Adenomatous polyposis coli interacts with flap endonuclease 1 to block its nuclear entry and function

Neoplasia (United States)

Volumn 14, Issue 6, 2012, Pages 495-508

  Jaiswal, Aruna S ^a   Armas, Melissa L ^b   Izumi, Tadahide ^c   Strauss, Phyllis R ^d   Narayan, Satya ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c Dept of Nutrition and Food Science   (United States)

^d NORTHEASTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 FLAP ENDONUCLEASE 1; ALPHA ACTIN; APC PROTEIN; BETA ACTIN; FLAP ENDONUCLEASE; LAMIN B; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; COLON CANCER; CONTROLLED STUDY; DNA REPAIR; EXCISION REPAIR; FAR WESTERN BLOTTING; HETEROCHROMATIN; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SITE DIRECTED MUTAGENESIS; YEAST;

EID: 84865617484     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.12680     Document Type: Article

References (69)

1. Cheng KC and Loeb LA (1997). Genomic stability and instability: a working paradigm. Curr Top Microbiol Immunol 21, 5-18.
2. Houtgraaf JH, Versmissen J, and van der Giessen WJ (2006). A concise review of DNA damage checkpoints and repair in mammalian cells. Cardiovasc Revasc Med 7, 165-172.
3. Lindahl T and Nyberg B (1972). Rate of depurination of native deoxyribonucleic acid. Biochemistry 11, 3610-3618.
4. Doetsch PW and Cunningham RP (1990). The enzymology of apurinic/ apyrimidinic endonucleases. Mutat Res 236, 173-201.
5. Huffman JL, Sundheim O, and Tainer JA (2005). DNA base damage recognition and removal: new twists and grooves. Mutat Res 7, 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. Mitra S, Boldogh I, Izumi T, and Hazra TK (2001). Complexities of the DNA base excision repair pathway for repair of oxidative DNA damage. Environ Mol Mutagen 38, 180-190.
8. Bodmer WF, Bailey CJ, Bodmer J, Bussey HJ, Ellis A, Gorman P, Lucibello FC, Murday VA, Rider SH, Scambler P, et al. (1987). Localization of the gene for familial adenomatous polyposis on chromosome 5. Nature 328, 614-616.
9. Powell SM, Zilz N, Beazer-Barclay Y, Bryan TM, Hamilton SR, Thibodeau SN, Vogelstein B, and Kinzler KW (1992). APC mutations occur early during colorectal tumorigenesis. Nature 359, 235-237.
10. Narayan S and Roy D (2003). Role of APC and DNA mismatch repair genes in the development of colorectal cancers. Mol Cancer 2, 41.
11. Beroud C and Soussi T (1996). APC gene: database of germline and somatic mutations in human tumors and cell lines. Nucleic Acids Res 24, 121-124.
12. Miyoshi Y, Nagase H, Ando H, Horii A, Ichii S, Nakatsuru S, Aoki T, Miki Y, Mori T, and Nakamura Y (1992). Somatic mutations of the APC gene in colorectal tumors: mutation cluster region in the APC gene. Hum Mol Genet 1, 229-233.
13. Morrison EE (2009). The APC-EB1 interaction. Adv Exp Med Biol 656, 41-50.
14. Kinzler KW and Vogelstein B (1996). Lessons from hereditary colorectal cancer. Cell 87, 159-170.
15. Aoki K and Taketo MM (2007). Adenomatous polyposis coli (APC): a multifunctional tumor suppressor gene. J Cell Sci 120, 3327-3335.
16. Rustagi AK (2007). The genetics of hereditary colon cancer. Genes Dev 21, 2525-2538.
17. Brocardo M and Henderson B (2008). APC shuttling to the membrane, nucleus and beyond. Trends Cell Biol 18, 587-596.
18. Zheng L, Dai H, Zhou M, Li M, Singh P, Qiu J, Tsark W, Huang Q, Kernstine K, Zhang X, et al. (2007). Fen1 mutations result in autoimmunity, chronic inflammation and cancers. Nat Med 13, 812-819.
19. Zheng L, Jia J, Finger LD, Guo Z, Zer C, and Shen B (2011). Functional regulation of FEN1 nuclease and its link to cancer. Nucleic Acids Res 39, 781-794.
20. Henneke G, Friedrich-Heineken E, and Hubscher U (2003). Flap endonuclease 1: a novel tumour suppressor protein. Trends Biochem Sci 28, 384-390.
21. Shen B, Singh P, Liu R, Qiu J, Zheng L, Finger LD, and Alas S (2005). Multiple but dissectible functions of FEN-1 nucleases in nucleic acid processing, genome stability and diseases. BioEssays 27, 717-729.
22. Goulian M, Richards SH, Heard CJ, and Bigsby BM (1990). Discontinuous DNA synthesis by purified mammalian proteins. J Biol Chem 265, 18461-18471.
23. Schweitzer JK and Livingston DM (1998). Expansions of CAG repeat tracts are frequent in a yeast mutant defective in Okazaki fragment maturation. Hum Mol Genet 7, 69-74.
24. Xu H, Zheng L, Dai H, Zhou M, Hua Y, and Shen B (2011). Chemical-induced cancer incidence and underlying mechanisms in Fen1 mutant mice. Oncogene 30, 1072-1081.
25. Liu Y, Kao HI, and Bambara RA (2004). Flap endonuclease 1: a central component of DNA metabolism. Annu Rev Biochem 73, 589-615.
26. Shibata Y and Nakamura T (2002). Defective flap endonuclease 1 activity in mammalian cells is associated with impaired DNA repair and prolonged S phase delay. J Biol Chem 277, 746-754.
27. Jaiswal AS, Balusu R, Armas ML, Kundu CN, and Narayan S (2006). Mechanism of adenomatous polyposis coli (APC)-mediated blockage of long-patch base excision repair. Biochemistry 45, 15903-15914.
28. Narayan S, Jaiswal AS, 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.
29. Balusu R, Jaiswal AS, Armas ML, Bloom LB, and Narayan S (2007). Structure/ function analysis of the interaction of adenomatous polyposis coli with DNA polymerase β and its implications for base excision repair. Biochemistry 46, 13961-13974.
30. Jaiswal AS and Narayan S (2008). A novel function of adenomatous polyposis coli (APC) in regulating DNA repair. Cancer Lett 271, 272-280.
31. Shapiro DJ, Sharp PA, Wahli WW, and Keller MJ (1988). A high-efficiency HeLa cell nuclear transcription extract. DNA 7, 47-55.
32. Narayan S and Jaiswal AS (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.
33. Henderson BR (2000). Nuclear-cytoplasmic shuttling of APC regulates β-catenin subcellular localization and turnover. Nat Cell Biol 2, 653-660.
34. Neufeld KL (2009). Nuclear APC. Adv Exp Med Biol 656, 13-29.
35. Jaiswal AS and Narayan S (2011). Assembly of the base excision repair complex on abasic DNA and role of adenomatous polyposis coli on its functional activity. Biochemistry 50, 1901-1909.
36. Kundu CN, Balusu R, Jaiswal AS, Gairola CG, 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.
37. Kundu CN, Balusu R, Jaiswal AS, 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.
38. Smith KJ, Johnson KA, Bryan TM, Hill DE, Markowitz S, Willson JK, Paraskeva C, Petersen GM, Hamilton SR, Vogelstein B, et al. (1993). The APC gene product in normal and tumor cells. Proc Natl Acad Sci USA 90, 2846-2850.
39. Neufeld KL and White RL (1997). Nuclear and cytoplasmic localizations of the adenomatous polyposis coli protein. Proc Natl Acad Sci USA 94, 3034-3039.
40. Galea MA, Eleftheriou A, and Henderson BR (2001). ARM domain-dependent nuclear import of adenomatous polyposis coli protein is stimulated by the B56α subunit of protein phosphatase 2A. J Biol Chem 276, 45833-45839.
41. Su LK, Burrell M, Hill DE, Gyuris J, Brent R, Wiltshire R, Trent J, Vogelstein B, and Kinzler KW (1995). APC binds to the novel protein EB1. Cancer Res 55, 2972-2977.
42. Hecht SS (2002). Tobacco smoke carcinogens and breast cancer. Environ Mol Mutagen 39, 119-126.
43. Russo J, Tahin Q, Lareef MH, Hu YF, and Russo IH (2002). Neoplastic transformation of human breast epithelial cells by estrogens and chemical carcinogens. Environ Mol Mutagen 39, 254-263.
44. Han X and Naeher LP (2006). A review of traffic-related air pollution exposure assessment studies in the developing world. Environ Internat 32, 106-120.
45. Sobol RW and Wilson SH (2001). Mammalian DNA β-polymerase in base excision repair of alkylation damage. Prog Nucleic Acid Res Mol Biol 68, 57-74.
46. Shen B, Nolan JP, Sklar LA, and Park MS (1996). Essential amino acids for substrate binding and catalysis of human flap endonuclease 1. J Biol Chem 271, 9173-9176.
47. Sharma S, Sommers JA, Gary RK, Friedrich-Heineken E, Hubscher U, and Brosh RM Jr (2005). The interaction site of flap endonuclease-1 with WRN helicase suggests a coordination of WRN and PCNA. Nucleic Acids Res 33, 6769-6781.
48. Guo Z, Chavez V, Singh P, Finger LD, Hang H, Hegde ML, and Shen B (2008). Comprehensive mapping of the C-terminus of flap endonuclease-1 reveals distinct interaction sites for five proteins that represent different DNA replication and repair pathways. J Mol Biol 377, 679-690.
49. 181 of 5′-flap endonuclease 1 is a useful target for chemotherapeutic development. Biochemistry 48, 9952-9958.
50. Levine AJ and Lane DP (2010). The p53 Family. Cold Spring Harbor Press, Agency for Science and Technology Research, Singapore, Singapore.
51. Kouzmenko AP, Takeyama K, Kawasaki Y, Akiyama T, and Kato S (2008). Truncation mutations abolish chromatin-associated activities of adenomatous polyposis coli. Oncogene 27, 4888-4899.
52. Ho KY, Kalle WH, Lo TH, Lam WY, and Tang CM (1999). Reduced expression of APC and DCC gene protein in breast cancer. Histopathology 35, 249-256.
53. Jönsson M, Borg A, Nilbert M, and Andersson T (2000). Involvement of adenomatous polyposis coli (APC)/β-catenin signaling in human breast cancer. Eur J Cancer 36, 242-248.
54. Morin PJ (1999). β-Catenin signaling and cancer. BioEssays 21, 1021-1030.
55. Polakis P (2000). Wnt signaling and cancer. Genes Dev 14, 1837-1851.
56. Schlosshauer PW, Brown SA, Eisinger K, Yan Q, Guglielminetti ER, Parsons R, Ellenson LH, and Kitajewski J (2000). APC truncation and increased β-catenin levels in a human breast cancer cell line. Carcinogenesis 21, 1453-1456.
57. Thompson AM, Morris RG, Wallace M, Wyllie AH, Steel CM, and Carter DC (1993). Allele loss from 5q21 (APC/MCC) and 18q21 (DCC) and DCC mRNA expression in breast cancer. Br J Cancer 68, 64-68.
58. Gaspar C, Franken P, Molenaar L, Breukel C, van der Valk M, Smits R, and Fodde R (2009). A targeted constitutive mutation in the APC tumor suppressor gene underlies mammary but not intestinal tumorigenesis. PLoS Genet 5, 1-13.
59. Hattrup CL, Fernandez-Rodriguez J, Schroeder JA, Hansson GC, and Gendler SJ (2004). MUC1 can interact with adenomatous polyposis coli in breast cancer. Biochem Biophys Res Commun 316, 364-369.
60. Kuraguchi M, Ohene-Baah NY, Sonkin D, Bronson RT, and Kucherlapati R (2009). Genetic mechanisms in Apc-mediated mammary tumorigenesis. PLoS Genet 5, 1-14.
61. Moser AR, Luongo C, Gould KA, McNeley MK, Shoemaker AR, and Dove WF (1995). ApcMin: a mouse model for intestinal and mammary tumorigenesis. Eur J Cancer 31A, 1061-1064.
62. Moser AR, Mattes EM, Dove WF, Lindstrom MJ, Haag JD, and Gould MN (1993). ApcMin, a mutation in the murine Apc gene, predisposes to mammary carcinomas and focal alveolar hyperplasias. Proc Natl Acad Sci USA 90, 8977-8981.
63. Kuraguchi M, Edelmann W, Yang K, Lipkin M, Kucherlapati R, and Brown AM (2000). Tumor-associated Apc mutations in Mlh1-/- Apc1638N mice reveal a mutational signature of Mlh1 deficiency. Oncogene 19, 5755-5763.
64. Kuraguchi M, Yang K, Wong E, Avdievich E, Fan K, Kolodner RD, Lipkin M, Brown AM, Kucherlapati R, and Edelmann W (2001). The distinct spectra of tumor-associated Apc mutations in mismatch repair-deficient Apc1638N mice define the roles of MSH3 and MSH6 in DNA repair and intestinal tumorigenesis. Cancer Res 61, 7934-7942.
65. Jaiswal AS 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.
66. Jaiswal AS, Balusu R, and Narayan S (2006). 7,12-Dimethylbenzanthracenedependent 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.
67. Parshad R, Price FM, Bohr VA, Cowans KH, Zujewski JA, and Sanford KK (1996). Deficient DNA repair capacity, a predisposing factor in breast cancer. Br J Cancer 74, 1-5.
68. Singh P, Yang M, Dai H, Yu D, Huang Q, Tan W, Kernstine KH, Lin D, and Shen B (2008). Overexpression and hypomethylation of flap endonuclease 1 gene in breast and other cancers. Mol Cancer Res 6, 1710-1717.
69. Sato M, Girard L, Sekine I, Sunaga N, Ramirez RD, Kamibayashi C, and Minna JD (2003). Increased expression and no mutation of the flap endonuclease (FEN1) gene in human lung cancer. Oncogene 22, 7243-7246.