The function of Dmrt genes in vertebrate development: It is not just about sex

Developmental Biology

Volumn 310, Issue 1, 2007, Pages 1-9

  Hong, Chang Soo ^a   Park, Byung Yong ^a   Saint Jeannet, Jean Pierre ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

DM domain; Dmrt; Gonads; Laterality; Nasal placode; Olfactory system; Sex determination; Somites

Indexed keywords

TRANSCRIPTION FACTOR;

DROSOPHILA MELANOGASTER; EMBRYO DEVELOPMENT; GENE CONTROL; GENE FUNCTION; GONAD DEVELOPMENT; PRIORITY JOURNAL; REVIEW; SPECIES IDENTIFICATION; VERTEBRATE;

INVERTEBRATA; VERTEBRATA;

EID: 34548812861     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2007.07.035     Document Type: Review

References (64)

1. Aoyama S., Shibata K., Tokunaga S., Takase M., Matsui K., and Nakamura M. Expression of Dmrt1 protein in developing and in sex-reversed gonads of amphibians. Cytogenet. Genome Res. 101 (2003) 295-301
2. Balciuniene J., Bardwell V.J., and Zarkower D. Mice mutant in the DM domain gene Dmrt4 are viable and fertile but have polyovular follicles. Mol. Cell. Biol. 26 (2006) 8984-8991
3. Bownes M. The regulation of the yolk protein genes, a family of sex differentiation genes in Drosophila melanogaster. BioEssays 16 (1994) 752-754
4. Calvari V., Bertini V., De Grandi A., Peverali G., Zuffardi O., Ferguson-Smith M., Knudtzon J., Camerino G., Borsani G., and Guioli S. A new submicroscopic deletion that refines the 9p region for sex reversal. Genomics 65 (2000) 203-212
5. El-Mogharbel N., Wakefield M., Deakin J.E., Tsend-Ayush E., Grutzner F., Alsop A., Ezaz T., and Graves J.A.M. DMRT gene cluster analysis in the platypus: new insights into genomic organization and regulatory regions. Genomics 89 (2007) 10-21
6. Guo Y., Li Q., Gao S., Zhou X., He Y., Shang X., Cheng H., and Zhou R. Molecular cloning, characterization, and expression in brain and gonad of Dmrt5 of zebrafish. Biochem. Biophys. Res. Commun. 324 (2004) 569-575
7. Guo Y., Cheng H., Huang X., Gao S., Yu H., and Zhou R. Gene structure, multiple alternative splicing, and expression in gonads of zebrafish Dmrt1. Biochem. Biophys. Res. Commun. 330 (2005) 950-957
8. Hodgkin J. The remarkable ubiquity of DM domain factors as regulators of sexual phenotype: ancestry or aptitude?. Genes Dev. 16 (2002) 2322-2326
9. Huang X., Guo Y., Shui Y., Gao S., Yu H., Cheng H., and Zhou R. Multiple alternative splicing and differential expression of dmrt1 during gonad transformation of the rice field eel. Biol. Reprod. 73 (2005) 1017-1024
10. Huang X., Hong C.S., O'Donnell M., and Saint-Jeannet J.P. The doublesex-related gene, XDmrt4, is required for neurogenesis in the olfactory system. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 11349-11354
11. Kawamata M., and Nishimori K. Mice deficient in Dmrt7 show infertility with spermatogenic arrest at pachytene stage. FEBS Lett. 580 (2006) 6442-6446
12. Kettlewell J.R., Raymond C.S., and Zarkower D. Temperature-dependent expression of turtle Dmrt1 prior to sexual differentiation. Genesis 26 (2000) 174-178
13. Keverne E.B. Importance of olfactory and vomeronasal systems for male sexual function. Physiol. Behav. 83 (2004) 177-187
14. Kim S., Kettlewell J.R., Anderson R.C., Bardwell V.J., and Zarkower D. Sexually dimorphic expression of multiple doublesex-related genes in the embryonic mouse gonad. Gene Expr. Patterns 3 (2003) 77-82
15. Kim S., Namekawa S.H., Niswander L.M., Ward J., Lee J.T., Bardwell V.J., and Zarkower D. A mammal-specific doublesex homolog associates with male sex chromatin and is required for male meiosis. Plos Genet. 3 (2007) 559-571
16. Kim S., Bardell V.J., and Zarkower D. Cell type-autonomous and non-autonomous requirements for Dmrt1 in postnatal testis differentiation. Dev. Biol. 307 (2007) 314-327
17. Kobayashi T., Matsuda M., Kajiura-Kobayashi H., Suzuki A., Saito N., Nakamoto M., Shibata N., and Nagahama Y. Two DM domain genes, DMY and DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes. Dev. Dyn. 231 (2004) 518-526
18. Koji H., Yamada A., Nagasawa T., and Gamou S. DMRT-1 expression during NEC8 human embryonic carcinoma cell differentiation. Cancer Sci. 97 (2006) 277-282
19. Kondo M., Froschauer A., Kitano A., Nanda I., Hornung U., Volff J.N., Asakawa S., Mitani H., Naruse K., Tanaka M., Schmid M., Shimizu N., Schartl M., and Shima A. Molecular cloning and characterization of DMRT genes from the medaka Oryzias latipes and the platyfish Xiphophorus maculatus. Gene 295 (2002) 213-222
20. Kondo M., Nanda I., Hornung U., Asakawa S., Shimizu N., Mitani H., Schmid M., Shima A., and Schartl M. Absence of the candidate male sex-determining gene dmrt1b(Y) of medaka from other fish species. Curr. Biol. 13 (2003) 416-420
21. Koopman P., and Loffler K.A. Sex determination: the fishy tale of Dmrt1. Curr. Biol. 13 (2003) R177-R179
22. Marchand O., Govoroun M., D'Cotta H., McMeel O., Lareyre J., Bernot A., Laudet V., and Guiguen Y. DMRT1 expression during gonadal differentiation and spermatogenesis in the rainbow trout, Oncorhynchus mykiss. Biochim. Biophys. Acta 1493 (2000) 180-187
23. Matsuda M. Sex determination in the teleost medaka, Oryzias lapides. Annu. Rev. Genet. 39 (2005) 293-307
24. Matsuda M., Nagahama Y., Shinomiya A., Sato T., Matsuda C., Kobayashi T., Morrey C.E., Shibata N., Asakawa S., Shimizu N., Hori H., Hamaguchi S., and Sakaizumi M. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417 (2002) 559-563
25. Matsuda M., Shinomiya A., Kinoshita M., Suzuki A., Kobayashi T., Paul-Prasanth B., Lau E.L., Hamaguchi S., Sakaizumi M., and Nagahama Y. DMY gene induces male development in genetically female (XX) medaka fish. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 3865-3870
26. Matsushita Y., Oshima Y., and Nakamura M. Expression of Dmrt genes in the gonads of Rana rugosa during sex determination. Zool. Sci. 24 (2007) 95-99
27. Meng A., Moore B., Tang H., Yuan B., and Lin S. A Drosophila doublesex-related gene, terra, is involved in somitogenesis in vertebrates. Development 126 (1999) 1259-1268
28. Miller S.W., Hayward D.C., Bunch T.A., Miller D.J., Ball E.E., Bardwell V.J., Zarkower D., and Brower D.L. A DM domain protein from a coral, Acropora millepora, homologous to proteins important for sex determination. Evol. Dev. 5 (2003) 251-258
29. Moniot B., Berta P., Scherer G., Südbeck P., and Poulat F. Male specific expression suggests role of DMRT1 in human sex determination. Mech. Dev. 91 (2000) 323-325
30. Muroya K., Okuyama T., Goishi K., Ogiso Y., Fukuda S., Kameyama J., Sato H., Suzuki Y., Terasaki H., Gomyo H., Wakui K., Fukushima Y., and Ogata T. Sex-determining gene(s) on distal 9p: clinical and molecular studies in six cases. J. Clin. Endocrinol. Metab. 85 (2000) 3094-3100
31. Nanda I., Zend-Ajusch E., Shan Z., Grutzner F., Schartl M., Burt D.W., Koehler M., Fowler V.M., Goodwin G., Schneider W.J., Mizuno S., Dechant G., Haaf T., and Schmid M. Conserved synteny between the chicken Z sex chromosome and human chromosome 9 includes the male regulatory DMRT1: a comparative (re)view on avian sex determination. Cytogenet. Cell Genet. 89 (2000) 67-78
32. Nanda I., Kondo M., Hornung U., Asakawa S., Winkler C., Shimizu A., Shan Z., Haaf T., Shimizu N., Shima A., Schmid M., and Schartl M. 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. 99 (2002) 11778-11783
33. Osawa N., Oshima Y., and Nakamura M. Molecular cloning of Dmrt1 and its expression in the gonad of Xenopus. Zool. Sci. 22 (2005) 681-687
34. Ottolenghi, and McElreavey K. Deletions of 9p and the quest for a conserved mechanism of sex determination. Mol. Genet. Metab. 71 (2000) 397-404
35. Ottolenghi C., Veitia R., Barbieri M., Fellous M., and McElreavey K. The human doublesex-related gene, DMRT2, is homologous to a gene involved in somitogenesis and encodes a potential bicistronic transcript. Genomics 64 (2000) 179-186
36. Ottolenghi C., Fellous M., Barbieri M., and McElreavey K. Novel paralogy relations among human chromosomes support a link between the phylogeny of doublesex-related genes and the evolution of sex determination. Genomics 79 (2002) 333-343
37. Ounap K., Uibo O., Zordania R., Kiho L., Ilus T., Oiglane-Shlik E., and Bartsch O. Three patients with 9p deletions including DMRT1 and DMRT2: a girl with XY complement, bilateral ovotestes, and extreme growth retardation, and two XX females with normal pubertal development. Am. J. Med. Genet., A 130 (2004) 415-423
38. Pask A.J., Behringer R.R., and Renfree M.B. Expression of DMRT1 in the mammalian ovary and testis: from marsupials to mice. Cytogenet. Genome Res. 101 (2003) 229-236
39. Raya A., and Izpisúa Belmonte J.C. Left-right asymmetry in the vertebrate embryo: from early information to higher-level integration. Nat. Rev., Genet. 7 (2006) 283-293
40. Raymond C.S., Shamu C.E., Shen M.M., Seifert K.J., Hirsch B., Hodgkin J., and Zarkower D. Evidence for evolutionary conservation of sex-determining genes. Nature 391 (1998) 691-695
41. Raymond C.S., Kettlewell J.R., Hirsch B., Bardwell V.J., and Zarkower D. Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexual development. Dev. Biol. 215 (1999) 208-220
42. Raymond C.S., Parker E.D., Kettlewell J.R., Brown L.G., Page D.C., Kusz K., Jaruzelska J.R., Reinberg Y., Fleijter W.L., Bardwell V.J., Hirsch B., and Zarkower D. A region of human chromosome 9p required for testis development contains two genes related to known sexual regulators. Hum. Mol. Genet. 8 (1999) 989-996
43. Raymond C.S., Murphy M.W., O'Sullivan M.G., Bardwell V.J., and Zarkower D. Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev. 14 (2000) 2587-2595
44. Saccone G., Pane A., and Polito L.C. Sex determination in flies, fruitflies and butterflies. Genetica 116 (2002) 15-23
45. Sakata N., Miyazaka K., and Wakahara M. Up-regulation of P450arom and down-regulation of Dmrt-1 genes in the temperature-dependent sex reversal from genetic males to phenotypic females in a salamander. Dev. Genes Evol. 216 (2006) 224-228
46. Saude L., Lourenco R., Goncalves A., and Palmeirim I. terra is a left-right asymmetry gene required for left-right synchronization of the segmentation clock. Nat. Cell Biol. 7 (2005) 918-920
47. Schartl M. A comparative view on sex determination in medaka. Mech. Dev. 121 (2004) 639-645
48. Seo K.W., Wang Y., Kokubo H., Kettlewell J.R., Zarkower D.A., and Johnson R.L. Targeted disruption of the DM domain containing transcription factor Dmrt2 reveals an essential role in somite patterning. Dev. Biol. 290 (2006) 200-210
49. Shan Z., Nanda I., Wang Y., Schmid M., Vortkamp A., and Haaf T. Sex-specific expression of an evolutionarily conserved male regulatory gene, DMRT1, in birds. Cytogenet. Cell Genet. 89 (2000) 252-257
50. Shen M.M., and Hodgkin H.R. mab-3, a gene required for sex-specific yolk protein expression and a male-specific lineage in C. elegans. Cell 54 (1988) 1019-1031
51. Shibata K., Takase M., and Nakamura M. The Dmrt1 expression in sex-reversed gonads of amphibians. Gen. Comp. Endocrinol. 127 (2002) 232-241
52. Smith C.A., and Sinclair A.H. Sex determination: insights from the chicken. BioEssays 26 (2004) 120-132
53. Smith C.A., McClive P.J., Western P.S., Reed K.J., and Sinclair A.H. Conservation of a sex-determining gene. Nature 402 (1999) 601-602
54. Smith C.A., Hurley T.M., McClive P.J., and Sinclair A.H. Restricted expression of DMRT3 in chicken and mouse embryos. Gene Expr. Patterns 2 (2002) 69-72
55. Sreenivasulu K., Ganesh S., and Raman R. Evolutionarily conserved, DMRT1, encodes alternatively spliced transcripts and shows dimorphic expression during gonadal differentiation in the lizard, Calotes versicolor. Gene Expr. Patterns 2 (2002) 51-60
56. Veith A.M., Froschauer A., Korting C., Nanda I., Hanel R., Schmid M., Schartl M., and Volff J.N. Cloning of the dmrt1 gene of Xiphophorus maculatus: dmY/dmrt1Y is not the master sex-determining gene in the platyfish. Gene 317 (2003) 59-66
57. Veith A.M., Schäfer M., Klüver N., Schmidt C., Schultheis C., Schartl M., Winkler C., and Volff J.N. Tissue-specific expression of dmrt genes in embryos and adults of the platyfish Xiphophorus maculates. Zebrafish 3 (2006) 325-337
58. Veith A.M., Klattig J., Dettai A., Schmidt C., Englert C., and Volff J.N. Male-biased expression of X-chromosomal DM domain-less Dmrt8 genes in the mouse. Genomics 88 (2006) 185-195
59. Veitia R., Nunes M., Brauner R., Doco-Fenzy M., Joanny-Flinois O., Jaubert F., Lortat-Jacob S., Fellous M., and McElreavey K. Deletions of distal 9p associated with 46,XY male to female sex reversal: definition of the breakpoints at 9p23.3-p24.1. Genomics 41 (1997) 271-274
60. Volff J.N., Zarkower D., Bardwell V.J., and Schartl M. Evolutionary dynamics of the DM domain gene family in metazoans. J. Mol. Evol. 57 (2003) S241-S249
61. Winkler C., Hornung U., Kondo M., Neuner C., Duschl J., Shima A., and Schartl M. Developmentally regulated and non-sex-specific expression of autosomal dmrt genes in embryos of the medaka fish (Oryzias latipes). Mech. Dev. 121 (2004) 997-1005
62. Yao H.H., and Capel B. Temperature, genes, and sex: a comparative view of sex determination in Trachemys scripta and Mus musculus. J. Biochem. 138 (2005) 5-12
63. Zarkower D. Establishing sexual dimorphism: conservation amidst diversity?. Nat. Rev., Genet. 2 (2001) 175-185
64. Zhu L., Wilken J., Phillips N.B., Narendra U., Chan G., Stratton S.M., Kent S.B., and Weiss M.A. Sexual dimorphism in diverse metazoans is regulated by a novel class of intertwined zinc fingers. Genes Dev. 14 (2000) 1750-1764