Germ cell sex determination: A collaboration between soma and germline

Current Opinion in Cell Biology

Volumn 22, Issue 6, 2010, Pages 722-729

  Murray, Sheryl M ^a   Yang, Shu Yuan ^a   Van Doren, Mark ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; ENDOSPERM; GAMETE; GENDER IDENTITY; GERM CELL; NONHUMAN; OOCYTE; PRIORITY JOURNAL; REVIEW; SEX CHROMOSOME; SEX DETERMINATION; SEXUAL DEVELOPMENT; SOMATIC CELL;

ANIMALS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM CELLS; MALE; OOCYTES; SEX DETERMINATION PROCESSES; SPERMATOZOA;

EID: 78649634788     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2010.09.006     Document Type: Review

References (103)

1. Hilfiker-Kleiner D., Dubendorfer A., Hilfiker A., Nothiger R. Genetic control of sex determination in the germ line and soma of the housefly, Musca domestica. Development 1994, 120:2531-2538.
2. Blackler A.W. Germ-cell transfer and sex ratio in Xenopus laevis. J Embryol Exp Morphol 1965, 13:51-61.
3. 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.
4. 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.
5. Shinomiya A., Shibata N., Sakaizumi M., Hamaguchi S. Sex reversal of genetic females (XX) induced by the transplantation of XY somatic cells in the medaka, Oryzias latipes. Int J Dev Biol 2002, 46:711-717.
6. Camara N., Whitworth C., Van Doren M. The creation of sexual dimorphism in the Drosophila soma. Curr Top Dev Biol 2008, 83:65-107.
7. Hempel L.U., Kalamegham R., Smith J.E., Oliver B. Drosophila germline sex determination: integration of germline autonomous cues and somatic signals. Curr Top Dev Biol 2008, 83:109-150.
8. Wolff J.R., Zarkower D. Somatic sexual differentiation in Caenorhabditis elegans. Curr Top Dev Biol 2008, 83:1-39.
9. Ellis R.E. Sex determination in the Caenorhabditis elegans germ line. Curr Top Dev Biol 2008, 83:41-64.
10. Durcova-Hills G., Capel B. Development of germ cells in the mouse. Curr Top Dev Biol 2008, 83:185-212.
11. Maatouk D.M., Capel B. Sexual development of the soma in the mouse. Curr Top Dev Biol 2008, 83:151-183.
12. Van Deusen E.B. Sex determination in germ line chimeras of Drosophila melanogaster. J Embryol Exp Morphol 1977, 37:173-185.
13. Steinmann-Zwicky M., Schmid H., Nothiger R. Cell-autonomous and inductive signals can determine the sex of the germ line of drosophila by regulating the gene Sxl. Cell 1989, 57:157-166.
14. Hinson S., Nagoshi R.N. Regulatory and functional interactions between the somatic sex regulatory gene transformer and the germline genes ovo and ovarian tumor. Development 1999, 126:861-871.
15. Waterbury J.A., Horabin J.I., Bopp D., Schedl P. Sex determination in the Drosophila germline is dictated by the sexual identity of the surrounding soma. Genetics 2000, 155:1741-1756.
16. Kelley R.L., Wang J., Bell L., Kuroda M.I. Sex lethal controls dosage compensation in Drosophila by a non-splicing mechanism. Nature 1997, 387:195-199.
17. Hildreth P.E. Doublesex, recessive gene that transforms both males and females of Drosophila into intersexes. Genetics 1965, 51:659-678.
18. 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.
19. Rideout E.J., Billeter J.C., Goodwin S.F. The sex-determination genes fruitless and doublesex specify a neural substrate required for courtship song. Curr Biol 2007, 17:1473-1478.
20. Robinett C.C., Vaughan A.G., Knapp J.M., Baker B.S. Sex and the single cell. II. There is a time and place for sex. PLoS Biol 2010, 8:e1000365.
21. Hempel L.U., Oliver B. Sex-specific DoublesexM expression in subsets of Drosophila somatic gonad cells. BMC Dev Biol 2007, 7:113.
22. DeFalco T., Camara N., Le Bras S., Van Doren M. Nonautonomous sex determination controls sexually dimorphic development of the Drosophila gonad. Dev Cell 2008, 14:275-286.
23. Steinmann-Zwicky M. Sex determination of the Drosophila germ line: tra and dsx control somatic inductive signals. Development 1994, 120:707-716.
24. Casper A.L., Van Doren M. The establishment of sexual identity in the Drosophila germline. Development 2009, 136:3821-3830.
25. Wei G., Oliver B., Mahowald A.P. Gonadal dysgenesis reveals sexual dimorphism in the embryonic germline of Drosophila. Genetics 1991, 129:203-210.
26. Staab S., Heller A., Steinmann-Zwicky M. Somatic sex-determining signals act on XX germ cells in Drosophila embryos. Development 1996, 122:4065-4071.
27. Janzer B., Steinmann-Zwicky M. Cell-autonomous and somatic signals control sex-specific gene expression in XY germ cells of Drosophila. Mech Dev 2001, 100:3-13.
28. Wawersik M., Milutinovich A., Casper A.L., Matunis E., Williams B., Van Doren M. Somatic control of germline sexual development is mediated by the JAK/STAT pathway. Nature 2005, 436:563-567.
29. Heller A., Steinmann-Zwicky M. In Drosophila, female gonadal cells repress male-specific gene expression in XX germ cells. Mech Dev 1998, 73:203-209.
30. Casper A., Van Doren M. The control of sexual identity in the Drosophila germline. Development 2006, 133:2783-2791.
31. Marsh J.L., Wieschaus E. Is sex determination in germ line and soma controlled by separate genetic mechanisms?. Nature 1978, 272:249-251.
32. Schupbach T. Autosomal mutations that interfere with sex determination in somatic cells of Drosophila have no direct effect on the germline. Dev Biol 1982, 89:117-127.
33. Schupbach T. Normal female germ cell differentiation requires the female X chromosome to autosome ratio and expression of sex-lethal in Drosophila melanogaster. Genetics 1985, 109:529-548.
34. Steinmann-Zwicky M. Sex determination in Drosophila: sis-b, a major numerator element of the X:A ratio in the soma, does not contribute to the X:A ratio in the germ line. Development 1993, 117:763-767.
35. Granadino B., Santamaria P., Sanchez L. Sex determination in the germ line of Drosophila melanogaster: activation of the gene Sex-lethal. Development 1993, 118:813-816.
36. Hager J.H., Cline T.W. Induction of female Sex-lethal RNA splicing in male germ cells: implications for Drosophila germline sex determination. Development 1997, 124:5033-5048.
37. Oliver B., Perrimon N., Mahowald A.P. The ovo locus is required for sex-specific germ line maintenance in Drosophila. Genes Dev 1987, 1:913-923.
38. King R. Aberrant fusomes in the ovarian cystocytes of the fs(1)231 mutant of Drosophila melanogaster Meigen (diptera: drosophilidae). Int J Insect Morph Embryol 1979, 8:297-309.
39. Lu J., Andrews J., Pauli D., Oliver B. Drosophila OVO zinc-finger protein regulates ovo and ovarian tumor target promoters. Dev Genes Evol 1998, 208:213-222.
40. Lee S., Garfinkel M.D. Characterization of Drosophila OVO protein DNA binding specificity using random DNA oligomer selection suggests zinc finger degeneration. Nucleic Acids Res 2000, 28:826-834.
41. Lu J., Oliver B. Drosophila OVO regulates ovarian tumor transcription by binding unusually near the transcription start site. Development 2001, 128:1671-1686.
42. Wei G., Oliver B., Pauli D., Mahowald A.P. Evidence for sex transformation of germline cells in ovarian tumor mutants of Drosophila. Dev Biol 1994, 161:318-320.
43. Oliver B., Singer J., Laget V., Pennetta G., Pauli D. Function of Drosophila ovo+ in germ-line sex determination depends on X-chromosome number. Development 1994, 120:3185-3195.
44. Andrews J., Oliver B. Sex determination signals control ovo-B transcription in Drosophila melanogaster germ cells. Genetics 2002, 160:537-545.
45. Evans P.C., Smith T.S., Lai M.J., Williams M.G., Burke D.F., Heyninck K., Kreike M.M., Beyaert R., Blundell T.L., Kilshaw P.J. A novel type of deubiquitinating enzyme. J Biol Chem 2003, 278:23180-23186.
46. Hashiyama K., Shigenobu S., Kobayashi S. Expression of genes involved in sumoylation in the Drosophila germline. Gene Expr Patterns 2009, 9:50-53.
47. Kimble J., Crittenden S.L. Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans. Annu Rev Cell Dev Biol 2007, 23:405-433.
48. Hunter C.P., Wood W.B. Evidence from mosaic analysis of the masculinizing gene her-1 for cell interactions in C. elegans sex determination. Nature 1992, 355:551-555.
49. Perry M.D., Li W., Trent C., Robertson B., Fire A., Hageman J.M., Wood W.B. Molecular characterization of the her-1 gene suggests a direct role in cell signaling during Caenorhabditis elegans sex determination. Genes Dev 1993, 7:216-228.
50. Doniach T., Hodgkin J. A sex-determining gene, fem-1, required for both male and hermaphrodite development in Caenorhabditis elegans. Dev Biol 1984, 106:223-235.
51. Hodgkin J. Sex determination in the nematode C. elegans: analysis of tra-3 suppressors and characterization of fem genes. Genetics 1986, 114:15-52.
52. Barton M.K., Kimble J. fog-1, a regulatory gene required for specification of spermatogenesis in the germ line of Caenorhabditis elegans. Genetics 1990, 125:29-39.
53. Ellis R.E., Kimble J. The fog-3 gene and regulation of cell fate in the germ line of Caenorhabditis elegans. Genetics 1995, 139:561-577.
54. Haag E.S. Chapter 3. Caenorhabditis nematodes as a model for the adaptive evolution of germ cells. Curr Top Dev Biol 2009, 86:43-66.
55. Baldi C., Cho S., Ellis R.E. Mutations in two independent pathways are sufficient to create hermaphroditic nematodes. Science 2009, 326:1002-1005.
56. Schedl T., Kimble J. fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics 1988, 119:43-61.
57. Francis R., Maine E., Schedl T. Analysis of the multiple roles of gld-1 in germline development: interactions with the sex determination cascade and the glp-1 signaling pathway. Genetics 1995, 139:607-630.
58. Jan E., Motzny C.K., Graves L.E., Goodwin E.B. The STAR protein, GLD-1, is a translational regulator of sexual identity in Caenorhabditis elegans. EMBO J 1999, 18:258-269.
59. Ahringer J., Kimble J. Control of the sperm-oocyte switch in Caenorhabditis elegans hermaphrodites by the fem-3,3' untranslated region. Nature 1991, 349:346-348.
60. Zhang B., Gallegos M., Puoti A., Durkin E., Fields S., Kimble J., Wickens M.P. A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line. Nature 1997, 390:477-484.
61. Kraemer B., Crittenden S., Gallegos M., Moulder G., Barstead R., Kimble J., Wickens M. NANOS-3 and FBF proteins physically interact to control the sperm-oocyte switch in Caenorhabditis elegans. Curr Biol 1999, 9:1009-1018.
62. Crittenden S.L., Bernstein D.S., Bachorik J.L., Thompson B.E., Gallegos M., Petcherski A.G., Moulder G., Barstead R., Wickens M., Kimble J. A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 2002, 417:660-663.
63. Graham P.L., Kimble J. The mog-1 gene is required for the switch from spermatogenesis to oogenesis in Caenorhabditis elegans. Genetics 1993, 133:919-931.
64. Graham P.L., Schedl T., Kimble J. More mog genes that influence the switch from spermatogenesis to oogenesis in the hermaphrodite germ line of Caenorhabditis elegans. Dev Genet 1993, 14:471-484.
65. Kasturi P., Zanetti S., Passannante M., Saudan Z., Muller F., Puoti A. The C. elegans sex determination protein MOG-3 functions in meiosis and binds to the CSL co-repressor CIR-1. Dev Biol 2010, 344(2):593-602.
66. Li W., Boswell R., Wood W.B. mag-1, a homolog of Drosophila mago nashi, regulates hermaphrodite germ-line sex determination in Caenorhabditis elegans. Dev Biol 2000, 218:172-182.
67. Kawano T., Kataoka N., Dreyfuss G., Sakamoto H. Ce-Y14 and MAG-1, components of the exon-exon junction complex, are required for embryogenesis and germline sexual switching in Caenorhabditis elegans. Mech Dev 2004, 121:27-35.
68. McCarter J., Bartlett B., Dang T., Schedl T. Soma-germ cell interactions in Caenorhabditis elegans: multiple events of hermaphrodite germline development require the somatic sheath and spermathecal lineages. Dev Biol 1997, 181:121-143.
69. Cho S., Rogers K.W., Fay DS: The C. elegans glycopeptide hormone receptor orthologm, FSHR-1, regulates germline differentiation and survival. Curr Biol 2007, 17:203-212.
70. Taketo-Hosotani T., Nishioka Y., Nagamine C.M., Villalpando I., Merchant-Larios H. Development and fertility of ovaries in the B6.YDOM sex-reversed female mouse. Development 1989, 107:95-105.
71. McLaren A. The fate of germ cells in the testis of fetal Sex-reversed mice. J Reprod Fertil 1981, 61:461-467.
72. Hunt P.A., Worthman C., Levinson H., Stallings J., LeMaire R., Mroz K., Park C., Handel M.A. Germ cell loss in the XXY male mouse: altered X-chromosome dosage affects prenatal development. Mol Reprod Dev 1998, 49:101-111.
73. Eicher E.M., Washburn L.L., Whitney J.B., Morrow K.E. Mus poschiavinus Y chromosome in the C57BL/6J murine genome causes sex reversal. Science 1982, 217:535-537.
74. Koopman P., Gubbay J., Vivian N., Goodfellow P., Lovell-Badge R. Male development of chromosomally female mice transgenic for Sry. Nature 1991, 351:117-121.
75. Lovell-Badge R., Robertson E. XY female mice resulting from a heritable mutation in the primary testis-determining gene, Tdy. Development 1990, 109:635-646.
76. Sekido R., Lovell-Badge R. Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 2008, 453:930-934.
77. DeFalco T., Capel B. Gonad morphogenesis in vertebrates: divergent means to a convergent end. Annu Rev Cell Dev Biol 2009, 25:457-482.
78. Colvin J.S., Green R.P., Schmahl J., Capel B., Ornitz D.M. Male-to-female sex reversal in mice lacking fibroblast growth factor 9. Cell 2001, 104:875-889.
79. Uhlenhaut N.H., Jakob S., Anlag K., Eisenberger T., Sekido R., Kress J., Treier A.C., Klugmann C., Klasen C., Holter N.I., et al. Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 2009, 139:1130-1142.
80. Kim Y., Kobayashi A., Sekido R., DiNapoli L., Brennan J., Chaboissier M.C., Poulat F., Behringer R.R., Lovell-Badge R., Capel B. Fgf9 and Wnt4 act as antagonistic signals to regulate mammalian sex determination. PLoS Biol 2006, 4:e187.
81. Ottolenghi C., Pelosi E., Tran J., Colombino M., Douglass E., Nedorezov T., Cao A., Forabosco A., Schlessinger D. Loss of Wnt4 and Foxl2 leads to female-to-male sex reversal extending to germ cells. Hum Mol Genet 2007, 16:2795-2804.
82. DiNapoli L., Batchvarov J., Capel B. FGF9 promotes survival of germ cells in the fetal testis. Development 2006, 133:1519-1527.
83. Naillat F., Prunskaite-Hyyrylainen R., Pietila I., Sormunen R., Jokela T., Shan J., Vainio S.J. Wnt4/5a signalling coordinates cell adhesion and entry into meiosis during presumptive ovarian follicle development. Hum Mol Genet 2010, 19:1539-1550.
84. Bowles J., Knight D., Smith C., Wilhelm D., Richman J., Mamiya S., Yashiro K., Chawengsaksophak K., Wilson M.J., Rossant J., et al. Retinoid signaling determines germ cell fate in mice. Science 2006, 312:596-600.
85. Koubova J., Menke D.B., Zhou Q., Capel B., Griswold M.D., Page D.C. Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl Acad Sci U S A 2006, 103:2474-2479.
86. Baltus A.E., Menke D.B., Hu Y.C., Goodheart M.L., Carpenter A.E., de Rooij D.G., Page D.C. In germ cells of mouse embryonic ovaries, the decision to enter meiosis precedes premeiotic DNA replication. Nat Genet 2006, 38:1430-1434.
87. Wang N., Tilly J.L. Epigenetic status determines germ cell meiotic commitment in embryonic and postnatal mammalian gonads. Cell Cycle 2010, 9:339-349.
88. Tsuda M., Sasaoka Y., Kiso M., Abe K., Haraguchi S., Kobayashi S., Saga Y. Conserved role of nanos proteins in germ cell development. Science 2003, 301:1239-1241.
89. Kusz K.M., Tomczyk L., Sajek M., Spik A., Latos-Bielenska A., Jedrzejczak P., Pawelczyk L., Jaruzelska J. The highly conserved NANOS2 protein: testis-specific expression and significance for the human male reproduction. Mol Hum Reprod 2009, 15:165-171.
90. Suzuki A., Igarashi K., Aisaki K., Kanno J., Saga Y. NANOS2 interacts with the CCR4-NOT deadenylation complex and leads to suppression of specific RNAs. Proc Natl Acad Sci U S A 2010, 107:3594-3599.
91. Suzuki A., Saga Y. Nanos2 suppresses meiosis and promotes male germ cell differentiation. Genes Dev 2008, 22:430-435.
92. Barrios F., Filipponi D., Pellegrini M., Paronetto M.P., Di Siena S., Geremia R., Rossi P., De Felici M., Jannini E.A., Dolci S. Opposing effects of retinoic acid and FGF9 on Nanos2 expression and meiotic entry of mouse germ cells. J Cell Sci 2010, 123:871-880.
93. Mroz K., Hassold T.J., Hunt P.A. Meiotic aneuploidy in the XXY mouse: evidence that a compromised testicular environment increases the incidence of meiotic errors. Hum Reprod 1999, 14:1151-1156.
94. Cattanach B.M., Pollard C.E., Hawker S.G. Sex-reversed mice: XX and XO males. Cytogenetics 1971, 10:318-337.
95. McLaren A. Germ cells and germ cell sex. Philos Trans R Soc Lond B Biol Sci 1995, 350:229-233.
96. Durcova-Hills G., Hajkova P., Sullivan S., Barton S., Surani M.A., McLaren A. Influence of sex chromosome constitution on the genomic imprinting of germ cells. Proc Natl Acad Sci U S A 2006, 103:11184-11188.
97. Durcova-Hills G., Burgoyne P., McLaren A. Analysis of sex differences in EGC imprinting. Dev Biol 2004, 268:105-110.
98. 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.
99. Dubendorfer A., Hediger M., Burghardt G., Bopp D. Musca domestica, a window on the evolution of sex-determining mechanisms in insects. Int J Dev Biol 2002, 46:75-79.
100. Berta P., Hawkins J.R., Sinclair A.H., Taylor A., Griffiths B.L., Goodfellow P.N., Fellous M. Genetic evidence equating SRY and the testis-determining factor. Nature 1990, 348:448-450.
101. Wikstrom A.M., Dunkel L. Testicular function in Klinefelter syndrome. Horm Res 2008, 69:317-326.
102. Sciurano R.B., Luna Hisano C.V., Rahn M.I., Brugo Olmedo S., Rey Valzacchi G., Coco R., Solari A.J. Focal spermatogenesis originates in euploid germ cells in classical Klinefelter patients. Hum Reprod 2009, 24:2353-2360.
103. Bergere M., Wainer R., Nataf V., Bailly M., Gombault M., Ville Y., Selva J. Biopsied testis cells of four 47,XXY patients: fluorescence in-situ hybridization and ICSI results. Hum Reprod 2002, 17:32-37.