Proteomic dissection of cell type-specific H2AX-Interacting protein complex associated with hepatocellular Carcinoma

Journal of Proteome Research

Volumn 9, Issue 3, 2010, Pages 1402-1415

  Yang, Xiaoli ^a   Zou, Peng ^a   Yao, Jun ^a   Yun, Dong ^a   Bao, Huimin ^a   Du, Ruyun ^a   Long, Jing ^a   Chen, Xian ^a,b  

^a FUDAN UNIVERSITY   (China)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

DNA repair; DSBs; H2AX; Hepatocellular carcinoma pathogenesis; In vivo dual tagging quantitative proteomic method; Protein protein interactions

Indexed keywords

BINDING PROTEIN; BLEOMYCIN; CALCIUM BINDING PROTEIN; COFILIN 1; HISTONE H2AX; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PEFLIN 1; STRATIFIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BIOINFORMATICS; CELL CYCLE; CELL TYPE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; LIVER CARCINOGENESIS; LIVER CELL; LIVER CELL CARCINOMA; MOLECULAR INTERACTION; NUCLEIC ACID METABOLISM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; QUANTITATIVE ANALYSIS;

CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; DATABASES, PROTEIN; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; EPITOPES; HISTONES; HUMANS; IMMUNOBLOTTING; LIVER NEOPLASMS; MICROSCOPY, CONFOCAL; PEPTIDES; PROTEIN INTERACTION MAPPING; PROTEOMICS; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION;

EID: 77949785319     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr900932y     Document Type: Article

References (101)

1. Franco, S.; Alt, F. W.; Manis, J. P. Pathways that suppress programmed DNA breaks from progressing to chromosomal breaks and translocations. DNA Repair (Amst.) 2006, 5 (9-10), 1030-1041
2. Phillips, E. R.; McKinnon, P. J. DNA double-strand break repair and development. Oncogene 2007, 26 (56), 7799-7808
3. Shrivastav, M.; De Haro, L. P.; Nickoloff, J. A. Regulation of DNA double-strand break repair pathway choice. Cell Res. 2008, 18 (1), 134-147
4. Pandita, T. K.; Richardson, C. Chromatin remodeling finds its place in the DNA double-strand break response. Nucleic Acids Res. 2009, 37, 1363-1377
5. Mahaney, B. L.; Meek, K.; Lees-Miller, S. P. Repair of ionizing radiation-induced DNA double-strand breaks by non-homologous end-joining. Biochem. T. 2009, 417(3), 639-650
6. Jeggo, P. A.; Lobrich, M. DNA double-strand breaks: their cellular and clinical impact. Oncogene 2007, 26 (56), 7717-7719
7. Redon, C.; Pilch, D.; Rogakou, E.; Sedelnikova, O.; Newrock, K.; Bonner, W. Histone H2A variants H2AX and H2AZ Curr. Opin. Genet. Dev. 2002, 12 (2), 162-169
8. Srivastava, N.; Gochhait, S.; de Boer, P.; Bamezai, R. N. Role of H2AX in DNA damage response and human cancers. Mutat. Res. 2009, 681 (2-3), 180-188
9. Kinner, A.; Wu, W.; Staudt, C.; Iliakis, G. Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 2008, 36 (17), 5678-5694
10. Riches, L. C.; Lynch, A. M.; Gooderham, N. J. Early events in the mammalian response to DNA double-strand breaks. Mutagenesis 2008, 23 (5), 331-339
11. Celeste, A.; Petersen, S.; Romanienko, P. J.; Fernandez-Capetillo, O.; Chen, H. T.; Sedelnikova, O. A.; Reina-San-Martin, B.; Coppola, V.; Meffre, E.; Difilippantonio, M. J.; Redon, C.; Pilch, D. R.; Olaru, A.; Eckhaus, M.; Camerlnl-Otero, R. D.; Tessarollo, L.; Livak, F.; Manova, K.; Bonner, W. M.; Nussenzweig, M. C.; Nussenzweig, A. Genomic instability in mice lacking histone H2AX. Science 2002, 296 (5569), 922z-7.
12. Stewart, G. S.; Wang, B.; Bignell, C. R.; Taylor, A. M.; Elledge, S. J. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 2003, 421 (6926), 961-966
13. Peng, A.; Chen, P. L NFBD1/Mdc1 mediates ATR-dependent DNA damage response. Cancer Res. 2005, 65 (4), 1158-1163
14. Yan, J.; Jetten, A. M. RAP80 and RNF8, key players in the recruitment of repair proteins to DNA damage sites. Cancer Lett. 2008, 271 (2), 179-190
15. Lou, Z.; Minter-Dykhouse, K.; Franco, S.; Gostissa, M.; Rivera, M. A.; Celeste, A.; Manis, J. P.; van Deursen, J.; Nussenzweig, A.; Pauli, T. T.; Alt, F. W.; Chen, J. MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol. Cell 2006, 21 (2), 187-200.
16. Wang, B.; Matsuoka, S.; Ballif, B. A.; Zhang, D.; Smogorzewska, A.; Gygi, S. P.; Elledge, S. J. Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 2007, 316(5828), 1194-1198
17. Sobhian, B.; Shao, G.; Lilli, D. R.; Culhane, A. C.; Moreau, L. A.; Xia, B.; Livingston, D. M.; Greenberg, R. A RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 2007, 316(5828), 1198-1202
18. Xie, A.; Hartlerode, A.; Stucki, M.; Odate, S.; Puget, N.; Kwok, A.; Nagaraju, G.; Yan, C.; Alt, F. W.; Chen, J.; Jackson, S. P.; Scully, R. Distinct roles of chromatin-associated proteins MDC1 and 53BP1 in mammalian double-strand break repair. Mol. Cell 2007, 28 (6), 1045-1057
19. Teoh, N. C.; Dan, Y. Y.; Swlsshelm, K.; Lehman, S.; Wright, J. H.; Haque, J.; Gu, Y.; Fausto, N. Defective DNA strand break repair causes chromosomal instability and accelerates liver carcinogenesis in mice. Hepatology 2008, 47 (6), 2078-2088
20. Downs, J. A. Chromatin structure and DNA double-strand break responses in cancer progression and therapy. Oncogene 2007, 26 (56), 7765-7772
21. Levitt, P. S.; Zhu, M.; Cassano, A.; Yazinski, S. A.; Liu, H.; Darfler, J.; Peters, R. M.; Weiss, R. S. Genome maintenance defects in cultured cells and mice following partial Inactivation of the essential cell cycle checkpoint gene Hus1. Mol. Cell Biol. 2007, 27 (6), 2189-2201
22. Parikh, R. A.; White, J. S.; Huang, X.; Schoppy, D. W.; Baysal, B. E.; Baskaran, R.; Bakkenist, C. J.; Saunders, W. S.; Hsu, L. C.; Romkes, M.; Gollin, S. M. Loss of distal Hq is associated with DNA repair deficiency and reduced sensitivity to ionizing radiation in head and neck squamous cell carcinoma. Genes Chromosomes Cancer 2007, 46 (8), 761-775
23. Bonner, W. M.; Redon, C. E.; Dickey, J. S.; Nakamura, A. J.; Sedelnikova, O. A.; Solier, S.; Pommier, Y. GammaH2AX. and cancer. Nat. Rev. Cancer 2008, 8 (12), 957-967
24. Srivastava, N.; Gochhait, S.; Gupta, P.; Bamezai, R. N. Copy number alterations of the H2AFXgene in sporadic breast cancer patients. Cancer Genet. Cytogenet. 2008, 180 (2), 121-128
25. Walsh, S. H.; Rosenquist, R. Absence of H2AX gene mutations in B-cell leukemias and lymphomas. Leukemia 2005, 19 (3), 464.
26. Chen, B.; Piel, W. H.; Gui, L.; Bruford, E.; Monteiro, A The HSP90 family of genes in the human genome: Insights into their divergence and evolution. Genomics 2005, 86 (6), 627-637
27. Yu, T.; MacPhall, S. H.; Banath, J. P.; Klokov, D.; Olive, P. L. Endogenous expression of phosphorylated histone H2AX in tumors In relation to DNA double-strand breaks and genomic instability. DMA Repair (Amst.) 2006, 5 (8), 935-946
28. Sedelnikova, O. A.; Bonner, W. M. GammaH2AX in cancer cells: a potential biomarker for cancer diagnostics, prediction and recurrence. Cell Cycle 2006, 5 (24), 2909-2913
29. Williams, R. S.; Williams, J. S.; Tainer, J. A. Mre11-Rad50-Nbs1 is a keystone complex connecting DNA repair machinery, doublestrand break signaling, and the chromatin template. Biochem. Cell Biol. 2007, 85 (4), 509-520
30. Lavin, M. F.; Delia, D.; Chessa, L. ATM and the DNA damage response. Workshop on ataxia-telangiectasia and related syndromes. EMBO Rep. 2006, 7(2), 154-160
31. Bartkova, J.; Horejsi, Z.; Koed, K.; Kramer, A.; Tort, F.; Zieger, K.; Guldberg, P.; Sehested, M.; Nesland, J. M.; Lukas, C.; Orntoft, T.; Lukas, J.; Bartek, J. DNA damage response as a candidate anticancer barrier in early human tumorigenesis. Nature 2005, 434 (7035), 864-870
32. Choudhury, A.; Elliott, F.; Iles, M. M.; Churchman, M.; Bristow, R. G.; Bishop, D. T.; Kiltie, A E. Analysis of variants in DNA damage signalling genes in bladder cancer. BMC Med. Genet. 2008, 9, 69.
33. Ishida, T.; Takizawa, Y.; Sakane, I.; Kurumizaka, H. Altered DNA binding by the human Rad51-R150Q mutant found in breast cancer patients. Biol. Pharm. Bull. 2007, 30 (8), 1374-1378
34. Bouwmeester, T.; Bauch, A.; Ruffner, H.; Angrand, P. O.; Bergamini, G.; Croughton, K.; Cruciat, C.; Eberhard, D.; Gagneur, J.; Ghldelli, S.; Hopf, C.; Huhse, B.; Mangano, R.; Michon, A. M.; Schirle, M.; Schlegl, J.; Schwab, M.; Stein, M. A.; Bauer, A.; Casari, G.; Drewes, G.; Gavin, A. C.; Jackson, D. B.; Joberty, G.; Neubauer, G.; Rick, J.; Kuster, B.; Superti-Furga, G. A physical and functional map of the human TNF-alpha/NF-kappa B signal transduction pathway. Nat. Cell Biol. 2004, 6 (2), 97-105.
35. Krogan, N. J.; Cagney, G.; Yu, H.; Zhong, G.; Guo, X.; Ignatchenko, A.; Li, J.; Pu, S.; Datta, N.; Tikuisis, A. P.; Punna, T.; PeregrinAlvarez, J. M.; Shales, M.; Zhang, X.; Davey, M.; Robinson, M. D.; Paccanaro, A.; Bray, J. E.; Sheung, A.; Beattie, B.; Richards, D. P.; Canadien, V.; Lalev, A.; Mena, F.; Wong, P.; Starostine, A.; Canete, M. M.; Vlasblom, J.; Wu, S.; Orsi, C.; Collins, S. R.; Chandran, S.; Haw, R.; Rilstone, J. J.; Gandi, K.; Thompson, N. J.; Musso, G.; St Onge, P.; Ghanny, S.; Lam, M. H.; Butland, G.; Altaf-Ul, A. M.; Kanaya, S.; Shilatifard A.; O'Shea, E.; Weissman, J. S.; Ingles, C. J.; Hughes, T. R.; Parkinson, J.; Gersteln, M.; Wodak, S. J.; Emili, A.; Greenblatt, J. F. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 2006, 440 (7084), 637-643
36. Collins, S. R.; Kemmeren, P.; Zhao, X. C.; Greenblatt, J. F.; Spencer, F.; Holstege, F. C.; Weissman, J. S.; Krogan, N. J. Toward a comprehensive atlas of the physical interactome of Saccharomyces cerevisiae. Mol. Cell. Proteomics 2007, 6 (3), 439-450
37. Wang, T.; Gu, S.; Ronni, T.; Du, Y. C.; Chen, X. In vivo dual-tagging proteomic approach in studying signaling pathways in immune response. T. Proteome Res. 2005, 4 (3), 941-949
38. Du, Y. C.; Gu, S.; Zhou, J.; Wang, T.; Cai, H.; Macinnes, M. A.; Bradbury, E. M.; Chen, X. The dynamic alterations of H2AX complex during DNA repair detected by a proteomic approach reveal the critical roles of Ca(2+)/calmodulin in the ionizing radiation-induced cell cycle arrest. Mol. Cell. Proteomics 2006, 5 (6), 1033-1044
39. Wong, C. M.; Ng, I. O. Molecular pathogenesis of hepatocellular carcinoma. Liver Int 2008. 28 (2), 160-174
40. Wurmbach, E.; Chen, Y. B.; Khitrov, G.; Zhang, W.; Roayaie, S.; Schwartz, M.; Fiel, I.; Thung, S.; Mazzaferro, V.; Bruix, J.; Bottinger, E.; Friedman, S.; Waxman, S.; Llovet, J. M. Genome-wide molecular profiles of HCV-induced dysplasia and hepatocellular carcinoma. Hepatology 2007, 45 (4), 938-1017
41. Nowsheen, S.; Wukovlch, R. L.; Aziz, K.; Kalogerinls, P. T.; Richardson, C. C.; Panayiotidis, M. I.; Bonner, W. M.; Sedelnikova, O. A.; Georgakilas, A. G., Accumulation of oxidatlvely induced clustered DNA lesions in human tumor tissues. Mutat. Res. 2008.
42. Koike, M.; Mashino, M.; Sugasawa, J.; Koike, A Histone H2AX phosphorylation independent of ATM after X-irradiation in mouse liver and kidney in situ. J. Radiat. Res. (Tokyo) 2008, 49 (4), 445-449
43. Koike, M.; Sugasawa, J.; Yasuda, M.; Koike, A. Tissue-specific DNA-PK-dependent H2AX. phosphorylation and gamma-H2AX elimination after X-irradiation in vivo. Biochem. Biophys. Res. Commun. 2008, 376 (1), 52-55
44. Wilda, M.; Demuth, I.; Concannon, P.; Sperling, K.; Hameister, H. Expression pattern of the Nijmegen breakage syndrome gene, Nbsl, during murine development, Hum. Mol. Genet. 2000, 9 (12), 1739-1744
45. Louro, H.; Pinheiro, I.; Costa, P.; Sousa, C.; Dias, A.; Boavida, M. G.; Silva, M. J. Mutagenic effects of poly (ADP-ribose) polymerase-1 deficiency in transgenic mice. Mutat. Res. 2008, 640 (1-2), 82-88
46. Morel, F.; Renoux, M.; Lachaume, P.; Alziari, S. Bleomycininduced double-strand breaks in mitochondrial DNA of Drosophila cells are repaired. Mutat. Res. 2008, 637 (1-2), 111-117
47. Schlade-Bartusiak, K.; Stembalska-Kozlowska, A.; Bernady, M.; Kudyba, M.; Sasiadek, M. Analysis of adaptive response to bleomycin and mitomycin C. Mutat. Res. 2002, 513 (1-2), 75-81.
48. Bao, M.; Song, P.; Qingping, L.; LIu, Y.; Yun, D.; Hexige, S.; Du, R.; Yang, Z.; Fan, H.; Yang, P.; Chen, X. Quantitative proteomic analysis of a paired human liver healthy versus carcinoma cell lines with the same genetic background to identify potential hepatocellular carcinoma markers. Proteomics-Clin. Appl. 2009, 3 (6), 705-719
49. Keller, A.; Nesvizhskii, A. I.; Kolker, E.; Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 2002, 74 (20), 5383-5392
50. Moore, R. E.; Young, M. K.; Lee, T. D. Qscore: an algorithm for evaluating SEQUEST database search results. J. Am. Soc. Mass Spectrom 2002, 13 (4), 378-386
51. Keller, A.; Eng, J.; Zhang, N.; Li, X. J.; Aebersold, R. A uniform proteomics MS/MS analysis platform utilizing open XML file formats. Mol. Syst. Biol. 1, 2005-2017
52. Blagoev, B.; Kratchmarova, I.; Ong, S. E.; Nielsen, M.; Foster, L. J.; Mann, M. A proteomics strategy to elucidate functional proteinprotein interactions applied to EGF signaling. Nat. Biotechnol. 2003, 21 (3), 315-318
53. Escargueil, A. E.; Soares, D. G.; Salvador, M.; Larsen, A. K.; Henriques, J. A. What histone code for DNA repair. Mutat. Res. 2008, 658 (3), 259-270
54. Luk, S. C.; Ngai, S. M.; Tsui, S. K.; Fung, K. P.; Lee, C. Y.; Waye, M. M. In vivo and in vitro association of 14-3-3 epsilon isoform with calmodulin: Implication for signal transduction and cell proliferation. J. Cell Biochem. 1999, 73 (1), 31-35
55. Tanaka, T.; Hallcka, H. D.; Huang, X.; Traganos, F.; Darzynkiewicz, Z. Constitutive histone H2AX phosphorylation and ATM activation, the reporters of DNA damage by endogenous oxidants. Cell Cycle 2006. 5(17), 1940-1945
56. Iwabuchi, K.; Matsui, T.; Hashimoto, M.; Matsumoto, Y.; Kurihara, T.; Date, T. Characterization of a cancer cell line that expresses a splicing variant form of 53BP1: separation of checkpoint and repair functions in 53BP1. Biochem. Biophys. Res. Commun. 2008, 376 (3), 509-513
57. Seiler, J. A.; Conti, C.; Syed, A.; Aladjem, M. I.; Pommier, Y. The intra-S-phase checkpoint affects both DNA replication initiation and elongation: single-cell and -DNA fiber analyses. Moi. Cell. Biol. 2007, 27 (16), 5806-5818
58. Bruneel, A.; Labas, V.; Mailloux, A.; Sharma, S.; Royer, N.; Vinh, J.; Pernet, P.; Vaubourdolle, M.; Baudin, B. Proteomics of human umbilical vein endothelial cells applied to etoposide-induced apoptosis. Proteomics 2005, 5 (15), 3876-3884
59. Bando, Y.; Katayama, T.; Aleshin, A. N.; Manabe, T.; Tohyama, M. GRP94 reduces cell death, in SH-SY5Y cells perturbated calcium homeostasis. Apoptosis 2004, 9 (4), 501-508
60. Hamaguchi, T.; Iizuka, N.; Tsunedomi, R.; Hamamoto, Y.; Miyamoto, T.; Iida, M.; Tokuhisa, Y.; Sakamoto, K.; Takashima, M.; Tamesa, T.; Oka, M. Glycolysis module activated by hypoxiainducible factor lalpha is related to the aggressive phenotype of hepatocellular carcinoma. Int. J. Oncol. 2008, 33 (4), 725-731
61. Wang, Y.; Lee, G. F.; Kelley, R. F.; Spellman, M. W. Identification of a GDP-L-fucose:polypeptide fucosyltransferase and enzymatic addition of O-linked fucose to EGF domains. Glvcobiology 1996, 6 (8), 837-842
62. Davis, G. L.; Dempster, J.; Meier, J. D.; Orr, D. W.; Walberg, M. W.; Brown, B.; Berger, B. D.; O'Connor, J. K.; Goldstein, R. M. Hepatocellular carcinoma: management of an increasingly common problem. Proc. (Bavl. Univ. Med. Cent.) 2008, 21 (3), 266-280
63. Solozobova, V.; Rolletschek, A.; Blattner, C. Nuclear accumulation and activation, of p53 in embryonic stem cells after DNA damage. BMC Cell. Biol. 2009, 10, 46.
64. Grover, R.; Candeias, M. M.; Fahraeus, R.; Das, S. p53 and little brother p53/47: linking IRES activities with protein functions. Oncogene 2009, 20(30), 2766-2772
65. Puigvert, J. C.; Huveneers, S.; Fredriksson, L.; op het Veld, M.; van de Water, B.; Danen, E. H. Cross-talk between integrins and oncogenes modulates chemosensitivity. Mol. Pharmacol. 2009, 75 (4), 947-955
66. Sugimura, K.; Takebayashi, S.; Taguchi, H.; Takeda, S.; Okumura, K. PARP-1 ensures regulation of replication fork progression by homologous recombination on damaged DNA. J. Cell Biol. 2008, 183 (7), 1203-1212
67. Cohen-Armon, M. PARP-1 activation in the ERK signaling pathway. Trends Pharmacol. Sci. 2007, 28 (11), 556-560
68. Marcos-Carcavilla, A.; Calvo, J. H.; Gonzalez, C.; Moazami-Goudarzi, K.; Laurent, P.; Bertaud, M.; Hayes, H.; Beattie, A. E.; Serrano, C.; Lyahyai, J.; Martin-Burrlel, I.; Serrano, M. Structural and functional analysis of the HSP90AA1 gene: distribution of polymorphisms among sheep with different responses to scrapie. Cell Stress Chaperones 2008, 13(1), 19-29.
69. Cepeda, V.; Fuertes, M. A.; Castilla, J.; Alonso, C.; Quevedo, C.; Soto, M.; Perez, J. M. Poly(ADP-ribose) polymerase-1 (PARP-1) inhibitors in cancer chemotherapy. Recent Pat. Anti-Cancer Drug Discovery 2006, 1(1), 39-53.
70. Oka, S.; Ohno, M.; Tsuchimoto, D.; Sakumi, K.; Furuichi, M.; Nakabeppu, Y. Two distinct pathways of cell death triggered by oxidative damage to nuclear and mitochondrial DNAs. Embo I. 2008, 27 (2), 421-432
71. Piskunova, T. S.; lurova, M. N.; Zabezhinskii, M. A.; Anisimov, V. N. [Poly(ADP-ribosa)polymerase-the relationships with life span and carcinogenesis]. Adv. Gerontol. 2007, 20 (2), 82-90.
72. Lewis, C.; Low, J. A. Clinical poly(ADP-ribose) polymerase inhibitors for the treatment of cancer. Curr. Opin. Investig. Drugs 2007, 8 (12), 1051-1056
73. Elser, M.; Borsig, L.; Hassa, P. O.; Erener, S.; Messner, S.; Valovka, T.; Keller, S.; Gassmann, M.; Hottiger, M. O. Poly(ADP-ribose) polymerase 1 promotes tumor cell survival by coactivating hypoxia-inducible factor-1-dependent gene expression. Mol. Cancer Res. 2008, 6 (2), 282-290
74. Zaremba, T.; Curtin, N. J. PARP inhibitor development for systemic cancer targeting. Anticancer Agents Med. Chem. 2007, 7 (5), 515-523
75. Genovese, T.; Cuzzocrea, S. Role of free radicals and poly(ADPribose)polymerase-1 in the development of spinal cord injury: new potential therapeutic targets. Curr. Med. Chem. 2008, 15 (5), 477-487
76. Shlmlzu, S.; Nomura, F.; Tomonaga, T.; Sunaga, M.; Noda, M.; Ebara, M.; Saisho, H. Expression of poly(ADP-ribose) polymerase In human hepatocellular carcinoma and analysis of biopsy specimens obtained, under sonographic guidance. Oncol. Rep. 2004, 12 (4), 821-825
77. Huang, S. H.; Xiong, M.; Chen, X. P.; Xiao, Z. Y.; Zhao, Y. F.; Huang, Z. Y. PJ34, an inhibitor of PARP-1, suppresses cell growth and enhances the suppressive effects of cisplatin in liver cancer cells. Oncol. Rep. 2008, 20 (3), 567-572
78. Dandri, M.; Burda, M. R.; Burkle, A.; Zuckerman, D. M.; Will, H.; Rogler, C. E.; Greten, H.; Petersen, J. Increase in de novo HBV DNA integrations in response to oxidative DNA damage or inhibition of poly(ADP-ribosyl)ation. Hepatology 2002, 35 (1), 217-223
79. Niemantsverdriet, M.; Wagner, K.; Visser, M.; Backendorf, C. Cellular functions of 14-3-3 zeta in apoptosis and cell adhesion emphasize its oncogenic character. Oncogene 2008, 27(9), 1315-1319
80. Kobayashi, R.; Deavers, M.; Patenia, R.; Rice-Stitt, T.; Halbe, J.; Gallardo, S.; Freedman, R. S. 14-3-3 zeta protein secreted by tumor associated monocytes/macrophages from ascites of epithelial ovarian cancer patients. Cancer Immunol. Immunother. 2009, 58, 247-258
81. Xing, H.; Zhang, S.; Weinheimer, C.; Kovacs, A.; Muslin, A. J. 14-3-3 proteins block apoptosis and differentially regulate MAPK cascades. Embo J. 2000, 19 (3), 349-358
82. Tlan, Q.; Feetham, M. C.; Tao, W. A.; He, X. C.; Li, L.; Aebersold, R.; Hood, L. Proteomic analysis identifies that 14-3-3zeta interacts with beta-catenin and facilitates its activation by Akt. Proc. Natl. Acad. Sci. U.S.A. 2004, 101 (43), 15370-15375
83. Li, Z.; Zhao, J.; Du, Y.; Park, H. R.; Sun, S. Y.; Bernal-Mizrachi, L.; Aitken, A.; Khuri, F. R.; Fu, H. Down-regulation of 14-3-3zeta suppresses anchorage-independent growth of lung cancer cells through anoikis activation. Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (1), 162-167
84. Fan, T.; Li, R.; Todd, N. W.; Qiu, Q.; Fang, H. B.; Wang, H.; Shen, J.; Zhao, R. Y.; Caraway, N. P.; Katz, R. L.; Stass, S. A.; Jiang, F. Up-regulation of 14-3-3zeta in lung cancer and its implication as prognostic and therapeutic target. Cancer Res. 2007, 67 (16), 7901-7906
85. Toivola, D. M.; Nieminen, M. I.; Hesse, M.; He, T.; Baribault H.; Magin, T. M.; Omary, M. B.; Eriksson, J. E. Disturbances in hepatic cell-cycle regulation in mice with assembly-deficient keratins 8/18. Hepatology 2001, 34 (6), 1174-1183
86. Bamburg, J. R.; Bernstein, B. W. ADF/Cofilin. Curr. Biol. 2008, 18 (7), R273-5.
87. Lee, Y. J.; Sheu, T. J.; Keng, P. C. Enhancement of radiosensitivity in H1299 cancer cells by actin-assoclated protein cofilin. Biochem. BioPhys. Pes. Commun. 2005, 335 (2), 286-291
88. Tojima, T.; Ito, E. Signal transduction cascades underlying de novo protein synthesis required for neuronal morphogenesis in differentiating neurons. Pros. Neurobiol. 2004, 72 (3), 1.83-93.
89. Ding, Y.; Milosavljevic, T.; Alahari, S. K. Nischarin inhibits LIM Mnase to regulate Cofilin phosphorylation and cell invasion. Mol. Cell. Biol. 2008, 28, 3742-3756
90. Sidani, M.; Wessels, D.; Mounelmne, G.; Ghosh, M.; Goswami, S.; Sarmiento, C.; Wang, W.; Kuhl, S.; El-Sibal, M.; Backer, J. M.; Eddy, R.; Soll, D.; Condeelis, J. Cofilin determines the migration behavior and turning frequency of metastatic cancer cells. J. Cell Biol. 2007, 179(4), 777-791
91. Ding, S. J.; Li, Y.; Shao, X. X.; Zhou, H.; Zeng, R.; Tang, Z. Y.; Xia, Q. C. Proteome analysis of hepatocellular carcinoma cell strains, MHCC97-H and MHCC97-L, with different metastasis potentials. Proteomics 2004, 4 (4), 982-994
92. 2+-dependent manner. J. Biol. Chem. 2001, 276 (17), 14053-14058
93. Kitaura, Y.; Watanabe, M.; Satoh, H.; Kawat, T.; Hitomi, K.; Maki, M. Peflin, a novel member of the five-EF-hand-protein family, is similar to the apoptosis-llnked gene 2 (ALG-2) protein but possesses nonapeptide repeats in the N-terminal hydrophobic region. Biochem. Biophys. Res. Commun. 1999, 263 (1), 68-75.
94. Lieberman, H. B. DNA damage repair and response proteins as targets for cancer therapy. Curr. Med. Chem. 2008, 15 (4), 360-367
95. Lowndes, N. F.; Toh, G. W. DNA repair: the importance of phosphorylating histone H2AX. Curr. Biol. 2005, 15 (3), R99-R102.
96. McManus, K. J.; Hendzel, M. J. ATM-dependent DNA damageindependent mitotic phosphorylation of H2AX. in normally growing mammalian cells. Mol. Biol. Cell 2005, 16 (10), 5013-5025
97. Ichijima, Y.; Sakasai, R.; Okita, N.; Asahina, K.; Mizutani, S.; Teraoka, H. Phosphorylation of histone H2AX at M phase in human cells without DNA damage response. Biochem. Biophys. Res. Commun. 2005, 336 (3), 807-812
98. Song, X.; Gjoneska, E.; Ren, Q.; Taverna, S. D.; Allis, C. D.; Gorovsky, M. A Phosphorylation of the SQ H2A.X motif is required for proper meiosis and mitosis in Tetrahymena thermophila. Mol. Cell. Biol. 2007, 27 (7), 2648-2660
99. Gorgoulls, V. G.; Vassillou, L V.; Karakaldos, P.; Zacharatos, P.; Kotsinas, A.; Liloglou, T.; Venere, M.; Ditullio, R. A., Jr.; Kastrinakis, N. G.; Levy, B.; Kletsas, D.; Yoneta, A.; Herlyn, M.; Klttas, C.; Halazonetis, T. D. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005, 434 (7035), 907-913
100. Nuciforo, P. G.; Luise, C.; Capra, M.; Pelosi, G.; d'Adda di Fagagna, F. Complex engagement of DNA damage response pathways In human cancer and in lung tumor progression. Carcinogenesis 2007, 28 (10), 2082-2088
101. Knock, E.; Deng, L.; Wu, Q.; Lawrance, A. K.; Wang, X. L.; Rozen, R. Strain differences in mice highlight the role of DNA damage in neoplasia induced by low dietary folate. I. Nutr. 2008, 138 (4), 653-658