Emerging concepts on the epigenetic and transcriptional regulation of the Kiss1 gene

International Journal of Developmental Neuroscience

Volumn 31, Issue 6, 2013, Pages 452-462

  Semaan, Sheila J ^a   Kauffman, Alexander S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Chromatin; Development; DNA methylation; Epigenetics; Histone acetylation; Histone methylation; Kiss1; Kisspeptin; Reproduction; Sexual differentiation

Indexed keywords

DNA METHYLTRANSFERASE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; HISTONE DEMETHYLASE; KISSPEPTIN; LSD1; MESSENGER RNA; POLYCOMB GROUP PROTEIN; PROTEIN BAX; TESTOSTERONE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CUX1; TRANSCRIPTION FACTOR EAP1; TRANSCRIPTION FACTOR TTF1; TRANSCRIPTION FACTOR YY1; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ADULTHOOD; ANTEROVENTRAL THIRD VENTRICLE REGION; ARCUATE NUCLEUS; ARTICLE; BAX GENE; CBX7 GENE; CPG ISLAND; DEVELOPMENTAL GENETICS; DNA METHYLATION; DOWN REGULATION; EED GENE; EMBRYO DEVELOPMENT; EPIGENETICS; GENE; GENE EXPRESSION REGULATION; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HORMONAL REGULATION; HUMAN; HYPOTHALAMUS; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; IN VITRO STUDY; KISS1 GENE; NEGATIVE FEEDBACK; NONHUMAN; POSITIVE FEEDBACK; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUBERTY; SEX DIFFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

CHROMATIN; DEVELOPMENT; DNA METHYLATION; EPIGENETICS; HISTONE ACETYLATION; HISTONE METHYLATION; KISS1; KISSPEPTIN; REPRODUCTION; SEXUAL DIFFERENTIATION;

ANIMALS; EPIGENESIS, GENETIC; EPIGENOMICS; HUMANS; KISSPEPTINS; MICE; SEX DIFFERENTIATION; TRANSCRIPTION, GENETIC;

MUS; RODENTIA;

EID: 84880169295     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2013.03.006     Document Type: Article

References (90)

1. Adachi S., Yamada S., Takatsu Y., Matsui H., Kinoshita M., Takase K., Sugiura H., Ohtaki T., Matsumoto H., Uenoyama Y., Tsukamura H., Inoue K., Maeda K. Involvement of anteroventral periventricular metastin/kisspeptin neurons in estrogen positive feedback action on luteinizing hormone release in female rats. Journal of Reproduction and Development 2007, 53:367-378.
2. Adams J.M., Cory S. The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 2007, 26:1324-1337.
3. Bateman H.L., Patisaul H.B. Disrupted female reproductive physiology following neonatal exposure to phytoestrogens or estrogen specific ligands is associated with decreased GnRH activation and kisspeptin fiber density in the hypothalamus. Neurotoxicology 2008, 29:988-997.
4. Bentsen A.H., Ansel L., Simonneaux V., Tena-Sempere M., Juul A., Mikkelsen J.D. Maturation of kisspeptinergic neurons coincides with puberty onset in male rats. Peptides 2010, 31:275-283.
5. Bernstein B.E., Meissner A., Lander E.S. The mammalian epigenome. Cell 2007, 128:669-681.
6. Cao J., Patisaul H.B. Sexually dimorphic expression of hypothalamic estrogen receptors alpha and beta and Kiss1 in neonatal male and female rats. Journal of Comparative Neurology 2011, 519:2954-2977.
7. Cao J., Mickens J.A., McCaffrey K.A., Leyrer S.M., Patisaul H.B. Neonatal Bisphenol A exposure alters sexually dimorphic gene expression in the postnatal rat hypothalamus. Neurotoxicology 2012, 33:23-36.
8. Cebrian V., Fierro M., Orenes-Pinero E., Grau L., Moya P., Ecke T., Alvarez M., Gil M., Algaba F., Bellmunt J., Cordon-Cardo C., Catto J., Lopez-Beltran A., Sanchez-Carbayo M. KISS1 methylation and expression as tumor stratification biomarkers and clinical outcome prognosticators for bladder cancer patients. American Journal of Pathology 2011, 179:540-546.
9. Cedar H., Bergman Y. Programming of DNA methylation patterns. Annual Review of Biochemistry 2012, 81:97-117.
10. Clarkson J., Herbison A.E. Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. Endocrinology 2006, 147:5817-5825.
11. Clarkson J., d'Anglemont de Tassigny X., Moreno A.S., Colledge W.H., Herbison A.E. Kisspeptin-GPR54 signaling is essential for preovulatory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge. Journal of Neuroscience 2008, 28:8691-8697.
12. Clarkson J., Boon W.C., Simpson E.R., Herbison A.E. Postnatal development of an estradiol-kisspeptin positive feedback mechanism implicated in puberty onset. Endocrinology 2009, 150:3214-3220.
13. d'Anglemont de Tassigny X., Fagg L.A., Dixon J.P.C., Day K., Leitch H.G., Hendrick A.G., Zahn D., Franceschini I., Caraty A., Carlton M.B.L., Aparicio S.A.J.R., Colledge W.H. Hypogonadotropic hypogonadism in mice lacking a functional Kiss1 gene. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:10714-10719.
14. de Roux N., Genin E., Carel J.C., Matsuda F., Chaussain J.L., Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:10972-10976.
15. Desroziers E., Droguerre M., Bentsen A.H., Robert V., Mikkelsen J.D., Caraty A., Tillet Y., Duittoz A., Franceschini I. Embryonic development of kisspeptin neurones in rat. Journal of Neuroendocrinology 2012.
16. Dhillo W.S., Chaudhri O.B., Thompson E.L., Murphy K.G., Patterson M., Ramachandran R., Nijher G.K., Amber V., Kokkinos A., Donaldson M., Ghatei M.A., Bloom S.R. Kisspeptin-54 stimulates gonadotropin release most potently during the preovulatory phase of the menstrual cycle in women. Journal of Clinical Endocrinology and Metabolism 2007, 92:3958-3966.
17. Eden S., Constancia M., Hashimshony T., Dean W., Goldstein B., Johnson A.C., Keshet I., Reik W., Cedar H. An upstream repressor element plays a role in Igf2 imprinting. EMBO Journal 2001, 20:3518-3525.
18. Forger N.G., Rosen G.J., Waters E.M., Jacob D., Simerly R.B., de Vries G.J. Deletion of Bax eliminates sex differences in the mouse forebrain. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:13666-13671.
19. Forger N.G. Control of cell number in the sexually dimorphic brain and spinal cord. Journal of Neuroendocrinology 2009, 21:393-399.
20. Gill J.C., Wang O., Kakar S., Martinelli E., Carroll R.S., Kaiser U.B. Reproductive hormone-dependent and -independent contributions to developmental changes in kisspeptin in GnRH-deficient hypogonadal mice. PLoS One 2010, 5:e11911.
21. Gill J.C., Kwong C., Clark E., Carroll R., Shi Y., Kaiser U. A role for the histone demethylase LSD1 in controlling the timing of pubertal onset. 94th Annual Meeting of The Endocrine Society 2012, Abstract OR012-3.
22. Goldberg A.D., Allis C.D., Bernstein E. Epigenetics: a landscape takes shape. Cell 2007, 128:635-638.
23. Gotsiridze T., Kang N., Jacob D., Forger N.G. Development of sex differences in the principal nucleus of the bed nucleus of the stria terminalis of mice: role of Bax-dependent cell death. Developmental Neurobiology 2007, 67:355-362.
24. Gottsch M.L., Cunningham M.J., Smith J.T., Popa S.M., Acohido B.V., Crowley W.F., Seminara S., Clifton D.K., Steiner R.A. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 2004, 145:4073-4077.
25. Gottsch M.L., Navarro V.M., Zhao Z., Glidewell-Kenney C., Weiss J., Jameson J.L., Clifton D.K., Levine J.E., Steiner R.A. Regulation of Kiss1 and dynorphin gene expression in the murine brain by classical and nonclassical estrogen receptor pathways. Journal of Neuroscience 2009, 29:9390-9395.
26. Guerriero K.A., Keen K.L., Terasawa E. Developmental increase in kisspeptin-54 release in vivo is independent of the pubertal increase in estradiol in female rhesus monkeys (Macaca mulatta). Endocrinology 2012, 153:1887-1897.
27. Guo, Junjie U., Su Y., Zhong C., Ming G.-l., Song H. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 2011, 145:423-434.
28. Han S.K., Gottsch M.L., Lee K.J., Popa S.M., Smith J.T., Jakawich S.K., Clifton D.K., Steiner R.A., Herbison A.E. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. Journal of Neuroscience 2005, 25:11349-11356.
29. Holmes M.M., McCutcheon J., Forger N.G. Sex differences in NeuN- and androgen receptor-positive cells in the bed nucleus of the stria terminalis are due to Bax-dependent cell death. Neuroscience 2009, 158:1251-1256.
30. Homma T., Sakakibara M., Yamada S., Kinoshita M., Iwata K., Tomikawa J., Kanazawa T., Matsui H., Takatsu Y., Ohtaki T., Matsumoto H., Uenoyama Y., Maeda K.-i., Tsukamura H. Significance of neonatal testicular sex steroids to defeminize anteroventral periventricular kisspeptin neurons and the GnRH/LH surge system in male rats. Biology of Reproduction 2009, 81:1216-1225.
31. Hrabovszky E., Ciofi P., Vida B., Horvath M.C., Keller E., Caraty A., Bloom S.R., Ghatei M.A., Dhillo W.S., Liposits Z., Kallo I. The kisspeptin system of the human hypothalamus: sexual dimorphism and relationship with gonadotropin-releasing hormone and neurokinin B neurons. European Journal of Neuroscience 2010, 31:1984-1998.
32. Jaenisch R., Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nature Genetics 2003, 33(Suppl.):245-254.
33. Jones P.A., Takai D. The role of DNA methylation in mammalian epigenetics. Science 2001, 293:1068-1070.
34. Jones P.L., Veenstra G.J., Wade P.A., Vermaak D., Kass S.U., Landsberger N., Strouboulis J., Wolffe A.P. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nature Genetics 1998, 19:187-191.
35. Kauffman A.S., Gottsch M.L., Roa J., Byquist A.C., Crown A., Clifton D.K., Hoffman G.E., Steiner R.A., Tena-Sempere M. Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology 2007, 148:1774-1783.
36. Kauffman A.S., Park J.H., McPhie-Lalmansingh A.A., Gottsch M.L., Bodo C., Hohmann J.G., Pavlova M.N., Rohde A.D., Clifton D.K., Steiner R.A., Rissman E.F. The kisspeptin receptor GPR54 is required for sexual differentiation of the brain and behavior. Journal of Neuroscience 2007, 27:8826-8835.
37. Kauffman A.S. Coming of age in the kisspeptin era: sex differences, development, and puberty. Molecular and Cellular Endocrinology 2010, 324:51-63.
38. Kim J., Semaan S.J., Clifton D.K., Steiner R.A., Dhamija S., Kauffman A.S. Regulation of Kiss1 expression by sex steroids in the amygdala of the rat and mouse. Endocrinology 2011, 152:2020-2030.
39. Kim W., Jessen H.M., Auger A.P., Terasawa E. Postmenopausal increase in KiSS-1, GPR54, and luteinizing hormone releasing hormone (LHRH-1) mRNA in the basal hypothalamus of female rhesus monkeys. Peptides 2009, 30:103-110.
40. Kimura S., Hara Y., Pineau T., Fernandez-Salguero P., Fox C.H., Ward J.M., Gonzalez F.J. The T/ebp null mouse: thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary. Genes and Development 1996, 10:60-69.
41. Kolodkin M.H., Auger A.P. Sex difference in the expression of DNA methyltransferase 3a in the rat amygdala during development. Journal of Neuroendocrinology 2011, 23:577-583.
42. Kooistra S.M., Helin K. Molecular mechanisms and potential functions of histone demethylases. Nature Reviews Molecular Cell Biology 2012, 13:297-311.
43. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
44. Krishnan S., Intlekofer K.A., Aggison L.K., Petersen S.L. Central role of TRAF-interacting protein in a new model of brain sexual differentiation. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:16692-16697.
45. Kurian J.R., Olesen K.M., Auger A.P. Sex differences in epigenetic regulation of the estrogen receptor-alpha promoter within the developing preoptic area. Endocrinology 2010, 151:2297-2305.
46. Lenz K.M., Nugent B.M., McCarthy M.M. Sexual differentiation of the rodent brain: dogma and beyond. Frontiers in Neuroscience 2012, 6.
47. Li B., Carey M., Workman J.L. The role of chromatin during transcription. Cell 2007, 128:707-719.
48. Lomniczi A., Loche A., Castellano J.M., Ronnekleiv O.K., Bosch M., Kaidar G., Knoll J.G., Wright H., Pfeifer G.P., Ojeda S.R. Epigenetic control of female puberty. Nature Neuroscience 2013.
49. Mastronardi C., Smiley G.G., Raber J., Kusakabe T., Kawaguchi A., Matagne V., Dietzel A., Heger S., Mungenast A.E., Cabrera R., Kimura S., Ojeda S.R. Deletion of the Ttf1 gene in differentiated neurons disrupts female reproduction without impairing basal ganglia function. Journal of Neuroscience 2006, 26:13167-13179.
50. Matsuda K.I., Mori H., Nugent B.M., Pfaff D.W., McCarthy M.M., Kawata M. Histone deacetylation during brain development is essential for permanent masculinization of sexual behavior. Endocrinology 2011, 152:2760-2767.
51. Mayer C., Boehm U. Female reproductive maturation in the absence of kisspeptin/GPR54 signaling. Nature Neuroscience 2011, 14:704-710.
52. McCarthy M.M., Auger A.P., Bale T.L., De Vries G.J., Dunn G.A., Forger N.G., Murray E.K., Nugent B.M., Schwarz J.M., Wilson M.E. The epigenetics of sex differences in the brain. Journal of Neuroscience 2009, 29:12815-12823.
53. Messager S., Chatzidaki E.E., Ma D., Hendrick A.G., Zahn D., Dixon J., Thresher R.R., Malinge I., Lomet D., Carlton M.B., Colledge W.H., Caraty A., Aparicio S.A. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:1761-1766.
54. Morey L., Helin K. Polycomb group protein-mediated repression of transcription. Trends in Biochemical Sciences 2010, 35:323-332.
55. Moya P., Esteban S., Fernandez-Suarez A., Maestro M., Morente M., Sanchez-Carbayo M. KiSS-1 methylation and protein expression patterns contribute to diagnostic and prognostic assessments in tissue specimens for colorectal cancer. Tumour Biology 2012.
56. Mueller J.K., Dietzel A., Lomniczi A., Loche A., Tefs K., Kiess W., Danne T., Ojeda S.R., Heger S. Transcriptional regulation of the human KiSS1 gene. Molecular and Cellular Endocrinology 2011, 342:8-19.
57. Murray E.K., Hien A., de Vries G.J., Forger N.G. Epigenetic control of sexual differentiation of the bed nucleus of the stria terminalis. Endocrinology 2009, 150:4241-4247.
58. Murray E.K., Varnum M.M., Fernandez J.L., de Vries G.J., Forger N.G. Effects of neonatal treatment with valproic acid on vasopressin immunoreactivity and olfactory behaviour in mice. Journal of Neuroendocrinology 2011.
59. Navarro V.M., Castellano J.M., Fernandez-Fernandez R., Tovar S., Roa J., Mayen A., Barreiro M.L., Casanueva F.F., Aguilar E., Dieguez C., Pinilla L., Tena-Sempere M. Effects of KiSS-1 peptide, the natural ligand of GPR54, on follicle-stimulating hormone secretion in the rat. Endocrinology 2005, 146:1689-1697.
60. Navarro V.M., Castellano J.M., Fernandez-Fernandez R., Tovar S., Roa J., Mayen A., Nogueiras R., Vazquez M.J., Barreiro M.L., Magni P., Aguilar E., Dieguez C., Pinilla L., Tena-Sempere M. Characterization of the potent luteinizing hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology 2005, 146:156-163.
61. Navarro V.M., Ruiz-Pino F., Sanchez-Garrido M.A., Garcia-Galiano D., Hobbs S.J., Manfredi-Lozano M., Leon S., Sangiao-Alvarellos S., Castellano J.M., Clifton D.K., Pinilla L., Steiner R.A., Tena-Sempere M. Role of neurokinin B in the control of female puberty and its modulation by metabolic status. Journal of Neuroscience 2012, 32:2388-2397.
62. Nugent B.M., McCarthy M.M. Epigenetic underpinnings of developmental sex differences in the brain. Neuroendocrinology 2010, 93:150-158.
63. Pineda R., Garcia-Galiano D., Roseweir A., Romero M., Sanchez-Garrido M.A., Ruiz-Pino F., Morgan K., Pinilla L., Millar R.P., Tena-Sempere M. Critical roles of kisspeptins in female puberty and preovulatory gonadotropin surges as revealed by a novel antagonist. Endocrinology 2010, 151:722-730.
64. Pinilla L., Aguilar E., Dieguez C., Millar R.P., Tena-Sempere M. Kisspeptins and reproduction: physiological roles and regulatory mechanisms. Physiological Reviews 2012, 92:1235-1316.
65. Poling M.C., Kauffman A.S. Sexually dimorphic testosterone secretion in prenatal and neonatal mice is independent of kisspeptin-kiss1r and GnRH signaling. Endocrinology 2012, 153:782-793.
66. Poling M.C., Kauffman A.S. Organizational and activational effects of sex steroids on kisspeptin neuron development. Frontiers in Neuroendocrinology 2012.
67. Ramaswamy S., Guerriero K.A., Gibbs R.B., Plant T.M. Structural interactions between kisspeptin and GnRH neurons in the mediobasal hypothalamus of the male rhesus monkey (Macaca mulatta) as revealed by double immunofluorescence and confocal microscopy. Endocrinology 2008, 149:4387-4395.
68. Rando O.J. Combinatorial complexity in chromatin structure and function: revisiting the histone code. Current Opinion in Genetics and Development 2012, 22:148-155.
69. Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 2007, 447:425-432.
70. Rometo A.M., Krajewski S.J., Voytko M.L., Rance N.E. Hypertrophy and increased kisspeptin gene expression in the hypothalamic infundibular nucleus of postmenopausal women and ovariectomized monkeys. Journal of Clinical Endocrinology and Metabolism 2007, 92:2744-2750.
71. Sansregret L., Nepveu A. The multiple roles of CUX1: insights from mouse models and cell-based assays. Gene 2008, 412:84-94.
72. Schwarz J.M., Nugent B.M., McCarthy M.M. Developmental and hormone-induced epigenetic changes to estrogen and progesterone receptor genes in brain are dynamic across the life span. Endocrinology 2010, 151:4871-4881.
73. Semaan S.J., Kauffman A.S. Sexual differentiation and development of forebrain reproductive circuits. Current Opinion in Neurobiology 2010, 20:424-431.
74. Semaan S.J., Murray E.K., Poling M.C., Dhamija S., Forger N.G., Kauffman A.S. BAX-dependent and BAX-independent regulation of Kiss1 neuron development in mice. Endocrinology 2010, 151:5807-5817.
75. Semaan S.J., Dhamija S., Kim J., Ku E.C., Kauffman A.S. Assessment of epigenetic contributions to sexually-dimorphic kiss1 expression in the anteroventral periventricular nucleus of mice. Endocrinology 2012, 153:1875-1886.
76. Semaan S.J., Kauffman A.S. Alterations in hypothalamic gene expression of reproductive neuropeptides during the pubertal transition in mice. 94th Annual Meeting of The Endocrine Society 2012, Abstract OR02-2.
77. Seminara S.B., Messager S., Chatzidaki E.E., Thresher R.R., Acierno J.S., Shagoury J.K., Bo-Abbas Y., Kuohung W., Schwinof K.M., Hendrick A.G., Zahn D., Dixon J., Kaiser U.B., Slaugenhaupt S.A., Gusella J.F., O'Rahilly S., Carlton M.B., Crowley W.F., Aparicio S.A., Colledge W.H. The GPR54 gene as a regulator of puberty. New England Journal of Medicine 2003, 349:1614-1627.
78. Shahab M., Mastronardi C., Seminara S.B., Crowley W.F., Ojeda S.R., Plant T.M. Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:2129-2134.
79. Simerly R.B. Organization and regulation of sexually dimorphic neuroendocrine pathways. Behavioural Brain Research 1998, 92:195-203.
80. Simerly R.B. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annual Review of Neuroscience 2002, 25:507-536.
81. Smith J.T., Cunningham M.J., Rissman E.F., Clifton D.K., Steiner R.A. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 2005, 146:3686-3692.
82. Smith J.T., Dungan H.M., Stoll E.A., Gottsch M.L., Braun R.E., Eacker S.M., Clifton D.K., Steiner R.A. Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology 2005, 146:2976-2984.
83. Smith J.T., Clay C.M., Caraty A., Clarke I.J. KiSS-1 messenger ribonucleic acid expression in the hypothalamus of the ewe is regulated by sex steroids and season. Endocrinology 2007, 148:1150-1157.
84. Smith J.T. Kisspeptin signalling in the brain: steroid regulation in the rodent and ewe. Brain Research Reviews 2008, 57:288-298.
85. Smith J.T., Shahab M., Pereira A., Pau K.Y., Clarke I.J. Hypothalamic expression of KISS1 and gonadotropin inhibitory hormone genes during the menstrual cycle of a non-human primate. Biology of Reproduction 2010, 83:568-577.
86. Takase K., Uenoyama Y., Inoue N., Matsui H., Yamada S., Shimizu M., Homma T., Tomikawa J., Kanda S., Matsumoto H., Oka Y., Tsukamura H., Maeda K.I. Possible role of oestrogen in pubertal increase of Kiss1/kisspeptin expression in discrete hypothalamic areas of female rats. Journal of Neuroendocrinology 2009, 21:527-537.
87. Tomikawa J., Uenoyama Y., Ozawa M., Fukanuma T., Takase K., Goto T., Abe H., Ieda N., Minabe S., Deura C., Inoue N., Sanbo M., Tomita K., Hirabayashi M., Tanaka S., Imamura T., Okamura H., Maeda K., Tsukamura H. Epigenetic regulation of Kiss1 gene expression mediating estrogen-positive feedback action in the mouse brain. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:E1294-E1301.
88. Wilkinson F.H., Park K., Atchison M.L. Polycomb recruitment to DNA in vivo by the YY1 REPO domain. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:19296-19301.
89. Woo C.J., Kharchenko P.V., Daheron L., Park P.J., Kingston R.E. A region of the human HOXD cluster that confers polycomb-group responsiveness. Cell 2010, 140:99-110.
90. Wu S.C., Zhang Y. Active DNA demethylation: many roads lead to Rome. Nature Reviews Molecular Cell Biology 2010, 11:607-620.