Dmrt genes in the development and evolution of sexual dimorphism

Trends in Genetics

Volumn 28, Issue 4, 2012, Pages 175-184

  Kopp, Artyom ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLESEX AND MAB 3 RELATED TRANSCRIPTION FACTOR 1; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX8; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG;

BINDING SITE; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL FATE; CHROMATIN; FEMINIZATION; GENDER IDENTITY; GENE EXPRESSION; GENE FUNCTION; GENETIC TRAIT; GENETIC VARIABILITY; GONAD DEVELOPMENT; HOX GENE; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; REPRODUCTION; REVIEW; SEX CHROMOSOME; SEX DETERMINATION PROCESS; SEX DIFFERENCE; SEX DIFFERENTIATION; SEXUAL BEHAVIOR; SEXUAL DEVELOPMENT; SIGNAL TRANSDUCTION; TESTIS DEVELOPMENT; Y CHROMOSOME;

ANIMALS; BIOLOGICAL EVOLUTION; BODY PATTERNING; DNA-BINDING PROTEINS; HUMANS; RNA SPLICING; SEX DIFFERENTIATION; TRANSCRIPTION FACTORS;

ANIMALIA;

EID: 84859005211     PISSN: 01689525     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tig.2012.02.002     Document Type: Review

References (100)

1. McKeown M. Sex differentiation: the role of alternative splicing. Curr. Opin. Genet. Dev. 1992, 2:299-303.
2. Wilhelm D., et al. Sex determination and gonadal development in mammals. Physiol. Rev. 2007, 87:1-28.
3. Zarkower D. Establishing sexual dimorphism: conservation amidst diversity?. Nat. Rev. Genet. 2001, 2:175-185.
4. Raymond C.S., et al. Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev. 2000, 14:2587-2595.
5. Raymond C.S., et al. Evidence for evolutionary conservation of sex-determining genes. Nature 1998, 391:691-695.
6. Burtis K.C., Baker B.S. Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 1989, 56:997-1010.
7. Chue J., Smith C.A. Sex determination and sexual differentiation in the avian model. FEBS J. 2011, 278:1027-1034.
8. Herpin A., Schartl M. Dmrt1 genes at the crossroads: a widespread and central class of sexual development factors in fish. FEBS J. 2011, 278:1010-1019.
9. Yoshimoto S., Ito M. A ZZ/ZW-type sex determination in Xenopus laevis. FEBS J. 2011, 278:1020-1026.
10. Gempe T., Beye M. Function and evolution of sex determination mechanisms, genes and pathways in insects. Bioessays 2011, 33:52-60.
11. Verhulst E.C., et al. Insect sex determination: it all evolves around transformer. Curr. Opin. Genet. Dev. 2010, 20:376-383.
12. Kim S., et al. Sexually dimorphic expression of multiple doublesex-related genes in the embryonic mouse gonad. Gene Expr. Patterns 2003, 3:77-82.
13. Raymond C.S., et al. Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexual development. Dev. Biol. 1999, 215:208-220.
14. Sinclair A., et al. A comparative analysis of vertebrate sex determination. Novartis Found. Symp. 2002, 244:102-111.
15. Shoemaker C., et al. Expression of Sox9, Mis, and Dmrt1 in the gonad of a species with temperature-dependent sex determination. Dev. Dyn. 2007, 236:1055-1063.
16. Hempel L.U., Oliver B. Sex-specific DoublesexM expression in subsets of Drosophila somatic gonad cells. BMC Dev. Biol. 2007, 7:113.
17. Kato Y., et al. Environmental sex determination in the branchiopod crustacean Daphnia magna: deep conservation of a Doublesex gene in the sex-determining pathway. PLoS Genet. 2011, 7:e1001345.
18. Zhang E.F., Qiu G.F. A novel Dmrt gene is specifically expressed in the testis of Chinese mitten crab, Eriocheir sinensis. Dev. Genes Evol. 2010, 220:151-159.
19. Farazmand A., et al. Expression of Dmrt family genes during gonadal differentiation in two species of Artemia (Branchiopoda, Anostraca) from Urmia Lake (Iran). Crustaceana 2010, 83:1153-1165.
20. Klinbunga S., et al. Isolation and characterization of testis-specific DMRT1 in the tropical abalone (Haliotis asinina). Biochem. Genet. 2009, 47:66-79.
21. Naimi A., et al. Identification and expression of a factor of the DM family in the oyster Crassostrea gigas. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2009, 152:189-196.
22. Miller S.W., et al. A DM domain protein from a coral, Acropora millepora, homologous to proteins important for sex determination. Evol. Dev. 2003, 5:251-258.
23. Kim S., et al. A mammal-specific Doublesex homolog associates with male sex chromatin and is required for male meiosis. PLoS Genet. 2007, 3:e62.
24. Balciuniene J., et al. Mice mutant in the DM domain gene Dmrt4 are viable and fertile but have polyovular follicles. Mol. Cell. Biol. 2006, 26:8984-8991.
25. Uhlenhaut N.H., et al. Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 2009, 139:1130-1142.
26. Sekido R., Lovell-Badge R. Sex determination and SRY: down to a wink and a nudge?. Trends Genet. 2009, 25:19-29.
27. Matson C.K., et al. DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 2011, 476:101-104.
28. Kim S., et al. Cell type-autonomous and non-autonomous requirements for Dmrt1 in postnatal testis differentiation. Dev. Biol. 2007, 307:314-327.
29. Murphy M.W., et al. Genome-wide analysis of DNA binding and transcriptional regulation by the mammalian Doublesex homolog DMRT1 in the juvenile testis. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:13360-13365.
30. DeFalco T., et al. Nonautonomous sex determination controls sexually dimorphic development of the Drosophila gonad. Dev. Cell 2008, 14:275-286.
31. Camara N., et al. The creation of sexual dimorphism in the Drosophila soma. Curr. Top. Dev. Biol. 2008, 83:65-107.
32. Robinett C.C., et al. Sex and the single cell. II. There is a time and place for sex. PLoS Biol. 2010, 8:e1000365.
33. Kato M., et al. An autosomal locus controls sex reversal in interspecific XY hybrids of the medaka fishes. Heredity 2011, 107:523-529.
34. Tanaka K., et al. Evolution of sex-specific traits through changes in HOX-dependent doublesex expression. PLoS Biol. 2011, 9:e1001131.
35. Hildreth P.E. Doublesex, recessive gene that transforms both males and temales of Drosophila into intersexes. Genetics 1965, 51:659-678.
36. Christiansen A.E., et al. Sex comes in from the cold: the integration of sex and pattern. Trends Genet. 2002, 18:510-516.
37. Baker B.S., Ridge K.A. Sex and the single cell. I. On the action of major loci affecting sex determination in Drosophila melanogaster. Genetics 1980, 94:383-423.
38. Kimura K., et al. Fruitless and doublesex coordinate to generate male-specific neurons that can initiate courtship. Neuron 2008, 59:759-769.
39. Rideout E.J., et al. The sex-determination genes fruitless and doublesex specify a neural substrate required for courtship song. Curr. Biol. 2007, 17:1473-1478.
40. Billeter J.C., et al. Isoform-specific control of male neuronal differentiation and behavior in Drosophila by the fruitless gene. Curr. Biol. 2006, 16:1063-1076.
41. Sanders L.E., et al. Doublesex establishes sexual dimorphism in the Drosophila central nervous system in an isoform-dependent manner by directing cell number. Dev. Biol. 2008, 320:378-390.
42. Zarkower D. Somatic sex determination 2006, WormBook, 1-12.
43. Mason D.A., et al. dmd-3, a doublesex-related gene regulated by tra-1, governs sex-specific morphogenesis in C. elegans. Development 2008, 135:2373-2382.
44. Lints R., Emmons S.W. Regulation of sex-specific differentiation and mating behavior in C. elegans by a new member of the DM domain transcription factor family. Genes Dev. 2002, 16:2390-2402.
45. Yi W., et al. Mab-3 is a direct tra-1 target gene regulating diverse aspects of C. elegans male sexual development and behavior. Development 2000, 127:4469-4480.
46. Nelson M.D., et al. A bow-tie genetic architecture for morphogenesis suggested by a genome-wide RNAi screen in Caenorhabditis elegans. PLoS Genet. 2011, 7:e1002010.
47. Arnold A.P. The end of gonad-centric sex determination in mammals. Trends Genet. 2011, 28:55-61.
48. Hong C.S., et al. The function of Dmrt genes in vertebrate development: it is not just about sex. Dev. Biol. 2007, 310:1-9.
49. Murray S.M., et al. Germ cell sex determination: a collaboration between soma and germline. Curr. Opin. Cell Biol. 2010, 22:722-729.
50. Herpin A., et al. Inhibition of primordial germ cell proliferation by the medaka male determining gene Dmrt I bY. BMC Dev. Biol. 2007, 7:99.
51. Casper A.L., Van Doren M. The establishment of sexual identity in the Drosophila germline. Development 2009, 136:3821-3830.
52. Wallis M.C., et al. Sex determination in mammals - before and after the evolution of SRY. Cell. Mol. Life Sci. 2008, 65:3182-3195.
53. Mank J.E., Avise J.C. Evolutionary diversity and turn-over of sex determination in teleost fishes. Sex Dev. 2009, 3:60-67.
54. Hediger M., et al. Molecular characterization of the key switch F provides a basis for understanding the rapid divergence of the sex-determining pathway in the housefly. Genetics 2010, 184:155-170.
55. Nanda I., et al. A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:11778-11783.
56. Matsuda M., et al. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 2002, 417:559-563.
57. Kondo M., et al. Absence of the candidate male sex-determining gene dmrt1b(Y) of medaka from other fish species. Curr. Biol. 2003, 13:416-420.
58. Yoshimoto S., et al. A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:2469-2474.
59. Bewick A.J., et al. Evolution of the closely related, sex-related genes DM-W and DMRT1 in African clawed frogs (Xenopus). Evolution 2011, 65:698-712.
60. Yoshimoto S., et al. Opposite roles of DMRT1 and its W-linked paralogue, DM-W, in sexual dimorphism of Xenopus laevis: implications of a ZZ/ZW-type sex-determining system. Development 2010.
61. Smith C.A., et al. The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 2009, 461:267-271.
62. Ross J.M., et al. The DM domain protein MAB-3 promotes sex-specific neurogenesis in C. elegans by regulating bHLH proteins. Dev. Cell 2005, 8:881-892.
63. Coschigano K.T., et al. Sex-specific transcriptional regulation by the male and female doublesex proteins of Drosophila. Genes Dev. 1993, 7:42-54.
64. Burtis K.C., et al. The doublesex proteins of Drosophila melanogaster bind directly to a sex-specific yolk protein gene enhancer. EMBO J. 1991, 10:2577-2582.
65. Shirangi T.R., et al. Rapid evolution of sex pheromone-producing enzyme expression in Drosophila. PLoS Biol. 2009, 7:e1000168.
66. Goldman T.D., Arbeitman M.N. Genomic and functional studies of Drosophila sex hierarchy regulated gene expression in adult head and nervous system tissues. PLoS Genet. 2007, 3:e216.
67. Luo S.D., et al. Direct targets of the D. melanogaster DSXF protein and the evolution of sexual development. Development 2011, 138:2761-2771.
68. Salvemini M., et al. Genomic organization and splicing evolution of the doublesex gene, a Drosophila regulator of sexual differentiation, in the dengue and yellow fever mosquito Aedes aegypti. BMC Evol. Biol. 2011, 11:41.
69. Cho S., et al. Sex-specific splicing of the honeybee doublesex gene reveals 300 million years of evolution at the bottom of the insect sex-determination pathway. Genetics 2007, 177:1733-1741.
70. Oliveira D.C., et al. Identification and characterization of the doublesex gene of Nasonia. Insect Mol. Biol. 2009, 18:315-324.
71. Suzuki M.G., et al. Role of the male BmDSX protein in the sexual differentiation of Bombyx mori. Evol. Dev. 2005, 7:58-68.
72. Kato Y., et al. Sequence divergence and expression of a transformer gene in the branchiopod crustacean, Daphnia magna. Genomics 2010, 95:160-165.
73. Williams T.M., Carroll S.B. Genetic and molecular insights into the development and evolution of sexual dimorphism. Nat. Rev. Genet. 2009, 10:797-804.
74. Kopp A., et al. Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 2000, 408:553-559.
75. Williams T.M., et al. The regulation and evolution of a genetic switch controlling sexually dimorphic traits in Drosophila. Cell 2008, 134:610-623.
76. Kopp A Drosophila sex combs as a model of evolutionary innovations. Evol. Dev. 2011, 13:504-522.
77. Barmina O., Kopp A. Sex-specific expression of a HOX gene associated with rapid morphological evolution. Dev. Biol. 2007, 311:277-286.
78. Loehlin D.W., et al. Non-coding changes cause sex-specific wing size differences between closely related species of Nasonia. PLoS Genet. 2010, 6:e1000821.
79. Bell L.R., et al. Positive autoregulation of sex-lethal by alternative splicing maintains the female determined state in Drosophila. Cell 1991, 65:229-239.
80. Nagoshi R.N., et al. The control of alternative splicing at genes regulating sexual differentiation in D. melanogaster. Cell 1988, 53:229-236.
81. Manoli D.S., et al. Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 2005, 436:395-400.
82. Demir E., Dickson B.J. fruitless splicing specifies male courtship behavior in Drosophila. Cell 2005, 121:785-794.
83. Jursnich V.A., Burtis K.C. A positive role in differentiation for the male doublesex protein of Drosophila. Dev. Biol. 1993, 155:235-249.
84. Waterbury J.A., et al. Analysis of the doublesex female protein in Drosophila melanogaster: role on sexual differentiation and behavior and dependence on intersex. Genetics 1999, 152:1653-1667.
85. Erdman S.E., et al. The Drosophila doublesex proteins share a novel zinc finger related DNA binding domain. EMBO J. 1993, 12:527-535.
86. Zhu L., et al. Sexual dimorphism in diverse metazoans is regulated by a novel class of intertwined zinc fingers. Genes Dev. 2000, 14:1750-1764.
87. Volff J.N., et al. Evolutionary dynamics of the DM domain gene family in metazoans. J. Mol. Evol. 2003, 57(Suppl. 1):S241-S249.
88. An W., et al. Sex-specific and non-sex-specific oligomerization domains in both of the doublesex transcription factors from Drosophila melanogaster. Mol. Cell. Biol. 1996, 16:3106-3111.
89. Murphy M.W., et al. Vertebrate DM domain proteins bind similar DNA sequences and can heterodimerize on DNA. BMC Mol. Biol. 2007, 8:58.
90. Yi W., Zarkower D. Similarity of DNA binding and transcriptional regulation by Caenorhabditis elegans MAB-3 and Drosophila melanogaster DSX suggests conservation of sex determining mechanisms. Development 1999, 126:873-881.
91. Matson C.K., et al. The mammalian doublesex homolog DMRT1 is a transcriptional gatekeeper that controls the mitosis versus meiosis decision in male germ cells. Dev. Cell 2010, 19:612-624.
92. Krentz A.D., et al. DMRT1 promotes oogenesis by transcriptional activation of Stra8 in the mammalian fetal ovary. Dev. Biol. 2011, 356:63-70.
93. Veith A.M., et al. Tissue-specific expression of dmrt genes in embryos and adults of the platyfish Xiphophorus maculatus. Zebrafish 2006, 3:325-337.
94. Raghuveer K., et al. Dimorphic expression of various transcription factor and steroidogenic enzyme genes during gonadal ontogeny in the air-breathing catfish, Clarias gariepinus. Sex Dev. 2011, 5:213-223.
95. Kobayashi T., et al. Two DM domain genes, DMY and DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes. Dev. Dyn. 2004, 231:518-526.
96. Kobayashi T., et al. Sexual dimorphic expression of DMRT1 and Sox9a during gonadal differentiation and hormone-induced sex reversal in the teleost fish Nile tilapia (Oreochromis niloticus). Dev. Dyn. 2008, 237:297-306.
97. Yamaguchi A., et al. Expression of the DMRT gene and its roles in early gonadal development of the Japanese pufferfish Takifugu rubripes. Comp. Biochem. Physiol. Part D: Genomics Proteomics 2006, 1:59-68.
98. Johnsen H., et al. Sexually dimorphic expression of dmrt1 in immature and mature Atlantic cod (Gadus morhua L.). Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 2010, 156:197-205.
99. Guo Y., et al. Gene structure, multiple alternative splicing, and expression in gonads of zebrafish Dmrt1. Biochem. Biophys. Res. Commun. 2005, 330:950-957.
100. Hempel L.U., et al. Drosophila germline sex determination: integration of germline autonomous cues and somatic signals. Curr. Top. Dev. Biol. 2008, 83:109-150.