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Genes of Cuticular Proteins and Their Regulation

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Extracellular Composite Matrices in Arthropods
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Abstract

In this chapter, recent development of the analysis of cuticular protein (CP) genes and the regulation of their expression are covered. Genomic analysis and annotation of CP genes have elucidated the overall number and kind of CP gene. The nomenclature and structure of cuticle layers are described first. The factors that regulate CP gene expression are described next. Expression of CP genes is regulated mainly by ecdysone responsive transcription factors (ERTFs). Ecdysone activates target ERTFs through its receptor complex. ERTFs interaction determines the expression pattern of themselves, resulting in the induction of their target genes. Ecdysone is known also to trigger chromatin remodeling by recruiting chromatin-remodeling factors that act by chromatin loosening. Juvenile hormone affects the type of cuticle layers through BR-C and HR38 and determines the type of CPs. Recent genomic analysis has generated new findings for the cuticle research. Annotation enabled to specify the kinds and number of all cuticular proteins. Now we can discuss cuticular layers depending on the classical studies. Genomic, proteomic and transcriptomic analysis brought about new findings. Clustering CP genes have been identified in several insects. Overall expression, its regulation, binding site analysis, genomic structure of CP genes, regulation of larval, pupal adult CP layers were described.

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References

  • Ables ET, Drummond-Barbosa D (2010) The steroid hormone ecdysone functions with intrinsic chromatin remodeling factors to control female germline stem cells in Drosophila. Cell Stem Cell 7:581–592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Andersen SO (2002) Characteristic properties of proteins from pre-ecdysial cuticle of larvae and pupae of the mealworm Tenebrio moritor. Insect Biochem Mol Biol 32:1077–1087

    Article  CAS  PubMed  Google Scholar 

  • Andersen OS (2010) Insect cuticular sclerotization: a review. Insect Biochem Mol Biol 40:166–178

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Andrew AJ, Cherbas P (1994) Tissue-specific regulation by ecdysone: distinct patterns of Eip28/29 expression are controlled by different ecdysone response elements. Dev Genet 15:320–331

    Article  Google Scholar 

  • Antoniewaki C, Laval M, Lepesant J-A (1993) Structural features critical to the activity of an ecdysone receptor binding site. Insect Biochem Mol Biol 23:105–114

    Article  Google Scholar 

  • Antoniewaki C, Laval M, Dahan A, Lepesant J-A (1994) The ecdysone response enhancer of the fbp1 gene of the Drosophila melanogaster is a direct target for the EcR/USP nuclear receptor. Mol Cell Biol 14:4465–4474

    Article  Google Scholar 

  • Apple RT, Fristrom JW (1991) 20-Hydroxyecdysone is required for, and negatively regulates, transcription of Drosophila pupal cuticle protein genes. Dev Biol 146:569–582

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asano T, Taoka M, Shinkawa T, Yamauchi Y, Isobe T, Sato D (2013) Identification of a cuticle protein with unique repeated motifs in the silkworm, Bombyx mori. Insect Biochem Mol Biol 42:344–351

    Article  CAS  Google Scholar 

  • Awolola TS, Oduola OA, Strode C, Koekemoer LL, Brooke B, Ranson H (2009) Evidence of multiple pyrethroid resistance mechanisms in the malaria vector Anopheles gambiae sensu stricto from Nigeria. Trans R Soc Trop Med Hyg 103:1139–1145

    Article  CAS  PubMed  Google Scholar 

  • Badenhorst P, Xiao H, Cherbas L, Kwon SY, Voas M, Rebay I, Cherbas P, Wu C (2005) The Drosophila nucleosome remodeling factor NURF is required for ecdysteroid signaling and metamorphosis. Genes Dev 19:2540–2545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Basso LR Jr, de C Neves M, Monesi N, Paçó-Larson ML (2006) Broad-Complex, E74 and E75 early genes control DNA puff BhC4-1 expression in prepupal salivary gland. Genesis 44:505–514

    Article  CAS  PubMed  Google Scholar 

  • Bayer CA, Holley B, Fristrom JW (1996) A switch in broad-complex zinc-finger isoform expression is regulated post transcriptionally during the metamorphosis of Drosophila imaginal discs. Dev Biol 177:1–14

    Article  CAS  PubMed  Google Scholar 

  • Bernardo TJ, Dubrovskaya VA, Jannat H, Maughan B, Dubrovsky EB (2009) Hormonal regulation of the E75 gene in Drosophila: identifying functional regulatory elements through computational and biological analysis. J Mol Biol 387:794–808

    Article  CAS  PubMed  Google Scholar 

  • Blalecki M, Shilton A, Fichtenberg C, Segraves WA, Thummel CS (2002) Loss of the ecdysteroid-inducible E75A orphan nuclear receptor uncouples from metamorphosis in Drosophila. Dev Cell 3:209–220

    Article  Google Scholar 

  • Blanco E, Pignatelli M, Beltran S, Punset A, Pérez-Lluch S, Serras F, Guigó R, Corominas M (2008) Conserved chromosomal clustering of genes governed by chromatin regulators in Drosophila. Genome Biol 9:R134

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bonneton F, Chaumot A, Laudet V (2008) Annotation of Tribolium nuclear receptors reveals an increase in evolutionary rate of a network controlling the ecdysone cascade. Insect Biochem Mol Biol 38:416–429

    Article  CAS  PubMed  Google Scholar 

  • Braquart C, Bouhin H, Quennedy A, Delachambre J (1996) Up-regulation of an adult cuticular gene by 20-hydroxyecdysone in insect metamorphosing epidermis cultured in vitro. Eur J Biochem 240:336–341

    Article  CAS  PubMed  Google Scholar 

  • Broadus J, McCabe JR, Endrizzi B, Thummel CS, Woodard CT (1999) The Drosophila βFTZ-F1 orphan nuclear recptor provides competence for stage-specific responses to the steroid hormone ecdysone. Mol Cell 3:143–149

    Article  CAS  PubMed  Google Scholar 

  • Bruey-Sedano N, Alabouvette J, Lestradet M, Hong L, Girard A, Gervasio E, Quennedey B, Charles JP (2005) The Drosophila ACP65A cuticle gene: deletion scanning analysis of cis-regulatory sequences and regulation by DHR38. Genesis 43:17–27

    Article  CAS  PubMed  Google Scholar 

  • Cáceres L, Necako AS, Schwartz C, Kimber S, Roberts IJH, Krause HM (2011) Nitric oxide coordinates metabolism, growth, and development via the nuclear receptor E75. Genes Dev 25:1476–1485

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cakouros D, Daish T, Martin D, Baehrecke EH, Kumar S (2002) Ecdysone induced expression of the caspase DRONC during hormone dependent programmed cell death in Drosophila is regulated by Broad-Complex. J Cell Biol 157:985–995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cakouros D, Daish TJ, Kumar S (2004) Ecdysone receptor directly binds the promoter of the Drosophila caspase dronc, regulating its expression in specific tissues. J Cell Biol 165:631–640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carbonel A, Mazo A, Serras F, Corominas M (2013) Ash2 acts as an ecdysone receptor coactivator by stabilizing the histone methytransferase Trr. Mol Biol Cell 24:361–372

    Article  CAS  Google Scholar 

  • Ceschin DG, Walia M, Wenk SS, Duboé C, Gaudon C, Xiao Y, Fauquier L, Sankar M, Vandel L, Gronemeyer H (2011) Methylation specifies distinct estrogen-induced binding site repertories of CBP to chromatin. Genes Dev 25:1132–1146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charles JP (2010) The regulation of expression of insect cuticle protein genes. Insect Biochem Mol Biol 40:205–213

    Article  CAS  PubMed  Google Scholar 

  • Charles J-P, Chihara C, Nejad S, Riddiford LM (1997) A cluster of cuticle protein genes of Drosophila melanogaster at 65A: sequence, structure and evolution. Genetics 147:1213–1224

    CAS  PubMed  PubMed Central  Google Scholar 

  • Charles J-P, Chihara C, Nejad S, Riddiford LM (1998) Identification of proteins and developmental expression of RNAs encoded by the 65A cuticle protein gene cluster in Drosophila melanogaster. Insect Biochem Mol Biol 28:131–138

    Article  CAS  PubMed  Google Scholar 

  • Charles JP, Shinoda T, Chinzei Y (1999) Characterization and DNA-binding properties of GRF, a novel monomeric binding orphan receptor to GCNF and βFTZ-F1. Eur J Biochem 266:181–190

    Article  CAS  PubMed  Google Scholar 

  • Chauhan C, Zraly CB, Parilla M, Diaz MO, Dingwall AK (2012) Histone recognition and nuclear receptor co-activator functions of Drosophila cara mitad, a homology of the N-terminal portion of mammalian MLL2 and MLL3. Development 139:1997–2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Reece C, O’Keefe SL, Hawryluk GWL, Engstrom MM, Hodgetts RB (2002) Induction of the early-late Ddc gene during Drosophila metamorphosis by the ecdysone receptor. Mech Dev 114:95–107

    Article  CAS  PubMed  Google Scholar 

  • Cherbas L, Lee K, Cherbas P (1991) Identification of ecdysone response elements by analysis of the Drosophila Eip28/29 gene. Genes Dev 5:120–131

    Article  CAS  PubMed  Google Scholar 

  • Cho K-H, Cheon HM, Kokoza V, Raikhel AS (2006) Regulatory region of the vitellogenin receptor gene sufficient for high-level, germ line cell-specific ovarian expression in transgenic Aedes aegypti mosquitoes. Insect Biochem Mol Biol 36:273–281

    Article  CAS  PubMed  Google Scholar 

  • Cho C, Liu Y, Lehmann M (2007) Fork head controls the timing and time selectivity of steroid-induced developmental cell death. J Cell Biol 176:843–853

    Article  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Cox DL, Willis JH (1987) Analysis of the cuticular proteins of Hyalophora cecropia with two dimensional electrophoresis. Insect Biochem 17:457–468

    Article  CAS  Google Scholar 

  • Crossgrove K, Bayer CA, Fristrom JW, Guild GM (1996) The Drosophila Broad-Complex early gene directly regulates late gene transcription during the ecdysone-induced puffing cascade. Dev Biol 180:745–758

    Article  CAS  PubMed  Google Scholar 

  • Cruz J, Martin D, Bellés X (2007) Redundant ecdysis regulatory functions of three nuclear receptor HR3 isoforms in the direct-developing insect Blattella germanica. Mech Dev 124:180–189

    Article  CAS  PubMed  Google Scholar 

  • Cui HY, Lestradet M, Bruey-Sedano N, Charles JP, Riddiford LM (2009) Elucidation of the regulation of an adult cuticle gene Acp65A by the transcription factor Broad. Insect Mol Biol 18:421–429

    Article  CAS  PubMed  Google Scholar 

  • Devarakonda S, Harp JM, Kim Y, Ozyhar A, Rastinejad F (2003) Structure of the heterodimeric ecdysone receptor DNA-binding complex. EMBO J 22:5827–5840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dittmer NT, Tetreau G, Cao X, Jiang H, Wang P (2015) Annotation and expression analysis of cuticular proteins from the tobacco hornworm, Manduca sexta. Insect Biochem Mol Biol 62:100–113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon JR et al (2015) Chromatin architecture reorganization during stem cell differentiation. Nature 518:331–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dotson EM, Cornel AJ, Willis JH, Collins FH (1998) A family of pupal-specific cuticular protein genes in the mosquito Anopheles gambiae. Insect Biochem Mol Biol 28:459–472

    Article  CAS  PubMed  Google Scholar 

  • Dubrovsky EB, Dubrovskaya VA, Berger EM (2001) Selective binding of Drosophila BR-C isoforms to a distal regulatory element in the hsp23 promoter. Insect Biochem Mol Biol 31:1231–1239

    Article  CAS  PubMed  Google Scholar 

  • Dubrovsky EB, Dubrovskaya VA, Berger EM (2004) Hormonal regulation and functional roles of Drosophila E75A orphan nuclear receptor in the juvenile hormone signaling pathway. Dev Biol 658:258–270

    Article  CAS  Google Scholar 

  • Emery IF, Bedian V, Guild GM (1994) Differential expression of Broad-Complex transcription factors may forecast tissue-specific developmental fates during Drosophila metamorphosis. Development 120:3275–3287

    CAS  PubMed  Google Scholar 

  • Erezyilmaz DF, Riddiford LM, Truman JW (2006) The pupal specifier broad directs progressive morphogenesis in a direct developing insect. Proc Natl Acad Sci U S A 103:6925–6930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fittinghoff-Lohmann CM, Riddiford LM (1992) Synthesis and secretion of low molecular weight cuticular proteins during heat shock in the tobacco hornworm, Manduca sexta. J Expl Zool 262:374–382

    Article  Google Scholar 

  • Fletcher JC, Thummel CS (1995) The Drosophila E74 gene is required for the proper stage- and tissue-specific transcription of ecdysone-regulated genes at the onset of metamorphosis. Development 121:1411–1421

    CAS  PubMed  Google Scholar 

  • Fletcher JC, D’avino PP, Thummel CS (1997) A steroid-triggered switch in E74 transcription factor isoforms regulates the timing of secondary-response gene expression. Proc Natl Acad Sci U S A 94:4582–4586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gauhar Z, Sun LV, Hua S, Mason CE, Fuchs F, Li T-R, Boutros M, White KP (2009) Genomic mapping of binding regions for the ecdysone receptor protein complex. Genome Res 19:1006–1013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu S, Willis JH (2003) Distribution of cuticular protein mRNAs in silk moth integument and imaginal discs. Insect Biochem Mol Biol 33:1177–1188

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hiruma K, Riddiford LM (2001) Regulation of transcription factors MHR4 and ßFTZ-F1 by 20-hydroxyecdysone during a larval molt in the tobacco hornworm, Manduca sexta. Dev Biol 232:265–274

    Article  CAS  PubMed  Google Scholar 

  • Hiruma K, Hardie J, Riddiford LM (1991) Hormonal regulation of epidermal metamorphosis in vitro: control of expression of a larval-specific cuticle gene. Dev Biol 144:369–378

    Article  CAS  PubMed  Google Scholar 

  • Ho JWK et al (2014) Comparative analysis of metazoan chromatin organization. Nature 512:449–452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Honeybee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931–949

    Article  CAS  Google Scholar 

  • Hopkins TL, Krchma LJ, Ahmad SA, Kramer KJ (2000) Pupal cuticle proteins of Manduca sexta: characterization and profiles during sclerotization. Insect Biochem Mol Biol 30:19–27

    Article  CAS  PubMed  Google Scholar 

  • Horner MA, Chen T, Thummel CS (1995) Ecdysteroid regulation and DNA binding properties of Drosophila nuclear hormone receptor superfamily members. Dev Biol 168:490–502

    Article  CAS  PubMed  Google Scholar 

  • Horodyski FM, Riddiford LM (1989) Expression and hormonal control of a new larval cuticular multigene family at the onset of metamorphosis of the tobacco hornworm. Dev Biol 132:292–303

    Article  CAS  PubMed  Google Scholar 

  • Huet F, Ruiz C, Richards G (1995) Sequential gene activation by ecdysone in Drosophila melanogaster: the hierarchical equivalence of early and early late genes. Development 121:1195–1204

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ijiro T, Urakawa H, Yasukochi Y, Takeda M, Fujiwara Y (2004) cDNA cloning, gene structure, and expression of Broad-Complex (BR-C) genes in the silkworm, Bombyx mori. Insect Biochem Mol Biol 34:963–969

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Islam AB, Richter WF, Lopez-Bigas N, Benevolenskaya EV (2011) Selective targeting of histone methylation. Cell Cycle 10:413–424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson TA, Elbi C, Parekh BS, Hager GL, John S (2008) Chromatin remodeling complexes interact dynamically with a glucocorticoid receptor-regulated promoter. Mol Biol Cell 19:3308–3322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnston DM, Sedkov Y, Petruk S, Riley KM, Fujuoka M, Jaynes JB (2011) Ecdysone- and NO-mediated gene regulation by competing EcR/Usp and E75A nuclear receptors during Drosophila development. Mol Cell 44:51–61

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karim FD, Thummel CS (1991) Ecdysone coordinates the timing and amounts of E74A and E74B transcription in Drosophila. Genes Dev 5:1067–1079

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kawasaki H, Kiguchi K, Agui N, Iwashita Y (1986) Ecdysteroid titer and wing development during the pupal-adult transformation of Bombyx mori. Zool Sci 30:301–304

    Google Scholar 

  • Kawasaki H, Hirose S, Ueda H (2002) ßFTZ-F1 dependent and independent activation of Edg78E, a pupal cuticle gene, during the early metamorphic period in Drosophila melanogaster. Develop Growth Differ 44:419–425

    Article  CAS  Google Scholar 

  • Kawasaki H, Ote M, Okano H, Shimada T, Quan G-X, Mita K (2004) Change in the expressed gene patterns of the wing disc during the metamorphosis of Bombyx mori. Gene 343:133–142

    Article  CAS  PubMed  Google Scholar 

  • Kawazu M, Saso K, Tong KI, McQuire T, Goto K, Son DO, Wakeham A, Miyagishi M, Mak TW, Okada H (2011) Histone demethylase JMJD2B functions as a o-factor of estrogen receptor in breast cancer proliferation and mammary gland development. PLoS ONE 6:e17830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kayashima Y, Hirose S, Ueda H (2005) Anterior epidermis-specific expression of the cuticle gene EDG84A is controlled by many cis-regulatory elements in Drosophila melanogaster. Dev Genes Evol 215:545–552

    Article  CAS  PubMed  Google Scholar 

  • Kim SR, Yoon HJ, Lee KS, Kim I, Je YH, Sohn HD, Jin BR (2003) Molecular cloning of three cDNAs encoding putative larval cuticle protein expressed differentially after larval ecdysis from the mulberry longicorn beetle, Apriona germari. Comp Biochem Physiol B Biochem Mol Biol 136:803–811

    Article  PubMed  CAS  Google Scholar 

  • Kimura S et al (2008) Drosophila arginine methyltransferase 1 (DART1) is an ecdysone receptor co-repressor. Biochem Biophys Res Commun 371:889–893

    Article  CAS  PubMed  Google Scholar 

  • King-Jones K, Charles J-P, Lam G, Thummel CS (2005) The ecdysone-induced DHR4 orphan nuclear receptor coordinates growth and maturation in Drosophila. Cell 121:773–784

    Article  CAS  PubMed  Google Scholar 

  • Kirilly D, Wong JJL, Lim EKH, Wang Y, Zhang H, Wang C, Liao Q, Wang H, Liou Y-C, Wang H, Yu F (2011) Intrinsic epigenetic factors cooperate with the steroid hormone ecdysone to govern dendrite pruning in Drosophila. Cell 72:86–100

    CAS  Google Scholar 

  • Koyama T, Syropyatova MO, Riddiford LM (2008) Insulin/IGF signaling regulates the change in commitment in imaginal discs and primordia by overriding the effect of juvenile hormone. Dev Biol 324:258–265

    Article  CAS  PubMed  Google Scholar 

  • Kozlova T, Thummel CS (2003) Essential roles for ecdysone signaling during Drosophila mid-embryonic development. Science 301:1911–1914

    Article  CAS  PubMed  Google Scholar 

  • Kozlova T, Lam G, Thummel CS (2009) Drosophila DHR38 nuclear receptor is required for adult cuticle integrity at eclosion. Dev Dyn 238:701–707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lam TG, Thummel CS (2000) Inducible expression of double-stranded RNA directs specific genetic interference in Drosophila. Curr Biol 10:957–963

    Article  CAS  PubMed  Google Scholar 

  • Lam TG, Jiang C, Thummel CS (1997) Coordination of larval and prepupal gene expression by DHR3 orphan receptor during Drosophila metamorphosis. Development 124:1757–1769

    CAS  PubMed  Google Scholar 

  • Lam TG, Bonnie LH, Bender M, Thummel CS (1999) DHR3 is required for the prepupal-pupal transition and differentiation of adult structures during Drosophila metamorphosis. Dev Biol 212:204–216

    Article  CAS  PubMed  Google Scholar 

  • Laval M, Pourrain F, Deutsch J, Jean-Antoine L (1993) In vivo functional characterization o an ecdysone response enhancer in the proximal upstream region of the fbp1 gene of D. melanogaster. Mech Dev 44:123–138

    Article  CAS  PubMed  Google Scholar 

  • Lee CY, Cooksey BA, Baehrecke EH (2002a) Steroid regulation of midgut cell death during Drosophila development. Dev Biol 250:101–111

    Article  CAS  PubMed  Google Scholar 

  • Lee CY, Simon CR, Woodard CT, Baehrecke EH (2002b) Genetic mechanism for the stage-specific regulation of steroid triggered programmed cell death in Drosophila. Dev Biol 252:138–148

    Article  CAS  PubMed  Google Scholar 

  • Lemoine A, Mathelin J, Braquart-Varnier C, Everaerts C, Delachambre J (2004) A functional analysis of ACP-20, adult specific cuticlar protein gene from the beetle Tenebrio: role of an intronic sequence in transcriptional activation during the late metamorphic period. Insect Mol Biol 13:481–493

    Article  CAS  PubMed  Google Scholar 

  • Lestradet M, Gervasio E, Fraichard S, Dupas S, Alabouvette J, Lemoine A, Charles JP (2009) The cis-regulatory sequences required for expression of the Drosophila melanogaster adult cuticle gene ACP65A. Insect Mol Biol 18:431–441

    Article  CAS  PubMed  Google Scholar 

  • Liang J, Zhang L, Xiang Z, He N (2010) Expession profile of cuticular genes of silkworm, Bombyx mori. BMC Genomics 11:173

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Locke M (1961) Pore canals and related structures in insect. J Biophys Biochem Cytol 10:589–618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mané-Padrós D, Cruz J, Vilaplana L, Pascual N, Bullés X, Martin D (2008) The nuclear hormone receptor BgE75 links molting and developmental progression in the direct-developing insect Blattela germanica. Dev Biol 315:147–160

    Article  PubMed  CAS  Google Scholar 

  • Martin D, Wang S-F, Raikhel AS (2001) The vitellogenin gene of the mosquito Aedes aegypti is a direct target of ecdysteroid receptor. Insect Biochem Mol Biol 31:827–837

    Article  Google Scholar 

  • Missios S, Davidson HC, Linder D, Moltimer L, Okobi AO, Doctor JS (2000) Characterization of cuticular proteins in the red flour beetle Tribolium castaneum. Insect Biochem Mol Biol 30:47–56

    Article  CAS  PubMed  Google Scholar 

  • Mita K, Morimyo M, Okano K, Koike Y, Nohata J, Kawasaki H, Kadono-Okuda K, Yamamoto K, Suzuki MG, Shimada T, Goldsmith MR, Maeda S (2003) The construction of an EST database for Bombyx mori and its application. Proc Natl Acad Sci U S A 100:14121–14126

    Article  PubMed  PubMed Central  Google Scholar 

  • Mouillet JF, Bousquet F, Sedano N, Alabouvette J, Nicolaï M, Zelus D, Laudet V, Delachambre J (1999) Cloning and characterization of new orphan nuclear receptors and their developmental profiles during Tenebrio metamorphosis. Eur J Biochem 265:972–981

    Article  CAS  PubMed  Google Scholar 

  • Mugat B, Brodu V, Kejzlarova-lepesant J, Antoniewski C, Bayer CA, Fristrom JW, Lepesant JA (2000) Dynamic expression of broad-complex isoforms mediates temporal control of ecdysteroid target gene at the onset of Drosophila metamorphosis. Dev Biol 227:104–117

    Article  CAS  PubMed  Google Scholar 

  • Mun S, Noh MY, Dittmer NT, Muthukrishnan S, Kramer KJ, Kanost MR (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

    Article  PubMed  PubMed Central  Google Scholar 

  • Murata T, Kagayama Y, Hirose S (1996) Regulation of the EDG84A gene by FTZ-F1 during metamorphosis in Drosophila malanogaster. Mol Cell Biol 16:6509–6515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nègre N et al (2011) Cis-regulatory map of the Drosophila genome. Nature 471:527–531

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nieva C, Spindler-Barth M, Azoitei A, Spindler KD (2007) Influence of hormone on intracellular localization of the Drosophila melanogaster ecdysteroid receptor. Cell Signal 19:2582–2587

    Article  CAS  PubMed  Google Scholar 

  • Niimi S, Sakurai S (1997) Development changes in juvenile hormone and juvenile hormone acid titers in the hemolymph and in vitro juvenile hormone synthesis by corpora allata of the silkworm, Bombyx mori. J Insect Physiol 43:875–884

    Article  CAS  PubMed  Google Scholar 

  • Nishita Y (2014) Ecdysone response elements in the distal promoter of the Broad Complex gene, BmBR-C. Insect Mol Biol 23:341–356

    CAS  PubMed  Google Scholar 

  • Nita M, Wang HB, Zhong YS, Mita K, Iwanaga M, Kawasaki H (2009) Analysis of ecdysone-pulse responsive region of BMWCP2 in wing disc of Bombyx mori. Comp Biochem Physiol B 153:101–108

    Article  PubMed  CAS  Google Scholar 

  • Noh MY, Kramer KJ, Muthukrishnan S, kanost MR, Beeman R, 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 53:22–29

    Article  CAS  PubMed  Google Scholar 

  • 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:e1004963. doi:10.1371/journal.pgen.1004963

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Noji T, Ote M, Takeda M, Mita K, Shimada T, Kawasaki H (2003) Isolation and comparison of different ecdysone-responsive cuticle protein genes in wing discs of Bombyx mori. Insect Biochem Mol Biol 33:671–679

    Article  CAS  PubMed  Google Scholar 

  • Okamoto S, Futahashi R, Kojima T, Mita K, Fujiwara H (2008) Catalogue of epidermal genes expressed in the epidermis during larval molt of the silkworm Bombyx mori. BMC Genomics 9:396

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Palli SR, Hiruma K, Riddiford LM (1992) An ecdysteroid inducible Manduca gene similar to the Drosophila DHR3 gene, a member of the steroid hormone receptor superfamily. Dev Biol 150:306–318

    Article  CAS  PubMed  Google Scholar 

  • Parthasarathy R, Tan A, Bai H, Palli SR (2008) Transcription factor broad suppresses precocious development of adult structures during larval-pupal metamorphosis in the red flour beetle, Tribolium castaneum. Mech Dev 125:299–313

    Article  CAS  PubMed  Google Scholar 

  • Pierceall WE, Li C, Biran A, Miura K, Raikhel AS, Segraves WA (1999) E75 expression in A. Aegypti mosquito ovary and fat body suggests reiterative use of ecdysone-regulated hierarchies in development and reproduction. Mol Cell Endocrinol 150:73–89

    Article  CAS  PubMed  Google Scholar 

  • Qiao L, Xiong G, Wang R-x, He S-z, Chen J, Tong X-l, Hu H, Li C-l, Gai T-t, Xin Y-q, Liu X-f, Chen B, Xiang Z-h, Lu C, Dai F-y (2014) Mutation of a cuticular protein, BmorCPR2, alters larval body shape and adaptability in silkworm, Bombyx mori. Genetics 196:1103–1115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raud AF, Lam G, Thummel CS (2010) The Drosophila nuclear receptors DHR3 and bFTZ-F1 control overlapping developmental responses in late embryos. Development 137:123–131

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Reinking J, Lam MMS, Pardee K, Sampson HM, Liu S, Yang P, Williams S, White W, Lajoie G, Edwards A, Krause HM (2005) The Drosophila nuclear receptor E75 contains heme and is gas responsive. Cell 122:195–207

    Article  CAS  PubMed  Google Scholar 

  • Riddiford LM, Hiruma K, Zhou X, Nelson CA (2003) Insights into the molecular basis of the hormonal control of molting and metamorphosis from Manduca sexta and Drosophila melanogaster. Insect Biochem Mol Biol 33:1327–1338

    Article  CAS  PubMed  Google Scholar 

  • Riddiford LM, Truman JW, Mirth CK, Shen YC (2010) A role for juvenile hormone in the prepupal development of Dosophila melanogaster. Development 137:1117–1126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rudolph K, Morganelli C, Berger EM (1991) Regulatory elements near the Drosophila hsp 22 gene required for ecdysterone and heat shock induction. Dev Genet 12:212–218

    Article  CAS  PubMed  Google Scholar 

  • Sallivan AA, Thummel CS (2003) Temporal profiles of nuclear receptor gene expression reveal co-ordinate transcriptional responses during Drosophila development. Mol Endocrinol 17:2125–2137

    Article  CAS  Google Scholar 

  • Sandstrom DJ, Restifo LL (1999) Epidermal tendon cells require broad complex function for correct attachment of the indirect flight muscles in Drosophila melanogaster. J Cell Sci 112:4051–4065

    CAS  PubMed  Google Scholar 

  • Sawatsubashi S et al (2010) A histone chaperone, DEK transcriptionally coactivates a nuclear receptor. Genes Dev 24:159–170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schaefer J, Kramer KJ, Garbow JR, Jacob GS, Stejskal EO, Hopkins TL, Speirs RD (1987) Aromatic cross-links in insect cuticle: detection by solid-state 13C and 15N NMR. Science 235:1200–1204

    Article  CAS  PubMed  Google Scholar 

  • Sedkov Y, Cho E, Petruk S, Cherbas L, Smith ST, Jones RS, Cherbas P, Canaani E, Jaynes JB, Mazo A (2003) Methylation at lysine 4 of histone H3 in ecdysone-dependent development of Drosophila. Nature 426:78–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sekimoto T, Iwami M, Sakurai S (2006) Coordinate responses of transcription factors to ecdysone during programmed cell death in the anterior silk gland of the silkworm, Bombyx mori. Insect Mol Biol 15:281–292

    Article  CAS  PubMed  Google Scholar 

  • Sekimoto T, Iwami M, Sakurai S (2007) 20-hydroxyecdysone regulation of two isoforms of the Ets transcription factor E74 gene in programmed cell death in the silkworm anterior silk gland. Insect Mol Biol 16:581–590

    Article  CAS  PubMed  Google Scholar 

  • Shahin R, Iwanaga M, Kawasaki H (2016) Cuticular protein and transcription factor genes expressed during prepupal-pupal transition and by ecdysone pulse treatment in wing discs of Bombyx mori. Insect Mol Biol 25:138–152

    Article  CAS  PubMed  Google Scholar 

  • Shi L et al (2011) Histone demethylase JMJD2B coordinates H3K4/H3K9 methylation and promotes hormonally responsive breast carcinogenesis. Proc Natl Acad Sci U S A 108:7541–7546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snyder M, Hunkapiller M, Yuen D, Silvert D, Fristrom J, Davidson N (1982) Cuticle protein genes of Drosophila: structure, organization, and evolution of four clustered genes. Cell 29:1027–1040

    Article  CAS  PubMed  Google Scholar 

  • Spokony RF, Restifo LL (2007) Anciently duplicated Broad Complex exons have distinct temporal functions during tissue morphogenesis. Dev Genes Evol 217:499–513

    Article  CAS  PubMed  Google Scholar 

  • Stilwell GE, Nelson CA, Weler J, Cui H, Hiruma K, Truman JW, Riddiford LM (2003) E74 exhibits stage-specific hormonal regulation in the epidermis of the tobacco hornworm, Manduca sexta. Dev Biol 258:76–90

    Article  CAS  PubMed  Google Scholar 

  • Sun GC, Hirose S, Ueda H (1994) Intermittent expression of BmFTZ-F1, a member of the nuclear hormone receptor superfamily during development of the silkworm Bombyx mori. Dev Biol 162:426–437

    Article  CAS  PubMed  Google Scholar 

  • Suzuki Y, Matsuoka T, Iimura Y, Fujiwara H (2002) Ecdysteroid dependent expression of a novel cuticle protein gene BMCPG1 in the silkworm, Bombyx mori. Insect Biochem Mol Biol 32:599–607

    Article  CAS  PubMed  Google Scholar 

  • Suzuki Y, Truman JW, Riddiford LM (2008) The role of Broad in the development of Tribolium castaneum: implications for the evolution of the holometabolous insect pupa. Development 135:569–577

    Article  CAS  PubMed  Google Scholar 

  • Swevers L, Ito K, Iatrou K (2002) The BmE75 nuclear receptors function as dominant repressors of the nuclear receptor BmHR3A. J Biol Chem 277:41637–41644

    Article  CAS  PubMed  Google Scholar 

  • Takeda M, Mita K, Quan GX, Shimada T, Okano K, Kanke E, Kawasaki H (2001) Mass isolation of cuticle protein cDNAs from wing discs of Bombyx mori and their characterization. Insect Biochem Mol Biol 31:1019–1028

    Article  CAS  PubMed  Google Scholar 

  • Tang L, Liang J, Zhan Z, Xiang Z, He N (2010) Identification of the chitin-binding proteins rom the larval proteins of silkworm, Bombyx mori. Insect Biochem Mol Biol 40:228–234

    Article  CAS  PubMed  Google Scholar 

  • Taniai K, Hirayama C, Mita K, Asaoka K (2014) Starvation-responsive glycine-rich protein gene in the silkworm Bombyx mori. J Comp Physiol B 184:827–834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • The ENCODE Project Consortium (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489:57–74

    Article  PubMed Central  CAS  Google Scholar 

  • The International Silkworm Genome Consortium (2008) The genome of a lepidopteran model insect, the silkworm Bombyx mori. Insect Biochem Mol Biol 38:1036–1045

    Article  CAS  Google Scholar 

  • Thummel CS, Burtis KC, Hogness DS (1990) Spatial and temporal patterns of E74 transcription during Drosophila development. Cell 61:101–111

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Togawa T, Dunn WA, Emmons AC, Nagao J, Willis JH (2008) Developmental expression patterns of cuticular protein genes with the R&R Consensus from Anopheles gambiae. Insect Biochem Mol Biol 38:508–519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsurumi A, Dutta O, Shang R, Yan SJ, Li WX (2013) Drosophila Kdm4 demethylases in histone H3 lysine 9 demethylation and ecdysteroid signaling. Sci Rep 3:2894

    Article  PubMed  PubMed Central  Google Scholar 

  • Tzolovsky G, Deng WM, Schlitt T, Bownes M (1999) The function of the broad-complex during Drosophila melanogaster oogenesis. Genetics 153:1371–1383

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ueda H, Hirose S (1990) Identification and purification of a Bombyx mori homologue of FTZ-F1. Nucleic Acids Res 18:7229–7234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uhlirova M, Foy BD, Beaty BJ, Olson KE, Riddiford LM, Jindra M (2003) Use of Sindbis virus-mediated RNA interference to demonstrate a conserved role of Broad-Complex in insect metamorphosis. Proc Natl Acad Sci U S A 100:15607–15612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Urness LD, Thummel CS (1990) Molecular interaction within the ecdysone regulatory hierarchy: DNA binding properties of the Drosophila ecdysone-inducible E74A protein. Cell 63:47–61

    Article  CAS  PubMed  Google Scholar 

  • Urness DL, Thummel SC (1995) Molecular analysis of a steroid-induced regulatory hierarchy: the Drosophila E74A protein directly regulates L71-6 transcription. EMBO J 14:6239–6246

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vicent GP, Nacht AS, Zaurin R, Font-Mateu J, Soronellas D, Le Dily F, Reyes D, Beato M (2013) Unliganded progesterone receptor-mediated targeting of an RNA-containing repressing complex silences a subset of hormone-inducible genes. Genes Dev 27:1179–1197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • von Kalm L, Crossgrove K, Von Seggern D, Guild GM, Beckendorf SK (1994) The Broad-Complex directly controls a tissue-specific response to the steroid hormone ecdysone at the onset of Drosophila metamorphosis. EMBO J 13:3505–3516

    Google Scholar 

  • Vontas J, David JP, Nikou D, Hemingway J, Christophides GK, Louis C, Ranson H (2007) Transcriptional analysis of insecticide resistance in Anopheles stephensi using cross-species microarray hybridization. Insect Mol Biol 16:315–324

    Google Scholar 

  • Wang H-B, Iwanaga M, Kawasaki H (2009a) Activation of BMWCP10 promoter and regulation by BR-C Z2 in wing disc of Bombyx mori. Insect Biochem Mol Biol 39:615–623

    Article  PubMed  CAS  Google Scholar 

  • Wang H-B, Nita M, Iwanaga M, Kawasaki H (2009b) βFTZ-F1 and Broad-Complex positively regulate the transcription of the wing cuticle protein gene, BMWCP5, in wing discs of Bombyx mori. Insect Biochem Mol Biol 39:624–633

    Article  CAS  PubMed  Google Scholar 

  • Wang H-B, Moriyama M, Iwanaga M, Kawasaki H (2010) Ecdysone directly and indirectly regulates a cuticle protein gene, BMWCP10, in the wing disc of Bombyx mori. Insect Biochem Mol Biol 40:453–459

    Article  CAS  PubMed  Google Scholar 

  • Wang H-B, Iwanaga M, Kawasaki H (2014) Stage-specific activation of the E74B promoter by low ecdysone concentrations in the wing disc of Bombyx mori. Gene 537:322–327

    Article  CAS  PubMed  Google Scholar 

  • Weller J, Sun G-C, Zhou B, Lan Q, Hiruma K, Riddiford LM (2001) Isolation and developmental expression of two nuclear receptors, MHR4 and βFTZ-F1, in the tobacco hornworm, Manduca sexta. Insect Biochem Mol Biol 31:827–837

    Article  CAS  PubMed  Google Scholar 

  • White KP, Hurban P, Watanabe T, Hogness DS (1997) Coordination of Drosophila metamorphosis by two ecdysone-induced nuclear receptors. Science 276:114–117

    Article  CAS  PubMed  Google Scholar 

  • Wigglesworth VB (1972) The principles of insect physiology, 7th edn. Chapman and Hall, London

    Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woodard CT, Baehrecke EH, Thummel CS (1994) A molecular mechanism for the stage specificity of the Drosophila prepupal genetic response to ecdysone. Cell 79:607–615

    Article  CAS  PubMed  Google Scholar 

  • Yamada M, Murata T, Hirose S, Lavorgna G, Suzuki E, Ueda H (2000) Temporally restricted expression of transcription factor betaFTZ-F1: significance for embryogenesis, molting and metamorphosis in Drosophila melanogaster. Development 127:5083–5092

    CAS  PubMed  Google Scholar 

  • Zhang J, Goyer C, Pelletier Y (2008) Environmental stresses induce the expression of putative glycine-rich insect cuticular protein genes in adult Leptinotarsa decemlineata (Say). Insect Mol Biol 17:209–216

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zhou B, Riddiford LM (2001) Hormonal regulation and patterning of the Broad-Complex in the epidermis and wing discs of the tobacco hornworm, Manduca sexta. Dev Biol 231:125–137

    Article  CAS  PubMed  Google Scholar 

  • Zhou X, Riddiford LM (2002) Broad specifies pupal development and mediates the “status quo” action of juvenile hormone on the pupal-adult transformation in Drosophila and Manduca. Development 129:2259–2269

    CAS  PubMed  Google Scholar 

  • Zhou B, Hiruma K, Shinoda T, Riddiford LM (1998) Juvenile hormone prevents ecdysteroid-induced expression of Broad Complex RNAs in the epidermis of the tobacco hornworm, Manduca sexta. Dev Biol 203:233–244

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Chen L, Raikhel AS (2003) Posttranscriptional control of the competence factor bFTZ-F1 by juvenile hormone in the mosquito Aedes aegypti. Proc Natl Acad Sci U S A 100:13338–13343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu J, Chen L, Raikhel AS (2007) Distinct roles of broad isoforms in regulation of the 20-hydroxyecdysone effector gene, Vitellogenin, in the mosquito Aedes aegypti. Mol Cell Endocrinol 267:97–106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zraly CB (2006) Hormone-response genes are direct in vivo regulating targets of Brahma (SWI/SNF) complex function. J Biol Chem 281:35305–35315

    Article  CAS  PubMed  Google Scholar 

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Kawasaki, H. (2016). Genes of Cuticular Proteins and Their Regulation. In: Cohen, E., Moussian, B. (eds) Extracellular Composite Matrices in Arthropods. Springer, Cham. https://doi.org/10.1007/978-3-319-40740-1_1

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