Structure/function analysis of the interaction of adenomatous polyposis coli with DNA polymerase β and its implications for base excision repair

Biochemistry

Volumn 46, Issue 49, 2007, Pages 13961-13974

  Balusu, Ramesh ^a   Jaiswal, Aruna S ^a   Armas, Melissa L ^a   Kundu, Chanakya N ^a,c   Bloom, Linda B ^b   Narayan, Satya ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATION; DNA; GENES; NUCLEOTIDES; OXIDATION;

ADENOMATOUS POLYPOSIS COLI (APC); DNA POLYMERASE; INTERACTION SITE; STRAND-DISPLACEMENT;

BIOCHEMISTRY;

DNA DIRECTED DNA POLYMERASE BETA; FLAP ENDONUCLEASE; TETRAHYDROFURAN;

ADENOMATOUS POLYP; ALKYLATION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVITY; EXCISION REPAIR; GENE MUTATION; HUMAN; HUMAN CELL; HYPERTHERMIA; NONHUMAN; OXIDATION; PRIORITY JOURNAL; REDUCTION;

ADENOMATOUS POLYPOSIS COLI PROTEIN; AMINO ACID SEQUENCE; CELL LINE, TUMOR; DNA POLYMERASE BETA; DNA REPAIR; HUMANS; METHYL METHANESULFONATE; MODELS, MOLECULAR; PHOSPHORUS-OXYGEN LYASES;

EID: 37149051581     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701632e     Document Type: Article

References (65)

1. Hoeijmakers, J. H. (2001) Genome maintenance mechanisms for preventing cancer, Nature 411, 366-374.
2. Barnes, D. E., and Lindahl, T. (2004) Repair and genetic consequences of endogenous DNA base damage in mammalian cells, Annu. Rev. Genet. 38, 445-476.
3. Biade, S., Sobol, R. W., Wilson, S. H., and Matsumoto, Y. (1998) Impairment of proliferating cell nuclear antigen-dependent apurinic/apyrimidinic site repair on linear DNA, J. Biol. Chem. 273, 898-902.
4. Klungland, A., and Lindahl, T. (1997) Second pathway for completion of human DNA base excision-repair: reconstitution with purified proteins and requirement for DNase IV (FEN1), EMBO J. 16, 3341-3348.
5. Huffman, J. L., Sundheim, O., and Tainer, J. A. (2005) DNA base damage recognition and removal: new twists and grooves, Mutat. Res. 577, 55-76.
6. Matsumoto, Y., and Kim, K. (1995) Excision of deoxyribose phosphate residues by DNA polymerase β during DNA repair, Science 269, 699-702.
7. Podlutsky, A., Dianova, I. I., Podust, V. N., Bohr, V. A., and Dianov, G. L. (2001) Human DNA polymerase β initiates DNA synthesis during long-patch repair of reduced AP sites in DNA, EMBO J. 20, 1477-1482.
8. Bambara, R. A., Murante, R. S., and Henricksen, L. A. (1997) Enzymes and reactions at the eukaryotic DNA replication fork, J. Biol. Chem. 272, 4647-4650.
9. Lieber, M. R. (1997) The FEN-1 family of structure-specific nucleases in eukaryotic DNA replication, recombination and repair, Bioessays 19, 233-240.
10. Memisoglu, A., and Samson, L. (2000) Base excision repair in yeast and mammals, Mutat. Res. 451, 39-51.
11. Moon, R. T., Kohn, A. D., De, Ferrari, G. V., and Kaykas, A. (2004) WNT and β-catenin signaling: diseases and therapies, Nat. Rev. Genet. 5, 691-701.
12. Bodmer, W. F., Bailey, C. J., Bodmer, J., Bussey, H. J., Ellis, A., Gorman, P., Lucibello, F. C., Murday, V. A., Rider, S. H., Scambler, P., et al. (1987) Localization of the gene for familial adenomatous polyposis on chromosome 5, Nature 328, 614-616.
13. Su, L. K., Kinzler, K. W., Vogelstein, B., Preisinger, A. C., Moser, A. R., Luongo, C., Gould, K. A., and Dove, W. F. (1992) Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene, Science 256, 668-670.
14. Powell, S. M., Zilz, N., Beazer-Barclay, Y., Bryan, T. M., Hamilton, S. R., Thibodeau, S. N., Vogelstein, B., and Kinzler, K. W. (1992) APC mutations occur early during colorectal tumorigenesis, Nature 359, 235-237.
15. Fearnhead, N. S., Britton, M. P., and Bodmer, W. F. (2001) The ABC of APC, Hum. Mol. Genet. 10, 721-733.
16. Fearon, E. R., and Vogelstein, B. (1990) A genetic model for colorectal tumorigenesis, Cell 61, 759-767.
17. Thomas, H. J. (1991) The genetics and molecular biology of colorectal cancer, Curr. Opin. Oncol. 3, 702-710.
18. Kuraguchi, M., Wang, X. P., Bronson, R. T., Rothenberg, R., Ohene-Baah, N. Y., Lund, J. J., Kucherlapati, M., Maas, R. L., and Kucherlapati, R. (2006) Adenomatous polyposis coli (APC) is required for normal development of skin and thymus, PLoS Genet. 2, 1362-1374.
19. Zhang, T., Otevrel, T., Gao, Z., Gao, Z., Ehrlich, S. M., Fields, J. Z., and Boman, B. M. (2001) Evidence that APC regulates survivin expression: a possible mechanism contributing to the stem cell origin of colon cancer, Cancer Res. 61, 8664-8667.
20. Fodde, R. (2003) The multiple functions of tumour suppressors: it's all in APC, Nat. Cell Biol. 5, 190-192.
21. Narayan, S., and Roy, D. (2003) Role of APC and DNA mismatch repair genes in the development of colorectal cancers, Mol. Cancer 2, 41-56.
22. Nathke, I. S. (2004) The adenomatous polyposis coli protein: the Achilles heel of the gut epithelium, Annu. Rev. Cell Dev. Biol. 20, 337-366.
23. Jaiswal, A. S., Balusu, R., Armas, M. L., Kundu, C. N., and Narayan, S. (2006) Mechanism of adenomatous polyposis coli (APC)-mediated blockage of long-patch base excision repair, Biochemistry 45, 15903-15914.
24. Kundu, C. N., Balusu, R., Jaiswal, A. S., Gairola, C. G., and Narayan, S. (2007) Cigarette smoke condensate-induced level of adenomatous polyposis coli blocks long-patch base excision repair in breast epithelial cells, Oncogene 26, 1428-1438.
25. Narayan, S., Jaiswal, A. S., and Balusu, R. (2005) Tumor suppressor APC blocks DNA polymerase β-dependent strand displacement synthesis during long patch but not short patch base excision repair and increases sensitivity to methylmethane sulfonate, J. Biol. Chem. 280, 6942-6949.
26. Beard, W. A., and Wilson, S. H. (2006) Structure and mechanism of DNA polymerase β, Chem. Rev. 106, 361-382.
27. Pelletier, H., Sawaya, M. R., Kumar, A., Wilson, S. H., and Kraut, J. (1994) Structures of ternary complexes of rat DNA polymerase β, a DNA template-primer, and ddCTP, Science 264, 1891-1903.
28. Liu, D., Prasad, R., Wilson, S. H., DeRose, E. F., and Mullen, G. P. (1996) Three-dimensional solution structure of the N-terminal domain of DNA polymerase β and mapping of the ssDNA interaction interface, Biochemistry 35, 6188-6200.
29. Pelletier, H., and Sawaya, M. R. (1996) Characterization of the metal ion binding helix-hairpin-helix motifs in human DNA polymerase β by X-ray structural analysis, Biochemistry 35, 12778-12787.
30. Piersen, C. E., Prasad, R., Wilson, S. H., and Lloyd, R. S. (1996) Evidence for an imino intermediate in the DNA polymerase β deoxyribose phosphate excision reaction, J. Biol. Chem. 271, 17811-17815.
31. Prasad, R., Beard, W. A., Chyan, J. Y., Maciejewski, M. W., Mullen, G. P., and Wilson, S. H. (1998) Functional analysis of the amino-terminal 8-kDa domain of DNA polymerase β as revealed by site-directed mutagenesis. DNA binding and 5′-deoxyribose phosphate lyase activities, J. Biol. Chem. 273, 11121-11126.
32. Deterding, L. J., Prasad, R., Mullen, G. P., Wilson, S. H., and Tomer, K. B. (2000) Mapping of the 5′-2-deoxyribose-5-phosphate lyase active site in DNA polymerase β by mass spectrometry, J. Biol. Chem. 275, 10463-10471.
33. Prasad, R., Batra, V. K., Yang, X. P., Krahn, J. M., Pedersen, L. C., Beard, W. A., and Wilson, S. H. (2005) Structural insight into the DNA polymerase β deoxyribose phosphate lyase mechanism, DNA Repair 4, 1347-1357.
34. Stucki, M., Jonsson, Z. O., and Hubscher, U. (2001) In eukaryotic flap endonuclease 1, the C terminus is essential for substrate binding, J. Biol. Chem. 276, 7843-7849.
35. Mackenney, V. J., Barnes, D. E., and Lindahl, T. (1997) Specific function of DNA ligase I in simian virus 40 DNA replication by human cell-free extracts is mediated by the amino-terminal non-catalytic domain, J. Biol. Chem. 272, 11550-11556.
36. Opresko, P. L., Shiman, R., and Eckert, K. A. (2000) Hydrophobic interactions in the hinge domain of DNA polymerase β are important but not sufficient for maintaining fidelity of DNA synthesis, Biochemistry 39, 11399-11407.
37. Shapiro, D. J., Sharp, P. A., Wahli, W. W., and Keller, M. J. (1988) A high-efficiency HeLa cell nuclear transcription extract, DNA 7, 47-55.
38. Kedar, P. S., Kim, S. J., Robertson, A., Hou, E., Prasad, R., Horton, J. K., and Wilson, S. H. (2002) Direct interaction between mammalian DNA polymerase β and proliferating cell nuclear antigen, J. Biol. Chem. 277, 31115-31123.
39. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera - a visualization system for exploratory research and analysis, J. Comput. Chem. 25, 1605-1612.
40. Batra, V. K., Beard, W. A., Shock, D. D., Krahn, J. M., Pedersen, L. C., and Wilson, S. H. (2006) Magnesium-induced assembly of a complete DNA polymerase catalytic complex, Structure 14, 757-766.
41. Beard, W. A., and Wilson, S. H. (1998) Structural insights into DNA polymerase β fidelity: hold tight if you want it right, Chem. Biol. 5, R7-13.
42. Jaiswal, A. S., Bloom, L. B., and Narayan, S. (2002) Long-patch base excision repair of apurinic/apyrimidinic site DNA is decreased in mouse embryonic fibroblast cell lines treated with plumbagin: involvement of cyclin-dependent kinase inhibitor p21Waf-1/Cip-1, Oncogene 21, 5912-5922.
43. Prasad, R., Dianov, G. L., Bohr, V. A., and Wilson, S. H. (2000) FEN1 stimulation of DNA polymerase β mediates an excision step in mammalian long patch base excision repair, J. Biol. Chem. 275, 4460-4466.
44. Podlutsky, A. J., Dianova, I. I., Wilson, S. H., Bohr, V. A., and Dianov, G. L. (2001) DNA synthesis and dRPase activities of polymerase β are both essential for single-nucleotide patch base excision repair in mammalian cell extracts, Biochemistry 40, 809-813.
45. Liu, Y., Beard, W. A., Shock, D. D., Prasad, R., Hou, E. W., and Wilson, S. H. (2005) DNA polymerase β and flap endonuclease 1 enzymatic specificities sustain DNA synthesis for long patch base excision repair, J. Biol. Chem. 280, 3665-3674.
46. Dianov, G. L., Sleeth, K. M., Dianova, I. I., and Allinson, S. L. (2003) Repair of abasic sites in DNA, Mutat. Res. 531, 157-163.
47. Petermann, E., Ziegler, M., and Oei, S. L. (2003) ATP-dependent selection between single nucleotide and long patch base excision repair, DNA Repair 2, 1101-1114.
48. Harrigan, J. A., Opresko, P. L., von Kobbe, C., Kedar, P. S., Prasad, R., Wilson, S. H., and Bohr, V. A. (2003) The Werner syndrome protein stimulates DNA polymerase β strand displacement synthesis via its helicase activity, J. Biol. Chem. 278, 22686-22695.
49. Harrigan, J. A., Wilson, D. M., 3rd, Prasad, R., Opresko, P. L., Beck, G., May, A., Wilson, S. H., and Bohr, V. A. (2006) The Werner syndrome protein operates in base excision repair and cooperates with DNA polymerase β, Nucleic Acids Res. 34, 745-754.
50. Dantzer, F., de La Rubia, G., Menissier-De Murcia, J., Hostomsky, Z., de Murcia, G., and Schreiber, V. (2000) Base excision repair is impaired in mammalian cells lacking Poly(ADP-ribose) polymerase-1, Biochemistry 39, 7559-7569.
51. Prasad, R., Lavrik, O. I., Kim, S. J., Kedar, P., Yang, X. P., Vande Berg, B. J., and Wilson, S. H. (2001) DNA polymerase β-mediated long patch base excision repair. Poly(ADP-ribose)polymerase-1 stimulates strand displacement DNA synthesis, J. Biol. Chem. 276, 32411-32414.
52. Fortini, P., Pascucci, B., Parlanti, E., Sobol, R. W., Wilson, S. H., and Dogliotti, E. (1998) Different DNA polymerases are involved in the short- and long-patch base excision repair in mammalian cells, Biochemistry 37, 3575-3580.
53. Matsumoto, Y., Kim, K., and Bogenhagen, D. F. (1994) Proliferating cell nuclear antigen-dependent abasic site repair in Xenopus laevis oocytes: an alternative pathway of base excision DNA repair, Mol. Cell Biol. 14, 6187-6197.
54. Zhou, J., Ahn, J., Wilson, S. H., and Prives, C. (2001) A role for p53 in base excision repair, EMBO J. 20, 914-923.
55. DeMott, M. S., Zigman, S., and Bambara, R. A. (1998) Replication protein A stimulates long patch DNA base excision repair, J. Biol. Chem. 273, 27492-27498.
56. Thompson, L. H., and West, M. G. (2000) XRCC1 keeps DNA from getting stranded, Mutat. Res., 459, 1-18.
57. El-Andaloussi, N., Valovka, T., Toueille, M., Steinacher, R., Focke, F., Gehrig, P., Covic, M., Hassa, P. O., Schar, P., Hubscher, U., and Hottiger, M. O. (2006) Arginine methylation regulates DNA polymerase β, Mol. Cell 22, 51-62.
58. Maitra, M., Gudzelak, A., Jr., Li, S. X., Matsumoto, Y., Eckert, K. A., Jager, J., and Sweasy, J. B. (2002) Threonine 79 is a hinge residue that governs the fidelity of DNA polymerase β by helping to position the DNA within the active site, J. Biol. Chem. 277, 35550-35560.
59. Srivastava, D. K., Berg, B. J., Prasad, R., Molina, J. T., Beard, W. A., Tomkinson, A. E., and Wilson, S. H. (1998) Mammalian abasic site base excision repair. Identification of the reaction sequence and rate-determining steps, J. Biol. Chem. 273, 21203-21209.
60. Gomez-Lazaro, M., Fernandez-Gomez, F. J., and Jordan, J. (2004) p53: twenty five years understanding the mechanism of genome protection, J. Physiol. Biochem. 60, 287-307.
61. Narayan, S., and Jaiswal, A. S. (1997) Activation of adenomatous polyposis coli (APC) gene expression by the DNA-alkylating agent N-methyl-N′-nitro-N-nitrosoguanidine requires p53, J. Biol. Chem. 272, 30619-30622.
62. Jaiswal, A. S., and Narayan, S. (2001) p53-dependent transcriptional regulation of the APC promoter in colon cancer cells treated with DNA alkylating agents, J. Biol. Chem. 276, 18193-18199.
63. Jaiswal, A. S., Balusu, R., and Narayan, S. (2006) 7,12- Dimethylbenzanthracene-dependent transcriptional regulation of adenomatous polyposis coli (APC) gene expression in normal breast epithelial cells is mediated by GC-box binding protein Sp3, Carcinogenesis 27, 252-261.
64. Narayan, S., Jaiswal, A. S., Kang, D., Srivastava, P., Das, G. M., and Gairola, C. G. (2004) Cigarette smoke condensate-induced transformation of normal human breast epithelial cells in vitro, Oncogene 23, 5880-5889.
65. Kundu, C. N., Balusu, R., Jaiswal, A. S., and Narayan, S. (2007) Adenomatous polyposis coli-mediated hypersensitivity of mouse embryonic fibroblast cell lines to methylmethane sulfonate treatment: implication of base excision repair pathways, Carcinogenesis 28, 2089-2095.