Proteolysis of the human DNA polymerase delta smallest subunit p12 by μ-calpain in calcium-triggered apoptotic hela cells

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Fan, Xiaoting ^a   Zhang, Qian ^a   You, Chao ^a   Qian, Yuanxia ^a   Gao, Jing ^a   Liu, Peng ^a   Chen, Huiqing ^a   Song, Huifang ^a   Chen, Yan ^a   Chen, Keping ^a   Zhou, Yajing ^a  

^a JIANGSU UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CALCIUM ION; CALPAIN 1; CASPASE 3; CYCLINE; DNA DIRECTED DNA POLYMERASE DELTA; DNA DIRECTED DNA POLYMERASE DELTA 3; DNA DIRECTED DNA POLYMERASE DELTA 4; DNA DIRECTED DNA POLYMERASE DELTA P12 SUBUNIT; DNA DIRECTED DNA POLYMERASE DELTA P125 SUBUNIT; DNA DIRECTED DNA POLYMERASE DELTA P50 SUBUNIT; DNA DIRECTED DNA POLYMERASE DELTA P68 SUBUNIT; PHOSPHATIDYLSERINE; UNCLASSIFIED DRUG; CALCIUM; CALPAIN; DNA DIRECTED DNA POLYMERASE GAMMA; DNA POLYMERASE DELTA P12 SUBUNIT, HUMAN; MU-CALPAIN;

APOPTOSIS; ARTICLE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INDUCTION; ENZYME SUBSTRATE COMPLEX; HELA CELL; HUMAN; IMMUNOPRECIPITATION; IN VITRO STUDY; MOLECULAR DYNAMICS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN LOCALIZATION; REACTION TIME; DNA DAMAGE; DNA REPLICATION; DRUG EFFECTS; GENETICS; HELA CELL LINE; METABOLISM; NEOPLASMS;

APOPTOSIS; CALCIUM; CALPAIN; DNA DAMAGE; DNA POLYMERASE III; DNA REPLICATION; HELA CELLS; HUMANS; NEOPLASMS; PROTEOLYSIS;

EID: 84898605402     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093642     Document Type: Article

References (55)

1. Zhang Z, Zhang S, Lin SH, Wang X, Wu L, et al. (2012) Structure of monoubiquitinated PCNA: implications for DNA polymerase switching and Okazaki fragment maturation. Cell Cycle 11: 2128-2136.
2. Zhou Y, Chen H, Li X, Wang Y, Chen K, et al. (2011) Production of recombinant human DNA polymerase delta in a Bombyx mori bioreactor. PLoS One 6: e22224.
3. Rahmeh AA, Zhou Y, Xie B, Li H, Lee EY, et al. (2012) Phosphorylation of the p68 subunit of Pol delta acts as a molecular switch to regulate its interaction with PCNA. Biochemistry 51: 416-424.
4. Meng X, Zhou Y, Lee EY, Lee MY, Frick DN (2010) The p12 subunit of human polymerase delta modulates the rate and fidelity of DNA synthesis. Biochemistry 49: 3545-3554.
5. Branzei D, Foiani M (2008) Regulation of DNA repair throughout the cell cycle. Nat Rev Mol Cell Biol 9: 297-308. (Pubitemid 351430844)
6. Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S (2004) Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73: 39-85. (Pubitemid 39050363)
7. Zhang S, Zhou Y, Trusa S, Meng X, Lee EY, et al. (2007) A novel DNA damage response: rapid degradation of the p12 subunit of dna polymerase delta. J Biol Chem 282: 15330-15340. (Pubitemid 47093258)
8. Meng X, Zhou Y, Zhang S, Lee EY, Frick DN, et al. (2009) DNA damage alters DNA polymerase delta to a form that exhibits increased discrimination against modified template bases and mismatched primers. Nucleic Acids Res 37: 647-657.
9. Chea J, Zhang S, Zhao H, Zhang Z, Lee EY, et al. (2012) Spatiotemporal recruitment of human DNA polymerase delta to sites of UV damage. Cell Cycle 11: 2885-2895.
10. Garg P, Burgers PM (2005) DNA polymerases that propagate the eukaryotic DNA replication fork. Crit Rev Biochem Mol Biol 40: 115-128. (Pubitemid 40604979)
11. Andersen PL, Xu F, Ziola B, McGregor WG, Xiao W (2011) Sequential assembly of translesion DNA polymerases at UV-induced DNA damage sites. Mol Biol Cell 22: 2373-2383.
12. Zhang W, Qin Z, Zhang X, Xiao W (2011) Roles of sequential ubiquitination of PCNA in DNA-damage tolerance. FEBS Lett 585: 2786-2794.
13. Sale JE, Lehmann AR, Woodgate R (2012) Y-family DNA polymerases and their role in tolerance of cellular DNA damage. Nat Rev Mol Cell Biol 13: 141-152.
14. Zhang S, Zhou Y, Sarkeshik A, Yates JR, 3rd, Thomson TM, et al. (2013) Identification of RNF8 as a ubiquitin ligase involved in targeting the p12 subunit of DNA polymerase delta for degradation in response to DNA damage. J Biol Chem 288: 2941-2950.
15. Zhang S, Zhao H, Darzynkiewicz Z, Zhou P, Zhang Z, et al. (2013) A novel function of CRL4(Cdt2): regulation of the subunit structure of DNA polymerase delta in response to DNA damage and during the S phase. J Biol Chem 288: 29550-29561.
16. Zhou Y, Meng X, Zhang S, Lee EY, Lee MY (2012) Characterization of human DNA polymerase delta and its subassemblies reconstituted by expression in the MultiBac system. PLoS One 7: e39156.
17. Nakagawa T, Yuan J (2000) Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J Cell Biol 150: 887-894.
18. Kusakawa G, Saito T, Onuki R, Ishiguro K, Kishimoto T, et al. (2000) Calpaindependent proteolytic cleavage of the p35 cyclin-dependent kinase 5 activator to p25. J Biol Chem 275: 17166-17172. (Pubitemid 30398964)
19. Kim MJ, Jo DG, Hong GS, Kim BJ, Lai M, et al. (2002) Calpain-dependent cleavage of cain/cabin1 activates calcineurin to mediate calcium-triggered cell death. Proc Natl Acad Sci U S A 99: 9870-9875. (Pubitemid 34831139)
20. Michetti M, Salamino F, Tedesco I, Averna M, Minafra R, et al. (1996) Autolysis of human erythrocyte calpain produces two active enzyme forms with different cell localization. FEBS Lett 392: 11-15. (Pubitemid 26268322)
21. Prelich G, Tan CK, Kostura M, Mathews MB, So AG, et al. (1987) Functional identity of proliferating cell nuclear antigen and a DNA polymerase-delta auxiliary protein. Nature 326: 517-520. (Pubitemid 17055499)
22. Nicholson DW, Thornberry NA (1997) Caspases: killer proteases. Trends Biochem Sci 22: 299-306. (Pubitemid 27327087)
23. Cohen GM (1997) Caspases: the executioners of apoptosis. Biochem J 326 (Pt 1): 1-16. (Pubitemid 27386911)
24. Kaufmann SH, Desnoyers S, Ottaviano Y, Davidson NE, Poirier GG (1993) Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res 53: 3976-3985. (Pubitemid 23267698)
25. An B, Dou QP (1996) Cleavage of retinoblastoma protein during apoptosis: an interleukin 1 beta-converting enzyme-like protease as candidate. Cancer Res 56: 438-442.
26. Lazebnik YA, Takahashi A, Moir RD, Goldman RD, Poirier GG, et al. (1995) Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc Natl Acad Sci U S A 92: 9042-9046.
27. Kothakota S, Azuma T, Reinhard C, Klippel A, Tang J, et al. (1997) Caspase-3-generated fragment of gelsolin: effector of morphological change in apoptosis. Science 278: 294-298. (Pubitemid 27450877)
28. Liu X, Zou H, Slaughter C, Wang X (1997) DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89: 175-184. (Pubitemid 27199890)
29. Liu X, Li P, Widlak P, Zou H, Luo X, et al. (1998) The 40-kDa subunit of DNA fragmentation factor induces DNA fragmentation and chromatin condensation during apoptosis. Proc Natl Acad Sci U S A 95: 8461-8466. (Pubitemid 28350510)
30. Johnson DE (2000) Noncaspase proteases in apoptosis. Leukemia 14: 1695-1703.
31. Goll DE, Thompson VF, Li H, Wei W, Cong J (2003) The calpain system. Physiol Rev 83: 731-801. (Pubitemid 36828925)
32. Friedrich P, Bozoky Z (2005) Digestive versus regulatory proteases: on calpain action in vivo. Biol Chem 386: 609-612. (Pubitemid 41448163)
33. Liu W, Linn S (2000) Proteolysis of the human DNA polymerase epsilon catalytic subunit by caspase-3 and calpain specifically during apoptosis. Nucleic Acids Res 28: 4180-4188.
34. Cuerrier D, Moldoveanu T, Davies PL (2005) Determination of peptide substrate specificity for mu-calpain by a peptide library-based approach: the importance of primed side interactions. J Biol Chem 280: 40632-40641. (Pubitemid 41780554)
35. Tompa P, Buzder-Lantos P, Tantos A, Farkas A, Szilagyi A, et al. (2004) On the sequential determinants of calpain cleavage. J Biol Chem 279: 20775-20785. (Pubitemid 38656474)
36. Banik NL, Chou CH, Deibler GE, Krutzch HC, Hogan EL (1994) Peptide bond specificity of calpain: proteolysis of human myelin basic protein. J Neurosci Res 37: 489-496. (Pubitemid 24105155)
37. DuVerle DA, Ono Y, Sorimachi H, Mamitsuka H (2011) Calpain cleavage prediction using multiple kernel learning. PLoS One 6: e19035.
38. Harwood SM, Yaqoob MM, Allen DA (2005) Caspase and calpain function in cell death: bridging the gap between apoptosis and necrosis. Ann Clin Biochem 42: 415-431. (Pubitemid 41640512)
39. Glading A, Chang P, Lauffenburger DA, Wells A (2000) Epidermal growth factor receptor activation of calpain is required for fibroblast motility and occurs via an ERK/MAP kinase signaling pathway. J Biol Chem 275: 2390-2398. (Pubitemid 30081997)
40. Glading A, Uberall F, Keyse SM, Lauffenburger DA, Wells A (2001) Membrane proximal ERK signaling is required for M-calpain activation downstream of epidermal growth factor receptor signaling. J Biol Chem 276: 23341-23348.
41. Glading A, Bodnar RJ, Reynolds IJ, Shiraha H, Satish L, et al. (2004) Epidermal growth factor activates m-calpain (calpain II), at least in part, by extracellular signal-regulated kinase-mediated phosphorylation. Mol Cell Biol 24: 2499-2512. (Pubitemid 38326004)
42. Momeni HR (2011) Role of calpain in apoptosis. Cell J 13: 65-72.
43. 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: 135-141. (Pubitemid 35025438)
44. Kannouche P, Lehmann A (2006) Localization of Y-family polymerases and the DNA polymerase switch in mammalian cells. Methods Enzymol 408: 407-415.
45. Kidd VJ, Lahti JM, Teitz T (2000) Proteolytic regulation of apoptosis. Semin Cell Dev Biol 11: 191-201. (Pubitemid 32095012)
46. Mani SK, Balasubramanian S, Zavadzkas JA, Jeffords LB, Rivers WT, et al. (2009) Calpain inhibition preserves myocardial structure and function following myocardial infarction. Am J Physiol Heart Circ Physiol 297: H1744-1751.
47. Camins A, Verdaguer E, Folch J, Pallas M (2006) Involvement of calpain activation in neurodegenerative processes. CNS Drug Rev 12: 135-148. (Pubitemid 44300381)
48. Lakshmikuttyamma A, Selvakumar P, Kanthan R, Kanthan SC, Sharma RK (2004) Overexpression of m-calpain in human colorectal adenocarcinomas. Cancer Epidemiol Biomarkers Prev 13: 1604-1609. (Pubitemid 39331881)
49. Roos WP, Kaina B (2006) DNA damage-induced cell death by apoptosis. Trends Mol Med 12: 440-450. (Pubitemid 44291571)
50. Kaina B (2003) DNA damage-triggered apoptosis: critical role of DNA repair, double-strand breaks, cell proliferation and signaling. Biochem Pharmacol 66: 1547-1554. (Pubitemid 38373345)
51. Fritz G, Kaina B (2006) Rho GTPases: promising cellular targets for novel anticancer drugs. Curr Cancer Drug Targets 6: 1-14.
52. Xiao T, Zhang Y, Wang Y, Xu Y, Yu Z, et al. (2013) Activation of an apoptotic signal transduction pathway involved in the upregulation of calpain and apoptosis-inducing factor in aldosterone-induced primary cultured cardiomyocytes. Food Chem Toxicol 53: 364-370.
53. Wang Y, Zhang Q, Chen H, Li X, Mai W, et al. (2011) P50, the small subunit of DNA polymerase delta, is required for mediation of the interaction of polymerase delta subassemblies with PCNA. PLoS One 6: e27092.
54. Li H, Xie B, Zhou Y, Rahmeh A, Trusa S, et al. (2006) Functional roles of p12, the fourth subunit of human DNA polymerase delta. J Biol Chem 281: 14748-14755. (Pubitemid 43855180)
55. Podust VN, Chang LS, Ott R, Dianov GL, Fanning E (2002) Reconstitution of human DNA polymerase delta using recombinant baculoviruses: the p12 subunit potentiates DNA polymerizing activity of the four-subunit enzyme. J Biol Chem 277: 3894-3901. (Pubitemid 34968641)