SIRT2 directs the replication stress response through CDK9 deacetylation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 33, 2013, Pages 13546-13551

  Zhang, Hui ^a   Park, Seong Hoon ^b   Pantazides, Brooke G ^a   Karpiuk, Oleksandra ^c   Warren, Matthew D ^a   Hardy, Claire W ^a   Duong, Duc M ^a   Park, So Jeong ^d   Kim, Hyun Seok ^d   Vassilopoulos, Athanassios ^b   Seyfried, Nicholas T ^a   Johnsen, Steven A ^c   Gius, David ^b   Yu, David S ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d Ewha Womans University   (South Korea)

Author keywords

Cell cycle checkpoint; DNA damage; Genome maintenance

Indexed keywords

ALPHA TUBULIN; CHECKPOINT KINASE RAD3; CYCLIN DEPENDENT KINASE 9; CYCLIN K; CYCLIN T; CYCLINE; SIRTUIN 2; UNCLASSIFIED DRUG;

ARTICLE; ATAXIA TELANGIECTASIA; CATALYSIS; CELL CYCLE S PHASE; DEACETYLATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; STRESS; WESTERN BLOTTING;

CELL CYCLE CHECKPOINT; DNA DAMAGE; GENOME MAINTENANCE;

ACETYLATION; ANIMALS; BLOTTING, WESTERN; CELL CYCLE CHECKPOINTS; CELL LINE; CHROMATOGRAPHY, LIQUID; COLONY-FORMING UNITS ASSAY; CYCLIN-DEPENDENT KINASE 9; DNA REPLICATION; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MICE; REPLICATION PROTEIN A; SIRTUIN 2; TANDEM MASS SPECTROMETRY;

EID: 84882418252     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1301463110     Document Type: Article

References (46)

1. Guarente L (2011) Franklin H. Epstein Lecture: Sirtuins, aging, and medicine. N Engl J Med 364(23):2235-2244.
2. Finkel T, Deng CX, Mostoslavsky R (2009) Recent progress in the biology and physiology of sirtuins. Nature 460(7255):587-591.
3. Saunders LR, Verdin E (2007) Sirtuins: Critical regulators at the crossroads between cancer and aging. Oncogene 26(37):5489-5504.
4. Fan W, Luo J (2010) SIRT1 regulates UV-induced DNA repair through deacetylating XPA. Mol Cell 39(2):247-258.
5. Jeong J, et al. (2007) SIRT1 promotes DNA repair activity and deacetylation of Ku70. Exp Mol Med 39(1):8-13.
6. Kaidi A, Weinert BT, Choudhary C, Jackson SP (2010) Human SIRT6 promotes DNA end resection through CtIP deacetylation. Science 329(5997):1348-1353.
7. Li K, et al. (2008) Regulation of WRN protein cellular localization and enzymatic activities by SIRT1-mediated deacetylation. J Biol Chem 283(12):7590-7598.
8. Mao Z, et al. (2011) SIRT6 promotes DNA repair under stress by activating PARP1. Science 332(6036):1443-1446.
9. McCord RA, et al. (2009) SIRT6 stabilizes DNA-dependent protein kinase at chromatin for DNA double-strand break repair. Aging (Albany, NY Online) 1(1):109-121.
10. Wang J, Chen J (2010) SIRT1 regulates autoacetylation and histone acetyltransferase activity of TIP60. J Biol Chem 285(15):11458-11464.
11. Yamagata K, Kitabayashi I (2009) Sirt1 physically interacts with Tip60 and negatively regulates Tip60-mediated acetylation of H2AX. Biochem Biophys Res Commun 390(4): 1355-1360.
12. Yuan Z, Seto E (2007) A functional link between SIRT1 deacetylase and NBS1 in DNA damage response. Cell Cycle 6(23):2869-2871.
13. Serrano L, et al. (2013) The tumor suppressor SirT2 regulates cell cycle progression and genome stability by modulating the mitotic deposition of H4K20 methylation. Genes Dev 27(6):639-653.
14. Kim HS, et al. (2011) SIRT2 maintains genome integrity and suppresses tumorigenesis through regulating APC/C activity. Cancer Cell 20(4):487-499.
15. Matsushita N, et al. (2005) Role of NAD-dependent deacetylases SIRT1 and SIRT2 in radiation and cisplatin-induced cell death in vertebrate cells. Genes Cells 10(4): 321-332.
16. Das C, Lucia MS, Hansen KC, Tyler JK (2009) CBP/p300-mediated acetylation of histone H3 on lysine. Nature 459(7243):113-117.
17. Bartkova J, et al. (2005) DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434(7035):864-870.
18. Gorgoulis VG, et al. (2005) Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434(7035):907-913.
19. Cimprich KA, Cortez D (2008) ATR: An essential regulator of genome integrity. Nat Rev Mol Cell Biol 9(8):616-627.
20. Brown EJ, Baltimore D (2000) ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev 14(4):397-402.
21. Cortez D, Guntuku S, Qin J, Elledge SJ (2001) ATR and ATRIP: Partners in checkpoint signaling. Science 294(5547):1713-1716.
22. Casper AM, Nghiem P, Arlt MF, Glover TW (2002) ATR regulates fragile site stability. Cell 111(6):779-789.
23. Byun TS, Pacek M, Yee MC, Walter JC, Cimprich KA (2005) Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev 19(9):1040-1052.
24. Brès V, Yoh SM, Jones KA (2008) The multi-tasking P-TEFb complex. Curr Opin Cell Biol 20(3):334-340.
25. Romano G, Giordano A (2008) Role of the cyclin-dependent kinase 9-related pathway in mammalian gene expression and human diseases. Cell Cycle 7(23):3664-3668.
26. Clausing E, et al. (2010) The transcription elongation factor Bur1-Bur2 interacts with replication protein A and maintains genome stability during replication stress. J Biol Chem 285(53):41665-41674.
27. Liu H, Herrmann CH (2005) Differential localization and expression of the Cdk9 42k and 55k isoforms. J Cell Physiol 203(1):251-260.
28. Yu DS, Cortez D (2011) A role for CDK9-cyclin K in maintaining genome integrity. Cell Cycle 10(1):28-32.
29. Yu DS, et al. (2010) Cyclin-dependent kinase 9-cyclin K functions in the replication stress response. EMBO Rep 11(11):876-882.
30. Morawska ME (2012) A role for CDK9 in UV damage response. Cell Cycle 11(12): 2229-2230.
31. Shchebet A, Karpiuk O, Kremmer E, Eick D, Johnsen SA (2012) Phosphorylation by cyclin-dependent kinase-9 controls ubiquitin-conjugating enzyme-2A function. Cell Cycle 11(11):2122-2127.
32. Zhang H, Yu DS (2012) One stone, two birds: CDK9-directed activation of UBE2A regulates monoubiquitination of both H2B and PCNA. Cell Cycle 11(13):2418.
33. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419(6903):135-141.
34. Pirngruber J, et al. (2009) CDK9 directs H2B monoubiquitination and controls replication-dependent histone mRNA 3?-end processing. EMBO Rep 10(8):894-900.
35. Blazek D, et al. (2011) The Cyclin K/Cdk12 complex maintains genomic stability via regulation of expression of DNA damage response genes. Genes Dev 25(20):2158-2172.
36. Dai Q, et al. (2012) Cyclin K-containing kinase complexes maintain self-renewal in murine embryonic stem cells. J Biol Chem 287(30):25344-25352.
37. Cheng SW, et al. (2012) Interaction of cyclin-dependent kinase 12/CrkRS with cyclin K1 is required for the phosphorylation of the C-terminal domain of RNA polymerase II. Mol Cell Biol 32(22):4691-4704.
38. Cho S, Schroeder S, Ott M (2010) CYCLINg through transcription: posttranslational modifications of P-TEFb regulate transcription elongation. Cell Cycle 9(9):1697-1705.
39. Fu J, Yoon HG, Qin J, Wong J (2007) Regulation of P-TEFb elongation complex activity by CDK9 acetylation. Mol Cell Biol 27(13):4641-4651.
40. Sabò A, Lusic M, Cereseto A, Giacca M (2008) Acetylation of conserved lysines in the catalytic core of cyclin-dependent kinase 9 inhibits kinase activity and regulates transcription. Mol Cell Biol 28(7):2201-2212.
41. North BJ, Marshall BL, Borra MT, Denu JM, Verdin E (2003) The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Mol Cell 11(2):437-444.
42. Yuan Z, Zhang X, Sengupta N, Lane WS, Seto E (2007) SIRT1 regulates the function of the Nijmegen breakage syndrome protein. Mol Cell 27(1):149-162.
43. Baumli S, et al. (2008) The structure of P-TEFb (CDK9/cyclin T1), its complex with flavopiridol and regulation by phosphorylation. EMBO J 27(13):1907-1918.
44. De Bondt HL, et al. (1993) Crystal structure of cyclin-dependent kinase. Nature 363(6430):595-602.
45. Hanks SK, Hunter T (1995) Protein kinases The eukaryotic protein kinase superfamily: Kinase (catalytic) domain structure and classification. FASEB J 9(8):576-596.
46. Eyers CE, et al. (2011) CONSeQuence: Prediction of reference peptides for absolute quantitative proteomics using consensus machine learning approaches. Mol Cell Proteomics 10(11):M110 003384.