Histone H3K4 demethylases are essential in development and differentiation

Biochemistry and Cell Biology

Volumn 85, Issue 4, 2007, Pages 435-443

  Benevolenskaya, Elizaveta V ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

H3K4me3; Histone methylation; JARID1; JmjC domain

Indexed keywords

CATALYSIS; CELLS; METHYLATION;

DEMETHYLATION; H3K4ME3; HISTONE METHYLATION; JMJC DOMAIN;

ENZYMES;

HISTONE H3; LYSINE; RETINOBLASTOMA PROTEIN;

BRAIN; CELL FATE; CHROMATIN; DEMETHYLATION; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; ENZYME SPECIFICITY; EPIGENETICS; GENE DELETION; GENE OVEREXPRESSION; HEMATOPOIETIC STEM CELL; METHYLATION; NONHUMAN; PATHOLOGY; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; SHORT SURVEY; TRANSCRIPTION INITIATION; ZEBRA FISH;

ANIMALS; CELL DIFFERENTIATION; HISTONES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYSINE; METHYLATION; PROTEIN ISOFORMS; RETINOBLASTOMA PROTEIN; TUMOR SUPPRESSOR PROTEINS;

EID: 34948900481     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/O07-057     Document Type: Short Survey

References (79)

1. Balciunas, D., and Ronne, H. 2000. Evidence of domain swapping within the jumonji family of transcription factors. Trends Biochem. Sci. 25: 274-276. doi:10.1016/S0968-0004(00)01593-0.
2. Barrett, A., Madsen, B., Copier, J., Lu, P.J., Cooper, L., Scibetta, A.G., Burchell, J., and Taylor-Papadimitriou, J. 2002. PLU-1 nuclear protein, which is upregulated in breast cancer, shows restricted expression in normal human adult tissues: a new cancer/testis antigen? Int. J. Cancer, 101: 581-588. doi:10.1002/ijc.10644.
3. Benevolenskaya, E.V., Murray, H.L., Branton, P., Young, R.A., and Kaelin, W.G., Jr. 2005. Binding of pRB to the PHD protein RBP2 promotes cellular differentiation. Mol. Cell, 18: 623-635. doi:10.1016/j.molcel.2005.05. 012.
4. Bernstein, B.E., Humphrey, E.L., Erlich, R.L., Schneider, R., Bouman, P., Liu, J.S., Kouzarides, T., and Schreiber, S.L. 2002. Methylation of histone H3 Lys 4 in coding regions of active genes. Proc. Natl. Acad. Sci. U.S.A. 99: 8695-8700.
5. Bernstein, B.E., Kamal, M., Lindblad-Toh, K., Bekiranov, S., Bailey, D.K., Huebert, D.J., et al. 2005. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell, 120: 169-181. doi:10.1016/j.cell.2005.01.001.
6. 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.
7. Bernstein, B.E., Meissner, A., and Lander, E.S. 2007. The mammalian epigenome. Cell, 128: 669-681. doi:10.1016/j.cell.2007.01.033.
8. Boyer, L.A., Plath, K., Zeitlinger, J., Brambrink, T., Medeiros, L.A., Lee, T.I., et al. 2006. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature (London), 441: 349-353. doi:10.1038/nature04733.
9. Chan, S.W., and Hong, W. 2001. Retinoblastoma-binding protein 2 (Rbp2) potentiates nuclear hormone receptor-mediated transcription. J. Biol. Chem. 276: 28402-28412. doi:10.1074/jbc.M100313200.
10. Chen, Z., Zang, J., Whetstine, J., Hong, X., Davrazou, F., Kutateladze, T.G., et al. 2006. Structural insights into histone demethylation by JMJD2 family members. Cell, 125: 691-702. doi:10.1016/j.cell.2006.04.024.
11. Christensen, J., Agger, K., Cloos, P.A., Pasini, D., Rose, S., Sennels, L., et al. 2007. RBP2 belongs to a family of demethylases, specific for tri-and dimethylated lysine 4 on histone 3. Cell, 128: 1063-1076. doi:10.1016/j.cell.2007.02.003.
12. Classon, M., and Harlow, E. 2002. The retinoblastoma tumour suppressor in development and cancer. Nat. Rev. Cancer, 2: 910-917. doi:10.1038/nrc950.
13. Clissold, P.M., and Ponting, C.P. 2001. JmjC: cupin metalloenzyme-like domains in jumonji, hairless and phospholipase A2beta. Trends Biochem. Sci. 26: 7-9. doi:10.1016/S0968-0004(00)01700-X.
14. Cole, M.D., and Nikiforov, M.A. 2006. Transcriptional activation by the Myc oncoprotein. Curr. Top. Microbiol. Immunol. 302: 33-50.
15. Coppola, J.A., and Cole, M.D. 1986. Constitutive c-myc oncogene expression blocks mouse erythroleukaemia cell differentiation but not commitment. Nature (London), 320: 760-763. doi:10.1038/320760a0.
16. Dahiya, A., Wong, S., Gonzalo, S., Gavin, M., and Dean, D.C. 2001. Linking the Rb and polycomb pathways. Mol. Cell, 8: 557-569. [erratum appears in Mol. Cell 2003 Jun;11(6):1693-6.] doi:10.1016/S1097-2765(01)00346-X.
17. Defeo-Jones, D., Huang, P.S., Jones, R.E., Haskell, K.M., Vuocolo, G.A., Hanobik, M.G., Huber, H.E., and Oliff, A. 1991. Cloning of cDNAs for cellular proteins that bind to the retinoblastoma gene product. Nature (London), 352: 251-254. doi:10.1038/352251a0.
18. Dyson, N. 1998. The regulation of E2F by pRB-family proteins. Genes Dev. 12: 2245-2262.
19. Eissenberg, J.C., Lee, M.G., Schneider, J., Ilvarsonn, A., Shiekhattar, R., and Shilatifard, A. 2007. The trithorax-group gene in Drosophila little imaginal discs encodes a trimethylated histone H3 Lys4 demethylase. Nat. Struct. Mol. Biol. 14: 344-346. doi:10.1038/nsmb1217.
20. Fattaey, A.R., Helin, K., Dembski, M.S., Dyson, N., Harlow, E., Vuocolo, G.A., et al. 1993. Characterization of the retinoblastoma binding proteins RBP1 and RBP2. Oncogene, 8: 3149-3156.
21. Forneris, F., Binda, C., Vanoni, M.A., Battaglioli, E., and Mattevi, A. 2005. Human histone demethylase LSD1 reads the histone code. J. Biol. Chem. 280: 41360-41365. doi:10.1074/jbc.M509549200.
22. Garcia-Bassets, I., Kwon, Y.S., Telese, F., Prefontaine, G.G., Hutt, K.R., Cheng, C.S., et al. 2007. Histone methylation-dependent mechanisms impose ligand dependency for gene activation by nuclear receptors. Cell, 128: 505-518.
23. Gildea, J.J., Lopez, R., and Shearn, A. 2000. A screen for new trithorax group genes identified little imaginal discs, the Drosophila melanogaster homologue of human retinoblastoma binding protein 2. Genetics, 156: 645-663.
24. Heard, E., Chaumeil, J., Masui, O., and Okamoto, I. 2004. Mammalian X-chromosome inactivation: an epigenetics paradigm. Cold Spring Harb. Symp. Quant. Biol. 69: 89-102. doi:10.1101/sqb.2004.69.89.
25. Heintzman, N.D., Stuart, R.K., Hon, G., Fu, Y., Ching, C.W., Hawkins, R.D., et al. 2007. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 39: 311-318. doi:10.1038/ng1966.
26. Helin, K., Harlow, E., and Fattaey, A. 1993. Inhibition of E2F-1 transactivation by direct binding of the retinoblastoma protein. Mol. Cell. Biol. 13: 6501-6508.
27. Iwase, S., Lan, F., Bayliss, P., de la Torre-Ubieta, L., Huarte, M., Qi, H.H., et al. 2007. The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell, 128: 1077-1088. doi:10.1016/j.cell.2007.02.017.
28. Jensen, L.R., Amende, M., Gurok, U., Moser, B., Gimmel, V., Tzschach, A., et al. 2005. Mutations in the JARID1C gene, which is involved in transcriptional regulation and chromatin remodeling, cause X-linked mental retardation. Am. J. Hum. Genet. 76: 227-236. doi:10.1086/427563.
29. Kennison, J.A. 1995. The Polycomb and Trithorax group proteins of Drosophila: trans-regulators of homeotic gene function. Annu. Rev. Genet. 29: 289-303. doi:10.1146/annurev.ge.29.120195.001445.
30. Klose, R.J., Yan, Q., Tothova, Z., Yamane, K., Erdjument-Bromage, H., Tempst, P., et al. 2007. The retinoblastoma binding protein RBP2 is an H3K4 demethylase. Cell, 128: 889-900. doi:10.1016/j.cell.2007.02.013.
31. Kortschak, R.D., Tucker, P.W., and Saint, R. 2000. ARID proteins come in from the desert. Trends Biochem. Sci. 25: 294-299. doi:10.1016/S0968- 0004(00)01597-8.
32. Lee, M.G., Wynder, C., Cooch, N., and Shiekhattar, R. 2005. An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation. Nature (London), 437: 432-435.
33. Lee, T.I., Jenner, R.G., Boyer, L.A., Guenther, M.G., Levine, S.S., Kumar, R.M., et al. 2006. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell, 125: 301-313. doi:10.1016/j.cell.2006. 02.043.
34. Lee, M.G., Norman, J., Shilatifard, A., and Shiekhattar, R. 2007a. Physical and functional association of a trimethyl H3K4 demethylase and Ring6a/MBLR, a polycomb-like protein. Cell, 128: 877-887. doi:10.1016/j.cell.2007.02.004.
35. Lee, N., Zhang, J., Klose, R.J., Erdjument-Bromage, H., Tempst, P., Jones, R.S., and Zhang, Y. 2007b. The trithorax-group protein Lid is a histone H3 trimethyl-Lys4 demethylase. Nat. Struct. Mol. Biol. 14: 341-343. doi:10.1038/nsmb1216.
36. Li, H., Ilin, S., Wang, W., Duncan, E.M., Wysocka, J., Allis, C.D., and Patel, D.J. 2006. Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF. Nature, 442: 91-95.
37. Liang, G., Klose, R.J., Gardner, K.E., and Zhang, Y. 2007. Yeast Jhd2p is a histone H3 Lys4 trimethyl demethylase. Nat. Struct. Mol. Biol. 14: 243-245. doi:10.1038/nsmb1204.
38. Lu, P.J., Sundquist, K., Baeckstrom, D., Poulsom, R., Hanby, A., Meier-Ewert, S., et al. 1999. A novel gene (PLU-1) containing highly conserved putative DNA/chromatin binding motifs is specifically up-regulated in breast cancer. J. Biol. Chem. 274: 15633-15645. doi:10.1074/jbc.274.22.15633.
39. Mao, S., Neale, G.A., and Goorha, R.M. 1997. T-cell oncogene rhombotin-2 interacts with retinoblastoma-binding protein 2. Oncogene, 14: 1531-1539. doi:10.1038/sj.onc.1200988.
40. Metzger, E., Wissmann, M., Yin, N., Muller, J.M., Schneider, R., Peters, A.H., et al. 2005. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature (London), 437: 436-439.
41. Milne, T.A., Briggs, S.D., Brock, H.W., Martin, M.E., Gibbs, D., Allis, C.D., and Hess, J.L. 2002. MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol. Cell, 10: 1107-1117. doi:10.1016/S1097-2765(02) 00741-4.
42. Morris, E.J., and Dyson, N.J. 2001. Retinoblastoma protein partners. Adv. Cancer Res. 82: 1-54.
43. Muchardt, C., and Yaniv, M. 2001. When the SWI/SNF complex remodels.the cell cycle. Oncogene, 20: 3067-3075. doi:10.1038/sj.onc.1204331.
44. Nakamura, T., Mori, T., Tada, S., Krajewski, W., Rozovskaia, T., Wassell, R., et al. 2002. ALL-1 is a histone methyltransferase that assembles a supercomplex of proteins involved in transcriptional regulation. Mol. Cell, 10: 1119-1128. doi:10.1016/S1097-2765(02)00740-2.
45. Narita, M., Nunez, S., Heard, E., Narita, M., Lin, A.W., Hearn, S.A., et al. 2003. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell, 113: 703-716. doi:10.1016/S0092-8674(03)00401-X.
46. Pavri, R., Zhu, B., Li, G., Trojer, P., Mandal, S., Shilatifard, A., and Reinberg, D. 2006. Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell, 125: 703-717. doi:10.1016/j.cell.2006.04.029.
47. Pokholok, D.K., Harbison, C.T., Levine, S., Cole, M., Hannett, N.M., Lee, T.I., et al. 2005. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell, 122: 517-527. doi:10.1016/j.cell.2005.06.026.
48. Quadbeck-Seeger, C., Wanner, G., Huber, S., Kahmann, R., and Kamper, J. 2000. A protein with similarity to the human retinoblastoma binding protein 2 acts specifically as a repressor for genes regulated by the b mating type locus in Ustilago maydis. Mol. Microbiol. 38: 154-166. doi:10.1046/j.1365-2958.2000.02128.x.
49. Roesch, A., Becker, B., Meyer, S., Wild, P., Hafner, C., Landthaler, M., and Vogt, T. 2005. Retinoblastoma-binding protein 2-homolog 1: a retinoblastoma-binding protein downregulated in malignant melanomas. Mod. Pathol. 18: 1249-1257. doi:10.1038/modpathol.3800413.
50. Roesch, A., Becker, B., Schneider-Brachert, W., Hagen, I., Landthaler, M., and Vogt, T. 2006. Re-expression of the retinoblastoma-binding protein 2-homolog 1 reveals tumor-suppressive functions in highly metastatic melanoma cells. J. Invest. Dermatol. 126: 1850-1859. doi:10.1038/sj.jid.5700324.
51. Ropers, H.H., and Hamel, B.C. 2005. X-linked mental retardation. Nat. Rev. Genet. 6: 46-57. doi:10.1038/nrg1501.
52. Ruthenburg, A.J., Allis, C.D., and Wysocka, J. 2007. Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol. Cell, 25: 15-30. doi:10.1016/j.molcel.2006.12.014.
53. Schubeler, D., MacAlpine, D.M., Scalzo, D., Wirbelauer, C., Kooperberg, C., van Leeuwen, F., et al. 2004. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 18: 1263-1271. doi:10.1101/gad.1198204.
54. Schuettengruber, B., Chourrout, D., Vervoort, M., Leblanc, B., and Cavalli, G. 2007. Genome regulation by polycomb and trithorax proteins. Cell, 128: 735-745. doi:10.1016/j.cell.2007.02.009.
55. Schwartz, Y.B., and Pirrotta, V. 2007. Polycomb silencing mechanisms and the management of genomic programmes. Nat. Rev. Genet. 8: 9-22. doi:10.1038/nrg1981.
56. Secombe, J., Li, L., Carlos, L., and Eisenman, R.N. 2007. The Trithorax group protein Lid is a trimethyl histone H3K4 demethylase required for dMyc-induced cell growth. Genes Dev. 21: 537-551. doi:10.1101/gad. 1523007.
57. Sellers, W.R., Novitch, B.G., Miyake, S., Heith, A., Otterson, G.A., Kaye, F.J., Lassar, A.B., and Kaelin, W.G., Jr. 1998. Stable binding to E2F is not required for the retinoblastoma protein to activate transcription, promote differentiation, and suppress tumor cell growth. Genes Dev. 12: 95-106.
58. Seward, D.J., Cubberley, G., Kim, S., Schonewald, M., Zhang, L., Tripet, B., and Bentley, D.L. 2007. Demethylation of trimethylated histone H3 Lys4 in vivo by JARID1 JmjC proteins. Nat. Struct. Mol. Biol. 14: 240-242. doi:10.1038/nsmb1200.
59. Sherr, C.J. 1996. Cancer cell cycles. Science (Washington, D.C.), 274: 1672-1677. doi:10.1126/science.274.5293.1672.
60. Shi, Y., and Whetstine, J.R. 2007. Dynamic regulation of histone lysine methylation by demethylases. Mol. Cell, 25: 1-14. doi:10.1016/j.molcel. 2006.12.010.
61. Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J.R., Cole, P.A., Casero, R.A., and Shi, Y. 2004. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell, 119: 941-953. doi:10.1016/j.cell.2004. 12.012.
62. Shi, Y.J., Matson, C., Lan, F., Iwase, S., Baba, T., and Shi, Y. 2005. Regulation of LSD1 histone demethylase activity by its associated factors. Mol. Cell, 19: 857-864. doi:10.1016/j.molcel.2005.08.027.
63. Shi, X., Hong, T., Walter, K.L., Ewalt, M., Michishita, E., Hung, T., et al. 2006. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature (London), 442: 96-99.
64. Sims, R.J., 3rd, and Reinberg, D. 2006. Histone H3 Lys 4 methylation: caught in a bind? Genes Dev. 20: 2779-2786. doi:10.1101/gad.1468206.
65. Sun, H., Chang, Y., Schweers, B., Dyer, M.A., Zhang, X., Hayward, S.W., and Goodrich, D.W. 2006. An E2F binding-deficient Rb1 protein partially rescues developmental defects associated with Rb1 nullizygosity. Mol. Cell. Biol. 26: 1527-1537. doi:10.1128/MCB.26.4.1527-1537.2006.
66. Tahiliani, M., Mei, P., Fang, R., Leonor, T., Rutenberg, M., Shimizu, F., et al. 2007. The histone H3K4 demethylase SMCX links REST target genes to X-linked mental retardation. Nature (London), 447: 601-605.
67. Tan, K., Shaw, A.L., Madsen, B., Jensen, K., Taylor-Papadimitriou, J., and Freemont, P.S. 2003. Human PLU-1 Has transcriptional repression properties and interacts with the developmental transcription factors BF-1 and PAX9. J. Biol. Chem. 278: 20507-20513. doi:10.1074/jbc.M301994200.
68. Tu, S., Bulloch, E.M., Yang, L., Ren, C., Huang, W.C., Hsu, P.H., et al. 2007. Identification of histone femethylases in Saccharomyces cerevisiae. J. Biol. Chem. 282: 14262-14271. doi:10.1074/jbc.M609900200.
69. van Zutven, L.J., Onen, E., Velthuizen, S.C., van Drunen, E., von Bergh, A.R., van den Heuvel-Eibrink, M.M., et al. 2006. Identification of NUP98 abnormalities in acute leukemia: JARID1A (12p13) as a new partner gene. Genes Chromosomes Cancer, 45: 437-446. doi:10.1002/gcc.20308.
70. Vogt, T., Kroiss, M., McClelland, M., Gruss, C., Becker, B., Bosserhoff, A.K., et al. 1999. Deficiency of a novel retinoblastoma binding protein 2-homolog is a consistent feature of sporadic human melanoma skin cancer. Lab. Invest. 79: 1615-1627.
71. Weinberg, R.A. 1995. The retinoblastoma protein and cell cycle control. Cell, 81: 323-330. doi:10.1016/0092-8674(95)90385-2.
72. Wilsker, D., Patsialou, A., Dallas, P.B., and Moran, E. 2002. ARID proteins: a diverse family of DNA binding proteins implicated in the control of cell growth, differentiation, and development. Cell Growth Differ. 13: 95-106.
73. Wilson, A., Murphy, M.J., Oskarsson, T., Kaloulis, K., Bettess, M.D., Oser, G.M., et al. 2004. c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev. 18: 2747-2763. doi:10.1101/gad.313104.
74. Wurtele, H., and Verreault, A. 2006. Histone post-translational modifications and the response to DNA double-strand breaks. Curr. Opin. Cell Biol. 18: 137-144. doi:10.1016/j.ceb.2006.02.008.
75. Wysocka, J., Swigut, T., Milne, T.A., Dou, Y., Zhang, X., Burlingame, A.L., et al. 2005. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell, 121: 859-872. doi:10.1016/j.cell.2005.03.036.
76. Wysocka, J., Swigut, T., Xiao, H., Milne, T.A., Kwon, S.Y., Landry, J., et al. 2006. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature (London), 442: 86-90.
77. Yamane, K., Toumazou, C., Tsukada, Y., Erdjument-Bromage, H., Tempst, P., Wong, J., and Zhang, Y. 2006. JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell, 125: 483-495. doi:10.1016/j.cell.2006.03.027.
78. Yang, M., Gocke, C.B., Luo, X., Borek, D., Tomchick, D.R., Machius, M., Otwinowski, Z., and Yu, H. 2006. Structural basis for CoREST-dependent demethylation of nucleosomes by the human LSD1 histone demethylase. Mol. Cell, 23: 377-387. doi:10.1016/j.molcel.2006.07.012.
79. Zhang, K., Siino, J.S., Jones, P.R., Yau, P.M., and Bradbury, E.M. 2004. A mass spectrometric "Western blot" to evaluate the correlations between histone methylation and histone acetylation. Proteomics, 4: 3765-3775. doi:10.1002/pmic.200400819.