Microsatellite instability in colorectal cancer: Clinicopathological significance

Polish Journal of Pathology

Volumn 66, Issue 3, 2015, Pages 203-218

  Setaffy, Lisa ^a   Langner, Cord ^a  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

Colorectal cancer; Lynch syndrome; Microsatellite instability; Mismatch repair deficiency; Serrated pathway

Indexed keywords

COLORECTAL TUMOR; GENETICS; HUMAN; MICROSATELLITE INSTABILITY;

COLORECTAL NEOPLASMS; HUMANS; MICROSATELLITE INSTABILITY;

EID: 84944883776     PISSN: 12339687     EISSN: None     Source Type: Journal    
DOI: 10.5114/pjp.2015.54953     Document Type: Review

References (108)

1. Siegel R, Desantis C, Jemal A. Colorectal cancer statistics, 2014. CA Cancer J Clin 2014; 64: 104-117.
2. Malvezzi M, Bertuccio P, Levi F, et al. European cancer mortality predictions for the year 2014. Ann Oncol 2014; 25: 1650-1656.
3. Samadder NJ, Vierkant RA, Tillmans LS, et al. Associations between colorectal cancer molecular markers and pathways with clinicopathologic features in older women. Gastroenterology 2013; 145: 348-356.
4. Leggett B, Whitehall V. Role of the serrated pathway in colorectal cancer pathogenesis. Gastroenterology 2010; 138: 2088-2100.
5. Snover DC. Update on the serrated pathway to colorectal carcinoma. Hum Pathol 2011; 42: 1-10.
6. Jasperson KW, Tuohy TM, Neklason DW, et al. Hereditary and familial colon cancer. Gastroenterology 2010; 138: 2044-2058.
7. Sideris M, Papagrigoriadis S. Molecular biomarkers and classification models in the evaluation of the prognosis of colorectal cancer. Anticancer Res 2014; 34: 2061-2068.
8. Jass JR. Classification of colorectal cancer based on correlation of clinical, morphological and molecular features. Histopathology 2007; 50: 113-130.
9. Pino MS, Chung DC. The chromosomal instability pathway in colon cancer. Gastroenterology 2010; 138: 2059-2072.
10. Bettington M, Walker N, Clouston A, et al. The serrated pathway to colorectal carcinoma: current concepts and challenges. Histopathology 2013; 62: 367-386.
11. Langner C. Serrated and Non-Serrated Precursor Lesions of Colorectal Cancer. Dig Dis 2015; 33: 28-37.
12. Boland CR, Koi M, Chang DK, et al. The biochemical basis of microsatellite instability and abnormal immunohistochemistry and clinical behavior in Lynch syndrome: from bench to bedside. Fam Cancer 2008; 7: 41-52.
13. Bellizzi AM, Frankel WL. Colorectal cancer due to deficiency in DNA mismatch repair function: a review. Adv Anat Pathol 2009; 16: 405-417.
14. Boland CR, Thibodeau SN, Hamilton SR, 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 1998; 58: 5248-5257.
15. Dietmaier W, Wallinger S, Bocker T, et al. Diagnostic microsatellite instability: definition and correlation with mismatch repair expression. Cancer Res 1997; 57: 4749-4756.
16. Suraweera N, Duval A, Reperant M, et al. Evaluation of tumor microsatellite instability using five quasimonomorphic mononucleotide repeats and pentaplex PCR. Gastroenterology 2002; 123: 1804-1811.
17. Patil DT, Bronner MP, Portier BP, et al. A five-marker panel in a multiplex PCR accurately detects microsatellite instability-high colorectal tumors without control DNA. Diagn Mol Pathol 2012; 21: 127-133.
18. Issa JP. CpG island methylator phenotype in cancer. Nat Rev Cancer 2004; 4: 988-993.
19. Lao VV, Grady WM. Epigenetics and colorectal cancer. Nat Rev Gastroenterol Hepatol 2011; 8: 686-700.
20. Toyota M, Ahuja N, Ohe-Toyota M, et al. CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci U S A 1999; 96: 8681-8686.
21. Hawkins N, Norrie M, Cheong K, et al. CpG island methylation in sporadic colorectal cancers and its relationship to microsatellite instability. Gastroenterology 2002; 122: 1376-1387.
22. Samowitz WS, Albertsen H, Herrick J, et al. Evaluation of a large, population-based sample supports a CpG island methylator phenotype in colon cancer. Gastroenterology 2005; 129: 837-845.
23. Dahlin AM, Palmqvist R, Henriksson ML, et al. The role of the CpG island methylator phenotype in colorectal cancer prognosis depends on microsatellite instability screening status. Clin Cancer Res 2010; 16: 1845-1855.
24. Kambara T, Simms LA, Whitehall VL, et al. BRAF mutation is associated with DNA methylation in serrated polyps and cancers of the colorectum. Gut 2004; 53: 1137-1144.
25. Hughes LA, Khalid-de Bakker CA, Smits KM, et al. The CpG island methylator phenotype in colorectal cancer: progress and problems. Biochim Biophys Acta 2012; 1825: 77-85.
26. Weisenberger DJ, Siegmund KD, Campan M, et al. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet 2006; 38: 787-793.
27. Ogino S, Kawasaki T, Kirkner GJ, et al. Evaluation of markers for CpG island methylator phenotype (CIMP) in colorectal cancer by a large population-based sample. J Mol Diagn 2007; 9: 305-314.
28. Berg M, Hagland HR, Søreide K. Comparison of CpG island methylator phenotype (CIMP) frequency in colon cancer using different probe- and gene-specific scoring alternatives on recommended multi-gene panels. PLoS One 2014; 9(1): e86657.
29. Bosman F, Yan P. Molecular pathology of colorectal cancer. Pol J Pathol 2014; 65: 257-266.
30. Acharya S, Wilson T, Gradia S, et al. hMSH2 forms specific mispair-binding complexes with hMSH3 and hMSH6. Proc Natl Acad Sci U S A 1996; 93: 13629-13634.
31. Kadyrov FA, Dzantiev L, Constantin N, et al. Endonucleolytic function of MutLalpha in human mismatch repair. Cell 2006; 126: 297-308.
32. Young J, Simms LA, Biden KG, et al. Features of colorectal cancers with high-level microsatellite instability occurring in familial and sporadic settings: parallel pathways of tumorigenesis. Am J Pathol 2001; 159: 2107-2116.
33. Shia J. Immunohistochemistry versus microsatellite instability testing for screening colorectal cancer patients at risk for hereditary nonpolyposis colorectal cancer syndrome. Part I. The utility of immunohistochemistry. J Mol Diagn 2008; 10: 293-300.
34. Salahshor S, Koelble K, Rubio C, et al. Microsatellite Instability and hMLH1 and hMSH2 expression analysis in familial and sporadic colorectal cancer. Lab Invest 2001; 81: 535-541.
35. Peltomäki P, Vasen H. Mutations associated with HNPCC predisposition -- Update of ICG-HNPCC/INSiGHT mutation database. Dis Markers 2004; 20: 269-276.
36. Zhang L. Immunohistochemistry versus microsatellite instability testing for screening colorectal cancer patients at risk for hereditary nonpolyposis colorectal cancer syndrome. Part II. The utility of microsatellite instability testing. J Mol Diagn 2008; 10: 301-307.
37. Cicek MS, Lindor NM, Gallinger S, et al. Quality assessment and correlation of microsatellite instability and immunohistochemical markers among population- and clinic-based colorectal tumors results from the Colon Cancer Family Registry. J Mol Diagn 2010; 13: 271-281.
38. Lynch HT, de la Chapelle A. Hereditary colorectal cancer. N Engl J Med 2003; 348: 919-932.
39. Vasen HFA, Mecklin J-P, Meera Khan P, et al. The International Collaborative Group on hereditary non-polyposis colorectal cancer (ICG-HNPCC). Dis Colon Rectum 1991; 34: 424-425.
40. Vasen HF, Watson P, Mecklin JP, et al. New clinical criteria for hereditary nonpolyposis colorectal cancer (HNPCC, Lynch syndrome) proposed by the International Collaborative group on HNPCC. Gastroenterology 1999; 116: 1453-1456.
41. Jass JR. Role of the pathologist in the diagnosis of hereditary non-polyposis colorectal cancer. Dis Markers 2004; 20: 215-224.
42. Umar A, Boland CR, Terdiman JP, et al. Revised Bethesda Guidelines for hereditary nonpolyposis colorectal cancer (Lynch syndrome) and microsatellite instability. J Natl Cancer Inst 2004; 96: 261-268.
43. Musulén E, Sanz C, Muñoz-Mármol AM, et al. Mismatch repair protein immunohistochemistry: a useful population screening strategy for Lynch syndrome. Hum Pathol 2014; 45: 1388-1396.
44. Dunlop MG, Farrington SM, Carothers AD, et al. Cancer risk associated with germline DNA mismatch repair gene mutations. Hum Mol Genet 1997; 6:105-110.
45. Quehenberger F, Vasen HF, van Houwelingen HC. Risk of colorectal and endometrial cancer for carriers of mutations of the hMLH1 and hMSH2 gene: correction for ascertainment. J Med Genet 2005; 42: 491-496.
46. Jenkins MA, Baglietto L, Dowty JG, et al. Cancer risks for mismatch repair gene mutation carriers: a population-based early onset case-family study. Clin Gastroenterol Hepatol 2006; 4: 489-498.
47. Alarcon F, Lasset C, Carayol J, et al. Estimating cancer risk in HNPCC by the GRL method. Eur J Hum Genet 2007; 15: 831-836.
48. Senter L, Clendenning M, Sotamaa K, et al. The clinical phenotype of Lynch syndrome due to germ-line PMS2 mutations. Gastroenterology 2008; 135: 419-428.
49. Choi YH, Cotterchio M, McKeown-Eyssen G, et al. Penetrance of colorectal cancer among MLH1/MSH2 carriers participating in the colorectal cancer familial registry in Ontario. Hered Cancer Clin Pract 2009; 7: 14.
50. Baglietto L, Lindor NM, Dowty JG, et al. Risks of Lynch syndrome cancers for MSH6 mutation carriers. J Natl Cancer Inst 2010; 102: 193-201.
51. Bonadona V, Bonaïti B, Olschwang S, et al. Cancer risks associated with germline mutations in MLH1, MSH2, and MSH6 genes in Lynch syndrome. JAMA 2011; 305: 2304-2310.
52. Watson P, Lynch HT. Extracolonic cancer in hereditary nonpolyposis colorectal cancer. Cancer 1993; 71: 677-685.
53. Steinke V, Engel C, Büttner R, et al. Hereditary nonpolyposis colorectal cancer (HNPCC)/Lynch syndrome. Dtsch Arztebl Int 2013; 110: 32-38.
54. Lynch PM. When and how to perform genetic testing for inherited colorectal cancer syndromes. J Natl Compr Canc Netw 2013; 11: 1577-1583.
55. Fearon ER. Molecular genetics of colorectal cancer. Annu Rev Pathol 2011; 6: 479-507.
56. Chirieac LR, Shen L, Catalano PJ, et al. Phenotype of microsatellite-stable colorectal carcinomas with CpG island methylation. Am J Surg Pathol 2005; 29: 429-436.
57. Juo YY, Johnston FM, Zhang DY, et al. Prognostic value of CpG island methylator phenotype among colorectal cancer patients: a systematic review and meta-analysis. Ann Oncol 2014; 25: 2314-2327.
58. Lee S, Cho NY, Choi M, et al. Clinicopathological features of CpG island methylator phenotype-positive colorectal cancer and its adverse prognosis in relation to KRAS/BRAF mutation. Pathol Int 2008; 58: 104-113.
59. Yamamoto E, Suzuki H, Yamano HO, et al. Molecular dissection of premalignant colorectal lesions reveals early onset of the CpG island methylator phenotype. Am J Pathol 2012; 181: 1847-1861.
60. Chan AO, Broaddus RR, Houlihan PS, et al. CpG island methylation in aberrant crypt foci of the colorectum. Am J Pathol 2002; 160: 1823-1830.
61. Rex DK, Ahnen DJ, Baron JA, et al. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol 2012; 107: 1315-1329.
62. Fernando WC, Miranda MS, Worthley DL, et al. The CIMP Phenotype in BRAF Mutant Serrated Polyps from a Prospective Colonoscopy Patient Cohort. Gastroenterol Res Pract 2014; 2014: 374926.
63. Spring KJ, Zhao ZZ, Karamatic R, et al. High prevalence of sessile serrated adenomas with BRAF mutations: a prospective study of patients undergoing colonoscopy. Gastroenterology 2006; 131: 1400-1407.
64. Chow E, Lipton L, Lynch E, et al. Hyperplastic polyposis syndrome: phenotypic presentations and the role of MBD4 and MYH. Gastroenterology 2006; 131: 30-39.
65. Snover DC, Ahnen DJ, Burt RW, Odze RD. Serrated polyps of the colon and rectum and serrated polyposis. In: Bosman FT, Carneiro F, Hruban RH, Theise ND (eds). World Health Organization Classification of Tumours of the Digestive System. IARC, Lyon 2010; 160-165.
66. Boparai KS, Mathus-Vliegen EM, Koornstra JJ, et al. Increased colorectal cancer risk during follow-up in patients with hyperplastic polyposis syndrome: a multicentre cohort study. Gut 2010; 59: 1094-1100.
67. Guarinos C, Sánchez-Fortún C, Rodríguez-Soler M, et al. Clinical subtypes and molecular characteristics of serrated polyposis syndrome. Clin Gastroenterol Hepatol 2013; 11: 705-711.
68. Lochhead P, Kuchiba A, Imamura Y, et al. Microsatellite instability and BRAF mutation testing in colorectal cancer prognostication. J Natl Cancer Inst 2013; 105: 1151-1156.
69. Pai RK, Jayachandran P, Koong AC, et al. BRAF-mutated, microsatellite-stable adenocarcinoma of the proximal colon: an aggressive adenocarcinoma with poor survival, mucinous differentiation, and adverse morphologic features. Am J Surg Pathol 2012; 36: 744-752.
70. Popovici V, Budinska E, Bosman FT, et al. Context-dependent interpretation of the prognostic value of BRAF and KRAS mutations in colorectal cancer. BMC Cancer 2013; 13: 439.
71. Mouradov D, Domingo E, Gibbs P, et al. Survival in stage II/ III colorectal cancer is independently predicted by chromosomal and microsatellite instability, but not by specific driver mutations. Am J Gastroenterol 2013; 108: 1785-1793.
72. Bae JM, Kim JH, Cho NY, et al. Prognostic implication of the CpG island methylator phenotype in colorectal cancers depends on tumour location. Br J Cancer 2013; 109: 1004-1012.
73. Alexander J, Watanabe T, Wu TT, et al. Histopathological identification of colon cancer with microsatellite instability. Am J Pathol 2001; 158: 527-535.
74. Greenson JK, Bonner JD, Ben-Yzhak O, 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 2003; 27: 563-570.
75. Shia J, Ellis NA, Paty PB, et al. Value of histopathology in predicting microsatellite instability in hereditary nonpolyposis colorectal cancer and sporadic colorectal cancer. Am J Surg Pathol 2003; 27: 1407-1417.
76. Yearsley M, Hampel H, Lehman A, et al. Histologic features distinguish microsatellite-high from microsatellite-low and microsatellite-stable colorectal carcinomas, but do not differentiate germline mutations from methylation of the MLH1 promoter. Hum Pathol 2006; 37: 831-838.
77. Greenson JK, Huang SC, Herron C, et al. Pathologic predictors of microsatellite instability in colorectal cancer. Am J Surg Pathol 2009; 33: 126-133.
78. Zlobec I, Bihl MP, Foerster A, et al. The impact of CpG island methylator phenotype and microsatellite instability on tumour budding in colorectal cancer. Histopathology 2012; 61: 777-787.
79. Hamilton SR, Bosman FT, Boffetta P et al. Carcinoma of the colon and rectum. In: Bosman FT, Carneiro F, Hruban RH, Theise ND (eds). World Health Organization Classification of Tumours of the Digestive System. Lyon: IARC; 2010; 134-146.
80. Hartman DJ, Nikiforova MN, Chang DT, et al. Signet ring cell colorectal carcinoma: a distinct subset of mucin-poor microsatellite-stable signet ring cell carcinoma associated with dismal prognosis. Am J Surg Pathol 2013; 37: 969-977.
81. Michael-Robinson JM, Biemer-Hüttmann A, Purdie DM, et al. Tumour infiltrating lymphocytes and apoptosis are independent features in colorectal cancer stratified according to microsatellite instability status. Gut 2001; 48: 360-366.
82. Jass JR. HNPCC and sporadic MSI-H colorectal cancer: a review of the morphological similarities and differences. Fam Cancer 2004; 3: 93-100.
83. Hyde A, Fontaine D, Stuckless S, et al. A histology-based model for predicting microsatellite instability in colorectal cancers. Am J Surg Pathol 2010; 34: 1820-1829.
84. Chetty R. Gastrointestinal cancers accompanied by a dense lymphoid component: an overview with special reference to gastric and colonic medullary and lymphoepithelioma-like carcinomas. J Clin Pathol 2012; 65: 1062-1065.
85. Schneider NI, Langner C. Prognostic stratification of colorectal cancer patients: current perspectives. Cancer Manag Res 2014; 6: 291-300.
86. Thirunavukarasu P, Sathaiah M, Singla S, et al. Medullary carcinoma of the large intestine: a population based analysis. Int J Oncol 2010; 37: 901-907.
87. Young J, Simms LA, Biden KG, et al. Features of colorectal cancers with high-level microsatellite instability occurring in familial and sporadic settings: parallel pathways of tumorigenesis. Am J Pathol 2001; 159: 2107-2116.
88. Jass JR, Walsh MD, Barker M, et al. Distinction between familial and sporadic forms of colorectal cancer showing DNA microsatellite instability. Eur J Cancer 2002; 38: 858-866.
89. McGregor DK, Wu TT, Rashid A, et al. Reduced expression of cytokeratin 20 in colorectal carcinomas with high levels of microsatellite instability. Am J Surg Pathol 2004; 28: 712-718.
90. Harbaum L, Pollheimer MJ, Kornprat P, et al. Keratin 20 - a diagnostic and prognostic marker in colorectal cancer? Histol Histopathol 2012; 27: 347-356.
91. Kim JH, Rhee YY, Bae JM, et al. Loss of CDX2/CK20 expression is associated with poorly differentiated carcinoma, the CpG island methylator phenotype, and adverse prognosis in microsatellite-unstable colorectal cancer. Am J Surg Pathol 2013; 37: 1532-1541.
92. Julié C, Trésallet C, Brouquet A, et al. Identification in daily practice of patients with Lynch syndrome (hereditary nonpolyposis colorectal cancer): revised Bethesda guidelines-based approach versus molecular screening. Am J Gastroenterol 2008; 103: 2825-2835.
93. van Lier MG, Leenen CH, Wagner A, et al. Yield of routine molecular analyses in colorectal cancer patients =70 years to detect underlying Lynch syndrome. J Pathol 2012; 226: 764-774.
94. Pérez-Carbonell L, Ruiz-Ponte C, Guarinos C, et al. Comparison between universal molecular screening for Lynch syndrome and revised Bethesda guidelines in a large population-based cohort of patients with colorectal cancer. Gut 2012; 61: 865-872.
95. Moreira L, Balaguer F, Lindor N, et al. Identification of Lynch syndrome among patients with colorectal cancer. JAMA 2012; 308: 1555-1565.
96. Zhang X, Li J. Era of universal testing of microsatellite instability in colorectal cancer. World J Gastrointest Oncol 2013; 5: 12-19.
97. Giardiello FM, Allen JI, Axilbund JE, et al. Guidelines on genetic evaluation and management of Lynch syndrome: a consensus statement by the U.S. Multi-Society Task Force on Colorectal Cancer. Gastrointest Endosc 2014; 80: 197-220.
98. Giardiello FM, Allen JI, Axilbund JE, et al. Guidelines on genetic evaluation and management of Lynch syndrome: a consensus statement by the US Multi-Society Task Force on colorectal cancer. Gastroenterology 2014; 147: 502-526.
99. Giardiello FM, Allen JI, Axilbund JE, et al. Guidelines on genetic evaluation and management of Lynch syndrome: a consensus statement by the US Multi-Society Task Force on Colorectal Cancer. Dis Colon Rectum 2014; 57: 1025-1048.
100. Giardiello FM, Allen JI, Axilbund JE, et al. Guidelines on genetic evaluation and management of Lynch syndrome: a consensus statement by the US Multi-society Task Force on colorectal cancer. Am J Gastroenterol 2014; 109: 1159-1179.
101. Vasen HF, Blanco I, Aktan-Collan K, et al. Revised guidelines for the clinical management of Lynch syndrome (HNPCC): recommendations by a group of European experts. Gut 2013; 62: 812-823.
102. Kazama Y, Watanabe T, Kanazawa T, et al. Microsatellite instability in poorly differentiated adenocarcinomas of the colon and rectum: relationship to clinicopathological features. J Clin Pathol 2007; 60: 701-704.
103. Xiao H, Yoon YS, Hong SM, et al. Poorly differentiated colorectal cancers: correlation of microsatellite instability with clinicopathologic features and survival. Am J Clin Pathol 2013; 140: 341-347.
104. Imai Y. Poorly differentiated adenocarcinoma of the colon: subsite location and clinicopathologic features. Int J Colorectal Dis 2015; 30: 187-196.
105. Vilkin A, Halpern M, Morgenstern S, et al. How reliable is immunohistochemical staining for DNA mismatch repair proteins performed after neoadjuvant chemoradiation? Hum Pathol 2014; 45: 2029-2036.
106. Bao F, Panarelli NC, Rennert H, et al. Neoadjuvant therapy induces loss of MSH6 expression in colorectal carcinoma. Am J Surg Pathol 2010; 34: 1798-1804.
107. Shia J, Zhang L, Shike M, et al. Secondary mutation in a coding mononucleotide tract in MSH6 causes loss of immunoexpression of MSH6 in colorectal carcinomas with MLH1/ PMS2 deficiency. Mod Pathol 2013; 26: 131-138.
108. Bellizzi AM. Immunohistochemistry in gastroenterohepatopancreatobiliary epithelial neoplasia – practical applications, pitfalls, and emerging markers. Surg Pathol 2013; 6: 567-609.