Interaction between hormonal signaling pathways in Drosophila melanogaster as revealed by genetic interaction between Methoprene-tolerant and Broad-Complex

Genetics

Volumn 172, Issue 1, 2006, Pages 253-264

  Wilson, Thomas G ^a   Yerushalmi, Yoram ^c,d   Donnell, David M ^c,e   Restifo, Linda L ^b,c  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

^d University of Arizona   (United States)

^e UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METHOPRENE;

ARTICLE; CELL VIABILITY; CORRELATION ANALYSIS; DROSOPHILA MELANOGASTER; GENE CONSTRUCT; GENE FREQUENCY; GENE INTERACTION; GENE MUTATION; GENETIC COMPLEMENTATION; HORMONAL REGULATION; METAMORPHOSIS; NONHUMAN; OOCYTE DEVELOPMENT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WILD TYPE;

ALLELES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL SURVIVAL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION TEST; INSECTICIDE RESISTANCE; MALE; METAMORPHOSIS, BIOLOGICAL; METHOPRENE; MUTATION; OOGENESIS; OVARY; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; ZINC FINGERS;

DROSOPHILA MELANOGASTER; INSECTA;

EID: 33644769166     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.105.046631     Document Type: Article

References (87)

1. ADAM, G., N. PERRIMON and S. NOSELLI, 2003 The retinoic-like juvenile hormone controls the looping of left-right asymmetric organs in Drosophila. Development 130: 2397-2406.
2. APPEL, L. F., M. PROUT, R. ABU-SHUMAYS, A. HAMMOND, J. C. GARBE et al., 1993 The Drosophila Stubble-stubboid gene encodes an apparent transmembrane serine protease required for epithelial morphogenesis. Proc. Natl. Acad. Sci. USA 90: 4937-4941.
3. ASHBURNER, M., 1970 Effects of juvenile hormone on adult differentiation of Drosophila melanogaster. Nature 227: 187-189.
4. ASHBURNER, M., C. CHIHARA, P. MELTZER and G. RICHARDS, 1974 Temporal control of puffing activity in polytene chromosomes. Cold Spring Harbor Symp. Quant. Biol. 38: 655-662.
5. 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.
6. BAINBRIDGE, S. P., and M. BOWNES, 1981 Staging the metamorphosis of Drosophila melanogaster. J. Embryol. Exp. Morphol. 66: 57-80.
7. BAYER, C. A., B. HOLLEY and J.W. FRISTROM, 1996 A switch in broadcomplex zinc-finger isoform expression is regulated posttranscriptionally during the metamorphosis of Drosophila imaginal discs. Dev. Biol. 177: 1-14.
8. BAYER, C. A., L. VON KALM and J. W. FRISTROM, 1997 Relationships between protein isoforms and genetic functions demonstrate functional redundancy at the Broad-Complex during Drosophila metamorphosis. Dev. Biol. 187: 267-282.
9. BEATON, A. H., I. KISS, D. FRISTROM and J. W. FRISTROM, 1988 Interaction of the Stubble-stubboid locus and the Broad-Complex of Drosophila melanogaster. Genetics 120: 453-464.
10. BELYAEVA, E. S., M. G. AIZENZON, V. F. SEMESHIN, I. KISS, K. KOCZYA et al., 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.
11. BOWNES, M., and H. REMBOLD, 1987 The titre of juvenile hormone during the pupal and adult stages of the life cycle of Drosophila melanogaster. Eur. J. Biochem. 164: 709-712.
12. CONSOULAS, C., R. B. LEVINE and L. L. RESTIFO, 2005 The steroid hormone-regulated gene Broad-Complex is required for dendritic growth of motorneurons during metamorphosis of Drosophila. J. Comp. Neurol. 485: 321-337.
13. CROSSGROVE, K., C. A. BAYER, J. W. FRISTROM 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.
14. DENG, W.-M., and M. BOWNES, 1997 Two signalling pathways specify localised expression of the Broad-Complex in Drosophila eggshell patterning and morphogenesis. Development 124: 4639-4647.
15. DIBELLO, P. R., D. A. WITHERS, C. A. BAYER, J.W. FRISTROM and G. M. GUILD, 1991 The Drosophila Broad-Complex encodes a family of related, zinc finger-containing proteins. Genetics 129: 385-397.
16. DUBROVSKY, E. B., G. DRETZEN and M. BELLARD, 1994 The Drosophila Broad-Complex regulates developmental changes in transcription and chromatin structure of the 67B heat-shock gene cluster. J. Mol. Biol. 241: 353-362.
17. DUBROVSKY, E. B., V. A. DUBROVSKAYA, A. L. BILDERBACK and E. M. BERGER, 2000 The isolation of two juvenile hormone-inducible genes in Drosophila melanogaster. Dev. Biol. 224: 486-495.
18. DUBROVSKY, E. B., V. A. DUBROVSKAYA and E. M. BERGER, 2001 Selective binding of Drosophila BR-C isoforms to a distal regulatory element in the hsp23 promoter. Insect Biochem. Mol. Biol. 31: 1231-1239.
19. DUBROVSKY, E. B., V. A. DUBROVSKAYA and E. M. BERGER, 2004 Hormonal regulation and functional role of Drosophila E75A orphan nuclear receptor in the juvenile hormone signaling pathway. Dev. Biol. 268: 258-270.
20. DUNNE, J. C., V. KONDYLIS and C. RABOUILLE, 2002 Ecdysone triggers the expression of Golgi genes in Drosophila imaginal discs via Broad-Complex. Dev. Biol. 245: 172-186.
21. EMERY, I. F., V. BEDIAN and G. M. GUILD, 1994 Differential expression of Broad-Complex transcription factors may forecast distinct developmental tissue fates during Drosophila metamorphosis. Development 120: 3275-3287.
22. FLETCHER, J. C., and C. S. THUMMEL, 1995 The ecdysone-inducible Broad-Complex and E75 early genes interact to regulate target gene transcription and Drosophila metamorphosis. Genetics 141: 1025-1035.
23. GILBERT, L. I., N. A. GRANGER and R. M. ROE, 2000 The juvenile hormones: historical facts and speculations on future research directions. Insect Biochem. Mol. Biol. 30: 617-644.
24. GONZY, G., G. V. POKHOLKOVA, F. PERONNET, B. MUGAT, O. V. DEMAKOVA et al., 2002 Isolation and characterization of novel mutations of the Broad-Complex, a key regulatory gene of ecdysone induction in Drosophila melanogaster. Insect Biochem. Mol. Biol. 32: 121-132.
25. GOTWALS, P. J., and J. W. FRISTROM, 1991 Three neighboring genes interact with the Broad-Complex and the Stubble-stubbloid locus to affect imaginal disc morphogenesis in Drosophila. Genetics 127: 747-759.
26. GUAY, P. S., and G. M. GUILD, 1991 The ecdysone-induced puffing cascade in Drosophila salivary glands: a Broad-Complex early gene regulates intermolt and late gene transcription. Genetics 129: 169-175.
27. HALL, B. L., and C. S. THUMMEL, 1998 The RXR homolog Ultraspiracle is an essential component of the Drosophila ecdysone receptor. Development 125: 4709-4717.
28. HANDLER, A. M., 1982 Ecdysteroid titers during pupal and adult development in Drosophila melanogaster. Dev. Biol. 93: 73-82.
29. 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.
30. HENRICH, V. C., and N. E. BROWN, 1995 Insect nuclear receptors: A developmental and comparative perspective. Insect Biochem. Mol. Biol. 25: 881-897.
31. HODGETTS, R., W. C. CLARK, S. O'KEEFE, M. SCHOULS, K. CROSSGROVE et al., 1995 Hormonal induction of dopa decarboxylase in the epidermis of Drosophila is mediated by the Broad-Complex. Development 121: 3913-3922.
32. HUANG, R.-Y., and W. C. ORR, 1992 Broad-Complex function during oogenesis in Drosophila melanogaster. Dev. Genet. 13: 277-288.
33. JONES, G., 1995 Molecular mechanisms of action of juvenile hormone. Annu. Rev. Entomol. 40: 147-169.
34. KARIM, F. D., G. M. GUILD and C. S. THUMMEL, 1993 The Drosophila Broad-Complex plays a key role in controlling ecdysone-regulated gene expression at the onset of metamorphosis. Development 118: 977-988.
35. KING, R. C., 1970 Ovarian Development in Drosophila melanogaster. Academic Press, New York.
36. 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.
37. KUCHAROVA-MAHMOOD, S., I. RASKA, B. M. MECHLER and R. FARKAS, 2002 Temporal regulation of Drosophila salivary gland degeneration by the Broad-Complex transcription factors. J. Struct. Biol. 140: 67-78.
38. LEE, C.-Y., and E. H. BAEHRECKE, 2001 Steroid regulation of autophagic programmed cell death during development. Development 128: 1443-1455.
39. LINDSLEY, D. L., and G. G. ZIMM, 1992 The Genome of Drosophila melanogaster. Academic Press, New York.
40. LIU, E., and L. L. RESTIFO, 1998 Identification of a Broad Complexregulated enhancer in the developing visual system of Drosophila. J. Neurobiol. 34: 253-270.
41. MACKLER, J. M., and N. E. REIST, 2001 Mutations in the second C2 domain of synaptotagmin disrupt synaptic transmission at Drosophila neuromuscular junctions. J. Comp. Neurol. 436: 4-16.
42. MADHAVAN, K., 1973 Morphogenetic effects of juvenile hormone and juvenile hormone mimics on adult development of Drosophila. J. Insect Physiol. 19: 441-453.
43. MELNICK, A., G. CARLILE, K. F. AHMAD, C.-L. KIANG, C. CORCORAN et al., 2002 Critical residues within the BTB domain of PLZF and Bcl-6 modulate interaction with corepressors. Mol. Cell. Biol. 22: 1804-1818.
44. MIURA, K., M. ODA, S. MAKITA and Y. CHINZEI, 2005 Characterization of the Drosophila Methoprene-tolerant gene product. FEBS J. 272: 1169-1178.
45. MOORE, A. W., S. BARBEL, L. Y. JAN and Y. N. JAN, 2000 A genome-wide survey of basic helix-loop-helix factors in Drosophila. Proc. Natl. Acad. Sci. USA 97: 10436-10441.
46. MORGAN, T. H., C. BRIDGES and A. H. STURTEVANT, 1925 The genetics of Drosophila. Bibliogr. Genet. 2: 145.
47. MUGAT, B., V. BRODU, J. KEJZLAROVA-LEPESANT, C. ANTONIEWSKI, C.A. BAYER et al., 2000 Dynamic expression of broad-complex isoforms mediates temporal control of an ecdysteroid target gene at the onset of Drosophila metamorphosis. Dev. Biol. 227: 104-117.
48. POSTLETHWAIT, J. H., 1974 Juvenile hormone and the adult development of Drosophila. Biol. Bull. 147: 119-135.
49. 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.
50. RENAULT, N., K. KING-JONES and M. LEHMANN, 2001 Downregulation of the tissue-specific transcription factor Fork head by Broad-Complex mediates a stage-specfic response. Development 128: 3729-3737.
51. RESTIFO, L. L., and W. HAUGLUM, 1998 Parallel molecular genetic pathways operate during CNS metamorphosis in Drosophila. Mol. Cell. Neurosci. 11: 134-148.
52. RESTIFO, L. L., and V. K. MERRILL, 1994 Two Drosophila regulatory genes, Deformed and the Broad Complex, share common functions in development of adult CNS, head, and salivary glands. Dev. Biol. 162: 465-485.
53. 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.
54. RESTIFO, L. L., and K. WHITE, 1992 Mutations in a steroid hormone-regulated gene disrupt the metamorphosis of internal tissues in Drosophila: salivary glands, muscle, and gut. Roux's Arch. Dev. Biol. 201: 221-234.
55. 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.
56. RICHARDS, G., 1997 The ecdysone regulatory cascades in Drosophila. Adv. Dev. Biol. 5: 81-135.
57. RIDDIFORD, L. M., 1993 Hormones and Drosophila development, pp. 899-939 in The Development of Drosophila melanogaster, edited by M. Bate and A. Martinez Arias. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
58. RIDDIFORD, L. M., 1994 Cellular and molecular actions of juvenile hormone I. General considerations and premetamorphic actions. Adv. Insect Physiol. 24: 213-274.
59. RIDDIFORD, L. M., 1996 Molecular aspects of juvenile hormone action in insect metamorphosis, pp. 223-251 in Metamorphosis: Post-embryonic Reprogramming of Gene Expression in Amphibian and Insect Cells, edited by L. I. Gilbert, J. R. Tata and B. G. Atkinson. Academic Press, San Diego.
60. 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.
61. RIDDIFORD, L. M., J. W. TRUMAN and P. CHERBAS, 2000 Ecdysone receptors and their biological actions. Vitam. Horm. 60: 1-73.
62. SANDSTROM, D. J., C. A. BAYER, J. W. FRISTROM and L. L. RESTIFO, 1997 Broad-Complex transcription factors regulate thoracic muscle attachment in Drosophila. Dev. Biol. 181: 168-185.
63. SEMPERE, L. F., E. B. DUBROVSKY, V. A. DUBROVSKAYA, E. M. BERGER and V. AMBROS, 2002 The expression of the let-7 small regulatory RNA is controlled by ecdysone during metamorphosis in Drosophila melanogaster. Dev. Biol. 244: 170-179.
64. SEMPERE, L. F., N. S. SOKOL, E. B. DUBROVSKY, E. M. BERGER and V. AMBROS, 2003 Temporal regulation of microRNA expression in Drosophila melanogaster mediated by hormonal signals and Broad-Complex gene activity. Dev. Biol. 259: 9-18.
65. 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.
66. 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.
67. SLITER, T. J., B. J. SEDLAK, F. C. BAKER and P. A. SCHOOLEY, 1987 Juvenile hormone in Drosophila melanogaster. Identification and titer determination during development. Insect Biochem. 17: 161-165.
68. SOLLER,M., M. BOWNES and E. KUBLI, 1999 Control of oocyte maturation in sexually mature Drosophila females. Dev. Biol. 208: 337-351.
69. SPINDLER, K.-D., S. PRZIBILLA and M. SPINDLER-BARTH, 2001 Moulting hormones of arthropods: molecular mechanisms. Zoology 103: 189-201.
70. STAAL, G. B., 1975 Insect growth regulators with juvenile hormone activity. Annu. Rev. Entomol. 20: 417-460.
71. THUMMEL, C. S., and J. CHORY, 2002 Steroid signaling in plants and insects-common themes, different pathways. Genes Dev. 16: 3113-3129.
72. TOWBIN, H., T. STAEHELIN and J. GORDON, 1979 Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76: 4350-4354.
73. TZOLOVSKY, G., W. M. DENG, T. SCHLITT and M. BOWNES, 1999 The function of the Broad-Complex during Drosophila melanogaster oogenesis. Genetics 153: 1371-1383.
74. VON KALM, L., K. CROSSGROVE, D. VON SEGGERN, G. M. GUILD and S. K. BECKENDORF, 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.
75. WARD, R. E., J. EVANS and C. S. THUMMEL, 2003 Genetic modifer screens in Drosophila demonstrate a role for Rho1 signaling in ecdysone-triggered imaginal disc morphogenesis. Genetics 165: 1397-1415.
76. WILLIAMS, C. M., 1961 The juvenile hormone. II. Its role in the endocrine control of molting, pupation, and adult development in the Cecropia silkworm. Biol. Bull. 121: 572-585.
77. 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.
78. WILSON, T. G., 1996 Genetic evidence that mutants of the Methoprene-tolerant gene of Drosophila melanogaster are null mutants. Arch. Insect Biochem. Physiol. 32: 641-649.
79. WILSON, T. G., 2004 The molecular site of action of juvenile hormone and juvenile hormone insecticides during metamorphosis: how these compounds kill insects. J. Insect Physiol. 50: 111-121.
80. WILSON, T. G., and M. ASHOK, 1998 Insecticide resistance resulting from an absence of target-site gene product. Proc. Natl. Acad. Sci. USA 95: 14040-14044.
81. WILSON, T. G., and J. FABIAN, 1986 A Drosophila melanogaster mutant resistant to a chemical analog of juvenile hormone. Develop. Biol. 118: 190-201.
82. WILSON, T. G., and J. FABIAN, 1987 Selection of methoprene-resistant mutants of Drosophila melanogaster, pp. 179-188 in Molecular Entomology, edited by J. Law. UCLA Symposia on Molecular and Cellular Biology, New Series, Los Angeles.
83. 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.
84. XU, L., C. K. GLASS and M. G. ROSENFELD, 1999 Coactivator and corepressor complexes in nuclear receptor function. Curr. Opin. Genet. Dev. 9: 140-147.
85. ZHOU, B., K. HIRUMA, T. SHINODA and L. M. RIDDIFORD, 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.
86. 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.
87. ZOLLMAN, S., D. GODT, G. G. PRIVE, J.-L. COUDERC and F. A. LASKI, 1994 The BTB domain, found primarily in zinc finger proteins, defines an evolutionarily conserved family that includes several developmentally regulated genes in Drosophila. Proc. Natl. Acad. Sci. USA 91: 10717-10721.