Mutation in the mismatch repair gene Msh6 causes cancer susceptibility

Cell

Volumn 91, Issue 4, 1997, Pages 467-477

  Edelmann, Winfried ^a   Yang, Kan ^b   Umar, Asad ^c   Heyer, Joerg ^a   Lau, Kirkland ^a   Fan, Kunhua ^b   Liedtke, Wolfgang ^a   Cohen, Paula E ^a   Kane, Michael F ^d,e   Lipford, James R ^d   Yu, Nianjun ^f   Crouse, Gray F ^f   Pollard, Jeffrey W ^a   Kunkel, Thomas ^c   Lipkin, Martin ^b   Kolodner, Richard ^d,e   Kucherlapati, Raju ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^d DANA FARBER CANCER INSTITUTE   (United States)

^e LUDWIG INSTITUTE FOR CANCER RESEARCH   (United States)

^f EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BASE MISPAIRING; CANCER SUSCEPTIBILITY; CARCINOGENESIS; GENE DELETION; GENE INSERTION; GENE REARRANGEMENT; GENETIC SUSCEPTIBILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; T CELL LYMPHOMA;

ANIMALIA;

EID: 0030709433     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80433-X     Document Type: Article

References (51)

1. Acharya, S., Wilson, T., Gradia, S., Kane, M.F., Guerrette, S., Marsischky, G.T., Kolodner, R., and Fishel, R. (1996). hMSH2 forms specific mispair-binding complexes with hMSHSand hMSH6. Proc. Natl. Acad. Sci. USA 93, 13629-13634.
2. Aaltonen, L.A., Peltomaki, P., Leach, F., Sistonen, P., Pylkkanen, S.M., Mecklin, J.-P., Jarvinen, H., Powell, S., Jen, J., Hamilton, S.R., et al. (1993). Clues to the pathogenesis of familial colorectal cancer. Science 260, 812-816.
3. Baker, S.M., Bronner, C.E., Zhang, I., Plug, A., Robatzek, M., Warren, G., Elliott, E.A., Yu, J., Ashley, T., Arnheim, N., Flavell, R.A., and Liskay, R.M. (1995). Male mice defective in the DNA mismatch repair gene PMS2exhibit abnormal chromosome synapsis in meiosis. Cell 82, 309-320.
4. Baker, S.M., Plug, A.W., Prolla, T.A., Bronner, C.E., Harris, A.C., Yao, X., Christie, D.M., Monell, C., Arnheim, N., Bradley, A., et al. (1996). Involvement of mouse MIh1 in DNA mismatch repair and meiotic crossing over. Nat. Genet. 13, 336-342.
5. Bhattacharyya, N.P., Skandalis, A., Ganesh, A., Groden, J., and Meuth, M. (1994). Mutator phenotypein human colorectal carcinoma cell lines. Proc. Natl. Acad. SCi. USA 91, 6319-6323.
6. Boyer, J.C., Umar, A., Risinger, J., Kane, M.F., Lipford, J., Barrett, J.C., Kolodner, R.D., and Kunkel, T.A. (1995). Microsatellite instability, mismatch repair deficiency and genetic defects in human cancer cell lines. Cancer Res. 55, 6062-6070.
7. Bronner, C.E., Baker, S.M., Morrison, P.T., Warren, G., Smith, L.G., Lescoe, M.K., Kane, M., Earabino, C., Lipford, J., Lindblom, A., et al. (1994). Mutation in the DNA mismatch repair gene homologue hMLH1 is associated with hereditary nonpolyposis colon cancer. Nature 368, 258-261.
8. Corradi, A., Croci, L., Stayton, C.L., Gulisano, M., Boncinelli, E., and Consalez, G.G. (1996). cDNA sequence, map, and expression of the murine homolog of GTBP, a DNA mismatch repair gene. Genomics 36, 288-295.
9. da Costa, L.T., Liu, B., el-Deiry, W., Hamilton, S.R., Kinzler, K.W., Vogelstein, B., Markowitz, S., Willson, J.K., dela Chapelle, A., Downey, K.M., and So, A.G. (1995). Polymerase delta variants in RER colorectal tumours. Nat. Genet. 9, 10-11.
10. de Wind, N., Dekker, M., Berns, A., Radman, M., and te Riele, H. (1995). Inactivation of the mouse Msh2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer. Cell 82, 321-330.
11. Dietrich, W.F., Miller, J.C., Steen, R.G., Merchant, M., Damron, D., Naht, R., Gross, A., Joyce, D.C., Wessel, M., Dredge, R.D., et al. (1994). A genetic map of the mouse with 4,006 simple sequence length polymorphisms. Nat. Genet. 7, 220-245.
12. Drummond, J.T., Li, G.-M., Longley, M.J., and Modrich, P. (1995). Mismatch recognition by an hMSH2-GTBP heterodimer and differential repair defects in tumor cells. Science 268, 1909-1912.
13. Edelmann, W., Cohen, P.E., Kane, M., Lau, K., Morrow, B., Bennett, S., Umar, A., Kunkel, T., Cattoretti, G., Chaganti, R., et al. (1996). Meiotic pachytene arrest in MLH1-deficient mice. Cell 85, 1125-1134.
14. Fishel, R., and Kolodner, R.D. (1995). Identification of mismatch repair genes and their role in the development of cancer. Curr.Opin. Genet. Dev. 5, 382-395.
15. Fishel, R.A., Lescoe, M.K., Rao, M.R.S., Copeland, N., Jenkins, N., Garber, J., Kane, M., and Kolodner, R. (1993). The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer. Cell 75, 1027-1038.
16. Habraken, Y., Sung, P., Prakash, L., and Prakash, S. (1996). Binding of insertion/deletion DNA mismatches by the heterodimer of yeast mismatch repair proteins MSH2 and MSH3. Curr. Biol. 6, 1185-1187.
17. Huang, J., Papadopoulos, N., McKinley, A.J., Farrington, S.M., Curtis, L.J., Wyllie, A.M., Zheng, S., Willson, J.K.V., Markowitz, S.D., Morin, P., et al. (1996). APC mutations in colorectal tumors with mismatch repair deficiency. Proc. Natl. Acad. Sci. USA 93, 9049-9054.
18. loffe, E., Liu, Y., Bhaumik, M., Poirier, F., Factor, S.M., and Stanley, P. (1995). WW6: an embryonic stem cell line with an inert genetic marker that can be traced in chimeras. Proc. Natl. Acad. Sci. USA 92, 7357-7361.
19. Johnson, R.E., Kovvali, G.K., Prakash, L., and Prakash, S. (1996). Requirement of the yeast MSH3 and MSH6 genes for MSH2-dependent genomic stability. J. Biol. Chem. 271, 7285-7288.
20. Kolodner, R. (1996). Biochemistry and genetics of eukaryotic mismatch repair. Genes Dev. 10, 1433-1442.
21. Kolodner, R.D., and Alani, E. (1994). Mismatch repair and cancer susceptibility. Curr. Opin. Biotech. 5, 585-594.
22. Kolodner, R.D., Hall, N.R., Lipford, J.R., Kane, M.F., Rao, M.R.S., Morrison, P., Wirth, L., Finan, P.J., Burn, J., Chapman, P., et al. (1994). Structure of the human MSH2 locus and analysis of two Muir-Torre kindreds for msh2 mutations. Genomics 24, 516-526.
23. Kolodner, R.D., Hall, N.R., Lipford, J.R., Kane, M.F., Morrison, P., Finan, P.J., Burn, J., Chapman, P., Earabino, C., Merchant, E., and Bishop, DT. (1995). Structure of the human MLH1 locus and analysis of HNPCC kindreds for MIh1 mutations. Cancer Res. 55, 242-248.
24. Lazar, V., Grandjouan, S., Bognel, C., Couturier, D., Rougier, P., Bellet, D., and Bressac-de Paillerets, B. (1994). Accumulation of multiple mutations in tumour suppressor genes during colorectal tumorigenesis in HNPCC patients. Hum. Mol. Genet. 3, 2257-2260.
25. Leach, F.S., Nicolaides, N.C., Papadopoulos, N., Liu, B., Jen, J., Parsons, R., Peltomaki, P., Sistonen, P., Aaltonen, L.A., Nystrom-Lahti, M., et al. (1993). Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer. Cell 75, 1215-1225.
26. Li, G.-M., and P. Modrich. (1995). Restoration of mismatch repair to nuclear extracts of H6 colorectal tumor cells by a heterodimer of human MutL homologs. Proc. Natl. Acad. Sei. USA 92, 1950-1954.
27. Lindblom, A., Tannergard, P., Nordenskjold, W., and Nordenskjold, M. (1993). Genetic mapping of a second locus predisposing to hereditary non-polyposis colon cancer. Nat. Genet. 5, 279-282.
28. Liu, B., Parsons, R., Papadopoulos, N., Nicolaides, N.C., Lynch, H.T., Watson, P., Jass, J.R., Dunlop, M., Wyllie, A., Peltomaki, P., et al. (1996). Analysis of mismatch repair genes in hereditary non-polyposis colorectal cancer patients. Nat. Med. 2, 169-174.
29. Marsischky, G.T., Filosi, N., Kane, M.F., and Kolodner, R. (1996). Redundancy of Saccharomyces cerevisiae MSH3 and MSH6 in MSH2-dependent mismatch repair. Genes Dev. 10, 407-420.
30. Mansour, S.L., Thomas, K.R., and Capecchi, M.R. (1988). Disruption of the proto-oncogene int-2 in mouse embryo-derived stem cells: a general strategy for targeting mutations to non-selectable genes. Nature 336, 348-352.
31. Malkhosyan, S., McCarty, A., Sawai, H., and Perucho, M. (1996). Differences in the spectrum of spontaneous mutations in the hprt gene between tumor cells of the microsatellite mutator phenotype. Mut. Res. 316, 249-259.
32. Modrich, P. (1991). Mechanisms and biological effects of mismatch repair. Annu. Rev. Genet. 25, 229-253.
33. Modrich, P., and Lahue, R. (1996). Mismatch repair in replication fidelity, genetic recombination and cancer biology. Annu. Rev. Biochem. 65, 101-133.
34. Nicolaides, N.C., Papadopoulos, N., Liu, B., Wei, Y., Carter, K.C., Ruben, S.M., Rosen, C.A., Haseltine, W.A., Fleischmann, R.D., Fraser, C.M., et al. (1994). Mutations of two PMS homologues in hereditary nonpolyposis colon cancer. Nature 371, 75-80.
35. Palombo, F., Gallinari, P., Iaccarino, I., Lettieri, T., Hughes, M., D'Arrigo, A., Truong, O., Hsuan, J.J., and Jiricny, J. (1995). GTBP, a 160 kD protein essential for mismatch binding activity in human cells. Science 268, 1912-1914.
36. Palombo, F., Iaccarino, I., Nakajima, E., Ikejima, M., Shimada, T., and Jiricny, J. (1996). hMutSbeta, a heterodimer of hMSH2 and hMSH3, binds to insertion/deletion loops in DNA. Curr. Biol. 6, 1181-1184.
37. Papadopoulos, N., Nicolaides, N.C., Wei, Y.-F., Ruben, S.M., Carter, K.C., Rosen, C.A., Haseltine, W.A., Fleischmann, R.D., Fraser, C.M., Adams, M.D., et al. (1994). Mutation of a mutL homolog in hereditary colon cancer. Science 263, 1625-1629.
38. Papadopoulos, N., Nicolaides, N.C., Liu, B., Parsons, R.E., Lengauer, C., Palombo, F., D'Arrigo, A., Markowitz, S., Wilson, J.K.V., Kinzler, K.W., et al. (1995). Mutations of GTBP in genetically unstable tumors. Science 268, 1915-1917.
39. Parsons, R., Li, G.-L., Longley, M., Modrich, P., Liu, B., Berk, T., Hamilton, S.R., Kinzler, K.W., and Vogelstein, B. (1995). Mismatch repair deficiency in phenotypically normal human cells. Science 268, 738-740.
40. Peltomaki, P., Vasen, H.F.A., and the International Collaborative Group on HNPCC. (1997). Mutations predisposing to hereditary non-polyposis colorectal cancer: database and results of a collaborative study. Gastroenterology, in press.
41. Prolla, T.A., Pang, Q., Alani, E., Kolodner, R.D., and Liskay, R.M. (1994). Interactions between the MSH2, MLH1 and PMS1 proteins during the initiation of DNA mismatch repair. Science 265, 1091-1093.
42. Reitmair, A.H., Schmits, R., Ewel, A., Bapat, B., Redston, M., Mitri, A., Waterhouse, P., Mittrucker, H.W., Wakeham, A., Liu, B., et al. (1995). MSH2 deficient mice are viable and susceptible to lymphoid tumours. Nat. Genet. 11, 64-70.
43. Reitmair, A.H., Redston, M., Cai, J.C., Chuang, T.C., Bjerknes, M., Cheng, H., Hay, K., Gallinger, S., Bapat, B., and Mak, T.W. (1996). Spontaneous intestinal carcinomas and skin neoplasms in Msh2-deficient mice. Cancer Res. 56, 3842-3849.
44. Risinger, J.I., Umar, A., Barrett, J.C. and Kunkel, T.A. (1995). A hPMS2 mutant cell line is defective in strand-specific mismatch repair. J. Biol. Chem. 270, 18183-18186.
45. Risinger, J.I., Umar, A., Boyd, J., Berchuck, A., Kunkel, T.A., and Barrett, J.C. (1996). Mutation of MSH3 in endometrial cancer and evidence for its functional role in heteroduplex repair. Nat. Genet. 14, 102-105.
46. Shibata, D., Peinado, M.A., Ionov, S., Malkhosyan, S., and Perucho, M. (1994). Genomic instability in repeated sequences is an early somatic event in colorectal tumorigenesis that persists after transformation. Nat. Genet. 6, 273-281.
47. Sirotkin, A.M., Edelmann, W., Cheng, G., Klein-Szantos, A., Kucherlapati, R., and Skoultchi, A.I. (1995). Mice develop normally without the H10 linker histone. Proc. Natl. Acad. Sci. USA 92, 6434-6438.
48. Sia, E.A., Kokoska, R.J., Dominska, M., Greenwell, P., and Petes, T.D. (1997). Microsatellite instability in yeast: dependence on repeat unit size and DNA mismatch repair genes. Mol. Cell. Biol. 17, 2851-2858.
49. Thomas, D.C., Roberts, J.D., and Kunkel, T.A. (1991). Heteroduplex repair in extracts of human HeLa cells. J. Biol. Chem. 266, 3744-3751.
50. Thomas, D.C., Umar, A., and Kunkel, T.A. (1995). Measurement of heteroduplex repair in human cell extracts. In Methods: A Companion to Methods in Enzymology 7, E.C. Friedberg, ed. (New York: Academic Press), pp. 187-197.
51. Umar, A., Boyer, J.C., and Kunkel, T.A. (1994). DNA loop repair by human cell extracts. Science 266, 814-816.