The potential role of SRY in epigenetic gene regulation during brain sexual differentiation in mammals

Advances in Genetics

Volumn 86, Issue , 2014, Pages 135-165

  Sekido, Ryohei ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Brain; DNA methylation; Histone modification; MicroRNA sponge; Noncoding RNA; Pre mRNA splicing; Sexual dimorphism; SRY

Indexed keywords

ANIMAL; BRAIN; FEMALE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; HUMAN; MALE; MAMMAL; PHYSIOLOGY; SEX DIFFERENTIATION; SRY GENE;

ANIMALS; BRAIN; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION; GENES, SRY; HUMANS; MALE; MAMMALS; SEX DIFFERENTIATION;

EID: 84906766409     PISSN: 00652660     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-800222-3.00007-3     Document Type: Chapter

References (165)

1. Agate R.J., Grisham W., Wade J., Mann S., Wingfield J., Schanen C., et al. Neural, not gonadal, origin of brain sex differences in a gynandromorphic finch. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:4873-4878.
2. Ahmed E.I., Zehr J.L., Schulz K.M., Lorenz B.H., DonCarlos L.L., Sisk C.L. Pubertal hormones modulate the addition of new cells to sexually dimorphic brain regions. Nature Neuroscience 2008, 11:995-997.
3. Albrecht K.H., Young M., Washburn L.L., Eicher E.M. Sry expression level and protein isoform differences play a role in abnormal testis development in C57BL/6J mice carrying certain Sry alleles. Genetics 2003, 164:277-288.
4. Arnold A.P., Burgoyne P.S. Are XX and XY brain cells intrinsically different?. Trends in Endocrinology and Metabolism 2004, 15:6-11.
5. Arvanitis D.N., Jungas T., Behar A., Davy A. Ephrin-B1 reverse signaling controls a posttranscriptional feedback mechanism via miR-124. Molecular and Cellular Biology 2010, 30:2508-2517.
6. Bannister S.C., Tizard M.L., Doran T.J., Sinclair A.H., Smith C.A. Sexually dimorphic microRNA expression during chicken embryonic gonadal development. Biology of Reproduction 2009, 81:165-176.
7. Barrionuevo F., Bagheri-Fam S., Klattig J., Kist R., Taketo M.M., Englert C., et al. Homozygous inactivation of Sox9 causes complete XY sex reversal in mice. Biology of Reproduction 2006, 74:195-201.
8. Bernard P., Sim H., Knower K., Vilain E., Harley V. Human SRY inhibits beta-catenin-mediated transcription. International Journal of Biochemistry & Cell Biology 2008, 40:2889-2900.
9. Bernstein E., Caudy A.A., Hammond S.M., Hannon G.J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001, 409:363-366.
10. Bhandari R.K., Sadler-Riggleman I., Clement T.M., Skinner M.K. Basic helix-loop-helix transcription factor TCF21 is a downstream target of the male sex determining gene SRY. PloS One 2011, 6:e19935.
11. Bishop C.E., Whitworth D.J., Qin Y., Agoulnik A.I., Agoulnik I.U., Harrison W.R., et al. A transgenic insertion upstream of Sox9 is associated with dominant XX sex reversal in the mouse. Nature Genetics 2000, 26:490-494.
12. Bleier R., Byne W., Siggelkow I. Cytoarchitectonic sexual dimorphisms of the medial preoptic and anterior hypothalamic areas in guinea pig, rat, hamster, and mouse. Journal of Comparative Neurology 1982, 212:118-130.
13. Bradford S.T., Hiramatsu R., Maddugoda M.P., Bernard P., Chaboissier M.C., Sinclair A., et al. The cerebellin 4 precursor gene is a direct target of SRY and SOX9 in mice. Biology of Reproduction 2009, 80:1178-1188.
14. Breedlove S.M., Arnold A.P. Hormonal control of a developing neuromuscular system. II. Sensitive periods for the androgen-induced masculinization of the rat spinal nucleus of the bulbocavernosus. Journal of Neuroscience 1983, 3:424-432.
15. Brembeck F.H., Schwarz-Romond T., Bakkers J., Wilhelm S., Hammerschmidt M., Birchmeier W. Essential role of BCL9-2 in the switch between beta-catenin's adhesive and transcriptional functions. Genes & Development 2004, 18:2225-2230.
16. Bullejos M., Koopman P. Spatially dynamic expression of Sry in mouse genital ridges. Developmental Dynamics 2001, 221:201-205.
17. Bullejos M., Koopman P. Delayed Sry and Sox9 expression in developing mouse gonads underlies B6-Y(DOM) sex reversal. Developmental Biology 2005, 278:473-481.
18. Capel B., Swain A., Nicolis S., Hacker A., Walter M., Koopman P., et al. Circular transcripts of the testis-determining gene Sry in adult mouse testis. Cell 1993, 73:1019-1030.
19. Carrel L., Willard H.F. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 2005, 434:400-404.
20. Carruth L.L., Reisert I., Arnold A.P. Sex chromosome genes directly affect brain sexual differentiation. Nature Neuroscience 2002, 5:933-934.
21. Cermak T., Doyle E.L., Christian M., Wang L., Zhang Y., Schmidt C., et al. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Research 2011, 39:e82.
22. Chaboissier M.C., Kobayashi A., Vidal V.I., Lutzkendorf S., van de Kant H.J., Wegner M., et al. Functional analysis of Sox8 and Sox9 during sex determination in the mouse. Development 2004, 131:1891-1901.
23. Chapman S.C., Woodruff T.K. Betaglycan localization in the female rat pituitary: implications for the regulation of follicle-stimulating hormone by inhibin. Endocrinology 2003, 144:5640-5649.
24. Chassot A.A., Ranc F., Gregoire E.P., Roepers-Gajadien H.L., Taketo M.M., Camerino G., et al. Activation of beta-catenin signaling by Rspo1 controls differentiation of the mammalian ovary. Human Molecular Genetics 2008, 17:1264-1277.
25. Cheng L.C., Pastrana E., Tavazoie M., Doetsch F. miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nature Neuroscience 2009, 12:399-408.
26. Cihak R., Gutmann E., Hanzlikova V. Involution and hormone-induced persistence of the M. sphincter (levator) ani in female rats. Journal of Anatomy 1970, 106:93-110.
27. Clement T.M., Bhandari R.K., Sadler-Riggleman I., Skinner M.K. SRY directly regulates the neurotrophin 3 promoter during male sex determination and testis development in rats. Biology of Reproduction 2011, 85:277-284.
28. Clepet C., Schafer A.J., Sinclair A.H., Palmer M.S., Lovell-Badge R., Goodfellow P.N. The human SRY transcript. Human Molecular Genetics 1993, 2:2007-2012.
29. 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.
30. Cong L., Ran F.A., Cox D., Lin S., Barretto R., Habib N., et al. Multiplex genome engineering using CRISPR/Cas systems. Science 2013, 339:819-823.
31. Czech D.P., Lee J., Sim H., Parish C.L., Vilain E., Harley V.R. The human testis-determining factor SRY localizes in midbrain dopamine neurons and regulates multiple components of catecholamine synthesis and metabolism. Journal of Neurochemistry 2012, 122:260-271.
32. Davis E.C., Popper P., Gorski R.A. The role of apoptosis in sexual differentiation of the rat sexually dimorphic nucleus of the preoptic area. Brain Research 1996, 734:10-18.
33. De Napoles M., Mermoud J.E., Wakao R., Tang Y.A., Endoh M., Appanah R., et al. Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Developmental Cell 2004, 7:663-676.
34. De Vries G.J., Rissman E.F., Simerly R.B., Yang L.Y., Scordalakes E.M., Auger C.J., et al. A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. Journal of Neuroscience 2002, 22:9005-9014.
35. Demir E., Dickson B.J. Fruitless splicing specifies male courtship behavior in Drosophila. Cell 2005, 121:785-794.
36. Dewing P., Chiang C.W., Sinchak K., Sim H., Fernagut P.O., Kelly S., et al. Direct regulation of adult brain function by the male-specific factor SRY. Current Biology 2006, 16:415-420.
37. Dolci S., Grimaldi P., Geremia R., Pesce M., Rossi P. Identification of a promoter region generating Sry circular transcripts both in germ cells from male adult mice and in male mouse embryonal gonads. Biology of Reproduction 1997, 57:1128-1135.
38. Ebert M.S., Neilson J.R., Sharp P.A. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nature Methods 2007, 4:721-726.
39. Eskildsen T., Taipaleenmaki H., Stenvang J., Abdallah B.M., Ditzel N., Nossent A.Y., et al. MicroRNA-138 regulates osteogenic differentiation of human stromal (mesenchymal) stem cells invivo. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:6139-6144.
40. Ford C.E., Jones K.W., Miller O.J., Mittwoch U., Penrose L.S., Ridler M., et al. The chromosomes in a patient showing both mongolism and the Klinefelter syndrome. Lancet 1959, 1:709-710.
41. Ford C.E., Jones K.W., Polani P.E., De Almeida J.C., Briggs J.H. A sex-chromosome anomaly in a case of gonadal dysgenesis (Turner's syndrome). Lancet 1959, 1:711-713.
42. Forger N.G. Cell death and sexual differentiation of the nervous system. Neuroscience 2006, 138:929-938.
43. Forwood J.K., Harley V., Jans D.A. The C-terminal nuclear localization signal of the sex-determining region Y (SRY) high mobility group domain mediates nuclear import through importin beta 1. Journal of Biological Chemistry 2001, 276:46575-46582.
44. Foster J.W., Dominguez-Steglich M.A., Guioli S., Kwok C., Weller P.A., Stevanovic M., et al. Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 1994, 372:525-530.
45. Friedman J.R., Fredericks W.J., Jensen D.E., Speicher D.W., Huang X.P., Neilson E.G., et al. KAP-1, a novel corepressor for the highly conserved KRAB repression domain. Genes & Development 1996, 10:2067-2078.
46. Gatewood J.D., Wills A., Shetty S., Xu J., Arnold A.P., Burgoyne P.S., et al. Sex chromosome complement and gonadal sex influence aggressive and parental behaviors in mice. Journal of Neuroscience 2006, 26:2335-2342.
47. Gorski R.A., Gordon J.H., Shryne J.E., Southam A.M. Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Brain Research 1978, 148:333-346.
48. Gorski R.A., Harlan R.E., Jacobson C.D., Shryne J.E., Southam A.M. Evidence for the existence of a sexually dimorphic nucleus in the preoptic area of the rat. Journal of Comparative Neurology 1980, 193:529-539.
49. Grant J., Mahadevaiah S.K., Khil P., Sangrithi M.N., Royo H., Duckworth J., et al. Rsx is a metatherian RNA with Xist-like properties in X-chromosome inactivation. Nature 2012, 487:254-258.
50. Groner A.C., Meylan S., Ciuffi A., Zangger N., Ambrosini G., Denervaud N., et al. KRAB-zinc finger proteins and KAP1 can mediate long-range transcriptional repression through heterochromatin spreading. PLoS Genetics 2010, 6:e1000869.
51. Gubbay J., Collignon J., Koopman P., Capel B., Economou A., Munsterberg A., et al. 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.
52. Hacker A., Capel B., Goodfellow P., Lovell-Badge R. Expression of Sry, the mouse sex determining gene. Development 1995, 121:1603-1614.
53. Hafner H., Riecher-Rossler A., An Der Heiden W., Maurer K., Fatkenheuer B., Loffler W. Generating and testing a causal explanation of the gender difference in age at first onset of schizophrenia. Psychological Medicine 1993, 23:925-940.
54. Hansen T.B., Jensen T.I., Clausen B.H., Bramsen J.B., Finsen B., Damgaard C.K., et al. Natural RNA circles function as efficient microRNA sponges. Nature 2013, 495:384-388.
55. Harley V.R., Lovell-Badge R., Goodfellow P.N., Hextall P.J. The HMG box of SRY is a calmodulin binding domain. FEBS Letters 1996, 391:24-28.
56. Hiramatsu R., Matoba S., Kanai-Azuma M., Tsunekawa N., Katoh-Fukui Y., Kurohmaru M., et al. A critical time window of Sry action in gonadal sex determination in mice. Development 2009, 136:129-138.
57. Huang B., Wang S., Ning Y., Lamb A.N., Bartley J. Autosomal XX sex reversal caused by duplication of SOX9. American Journal of Medical Genetics 1999, 87:349-353.
58. Hwang W.Y., Fu Y., Reyon D., Maeder M.L., Tsai S.Q., Sander J.D., et al. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nature Biotechnology 2013, 31:227-229.
59. Ito H., Sato K., Koganezawa M., Ote M., Matsumoto K., Hama C., et al. Fruitless recruits two antagonistic chromatin factors to establish single-neuron sexual dimorphism. Cell 2012, 149:1327-1338.
60. Jacobs P.A., Strong J.A. A case of human intersexuality having a possible XXY sex-determining mechanism. Nature 1959, 183:302-303.
61. Jakobsson J., Cordero M.I., Bisaz R., Groner A.C., Busskamp V., Bensadoun J.C., et al. KAP1-mediated epigenetic repression in the forebrain modulates behavioral vulnerability to stress. Neuron 2008, 60:818-831.
62. Jeck W.R., Sorrentino J.A., Wang K., Slevin M.K., Burd C.E., Liu J., et al. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 2013, 19:141-157.
63. Jeske Y.W., Bowles J., Greenfield A., Koopman P. Expression of a linear Sry transcript in the mouse genital ridge. Nature Genetics 1995, 10:480-482.
64. Kennedy N., Boydell J., Kalidindi S., Fearon P., Jones P.B., van Os J., et al. Gender differences in incidence and age at onset of mania and bipolar disorder over a 35-year period in Camberwell, England. The American Journal of Psychiatry 2005, 162:257-262.
65. Kent J., Wheatley S.C., Andrews J.E., Sinclair A.H., Koopman P. A male-specific role for SOX9 in vertebrate sex determination. Development 1996, 122:2813-2822.
66. Kim Y., Bingham N., Sekido R., Parker K.L., Lovell-Badge R., Capel B. Fibroblast growth factor receptor 2 regulates proliferation and Sertoli differentiation during male sex determination. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:16558-16563.
67. Kim Y., Kobayashi A., Sekido R., DiNapoli L., Brennan J., Chaboissier M.C., et al. Fgf9 and Wnt4 act as antagonistic signals to regulate mammalian sex determination. PLoS Biology 2006, 4:e187.
68. Kimchi T., Xu J., Dulac C. A functional circuit underlying male sexual behaviour in the female mouse brain. Nature 2007, 448:1009-1014.
69. Kimura K., Ote M., Tazawa T., Yamamoto D. Fruitless specifies sexually dimorphic neural circuitry in the Drosophila brain. Nature 2005, 438:229-233.
70. Kong A., Frigge M.L., Masson G., Besenbacher S., Sulem P., Magnusson G., et al. Rate of de novo mutations and the importance of father's age to disease risk. Nature 2012, 488:471-475.
71. Ladd-Acosta C., Hansen K.D., Briem E., Fallin M.D., Kaufmann W.E., Feinberg A.P. Common DNA methylation alterations in multiple brain regions in autism. Molecular Psychiatry 2013, 10.1038/mp.2013.114.
72. Lahr G., Maxson S.C., Mayer A., Just W., Pilgrim C., Reisert I. Transcription of the Y chromosomal gene, Sry, in adult mouse brain. Molecular Brain Research 1995, 33:179-182.
73. Lalli E., Ohe K., Hindelang C., Sassone-Corsi P. Orphan receptor DAX-1 is a shuttling RNA binding protein associated with polyribosomes via mRNA. Molecular and Cellular Biology 2000, 20:4910-4921.
74. Lau Y.F., Li Y. The human and mouse sex-determining SRY genes repress the Rspol/beta-catenin signaling. Journal of Genetics and Genomics 2009, 36:193-202.
75. Lechner M.S., Begg G.E., Speicher D.W., Rauscher F.J. Molecular determinants for targeting heterochromatin protein 1-mediated gene silencing: direct chromoshadow domain-KAP-1 corepressor interaction is essential. Molecular and Cellular Biology 2000, 20:6449-6465.
76. Lee Y., Ahn C., Han J., Choi H., Kim J., Yim J., et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003, 425:415-419.
77. Lee Y., Kim M., Han J., Yeom K.H., Lee S., Baek S.H., et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO Journal 2004, 23:4051-4060.
78. Li Y., Oh H.J., Lau Y.F. The poly(ADP-ribose) polymerase 1 interacts with Sry and modulates its biological functions. Molecular and Cellular Endocrinology 2006, 257-258:35-46.
79. Maatouk D.M., DiNapoli L., Alvers A., Parker K.L., Taketo M.M., Capel B. Stabilization of beta-catenin in XY gonads causes male-to-female sex-reversal. Human Molecular Genetics 2008, 17:2949-2955.
80. MacConell L.A., Leal A.M., Vale W.W. The distribution of betaglycan protein and mRNA in rat brain, pituitary, and gonads: implications for a role for betaglycan in inhibin-mediated reproductive functions. Endocrinology 2002, 143:1066-1075.
81. Maekawa F., Sakurai M., Yamashita Y., Tanaka K., Haraguchi S., Yamamoto K., et al. A genetically female brain is required for a regular reproductive cycle in chicken brain chimeras. Nature Communications 2013, 4:1372.
82. Maenner S., Blaud M., Fouillen L., Savoye A., Marchand V., Dubois A., et al. 2-D structure of the A region of Xist RNA and its implication for PRC2 association. PLoS Biology 2010, 8:e1000276.
83. Maerkel K., Durrer S., Henseler M., Schlumpf M., Lichtensteiger W. Sexually dimorphic gene regulation in brain as a target for endocrine disrupters: developmental exposure of rats to 4-methylbenzylidene camphor. Toxicology and Applied Pharmacology 2007, 218:152-165.
84. Mahadevaiah S.K., Odorisio T., Elliott D.J., Rattigan A., Szot M., Laval S.H., et al. Mouse homologues of the human AZF candidate gene RBM are expressed in spermatogonia and spermatids, and map to a Y chromosome deletion interval associated with a high incidence of sperm abnormalities. Human Molecular Genetics 1998, 7:715-727.
85. Maiorano N.A., Mallamaci A. Promotion of embryonic cortico-cerebral neuronogenesis by miR-124. Neural Development 2009, 4:40.
86. Mak W., Baxter J., Silva J., Newall A.E., Otte A.P., Brockdorff N. Mitotically stable association of polycomb group proteins Eed and Enx1 with the inactive X chromosome in trophoblast stem cells. Current Biology 2002, 12:1016-1020.
87. Makeyev E.V., Zhang J., Carrasco M.A., Maniatis T. The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Molecular Cell 2007, 27:435-448.
88. Mali P., Yang L., Esvelt K.M., Aach J., Guell M., DiCarlo J.E., et al. RNA-guided human genome engineering via Cas9. Science 2013, 339:823-826.
89. Malki S., Nef S., Notarnicola C., Thevenet L., Gasca S., Mejean C., et al. Prostaglandin D2 induces nuclear import of the sex-determining factor SOX9 via its cAMP-PKA phosphorylation. EMBO Journal 2005, 24:1798-1809.
90. Manoli D.S., Foss M., Villella A., Taylor B.J., Hall J.C., Baker B.S. Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 2005, 436:395-400.
91. 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.
92. Matsuzawa-Watanabe Y., Inoue J., Semba K. Transcriptional activity of testis-determining factor SRY is modulated by the Wilms' tumor 1 gene product, WT1. Oncogene 2003, 22:7900-7904.
93. Mayer A., Lahr G., Swaab D.F., Pilgrim C., Reisert I. The Y-chromosomal genes SRY and ZFY are transcribed in adult human brain. Neurogenetics 1998, 1:281-288.
94. Mayer A., Mosler G., Just W., Pilgrim C., Reisert I. Developmental profile of Sry transcripts in mouse brain. Neurogenetics 2000, 3:25-30.
95. McArthur S., McHale E., Gillies G.E. The size and distribution of midbrain dopaminergic populations are permanently altered by perinatal glucocorticoid exposure in a sex- region- and time-specific manner. Neuropsychopharmacology 2007, 32:1462-1476.
96. McElreavey K., Vilain E., Abbas N., Herskowitz I., Fellous M. A regulatory cascade hypothesis for mammalian sex determination: SRY represses a negative regulator of male development. Proceedings of the National Academy of Sciences of the United States of America 1993, 90:3368-3372.
97. Memczak S., Jens M., Elefsinioti A., Torti F., Krueger J., Rybak A., et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 2013, 495:333-338.
98. Miller J.C., Tan S., Qiao G., Barlow K.A., Wang J., Xia D.F., et al. A TALE nuclease architecture for efficient genome editing. Nature Biotechnology 2011, 29:143-148.
99. Mishima T., Takizawa T., Luo S.S., Ishibashi O., Kawahigashi Y., Mizuguchi Y., et al. MicroRNA (miRNA) cloning analysis reveals sex differences in miRNA expression profiles between adult mouse testis and ovary. Reproduction 2008, 136:811-822.
100. Moosmann P., Georgiev O., Le Douarin B., Bourquin J.P., Schaffner W. Transcriptional repression by RING finger protein TIF1 beta that interacts with the KRAB repressor domain of KOX1. Nucleic Acids Research 1996, 24:4859-4867.
101. Morais da Silva S., Hacker A., Harley V., Goodfellow P., Swain A., Lovell-Badge R. Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nature Genetics 1996, 14:62-68.
102. Morgan C.P., Bale T.L. Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage. Journal of Neuroscience 2011, 31:11748-11755.
103. Morton S.U., Scherz P.J., Cordes K.R., Ivey K.N., Stainier D.Y., Srivastava D. microRNA-138 modulates cardiac patterning during embryonic development. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:17830-17835.
104. Mueller B.R., Bale T.L. Sex-specific programming of offspring emotionality after stress early in pregnancy. Journal of Neuroscience 2008, 28:9055-9065.
105. Murray H.E., Pillai A.V., McArthur S.R., Razvi N., Datla K.P., Dexter D.T., et al. Dose- and sex-dependent effects of the neurotoxin 6-hydroxydopamine on the nigrostriatal dopaminergic pathway of adult rats: differential actions of estrogen in males and females. Neuroscience 2003, 116:213-222.
106. Naftolin F., Ryan K.J., Davies I.J., Reddy V.V., Flores F., Petro Z., et al. The formation of estrogens by central neuroendocrine tissues. Recent Progress in Hormone Research 1975, 31:295-319.
107. Nagano T., Mitchell J.A., Sanz L.A., Pauler F.M., Ferguson-Smith A.C., Feil R., et al. The Air noncoding RNA epigenetically silences transcription by targeting G9a to chromatin. Science 2008, 322:1717-1720.
108. Nan X., Ng H.H., Johnson C.A., Laherty C.D., Turner B.M., Eisenman R.N., et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998, 393:386-389.
109. Neale B.M., Kou Y., Liu L., Ma'ayan A., Samocha K.E., Sabo A., et al. Patterns and rates of exonic de novo mutations in autism spectrum disorders. Nature 2012, 485:242-245.
110. Nordeen E.J., Nordeen K.W., Sengelaub D.R., Arnold A.P. Androgens prevent normally occurring cell death in a sexually dimorphic spinal nucleus. Science 1985, 229:671-673.
111. O'Roak B.J., Vives L., Girirajan S., Karakoc E., Krumm N., Coe B.P., et al. Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations. Nature 2012, 485:246-250.
112. Obernosterer G., Leuschner P.J., Alenius M., Martinez J. Post-transcriptional regulation of microRNA expression. RNA 2006, 12:1161-1167.
113. Oh H.J., Li Y., Lau Y.F. Sry associates with the heterochromatin protein 1 complex by interacting with a KRAB domain protein. Biology of Reproduction 2005, 72:407-415.
114. Ohe K., Lalli E., Sassone-Corsi P. A direct role of SRY and SOX proteins in pre-mRNA splicing. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:1146-1151.
115. Ohe K., Tamai K.T., Parvinen M., Sassone-Corsi P. DAX-1 and SOX6 molecular interplay results in an antagonistic effect in pre-mRNA splicing. Developmental Dynamics 2009, 238:1595-1604.
116. Pailhoux E., Vigier B., Chaffaux S., Servel N., Taourit S., Furet J.P., et al. A 11.7-kb deletion triggers intersexuality and polledness in goats. Nature Genetics 2001, 29:453-458.
117. Parma P., Radi O., Vidal V., Chaboissier M.C., Dellambra E., Valentini S., et al. R-spondin1 is essential in sex determination, skin differentiation and malignancy. Nature Genetics 2006, 38:1304-1309.
118. Peng H., Ivanov A.V., Oh H.J., Lau Y.F., Rauscher F.J. Epigenetic gene silencing by the SRY protein is mediated by a KRAB-O protein that recruits the KAP1 co-repressor machinery. Journal of Biological Chemistry 2009, 284:35670-35680.
119. Phoenix C.H., Goy R.W., Gerall A.A., Young W.C. Organizing action of prenatally administered testosterone propionate on the tissue mediating mating behavior in the female guinea pig. Endocrinology 1959, 65:369-382.
120. Pontiggia A., Rimini R., Harley V.R., Goodfellow P.N., Lovell-Badge R., Bianchi M.E. Sex-reversing mutations affect the architecture of SRY-DNA complexes. EMBO Journal 1994, 13:6115-6124.
121. Poulat F., de Santa Barbara P., Desclozeaux M., Soullier S., Moniot B., Bonneaud N., et al. The human testis determining factor SRY binds a nuclear factor containing PDZ protein interaction domains. Journal of Biological Chemistry 1997, 272:7167-7172.
122. Rakoczy J., Fernandez-Valverde S.L., Glazov E.A., Wainwright E.N., Sato T., Takada S., et al. MicroRNAs-140-5p/140-3p modulate Leydig cell numbers in the developing mouse testis. Biology of Reproduction 2013, 88:143.
123. Real F.M., Sekido R., Lupianez D.G., Lovell-Badge R., Jimenez R., Burgos M. A microRNA (mmu-miR-124) prevents Sox9 expression in developing mouse ovarian cells. Biology of Reproduction 2013, 89:78.
124. Reisert I., Pilgrim C. Sexual differentiation of monoaminergic neurons-genetic or epigenetic?. Trends in Neurosciences 1991, 14:468-473.
125. Rideout E.J., Dornan A.J., Neville M.C., Eadie S., Goodwin S.F. Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nature Neuroscience 2010, 13:458-466.
126. Salzman J., Gawad C., Wang P.L., Lacayo N., Brown P.O. Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PloS One 2012, 7:e30733.
127. Sander J.D., Dahlborg E.J., Goodwin M.J., Cade L., Zhang F., Cifuentes D., et al. Selection-free zinc-finger-nuclease engineering by context-dependent assembly (CoDA). Nature Methods 2011, 8:67-69.
128. Sanders S.J., Murtha M.T., Gupta A.R., Murdoch J.D., Raubeson M.J., Willsey A.J., et al. De novo mutations revealed by whole-exome sequencing are strongly associated with autism. Nature 2012, 485:237-241.
129. Sato Y., Yano S., Ewis A.A., Nakahori Y. SRY interacts with ribosomal proteins S7 and L13a in nuclear speckles. Cell Biology International 2011, 35:449-452.
130. Schmidt D., Ovitt C.E., Anlag K., Fehsenfeld S., Gredsted L., Treier A.C., et al. The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development 2004, 131:933-942.
131. Schultz D.C., Ayyanathan K., Negorev D., Maul G.G., Rauscher F.J. SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes & Development 2002, 16:919-932.
132. Schultz D.C., Friedman J.R., Rauscher F.J. Targeting histone deacetylase complexes via KRAB-zinc finger proteins: the PHD and bromodomains of KAP-1 form a cooperative unit that recruits a novel isoform of the Mi-2alpha subunit of NuRD. Genes & Development 2001, 15:428-443.
133. Sekido R. SRY: a transcriptional activator of mammalian testis determination. International Journal of Biochemistry & Cell Biology 2010, 42:417-420.
134. 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. Developmental Biology 2004, 274:271-279.
135. Sekido R., Lovell-Badge R. Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 2008, 453:930-934.
136. Siegel G., Obernosterer G., Fiore R., Oehmen M., Bicker S., Christensen M., et al. A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nature Cell Biology 2009, 11:705-716.
137. Silva J., Mak W., Zvetkova I., Appanah R., Nesterova T.B., Webster Z., et al. Establishment of histone H3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 Polycomb group complexes. Developmental Cell 2003, 4:481-495.
138. Sinclair A.H., Berta P., Palmer M.S., Hawkins J.R., Griffiths B.L., Smith M.J., et al. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 1990, 346:240-244.
139. Sleutels F., Zwart R., Barlow D.P. The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature 2002, 415:810-813.
140. Smallwood A., Esteve P.O., Pradhan S., Carey M. Functional cooperation between HP1 and DNMT1 mediates gene silencing. Genes & Development 2007, 21:1169-1178.
141. Song R., Ro S., Michaels J.D., Park C., McCarrey J.R., Yan W. Many X-linked microRNAs escape meiotic sex chromosome inactivation. Nature Denetics 2009, 41:488-493.
142. Sripathy S.P., Stevens J., Schultz D.C. The KAP1 corepressor functions to coordinate the assembly of de novo HP1-demarcated microenvironments of heterochromatin required for KRAB zinc finger protein-mediated transcriptional repression. Molecular and Cellular Biology 2006, 26:8623-8638.
143. St Clair D., Blackwood D., Muir W., Carothers A., Walker M., Spowart G., et al. Association within a family of a balanced autosomal translocation with major mental illness. Lancet 1990, 336:13-16.
144. Swain A., Narvaez V., Burgoyne P., Camerino G., Lovell-Badge R. Dax1 antagonizes Sry action in mammalian sex determination. Nature 1998, 391:761-767.
145. Taketo T., Lee C.H., Zhang J., Li Y., Lee C.Y., Lau Y.F. Expression of SRY proteins in both normal and sex-reversed XY fetal mouse gonads. Developmental Dynamics 2005, 233:612-622.
146. Thiru A., Nietlispach D., Mott H.R., Okuwaki M., Lyon D., Nielsen P.R., et al. Structural basis of HP1/PXVXL motif peptide interactions and HP1 localisation to heterochromatin. EMBO Journal 2004, 23:489-499.
147. Tomizuka K., Horikoshi K., Kitada R., Sugawara Y., Iba Y., Kojima A., et al. R-spondin1 plays an essential role in ovarian development through positively regulating Wnt-4 signaling. Human Molecular Genetics 2008, 17:1278-1291.
148. Tsukahara S., Kakeyama M., Toyofuku Y. Sex differences in the level of Bcl-2 family proteins and caspase-3 activation in the sexually dimorphic nuclei of the preoptic area in postnatal rats. Journal of Neurobiology 2006, 66:1411-1419.
149. Uhlenhaut N.H., Jakob S., Anlag K., Eisenberger T., Sekido R., Kress J., et al. Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 2009, 139:1130-1142.
150. Vainio S., Heikkila M., Kispert A., Chin N., McMahon A.P. Female development in mammals is regulated by Wnt-4 signalling. Nature 1999, 397:405-409.
151. Vidal V.P., Chaboissier M.C., de Rooij D.G., Schedl A. Sox9 induces testis development in XX transgenic mice. Nature Genetics 2001, 28:216-217.
152. Wagner T., Wirth J., Meyer J., Zabel B., Held M., Zimmer J., et al. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the Sry-related gene Sox9. Cell 1994, 79:1111-1120.
153. Wainwright E.N., Jorgensen J.S., Kim Y., Truong V., Bagheri-Fam S., Davidson T., et al. SOX9 regulates microRNA miR-202-5p/3p expression during mouse testis differentiation. Biology of Reproduction 2013, 89:34.
154. Waldron J., McCourty A., Lecanu L. Neural stem cell sex dimorphism in aromatase (CYP19) expression: a basis for differential neural fate. Stem Cells and Cloning 2010, 3:175-182.
155. Wang H., Hu Y.C., Markoulaki S., Welstead G.G., Cheng A.W., Shivalila C.S., et al. TALEN-mediated editing of the mouse Y chromosome. Nature Biotechnology 2013, 31:530-532.
156. Wang H., Yang H., Shivalila C.S., Dawlaty M.M., Cheng A.W., Zhang F., et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 2013, 153:910-918.
157. Weng R., Chin J.S., Yew J.Y., Bushati N., Cohen S.M. miR-124 controls male reproductive success in Drosophila. eLife 2013, 2:e00640.
158. Wiater E., Lewis K.A., Donaldson C., Vaughan J., Bilezikjian L., Vale W. Endogenous betaglycan is essential for high-potency inhibin antagonism in gonadotropes. Molecular Endocrinology 2009, 23:1033-1042.
159. Wijchers P.J., Yandim C., Panousopoulou E., Ahmad M., Harker N., Saveliev A., et al. Sexual dimorphism in mammalian autosomal gene regulation is determined not only by Sry but by sex chromosome complement as well. Developmental Cell 2010, 19:477-484.
160. Wilhelm D., Hiramatsu R., Mizusaki H., Widjaja L., Combes A.N., Kanai Y., et al. SOX9 regulates prostaglandin D synthase gene transcription invivo to ensure testis development. Journal of Biological Chemistry 2007, 282:10553-10560.
161. Wong C.C., Meaburn E.L., Ronald A., Price T.S., Jeffries A.R., Schalkwyk L.C., et al. Methylomic analysis of monozygotic twins discordant for autism spectrum disorder and related behavioural traits. Molecular Psychiatry 2013, 10.1038/mp.2013.41.
162. Wu J.B., Chen K., Li Y., Lau Y.F., Shih J.C. Regulation of monoamine oxidase A by the SRY gene on the Y chromosome. FASEB Journal 2009, 23:4029-4038.
163. Zhang F., Cong L., Lodato S., Kosuri S., Church G.M., Arlotta P. Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription. Nature Biotechnology 2011, 29:149-153.
164. Zhao D., McBride D., Nandi S., McQueen H.A., McGrew M.J., Hocking P.M., et al. Somatic sex identity is cell autonomous in the chicken. Nature 2010, 464:237-242.
165. Zhao J., Sun B.K., Erwin J.A., Song J.J., Lee J.T. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 2008, 322:750-756.