hMLH1 promoter methylation and lack of hMLH1 expression in sporadic gastric carcinomas with high-frequency microsatellite instability

Cancer Research

Volumn 59, Issue 1, 1999, Pages 159-164

  Leung, Suet Yi ^a   Yuen, Siu Tsan ^b   Chung, Lap Ping ^b   Chu, Kent Man ^b   Chan, Annie S Y ^b   Ho, Joana C I ^b  

^a QUEEN MARY HOSPITAL   (Hong Kong)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CARCINOGENESIS; CLINICAL ARTICLE; DNA REPAIR; GENE EXPRESSION; GENE MUTATION; HUMAN; IMMUNOHISTOCHEMISTRY; MICROSATELLITE INSTABILITY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN METHYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STOMACH CARCINOMA;

CARCINOMA; CARRIER PROTEINS; DNA METHYLATION; DNA REPAIR; DNA, SATELLITE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MUTATION; NEOPLASM PROTEINS; NUCLEAR PROTEINS; PROMOTER REGIONS (GENETICS); STOMACH NEOPLASMS;

EID: 0001119305     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (53)

1. Han, H. J., Yanagisawa, A., Kato, Y., Park, J. G., and Nakamura, Y. Genetic instability in pancreatic cancer and poorly differentiated type of gastric cancer. Cancer Res., 53: 5087-5089, 1993.
2. Strickler, J. G., Zheng, J., Shu. Q., Burgart, L. J., Alberts, S. R., and Shibata, D p53 mutations and microsatellite instability in sporadic gastric cancer: when guardians fail. Cancer Res., 54: 4750-4755, 1994.
3. Chong, J. M., Fukayama, M., Hayashi, Y., Takizawa, T., Koike, M., Konishi, M., Kikuchi Yanoshita, R., and Miyaki, M. Microsatellite instability in the progression of gastric carcinoma. Cancer Res., 54: 4595-4597, 1994.
4. dos Santos, N. R., Seruca, R., Constancia, M., Seixas, M., and Sobrinho Simoes, M. Microsatellite instability at multiple loci in gastric carcinoma: clinicopathologic implications and prognosis. Gastroenterology, 110: 38-44, 1996.
5. Chung, Y. J., Song, J. M., Lee, J. Y., Jung, Y. T., Seo, E. J., Choi, S. W., and Rhyu, M. G. Microsatellite instability-associated mutations associate preferentially with the intestinal type of primary gastric carcinomas in a high-risk population. Cancer Res., 56: 4662-4665, 1996.
6. Ottini, L., Palli, D., Falchetti, M., D'Amico, C., Amorosi, A., Saieva, C., Calzolari, A., Cimoli, F., Tatarelli, C., Marchis, L. D., Masala, G., Mariani-Costantini, R., and Cama, A. Microsatellite instability in gastric cancer is associated with tumor location and family history in a high-risk population from Tuscany. Cancer Res., 57: 4523-4529, 1997.
7. Hayden, J. D., Cawkwell, L., Quirke, P., Dixon, M. F., Goldstone, A. R., Sue-Ling, H., Johnston, D., and Martin, I. G. Prognostic significance of microsatellite instability in patients with gastric carcinoma. Eur. J. Cancer, 33: 2342-2346, 1997.
8. Wu, M. S., Lee, C. W., Shun, C. T., Wang, H. P., Lee, W. J., Sheu, J. C., and Lin, J. T. Clinicopathologial significance of altered loci of replication error and microsatellite instability-associated mutations in gastric cancer. Cancer Res., 58: 1494-1497, 1998.
9. Leung, S. Y., Yuen, S. T., Chung, L. P., Chu, K. M., Wong, M. P., Branicki, F. J., and Ho, J. C. I. Microsatellite instability, Epstein-Barr virus, mutation of type II transforming growth factor β receptor and Bax in gastric carcinomas in Hong Kong Chinese. Br. J. Cancer, in press, 1998.
10. Liu, B., Farrington, S. M., Petersen, G. M., Hamilton, S. R., Parsons, R., Papadopoulos, N., Fujiwara, T., Jen, J., Kinzler, K. W., Wyllie, A. H., Vogelstein, B., and Dunlop, M. G. Genetic instability occurs in the majority of young patients with colorectal cancer. Nat. Med., 1: 348-352, 1995.
11. Yuen, S. T., Chan, T. L., Leung, S. Y., Ho, J. W. C., Kwan, K., and Chung, L. P. Microsatellite instability and mismatch repair gene mutation in colorectal cancer patients in Hong Kong. Proc. Am. Assoc. Cancer Res., 39: 474, 1998.
12. Fishel, R., Lescoe, M. K., Rao, M. R., Copeland, N. G., Jenkins, N. A., Garber, J., Kane, M., and Kolodner, R. The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer. Cell, 75: 1027-1038, 1993.
13. Liu, B., Parsons, R. E., Hamilton, S. R., Petersen, G. M., Lynch, H. T., Watson, P. Markowitz, S., Willson, J. K., Green, J., de la Chapelle, A., Kinzler, K. W., and Vogelstein, B. hMSH2 mutations in hereditary nonpolyposis colorectal cancer kindreds. Cancer Res., 54: 4590-4594, 1994.
14. Papadopoulos, N., Nicolaides, N. C., Wei, Y. F., Ruben, S. M., Carter, K. C., Rosen, C., Haseltine, W. A., Fleischmann, R. D., Fraser, C. M., Adams, M. D., Venter, J. C., Hamilton, S. R., Petersen, G. M., Watson, P., Lynch, H. T., Peltomaki, P., Mecklin, J. P., de la Chapelle, A., Kinzler, K. W., and Vogelstein, B. Mutation of a mutL homolog in hereditary colon cancer. Science (Washington DC), 263: 1625-1629, 1994.
15. Nicolaides, N. C., Papadopoulos, N., Liu, B., Wei, Y. F., Carter, K. C., Ruben, S. M., Rosen, C. A., Haseltine, W. A., Fleischmann, R. D., Fraser, C. M., Adams, M. D., Venter, J. C., Dunlop, M. G., Hamilton, S. R., Petersen, G. M., de la Chapelle, A., Vogelstein, B., and Kinzler, K. W. Mutations of two PMS homologues in hereditary nonpolyposis colon cancer. Nature (Lond.), 371: 75-80, 1994.
16. Bronner, C. E., Baker, S. M., Morrison, P. T., Warren, G., Smith, L. G., Lescoe, M. K., Kane, M., Earabino, C., Lipford, J., Lindblom, A., Tannergard, P., Bollag, R. J., Godwin, A. R., Ward, D. C., Nordenskjold, M., Fishel, R., Kolodner, R., and Liskay, R. M. Mutation in the DNA mismatch repair gene homologue hMLH1 is associated with hereditary non-polyposis colon cancer. Nature (Lond.), 368: 258-261, 1994.
17. Borresen, A. L., Lothe, R. A., Meling, G. I., Lystad, S., Morrison, P., Lipford, J., Kane, M. F., Rognum, T. O., and Kolodner, R. D. Somatic mutations in the hMSH2 gene in microsatellite unstable colorectal carcinomas. Hum. Mol. Genet., 4: 2065-2072, 1995.
18. Liu, B., Nicolaides, N. C., Markowitz, S., Willson, J. K., Parsons, R. E., Jen, J., Papadopoulos, N., Peltomaki, P., de la Chapelle, A., Hamilton, S. R., Kinzler, K. W., and Vogelstein, B. Mismatch repair gene defects in sporadic colorectal cancers with microsatellite instability. Nat. Genet., 9: 48-55, 1995.
19. Moslein, G., Tester, D. J., Lindor, N. M., Honchel, R., Cunningham, J. M., French, A., Halling, K. C., Schwab, M., Goretzki, P., and Thibodeau, S. N. Microsatellile instability and mutation analysis of HMSH2 and hMLH1 in patients with sporadic, familial and hereditary colorectal cancer. Hum. Mol. Genet., 5: 1245-1252, 1996.
20. Bubb, V. J., Curtis, L. J., Cunningham, C., Dunlop, M. G., Carothers, A. D., Morris, R., White, S., Bird, C. C., and Wyllie, A. H. Microsatellite instability and the role of hMSH2 in sporadic colorectal cancer. Oncogene, 12: 2641-2649, 1996.
21. Thibodeau, S. N., French, A. J., Roche, P. C. Cunningham, J. M., Tester, D. J., Lindor, N. M., Moslein, G., Baker, S. M., Liskay, R. M., Burgart, L. J., Honchel, R., and Hailing, K. C. Altered expression of hMSH2 and HMLH1 in tumors with microsatellite instability and genetic alterations in mismatch repair genes. Cancer Res., 56: 4836-4840, 1996.
22. Wu, Y., Nystrom Lahti, M., Osinga, J., Looman, M. W., Peltomaki, P., Aaltonen, L., de la Chapelle, A., Hofstra, R. M., and Buys, C. H. MSH2 and MLH1 mutations in sporadic replication error-positive colorectal carcinoma as assessed by two-dimensional DNA electrophoresis. Genes Chromosomes Cancer, 18: 269-278, 1997.
23. Katabuchi, H., van Rees, B., Lambers, A. R., Ronnett, B. M., Blazes, M. S., Leach, F., Cho, K. R., and Hedrick, L. Mutations in DNA mismatch repair genes are not responsible for microsatellite instability in most sporadic endometrial carcinomas. Cancer Res., 55: 5556-5560, 1995.
24. Kobayashi, K., Matsushima, M., Koi, S., Saito, H., Sagae, S., Kudo, R., and Nakamura, Y. Mutational analysis of mismatch repair genes, HMLH1 and HMSH2, in sporadic endometrial carcinomas with microsatellite instability. Jpn. J. Cancer Res., 87: 141-145, 1996.
25. Kowalski, L. D., Mutch, D. G., Herzog, T. J., Rader, J. S., and Goodfellow, P. J. Mutational analysis of MLH1 and MSH2 in 25 prospectively acquired RER+ endometrial cancers. Genes Chromosomes Cancer, 18: 219-227, 1997.
26. Leach, F. S., Polyak, K., Burrell, M., Johnson, K. A., Hill, D., Dunlop, M. G., Wyllie, A. H., Peltomaki, P., de la Chapelle, A., Hamilton, S. R., Kinzler, K. W., and Vogelstein, B. Expression of the human mismatch repair gene hMSH2 in normal and neoplastic tissues. Cancer Res., 56: 235-240, 1996.
27. Leung, S. Y., Chan, T. L., Chung, L. P., Chan, A. S. Y., Fan, Y. W., Hung, K. N., Kwong, W. K., Ho, J. W. C., and Yuen, S. T. Microsatellite instability and mutation of DNA mismatch repair genes in gliomas. Am. J Pathol., 153: 1181-1188, 1998.
28. Thibodeau, S. N., French, A. J., Cunningham, J. M., Tester, D., Burgart, L. J., Roche, P. C., McDonnell, S. K., Schaid, D. J., Vockley, C. W., Michels, V. V., Farr, G. H., and O'Connell, M. J. Microsatellite instability in colorectal cancer: different mulator phenotypes and the principal involvement of hMLH1. Cancer Res., 58: 1713-1718, 1998.
29. Merlo, A., Herman, J. G., Mao, L., Lee, D. J., Gabrielson, E., Burger, P. C., Baylin, S., and Sidransky, D. 5′ CpG island methylation is associated with transcriptional silencing of the tumour suppressor p16/CDKN2/MTS1 in human cancers. Nat. Med., 1: 686-692, 1995.
30. Herman, J. G., Merlo, A., Mao. L., Lapidus, R. G., Issa, J. P., Davidson, N. E., Sidransky, D., and Baylin, S. B. Inactivation of the CDKN2/p16/MTS1 gene is frequently associated with aberrant DNA methylation in all common human cancers. Cancer Res., 55: 4525-4530, 1995.
31. Gonzalez-Zulueta, M., Bender, C. M., Yang, A. S., Nguyen, T., Beart, R. W., Van Tornout, J. M., and Jones, P. A. Methylation of the 5′ CpG island of the p16/CDKN2 tumor suppressor gene in normal and transformed human tissues correlates with gene silencing. Cancer Res., 55: 4531-4535, 1995.
32. Graff, J. R., Herman, J. G., Lapidus, R. G., Chopra, H., Xu, R., Jarrard, D. F., Isaacs, W. B., Pitha, P. M., Davidson, N. E., and Baylin, S. B. E-cadherin expression is silenced by DNA hypermethylation in human breast and prostate carcinomas. Cancer Res., 55: 5195-5199, 1995.
33. Herman, J. G., Latif, F., Weng, Y., Lerman, M. I., Zbar, B., Liu, S., Samid, D., Duan, D. S., Gnarra, J. R., Linehan, W. M., and Baylin, S. B. Silencing of the VHL tumor-suppressor gene by DNA methylation in renal carcinoma. Proc. Natl. Acad. Sci. USA. 91: 9700-9704, 1994.
34. Baylin, S. B., Herman, J. G., Graff, J. R., Vertino, P. M., and Issa, J. P. Alterations in DNA methylation: a fundamental aspect of neoplasia. Adv. Cancer Res., 72: 141-196, 1998.
35. Kane, M. F., Loda, M., Gaida, G. M., Lipman, J., Mishra, R., Goldman, H., Jessup, J., 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. Herman, J. G., Umar, A., Polyak, K., Graff, J. R., Ahuja, N., Issa, J. J., Markowitz, S , Willson, J. V., 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 coloreclal carcinoma. Proc. Natl. Acad. Sci. USA, 95: 6870-6875, 1998.
37. Veigl, M. L., Kasturi, L., Olechnowicz, J., Ma, A. H., Lutterbaugh, J. D., Periyasamy, S., Li, G. M., Drummond, J., Modrich, P. L., Sedwick, W. D., and Markowitz, S. D. Biallelic inactivation of hMLH1 by epigenetic gene silencing, a novel mechanism causing human MSI cancers. Proc. Natl. Acad. Sci. USA, 95: 8698-8702, 1998.
38. Cunningham, J. M., Christensen, E. R., Tester, D. J., Kim, C. Y., Roche, P. C., Burgart, L. J., and Thibodeau, S. N. Hypermethylation of the hMLH1 promoter in colon cancer with microsatellite instability. Cancer Res., 58: 3455-3460, 1998.
39. Dietmaier, W., Wallinger, S., Bocker, T., Kulimann, F., Fishel, R., and Ruschoff, J. Diagnostic microsatellite instability: definition and correlation with mismatch repair protein expression. Cancer Res., 57: 4749-4756, 1997.
40. Bocker, T., Diermann, J., Friedl, W., Gebert, J., Holinski Feder, E., Karner, H-J., von Knebel Doeberitz, M., Koelble, K., Moeslein, G., Schackert, H. K., Wirtz, H. C., Fishel, R., and Ruschoff, J. Microsatellite instability analysis: a multicenter study for reliability and quality control. Cancer Res., 57: 4739-4743, 1997.
41. Cheung, M. N., Wong, M. P., Yuen, S. T., Leung, S. Y., and Chung, L. P. Tissue-specific expression pattern of vascular endothelial growth factor isoforms changes during malignant transformation. Hum. Pathol., 29: 910-914, 1998.
42. Fink, D., Nebel, S., Aebi, S., Zheng, H., Kim, H. K., Christen, R. D., and Howell, S. B. Expression of the DNA mismatch repair proteins hMLH1 and hPMS2 in normal human tissues. Br. J. Cancer, 76: 890-893, 1997.
43. Wilson, T. M., Ewel, A., Duguid, J. R., Eble, J. N., Lescoe, M. K., Fishel, R., and Kelley, M. Differenlial cellular expression of the human MSH2 repair enzyme in small and large intestine. Cancer Res., 55: 5146-5150, 1995.
44. Semba, S., Yokozaki, H., Yasui, W., and Tahara, E. Frequent microsatellite instability and loss of heterozygosity in the region including BRCA1 (17q21) in young patients with gastric cancer. Int. J. Oncol., 12: 1245-1251, 1998.
45. Hatta, Y., Wada, M., Takeuchi, S., Tasaka, T., Lee, E., Lee, Y. Y., Kim, B. K., Bang, Y. J., Lee, S., Yamada, Y., Tomonaga, M., Wilczynski, S. P., Said, J. W., and Koeffler, H. P. Mutational analysis of the hMSH2 gene in a wide variety of tumors. Int. J. Oncol., 11: 465-469, 1997.
46. 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.
47. Samowitz, W. S., and Slattery, M. L. Microsatellite instability in colorectal adenomas. Gastroenterology, 112: 1515-1519, 1997.
48. Young, J., Searle, J., Buttenshaw, R., Thomas, L., Ward, M., Chenevix, T., and Leggett, B. An Alu VpA marker on chromosome 1 demonstrates that replication errors manifest at the adenoma-carcinoma transition in sporadic colorectal tumors. Genes Chromosomes Cancer, 12: 251-254, 1995.
49. Jacoby, R. F., Marshall, D. J., Kailas, S., Schlack, S., Harms, B., and Love, R. Genetic instability associated with adenoma to carcinoma progression in hereditary nonpolyposis colon cancer. Gastroenterology, 109: 73-82, 1995.
50. Young, J., Leggett, B., Gustafson, C., Ward, M., Searle, J., Thomas, L., Buttenshaw, R., and Chenevix Trench, G. Genomic instability occurs in colorectal carcinomas but not in adenomas. Hum. Mutat., 2: 351-354, 1993.
51. Esteller, M., Levine, R., Baylin, S. B., Hendrick Ellenson L, and Herman, J. G. hMLH1 promoter hypermethylation is associated with the microsatellite instability phenotype in sporadic endometrial carcinomas. Proc. Am. Assoc. Cancer Res., 39: 538, 1998.
52. Ahuja, N., Mohan, A. L., Li. Q., Stolker, J. M., Herman, J. G., Hamilton, S. R., Baylin, S. B., and Issa, J. P. Association between CpG island methylation and microsatellite instability in colorectal cancer. Cancer Res., 57: 3370-3374, 1997
53. Lengauer, C., Kinzler, K. W., and Vogelstein, B. DNA methylation and genetic instability in colorectal cancer cells. Proc. Natl. Acad. Sci. USA, 94: 2545-2550, 1997.