The Xenopus doublesex-related gene Dmrt5 is required for olfactory placode neurogenesis

Developmental Biology

Volumn 373, Issue 1, 2013, Pages 39-52

  Parlier, Damien ^a   Moers, Virginie ^a   Van Campenhout, Claude ^a   Preillon, Julie ^a   Leclère, Lucas ^b   Saulnier, Amandine ^a   Sirakov, Maria ^a   Busengdal, Henriette ^b   Kricha, Sadia ^a   Marine, Jean Christophe ^c   Rentzsch, Fabian ^b   Bellefroid, Eric J ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b UNIVERSITY OF BERGEN   (Norway)

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Dmrt; Ebf2; Nematostella; Notch; Olfactory placode; OTX2; Xenopus

Indexed keywords

CARBOXY TERMINAL TELOPEPTIDE; DOUBLE SEX AND MAB 3 RELATED TRANSCRIPTION FACTOR; NOTCH RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR OTX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DMRT4 GENE; DMRT5 GENE; DNA BINDING MOTIF; ECTODERM; EMBRYO; ENZYME ACTIVATION; GENE; GENE ACTIVATION; GENE ACTIVITY; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE SEQUENCE; GENETIC REGULATION; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; OLFACTORY SYSTEM; PRIORITY JOURNAL; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; XENOPUS;

ANIMALIA; BILATERIA; CNIDARIA; NEMATOSTELLA; VERTEBRATA;

EID: 84870061450     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.10.003     Document Type: Article

References (78)

1. -/- mutants due to a défective anterior neurectoderm specification during gastrulation. Development 1995, 121:3279-3290.
2. Ahrens K., Schlosser G. Tissues and signals involved in the induction of placodal Six1 expression in Xenopus laevis. Dev. Biol. 2005, 288:40-59.
3. Balcuniene J., Bardwell V.J., Zarkower D. Mice mutant in the DM domain gene Dmrt4 are viable and fertile but have polyovular follicles. Mol. Cell. Biol. 2006, 26:8984-8991.
4. Bellefroid E.J., Bourguignon C., Holleman T., Ma Q., Anderson D.J., Kintner C., Pieler T. X-Myt1, a Xenopus C2HC type zinc finger protein with a regulatory function in neuronal differentiation. Cell 1996, 87:1191-1202.
5. Bourguignon C., Li J., Papalopulu N. XBF-1, a winged hélix transcription factor with a dual activity, has a role in positioning neurogenesis in competent ectoderm. Development 1998, 125:4889-4900.
6. Brugmann S., Pandur P., Kenyon K.L., Pignoni F., Moody S.A. Six1 promotes a placodal fate within the lateral neurogenic ectoderm by functioning as both a transcriptional activator and repressor. Development 2004, 131:5871-5881.
7. Burns C.J., Vetter M.L. Xath5 regulates neurogenesis in the Xenopus olfactory placode. Dev. Dyn. 2002, 225:536-543.
8. Chitnis A., Henrique D., Lewis J., Ish-Horowicz D., Kintner C. Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature 1995, 375:761-766.
9. Dickinson K., Leonard J., Baker J.C. Genomic profiling of mixer and Sox17b targets during Xenopus endoderm development. Dev. Dyn. 2006, 235:368-381.
10. Dubois L., Bally-Cuif L., Crozatier M., Moreau J., Paquereau L., Vincent A. XCoe2, a transcription factor of the Col/Olf-1/EBF family involved in the specification of primary neurons in Xenopus. Curr. Biol. 1998, 8:199-209.
11. El-Hodiri H.M., Seufert D.W., Nekkalapudi S., Prescott N.L., Kelly L.E., Jamrich M. Xenopus laevis FoxE1 is primarily expressed in the developing pituitary gland. Int. J. Dev. Biol. 2005, 49:881-884.
12. Fritzenwanker J.H., Technau U. Induction of gametogenesis in the basal cnidarian Nematostella vectensis (Anthozoa). Dev. Genes Evol. 2002, 212:99-103.
13. Galliot B., Quiquand M., Ghila L., de Rosa R., Miljkovic-Licina M., Chera S. Origins of neurogenesis, a cnidarian view. Dev. Biol. 2009, 332:2-24.
14. Gammill L.S., Sive H. Otx2 expression in the ectoderm activates anterior neural determination and is required for xenopus cement gland formation. Dev. Biol. 2001, 240:223-236.
15. Gennet N., Gale E., Nan X., Farley E., Takacs K., Oberwallner B., Chambers D., Li M. Doublesex and Mab-3-related transcription factor 5 promotes midbrain dopaminergic identity in pluripotent stem cells by enforcing a ventral-medial progenitor fate. Proc. Natl. Acad. Sci. 2011, 108:9131-9136.
16. Glavic A., Maris Honoré S., Gloria F.C., Bastidas F., Allende M.L., Mayor R. Role of BMP signaling and the homeoprotein Iroquois in the specification of the cranial placodal field. Dev. Biol. 2004, 272:89-103.
17. Guo Y., Li Q., Gao S., Zhou X., He Y., Shang X., Cheng H., Zhou R. Molecular cloning, characterization, and expression in brain and gonad of Dmrt5 of zebrafish. Biochem. Biophys. Res. Commun. 2004, 324:569-575.
18. Green Y.S., Vetter M. EBF factors drive expression of multiple classes of target genes governing neuronal development. Neural Dev. 2011, 6:19.
19. Hand C., Uhlinger K. The culture, sexual and asexual reproduction, and growth of the sea anemone Nematostella vectensis. Biol. Bull. 1992, 182:169-176.
20. Hemmati-Brivanlou A., de la Torre J.R., Holt C., Harland R.M. Cephalic expression and molecular characterization of Xenopus En-2. Development 1991, 111:715-724.
21. Hensey C., Gautier J. Programmed cell death during Xenopus development: a spatio-temporal analysis. Dev. Biol. 1998, 203:36-48.
22. Hong C.-S., Park B.Y., Saint-Jeannet J.P. The function of DMRT genes in vertebrate development: it is not just about sex. Dev. Biol. 2007, 310:1-9.
23. Huang X., Hong C.S., O'Donnell M., Saint-Jeannet J.P. The doublesex-related gene, XDmrt4, is required for neurogenesis in the olfactory system. Proc. Natl. Acad. Sci. 2005, 102:11349-11354.
24. Jonas E., Sargent T.D., Dawid I.B. Epidermal keratin gene expressed in embryos of Xenopus laevis. Proc. Natl. Acad. Sci. U.S.A 1985, 82:5413-5417.
25. Kanekar S., Perron M., Dorsky R., Harris W.A., Jan L.Y., Jan Y.N., Vetter M.L. Xath5 participates in a network of bHLH genes in the developing Xenopus retina. Neuron 1997, 19:981-994.
26. Kenyon K.L., Moody S.A., Jamrich M. A novel fork-head gene mediates early steps during Xenopus lens formation. Development 1999, 126:5107-5116.
27. Kim S., Kettlewell J.R., Anderson R.C., Bardwell V.J., Zarkower D. Gene Exp. Patterns 2003, 3:77-82.
28. Kimura K., Hachiya T., Koganezawa M., Tazawa T., Yamamoto D. Fruitless and doublesex coordinate to generate male-specific neurons that can initiate courtship. Neuron 2008, 59:759-769.
29. Kwon H.J., Bhat N., Sweet E.M., Cornell R.A., Riley B.B. Identification of early requirements for preplacodal ectoderm and sensory organ development. Plos Genet. 2010, 6(9):e1001133. pii.
30. Li Q., Zhou X., Shang X., Chen H., Lu H., Cheng H., Zhou R. Biol. Cell. 2008, 100:453-463.
31. Litsiou A., Hanson S., Streit A. A balance of FGF, BMP and WNT signaling positions the future placode territory in the head. Development 2005, 132:4051-4062.
32. Luo T., Marsuo-Takasaki M., Lim J.H., Sargent T.D. Differential regulation of Dlx gene expression by a BMP morphogenetic gradient. Int. J. Dev. Biol. 2001, 45:681-684.
33. Logan M.A., Steele M.R., Van Raay T.J., Vetter M.L. Identification of shared transcriptional targets for the proneural bHLH factors Xath5 and XNeuroD. Dev. Biol. 2005, 285:570-583.
34. Ma Q., Kintner C., Anderson D.J. Identification of neurogenin, a vertebrate neuronal differentiation gene. Cell 1996, 87:43-52.
35. Maier E., Nord H., von Hofsten J., Gunhaga L. A balance of BMP and Notch activity regulates neurogenesis and olfactory nerve formation. Plos One 2011, 6:e173-179.
36. Martoriati A., Doumont G., Alcalay M., Bellefroid E.J., Pelicci P.G. dapk1, encoding an activator of a p19ARF-p53-mediated apoptotic checkpoint, is a transcription target of p53. Marine, J.C. Oncogene 2005, 24:1461-1466.
37. Matson C.K., Murphy M.W., Griswold M.D., Yoshida S., Bardwell V.J., Zarkower D. 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.
38. Matson C.K., Murphy M.W., Sarver A.L., Griswold M.D., Bardwell V.J., Zarkower D. Dmrt1 prevents female reprogramming in the postnatal mammalian testis. Nature 2011, 476:101-104.
39. Matsuo I., Kuratani S., Kimura C., Takeda N., Aizawa S. Mouse Otx2 functions in the formation and patterning of rostral head. Genes Dev. 1995, 9:2646-2658.
40. Mayor R., Morgan R., Sargent M.G. Induction of the prospective neural crest of xenopus. Development 1995, 121:767-777.
41. Meng A., Moore B., Tang H., Yuan B., Lin S. A Drosophila doublesex-related gene, terra, is involved in somitogenesis in vertebrates. Development 1999, 126:1259-1268.
42. Murphy M., Sarver A.L., Rice D., Hatzi K., Ye K., Melnick A., Heckert L.L., Zarkower D., Bardwell V.J. Genome-wide analysis of DNA binding and transcriptional regulation by the mammalian Doublesex homolog DMRT1 in the juvenile testis. Proc. Natl. Acad. Sci 2010, 107:13360-13365.
43. Nakanishi N., Renfer E., Technau U., Rentzsch F. Nervous systems of the sea anemone Nematostella vectensis are generated by ectoderm and endoderm and shaped by distinct mechanisms. Development 2012, 139:347-357.
44. Nieber F., Pieler T., Henningfeld K.A. Comparative expression analysis of the neurogenins in Xenopus tropicalis and Xenopus laevis. Dev. Dyn. 2009, 451-458.
45. Ogino H., Fisher M., Grainger R.M. Convergence of a head-field selector Otx2 and Notch signaling: a mechanism for lens spécification. Development 2008, 135:249-258.
46. Nieuwkoop P.D., Faber J. Normal table of Xenopus laevis (Daudin) 1967, North-Holland, Publishing Co, Amsterdam, The Netherlands.
47. Pannese M., Polo C., Andreazzoli M., Vignali R., Kablar B., Barsacchi G., Boncinelli E. The xenopus homologue of Otx2 is a maternal homeobox gene that demarcates and specifies anterior body regions. Development 1995, 121:707-720.
48. Park B.Y., Saint Jeannet J.P. Induction and Segregation of the Vertebrate Cranial Placodes 2010, Morgan & Claypool Life Sciences, San Rafael,CA.
49. Peres J.N., Durston A.J. Role of X-Delta2 in the early neural development of Xenopus laevis. Dev. Dyn. 2006, 235:802-810.
50. Pichon B., Taelman V., Bellefroid E.J., Christophe D. Transcriptional repression by the bHLH-Orange factor XHRT1 does not involve the C-terminal YRPW motif. Biochem. Biophys. Acta 2004, 1680:46-52.
51. Putnam N.H., Srivastava M., Hellsten U., Dirks B., Chapman J., Salamov A., Terry A., Shapiro H., Lindquist E., Kapitonov V.V., Jurka J., Genikhovich G., Grigoriev I.V., Lucas S.M., Steele R.E., Finnerty J.R., Technau U., Martindale M.Q., Rokhsar D.S. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 2007, 317:86-94.
52. Raymond C.S., Murphy M.W., O'Sullivan M.G., Bardwell V.J., Zarkower D. Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis différentiation. Genes Dev. 2000, 14:2587-2595.
53. Rentzsch F., Anton R., Saina M., Hammerschmidt M., Holstein T.W., Technau U. Asymetric expression of the BMP antagonists chordin and gremlin in the sea anemone Nematostella vectensis: implications for the evolution of axial patterning. Dev. Biol. 2006, 296:375-387.
54. Rentzsch F., Fritzenwanker J.H., Scholz C.B., Technau U. FGF signalling controls formation of the apical sensory organ in the cnidarian Nematostella vectensis. Development 2008, 135:1761-1769.
55. Ross J.M., Kalis A.K., Murphy M.W., Zarkower D. The DM domain protein MAB-3 promotes sex-specific neurogenesis in C. elegans by regulating bHLH proteins. Dev. Cell. 2005, 8:881-892.
56. Saulnier A., Keruzore M., De Clercq S., Bar I., Moers V., Magnani D., Walcher T., Filippis C., Kricha S., Parlier D., Viviani L., Matson C.K., Nakagawa Y., Theil T., Götz M., Mallamaci M., Marine J.-C., Zarkower D., Bellefroid E.J. The doublesex homolog Dmrt5 is required for the development of the caudomedial cerebral cortex in mammals. Cereb. Cortex, in press. http://dx.doi.org/10.1093/cercor/bhs234.
57. Schlosser G. Induction and specification of cranial placodes. Dev. Biol. 2006, 294:303-351.
58. Schlosser G. Making senses development of vertebrate cranial placodes. Int. Rev. Cell Mol. Biol. 2010, 283:129-234.
59. Schwarting G.A., Gridley T., Henion T.R. Notch1 expression and ligand interactions in progenitor cells of the mouse olfactory epithelium. J. Mol. Histol. 2007, 38:543-553.
60. Seo K.W., Wang Y., Kobubo H., Kettlewell J.R., Zarkower D.A., Johnson R.L. Targeted disruption of the DM domain containing transcription factor Dmrt2 reveals an essential role in somite patterning. Dev. Biol. 2006, 290:200-210.
61. Simeone A., Acampora D., Mallamaci A., Stornaiuolo A., Rambaldi M., Boncinelli E. A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neurectoderm in the gastrulating mouse embryo. EMBO J. 1993, 12:2735-2747.
62. Sive H.L., Grainger R.M., Harland R.M. Early Development of Xenopus laevis. A laboratory manual 2000, CSHL Press, Cold Spring Harbor, NY.
63. Small E.M., Vokes S.A., Garriok R.J., Li D., Krieg P.A. Developmental expression of the xenopus Nkx2-1 and Nkx2-4 genes. Mech. Dev. 2000, 96:259-262.
64. Smith W.C., Harland R.M. Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus. Cell 1992, 70:829-840.
65. Smith C.A., Hurley T.M., McClive P.J., Sinclair A.H. Restricted expression of Dmrt3 in chicken and mouse embryos. Gene Exp. Patterns 2002, 2:69-72.
66. Sölter M., Locker M., Boy S., Taelman V., Bellefroid E.J., Perron M., Pieler T. Characterization and function of the bHLH-O protein XHes2: insight into the mechanisms controlling retinal cell fate decision. Development 2006, 133:4097-4108.
67. Streit A. The cranial sensory nervous system: specification of sensory progenitors and placodes 2008, Stembook, Cambridge, MA.
68. Tresser J., Chiba S., Veeman M., El-Nachef D., Newman-Smith E., Horie T., Tsuda M., Smith W.C. doublesex/mab3 related-1 (Dmrt1) is essential for development of anterior neural plate derivatives in Ciona. Development 2010, 137:2197-2203.
69. Veith A.M., Schäfer M., Klüver N., Schmidt C., Schultheis C., Schartl M., Volff J.N. Tissue-specific expression of Dmrt genes in embryos and adults of the platyfish Xiphophorus maculatus. Zebrafish 2006, 3:325-337.
70. Wang S.S., Tsai R.Y.L., Reed R.R. The characterization of the Olf-1/EBF-Like HLH transcription factor family: implications in olfactory gene regulation and neuronal development. J. Neurosci. 1997, 17:4149-4158.
71. Wang S.S., Lewcock J.W., Feinstein P., Mombaerts P., Reed R.R. Genetic disruptions of O/E2 and O/E3 genes reveal involvment in olfactory receptor neuron projection. Development 2004, 131:1377-1388.
72. Watanabe H., Fujisawa T., Holstein T.W. Cnidarians and the evolutionary origin of the nervous system. Dev. Growth Differ. 2009, 51:167-183.
73. Wettstein D.A., Turner D.L., Kintner C. The Xenopus homolog of Drosophila Suppressor of hairless mediates Notch signaling during primary neurogenesis. Development 1997, 124:693-702.
74. Winkler C., Hornung U., Kondo M., Neuner C., Duschl J., Shima A., Schartl M. Developmentally regulated and non-sexspecific expression of autosomal Dmrt genes in embryos of the medaka fish (oryzias latipes). Mech. Dev. 2004, 121:997-1005.
75. Wullimann M.F., Rink E., Vernier P., Schlosser G. Secondary neurogenesis in the brain of the African Clawed frog, Xenopus laevis, as revealed by PCNA, Delta-1, Neurogenin-related-1, and NeuroD expression. J. Comp. Neur. 2005, 489:387-402.
76. Yeo W., Gautier J. Early neural cell death: dying to become neurons. Dev. Biol. 2004, 274:233-244.
77. Yi W., Zarkower D. Similarity of DNA binding and transcriptional régulation by Caenorhabditis elegans MAB-3 and Drosophila melanogaster DSX suggests conservation of sex determining mechanisms. Development 1999, 126:873-881.
78. Yoshizawa A., Nakahara Y., Izawa T., Ishitani T., Tsutsumi M., Kuroiwa A., Itoh M., Kikuchi Y. Zebrafish Dmrta2 regulates neurogenesis in the telencephalon. Genes Cells 2011, 16:1097-1109.