Frequent loss of hMLH1 by promoter hypermethylation leads to microsatellite instability in adenomatous polyps of patients with a single first-degree member affected by colon cancer

Cancer Research

Volumn 63, Issue 4, 2003, Pages 787-792

  Ricciardiello, Luigi ^a   Goel, Ajay ^a   Mantovani, Vilma ^a   Fiorini, Tania ^a   Fossi, Stefania ^a   Chang, Dong K ^a   Lunedei, Veronica ^a   Pozzato, Paolo ^a   Zagari, Rocco M ^a   De Luca, Luca ^a   Fuccio, Lorenzo ^a   Martinelli, Giuseppe N ^a   Roda, Enrico ^a   Boland, C Richard ^a   Bazzoli, Franco ^a,b,c  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; PROTEIN BAX; PROTEIN MBD4; PROTEIN MLH1; PROTEIN MSH6; UNCLASSIFIED DRUG;

ADENOMATOUS POLYP; ADULT; AGED; ANAMNESIS; ARTICLE; CANCER RISK; COLORECTAL CANCER; CONTROLLED STUDY; FAMILY HISTORY; FEMALE; FRAMESHIFT MUTATION; GENE MUTATION; HETEROZYGOSITY LOSS; HIGH RISK POPULATION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; ITALY; MAJOR CLINICAL STUDY; MALE; METHYLATION; MICROSATELLITE INSTABILITY; MISMATCH REPAIR; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RELATIVE; RISK FACTOR;

ADENOMATOUS POLYPOSIS COLI; ADULT; AGED; AGED, 80 AND OVER; CARRIER PROTEINS; COLORECTAL NEOPLASMS; DNA METHYLATION; DNA-BINDING PROTEINS; FEMALE; FRAMESHIFT MUTATION; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MALE; MICROSATELLITE REPEATS; MIDDLE AGED; MUTS HOMOLOG 2 PROTEIN; NEOPLASM PROTEINS; NUCLEAR PROTEINS; PROMOTER REGIONS (GENETICS); PROTO-ONCOGENE PROTEINS;

EID: 0037442753     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (43)

1. Burt, R. W. Impact of family history on screening and surveillance. Gastrointest. Endosc., 49: S41-S44, 1999.
2. Ahsan, H., Neugut, A. I., Garbowski, G. C., Jacobson, J. S., Forde, K. A., Treat, M. R., and Waye, J. D. Family history of colorectal adenomatous polyps and increased risk for colorectal cancer. Ann. Intern. Med., 128: 900-905, 1998.
3. Bazzoli, F., Fossi, S., Sottili, S., Pozzato, P., Zagari, R. M., Morelli, M. C., Taroni, F., and Roda, E. The risk of adenomatous polyps in asymptomatic first-degree relatives of persons with colon cancer. Gastroenterology, 109: 783-788, 1995.
4. Fossi, S., Bazzoli, F., Ricciardiello, L., Nicolini, G., Zagari, R. M., Pozzato, P., Palli, D., and Roda, E. Incidence and recurrence rates of colorectal adenomas in first-degree asymptomatic relatives of patients with colon cancer. Am. J. Gastroenterol., 96: 1601-1604, 2001.
5. Fearon, E. R., and Vogelstein, B. A genetic model for colorectal tumorigenesis. Cell, 61: 759-767, 1990.
6. Powell, S. M., Zilz, N., Beazer-Barclay, Y., Bryan, T. M., Hamilton, S. R., Thibodeau, S. N., Vogelstein, B., and Kinzler, K. W. APC mutations occur early during colorectal tumorigenesis. Nature (Lond.), 359: 235-237, 1992.
7. Huang, J., Papadopoulos, N., McKinley, A. J., Farrington, S. M., Curtis, L. J., Wyllie, A. H., Zheng, S., Willson, J. K., Markowitz, S. D., Morin, P., Kinzler, K. W., Vogelstein, B., and Dunlop, M. G. APC mutations in colorectal tumors with mismatch repair deficiency. Proc. Natl. Acad. Sci. USA, 93: 9049-9054, 1996.
8. Boland, C. R., and Ricciardiello, L. How many mutations does it take to make a tumor? [comment]. Proc. Natl. Acad Sci. USA, 96: 14675-14677, 1999.
9. Lengauer, C., Kinzler, K. W., and Vogelstein, B. Genetic instability in colorectal cancers. Nature (Lond.), 386: 623-627, 1997.
10. Loeb, L. A. Mutator phenotype may be required for multistage carcinogenesis. Cancer Res., 51: 3075-3079, 1991.
11. Ionov, Y., Peinado, M. A., Malkhosyan, S., Shibata, D., and Perucho, M. Ubiquitous somatic mutations in simple repeated sequences reveal a new mechanism for colonic carcinogenesis. Nature (Lond.), 363: 558-561, 1993.
12. Fishel, R., and Kolodner, R. D. Identification of mismatch repair genes and their role in the development of cancer. Curr. Opin. Genet. Dev., 5: 382-395, 1995.
13. Herman, J. G., Umar, A., Polyak, K., Graft, J. R., Ahuja, N., Issa, J. P., Markowitz, S., Willson, J. K., Hamilton, S. R., Kinzler, K. W., Kane, M. F., Kolodner, R. D., Vogelstein, B., Kunkel, T. A., and Baylin, S. B. Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc. Natl. Acad. Sci. USA, 95: 6870-6875, 1998.
14. Kinzler, K. W., and Vogelstein, B. Lessons from hereditary colorectal cancer. Cell, 87: 159-170, 1996.
15. Marra, G., and Boland, C. R. Hereditary nonpolyposis colorectal cancer: the syndrome, the genes, and historical perspectives. J. Natl. Cancer Inst. (Bethesda), 87: 1114-1125, 1995.
16. Thibodeau, S. N., Bren, G., and Schaid, D. Microsatellite instability in cancer of the proximal colon. Science (Wash. DC), 260: 816-819, 1993.
17. Lindblom, A. Different mechanisms in the tumorigenesis of proximal and distal colon cancers. Curr. Opin. Oncol., 13: 63-69, 2001.
18. Yashiro, M., Carethers, J. M., Laghi, L., Saito, K., Slezak, P., Jaramillo, E., Rubio, C., Koizumi, K., Hirakawa, K., and Boland, C. R. Genetic pathways in the evolution of morphologically distinct colorectal neoplasms. Cancer Res., 61: 2676-2683, 2001.
19. Boland, C. R., Thibodeau, S. N., Hamilton, S. R., Sidransky, D., Eshleman, J. R., Burt, R. W., Meltzer, S. J., Rodriguez-Bigas, M. A., Fodde, R., Ranzani, G. N., and Srivastava, S. A National Cancer Institute Workshop on microsatellite instability for cancer detection and familial predisposition: development of international criteria for the determination of microsatellite instability in colorectal cancer. Cancer Res., 58: 5248-5257, 1998.
20. Rampino, N., Yamamoto, H., Ionov, Y., Li, Y., Sawai, H., Reed, J. C., and Perucho, M. Somatic frameshift mutations in the BAX gene in colon cancers of the microsatellite mutator phenotype. Science (Wash. DC), 275: 967-969, 1997.
21. Riccio, A., Aaltonen, L. A., Godwin, A. K., Loukola, A., Percesepe, A., Salovaara, R., Masciullo, V., Genuardi, M., Paravatou-Petsotas, M., Bassi, D. E., Ruggeri, B. A., Klein-Szanto, A. J., Testa, J. R., Neri, G., and Bellacosa, A. The DNA repair gene MBD4 (MED1) is mutated in human carcinomas with microsatellite instability. Nat. Genet., 23: 266-268, 1999.
22. Yamamoto, H., Sawai, H., Weber, T. K., Rodriguez-Bigas, M. A., and Perucho, M. Somatic frameshift mutations in DNA mismatch repair and proapoptosis genes in hereditary nonpolyposis colorectal cancer. Cancer Res., 58: 997-1003, 1998.
23. Grady, W. M., Rajput, A., Lutterbaugh, J. D., and Markowitz, S. D. Detection of aberrantly methylated hMLH1 promoter DNA in the serum of patients with microsatellite unstable colon cancer. Cancer Res., 61: 900-902, 2001.
24. Samowitz, W. S., and Slattery, M. L. Transforming growth factor-β receptor type 2 mutations and microsatellite instability in sporadic colorectal adenomas and carcinomas. Am. J. Pathol., 151: 33-35, 1997.
25. Aaltonen, L. A., Peltomaki, P., Mecklin, J. P., Jarvinen, H., Jass, J. R., Green, J. S., Lynch, H. T., Watson, P., Tallqvist, G., and Juhola, M. Replication errors in benign and malignant tumors from hereditary nonpolyposis colorectal cancer patients. Cancer Res., 54: 1645-1648, 1994.
26. Grady, W. M., Rajput, A., Myeroff, L., Liu, D. F., Kwon, K., Willis, J., and Markowitz, S. Mutation of the type 11 transforming growth factor β receptor is coincident with the transformation of human colon adenomas to malignant carcinomas. Cancer Res., 58: 3101-3104, 1998.
27. Young, J., Searle, J., Buttenshaw, R., Thomas, L., Ward, M., Chenevix-Trench, G., and Leggett, B. An Alu VpA marker on chromosome I demonstrates that replication errors manifest at the adenoma-carcinoma transition in sporadic colorectal tumors. Genes Chromosomes Cancer, 12: 251-254, 1995.
28. Sasaki, S., Masaki, T., Umetani, N., Shinozaki, M., Yokoyama, T., Ono, M., Nagawa, H., and Muto, T. Microsatellite instability is associated with the macroscopic configuration of neoplasms in patients with multiple colorectal adenomas. Jpn. J. Clin. Oncol., 28: 427-430, 1998.
29. Pedroni, M., Sala, E., Scarselli, A., Borghi, F., Menigatti, M., Benatti, P., Percesepe, A., Rossi, G., Foroni, M., Losi, L., Di Gregorio, C., De Pol, A., Nascimbeni, R., Di Betta, E., Salerni, B., de Leon, M. P., and Roncucci, L. Microsatellite instability and mismatch-repair protein expression in hereditary and sporadic colorectal carcinogenesis. Cancer Res., 61: 896-899, 2001.
30. Loukola, A., Salovaara, R., Kristo, P., Moisio, A. L., Kaariainen, H., Ahtola, H., Eskelinen, M., Harkonen, N., Julkunen, R., Kangas, E., Ojala, S., Tulikoura, J., Valkamo, E., Jarvinen, H., Mecklin, J. P., de la Chapelle, A., and Aaltonen, L. A. Microsatellite instability in adenomas as a marker for hereditary nonpolyposis colorectal cancer. Am. J. Pathol., 155: 1849-1853, 1999.
31. Samowitz, W. S., Slattery, M. L., Potter, J. D., and Leppert, M. F. BAT-26 and BAT-40 instability in colorectal adenomas and carcinomas and germline polymorphisms. Am. J. Pathol., 154: 1637-1641, 1999.
32. Marra, G., and Boland, C. R. DNA repair and colorectal cancer. Gastroenterol. Clin. N. Am., 25: 755-772, 1996.
33. Edelmann, W., Yang, K., Umar, A., Heyer, J., Lau, K., Fan, K., Liedtke, W., Cohen, P. E., Kane, M. F., Lipford, J. R., Yu, N., Crouse, G. F., Pollard, J. W., Kunkel, T., Lipkin, M., Kolodner, R., and Kucherlapati, R. Mutation in the mismatch repair gene Msh6 causes cancer susceptibility. Cell, 91: 467-477, 1997.
34. Wu, Y., Berends, M. J., Sijmons, R. H., Mensink, R. G., Verlind, E., Kooi, K. A., van der Sluis, T., Kempinga, C., van dDer Zee, A. G., Hollema, H., Buys, C. H., Kleibeuker, J. H., and Hofstra, R. M. A role for MLH3 in hereditary nonpolyposis colorectal cancer. Nat. Genet., 29: 137-138, 2001.
35. Kane, M. F., Loda, M., Gaida, G. M., Lipman, J., Mishra, R., Goldman, H., Jessup, J. M., and Kolodner, R. Methylation of the hMLH1 promoter correlates with lack of expression of hMLH1 in sporadic colon tumors and mismatch repair-defective human tumor cell lines. Cancer Res., 57: 808-811, 1997.
36. Miyakura, Y., Sugano, K., Konishi, F., Ichikawa, A., Maekawa, M., Shitoh, K., Igarashi, S., Kotake, K., Koyama, Y., and Nagai, H. Extensive methylation of hMLH1 promoter region predominates in proximal colon cancer with microsatellite instability. Gastroenterology, 121: 1300-1309, 2001.
37. Esteller, M., Corn, P. G., Baylin, S. B., and Herman, J. G. A gene hypermethylation profile of human cancer. Cancer Res., 61: 3225-3229, 2001.
38. Toyota, M., Ohe-Toyota, M., Ahuja, N., and Issa, J. P. Distinct genetic profiles in colorectal tumors with or without the CpG island methylator phenotype. Proc. Natl. Acad. Sci. USA, 97: 710-715, 2000.
39. Toyota, M., Ahuja, N., Ohe-Toyota, M., Herman, J. G., Baylin, S. B., and Issa, J. P. CpG island methylator phenotype in colorectal cancer. Proc. Natl. Acad. Sci. USA, 96: 8681-8686, 1999.
40. Goel, A., Arnold, C. N., and Boland, C. R. Multistep progression of colorectal cancer in the setting of microsatellite instability: new details and novel insights. Gastroenterology, 121: 1497-1502, 2001.
41. Sugimura, T., and Ushijima, T. Genetic and epigenetic alterations in carcinogenesis. Mutat. Res., 462: 235-246, 2000.
42. Kim, D. H., Nelson, H. H., Wiencke, J. K., Zheng, S., Christiani, D. C., Wain, J. C., Mark, E. J., and Kelsey, K. T. p16(INK4a) and histology-specific methylation of CpG islands by exposure to tobacco smoke in non-small cell lung cancer. Cancer Res., 61: 3419-3424, 2001.
43. Palli, D., Fossi, S., and Bazzoli, F. Colonoscopic screening of first-degree relatives of patients with colorectal cancer. Gastroenterology, 117, 747, 1999.