Spatial, temporal, and sexually dimorphic expression patterns of the fruitless gene in the Drosophila central nervous system

Journal of Neurobiology

Volumn 43, Issue 4, 2000, Pages 404-426

  Lee, Gyunghee ^a   Foss, Margit ^b   Goodwin, Stephen F ^a,c   Carlo, Troy ^a   Taylor, Barbara J ^b   Hall, Jeffrey C ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b OREGON STATE UNIVERSITY   (United States)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

fru mutants; FRU proteins; fruitless mRNA; Larval, pupal, and adult CNS; Neural expression; Sexual dimorphisms

Indexed keywords

ANIMAL BEHAVIOR; ARTICLE; CENTRAL NERVOUS SYSTEM FUNCTION; DROSOPHILA; GENE EXPRESSION SYSTEM; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NONHUMAN; PRIORITY JOURNAL; SEX DIFFERENCE; TISSUE DISTRIBUTION;

ANIMALS; DNA, RECOMBINANT; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION; LARVA; MALE; NERVE TISSUE PROTEINS; NEURONS; PROTEIN ISOFORMS; PUPA; RNA, MESSENGER; SEX CHARACTERISTICS; TIME FACTORS; TISSUE DISTRIBUTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 0034659925     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/1097-4695(20000615)43:4<404::AID-NEU8>3.0.CO;2-D     Document Type: Article

References (42)

1. Albagli O, Dhordain P, Deweindt C, Lecocq G, 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. Arthur BI Jr, Jallon JM, Caflisch B, Choffat Y, Nöthiger R. 1998. Sexual behaviour in Drosophila is irreversibly programmed during a critical period. Curr Biol 8:1187-1190.
3. Bainbridge SP, Bownes M. 1981. Staging the metamorphosis of Drosophila melanogaster. J Embryol Exp Morphol 66:57-80.
4. Belote JM, Baker BS. 1987. Sexual behavior: its genetic control during development and adulthood in Drosophila melanogaster. Proc Natl Acad Sci USA 84:8026-8030.
5. Bodenstein D. 1950. The postembryonic development of Drosophila. In: Demerec M, editor. Biology of Drosophila. New York: Wiley, p. 275-367.
6. Cook R. 1980. The extent of visual control in the courtship tracking of D. melanogaster. Biol Cybernet 37:41-51.
7. Currie DA, Bate M. 1995. Innervation is essential for the development and differentiation of a sex-specific adult muscle in Drosophila melanogaster. Development 121: 2549-2557.
8. Ferveur J-F, Greenspan R. 1998. Courtship behavior of brain mosaics in Drosophila. J Neurogenet 12:205-226.
9. Ferveur J-F, Störtkuhl KF, Stocker RF, Greenspan RJ. 1995. Genetic feminization of brain structures and changed sexual orientation in male Drosophila. Science 267:902-905.
10. Gailey DA, Hall JC. 1989. Behavior and cytogenetics of fruitless in Drosophila melanogaster: different courtship defects caused by separated, closely linked lesions. Genetics 121:773-785.
11. Gailey DA, Taylor BJ, Hall JC. 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.
12. Goodwin SF. 1999. Molecular neurogenetics of sexual differentiation and behaviour. Curr Opin Neurobiol 9:759-765.
13. Goodwin SF, Taylor BJ, Villella A, Foss M, Ryner LC, Baker BS, Hall JC. 2000. Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster. Genetics 154:725-745.
14. Greenspan RJ. 1995. Understanding the genetic construction of behavior. Sci Am 272(4):72-78.
15. Hall JC. 1978. Courtship among males due to a male-sterile mutation in Drosophila melanogaster. Behav Genet 8:125-141.
16. Hall JC. 1979. Control of male reproductive behavior by the central nervous system of Drosophila: dissection of a courtship pathway by genetic mosaics. Genetics 92:437-457.
17. Hall JC. 1994. The mating of a fly. Science 264:1702-1714.
18. Heinrichs V, Ryner LC, Baker BS. 1998. Regulation of sex-specific selection of fruitless 5′ splice sites by transformer and transformer-2. Mol Cell Biol 18:450-458.
19. Heisenberg M, Heusipp M, Wanke C. 1995. Structural plasticity in the Drosophila brain J Neurosci 15:1951-1960.
20. Hu S, Fambrough D, Atashi JR, Goodman CS, Crews ST. 1995. The Drosophila abrupt gene encodes a BTB-zinc finger regulatory protein that controls the specificity of neuromuscular connections. Genes Dev 9:2936-2948.
21. Ito H, Fujitani K, Usui K, Shimizu-Nishikawa K, Tanaka S, Yumamoto 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.
22. Joiner MIA, Griffith LC. 1997. CaM kinase II and visual input modulate memory formation in the neuronal circuit controlling courtship conditioning. J Neurosci 17: 9384-9391.
23. Kaneko M, Helfrich-Förster C, Hall JC. 1997. Spatial and temporal expression of the period and timeless genes in the developing nervous system of Drosophila: newly identified pacemaker candidates and novel features of clock-gene product cycling. J Neurosci 17:6745-6760.
24. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-683.
25. Lawrence PA, 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. Miller A. 1950. The internal anatomy and histology of the imago of Drosophila melanogaster. In: Demerec M, editor. Biology of Drosophila. New York: Wiley, p. 481-495.
27. O'Dell KM, Armstrong JD, Yang MY, Kaiser K. 1995. Functional dissection of the Drosophila mushroom bodies by selective feminization of genetically defined subcompartments. Neuron 15:55-61.
28. Pathak SC, Ghosh S. 1990. Neurosecretory cells in Diptera. Folia Morphol (Praha) 38:174-185.
29. Poulson DF. 1950. Histogenesis, organogenesis, and differentiation in the embryo of Drosophila melanogaster. In: Demerec M, editor. Biology of Drosophila. New York: Wiley, p. 168-270.
30. Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, Baker BS, Hall JC, Wasserman SA. 1996. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87:1079-1089.
31. Sakai T, lsono K, Tomaru M, Oguma Y. 1997. Light-affected male following behavior is involved in light-dependent mating in Drosophila melanogaster. Genes Genet Syst 72:275-281.
32. Schilcher Fv, Hall JC. 1979. Neural topography of courtship song in sex mosaics of Drosophila melanogaster. J. Comp Physiol A 129:85-95.
33. Sherrier DJ, VandenBosch KA. 1994. Localization of repetitive proline-rich proteins in the extracellular matrix of pea root nodules. Protoplasma 193:148-161.
34. Szabad J, Fajszi C. 1982. Control of female reproduction in Drosophila: genetic dissection using gynandromorphs. Genetics 100:61-78.
35. Tautz D, Pfeifle C. 1989. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98:81-85.
36. Taylor BJ, Knittel L. 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.
37. Taylor BJ, Villella A, Ryner LC, Baker BS, Hall JC. 1994. Behavioral and neurobiological implications of sex-determining factors in Drosophila. Dev Genet 15:275-296.
38. Tompkins L, Hall JC. 1983. Identification of brain sites controlling female receptivity in mosaics of Drosophila melanogaster. Genetics 103:179-199.
39. Truman JW. 1990. Metamorphosis of the central nervous system of Drosophila. J Neurobiol 21:1072-0184.
40. Villella A, Gailey DA, Berwald B, Ohshima S, Barnes PT, Hall JC. 1997. Extended reproductive roles of the fruitless gene in Drosophila melanogaster revealed by behavioral analysis of new fru mutants. Genetics 147:1107-1130.
41. Yao, K-M, Samson M-L, Reeves R, White K. 1993. Gene elav of Drosophila melanogaster: a prototype for neuronal-specific binding protein gene family that is conserved in flies and humans. J Neurobiol 24:723-739.
42. Zollman S, Godt D, Prive GG, Couderc J-L, Laski FA. 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.