Methoprene-Tolerant, A PAS Gene Critical for Juvenile Hormone Signaling in Drosophila Melanogaster

  • Thomas G. Wilson

Abstract

Since their discovery, bHLH-PAS genes have been found to be widespread among organisms, ranging from prokaryotes to humans (1,2). Proteins encoded by genes in the PAS family function to sense environmental and developmental signals that reach an organism or a tissue within an organism, and they initiate a response that usually involves the regulation of target gene(s). As discussed in these chapters, the environmental signals range from chemical (planar aromatic hydrocarbons; oxygen tension) to physical (light). The developmental signals are less well-understood, but PAS mutants have shown the importance of PAS genes during development (3, 4, 5, 6, 7, 8, 9, 10). The availability of the genomic sequence of humans, Drosophila melanogaster, and Caenorhabditis elegans within the past several years has allowed the constellation of PAS genes to be identified in these organisms, and it seems unlikely that new PAS genes having functions that are radically different from those of the present family members will be uncovered. So, our task at present is to elucidate the functions and molecular mechanisms of these genes.

Keywords

Toxicity Estrogen Recombination Hydrocarbon Retinoid 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Gu, Y.-Z., J. B. Hogenesch, and C. A. Bradfield. 2000. The PAS superfamily: Sensors of environmental and developmental signals. Annu. Rev. Pharmacol Toxicol. 40:519–561.PubMedCrossRefGoogle Scholar
  2. 2.
    Crews, S. T., and C. M. Fan. 1999. Remembrance of things PAS: regulation of development by bHLH-PAS proteins. Curr. Opin. Genet. Dev. 9:580–587.PubMedCrossRefGoogle Scholar
  3. 3.
    Wilson, T. G., and M. Ashok. 1998. Insecticide resistance resulting from an absence of target-site gene product. Proc. Natl. Acad. Set USA 95:14040–14044.CrossRefGoogle Scholar
  4. 4.
    Sonnenfeld, M., and J. R. Jacobs. 1994. Mesectodermal cell fate analysis in Drosophila midline mutants. Mech. Dev. 46:3–13.PubMedCrossRefGoogle Scholar
  5. 5.
    Isaac, D. D., and D. Andrew. 1996. Tubulogenesis in Drosophila: a requirement for the trachealess gene product. Genes & Dev. 10:103–117.CrossRefGoogle Scholar
  6. 6.
    Gehin, M., M. Mark, C. Dennefeld, A. Dierich, H. Gronemeyer, and P. Chambon. 2002. The function of TIF2/GRIP1 in mouse reproduction is distinct from those of SRC-1 andp/CIP. Mol. Cell Biol. 22:5923–5937.PubMedCrossRefGoogle Scholar
  7. 7.
    Michaud, J. L., T. Rosenquist, N. R. May, and C.-M. Fan. 1998. Development of neuroendocrine lineages requires the bHLH-PAS transcription factor SIM1. Genes & Dev. 12:3264–3275.CrossRefGoogle Scholar
  8. 8.
    Keith, B., D. M. Adelman, and M. C. Simon. 2001. Targeted mutation of the murine arylhydrocarbon receptor nuclear translocator 2 (Arnt2) gene reveals partial redundancy with Arnt. Proc. Natl Acad. Sci. USA 98:6692–6697.PubMedCrossRefGoogle Scholar
  9. 9.
    Maltepe, E., J. V. Schmidt, D. Baunoch, C. A. Bradfield, and M. C. Simon. 1997. Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature 386:403–407.PubMedCrossRefGoogle Scholar
  10. 10.
    Kozak, K. R., B. Abbott, and O. Hankinson. 1997. ARNT-deficient mice and placental differentiation. Dev. Biol. 191:297–305.CrossRefGoogle Scholar
  11. 11.
    Wilson, T. G., and J. Fabian. 1986. A Drosophila melanogaster mutant resistant to a chemical analog of juvenile hormone. Develop. Biol. 118:190–201.PubMedCrossRefGoogle Scholar
  12. 12.
    Sonnenfeld, ML, M. Ward, G. Nystrom, J. Mosher, S. Stahl, and S. Crews. 1997. The Drosophila tango gene encodes a bHLH-PAS protein that is orthologous to mammalian Arnt and controls CNS midline and tracheal development. Development 124:457Google Scholar
  13. 13.
    Bacon, N. C. M., P. Wappner, J. F. O’Rourke, S. M. Bartlett, B. Shilo, C. W. Pugh, and P. J. Ratcliffe. 1998. Regulation of the Drosophila bHLH-PAS protein Sima by hypoxia: functional evidence for homology with mammalian HIF-la. Biochem. Biophys. Res. Comm. 249:811–816.PubMedCrossRefGoogle Scholar
  14. 14.
    Riddiford, L. M. 1994. Cellular and molecular actions of juvenile hormone I. General considerations and premetamorphic actions. Adv. Insect Physiol. 24:213–274.CrossRefGoogle Scholar
  15. 15.
    Wyatt, G. R., and K. G. Davey. 1996. Cellular and molecular actions of juvenile hormone II. Roles of juvenile hormone in adult insects. Adv. Insect Physiol. 26:1–155.CrossRefGoogle Scholar
  16. 16.
    Koelle, M. R., W. S. Talbot, W. A. Segraves, M. T. Bender, P. Cherbas, and D. S. Hogness. 1991. The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell 67:59–77.PubMedCrossRefGoogle Scholar
  17. 17.
    Andres, A. J., and C. S. Thummel. 1992. Hormones, puffs, and flies: The molecular control of metamorphosis by ecdysone. Trends Genet. 8:132–138.PubMedGoogle Scholar
  18. 18.
    Willis, J. H. 1974. Morphogenetic action of juvenile hormones. Annu. Rev. Entomol. 19:97–115.PubMedCrossRefGoogle Scholar
  19. 19.
    Henrich, V. C, T. J. Sliter, D. B. Lubahn, A. Maclntyre, and L. I. Gilbert. 1990. A steroid/thyroid hormone receptor superfamily member in Drosophila melanogaster that shares extensive sequence similarity with a mammalian homologue. Nucl. Acids Res. 18:4143–4148.PubMedCrossRefGoogle Scholar
  20. 20.
    Yao, T.-P., B. M. Forman, Z. Jiang, L. Cherbas, J.-D. Chen, M. McKeown, P. Cherbas, and R. M. Evans. 1993. Functional ecdysone receptor is the product of EcR and Ultraspiracle genes. Nature 366:476–479.PubMedCrossRefGoogle Scholar
  21. 21.
    Oro, A. E., M. McKeown, and R. M. Evans. 1992. The Drosophila retinoid X receptor homolog ultraspiracle functions in both female reproduction and eye morphogenesis. Development 115:449–462.PubMedGoogle Scholar
  22. 22.
    White, K. P., S. A. Rifkin, P. Hurban, and D. S. Hogness. 1999. Microarray analysis of Drosophila development during metamorphosis. Science 286:2179–2184.PubMedCrossRefGoogle Scholar
  23. 23.
    Staal, G. B. 1975. Insect growth regulators with juvenile hormone activity. Annu. Rev. Entomol. 20:417–460.PubMedCrossRefGoogle Scholar
  24. 24.
    Cerf, D. C, and G. P. Georghiou. 1974. Cross resistance to juvenile hormone analogues in insecticide-resistant strains of Musca domestica. Pestic. Sci. 5:759–767.CrossRefGoogle Scholar
  25. 25.
    Dame, D. A., G. J. Wichterman, and J. A. Hornby. 1998. Mosquito (Aedes taeniorhynchus) resistance to methoprene in an isolated habitat. J. Amer. Mosq. Control Assoc. 14:200–203.Google Scholar
  26. 26.
    Schooley, D. A., F. C. Baker, L. W. Tsai, C. A. Miller, and G. C. Jamieson. 1984. Juvenile hormones 0,1 and II exist only in Lepidoptera, p. 371-381. In M. Porchet (ed.), Biosynthesis, metabolism, and mode of action of invertebrate hormones. Springer-Verlag, Berlin.Google Scholar
  27. 27.
    Richard, D. S., S. W. Applebaum, T. J. Sliter, F. C. Baker, D. A. Schooley, C. C. Reuter, V. C. Henrich, and L. I. Gilbert. 1989. Juvenile hormone bisepoxide biosynthesis in vitro by the ring gland of Drosophila melanogaster: A putative juvenile hormone in the higher Diptera. Proc. Natl. Acad. Sci. USA 86:1421–1425.PubMedCrossRefGoogle Scholar
  28. 28.
    Williams, C. M. 1967. Third-generation pesticides. Sci. Am. 217:13–17.PubMedCrossRefGoogle Scholar
  29. 29.
    Wilson, T. G., and J. Fabian (ed.). 1987. Selection of methoprene-resistant mutants of Drosophila melanogaster, vol. 49. UCLA symposia on molecular and cellular biology, new series.Google Scholar
  30. 30.
    Riddiford, L. M., and M. Ashburner. 1991. Effects of juvenile hormone mimics on larval development and metamorphosis of Drosophila melanogaster. Gen. Comp. Endocrinol. 82:172–183.PubMedCrossRefGoogle Scholar
  31. 31.
    Wilson, T. G. 2001. Resistance of Drosophila to toxins. Annu. Rev. Entomol. 46:545–571.PubMedCrossRefGoogle Scholar
  32. 32.
    Taylor, M., and R. Feyereisen. 1996. Molecular biology and evolution of resistance to toxicants. Mol. Biol. Evol. 13:719–734.PubMedCrossRefGoogle Scholar
  33. 33.
    Feyereisen, R. 1995. Molecular biology of insecticide resistance. Toxicol. Lett. 82:83–90.PubMedCrossRefGoogle Scholar
  34. 34.
    Shemshedini, L., and T. G. Wilson. 1990. Resistance to juvenile hormone and an insect growth regulator in Drosophila is associated with an altered cytosolic juvenile hormone binding protein. Proc. Natl. Acad. Sci. USA 87:2072–2076.PubMedCrossRefGoogle Scholar
  35. 35.
    ffrench-Constant, R. H. 1999. Target site mediated insecticide resistance: what questions remain? Insect Biochem. Mol. Biol. 29:397–403.CrossRefGoogle Scholar
  36. 36.
    Shemshedini, L., M. Lanoue, and T. G. Wilson. 1990. Evidence for a juvenile hormone receptor involved in protein synthesis in Drosophila melanogaster. J. Biol Chem. 265:1913–1918.PubMedGoogle Scholar
  37. 37.
    Poland, A., and E. Glover. 1980. 2,3,7,8-tetrachlorodibenzo-p-dioxin: Segregation of toxicity with the Ah locus. Mol. Pharmacol. 17:86–94.PubMedGoogle Scholar
  38. 38.
    Brattsten, L., C. W. J. Holyoke, J. R. Leeper, and K. F. Raffa. 1986. Insecticide resistance: challenge to pest management and basic research. Science 231:1255–1260.PubMedCrossRefGoogle Scholar
  39. 39.
    Wilson, T. G., and J. W. Cain. 1997. Resistance to the insecticides lufenuron and propoxur in natural populations of Drosophila melanogaster (Diptera: Drosophilidae). J. Econ. Entomol. 90:1131–1136.PubMedGoogle Scholar
  40. 40.
    Gruntenko, N. E., T. G. Wilson, M. Monastirioti, and I. Y. Rauschenbach. 2000. Stress-reactivity and juvenile hormone degradation in Drosophila melanogaster strains having stress-related mutations. Insect Biochem. Mol. Biol. 30:775–783.PubMedCrossRefGoogle Scholar
  41. 41.
    Bingham, P. M., M. G. Kidwell, and G. M. Rubin. 1981. Cloning of DNA sequences from the white locus of D. melanogaster by a novel and general method. Cell 25:693–704.PubMedCrossRefGoogle Scholar
  42. 42.
    Turner, C, and T. G. Wilson. 1995. Molecular analysis of the Methoprene-tolerant gene region of Drosophila melanogaster. Arch. Insect Biochem. Physiol. 30:133–147.PubMedCrossRefGoogle Scholar
  43. 43.
    Spradling, A. C. 1986. P element-mediated transformation, p. 175–197. In D. B. Roberts (ed.), Drosophila: a practical approach. IRL Press, Oxford.Google Scholar
  44. 44.
    Ashok, M., C. Turner, and T. G. Wilson. 1998. Insect juvenile hormone resistance gene homology with the bHLH-PAS family of transcriptional regulators. Proc. Natl Acad. Sci. USA 95:2761–2766.PubMedCrossRefGoogle Scholar
  45. 45.
    Ashok, M., C. Turner, and T. G. Wilson. 1998. Insect juvenile hormone resistance gene homology with the bHLH-PAS family of transcriptional regulators. Proc. Natl. Acad. Sci. USA 95:2761–6.PubMedCrossRefGoogle Scholar
  46. 46.
    Huang, Z. J., I. Edery, and M. Rosbash. 1993. PAS is a dimerization domain common to Drosophila Period and several transcription factors. Nature 364:259–262.PubMedCrossRefGoogle Scholar
  47. 47.
    Zelzer, E., P. Wappner, and B.-Z. Shilo. 1997. The PAS domain confers target gene specificity of Drosophila bHLH-PAS proteins. Genes & Dev. 11:2079–2089.CrossRefGoogle Scholar
  48. 48.
    Burbach, K. M., A. Poland, and C. A. Bradfield. 1992. Cloning of the Ah-receptor cDNA reveals a distinctive ligand-activated transcription factor. Proc. Natl. Acad. Sci. USA 89:8185–8189.PubMedCrossRefGoogle Scholar
  49. 49.
    Ponting, C. P., and L. Aravind. 1998. PAS: a multifunctional domain family comes to light. Curr.Biol. 7.R674–R677.CrossRefGoogle Scholar
  50. 50.
    Beverley, S. M., and A. C. Wilson. 1984. Molecular evolution in Drosophila and the higher Diptera. II. A time scale for fly evolution. J. Mol. Evol. 21:1–13.PubMedCrossRefGoogle Scholar
  51. 51.
    Duncan, D. M., E. A. Burgess, and I. Duncan. 1998. Control of distal antennal identity and tarsal development in Drosophila by spineless-aristapedia, a homolog of the mammalian dioxin receptor. Genes & Dev 12:1290–1303.CrossRefGoogle Scholar
  52. 52.
    Nambu, J. R., J. O. Lewis, K. A. Wharton, Jr., and S. T. Crews. 1991. The Drosophila single-minded gene encodes a helix-loop-helix protein that acts as a master regulator of CNS midline development. Cell 67:1157–1167.PubMedCrossRefGoogle Scholar
  53. 53.
    Wilson, T. G., and C. Turner (ed.). 1992. Molecular analysis of Methoprene-tolerant, a gene in Drosophila involved in resistance to juvenile hormone analog growth regulators, vol. 505. American Chemical Society, Washington,DC.Google Scholar
  54. 54.
    Soller, M., M. Bownes, and E. Kubli. 1999. Control of oocyte maturation in sexually mature Drosophila females. Dev. Biol. 208:337–351.PubMedCrossRefGoogle Scholar
  55. 55.
    Wilson, T. G. 1982. A correlation between juvenile hormone deficiency and vitellogenic oocyte degeneration in Drosophila melanogaster. Wilhelm Roux Arch. Entwicklungsmech. Org. 191:257–263.CrossRefGoogle Scholar
  56. 56.
    Jowett, T., and J. H. Postlethwait. 1980. The regulation of yolk polypeptide synthesis in Drosophila ovaries and fat body by 20-hydroxyecdysone and a juvenile hormone analog. Develop. Biol. 80:225–234.PubMedCrossRefGoogle Scholar
  57. 57.
    Greenleaf, A. L., L. M. Borsett, P. F. Jiamachello, and D. E. Coulter. 1979. Alpha-amanitin-resistant D. melanogaster with an altered RNA polymerase. Cell 18:613–622.PubMedCrossRefGoogle Scholar
  58. 58.
    Minkoff, C, III, and T. G. Wilson. 1992. The competitive ability and fitness components of the Methoprene-tolerant (Met) Drosophila mutant resistant to juvenile hormone analog insecticides. Genetics 131:91–97.PubMedGoogle Scholar
  59. 59.
    Brookfield, J. F. Y. 1997. Genetic redundancy. Adv. Genet. 36:137–155.PubMedCrossRefGoogle Scholar
  60. 60.
    Goshu, E., H. Jin, R. Fasnacht, M. Sepenski, J. L. Michaud, and C. M. Fan. 2002. Sim2 mutants have developmental defects not overlapping with those of Sim1 mutants. Mol. Cell Biol. 22:4147–4157.PubMedCrossRefGoogle Scholar
  61. 61.
    Moore, A. W., S. Barbel, L. Y. Jan, and Y. N. Jan. 2000. A genomewide survey of basic helix-loop-helix factors in Drosophila. Proc. Natl. Acad. Sci. USA 97:10436–10441.PubMedCrossRefGoogle Scholar
  62. 62.
    Hirose, K., M. Morita, M. Ema, J. Mimura, H. Hamada, H. Fujii, Y. Saijo, O. Gotoh, K. Sogawa, and Y. Fujii-Kuriyama. 1996. cDNA cloning and tissue-specific expression of a novel basic helix-loop-helix/PAS factor (Arnt2) with close sequence similarity to the aryl hydrocarbon receptor nuclear translocator (Arnt). Mol. Cell Biol. 16:1706–1713.PubMedGoogle Scholar
  63. 63.
    Baker, F. C, H. H. Hagedorn, D. A. Schooley, and G. Wheelock. 1983. Mosquito juvenile hormone: identification and bioassay activity. J. Insect Physiol. 29:465–470.CrossRefGoogle Scholar
  64. 64.
    Klowden, M. J. 1997. Endocrine aspects of mosquito reproduction. Arch. Insect Biochem. Physiol. 35:491–512.CrossRefGoogle Scholar
  65. 65.
    O’Donnell, P. P., and M. J. Klowden. 1997. Methoprene affects the rotation of the male terminalia of Aedes aegypti mosquitoes. J. Amer. Mosq. Control Assoc. 13:1–4.Google Scholar
  66. 66.
    Wilk, R., I. Wiezman, and B.-Z. Shilo. 1996. trachealess encodes a bHLH-PAS protein that is an inducer of tracheal cell fates in Drosophila. Genes & Dev. 10:93–102.CrossRefGoogle Scholar
  67. 67.
    Crews, S. T. 1998. Control of cell lineage-specific development and transcription by bHLH-PAS proteins. Genes & Dev. 12:607–620.CrossRefGoogle Scholar
  68. 68.
    Crews, S. T., J. B. Thomas, and C. S. Goodman. 1988. The Drosophila single-minded gene encodes a nuclear protein with sequence similarity to the per gene product. Cell 52:143–151.PubMedCrossRefGoogle Scholar
  69. 69.
    Ma, Q., and J. J. P. Whitlock. 1997. A novel cytoplasmic protein that interacts with the Ah receptor, contains tetratricopeptide repeat motifs, and augments the transcriptional response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. J. Biol. Chem. 272:8878–8884.PubMedCrossRefGoogle Scholar
  70. 70.
    Wilson, C. L., and S. Safe. 1998. Mechanisms of ligand-induced aryl hydrocarbon receptor-mediated biochemical and toxic responses. Toxicol. Path. 26:657–671.Google Scholar
  71. 71.
    Pursley, S., M. Ashok, and T. G. Wilson. 2000. Intracellular localization and tissue specificity of the Methoprene-tolerant (Met) gene product in Drosophila melanogaster. Insect Biochem. Mol. Biol. 30:839–845.PubMedCrossRefGoogle Scholar
  72. 72.
    Ashburner, M. 1970. Effects of juvenile hormone on adult differentiation of Drosophila melanogaster. Nature 227:187–189.PubMedCrossRefGoogle Scholar
  73. 73.
    Madhavan, K. 1973. Morphogenetic effects of juvenile hormone and juvenile hormone mimics on adult development of Drosophila. J. Insect Physiol. 19:441–453.PubMedCrossRefGoogle Scholar
  74. 74.
    Postlethwait, J. H. 1974. Juvenile hormone and the adult development of Drosophila. Biol. Bull. 147:119–135.PubMedCrossRefGoogle Scholar
  75. 75.
    Sehnal, F., and J. Zdarek. 1976. Action of juvenoids on the metamorphosis of cyclorrhaphous Diptera. J. Insect Physiol. 22:673–682.CrossRefGoogle Scholar
  76. 76.
    Restifo, L. L., and T. G. Wilson. 1998. A juvenile hormone agonist reveals distinct developmental pathways mediated by ecdysone-inducible Broad Complex transcription factors. Develop. Genet. 22:141–159.CrossRefGoogle Scholar
  77. 77.
    Chao, A. T., and G. M. Guild. 1986. Molecular analysis of the ecdysterone-inducible 2B5 “early” puff in Drosophila melanogaster. EMBOJ. 5:143–150.Google Scholar
  78. 78.
    Restifo, L. L., and K. White. 1991. Mutations in a steroid hormone-regulated gene disrupt the metamorphosis of the central nervous system in Drosophila. Dev. Biol. 148:174–194.PubMedCrossRefGoogle Scholar
  79. 79.
    Kiss, I., A. H. Beaton, J. Tardiff, D. Fristrom, and J. W. Fristrom. 1988. Interactions and developmental effects of mutations in the Broad-Complex of Drosophila melanogaster. Genetics 118:247–259.PubMedGoogle Scholar
  80. 80.
    Crossgrove, K., C. A. Bayer, F. J.W., and G. M. Guild. 1996. The Drosophila Broad-Complex early gene directly regulates late gene transcription during the ecdysone-induced puffing cascade. Dev. Biol. 180:745–758.PubMedCrossRefGoogle Scholar
  81. 81.
    Zhou, X., and L. M. Riddiford. 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.PubMedGoogle Scholar
  82. 82.
    Safe, S., F. Wang, W. Porter, R. Duan, and A. McDougal. 1998. Ah receptor agonists as endocrine disruptors: antiestrogenic activity and mechanisms. Toxicol. Lett. 102–103:343–347.PubMedCrossRefGoogle Scholar
  83. 83.
    Makino, Y., R. Cao, K. Svensson, G. Bertilsson, M. Asman, H. Tanaka, Y. Cao, A. Berkenstam, and L. Poellinger. 2001. Inhibitory PAS domain protein is a negative regulator of hypoxia-inducible gene expression. Nature 414:550–554.PubMedCrossRefGoogle Scholar
  84. 84.
    Ma, Y., L. Certel, Y. Gao, E. Niemitz, J. Mosher, A. Mukherjee, M. Mutsuddi, N. Huseinovic, S. T. Crews, W. A. Johnson, et al. 2000. Functional interactions between Drosophila bHLH-PAS, Sox, and POU transcription factors regulate CNS midline expression of the slit gene. J. Neurosci. 20:4596–4605.PubMedGoogle Scholar
  85. 85.
    Chen, Y., M. J. Riese, M. A. Killinger, and F. M. Hoffmann. 1998. A genetic screen for modifiers of Drosophila decapentaplegic signaling identifies mutations in punt, Mothers against dpp, and the BMP-7 homologue, 60A. Development 125:1759–1768.PubMedGoogle Scholar
  86. 86.
    Belyaeva, E. S., M. G. Aizenzon, V. F. Semeshin, I. Kiss, K. Koczya, M. Baritcheva, T. D. Gorelova, and I. F. Zhimulev. 1980. Cytogenetic analysis of the 2B3–4–2B11 region of the X-chromosome of Drosophila melanogaster. I. Cytology of the region and mutant complementation groups. Chromosoma 81:281–306.PubMedCrossRefGoogle Scholar
  87. 87.
    Segraves, W. A. 1994. Steroid receptors and other transcription factors in ecdysone response. Rec. Prog. Horm. Res. 49:167–194.PubMedGoogle Scholar
  88. 88.
    Jones, G., and P. A. Sharp. 1997. Ultraspiracle: An invertebrate nuclear receptor for juvenile hormones. Proc. Natl. Acad. Sci. USA 94:13499–13503.PubMedCrossRefGoogle Scholar
  89. 89.
    Xu, J., Y. Qiu, F. J. DeMayo, S. Y. Tsai, M.-J. Tsai, and B. W. O’Malley. 1998. Partial hormone resistance in mice with disruption of the steroid receptor coactivator-1 (SRC-1) gene. Science 279:1922–1925.PubMedCrossRefGoogle Scholar
  90. 90.
    Heery, D. M., E. Kalkhoven, S. Hoare, and M. G. Parker. 1997. A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature 387:733–736.PubMedCrossRefGoogle Scholar
  91. 91.
    Torchia, J., D. W. Rose, J. Inostroza, Y. Kamei, S. Westin, C. K. Glass, and M. G. Rosenfeld. 1997. The transcriptional co-activator p/CIP binds CBP and mediates nuclear-receptor function. Nature 387:677–684.PubMedCrossRefGoogle Scholar
  92. 92.
    Jones, G. 1995. Molecular mechanisms of action of juvenile hormone. Annu. Rev. Entomol. 40:147–169.PubMedCrossRefGoogle Scholar
  93. 93.
    Feyereisen, R. 1999. Insect P450 enzymes. Annu. Rev. Entomol. 44:507–533.PubMedCrossRefGoogle Scholar
  94. 94.
    Emmons, R. B., D. D., P. A. Estes, P. Kiefel, J. T. Mosher, M. Sonnenfeld, M. P. Ward, I. Duncan, and S. T. Crews. 1999. The Drosophila spineless-aristapedia and tango bHLH-PAS proteins interact to control antennal and tarsal development. Development 126:3937–3945.PubMedGoogle Scholar
  95. 95.
    Butler, R. a., M. L. Kelley, W. H. Powell, M. E. Hahn, and R. J. Van Beneden. 2001. An aryl hydrocarbon receptor (AHR) homologue from the soft-shell clam, Mya arenaria: evidence that invertebrate AHR homologues lack 2,3,7,8-tetrachlorodibenzo-p-dioxin and β-naphthoflavone binding. Gene 278:223–234.PubMedCrossRefGoogle Scholar
  96. 96.
    Hahn, M. E., S. I. Karchner, M. A. Shapiro, and S. A. Perera. 1997. Molecular evolution of two vertebrate aryl hydrocarbon (dioxin) receptors (AHR1 and AHR2) and the PAS family. Proc. Natl. Acad. Sci. USA 94:13743–13748.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2003

Authors and Affiliations

  • Thomas G. Wilson
    • 1
  1. 1.The Ohio State UniversityColumbusUSA

Personalised recommendations