Chromosoma

, Volume 122, Issue 1–2, pp 103–119 | Cite as

Isolation and characterization of the ecdysone receptor and its heterodimeric partner ultraspiracle through development in Sciara coprophila

  • Michael S. Foulk
  • John M. Waggener
  • Janell M. Johnson
  • Yutaka Yamamoto
  • Gerald M. Liew
  • Fyodor D. Urnov
  • Yuki Young
  • Genee Lee
  • Heidi S. Smith
  • Susan A. Gerbi
Research Article

Abstract

Regulation of DNA replication is critical, and loss of control can lead to DNA amplification. Naturally occurring, developmentally regulated DNA amplification occurs in the DNA puffs of the late larval salivary gland giant polytene chromosomes in the fungus fly, Sciara coprophila. The steroid hormone ecdysone induces DNA amplification in Sciara, and the amplification origin of DNA puff II/9A contains a putative binding site for the ecdysone receptor (EcR). We report here the isolation, cloning, and characterizing of two ecdysone receptor isoforms in Sciara (ScEcR-A and ScEcR-B) and the heterodimeric partner, ultraspiracle (ScUSP). ScEcR-A is the predominant isoform in larval tissues and ScEcR-B in adult tissues, contrary to the pattern in Drosophila. Moreover, ScEcR-A is produced at amplification but is absent just prior. We discuss these results in relation to the model of ecdysone regulation of DNA amplification.

Notes

Acknowledgements

We thank Beth Ryder for her initial work on developmental expression of Sciara EcR. Grant funding from National Institutes of Health to SAG (GM35929) is gratefully acknowledged. GML was supported by a student fellowship from the Agency for Science, Technology and Research (A*STAR), Singapore.

Ethical standards

The experiments in this manuscript comply with current laws in the USA.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

412_2012_395_Fig8_ESM.jpg (110 kb)
Online Resource 1

EcR phylogenetic tree. Phylogenetic tree derived from Clustal W multiple protein sequence alignment of ecdysone receptors from several insect species. Sciara EcRs are highlighted in yellow. (JPEG 109 kb)

412_2012_395_MOESM1_ESM.tif (1021 kb)
High Resolution Image (TIFF 1020 kb)
412_2012_395_Fig9_ESM.jpg (109 kb)
Online Resource 2

USP phylogenetic tree. Phylogenetic tree derived from Clustal W multiple protein sequence alignment of ultraspiracle proteins from several insect species. Sciara USP is highlighted in yellow. (JPEG 108 kb)

412_2012_395_MOESM2_ESM.tif (804 kb)
High Resolution Image (TIFF 804 kb)
412_2012_395_Fig10_ESM.jpg (80 kb)
Online Resource 3

a No ScEcR antibody cross-reactivity. GST-ScEcR-A (∼44 kDa) and GST-ScEcR-B (∼36 kDa) N-termini fusion proteins expressed in E. coli and ScEcR-A (∼19 kDa) and ScEcR-B (∼11 kDa) N-termini purified from chitin bead columns after intein cleavage were run out on SDS-PAGE and blotted to nitrocellulose membranes and probed with the antisera indicated (top panel = αScEcR-A; bottom panel = αScEcR-B). There are GST fusion protein degradation products in lanes 1 and 2. b ScEcR-B salivary gland developmental western blot. Salivary gland protein extracts (125 μg) from the stages indicated run on SDS-PAGE and blotted to nitrocellulose. As a positive control, purified GST-EcR-B was run on the same gel. The blot was probed with an affinity purified αScEcR-B antibody. The position where ScEcR-B should run (∼61 kDa) is indicated. c ScEcR-B in situ hybridization to polytene chromosomes. DAPI-stained chromosomes, ScEcR-B in situ hybridization, and the merged images are shown. (JPEG 80 kb)

412_2012_395_MOESM3_ESM.tif (2.5 mb)
High Resolution Image (TIFF 2552 kb)

References

  1. Arbeitman MN, Hogness DS (2000) Molecular chaperones activate the Drosophila ecdysone receptor, an RXR heterodimer. Cell 101:67–77PubMedCrossRefGoogle Scholar
  2. Ashburner M (1975) The genetic and hormonal control of puffing in the salivary gland chromosomes of Drosophila. Sov J Dev Biol 5:97–107PubMedGoogle Scholar
  3. Ashburner M, Chihara C, Meltzer P, Richards G (1974) Temporal control of puffing activity in polytene chromosomes. Cold Spring Harb Symp Quant Biol 38:655–662PubMedCrossRefGoogle Scholar
  4. Azoitei A, Spindler-Barth M (2009) DNA affects ligand binding of the ecdysone receptor of Drosophila melanogaster. Mol Cell Endocrinol 303:91–99PubMedCrossRefGoogle Scholar
  5. 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 19:2540–2545PubMedCrossRefGoogle Scholar
  6. Beall EL, Manak JR, Zhou S, Bell M, Lipsick JS, Botchan MR (2002) Role for a Drosophila Myb-containing protein complex in site-specific DNA replication. Nature 420:833–837PubMedCrossRefGoogle Scholar
  7. Beall EL, Bell M, Georlette D, Botchan MR (2004) Dm-myb mutant lethality in Drosophila is dependent upon mip130: positive and negative regulation of DNA replication. Genes Dev 18:1667–1680PubMedCrossRefGoogle Scholar
  8. Bender M, Imam FB, Talbot WS, Ganetzky B, Hogness DS (1997) Drosophila ecdysone receptor mutations reveal functional differences among receptor isoforms. Cell 91:777–788PubMedCrossRefGoogle Scholar
  9. Betanska K, Czogalla S, Spindler-Barth M, Spindler KD (2009) Influence of cell cycle on ecdysteroid receptor in CHO-K1 cells. Arch Insect Biochem Physiol 72:142–153PubMedCrossRefGoogle Scholar
  10. Bielinsky AK, Blitzblau H, Beall EL, Ezrokhi M, Smith HS, Botchan MR, Gerbi SA (2001) Origin recognition complex binding to a metazoan replication origin. Curr Biol 11:1427–1431PubMedCrossRefGoogle Scholar
  11. Bienz-Tadmor B, Smith HS, Gerbi SA (1991) The promoter of DNA puff gene II/9-1 of Sciara coprophila is inducible by ecdysone in late prepupal salivary glands of Drosophila melanogaster. Cell Regulation (Mol Biol Cell) 2:875–888Google Scholar
  12. Bosco G, Du W, Orr-Weaver TL (2001) DNA replication control through interaction of E2F-RB and the origin recognition complex. Nat Cell Biol 3:289–295PubMedCrossRefGoogle Scholar
  13. Burtis KC, Thummel CS, Jones CW, Karim FD, Hogness DS (1990) The Drosophila 74EF early puff contains E74, a complex ecdysone-inducible gene that encodes two ets-related proteins. Cell 61:85–99PubMedCrossRefGoogle Scholar
  14. Cakouros D, Daish TJ, Mills K, Kumar S (2004) An arginine-histone methyltransferase, CARMER, coordinates ecdysone-mediated apoptosis in Drosophila cells. J Biol Chem 279:18467–18471PubMedCrossRefGoogle Scholar
  15. Cayirlioglu P, Bonnette PC, Dickson MR, Duronio RJ (2001) Drosophila E2f2 promotes the conversion from genomic DNA replication to gene amplification in ovarian follicle cells. Development 128:5085–5098PubMedGoogle Scholar
  16. Cayirlioglu P, Ward WO, Silver-Key SC, Duronio RJ (2003) Transcriptional repressor functions of Drosophila E2F1 and E2F2 cooperate to inhibit genomic DNA synthesis in ovarian follicle cells. Mol Cell Biol 23:2123–2134PubMedCrossRefGoogle Scholar
  17. Chaudhuri B, Xu H, Todorov I, Dutta A, Yates JL (2001) Human DNA replication initiation factors, ORC and MCM, associate with oriP of Epstein-Barr virus. Proc Natl Acad Sci USA 98:10085–10089PubMedCrossRefGoogle Scholar
  18. Chawla G, Sokol NS (2012) Hormonal activation of let-7-C microRNAs via EcR is required for adult Drosophila melanogaster morphology and function. Development 139:1788–1797PubMedCrossRefGoogle Scholar
  19. Cherbas L, Lee K, Cherbas P (1991) Identification of ecdysone response elements by analysis of the Drosophila Eip28/29 gene. Genes Dev 5:120–131PubMedCrossRefGoogle Scholar
  20. Cherbas L, Hu X, Zhimulev I, Belyaeva E, Cherbas P (2003) EcR isoforms in Drosophila: testing tissue-specific requirements by targeted blockade and rescue. Development 130:271–284PubMedCrossRefGoogle Scholar
  21. Costantino BF, Bricker DK, Alexandre K, Shen K, Merriam JR, Antoniewski C, Callender JL, Henrich VC, Presente A, Andres AJ (2008) A novel ecdysone receptor mediates steroid-regulated developmental events during the mid-third instar of Drosophila. PLoS Genet 4:e1000102PubMedCrossRefGoogle Scholar
  22. Cranna N, Quinn L (2009) Impact of steroid hormone signals on Drosophila cell cycle during development. Cell Div 20(4):3CrossRefGoogle Scholar
  23. Crouse HV, Keyl HG (1968) Extra replications in the “DNA-puffs” of Sciara coprophila. Chromosoma 25:357–364PubMedCrossRefGoogle Scholar
  24. Davis MB, Carney GE, Robertson AE, Bender M (2005) Phenotypic analysis of EcR-a mutants suggests that EcR isoforms have unique functions during Drosophila development. Dev Biol 282:385–396PubMedCrossRefGoogle Scholar
  25. Delanoue R, Slaidina M, Léopold P (2010) The steroid hormone ecdysone controls systemic growth by repressing dMyc function in Drosophila fat cells. Dev Cell 18:1012–1021PubMedCrossRefGoogle Scholar
  26. Dhar SK, Yoshida K, Machida Y, Khaira P, Chaudhuri B, Wohlschlegel JA, Leffak M, Yates J, Dutta A (2001) Replication from oriP of Epstein-Barr virus requires human ORC and is inhibited by geminin. Cell 106:287–296PubMedCrossRefGoogle Scholar
  27. DiBartolomeis SM, Gerbi SA (1989) Molecular characterization of DNA puff II/9A genes in Sciara coprophila. J Mol Biol 210:531–540PubMedCrossRefGoogle Scholar
  28. Dobens L, Rudolph K, Berger EM (1991) Ecdysterone regulatory elements function as both transcriptional activators and repressors. Mol Cell Biol 11:1846–1853PubMedGoogle Scholar
  29. Dressel U, Thormeyer D, Atinicek B, Paululat A, Eggert M, Schneider S, Tenbaum SP, Renkawitz R, Baniahmad A (1999) Alien, a highly conserved protein with characteristics of a corepressor for members of the nuclear hormone receptor superfamily. Mol Cell Biol 19:3383–3394PubMedGoogle Scholar
  30. Fisk GJ, Thummel CS (1998) The DHR78 nuclear receptor is required for ecdysteroid signaling during the onset of Drosophila metamorphosis. Cell 93:543–555PubMedCrossRefGoogle Scholar
  31. Fletcher JC, Thummel CS (1995a) The ecdysone-inducible broad-complex and E74 early genes interact to regulate target gene transcription and Drosophila metamorphosis. Genetics 141:1025–1035PubMedGoogle Scholar
  32. Fletcher JC, Thummel CS (1995b) The Drosophila E74 gene is required for the proper stage- and tissue-specific transcription of ecdysone-regulated genes at the onset of metamorphosis. Development 121:1411–1421PubMedGoogle Scholar
  33. Foulk MS, Liang C, Wu N, Blitzblau HG, Smith H, Alam D, Batra M, Gerbi SA (2006) Ecdysone induces transcription and amplification in Sciara coprophila DNA puff II/9A. Dev Biol 299:151–163PubMedCrossRefGoogle Scholar
  34. Gabrusewycz-Garcia N (1964) Cytological and autoradiographic in Sciara coprophila salivary gland chromosomes. Chromosoma 15:312–344PubMedCrossRefGoogle Scholar
  35. Gabrusewycz-Garcia N (1971) Studies of polytene chromosomes of sciarids. I. The salivary gland chromosomes of Sciara (Lycoriella) pauciseta (II), Felt. Chromosoma 33:421–435CrossRefGoogle Scholar
  36. Gauhar Z, Sun LV, Hua S, Mason CE, Fuchs F, Li TR, Boutros M, White KP (2009) Genomic mapping of binding regions for the ecdysone receptor protein complex. Genome Res 19:1006–1013PubMedCrossRefGoogle Scholar
  37. Gerbi SA, Liang C, Wu N, DiBartolomeis SM, Bienz-Tadmor B, Smith HS, Urnov FD (1993) DNA amplification in DNA puff II/9A of Sciara coprophila. Cold Spring Harb Symp Quant Biol 58:487–494PubMedCrossRefGoogle Scholar
  38. Glover DM, Zaha A, Stocker AJ, Santelli RV, Pueyo MT, De Toledo SM, Lara FJ (1982) Gene amplification in Rhynchosciara salivary gland chromosomes. Proc Natl Acad Sci USA 79:2947–2951PubMedCrossRefGoogle Scholar
  39. Guay PS, Guild GM (1991) The ecdysone-induced puffing cascade in Drosophila salivary glands: a broad-complex early gene regulates intermolt and late gene transcription. Genetics 129:169–175PubMedGoogle Scholar
  40. Hackney JF, Pucci C, Naes E, Dobens L (2007) Ras signaling modulates activity of the ecdysone receptor EcR during cell migration in the Drosophila ovary. Dev Dyn 236:1213–1226PubMedCrossRefGoogle Scholar
  41. Hayward DC, Dhadialla TS, Zhou S, Kuiper MJ, Ball EE, Wyatt GR, Walker VK (2003) Ligand specificity and developmental expression of RXR and ecdysone receptor in the migratory locust. J Insect Physiol 49:1135–1144PubMedCrossRefGoogle Scholar
  42. Hock T, Cottrill T, Keegan J, Garza D (2000) The E23 early gene of Drosophila encodes an ecdysone-inducible ATP-binding cassette transporter capable of repressing ecdysone-mediated gene activation. Proc Natl Acad Sci USA 97:9519–9524PubMedCrossRefGoogle Scholar
  43. Hurban P, Thummel CS (1993) Isolation and characterization of fifteen ecdysone-inducible Drosophila genes reveal unexpected complexities in ecdysone regulation. Mol Cell Biol 13:7101–7111PubMedGoogle Scholar
  44. Hu YF, Hao ZL, Li R (1999) Chromatin remodeling and activation of chromosomal DNA replication by an acidic transcriptional activation domain from BRCA1. Genes Dev 13:637–642PubMedCrossRefGoogle Scholar
  45. Hu X, Cherbas L, Cherbas P (2003) Transcription activation by the ecdysone receptor (EcR/USP): identification of activation functions. Mol Endocrinol 17:716–731PubMedCrossRefGoogle Scholar
  46. Imhof MO, Rusconi S, Lezzi M (1993) Cloning of a Chironomus tentans cDNA encoding a protein (cEcRH) homologous to the Drosophila melanogaster ecdysteroid receptor (dEcR). Insect Biochem Mol Biol 23:115–124PubMedCrossRefGoogle Scholar
  47. Ito K, Asano M, Hughes P, Kohzaki H, Masutani C, Hanaoka F, Kerppola T, Curran T, Murakami Y, Ito Y (1996) c-Jun stimulates origin-dependent DNA unwinding by polyomavirus large T-antigen. EMBO J 15:5636–5646PubMedGoogle Scholar
  48. Johnston DM, Sedkov Y, Petruk S, Riley KM, Fujioka M, Jaynes JB, Mazo A (2011) Ecdysone- and NO-mediated gene regulation by competing EcR/USP and E75A nuclear receptors during Drosophila development. Mol Cell 44:51–61PubMedCrossRefGoogle Scholar
  49. Kapitskaya M, Wang S, Cress DE, Dhadialla TS, Raikhel AS (1996) The mosquito ultraspiracle homologue, a partner of ecdysteroid receptor heterodimer: cloning and characterization of isoforms expressed during vitellogenesis. Mol Cell Endocrinol 121:119–132PubMedCrossRefGoogle Scholar
  50. Karim FD, Thummel CS (1992) Temporal coordination of regulatory gene expression by the steroid hormone ecdysone. EMBO J 11:4083–4093PubMedGoogle Scholar
  51. Kimura S, Sawatsubashi S, Ito S, Kouzmenko A, Suzuki E, Zhao Y, Yamagata K, Tanabe M, Ueda T, Fujiyama S, Murata T, Matsukawa H, Takeyama K, Yaegashi N, Kato S (2008) Drosophila arginine methyltransferase 1 (DART1) is an ecdysone receptor co-repressor. Biochem Biophys Res Commun 371:889–893PubMedCrossRefGoogle Scholar
  52. Koelle MR, Talbot WS, Segraves WA, Bender MT, Cherbas P, Hogness DS (1991) The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell 67:59–77PubMedCrossRefGoogle Scholar
  53. Koelle MR, Segraves WA, Hogness DS (1992) DHR3: a Drosophila steroid receptor homolog. Proc Natl Acad Sci USA 89:6167–6171PubMedCrossRefGoogle Scholar
  54. Kohzaki H, Ito Y, Murakami Y (1999) Context-dependent modulation of replication activity of Saccharomyces cerevisiae autonomously replicating sequences by transcription factors. Mol Cell Biol 19:7428–7435PubMedGoogle Scholar
  55. Kothapalli R, Palli SR, Ladd TR, Sohi SS, Cress D, Dhadialla TS, Tzertzinis G, Retnakaran A (1995) Cloning and developmental expression of the ecdysone receptor gene from the spruce budworm, Choristoneura fumiferana. Dev Genet 17:319–330PubMedCrossRefGoogle Scholar
  56. Li R, Yu DS, Tanaka M, Zheng L, Berger S, Stillman B (1998) Activation of chromosomal DNA replication in Saccharomyces cerevisiae by acidic transcriptional activation domains. Mol Cell Biol 18:1296–1302PubMedGoogle Scholar
  57. Li TR, White KP (2003) Tissue-specific gene expression and ecdysone-regulated genomic networks in Drosophila. Dev Cell 5:59–72PubMedCrossRefGoogle Scholar
  58. Liang C, Spitzer JD, Smith HS, Gerbi SA (1993) Replication initiates at a confined region during DNA amplification in Sciara DNA puff II/9A. Genes Dev 7:1072–1084PubMedCrossRefGoogle Scholar
  59. Liang C, Gerbi SA (1994) Analysis of an origin of DNA amplification in Sciara coprophila by a novel three-dimensional gel method. Mol Cell Biol 14:1520–1529PubMedGoogle Scholar
  60. Liew GM, Foulk MS, Gerbi SA (2013) The ecdysone receptor (ScEcR-A) binds DNA puffs at the start of DNA amplification in Sciara coprophila. (submitted)Google Scholar
  61. Lunyak VV, Ezrokhi M, Smith HS, Gerbi SA (2002) Developmental changes in the Sciara II/9A initiation zone for DNA replication. Mol Cell Biol 22:8426–8437PubMedCrossRefGoogle Scholar
  62. Maki A, Sawatsubashi S, Ito S, Shirode Y, Suzuki E, Zhao Y, Yamagata K, Kouzmenko A, Takeyama K, Kato S (2004) Juvenile hormones antagonize ecdysone actions through co-repressor recruitment to EcR/USP heterodimers. Biochem Biophys Res Commun 320:262–267PubMedCrossRefGoogle Scholar
  63. Marahrens Y, Stillman B (1992) A yeast chromosomal origin of DNA replication defined by multiple functional elements. Science 255:817–823PubMedCrossRefGoogle Scholar
  64. Meijsing SH, Pufall MA, So AY, Bates DL, Chen L, Yamamoto KR (2009) DNA binding site sequence directs glucocorticoid receptor structure and activity. Science 324:407–410PubMedCrossRefGoogle Scholar
  65. Mouillet JF, Delbecque JP, Quennedey B, Delachambre J (1997) Cloning of two putative ecdysteroid receptor isoforms from Tenebrio molitor and their developmental expression in the epidermis during metamorphosis. Eur J Biochem 248:856–863PubMedCrossRefGoogle Scholar
  66. Mouillet JF, Henrich VC, Lezzi M, Vögtli M (2001) Differential control of gene activity by isoforms a, B1 and B2 of the Drosophila ecdysone receptor. Eur J Biochem 268:1811–1819PubMedCrossRefGoogle Scholar
  67. Murakami Y, Satake M, Yamaguchi-Iwai Y, Sakai M, Muramatsu M, Ito Y (1991) The nuclear protooncogenes c-jun and c-fos as regulators of DNA replication. Proc Natl Acad Sci USA 88:3947–3951PubMedCrossRefGoogle Scholar
  68. Oro AE, McKeown M, Evans RM (1990) Relationship between the product of the Drosophila ultraspiracle locus and the vertebrate retinoid X receptor. Nature 347:298–301PubMedCrossRefGoogle Scholar
  69. Oro AE, McKeown M, Evans RM (1992) The Drosophila retinoid X receptor homolog ultraspiracle functions in both female reproduction and eye morphogenesis. Development 115:449–462PubMedGoogle Scholar
  70. Perera SC, Palli SR, Ladd TR, Krell PJ, Retnakaran A (1998) The ultraspiracle gene of the spruce budworm, Choristoneura fumiferana: cloning of cDNA and developmental expression of mRNA. Dev Genet 22:169–179PubMedCrossRefGoogle Scholar
  71. Perera SC, Ladd TR, Dhadialla TS, Krell PJ, Sohi SS, Retnakaran A, Palli SR (1999) Studies on two ecdysone receptor isoforms of the spruce budworm, Choristoneura fumiferana. Mol Cell Endocrinol 152:73–84PubMedCrossRefGoogle Scholar
  72. Poulson DF, Metz CW (1938) Studies on the structure of the nucleolus-forming regions in the giant salivary gland chromosomes of Diptera. J Morphol 63:363–395CrossRefGoogle Scholar
  73. Rachez C, Lemon BD, Suldan Z, Bromleigh V, Gamble M, Näär AM, Erdjument-Bromage H, Tempst P, Freedman LP (1999) Ligand-dependent transcription activation by nuclear receptors requires the DRIP complex. Nature 398:824–828PubMedCrossRefGoogle Scholar
  74. Rasch EM (1970) Two-wavelength cytophotometry of Sciara salivary gland chromosomes. In: Wied GL, Bahr GF (eds) Introduction to quantitative cytochemistry. Academic, New York, pp 335–355Google Scholar
  75. Ritzi M, Tillack K, Gerhardt J, Ott E, Humme S, Kremmer E, Hammerschmidt W, Schepers A (2003) Complex protein-DNA dynamics at the latent origin of DNA replication of Epstein-Barr virus. J Cell Sci 116:3971–3984PubMedCrossRefGoogle Scholar
  76. Robert M (1971) Einfluss von ionenstärke und pH auf die differentielle dekondesation der nukleoproteide isolierter speicheldrüsen zellkerne und chromosomen von Chironomus thummi. Chromosoma 36:1–33PubMedCrossRefGoogle Scholar
  77. Royzman I, Austin RJ, Bosco G, Bell SP, Orr-Weaver TL (1999) ORC localization in Drosophila follicle cells and the effects of mutations in dE2F and dDP. Genes Dev 13:827–840PubMedCrossRefGoogle Scholar
  78. Rudkin G, Corlette SL (1957) Disproportionate synthesis of DNA in a polytene chromosome region. Proc Natl Acad Sci USA 43:964–968PubMedCrossRefGoogle Scholar
  79. Saleh DS, Zhang J, Wyatt GR, Walker VK (1998) Cloning and characterization of an ecdysone receptor cDNA from Locusta migratoria. Mol Cell Endocrinol 143:91–99PubMedCrossRefGoogle Scholar
  80. Schepers A, Ritzi M, Bousset K, Kremmer E, Yates JL, Harwood J, Diffley JF, Hammerschmidt W (2001) Human origin recognition complex binds to the region of the latent origin of DNA replication of Epstein-Barr virus. EMBO J 20:4588–4602PubMedCrossRefGoogle Scholar
  81. Schmidt ER (1992) A simplified and efficient protocol for non-radioactive in situ hybridisation to polytene chromosomes with a DIG.-labeled DNA probe. In: Non radioactive in situ hybridisation application manual. Roche, Indianapolis, pp 36–38.Google Scholar
  82. 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 426:78–83PubMedCrossRefGoogle Scholar
  83. Segraves WA, Hogness DS (1990) The E75 ecdysone-inducible gene responsible for the 75B early puff in Drosophila encodes two new members of the steroid receptor superfamily. Genes Dev 4:204–219PubMedCrossRefGoogle Scholar
  84. Shea MJ, King DL, Conboy MJ, Mariani BD, Kafatos FC (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 4:1128–1140PubMedCrossRefGoogle Scholar
  85. Stocker AJ, Pueyo MT, Pereira SD, Lara FJS (1984) Ecdysteroid titers and changes in the chromosomal activity in the salivary glands of Rhynchosciara americana. Chromosoma 90:26–38CrossRefGoogle Scholar
  86. Stone BL, Thummel CS (1993) The Drosophila 78C early late puff contains E78, an ecdysone-inducible gene that encodes a novel member of the nuclear hormone receptor superfamily. Cell 75:307–320PubMedCrossRefGoogle Scholar
  87. Stowers RS, Garza D, Rascle A, Hogness DS (2000) The L63 gene is necessary for the ecdysone-induced 63E late puff and encodes CDK proteins required for Drosophila development. Dev Biol 221:23–40PubMedCrossRefGoogle Scholar
  88. Sun J, Smith L, Armento A, Deng WM (2008) Regulation of the endocycle/gene amplification switch by notch and ecdysone signaling. J Cell Biol 182:885–896PubMedCrossRefGoogle Scholar
  89. Talbot WS, Swyryd EA, Hogness DS (1993) Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. Cell 73:1323–1337PubMedCrossRefGoogle Scholar
  90. Thomas HE, Stunnenberg HG, Stewart AF (1993) Heterodimerization of the Drosophila ecdysone receptor with retinoid X receptor and ultraspiracle. Nature 362:471–475PubMedCrossRefGoogle Scholar
  91. Thummel CS (2002) Ecdysone-regulated puff genes 2000. Insect Biochem Mol Biol 32:113–120PubMedCrossRefGoogle Scholar
  92. Thummel CS, Burtis KC, Hogness DS (1990) Spatial and temporal patterns of E74 transcription during Drosophila development. Cell 61:101–111PubMedCrossRefGoogle Scholar
  93. Tsai CC, Kao HY, Yao TP, McKeown M, Evans RM (1999) SMRTER, a Drosophila nuclear receptor coregulator, reveals that EcR-mediated repression is critical for development. Mol Cell 4:175–186PubMedCrossRefGoogle Scholar
  94. Vögtli M, Imhof MO, Brown NE, Rauch P, Spindler-Barth M, Lezzi M, Henrich VC (1999) Functional characterization of two ultraspiracle forms (CtUSP-1 and CtUSP-2) from Chironomus tentans. Insect Biochem Mol Biol 29:931–942PubMedCrossRefGoogle Scholar
  95. Wang SF, Li C, Sun G, Zhu J, Raikhel AS (2002) Differential expression and regulation by 20-hydroxyecdysone of mosquito ecdysteroid receptor isoforms A and B. Mol Cell Endocrinol 196:29–42PubMedCrossRefGoogle Scholar
  96. Watzinger F, Hörth E, Lion T (2001) Quantification of mRNA expression by competitive PCR using non-homologous competitors containing a shifted restriction site. Nucleic Acids Res 29:E52–2PubMedCrossRefGoogle Scholar
  97. Wu N, Liang C, DiBartolomeis SM, Smith HS, Gerbi SA (1993) Developmental progression of DNA puffs in Sciara coprophila: amplification and transcription. Dev Biol 160:73–84PubMedCrossRefGoogle Scholar
  98. Yao TP, Segraves WA, Oro AE, McKeown M, Evans RM (1992) Drosophila ultraspiracle modulates ecdysone receptor function via heterodimer formation. Cell 71:63–72PubMedCrossRefGoogle Scholar
  99. Yao TP, Forman BM, Jiang Z, Cherbas L, Chen JD, McKeown M, Cherbas P, Evans RM (1993) Functional ecdysone receptor is the product of EcR and ultraspiracle genes. Nature 366:476–479PubMedCrossRefGoogle Scholar
  100. Zink B, Engström Y, Gehring WJ, Paro R (1991) Direct interaction of the polycomb protein with antennapedia regulatory sequences in polytene chromosomes of Drosophila melanogaster. EMBO J 10:153–162PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Michael S. Foulk
    • 1
  • John M. Waggener
    • 1
  • Janell M. Johnson
    • 1
  • Yutaka Yamamoto
    • 1
  • Gerald M. Liew
    • 1
    • 2
  • Fyodor D. Urnov
    • 1
    • 3
  • Yuki Young
    • 1
  • Genee Lee
    • 1
  • Heidi S. Smith
    • 1
  • Susan A. Gerbi
    • 1
  1. 1.Department of Molecular Biology, Cell Biology and BiochemistryBrown UniversityProvidenceUSA
  2. 2.Department of BiochemistryStanford University School of MedicineStanfordUSA
  3. 3.Sangamo BioSciences, IncRichmondUSA

Personalised recommendations