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Annual Review of Entomology

Volume 60, 2015

Chorion Genes: A Landscape of Their Evolution, Structure, and Regulation

Abstract

Differential regulation at the level of transcription provides a means for controlling gene expression in eukaryotes, especially during development. Insect model systems have been extensively used to decipher the molecular basis of such regulatory cascades, and one of the oldest such model systems is the regulation of chorion gene expression during ovarian follicle maturation. Recent experimental and technological advances have shed new light onto the system, allowing us to revisit it. Thus, in this review we try to summarize almost 40 years' worth of studies on chorion gene regulation while—by comparing and models—attempting to present a comprehensive, unified model of the various regulatory aspects of choriogenesis that takes into account the evolutionary conservation and divergence of the underlying mechanisms.

Keyword(s): bidirectional promoters, choriogenesis, cis-element architecture, differential gene expression, transcription factors, vitellogenesis
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2015-01-07
2024-05-03
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Literature Cited

  1. Bai J, Uehara Y, Montell DJ. 1.  2000. Regulation of invasive cell behavior by Taiman, a Drosophila protein related to AIB1, a steroid receptor coactivator amplified in breast cancer. Cell 103:1047–58 [Google Scholar]
  2. Bellés X. 2.  2010. Beyond Drosophila: RNAi in vivo and functional genomics in insects. Annu. Rev. Entomol. 55:111–28 [Google Scholar]
  3. Bernardi F, Romani P, Tzertzinis G, Gargiulo G, Cavaliere V. 3.  2009. EcR-B1 and Usp nuclear hormone receptors regulate expression of the VM32E eggshell gene during Drosophila oogenesis. Dev. Biol. 328:541–51 [Google Scholar]
  4. Broadus J, McCabe JR, Endrizzi B, Thummel CS, Woodard CT. 4.  1999. The Drosophila βFTZ-F1 orphan nuclear receptor provides competence for stage-specific responses to the steroid hormone ecdysone. Mol. Cell 3:143–49 [Google Scholar]
  5. Buszczak M, Freeman MR, Carlson JR, Bender M, Cooley L, Segraves WA. 5.  1999. Ecdysone response genes govern egg chamber development during mid-oogenesis in Drosophila. Development 126:4581–89 [Google Scholar]
  6. Carter J-M, Baker SC, Pink R, Carter DRF, Collins A. 6.  et al. 2013. Unscrambling butterfly oogenesis. BMC Genomics 14:283 [Google Scholar]
  7. Cavaliere V, Bernardi F, Romani P, Duchi S, Gargulio G. 7.  2008. Building up the Drosophila eggshell: First of all the eggshell genes must be transcribed. Dev. Dyn. 237:2061–72 [Google Scholar]
  8. Chen A, Xia D, Qiu Z, Gao P, Tang S. 8.  et al. 2013. Expression of a vitelline membrane protein, BmVMP23, is repressed by bmo-miR-1a-3p in silkworm, Bombyx mori. FEBS Lett. 587:970–75 [Google Scholar]
  9. Cherbas L, Hu X, Zhimulev I, Belyaeva E, Cherbas P. 9.  2003. EcR isoforms in Drosophila: testing tissue-specific requirements by targeted blockade and rescue. Development 130:271–84 [Google Scholar]
  10. Claycomb JM, Benasutti M, Bosco G, Fenger DD, Orr-Weaver TL. 10.  2004. Gene amplification as a developmental strategy: isolation of two developmental amplicons in Drosophila. Dev. Cell 6:145–55 [Google Scholar]
  11. Dai H, Jiang R, Wang J, Xu G, Cao M. 11.  et al. 2007. Development of a heat shock inducible and inheritable RNAi system in silkworm. Biomol. Eng. 24:625–30 [Google Scholar]
  12. Daimon T, Kiuchi T, Takasu Y. 12.  2014. Recent progress in genome engineering techniques in the silkworm, Bombyx mori. Dev. Growth Differ. 56:14–25 [Google Scholar]
  13. Dansereau DA, Lasko P, McKearin D. 13.  2005. Oogenesis. Comprehensive Molecular Insect Science Vol. 1: Reproduction and Development, ed. LI Gilbert, K Iatrou, SS Gill 39–85 New York: Elsevier/Pergamon [Google Scholar]
  14. Deng H, Zhang J, Li Y, Zheng S, Liu L. 14.  et al. 2012. Homeodomain POU and Abd-A proteins regulate the transcription of pupal genes during metamorphosis of the silkworm, Bombyx mori. Proc. Natl. Acad. Sci. USA 109:12598–603 [Google Scholar]
  15. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y. 15.  et al. 2007. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448:151–56 [Google Scholar]
  16. Drevet JR, Skeiky YAW, Iatrou K. 16.  1994. GATA-type zinc finger motif-containing sequences and chorion gene transcription factors of the silkworm Bombyx mori. J. Biol. Chem. 269:10660–67 [Google Scholar]
  17. Drevet JR, Swevers L, Iatrou K. 17.  1995. Developmental regulation of a silkworm gene encoding “GATA”-type transcription factors by alternative splicing. J. Mol. Biol. 246:43–53 [Google Scholar]
  18. Eickbush TH, Kafatos FC. 18.  1982. A walk in the chorion locus of Bombyx mori. Cell 29:633–43 [Google Scholar]
  19. Fakhouri M, Elalayli M, Sherling D, Hall JD, Miller E. 19.  et al. 2006. Minor proteins and enzymes of the Drosophila eggshell matrix. Dev. Biol. 293:127–41 [Google Scholar]
  20. Freeman MR, Dobritsa A, Gaines P, Segraves WA, Carlson JR. 20.  1999. The dare gene: steroid hormone production, olfactory behaviour, and neural degeneration in Drosophila. Development 126:4591–602 [Google Scholar]
  21. Gao P, Chen AL, Zhao QL, Shen XJ, Qiu ZY. 21.  et al. 2013. Differentially expressed genes in the ovary of the sixth day of pupal “Ming” lethal egg mutant of silkworm, Bombyx mori. Gene 527:161–66 [Google Scholar]
  22. Gates J. 22.  2012. Drosophila egg chamber elongation: insights into how tissues and organs are shaped. Fly 6:213–27 [Google Scholar]
  23. Gautreau D, Zetlan SR, Mazur GD, Goldsmith MR. 23.  1993. A subtle defect underlies altered lamellar orientation in the Gr16 chorion mutant of Bombyx mori. Dev. Biol. 157:60–72 [Google Scholar]
  24. Goldsmith MR. 24.  1989. Organization and developmental timing of the Bombyx mori chorion gene clusters in strain C108. Dev. Genet. 10:16–23 [Google Scholar]
  25. Griffin-Shea R, Thireos G, Kafatos FC. 25.  1982. Organization of a cluster of four chorion genes in Drosophila and its relationship to developmental expression and amplification. Dev. Biol. 91:325–36 [Google Scholar]
  26. Hackney JF, Pucci C, Naes E, Dobens L. 26.  2007. Ras signaling modulates activity of the ecdysone receptor EcR during cell migration in the Drosophila ovary. Dev. Dyn. 236:1213–26 [Google Scholar]
  27. Hamodrakas SJ, Kamitsos EI, Papanikolaou A. 27.  1984. Laser-Raman spectroscopic studies of the eggshell (chorion) of Bombyx mori. Int. J. Biol. Macromol. 6:333–36 [Google Scholar]
  28. Herraiz A, Bellés X, Piulachs M-D. 28.  2014. Chorion formation in panoistic ovaries requires Windei and trimethylation of histone 3 lysine 9. Exp. Cell Res. 220:46–53 [Google Scholar]
  29. Hibner BL, Burke WD, Eickbush TH. 29.  1991. Sequence identity in an early chorion multigene family is the result of localized gene conversion. Genetics 128:595–606 [Google Scholar]
  30. Hibner BL, Burke WD, Lecanidou R, Rodakis GC, Eickbush TH. 30.  1988. Organization and expression of three genes from the silkmoth early chorion locus. Dev. Biol. 125:423–31 [Google Scholar]
  31. Hock R, Furusawa T, Ueda T, Bustin M. 31.  2007. HMG chromosomal proteins in development and disease. Trends Cell Biol. 17:72–79 [Google Scholar]
  32. Iatrou K, Tsitilou SG, Goldsmith MR, Kafatos FC. 32.  1980. Molecular analysis of the GrB mutation in Bombyx mori through the use of a chorion cDNA library. Cell 20:659–69 [Google Scholar]
  33. Iatrou K, Tsitilou SG, Kafatos FC. 33.  1984. DNA sequence transfer between two high-cysteine chorion gene families in the silkmoth Bombyx mori. Proc. Natl. Acad. Sci. USA 81:4452–54 [Google Scholar]
  34. Irles P, Bellés X, Piulachs MD. 34.  2009. Brownie, a gene involved in building complex respiratory devices in insect eggshells. PLOS ONE 4:e8353 [Google Scholar]
  35. Irles P, Piulachs M-D. 35.  2011. Citrus, a key insect eggshell protein. Insect Biochem. Mol. Biol. 41:101–8 [Google Scholar]
  36. Jagadeeswaran G, Zheng Y, Sumathipala N, Jiang H, Arrese EL. 36.  et al. 2010. Deep sequencing of small RNA libraries reveals dynamic regulation of conserved and novel microRNAs and microRNA-stars during silkworm development. BMC Genomics 11:52 [Google Scholar]
  37. Kafatos FC, Spoerel N, Mitsialis SA, Nguyen HT, Romano C. 37.  et al. 1987. Developmental control and evolution in the chorion gene families of insects. Adv. Genet. 24:223–42 [Google Scholar]
  38. Kafatos FC, Tzertzinis G, Spoerel NA, Nguyen HT. 38.  1995. Chorion genes: an overview of their structure, function and transcriptional regulation. Molecular Model Systems in the Lepidoptera MR Goldsmith, AS Wilkins 181–215 Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  39. Kanginakudru S, Royer C, Edupalli SV, Jalabert A, Mauchamp B. 39.  et al. 2007. Targeting ie-1 gene by RNAi induces baculoviral resistance in lepidopteran cell lines and in transgenic silkworms. Insect Mol. Biol. 16:635–44 [Google Scholar]
  40. Kendirgi F, Swevers L, Iatrou K. 40.  2002. An ovarian follicular epithelium protein of the silkworm (Bombyx mori) that associates with the vitelline membrane and contributes to the structural integrity of the follicle. FEBS Lett. 524:59–68 [Google Scholar]
  41. Kravariti L, Lecanidou R, Rodakis GC. 41.  1995. Sequence analysis of a small early chorion gene subfamily interspersed within the late gene locus in Bombyx mori. J. Mol. Evol. 41:24–33 [Google Scholar]
  42. Kravariti L, Thomas J, Sourmeli S, Rodakis GC, Mauchamp B. 42.  et al. 2001. The biolistic method as a tool for testing the differential activity of putative silkmoth chorion gene promoters. Insect Biochem. Mol. Biol. 31:473–79 [Google Scholar]
  43. Lecanidou R, Papantonis A. 43.  2010. Modeling bidirectional transcription using silkmoth chorion gene promoters. Organogenesis 6:54–58 [Google Scholar]
  44. Lecanidou R, Papantonis A. 44.  2010. Silkmoth chorion gene regulation revisited: promoter architecture as a key player. Insect Mol. Biol. 19:141–51 [Google Scholar]
  45. Lecanidou R, Rodakis GC. 45.  1992. Three copies of the early gene 6F6 are interspersed in and around the late chorion gene cluster of Bombyx mori. J. Mol. Evol. 34:304–14 [Google Scholar]
  46. Lecanidou R, Rodakis GC, Eickbush TH, Kafatos FC. 46.  1986. Evolution of the silk moth chorion gene superfamily: gene families CA and CB. Proc. Natl. Acad. Sci. USA 83:6514–18 [Google Scholar]
  47. Leclerc RF, Regier JC. 47.  1994. Evolution of chorion gene families in Lepidoptera: characterization of 15 cDNAs from the gypsy moth. J. Mol. Evol. 39:244–54 [Google Scholar]
  48. Levine J, Spradling A. 48.  1985. DNA sequence of a 3.8 kilobase pair region controlling Drosophila chorion gene amplification. Chromosoma 92:136–42 [Google Scholar]
  49. Li Y, Wang G, Tian J, Liu H, Yang H. 49.  et al. 2012. Transcriptome analysis of the silkworm (Bombyx mori) by high-throughput RNA sequencing. PLOS ONE 7:e43713 [Google Scholar]
  50. Lin JM, Collins PJ, Trinklein ND, Fu Y, Xi H. 50.  et al. 2007. Transcription factor binding and modified histones in human bidirectional promoters. Genome Res. 17:818–27 [Google Scholar]
  51. Liu S, Xia Q, Zhao P, Cheng T, Hong K, Xiang Z. 51.  2007. Characterization and expression patterns of let-7 microRNA in the silkworm (Bombyx mori). BMC Dev. Biol. 7:88 [Google Scholar]
  52. Machado E, Swevers L, Sdralia N, Medeiros MN, Mello FG, Iatrou K. 52.  2007. Prostaglandin signaling and ovarian follicle development in the silkmoth, Bombyx mori. Insect Biochem. Mol. Biol. 37:876–85 [Google Scholar]
  53. Margaritis LH. 53.  1985. Structure and physiology of the eggshell. Comprehensive Insect Physiology, Biochemistry and Pharmacology GA Kerkut, LI Gilbert 153–73 New York: Elsevier/Pergamon [Google Scholar]
  54. Mariani BD, Shea MJ, Conboy MJ, Conboy I, King DL, Kafatos FC. 54.  1996. Analysis of regulatory elements of the developmentally controlled chorion s15 promoter in transgenic Drosophila. Dev. Biol. 174:115–24 [Google Scholar]
  55. Mazur GD, Regier JC, Kafatos FC. 55.  1982. Order and defects in the silkmoth chorion, a biological analogue of a cholesteric liquid crystal. Insect Ultrastructure H Akai, RC King 150–83 New York: Plenum [Google Scholar]
  56. McDaniel IE, Lee JM, Berger MS, Hanagami CK, Armstrong JA. 56.  2008. Investigations of CHD1 function in transcription and development of Drosophila melanogaster. Genetics 178:583–87 [Google Scholar]
  57. Medeiros MN, Logullo R, Ramos IB, Sorgine MHF, Paiva-Silva GO. 57.  et al. 2011. Transcriptome and gene expression profile of ovarian follicle tissue of the triatomine bug Rhodnius prolixus. Insect Biochem. Mol. Biol. 41:823–31 [Google Scholar]
  58. Miller M. 58.  2009. The importance of being flexible: the case of basic region leucine zipper transcriptional regulators. Curr. Protein Pept. Sci. 10:244–69 [Google Scholar]
  59. Mita K, Kasahara M, Sasaki S, Nagayasu Y, Yamada T. 59.  et al. 2004. The genome sequence of silkworm, Bombyx mori. DNA Res. 11:27–35 [Google Scholar]
  60. Mitsialis SA, Kafatos FC. 60.  1985. Regulatory elements controlling chorion gene expression are conserved between flies and moths. Nature 317:453–56 [Google Scholar]
  61. Nadel MR, Kafatos FC. 61.  1980. Specific protein synthesis in cellular differentiation. IV. The chorion proteins of Bombyx mori and their program of synthesis. Dev. Biol. 75:26–40 [Google Scholar]
  62. Ohnishi A, Hull JJ, Matsumoto S. 62.  2006. Targeted disruption of genes in the Bombyx mori sex pheromone biosynthetic pathway. Proc. Natl. Acad. Sci. USA 103:4398–403 [Google Scholar]
  63. Oro AE, McKeown M, Evans RM. 63.  1992. The Drosophila retinoid X receptor homolog ultraspiracle functions in both female reproduction and eye morphogenesis. Development 115:449–62 [Google Scholar]
  64. Ote M, Mita K, Kawasaki H, Seki M, Nohata J. 64.  et al. 2004. Microarray analysis of gene expression profiles in wing discs of Bombyx mori during pupal ecdysis. Insect Biochem. Mol. Biol. 34:775–84 [Google Scholar]
  65. Papantonis A. 65.  2008. Nucleosomal organization and regulation of expression of silkmoth chorion genes by architectural factors PhD Thesis, Natl. Kapodistr. Univ. Athens
  66. Papantonis A, Lecanidou R. 66.  2009. A modified chromatin-immunoprecipitation protocol for silkmoth ovarian follicular cells reveals C/EBP and GATA binding modes on an early chorion gene promoter. Mol. Biol. Rep. 36:733–36 [Google Scholar]
  67. Papantonis A, Sourmeli S, Lecanidou R. 67.  2008. Chorion gene activation and repression is dependent on BmC/EBP expression and binding to cognate cis-elements. Biochem. Biophys. Res. Commun. 369:905–9 [Google Scholar]
  68. Papantonis A, Tsatsarounos S, Vanden Broeck J, Lecanidou R. 68.  2008. CHD1 assumes a central role during follicle development. J. Mol. Biol. 383:957–69 [Google Scholar]
  69. Papantonis A, Vanden Broeck J, Lecanidou R. 69.  2008. Architectural factor HMGA induces promoter bending and recruits C/EBP and GATA during silkmoth chorion gene regulation. Biochem. J. 416:85–97 [Google Scholar]
  70. Parks S, Spradling A. 70.  1987. Spatially regulated expression of chorion genes during Drosophila oogenesis. Genes Dev. 1:497–509 [Google Scholar]
  71. Piontkivska H, Yang MQ, Larkin DM, Lewin HA, Reecy J, Elnitski L. 71.  2009. Cross-species mapping of bidirectional promoters enables prediction of unannotated 5′ UTRs and identification of species-specific transcripts. BMC Genomics 10:189 [Google Scholar]
  72. Ptashne M. 72.  2005. Regulation of transcription: from lambda to eukaryotes. Trends Biochem. Sci. 30:275–79 [Google Scholar]
  73. Regier JC, Friedlander T, Leclerc RF, Mitter C, Wiegmann BM. 73.  1995. Lepidopteran phylogeny and applications to comparative studies of development. Molecular Model Systems in the Lepidoptera MR Goldsmith, AS Wilkins 107–37 Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  74. Respuela P, Ferella M, Rada-Iglesias A, Åslund L. 74.  2008. Histone acetylation and methylation at sites initiating divergent polycistronic transcription in Trypanosoma cruzi. J. Biol. Chem. 283:15884–92 [Google Scholar]
  75. Retnakaran A, Hiruma K, Palli SR, Riddiford LM. 75.  1995. Molecular analysis of the mode of action of RH-5992, a lepidopteran-specific, non-steroidal ecdysteroid agonist. Insect Biochem. Mol. Biol. 25:109–17 [Google Scholar]
  76. Rørth P. 76.  2009. Collective cell migration. Annu. Rev. Cell Dev. Biol. 25:407–29 [Google Scholar]
  77. Roth S, Lynch JA. 77.  2009. Symmetry breaking during Drosophila oogenesis. Cold Spring Harb. Perspect. Biol. 1:a001891 [Google Scholar]
  78. Sdralia N, Swevers L, Iatrou K. 78.  2012. BmVMP90, a large vitelline membrane protein of the domesticated silkmoth Bombyx mori, is an essential component of the developing ovarian follicle. Insect Biochem. Mol. Biol. 42:717–27 [Google Scholar]
  79. Shea MJ, King DL, Conboy MJ, Mariani BD, Kafatos FC. 79.  1990. Proteins that bind to Drosophila chorion cis-regulatory elements: a new C2H2 zinc finger protein and a C2C2 steroid receptor-like component. Genes Dev. 4:1128–40 [Google Scholar]
  80. Skeiky YA, Drevet JR, Swevers L, Iatrou K. 80.  1994. Protein phosphorylation and control of chorion gene activation through temporal mobilization of a promoter DNA binding factor from the cytoplasm into the nucleus. J. Biol. Chem. 269:12196–203 [Google Scholar]
  81. Skeiky YA, Iatrou K. 81.  1990. Silkmoth chorion antisense RNA: structural characterization, developmental regulation and evolutionary conservation. J. Mol. Biol. 213:53–66 [Google Scholar]
  82. Skeiky YA, Iatrou K. 82.  1991. Synergistic interactions of silkmoth chorion promoter-binding factors. Mol. Cell. Biol. 11:1954–64 [Google Scholar]
  83. Soller M, Bownes M, Kubli E. 83.  1999. Control of oocyte maturation in sexually mature Drosophila females. Dev. Biol. 208:337–51 [Google Scholar]
  84. Sourmeli S, Kravariti L, Lecanidou R. 84.  2003. In vitro analysis of Bombyx mori early chorion gene regulation: Stage specific expression involves interactions with C/EBP-like and GATA factors. Insect Biochem. Mol. Biol. 33:525–40 [Google Scholar]
  85. Sourmeli S, Papantonis A, Lecanidou R. 85.  2005. A novel role for the Bombyx Slbo homologue, BmC/EBP, in insect choriogenesis. Biochem. Biophys. Res. Commun. 337:713–19 [Google Scholar]
  86. Sourmeli S, Papantonis A, Lecanidou R. 86.  2005. BmCbZ, an insect-specific factor featuring a composite DNA-binding domain, interacts with BmC/EBPγ. Biochem. Biophys. Res. Commun. 338:1957–65 [Google Scholar]
  87. Spoerel NA, Nguyen HT, Eickbush TH, Kafatos FC. 87.  1989. Gene evolution and regulation in the chorion complex of Bombyx mori: hybridization and sequence analysis of multiple developmentally middle A/B chorion gene pairs. J. Mol. Biol. 209:1–19 [Google Scholar]
  88. Spoerel NA, Nguyen HT, Kafatos FC. 88.  1986. Gene evolution and regulation in the chorion complex of Bombyx mori: structural and developmental characterization of four eggshell genes and their flanking DNA regions. J. Mol. Biol. 190:23–35 [Google Scholar]
  89. Spoerel NA, Nguyen HT, Towne S, Kafatos FC. 89.  1993. Negative and positive regulators modulate activity of a silkmoth chorion gene during choriogenesis. J. Mol. Biol. 230:151–60 [Google Scholar]
  90. Spradling AC. 90.  1993. Developmental genetics of oogenesis. The Development of Drosophila melanogaster M Bate, A Martinez Arias 11–70 New York: Cold Spring Harbor Laboratory Press [Google Scholar]
  91. Sridhara S, Lee VH. 91.  2013. Tebufenozide disrupts ovarian development and function in silkmoths. Insect Biochem. Mol. Biol. 43:1087–99 [Google Scholar]
  92. Stokes DG, Tartof KD, Perry RP. 92.  1996. CHD1 is concentrated in interbands and puffed regions of Drosophila polytene chromosomes. Proc. Natl. Acad. Sci. USA 93:7137–42 [Google Scholar]
  93. Swevers L, Drevet JR, Lunke MD, Iatrou K. 93.  1995. The silkmoth homolog of the Drosophila ecdysone receptor (B1 isoform): cloning and analysis of expression during follicular cell differentiation. Insect Biochem. Mol. Biol. 25:857–66 [Google Scholar]
  94. Swevers L, Eystathioy T, Iatrou K. 94.  2002. The orphan nuclear receptors BmE75A and BmE75C of the silkmoth Bombyx mori: hormonal control and ovarian expression. Insect Biochem. Mol. Biol. 32:1643–52 [Google Scholar]
  95. Swevers L, Iatrou K. 95.  1992. Early establishment and autonomous implementation of a developmental program controlling silkmoth chorion gene expression. Dev. Biol. 150:12–22 [Google Scholar]
  96. Swevers L, Iatrou K. 96.  1999. The ecdysone agonist tebufenozide (RH-5992) blocks the progression into the ecdysteroid-induced regulatory cascade and arrests silkmoth oogenesis at mid-vitellogenesis. Insect Biochem. Mol. Biol. 29:955–63 [Google Scholar]
  97. Swevers L, Iatrou K. 97.  2003. The ecdysone regulatory cascade and ovarian development in lepidopteran insects: insights from the silkmoth paradigm. Insect Biochem. Mol. Biol. 33:1285–97 [Google Scholar]
  98. Swevers L, Ito K, Iatrou K. 98.  2002. The BmE75 nuclear receptors function as dominant repressors of the nuclear receptor BmHR3A. J. Biol. Chem. 277:41637–44 [Google Scholar]
  99. Swevers L, Raikhel AS, Sappington TW, Shirk P, Iatrou K. 99.  2005. Vitellogenesis and post-vitellogenic maturation of the insect ovarian follicle. Comprehensive Molecular Insect Science Vol. 1: Reproduction and Development, ed. LI Gilbert, K Iatrou, SS Gill 87–155 New York: Elsevier/Pergamon [Google Scholar]
  100. Swevers L, Vanden Broeck J, Smagghe G. 100.  2013. The possible impact of persistent virus infection on the function of the RNAi machinery in insects: a hypothesis. Front. Physiol. 4:319 [Google Scholar]
  101. Telfer WH. 101.  2009. Egg formation in Lepidoptera. J. Insect Sci. 9:50 [Google Scholar]
  102. Terashima J, Bownes M. 102.  2006. E75A and E75B have opposite effects on the apoptosis/development choice of the Drosophila egg chamber. Cell Death Diff. 13:454–64 [Google Scholar]
  103. Terenius O, Papanicolaou A, Garbutt JS, Eleftherianos I, Huvenne H. 103.  et al. 2011. RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. J. Insect Physiol. 57:231–45 [Google Scholar]
  104. 104. The International Silkworm Genome Consortium 2008. The genome of a lepidopteran model insect, the silkworm Bombyx mori. Insect Biochem. Mol. Biol. 38:1036–45 [Google Scholar]
  105. Tootle TL, Williams D, Hubb A, Frederick R, Spradling A. 105.  2011. Drosophila eggshell production: identification of new genes and coordination by Pxt. PLOS ONE 6:e19943 [Google Scholar]
  106. Tran HG, Steger DJ, Iyer VR, Johnson AD. 106.  2000. The chromodomain protein Chd1p from budding yeast is an ATP-dependent chromatin-modifying factor. EMBO J. 19:2323–31 [Google Scholar]
  107. Tsitilou SG, Rodakis GC, Alexopoulou M, Kafatos FC, Ito K, Iatrou K. 107.  1983. Structural features of B family chorion sequences in the silkmoth Bombyx mori, and their evolutionary implications. EMBO J. 2:1845–52 [Google Scholar]
  108. Tsuchida K, Nagata M, Suzuki A. 108.  1987. Hormonal control of ovarian development in the silkworm, Bombyx mori. Arch. Insect Biochem. Biophys. 5:167–77 [Google Scholar]
  109. Tsukada J, Yoshida Y, Kominato Y, Auron PE. 109.  2011. The CCAAT/enhancer (C/EBP) family of basic-leucine zipper (bZIP) transcription factors is a multifaceted highly-regulated system for gene regulation. Cytokine 54:6–19 [Google Scholar]
  110. Vlachou D, Konsolaki M, Tolias PP, Kafatos FC, Komitopoulou K. 110.  1997. The autosomal chorion locus of the medfly Ceratitis capitata. I. Conserved synteny, amplification and tissue specificity but sequence divergence and altered temporal regulation. Genetics 147:1829–42 [Google Scholar]
  111. Wilson HL, Roesler WJ. 111.  2002. CCAAT/enhancer binding proteins: Do they possess intrinsic cAMP-inducible activity?. Mol. Cell. Endocrinol. 188:15–20 [Google Scholar]
  112. Wiśniewski JR, Schulze E. 112.  1992. Insect proteins homologous to mammalian high mobility group protein 1. Characterization and DNA-binding properties. J. Biol. Chem. 267:17170–77 [Google Scholar]
  113. Woods HA. 113.  2010. Water loss and gas exchange by eggs of Manduca sexta: trading off costs and benefits. J. Insect Physiol. 56:480–87 [Google Scholar]
  114. Wu T, Manogaran AL, Beauchamp JM, Waring GL. 114.  2010. Drosophila vitelline membrane assembly: a critical role for an evolutionarily conserved cysteine in the “VM domain” of sV23. Dev. Biol. 347:360–68 [Google Scholar]
  115. Xia Q, Cheng D, Duan J, Wang G, Cheng T. 115.  et al. 2007. Microarray-based gene expression profiles in multiple tissues of the domesticated silkworm, Bombyx mori. Genome Biol. 8:R162 [Google Scholar]
  116. Xia Q, Zhou Z, Lu C, Cheng D, Dai F. 116.  et al. 2004. A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306:1937–40 [Google Scholar]
  117. Xu Y, Fu Q, Li S, He N. 117.  2011. Silkworm egg proteins at the germ-band formation stage and a functional analysis of BmEP80 protein. Insect Biochem. Mol. Biol. 41:572–81 [Google Scholar]
  118. Xu Y, Zou Z, Zha X, Xiang Z, He N. 118.  2011. A syntenic coding region for vitelline membrane proteins in four lepidopteran insects. J. Mol. Biochem. 1:155–60 [Google Scholar]
  119. Yu X, Zhou Q, Cai Y, Luo Q, Lin H. 119.  et al. 2009. A discovery of novel microRNAs in the silkworm (Bombyx mori) genome. Genomics 94:438–44 [Google Scholar]
  120. Zhang Y, Zhou X, Ge X, Jiang J, Li M. 120.  et al. 2009. Insect-specific microRNA involved in the development of the silkworm Bombyx mori. PLOS ONE 4:e4677 [Google Scholar]
  121. Zhu KY. 121.  2013. RNA interference: a powerful tool in entomological research and a novel approach for insect pest management. Insect Sci. 20:1–3 [Google Scholar]
  122. Tsatsarounos SP, Rodakis GC, Lecanidou R. 122.  2014. Analysis of developmentally regulated chorion gene promoter architecture via electroporation of silk moth follicles. Insect Mol. Biol. In press. doi: 10.1111/imb.12136
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Chorion Genes: A Landscape of Their Evolution, Structure, and Regulation
Annual Review of Entomology 60, 177 (2015); https://doi.org/10.1146/annurev-ento-010814-020810
/content/journals/10.1146/annurev-ento-010814-020810
/content/journals/10.1146/annurev-ento-010814-020810
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  • Article Type: Review Article

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