Papandreou NC, Iconomidou VA, Hamodrakas SJ (2012) Cuticular Proteins. In: Gilbert LI (ed) Insect molecular biology and biochemistry. Academic Press, San Diego, pp 134–166CrossRefGoogle Scholar
  130. Wu J-J, Chen Z-C, Wang Y-W, Fu K-Y, Guo W-C, Li G-Q (2018). Silencing chitin deacetylase 2 impairs larval-pupal and pupal-adult molts in Leptinotarsa decemlineata. Insect Molecul Biol 28(1):52–64Google Scholar
  131. Xi Y, Pan P-L, Ye Y-X, Yu B, Zhang C-X (2014) Chitin deacetylase family genes in the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). Insect Molecul Biol 23(6):695–705Google Scholar
  132. Xi Y, Pan PL, Ye YX, Yu B, Xu HJ, Zhang CX (2015) Chitinase-like gene family in the brown planthopper, Nilaparvata lugens. Insect Molecular Biology 24(1):29–40CrossRefPubMedGoogle Scholar
  133. Yahouédo GA, Chandre F, Rossignol M, Ginibre C, Balabanidou V, Mendez NGA et al (2017). Contributions of cuticle permeability and enzyme detoxification to pyrethroid resistance in the major malaria vector Anopheles gambiae. Scientif Rep 7(1):11091Google Scholar
  134. Yang W-J, Xu K-K, Yan X, Chen C-X, Cao Y, Meng Y-L et al (2018) Functional characterization of chitin deacetylase 1 gene disrupting larval–pupal transition in the drugstore beetle using RNA interference. Comp Biochem Physiol B: Biochem Mol Biol 219–220:10–16Google Scholar
  135. Zhang D, Chen J, Yao Q, Pan Z, Chen J, Zhang W (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(4–5):220–234CrossRefPubMedGoogle Scholar
  136. Zhu KY, Merzendorfer H, Zhang W, Zhang J, Muthukrishnan S (2016) Biosynthesis, turnover, and functions of chitin in insects. Annu Rev Entomol 61:177–196CrossRefPubMedGoogle Scholar
  137. Zhu Q, Arakane Y, Beeman RW, Kramer KJ, Muthukrishnan S (2008) Functional specialization among insect chitinase family genes revealed by RNA interference. Proc Natl Acad Sci USA 105(18):6650–6655CrossRefPubMedGoogle Scholar
  138. 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(6):515–527CrossRefPubMedGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.University of Grenoble Alpes, CNRS, CEA, IBSGrenobleFrance
  2. 2.Department of EntomologyCornell UniversityGenevaUSA

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