The role of arginine methylation in the DNA damage response

DNA Repair

Volumn 12, Issue 7, 2013, Pages 459-465

  Auclair, Yannick ^a   Richard, Stéphane ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Arginine methylation; Cancer; DNA damage; PRMTs

Indexed keywords

BRCA1 PROTEIN; HISTONE; MRE11 PROTEIN; PROTEIN ARGININE METHYLTRANSFERASE; PROTEIN P53; PROTEIN RAD9; RNA BINDING PROTEIN;

CATALYSIS; DNA DAMAGE; DNA REPAIR; EPIGENETICS; GENE EXPRESSION; GENETIC REGULATION; GENOMIC INSTABILITY; PRIORITY JOURNAL; PROTEIN METHYLATION; PROTEIN PROCESSING; REVIEW; RNA METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; ARGININE; DNA DAMAGE; DNA REPAIR; HUMANS; METHYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84878658883     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2013.04.006     Document Type: Review

References (118)

1. Ciccia A., Elledge S.J. The DNA damage response: making it safe to play with knives. Mol. Cell 2010, 40:179-204.
2. Polo S.E., Jackson S.P. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev. 2011, 25:409-433.
3. Natarajan A.T., Palitti F. DNA repair and chromosomal alterations. Mutat. Res. 2008, 657:3-7.
4. Sancar A., Lindsey-Boltz L.A., Unsal-Kacmaz K., Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 2004, 73:39-85.
5. Curtin N.J. DNA repair dysregulation from cancer driver to therapeutic target. Nat. Rev. Cancer 2012, 12:801-817.
6. Nicholson T.B., Chen T., Richard S. The physiological and pathophysiological role of prmt1-mediated protein arginine methylation. Pharmacol. Res. 2009, 60:466-474.
7. Bedford M.T., Clarke S.G. Protein arginine methylation in mammals: who, what, and why. Mol. Cell 2009, 33:1-13.
8. Yang Y., Bedford M.T. Protein arginine methyltransferases and cancer. Nat. Rev. Cancer 2013, 13:37-50.
9. Miranda T.B., Miranda M., Frankel A., Clarke S. Prmt7 is a member of the protein arginine methyltransferase family with a distinct substrate specificity. J. Biol. Chem. 2004, 279:22902-22907.
10. Tang J., Frankel A., Cook R.J., Kim S., Paik W.K., Williams K.R., Clarke S., Herschman H.R. Prmt1 is the predominant type i protein arginine methyltransferase in mammalian cells. J. Biol. Chem. 2000, 275:7723-7730.
11. Pawlak M.R., Scherer C.A., Chen J., Roshon M.J., Ruley H.E. Arginine n-methyltransferase 1 is required for early postimplantation mouse development, but cells deficient in the enzyme are viable. Mol. Cell. Biol. 2000, 20:4859-4869.
12. Boisvert F.M., Chenard C.A., Richard S. Protein interfaces in signaling regulated by arginine methylation. Sci. STKE 2005, 2005:re2.
13. Jenuwein T., Allis C.D. Translating the histone code. Science 2001, 293:1074-1080.
14. Strahl B.D., Briggs S.D., Brame C.J., Caldwell J.A., Koh S.S., Ma H., Cook R.G., Shabanowitz J., Hunt D.F., Stallcup M.R., et al. Methylation of histone h4 at arginine 3 occurs in vivo and is mediated by the nuclear receptor coactivator prmt1. Curr. Biol.: CB 2001, 11:996-1000.
15. Wang H., Huang Z.Q., Xia L., Feng Q., Erdjument-Bromage H., Strahl B.D., Briggs S.D., Allis C.D., Wong J., Tempst P., et al. Methylation of histone h4 at arginine 3 facilitating transcriptional activation by nuclear hormone receptor. Science 2001, 293:853-857.
16. Yu Z., Chen T., Hebert J., Li E., Richard S. A mouse prmt1 null allele defines an essential role for arginine methylation in genome maintenance and cell proliferation. Mol. Cell. Biol. 2009, 29(11):2982-2996.
17. Boisvert F.M., Rhie A., Richard S., Doherty A.J. The gar motif of 53bp1 is arginine methylated by prmt1 and is necessary for 53bp1 DNA binding activity. Cell Cycle 2005, 4:1834-1841.
18. Boisvert F.M., Dery U., Masson J.Y., Richard S. Arginine methylation of mre11 by prmt1 is required for DNA damage checkpoint control. Genes Dev. 2005, 19:671-676.
19. Boisvert F.M., Hendzel M.J., Masson J.Y., Richard S. Methylation of mre11 regulates its nuclear compartmentalization. Cell Cycle 2005, 4:981-989.
20. Guendel I., Carpio L., Pedati C., Schwartz A., Teal C., Kashanchi F., Kehn-Hall K. Methylation of the tumor suppressor protein, brca1, influences its transcriptional cofactor function. PloS ONE 2010, 5:e11379.
21. El-Andaloussi N., Valovka T., Toueille M., Hassa P.O., Gehrig P., Covic M., Hubscher U., Hottiger M.O. Methylation of DNA polymerase beta by protein arginine methyltransferase 1 regulates its binding to proliferating cell nuclear antigen. FASEB J. 2007, 21:26-34.
22. Adams M.M., Wang B., Xia Z., Morales J.C., Lu X., Donehower L.A., Bochar D.A., Elledge S.J., Carpenter P.B. 53bp1 oligomerization is independent of its methylation by prmt1. Cell Cycle 2005, 4:1854-1861.
23. Mirzoeva O.K., Petrini J.H. DNA damage-dependent nuclear dynamics of the mre11 complex. Mol. Cell. Biol. 2001, 21:281-288.
24. Berkovich E., Monnat R.J., Kastan M.B. Roles of atm and nbs1 in chromatin structure modulation and DNA double-strand break repair. Nat. Cell Biol. 2007, 9:683-690.
25. de Jager M., Dronkert M.L., Modesti M., Beerens C.E., Kanaar R., van Gent D.C. DNA-binding and strand-annealing activities of human mre11: implications for its roles in DNA double-strand break repair pathways. Nucleic Acids Res. 2001, 29:1317-1325.
26. Falck J., Coates J., Jackson S.P. Conserved modes of recruitment of atm, atr and DNA-pkcs to sites of DNA damage. Nature 2005, 434:605-611.
27. Lee J.H., Paull T.T. Atm activation by DNA double-strand breaks through the mre11-rad50-nbs1 complex. Science 2005, 308:551-554.
28. Buis J., Wu Y., Deng Y., Leddon J., Westfield G., Eckersdorff M., Sekiguchi J.M., Chang S., Ferguson D.O. Mre11 nuclease activity has essential roles in DNA repair and genomic stability distinct from atm activation. Cell 2008, 135:85-96.
29. Xie A., Kwok A., Scully R. Role of mammalian mre11 in classical and alternative nonhomologous end joining. Nat. Struct. Mol. Biol. 2009, 16:814-818.
30. Dinkelmann M., Spehalski E., Stoneham T., Buis J., Wu Y., Sekiguchi J.M., Ferguson D.O. Multiple functions of mrn in end-joining pathways during isotype class switching. Nat. Struct. Mol. Biol. 2009, 16:808-813.
31. Deng Y., Guo X., Ferguson D.O., Chang S. Multiple roles for mre11 at uncapped telomeres. Nature 2009, 460:914-918.
32. Mirzoeva O.K., Petrini J.H. DNA replication-dependent nuclear dynamics of the mre11 complex. Mol. Cancer Res.: MCR 2003, 1:207-218.
33. Williams R.S., Moncalian G., Williams J.S., Yamada Y., Limbo O., Shin D.S., Groocock L.M., Cahill D., Hitomi C., Guenther G., et al. Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strand-break repair. Cell 2008, 135:97-109.
34. Paull T.T., Gellert M. The 3' to 5' exonuclease activity of mre 11 facilitates repair of DNA double-strand breaks. Mol. Cell 1998, 1:969-979.
35. Hopfner K.P., Craig L., Moncalian G., Zinkel R.A., Usui T., Owen B.A., Karcher A., Henderson B., Bodmer J.L., McMurray C.T., et al. The rad50 zinc-hook is a structure joining mre11 complexes in DNA recombination and repair. Nature 2002, 418:562-566.
36. Garcia V., Phelps S.E., Gray S., Neale M.J. Bidirectional resection of DNA double-strand breaks by mre11 and exo1. Nature 2011, 479:241-244.
37. Mimitou E.P., Symington L.S. Sae2, exo1 and sgs1 collaborate in DNA double-strand break processing. Nature 2008, 455:770-774.
38. Zhu Z., Chung W.H., Shim E.Y., Lee S.E., Ira G. Sgs1 helicase and two nucleases dna2 and exo1 resect DNA double-strand break ends. Cell 2008, 134:981-994.
39. Jazayeri A., Falck J., Lukas C., Bartek J., Smith G.C., Lukas J., Jackson S.P. Atm- and cell cycle-dependent regulation of atr in response to DNA double-strand breaks. Nat. Cell Biol. 2006, 8:37-45.
40. Limbo O., Chahwan C., Yamada Y., de Bruin R.A., Wittenberg C., Russell P. Ctp1 is a cell-cycle-regulated protein that functions with mre11 complex to control double-strand break repair by homologous recombination. Mol. Cell 2007, 28:134-146.
41. Boisvert F.M., Cote J., Boulanger M.C., Richard S. A proteomic analysis of arginine-methylated protein complexes. Mol. Cell. Proteomics 2003, 2:1319-1330.
42. Dery U., Coulombe Y., Rodrigue A., Stasiak A., Richard S., Masson J.Y. A glycine-arginine domain in control of the human mre11 DNA repair protein. Mol. Cell. Biol. 2008, 28:3058-3069.
43. Yu Z., Chen T., Hebert J., Li E., Richard S. A mouse prmt1 null allele defines an essential role for arginine methylation in genome maintenance and cell proliferation. Mol. Cell. Biol. 2009, 29:2982-2996.
44. Cimprich K.A., Cortez D. Atr An essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol. 2008, 9:616-627.
45. King M.C., Marks J.H., Mandell J.B., Grp N.Y.B.C.S. Breast and ovarian cancer risks due to inherited mutations in brca1 and brca2. Science 2003, 302:643-646.
46. Narod S.A., Foulkes W.D. Brca1 and brca2: 1994 and beyond. Nat. Rev. Cancer 2004, 4:665-676.
47. Deng C.X. Brca1. Cell cycle checkpoint, genetic instability, DNA damage response and cancer evolution. Nucleic Acids Res. 2006, 34:1416-1426.
48. Durant S.T., Nickoloff J.A. Good timing in the cell cycle for precise DNA repair by brca1. Cell Cycle 2005, 4:1216-1222.
49. Hashizume R., Fukuda M., Maeda I., Nishikawa H., Oyake D., Yabuki Y., Ogata H., Ohta T. The ring heterodimer brca1-bard1 is a ubiquitin ligase inactivated by a breast cancer-derived mutation. J. Biol. Chem. 2001, 276:14537-14540.
50. Yu X., Fu S., Lai M., Baer R., Chen J. Brca1 ubiquitinates its phosphorylation-dependent binding partner ctip. Genes Dev. 2006, 20:1721-1726.
51. Zhu Q., Pao G.M., Huynh A.M., Suh H., Tonnu N., Nederlof P.M., Gage F.H., Verma I.M. Brca1 tumour suppression occurs via heterochromatin-mediated silencing. Nature 2011, 477:179-184.
52. Yarden R.I., Brody L.C. Brca1 interacts with components of the histone deacetylase complex. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:4983-4988.
53. Chai Y.L., Cui J., Shao N., Shyam E., Reddy P., Rao V.N. The second brct domain of brca1 proteins interacts with p53 and stimulates transcription from the p21waf1/cip1 promoter. Oncogene 1999, 18:263-268.
54. Bochar D.A., Wang L., Beniya H., Kinev A., Xue Y., Lane W.S., Wang W., Kashanchi F., Shiekhattar R. Brca1 is associated with a human swi/snf-related complex: linking chromatin remodeling to breast cancer. Cell 2000, 102:257-265.
55. Cortez D., Wang Y., Qin J., Elledge S.J. Requirement of atm-dependent phosphorylation of brca1 in the DNA damage response to double-strand breaks. Science 1999, 286:1162-1166.
56. Okada S., Ouchi T. Cell cycle differences in DNA damage-induced brca1 phosphorylation affect its subcellular localization. J. Biol. Chem. 2003, 278:2015-2020.
57. Rappold I., Iwabuchi K., Date T., Chen J. Tumor suppressor p53 binding protein 1 (53bp1) is involved in DNA damage-signaling pathways. J. Cell Biol. 2001, 153:613-620.
58. Fernandez-Capetillo O., Chen H.T., Celeste A., Ward I., Romanienko P.J., Morales J.C., Naka K., Xia Z., Camerini-Otero R.D., Motoyama N., et al. DNA damage-induced g2-m checkpoint activation by histone h2ax and 53bp1. Nat. Cell Biol. 2002, 4:993-997.
59. Chapman J.R., Sossick A.J., Boulton S.J., Jackson S.P. Brca1-associated exclusion of 53bp1 from DNA damage sites underlies temporal control of DNA repair. J. Cell Sci. 2012, 125:3529-3534.
60. Chapman J.R., Taylor M.R., Boulton S.J. Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell 2012, 47:497-510.
61. Bunting S.F., Callen E., Wong N., Chen H.T., Polato F., Gunn A., Bothmer A., Feldhahn N., Fernandez-Capetillo O., Cao L., et al. 53bp1 inhibits homologous recombination in brca1-deficient cells by blocking resection of DNA breaks. Cell 2010, 141:243-254.
62. Bouwman P., Aly A., Escandell J.M., Pieterse M., Bartkova J., van der Gulden H., Hiddingh S., Thanasoula M., Kulkarni A., Yang Q., et al. 53bp1 loss rescues brca1 deficiency and is associated with triple-negative and brca-mutated breast cancers. Nat. Struct. Mol. Biol. 2010, 17:688-695.
63. Ward I.M., Minn K., van Deursen J., Chen J. P53 binding protein 53bp1 is required for DNA damage responses and tumor suppression in mice. Mol. Cell. Biol. 2003, 23:2556-2563.
64. Botuyan M.V., Lee J., Ward I.M., Kim J.E., Thompson J.R., Chen J., Mer G. Structural basis for the methylation state-specific recognition of histone h4-k20 by 53bp1 and crb2 in DNA repair. Cell 2006, 127:1361-1373.
65. Beard W.A., Wilson S.H. Structure and mechanism of DNA polymerase beta. Chem. Rev. 2006, 106:361-382.
66. Stivers J.T., Jiang Y.L. A mechanistic perspective on the chemistry of DNA repair glycosylases. Chem. Rev. 2003, 103:2729-2759.
67. Podlutsky A.J., Dianova I.I., Podust V.N., Bohr V.A., Dianov G.L. Human DNA polymerase beta initiates DNA synthesis during long-patch repair of reduced ap sites in DNA. EMBO J. 2001, 20:1477-1482.
68. Tokui T., Inagaki M., Nishizawa K., Yatani R., Kusagawa M., Ajiro K., Nishimoto Y., Date T., Matsukage A. Inactivation of DNA polymerase beta by in vitro phosphorylation with protein kinase c. J. Biol. Chem. 1991, 266:10820-10824.
69. Hasan S., El-Andaloussi N., Hardeland U., Hassa P.O., Burki C., Imhof R., Schar P., Hottiger M.O. Acetylation regulates the DNA end-trimming activity of DNA polymerase beta. Mol. Cell 2002, 10:1213-1222.
70. El-Andaloussi N., Valovka T., Toueille M., Steinacher R., Focke F., Gehrig P., Covic M., Hassa P.O., Schar P., Hubscher U., et al. Arginine methylation regulates DNA polymerase beta. Mol. Cell 2006, 22:51-62.
71. Guo Z., Zheng L., Dai H., Zhou M., Xu H., Shen B. Human DNA polymerase beta polymorphism, arg137gln, impairs its polymerase activity and interaction with pcna and the cellular base excision repair capacity. Nucleic Acids Res. 2009, 37:3431-3441.
72. Pollack B.P., Kotenko S.V., He W., Izotova L.S., Barnoski B.L., Pestka S. The human homologue of the yeast proteins skb1 and hsl7p interacts with jak kinases and contains protein methyltransferase activity. J. Biol. Chem. 1999, 274:31531-31542.
73. Wang L., Pal S., Sif S. Protein arginine methyltransferase 5 suppresses the transcription of the rb family of tumor suppressors in leukemia and lymphoma cells. Mol. Cell. Biol. 2008, 28:6262-6277.
74. Tee W.W., Pardo M., Theunissen T.W., Yu L., Choudhary J.S., Hajkova P., Surani M.A. Prmt5 is essential for early mouse development and acts in the cytoplasm to maintaines cell pluripotency. Genes Dev. 2010, 24:2772-2777.
75. Lacroix M., El Messaoudi S., Rodier G., Le Cam A., Sardet C., Fabbrizio E. The histone-binding protein copr5 is required for nuclear functions of the protein arginine methyltransferase prmt5. EMBO Rep. 2008, 9:452-458.
76. Pal S., Vishwanath S.N., Erdjument-Bromage H., Tempst P., Sif S. Human swi/snf-associated prmt5 methylates histone h3 arginine 8 and negatively regulates expression of st7 and nm23 tumor suppressor genes. Mol. Cell. Biol. 2004, 24:9630-9645.
77. Sanchez S.E., Petrillo E., Beckwith E.J., Zhang X., Rugnone M.L., Hernando C.E., Cuevas J.C., Godoy Herz M.A., Depetris-Chauvin A., Simpson C.G., et al. A methyl transferase links the circadian clock to the regulation of alternative splicing. Nature 2010, 468:112-116.
78. Azzouz T.N., Pillai R.S., Dapp C., Chari A., Meister G., Kambach C., Fischer U., Schumperli D. Toward an assembly line for u7 snrnps: interactions of u7-specific lsm proteins with prmt5 and smn complexes. J. Biol. Chem. 2005, 280:34435-34440.
79. Cho E.C., Zheng S., Munro S., Liu G., Carr S.M., Moehlenbrink J., Lu Y.C., Stimson L., Khan O., Konietzny R., et al. Arginine methylation controls growth regulation by e2f-1. EMBO J. 2012, 31:1785-1797.
80. Jansson M., Durant S.T., Cho E.C., Sheahan S., Edelmann M., Kessler B., La Thangue N.B. Arginine methylation regulates the p53 response. Nat. Cell Biol. 2008, 10:1431-1439.
81. Guo Z., Zheng L., Xu H., Dai H., Zhou M., Pascua M.R., Chen Q.M., Shen B. Methylation of fen1 suppresses nearby phosphorylation and facilitates pcna binding. Nat. Chem. Biol. 2010, 6:766-773.
82. He W., Ma X., Yang X., Zhao Y., Qiu J., Hang H. A role for the arginine methylation of rad9 in checkpoint control and cellular sensitivity to DNA damage. Nucleic Acids Res. 2011, 39:4719-4727.
83. Friesen W.J., Paushkin S., Wyce A., Massenet S., Pesiridis G.S., Van Duyne G., Rappsilber J., Mann M., Dreyfuss G. The methylosome, a 20s complex containing jbp1 and picln, produces dimethylarginine-modified sm proteins. Mol. Cell. Biol. 2001, 21:8289-8300.
84. Reinhardt H.C., Schumacher B. The p53 network: cellular and systemic DNA damage responses in aging and cancer. Trends Genet.: TIG 2012, 28:128-136.
85. Momand J., Zambetti G.P., Olson D.C., George D., Levine A.J. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 1992, 69:1237-1245.
86. Sakaguchi K., Herrera J.E., Saito S., Miki T., Bustin M., Vassilev A., Anderson C.W., Appella E. DNA damage activates p53 through a phosphorylation-acetylation cascade. Genes Dev. 1998, 12:2831-2841.
87. Shieh S.Y., Ahn J., Tamai K., Taya Y., Prives C. The human homologs of checkpoint kinases chk1 and cds1 (chk2) phosphorylate p53 at multiple DNA damage-inducible sites. Genes Dev. 2000, 14:289-300.
88. Khanna K.K., Keating K.E., Kozlov S., Scott S., Gatei M., Hobson K., Taya Y., Gabrielli B., Chan D., Lees-Miller S.P., et al. Atm associates with and phosphorylates p53: mapping the region of interaction. Nat. Genet. 1998, 20:398-400.
89. Serrano M.A., Li Z., Dangeti M., Musich P.R., Patrick S., Roginskaya M., Cartwright B., Zou Y. DNA-pk, atm and atr collaboratively regulate p53-rpa interaction to facilitate homologous recombination DNA repair. Oncogene 2012.
90. Demonacos C., Krstic-Demonacos M., La Thangue N.B. A tpr motif cofactor contributes to p300 activity in the p53 response. Mol. Cell 2001, 8:71-84.
91. Demonacos C., Krstic-Demonacos M., Smith L., Xu D., O'Connor D.P., Jansson M., La Thangue N.B. A new effector pathway links atm kinase with the DNA damage response. Nat. Cell Biol. 2004, 6:968-976.
92. Lieber M.R. The fen-1 family of structure-specific nucleases in eukaryotic DNA replication, recombination and repair. Bioessays 1997, 19:233-240.
93. Tomlinson C.G., Atack J.M., Chapados B., Tainer J.A., Grasby J.A. Substrate recognition and catalysis by flap endonucleases and related enzymes. Biochem. Soc. Trans. 2010, 38:433-437.
94. Singh P., Zheng L., Chavez V., Qiu J., Shen B. Concerted action of exonuclease and gap-dependent endonuclease activities of fen-1 contributes to the resolution of triplet repeat sequences (ctg)n- and (gaa)n-derived secondary structures formed during maturation of okazaki fragments. J. Biol. Chem. 2007, 282:3465-3477.
95. Zheng L., Zhou M., Chai Q., Parrish J., Xue D., Patrick S.M., Turchi J.J., Yannone S.M., Chen D., Shen B. Novel function of the flap endonuclease 1 complex in processing stalled DNA replication forks. EMBO Rep. 2005, 6:83-89.
96. Hasan S., Stucki M., Hassa P.O., Imhof R., Gehrig P., Hunziker P., Hubscher U., Hottiger M.O. Regulation of human flap endonuclease-1 activity by acetylation through the transcriptional coactivator p300. Mol. Cell 2001, 7:1221-1231.
97. Guo Z., Kanjanapangka J., Liu N., Liu S., Liu C., Wu Z., Wang Y., Loh T., Kowolik C., Jamsen J., et al. Sequential posttranslational modifications program fen1 degradation during cell-cycle progression. Mol. Cell 2012, 47:444-456.
98. Qiu J., Li X., Frank G., Shen B. Cell cycle-dependent and DNA damage-inducible nuclear localization of fen-1 nuclease is consistent with its dual functions in DNA replication and repair. J. Biol. Chem. 2001, 276:4901-4908.
99. Shibata Y., Nakamura T. Defective flap endonuclease 1 activity in mammalian cells is associated with impaired DNA repair and prolonged s phase delay. J. Biol. Chem. 2002, 277:746-754.
100. Henneke G., Koundrioukoff S., Hubscher U. Phosphorylation of human fen1 by cyclin-dependent kinase modulates its role in replication fork regulation. Oncogene 2003, 22:4301-4313.
101. Delacroix S., Wagner J.M., Kobayashi M., Yamamoto K., Karnitz L.M. The rad9-hus1-rad1 (9-1-1) clamp activates checkpoint signaling via topbp1. Genes Dev. 2007, 21:1472-1477.
102. Furuya K., Poitelea M., Guo L., Caspari T., Carr A.M. Chk1 activation requires rad9 s/tq-site phosphorylation to promote association with c-terminal brct domains of rad4topbp1. Genes Dev. 2004, 18:1154-1164.
103. Balakrishnan L., Brandt P.D., Lindsey-Boltz L.A., Sancar A., Bambara R.A. Long patch base excision repair proceeds via coordinated stimulation of the multienzyme DNA repair complex. J. Biol. Chem. 2009, 284:15158-15172.
104. Guan X., Madabushi A., Chang D.Y., Fitzgerald M.E., Shi G., Drohat A.C., Lu A.L. The human checkpoint sensor rad9-rad1-hus1 interacts with and stimulates DNA repair enzyme tdg glycosylase. Nucleic Acids Res. 2007, 35:6207-6218.
105. St Onge R.P., Besley B.D., Pelley J.L., Davey S. A role for the phosphorylation of hrad9 in checkpoint signaling. J. Biol. Chem. 2003, 278:26620-26628.
106. Yoshida K., Komatsu K., Wang H.G., Kufe D. C-abl tyrosine kinase regulates the human rad9 checkpoint protein in response to DNA damage. Mol. Cell. Biol. 2002, 22:3292-3300.
107. Yoshida K., Wang H.G., Miki Y., Kufe D. Protein kinase cdelta is responsible for constitutive and DNA damage-induced phosphorylation of rad9. EMBO J. 2003, 22:1431-1441.
108. Zurita-Lopez C.I., Sandberg T., Kelly R., Clarke S.G. Human protein arginine methyltransferase 7 (prmt7) is a type iii enzyme forming omega-ng-monomethylated arginine residues. J. Biol. Chem. 2012, 287:7859-7870.
109. Lee J.H., Cook J.R., Yang Z.H., Mirochnitchenko O., Gunderson S.I., Felix A.M., Herth N., Hoffmann R., Pestka S. Prmt7, a new protein arginine methyltransferase that synthesizes symmetric dimethylarginine. J. Biol. Chem. 2005, 280:3656-3664.
110. Gonsalvez G.B., Tian L., Ospina J.K., Boisvert F.M., Lamond A.I., Matera A.G. Two distinct arginine methyltransferases are required for biogenesis of sm-class ribonucleoproteins. J. Cell Biol. 2007, 178:733-740.
111. Jelinic P., Stehle J.C., Shaw P. The testis-specific factor ctcfl cooperates with the protein methyltransferase prmt7 in h19 imprinting control region methylation. PLoS Biol. 2006, 4:e355.
112. Dhar S.S., Lee S.H., Kan P.Y., Voigt P., Ma L., Shi X., Reinberg D., Lee M.G. Trans-tail regulation of mll4-catalyzed h3k4 methylation by h4r3 symmetric dimethylation is mediated by a tandem phd of mll4. Genes Dev. 2012, 26:2749-2762.
113. Migliori V., Muller J., Phalke S., Low D., Bezzi M., Mok W.C., Sahu S.K., Gunaratne J., Capasso P., Bassi C., et al. Symmetric dimethylation of h3r2 is a newly identified histone mark that supports euchromatin maintenance. Nat. Struct. Mol. Biol. 2012, 19:136-144.
114. Karkhanis V., Wang L., Tae S., Hu Y.J., Imbalzano A.N., Sif S. Protein arginine methyltransferase 7 regulates cellular response to DNA damage by methylating promoter histones h2a and h4 of the polymerase delta catalytic subunit gene, pold1. J. Biol. Chem. 2012, 287:29801-29814.
115. Gros L., Delaporte C., Frey S., Decesse J., de Saint-Vincent B.R., Cavarec L., Dubart A., Gudkov A.V., Jacquemin-Sablon A. Identification of new drug sensitivity genes using genetic suppressor elements: protein arginine n-methyltransferase mediates cell sensitivity to DNA-damaging agents. Cancer Res. 2003, 63:164-171.
116. Hornbeck, Kornhauser P.V., Tkachev J.M., Zhang S., Skrzypek B., Murray E., Latham B., Sullivan V., Phosphositeplus M. A comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res. 2012, 40:D261-D270.
117. Verbiest V., Montaudon D., Tautu M.T., Moukarzel J., Portail J.P., Markovits J., Robert J., Ichas F., Pourquier P. Protein arginine (n)-methyl transferase 7 (prmt7) as a potential target for the sensitization of tumor cells to camptothecins. FEBS Lett. 2008, 582:1483-1489.
118. Bleibel W.K., Duan S., Huang R.S., Kistner E.O., Shukla S.J., Wu X., Badner J.A., Dolan M.E. Identification of genomic regions contributing to etoposide-induced cytotoxicity. Hum. Genet. 2009, 125:173-180.