The PMS2 Subunit of Human MutLα Contains a Metal Ion Binding Domain of the Iron-Dependent Repressor Protein Family

Journal of Molecular Biology

Volumn 382, Issue 3, 2008, Pages 610-627

  Kosinski, Jan ^a,b   Plotz, Guido ^c   Guarné, Alba ^d   Bujnicki, Janusz M ^a   Friedhoff, Peter ^b  

^a INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c GOETHE UNIVERSITY   (Germany)

^d MCMASTER UNIVERSITY   (Canada)

Author keywords

DNA mismatch repair; fold recognition; homology modeling; metal ion binding; MutL

Indexed keywords

BINDING PROTEIN; MISMATCH REPAIR PROTEIN PMS2; PROTEIN MUTL ALPHA; REPRESSOR PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CHEMICAL ANALYSIS; DIMERIZATION; METAL BINDING; MISMATCH REPAIR; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS;

EID: 50149104597     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.06.056     Document Type: Article

References (98)

1. Modrich P. Mechanisms and biological effects of mismatch repair. Annu. Rev. Genet. 25 (1991) 229-253
2. Iyer R.R., Pluciennik A., Burdett V., and Modrich P.L. DNA mismatch repair: functions and mechanisms. Chem. Rev. 106 (2006) 302-323
3. Kunkel T.A., and Erie D.A. DNA mismatch repair. Annu. Rev. Biochem. 74 (2005) 681-710
4. Zhang Y., Yuan F., Presnell S.R., Tian K., Gao Y., Tomkinson A.E., et al. Reconstitution of 5′-directed human mismatch repair in a purified system. Cell 122 (2005) 693-705
5. Constantin N., Dzantiev L., Kadyrov F.A., and Modrich P. Human mismatch repair: reconstitution of a nick-directed bidirectional reaction. J. Biol. Chem. 280 (2005) 39752-39761
6. Kadyrov F.A., Dzantiev L., Constantin N., and Modrich P. Endonucleolytic function of MutLα in human mismatch repair. Cell 126 (2006) 297-308
7. Kadyrov F.A., Holmes S.F., Arana M.E., Lukianova O.A., O'Donnell M., Kunkel T.A., and Modrich P. Saccharomyces cerevisiae MutLα is a mismatch repair endonuclease. J. Biol. Chem. 282 (2007) 37181-37190
8. Deschenes S.M., Tomer G., Nguyen M., Erdeniz N., Juba N.C., Sepulveda N., et al. The E705K mutation in hPMS2 exerts recessive, not dominant, effects on mismatch repair. Cancer Lett. 249 (2007) 148-156
9. Erdeniz N., Nguyen M., Deschenes S.M., and Liskay R.M. Mutations affecting a putative MutLα endonuclease motif impact multiple mismatch repair functions. DNA Repair (Amst.) 6 (2007) 1463-1470
10. Ban C., and Yang W. Crystal structure and ATPase activity of MutL: implications for DNA repair and mutagenesis. Cell 95 (1998) 541-552
11. Ban C., Junop M., and Yang W. Transformation of MutL by ATP binding and hydrolysis: a switch in DNA mismatch repair. Cell 97 (1999) 85-97
12. Sacho E.J., Kadyrov F.A., Modrich P., Kunkel T.A., and Erie D.A. Direct visualization of asymmetric adenine nucleotide-induced conformational changes in MutLα. Mol. Cell 29 (2008) 112-121
13. Guarne A., Junop M.S., and Yang W. Structure and function of the N-terminal 40 kDa fragment of human PMS2: a monomeric GHL ATPase. EMBO J. 20 (2001) 5521-5531
14. Dutta R., and Inouye M. GHKL, an emergent ATPase/kinase superfamily. Trends Biochem. Sci. 25 (2000) 24-28
15. Guarne A., Ramon-Maiques S., Wolff E.M., Ghirlando R., Hu X., Miller J.H., and Yang W. Structure of the MutL C-terminal domain: a model of intact MutL and its roles in mismatch repair. EMBO J. 23 (2004) 4134-4145
16. Kosinski J., Steindorf I., Bujnicki J.M., Giron-Monzon L., and Friedhoff P. Analysis of the quaternary structure of the MutL C-terminal domain. J. Mol. Biol. 351 (2005) 895-909
17. Raschle M., Marra G., Nystrom-Lahti M., Schar P., and Jiricny J. Identification of hMutLb, a heterodimer of hMLH1 and hPMS1. J. Biol. Chem. 274 (1999) 32368-32375
18. Lin Z., Nei M., and Ma H. The origins and early evolution of DNA mismatch repair genes-multiple horizontal gene transfers and co-evolution. Nucleic Acids Res. 35 (2007) 7591-7603
19. Cannavo E., Marra G., Sabates-Bellver J., Menigatti M., Lipkin S.M., Fischer F., et al. Expression of the MutL homologue hMLH3 in human cells and its role in DNA mismatch repair. Cancer Res. 65 (2005) 10759-10766
20. Korhonen M.K., Raevaara T.E., Lohi H., and Nystrom M. Conditional nuclear localization of hMLH3 suggests a minor activity in mismatch repair and supports its role as a low-risk gene in HNPCC. Oncol. Rep. 17 (2007) 351-354
21. Pang Q., Prolla T.A., and Liskay R.M. Functional domains of the Saccharomyces cerevisiae Mlh1p and Pms1p DNA mismatch repair proteins and their relevance to human hereditary nonpolyposis colorectal cancer-associated mutations. Mol. Cell. Biol. 17 (1997) 4465-4473
22. Guerrette S., Acharya S., and Fishel R. The interaction of the human MutL homologues in hereditary nonpolyposis colon cancer. J. Biol. Chem. 274 (1999) 6336-6341
23. Yang W. Human MutLα: the jack of all trades in MMR is also an endonuclease. DNA Repair (Amst.) 6 (2007) 135-139
24. Pennella M.A., and Giedroc D.P. Structural determinants of metal selectivity in prokaryotic metal-responsive transcriptional regulators. BioMetals 18 (2005) 413-428
25. Giedroc D.P., and Arunkumar A.I. Metal sensor proteins: nature's metalloregulated allosteric switches. Dalton Trans. (2007) 3107-3120 10.1039/b706769k
26. Wheeler D.L., Barrett T., Benson D.A., Bryant S.H., Canese K., Chetvernin V., et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 36 (2008) D13-D21
27. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
28. Kabsch W., and Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22 (1983) 2577-2637
29. Anisimova M., and Gascuel O. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst. Biol. 55 (2006) 539-552
30. Kosinski J., Cymerman I.A., Feder M., Kurowski M.A., Sasin J.M., and Bujnicki J.M. A "FRankenstein's monster" approach to comparative modeling: merging the finest fragments of fold-recognition models and iterative model refinement aided by 3D structure evaluation. Proteins: Struct. Funct. Genet. 53 (2003) 369-379
31. Kosinski J., Gajda M.J., Cymerman I.A., Kurowski M.A., Pawlowski M., Boniecki M., et al. FRankenstein becomes a cyborg: the automatic recombination and realignment of fold recognition models in CASP6. Proteins: Struct. Funct. Genet. 61 (2005) 106-113
32. Kurowski M.A., and Bujnicki J.M. GeneSilico protein structure prediction meta-server. Nucleic Acids Res. 31 (2003) 3305-3307
33. DeLano W.L. The PyMOL Molecular Graphics System (2002), DeLano Scientific, San Carlos, CA
34. Soding J., Biegert A., and Lupas A.N. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33 (2005) W244-W248
35. Rohl C.A., Strauss C.E., Misura K.M., and Baker D. Protein structure prediction using Rosetta. Methods Enzymol. 383 (2004) 66-93
36. Wallner B., Fang H., and Elofsson A. Automatic consensus-based fold recognition using Pcons, ProQ, and Pmodeller. Proteins: Struct. Funct. Genet. 53 (2003) 534-541
37. Wallner B., and Elofsson A. Identification of correct regions in protein models using structural, alignment, and consensus information. Protein Sci. 15 (2006) 900-913
38. Kosinski J., Kubareva E., and Bujnicki J.M. A model of restriction endonuclease MvaI in complex with DNA: a template for interpretation of experimental data and a guide for specificity engineering. Proteins: Struct. Funct. Genet. 68 (2007) 324-336
39. Sodhi J.S., Bryson K., McGuffin L.J., Ward J.J., Wernisch L., and Jones D.T. Predicting metal-binding site residues in low-resolution structural models. J. Mol. Biol. 342 (2004) 307-320
40. Babor M., Gerzon S., Raveh B., Sobolev V., and Edelman M. Prediction of transition metal-binding sites from apo protein structures. Proteins: Struct. Funct. Genet. 70 (2008) 208-217
41. Ebert J.C., and Altman R.B. Robust recognition of zinc binding sites in proteins. Protein Sci. 17 (2008) 54-65
42. Cai C.Z., Han L.Y., Ji Z.L., Chen X., and Chen Y.Z. SVM-Prot: web-based support vector machine software for functional classification of a protein from its primary sequence. Nucleic Acids Res. 31 (2003) 3692-3697
43. Passerini A., Andreini C., Menchetti S., Rosato A., and Frasconi P. Predicting zinc binding at the proteome level. BMC Bioinformatics 8 (2007) 39
44. Gee K.R., Zhou Z.L., Qian W.J., and Kennedy R. Detection and imaging of zinc secretion from pancreatic beta-cells using a new fluorescent zinc indicator. J. Am. Chem. Soc. 124 (2002) 776-778
45. Krezel A., and Maret W. Dual nanomolar and picomolar Zn(II) binding properties of metallothionein. J. Am. Chem. Soc. 129 (2007) 10911-10921
46. Trojan J., Zeuzem S., Randolph A., Hemmerle C., Brieger A., Raedle J., et al. Functional analysis of hMLH1 variants and HNPCC-related mutations using a human expression system. Gastroenterology 122 (2002) 211-219
47. Brieger A., Plotz G., Raedle J., Weber N., Baum W., Caspary W.F., et al. Characterization of the nuclear import of human MutLα. Mol. Carcinog. 43 (2005) 51-58
48. Plotz G., Raedle J., Brieger A., Trojan J., and Zeuzem S. N-terminus of hMLH1 confers interaction of hMutLα and hMutLβ with hMutSα. Nucleic Acids Res. 31 (2003) 3217-3226
49. Plotz G., Raedle J., Spina A., Welsch C., Stallmach A., Zeuzem S., and Schmidt C. Evaluation of the MLH1 I219V alteration in DNA mismatch repair activity and ulcerative colitis. Inflamm. Bowel Dis. 14 (2008) 605-611
50. Plotz G., Piiper A., Wormek M., Zeuzem S., and Raedle J. Analysis of the human MutLα.hMutSα complex. Biochem. Biophys. Res. Commun. 340 (2006) 852-859
51. Raevaara T.E., Korhonen M.K., Lohi H., Hampel H., Lynch E., Lonnqvist K.E., et al. Functional significance and clinical phenotype of nontruncating mismatch repair variants of MLH1. Gastroenterology 129 (2005) 537-549
52. Fukui K., Nishida M., Nakagawa N., Masui R., and Kuramitsu S. Bound nucleotide controls the endonuclease activity of a mismatch repair enzyme MutL. J. Biol. Chem. 283 (2008) 12136-12145
53. Glasfeld A., Guedon E., Helmann J.D., and Brennan R.G. Structure of the manganese-bound manganese transport regulator of Bacillus subtilis. Nat. Struct. Biol. 10 (2003) 652-657
54. D'Aquino J.A., Tetenbaum-Novatt J., White A., Berkovitch F., and Ringe D. Mechanism of metal ion activation of the diphtheria toxin repressor DtxR. Proc. Natl. Acad. Sci. USA 102 (2005) 18408-18413
55. Mohd A.B., Palama B., Nelson S.E., Tomer G., Nguyen M., Huo X., and Buermeyer A.B. Truncation of the C-terminus of human MLH1 blocks intracellular stabilization of PMS2 and disrupts DNA mismatch repair. DNA Repair (Amst.) 5 (2006) 347-361
56. Argueso J.L., Kijas A.W., Sarin S., Heck J., Waase M., and Alani E. Systematic mutagenesis of the Saccharomyces cerevisiae MLH1 gene reveals distinct roles for Mlh1p in meiotic crossing over and in vegetative and meiotic mismatch repair. Mol. Cell. Biol. 23 (2003) 873-886
57. Perera S., and Bapat B. The MLH1 variants p.Arg265Cys and p.Lys618Ala affect protein stability while p.Leu749Gln affects heterodimer formation. Hum. Mutat. 29 (2008) 332
58. Takahashi M., Shimodaira H., Andreutti-Zaugg C., Iggo R., Kolodner R.D., and Ishioka C. Functional analysis of human MLH1 variants using yeast and in vitro mismatch repair assays. Cancer Res. 67 (2007) 4595-4604
59. Hendriks Y.M., Jagmohan-Changur S., van der Klift H.M., Morreau H., van Puijenbroek M., Tops C., et al. Heterozygous mutations in PMS2 cause hereditary nonpolyposis colorectal carcinoma (Lynch syndrome). Gastroenterology 130 (2006) 312-322
60. Worthley D.L., Walsh M.D., Barker M., Ruszkiewicz A., Bennett G., Phillips K., and Suthers G. Familial mutations in PMS2 can cause autosomal dominant hereditary nonpolyposis colorectal cancer. Gastroenterology 128 (2005) 1431-1436
61. Cheng J., Randall A.Z., Sweredoski M.J., and Baldi P. SCRATCH: a protein structure and structural feature prediction server. Nucleic Acids Res. 33 (2005) W72-W76
62. Lipkin S.M., Wang V., Jacoby R., Banerjee-Basu S., Baxevanis A.D., Lynch H.T., et al. MLH3: a DNA mismatch repair gene associated with mammalian microsatellite instability. Nat. Genet. 24 (2000) 27-35
63. Raschle M., Dufner P., Marra G., and Jiricny J. Mutations within the hMLH1 and hPMS2 subunits of the human MutLα mismatch repair factor affect its ATPase activity, but not its ability to interact with hMutSα. J. Biol. Chem. 277 (2002) 21810-21820
64. Pommer A.J., Kuhlmann U.C., Cooper A., Hemmings A.M., Moore G.R., James R., and Kleanthous C. Homing in on the role of transition metals in the HNH motif of colicin endonucleases. J. Biol. Chem. 274 (1999) 27153-27160
65. Jin Y.H., Clark A.B., Slebos R.J., Al-Refai H., Taylor J.A., Kunkel T.A., et al. Cadmium is a mutagen that acts by inhibiting mismatch repair. Nat. Genet. 34 (2003) 326-329
66. Lutzen A., Liberti S.E., and Rasmussen L.J. Cadmium inhibits human DNA mismatch repair in vivo. Biochem. Biophys. Res. Commun. 321 (2004) 21-25
67. Banerjee S., and Flores-Rozas H. Cadmium inhibits mismatch repair by blocking the ATPase activity of the MSH2-MSH6 complex. Nucleic Acids Res. 33 (2005) 1410-1419
68. Clark A.B., and Kunkel T.A. Cadmium inhibits the functions of eukaryotic MutS complexes. J. Biol. Chem. 279 (2004) 53903-53906
69. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32 (2004) 1792-1797
70. Abascal F., Zardoya R., and Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21 (2005) 2104-2105
71. Guindon S., and Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52 (2003) 696-704
72. Crooks G.E., Hon G., Chandonia J.M., and Brenner S.E. WebLogo: a sequence logo generator. Genome Res. 14 (2004) 1188-1190
73. George R.A., Lin K., and Heringa J. Scooby-domain: prediction of globular domains in protein sequence. Nucleic Acids Res. 33 (2005) W160-W163
74. Suyama M., and Ohara O. DomCut: prediction of inter-domain linker regions in amino acid sequences. Bioinformatics 19 (2003) 673-674
75. Marsden R.L., McGuffin L.J., and Jones D.T. Rapid protein domain assignment from amino acid sequence using predicted secondary structure. Protein Sci. 11 (2002) 2814-2824
76. Linding R., Russell R.B., Neduva V., and Gibson T.J. GlobPlot: exploring protein sequences for globularity and disorder. Nucleic Acids Res. 31 (2003) 3701-3708
77. Cheng J. DOMAC: an accurate, hybrid protein domain prediction server. Nucleic Acids Res. 35 (2007) W354-W356
78. Vucetic S., Brown C.J., Dunker A.K., and Obradovic Z. Flavors of protein disorder. Proteins: Struct. Funct. Genet. 52 (2003) 573-584
79. Ishida T., and Kinoshita K. PrDOS: prediction of disordered protein regions from amino acid sequence. Nucleic Acids Res. 35 (2007) W460-W464
80. Ward J.J., McGuffin L.J., Bryson K., Buxton B.F., and Jones D.T. The DISOPRED server for the prediction of protein disorder. Bioinformatics 20 (2004) 2138-2139
81. Vullo A., Bortolami O., Pollastri G., and Tosatto S.C. Spritz: a server for the prediction of intrinsically disordered regions in protein sequences using kernel machines. Nucleic Acids Res. 34 (2006) W164-W168
82. Dosztanyi Z., Csizmok V., Tompa P., and Simon I. IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 21 (2005) 3433-3434
83. Su C.T., Chen C.Y., and Hsu C.M. iPDA: integrated protein disorder analyzer. Nucleic Acids Res. 35 (2007) W465-W472
84. Jones D.T. Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 292 (1999) 195-202
85. Adamczak R., Porollo A., and Meller J. Combining prediction of secondary structure and solvent accessibility in proteins. Proteins: Struct. Funct. Genet. 59 (2005) 467-475
86. Cuff J.A., and Barton G.J. Application of multiple sequence alignment profiles to improve protein secondary structure prediction. Proteins: Struct. Funct. Genet. 40 (2000) 502-511
87. Pollastri G., and McLysaght A. Porter: a new, accurate server for protein secondary structure prediction. Bioinformatics 21 (2005) 1719-1720
88. Soding J. Protein homology detection by HMM-HMM comparison. Bioinformatics 21 (2005) 951-960
89. Jaroszewski L., Rychlewski L., Li Z., Li W., and Godzik A. FFAS03: a server for profile-profile sequence alignments. Nucleic Acids Res. 33 (2005) W284-W288
90. Karplus K., Katzman S., Shackleford G., Koeva M., Draper J., Barnes B., et al. SAM-T04: what is new in protein-structure prediction for CASP6. Proteins: Struct. Funct. Genet. 61 (2005) 135-142
91. Bennett-Lovsey R.M., Herbert A.D., Sternberg M.J., and Kelley L.A. Exploring the extremes of sequence/structure space with ensemble fold recognition in the program Phyre. Proteins: Struct. Funct. Genet. 70 (2008) 611-625
92. Fischer D. Hybrid fold recognition: combining sequence derived properties with evolutionary information. Pac. Symp. Biocomput. (2000) 119-130
93. Shi J., Blundell T.L., and Mizuguchi K. FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J. Mol. Biol. 310 (2001) 243-257
94. McGuffin L.J., and Jones D.T. Improvement of the GenTHREADER method for genomic fold recognition. Bioinformatics 19 (2003) 874-881
95. Liu S., Zhang C., Liang S., and Zhou Y. Fold recognition by concurrent use of solvent accessibility and residue depth. Proteins: Struct. Funct. Genet. 68 (2007) 636-645
96. Lundstrom J., Rychlewski L., Bujnicki J., and Elofsson A. Pcons: a neural-network-based consensus predictor that improves fold recognition. Protein Sci. 10 (2001) 2354-2362
97. Sali A., and Blundell T.L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234 (1993) 779-815
98. Plotz G., Welsch C., Giron-Monzon L., Friedhoff P., Albrecht M., Piiper A., et al. Mutations in the MutSα interaction interface of MLH1 can abolish DNA mismatch repair. Nucleic Acids Res. 34 (2006) 6574-6586