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[Cancer Research 53, 5849-5852, December 15, 1993]
© 1993 American Association for Cancer Research
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Genomic Instability in Colorectal Cancer: Relationship to Clinicopathological Variables and Family History1

Ragnhild A. Lothe2, Päivi Peltomäki, Gunn Iren Meling, Lauri A. Aaltonen, Minna Nyström-Lahti, Lea Pylkkänen, Ketil Heimdal, Tone I. Andersen, Pål Møller, Torleiv O. Rognum, Sophie D. Fosså, Tor Haldorsen, Frøydis Langmark, Anton Brøgger, Albert de la Chapelle and Anne-Lise Børresen

Department of Genetics, Institute for Cancer Research [R. A. L., K. H., T. I. A., P. M., A. B., A-L. B.], and Department of Medical Oncology and Radiotherapy [S. D. F.], The Norwegian Radium Hospital, 0310 Oslo, Norway; Department of Medical Genetics, P. O. Box 21, University of Helsinki, SF-00014 Helsinki, Finland [P. P., L. A. A., M. N-L., L. P., A. d. l. C.]; Institute of Forensic Medicine, The National Hospital, University of Oslo, 0027 Oslo, Norway [G. I. M., T. O. R.]; Surgical Department, Norwegian Lutheran Hospital, 0319 Oslo, Norway [G. I. M.]; Section of Medical Statistics, University of Oslo, 0317 Oslo, Norway [T. H.]; and the Norwegian Cancer Registry, Fritjof Nansens v.17, Oslo, Norway [F. L.]

Recent reports have suggested that one or more genes may cause replication errors (RER) during colorectal tumorigenesis. Additional alleles are seen in the tumors when analyzing random microsatellite loci. We have studied seven dinucleotide repeat loci, located on seven different chromosomes, by use of polymerase chain reaction amplification and denaturing polyacrylamide gel electrophoresis. We found that 16.5% (40 of 243) colorectal cancers showed RER at one or several loci (RER+). This includes 31% (4 of 13) among cases with a strong positive family history according to previously published criteria and 17% (35 of 207) among cases with no history of familial cancer. Interestingly, no significant association was found between RER+ tumors and a general familial clustering of cancer. Microsatellite instability was significantly associated with DNA diploid status of the tumor (P < 0.001), with the location of the tumor in the proximal colon (P < 0.001), and with poorly differentiated tumor phenotype (P < 0.001). Patients with RER+ at ≥ 2 loci tumors had an increased survival (P = 0.05).

We further analyzed 84 breast cancers and 86 male germ cell cancers using the same seven markers. None of the tumors were RER+, indicating that this phenomenon may be specific to certain types of tumors.

1 Supported by grants from the Norwegian Research Council for Science and Humanities, the Norwegian Cancer Society, the Academy of Finland, the Finnish Cancer Society, and the Sigrid Juselius Foundation. Part of this study was done at the Folkhalsan Institute of Genetics.

2 To whom requests for reprints should be addressed.

Received 10/ 9/93. Accepted 11/ 2/93.




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Gut, June 1, 2001; 48(6): 821 - 829.
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A. Loukola, K. Eklin, P. Laiho, R. Salovaara, P. Kristo, H. Jarvinen, J.-P. Mecklin, V. Launonen, and L. A. Aaltonen
Microsatellite Marker Analysis in Screening for Hereditary Nonpolyposis Colorectal Cancer (HNPCC)
Cancer Res., June 1, 2001; 61(11): 4545 - 4549.
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H. Elsaleh, B. Powell, K. McCaul, F. Grieu, R. Grant, D. Joseph, and B. Iacopetta
P53 Alteration and Microsatellite Instability Have Predictive Value for Survival Benefit from Chemotherapy in Stage III Colorectal Carcinoma
Clin. Cancer Res., May 1, 2001; 7(5): 1343 - 1349.
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T. Watanabe, T.-T. Wu, P. J. Catalano, T. Ueki, R. Satriano, D. G. Haller, A. B. Benson, and S. R. Hamilton
Molecular Predictors of Survival after Adjuvant Chemotherapy for Colon Cancer
N. Engl. J. Med., April 19, 2001; 344(16): 1196 - 1206.
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A. Duval, S. Rolland, A. Compoint, E. Tubacher, B. Iacopetta, G. Thomas, and R. Hamelin
Evolution of instability at coding and non-coding repeat sequences in human MSI-H colorectal cancers
Hum. Mol. Genet., March 1, 2001; 10(5): 513 - 518.
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J M Michael-Robinson, A-E Biemer-Huttmann, D M Purdie, M D Walsh, L A Simms, K G Biden, J P Young, B A Leggett, J R Jass, and G L Radford-Smith
Tumour infiltrating lymphocytes and apoptosis are independent features in colorectal cancer stratified according to microsatellite instability status
Gut, March 1, 2001; 48(3): 360 - 366.
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M. Alonso, R. Hamelin, M. Kim, K. Porwancher, T. Sung, P. Parhar, D. C. Miller, and E. W. Newcomb
Microsatellite Instability Occurs in Distinct Subtypes of Pediatric but not Adult Central Nervous System Tumors
Cancer Res., March 1, 2001; 61(5): 2124 - 2128.
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S. Fiumicino, A. Ercoli, G. Ferrandina, P. Hess, G. Raspaglio, M. Genuardi, V. Rovella, A. Bellacosa, L. Cicchillitti, S. Mancuso, et al.
Microsatellite Instability Is an Independent Indicator of Recurrence in Sporadic Stage I-II Endometrial Adenocarcinoma
J. Clin. Oncol., February 15, 2001; 19(4): 1008 - 1014.
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J. Alexander, T. Watanabe, T.-T. Wu, A. Rashid, S. Li, and S. R. Hamilton
Histopathological Identification of Colon Cancer with Microsatellite Instability
Am. J. Pathol., February 1, 2001; 158(2): 527 - 535.
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A. L. Bacon, S. M. Farrington, and M. G. Dunlop
Sequence interruptions confer differential stability at microsatellite alleles in mismatch repair-deficient cells
Hum. Mol. Genet., November 1, 2000; 9(18): 2707 - 2713.
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S. Markowitz
DNA Repair Defects Inactivate Tumor Suppressor Genes and Induce Hereditary and Sporadic Colon Cancers
J. Clin. Oncol., November 1, 2000; 18(90001): 75s - 80.
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J R JASS;, B CURRAN, K LENEHAN, H MULCAHY, O TIGHE, M A BENNETT, E W KAY, D P O'DONOGHUE, M LEADER, and D T CROKE
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Gut, October 1, 2000; 47(4): 597 - 598.
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C. VAURS-BARRIÈRE, F. PENAULT-LLORCA, V. LAPLACE-MARIEZE, N. PRESNEAU, C. M MAUGARD, M. FICHE, A. HARDOUIN, and Y.-J. BIGNON
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J. Med. Genet., October 1, 2000; 37(10): 32e - 32.
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D. J. Peel, A. Ziogas, E. A. Fox, M. Gildea, B. Laham, E. Clements, R. D. Kolodner, and H. Anton-Culver
Characterization of Hereditary Nonpolyposis Colorectal Cancer Families From a Population-Based Series of Cases
J Natl Cancer Inst, September 20, 2000; 92(18): 1517 - 1522.
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M. J. Sobrido, C. R. Pereira, F. Barros, J. Forteza, A. Carracedo, and M. Lema
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J. Neurol. Neurosurg. Psychiatry, September 1, 2000; 69(3): 369 - 375.
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J M D WHEELER, W F BODMER, and N J M. MORTENSEN
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Gut, July 1, 2000; 47(1): 148 - 153.
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A. Chao, F. Gilliland, C. Willman, N. Joste, I-M. Chen, N. Stone, J. Ruschulte, D. Viswanatha, P. Duncan, R. Ming, et al.
Patient and Tumor Characteristics of Colon Cancers with Microsatellite Instability: A Population-based Study
Cancer Epidemiol. Biomarkers Prev., June 1, 2000; 9(6): 539 - 544.
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A.-E. Biemer-Huttmann, M. D. Walsh, M. A. McGuckin, L. A. Simms, J. Young, B. A. Leggett, and J. R. Jass
Mucin Core Protein Expression in Colorectal Cancers with High Levels of Microsatellite Instability Indicates a Novel Pathway of Morphogenesis
Clin. Cancer Res., May 1, 2000; 6(5): 1909 - 1916.
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R. E. Wilentz, M. Goggins, M. Redston, V. A. Marcus, N. V. Adsay, T. A. Sohn, S. S. Kadkol, C. J. Yeo, M. Choti, M. Zahurak, et al.
Genetic, Immunohistochemical, and Clinical Features of Medullary Carcinoma of the Pancreas : A Newly Described and Characterized Entity
Am. J. Pathol., May 1, 2000; 156(5): 1641 - 1651.
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L Cawkwell, F Sutherland, H Murgatroyd, P Jarvis, S Gray, D Cross, N Shepherd, D Day, and P Quirke
Defective hMSH2/hMLH1 protein expression is seen infrequently in ulcerative colitis associated colorectal cancers
Gut, March 1, 2000; 46(3): 367 - 369.
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N. D. MacDonald, H. B. Salvesen, A. Ryan, O.-E. Iversen, L. A. Akslen, and I. J. Jacobs
Frequency and Prognostic Impact of Microsatellite Instability in a Large Population-based Study of Endometrial Carcinomas
Cancer Res., March 1, 2000; 60(6): 1750 - 1752.
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B Curran, K Lenehan, H Mulcahy, O Tighe, M A Bennett, E W Kay, D P O'Donoghue, M Leader, and D T Croke
Replication error phenotype, clinicopathological variables, and patient outcome in Dukes' B stage II (T3,N0,M0) colorectal cancer
Gut, February 1, 2000; 46(2): 200 - 204.
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R. Gryfe, H. Kim, E. T.K. Hsieh, M. D. Aronson, E. J. Holowaty, S. B. Bull, M. Redston, and S. Gallinger
Tumor Microsatellite Instability and Clinical Outcome in Young Patients with Colorectal Cancer
N. Engl. J. Med., January 13, 2000; 342(2): 69 - 77.
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D. A. VASSILAKIS, G. SOURVINOS, M. MARKATOS, K. PSATHAKIS, D. A. SPANDIDOS, N. M. SIAFAKAS, and D. BOUROS
Microsatellite DNA Instability and Loss of Heterozygosity in Pulmonary Sarcoidosis
Am. J. Respir. Crit. Care Med., November 1, 1999; 160(5): 1729 - 1733.
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S. A. Kuismanen, M. T. Holmberg, R. Salovaara, P. Schweizer, L. A. Aaltonen, A. de la Chapelle, M. Nystrom-Lahti, and P. Peltomaki
Epigenetic phenotypes distinguish microsatellite-stable and -unstable colorectal cancers
PNAS, October 26, 1999; 96(22): 12661 - 12666.
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M. Miyazaki, T. Furuya, A. Shiraki, T. Sato, A. Oga, and K. Sasaki
The Relationship of DNA Ploidy to Chromosomal Instability in Primary Human Colorectal Cancers
Cancer Res., October 1, 1999; 59(20): 5283 - 5285.
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Gut, September 1, 1999; 45(3): 325 - 326.
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L Cawkwell, S Gray, H Murgatroyd, F Sutherland, L Haine, M Longfellow, S O'Loughlin, D Cross, O Kronborg, C Fenger, et al.
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Y. Daigo, Y. Furukawa, T. Kawasoe, H. Ishiguro, M. Fujita, S. Sugai, S. Nakamori, G.-J. Liefers, R. A. E. M. Tollenaar, C. J. H. van de Velde, et al.
Absence of Genetic Alteration at Codon 531 of the Human c-src Gene in 479 Advanced Colorectal Cancers from Japanese and Caucasian Patients
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I. D. Nicholl and M. G. Dunlop
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J Natl Cancer Inst, August 4, 1999; 91(15): 1267 - 1269.
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K. C. Halling, A. J. French, S. K. McDonnell, L. J. Burgart, D. J. Schaid, B. J. Peterson, L. Moon-Tasson, M. R. Mahoney, D. J. Sargent, M. J. O'Connell, et al.
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J Natl Cancer Inst, August 4, 1999; 91(15): 1295 - 1303.
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G. Lanza, R. Gafa, M. Matteuzzi, and A. Santini
Medullary-Type Poorly Differentiated Adenocarcinoma of the Large Bowel: A Distinct Clinicopathologic Entity Characterized by Microsatellite Instability and Improved Survival
J. Clin. Oncol., August 1, 1999; 17(8): 2429 - 2429.
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F. A. Sinicrope, J. Hart, H.-A. Hsu, M. Lemoine, F. Michelassi, and L. C. Stephens
Apoptotic and Mitotic Indices Predict Survival Rates in Lymph Node-negative Colon Carcinomas
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W. S. Samowitz, M. L. Slattery, J. D. Potter, and M. F. Leppert
BAT-26 and BAT-40 Instability in Colorectal Adenomas and Carcinomas and Germline Polymorphisms
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R. Dolcetti, A. Viel, C. Doglioni, A. Russo, M. Guidoboni, E. Capozzi, N. Vecchiato, E. Macri, M. Fornasarig, and M. Boiocchi
High Prevalence of Activated Intraepithelial Cytotoxic T Lymphocytes and Increased Neoplastic Cell Apoptosis in Colorectal Carcinomas with Microsatellite Instability
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G. Sourvinos, J. Parissis, F. Sotsiou, D. L. Arvanitis, and D. A. Spandidos
Detection of microsatellite instability in sporadic cardiac myxomas
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Hypermethylation of the hMLH1 Gene Promoter in Human Gastric Cancers with Microsatellite Instability
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W. Edelmann, K. Yang, M. Kuraguchi, J. Heyer, M. Lia, B. Kneitz, K. Fan, A. M. C. Brown, M. Lipkin, and R. Kucherlapati
Tumorigenesis in Mlh1 and Mlh1/Apc1638N Mutant Mice
Cancer Res., March 1, 1999; 59(6): 1301 - 1307.
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S R Brown, P J Finan, L Cawkwell, P Quirke, and D T Bishop
Frequency of replication errors in colorectal cancer and their association with family history
Gut, October 1, 1998; 43(4): 553 - 557.
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T. Fujiwara, J. M. Stolker, T. Watanabe, A. Rashid, P. Longo, J. R. Eshleman, S. Booker, H. T. Lynch, J. R. Jass, J. S. Green, et al.
Accumulated Clonal Genetic Alterations in Familial and Sporadic Colorectal Carcinomas with Widespread Instability in Microsatellite Sequences
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T. L. DeWeese, J. M. Shipman, N. A. Larrier, N. M. Buckley, L. R. Kidd, J. D. Groopman, R. G. Cutler, H. te Riele, and W. G. Nelson
Mouse embryonic stem cells carrying one or two defective Msh2 alleles respond abnormally to oxidative stress inflicted by low-level radiation
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