Germ cells are required to maintain a stable sexual phenotype in adult zebrafish

Developmental Biology

Volumn 376, Issue 1, 2013, Pages 43-50

  Dranow, Daniel B ^a   Tucker, Richard P ^b   Draper, Bruce W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Germ cells; Oocyte; Sex determination

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GERM CELL; GERMLINE MICRONUCLEUS; MALE; MORPHOLOGY; NONHUMAN; NUCLEAR REPROGRAMMING; OOCYTE; PHENOTYPE; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; SERTOLI CELL; SEX DETERMINATION; SEXUAL DEVELOPMENT; SIGNAL TRANSDUCTION; SPERMATOGENESIS;

ANIMALIA; DANIO RERIO;

EID: 84875235993     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.01.016     Document Type: Article

References (51)

1. Anderson J.L., Rodriguez Mari A., Braasch I., Amores A., Hohenlohe P., Batzel P., Postlethwait J.H. Multiple sex-associated regions and a putative sex chromosome in zebrafish revealed by RAD mapping and population genomics. PLoS One 2012, 7:e40701.
2. Avise J.C., Mank J.E. Evolutionary perspectives on hermaphroditism in fishes. Sex Dev. 2009, 3:152-163.
3. Beer, R.L., Draper, B.W., 2012. nanos3 maintains germline stem cells and expression of the conserved germline stem cell gene nanos2 in the zebrafish ovary. Dev. Biol.
4. Bradley K.M., Breyer J.P., Melville D.B., Broman K.W., Knapik E.W., Smith J.R. An SNP-based linkage map for zebrafish reveals sex determination loci. G3 (Bethesda) 2011, 1:3-9.
5. Carabatsos M.J., Elvin J., Matzuk M.M., Albertini D.F. Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Dev. Biol. 1998, 204:373-384.
6. Carrasco L.A., Doroshov S., Penman D.J., Bromage N. Long-term, quantitative analysis of gametogenesis in autotriploid rainbow trout, Oncorhynchus mykiss. J. Reprod. Fertil. 1998, 113:197-210.
7. Chiang E.F., Yan Y.L., Tong S.K., Hsiao P.H., Guiguen Y., Postlethwait J., Chung B.C. Characterization of duplicated zebrafish cyp19 genes. J. Exp. Zool. 2001, 290:709-714.
8. Clelland E., Kohli G., Campbell R.K., Sharma S., Shimasaki S., Peng C. Bone morphogenetic protein-15 in the zebrafish ovary: complementary deoxyribonucleic acid cloning, genomic organization, tissue distribution, and role in oocyte maturation. Endocrinology 2006, 147:201-209.
9. Curado S., Anderson R.M., Jungblut B., Mumm J., Schroeter E., Stainier D.Y. Conditional targeted cell ablation in zebrafish: a new tool for regeneration studies. Dev. Dyn. 2007, 236:1025-1035.
10. Curado S., Stainier D.Y., Anderson R.M. Nitroreductase-mediated cell/tissue ablation in zebrafish: a spatially and temporally controlled ablation method with applications in developmental and regeneration studies. Nat. Protocol 2008, 3:948-954.
11. Devlin R.H., Nagahama Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 2002, 208:191-364.
12. Dong J., Albertini D.F., Nishimori K., Kumar T.R., Lu N., Matzuk M.M. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 1996, 383:531-535.
13. Draper B.W., McCallum C.M., Moens C.B. nanos1 is required to maintain oocyte production in adult zebrafish. Dev. Biol. 2007, 305:589-598.
14. Fujimoto T., Nishimura T., Goto-Kazeto R., Kawakami Y., Yamaha E., Arai K. Sexual dimorphism of gonadal structure and gene expression in germ cell-deficient loach, a teleost fish. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:17211-17216.
15. Goto-Kazeto R., Kight K.E., Zohar Y., Place A.R., Trant J.M. Localization and expression of aromatase mRNA in adult zebrafish. Gen. Comp. Endocrinol. 2004, 139:72-84.
16. Goto R., Saito T., Takeda T., Fujimoto T., Takagi M., Arai K., Yamaha E. Germ cells are not the primary factor for sexual fate determination in goldfish. Dev. Biol. 2012, 370:98-109.
17. Houwing S., Kamminga L.M., Berezikov E., Cronembold D., Girard A., van den Elst H., Filippov D.V., Blaser H., Raz E., Moens C.B., Plasterk R.H., Hannon G.J., Draper B.W., Ketting R.F. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell 2007, 129:69-82.
18. Kishida M., Callard G.V. Distinct cytochrome P450 aromatase isoforms in zebrafish (Danio rerio) brain and ovary are differentially programmed and estrogen regulated during early development. Endocrinology 2001, 142:740-750.
19. Kobayashi Y., Sunobe T., Kobayashi T., Nagahama Y., Nakamura M. Gonadal structure of the serial-sex changing gobiid fish Trimma okinawae. Dev. Growth Differ. 2005, 47:7-13.
20. Kurokawa H., Saito D., Nakamura S., Katoh-Fukui Y., Ohta K., Baba T., Morohashi K., Tanaka M. Germ cells are essential for sexual dimorphism in the medaka gonad. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:16958-16963.
21. Kwan K.M., Fujimoto E., Grabher C., Mangum B.D., Hardy M.E., Campbell D.S., Parant J.M., Yost H.J., Kanki J.P., Chien C.B. The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev. Dyn. 2007, 236:3088-3099.
22. Leu D.H., Draper B.W. The ziwi promoter drives germline-specific gene expression in Zebrafish. Dev. Dyn. 2010, 239:2714-2721.
23. Liew W.C., Bartfai R., Lim Z., Sreenivasan R., Siegfried K.R., Orban L. Polygenic sex determination system in Zebrafish. PLoS One 2012, 7:e34397.
24. Liu L., Ge W. Growth differentiation factor 9 and its spatiotemporal expression and regulation in the Zebrafish ovary. Biol. Reprod. 2007, 76:294-302.
25. Maack G., Segner H. Morphological development of the gonads in Zebrafish. J. Fish Biol. 2003, 62:895-906.
26. Maatouk D.M., Mork L., Hinson A., Kobayashi A., McMahon A.P., Capel B. Germ cells are not required to establish the female pathway in mouse fetal gonads. PLoS One 2012, 7:e47238.
27. Mank J.E., Promislow D.E.L., Avise J.C. Evolution of alternative sex-determining mechanisms in teleost fishes. Biol. J. Linnean Soc. 2006, 87:83-93.
28. 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.
29. McLaren A. Development of the mammalian gonad: the fate of the supporting cell lineage. BioEssays 1991, 13:151-156.
30. Nakamura S., Aoki Y., Saito D., Kuroki Y., Fujiyama A., Naruse K., Tanaka M. Sox9b/sox9a2-EGFP transgenic medaka reveals the morphological reorganization of the gonads and a common precursor of both the female and male supporting cells. Mol. Reprod. Dev. 2008, 75:472-476.
31. Nakamura S., Kurokawa H., Asakawa S., Shimizu N., Tanaka M. Two distinct types of theca cells in the medaka gonad: germ cell-dependent maintenance of cyp19a1-expressing theca cells. Dev. Dyn. 2009, 238:2652-2657.
32. Okutsu T., Suzuki K., Takeuchi Y., Takeuchi T., Yoshizaki G. Testicular germ cells can colonize sexually undifferentiated embryonic gonad and produce functional eggs in fish. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:2725-2729.
33. Rodriguez-Mari A., Canestro C., Bremiller R.A., Nguyen-Johnson A., Asakawa K., Kawakami K., Postlethwait J.H. Sex reversal in zebrafish fancl mutants is caused by Tp53-mediated germ cell apoptosis. PLoS Genet. 2010, 6:e1001034.
34. Rodriguez-Mari A., Yan Y.L., Bremiller R.A., Wilson C., Canestro C., Postlethwait J.H. Characterization and expression pattern of zebrafish anti-mullerian hormone (Amh) relative to sox9a, sox9b, and cyp19a1a, during gonad development. Gene Expression Patterns 2005, 5:655-667.
35. Rohner N., Perathoner S., Frohnhofer H.G., Harris M.P. Enhancing the efficiency of N-ethyl-N-nitrosourea-induced mutagenesis in the zebrafish. Zebrafish 2011, 8:119-123.
36. Schilling T. The morphology of larval and adult zebrafish. Zebrafish: A Practical Approach 2002, 59-94. Oxford University Press, Oxford. 1st ed. C. Nusslein-Volhard, R. Dahm (Eds.).
37. Siegfried K.R., Nusslein-Volhard C. Germ line control of female sex determination in zebrafish. Dev. Biol. 2008, 324:277-287.
38. Simpson E.R., Mahendroo M.S., Means G.D., Kilgore M.W., Hinshelwood M.M., Graham-Lorence S., Amarneh B., Ito Y., Fisher C.R., Michael M.D., et al. Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr. Rev. 1994, 15:342-355.
39. Slanchev K., Stebler J., de la Cueva-Mendez G., Raz E. Development without germ cells: the role of the germ line in zebrafish sex differentiation. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:4074-4079.
40. Spence R., Gerlach G., Lawrence C., Smith C. The behaviour and ecology of the zebrafish, Danio rerio. Biol. Rev. Cambridge Philos. Soc. 2008, 83:13-34.
41. Su Y.Q., Wu X., O'Brien M.J., Pendola F.L., Denegre J.N., Matzuk M.M., Eppig J.J. Synergistic roles of BMP15 and GDF9 in the development and function of the oocyte-cumulus cell complex in mice: genetic evidence for an oocyte-granulosa cell regulatory loop. Dev. Biol. 2004, 276:64-73.
42. Sugiura K., Su Y.Q., Diaz F.J., Pangas S.A., Sharma S., Wigglesworth K., O'Brien M.J., Matzuk M.M., Shimasaki S., Eppig J.J. Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development 2007, 134:2593-2603.
43. Takahashi H. Juvenile hermaphroditism in the zebrafish, Brachydanio rerio. Bull. Fac. Fish. Hokkaido Uni. 1977, 28:57-65.
44. Thisse C., Thisse B. High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protocol 2008, 3:59-69.
45. Uchida D., Yamashita M., Kitano T., Iguchi T. An aromatase inhibitor or high water temperature induce oocyte apoptosis and depletion of P450 aromatase activity in the gonads of genetic female zebrafish during sex-reversal. Comp. Biochem. Physiol. A Mol. Integrative Physiol. 2004, 137:11-20.
46. Uhlenhaut N.H., Jakob S., Anlag K., Eisenberger T., Sekido R., Kress J., Treier A.C., Klugmann C., Klasen C., Holter N.I., Riethmacher D., Schutz G., Cooney A.J., Lovell-Badge R., Treier M. Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 2009, 139:1130-1142.
47. Villefranc J.A., Amigo J., Lawson N.D. Gateway compatible vectors for analysis of gene function in the zebrafish. Dev. Dyn. 2007, 236:3077-3087.
48. Westerfield The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio) 2000, University of Oregon Press, Eugene. 4th ed.
49. Wong T.T., Saito T., Crodian J., Collodi P. Zebrafish germline chimeras produced by transplantation of ovarian germ cells into sterile host larvae. Biol. Reprod. 2011, 84:1190-1197.
50. Yan C., Wang P., DeMayo J., DeMayo F.J., Elvin J.A., Carino C., Prasad S.V., Skinner S.S., Dunbar B.S., Dube J.L., Celeste A.J., Matzuk M.M. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol. Endocrinol. 2001, 15:854-866.
51. Yoshizaki G., Ichikawa M., Hayashi M., Iwasaki Y., Miwa M., Shikina S., Okutsu T. Sexual plasticity of ovarian germ cells in rainbow trout. Development 2010, 137:1227-1230.