Sex and the circuitry: Progress toward a systems-level understanding of vertebrate sex determination

Wiley Interdisciplinary Reviews: Systems Biology and Medicine

Volumn 4, Issue 4, 2012, Pages 401-412

  Munger, Steven C ^a   Capel, Blanche ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 9; OCTAMER TRANSCRIPTION FACTOR; PROSTAGLANDIN D2; TRANSCRIPTION FACTOR SOX9; WNT4 PROTEIN;

ARTICLE; CELL PROLIFERATION; GENE MUTATION; GENETIC RESOURCE; GONAD; HUMAN; MEDICAL DECISION MAKING; NONHUMAN; OUTCOME ASSESSMENT; PHENOTYPE; PREDICTION; PROTEIN EXPRESSION; SEX DETERMINATION; SEX DETERMINATION PROCESS; SEXUAL DEVELOPMENT; TESTIS; VERTEBRATE;

ANIMALS; FEMALE; GENE REGULATORY NETWORKS; GONADS; MALE; MICE; OVARY; SEX DETERMINATION PROCESSES; SOX9 TRANSCRIPTION FACTOR; TESTIS; VERTEBRATES; X CHROMOSOME; Y CHROMOSOME;

EID: 84862530428     PISSN: 19395094     EISSN: 1939005X     Source Type: Journal    
DOI: 10.1002/wsbm.1172     Document Type: Article

References (75)

1. Sekido R, Lovell-Badge R. Sex determination and SRY: down to a wink and a nudge? Trends Genet 2009, 25:19-29.
2. Wainwright EN, Wilhelm D. The game plan: cellular and molecular mechanisms of mammalian testis development. Curr Top Dev Biol 2010, 90:231-262.
3. Liu CF, Liu C, Yao HH. Building pathways for ovary organogenesis in the mouse embryo. Curr Top Dev Biol 2010, 90:263-290.
4. Nef S, Schaad O, Stallings NR, Cederroth CR, Pitetti JL, Schaer G, Malki S, Dubois-Dauphin M, Boizet-Bonhoure B, Descombes P, et al. Gene expression during sex determination reveals a robust female genetic program at the onset of ovarian development. Dev Biol 2005, 287:361-377.
5. Beverdam A, Koopman P. Expression profiling of purified mouse gonadal somatic cells during the critical time window of sex determination reveals novel candidate genes for human sexual dysgenesis syndromes. Hum Mol Genet 2006, 15:417-431.
6. Kim Y, Kobayashi A, Sekido R, DiNapoli L, Brennan J, Chaboissier MC, Poulat F, Behringer RR, Lovell-Badge R, Capel B. Fgf9 and Wnt4 act as antagonistic signals to regulate mammalian sex determination. PLoS Biol 2006, 4:e187.
7. Munger SC, Aylor DL, Syed HA, Magwene PM, Threadgill DW, Capel B. Elucidation of the transcription network governing mammalian sex determination by exploiting strain-specific susceptibility to sex reversal. Genes Dev 2009, 23:2521-2536.
8. Jameson SA, Natarajan A, Cool J, Defalco T, Maatouk DM, Mork L, Munger SC, Capel B. Temporal transcriptional profiling of somatic and germ cells reveals biased lineage priming of sexual fate in the fetal mouse gonad. PLoS Genet 2012, 8:e1002575.
9. Vainio S, Heikkila M, Kispert A, Chin N, McMahon AP. Female development in mammals is regulated by Wnt-4 signalling. Nature 1999, 397:405-409.
10. Parma P, Radi O, Vidal V, Chaboissier MC, Dellambra E, Valentini S, Guerra L, Schedl A, Camerino G. R-spondin1 is essential in sex determination, skin differentiation and malignancy. Nat Genet 2006, 38:1304-1309.
11. Hiramatsu R, Matoba S, Kanai-Azuma M, Tsunekawa N, Katoh-Fukui Y, Kurohmaru M, Morohashi K, Wilhelm D, Koopman P, Kanai Y. A critical time window of Sry action in gonadal sex determination in mice. Development 2009, 136:129-138.
12. Palmer SJ, Burgoyne PS. In situ analysis of fetal, prepuberal and adult XX-XY chimaeric mouse testes: sertoli cells are predominantly, but not exclusively, XY. Development 1991, 112:265-268.
13. Gubbay J, Collignon J, Koopman P, Capel B, Economou A, Munsterberg A, Vivian N, Goodfellow P, Lovell-Badge R. A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature 1990, 346:245-250.
14. Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, Smith MJ, Foster JW, Frischauf AM, Lovell-Badge R, Goodfellow PN. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 1990, 346:240-244.
15. Sekido R, Bar I, Narvaez V, Penny G, Lovell-Badge R. SOX9 is up-regulated by the transient expression of SRY specifically in Sertoli cell precursors. Dev Biol 2004, 274:271-279.
16. Koopman P, Munsterberg A, Capel B, Vivian N, Lovell-Badge R. Expression of a candidate sex-determining gene during mouse testis differentiation. Nature 1990, 348:450-452.
17. Albrecht KH, Eicher EM. Evidence that Sry is expressed in pre-Sertoli cells and Sertoli and granulosa cells have a common precursor. Dev Biol 2001, 240:92-107.
18. Bullejos M, Koopman P. Spatially dynamic expression of Sry in mouse genital ridges. Dev Dyn 2001, 221:201-205.
19. Kreidberg JA, Sariola H, Loring JM, Maeda M, Pelletier J, Housman D, Jaenisch R. WT-1 is required for early kidney development. Cell 1993, 74:679-691.
20. Hammes A, Guo JK, Lutsch G, Leheste JR, Landrock D, Ziegler U, Gubler MC, Schedl A. Two splice variants of the Wilms' tumor 1 gene have distinct functions during sex determination and nephron formation. Cell 2001, 106:319-329.
21. Luo X, Ikeda Y, Parker KL. A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell 1994, 77:481-490.
22. Birk OS, Casiano DE, Wassif CA, Cogliati T, Zhao L, Zhao Y, Grinberg A, Huang S, Kreidberg JA, Parker KL, et al. The LIM homeobox gene Lhx9 is essential for mouse gonad formation. Nature 2000, 403:909-913.
23. Miyamoto N, Yoshida M, Kuratani S, Matsuo I, Aizawa S. Defects of urogenital development in mice lacking Emx2. Development 1997, 124:1653-1664.
24. Katoh-Fukui Y, Tsuchiya R, Shiroishi T, Nakahara Y, Hashimoto N, Noguchi K, Higashinakagawa T. Male-to-female sex reversal in M33 mutant mice. Nature 1998, 393:688-692.
25. Nef S, Verma-Kurvari S, Merenmies J, Vassalli JD, Efstratiadis A, Accili D, Parada LF. Testis determination requires insulin receptor family function in mice. Nature 2003, 426:291-295.
26. Tevosian SG, Albrecht KH, Crispino JD, Fujiwara Y, Eicher EM, Orkin SH. Gonadal differentiation, sex determination and normal Sry expression in mice require direct interaction between transcription partners GATA4 and FOG2. Development 2002, 129:4627-4634.
27. Sekido R, Lovell-Badge R. Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 2008, 453:930-934.
28. Smith CA, Roeszler KN, Ohnesorg T, Cummins DM, Farlie PG, Doran TJ, Sinclair AH. The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 2009, 461:267-271.
29. Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, et al. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 2002, 417:559-563.
30. Janzen FJ, Phillips PC. Exploring the evolution of environmental sex determination, especially in reptiles. J Evol Biol 2006, 19:1775-1784.
31. Quinn AE, Georges A, Sarre SD, Guarino F, Ezaz T, Graves JA. Temperature sex reversal implies sex gene dosage in a reptile. Science 2007, 316:411.
32. Radder RS, Quinn AE, Georges A, Sarre SD, Shine R. Genetic evidence for co-occurrence of chromosomal and thermal sex-determining systems in a lizard. Biol Lett 2008, 4:176-178.
33. Barske LA, Capel B. Estrogen represses SOX9 during sex determination in the red-eared slider turtle Trachemys scripta. Dev Biol 2010, 341:305-314.
34. Wilhelm D, Martinson F, Bradford S, Wilson MJ, Combes AN, Beverdam A, Bowles J, Mizusaki H, Koopman P. Sertoli cell differentiation is induced both cell-autonomously and through prostaglandin signaling during mammalian sex determination. Dev Biol 2005, 287:111-124.
35. Bouma GJ, Albrecht KH, Washburn LL, Recknagel AK, Churchill GA, Eicher EM. Gonadal sex reversal in mutant Dax1 XY mice: a failure to upregulate Sox9 in pre-Sertoli cells. Development 2005, 132:3045-3054.
36. Nikolova G, Sinsheimer JS, Eicher EM, Vilain E. The chromosome 11 region from strain 129 provides protection from sex reversal in XYPOS mice. Genetics 2008, 179:419-427.
37. Uhlenhaut NH, Jakob S, Anlag K, Eisenberger T, Sekido R, Kress J, Treier AC, Klugmann C, Klasen C, Holter NI, et al. Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 2009, 139:1130-1142.
38. Wilhelm D, Washburn LL, Truong V, Fellous M, Eicher EM, Koopman P. Antagonism of the testis- and ovary-determining pathways during ovotestis development in mice. Mech Dev 2009, 126:324-336.
39. Bullejos M, Koopman P. Delayed Sry and Sox9 expression in developing mouse gonads underlies B6-Y(DOM) sex reversal. Dev Biol 2005, 278:473-481.
40. Morrish BC, Sinclair AH. Vertebrate sex determination: many means to an end. Reproduction 2002, 124:447-457.
41. Pask AJ, Calatayud NE, Shaw G, Wood WM, Renfree MB. Oestrogen blocks the nuclear entry of SOX9 in the developing gonad of a marsupial mammal. BMC Biol 2010, 8:113.
42. de Santa Barbara P, Moniot B, Poulat F, Berta P. Expression and subcellular localization of SF-1, SOX9, WT1, and AMH proteins during early human testicular development. Dev Dyn 2000, 217:293-298.
43. Matson CK, Murphy MW, Sarver AL, Griswold MD, Bardwell VJ, Zarkower D. DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 2011, 476:101-104.
44. Guo G, Huss M, Tong GQ, Wang C, Li Sun L, Clarke ND, Robson P. Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev Cell 2010, 18:675-685.
45. Tang F, Barbacioru C, Bao S, Lee C, Nordman E, Wang X, Lao K, Surani MA. Tracing the derivation of embryonic stem cells from the inner cell mass by single-cell RNA-Seq analysis. Cell Stem Cell 2010, 6:468-478.
46. Brennan J, Tilmann C, Capel B. Pdgfr-alpha mediates testis cord organization and fetal Leydig cell development in the XY gonad. Genes Dev 2003, 17:800-810.
47. Bitgood MJ, Shen L, McMahon AP. Sertoli cell signaling by Desert hedgehog regulates the male germline. Curr Biol 1996, 6:298-304.
48. Eicher EM, Washburn LL. Inherited sex reversal in mice: identification of a new primary sex-determining gene. J Exp Zool 1983, 228:297-304.
49. DeFalco T, Capel B. Gonad morphogenesis in vertebrates: divergent means to a convergent end. Annu Rev Cell Dev Biol 2009, 25:457-482.
50. Yanai I, Peshkin L, Jorgensen P, Kirschner MW. Mapping gene expression in two Xenopus species: evolutionary constraints and developmental flexibility. Dev Cell 2011, 20:483-496.
51. Tohonen V, Frygelius J, Mohammadieh M, Kvist U, Pelliniemi LJ, O'Brien K, Nordqvist K, Wedell A. Normal sexual development and fertility in testatin knockout mice. Mol Cell Biol 2005, 25:4892-4902.
52. Ross A, Munger S, Capel B. Bmp7 regulates germ cell proliferation in mouse fetal gonads. Sex Dev 2007, 1:127-137.
53. Frygelius J, Oscarson M, Nordqvist K, Wedell A, Tohonen V. The reproductive tissue specific cystatin subgroup of genes: expression during gonadal development in wildtype and testatin knockout animals. Sex Dev 2007, 1:363-372.
54. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A, et al. Finding the missing heritability of complex diseases. Nature 2009, 461:747-753.
55. Roberts A, Pardo-Manuel de Villena F, Wang W, McMillan L, Threadgill DW. The polymorphism architecture of mouse genetic resources elucidated using genome-wide resequencing data: implications for QTL discovery and systems genetics. Mamm Genome 2007, 18:473-481.
56. Aylor DL, Valdar W, Foulds-Mathes W, Buus RJ, Verdugo RA, Baric RS, Ferris MT, Frelinger JA, Heise M, Frieman MB, et al. Genetic analysis of complex traits in the emerging collaborative cross. Genome Res 2011, 21:1213-1222.
57. Durrant C, Tayem H, Yalcin B, Cleak J, Goodstadt L, Pardo-Manuel de Villena F, Mott R, Iraqi F. Collaborative cross mice and their power to map host susceptibility to Aspergillus fumigatus infection. Genome Res 2011, 21:1239-1248.
58. Mathes WF, Aylor DL, Miller DR, Churchill GA, Chesler EJ, Pardo Manuel de Villena F, Threadgill DW, Pomp D. Architecture of energy balance traits in emerging lines of the Collaborative Cross. Am J Physiol Endocrinol Metab 2011, 300:E1124-1134.
59. Svenson K, Gatti D, Valdar W, Welsh CE, Cheng R, Chesler E, Palmer AA, McMillan L, Churchill GA. The mouse diversity outbred population. Genetics 2012, 190:437-447.
60. Keane TM, Goodstadt L, Danecek P, White MA, Wong K, Yalcin B, Heger A, Agam A, Slater G, Goodson M, et al. Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 2011, 477:289-294.
61. Hutchins LN, Ding Y, Szatkiewicz JP, Von Smith R, Yang H, de Villena FP, Churchill GA, Graber JH. CGDSNPdb: a database resource for error-checked and imputed mouse SNPs. Database (Oxford) 2010, 2010:baq008.
62. Szatkiewicz JP, Beane GL, Ding Y, Hutchins L, Pardo-Manuel de Villena F, Churchill GA. An imputed genotype resource for the laboratory mouse. Mamm Genome 2008, 19:199-208.
63. Ledig S, Hiort O, Scherer G, Hoffmann M, Wolff G, Morlot S, Kuechler A, Wieacker P. Array-CGH analysis in patients with syndromic and non-syndromic XY gonadal dysgenesis: evaluation of array CGH as diagnostic tool and search for new candidate loci. Hum Reprod 2010, 25:2637-2646.
64. Tannour-Louet M, Han S, Corbett ST, Louet JF, Yatsenko S, Meyers L, Shaw CA, Kang SH, Cheung SW, Lamb DJ. Identification of de novo copy number variants associated with human disorders of sexual development. PLoS One 2010, 5:e15392.
65. White S, Ohnesorg T, Notini A, Roeszler K, Hewitt J, Daggag H, Smith C, Turbitt E, Gustin S, van den Bergen J, et al. Copy number variation in patients with disorders of sex development due to 46, XY gonadal dysgenesis. PLoS One 2011, 6:e17793.
66. Bouma GJ, Hudson QJ, Washburn LL, Eicher EM. New candidate genes identified for controlling mouse gonadal sex determination and the early stages of granulosa and Sertoli cell differentiation. Biol Reprod 2010, 82:380-389.
67. Ewen K, Baker M, Wilhelm D, Aitken RJ, Koopman P. Global survey of protein expression during gonadal sex determination in mice. Mol Cell Proteomics 2009, 8:2624-2641.
68. Kim YA, Wuchty S, Przytycka TM. Identifying causal genes and dysregulated pathways in complex diseases. PLoS Comput Biol 2011, 7:e1001095.
69. Hageman RS, Leduc MS, Korstanje R, Paigen B, Churchill GA. A bayesian framework for inference of the genotype-phenotype map for segregating populations. Genetics 2011, 187:1163-1170.
70. Ryan J, Ludbrook L, Wilhelm D, Sinclair A, Koopman P, Bernard P, Harley VR. Analysis of gene function in cultured embryonic mouse gonads using nucleofection. Sex Dev 2011, 5:7-15.
71. Svingen T, Wilhelm D, Combes AN, Hosking B, Harley VR, Sinclair AH, Koopman P. Ex vivo magnetofection: a novel strategy for the study of gene function in mouse organogenesis. Dev Dyn 2009, 238:956-964.
72. Parrington J, Coward K, Hibbitt O, Kubota H, Young C, McIlhinney J, Jones O. In vivo gene transfer into the testis by electroporation and viral infection-a novel way to study testis and sperm function. Soc Reprod Fertil Suppl 2007, 65:469-474.
73. Polanco JC, Wilhelm D, Mizusaki H, Jackson A, Browne C, Davidson T, Harley V, Sinclair A, Koopman P. Functional analysis of the SRY-KRAB interaction in mouse sex determination. Biol Cell 2009, 101:55-67.
74. Knower KC, Sim H, McClive PJ, Bowles J, Koopman P, Sinclair AH, Harley VR. Characterisation of urogenital ridge gene expression in the human embryonal carcinoma cell line NT2/D1. Sex Dev 2007, 1:114-126.
75. Hiramatsu R, Harikae K, Tsunekawa N, Kurohmaru M, Matsuo I, Kanai Y. FGF signaling directs a center-to-pole expansion of tubulogenesis in mouse testis differentiation. Development 2010, 137:303-312.