Microsatellite instability is a predictive factor of the tumor response to irinotecan in patients with advanced colorectal cancer

Cancer Research

Volumn 63, Issue 18, 2003, Pages 5738-5744

  Fallik, David ^a,b   Borrini, Francesco ^a   Boige, Valérie ^a   Viguier, Jérôme ^c   Jacob, Sandrine ^c   Miquel, Catherine ^a   Sabourin, Jean Christophe ^a   Ducreux, Michel ^a   Praz, Françoise ^b,c,d  

^a Department of Medicine ^*  (France)

^b CNRS   (France)

^c Unite Propre de Recherche 2169   (France)

^d INSTITUT GUSTAVE ROUSSY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

IRINOTECAN; PROTEIN BAX; PROTEIN MLH1; PROTEIN MSH2; PROTEIN MSH3; PROTEIN MSH6; TRANSFORMING GROWTH FACTOR BETA;

ADULT; ADVANCED CANCER; AGED; ARTICLE; CHEMOSENSITIVITY; COLORECTAL CANCER; FEMALE; GENE DELETION; GENE INACTIVATION; GENE LOCATION; GENE MUTATION; GENE TARGETING; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; MICROSATELLITE INSTABILITY; MISMATCH REPAIR; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETROSPECTIVE STUDY; TREATMENT OUTCOME;

ADENOSINE TRIPHOSPHATASES; ADULT; AGED; AGED, 80 AND OVER; ANTINEOPLASTIC AGENTS, PHYTOGENIC; BASE PAIR MISMATCH; BCL-2-ASSOCIATED X PROTEIN; CAMPTOTHECIN; CARRIER PROTEINS; COLORECTAL NEOPLASMS; DNA REPAIR; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; EXONS; FEMALE; GENE DELETION; GENOMIC INSTABILITY; HUMANS; MALE; MIDDLE AGED; MUTS HOMOLOG 2 PROTEIN; NEOPLASM PROTEINS; NUCLEAR PROTEINS; PREDICTIVE VALUE OF TESTS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 0141731323     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (67)

1. Moertel, C. G. Chemotherapy for colorectal cancer. N. Engl. J. Med., 330: 1136-1142, 1994.
2. de Gramont, A., Bosset, J. F., Milan, C., Rougier, P., Bouche, O., Etienne, P. L., Morvan, F., Louvet, C., Guillot, T., Francois, E., and Bedenne, L. Randomized trial comparing monthly low-dose leucovorin and fluorouracil bolus with bimonthly high-dose leucovorin and fluorouracil bolus plus continuous infusion for advanced colorectal cancer: a French intergroup study. J. Clin. Oncol., 15: 808-815, 1997.
3. Cunningham, D., Pyrhonen, S., James, R. D., Punt, C. J., Hickish, T. F., Heikkila, R., Johannesen, T. B., Starkhammar, H., Topham, C. A., Awad, L., Jacques, C., and Herait, P. Randomised trial of irinotecan plus supportive care versus supportive care alone after fluorouracil failure for patients with metastatic colorectal cancer. Lancet, 352: 1413-1418, 1998.
4. Rougier, P., Van Cutsem, E., Bajetta, E., Niederle, N., Possinger, K., Labianca, R., Navarro, M., Morant, R., Bleiberg, H., Wils, J., Awad, L., Herait, P., and Jacques, C. Randomised trial of irinotecan versus fluorouracil by continuous infusion after fluorouracil failure in patients with metastatic colorectal cancer. Lancet, 352: 1407-1412, 1998.
5. Hsiang, Y. H., Lihou, M. G., and Liu, L. F. Arrest of replication forks by drug-stabilized topoisomerase I-DNA cleavable complexes as a mechanism of cell killing by camptothecin. Cancer Res., 49: 5077-5082, 1989.
6. Jacob, S., Aguado, M., Fallik, D., and Praz, F. The role of the DNA mismatch repair system in the cytotoxicity of the topoisomerase inhibitors camptothecin and etoposide to human colorectal cancer cells. Cancer Res., 61: 6555-6562, 2001.
7. Buermeyer, A. B., Deschenes, S. M., Baker, S. M., and Liskay, R. M. Mammalian DNA mismatch repair. Annu. Rev. Genet., 33: 533-564, 1999.
8. Kolodner, R. D., and Marsischky, G. T. Eukaryotic DNA mismatch repair. Curr. Opin. Genet. Dev., 9: 89-96, 1999.
9. Jiricny, J., and Nystrom-Lahti, M. Mismatch repair defects in cancer. Curr. Opin. Genet. Dev., 10: 157-161, 2000.
10. Harfe, B. D., and Jinks-Robertson, S. DNA mismatch repair and genetic instability. Annu. Rev. Genet., 34: 359-399, 2000.
11. Duckett, D. R., Bronstein, S. M., Taya, Y., and Modrich, P. hMutSalpha- and hMutLalpha-dependent phosphorylation of p53 in response to DNA methylator damage. Proc. Natl. Acad. Sci. USA, 96: 12384-12388, 1999.
12. Toft, N. J., Winton, D. J., Kelly, J., Howard, L. A., Dekker, M., te Riele, H., Arends, M. J., Wyllie, A. H., Margison, G. P., and Clarke, A. R. Msh2 status modulates both apoptosis and mutation frequency in the murine small intestine. Proc. Natl. Acad. Sci. USA, 96: 3911-3915, 1999.
13. Wu, J., Gu, L., Wang, H., Geacintov, N. E., and Li, G. M. Mismatch repair processing of carcinogen-DNA adducts triggers apoptosis. Mol. Cell. Biol., 19: 8292-8301, 1999.
14. Li, G. M., and Modrich, P. Restoration of mismatch repair to nuclear extracts of H6 colorectal tumor cells by a heterodimer of human MutL homologs. Proc. Natl. Acad. Sci. USA, 92: 1950-1954, 1995.
15. 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., et al. Mutation in the DNA mismatch repair gene homologue hMLH1 is associated with hereditary non-polyposis colon cancer. Nature, 368: 258-261, 1994.
16. 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.
17. Leach, F. S., Nicolaides, N. C., Papadopoulos, N., Liu, B., Jen, J., Parsons, R., Peltomaki, P., Sistonen, P., Aaltonen, L. A., Nystrom-Lahti, M., et al. Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer. Cell, 75: 1215-1225, 1993.
18. Fishel, R. Signaling mismatch repair in cancer. Nat. Med., 5: 1239-1241, 1999.
19. Wheeler, J. M., Bodmer, W. F., and Mortensen, N. J. DNA mismatch repair genes and colorectal cancer. Gut, 47: 148-153, 2000.
20. Jacob, S., and Praz, F. DNA mismatch repair defects: role in colorectal carcinogenesis. Biochimie, 84: 27-47, 2002.
21. Hemminki, A., Peltomaki, P., Mecklin, J. P., Jarvinen, H., Salovaara, R., Nystrom-Lahti, M., de la Chapelle, A., and Aaltonen, L. A. Loss of the wild type MLH1 gene is a feature of hereditary nonpolyposis colorectal cancer. Nat. Genet., 8: 405-410, 1994.
22. Liu, B., Nicolaides, N. C., Markowitz, S., Willson, J. K., Parsons, R. E., Jen, J., Papadopolous, N., Peltomaki, P., de la Chapelle, A., Hamilton, S. R., et al. Mismatch repair gene defects in sporadic colorectal cancers with microsatellite instability. Nat. Genet., 9: 48-55, 1995.
23. 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.
24. Herman, J. G., Umar, A., Polyak, K., Graff, 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.
25. 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., Jr., and O'Connell, M. J. Microsatellite instability in colorectal cancer: different mutator phenotypes and the principal involvement of hMLH1. Cancer Res., 58: 1713-1718, 1998.
26. Duval, A., and Hamelin, R. Mutations at coding repeat sequences in mismatch repair-deficient human cancers: toward a new concept of target genes for instability. Cancer Res., 62: 2447-2454, 2002.
27. Miller, A. B., Hoogstraten, B., Staquet, M., and Winkler, A. Reporting results of cancer treatment. Cancer (Phila.), 47: 207-214, 1981.
28. Malkhosyan, S., Rampino, N., Yamamoto, H., and Perucho, M. Frameshift mutator mutations. Nature (Lond.), 382: 499-500, 1996.
29. Dieumegard, B., Grandjouan, S., Sabourin, J. C., Le Bihan, M. L., Lefrere, I., Bellefqih, Pignon, J. P., Rougier, P., Lasser, P., Benard, J., Couturier, D., and Bressae-de Paillerets, B. Extensive molecular screening for hereditary non-polyposis colorectal cancer. Br. J. Cancer, 82: 871-880, 2000.
30. Parsons, R., Myeroff, L. L., Liu, B., Willson, J. K., Markowitz, S. D., Kinzler, K. W., and Vogelstein, B. Microsatellite instability and mutations of the transforming growth factor beta type II receptor gene in colorectal cancer. Cancer Res., 55: 5548-5550, 1995.
31. 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.
32. Loukola, A., Eklin, K., Laiho, P., Salovaara, R., Kristo, P., Jarvinen, H., Mecklin, J. P., Launonen, V., and Aaltonen, L. A. Microsatellite marker analysis in screening for hereditary nonpolyposis colorectal cancer (HNPCC). Cancer Res., 61: 4545-4549, 2001.
33. Gryfe, R., Kim, H., Hsieh, E. T., Aronson, M. D., Holowaty, E. J., Bull, S. B., Redston, M., and Gallinger, S. Tumor microsatellite instability and clinical outcome in young patients with colorectal cancer. N. Engl. J. Med., 342: 69-77, 2000.
34. Ward, R., Meagher, A., Tomlinson, I., O'Connor, T., Norrie, M., Wu, R., and Hawkins, N. Microsatellite instability and the clinicopathological features of sporadic colorectal cancer. Gut, 48: 821-829, 2001.
35. Fink, D., Aebi, S., and Howell, S. B. The role of DNA mismatch repair in drug resistance. Clin. Cancer Res., 4: 1-6, 1998.
36. Claij, N., and te Riele, H. Microsatellite instability in human cancer: a prognostic marker for chemotherapy? Exp. Cell Res., 246: 1-10, 1999.
37. Branch, P., Aquilina, G., Bignami, M., and Karran, P. Defective mismatch binding and a mutator phenotype in cells tolerant to DNA damage. Nature (Lond.), 362: 652-654, 1993.
38. Fink, D., Nebel, S., Aebi, S., Zheng, H., Cenni, B., Nehme, A., Christen, R. D., and Howell, S. B. The role of DNA mismatch repair in platinum drug resistance. Cancer Res., 56: 4881-4886, 1996.
39. Carethers, J. M., Chauhan, D. P., Fink, D., Nebel, S., Bresalier, R. S., Howell, S. B., and Boland, C. R. Mismatch repair proficiency and in vitro response to 5-fluorouracil. Gastroenterology, 117: 123-131, 1999.
40. Meyers, M., Wagner, M. W., Hwang, H. S., Kinsella, T. J., and Boothman, D. A. Role of the hMLH1 DNA mismatch repair protein in fluoropyrimidine-mediated cell death and cell cycle responses. Cancer Res., 61: 5193-5201, 2001.
41. Buyse, M., Piedbois, Y., Piedbois, P., and Gray, R. Tumour site, sex, and survival in colorectal cancer. Lancet, 356: 858, 2000.
42. Elsaleh, H., Joseph, D., Grieu, F., Zeps, N., Spry, N., and Iacopetta, B. Association of tumour site and sex with survival benefit from adjuvant chemotherapy in colorectal cancer. Lancet, 355: 1745-1750, 2000.
43. Bras-Goncalves, R. A., Rosty, C., Laurent-Puig, P., Soulie, P., Dutrillaux, B., and Poupon, M. F. Sensitivity to CPT-11 of xenografted human colorectal cancers as a function of microsatellite instability and p53 status. Br. J. Cancer, 82: 913-923, 2000.
44. Fallik, D., Sabourin, J. C., Borrini, F., Jacob, S., Boige, V., Praz, F., and Ducreux, M. Responsivness of metastatic colorectal cancers to chemotherapy with CPT11 (irinotecan): possible role of the DNA mismatch repair system. Gastroenterol. Clin. Biol., 24: 917-922, 2000.
45. Charbonnier, F., Olschwang, S., Wang, Q., Boisson, C., Martin, C., Buisine, M. P., Puisieux, A., and Frebourg, T. MSH2 in contrast to MLH1 and MSH6 is frequently inactivated by exonic and promoter rearrangements in hereditary nonpolyposis colorectal cancer. Cancer Res., 62: 848-853, 2002.
46. Wijnen, J., van der Klift, H., Vasen, H., Khan, P. M., Menko, F., Tops, C., Meijers Heijboer, H., Lindhout, D., Moller, P., and Fodde, R. MSH2 genomic deletions are a frequent cause of HNPCC. Nat. Genet., 20: 326-328, 1998.
47. Ruszkiewicz, A., Bennett, G., Moore, J., Manavis, J., Rudzki, B., Shen, L., and Suthers, G. Correlation of mismatch repair genes immunohistochemistry and microsatellite instability status in HNPCC-associated tumours. Pathology, 34: 541-547, 2002.
48. 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.
49. Plumb, J. A., Strathdee, G., Sludden, J., Kaye, S. B., and Brown, R. Reversal of drug resistance in human tumor xenografts by 2′ -deoxy-5-azacytidine-induced demethylation of the hMLH1 gene promoter. Cancer Res., 60: 6039-6044, 2000.
50. Hoang, J. M., Cottu, P. H., Thuille, B., Salmon, R. J., Thomas, G., and Hamelin, R. BAT-26, an indicator of the replication error phenotype in colorectal cancers and cell lines. Cancer Res., 57: 300-303, 1997.
51. Zhou, X. P., Hoang, J. M., Li, Y. J., Seruca, R., Carneiro, F., Sobrinho-Simoes, M., Lothe, R. A., Gleeson, C. M., Russell, S. E., Muzeau, F., Flejou, J. F., Hoang-Xuan, K., Lidereau, R., Thomas, G., and Hamelin, R. Determination of the replication error phenotype in human tumors without the requirement for matching normal DNA by analysis of mononucleotide repeat microsatellites. Genes Chromosomes Cancer, 21: 101-107, 1998.
52. Akiyama, Y., Sato, H., Yamada, T., Nagasaki, H., Tsuchiya, A., Abe, R., and Yuasa, Y. Germ-line mutation of the hMSH6/GTBP gene in an atypical hereditary nonpolyposis colorectal cancer kindred. Cancer Res., 57: 3920-3923, 1997.
53. Wijnen, J., de Leeuw, W., Vasen, H., van der Klift, H., Moller, P., Stormorken, A., Meijers-Heijboer, H., Lindhout, D., Menko, F., Vossen, S., Moslein, G., Tops, C., Brocker-Vriends, A., Wu, Y., Hofstra, R., Sijmons, R., Cornelisse, C., Morreau, H., and Fodde, R. Familial endometrial cancer in female carriers of MSH6 germline mutations. Nat. Genet., 23: 142-144, 1999.
54. Berney, C. R., Fisher, R. J., Yang, J., Russell, P. J., and Crowe, P. J. Genomic alterations (LOH, MI) on chromosome 17q21-23 and prognosis of sporadic colorectal cancer. Int. J. Cancer, 89: 1-7, 2000.
55. 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.
56. Rosty, C., Chazal, M., Etienne, M. C., Letoublon, C., Bourgeon, A., Delpero, J. R., Pezet, D., Beaune, P., Laurent-Puig, P., and Milano, G. Determination of microsatellite instability, p53 and K-RAS mutations in hepatic metastases from patients with colorectal cancer: relationship with response to 5-fluorouracil and survival. Int. J. Cancer, 95: 162-167, 2001.
57. Markowitz, S., Wang, J., Myeroff, L., Parsons, R., Sun, L., Lutterbaugh, J., Fan, R. S., Zborowska, E., Kinzler, K. W., Vogelstein, B., et al. Inactivation of the type II TGF-beta receptor in colon cancer cells with microsatellite instability. Science, 268: 1336-1338, 1995.
58. 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.
59. Iacopetta, B. J., Welch, J., Soong, R., House, A. K., Zhou, X. P., and Hamelin, R. Mutation of the transforming growth factor-beta type II receptor gene in right-sided colorectal cancer: relationship to clinicopathological features and genetic alterations. J. Pathol., 184: 390-395, 1998.
60. Abdel-Rahman, W. M., Georgiades, I. B., Curtis, L. J., Arends, M. J., and Wyllie, A. H. Role of BAX mutations in mismatch repair-deficient colorectal carcinogenesis. Oncogene, 18: 2139-2142, 1999.
61. Calin, G. A., Gafa, R., Tibiletti, M. G., Herlea, V., Becheanu, G., Cavazzini, L., Barbanti-Brodano, G., Nenci, I., Negrini, M., and Lanza, G. Genetic progression in microsatellite instability high (MSI-H) colon cancers correlates with clinico-pathological parameters: a study of the TGRbetaRII, BAX, hMSH3, hMSH6, IGFIIR and BLM genes. Int. J. Cancer, 89: 230-235, 2000.
62. Duval, A., Rolland, S., Compoint, A., Tubacher, E., Iacopetta, B., Thomas, G., and Hamelin, R. Evolution of instability at coding and non-coding repeat sequences in human MSI-H colorectal cancers. Hum. Mol. Genet., 10: 513-518, 2001.
63. Simms, L. A., Radford-Smith, G., Biden, K. G., Buttenshaw, R., Cummings, M., Jass, J. R., Young, J., Meltzer, S. J., and Leggett, B. A. Reciprocal relationship between the tumor suppressors p53 and BAX in primary colorectal cancers. Oncogene, 17: 2003-2008, 1998.
64. Ionov, Y., Yamamoto, H., Krajewski, S., Reed, J. C., and Perucho, M. Mutational inactivation of the proapoptotic gene BAX confers selective advantage during tumor clonal evolution. Proc. Natl. Acad. Sci. USA, 97: 10872-10877, 2000.
65. Jansson, A., and Sun, X. F. Bax expression decreases significantly from primary tumor to metastasis in colorectal cancer. J. Clin. Oncol., 20: 811-816, 2002.
66. Giannini, G., Ristori, E., Cerignoli, F., Rinaldi, C., Zani, M., Viel, A., Ottini, L., Crescenzi, M., Martinotti, S., Bignami, M., Frati, L., Screpanti, I., and Gulino, A. Human MRE11 is inactivated in mismatch repair-deficient cancers. EMBO Rep., 3: 248-254, 2002.
67. Kim, N. G., Choi, Y. R., Baek, M. J., Kim, Y. H., Kang, H., Kim, N. K., Min, J. S., and Kim, H. Frameshift mutations at coding mononucleotide repeats of the hRAD50 gene in gastrointestinal carcinomas with microsatellite instability. Cancer Res., 61: 36-38, 2001.