The utility of immunohistochemical detection of DNA mismatch repair gene proteins

Virchows Archiv

Volumn 445, Issue 5, 2004, Pages 431-441

  Shia, Jinru ^a   Ellis, Nathan A ^a   Klimstra, David S ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

DNA mismatch repair gene proteins; Immunohistochemistry; Microsatellite instability

Indexed keywords

CANCER GENETICS; CANCER RISK; CORRELATION ANALYSIS; GENE CONTROL; GENE IDENTIFICATION; GENE MUTATION; GENETIC LINKAGE; GENETIC VARIABILITY; HERITABILITY; HIGH RISK POPULATION; HUMAN; IMMUNOHISTOCHEMISTRY; MISMATCH REPAIR; MISSENSE MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVIEW; RISK FACTOR; SENSITIVITY ANALYSIS; STAINING; STATISTICAL SIGNIFICANCE;

BASE PAIR MISMATCH; CARRIER PROTEINS; DNA REPAIR; DNA-BINDING PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; MUTS HOMOLOG 2 PROTEIN; NEOPLASM PROTEINS; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS; SENSITIVITY AND SPECIFICITY;

EID: 9944243710     PISSN: 09456317     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00428-004-1090-5     Document Type: Review

References (65)

1. Aaltonen LA, Peltomaki P, Leach FS, Sistonen P, Pylkkanen L, Mecklin JP, Jarvinen H, Powell SM, Jen J, Hamilton SR et al (1993) Clues to the pathogenesis of familial colorectal cancer. Science 260:812-816
2. Aaltonen LA, Salovaara R, Kristo P, Canzian F, Hemminki A, Peltomaki P, Chadwick RB, Kaariainen H, Eskelinen M, Jarvinen 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
3. Aarnio M, Sankila R, Pukkala E, Salovaara R, Aaltonen LA, de la Chapelle A, Peltomaki P, Mecklin JP, Jarvinen HJ (1999) Cancer risk in mutation carriers of DNA-mismatch-repair genes. Int J Cancer 81:214-218
4. Acharya S, Wilson T, Gradia S, Kane MF, Guerrette S, Marsischky GT, Kolodner R, Fishel R (1996) hMSH2 forms specific mispair-binding complexes with hMSH3 and hMSH6. Proc Natl Acad Sci U S A 93:13629-13634
5. Bapat BV, Madlensky L, Temple LK, Hiruki T, Redston M, Baron DL, Xia L, Marcus VA, Soravia C, Mitri A, Shen W, Gryfe R, Berk T, Chodirker BN, Cohen Z, Gallinger S (1999) Family history characteristics, tumor microsatellite instability and germline MSH2 and MLH1 mutations in hereditary colorectal cancer. Hum Genet 104:167-176
6. Berends MJ, Wu Y, Sijmons RH, Mensink RG, van der Sluis T, Hordijk-Hos JM, de Vries EG, Hollema H, Karrenbeld A, Buys CH, van der Zee AG, Hofstra RM, Kleibeuker JH (2002) Molecular and clinical characteristics of MSH6 variants: an analysis of 25 index carriers of a germline variant. Am J Hum Genet 70:26-37
7. Boland CR (2000) Molecular genetics of hereditary nonpolyposis colorectal cancer. Ann N Y Acad Sci 910:50-61
8. Boland CR, Thibodeau SN, Hamilton SR, Sidransky D, Eshleman JR, Burt RW, Meltzer SJ, Rodriguez-Bigas MA, Fodde R, Ranzani GN, Srivastava S (1998) 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
9. Cawkwell L, Gray S, Murgatroyd H, Sutherland F, Haine L, Longfellow M, O'Loughlin S, Cross D, Kronborg O, Fenger C, Mapstone N, Dixon M, Quirke P (1999) Choice of management strategy for colorectal cancer based on a diagnostic immunohistochemical test for defective mismatch repair. Gut 45:409-415
10. Chapusot C, Martin L, Bouvier AM, Bonithon-Kopp C, Ecarnot-Laubriet A, Rageot D, Ponnelle T, Laurent Puig P, Faivre J, Piard F (2002) Microsatellite instability and intratumoural heterogeneity in 100 right-sided sporadic colon carcinomas. Br J Cancer 87:400-404
11. Chaves P, Cruz C, Lage P, Claro I, Cravo M, Leitao CN, Soares J (2000) Immunohistochemical detection of mismatch repair gene proteins as a useful tool for the identification of colorectal carcinoma with the mutator phenotype. J Pathol 191:355-360
12. Chiaravalli AM, Furlan D, Facco C, Tibiletti MG, Dionigi A, Casati B, Albarello L, Riva C, Capella C (2001) Immunohistochemical pattern of hMSH2/hMLH1 in familial and sporadic colorectal, gastric, endometrial and ovarian carcinomas with instability in microsatellite sequences. Virchows Arch 438:39-48
13. Cunningham JM, Kim CY, Christensen ER, Tester DJ, Parc Y, Burgart LJ, Halling KC, McDonnell SK, Schaid DJ, Walsh Vockley C, Kubly V, Nelson H, Michels VV, Thibodeau SN (2001) The frequency of hereditary defective mismatch repair in a prospective series of unselected colorectal carcinomas. Am J Hum Genet 69:780-790
14. Debniak T, Kurzawski G, Gorski B, Kladny J, Domagala W, Lubinski J (2000) Value of pedigree/clinical data, immunohistochemistry and microsatellite instability analyses in reducing the cost of determining hMLH1 and hMSH2 gene mutations in patients with colorectal cancer. Eur J Cancer 36:49-54
15. Debniak T, Gorski B, Cybulski C, Jakubowska A, Kurzawski G, Kladny J, Lubinski J (2001) Comparison of Alu-PCR, microsatelite instability, and immunohistochemical analyses in finding features characteristic for hereditary nonpolyposis colorectal cancer. J Cancer Res Clin Oncol 127:565-569
16. Deng G, Peng E, Gum J, Terdiman J, Sleisenger M, Kim YS (2002) Methylation of hMLH1 promoter correlates with the gene silencing with a region-specific manner in colorectal cancer. Br J Cancer 86:574-579
17. Dietmaier W, Wallinger S, Bocker T, Kullmann F, Fishel R, Ruschoff J (1997) Diagnostic microsatellite instability: definition and correlation with mismatch repair protein expression. Cancer Res 57:4749-4756
18. Dieumegard B, Grandjouan S, Sabourin JC, Le Bihan ML, Lefrere I, Bellefqih, Pignon JP, Rougier P, Lasser P, Benard J, Couturier D, Bressac-de Paillerets B (2000) Extensive molecular screening for hereditary non-polyposis colorectal cancer. Br J Cancer 82:871-880
19. Elsaleh H, Joseph D, Grieu F, Zeps N, Spry N, Iacopetta B (2000) Association of tumour site and sex with survival benefit from adjuvant chemotherapy in colorectal cancer. Lancet 355:1745-1750
20. Furukawa T, Konishi F, Masubuchi S, Shitoh K, Nagai H, Tsukamoto T (2002) Densely methylated MLH1 promoter correlates with decreased mRNA expression in sporadic colorectal cancers. Genes Chromosomes Cancer 35:1-10
21. Furukawa T, Konishi F, Shitoh K, Kojima M, Nagai H, Tsukamoto T (2002) Evaluation of screening strategy for detecting hereditary nonpolyposis colorectal carcinoma. Cancer 94:911-920
22. Halvarsson B, Lindblom A, Rambech E, Lagerstedt K, Nilbert M (2004) Microsatellite instability analysis and/or immunostaining for the diagnosis of hereditary nonpolyposis colorectal cancer? Virchows Arch 444:135-141
23. Hendriks Y, Franken P, Dierssen JW, De Leeuw W, Wijnen J, Dreef E, Tops C, Breuning M, Brocker-Vriends A, Vasen H, Fodde R, Morreau H (2003) Conventional and tissue microarray immunohistochemical expression analysis of mismatch repair in hereditary colorectal tumors. Am J Pathol 162:469-477
24. Herman JG, Umar A, Polyak K, Graff JR, Ahuja N, Issa JP, Markowitz S, Willson JK, Hamilton SR, Kinzler KW, Kane MF, Kolodner RD, Vogelstein B, Kunkel TA, Baylin SB (1998) Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc Natl Acad Sci U S A 95:6870-6875
25. Hoedema R, Monroe T, Bos C, Palmer S, Kim D, Marvin M, Luchtefeld M (2003) Genetic testing for hereditary nonpolyposis colorectal cancer. Am Surg 69:387-392
26. Jansson A, Arbman G, Zhang H, Sun XF (2003) Combined deficiency of hMLH1, hMSH2, hMSH3 and hMSH6 is an independent prognostic factor in colorectal cancer. Int J Oncol 22:41-49
27. Jeong SY, Shin KH, Shin JH, Ku JL, Shin YK, Park SY, Kim WH, Park JG (2003) Microsatellite instability and mutations in DNA mismatch repair genes in sporadic colorectal cancers. Dis Colon Rectum 46:1069-1077
28. Jourdan F, Sebbagh N, Comperat E, Mourra N, Flahault A, Olschwang S, Duval A, Hamelin R, Flejou JF (2003) Tissue microarray technology: validation in colorectal carcinoma and analysis of p53, hMLH1, and hMSH2 immunohistochemical expression. Virchows Arch 443:115-121
29. Kane MF, Loda M, Gaida GM, Lipman J, Mishra R, Goldman H, Jessup JM, Kolodner R (1997) 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
30. Kim H, Piao Z, Kim JW, Choi JS, Kim NK, Lee JM, Park JH (1998) Expression of hMSH2 and hMLH1 in colorectal carcinomas with microsatellite instability. Pathol Res Pract 194:3-9
31. Kim HC, Kim CN, Yu CS, Roh SA, Kim JC (2003) Methylation of the hMLH1 and hMSH2 promoter in early-onset sporadic colorectal carcinomas with microsatellite instability. Int J Colorectal Dis 18:196-202
32. Kolodner RD, Marsischky GT (1999) Eukaryotic DNA mismatch repair. Curr Opin Genet Dev 9:89-96
33. Kuismanen SA, Holmberg MT, Salovaara R, de la Chapelle A, Peltomaki P (2000) Genetic and epigenetic modification of MLH1 accounts for a major share of microsatellite-unstable colorectal cancers. Am J Pathol 156:1773-1779
34. Lamberti C, Kruse R, Ruelfs C, Caspari R, Wang Y, Jungck M, Mathiak M, Malayeri HR, Friedl W, Sauerbruch T, Propping P (1999) Microsatellite instability-a useful diagnostic tool to select patients at high risk for hereditary non-polyposis colorectal cancer: a study in different groups of patients with colorectal cancer. Gut 44:839-843
35. Lanza G, Gafa R, Maestri I, Santini A, Matteuzzi M, Cavazzini L (2002) Immunohistochemical pattern of MLH1/MSH2 expression is related to clinical and pathological features in colorectal adenocarcinomas with microsatellite instability. Mod Pathol 15:741-749
36. Leach FS, Nicolaides NC, Papadopoulos N, Liu B, Jen J, Parsons R, Peltomaki P, Sistonen P, Aaltonen LA, Nystrom-Lahti M et al (1993) Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer. Cell 75:1215-1225
37. Lindor NM, Burgart LJ, Leontovich O, Goldberg RM, Cunningham JM, Sargent DJ, Walsh-Vockley C, Petersen GM, Walsh MD, Leggett BA, Young JP, Barker MA, Jass JR, Hopper J, Gallinger S, Bapat B, Redston M, Thibodeau SN (2002) Immunohistochemistry versus microsatellite instability testing in phenotyping colorectal tumors. J Clin Oncol 20:1043-1048
38. Liu B, Parsons R, Papadopoulos N, Nicolaides NC, Lynch HT, Watson P, Jass JR, Dunlop M, Wyllie A, Peltomaki P, de la Chapelle A, Hamilton SR, Vogelstein B, Kinzler KW (1996) Analysis of mismatch repair genes in hereditary non-polyposis colorectal cancer patients. Nat Med 2:169-174
39. Liu T, Tannergard P, Hackman P, Rubio C, Kressner U, Lindmark G, Hellgren D, Lambert B, Lindblom A (1999) Missense mutations in hMLH1 associated with colorectal cancer. Hum Genet 105:437-441
40. Liu T, Wahlberg S, Burek E, Lindblom P, Rubio C, Lindblom A (2000) Microsatellite instability as a predictor of a mutation in a DNA mismatch repair gene in familial colorectal cancer. Genes Chromosomes Cancer 27:17-25
41. Marcus VA, Madlensky L, Gryfe R, Kim H, So K, Millar A, Temple LK, Hsieh E, Hiruki T, Narod S, Bapat BV, Gallinger S, Redston M (1999) Immunohistochemistry for hMLH1 and hMSH2: a practical test for DNA mismatch repair-deficient tumors. Am J Surg Pathol 23:1248-1255
42. Miyakura Y, Sugano K, Konishi F, Ichikawa A, Maekawa M, Shitoh K, Igarashi S, Kotake K, Koyama Y, Nagai H (2001) Extensive methylation of hMLH1 promoter region predominates in proximal colon cancer with microsatellite instability. Gastroenterology 121:1300-1309
43. Modrich P (1991) Mechanisms and biological effects of mismatch repair. Annu Rev Genet 25:229-253
44. Muller W, Burgart LJ, Krause-Paulus R, Thibodeau SN, Almeida M, Edmonston TB, Boland CR, Sutter C, Jass JR, Lindblom A, Lubinski J, MacDermot K, Sanders DS, Morreau H, Muller A, Oliani C, Orntoft T, Ponz De Leon M, Rosty C, Rodriguez-Bigas M, Ruschoff J, Ruszkiewicz A, Sabourin J, Salovaara R, Moslein G (2001) The reliability of immunohistochemistry as a prescreening method for the diagnosis of hereditary nonpolyposis colorectal cancer (HNPCC) - results of an international collaborative study. Fam Cancer 1:87-92
45. Peltomaki P (2003) Role of DNA mismatch repair defects in the pathogenesis of human cancer. J Clin Oncol 21:1174-1179
46. Peltomaki P, Vasen HF (1997) Mutations predisposing to hereditary nonpolyposis colorectal cancer: database and results of a collaborative study. The International Collaborative Group on Hereditary Nonpolyposis Colorectal Cancer. Gastroenterology 113:1146-1158
47. Potocnik U, Glavac D, Golouh R, Ravnik-Glavac M (2001) Causes of microsatellite instability in colorectal tumors: implications for hereditary non-polyposis colorectal cancer screening. Cancer Genet Cytogenet 126:85-96
48. Ribic CM, Sargent DJ, Moore MJ, Thibodeau SN, French AJ, Goldberg RM, Hamilton SR, Laurent-Puig P, Gryfe R, Shepherd LE, Tu D, Redston M, Gallinger S (2003) Tumor microsatellite-instability status as a predictor of benefit from fluorouracil-based adjuvant chemotherapy for colon cancer. N Engl J Med 349:247-257
49. Rigau V, Sebbagh N, Olschwang S, Paraf F, Mourra N, Parc Y, Flejou JF (2003) Microsatellite instability in colorectal carcinoma. The comparison of immunohistochemistry and molecular biology suggests a role for hMSH6 [correction of hMLH6] immunostaining. Arch Pathol Lab Med 127:694-700
50. Ruszkiewicz A, Bennett G, Moore J, Manavis J, Rudzki B, Shen L, Suthers G (2002) Correlation of mismatch repair genes immunohistochemistry and microsatellite instability status in HNPCC-associated tumours. Pathology 34:541-547
51. Salahshor S, Koelble K, Rubio C, Lindblom A (2001) Microsatellite Instability and hMLH1 and hMSH2 expression analysis in familial and sporadic colorectal cancer. Lab Invest 81:535-541
52. Scartozzi M, Bianchi F, Rosati S, Galizia E, Antolini A, Loretelli C, Piga A, Bearzi I, Cellerino R, Porfiri E (2002) Mutations of hMLH1 and hMSH2 in patients with suspected hereditary nonpolyposis colorectal cancer: correlation with microsatellite instability and abnormalities of mismatch repair protein expression. J Clin Oncol 20:1203-1208
53. Shia J, Ellis NA, Paty PB, Nash GM, Qin J, Offit K, Zhang XM, Markowitz AJ, Nafa K, Guillem JG, Wong WD, Gerald WL, Klimstra DS (2003) Value of histopathology in predicting microsatellite instability in hereditary nonpolyposis colorectal cancer and sporadic colorectal cancer. Am J Surg Pathol 27:1407-1417
54. Stone JG, Robertson D, Houlston RS (2001) Immunohistochemistry for MSH2 and MHL1: a method for identifying mismatch repair deficient colorectal cancer. J Clin Pathol 54:484-487
55. Terdiman JP, Gum JR Jr, Conrad PG, Miller GA, Weinberg V, Crawley SC, Levin TR, Reeves C, Schmitt A, Hepburn M, Sleisenger MH, Kim YS (2001) Efficient detection of hereditary nonpolyposis colorectal cancer gene carriers by screening for tumor microsatellite instability before germline genetic testing. Gastroenterology 120:21-30
56. Thibodeau SN, French AJ, Cunningham JM, Tester D, Burgart LJ, Roche PC, McDonnell SK, Schaid DJ, Vockley CW, Michels VV, Farr GH Jr, O'Connell MJ (1998) Microsatellite instability in colorectal cancer: different mutator phenotypes and the principal involvement of hMLH1. Cancer Res 58:1713-1718
57. Umar A, Boland CR, Terdiman JP, Syngal S, de la Chapelle A, Ruschoff J, Fishel R, Lindor NM, Burgart LJ, Hamelin R, Hamilton SR, Hiatt RA, Jass J, Lindblom A, Lynch HT, Peltomaki P, Ramsey SD, Rodriguez-Bigas MA, Vasen HF, Hawk ET, Barrett JC, Freedman AN, Srivastava S (2004) Revised Bethesda Guidelines for hereditary nonpolyposis colorectal cancer (Lynch syndrome) and microsatellite instability. J Natl Cancer Inst 96:261-268
58. Van Rijnsoever M, Elsaleh H, Joseph D, McCaul K, Iacopetta B (2003) 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
59. Vasen HF, Wijnen JT, Menko FH, Kleibeuker JH, Taal BG, Griffioen G, Nagengast FM, Meijers-Heijboer EH, Bertario L, Varesco L, Bisgaard ML, Mohr J, Fodde R, Khan PM (1996) Cancer risk in families with hereditary nonpolyposis colorectal cancer diagnosed by mutation analysis. Gastroenterology 110:1020-1027
60. Wagner A, Barrows A, Wijnen JT, van der Klift H, Franken PF, Verkuijlen P, Nakagawa H, Geugien M, Jaghmohan-Changur S, Breukel C, Meijers-Heijboer H, Morreau H, van Puijenbroek M, Burn J, Coronel S, Kinarski Y, Okimoto R, Watson P, Lynch JF, de la Chapelle A, Lynch HT, Fodde R (2003) Molecular analysis of hereditary nonpolyposis colorectal cancer in the United States: high mutation detection rate among clinically selected families and characterization of an American founder genomic deletion of the MSH2 gene. Am J Hum Genet 72:1088-1100
61. Wahlberg SS, Schmeits J, Thomas G, Loda M, Garber J, Syngal S, Kolodner RD, Fox E (2002) Evaluation of microsatellite instability and immunohistochemistry for the prediction of germ-line MSH2 and MLH1 mutations in hereditary nonpolyposis colon cancer families. Cancer Res 62:3485-3492
62. 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
63. Wheeler JM, Loukola A, Aaltonen LA, Mortensen NJ, Bodmer WF (2000) The role of hypermethylation of the hMLH1 promoter region in HNPCC versus MSI+ sporadic colorectal cancers. J Med Genet 37:588-592
64. Yan H, Papadopoulos N, Marra G, Perrera C, Jiricny J, Boland CR, Lynch HT, Chadwick RB, de la Chapelle A, Berg K, Eshleman JR, Yuan W, Markowitz S, Laken SJ, Lengauer C, Kinzler KW, Vogelstein B (2000) Conversion of diploidy to haploidy. Nature 403:723-724
65. Young J, Simms LA, Biden KG, Wynter C, Whitehall V, Karamatic R, George J, Goldblatt J, Walpole I, Robin SA, Borten MM, Stitz R, Searle J, McKeone D, Fraser L, Purdie DR, Podger K, Price R, Buttenshaw R, Walsh MD, Barker M, Leggett BA, Jass JR (2001) Features of colorectal cancers with high-level microsatellite instability occurring in familial and sporadic settings: parallel pathways of tumorigenesis. Am J Pathol 159:2107-2116