Home LiteratureArticle Details
PMID: 9564049 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

hMSH2 and hMSH6 play distinct roles in mismatch binding and contribute differently to the ATPase activity of hMutSalpha.

The EMBO journal ·Vol. 17 ·No. 9 ·1998-05-01 ·Pages 2677-86

Iaccarino I, Marra G, Palombo F, Jiricny J

Abstract

In extracts of human cells, base-base mismatches and small insertion/deletion loops are bound primarily by hMutSalpha, a heterodimer of hMSH2 and hMSH6 (also known as GTBP or p160). Recombinant hMutSalpha bound a G/T mismatch-containing oligonucleotide with an apparent dissociation constant Kd = 2.6 nM, while its affinity for a homoduplex substrate was >20-fold lower. In the presence of ATP, hMutSalpha dissociated from mismatched oligonucleotide substrates, and this reaction was attenuated by mutating the conserved lysine in the ATP-binding domains of hMSH6, hMSH2 or both to arginine. Surprisingly, this reaction required only ATP binding, not hydrolysis. The ATPase activity of hMutSalpha variants carrying the Lys-->Arg mutation in hMSH2 or in hMSH6 was severely affected, but these mutants were still proficient in mismatch binding and were able to complement, albeit to different extents, mismatch repair-deficient cell extracts. The mismatch binding-proficient, ATPase-deficient double mutant was inactive in the complementation assay and its presence in repair-proficient extracts was inhibitory. We conclude that although the ATPase activity of hMutSalpha is dispensible for mismatch binding, it is required for mismatch correction.

MeSH Terms
Adenosine Triphosphatases/metabolism Amino Acid Sequence Base Sequence Binding Sites Conserved Sequence DNA Repair DNA-Binding Proteins/chemistry,metabolism Dimerization Escherichia coli/metabolism Humans Kinetics Macromolecular Substances Molecular Sequence Data Multidrug Resistance-Associated Proteins MutS Homolog 2 Protein MutS Homolog 3 Protein Mutagenesis, Site-Directed Oligodeoxyribonucleotides Point Mutation Proto-Oncogene Proteins/chemistry,metabolism Recombinant Proteins/chemistry,metabolism Saccharomyces cerevisiae/metabolism Sequence Alignment Streptococcus pneumoniae/metabolism
Chemicals
DNA-Binding Proteins G-T mismatch-binding protein MSH3 protein, human Macromolecular Substances Multidrug Resistance-Associated Proteins MutS Homolog 3 Protein Oligodeoxyribonucleotides Proto-Oncogene Proteins Recombinant Proteins Adenosine Triphosphatases MSH2 protein, human MutS Homolog 2 Protein multidrug resistance-associated protein 1
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Iaccarino I
Institute of Medical Radiobiology, P.O. Box 424, August Forel-Strasse 7, CH-8029, Zürich, Switzerland.
Marra G
Palombo F
Jiricny J
References (35)
35 references, click to expand
  1. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold.
    EMBO J. 1982;1(8):945-51 PMID: 6329717
  2. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  3. Mutation of lysine-48 to arginine in the yeast RAD3 protein abolishes its ATPase and DNA helicase activities but not the ability to bind ATP.
    EMBO J. 1988 Oct;7(10):3263-9 PMID: 2846277
  4. A human 200-kDa protein binds selectively to DNA fragments containing G.T mismatches.
    Proc Natl Acad Sci U S A. 1988 Dec;85(23):8860-4 PMID: 3194394
  5. Isolation and characterization of the Escherichia coli mutL gene product.
    J Biol Chem. 1989 Jan 15;264(2):1000-4 PMID: 2536011
  6. Methyl-directed DNA mismatch correction.
    J Biol Chem. 1989 Apr 25;264(12):6597-600 PMID: 2651430
  7. DNA mismatch correction in a defined system.
    Science. 1989 Jul 14;245(4914):160-4 PMID: 2665076
  8. Superfamily of UvrA-related NTP-binding proteins. Implications for rational classification of recombination/repair systems.
    J Mol Biol. 1990 Jun 20;213(4):583-91 PMID: 2162963
  9. Heteroduplex repair in extracts of human HeLa cells.
    J Biol Chem. 1991 Feb 25;266(6):3744-51 PMID: 1995629
  10. Altering the conserved nucleotide binding motif in the Salmonella typhimurium MutS mismatch repair protein affects both its ATPase and mismatch binding activities.
    EMBO J. 1991 Sep;10(9):2707-15 PMID: 1651234
  11. Sequence and expression in Escherichia coli of the 40-kDa subunit of activator 1 (replication factor C) of HeLa cells.
    Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):2516-20 PMID: 1313560
  12. The purification of a human mismatch-binding protein and identification of its associated ATPase and helicase activities.
    J Biol Chem. 1992 Nov 25;267(33):23876-82 PMID: 1429725
  13. Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer.
    Cell. 1993 Dec 17;75(6):1215-25 PMID: 8261515
  14. Dominant negative mutator mutations in the mutS gene of Escherichia coli.
    J Bacteriol. 1994 Sep;176(17):5393-400 PMID: 8071216
  15. Purified human MSH2 protein binds to DNA containing mismatched nucleotides.
    Cancer Res. 1994 Nov 1;54(21):5539-42 PMID: 7923193
  16. Genetic instability in human ovarian cancer cell lines.
    Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9495-9 PMID: 7937795
  17. Binding of mismatched microsatellite DNA sequences by the human MSH2 protein.
    Science. 1994 Nov 25;266(5189):1403-5 PMID: 7973733
  18. Isolation of an hMSH2-p160 heterodimer that restores DNA mismatch repair to tumor cells.
    Science. 1995 Jun 30;268(5219):1909-12 PMID: 7604264
  19. GTBP, a 160-kilodalton protein essential for mismatch-binding activity in human cells.
    Science. 1995 Jun 30;268(5219):1912-4 PMID: 7604265
  20. Mutations of GTBP in genetically unstable cells.
    Science. 1995 Jun 30;268(5219):1915-7 PMID: 7604266
  21. Hereditary nonpolyposis colorectal cancer: the syndrome, the genes, and historical perspectives.
    J Natl Cancer Inst. 1995 Aug 2;87(15):1114-25 PMID: 7674315
  22. Identification of mismatch repair genes and their role in the development of cancer.
    Curr Opin Genet Dev. 1995 Jun;5(3):382-95 PMID: 7549435
  23. Analysis of mismatch repair genes in hereditary non-polyposis colorectal cancer patients.
    Nat Med. 1996 Feb;2(2):169-74 PMID: 8574961
  24. MSH6, a Saccharomyces cerevisiae protein that binds to mismatches as a heterodimer with MSH2.
    Curr Biol. 1996 Apr 1;6(4):484-6 PMID: 8723353
  25. hMutSbeta, a heterodimer of hMSH2 and hMSH3, binds to insertion/deletion loops in DNA.
    Curr Biol. 1996 Sep 1;6(9):1181-4 PMID: 8805365
  26. Mismatch repair in replication fidelity, genetic recombination, and cancer biology.
    Annu Rev Biochem. 1996;65:101-33 PMID: 8811176
  27. A partially functional DNA helicase II mutant defective in forming stable binary complexes with ATP and DNA. A role for helicase motif III.
    J Biol Chem. 1996 Oct 11;271(41):25360-8 PMID: 8810301
  28. Molecular cloning of the N-terminus of GTBP.
    Genomics. 1996 Feb 1;31(3):395-7 PMID: 8838326
  29. hMSH2 forms specific mispair-binding complexes with hMSH3 and hMSH6.
    Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13629-34 PMID: 8942985
  30. DNA repair and colorectal cancer.
    Gastroenterol Clin North Am. 1996 Dec;25(4):755-72 PMID: 8960891
  31. Mismatch repair and cancer.
    Cancer Surv. 1996;28:47-68 PMID: 8977028
  32. Genetic and biochemical analysis of Msh2p-Msh6p: role of ATP hydrolysis and Msh2p-Msh6p subunit interactions in mismatch base pair recognition.
    Mol Cell Biol. 1997 May;17(5):2436-47 PMID: 9111312
  33. MutS mediates heteroduplex loop formation by a translocation mechanism.
    EMBO J. 1997 Jul 16;16(14):4467-76 PMID: 9250691
  34. The human mismatch recognition complex hMSH2-hMSH6 functions as a novel molecular switch.
    Cell. 1997 Dec 26;91(7):995-1005 PMID: 9428522
  35. A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions.
    Nucleic Acids Res. 1988 Aug 11;16(15):7351-67 PMID: 3045756
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1998-05-01
Pages
2677-86
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1170608
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]