Molecular mechanisms underlying hereditary nonpolyposis colorectal carcinoma

Journal of the National Cancer Institute

Volumn 88, Issue 5, 1996, Pages 240-251

  Rhyu, Michelle S ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL GENE; BASE MISPAIRING; CARCINOGENESIS; COLORECTAL CARCINOMA; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; EUKARYOTE; FAMILIAL CANCER; GENE MUTATION; NONHUMAN; PROKARYOTE; REVIEW;

BACTERIA; BASE SEQUENCE; COLORECTAL NEOPLASMS, HEREDITARY NONPOLYPOSIS; DNA REPAIR; DNA REPLICATION; HUMANS; MOLECULAR SEQUENCE DATA; RECOMBINATION, GENETIC;

EID: 0029990917     PISSN: 00278874     EISSN: None     Source Type: Journal    
DOI: 10.1093/jnci/88.5.240     Document Type: Review

References (123)

1. Loeb LA. Endogenous carcinogenesis: molecular oncology into the twenty-first century - presidential address. Cancer Res 1989;49:5489-96.
2. Loeb LA. Mutator phenotype may be required for multistage carcinogenesis. Cancer Res 1991;51:3075-9.
3. Sankaranarayanan K, Chakraborty R. Cancer predisposition, radiosensitivity and the risk of radiation-induced cancers. I. Background. Radiation Res 1995;143:121-43.
4. Bootsma D, Hoeijmakers JH. The molecular basis of nucleotide excision repair syndromes. Mutat Res 1994;307:15-23.
5. 2 cell cycle checkpoint. Cancer Res 1995;55:3721-5.
6. Peltomaki P, Aaltonen LA, Sistonen P, Pylkkanen L, Mecklin JP, Jarvinen H, et al. Genetic mapping of a locus predisposing to human colorectal cancer. Science 1993;260:810-2.
7. Lindblom A, Tannergard P, Werelius B, Nordenskjold M. Genetic mapping of a second locus predisposing to hereditary non-polyposis colon cancer. Nat Genet 1993;5:279-82.
8. Nystrom-Lahti M, Sistonen P, Mecklin JP, Pylkkanen L, Aaltonen LA, Jarvinen H, et al. Close linkage to chromosome 3p and conservation of ancestral founding haplotype in hereditary nonpolyposis colorectal cancer families. Proc Natl Acad Sci U S A 1994;91:6054-8.
9. Modrich P, Lahue R. Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu Rev Biochem. In press.
10. Marra G, Boland CR. Hereditary nonpolyposis colorectal cancer: the syndrome, the genes, and historical perspectives. J Natl Cancer Inst 1995; 87:1114-25.
11. Kolodner RD. Mismatch repair: mechanisms and relationship to cancer susceptibility. Trends Biochem Sci 1995;20:397-401.
12. Van Houten B, McCullough A. Nucleotide excision repair in E. coli. Ann N Y Acad Sci 1994;726:236-51.
13. Seeberg E, Eide L, Bjoras M. The base excision repair pathway. Trends Biochem Sci 1995;20:391-7.
14. Kow YW. Base excision repair in E. coli - an overview. Ann N Y Acad Sci 1994;726:178-80.
15. Modrich P. Mechanisms and biological effects of mismatch repair. Annu Rev Genet 1991;25:229-53.
16. Claverys JP, Lacks SA. Heteroduplex deoxyribonucleic acid base mismatch repair in bacteria. Microbiol Rev 1986;50:133-65.
17. Cox EC. Bacterial mutator genes and the control of spontaneous mutation. Annu Rev Genet 1976;10:135-56.
18. Holliday RA. A mechanism for gene conversion in fungi. Genet Res 1964;5:282-304.
19. Ephrussi-Taylor H, Gray TC. Genetic studies of recombining DNA in pneumococcal transformation. J Gen Physiol 1966;49:211-31.
20. Lacks S. Mutants of Diplococcus pneumoniae that lack deoxyribonucleases and other activities possibly pertinent to genetic transformation. J Bacteriol 1970;101:373-83.
21. Tiraby JG, Fox MS. Marker discrimination in transformation and mutation of pneumococcus. Proc Natl Acad Sci U S A 1973;70:3541-5.
22. Radman M, Wagner R. Mismatch repair in Escherichia coli. Annu Rev Genet 1986;20:523-38.
23. Lu AL, Clark S, Modrich P. Methyl-directed repair of DNA base-pair mismatches in vitro. Proc Natl Acad Sci USA 1983;80:4639-43.
24. Lu AL, Welsh K, Clark S, Su SS, Modrich P. Repair of DNA base-pair mismatches in extracts of Escherichia coli. Cold Spring Harb Symp Quant Biol 1984;49:589-96.
25. Modrich P. Methyl-directed DNA mismatch correction. J Biol Chem 1989;264:6597-600.
26. Wagner R Jr, Meselson M. Repair tracts in mismatched DNA hetero-duplexes. Proc Natl Acad Sci U S A 1976;73:4135-9.
27. Lyons SM, Schendel PF. Kinetics of methylation in Escherichia coli K-12. J Bacteriol 1984;159:421-3.
28. Glickman BW, Radman M. Escherichia coli mutator mutants deficient in methylation-instructed DNA mismatch correction. Proc Natl Acad Sci USA 1980;77:1063-7.
29. McGraw BR, Marinus MG. Isolation and characterization of Dam+ revertants and suppressor mutations that modify secondary phenotypes of dam3 strains of Escherichia coli K-12. Mol Gen Genet 1980;178:309-15.
30. Nevers P, Spatz HC. Escherichia coli mutants uvr D and uvr E deficient in gene conversion of lambda-heteroduplexes. Mol Gen Genet 1975;139: 233-43.
31. Welsh KM, Lu AL, Clark S, Modrich P. Isolation and characterization of the Escherichia coli mutH gene product. J Biol Chem 1987;262: 15624-9.
32. Su SS, Modrich P. Escherichia coli mutS-encoded protein binds to mismatched DNA base pairs. Proc Natl Acad Sci U S A 1986;83:5057-61.
33. Grilley M, Welsh KM, Su SS, Modrich P. Isolation and characterization of the Escherichia coli mutL gene product. J Biol Chem 1989;264:1000-4.
34. Kumura K, Sekiguchi M. Identification of the uvrD gene product of Escherichia coli as DNA helicase II and its induction by DNA-damaging agents. J Biol Chem 1984;259:1560-5.
35. Maples VF, Kushner SR. DNA repair in Escherichia coli: identification of the uvrD gene product. Proc Natl Acad Sci USA 1982;79:5616-20.
36. Lahue RS, Au KG, Modrich P. DNA mismatch correction in a defined system. Science 1989;245:160-4.
37. Cooper DL, Lahue RS, Modrich P. Methyl-directed mismatch repair is bidirectional. J Biol Chem 1993;268:11823-9.
38. Grilley M, Griffith J, Modrich P. Bidirectional excision in methyldirected mismatch repair. J Biol Chem 1993;268:11830-7.
39. Su SS, Grilley M, Thresher R, Griffith J, Modrich P. Gap formation is associated with methyl-directed mismatch correction under conditions of restricted DNA synthesis. Genome 1989;31:104-11.
40. Au KG, Welsh K, Modrich P. Initiation of methyl-directed mismatch repair. J Biol Chem 1992;267:12142-8.
41. Loeb LA, Kunkel TA. Fidelity of DNA synthesis. Annu Rev Biochem 1982;52:429-57.
42. Echols H, Goodman MF. Fidelity mechanisms in DNA replication. Annu Rev Biochem 1991;60:477-511.
43. Topal MD, Fresco JR. Complementary base pairing and the origin of substitution mutations. Nature 1976;263:285-9.
44. Drake JW. Comparative rates of spontaneous mutation. Nature 1969;221: 1132.
45. Fersht AR, Knill-Jones JW. DNA polymerase accuracy and spontaneous mutation rates: frequencies of purine-purine, purine-pyrimidine, and pyrimidine-pyrimidine mismatches during DNA replication. Proc Natl Acad Sci U S A 1981;78:4251-5.
46. Brutlag D, Kornberg A. Enzymatic synthesis of deoxyribonucleic acid. 36. A proofreading function for the 3′ leads to 5′ exonuclease activity in deoxyribonucleic acid polymerases. J Biol Chem 1972;247:241-8.
47. Scheuermann R, Tam S, Burgers PM, Lu C, Echols H. Identification of the epsilon-subunit of Escherichia coli DNA polymerase II holoenzyme as the dnaQ gene product: a fidelity subunit for DNA replication. Proc Natl Acad Sci U S A 1983;80:7085-9.
48. Maloney DH, Fogel S. Mitotic recombination in yeast: isolation and characterization of mutants with enhanced spontaneous mitotic gene conversion rates. Genetics 1980;94:825-39.
49. Feinstein SI, Low KB. Hyper-recombining recipient strains in bacterial conjugation. Genetics 1986;113:13-33.
50. Haber JE. Exploring the pathways of homologous recombination. Curr Opin Cell Biol 1992;4:401-12.
51. West SC. The processing of recombination intermediates: mechanistic insights from studies of bacterial proteins. Cell 1994;76:9-15.
52. Alani E, Reenan RA, Kolodner RD. Interaction between mismatch repair and genetic recombination in Saccharomyces cerevisiae. Genetics 1994; 137:19-39.
53. Shen P, Huang HV. Homologous recombination in Escherichia coli: dependence on substrate length and homology. Genetics 1986;112:441-57.
54. Rayssiguier C, Thaler DS, Radman M. The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature 1989;342:396-401.
55. Radman M, Matic I, Halliday JA, Taddei F. Editing DNA replication and recombination by mismatch repair: from bacterial genetics to mechanisms of predisposition to cancer in humans. Philos Trans R Soc Lond B Biol Sci 1995;347:97-103.
56. Petit MA, Dimpfl J, Radman M, Echols H. Control of large chromosomal duplications in Escherichia coli by the mismatch repair system. Genetics 1991;129:327-32.
57. Worth L Jr, Clark S, Radman M, Modrich P. Mismatch repair proteins MutS and MutL inhibit RecA-catalyzed strand transfer between diverged DNAs. Proc Natl Acad Sci USA 1994;91:3238-41.
58. Selva EM, New L, Crouse GF, Lahue RS. Mismatch correction acts as a barrier to homeologous recombination in Saccharomyces cerevisiae. Genetics 1995;139:1175-88.
59. Williamson MS, Game JC, Fogel S. Meiotic gene conversion mutants in Saccharomyces cerevisiae. I. Isolation and characterization of pmsl-1 and pms1-2. Genetics 1985;110:609-46.
60. Bishop DK, Williamson MS, Fogel S, Kolodner RD. The role of heteroduplex correction in gene conversion in Saccharomyces cerevisiae. Nature 1987;328:362-4.
61. Bishop DK, Andersen J, Kolodner RD. Specificity of mismatch repair following transformation of Saccharomyces cererisiae with heleroduplex plasmid DNA. Proc Natl Acad Sci U S A 1989;86:3713-7.
62. Kramer B, Kramer W, Williamson MS, Fogel S. Heteroduplex DNA correction in Saccharomyces cerevisiae is mismatch specific and requires functional PMS genes. Mol Cell Biol 1989;9:4432-40.
63. Kramer W, Kramer B, Williamson MS, Fogel S. Cloning and nucleotide sequence of DNA mismatch repair gene PMS1 from Saccharomyces cerevisiae: homology of PMS/ to procaryotic MutL and HexB. J Bacteriol 1989;171:5339-46.
64. Reenan RA, Kolodner RD. Characterization of insertion mutations in the Saccharomyces cerevisiae MSH1 and MSH2 genes: evidence for separate mitochondrial and nuclear functions. Genetics 1992;132:975-85.
65. New L, Liu K, Crouse GF. The yeast gene MSH3 defines a new class of eukaryotic MutS homologues. Mol Gen Genet 1993;239:97-108.
66. Prolla TA, Pang Q, Alani E, Kolodner RD, Liskay RM. MLH1, PMSI, and MSH2 interactions during the initiation of DNA mismatch repair in yeast. Science 1994;265:1091-3.
67. Bhattacharyya NP, Skandalis A, Ganesh A, Groden J, Meuth M. Mutator phenotypes in human colorectal carcinoma cell lines. Proc Natl Acad Sci USA 1994;91:6319-23.
68. Koi M, Umar A, Chauhan DP, Cheriar SP, Carethers JM, Kunkel TA, et al. Human chromosome 3 corrects mismatch repair deficiency and microsatellite instability and reduces N-methyl-N′-nitro-N-nitrosoguanidine tolerance in colon tumor cells with homozygous hMLH1 mutation [published erratum appears in Cancer Res 1995;55:201]. Cancer Res 1994;54:4308-12.
69. Fram RJ, Cusick PS, Wilson JM, Marinus MG, Mismatch repair of cisdiamminedichloroplatinum(II)-induced DNA damage. Mol Pharmacol 1985;28:51-5.
70. Coulondre C, Miller JH, Farabaugh PJ, Gilbert W. Molecular basis of base substitution hot spots in Escherichia coli. Nature 1978;274:775-80.
71. Ehrlich M, Zhang XY, Inamdar NM. Spontaneous deamination of cytosine and 5-methylcytosine residues in DNA and replacement of 5-methylcytosine residues with cytosine residues. Mutat Res 1990;238:277-86.
72. Rideout WM 3d, Coetzee GA, Olumi AF, Jones PA. 5-Methylcytosine as an endogenous mutagen in the human LDL receptor and p53 genes. Science 1990;249:1288-90.
73. Zell R, Fritz HJ. DNA mismatch-repair in Escherichia coli counteracting the hydrolytic deamination of 5-methyl-cytosine residues. EMBOJ 1987; 6:1809-15.
74. Lieb M, Bacterial genes mutL, mutS, and dem participate in repair of mismatches at 5-methylcytosine sites. J Bacteriol 1987;169:5241-6.
75. 6-methylguanine residues in E. coli DNA. Nature 1982;296:868-9.
76. Branch P, Aquilina G, Bignami M, Karran P. Defective mismatch binding and mutator phenotype in cells tolerant to DNA damage. Nature 1993; 362:652-4.
77. Aquilina G, Hess P, Branch P, MacGoech C. Casciano I, Karran P, et al. A mismatch recognition defect in colon carcinoma confers DNA microsatellite instability and a mutator phenotype. Proc Natl Acad Sci USA 1944;91:8905-9.
78. Glazer PM, Sarkar SN, Chisholm GE, Summers WC. DNA mismatch repair detected in human cell extracts. Mol Cell Biol 1987;7:218-24.
79. Brown TC, Jiricny J. Different base/base mispairs are corrected with different efficiencies and specificities in monkey kidney cells. Cell 1988; 54:705-11.
80. Holmes J Jr, Clark S, Modrich P. Strand-specific mismatch correction in nuclear extracts of human and Drosophila melanogaster cell lines. Proc Natl Acad Sci USA 1990;87:5837-41.
81. Thomas DC, Roberts JD, Kunkel TA, Heteroduplex repair in extracts of human HeLa cells. J Biol Chem 1991;266:3744-51.
82. Varlet I, Radman M, Brooks P. DNA mismatch repair in Xenopus egg extracts: repair efficiency and DNA repair synthesis for all single base-pair mismatches. Proc Natl Acad Sci USA 1990;87:7883-7.
83. Boland CR, Troncale FJ. Familial colonic cancer without antecedent polyposis. Ann Intern Med 1984;100:700-1.
84. Lynch HT, Smyrk TC, Watson P, Lanspa SJ, Lynch JF, Lynch PM, et al. Genetics, natural history, tumor spectrum, and pathology of hereditary nonpolyposis colorectal cancer: an updated review. Gastroenterology 1993;104:1535-49.
85. Bailey-Wilson JE, Elston RC, Schuelke GS, Kimberling W, Albano W, Lynch JF, et al. Segregation analysis of hereditary nonpolyposis colorectal cancer. Genet Epidemiol 1986;3:27-38.
86. Thibodeau SN, Bren G, Schaid D. Microsatellite instability in cancer of the proximal colon [see comment citation in Medline]. Science 1993;260:816-9.
87. Ionov Y, Peinado MA, Malkhosyan S, Shibata D, Perucho M. Ubiquitous somatic mutations in simple repeated sequences reveal a new mechanism for colonic carcinogenesis. Nature 1993;363:558-61.
88. Aaltonen LA, Peltomaki P, Leach FS, Systonen P, Pylkkanen L, Mecklin JP, et al. Clues to the pathogenesis of familial colorectal cancer [see comment citation in Medline]. Science 1993;260:812-6.
89. Leach FS, Nicolaides NC, Papadopoulos N, Liu B, Jen J, Parsons R, et al. Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer. Cell 1993;75:1215-25.
90. Strand M, Prolla TA, Liskay RM, Petes TD. Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair (published erratum appears in Nature 1994;368:569] [see comment citation in Medline]. Nature 1993;365:274-6.
91. Fishel R, Lescoe MK, Rao MR, Copeland NG, Jenkins NA, Garber J, et al. The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer [published erratum appears in Cell 1994;77:167]. Cell 1993;75:1027-38.
92. Reenan RA, Kolodner RD. Isolation and characterization of two Saccharomyces cerevisiae genes encoding homologs of the bacterial Hex A and MutS mismatch repair proteins. Genetics 1992;132:963-73.
93. Parsons R, Li GM, Longley MJ, Fang WH, Papadopoulos N, Jen J, et al. Hypermutability and mismatch repair deficiency in RER+ tumor cells. Cell 1993;75:1227-36.
94. Palombo F, Hughes M. Jiricny J, Truong O, Hsuan J. Mismatch repair and cancer [letter]. Nature 1994;367:417.
95. Bronner CE, Baker SM, Morrison PT, Warren G, Smith LG, Lescoe MK, et al. Mutation in the DNA mismatch repair gene homologue hMLH1 is associated with hereditary non-polyposis colon cancer. Nature 1994; 368:258-61.
96. Nicolaides NC, Papadopoulos N, Liu B, Wei YF, Carter KC, Ruben SM, et al. Mutations of two PMS homologues in hereditary nonpolyposis colon cancer. Nature 1994;371:75-80.
97. Papadopoulos N, Nicolaides NC, Wei YF, Ruben SM, Carter KC, Rosen CA, et al. Mutation of a mutL homolog in hereditary colon cancer [see comment citation in Medline]. Science 1994;263:1625-9.
98. Horii A,. Han HJ, Sasaki S, Shimada M, Nakamura Y. Cloning, characterization and chromosomal assignment of the human genes homologous to yeast PMS1, a member of mismatch repair genes. Biochem Biophys Res Commun 1994;204:1257-64.
99. Nicolaides NC, Carter KC, Shell BK, Papadopoulos N, Vogelstein B, Kinzler KW. Genomic organization of the human PMS2 gene family. Genomics 1995;80:195-206.
100. Drummond JT, Li GM, Longley MJ, Modrich P. Isolation of an hMSH2-p160 heterodimer that restores DNA mismatch repair to tumor cells [see comment citation in Medline]. Science 1995;268:1909-12.
101. Palombo F, Gallinari P, Iaccarino I, Lettieri T, Hughes M, D'Arrigo A, et al. GTBP, a 160-kilodalton protein essential for mismatch-binding activity in human cells [see comment citation in Medline]. Science 1995; 268:1912-4.
102. Hare JT, Taylor JH. One role for DNA methylation in vertebrate cells is strand discrimination in mismatch repair. Proc Natl Acad Sci U S A 1985; 82:7350-4 .
103. L'mar A, Boyer JC, Kunkel TA, DNA loop repair by human cell extracts [see comment citation in Medline]. Science 1994;266:814-6.
104. Li GM, Modrich P. Restoration of mismatch repair to nuclear extracts of H6 colorectal tumor cells by a heterodimer of human MutL homologs. Proc Natl Acad Sci U S A 1995;92:1950-4.
105. Risinger JI, Umar A, Barrett JC, Kunkel TA. A hPMS2 mutant cell line is defective in strand-specific mismatch repair. J Biol Chem 1995;270: 18183-6.
106. Fang WH, Li GM, Longley M, Holmes J, Thilly W, Modrich P. Mismatch repair and genetic stability in human cells. Cold Spring Harb Symp Quant Biol 1993;58:597-603.
107. Su SS, Lahue RS, Au KG, Modrich P. Mispair specificity of methyl-directed DNA mismatch correction in vitro (published erratum appears in J Biol Chem 1988;263:11015]. J Biol Chem 1988;263:6829-35.
108. Alani E, Chi NW, Kolodner R. The Saccharomyces cerevisiae Msh2 protein specifically binds to duplex oligonucleotides containing mismatched DNA base pairs and insertions. Genes Dev 1995;9:234-47.
109. Papadopoulos N, Nicolaides NC, Liu B, Parsons R, Lengauer C, Palombo F, et al. Mutations of GTBP in genetically unstable cells [see comment citation in Medline]. Science 1995;268:1915-7.
110. Strand M, Earley MC, Crouse GF, et al. Mutations in the MSH3 gene preferentially lead to deletions within tracts of simple repetive DNA in Saccharomyces cerevisitie. Proc Natl Acad Sci U S A 1995;92:10418-21.
111. Fang WH, Modrich P. Human strand-specific mismatch repair occurs by a bidirectional mechanism similar to that of the bacterial reaction. J Biol Chem 1993;268:11838-44.
112. Parsons R, Li GM, Longley M, Modrich P, Liu B, Berk T, et al. Mismatch repair deficiency in phenotypically normal human cells [see comment citation in MedlineJ. Science 1995;268:738-40.
113. Magewu AN, Jones PA. Ubiquitous and tenacious methylation of the CpG site in codon 248 of the p53 gene may explain its frequent appearance as a mutational hot spot in human cancer. Mol Cell Biol 1994; 14:4225-32.
114. Tornaletti S, Pfeifer GP. Complete and tissue-independent methylation of CpG sites in the p53 gene-implications for mutations in human cancers. Oncogene 1995;10:1493-9.
115. Markowitz S, Wang J, Myeroff L, Parsons R, Sun L, Lutterbaugh J, et al. Inactivation of the type II TGF-β receptor in colon cancer cells with microsatellite instability. Science 1995;268:1336-8.
116. Geiser AG, Burmester JK, Webbink R, Roberts AB, Sporn MB. Inhibition of growth by transforming growth factor-beta following fusion of two nonresponsive human carcinoma cell lines. Implication of the type II receptor ingrowth inhibitory responses. J Biol Chem 1992;267:2588-93.
117. Wrana JL, Attisano L, Carcamo J, Zentella A, Doody J, Laiho M. et al. TGF beta signals through a heteromeric protein kinase receptor complex. Cell 1992;71:1003-14.
118. Boyd FT, Massague J. Transforming growth factor-beta inhibition of epithelial cell proliferation linked to the expression of a 53-kDa membrane receptor. J Biol Chem 1989;264:2272-8.
119. Laiho M, Weis FM, Boyd FT, Ignotz RA, Massague J. Responsiveness to transforming growth factor-beta (TGF-beta) restored by genetic complementation between cells defective in TGF-beta receptors I and II. J Biol Chem 1991;266:9108-12.
120. Laiho M, Weis MB, Massague J. Concomitant loss of transforming growth factor (TGF)-beta receptor types I and II in TGF-beta-resistant cell mutants implicates both receptor types in signal transduction. J Biol Chem 1990;265:18518-24.
121. Lothe RA, Peltomaki P, Meling GI, Aaltonen LA, Nystrom-Lahti M, Pylkkanen L, et al. Genomic instability in colorectal cancer: relationship to clinicopathological variables and family history. Cancer Res 1993;53: 5849-52.
122. Baker SM, Bronner E, Zhang L, Plug AW, Robatzek M, Warren G, et al. Male mice defective in the DNA mismatch repair gene PMS2 exhibit abnormal chromosome synapsis in meiosis. Cell 1995;82:309-19.
123. de Wind N, Dekker M, Berns A, Radman M, te Riele H. Inactivation of the mouse Msh2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer. Cell 1995; 82:321-30.