Molecular mechanism of adenomatous polyposis coli-induced blockade of base excision repair pathway in colorectal carcinogenesis

Life Sciences

Volumn 139, Issue , 2015, Pages 145-152

  Narayan, Satya ^a   Sharma, Ritika ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Adenomatous polyposis coli; Base excision repair; Colorectal carcinogenesis; DNA damage

Indexed keywords

APC PROTEIN; DNA DIRECTED DNA POLYMERASE BETA; FLAP ENDONUCLEASE; FLAP ENDONUCLEASE 1; TEMOZOLOMIDE; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; DACARBAZINE;

APOPTOSIS; CANCER CHEMOTHERAPY; CARCINOGENESIS; COLON POLYPOSIS; COLORECTAL CANCER; COLORECTAL TUMOR; DNA ALKYLATION; EXCISION REPAIR; GENE MUTATION; HUMAN; MISMATCH REPAIR; PROTEIN PROTEIN INTERACTION; REVIEW; ADENOMATOUS POLYPOSIS COLI; ANALOGS AND DERIVATIVES; ANIMAL; COLON; DNA REPAIR; DRUG EFFECTS; GENETICS; METABOLISM; MOLECULAR MODEL; MOLECULARLY TARGETED THERAPY; MUTATION; PATHOLOGY; RECTUM;

ADENOMATOUS POLYPOSIS COLI; ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOGENESIS; COLON; DACARBAZINE; DNA POLYMERASE BETA; DNA REPAIR; FLAP ENDONUCLEASES; HUMANS; MODELS, MOLECULAR; MOLECULAR TARGETED THERAPY; MUTATION; RECTUM;

EID: 84941645706     PISSN: 00243205     EISSN: 18790631     Source Type: Journal    
DOI: 10.1016/j.lfs.2015.08.019     Document Type: Review

References (168)

1. R.L. Siegel, K.D. Miller, and A. Jemal Cancer statistics, 2015 CA Cancer J. Clin. 65 2015 5 29
2. M. Aghili, S. Izadi, H. Madani, and H. Mortazavi Clinical and pathological evaluation of patients with early and late recurrence of colorectal cancer Asia Pac. J. Clin. Oncol. 6 2010 35 41
3. M.J. O'Connell, M.E. Campbell, R.M. Goldberg, A. Grothey, J.F. Seitz, J.K. Benedetti, T. Andre, D.G. Haller, and D.J. Sargent Survival following recurrence in stage II and III colon cancer: findings from the ACCENT data set J. Clin. Oncol. 26 2008 2336 2341
4. G.P. Kanas, A. Taylor, J.N. Primrose, W.J. Langeberg, M.A. Kelsh, F.S. Mowat, D.D. Alexander, M.A. Choti, and G. Poston Survival after liver resection in metastatic colorectal cancer: review and meta-analysis of prognostic factors Clin. Epidemiol. 4 2012 283 301
5. T. Muto, H.J. Bussey, and B.C. Morson The evolution of cancer of the colon and rectum Cancer 36 1975 2251 2270
6. E.R. Fearon, and B. Vogelstein A genetic model for colorectal tumorigenesis Cell 61 1990 759 767
7. E.R. Fearon Molecular genetics of colorectal cancer Annu. Rev. Pathol. 6 2011 479 507
8. N.S. Fearnhead, J.L. Wilding, and W.F. Bodmer Genetics of colorectal cancer: hereditary aspects and overview of colorectal tumorigenesis Br. Med. Bull. 64 2002 27 43
9. M. Pancione, A. Remo, and V. Colantuoni Genetic and epigenetic events generate multiple pathways in colorectal cancer progression Pathol. Res. Int. 2012 2012 509348
10. Y. Miyoshi, H. Nagase, H. Ando, A. Horii, S. Ichii, S. Nakatsuru, T. Aoki, Y. Miki, T. Mori, and Y. Nakamura Somatic mutations of the APC gene in colorectal tumors: mutation cluster region in the APC gene Hum. Mol. Genet. 1 1992 229 233
11. S.M. Powell, N. Zilz, Y. Beazer-Barclay, T.M. Bryan, S.R. Hamilton, S.N. Thibodeau, B. Vogelstein, and K.W. Kinzler APC mutations occur early during colorectal tumorigenesis Nature 359 1992 235 237
12. J. Tsao, and D. Shibata Further evidence that one of the earliest alterations in colorectal carcinogenesis involves APC Am. J. Pathol. 145 1994 531 534
13. S. Ichii, A. Horii, S. Nakatsuru, J. Furuyama, J. Utsunomiya, and Y. Nakamura Inactivation of both APC alleles in an early stage of colon adenomas in a patient with familial adenomatous polyposis (FAP) Hum. Mol. Genet. 1 1992 387 390
14. H. Shibata, K. Toyama, H. Shioya, M. Ito, M. Hirota, S. Hasegawa, H. Matsumoto, H. Takano, T. Akiyama, K. Toyoshima, R. Kanamaru, Y. Kanegae, I. Saito, Y. Nakamura, K. Shiba, and T. Noda Rapid colorectal adenoma formation initiated by conditional targeting of the Apc gene Science 278 1997 120 123
15. V. Meniel, M. Megges, M.A. Young, A. Cole, O.J. Sansom, and A.R. Clarke Apc and p53 interaction in DNA damage and genomic instability in hepatocytes Oncogene 34 2015 4118 4129
16. B.R. Henderson Nuclear-cytoplasmic shuttling of APC regulates beta-catenin subcellular localization and turnover Nat. Cell Biol. 2 2000 653 660
17. S. Munemitsu, B. Souza, O. Muller, I. Albert, B. Rubinfeld, and P. Polakis The APC gene product associates with microtubules in vivo and promotes their assembly in vitro Cancer Res. 54 1994 3676 3681
18. K.L. Neufeld, and R.L. White Nuclear and cytoplasmic localizations of the adenomatous polyposis coli protein Proc. Natl. Acad. Sci. U. S. A. 94 1997 3034 3039
19. K.L. Neufeld, D.A. Nix, H. Bogerd, Y. Kang, M.C. Beckerle, B.R. Cullen, and R.L. White Adenomatous polyposis coli protein contains two nuclear export signals and shuttles between the nucleus and cytoplasm Proc. Natl. Acad. Sci. U. S. A. 97 2000 12085 12090
20. R. Rosin-Arbesfeld, F. Townsley, and M. Bienz The APC tumour suppressor has a nuclear export function Nature 406 2000 1009 1012
21. M.H. Wong, M.L. Hermiston, A.J. Syder, and J.I. Gordon Forced expression of the tumor suppressor adenomatosis polyposis coli protein induces disordered cell migration in the intestinal epithelium Proc. Natl. Acad. Sci. U. S. A. 93 1996 9588 9593
22. K.J. Smith, D.B. Levy, P. Maupin, T.D. Pollard, B. Vogelstein, and K.W. Kinzler Wild-type but not mutant APC associates with the microtubule cytoskeleton Cancer Res. 54 1994 3672 3675
23. A.I. Barth, A.L. Pollack, Y. Altschuler, K.E. Mostov, and W.J. Nelson NH2-terminal deletion of beta-catenin results in stable colocalization of mutant beta-catenin with adenomatous polyposis coli protein and altered MDCK cell adhesion J. Cell Biol. 136 1997 693 706
24. M. Bienz, and F. Hamada Adenomatous polyposis coli proteins and cell adhesion Curr. Opin. Cell Biol. 16 2004 528 535
25. E.S. Harris, and W.J. Nelson Adenomatous polyposis coli regulates endothelial cell migration independent of roles in beta-catenin signaling and cell-cell adhesion Mol. Biol. Cell 21 2010 2611 2623
26. N.S. Fearnhead, M.P. Britton, and W.F. Bodmer The ABC of APC Hum. Mol. Genet. 10 2001 721 733
27. S. Narayan, and D. Roy Role of APC and DNA mismatch repair genes in the development of colorectal cancers Mol. Cancer 2 2003 41
28. K.H. Goss, and J. Groden Biology of the adenomatous polyposis coli tumor suppressor J. Clin. Oncol. 18 2000 1967 1979
29. L.K. Su, M. Burrell, D.E. Hill, J. Gyuris, R. Brent, R. Wiltshire, J. Trent, B. Vogelstein, and K.W. Kinzler APC binds to the novel protein EB1 Cancer Res. 55 1995 2972 2977
30. L. Berrueta, J.S. Tirnauer, S.C. Schuyler, D. Pellman, and B.E. Bierer The APC-associated protein EB1 associates with components of the dynactin complex and cytoplasmic dynein intermediate chain Curr. Biol. 9 1999 425 428
31. T. Kanaba, R. Maesaki, T. Mori, Y. Ito, T. Hakoshima, and M. Mishima Microtubule-binding sites of the CH domain of EB1 and its autoinhibition revealed by NMR Biochim. Biophys. Acta 1834 2013 499 507
32. Y. Stypula-Cyrus, N.N. Mutyal, M. Dela Cruz, D.P. Kunte, A.J. Radosevich, R. Wali, H.K. Roy, and V. Backman End-binding protein 1 (EB1) up-regulation is an early event in colorectal carcinogenesis FEBS Lett. 588 2014 829 835
33. T. Ishidate, A. Matsumine, K. Toyoshima, and T. Akiyama The APC-hDLG complex negatively regulates cell cycle progression from the G0/G1 to S phase Oncogene 19 2000 365 372
34. V. Korinek, N. Barker, P.J. Morin, D. van Wichen, R. de Weger, K.W. Kinzler, B. Vogelstein, and H. Clevers Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC -/- colon carcinoma Science 275 1997 1784 1787
35. P.J. Morin, A.B. Sparks, V. Korinek, N. Barker, H. Clevers, B. Vogelstein, and K.W. Kinzler Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC Science 275 1997 1787 1790
36. T.C. He, A.B. Sparks, C. Rago, H. Hermeking, L. Zawel, L.T. da Costa, P.J. Morin, B. Vogelstein, and K.W. Kinzler Identification of c-MYC as a target of the APC pathway Science 281 1998 1509 1512
37. M. Shtutman, J. Zhurinsky, I. Simcha, C. Albanese, M. D'Amico, R. Pestell, and A. Ben-Ze'ev The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway Proc. Natl. Acad. Sci. U. S. A. 96 1999 5522 5527
38. H.C. Crawford, B.M. Fingleton, L.A. Rudolph-Owen, K.J. Goss, B. Rubinfeld, P. Polakis, and L.M. Matrisian The metalloproteinase matrilysin is a target of beta-catenin transactivation in intestinal tumors Oncogene 18 1999 2883 2891
39. B. Mann, M. Gelos, A. Siedow, M.L. Hanski, A. Gratchev, M. Ilyas, W.F. Bodmer, M.P. Moyer, E.O. Riecken, H.J. Buhr, and C. Hanski Target genes of beta-catenin-T cell-factor/lymphoid-enhancer-factor signaling in human colorectal carcinomas Proc. Natl. Acad. Sci. U. S. A. 96 1999 1603 1608
40. K. Myant, and O. Sansom Efficient Wnt mediated intestinal hyperproliferation requires the cyclin D2-CDK4/6 complex Cell Div. 6 2011 3
41. H. Hermeking, C. Rago, M. Schuhmacher, Q. Li, J.F. Barrett, A.J. Obaya, B.C. O'Connell, M.K. Mateyak, W. Tam, F. Kohlhuber, C.V. Dang, J.M. Sedivy, D. Eick, B. Vogelstein, and K.W. Kinzler Identification of CDK4 as a target of c-MYC Proc. Natl. Acad. Sci. U. S. A. 97 2000 2229 2234
42. O.J. Sansom, V.S. Meniel, V. Muncan, T.J. Phesse, J.A. Wilkins, K.R. Reed, J.K. Vass, D. Athineos, H. Clevers, and A.R. Clarke Myc deletion rescues Apc deficiency in the small intestine Nature 446 2007 676 679
43. D. Athineos, and O.J. Sansom Myc heterozygosity attenuates the phenotypes of APC deficiency in the small intestine Oncogene 29 2010 2585 2590
44. F. Ficari, A. Cama, R. Valanzano, M.C. Curia, R. Palmirotta, G. Aceto, D.L. Esposito, S. Crognale, A. Lombardi, L. Messerini, R. Mariani-Costantini, F. Tonelli, and P. Battista APC gene mutations and colorectal adenomatosis in familial adenomatous polyposis Br. J. Cancer 82 2000 348 353
45. H. Nagase, Y. Miyoshi, A. Horii, T. Aoki, M. Ogawa, J. Utsunomiya, S. Baba, T. Sasazuki, and Y. Nakamura Correlation between the location of germ-line mutations in the APC gene and the number of colorectal polyps in familial adenomatous polyposis patients Cancer Res. 52 1992 4055 4057
46. P. Polakis Wnt signaling and cancer Genes Dev. 14 2000 1837 1851
47. J.S. Wu, P. Paul, E.A. McGannon, and J.M. Church APC genotype, polyp number, and surgical options in familial adenomatous polyposis Ann. Surg. 227 1998 57 62
48. R.A. Phelps, S. Chidester, S. Dehghanizadeh, J. Phelps, I.T. Sandoval, K. Rai, T. Broadbent, S. Sarkar, R.W. Burt, and D.A. Jones A two-step model for colon adenoma initiation and progression caused by APC loss Cell 137 2009 623 634
49. R.A. Phelps, T.J. Broadbent, D.M. Stafforini, and D.A. Jones New perspectives on APC control of cell fate and proliferation in colorectal cancer Cell Cycle 8 2009 2549 2556
50. Y. Nakamura The role of the adenomatous polyposis coli (APC) gene in human cancers Adv. Cancer Res. 62 1993 65 87
51. R. Smits, M.F. Kielman, C. Breukel, C. Zurcher, K. Neufeld, S. Jagmohan-Changur, N. Hofland, J. van Dijk, R. White, W. Edelmann, R. Kucherlapati, P.M. Khan, and R. Fodde Apc1638T: a mouse model delineating critical domains of the adenomatous polyposis coli protein involved in tumorigenesis and development Genes Dev. 13 1999 1309 1321
52. A. Plawski, T. Banasiewicz, P. Borun, L. Kubaszewski, P. Krokowicz, M. Skrzypczak-Zielinska, and J. Lubinski Familial adenomatous polyposis of the colon, Hered Cancer Clin. Pract. 11 2013 15
53. L.N. Kwong, and W.F. Dove APC and its modifiers in colon cancer Adv. Exp. Med. Biol. 656 2009 85 106
54. A.S. Jaiswal, and S. Narayan A novel function of adenomatous polyposis coli (APC) in regulating DNA repair Cancer Lett. 271 2008 272 280
55. G.P. Holmquist Endogenous lesions, S-phase-independent spontaneous mutations, and evolutionary strategies for base excision repair Mutat. Res. 400 1998 59 68
56. J.H. Hoeijmakers Genome maintenance mechanisms for preventing cancer Nature 411 2001 366 374
57. H.E. Krokan, R. Standal, and G. Slupphaug DNA glycosylases in the base excision repair of DNA Biochem. J. 325 Pt 1 1997 1 16
58. P. Modrich Mismatch repair, genetic stability, and cancer Science 266 1994 1959 1960
59. B.P. Muniappan, and W.G. Thilly The DNA polymerase beta replication error spectrum in the adenomatous polyposis coli gene contains human colon tumor mutational hotspots Cancer Res. 62 2002 3271 3275
60. A. Sancar, and G.B. Sancar DNA repair enzymes Annu. Rev. Biochem. 57 1988 29 67
61. A.R. Sarasin, and P.C. Hanawalt Carcinogens enhance survival of UV-irradiated simian virus 40 in treated monkey kidney cells: induction of a recovery pathway? Proc. Natl. Acad. Sci. U. S. A. 75 1978 346 350
62. A.K. Mantha, B. Sarkar, and G. Tell A short review on the implications of base excision repair pathway for neurons: relevance to neurodegenerative diseases Mitochondrion 16 2014 38 49
63. G.L. Dianov, and U. Hubscher Mammalian base excision repair: the forgotten archangel Nucleic Acids Res. 41 2013 3483 3490
64. S. Biade, R.W. Sobol, S.H. Wilson, and Y. Matsumoto Impairment of proliferating cell nuclear antigen-dependent apurinic/apyrimidinic site repair on linear DNA J. Biol. Chem. 273 1998 898 902
65. A. Klungland, and T. Lindahl Second pathway for completion of human DNA base excision-repair: reconstitution with purified proteins and requirement for DNase IV (FEN1) EMBO J. 16 1997 3341 3348
66. N. El-Andaloussi, T. Valovka, M. Toueille, R. Steinacher, F. Focke, P. Gehrig, M. Covic, P.O. Hassa, P. Schar, U. Hubscher, and M.O. Hottiger Arginine methylation regulates DNA polymerase beta Mol. Cell 22 2006 51 62
67. J.L. Huffman, O. Sundheim, and J.A. Tainer DNA base damage recognition and removal: new twists and grooves Mutat. Res. 577 2005 55 76
68. S. Narayan, A.S. Jaiswal, and R. Balusu Tumor suppressor APC blocks DNA polymerase beta-dependent strand displacement synthesis during long patch but not short patch base excision repair and increases sensitivity to methylmethane sulfonate J. Biol. Chem. 280 2005 6942 6949
69. B. Demple, T. Herman, and D.S. Chen Cloning and expression of APE, the cDNA encoding the major human apurinic endonuclease: definition of a family of DNA repair enzymes Proc. Natl. Acad. Sci. U. S. A. 88 1991 11450 11454
70. C.M. Kane, and S. Linn Purification and characterization of an apurinic/apyrimidinic endonuclease from HeLa cells J. Biol. Chem. 256 1981 3405 3414
71. Y. Matsumoto, and K. Kim Excision of deoxyribose phosphate residues by DNA polymerase beta during DNA repair Science 269 1995 699 702
72. A.J. Podlutsky, I.I. Dianova, V.N. Podust, V.A. Bohr, and G.L. Dianov Human DNA polymerase beta initiates DNA synthesis during long-patch repair of reduced AP sites in DNA EMBO J. 20 2001 1477 1482
73. R.A. Bambara, R.S. Murante, and L.A. Henricksen Enzymes and reactions at the eukaryotic DNA replication fork J. Biol. Chem. 272 1997 4647 4650
74. M.R. Lieber The FEN-1 family of structure-specific nucleases in eukaryotic DNA replication, recombination and repair Bioessays 19 1997 233 240
75. A. Memisoglu, and L. Samson Base excision repair in yeast and mammals Mutat. Res. 451 2000 39 51
76. C.J. Norbury, and I.D. Hickson Cellular responses to DNA damage Annu. Rev. Pharmacol. Toxicol. 41 2001 367 401
77. J.A. Harrigan, P.L. Opresko, C. von Kobbe, P.S. Kedar, R. Prasad, S.H. Wilson, and V.A. Bohr The Werner syndrome protein stimulates DNA polymerase beta strand displacement synthesis via its helicase activity J. Biol. Chem. 278 2003 22686 22695
78. J.A. Harrigan, D.M. Wilson III, R. Prasad, P.L. Opresko, G. Beck, A. May, S.H. Wilson, and V.A. Bohr The Werner syndrome protein operates in base excision repair and cooperates with DNA polymerase beta Nucleic Acids Res. 34 2006 745 754
79. F. Dantzer, G. de La Rubia, J. Menissier-De Murcia, Z. Hostomsky, G. de Murcia, and V. Schreiber Base excision repair is impaired in mammalian cells lacking Poly(ADP-ribose) polymerase-1 Biochemistry 39 2000 7559 7569
80. R. Prasad, O.I. Lavrik, S.J. Kim, P. Kedar, X.P. Yang, B.J. Vande Berg, and S.H. Wilson DNA polymerase beta-mediated long patch base excision repair. Poly(ADP-ribose)polymerase-1 stimulates strand displacement DNA synthesis J. Biol. Chem. 276 2001 32411 32414
81. P.S. Kedar, S.J. Kim, A. Robertson, E. Hou, R. Prasad, J.K. Horton, and S.H. Wilson Direct interaction between mammalian DNA polymerase beta and proliferating cell nuclear antigen J. Biol. Chem. 277 2002 31115 31123
82. P. Fortini, B. Pascucci, E. Parlanti, R.W. Sobol, S.H. Wilson, and E. Dogliotti Different DNA polymerases are involved in the short- and long-patch base excision repair in mammalian cells Biochemistry 37 1998 3575 3580
83. Y. Matsumoto, K. Kim, and D.F. Bogenhagen Proliferating cell nuclear antigen-dependent abasic site repair in Xenopus laevis oocytes: an alternative pathway of base excision DNA repair Mol. Cell. Biol. 14 1994 6187 6197
84. J. Zhou, J. Ahn, S.H. Wilson, and C. Prives A role for p53 in base excision repair EMBO J. 20 2001 914 923
85. M.S. DeMott, S. Zigman, and R.A. Bambara Replication protein A stimulates long patch DNA base excision repair J. Biol. Chem. 273 1998 27492 27498
86. L.H. Thompson, and M.G. West XRCC1 keeps DNA from getting stranded Mutat. Res. 459 2000 1 18
87. A.S. Jaiswal, R. Balusu, M.L. Armas, C.N. Kundu, and S. Narayan Mechanism of adenomatous polyposis coli (APC)-mediated blockage of long-patch base excision repair Biochemistry 45 2006 15903 15914
88. C.N. Kundu, R. Balusu, A.S. Jaiswal, and S. Narayan Adenomatous polyposis coli-mediated hypersensitivity of mouse embryonic fibroblast cell lines to methylmethane sulfonate treatment: implication of base excision repair pathways Carcinogenesis 28 2007 2089 2095
89. R. Balusu, A.S. Jaiswal, M.L. Armas, C.N. Kundu, L.B. Bloom, and S. Narayan Structure/function analysis of the interaction of adenomatous polyposis coli with DNA polymerase beta and its implications for base excision repair Biochemistry 46 2007 13961 13974
90. C.N. Kundu, R. Balusu, A.S. Jaiswal, C.G. Gairola, and S. Narayan Cigarette smoke condensate-induced level of adenomatous polyposis coli blocks long-patch base excision repair in breast epithelial cells Oncogene 26 2007 1428 1438
91. S. Narayan, A.S. Jaiswal, D. Kang, P. Srivastava, G.M. Das, and C.G. Gairola Cigarette smoke condensate-induced transformation of normal human breast epithelial cells in vitro Oncogene 23 2004 5880 5889
92. A.S. Jaiswal, H. Panda, C.A. Pampo, D.W. Siemann, C.G. Gairola, R. Hromas, and S. Narayan Adenomatous polyposis coli-mediated accumulation of abasic DNA lesions lead to cigarette smoke condensate-induced neoplastic transformation of normal breast epithelial cells Neoplasia 15 2013 454 460
93. R. Fodde, J. Kuipers, C. Rosenberg, R. Smits, M. Kielman, C. Gaspar, J.H. van Es, C. Breukel, J. Wiegant, R.H. Giles, and H. Clevers Mutations in the APC tumour suppressor gene cause chromosomal instability Nat. Cell Biol. 3 2001 433 438
94. S.N. Thibodeau, G. Bren, and D. Schaid Microsatellite instability in cancer of the proximal colon Science 260 1993 816 819
95. A.S. Jaiswal, and S. Narayan Assembly of the base excision repair complex on abasic DNA and role of adenomatous polyposis coli on its functional activity Biochemistry 50 2011 1901 1909
96. J. Deka, P. Herter, M. Sprenger-Haussels, S. Koosch, D. Franz, K.M. Muller, C. Kuhnen, I. Hoffmann, and O. Muller The APC protein binds to A/T rich DNA sequences Oncogene 18 1999 5654 5661
97. J. Qian, A.A. Sarnaik, T.M. Bonney, J. Keirsey, K.A. Combs, K. Steigerwald, S. Acharya, G.K. Behbehani, M.C. Barton, A.M. Lowy, and J. Groden The APC tumor suppressor inhibits DNA replication by directly binding to DNA via its carboxyl terminus Gastroenterology 135 2008 152 162
98. E.M. Perchiniak, and J. Groden Mechanisms Regulating Microtubule Binding, DNA Replication, and Apoptosis are Controlled by the Intestinal Tumor Suppressor APC Curr. Colorectal Cancer Rep. 7 2011 145 151
99. M.G. Brocardo, J.A. Borowiec, and B.R. Henderson Adenomatous polyposis coli protein regulates the cellular response to DNA replication stress Int. J. Biochem. Cell Biol. 43 2011 1354 1364
100. A.S. Jaiswal, S. Banerjee, R. Aneja, F.H. Sarkar, D.A. Ostrov, and S. Narayan DNA polymerase beta as a novel target for chemotherapeutic intervention of colorectal cancer PLoS One 6 2011 e16691
101. A.S. Jaiswal, S. Banerjee, H. Panda, C.D. Bulkin, T. Izumi, F.H. Sarkar, D.A. Ostrov, and S. Narayan A novel inhibitor of DNA polymerase beta enhances the ability of temozolomide to impair the growth of colon cancer cells Mol. Cancer Res. 7 2009 1973 1983
102. A.S. Jaiswal, H. Panda, B.K. Law, J. Sharma, J. Jani, R. Hromas, and S. Narayan NSC666715 and its analogs inhibit strand-displacement activity of DNA polymerase beta and potentiate temozolomide-induced DNA Damage, senescence and apoptosis in colorectal cancer cells PLoS One 10 2015 e0123808
103. H. Panda, A.S. Jaiswal, P.E. Corsino, M.L. Armas, B.K. Law, and S. Narayan Amino acid Asp181 of 5′-flap endonuclease 1 is a useful target for chemotherapeutic development Biochemistry 48 2009 9952 9958
104. E. Martino-Echarri, B.R. Henderson, and M.G. Brocardo Targeting the DNA replication checkpoint by pharmacologic inhibition of Chk1 kinase: a strategy to sensitize APC mutant colon cancer cells to 5-fluorouracil chemotherapy Oncotarget 5 2014 9889 9900
105. S. Quiros, W.P. Roos, and B. Kaina Processing of O6-methylguanine into DNA double-strand breaks requires two rounds of replication whereas apoptosis is also induced in subsequent cell cycles Cell Cycle 9 2010 168 178
106. M. Guerard, M. Baum, A. Bitsch, G. Eisenbrand, A. Elhajouji, B. Epe, M. Habermeyer, B. Kaina, H.J. Martus, S. Pfuhler, C. Schmitz, A. Sutter, A.D. Thomas, C. Ziemann, and R. Froetschl Assessment of mechanisms driving non-linear dose-response relationships in genotoxicity testing, Mutation research Rev. Mut. Res. 763 2015 181 201
107. K. Becker, A.D. Thomas, and B. Kaina Does increase in DNA repair allow "tolerance-to-insult" in chemical carcinogenesis? Skin tumor experiments with MGMT-overexpressing mice Environ. Mol. Mutagen. 55 2014 145 150
108. K. Vahakangas, H. Autrup, and C.C. Harris Interindividual variation in carcinogen metabolism, DNA damage and DNA repair IARC Sci. Publ. 1984 85 98
109. C.C. Harris, B.F. Trump, R. Grafstrom, and H. Autrup Differences in metabolism of chemical carcinogens in cultured human epithelial tissues and cells J. Cell. Biochem. 18 1982 285 294
110. K.S. Park, S.H. Jeon, S.E. Kim, Y.Y. Bahk, S.L. Holmen, B.O. Williams, K.C. Chung, Y.J. Surh, and K.Y. Choi APC inhibits ERK pathway activation and cellular proliferation induced by RAS J. Cell Sci. 119 2006 819 827
111. M. Tanaka, G. Jin, Y. Yamazaki, T. Takahara, M. Takuwa, and T. Nakamura Identification of candidate cooperative genes of the Apc mutation in transformation of the colon epithelial cell by retroviral insertional mutagenesis Cancer Sci. 99 2008 979 985
112. J.L. Pope, R. Ahmad, A.A. Bhat, M.K. Washington, A.B. Singh, and P. Dhawan Claudin-1 overexpression in intestinal epithelial cells enhances susceptibility to adenamatous polyposis coli-mediated colon tumorigenesis Mol. Cancer 13 2014 167
113. M.P. Moyer, and J.B. Aust Human colon cells: culture and in vitro transformation Science 224 1984 1445 1447
114. L.S. Nyskohus, A.J. Watson, G.P. Margison, R.K. Le Leu, S.W. Kim, T.J. Lockett, R.J. Head, G.P. Young, and Y. Hu Repair and removal of azoxymethane-induced O6-methylguanine in rat colon by O6-methylguanine DNA methyltransferase and apoptosis Mutat. Res. 758 2013 80 86
115. J.M. Bugni, L.B. Meira, and L.D. Samson Alkylation-induced colon tumorigenesis in mice deficient in the Mgmt and Msh6 proteins Oncogene 28 2009 734 741
116. T. Maltzman, J. Whittington, L. Driggers, J. Stephens, and D. Ahnen AOM-induced mouse colon tumors do not express full-length APC protein Carcinogenesis 18 1997 2435 2439
117. C. De Filippo, G. Caderni, M. Bazzicalupo, C. Briani, A. Giannini, M. Fazi, and P. Dolara Mutations of the Apc gene in experimental colorectal carcinogenesis induced by azoxymethane in F344 rats Br. J. Cancer 77 1998 2148 2151
118. J.E. McCormick, and R.S. McElhinney Nitrosoureas from chemist to physician: classification and recent approaches to drug design Eur. J. Cancer 26 1990 207 221
119. S.G. Chaney, and A. Sancar DNA repair: enzymatic mechanisms and relevance to drug response J. Natl. Cancer Inst. 88 1996 1346 1360
120. M.L. Fishel, Y. He, M.L. Smith, and M.R. Kelley Manipulation of base excision repair to sensitize ovarian cancer cells to alkylating agent temozolomide Clin. Cancer Res. 13 2007 260 267
121. B.J. Denny, R.T. Wheelhouse, M.F. Stevens, L.L. Tsang, and J.A. Slack NMR and molecular modeling investigation of the mechanism of activation of the antitumor drug temozolomide and its interaction with DNA Biochemistry 33 1994 9045 9051
122. N. Mutter, and R. Stupp Temozolomide: a milestone in neuro-oncology and beyond? Expert. Rev. Anticancer. Ther. 6 2006 1187 1204
123. B. Kaina, M. Christmann, S. Naumann, and W.P. Roos MGMT: key node in the battle against genotoxicity, carcinogenicity and apoptosis induced by alkylating agents DNA Repair 6 2007 1079 1099
124. G.P. Margison, M.F. Santibanez Koref, and A.C. Povey Mechanisms of carcinogenicity/chemotherapy by O6-methylguanine Mutagenesis 17 2002 483 487
125. S.L. Gerson MGMT: its role in cancer aetiology and cancer therapeutics Nat. Rev. Cancer 4 2004 296 307
126. P. Modrich, and R. Lahue Mismatch repair in replication fidelity, genetic recombination, and cancer biology Annu. Rev. Biochem. 65 1996 101 133
127. A. Umar, and T.A. Kunkel DNA-replication fidelity, mismatch repair and genome instability in cancer cells Eur. J. Biochem. 238 1996 297 307
128. J. Jiricny Mediating mismatch repair Nat. Genet. 24 2000 6 8
129. D.T. Beranek Distribution of methyl and ethyl adducts following alkylation with monofunctional alkylating agents Mutat. Res. 231 1990 11 30
130. N. Shrivastav, D. Li, and J.M. Essigmann Chemical biology of mutagenesis and DNA repair: cellular responses to DNA alkylation Carcinogenesis 31 2010 59 70
131. L.A. Loeb, and B.D. Preston Mutagenesis by apurinic/apyrimidinic sites Annu. Rev. Genet. 20 1986 201 230
132. J. Laval, S. Boiteux, and T.R. O'Connor Physiological properties and repair of apurinic/apyrimidinic sites and imidazole ring-opened guanines in DNA Mutat. Res. 233 1990 73 79
133. E.W. Vogel, and M.J. Nivard International commission for protection against environmental mutagens and carcinogens. The subtlety of alkylating agents in reactions with biological macromolecules Mutat. Res. 305 1994 13 32
134. W.E. Glaab, K.R. Tindall, and T.R. Skopek Specificity of mutations induced by methyl methanesulfonate in mismatch repair-deficient human cancer cell lines Mutat. Res. 427 1999 67 78
135. B.S. Strauss The 'A rule' of mutagen specificity: a consequence of DNA polymerase bypass of non-instructional lesions? Bioessays 13 1991 79 84
136. M.F. Goodman, H. Cai, L.B. Bloom, and R. Eritja Nucleotide insertion and primer extension at abasic template sites in different sequence contexts Ann. N. Y. Acad. Sci. 726 1994 132 142 (discussion 142-133)
137. L. Liu, Y. Nakatsuru, and S.L. Gerson Base excision repair as a therapeutic target in colon cancer Clin. Cancer Res. 8 2002 2985 2991
138. S. Madhusudan, and M.R. Middleton The emerging role of DNA repair proteins as predictive, prognostic and therapeutic targets in cancer Cancer Treat. Rev. 31 2005 603 617
139. S.H. Wilson, W.A. Beard, D.D. Shock, V.K. Batra, N.A. Cavanaugh, R. Prasad, E.W. Hou, Y. Liu, K. Asagoshi, J.K. Horton, D.F. Stefanick, P.S. Kedar, M.J. Carrozza, A. Masaoka, and M.L. Heacock Base excision repair and design of small molecule inhibitors of human DNA polymerase beta Cell. Mol. Life Sci. 67 2010 3633 3647
140. S. Kosmider, and L. Lipton Adjuvant therapies for colorectal cancer World J. Gastroenterol. 13 2007 3799 3805
141. C.E. Desch, A.B. Benson III, M.R. Somerfield, P.J. Flynn, C. Krause, C.L. Loprinzi, B.D. Minsky, D.G. Pfister, K.S. Virgo, and N.J. Petrelli O, American Society of Clinical, colorectal cancer surveillance: 2005 update of an American Society of Clinical Oncology practice guideline J. Clin. Oncol. 23 2005 8512 8519
142. J. Cassidy, and J.L. Misset Oxaliplatin-related side effects: characteristics and management Semin. Oncol. 29 2002 11 20
143. H.K. Sanoff, W.R. Carpenter, J. Freburger, L. Li, K. Chen, L.L. Zullig, R.M. Goldberg, M.J. Schymura, and D. Schrag Comparison of adverse events during 5-fluorouracil versus 5-fluorouracil/oxaliplatin adjuvant chemotherapy for stage III colon cancer: a population-based analysis Cancer 118 2012 4309 4320
144. C. Sawyers Targeted cancer therapy Nature 432 2004 294 297
145. T. Helleday, E. Petermann, C. Lundin, B. Hodgson, and R.A. Sharma DNA repair pathways as targets for cancer therapy Nat. Rev. Cancer 8 2008 193 204
146. D. Arian, M. Hedayati, H. Zhou, Z. Bilis, K. Chen, T.L. DeWeese, and M.M. Greenberg Irreversible inhibition of DNA polymerase beta by small-molecule mimics of a DNA lesion J. Am. Chem. Soc. 136 2014 3176 3183
147. S. Izuta, M. Saneyoshi, T. Sakurai, M. Suzuki, K. Kojima, and S. Yoshida The 5′-triphosphates of 3′-azido-3′-deoxythymidine and 2′, 3′-dideoxynucleosides inhibit DNA polymerase gamma by different mechanisms Biochem. Biophys. Res. Commun. 179 1991 776 783
148. H.D. Sun, S.X. Qiu, L.Z. Lin, Z.Y. Wang, Z.W. Lin, T. Pengsuparp, J.M. Pezzuto, H.H. Fong, G.A. Cordell, and N.R. Farnsworth Nigranoic acid, a triterpenoid from Schisandra sphaerandra that inhibits HIV-1 reverse transcriptase J. Nat. Prod. 59 1996 525 527
149. K. Ono, H. Nakane, and M. Fukushima Differential inhibition of various deoxyribonucleic and ribonucleic acid polymerases by suramin Eur. J. Biochem. 172 1988 349 353
150. Y. Mizushina, S. Yoshida, A. Matsukage, and K. Sakaguchi The inhibitory action of fatty acids on DNA polymerase beta Biochim. Biophys. Acta 1336 1997 509 521
151. D.A. Sun, S.R. Starck, E.P. Locke, and S.M. Hecht DNA polymerase beta inhibitors from Sandoricum koetjape J. Nat. Prod. 62 1999 1110 1113
152. Y. Mizushina, N. Takahashi, A. Ogawa, K. Tsurugaya, H. Koshino, M. Takemura, S. Yoshida, A. Matsukage, F. Sugawara, and K. Sakaguchi The cyanogenic glucoside, prunasin (D-mandelonitrile-beta-D-glucoside), is a novel inhibitor of DNA polymerase beta J. Biochem. 126 1999 430 436
153. H.Y. Hu, J.K. Horton, M.R. Gryk, R. Prasad, J.M. Naron, D.A. Sun, S.M. Hecht, S.H. Wilson, and G.P. Mullen Identification of small molecule synthetic inhibitors of DNA polymerase beta by NMR chemical shift mapping J. Biol. Chem. 279 2004 39736 39744
154. N. Tanaka, A. Kitamura, Y. Mizushina, F. Sugawara, and K. Sakaguchi Fomitellic acids, triterpenoid inhibitors of eukaryotic DNA polymerases from a basidiomycete, Fomitella fraxinea J. Nat. Prod. 61 1998 193 197
155. A. Ogawa, T. Murate, M. Suzuki, Y. Nimura, and S. Yoshida Lithocholic acid, a putative tumor promoter, inhibits mammalian DNA polymerase beta Jpn. J. Cancer Res. 89 1998 1154 1159
156. W.B. Parker, M. Nishizawa, M.H. Fisher, N. Ye, K.H. Lee, and Y.C. Cheng Characterization of a novel inhibitor of human DNA polymerases: 3,4,5-tri-O-galloylquinic acid Biochem. Pharmacol. 38 1989 3759 3765
157. A. Ogawa, T. Murate, S. Izuta, M. Takemura, K. Furuta, J. Kobayashi, T. Kamikawa, Y. Nimura, and S. Yoshida Sulfated glycoglycerolipid from archaebacterium inhibits eukaryotic DNA polymerase alpha, beta and retroviral reverse transcriptase and affects methyl methanesulfonate cytotoxicity Int. J. Cancer 76 1998 512 518
158. S.S. Li, Z. Gao, X. Feng, and S.M. Hecht Biscoumarin derivatives from Edgeworthia gardneri that inhibit the lyase activity of DNA polymerase beta J. Nat. Prod. 67 2004 1608 1610
159. S.S. Li, Z. Gao, X. Feng, S.H. Jones, and S.M. Hecht Plant sterols as selective DNA polymerase beta lyase inhibitors and potentiators of bleomycin cytotoxicity Bioorg. Med. Chem. 12 2004 4253 4258
160. S. Cao, Z. Gao, S.J. Thomas, S.M. Hecht, J.S. Lazo, and D.G. Kingston Marine sesquiterpenoids that inhibit the lyase activity of DNA polymerase beta J. Nat. Prod. 67 2004 1716 1718
161. V.S. Chaturvedula, B.N. Zhou, Z. Gao, S.J. Thomas, S.M. Hecht, and D.G. Kingston New lupane triterpenoids from Solidago canadensis that inhibit the lyase activity of DNA polymerase beta Bioorg. Med. Chem. 12 2004 6271 6275
162. T. Strittmatter, A. Brockmann, M. Pott, A. Hantusch, T. Brunner, and A. Marx Expanding the scope of human DNA polymerase lambda and beta inhibitors ACS Chem. Biol. 9 2014 282 290
163. T. Strittmatter, B. Bareth, T.A. Immel, T. Huhn, T.U. Mayer, and A. Marx Small molecule inhibitors of human DNA polymerase lambda ACS Chem. Biol. 6 2011 314 319
164. C. Hazan, F. Boudsocq, V. Gervais, O. Saurel, M. Ciais, C. Cazaux, J. Czaplicki, and A. Milon Structural insights on the pamoic acid and the 8 kDa domain of DNA polymerase beta complex: towards the design of higher-affinity inhibitors BMC Struct. Biol. 8 2008 22
165. S. Madhusudan, F. Smart, P. Shrimpton, J.L. Parsons, L. Gardiner, S. Houlbrook, D.C. Talbot, T. Hammonds, P.A. Freemont, M.J. Sternberg, G.L. Dianov, and I.D. Hickson Isolation of a small molecule inhibitor of DNA base excision repair Nucleic Acids Res. 33 2005 4711 4724
166. A.C. Lesko, K.H. Goss, and J.R. Prosperi Exploiting APC function as a novel cancer therapy Curr. Drug Targets 15 2014 90 102
167. M. Brocardo, and B.R. Henderson APC shuttling to the membrane, nucleus and beyond Trends Cell Biol. 18 2008 587 596
168. D. Das, R. Preet, P. Mohapatra, S.R. Satapathy, S. Siddharth, T. Tamir, V. Jain, P.V. Bharatam, M.D. Wyatt, and C.N. Kundu 5-Fluorouracil mediated anti-cancer activity in colon cancer cells is through the induction of adenomatous polyposis coli: implication of the long-patch base excision repair pathway DNA Repair 24 2014 15 25