Sporadic colorectal carcinomas with low-level microsatellite instability: A distinct subgroup with specific clinicopathological and molecular features

International Journal of Colorectal Disease

Volumn 26, Issue 4, 2011, Pages 445-453

  Azzoni, Cinzia ^a   Bottarelli, Lorena ^a   Cecchini, Stefano ^a   Maria Silini, Enrico ^a   Bordi, Cesare ^a   Sarli, Leopoldo ^a  

^a UNIVERSITY OF PARMA   (Italy)

Author keywords

Colorectal cancer; Microsatellite instability; Microsatellite low; Prognosis

Indexed keywords

CYCLOOXYGENASE 2; FRAGILE HISTIDINE TRIAD PROTEIN; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; PROTEIN MLH1; PROTEIN MSH2; PROTEIN P21; PROTEIN P27;

ADENOCARCINOMA; ADULT; AGED; ALLELE; ALLELIC LOSS; ARTICLE; CHROMOSOME 18Q; CHROMOSOME 4P; CHROMOSOME 8P; COLORECTAL CANCER; CONTROLLED STUDY; FEMALE; HETEROZYGOSITY LOSS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; MICROSATELLITE INSTABILITY; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; SURVIVAL RATE; TUMOR LOCALIZATION; COLORECTAL TUMOR; GENETICS; KAPLAN MEIER METHOD; MIDDLE AGED; PATHOLOGY;

ADULT; AGED; AGED, 80 AND OVER; COLORECTAL NEOPLASMS; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; LOSS OF HETEROZYGOSITY; MALE; MICROSATELLITE INSTABILITY; MIDDLE AGED;

EID: 79960118881     PISSN: 01791958     EISSN: 14321262     Source Type: Journal    
DOI: 10.1007/s00384-011-1133-8     Document Type: Article

References (44)

1. Chapuis PH, Dent OF, Fisher R, Newland RC, Pheils MT, Smyth E, Colquhoun K (1985) A multivariate analysis of clinical and pathological variables in prognosis after resection of large bowel cancer. Br J Surg 72:698-702 (Pubitemid 16215165)
2. Offit K (2000) Genetic prognostic markers for colorectal cancer. N Engl J Med 342:124-125 (Pubitemid 30036605)
3. Lengauer C, Kinzler KW, Vogelstein B (1997) Genetic instability in colorectal cancers. Nature 386:623-627 (Pubitemid 27175430)
4. Aaltonen LA, PeltomÄki P, Leach FS, Sistonen P, PylkkÄnen L, Mecklin JP, JÄrvinen H, Powell SM, Jen J, Hamilton SR et al (1993) Clues to the pathogenesis of familial colorectal cancer. Science 260:812-816 (Pubitemid 23167611)
5. Thibodeau SN, Bren G, Schaid D (1993) Microsatellite instability in cancer of the proximal colon. Science 260:816-819 (Pubitemid 23167612)
6. Umar A, Boland C, Terdiman J, Syngal S, de la Chapelle A, Rüschoff J, Fishel R, Lindor N, Burgart L, Hamelin R, Hamilton S, Hiatt R, Jass J, Lindblom A, Lynch H, Peltomaki P, Ramsey S, Rodriguez-Bigas M, Vasen H, Hawk E, Barrett J, Freedman A, Srivastava S (2004) Revised Bethesda guidelines for hereditary nonpolyposis colorectal cancer (Lynch syndrome) and microsatellite instability. J Natl Cancer Inst 96:261-268 (Pubitemid 38256271)
7. Aaltonen LA, Salovaara R, Kristo P, Canzian F, Hemminki A, PeltomÄki P, Chadwick RB, KÄÄriÄinen H, Eskelinen M, JÄrvinen H, Mecklin JP, de la Chapelle A (1998) Incidence of hereditary nonpolyposis colorectal cancer and the feasibility of molecular screening for the disease. N Engl J Med 338:1481-1487 (Pubitemid 28226275)
8. Asaka S, Arai Y, Nishimura Y, Yamaguchi K, Ishikubo T, Yatsuoka T, Tanaka Y, Akagi K (2009) Microsatellite instability-low colorectal cancer acquires a KRAS mutation during the progression from Dukes' A to Dukes' B. Carcinogenesis 30:494-499
9. Kohonen-Corish MR, Daniel JJ, Chan C, Lin BP, Kwun SY, Dent OF, Dhillon VS, Trent RJ, Chapuis PH, Bokey EL (2005) Low microsatellite instability is associated with poor prognosis in stage C colon cancer. J Clin Oncol 23:2318-2324 (Pubitemid 46218724)
10. Halford SE, Sawyer EJ, Lambros MB, Gorman P, Macdonald ND, Talbot IC, Foulkes WD, Gillett CE, Barnes DM, Akslen LA, Lee K, Jacobs IJ, Hanby AM, Ganesan TS, Salvesen HB, Bodmer WF, Tomlinson IP, Roylance RR (2003) MSI-low, a real phenomenon which varies in frequency among cancer types. J Pathol 201:389-394 (Pubitemid 37408259)
11. Biden KG, Simms LA, Cummings M, Buttenshaw R, Schoch E, Searle J, Gobe G, Jass JR, Meltzer SJ, Leggett BA, Young J (1999) Expression of Bcl-2 protein is decreased in colorectal adenocarcinomas with microsatellite instability. Oncogene 18:1245-1249 (Pubitemid 29085998)
12. Wright CM, Dent OF, Newland RC, Barker M, Chapuis PH, Bokey EL, Young JP, Leggett BA, Jass JR, Macdonald GA (2005) Low level microsatellite instability may be associated with reduced cancer specific survival in sporadic stage C colorectal carcinoma. Gut 54:103-108 (Pubitemid 40007227)
13. Sarli L, Bottarelli L, Bader G, Iusco D, Pizzi S, Costi R, D'adda T, Bertolani M, Roncoroni L, Bordi C (2004) Association between recurrence of sporadic colorectal cancer, high level of microsatellite instability, and loss of heterozygosity at chromosome 18q. Dis Colon Rectum 47:1467-1482 (Pubitemid 39295874)
14. Wright CM, Dent OF, Barker M, Newland RC, Chapuis PH, Bokey EL, Young JP, Leggett BA, Jass JR, Macdonald GA (2000) Prognostic significance of extensive microsatellite instability in sporadic clinicopathological stage C colorectal cancer. Br J Surg 87:1197-1202
15. Halling KC, French AJ, McDonnell SK, Burgart LJ, Schaid DJ, Peterson BJ, Moon-Tasson L, Mahoney MR, Sargent DJ, O'Connell MJ, Witzig TE, Farr GHJ, Goldberg RM, Thibodeau SN (1999) Microsatellite instability and 8p allelic imbalance in stage B2 and C colorectal cancers. J Natl Cancer Inst 91:1295-1303 (Pubitemid 29387571)
16. Ward R, Meagher A, Tomlinson I, O'Connor T, Norrie M, Wu R, Hawkins N (2001) Microsatellite instability and the clinicopathological features of sporadic colorectal cancer. Gut 48:821-829 (Pubitemid 32476985)
17. Mori Y, Selaru FM, Sato F, Yin J, Simms LA, Xu Y, Olaru A, Deacu E, Wang S, Taylor JM, Young J, Leggett B, Jass JR, Abraham JM, Shibata D, Meltzer SJ (2003) The impact of microsatellite instability on the molecular phenotype of colorectal tumors. Cancer Res 63:4577-4582 (Pubitemid 36951032)
18. Guda K, Upender MB, Belinsky G, Flynn C, Nakanishi M, Marino JN, Ried T, Rosenberg DW (2004) Carcinogen-induced colon tumors in mice are chromosomally stable and are characterized by low-level microsatellite instability. Oncogene 23:3813-3821 (Pubitemid 38725694)
19. Rudzki Z, Zazula M, Okon K, Stachura J (2003) Low-level microsatellite instability colorectal carcinomas: do they really belong to a gray zone between high-level microsatellite instability and microsatellite-stable cancers? Int J Colorectal Dis 18:216-221 (Pubitemid 36764167)
20. Jass JR, Biden KG, Cummings MC, Simms LA, Walsh M, Schoch E, Meltzer SJ, Wright C, Searle J, Young J, Leggett BA (1999) Characterisation of a subtype of colorectal cancer combining features of the suppressor and mild mutator pathways. J Clin Pathol 52:455-460 (Pubitemid 29281765)
21. Whitehall VL, Walsh MD, Young J, Leggett BA, Jass JR (2001) Methylation of O-6-methylguanine DNA methyltransferase characterizes a subset of colorectal cancer with low-level DNA microsatellite instability. Cancer Res 61:827-830 (Pubitemid 32174386)
22. Kominami K, Nagasaka T, CullingsHM, Hoshizima N, Sasamoto H, Young J, Leggett BA, Tanaka N,Matsubara N (2009)Methylation in p14(ARF) is frequently observed in colorectal cancer with low-level microsatellite instability. J Int Med Res 37:1038-1045
23. Tomlinson I, Halford S, Aaltonen L, Hawkins N, Ward R (2002) Does MSI-low exist? J Pathol 197:6-13 (Pubitemid 34450158)
24. Cheng JD, Werness BA, Babb JS, Meropol NJ (1999) Paradoxical correlation of cyclin-dependent kinase inhibitors p21 waf1/cip1 and p27kip1 in metastatic colorectal carcinoma. Clin Cancer Res 5:1057-1062 (Pubitemid 29233219)
25. McKay JA, Douglas JJ, Ross VG, Curran S, Loane JF, Ahmed FY, Cassidy J,McLeod HL,Murray GI (2002) Analysis of key cell-cycle checkpoint proteins in colorectal tumours. J Pathol 196:386-393 (Pubitemid 34262849)
26. Sarli L, Bottarelli L, Azzoni C, Campanini N, Di Cola G, Bader G, Iusco D, Salvemini C, Caruso G, Donadei E, Pizzi S, D'Adda T, Costi R, Roncoroni L, Bordi C (2004) Abnormal Fhit protein expression and high frequency of microsatellite instability in sporadic colorectal cancer. Eur J Cancer 40:1581-1588 (Pubitemid 38757747)
27. Sheehan KM, O'Connell F, O'Grady A, Conroy RM, Leader MB, Byrne MF, Murray FE, Kay EW (2004) The relationship between cyclooxygenase-2 expression and characteristics of malignant transformation in human colorectal adenomas. Eur J Gastroenterol Hepatol 16:619-625 (Pubitemid 38703872)
28. Jass JR, Sobin LH (1989) Histological typing of intestinal tumours. Springer, Berlin
29. Sobin LH, Wittekind CH (eds) (1997) TNM classification of malignant tumours, 5th edn. Wiley-Liss, New York
30. Jen J, Kim H, Piantadosi S, Liu ZF, Levitt RC, Sistonen P, Kinzler KW, Vogelstein B, Hamilton SR (1994) Allelic loss of chromosome 18q and prognosis in colorectal cancer. N Engl J Med 331:213-221 (Pubitemid 24226678)
31. Samowitz WS, Slattery ML, Potter JD, Leppert MF (1999) BAT-26 and BAT-40 instability in colorectal adenomas and carcinomas and germline polymorphisms. Am J Pathol 154:1637-1641 (Pubitemid 29262844)
32. Arribas R, Ribas M, Risques RA, Masramon L, Tórtola S, Marcuello E, Aiza G, Miró R, Capellà G, Peinado MA (1999) Prospective assessment of allelic losses at 4p14-16 in colorectal cancer: two mutational patterns and a locus associated with poorer survival. Clin Cancer Res 5:3454-3459
33. Mueller JD, Haegle N, Keller G, Mueller E, Saretzky G, Bethke B, Stolte M, Hofler H (1998) Loss of heterozygosity and microsatellite instability in de novo versus ex-adenoma carcinomas of the colorectum. Am J Pathol 153:1977-1984 (Pubitemid 28550684)
34. Beckmann MW, Picard F, An HX, van Roeyen CR, Dominik SI, Mosny DS, Schnurch HG, Bender HG, Niederacher D (1996) Clinical impact of detection of loss of heterozygosity of BRCA1 and BRCA2 markers in sporadic breast cancer. Br J Cancer 73:1220-1226 (Pubitemid 26162336)
35. Huang L, Jiang T, Yuan F, Li GL, Cui Y, Liu EZ, Wang ZC (2008) Correlation of chromosome 1p and 19q status and expression of MGMT, p53 and Ki-67 in diffuse gliomas of WHO grade II and III: a clinicopathological study. Neuropathol Appl Neurobiol 35:367-379
36. Sarli L, Bottarelli L, Azzoni C, Campanini N, Di Cola G, Barilli AL, Marchesi F, Mazzeo A, Salvemini C, Morari S, Di Mauro D, Donadei E, Necchi F, Roncoroni L, Bordi C (2006) Loss of p27 expression and microsatellite instability in sporadic colorectal cancer. Surg Oncol 15:97-106 (Pubitemid 44802810)
37. Ogino S, Kawasaki T, Kirkner GJ, Ogawa A, Dorfman I, Loda M, Fuchs CS (2006) Down-regulation of p21 (CDKN1A/CIP1) is inversely associated with microsatellite instability and CpG island methylator phenotype (CIMP) in colorectal cancer. J Pathol 210:147-154 (Pubitemid 44463929)
38. Lim HY, Joo HJ, Choi JH, Yi JW, Yang MS, Cho DY, Kim HS, Nam DK, Lee KB, Kim HC (2000) Increased expression of cyclooxygenase-2 protein in human gastric carcinoma. Clin Cancer Res 6:519-525 (Pubitemid 30111473)
39. Tuppurainen K, Makinen JM, Junttila O, Liakka A, Kyllönen AP, Tuominen H, Karttunen TJ, MÄkinen MJ (2005) Morphology and microsatellite instability in sporadic serrated and non-serrated colorectal cancer. J Pathol 207:285-294 (Pubitemid 41556452)
40. Kim YH, Min BH, Choi HK, Kim SJ, Kim KM, Kim JY, Chang DK, Son HJ, Rhee PL, Kim JJ, Rhee JC, Chun HK (2009) Sporadic colorectal carcinomas with low-level microsatellite instability in Korea: do they form a distinct subgroup with distinguished clinicopathological features? J Surg Oncol 99:351-355
41. Esteller M, Risques RA, Toyota M, Capella G, Moreno V, Peinado MA, Baylin SB, Herman JG (2001) Promoter hypermethylation of the DNA repair gene O(6)-methylguanine-DNA methyltransferase is associated with the presence of G:C to A:T transition mutations in p53 in human colorectal tumorigenesis. Cancer Res 61:4689-4692 (Pubitemid 32691877)
42. Brabender J, Usadel H, Metzger R, Schneider PM, Park J, Salonga D, Tsao-Wei DD, Groshen S, Lord RV, Takebe N, Schneider S, Hölscher AH, Danenberg KD, Danenberg PV (2003) Quantitative O(6)-methylguanine DNA methyltransferase methylation analysis in curatively resected non-small cell lung cancer: associations with clinical outcome. Clin Cancer Res 9:223-227 (Pubitemid 36109737)
43. Dietmaier W, Wallinger S, Bocker T, Kullmann F, Fishel R, Rüschoff J (1997) Diagnostic microsatellite instability: definition and correlation with mismatch repair protein expression. Cancer Res 57:4749-4756 (Pubitemid 27468981)
44. Oliart S, Martínez-Santos C, Moreno-Azcoita M, Cerquella C, Nejda N, Daimiel L, Iglesias D, Fernández-Peralta AM, González-Aguilera JJ (2006) Do MSI-L sporadic colorectal tumors develop through mild mutator pathway? Am J Clin Oncol 29:364-370 (Pubitemid 44197541)