The ubiquitin-conjugating enzyme HR6B is required for maintenance of X chromosome silencing in mouse spermatocytes and spermatids

BMC Genomics

Volumn 11, Issue 1, 2010, Pages

  Mulugeta Achame, Eskeatnaf ^a   Wassenaar, Evelyne ^a   Hoogerbrugge, Jos W ^a   Sleddens Linkels, Esther ^a   Ooms, Marja ^b   Sun, Zu Wen ^c   van IJcken, Wilfred F J ^a   Grootegoed, J Anton ^a   Baarends, Willy M ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b VANDERBILT INGRAM CANCER CENTER   (United States)

^c Erasmus MC ^*

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H2B; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN CONJUGATING ENZYME HR6B; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; HISTONE; MICROTUBULE ASSOCIATED PROTEIN; PHOSPHOPROTEIN; SPINDLIN; UBE2A PROTEIN, MOUSE; UBE2B PROTEIN, MOUSE; UBIQUITIN PROTEIN LIGASE; UBR2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOSOME; CELL SPECIFICITY; CENTROMERE; CHROMATIN; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; FEMALE; GENE EXPRESSION REGULATION; GENE SILENCING; KNOCKOUT MOUSE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PACHYTENE; PROPHASE; SPERMATID; SPERMATOCYTE; TRANSCRIPTION REGULATION; UBIQUITINATION; X CHROMOSOME; X CHROMOSOME LINKAGE; Y CHROMOSOME; ANIMAL; ANTIBODY SPECIFICITY; GENE DOSAGE; GENE EXPRESSION PROFILING; GENE INACTIVATION; GENETIC TRANSCRIPTION; GENETICS; MALE; METABOLISM; TESTIS; TRANSCRIPTION INITIATION; UPREGULATION; X CHROMOSOMAL INHERITANCE; X CHROMOSOME INACTIVATION;

ANIMALS; CELL CYCLE PROTEINS; CENTROMERE; CHROMATIN; GENE DOSAGE; GENE EXPRESSION PROFILING; GENE KNOCKOUT TECHNIQUES; GENES, X-LINKED; HISTONES; MALE; MICE; MICROTUBULE-ASSOCIATED PROTEINS; ORGAN SPECIFICITY; PHOSPHOPROTEINS; SPERMATIDS; SPERMATOCYTES; TESTIS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; UP-REGULATION; X CHROMOSOME; X CHROMOSOME INACTIVATION; Y CHROMOSOME;

EID: 77954887917     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-11-367     Document Type: Article

References (65)

1. Koken MH, Reynolds P, Jaspers-Dekker I, Prakash L, Prakash S, Bootsma D, Hoeijmakers JH. Structural and functional conservation of two human homologs of the yeast DNA repair gene RAD6. Proc Natl Acad Sci USA 1991, 88(20):8865-8869. 10.1073/pnas.88.20.8865, 52611, 1717990.
2. Varshavsky A. Regulated protein degradation. Trends Biochem Sci 2005, 30(6):283-286. 10.1016/j.tibs.2005.04.005, 15950869.
3. Pickart CM, Fushman D. Polyubiquitin chains: polymeric protein signals. Curr Opin Chem Biol 2004, 8(6):610-616. 10.1016/j.cbpa.2004.09.009, 15556404.
4. Varshavsky A. The N-end rule pathway of protein degradation. Genes Cells 1997, 2(1):13-28. 10.1046/j.1365-2443.1997.1020301.x, 9112437.
5. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 2002, 419(6903):135-141. 10.1038/nature00991, 12226657.
6. Robzyk K, Recht J, Osley MA. Rad6-dependent ubiquitination of histone H2B in yeast. Science 2000, 287(5452):501-504. 10.1126/science.287.5452.501, 10642555.
7. Hwang WW, Venkatasubrahmanyam S, Ianculescu AG, Tong A, Boone C, Madhani HD. A Conserved RING Finger Protein Required for Histone H2B Monoubiquitination and Cell Size Control. Mol Cell 2003, 11(1):261-266. 10.1016/S1097-2765(02)00826-2, 12535538.
8. Wood A, Krogan NJ, Dover J, Schneider J, Heidt J, Boateng MA, Dean K, Golshani A, Zhang Y, Greenblatt JF, Johnston M, Shilatifard A. Bre1, an e3 ubiquitin ligase required for recruitment and substrate selection of rad6 at a promoter. Mol Cell 2003, 11(1):267-274. 10.1016/S1097-2765(02)00802-X, 12535539.
9. Davie JR, Murphy LC. Inhibition of transcription selectively reduces the level of ubiquitinated histone H2B in chromatin. Biochem Biophys Res Commun 1994, 203(1):344-350. 10.1006/bbrc.1994.2188, 8074677.
10. Davie JR, Murphy LC. Level of ubiquitinated histone H2B in chromatin is coupled to ongoing transcription. Biochemistry 1990, 29(20):4752-4757. 10.1021/bi00472a002, 2163669.
11. Nickel BE, Allis CD, Davie JR. Ubiquitinated histone H2B is preferentially located in transcriptionally active chromatin. Biochemistry 1989, 28(3):958-963. 10.1021/bi00429a006, 2713375.
12. Daniel JA, Torok MS, Sun ZW, Schieltz D, Allis CD, Yates JR, Grant PA. Deubiquitination of histone H2B by a yeast acetyltransferase complex regulates transcription. J Biol Chem 2004, 279(3):1867-1871. 10.1074/jbc.C300494200, 14660634.
13. Henry KW, Wyce A, Lo WS, Duggan LJ, Emre NC, Kao CF, Pillus L, Shilatifard A, Osley MA, Berger SL. Transcriptional activation via sequential histone H2B ubiquitylation and deubiquitylation, mediated by SAGA-associated Ubp8. Genes Dev 2003, 17(21):2648-2663. 10.1101/gad.1144003, 280615, 14563679.
14. Sun ZW, Allis CD. Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 2002, 418(6893):104-108. 10.1038/nature00883, 12077605.
15. Wood A, Schneider J, Dover J, Johnston M, Shilatifard A. The Bur1/Bur2 Complex Is Required for Histone H2B Monoubiquitination by Rad6/Bre1 and Histone Methylation by COMPASS. Mol Cell 2005, 20(4):589-599. 10.1016/j.molcel.2005.09.010, 16307922.
16. Sarcevic B, Mawson A, Baker RT, Sutherland RL. Regulation of the ubiquitin-conjugating enzyme hHR6A by CDK-mediated phosphorylation. EMBO J 2002, 21(8):2009-2018. 10.1093/emboj/21.8.2009, 125963, 11953320.
17. Jenuwein T, Allis CD. Translating the histone code. Science 2001, 293(5532):1074-1080. 10.1126/science.1063127, 11498575.
18. Briggs SD, Xiao T, Sun ZW, Caldwell JA, Shabanowitz J, Hunt DF, Allis CD, Strahl BD. Gene silencing: trans-histone regulatory pathway in chromatin. Nature 2002, 418(6897):498. 10.1038/nature00970, 12152067.
19. Dover J, Schneider J, Boateng MA, Wood A, Dean K, Johnston M, Shilatifard A. Methylation of histone H3 by COMPASS requires ubiquitination of histone H2B by RAD6. J Biol Chem 2002, 277:28368-28371. 10.1074/jbc.C200348200, 12070136.
20. Ng HH, Xu RM, Zhang Y, Struhl K. Ubiquitination of histone H2B by Rad6 is required for efficient Dot1-mediated methylation of histone H3 lysine 79. J Biol Chem 2002, 277(38):34655-34657. 10.1074/jbc.C200433200, 12167634.
21. Foster ER, Downs JA. Methylation of H3 K4 and K79 is not strictly dependent on H2B K123 ubiquitylation. J Cell Biol 2009, 184(5):631-638. 10.1083/jcb.200812088, 2686411, 19255247.
22. Kim J, Hake SB, Roeder RG. The human homolog of yeast BRE1 functions as a transcriptional coactivator through direct activator interactions. Mol Cell 2005, 20(5):759-770. 10.1016/j.molcel.2005.11.012, 16337599.
23. Zhu B, Zheng Y, Pham AD, Mandal SS, Erdjument-Bromage H, Tempst P, Reinberg D. Monoubiquitination of Human Histone H2B: The Factors Involved and Their Roles in HOX Gene Regulation. Mol Cell 2005, 20(4):601-611. 10.1016/j.molcel.2005.09.025, 16307923.
24. Kim J, Guermah M, McGinty RK, Lee JS, Tang Z, Milne TA, Shilatifard A, Muir TW, Roeder RG. RAD6-Mediated transcription-coupled H2B ubiquitylation directly stimulates H3K4 methylation in human cells. Cell 2009, 137(3):459-471. 10.1016/j.cell.2009.02.027, 2678028, 19410543.
25. Roest HP, Klaveren van J, Wit de J, Gurp van CG, Koken MHM, Vermey M, Roijen van JH, Vreeburg JTM, Baarends WM, Bootsma D, Grootegoed JA, Hoeijmakers JHJ. Inactivation of the HR6B ubiquitin-conjugating DNA repair enzyme in mice causes a defect in spermatogenesis associated with chromatin modification. Cell 1996, 86:799-810. 10.1016/S0092-8674(00)80154-3, 8797826.
26. Roest HP, Baarends WM, de Wit J, van Klaveren JW, Wassenaar E, Hoogerbrugge JW, van Cappellen WA, Hoeijmakers JH, Grootegoed JA. The ubiquitin-conjugating DNA repair enzyme HR6A is a maternal factor essential for early embryonic development in mice. Mol Cell Biol 2004, 24(12):5485-5495. 10.1128/MCB.24.12.5485-5495.2004, 419895, 15169909.
27. Koken MHM, Hoogerbrugge JW, Jaspers-Dekker I, de Wit J, Willemsen R, Roest HP, Grootegoed JA, Hoeijmakers JHJ. Expression of the ubiquitin-conjugating DNA repair enzymes HHR6A and B suggests a role in spermatogenesis and chromatin modification. Dev Biol 1996, 173:119-132. 10.1006/dbio.1996.0011, 8575614.
28. Epstein CJ. Mammalian oocytes: X chromosome activity. Science 1969, 163(871):1078-1079. 10.1126/science.163.3871.1078, 5764873.
29. Johnston PG. X chromosome activity in female germ cells of mice heterozygous for Searle's translocation T(X;16)16H. Genet Res 1981, 37(3):317-322. 10.1017/S0016672300020322, 7262556.
30. Monk M, McLaren A. X-chromosome activity in foetal germ cells of the mouse. J Embryol Exp Morphol 1981, 63:75-84.
31. Monesi V. Differential rate of ribonucleic acid synthesis in the autosomes and sex chromosomes during male meiosis in the mouse. Chromosoma 1965, 17:11-21. 10.1007/BF00285153, 5833946.
32. Yang F, Wang PJ. The Mammalian synaptonemal complex: a scaffold and beyond. Genome dynamics 2009, 5:69-80. full_text, 18948708.
33. Turner JM, Mahadevaiah SK, Fernandez-Capetillo O, Nussenzweig A, Xu X, Deng CX, Burgoyne PS. Silencing of unsynapsed meiotic chromosomes in the mouse. Nat Genet 2005, 37(1):41-47.
34. Namekawa SH, Park PJ, Zhang LF, Shima JE, McCarrey JR, Griswold MD, Lee JT. Postmeiotic sex chromatin in the male germline of mice. Curr Biol 2006, 16(7):660-667. 10.1016/j.cub.2006.01.066, 16581510.
35. Turner JM, Mahadevaiah SK, Ellis PJ, Mitchell MJ, Burgoyne PS. Pachytene asynapsis drives meiotic sex chromosome inactivation and leads to substantial postmeiotic repression in spermatids. Dev Cell 2006, 10(4):521-529. 10.1016/j.devcel.2006.02.009, 16580996.
36. Mueller JL, Mahadevaiah SK, Park PJ, Warburton PE, Page DC, Turner JM. The mouse X chromosome is enriched for multicopy testis genes showing postmeiotic expression. Nat Genet 2008, 40(6):794-799. 10.1038/ng.126, 2740655, 18454149.
37. van der Laan R, Uringa EJ, Wassenaar E, Hoogerbrugge JW, Sleddens E, Odijk H, Roest HP, de Boer P, Hoeijmakers JH, Grootegoed JA, Baarends WM. Ubiquitin ligase Rad18Sc localizes to the XY body and to other chromosomal regions that are unpaired and transcriptionally silenced during male meiotic prophase. J Cell Sci 2004, 117(Pt 21):5023-5033. 10.1242/jcs.01368, 15383616.
38. Baarends WM, Wassenaar E, Hoogerbrugge JW, van Cappellen G, Roest HP, Vreeburg J, Ooms M, Hoeijmakers JH, Grootegoed JA. Loss of HR6B ubiquitin-conjugating activity results in damaged synaptonemal complex structure and increased crossing-over frequency during the male meiotic prophase. Mol Cell Biol 2003, 23(4):1151-1162. 10.1128/MCB.23.4.1151-1162.2003, 141135, 12556476.
39. Baarends WM, Wassenaar E, Hoogerbrugge JW, Schoenmakers S, Sun ZW, Grootegoed JA. Increased phosphorylation and dimethylation of XY body histones in the Hr6b-knockout mouse is associated with derepression of the X chromosome. J Cell Sci 2007, 120(Pt 11):1841-1851. 10.1242/jcs.03451, 17488778.
40. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K. High-resolution profiling of histone methylations in the human genome. Cell 2007, 129(4):823-837. 10.1016/j.cell.2007.05.009, 17512414.
41. Rosenfeld JA, Wang Z, Schones DE, Zhao K, DeSalle R, Zhang MQ. Determination of enriched histone modifications in non-genic portions of the human genome. BMC genomics 2009, 10:143. 10.1186/1471-2164-10-143, 2667539, 19335899.
42. Hendriksen PJM, Hoogerbrugge JW, Themmen APN, Koken MHM, Hoeijmakers JHJ, Oostra BA, Van der Lende T, Grootegoed JA. Postmeiotic transcription of X and Y chromosomal genes during spermatogenesis in the mouse. Dev Biol 1995, 170:730-733. 10.1006/dbio.1995.1252, 7649399.
43. Hadjantonakis AK, Cox LL, Tam PP, Nagy A. An X-linked GFP transgene reveals unexpected paternal X-chromosome activity in trophoblastic giant cells of the mouse placenta. Genesis 2001, 29(3):133-140. 10.1002/gene.1016, 11252054.
44. An JY, Kim EA, Jiang Y, Zakrzewska A, Kim DE, Lee MJ, Mook-Jung I, Zhang Y, Kwon YT. UBR2 mediates transcriptional silencing during spermatogenesis via histone ubiquitination. Proc Natl Acad Sci USA 2010, 107(5):1912-1917. 10.1073/pnas.0910267107, 20080676.
45. Lu LY, Wu J, Ye L, Gavrilina GB, Saunders TL, Yu X. RNF8-dependent histone modifications regulate nucleosome removal during spermatogenesis. Dev Cell 2010, 18(3):371-384. 10.1016/j.devcel.2010.01.010, 20153262.
46. Schultz N, Hamra FK, Garbers DL. A multitude of genes expressed solely in meiotic or postmeiotic spermatogenic cells offers a myriad of contraceptive targets. Proc Natl Acad Sci USA 2003, 100(21):12201-12206. 10.1073/pnas.1635054100, 218736, 14526100.
47. van Leeuwen F, Gafken PR, Gottschling DE. Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell 2002, 109(6):745-756. 10.1016/S0092-8674(02)00759-6, 12086673.
48. Ng HH, Ciccone DN, Morshead KB, Oettinger MA, Struhl K. Lysine-79 of histone H3 is hypomethylated at silenced loci in yeast and mammalian cells: a potential mechanism for position-effect variegation. Proc Natl Acad Sci USA 2003, 100(4):1820-1825. 10.1073/pnas.0437846100, 149917, 12574507.
49. Schubeler D, MacAlpine DM, Scalzo D, Wirbelauer C, Kooperberg C, van Leeuwen F, Gottschling DE, O'Neill LP, Turner BM, Delrow J, Bell SP, Groudine M. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev 2004, 18(11):1263-1271. 10.1101/gad.1198204, 420352, 15175259.
50. Tanny JC, Erdjument-Bromage H, Tempst P, Allis CD. Ubiquitylation of histone H2B controls RNA polymerase II transcription elongation independently of histone H3 methylation. Genes Dev 2007, 21(7):835-847. 10.1101/gad.1516207, 1838534, 17374714.
51. Shema E, Tirosh I, Aylon Y, Huang J, Ye C, Moskovits N, Raver-Shapira N, Minsky N, Pirngruber J, Tarcic G, Hublarova P, Moyal L, Gana-Weisz M, Shiloh Y, Yarden Y, Johnsen SA, Vojtesek B, Berger SL, Oren M. The histone H2B-specific ubiquitin ligase RNF20/hBRE1 acts as a putative tumor suppressor through selective regulation of gene expression. Genes Dev 2008, 22(19):2664-2676. 10.1101/gad.1703008, 2559905, 18832071.
52. Chandrasekharan MB, Huang F, Sun ZW. Ubiquitination of histone H2B regulates chromatin dynamics by enhancing nucleosome stability. Proc Natl Acad Sci USA 2009, 106(39):16686-16691. 10.1073/pnas.0907862106, 2757834, 19805358.
53. Singer MS, Kahana A, Wolf AJ, Meisinger LL, Peterson SE, Goggin C, Mahowald M, Gottschling DE. Identification of high-copy disruptors of telomeric silencing in Saccharomyces cerevisiae. Genetics 1998, 150(2):613-632. 1460361, 9755194.
54. Krogan NJ, Dover J, Khorrami S, Greenblatt JF, Schneider J, Johnston M, Shilatifard A. COMPASS, a histone H3 (Lysine 4) methyltransferase required for telomeric silencing of gene expression. J Biol Chem 2002, 277(13):10753-10755. 10.1074/jbc.C200023200, 11805083.
55. Ng HH, Feng Q, Wang H, Erdjument-Bromage H, Tempst P, Zhang Y, Struhl K. Lysine methylation within the globular domain of histone H3 by Dot1 is important for telomeric silencing and Sir protein association. Genes Dev 2002, 16(12):1518-1527. 10.1101/gad.1001502, 186335, 12080090.
56. Verzijlbergen KF, Faber AW, Stulemeijer IJ, van Leeuwen F. Multiple histone modifications in euchromatin promote heterochromatin formation by redundant mechanisms in Saccharomyces cerevisiae. BMC Mol Biol 2009, 10:76. 10.1186/1471-2199-10-76, 2724485, 19638198.
57. Baarends WM, Hoogerbrugge JW, Roest HP, Ooms M, Vreeburg J, Hoeijmakers JHJ, Grootegoed JA. Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. Dev Biol 1999, 207:322-333. 10.1006/dbio.1998.9155, 10068466.
58. Hazzouri M, Pivot-Pajot C, Faure AK, Usson Y, Pelletier R, Sele B, Khochbin S, Rousseaux S. Regulated hyperacetylation of core histones during mouse spermatogenesis: involvement of histone deacetylases. Eur J Cell Biol 2000, 79(12):950-960. 10.1078/0171-9335-00123, 11152286.
59. Cocquet J, Ellis PJ, Yamauchi Y, Mahadevaiah SK, Affara NA, Ward MA, Burgoyne PS. The multicopy gene Sly represses the sex chromosomes in the male mouse germline after meiosis. PLoS biology 2009, 7(11):e1000244. 10.1371/journal.pbio.1000244, 2770110, 19918361.
60. Song R, Ro S, Michaels JD, Park C, McCarrey JR, Yan W. Many X-linked microRNAs escape meiotic sex chromosome inactivation. Nat Genet 2009, 41(4):488-493. 10.1038/ng.338, 2723799, 19305411.
61. Grootegoed JA, Jansen R, van der Molen HJ. Effect of glucose on ATP dephosphorylation in rat spermatids. J Reprod Fertil 1986, 77(1):99-107.
62. Martens JH, O'Sullivan RJ, Braunschweig U, Opravil S, Radolf M, Steinlein P, Jenuwein T. The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J 2005, 24(4):800-812. 10.1038/sj.emboj.7600545, 549616, 15678104.
63. Peters AH, Plug AW, de Boer P. Meiosis in carriers of heteromorphic bivalents: sex differences and implications for male fertility. Chromosome Res 1997, 5(5):313-324. 10.1023/B:CHRO.0000038762.60086.ef, 9292236.
64. Smith GK. Limma: linear models for microarray data. Bioinformatics and Computational Biology Solutions using R and Bioconductor 2005, 397-420. New York: Springer, Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W.
65. Smith GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Statistical Applications in Genetics and Molecular Biology 2004, 3(1). Article 1.