Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene

Cell

Volumn 87, Issue 6, 1996, Pages 1079-1089

  Ryner, Lisa C ^a   Goodwin, Stephen F ^b   Castrillon, Diego H ^c,e   Anand, Anuranjan ^a   Villella, Adriana ^b   Baker, Bruce S ^a   Hall, Jeffrey C ^b   Taylor, Barbara J ^d   Wasserman, Steven A ^c  

^a STANFORD UNIVERSITY   (United States)

^b BRANDEIS UNIVERSITY   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d OREGON STATE UNIVERSITY   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; TRANSCRIPTION FACTOR;

ALTERNATIVE RNA SPLICING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; COURTSHIP; DNA SEQUENCE; DROSOPHILA; FEMALE; GENETIC REGULATION; MALE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SEX DIFFERENTIATION; SEXUAL BEHAVIOR; SEXUAL ORIENTATION;

ANIMALIA;

EID: 0030582732     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81802-4     Document Type: Article

References (46)

1. Albagli, O., Dhordain, P., Deweindt, C., Lecocq, G., and Leprince, D. (1995). The BTB/POZ domain: a new protein-protein interaction motif common to DNA- and actin-binding proteins. Cell Growth Differ. 6, 1193-1198.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
3. Banfi, S., Borsani, G., Rossi, E., Bernard, L., Guffanti, A., Rubboli, F., Marchitiello, A., Giglio, S., Coluccia, E., Zolla, M., Zuffardi, O., and Ballabio, A. (1996). Identification and mapping of human cDNAs homologous to Drosophila mutant genes through EST database searching. Nature Genet. 13, 167-174.
4. 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.
5. Breedlove, S.M. (1992). Sexual dimorphism in the vertebrate nervous system. J. Neurosci. 12, 4133-4142.
6. Breedlove, S.M. (1994). Sexual differentiation of the human nervous system. Annu. Rev. Psychol. 45, 389-418.
7. Burrows, M. (1992). Local circuits for the control of leg movements in an insect. Trends Neurosci. 15, 226-232.
8. Burtis, K.C. (1993). The regulation of sex determination and sexually dimorphic differentiation in Drosophila. Curr. Opin. Cell Biol. 5, 1006-1014.
9. 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.
10. Castrillon, D.H., Gönczy, P., Alexander, S., Rawson, R., Eberhart, G.G., Viswanathan, S., DiNardo, S., and Wasserman, S.A. (1993). Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: characterization of male-sterile mutants generated by single P element mutagenesis. Genetics 135, 489-505.
11. Dauwalder, B., Amaya-Manzanares, F., and Mattox, W. (1996). A human homologue of the Drosophila sex determination factor transformer-2 has conserved splicing regulatory functions. Proc. Natl. Acad. Sci. USA 93, 9004-9009.
12. DiAntonio, A., Burgess, R.W., Chin, A.C., Deitcher, D.L., Scheller, R.H., and Schwarz, T.L. (1993). Identification and characterization of Drosophila genes for synaptic vesicle proteins. J. Neurosci. 13, 4924-4935.
13. Emery, I.F., Bedian, V., and Guild, G.M. (1994). Differential expression of Broad-Complex transcription factors may forecast tissue-specific developmental fates during Drosophila metamorphosis. Development 120, 3275-3287.
14. Gailey, D.A., Taylor, B.J., and Hall, J.C. (1991). Elements of the fruitless locus regulate development of the muscle of Lawrence, a male-specific structure in the abdomen of Drosophila melanogaster adults. Development 113, 879-890.
15. Greenspan, R.J. (1995). Understanding the genetic construction of behavior. Sci. Am. 272(4), 74-79.
16. Hall, J.C. (1994). The mating of a fly. Science 264, 1702-1714.
17. Hamblen-Coyle, M., Konopka, R.J., Zwiebel, L.J., Colot, H.V., Dowse, H.B., Rosbash, M., and Hall, J.C. (1989). A new mutation at the period locus of Drosophila melanogaster with some novel effects on circadian rhythms. J. Neurogenet. 5, 229-256.
18. Heisenberg, M. (1994). Central brain function in insects: genetic studies on the mushroom bodies and central complex in Drosophila. In Neural Basis of Behavioral Adaptations, K. Schildberger and N. Elsner, eds. (Stuttgart, Germany: Gustav Fischer Verlag), 61-79.
19. Heisenberg, M., Heusip, M., and Wanke, C. (1995). Structural plasticity in the Drosophila brain. J. Neurosci. 15, 1951-1960.
20. Hing, A.L.Y., and Carlson, J.R. (1996). Male-male courtship behavior induced by ectopic expression of the Drosophila white gene: role of sensory function and age. J. Neurobiol. 30, 454-464.
21. Hu, S., Fambrough, D., Atashi, J.R., Goodman, C.S., and Crews, S.T. (1995a). The Drosophila abrupt gene encodes a BTB-zinc finger regulatory protein that controls the specificity of neuromuscular connections. Genes Dev. 9, 2936-2948.
22. Hu, S., Pattatucci, A.M.L., Patterson, C., Li, L., Fulker, D.W., Cherny, S.S., Kruglyak, L., and Hamer, D.H. (1995b). Linkage between sexual orientation and chromosome Xq28 in males but not in females. Nature Genet. 11, 248-256.
23. Ito, H., Fujitani, K., Usui, K., Shimizu-Nishikawa, K., Tanaka, S., and Yamamoto, D. (1996). Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. Proc. Natl. Acad. Sci. USA 93, 9687-9692.
24. Kulkarni, S.J., and Hall, J.C. (1987). Behavioral and cytogenetic analysis of the cacophony courtship song mutant and interacting genetic variants in Drosophila melanogaster. Genetics 115, 461-475.
25. Lawrence, P.A., and Johnston, P. (1986). The muscle pattern of a segment of Drosophila may be determined by neurons and not by contributing myoblasts. Cell 45, 505-513.
26. LeVay, S. (1996). Queer Science. (Cambridge, Massachusetts: MIT Press).
27. Maniatis,T., Hardison, R.C., Lacy, E., Lauer, J., O'Connell, C., Quon, D., Sim, G.K., and Estratiadis, A. (1978). The isolation of structural genes from libraries of eukaryotic DNA. Cell 15, 687-701.
28. Matsuo, N., Ogawa, S., Imai, Y., Takagi, T., Tohyama, M., Stern, D., and Wanaka, A. (1995). Cloning of a novel RNA binding polypeptide (RA301) induced by hypoxia/reoxygenation. J. Biol. Chem. 270, 28216-28222.
29. McKeown, M. (1994). Sex determination and differentiation. Dev. Genet. 15, 201-204.
30. O'Connell, P., and Rosbash, M. (1984). Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene. Nucl. Acids Res. 12, 5495-5513.
31. Perkins, A., Fitzgerald, J.A., and Moss, G.E. (1995). A comparison of LH secretion and brain estradiol receptors in heterosexual and homosexual rams and female sheep. Horm. Behav. 29, 31-41.
32. Pirrotta, V. (1986). Cloning Drosophila genes. In Drosophila: A Practical Approach. D.B. Roberts, ed. (Oxford: IRL Press).
33. Read, D., Levine, M., and Manley, J.L. (1992). Ectopic expression of the Drosophila tramtrack gene results in multiple embryonic defects, including repression of even-skipped and fushi tarazu. Mech. Dev. 38, 183-196.
34. Read, D., and Manley, J.L. (1992). Alternatively spliced transcripts of the Drosophila tramtrack gene encode zinc finger proteins with distinct DNA binding specificities. EMBO J. 11, 1035-1044.
35. Ryner, L.C., and Swain, A. (1995). Sex in the '90s. Cell 81, 483-493.
36. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press).
37. Segade, F., Hurle, B., Claudio, E., Ramos, S., and Lazo, P.S. (1996). Molecular cloning of a mouse homologue for the Drosophila splicing regulator Tra-2. FEBS Lett. 387, 152-156.
38. Stocker, R.F. (1994). The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res. 275, 3-26.
39. Swaab, D.F., and Hofman, M.A. (1995). Sexual differentiation of the human hypothalamus in relation to gender and sexual orientation. Trends Neurosci. 18, 264-270.
40. Tamkun, J.W., Deuring, R., Scott, M.P., Kissinger, M., Pattatucci, A.M., Kaufman, T.C., and Kennison, J.A. (1992). brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68, 561-572.
41. Taylor, B.J. (1992). Differentiation of a male-specific muscle in Drosophila melanogaster does not require the sex-determining genes doublesex or intersex. Genetics 132, 179-191.
42. Taylor, B.J., and Knittel, L.M. (1995). Sex-specific differentiation of a male-specific abdominal muscle, the Muscle of Lawrence, is abnormal in hydroxyurea-treated and in fruitless male flies. Development 121, 3079-3088.
43. Taylor, B.J., Villella, A., Ryner, L.C., Baker, B.S., and Hall, J.C. (1994). Behavioral and neurobiological implications of sex-determining factors in Drosophila. Dev. Genet. 15, 275-296.
44. Villella, A., and Hall, J.C. (1996). Courtship anomalies caused by doublesex mutations in Drosophila melanogaster. Genetics 143, 331-344.
45. von Kalm, L., Crossgrove, K., Von Seggern, D., Guild, G.M., and Beckendorf, S.K. (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.
46. Zhang, S.-D., and Odenwald, W.F. (1995). Misexpression of the white (w) gene triggers male-male courtship in Drosophila. Proc. Natl. Acad. Sci. USA 92, 5525-5529.