Epigenetic control of gonadotropin releasing hormone neurons

Frontiers in Endocrinology

Volumn 4, Issue MAY, 2013, Pages

  Kurian, Joseph R ^a   Terasawa, Ei ^a,b  

^a UNIVERSITY OF WISCONSIN   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Epigenetic; Gonadotropin releasing hormone; Histone; Kisspeptin; Methylation; Neuroendocrine; Puberty; Reproduction

Indexed keywords

DNA METHYLTRANSFERASE; GONADORELIN; HISTONE H2A; KISSPEPTIN; MESSENGER RNA;

CHROMATIN STRUCTURE; CPG ISLAND; DNA METHYLATION; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; ENVIRONMENTAL FACTOR; EPIGENETICS; GENE EXPRESSION; GENETIC REGULATION; HISTONE MODIFICATION; HUMAN; MEDIOBASAL HYPOTHALAMUS; NERVE CELL; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN PROCESSING; PUBERTY; REPRODUCTION; REVIEW; STIMULUS;

EID: 84884175651     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2013.00061     Document Type: Review

References (61)

1. Azuara, V., Perry, P., Sauer, S., Spivakov, M., Jørgensen, H. F., John, R. M., et al. (2006). Chromatin signatures of pluripotent cell lines. Nat. Cell Biol. 8, 532-538. doi:10.1038/ncb1403
2. Banks, G. C., Deterding, L. J., Tomer, K. B., and Archer, T. K. (2001). Hormone-mediated dephosphorylation of specific histone H1 isoforms. J. Biol. Chem. 276, 36467-36473. doi:10.1074/jbc.M104641200
3. Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., et al. (2006). A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326. doi:10.1016/j.cell.2006.02.041
4. Bestor, T., Laudano, A., Mattaliano, R., and Ingram, V. (1988). Cloning and sequencing of a cDNA encoding DNA methyltransferase of mouse cells. The carboxylterminal domain of the mammalian enzymes is related to bacterial restriction methyltransferases. J. Mol. Biol. 203, 971-983. doi:10.1016/0022-2836(88)90122-2
5. Bestor, T. H., and Ingram, V. M. (1983). Two DNA methyltransferases from murine erythroleukemia cells: purification, sequence specificity, and mode of interaction with DNA. Proc. Natl. Acad. Sci. U.S.A. 80, 5559-5563. doi:10.1073/pnas.80.18.5559
6. Branco, M. R., Ficz, G., and Reik, W. (2012). Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat. Rev. Genet. 13, 7-13.
7. Clark, M. E., and Mellon, P. L. (1995). The POU homeodomain transcription factor Oct-1 is essential for activity of the gonadotropin-releasing hormone neuronspecific enhancer. Mol. Cell. Biol. 15, 6169-6177.
8. Constantin, S., Caraty, A., Wray, S., and Duittoz, A. H. (2009). Development of gonadotropin-releasing hormone-1 secretion in mouse nasal explants. Endocrinology 150, 3221-3227. doi:10.1210/en.2008-1711
9. Dawlaty, M. M., Breiling, A., Le, T., Raddatz, G., Barrasa, M. I., Cheng, A. W., et al. (2013). Combined deficiency of Tet1 and Tet2 causes epigenetic abnormalities but is compatible with postnatal development. Dev. Cell 24, 310-323. doi:10.1016/j.devcel.2012.12.015
10. Dawlaty, M. M., Ganz, K., Powell, B. E., Hu, Y. C., Markoulaki, S., Cheng, A. W., et al. (2011). Tet1 is dispensable for maintaining pluripotency and its loss is compatible with embryonic and postnatal development. Cell Stem Cell 9, 166-175. doi:10.1016/j.stem.2011.07.010
11. Deaton, A. M., and Bird, A. (2011). CpG islands and the regulation of transcription. Genes Dev. 25, 1010-1022. doi:10.1101/gad.2037511
12. Deplus, R., Delatte, B., Schwinn, M. K., Defrance, M., Méndez, J., Murphy, N., et al. (2013). TET2 and TET3 regulate GlcNAcylation and H3K4 methylation through OGT and SET1/COMPASS. EMBO J. 32, 645-655. doi:10.1038/emboj.2012.357
13. El Majdoubi, M., Sahu, A., Ramaswamy, S., and Plant, T. M. (2000). Neuropeptide Y: a hypothalamic brake restraining the onset of puberty in primates. Proc. Natl. Acad. Sci. U.S.A. 97, 6179-6184. doi:10.1073/pnas.090099697
14. Fueshko, S., and Wray, S. (1994). LHRH cells migrate on peripherin fibers in embryonic olfactory explant cultures: an in vitro model for neurophilic neuronal migration. Dev. Biol. 166, 331-348. doi:10.1006/dbio.1994.1319
15. Gardiner-Garden, M., and Frommer, M. (1987). CpG islands in vertebrate genomes. J. Mol. Biol. 196, 261-282. doi:10.1016/0022-2836(87)90689-9
16. Gill, J. C., Kwong, C., Clark, E., Carroll, R. S., Shi, Y. G., and Kaiser, U. B. (2012a). A role for the histobe demethylase LSD1 in controlling the timing of pubertal onset. Endocr. Soc. 33, OR12-1.
17. Gill, J. C., Navarro, V. M., Kwong, C., Noel, S. D., Martin, C., Xu, S., et al. (2012b). Increased neurokinin B (Tac2) expression in the mouse arcuate nucleus is an early marker of pubertal onset with differential sensitivity to sex steroid-negative feedback than Kiss1. Endocrinology 153, 4883-4893. doi:10.1210/en.2012-1529
18. Glaser, S., Schaft, J., Lubitz, S., Vintersten, K., van der Hoeven, F., Tufteland, K. R., et al. (2006). Multiple epigenetic maintenance factors implicated by the loss of Mll2 in mouse development. Development 133, 1423-1432. doi:10.1242/dev.02302
19. Hahn, M. A., Qiu, R., Wu, X., Li, A. X., Zhang, H., Wang, J., et al. (2013). Dynamics of 5-hydroxymethylcytosine and chromatin marks in mammalian neurogenesis. Cell Rep. 3, 291-300. doi:10.1016/j.celrep.2013.01.011
20. Hermann, A., Goyal, R., and Jeltsch, A. (2004). The Dnmt1 DNA-(cytosine-C5)-methyltransferase methylates DNA processively with high preference for hemimethylated target sites. J. Biol. Chem. 279, 48350-48359. doi:10.1074/jbc.M403427200
21. Iyer, A. K., Brayman, M. J., and Mellon, P. L. (2011). Dynamic chromatin modifications control GnRH gene expression during neuronal differentiation and protein kinase C signal transduction. Mol. Endocrinol. 25, 460-473. doi:10.1210/me.2010-0403
22. Kepa, J. K., Spaulding, A. J., Jacobsen, B. M., Fang, Z., Xiong, X., Radovick, S., et al. (1996a). Structure of the distal human gonadotropin releasing hormone (hGnrh) gene promoter and functional analysis in Gt1-7 neuronal cells. Nucleic Acids Res. 24, 3614-3620. doi:10.1093/nar/24.18.361
23. Kepa, J. K., Jacobsen, B. M., Boen, E. A., Prendergast, P., Edwards, D. P., Takimoto, G., et al. (1996b). Direct binding of progesterone receptor to nonconsensus DNA sequences represses rat GnRH. Mol. Cell. Endocrinol. 117, 27-39. doi:10.1016/0303-7207(95)03723-3
24. Kepa, J. K., Wang, C., Neeley, C. I., Raynolds, M. V., Gordon, D. F., Wood, W. M., et al. (1992). Structure of the rat gonadotropin releasing hormone (rGnRH) gene promoter and functional analysis in hypothalamic cells. Nucleic Acids Res. 20, 1393-1399. doi:10.1093/nar/20.6.1393
25. Kurian, J. R., Keen, K. L., and Terasawa, E. (2010). Epigenetic changes coincide with in vitro primate GnRH neuronal maturation. Endocrinology 151, 5359-5368. doi:10.1210/en.2010-0555
26. Kurian, J. R., and Terasawa, E. (2012). Elevated methylcytosine dioxygenase (Tet1) levels stimulate GnRH gene expression in immature neurons. Abstracts for the Society of Behavioral Neuroendocrinology Meeting, Madison, Number O.62.
27. Kurian, J. R., Kapke, J. A., and Terasawa, E. (2011). Epigenetic contribution to GnRH neuronal development in male pubertal development. Abstracts for the Society for Neuroscience Meeting, Washington, Number 500.03.
28. Lee, S. Y., Lau, A. T., Jeong, C. H., Shim, J. H., Kim, H. G., Kim, J., et al. (2010). Histone XH2AX is required for Xenopus anterior neural development: critical role of threonine 16 phosphorylation. J. Biol. Chem. 285, 29525-29534. doi:10.1074/jbc.M110.127233.
29. Li, E., Bestor, T. H., and Jaenisch, R. (1992). Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915-926. doi:10.1016/0092-8674(92)90611-F
30. Lomniczi, A., Loche, A., Castellano, J. M., Ronnekleiv, O. K., Bosch, M., Kaidar, G., et al. (2013). Epigenetic control of female puberty. Nat. Neurosci. 16, 281-289. doi:10.1038/nn.3319
31. Maurer, J. A., and Wray, S. (1997). Luteinizing hormone-releasing hormone (LHRH) neurons maintained in hypothalamic slice explant cultures exhibit a rapid LHRH mRNA turnover rate. J. Neurosci. 17, 9481-9491.
32. Mehlmann, L. M. (2005). Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 30, 791-799. doi:10.1530/rep.1.00793
33. Mellon, P. L., Windle, J. J., Goldsmith, P. C., Padula, C. A., Roberts, J. L., and Weiner, R. I. (1990). Immortalization of hypothalamic GnRH neurons by genetically targeted tumorigenesis. Neuron 5, 1-10. doi:10.1016/0896-6273(90)90028-E
34. Metzger, E., Wissmann, M., Yin, N., Müller, J. M., Schneider, R., Peters, A. H., et al. (2005). LSD1 demethylates repressive histone marks to promote androgenreceptor- dependent transcription. Nature 437, 436-439.
35. Moore, J. P. Jr., and Wray, S. (2000). Luteinizing hormone-releasing hormone biosynthesis and secretion in embryonic LHRH neurons. Endocrinology 141, 4486- 4495. doi:10.1210/en.141.12.4486
36. Okano, M., Bell, D. W., Haber, D. A., and Li, E. (1999). DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247-257. doi:10.1016/S0092-8674(00)81656-6
37. Okano, M., Xie, S., and Li, E. (1998). Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat. Genet. 19, 219-220. doi:10.1038/890
38. Pan, G., Tian, S., Nie, J., Yang, C., Ruotti, V., Wei, H., et al. (2007). Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 1, 299-312. doi:10.1016/j.stem.2007.08.003
39. Pasini, D., Bracken, A. P., Hansen, J. B., Capillo, M., and Helin, K. (2007). The polycomb group protein Suz12 is required for embryonic stem cell differentiation. Mol. Cell. Biol. 27, 3769-3779. doi:10.1128/MCB.01432-06
40. Quanbeck, C., Sherwood, N. M., Millar, R. P., and Terasawa, E. (1997). Two populations of luteinizing hormone-releasing hormone neurons in the forebrain of the rhesus macaque during embryonic development. J. Comp. Neurol. 380, 293-309. doi:10.1002/(SICI)1096-9861(19970414)380:3<293::AIDCNE1>3.0.CO;2-Y
41. Radovick, S., Wray, S., Lee, E., Nicols, D. K., Nakayama, Y., Weintraub, B. D., et al. (1991). Migratory arrest of gonadotropin-releasing hormone neurons in transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 88, 3402-3406. doi:10.1073/pnas.88.8.3402
42. Ronnekleiv, O. K., and Resko, J. A. (1990). Ontogeny of gonadotropin-releasing hormone-containing neurons in early fetal development of rhesus macaques. Endocrinology 126, 498-511. doi:10.1210/endo-126-1-498
43. Schermelleh, L., Spada, F., Easwaran, H. P., Zolghadr, K., Margot, J. B., Cardoso, M. C., et al. (2005). Trapped in action: direct visualization of DNA methyltransferase activity in living cells. Nat. Methods 2, 751-756. doi:10.1038/nmeth794
44. Schmitz, S. U., Albert, M., Malatesta, M., Morey, L., Johansen, J. V., Bak, M., et al. (2011). Jarid1b targets genes regulating development and is involved in neural differentiation. EMBO J. 30, 4586-4600. doi:10.1038/emboj.2011.383
45. Semaan, S. J., Dhamija, S., Kim, J., Ku, E. C., and Kauffman, A. S. (2012). Assessment of epigenetic contributions to sexually-dimorphic Kiss1 expression in the anteroventral periventricular nucleus of mice. Endocrinology 153, 1875-1886. doi:10.1210/en.2011-1975
46. Semaan, S. J., and Kauffman, A. S. (2013). Emerging concepts on the epigenetic and transcriptional regulation of the Kiss1 gene. Int. J. Dev. Neurosci.. doi:10.1016/j.ijdevneu.2013.03.006. [Epub ahead of print].
47. Shen, X., Liu, Y., Hsu, Y. J., Fujiwara, Y., Kim, J., Mao, X., et al. (2008). EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol. Cell 32, 491-502. doi:10.1016/j.molcel.2008.10.016
48. Stresemann, C., and Lyko, F. (2008). Modes of action of the DNA methyltransferase inhibitors azacytidine and decitabine. Int. J. Cancer 123, 8-13. doi:10.1002/ijc.23607
49. Suberbielle, E., Sanchez, P. E., Kravitz, A. V., Wang, X., Ho, K., Eilertson, K., et al. (2013). Physiologic brain activity causes DNA double-strand breaks in neurons, with exacerbation by amyloid-β. Nat. Neurosci. 16, 613-621. doi:10.1038/nn.3356.
50. Svedruzic, Z. M. (2008). Mammalian cytosine DNA methyltransferase Dnmt1: enzymatic mechanism novel mechanism-based inhibitors, and RNA-directed DNA methylation. Curr. Med. Chem. 15, 92-106. doi:10.2174/092986708783330700
51. Terasawa, E., Busser, B. W., Luchansky, L. L., Sherwood, N. M., Jennes, L., Millar, R. P., et al. (2001). Presence of luteinizing hormone-releasing hormone fragments in the rhesus monkey forebrain. J. Comp. Neurol. 439, 491-504. doi:10.1002/cne.1364
52. Terasawa, E., Keen, K. L., Mogi, K., and Claude, P. (1999). Pulsatile release of luteinizing hormone-releasing hormone (LHRH) in cultured LHRH neurons derived from the embryonic olfactory placode of the rhesus monkey. Endocrinology 140, 1432-1441. doi:10.1210/en.140.3.1432
53. Terasawa, E., Quanbeck, C. D., Schulz, C. A., Burich, A. J., Luchansky, L. L., and Claude, P. (1993). A primary cell culture system of luteinizing hormone releasing hormone (LHRH) neurons derived from fetal olfactory placode in the rhesus monkey. Endocrinology 133, 2379-2390. doi:10.1210/en.133.5.2379
54. Tomikawa, J., Uenoyama, Y., Ozawa, M., Fukanuma, T., Takase, K., Goto, T., et al. (2012). Epigenetic regulation of Kiss1 gene expression mediating estrogen-positive feedback action in the mouse brain. Proc. Natl. Acad. Sci. U.S.A. 109, 1294-1301. doi:10.1073/pnas.1114245109
55. Whyte, D. B., Lawson, M. A., Belsham, D. D., Eraly, S. A., Bond, C. T., Adelman, J. P., et al. (1995). A neuron-specific enhancer targets expression of the gonadotropin-releasing hormone gene to hypothalamic neurosecretory neurons. Mol. Endocrinol. 9, 467-477. doi:10.1210/me.9.4.467
56. Winter, S., Simboeck, E., Fischle, W., Zupkovitz, G., Dohnal, I., Mechtler, K., et al. (2008). 14-3-3 proteins recognize a histone code at histone H3 and are required for transcriptional activation. EMBO J. 27, 88-99. doi:10.1038/sj.emboj.7601954
57. Wray, S. (2010). From nose to brain: development of gonadotropin-releasing hormone-1 neurones. J. Neuroendocrinol. 22, 743-753. doi:10.1111/j.1365- 2826.2010.02034.x
58. Wu, S. C., and Zhang, Y. (2010). Active DNA demethylation: many roads lead to Rome. Nat. Rev. Mol. Cell Biol. 11, 607-620. doi:10.1038/nrm2950
59. Yagi, H., Deguchi, K., Aono, A., Tani, Y., Kishimoto, T., and Komori, T. (1998). Growth disturbance in fetal liver hematopoiesis of Mll-mutant mice. Blood 92, 108- 117.
60. Yamaguchi, S., Hong, K., Liu, R., Shen, L., Inoue, A., Diep, D., et al. (2012). Tet1 controls meiosis by regulating meiotic gene expression. Nature 492, 443-447. doi:10.1038/nature11709
61. Yu, B. D., Hess, J. L., Horning, S. E., Brown, G. A., and Korsmeyer, S. J. (1995). Altered Hox expression and segmental identity in Mll-mutant mice. Nature 378, 505 -508. doi:10.1038/378505a0