The Saccharomyces cerevisiae Mlh1-Mlh3 heterodimer is an endonuclease that preferentially binds to holliday junctions

Journal of Biological Chemistry

Volumn 289, Issue 9, 2014, Pages 5674-5686

  Ranjha, Lepakshi ^a   Anand, Roopesh ^a   Cejka, Petr ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL DATA; DNA RECOGNITION; DOUBLE STRANDED DNA; HOLLIDAY JUNCTIONS; HOMOLOGOUS RECOMBINATION; NUCLEASE ACTIVITY; PREFERENTIAL BINDING; PROTEIN FAMILY;

BIOMOLECULES; DNA; MOLECULES;

YEAST;

DOUBLE STRANDED DNA; ENDONUCLEASE; HETERODIMER; MUTL GAMMA PROTEIN; PROTEIN MLH1; PROTEIN MUTL; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; CROSSING OVER; GENETIC CONSERVATION; HOLLIDAY JUNCTION; HUMAN; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY;

DNA ENDONUCLEASE; DNA MISMATCH REPAIR; DNA REPAIR; DNA-BINDING PROTEIN; HOLLIDAY JUNCTION; HOMOLOGOUS RECOMBINATION; MEIOSIS; MLH1; MLH3; MUTLΓ;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; DEOXYRIBONUCLEASE I; DNA BREAKS, DOUBLE-STRANDED; DNA BREAKS, SINGLE-STRANDED; DNA, CRUCIFORM; DNA, FUNGAL; HUMANS; PROTEIN MULTIMERIZATION; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84896874313     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.533810     Document Type: Article

References (62)

1. Jackson, S. P., and Bartek, J. (2009) The DNA-damage response in human biology and disease. Nature 461, 1071-1078
2. Phadnis, N., Hyppa, R. W., and Smith, G. R. (2011) New and old ways to control meiotic recombination. Trends Genet. 27, 411-421
3. Zickler, D. (2006) From early homologue recognition to synaptonemal complex formation. Chromosoma 115, 158-174
4. Acharya, S., Foster, P. L., Brooks, P., and Fishel, R. (2003) The coordinated functions of the E. coli MutS and MutL proteins in mismatch repair. Mol. Cell 12, 233-246 (Pubitemid 36945047)
5. Jiricny, J. (2013) Postreplicative mismatch repair. Cold Spring Harb. Perspect. Biol. 5, a012633
6. Kunkel, T. A., and Erie, D. A. (2005) DNA mismatch repair. Annu. Rev. Biochem. 74, 681-710 (Pubitemid 40995521)
7. Flores-Rozas, H., and Kolodner, R. D. (1998) The Saccharomyces cerevisiae MLH3 gene functions in MSH3-dependent suppression of frameshift mutations. Proc. Natl. Acad. Sci. U.S.A. 95, 12404-12409 (Pubitemid 28483778)
8. Harfe, B. D., Minesinger, B. K., and Jinks-Robertson, S. (2000) Discrete in vivo roles for the MutL homologs Mlh2p and Mlh3p in the removal of frameshift intermediates in budding yeast. Curr. Biol. 10, 145-148 (Pubitemid 30115745)
9. Lipkin, S. M., Wang, V., Jacoby, R., Banerjee-Basu, S., Baxevanis, A. D., Lynch, H. T., Elliott, R. M., and Collins, F. S. (2000) MLH3. A DNA mismatch repair gene associated with mammalian microsatellite instability. Nat. Genet. 24, 27-35 (Pubitemid 30041416)
10. Wang, T. F., Kleckner, N., and Hunter, N. (1999) Functional specificity of MutL homologs in yeast. Evidence for three Mlh1-based heterocomplexes with distinct roles during meiosis in recombination and mismatch correction. Proc. Natl. Acad. Sci. U.S.A. 96, 13914-13919
11. Cannavo, E., Marra, G., Sabates-Bellver, J., Menigatti, M., Lipkin, S. M., Fischer, F., Cejka, P., and Jiricny, J. (2005) Expression of the MutL homologue hMLH3 in human cells and its role in DNA mismatch repair. Cancer Res. 65, 10759-10766 (Pubitemid 41713344)
12. Kadyrov, F. A., Dzantiev, L., Constantin, N., and Modrich, P. (2006) Endonucleolytic function of MutLα in human mismatch repair. Cell 126, 297-308 (Pubitemid 44092957)
13. Kadyrov, F. A., Holmes, S. F., Arana, M. E., Lukianova, O. A., O'Donnell, M., Kunkel, T.A., and Modrich, P. (2007) Saccharomyces cerevisiae MutLα is a mismatch repair endonuclease. J. Biol. Chem. 282, 37181-37190
14. Guarné, A. (2012) The functions of MutL in mismatch repair. The power of multitasking. Prog. Mol. Biol. Transl. Sci. 110, 41-70
15. Gueneau, E., Dherin, C., Legrand, P., Tellier-Lebegue, C., Gilquin, B., Bonnesoeur, P., Londino, F., Quemener, C., Le Du, M. H., Márquez, J. A., Moutiez, M., Gondry, M., Boiteux, S., and Charbonnier, J. B. (2013) Structure of the MutLα C-terminal domain reveals how Mlh1 contributes to Pms1 endonuclease site. Nat. Struct. Mol. Biol. 20, 461-468
16. Hall, M. C., Shcherbakova, P. V., Fortune, J. M., Borchers, C. H., Dial, J. M., Tomer, K. B., and Kunkel, T. A. (2003) DNA binding by yeast Mlh1 and Pms1. Implications for DNA mismatch repair. Nucleic Acids Res. 31, 2025-2034 (Pubitemid 37442070)
17. Habraken, Y., Sung, P., Prakash, L., and Prakash, S. (1997) Enhancement of MSH2-MSH3-mediated mismatch recognition by the yeast MLH1-PMS1 complex. Curr. Biol. 7, 790-793 (Pubitemid 27441833)
18. Pillon, M. C., Lorenowicz, J. J., Uckelmann, M., Klocko, A. D., Mitchell, R. R., Chung, Y. S., Modrich, P., Walker, G. C., Simmons, L. A., Friedhoff, P., and Guarné, A. (2010) Structure of the endonuclease domain of MutL. Unlicensed to cut. Mol. Cell 39, 145-151
19. Keeney, S. (2008) Spo11 and the formation of DNA double-strand breaks in meiosis. Genome Dyn. Stab. 2, 81-123
20. Lynn, A., Soucek, R., and Börner, G. V. (2007) ZMM proteins during meiosis. Crossover artists at work. Chromosome Res. 15, 591-605 (Pubitemid 47221377)
21. Börner, G. V., Kleckner, N., and Hunter, N. (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117, 29-45 (Pubitemid 38469896)
22. Hunter, N., and Kleckner, N. (2001) The single-end invasion. An asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination. Cell 106, 59-70 (Pubitemid 32709958)
23. Argueso, J. L., Wanat, J., Gemici, Z., and Alani, E. (2004) Competing crossover pathways act during meiosis in Saccharomyces cerevisiae. Genetics 168, 1805-1816
24. de los Santos, T., Hunter, N., Lee, C., Larkin, B., Loidl, J., and Hollingsworth, N. M. (2003) The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics 164, 81-94
25. Kneitz, B., Cohen, P. E., Avdievich, E., Zhu, L., Kane, M. F., Hou, H., Jr., Kolodner, R. D., Kucherlapati, R., Pollard, J. W., and Edelmann, W. (2000) MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev. 14, 1085-1097 (Pubitemid 30324422)
26. Santucci-Darmanin, S., Neyton, S., Lespinasse, F., Saunières, A., Gaudray, P., and Paquis-Flucklinger, V. (2002) The DNA mismatch-repair MLH3 protein interacts with MSH4 in meiotic cells, supporting a role for this MutL homolog in mammalian meiotic recombination. Hum. Mol. Genet. 11, 1697-1706 (Pubitemid 34812091)
27. Snowden, T., Acharya, S., Butz, C., Berardini, M., and Fishel, R. (2004) hMSH4-hMSH5 recognizes Holliday junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes. Mol. Cell 15, 437-451 (Pubitemid 39092759)
28. Lenzi, M. L., Smith, J., Snowden, T., Kim, M., Fishel, R., Poulos, B. K., and Cohen, P. E. (2005) Extreme heterogeneity in the molecular events leading to the establishment of chiasmata during meiosis i in human oocytes. Am. J. Hum. Genet. 76, 112-127 (Pubitemid 40023770)
29. Zakharyevich, K., Tang, S., Ma, Y., and Hunter, N. (2012) Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase. Cell 149, 334-347
30. Zakharyevich, K., Ma, Y., Tang, S., Hwang, P. Y., Boiteux, S., and Hunter, N. (2010) Temporally and biochemically distinct activities of Exo1 during meiosis. Double-strand break resection and resolution of double Holliday junctions. Mol. Cell 40, 1001-1015
31. Nishant, K. T., Plys, A. J., and Alani, E. (2008) A mutation in the putative MLH3 endonuclease domain confers a defect in both mismatch repair and meiosis in Saccharomyces cerevisiae. Genetics 179, 747-755
32. De Muyt, A., Jessop, L., Kolar, E., Sourirajan, A., Chen, J., Dayani, Y., and Lichten, M. (2012) BLM helicase ortholog Sgs1 is a central regulator of meiotic recombination intermediate metabolism. Mol. Cell 46, 43-53
33. Kolas, N. K., Svetlanov, A., Lenzi, M. L., Macaluso, F. P., Lipkin, S. M., Liskay, R. M., Greally, J., Edelmann, W., and Cohen, P. E. (2005) Localization ofMMRproteins on meiotic chromosomes in mice indicates distinct functions during prophase I. J. Cell Biol. 171, 447-458 (Pubitemid 41586934)
34. Marcon, E., and Moens, P. (2003) MLH1p and MLH3p localize to precociously induced chiasmata of okadaic acid-treated mouse spermatocytes. Genetics 165, 2283-2287 (Pubitemid 38040307)
35. 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., Ashley, T., and Liskay, R. M. (1996) Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat. Genet. 13, 336-342 (Pubitemid 26230500)
36. Barlow, A. L., and Hultén, M. A. (1998) Crossing over analysis at pachytene in man. Eur. J. Hum. Genet. 6, 350-358 (Pubitemid 28395797)
37. Cejka, P., and Kowalczykowski, S. C. (2010) The full-length Saccharomyces cerevisiae Sgs1 protein is a vigorous DNA helicase that preferentially unwinds holliday junctions. J. Biol. Chem. 285, 8290-8301
38. Cejka, P., Plank, J. L., Dombrowski, C. C., and Kowalczykowski, S. C. (2012) Decatenation of DNA by the S. cerevisiae Sgs1-Top3-Rmi1 and RPA complex. A mechanism for disentangling chromosomes. Mol. Cell 47, 886-896
39. Räschle, M., Marra, G., Nyström-Lahti, M., Schär, P., and Jiricny, J. (1999) Identification of hMutLβ, a heterodimer of hMLH1 and hPMS1. J. Biol. Chem. 274, 32368-32375
40. Cannavo, E., Cejka, P., and Kowalczykowski, S. C. (2013) Relationship of DNA degradation by Saccharomyces cerevisiae exonuclease 1 and its stimulation by RPA and Mre11-Rad50-Xrs2 to DNA end resection. Proc. Natl. Acad. Sci. U.S.A. 110, E1661-E1668
41. Biswas, E. E., Chen, P. H., and Biswas, S. B. (1995) Overexpression and rapid purification of biologically active yeast proliferating cell nuclear antigen. Protein Expr. Purif. 6, 763-770
42. Finkelstein, J., Antony, E., Hingorani, M. M., and O'Donnell, M. (2003) Overproduction and analysis of eukaryotic multiprotein complexes in Escherichia coli using a dual-vector strategy. Anal. Biochem. 319, 78-87 (Pubitemid 36802145)
43. Rass, U., Compton, S. A., Matos, J., Singleton, M. R., Ip, S. C., Blanco, M. G., Griffith, J. D., and West, S. C. (2010) Mechanism of Holliday junction resolution by the human GEN1 protein. Genes Dev. 24, 1559-1569
44. Sonntag Brown, M., Lim, E., Chen, C., Nishant, K. T., and Alani, E. (2013) Genetic analysis of mlh3 mutations reveals interactions between crossover promoting factors during meiosis in baker's yeast. G3 3, 9-22
45. Räschle, M., Dufner, P., Marra, G., and Jiricny, J. (2002) 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, 21810-21820 (Pubitemid 34952333)
46. Tran, P. T., Erdeniz, N., Dudley, S., and Liskay, R. M. (2002) Characterization of nuclease-dependent functions of Exo1p in Saccharomyces cerevisiae. DNA Repair 1, 895-912
47. Hall, M. C., Wang, H., Erie, D. A., and Kunkel, T. A. (2001) High affinity cooperative DNA binding by the yeast Mlh1-Pms1 heterodimer. J. Mol. Biol. 312, 637-647 (Pubitemid 33116730)
48. Hall, M. C., Shcherbakova, P. V., and Kunkel, T. A. (2002) Differential ATP binding and intrinsic ATP hydrolysis by amino-terminal domains of the yeast Mlh1 and Pms1 proteins. J. Biol. Chem. 277, 3673-3679 (Pubitemid 34953241)
49. Plys, A. J., Rogacheva, M. V., Greene, E. C., and Alani, E. (2012) The unstructured linker arms of Mlh1-Pms1 are important for interactions with DNA during mismatch repair. J. Mol. Biol. 422, 192-203
50. Marsischky, G. T., and Kolodner, R. D. (1999) Biochemical characterization of the interaction between the Saccharomyces cerevisiae MSH2-MSH6 complex and mispaired bases in DNA. J. Biol. Chem. 274, 26668-26682
51. Gradia, S., Acharya, S., and Fishel, R. (1997) The human mismatch recognition complex hMSH2-hMSH6 functions as a novel molecular switch. Cell 91, 995-1005 (Pubitemid 28027832)
52. Lilley, D. M., and Clegg, R. M. (1993) The structure of the four-way junction in DNA. Annu. Rev. Biophys. Biomol. Struct. 22, 299-328 (Pubitemid 23180326)
53. Duckett, D. R., Murchie, A. I., Diekmann, S., von Kitzing, E., Kemper, B., and Lilley, D. M. (1988) The structure of the Holliday junction, and its resolution. Cell 55, 79-89
54. Lipkin, S. M., Moens, P. B., Wang, V., Lenzi, M., Shanmugarajah, D., Gilgeous, A., Thomas, J., Cheng, J., Touchman, J. W., Green, E. D., Schwartzberg, P., Collins, F. S., and Cohen, P. E. (2002) Meiotic arrest and aneuploidy in MLH3-deficient mice. Nat. Genet. 31, 385-390 (Pubitemid 35154447)
55. Svetlanov, A., Baudat, F., Cohen, P. E., and de Massy, B. (2008) Distinct functions of MLH3 at recombination hot spots in the mouse. Genetics 178, 1937-1945
56. Habraken, Y., Sung, P., Prakash, L., and Prakash, S. (1998) ATP-dependent assembly of a ternary complex consisting of a DNA mismatch and the yeast MSH2-MSH6 and MLH1-PMS1 protein complexes. J. Biol. Chem. 273, 9837-9841 (Pubitemid 28183079)
57. Gorman, J., Plys, A. J., Visnapuu, M. L., Alani, E., and Greene, E. C. (2010) Visualizing one-dimensional diffusion of eukaryotic DNA repair factors along a chromatin lattice. Nat. Struct. Mol. Biol. 17, 932-938
58. Hombauer, H., Campbell, C. S., Smith, C. E., Desai, A., and Kolodner, R. D. (2011) Visualization of eukaryotic DNA mismatch repair reveals distinct recognition and repair intermediates. Cell 147, 1040-1053
59. White, M. F., and Lilley, D. M. (1997) The resolving enzyme CCE1 of yeast opens the structure of the four-wayDNAjunction. J. Mol. Biol. 266, 122-134 (Pubitemid 27170523)
60. Bennett, R. J., and West, S. C. (1995) Structural analysis of the RuvC-Holliday junction complex reveals an unfolded junction. J. Mol. Biol. 252, 213-226
61. Snowden, T., Shim, K. S., Schmutte, C., Acharya, S., and Fishel, R. (2008) hMSH4-hMSH5 adenosine nucleotide processing and interactions with homologous recombination machinery. J. Biol. Chem. 283, 145-154
62. Wang, T. F., and Kung, W. M. (2002) Supercomplex formation between Mlh1-Mlh3 and Sgs1-Top3 heterocomplexes in meiotic yeast cells. Biochem. Biophys. Res. Commun. 296, 949-953