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Science 30 June 1995:
Vol. 268. no. 5219, pp. 1909 - 1912
DOI: 10.1126/science.7604264
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Articles

Science, Vol 268, Issue 5219, 1909-1912
Copyright © 1995 by American Association for the Advancement of Science

articles

Isolation of an hMSH2-p160 heterodimer that restores DNA mismatch repair to tumor cells

JT Drummond, GM Li, MJ Longley, and P Modrich

Howard Hughes Medical Institute, Duke University Medical Center, Durham, NC 27710, USA.

A mismatch-binding heterodimer of hMSH2 and a 160-kilodalton polypeptide has been isolated from HeLa cells by virtue of its ability to restore mismatch repair to nuclear extracts of hMSH2-deficient LoVo colorectal tumor cells. This heterodimer, designated hMutS alpha, also restores mismatch repair to extracts of alkylation-tolerant MT1 lymphoblastoid cells and HCT-15 colorectal tumor cells, which are selectively defective in the repair of base-base and single-nucleotide insertion-deletion mismatches. Because HOT-15 cells appear to be free of hMSH2 mutations, this selective repair defect is likely a result of a deficiency of the hMutS alpha 160-kilodalton subunit, and mutations in the corresponding gene may confer hypermutability and cancer predisposition.


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DNA Template Requirements for Human Mismatch Repair in Vitro.
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Dominant Saccharomyces cerevisiae msh6 Mutations Cause Increased Mispair Binding and Decreased Dissociation from Mispairs by Msh2-Msh6 in the Presence of ATP.
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Deficiency of a novel mismatch repair activity in a bladder tumor cell line.
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G. Tomer, A. B. Buermeyer, M. M. Nguyen, and R. M. Liskay (2002)
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Functional analysis of MSH6 mutations linked to kindreds with putative hereditary non-polyposis colorectal cancer syndrome.
R. Kariola, T. E. Raevaara, K. E. Lonnqvist, and M. Nystrom-Lahti (2002)
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Human Exonuclease I Is Required for 5' and 3' Mismatch Repair.
J. Genschel, L. R. Bazemore, and P. Modrich (2002)
J. Biol. Chem. 277, 13302-13311
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Partial Reconstitution of Human DNA Mismatch Repair In Vitro: Characterization of the Role of Human Replication Protein A.
C. Ramilo, L. Gu, S. Guo, X. Zhang, S. M. Patrick, J. J. Turchi, and G.-M. Li (2002)
Mol. Cell. Biol. 22, 2037-2046
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hMutS{beta} Is Required for the Recognition and Uncoupling of Psoralen Interstrand Cross-Links In Vitro.
N. Zhang, X. Lu, X. Zhang, C. A. Peterson, and R. J. Legerski (2002)
Mol. Cell. Biol. 22, 2388-2397
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Human MutY Homolog, a DNA Glycosylase Involved in Base Excision Repair, Physically and Functionally Interacts with Mismatch Repair Proteins Human MutS Homolog 2/Human MutS Homolog 6.
Y. Gu, A. Parker, T. M. Wilson, H. Bai, D.-Y. Chang, and A-L. Lu (2002)
J. Biol. Chem. 277, 11135-11142
   Abstract »    Full Text »    PDF »
Construction and characterization of mismatch-containing circular DNA molecules competent for assessment of nick-directed human mismatch repair in vitro.
E. D. Larson, D. Nickens, and J. T. Drummond (2002)
Nucleic Acids Res. 30, e14
   Abstract »    Full Text »    PDF »
Asymmetric Recognition of DNA Local Distortion. STRUCTURE-BASED FUNCTIONAL STUDIES OF EUKARYOTIC Msh2-Msh6.
K. Drotschmann, W. Yang, F. E. Brownewell, E. T. Kool, and T. A. Kunkel (2001)
J. Biol. Chem. 276, 46225-46229
   Abstract »    Full Text »    PDF »
exo1-Dependent Mutator Mutations: Model System for Studying Functional Interactions in Mismatch Repair.
N. S. Amin, M.-N. Nguyen, S. Oh, and R. D. Kolodner (2001)
Mol. Cell. Biol. 21, 5142-5155
   Abstract »    Full Text »    PDF »
hMSH3 overexpression and cellular response to cytotoxic anticancer agents.
R. Pepponi, G. Graziani, S. Falcinelli, P. Vernole, L. Levati, P. M. Lacal, E. Pagani, E. Bonmassar, J. Jiricny, and S. D'Atri (2001)
Carcinogenesis 22, 1131-1137
   Abstract »    Full Text »    PDF »
Tolerance of human MSH2+/- lymphoblastoid cells to the methylating agent temozolomide.
G. Marra, S. D'Atri, C. Corti, L. Bonmassar, M. S. Cattaruzza, P. Schweizer, K. Heinimann, Z. Bartosova, M. Nystrom-Lahti, and J. Jiricny (2001)
PNAS 98, 7164-7169
   Abstract »    Full Text »    PDF »
Human DNA mismatch repair in vitro operates independently of methylation status at CpG sites.
J. T. Drummond and A. Bellacosa (2001)
Nucleic Acids Res. 29, 2234-2243
   Abstract »    Full Text »    PDF »
Initiation of strand incision at G:T and O6-methylguanine:T base mismatches in DNA by human cell extracts.
S.-U. Lari, R. S. Day, K. Dobler, and M. C. Paterson (2001)
Nucleic Acids Res. 29, 2409-2417
   Abstract »    Full Text »    PDF »
Repair of Double-Strand Breaks by Homologous Recombination in Mismatch Repair-Defective Mammalian Cells.
B. Elliott and M. Jasin (2001)
Mol. Cell. Biol. 21, 2671-2682
   Abstract »    Full Text »
hMSH3 and hMSH6 interact with PCNA and colocalize with it to replication foci.
H. E. Kleczkowska, G. Marra, T. Lettieri, and J. Jiricny (2001)
Genes & Dev. 15, 724-736
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A Novel Protein Complex Distinct from Mismatch Repair Binds Thioguanylated DNA.
E. Y. Krynetski, N. F. Krynetskaia, A. E. Gallo, K. G. Murti, and W. E. Evans (2001)
Mol. Pharmacol. 59, 367-374
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The DNA strand of chimeric RNA/DNA oligonucleotides can direct gene repair/conversion activity in mammalian and plant cell-free extracts.
H. B. Gamper, H. Parekh, M. C. Rice, M. Bruner, H. Youkey, and E. B. Kmiec (2000)
Nucleic Acids Res. 28, 4332-4339
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DNA Repair Defects Inactivate Tumor Suppressor Genes and Induce Hereditary and Sporadic Colon Cancers.
S. Markowitz (2000)
J. Clin. Oncol. 18, 75s-80
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Functional Studies on the Candidate ATPase Domains of Saccharomyces cerevisiae MutLalpha.
P. T. Tran and R. M. Liskay (2000)
Mol. Cell. Biol. 20, 6390-6398
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DNA mismatch repair genes and colorectal cancer.
J M D WHEELER, W F BODMER, and N J M. MORTENSEN (2000)
Gut 47, 148-153
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Mutagenesis in PMS2- and MSH2-deficient mice indicates differential protection from transversions and frameshifts.
S. E. Andrew, X. S. Xu, A. Baross-Francis, L. Narayanan, K. Milhausen, R.M. Liskay, F. R. Jirik, and P. M. Glazer (2000)
Carcinogenesis 21, 1291-1296
   Abstract »    Full Text »    PDF »
Temozolomide and Treatment of Malignant Glioma.
H. S. Friedman, T. Kerby, and H. Calvert (2000)
Clin. Cancer Res. 6, 2585-2597
   Abstract »    Full Text »
The cellular mismatch repair system is able to repair mismatches within MLV retroviral double-stranded DNA at a low frequency.
L.-Y. Tang and J. Zhang (2000)
Nucleic Acids Res. 28, 2302-2306
   Abstract »    Full Text »    PDF »
hMSH6 Alterations in Patients with Microsatellite Instability-Low Colorectal Cancer.
Y. R. Parc, K. C. Halling, L. Wang, E. R. Christensen, J. M. Cunningham, A. J. French, L. J. Burgart, T. L. Price-Troska, P. C. Roche, and S. N. Thibodeau (2000)
Cancer Res. 60, 2225-2231
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Most Retroviral Recombinations Occur during Minus-Strand DNA Synthesis.
J. Zhang, L.-Y. Tang, T. Li, Y. Ma, and C. M. Sapp (2000)
J. Virol. 74, 2313-2322
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The Role of Mismatched Nucleotides in Activating the hMSH2-hMSH6 Molecular Switch.
S. Gradia, S. Acharya, and R. Fishel (2000)
J. Biol. Chem. 275, 3922-3930
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Detection of Microsatellite Instability by Fluorescence Multiplex Polymerase Chain Reaction.
K. D. Berg, C. L. Glaser, R. E. Thompson, S. R. Hamilton, C. A. Griffin, and J. R. Eshleman (2000)
J. Mol. Diagn. 2, 20-28
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Mutation in the Magnesium Binding Site of hMSH6 Disables the hMutSalpha Sliding Clamp from Translocating along DNA.
I. Iaccarino, G. Marra, P. Dufner, and J. Jiricny (2000)
J. Biol. Chem. 275, 2080-2086
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Evolutionary origin, diversification and specialization of eukaryotic MutS homolog mismatch repair proteins.
K. M. Culligan, G. Meyer-Gauen, J. Lyons-Weiler, and J. B. Hays (2000)
Nucleic Acids Res. 28, 463-471
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Signaling Mismatch Repair: The Mechanics of an Adenosine-Nucleotide Molecular Switch.
R. FISHEL, S. ACHARYA, M. BERARDINI, T. BOCKER, N. CHARBONNEAU, A. CRANSTON, S. GRADIA, S. GUERRETTE, C.D. HEINEN, A. MAZUREK, et al. (2000)
Cold Spring Harb Symp Quant Biol 65, 217-224
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Mismatch Repair Processing of Carcinogen-DNA Adducts Triggers Apoptosis.
J. Wu, L. Gu, H. Wang, N. E. Geacintov, and G.-M. Li (1999)
Mol. Cell. Biol. 19, 8292-8301
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Mismatch repair, G2/M cell cycle arrest and lethality after DNA damage.
G. Aquilina, M. Crescenzi, and M. Bignami (1999)
Carcinogenesis 20, 2317-2326
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Identification of hMutLbeta , a Heterodimer of hMLH1 and hPMS1.
M. Raschle, G. Marra, M. Nystrom-Lahti, P. Schar, and J. Jiricny (1999)
J. Biol. Chem. 274, 32368-32375
   Abstract »    Full Text »    PDF »
Separation-of-Function Mutations in Saccharomyces cerevisiae MSH2 That Confer Mismatch Repair Defects but Do Not Affect Nonhomologous-Tail Removal during Recombination.
B. Studamire, G. Price, N. Sugawara, J. E. Haber, and E. Alani (1999)
Mol. Cell. Biol. 19, 7558-7567
   Abstract »    Full Text »    PDF »
hMutSalpha - and hMutLalpha -dependent phosphorylation of p53 in response to DNA methylator damage.
D. R. Duckett, S. M. Bronstein, Y. Taya, and P. Modrich (1999)
PNAS 96, 12384-12388
   Abstract »    Full Text »    PDF »
Biochemical Characterization of the Interaction between the Saccharomyces cerevisiae MSH2-MSH6 Complex and Mispaired Bases in DNA.
G. T. Marsischky and R. D. Kolodner (1999)
J. Biol. Chem. 274, 26668-26682
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Role of DNA mismatch repair and p53 in signaling induction of apoptosis by alkylating agents.
M. J. Hickman and L. D. Samson (1999)
PNAS 96, 10764-10769
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The cytotoxicity of DNA carboxymethylation and methylation by the model carboxymethylating agent azaserine in human cells.
M. O'Driscoll, P. Macpherson, Y.-Z. Xu, and P. Karran (1999)
Carcinogenesis 20, 1855-1862
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Mononucleotide microsatellite instability and germline MSH6 mutation analysis in early onset colorectal cancer.
L. Verma, M. F Kane, C. Brassett, J. Schmeits, D G. R Evans, R. D Kolodner, and E. R Maher (1999)
J. Med. Genet. 36, 678-682
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Oligomerization of a MutS Mismatch Repair Protein from Thermus aquaticus.
I. Biswas, C. Ban, K. G. Fleming, J. Qin, J. W. Lary, D. A. Yphantis, W. Yang, and P. Hsieh (1999)
J. Biol. Chem. 274, 23673-23678
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Inefficient in vivo repair of mismatches at an oncogenic hotspot correlated with lack of binding by mismatch repair proteins and with phase of the cell cycle.
N. Matton, J. Simonetti, and K. Williams (1999)
Carcinogenesis 20, 1417-1424
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Dissociation of Mismatch Recognition and ATPase Activity by hMSH2-hMSH3.
T. Wilson, S. Guerrette, and R. Fishel (1999)
J. Biol. Chem. 274, 21659-21664
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Sequence-dependent mutations in a shuttle vector plasmid replicated in a mismatch repair deficient human cell line.
S. E. Tobi, D. D. Levy, M. M. Seidman1, and K. H. Kraemer1 (1999)
Carcinogenesis 20, 1293-1301
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Apoptosis Induced by Overexpression of hMSH2 or hMLH1.
H. Zhang, B. Richards, T. Wilson, M. Lloyd, A. Cranston, A. Thorburn, R. Fishel, and M. Meuth (1999)
Cancer Res. 59, 3021-3027
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Specific Binding of Human MSH2·MSH6 Mismatch-Repair Protein Heterodimers to DNA Incorporating Thymine- or Uracil-containing UV Light Photoproducts Opposite Mismatched Bases.
H. Wang, C. W. Lawrence, G.-M. Li, and J. B. Hays (1999)
J. Biol. Chem. 274, 16894-16900
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A Mutation in the MSH6 Subunit of the Saccharomyces cerevisiae MSH2-MSH6 Complex Disrupts Mismatch Recognition.
J. Bowers, T. Sokolsky, T. Quach, and E. Alani (1999)
J. Biol. Chem. 274, 16115-16125
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Overexpression of DNA polymerase ß: a genomic instability enhancer process.
Y. CANITROT, M. FRÉCHET, L. SERVANT, C. CAZAUX, and J.-S. HOFFMANN (1999)
FASEB J 13, 1107-1111
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Msh2 status modulates both apoptosis and mutation frequency in the murine small intestine.
N. J. Toft, D. J. Winton, J. Kelly, L. A. Howard, M. Dekker, H. te Riele, M. J. Arends, A. H. Wyllie, G. P. Margison, and A. R. Clarke (1999)
PNAS 96, 3911-3915
   Abstract »    Full Text »    PDF »
MED1, a novel human methyl-CpG-binding endonuclease, interacts with DNA mismatch repair protein MLH1.
A. Bellacosa, L. Cicchillitti, F. Schepis, A. Riccio, A. T. Yeung, Y. Matsumoto, E. A. Golemis, M. Genuardi, and G. Neri (1999)
PNAS 96, 3969-3974
   Abstract »    Full Text »    PDF »
Mutator phenotypes of yeast strains heterozygous for mutations in the MSH2 gene.
K. Drotschmann, A. B. Clark, H. T. Tran, M. A. Resnick, D. A. Gordenin, and T. A. Kunkel (1999)
PNAS 96, 2970-2975
   Abstract »    Full Text »    PDF »
`Saccharomyces cerevisiae MSH2/6 Complex Interacts with Holliday Junctions and Facilitates Their Cleavage by Phage Resolution Enzymes.
G. T. Marsischky, S. Lee, J. Griffith, and R. D. Kolodner (1999)
J. Biol. Chem. 274, 7200-7206
   Abstract »    Full Text »    PDF »
Repair of Large Insertion/Deletion Heterologies in Human Nuclear Extracts Is Directed by a 5' Single-strand Break and Is Independent of the Mismatch Repair System.
S. J. Littman, W.-h. Fang, and P. Modrich (1999)
J. Biol. Chem. 274, 7474-7481
   Abstract »    Full Text »    PDF »
Effect of hMSH6 cDNA expression on the phenotype of mismatch repair-deficient colon cancer cell line HCT15.
T. Lettieri, G. Marra, G. Aquilina, M. Bignami, N. E.A. Crompton, F. Palombo, and J. Jiricny (1999)
Carcinogenesis 20, 373-382
   Abstract »    Full Text »    PDF »
Mouse MutS-like protein Msh5 is required for proper chromosome synapsis in male and female meiosis.
S. S. de Vries, E. B. Baart, M. Dekker, A. Siezen, D. G. de Rooij, P. de Boer, and H. te Riele (1999)
Genes & Dev. 13, 523-531
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hMSH5: A Human MutS Homologue That Forms a Novel Heterodimer with hMSH4 and Is Expressed during Spermatogenesis.
T. Bocker, A. Barusevicius, T. Snowden, D. Rasio, S. Guerrette, D. Robbins, C. Schmidt, J. Burczak, C. M. Croce, T. Copeland, et al. (1999)
Cancer Res. 59, 816-822
   Abstract »    Full Text »    PDF »
Mismatch repair and differential sensitivity of mouse and human cells to methylating agents.
O. Humbert, S. Fiumicino, G. Aquilina, P. Branch, S. Oda, A. Zijno, P. Karran, and M. Bignami (1999)
Carcinogenesis 20, 205-214
   Abstract »    Full Text »    PDF »
MSH3 deficiency is not sufficient for a mutator phenotype in Chinese hamster ovary cells.
J. M. Hinz and M. Meuth (1999)
Carcinogenesis 20, 215-220
   Abstract »    Full Text »    PDF »
Saccharomyces cerevisiae Msh2p and Msh6p ATPase Activities Are Both Required during Mismatch Repair.
B. Studamire, T. Quach, and E. Alani (1998)
Mol. Cell. Biol. 18, 7590-7601
   Abstract »    Full Text »


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