Microsatellite instability in colorectal cancerthe stable evidence

Nature Reviews Clinical Oncology

Volumn 7, Issue 3, 2010, Pages 153-162

  Vilar, Eduardo ^a   Gruber, Stephen B ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; FLUOROPYRIMIDINE; FLUOROURACIL; FOLINIC ACID; IRINOTECAN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1 INHIBITOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; OXALIPLATIN; PROTEIN MSH2; RAPAMYCIN; UNCLASSIFIED DRUG;

CANCER STAGING; CLINICAL EFFECTIVENESS; CLINICAL TRIAL; COLORECTAL CANCER; DRUG EFFICACY; DRUG RESPONSE; DRUG TARGETING; EVIDENCE BASED PRACTICE; FAMILIAL CANCER; GENE AMPLIFICATION; GENE EXPRESSION PROFILING; GENE MUTATION; GENE TARGETING; GENETIC ANALYSIS; GENETIC MARKER; HUMAN; IMMUNOHISTOCHEMISTRY; MICROSATELLITE INSTABILITY; MISMATCH REPAIR; POLYMERASE CHAIN REACTION; PREDICTION; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; RELIABILITY; REVIEW; SYSTEMS BIOLOGY;

COLORECTAL NEOPLASMS; DNA REPAIR; DNA REPAIR ENZYMES; GERM-LINE MUTATION; HUMANS; MICROSATELLITE INSTABILITY;

EID: 77949270273     PISSN: 17594774     EISSN: 17594782     Source Type: Journal    
DOI: 10.1038/nrclinonc.2009.237     Document Type: Review

References (94)

1. Aaltonen, L. A. et al. Clues to the pathogenesis of familial colorectal cancer. Science 260, 812-816 (1993).
2. Ionov, Y., Peinado, M. A., Malkhosyan, S., Shibata, D. & Perucho, M. Ubiquitous somatic mutations in simple repeated sequences reveal a new mechanism for colonic carcinogenesis. Nature 363, 558-561 (1993).
3. Thibodeau, S. N., Bren, G. & Schaid, D. Microsatellite instability in cancer of the proximal colon. Science 260, 816-819 (1993).
4. Aaltonen, L. A. et al. Incidence of hereditary nonpolyposis colorectal cancer and the feasibility of molecular screening for the disease. N. Engl. J. Med. 338, 1481-1487 (1998).
5. Hampel, H. et al. Screening for the Lynch syndrome (hereditary nonpolyposis colorectal cancer). N. Engl. J. Med. 352, 1851-1860 (2005).
6. Hendriks, Y. M. et al. Diagnostic approach and management of Lynch syndrome (hereditary nonpolyposis colorectal carcinoma): a guide for clinicians. CA Cancer J. Clin. 56, 213-225 (2006).
7. Jiricny, J. The multifaceted mismatch-repair system. Nat. Rev. Mol. Cell Biol. 7, 335-346 (2006).
8. Hoeijmakers, J. H. Genome maintenance mechanisms for preventing cancer. Nature 411, 366-374 (2001).
9. Boland, C. R. et al. 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).
10. Pal, T., Permuth-wey, J., Kumar, A. & Sellers, T. A. Systematic review and meta-analysis of ovarian cancers: estimation of microsatellite-high frequency and characterization of mismatch repair deficient tumor histology. Clin. Cancer Res. 14, 6847-6854 (2008).
11. Vogelstein, B. & Kinzler, K. W. in The Genetic Basis of Human Cancer (McGraw-Hill Medical, New York, 2002).
12. Salovaara, R. et al. Population-based molecular detection of hereditary nonpolyposis colorectal cancer. J. Clin. Oncol. 18, 2193-2200 (2000).
13. Ligtenberg, M. J. et al. Heritable somatic methylation and inactivation of MSH2 in families with Lynch syndrome due to deletion of the 3′ exons of TACSTD1. Nat. Genet. 41, 112-117 (2009).
14. Chen, S. et al. Prediction of germline mutations and cancer risk in the Lynch syndrome. JAMA 296, 1479-1487 (2006).
15. Stoffel, E. et al. Calculation of risk of colorectal and endometrial cancer among patients with Lynch syndrome. Gastroenterology 137, 1621-1627 (2009).
16. Herman, J. G. et al. Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc. Natl Acad. Sci. USA 95, 6870-6875 (1998).
17. Gryfe, R. et al. Tumor microsatellite instability and clinical outcome in young patients with colorectal cancer. N. Engl. J. Med. 342, 69-77 (2000).
18. Piñol, V. et al. Accuracy of revised Bethesda guidelines, microsatellite instability, and immunohistochemistry for the identification of patients with hereditary nonpolyposis colorectal cancer. JAMA 293, 1986-1994 (2005).
19. Roth, A. D. et al. Stage-specific prognostic value of molecular markers in colon cancer: Results of the translational study on the PETACC 3-EORTC 40993-SAKK 60-00 trial [abstract]. J. Clin. Oncol. 27, a4002 (2009).
20. Koopman, M. et al. Deficient mismatch repair system in patients with sporadic advanced colorectal cancer. Br. J. Cancer 100, 266-273 (2009).
21. Ashktorab, H. et al. High incidence of microsatellite instability in colorectal cancer from African Americans. Clin. Cancer Res. 9, 1112-1117 (2003).
22. Kumar, K. et al. Distinct BRAF (V600E) and KRAS mutations in high microsatellite instability sporadic colorectal cancer in African Americans. Clin. Cancer Res. 15, 1155-1161 (2009).
23. Soliman, A. S. et al. Contrasting molecular pathology of colorectal carcinoma in Egyptian and western patients. Br. J. Cancer 85, 1037-1046 (2001).
24. Gruber, S. B. New developments in Lynch syndrome (hereditary nonpolyposis colorectal cancer) and mismatch repair gene testing. Gastroenterology 130, 577-587 (2006).
25. Laghi, L., Bianchi, P. & Malesci, A. Differences and evolution of the methods for the assessment of microsatellite instability. Oncogene 27, 6313-6321 (2008).
26. Umar, A. et al. Revised Bethesda Guidelines for hereditary nonpolyposis colorectal cancer (Lynch syndrome) and microsatellite instability. J. Natl Cancer Inst. 96, 261-268 (2004).
27. Vogelstein, B. et al. Allelotype of colorectal carcinomas. Science 244, 207-211 (1989).
28. Fearon, E. R. & Vogelstein, B. A genetic model for colorectal tumorigenesis. Cell 61, 759-767 (1990).
29. Duval, A. & 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).
30. Davies, H. et al. Mutations of the BRAF gene in human cancer. Nature 417, 949-954 (2002).
31. Rajagopalan, H. et al. Tumorigenesis: RAF/RAS oncogenes and mismatch-repair status. Nature 418, 934 (2002).
32. Oliveira, C. et al. BRAF mutations characterize colon but not gastric cancer with mismatch repair deficiency. Oncogene 22, 9192-9196 (2003).
33. Domingo, E. et al. BRAF screening as a low-cost effective strategy for simplifying HNPCC genetic testing. J. Med. Genet. 41, 664-668 (2004).
34. Bessa, X. et al. A prospective, multicenter, population-based study of BRAF mutational analysis for Lynch syndrome screening. Clin. Gastroenterol. Hepatol. 6, 206-214 (2008).
35. Deng, G. et al. BRAF mutation is frequently present in sporadic colorectal cancer with methylated hMLH1, but not in hereditary nonpolyposis colorectal cancer. Clin. Cancer Res. 10, 191-195 (2004).
36. McGivern, A. et al. Promoter hypermethylation frequency and BRAF mutations distinguish hereditary non-polyposis colon cancer from sporadic MSI-H colon cancer. Fam. Cancer 3, 101-107 (2004).
37. Wang, L. et al. BRAF mutations in colon cancer are not likely attributable to defective DNA mismatch repair. Cancer Res. 63, 5209-5212 (2003).
38. Andreyev, H. J., Norman, A. R., Cunningham, D., Oates, J. R. & Clarke, P. A. Kirsten ras mutations in patients with colorectal cancer: the multicenter "RASCAL" study. J. Natl Cancer Inst. 90, 675-684 (1998).
39. Vivanco, I. & Sawyers, C. L. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat. Rev. Cancer 2, 489-501 (2002).
40. Samuels, Y. et al. High frequency of mutations of the PIK3CA gene in human cancers. Science 304, 554 (2004).
41. Barault, L. et al. Mutations in the RAS-MAPK, PI(3)K (phosphatidylinositol-3-OH kinase) signaling network correlate with poor survival in a population-based series of colon cancers. Int. J. Cancer 122, 2255-2259 (2008).
42. Benvenuti, S. et al. PIK3CA cancer mutations display gender and tissue specificity patterns. Hum. Mutat. 29, 284-288 (2008).
43. Frattini, M. et al. Phosphatase protein homologue to tensin expression and phosphatidylinositol-3 phosphate kinase mutations in colorectal cancer. Cancer Res. 65, 11227 (2005).
44. Kato, S. et al. PIK3CA mutation is predictive of poor survival in patients with colorectal cancer. Int. J. Cancer 121, 1771-1778 (2007).
45. Sartore-Bianchi, A. et al. PIK3CA mutations in colorectal cancer are associated with clinical resistance to EGFR-targeted monoclonal antibodies. Cancer Res. 69, 1851-1857 (2009).
46. Ogino, S. et al. PIK3CA mutation is associated with poor prognosis among patients with curatively resected colon cancer. J. Clin. Oncol. 27, 1477-1484 (2009).
47. Abubaker, J. et al. Clinicopathological analysis of colorectal cancers with PIK3CA mutations in Middle Eastern population. Oncogene 27, 3539-3545 (2008).
48. Parsons, D. W. et al. Colorectal cancer: mutations in a signalling pathway. Nature 436, 792 (2005).
49. Goel, A. et al. Frequent inactivation of PTEN by promoter hypermethylation in microsatellite instability-high sporadic colorectal cancers. Cancer Res. 64, 3014-3021 (2004).
50. Banerjea, A. et al. Colorectal cancers with microsatellite instability display mRNA expression signatures characteristic of increased immunogenicity. Mol. Cancer 3, 21 (2004).
51. Koinuma, K. et al. Mutations of BRAF are associated with extensive hMLH1 promoter methylation in sporadic colorectal carcinomas. Int. J. Cancer 108, 237-242 (2004).
52. Vilar, E. et al. Gene expression patterns in mismatch repair-deficient colorectal cancers highlight the potential therapeutic role of inhibitors of the phosphatidylinositol 3-kinase-AKT-mammalian target of rapamycin pathway. Clin. Cancer Res. 15, 2829-2839 (2009).
53. Watanabe, T. et al. Distal colorectal cancers with microsatellite instability (MSI) display distinct gene expression profiles that are different from proximal MSI cancers. Cancer Res. 66, 9804-9808 (2006).
54. Kruhøffer, M. et al. Gene expression signatures for colorectal cancer microsatellite status and HNPCC. Br. J. Cancer 92, 2240-2248 (2005).
55. Giacomini, C. P. et al. A gene expression signature of genetic instability in colon cancer. Cancer Res. 65, 9200-9205 (2005).
56. Michiels, S., Koscielny, S. & Hill, C. Interpretation of microarray data in cancer. Br. J. Cancer 96, 1155-1158 (2007).
57. Cardoso, F. et al. Clinical application of the 70-gene profile: the MINDACT trial. J. Clin. Oncol. 26, 729-735 (2008).
58. Sparano, J. A. & Paik, S. Development of the 21-gene assay and its application in clinical practice and clinical trials. J. Clin. Oncol. 26, 721-728 (2008).
59. Greenson, J. K. et al. Phenotype of microsatellite unstable colorectal carcinomas: well-differentiated and focally mucinous tumors and the absence of dirty necrosis correlate with microsatellite instability. Am. J. Surg. Pathol. 27, 563-570 (2003).
60. Jorissen, R. N. et al. DNA copy-number alterations underlie gene expression differences between microsatellite stable and unstable colorectal cancers. Clin. Cancer Res. 14, 8061-8069 (2008).
61. Poynter, J. N. et al. Associations between smoking, alcohol consumption, and colorectal cancer, overall and by tumor microsatellite instability status. Cancer Epidemiol. Biomarkers Prev. 18, 2745-2750 (2009).
62. Ribic, C. M. et al. Tumor microsatellite-instability status as a predictor of benefit from fluorouracil-based adjuvant chemotherapy for colon cancer. N. Engl. J. Med. 349, 247-257 (2003).
63. Watanabe, T. et al. Molecular predictors of survival after adjuvant chemotherapy for colon cancer. N. Engl. J. Med. 344, 1196-1206 (2001).
64. Popat, S., Hubner, R. & Houlston, R. S. Systematic review of microsatellite instability and colorectal cancer prognosis. J. Clin. Oncol. 23, 609-618 (2005).
65. Carethers, J. M. et al. Mismatch repair proficiency and in vitro response to 5-fluorouracil. Gastroenterology 117, 123-131 (1999).
66. Elsaleh, H. et al. Association of tumour site and sex with survival benefit from adjuvant chemotherapy in colorectal cancer. Lancet 355, 1745-1750 (2000).
67. Hemminki, A., Mecklin, J. P., Järvinen, H., Aaltonen, L. A. & Joensuu, H. Microsatellite instability is a favorable prognostic indicator in patients with colorectal cancer receiving chemotherapy. Gastroenterology 119, 921-928 (2000).
68. Liang, J. T. et al. High-frequency microsatellite instability predicts better chemosensitivity to high-dose 5-fluorouracil plus leucovorin chemotherapy for stage IV sporadic colorectal cancer after palliative bowel resection. Int. J. Cancer 101, 519-525 (2002).
69. Benatti, P. et al. Microsatellite instability and colorectal cancer prognosis. Clin. Cancer Res. 11, 8332-8340 (2005).
70. Jover, R. et al. Mismatch repair status in the prediction of benefit from adjuvant fluorouracil chemotherapy in colorectal cancer. Gut 55, 848-855 (2006).
71. Kim, G. P. et al. Prognostic and predictive roles of high-degree microsatellite instability in colon cancer: a National Cancer Institute-National Surgical Adjuvant Breast and Bowel Project Collaborative Study. J. Clin. Oncol. 25, 767-772 (2007).
72. Lamberti, C. et al. Microsatellite instability did not predict individual survival of unselected patients with colorectal cancer. Int. J. Colorectal Dis. 22, 145-152 (2007).
73. Sargent, D. J. et al. Confirmation of deficient mismatch repair (dMMR) as a predictive marker for lack of benefit from 5-FU based chemotherapy in stage II and III colon cancer (CC): A pooled molecular reanalysis of randomized chemotherapy trials [abstract]. J. Clin. Oncol. 26, a4008 (2008).
74. Des Guetz, G. et al. Does microsatellite instability predict the efficacy of adjuvant chemotherapy in colorectal cancer? A systematic review with meta-analysis. Eur. J. Cancer 45, 1890-1896 (2009).
75. Baddi, L. & Benson, A. III. Adjuvant therapy in stage II colon cancer: current approaches. Oncologist 10, 325-331 (2005).
76. Van Rijnsoever, M., Elsaleh, H., Joseph, D., McCaul, K. & Iacopetta, B. CpG island methylator phenotype is an independent predictor of survival benefit from 5-fluorouracil in stage III colorectal cancer. Clin. Cancer Res. 9, 2898-2903 (2003).
77. Nagasaka, T. et al. Hypermethylation of O6-methylguanine-DNA methyltransferase promoter may predict nonrecurrence after chemotherapy in colorectal cancer cases. Clin. Cancer Res. 9, 5306-5312 (2003).
78. Vilar, E. et al. Microsatellite instability due to hMLH1 deficiency is associated with increased cytotoxicity to irinotecan in human colorectal cancer cell lines. Br. J. Cancer 99, 1607-1612 (2008).
79. Magrini, R. et al. Cellular effects of CPT-11 on colon carcinoma cells: dependence on p53 and hMLH1 status. Int. J. Cancer 101, 23-31 (2002).
80. Jacob, S., Aguado, M., Fallik, D. & 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).
81. Rodriguez, R. et al. Thymidine selectively enhances growth suppressive effects of camptothecin/irinotecan in MSI+ cells and tumors containing a mutation of MRE11. Clin. Cancer Res. 14, 5476-5483 (2008).
82. Pommier, Y. Topoisomerase I inhibitors: camptothecins and beyond. Nat. Rev. Cancer 6, 789-802 (2006).
83. Giannini, G. et al. Mutations of an intronic repeat induce impaired MRE11 expression in primary human cancer with microsatellite instability. Oncogene 23, 2640-2647 (2004).
84. Miquel, C. et al. Frequent alteration of DNA damage signalling and repair pathways in human colorectal cancers with microsatellite instability. Oncogene 26, 5919-5926 (2007).
85. Fallik, D. et al. Microsatellite instability is a predictive factor of the tumor response to irinotecan in patients with advanced colorectal cancer. Cancer Res. 63, 5738-5744 (2003).
86. Bertagnolli, M. M. et al. Microsatellite instability predicts improved response to adjuvant therapy with irinotecan, fluorouracil, and leucovorin in stage III colon cancer: Cancer and Leukemia Group B Protocol 89803. J. Clin. Oncol. 27, 1814-1821 (2009).
87. Tejpar, S. et al. Microsatellite instability (MSI) in stage II and III colon cancer treated with 5FU-LV or 5FU-LV and irinotecan (PETACC 3-EORTC 40993-SAKK 60/00 trial) [abstract]. J. Clin. Oncol. 27, a4001 (2009).
88. Koopman, M. et al. Sequential versus combination chemotherpay with capecitabine, irinotecan, and oxaliplatin in advanced colorectal cancer (CAIRO): a phase III randomised controlled trial. Lancet 370, 135-142 (2007).
89. Des Guetz, G. et al. Microsatellite instability does not predict the efficacy of chemotherapy in metastatic colorectal cancer. A systematic review and meta-analysis. Anticancer Res. 29, 1615-1620 (2009).
90. Swanton, C. & Caldas, C. Molecular classification of solid tumours: towards pathway-driven therapeutics. Br. J. Cancer 100, 1517-1522 (2009).
91. Engstrom, P. F. et al. NCCN Clinical Practice Guideline in Oncology: colon cancer. J. Natl Compr. Canc. Netw. 7, 778-831 (2009).
92. Vilar, E. et al. Preclinical testing of the PARP inhibitor ABT-888 in microsatellite instable colorectal cancer [abstract]. J. Clin. Oncol. 27, a11028 (2009).
93. Farmer, H. et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434, 917-921 (2005).
94. Ropero, S. et al. A truncating mutation of HDAC2 in human cancers confers resistance to histone deacetylase inhibition. Nat. Genet. 38, 566-569 (2006).