Genes expressed in the Drosophila head reveal a role for fat cells in sex-specific physiology

EMBO Journal

Volumn 21, Issue 20, 2002, Pages 5353-5363

  Fujii, Shinsuke ^a   Amrein, Hubert ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Drosophila; Fat cells; Mating behavior; SAGE; Sex specific genes

Indexed keywords

PROTEIN DERIVATIVE; PROTEIN FIT; PROTEIN SXE1; PROTEIN SXE2; PROTEIN TSX; UNCLASSIFIED DRUG;

ADIPOCYTE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; DROSOPHILA; FEMALE; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; HEAD; MALE; MATING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEX DETERMINATION; SEX DIFFERENTIATION;

ADIPOCYTES; ANIMALS; BRAIN; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; HEAD; IN SITU HYBRIDIZATION; MALE; NUCLEAR PROTEINS; RNA; SEX DETERMINATION (GENETICS); SEX DIFFERENTIATION; SEXUAL BEHAVIOR, ANIMAL;

ANIMALIA; ARACHNIDA; EUKARYOTA; HEXAPODA; SALVIA;

EID: 0037107446     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdf556     Document Type: Article

References (58)

1. Abrahamsen, N., Martinez, A., Kjaer, T., Sondergaard, L. and Bownes, M. (1993) Cis-regulatory sequences leading to female-specific expression of yolk protein genes 1 and 2 in the fat body of Drosophila melanogaster. Mol. Gen. Genet., 237, 41-48.
2. Adams, M.D. et al. (2000) The genome sequence of Drosophila melanogaster. Science, 287, 2185-2195.
3. Amrein, H. and Axel, R. (1997) Genes expressed in neurons of adult male Drosophila. Cell, 88, 459-469.
4. Amrein, H., Gorman, M. and Nöthiger, R. (1988) The sex-determining gene tra-2 of Drosophila encodes a putative RNA binding protein. Cell, 55, 1025-1035.
5. An, W. and Wensink, P.C. (1995a) Integrating sex- and tissue-specific regulation within a single Drosophila enhancer. Genes Dev., 9, 256-266.
6. An, W. and Wensink, P.C. (1995b) Three protein binding sites form an enhancer that regulates sex- and fat body-specific transcription of Drosophila yolk protein genes. EMBO J., 14, 1221-1230.
7. Baker, B.S. and Ridge, K.A. (1980) Sex and the single cell. I. On the action of major loci affecting sex determination in Drosophila melanogaster. Genetics, 94, 383-423.
8. Baker, B.S., Taylor, B.J. and Hall, J.C. (2001) Are complex behaviors specified by dedicated regulatory genes? Reasoning from Drosophila. Cell, 105, 13-24.
9. Bashaw, G.J. and Baker, B.S. (1995) The msl-2 dosage compensation gene of Drosophila encodes a putative DNA-binding protein whose expression is sex specifically regulated by Sex-lethal. Development, 121, 3245-3258.
10. Bell, L.R., Maine, E.M., Schedl, P. and Cline, T.W. (1988) Sex-lethal, a Drosophila sex determination switch gene, exhibits sex-specific RNA splicing and sequence similarity to RNA binding proteins. Cell, 55, 1037-1046.
11. Bell, L.R., Horabin, J.I., Schedl, P. and Cline, T.W. (1991) Positive autoregulation of sex-lethal by alternative splicing maintains the female determined state in Drosophila. Cell, 65, 229-239.
12. Belote, J.M. and Baker, B.S. (1987) Sexual behavior: Its genetic control during development and adulthood in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA, 84, 8026-8030.
13. Brand, A.H. and Perrimon, N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development, 118, 401-415.
14. Burtis, K.C. (1993) The regulation of sex determination and sexually dimorphic differentiation in Drosophila. Curr. Opin. Cell Biol., 5, 1006-1014.
15. Burtis, K.C. and Baker, B.S. (1989) Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell, 56, 997-1010.
16. Burtis, K.C., Coschigano, K.T., Baker, B.S. and Wensink, P.C. (1991) The doublesex proteins of Drosophila melanogaster bind directly to a sex-specific yolk protein gene enhancer. EMBO J., 10, 2577-2582.
17. Butterworth, F.M., Bownes, M. and Burde, V.S. (1991) Genetically modified yolk proteins precipitate in the adult Drosophila fat body. J. Cell Biol., 112, 727-737.
18. Butterworth, F.M., Burde, V.S., Mauchline, D. and Bownes, M. (1999) A yolk protein mutant leads to defects in the secretion machinery of Drosophila melanogaster. Tissue Cell, 31, 212-222.
19. Chase, B.A. and Baker, B.S. (1995) A genetic analysis of intersex, a gene regulating sexual differentiation in Drosophila melanogaster females. Genetics, 139, 1649-1661.
20. Chavez, V.M., Marques, G., Delbecque, J.P., Kobayashi, K., Hollingsworth, M., Burr, J., Natzle, J.E. and O'Connor, M.B. (2000) The Drosophila disembodied gene controls late embryonic morphogenesis and codes for a cytochrome P450 enzyme that regulates embryonic ecdysone levels. Development, 127, 4115-4126.
21. Childress, D. (1973) The inter- and intrachromosomal effects of the bar-stone translocation in Drosophila melanogaster. Mol. Gen. Genet., 121, 133-138.
22. Cline, T.W. and Meyer, B.J. (1996) Vive la difference: Males vs females in flies vs worms. Annu. Rev. Genet., 30, 637-702.
23. Conley, A. and Hinshelwood, M. (2001) Mammalian aromatases. Reproduction, 121, 685-695.
24. Coschigano, K.T. and Wensink, P.C. (1993) Sex-specific transcriptional regulation by the male and female doublesex proteins of Drosophila. Genes Dev., 7, 42-54.
25. Erdman, S.E. and Burtis, K.C. (1993) The Drosophila doublesex proteins share a novel zinc finger related DNA binding domain. EMBO J., 12, 527-535.
26. Finley, K.D., Taylor, B.J., Milstein, M. and McKeown, M. (1997) dissatisfactions, a gene involved in sex-specific behavior and neural development of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA, 94, 913-918.
27. Finley, K.D., Edeen, P.T., Foss, M., Gross, E., Ghbeish, N., Palmer, R.H., Taylor, B.J. and McKeown, M. (1998) Dissatisfaction encodes a tailless-like nuclear receptor expressed in a subset of CNS neurons controlling Drosophila sexual behavior. Neuron, 21, 1363-1374.
28. Fisher, C.R., Graves, K.H., Parlow, A.F. and Simpson, E.R. (1998) Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. Proc. Natl. Acad. Sci. USA, 95, 6965-6970.
29. Galindo, K. and Smith, D.P. (2001) A large family of divergent Drosophila odorant-binding proteins expressed in gustatory and olfactory sensilla. Genetics, 159, 1059-1072.
30. Garabedian, M.J., Shirras, A.D., Bownes, M. and Wensink, P.C. (1987) The nucleotide sequence of the gene coding for Drosophila melanogaster yolk protein 3. Gene, 55, 1-8.
31. Goralski, T.J., Edstrom, J.E. and Baker, B.S. (1989) The sex determination locus transformer-2 of Drosophila encodes a polypeptide with similarity to RNA binding proteins. Cell, 56, 1011-1018.
32. Grieneisen, M.L., Warren, J.T. and Gilbert, L.I. (1993) Early steps in ecdysteroid biosynthesis: Evidence for the involvement of cytochrome P-450 enzymes. Insect Biochem. Mol. Biol., 23, 13-23.
33. Helfrich-Forster, C., Winter, C., Hofbauer, A., Hall, J.C. and Stanewsky, R. (2001) The circadian clock of fruit flies is blind after elimination of all known photoreceptors. Neuron, 30, 249-261.
34. Inoue, K., Hoshijima, K., Sakamoto, H. and Shimura, Y. (1990) Binding of the Drosophila sex-lethal gene product to the alternative splice site of transformer primary transcript. Nature, 344, 461-463.
35. Kelley, R.L., Solovyeva, I., Lyman, L.M., Richman, R., Solovyev, V. and Kuroda, M.I. (1995) Expression of msl-2 causes assembly of dosage compensation regulators on the X chromosomes and female lethality in Drosophila. Cell, 81, 867-877.
36. Li, H. and Baker, B.S. (1998) Her, a gene required for sexual differentiation in Drosophila, encodes a zinc finger protein with characteristics of ZFY-like proteins and is expressed independently of the sex determination hierarchy. Development, 125, 225-235.
37. Mayer, R.T., Svoboda, J.A. and Weirich, G.F. (1978) Ecdysone 20-hydroxylase in midgut mitochondria of Manduca sexta (L.). Hoppe Seyler's Z. Physiol. Chem., 359, 1247-1257.
38. McDonald, M.J. and Rosbash, M. (2001) Microarray analysis and organization of circadian gene expression in Drosophila. Cell, 107, 567-578.
39. McKeown, M. (1994) Sex determination and differentiation. Dev. Genet., 15, 201-204.
40. McKeown, M., Belote, J.M. and Baker, B.S. (1987) A molecular analysis of transformer, a gene in Drosophila melanogaster that controls female sexual differentiation. Cell, 48, 489-499.
41. Mitsui, T. and Riddiford, L.M. (1978) Hormonal requirements for the larval-pupal transformation of the epidermis of Manduca sexta in vitro. Dev. Biol., 62, 193-205.
42. Nagoshi, R.N. and Baker, B.S. (1990) Regulation of sex-specific RNA splicing at the Drosophila doublesex gene: Cis-acting mutations in exon sequences alter sex-specific RNA splicing patterns. Genes Dev., 4, 89-97.
43. Nayak, S.V. and Singh, R.N. (1983) Sensilla on the tarsal segments and the mouthparts of adult Drosophila melanogaster. Int. J. Insect Morphol. Embryol., 12, 273-291.
44. Nöthiger, R., Leuthold, M., Anderesen, N., Gerschwiler, P., Grueter, A., Keller, W., Leist, C., Roost, M. and Schmid, H. (1987) Genetic and developmental analysis of the sex-determining gene doublesex (dsx) of Drosophila melanogaster. Genet. Res., 50, 113-123.
45. Pikielny, C.W., Hasan, G., Rouyer, F. and Rosbash, M. (1994) Members of a family of Drosophila putative odorant-binding proteins are expressed in different subsets of olfactory hairs. Neuron, 12, 35-49.
46. Riddiford, L.M. (1993) Hormone receptors and the regulation of insect metamorphosis. Receptor, 3, 203-209.
47. Roselli, C.E. and Resko, J.A. (1997) Sex differences in androgen-regulated expression of cytochrome P450 aromatase in the rat brain. J. Steroid Biochem. Mol. Biol., 61, 365-374.
48. Ryner, L.C., Goodwin, S.F., Castrillon, D.H., Anand, A., Villella, A., Baker, B.S., Hall, J.C., Taylor, B.J. and Wasserman, S.A. (1996) Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell, 87, 1079-1089.
49. Salz, H.K., Maine, E.M., Keyes, L.N., Samuels, M.E., Cline, T.W. and Schedl, P. (1989) The Drosophila female-specific sex-determination gene, Sex-lethal, has stage-, tissue- and sex-specific RNAs suggesting multiple modes of regulation. Genes Dev., 3, 708-719.
50. Schaeren-Wiemers, N. and Gerfin-Moser, A. (1993) A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: In situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry, 100, 431-440.
51. Schoentgen, F. and Jolles, P. (1995) From structure to function: Possible biological roles of a new widespread protein family binding hydrophobic ligands and displaying a nucleotide binding site. FEBS Lett., 369, 22-26.
52. Shirk, P.D., Minoo, P. and Postlethwait, J.H. (1983) 20-Hydroxyecdysone stimulates the accumulation of translatable yolk polypeptide gene transcript in adult male Drosophila melanogaster. Proc. Natl. Acad. Sci. USA, 80, 186-190.
53. Smith, S.L., Bollenbacher, W.E., Cooper, D.Y., Schleyer, H., Wielgus, J.J. and Gilbert, L.I. (1979) Ecdysone 20-monooxygenase: Characterization of an insect cytochrome p-450 dependent steroid hydroxylase. Mol. Cell. Endocrinol., 15, 111-133.
54. Sosnowski, B.A., Belote, J.M. and McKeown, M. (1989) Sex-specific alternative splicing of RNA from the transformer gene results from sequence-dependent splice site blockage. Cell, 58, 449-459.
55. Sudhof, T.C., Baumert, M., Perin, M.S. and Jahn, R. (1989) A synaptic vesicle membrane protein is conserved from mammals to Drosophila. Neuron, 2, 1475-1481.
56. Valcarcel, J., Singh, R., Zamore, P.D. and Green, M.R. (1993) The protein Sex-lethal antagonizes the splicing factor U2AF to regulate alternative splicing of transformer pre-mRNA. Nature, 362, 171-175.
57. Velculescu, V.E., Zhang, L., Vogelstein, B. and Kinzler, K.W. (1995) Serial analysis of gene expression. Science, 270, 484-487.
58. Zhou, S. et al. (1995) Male-specific lethal 2, a dosage compensation gene of Drosophila, undergoes sex-specific regulation and encodes a protein with a RING finger and a metallothionein-like cysteine cluster. EMBO J., 14, 2884-2895.