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Review Article

Insect Cuticular Chitin Contributes to Form and Function

Author(s): Subbaratnam Muthukrishnan*, Seulgi Mun, Mi Y. Noh, Erika R. Geisbrecht and Yasuyuki Arakane*

Volume 26, Issue 29, 2020

Page: [3530 - 3545] Pages: 16

DOI: 10.2174/1381612826666200523175409

Price: $65

Abstract

Chitin contributes to the rigidity of the insect cuticle and serves as an attachment matrix for other cuticular proteins. Deficiency of chitin results in abnormal embryos, cuticular structural defects and growth arrest. When chitin is not turned over during molting, the developing insect is trapped inside the old cuticle. Partial deacetylation of cuticular chitin is also required for proper laminar organization of the cuticle and vertical pore canals, molting, and locomotion. Thus, chitin and its modifications strongly influence the structure of the exoskeleton as well as the physiological functions of the insect.

Internal tendons and specialized epithelial cells called “tendon cells” that arise from the outer layer of epidermal cells provide attachment sites at both ends of adult limb muscles. Membrane processes emanating from both tendon and muscle cells interdigitate extensively to strengthen the attachment of muscles to the extracellular matrix (ECM). Protein ligands that bind to membrane-bound integrin complexes further enhance the adhesion between muscles and tendons. Tendon cells contain F-actin fiber arrays that contribute to their rigidity. In the cytoplasm of muscle cells, proteins such as talin and other proteins provide attachment sites for cytoskeletal actin, thereby increasing integrin binding and activation to mechanically couple the ECM with actin in muscle cells. Mutations in integrins and their ligands, as well as depletion of chitin deacetylases, result in defective locomotion and muscle detachment from the ECM. Thus, chitin in the cuticle and chitin deacetylases strongly influence the shape and functions of the exoskeleton as well as locomotion of insects.

Keywords: Chitin, cuticle, insects, deacetylation, molting, locomotion, muscle attachment.

« Previous Next »
[1]
Neville AC, Parry DA, Woodhead-Galloway J. The chitin crystallite in arthropod cuticle. J Cell Sci 1976; 21(1): 73-82.
[PMID: 932111]
[2]
Fabritius HO, Sachs C, Triguero PR, Roobe D. Influence of structural principles on the mechanics of a biological fiber-based composite material with hierarchical organization: the exoskeleton of the lobster Homarus americanus. Adv Mater 2009; 21: 391-400.
[http://dx.doi.org/10.1002/adma.200801219]
[3]
Rebers JE, Willis JH. A conserved domain in arthropod cuticular proteins binds chitin. Insect Biochem Mol Biol 2001; 31(11): 1083-93.
[http://dx.doi.org/10.1016/S0965-1748(01)00056-X] [PMID: 11520687]
[4]
Jasrapuria S, Arakane Y, Osman G, Kramer KJ, Beeman RW, Muthukrishnan S. 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 2010; 40(3): 214-27.
[http://dx.doi.org/10.1016/j.ibmb.2010.01.011] [PMID: 20144715]
[5]
Rudall KM, Kenchington W. The chitin system. Biol Rev Camb Philos Soc 1973; 49: 597-636.
[http://dx.doi.org/10.1111/j.1469-185X.1973.tb01570.x]
[6]
Zhou Y, Badgett MJ, Bowen JH, Vannini L, Orlando R, Willis JH. Distribution of cuticular proteins in different structures of adult Anopheles gambiae. Insect Biochem Mol Biol 2016; 75: 45-57.
[http://dx.doi.org/10.1016/j.ibmb.2016.05.001] [PMID: 27179905]
[7]
Vannini L, Willis JH. Localization of RR-1 and RR-2 cuticular proteins within the cuticle of Anopheles gambiae. Arthropod Struct Dev 2017; 46(1): 13-29.
[http://dx.doi.org/10.1016/j.asd.2016.10.002] [PMID: 27717796]
[8]
Dittmer NT, Hiromasa Y, Tomich JM, et al. Proteomic and transcriptomic analyses of rigid and membranous cuticles and epidermis from the elytra and hindwings of the red flour beetle, Tribolium castaneum. J Proteome Res 2012; 11(1): 269-78.
[http://dx.doi.org/10.1021/pr2009803] [PMID: 22087475]
[9]
Kramer KJ, Muthukrishnan S. Chitin metabolism in insects Comprehensive Molecular Insect Science. Oxford, UK: Elsevier 2005; pp. 111-44.
[http://dx.doi.org/10.1016/B0-44-451924-6/00051-X]
[10]
Moreira MF, Dos Santos AS, Marotta HR, et al. A chitin-like component in Aedes aegypti eggshells, eggs and ovaries. Insect Biochem Mol Biol 2007; 37(12): 1249-61.
[http://dx.doi.org/10.1016/j.ibmb.2007.07.017] [PMID: 17967344]
[11]
Noh MY, Muthukrishnan S, Kramer KJ, Arakane Y. Development and ultrastructure of the rigid dorsal and flexible ventral cuticles of the elytron of the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol 2017; 91: 21-33.
[http://dx.doi.org/10.1016/j.ibmb.2017.11.003] [PMID: 29117500]
[12]
Cohen E. Chitin biochemistry: synthesis, hydrolysis and inhibition. Adv Insect Physiol 2010; 38: 5-74.
[http://dx.doi.org/10.1016/S0065-2806(10)38005-2]
[13]
Carlstrom D. The crystal structure of alpha-chitin (poly-N-acetyl-D-glucosamine). J Biophys Biochem Cytol 1957; 3(5): 669-83.
[http://dx.doi.org/10.1083/jcb.3.5.669] [PMID: 13475384]
[14]
Minke R, Blackwell J. The structure of alpha-chitin. J Mol Biol 1978; 120(2): 167-81.
[http://dx.doi.org/10.1016/0022-2836(78)90063-3] [PMID: 642008]
[15]
Sikorski P, Hori R, Wada M. Revisit of alpha-chitin crystal structure using high resolution X-ray diffraction data. Biomacromolecules 2009; 10(5): 1100-5.
[http://dx.doi.org/10.1021/bm801251e] [PMID: 19334783]
[16]
Beckham GT, Crowley MF. Examination of the α-chitin structure and decrystallization thermodynamics at the nanoscale. J Phys Chem B 2011; 115(15): 4516-22.
[http://dx.doi.org/10.1021/jp200912q] [PMID: 21452798]
[17]
Bouligand Y. Twisted fibrous arrangements in biological materials and cholesteric mesophases. Tissue Cell 1972; 4(2): 189-217.
[http://dx.doi.org/10.1016/S0040-8166(72)80042-9] [PMID: 4600349]
[18]
Cheng L, Wang LY, Karlsson AM. Mechanics-based analysis of selected features of the exoskeletal microstructure of Popillia japonica. J Mater Res 2009; 24: 3253-67.
[http://dx.doi.org/10.1557/jmr.2009.0409]
[19]
Barbakadze N, Enders S, Gorb S, Arzt E. Local mechanical properties of the head articulation cuticle in the beetle Pachnoda marginata (Coleoptera, Scarabaeidae). J Exp Biol 2006; 209(Pt 4): 722-30.
[http://dx.doi.org/10.1242/jeb.02065] [PMID: 16449566]
[20]
van de Kamp T, Riedel A, Greven H. Micromorphology of the elytral cuticle of beetles, with an emphasis on weevils (Coleoptera: Curculionoidea). Arthropod Struct Dev 2016; 45(1): 14-22.
[http://dx.doi.org/10.1016/j.asd.2015.10.002] [PMID: 26529582]
[21]
Noh MY, Kramer KJ, Muthukrishnan S, Kanost MR, Beeman RW, Arakane Y. 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 2014; 53: 22-9.
[http://dx.doi.org/10.1016/j.ibmb.2014.07.005] [PMID: 25042128]
[22]
Noh MY, Muthukrishnan S, Kramer KJ, Arakane Y. Tribolium castaneum RR-1 cuticular protein TcCPR4 is required for formation of pore canals in rigid cuticle. PLoS Genet 2015; 11(2) e1004963
[http://dx.doi.org/10.1371/journal.pgen.1004963] [PMID: 25664770]
[23]
Mun S, Noh MY, Dittmer NT, et al. Cuticular protein with a low complexity sequence becomes cross-linked during insect cuticle sclerotization and is required for the adult molt. Sci Rep 2015; 5: 10484.
[http://dx.doi.org/10.1038/srep10484] [PMID: 25994234]
[24]
Arakane Y, Hogenkamp DG, Zhu YC, et al. 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 2004; 34(3): 291-304.
[http://dx.doi.org/10.1016/j.ibmb.2003.11.004] [PMID: 14871625]
[25]
Ashfaq M, Sonoda S, Tsumuki H. Developmental and tissue-specific expression of CHS1 from Plutella xylostella and its response to chlorfluazuron. Pestic Biochem Physiol 2007; 89: 20-30.
[http://dx.doi.org/10.1016/j.pestbp.2007.02.004]
[26]
Wang Y, Fan HW, Huang HJ, et al. 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 2012; 42(9): 637-46.
[http://dx.doi.org/10.1016/j.ibmb.2012.04.009] [PMID: 22634163]
[27]
Yang WJ, Xu KK, Cong L, Wang JJ. 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 2013; 9(4): 331-42.
[http://dx.doi.org/10.7150/ijbs.6022] [PMID: 23569438]
[28]
Muthukrishnan S, Merzendorfer H, Arakane Y, Yang Q. Chitin metabolic pathways in insects and their regulationExtracellular composite matrices in arthropods. Switzerland: Springer 2016; pp. 31-65.
[http://dx.doi.org/10.1007/978-3-319-40740-1_2]
[29]
Merzendorfer H. Insect chitin synthases: a review. J Comp Physiol B 2006; 176(1): 1-15.
[http://dx.doi.org/10.1007/s00360-005-0005-3] [PMID: 16075270]
[30]
Jürgens G, Wieschaus E, Nüsslein-Volhard C, Kluding H. Mutations affecting the pattern of the larval cuticle inDrosophila melanogaster: II. Zygotic loci on the third chromosome. Wilehm Roux Arch Dev Biol 1984; 193(5): 283-95.
[http://dx.doi.org/10.1007/BF00848157] [PMID: 28305338]
[31]
Tellam RL, Vuocolo T, Johnson SE, Jarmey J, Pearson RD. Insect chitin synthase cDNA sequence, gene organization and expression. Eur J Biochem 2000; 267(19): 6025-43.
[http://dx.doi.org/10.1046/j.1432-1327.2000.01679.x] [PMID: 10998064]
[32]
Ibrahim GH, Smartt CT, Kiley LM, Christensen BM. Cloning and characterization of a chitin synthase cDNA from the mosquito Aedes aegypti. Insect Biochem Mol Biol 2000; 30(12): 1213-22.
[http://dx.doi.org/10.1016/S0965-1748(00)00100-4] [PMID: 11044667]
[33]
Zhu YC, Specht CA, Dittmer NT, Muthukrishnan S, Kanost MR, Kramer KJ. Sequence of a cDNA and expression of the gene encoding a putative epidermal chitin synthase of Manduca sexta. Insect Biochem Mol Biol 2002; 32(11): 1497-506.
[http://dx.doi.org/10.1016/S0965-1748(02)00070-X] [PMID: 12530217]
[34]
Ostrowski S, Dierick HA, Bejsovec A. Genetic control of cuticle formation during embryonic development of Drosophila melanogaster. Genetics 2002; 161(1): 171-82.
[PMID: 12019232]
[35]
Moussian B, Schwarz H, Bartoszewski S, Nüsslein-Volhard C. Involvement of chitin in exoskeleton morphogenesis in Drosophila melanogaster. J Morphol 2005; 264(1): 117-30.
[http://dx.doi.org/10.1002/jmor.10324] [PMID: 15747378]
[36]
Noh MY, Muthukrishnan S, Kramer KJ, Arakane Y. A chitinase with two catalytic domains is required for organization of the cuticular extracellular matrix of a beetle. PLoS Genet 2018; 14(3) e1007307
[http://dx.doi.org/10.1371/journal.pgen.1007307] [PMID: 29590098]
[37]
Tian H, Peng H, Yao Q, et al. Developmental control of a lepidopteran pest Spodoptera exigua by ingestion of bacteria expressing dsRNA of a non-midgut gene. PLoS One 2009; 4(7) e6225
[http://dx.doi.org/10.1371/journal.pone.0006225] [PMID: 19593438]
[38]
Arakane Y, Muthukrishnan S, Kramer KJ, et al. The Tribolium chitin synthase genes TcCHS1 and TcCHS2 are specialized for synthesis of epidermal cuticle and midgut peritrophic matrix. Insect Mol Biol 2005; 14(5): 453-63.
[http://dx.doi.org/10.1111/j.1365-2583.2005.00576.x] [PMID: 16164601]
[39]
Zhang J, Liu X, Zhang J, et al. 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 2010; 40(11): 824-33.
[http://dx.doi.org/10.1016/j.ibmb.2010.08.001] [PMID: 20713155]
[40]
Rezende GL, Martins AJ, Gentile C, et al. Embryonic desiccation resistance in Aedes aegypti: presumptive role of the chitinized serosal cuticle. BMC Dev Biol 2008; 8: 82.
[http://dx.doi.org/10.1186/1471-213X-8-82] [PMID: 18789161]
[41]
Jacobs CG, Braak N, Lamers GE, van der Zee M. 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 2015; 60: 7-12.
[http://dx.doi.org/10.1016/j.ibmb.2015.02.014] [PMID: 25747006]
[42]
Chaudhari SS, Arakane Y, Specht CA, et al. Knickkopf protein protects and organizes chitin in the newly synthesized insect exoskeleton. Proc Natl Acad Sci USA 2011; 108(41): 17028-33.
[http://dx.doi.org/10.1073/pnas.1112288108] [PMID: 21930896]
[43]
Souza-Ferreira PS, Mansur JF, Berni M, et al. 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 2014; 51: 101-9.
[http://dx.doi.org/10.1016/j.ibmb.2013.12.004] [PMID: 24412274]
[44]
Ye C, Jiang YD, An X, et al. Effects of RNAi-based silencing of chitin synthase gene on moulting and fecundity in pea aphids (Acyrthosiphon pisum). Sci Rep 2019; 9(1): 3694.
[http://dx.doi.org/10.1038/s41598-019-39837-4] [PMID: 30842508]
[45]
Mansur JF, Figueira-Mansur J, Santos AS, et al. The effect of lufenuron, a chitin synthesis inhibitor, on oogenesis of Rhodnius prolixus. Pestic Biochem Physiol 2010; 98: 59-67.
[http://dx.doi.org/10.1016/j.pestbp.2010.04.013]
[46]
Bansal R, Mian MAR, Mittapalli O, Michel AP. Characterization of a chitin synthase encoding gene and effect of diflubenzuron in soybean aphid, Aphis glycines. Int J Biol Sci 2012; 8(10): 1323-34.
[http://dx.doi.org/10.7150/ijbs.4189] [PMID: 23139631]
[47]
Chaudhari SS, Noh MY, Moussian B, et al. Knickkopf and retroactive proteins are required for formation of laminar serosal procuticle during embryonic development of Tribolium castaneum. Insect Biochem Mol Biol 2015; 60: 1-6.
[http://dx.doi.org/10.1016/j.ibmb.2015.02.013] [PMID: 25747009]
[48]
Arakane Y, Specht CA, Kramer KJ, Muthukrishnan S, Beeman RW. Chitin synthases are required for survival, fecundity and egg hatch in the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol 2008; 38(10): 959-62.
[http://dx.doi.org/10.1016/j.ibmb.2008.07.006] [PMID: 18718535]
[49]
Farnesi LC, Menna-Barreto RF, Martins AJ, Valle D, Rezende GL. Physical features and chitin content of eggs from the mosquito vectors Aedes aegypti, Anopheles aquasalis and Culex quinquefasciatus: Connection with distinct levels of resistance to desiccation. J Insect Physiol 2015; 83: 43-52.
[http://dx.doi.org/10.1016/j.jinsphys.2015.10.006] [PMID: 26514070]
[50]
Qu M, Yang Q. 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 2011; 41(12): 923-31.
[http://dx.doi.org/10.1016/j.ibmb.2011.09.001] [PMID: 21933709]
[51]
Qu M, Yang Q. 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 2012; 21(4): 395-404.
[http://dx.doi.org/10.1111/j.1365-2583.2012.01145.x] [PMID: 22607200]
[52]
Moussian B, Tång E, Tonning A, et al. Drosophila Knickkopf and Retroactive are needed for epithelial tube growth and cuticle differentiation through their specific requirement for chitin filament organization. Development 2006; 133(1): 163-71.
[http://dx.doi.org/10.1242/dev.02177] [PMID: 16339194]
[53]
Hogenkamp DG, Arakane Y, Zimoch L, et al. 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 2005; 35(6): 529-40.
[http://dx.doi.org/10.1016/j.ibmb.2005.01.016] [PMID: 15857759]
[54]
Zimoch L, Hogenkamp DG, Kramer KJ, Muthukrishnan S, Merzendorfer H. Regulation of chitin synthesis in the larval midgut of Manduca sexta. Insect Biochem Mol Biol 2005; 35(6): 515-27.
[http://dx.doi.org/10.1016/j.ibmb.2005.01.008] [PMID: 15857758]
[55]
Bolognesi R, Arakane Y, Muthukrishnan S, Kramer KJ, Terra WR, Ferreira C. Sequences of cDNAs and expression of genes encoding chitin synthase and chitinase in the midgut of Spodoptera frugiperda. Insect Biochem Mol Biol 2005; 35(11): 1249-59.
[http://dx.doi.org/10.1016/j.ibmb.2005.06.006] [PMID: 16203206]
[56]
Kumar NS, Tang B, Chen X, Tian H, Zhang W. Molecular cloning, expression pattern and comparative analysis of chitin synthase gene B in Spodoptera exigua. Comp Biochem Physiol B Biochem Mol Biol 2008; 149(3): 447-53.
[http://dx.doi.org/10.1016/j.cbpb.2007.11.005] [PMID: 18178495]
[57]
Kato N, Mueller CR, Fuchs JF, Wessely V, Lan Q, Christensen BM. Regulatory mechanisms of chitin biosynthesis and roles of chitin in peritrophic matrix formation in the midgut of adult Aedes aegypti. Insect Biochem Mol Biol 2006; 36(1): 1-9.
[http://dx.doi.org/10.1016/j.ibmb.2005.09.003] [PMID: 16360944]
[58]
Agrawal S, Kelkenberg M, Begum K, et al. Two essential peritrophic matrix proteins mediate matrix barrier functions in the insect midgut. Insect Biochem Mol Biol 2014; 49: 24-34.
[http://dx.doi.org/10.1016/j.ibmb.2014.03.009] [PMID: 24680676]
[59]
Kelkenberg M, Odman-Naresh J, Muthukrishnan S, Merzendorfer H. Chitin is a necessary component to maintain the barrier function of the peritrophic matrix in the insect midgut. Insect Biochem Mol Biol 2015; 56: 21-8.
[http://dx.doi.org/10.1016/j.ibmb.2014.11.005] [PMID: 25449129]
[60]
Zhang X, Zhang J, Zhu KY. 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 2010; 19(5): 683-93.
[http://dx.doi.org/10.1111/j.1365-2583.2010.01029.x] [PMID: 20629775]
[61]
Locke M, Huie P. Apolysis and the turnover of plasma membrane plaques during cuticle formation in an insect. Tissue Cell 1979; 11(2): 277-91.
[http://dx.doi.org/10.1016/0040-8166(79)90042-9] [PMID: 473162]
[62]
Leopold RA, Newman SM, Helgeson G. A comparison of cuticle deposition during the pre- and posteclosion stages of the adult weevil, Anthonomus grandis Boheman (Coleoptera: Curculionidae). Int J Insect Morphol Embryol 1992; 21: 37-62.
[http://dx.doi.org/10.1016/0020-7322(92)90004-7]
[63]
Moussian B, Seifarth C, Müller U, Berger J, Schwarz H. Cuticle differentiation during Drosophila embryogenesis. Arthropod Struct Dev 2006; 35(3): 137-52.
[http://dx.doi.org/10.1016/j.asd.2006.05.003] [PMID: 18089066]
[64]
Sobala LF, Adler PN. The gene expression program for the formation of wing cuticle in Drosophila. PLoS Genet 2016; 12(5) e1006100
[http://dx.doi.org/10.1371/journal.pgen.1006100] [PMID: 27232182]
[65]
Gullion JD, Gullion T. Solid-state NMR study of the cicada wing. J Phys Chem B 2017; 121(32): 7646-51.
[http://dx.doi.org/10.1021/acs.jpcb.7b05598] [PMID: 28727439]
[66]
Smith CW, Herbert R, Wootton RJ, Evans KE. The hind wing of the desert locust (Schistocerca gregaria Forskål). II. Mechanical properties and functioning of the membrane. J Exp Biol 2000; 203(Pt 19): 2933-43.
[PMID: 10976030]
[67]
Reynolds SE, Samuels RI. Physiology and biochemistry of insect moulting fluid. Adv Insect Physiol 1996; 26: 157-232.
[http://dx.doi.org/10.1016/S0065-2806(08)60031-4]
[68]
Barry MK, Triplett AA, Christensen AC. A peritrophin-like protein expressed in the embryonic tracheae of Drosophila melanogaster. Insect Biochem Mol Biol 1999; 29(4): 319-27.
[http://dx.doi.org/10.1016/S0965-1748(99)00004-1] [PMID: 10333571]
[69]
Behr M, Hoch M. Identification of the novel evolutionary conserved obstructor multigene family in invertebrates. FEBS Lett 2005; 579(30): 6827-33.
[http://dx.doi.org/10.1016/j.febslet.2005.11.021] [PMID: 16325182]
[70]
Jasrapuria S, Specht CA, Kramer KJ, Beeman RW, Muthukrishnan S. Gene families of cuticular proteins analogous to peritrophins (CPAPs) in Tribolium castaneum have diverse functions. PLoS One 2012; 7(11) e49844
[http://dx.doi.org/10.1371/journal.pone.0049844] [PMID: 23185457]
[71]
Qu M, Ren Y, Liu Y, Yang Q. Studies on the chitin/chitosan binding properties of six cuticular proteins analogous to peritrophin 3 from Bombyx mori. Insect Mol Biol 2017; 26(4): 432-9.
[http://dx.doi.org/10.1111/imb.12308] [PMID: 28432772]
[72]
Pesch YY, Riedel D, Behr M. Obstructor A organizes matrix assembly at the apical cell surface to promote enzymatic cuticle maturation in Drosophila. J Biol Chem 2015; 290(16): 10071-82.
[http://dx.doi.org/10.1074/jbc.M114.614933] [PMID: 25737451]
[73]
Petkau G, Wingen C, Jussen LCA, Radtke T, Behr M. Obstructor-A is required for epithelial extracellular matrix dynamics, exoskeleton function, and tubulogenesis. J Biol Chem 2012; 287(25): 21396-405.
[http://dx.doi.org/10.1074/jbc.M112.359984] [PMID: 22544743]
[74]
Broehan G, Arakane Y, Beeman RW, Kramer KJ, Muthukrishnan S, Merzendorfer H. Chymotrypsin-like peptidases from Tribolium castaneum: a role in molting revealed by RNA interference. Insect Biochem Mol Biol 2010; 40(3): 274-83.
[http://dx.doi.org/10.1016/j.ibmb.2009.10.009] [PMID: 19897036]
[75]
Qu M, Ma L, Chen P, Yang Q. Proteomic analysis of insect molting fluid with a focus on enzymes involved in chitin degradation. J Proteome Res 2014; 13(6): 2931-40.
[http://dx.doi.org/10.1021/pr5000957] [PMID: 24779478]
[76]
Liu HW, Wang LL, Tang X, et al. Proteomic analysis of Bombyx mori molting fluid: Insights into the molting process. J Proteomics 2018; 173: 115-25.
[http://dx.doi.org/10.1016/j.jprot.2017.11.027] [PMID: 29197581]
[77]
Zhang J, Lu A, Kong L, Zhang Q, Ling E. Functional analysis of insect molting fluid proteins on the protection and regulation of ecdysis. J Biol Chem 2014; 289(52): 35891-906.
[http://dx.doi.org/10.1074/jbc.M114.599597] [PMID: 25368323]
[78]
Vaaje-Kolstad G, Bøhle LA, Gåseidnes S, et al. Characterization of the chitinolytic machinery of Enterococcus faecalis V583 and high-resolution structure of its oxidative CBM33 enzyme. J Mol Biol 2012; 416(2): 239-54.
[http://dx.doi.org/10.1016/j.jmb.2011.12.033] [PMID: 22210154]
[79]
Vaaje-Kolstad G, Westereng B, Horn SJ, et al. An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science 2010; 330(6001): 219-22.
[http://dx.doi.org/10.1126/science.1192231] [PMID: 20929773]
[80]
Courtade G, Aachmann FL. Chitin-active lytic polysaccharide monooxygenasesAdv Exp Med Biol. Singapore: Springer 2019; pp. 115-29.
[81]
Sabbadin F, Hemsworth GR, Ciano L, et al. An ancient family of lytic polysaccharide monooxygenases with roles in arthropod development and biomass digestion. Nat Commun 2018; 9(1): 756.
[http://dx.doi.org/10.1038/s41467-018-03142-x] [PMID: 29472725]
[82]
Filiatrault-Chastel C, Navarro D, Haon M, et al. AA16, a new lytic polysaccharide monooxygenase family identified in fungal secretomes. Biotechnol Biofuels 2019; 12: 55.
[http://dx.doi.org/10.1186/s13068-019-1394-y] [PMID: 30923563]
[83]
Zhu Q, Arakane Y, Banerjee D, Beeman RW, Kramer KJ, Muthukrishnan S. Domain organization and phylogenetic analysis of the chitinase-like family of proteins in three species of insects. Insect Biochem Mol Biol 2008; 38(4): 452-66.
[http://dx.doi.org/10.1016/j.ibmb.2007.06.010] [PMID: 18342250]
[84]
Tetreau G, Cao X, Chen YR, et al. Overview of chitin metabolism enzymes in Manduca sexta: Identification, domain organization, phylogenetic analysis and gene expression. Insect Biochem Mol Biol 2015; 62: 114-26.
[http://dx.doi.org/10.1016/j.ibmb.2015.01.006] [PMID: 25616108]
[85]
Nakabachi A, Shigenobu S, Miyagishima S. Chitinase-like proteins encoded in the genome of the pea aphid, Acyrthosiphon pisum. Insect Mol Biol 2010; 19(Suppl. 2): 175-85.
[http://dx.doi.org/10.1111/j.1365-2583.2009.00985.x] [PMID: 20482649]
[86]
Zhu Q, Arakane Y, Beeman RW, Kramer KJ, Muthukrishnan S. Functional specialization among insect chitinase family genes revealed by RNA interference. Proc Natl Acad Sci USA 2008; 105(18): 6650-5.
[http://dx.doi.org/10.1073/pnas.0800739105] [PMID: 18436642]
[87]
Xi Y, Pan PL, Ye YX, Yu B, Xu HJ, Zhang CX. Chitinase-like gene family in the brown planthopper, Nilaparvata lugens. Insect Mol Biol 2015; 24(1): 29-40.
[http://dx.doi.org/10.1111/imb.12133] [PMID: 25224926]
[88]
Li D, Zhang J, Wang Y, et al. Two chitinase 5 genes from Locusta migratoria: molecular characteristics and functional differentiation. Insect Biochem Mol Biol 2015; 58: 46-54.
[http://dx.doi.org/10.1016/j.ibmb.2015.01.004] [PMID: 25623241]
[89]
Hogenkamp DG, Arakane Y, Kramer KJ, Muthukrishnan S, Beeman RW. Characterization and expression of the β-N-acetylhexosaminidase gene family of Tribolium castaneum. Insect Biochem Mol Biol 2008; 38(4): 478-89.
[http://dx.doi.org/10.1016/j.ibmb.2007.08.002] [PMID: 18342252]
[90]
Liu F, Liu T, Qu M, Yang Q. Molecular and biochemical characterization of a novel β-N-acetyl-D-hexosaminidase with broad substrate-spectrum from the Aisan corn borer, Ostrinia furnacalis. Int J Biol Sci 2012; 8(8): 1085-96.
[http://dx.doi.org/10.7150/ijbs.4406] [PMID: 22991497]
[91]
Rong S, Li DQ, Zhang XY, et al. RNA interference to reveal roles of β-N-acetylglucosaminidase gene during molting process in Locusta migratoria. Insect Sci 2013; 20(1): 109-19.
[http://dx.doi.org/10.1111/j.1744-7917.2012.01573.x] [PMID: 23955831]
[92]
Yang WJ, Xu KK, Yan X, Li C. Knockdown of β-N-acetylglucosaminidase 2 impairs molting and wing development in Lasioderma serricorne (Fabricius). Insects 2019; 10(11): 396.
[http://dx.doi.org/10.3390/insects10110396] [PMID: 31717288]
[93]
Fukamizo T, Kramer KJ. Mechanism of chitin oligosaccharide hydrolysis by the binary enzyme chitinase system in insect molting fluid. Insect Biochem 1985; 15: 1-7.
[http://dx.doi.org/10.1016/0020-1790(85)90037-X]
[94]
Fukamizo T, Kramer KJ. Mechanism of chitin hydrolysis by the binary chitinase system in insect molting fluid. Insect Biochem 1985; 15: 141-5.
[http://dx.doi.org/10.1016/0020-1790(85)90001-0]
[95]
Zhao Y, Park RD, Muzzarelli RA. Chitin deacetylases: properties and applications. Mar Drugs 2010; 8(1): 24-46.
[http://dx.doi.org/10.3390/md8010024] [PMID: 20161969]
[96]
Grifoll-Romero L, Pascual S, Aragunde H, Biarnés X, Planas A. Chitin deacetylases: structures, specificities, and biotech applications. Polymers (Basel) 2018; 10(4): 10.
[http://dx.doi.org/10.3390/polym10040352] [PMID: 30966387]
[97]
Kafetzopoulos D, Thireos G, Vournakis JN, Bouriotis V. The primary structure of a fungal chitin deacetylase reveals the function for two bacterial gene products. Proc Natl Acad Sci USA 1993; 90(17): 8005-8.
[http://dx.doi.org/10.1073/pnas.90.17.8005] [PMID: 8367456]
[98]
Dixit R, Arakane Y, Specht CA, et al. 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 2008; 38(4): 440-51.
[http://dx.doi.org/10.1016/j.ibmb.2007.12.002] [PMID: 18342249]
[99]
Campbell PM, Cao AT, Hines ER, East PD, Gordon KHJ. Proteomic analysis of the peritrophic matrix from the gut of the caterpillar, Helicoverpa armigera. Insect Biochem Mol Biol 2008; 38(10): 950-8.
[http://dx.doi.org/10.1016/j.ibmb.2008.07.009] [PMID: 18760362]
[100]
Xi Y, Pan PL, Ye YX, Yu B, Zhang CX. Chitin deacetylase family genes in the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). Insect Mol Biol 2014; 23(6): 695-705.
[http://dx.doi.org/10.1111/imb.12113] [PMID: 24989071]
[101]
Tetreau G, Dittmer NT, Cao X, et al. Analysis of chitin-binding proteins from Manduca sexta provides new insights into evolution of peritrophin A-type chitin-binding domains in insects. Insect Biochem Mol Biol 2015; 62: 127-41.
[http://dx.doi.org/10.1016/j.ibmb.2014.12.002] [PMID: 25524298]
[102]
Luschnig S, Bätz T, Armbruster K, Krasnow MA. serpentine and vermiform encode matrix proteins with chitin binding and deacetylation domains that limit tracheal tube length in Drosophila. Curr Biol 2006; 16(2): 186-94.
[http://dx.doi.org/10.1016/j.cub.2005.11.072] [PMID: 16431371]
[103]
Wang S, Jayaram SA, Hemphälä J, et al. Septate-junction-dependent luminal deposition of chitin deacetylases restricts tube elongation in the Drosophila trachea. Curr Biol 2006; 16(2): 180-5.
[http://dx.doi.org/10.1016/j.cub.2005.11.074] [PMID: 16431370]
[104]
Arakane Y, Dixit R, Begum K, et al. Analysis of functions of the chitin deacetylase gene family in Tribolium castaneum. Insect Biochem Mol Biol 2009; 39(5-6): 355-65.
[http://dx.doi.org/10.1016/j.ibmb.2009.02.002] [PMID: 19268706]
[105]
Quan G, Ladd T, Duan J, et al. Characterization of a spruce budworm chitin deacetylase gene: stage- and tissue-specific expression, and inhibition using RNA interference. Insect Biochem Mol Biol 2013; 43(8): 683-91.
[http://dx.doi.org/10.1016/j.ibmb.2013.04.005] [PMID: 23628857]
[106]
Yu R, Liu W, Li D, et al. Helicoidal organization of chitin in the cuticle of the migratory locust requires the function of the chitin deacetylase2 enzyme (LmCDA2). J Biol Chem 2016; 291(47): 24352-63.
[http://dx.doi.org/10.1074/jbc.M116.720581] [PMID: 27637332]
[107]
Yu RR, Liu WM, Zhao XM, et al. LmCDA1 organizes the cuticle by chitin deacetylation in Locusta migratoria. Insect Mol Biol 2019; 28(3): 301-12.
[http://dx.doi.org/10.1111/imb.12554] [PMID: 30471154]
[108]
Wu JJ, Chen ZC, Wang YW, Fu KY, Guo WC, Li GQ. Silencing chitin deacetylase 2 impairs larval-pupal and pupal-adult molts in Leptinotarsa decemlineata. Insect Mol Biol 2019; 28(1): 52-64.
[http://dx.doi.org/10.1111/imb.12524] [PMID: 30058750]
[109]
Noh MY, Muthukrishnan S, Kramer KJ, Arakane Y. Group I chitin deacetylases are essential for higher order organization of chitin fibers in beetle cuticle. J Biol Chem 2018; 293(18): 6985-95.
[http://dx.doi.org/10.1074/jbc.RA117.001454] [PMID: 29567838]
[110]
Jakubowska AK, Caccia S, Gordon KH, Ferré J, Herrero S. Downregulation of a chitin deacetylase-like protein in response to baculovirus infection and its application for improving baculovirus infectivity. J Virol 2010; 84(5): 2547-55.
[http://dx.doi.org/10.1128/JVI.01860-09] [PMID: 20032185]
[111]
Leptin M, Bogaert T, Lehmann R, Wilcox M. The function of PS integrins during Drosophila embryogenesis. Cell 1989; 56(3): 401-8.
[http://dx.doi.org/10.1016/0092-8674(89)90243-2] [PMID: 2492451]
[112]
Brown NH. Null mutations in the alpha PS2 and beta PS integrin subunit genes have distinct phenotypes. Development 1994; 120(5): 1221-31.
[PMID: 8026331]
[113]
Brower DL, Bunch TA, Mukai L, et al. Nonequivalent requirements for PS1 and PS2 integrin at cell attachments in Drosophila: genetic analysis of the alpha PS1 integrin subunit. Development 1995; 121(5): 1311-20.
[PMID: 7789263]
[114]
Green N, Odell N, Zych M, et al. A common suite of coagulation proteins function in Drosophila muscle attachment. Genetics 2016; 204(3): 1075-87.
[http://dx.doi.org/10.1534/genetics.116.189787] [PMID: 27585844]
[115]
Bunch TA, Graner MW, Fessler LI, et al. The PS2 integrin ligand tiggrin is required for proper muscle function in Drosophila. Development 1998; 125(9): 1679-89.
[PMID: 9521906]
[116]
Klapholz B, Brown NH. Talin - the master of integrin adhesions. J Cell Sci 2017; 130(15): 2435-46.
[http://dx.doi.org/10.1242/jcs.190991] [PMID: 28701514]
[117]
Soler C, Laddada L, Jagla K. Coordinated development of muscles and tendon-like structures: early interactions in the Drosophila leg. Front Physiol 2016; 7: 22.
[http://dx.doi.org/10.3389/fphys.2016.00022] [PMID: 26869938]
[118]
Alves-Silva J, Hahn I, Huber O, Mende M, Reissaus A, Prokop A. Prominent actin fiber arrays in Drosophila tendon cells represent architectural elements different from stress fibers. Mol Biol Cell 2008; 19(10): 4287-97.
[http://dx.doi.org/10.1091/mbc.e08-02-0182] [PMID: 18667532]
[119]
Reedy MC, Beall C. Ultrastructure of developing flight muscle in Drosophila. II. Formation of the myotendon junction. Dev Biol 1993; 160(2): 466-79.
[http://dx.doi.org/10.1006/dbio.1993.1321] [PMID: 8253278]
[120]
Fernandes JJ, Celniker SE. VijayRaghavan K. Development of the indirect flight muscle attachment sites in Drosophila: role of the PS integrins and the stripe gene. Dev Biol 1996; 176(2): 166-84.
[http://dx.doi.org/10.1006/dbio.1996.0125] [PMID: 8660859]
[121]
Qu M, Sun S, Liu Y, Deng X, Yang J, Yang Q. Insect group II chitinase OfChtII promotes chitin degradation during larva-pupa molting. Insect Sci 2020. In press
[http://dx.doi.org/10.1111/1744-7917.12791] [PMID: 32306549]

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