The transformer2 gene in Musca domestica is required for selecting and maintaining the female pathway of development

Development Genes and Evolution

Volumn 215, Issue 4, 2005, Pages 165-176

  Burghardt, Géza ^a   Hediger, Monika ^a   Siegenthaler, Christina ^a   Moser, Martin ^a   Dübendorfer, Andreas ^a   Bopp, Daniel ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Musca domestica; Sex determination; Splicing regulation; Transformer2

Indexed keywords

DOUBLE STRANDED RNA; REGULATOR PROTEIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COURTSHIP; DROSOPHILA; EMBRYO; FEMALE; GENE ACTIVITY; GENE EXPRESSION; GENE FUNCTION; GENE ISOLATION; GENOTYPE; HOUSE FLY; INSECT DEVELOPMENT; MALE; NONHUMAN; PRIORITY JOURNAL; REPRODUCTION; RNA SPLICING; SEQUENCE HOMOLOGY; SEXUAL DEVELOPMENT;

AMINO ACID SEQUENCE; ANIMALS; BEHAVIOR, ANIMAL; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REGULATOR; HOUSEFLIES; IN SITU HYBRIDIZATION; INSECT PROTEINS; MICROINJECTIONS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; RIBONUCLEOPROTEINS; RNA; RNA SPLICING; SELECTION (GENETICS); SEQUENCE HOMOLOGY, AMINO ACID; SEX DETERMINATION (GENETICS); SEX REVERSAL, GONADAL; VARIATION (GENETICS);

EID: 17544363338     PISSN: 0949944X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00427-004-0464-7     Document Type: Article

References (55)

1. Amrein H, Gorman M, Nöthiger R (1988) The sex-determining gene tra-2 of Drosophila encodes a putative RNA binding protein (published erratum appears in Cell 1989 Jul 28; 58(2) :fOllowing 419). Cell 55:1025-1035
2. Amrein H, Maniatis T, Nöthiger R (1990) Alternatively spliced transcripts of the sex-determining gene tra-2 of Drosophila encode functional proteins of different size. EMBO J 9:3619-3629
3. Amrein H, Hedley ML, Maniatis T (1994) The role of specific protein-RNA and protein-protein interactions in positive and negative control of pre-mRNA splicing by Transformer 2. Cell 76:735-746
4. Baker BS, Wolfner MF (1988) A molecular analysis of doublesex, a bifunctional gene that controls both male and female sexual differentiation in Drosophila melanogaster. Genes Dev 2:477-489 1:CAS:528:DyaL1cXktlejt74%3D
5. Beil B, Screaton G, Stamm S (1997) Molecular cloning of htra2-beta-1 and htra2-beta-2, two human homologs of tra-2 generated by alternative splicing. DNA Cell Biol 16:679-690
6. Bell LR, Horabin JI, Schedl P, Cline TW (1991) Positive autoregulation of Sex-lethal by alternative splicing maintains the female determined state in Drosophila. Cell 65:229-239
7. Burtis KC, Baker BS (1989) Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 56:997-1010 10.1016/ 0092-8674(89)90633-8
8. Chandler D, McGuffin ME, Piskur J, Yao J, Baker BS, Mattox W (1997) Evolutionary conservation of regulatory strategies for the sex determination factor transformer-2. Mol Cell Biol 17:2908-2919
9. Cline TW, Meyer BJ (1996) Vive la différence: Males vs females in flies vs worms. Annu Rev Genet 30:637-702 10.1146/annurev.genet.30.1.637
10. Dauwalder B, Amaya-Manzanares F, 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
11. Dubendorfer A, Hediger M (1998) The female-determining gene F of the housefly, Musca domestica, acts maternally to regulate its own zygotic activity. Genetics 150:221-226
12. Dubendorfer A, Hediger M, Burghardt G, Bopp D (2002) Musca domestica, a window on the evolution of sex-determining mechanisms in insects. Int J Dev Biol 46:75-79
13. Fortier E, Belote JM (2000)Temperature-dependent gene silencing by an expressed inverted repeat in Drosophila. Genesis 26:240-244
14. Goralski TJ, Edstrom JE, Baker BS (1989) The sex determination locus transformer-2 of Drosophila encodes a polypeptide with similarity to RNA binding proteins. Cell 56:1011-1018
15. Hall JC (1994) The mating of a fly. Science 264:1702-1714
16. Hazelrigg T, Tu C (1994) Sex-specific processing of the Drosophila exuperantia transcript is regulated in male germ cells by the tra-2 gene. Proc Natl Acad Sci USA 91:10752-10756
17. Hediger M, Niessen M, Wimmer EA, Dubendorfer A, Bopp D (2001) Genetic transformation of the housefly Musca domestica with the lepidopteran derived transposon piggyBac. Insect Mol Biol 10:113-119
18. Hediger M, Burghardt G, Siegenthaler C, Buser N, Hilfiker-Kleiner D, Dubendorfer A, Bopp D (2004) Sex determination in Drosophila melanogaster and Musca domestica converges at the level of the terminal regulator doublesex. Dev Genes Evol 214:29-42
19. Hedley ML, Maniatis T (1991) Sex-specific splicing and polyadenylation of dsx pre-mRNA requires a sequence that binds specifically to tra-2 protein in vivo. Cell 65:579-586
20. 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
21. Hertel KJ, Lynch KW, Hsiao EC, Liu EH, Maniatis T (1996) Structural and functional conservation of the Drosophila doublesex splicing enhancer repeat elements. RNA 2:969-981
22. Hilfiker-Kleiner D, Dübendorfer A, Hilfiker A, Nöthiger R (1993) Developmental analysis of two sex-determining genes, M and F, in the housefly, Musca domestica. Genetics 134:1189-1194
23. Hilfiker-Kleiner D, Dubendorfer A, Hilfiker A, Nothiger R (1994) Genetic control of sex determination in the germ line and soma of the housefly, Musca domestica. Development 120:2531-2538
24. Hoshijima K, Inoue K, Higuchi I, Sakamoto H, Shimura Y (1991) Control of doublesex alternative splicing by transformer and transformer-2 in Drosophila. Science 252:833-836
25. Inoue K, Hoshijima K, Sakamoto H, Shimura Y (1990) Binding of the Drosophila sex-lethal gene product to the alternative splice site of transformer primary transcript. Nature 344:461-463
26. Ito H, Fujitani K, Usui K, Shimizu-Nishikawa K, Tanaka S, 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
27. Kohtz JD, Jamison SF, Will CL, Zuo P, Luhrmann R, Garcia-Blanco MA, Manley JL (1994) Protein-protein interactions and 5′-splice-site recognition in mammalian mRNA precursors. Nature 368:119-124
28. Lam BJ, Bakshi A, Ekinci FY, Webb J, Graveley BR, Hertel KJ (2003) Enhancer-dependent 5′-splice site control of fruitless pre-mRNA splicing. J Biol Chem 278:22740-22747
29. Lynch K, Maniatis T (1995) Synergistic interactions between two distinct elements of a regulated splicing enhancer. Genes Dev 9:284-293
30. Lynch KW, Maniatis T (1996) Assembly of specific SR protein complexes on distinct regulatory elements of the Drosophila doublesex splicing enhancer. Genes Dev 10:2089-2101
31. Madigan SJ, Edeen P, Esnayra J, McKeown M (1996) att, a target for regulation by tra2 in the testes of Drosophila melanogaster, encodes alternative RNAs and alternative proteins. Mol Cell Biol 16:4222-4230
32. Manley JL, Tacke R (1996) SR proteins and splicing control. Genes Dev 10:1569-1579
33. Mattox W, Baker BS (1991) Autoregulation of the splicing of transcripts from the transformer-2 gene of Drosophila. Genes Dev 5:786-796
34. Mattox W, Palmer MJ, Baker BS (1990) Alternative splicing of the sex determination gene transformer-2 is sex-specific in the germ line but not in the soma. Genes Dev 4:789-805
35. Mattox W, McGuffin ME, Baker BS (1996) A negative feedback mechanism revealed by functional analysis of the alternative isoforms of the Drosophila splicing regulator transformer-2. Genetics 143:303-314
36. McDonald IC, Evenson P, Nickel CA, Johnson OA (1978) House fly genetics: isolation of a female determining factor on chromosome 4. Ann Entomol Soc Am 71:692-694
37. McGregor AP, Shaw PJ, Hancock JM, Bopp D, Hediger M, Wratten NS, Dover GA (2001) Rapid restructuring of bicoid-dependent hunchback promoters within and between Dipteran species: Implications for molecular coevolution. Evol Dev 3:397-407
38. McGuffin ME, Chandler D, Somaiya D, Dauwalder B, Mattox W (1998) Autoregulation of transformer-2 alternative splicing is necessary for normal male fertility in Drosophila. Genetics 149:1477-486
39. Meise M, Hilfiker-Kleiner D, Dubendorfer A, Brunner C, Nothiger R, Bopp D (1998) Sex-lethal, the master sex-determining gene in Drosophila, is not sex-specifically regulated in Musca domestica. Development 125:1487-1494 1:CAS:528:DyaK1cXjsVGgsrc%3D
40. R Nöthiger M Steinmann-Zwicky 1985 A single principle for sex determination in insects, vol 50 Cold Spring Harbor Symposium Cold Spring Harbor, N.Y. 615-621
41. Pane A, Salvemini M, Delli Bovi P, Polito C, Saccone G (2002) The transformer gene in Ceratitis capitata provides a genetic basis for selecting and remembering the sexual fate. Development 129:3715-3725 1:CAS:528:DC%2BD38XmsFOksbo%3D
42. Parkhurst SM, Meneeley PM (1994) Sex determination and dosage compensation: Lessons from flies and worms. Science 264:924-932
43. Perje A-M (1948) Studies on the spermatogenesis in Musca domestica. Hereditas 34:209-232
44. Rubini PG, Franco MG, Vanossi Este S (1972) Polymorphisms for heterochromosomes and autosomal sex-determinants in Musca dmestica L. Atti IX Congr Naz It Entomol 9:341-352 341-352
45. Ryner LC, Baker BS (1991) Regulation of doublesex pre-mRNA processing occurs by 3′ splice site activation. Genes Dev 5:2071-2085
46. Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, Baker BS, Hall JC, Taylor BJ, Wasserman SA (1996) Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87:1079-1089
47. Saccone G, Peluso I, Artiaco D, Giordano E, Bopp D, Polito LC (1998) The Ceratitis capitata homologue of the Drosophila sex-determining gene sex-lethal is structurally conserved, but not sex-specifically regulated. Development 125:1495-1500 1:CAS:528:DyaK1cXjsVGgsL4%3D
48. Saccone G, Pane A, Polito LC (2002) Sex determination in flies, fruitflies and butterflies. Genetica 116:15-23
49. Schmidt R, Hediger M, Nöthiger R, Dübendorfer A (1997) The mutation masculinizer (man) defines a sex determining gene with maternal and zygotic functions in Musca domestica L. Genetics 145:173-183
50. Schutt C, Nothiger R (2000) Structure, function and evolution of sex-determining systems in dipteran insects. Development 127:667-677
51. Sosnowski BA, Belote JM, McKeown M (1989) Sex-specific alternative splicing of RNA from the transformer gene results from sequence-dependent splice site blockage. Cell 58:449-459
52. 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 10.1007/BF00291041
53. 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
54. Tian M, Maniatis T (1993) A splicing enhancer complex controls alternative splicing of doublesex pre-mRNA. Cell 74:105-114
55. Wu JY, Maniatis T (1993) Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell 75:1061-1070