XAcetylation-mediated proteasomal degradation of core histones during DNA repair and spermatogenesis

Cell

Volumn 153, Issue 5, 2013, Pages 1012-

  Qian, Min Xian ^a   Pang, Ye ^a   Liu, Cui Hua ^a,b   Haratake, Kousuke ^d   Du, Bo Yu ^e   Ji, Dan Yang ^a   Wang, Guang Fei ^a   Zhu, Qian Qian ^a   Song, Wei ^e   Yu, Yadong ^f   Zhang, Xiao Xu ^a   Huang, Hai Tao ^e   Miao, Shiying ^e   Chen, Lian Bin ^a   Zhang, Zi Hui ^a   Liang, Ya Nan ^a   Liu, Shan ^a   Cha, Hwangho ^a   Yang, Dong ^a   Zhai, Yonggong ^a   Komatsu, Takuo ^d   Tsuruta, Fuminori ^d   Li, Haitao ^g   Cao, Cheng ^h   Li, Wei ^c   Li, Guo Hong ^c   Cheng, Yifan ^f   Chiba, Tomoki ^d   Wang, Linfang ^e   Goldberg, Alfred L ⁱ   Shen, Yan ^e   Qiu, Xiao Bo ^a,e   more..

^a BEIJING NORMAL UNIVERSITY   (China)

^b INSTITUTE OF MICROBIOLOGY   (China)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^d UNIVERSITY OF TSUKUBA   (Japan)

^e PEKING UNION MEDICAL COLLEGE   (China)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g TSINGHUA UNIVERSITY   (China)

^h BEIJING INSTITUTE OF BIOTECHNOLOGY   (China)

ⁱ HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DOUBLE STRANDED DNA; HISTONE; PROTEASOME;

ACETYLATION; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; EPIGENETICS; GENE DELETION; GENE EXPRESSION; IMMUNOBLOTTING; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; SPERMATID; SPERMATOGENESIS; TESTIS; UBIQUITINATION;

MAMMALIA; MUS;

EID: 84878314537     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.04.032     Document Type: Article

References (51)

1. J. Blickwedehl, M. Agarwal, C. Seong, R.K. Pandita, T. Melendy, P. Sung, T.K. Pandita, and N. Bangia Role for proteasome activator PA200 and postglutamyl proteasome activity in genomic stability Proc. Natl. Acad. Sci. USA 105 2008 16165 16170
2. E.I. Campos, and D. Reinberg Histones: annotating chromatin Annu. Rev. Genet. 43 2009 559 599
3. P. Cascio, M. Call, B.M. Petre, T. Walz, and A.L. Goldberg Properties of the hybrid form of the 26S proteasome containing both 19S and PA28 complexes EMBO J. 21 2002 2636 2645
4. Y.S. Chen, and X.B. Qiu Transcription-coupled replacement of histones: degradation or recycling? J. Genet. Genomics 39 2012 575 580
5. T. Dange, D. Smith, T. Noy, P.C. Rommel, L. Jurzitza, R.J. Cordero, A. Legendre, D. Finley, A.L. Goldberg, and M. Schmidt Blm10 protein promotes proteasomal substrate turnover by an active gating mechanism J. Biol. Chem. 286 2011 42830 42839
6. R.B. Deal, J.G. Henikoff, and S. Henikoff Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones Science 328 2010 1161 1164
7. C. Dhalluin, J.E. Carlson, L. Zeng, C. He, A.K. Aggarwal, and M.M. Zhou Structure and ligand of a histone acetyltransferase bromodomain Nature 399 1999 491 496
8. M.F. Dion, T. Kaplan, M. Kim, S. Buratowski, N. Friedman, and O.J. Rando Dynamics of replication-independent histone turnover in budding yeast Science 315 2007 1405 1408
9. J.A. Downs, S. Allard, O. Jobin-Robitaille, A. Javaheri, A. Auger, N. Bouchard, S.J. Kron, S.P. Jackson, and J. Côté Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites Mol. Cell 16 2004 979 990
10. P. Filippakopoulos, S. Picaud, M. Mangos, T. Keates, J.P. Lambert, D. Barsyte-Lovejoy, I. Felletar, R. Volkmer, S. Müller, and T. Pawson Histone recognition and large-scale structural analysis of the human bromodomain family Cell 149 2012 214 231
11. D. Finley Recognition and processing of ubiquitin-protein conjugates by the proteasome Annu. Rev. Biochem. 78 2009 477 513
12. J. Gaucher, N. Reynoird, E. Montellier, F. Boussouar, S. Rousseaux, and S. Khochbin From meiosis to postmeiotic events: the secrets of histone disappearance FEBS J. 277 2010 599 604
13. M.H. Glickman, and A. Ciechanover The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction Physiol. Rev. 82 2002 373 428
14. A.L. Goldberg Protein degradation and protection against misfolded or damaged proteins Nature 426 2003 895 899
15. S.S. Hammoud, D.A. Nix, H. Zhang, J. Purwar, D.T. Carrell, and B.R. Cairns Distinctive chromatin in human sperm packages genes for embryo development Nature 460 2009 473 478
16. M.S. Huen, R. Grant, I. Manke, K. Minn, X. Yu, M.B. Yaffe, and J. Chen RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly Cell 131 2007 901 914
17. C. Janke, M.M. Magiera, N. Rathfelder, C. Taxis, S. Reber, H. Maekawa, A. Moreno-Borchart, G. Doenges, E. Schwob, E. Schiebel, and M. Knop A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes Yeast 21 2004 947 962
18. B. Khor, A.L. Bredemeyer, C.Y. Huang, I.R. Turnbull, R. Evans, L.B. Maggi Jr., J.M. White, L.M. Walker, K. Carnes, R.A. Hess, and B.P. Sleckman Proteasome activator PA200 is required for normal spermatogenesis Mol. Cell. Biol. 26 2006 2999 3007
19. A.F. Kisselev, T.N. Akopian, and A.L. Goldberg Range of sizes of peptide products generated during degradation of different proteins by archaeal proteasomes J. Biol. Chem. 273 1998 1982 1989
20. N. Kotaja, S. Kimmins, S. Brancorsini, D. Hentsch, J.L. Vonesch, I. Davidson, M. Parvinen, and P. Sassone-Corsi Preparation, isolation and characterization of stage-specific spermatogenic cells for cellular and molecular analysis Nat. Methods 1 2004 249 254
21. X. Li, D.M. Lonard, S.Y. Jung, A. Malovannaya, Q. Feng, J. Qin, S.Y. Tsai, M.J. Tsai, and B.W. O'Malley The SRC-3/AIB1 coactivator is degraded in a ubiquitin- and ATP-independent manner by the REGgamma proteasome Cell 124 2006 381 392
22. Z. Liu, D. Miao, Q. Xia, L. Hermo, and S.S. Wing Regulated expression of the ubiquitin protein ligase, E3(Histone)/LASU1/Mule/ARF-BP1/HUWE1, during spermatogenesis Dev. Dyn. 236 2007 2889 2898
23. L.Y. Lu, J. Wu, L. Ye, G.B. Gavrilina, T.L. Saunders, and X. Yu RNF8-dependent histone modifications regulate nucleosome removal during spermatogenesis Dev. Cell 18 2010 371 384
24. F. Mateo, M. Vidal-Laliena, N. Canela, L. Busino, M.A. Martinez-Balbas, M. Pagano, N. Agell, and O. Bachs Degradation of cyclin A is regulated by acetylation Oncogene 28 2009 2654 2666
25. N.C. Mills, N.T. Van, and A.R. Means Histones of rat testis chromatin during early postnatal development and their interactions with DNA Biol. Reprod. 17 1977 760 768
26. S. Murata, K. Sasaki, T. Kishimoto, S. Niwa, H. Hayashi, Y. Takahama, and K. Tanaka Regulation of CD8+ T cell development by thymus-specific proteasomes Science 316 2007 1349 1353
27. R. Murr, J.I. Loizou, Y.G. Yang, C. Cuenin, H. Li, Z.Q. Wang, and Z. Herceg Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks Nat. Cell Biol. 8 2006 91 99
28. J. Ortega, J.B. Heymann, A.V. Kajava, V. Ustrell, M. Rechsteiner, and A.C. Steven The axial channel of the 20S proteasome opens upon binding of the PA200 activator J. Mol. Biol. 346 2005 1221 1227
29. B. Petersen, T.N. Petersen, P. Andersen, M. Nielsen, and C. Lundegaard A generic method for assignment of reliability scores applied to solvent accessibility predictions BMC Struct. Biol. 9 2009 51
30. X.B. Qiu, and A.L. Goldberg Nrdp1/FLRF is a ubiquitin ligase promoting ubiquitination and degradation of the epidermal growth factor receptor family member, ErbB3 Proc. Natl. Acad. Sci. USA 99 2002 14843 14848
31. X.B. Qiu, S.Y. Ouyang, C.J. Li, S. Miao, L. Wang, and A.L. Goldberg hRpn13/ADRM1/GP110 is a novel proteasome subunit that binds the deubiquitinating enzyme, UCH37 EMBO J. 25 2006 5742 5753
32. H. Reinke, and W. Hörz Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter Mol. Cell 11 2003 1599 1607
33. T. Robert, F. Vanoli, I. Chiolo, G. Shubassi, K.A. Bernstein, R. Rothstein, O.A. Botrugno, D. Parazzoli, A. Oldani, S. Minucci, and M. Foiani HDACs link the DNA damage response, processing of double-strand breaks and autophagy Nature 471 2011 74 79
34. K.L. Rock, and A.L. Goldberg Degradation of cell proteins and the generation of MHC class I-presented peptides Annu. Rev. Immunol. 17 1999 739 779
35. K. Sadre-Bazzaz, F.G. Whitby, H. Robinson, T. Formosa, and C.P. Hill Structure of a Blm10 complex reveals common mechanisms for proteasome binding and gate opening Mol. Cell 37 2010 728 735
36. M. Schmidt, W. Haas, B. Crosas, P.G. Santamaria, S.P. Gygi, T. Walz, and D. Finley The HEAT repeat protein Blm10 regulates the yeast proteasome by capping the core particle Nat. Struct. Mol. Biol. 12 2005 294 303
37. U. Seifert, L.P. Bialy, F. Ebstein, D. Bech-Otschir, A. Voigt, F. Schröter, T. Prozorovski, N. Lange, J. Steffen, and M. Rieger Immunoproteasomes preserve protein homeostasis upon interferon-induced oxidative stress Cell 142 2010 613 624
38. J.E. Shabason, P.J. Tofilon, and K. Camphausen Grand rounds at the National Institutes of Health: HDAC inhibitors as radiation modifiers, from bench to clinic J. Cell. Mol. Med. 15 2011 2735 2744
39. R.K. Singh, M.H. Kabbaj, J. Paik, and A. Gunjan Histone levels are regulated by phosphorylation and ubiquitylation-dependent proteolysis Nat. Cell Biol. 11 2009 925 933
40. D.M. Smith, S.C. Chang, S. Park, D. Finley, Y. Cheng, and A.L. Goldberg Docking of the proteasomal ATPases' carboxyl termini in the 20S proteasome's alpha ring opens the gate for substrate entry Mol. Cell 27 2007 731 744
41. A. Toulmay, and R. Schneiter A two-step method for the introduction of single or multiple defined point mutations into the genome of Saccharomyces cerevisiae Yeast 23 2006 825 831
42. T. Tsukuda, A.B. Fleming, J.A. Nickoloff, and M.A. Osley Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae Nature 438 2005 379 383
43. V. Ustrell, G. Pratt, C. Gorbea, and M. Rechsteiner Purification and assay of proteasome activator PA200 Methods Enzymol. 398 2005 321 329
44. J. van Loosdregt, Y. Vercoulen, T. Guichelaar, Y.Y. Gent, J.M. Beekman, O. van Beekum, A.B. Brenkman, D.J. Hijnen, T. Mutis, and E. Kalkhoven Regulation of Treg functionality by acetylation-mediated Foxp3 protein stabilization Blood 115 2010 965 974
45. B. Zhong, L. Zhang, C. Lei, Y. Li, A.P. Mao, Y. Yang, Y.Y. Wang, X.L. Zhang, and H.B. Shu The ubiquitin ligase RNF5 regulates antiviral responses by mediating degradation of the adaptor protein MITA Immunity 30 2009 397 407
46. B. Zhu, and D. Reinberg Epigenetic inheritance: uncontested? Cell Res. 21 2011 435 441
47. J. Frank, M. Radermacher, P. Penczek, J. Zhu, Y. Li, M. Ladjadj, and A. Leith SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields J. Struct. Biol. 116 1996 190 199
48. K. Luger, T.J. Rechsteiner, and T.J. Richmond Expression and purification of recombinant histones and nucleosome reconstitution Methods Mol. Biol. 119 1999 1 16
49. M. Ohi, Y. Li, Y. Cheng, and T. Walz Negative Staining and Image Classification - Powerful Tools in Modern Electron Microscopy Biol. Proced. Online 6 2004 23 34
50. D. Shechter, H.L. Dormann, C.D. Allis, and S.B. Hake Extraction, purification and analysis of histones Nat. Protoc. 2 2007 1445 1457
51. C. Wójcik, M. Rowicka, A. Kudlicki, D. Nowis, E. McConnell, M. Kujawa, and G.N. DeMartino Valosin-containing protein (p97) is a regulator of endoplasmic reticulum stress and of the degradation of N-end rule and ubiquitin-fusion degradation pathway substrates in mammalian cells Mol. Biol. Cell 17 2006 4606 4618