The Characterization of Saccharomyces cerevisiae Mre11/Rad50/Xrs2 Complex Reveals that Rad50 Negatively Regulates Mre11 Endonucleolytic but not the Exonucleolytic Activity

Journal of Molecular Biology

Volumn 372, Issue 4, 2007, Pages 864-882

  Ghosal, Gargi ^a   Muniyappa, K ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

endonuclease; G quadruplex DNA; MRX N complex; negative regulation; telomeres

Indexed keywords

DOUBLE STRANDED DNA; ENDONUCLEASE; FUNGAL DNA; FUNGAL PROTEIN; MRE11 PROTEIN; PROTEIN XRS2; RAD50 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; DNA DAMAGE; DNA REPAIR; DNA SEQUENCE; ENZYME ACTIVATION; ENZYME REGULATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; HOMEOSTASIS; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

EID: 34548396349     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.07.013     Document Type: Article

References (75)

1. Sancar A., Lindsey-Boltz L.A., Unsal-Kacmaz K., and Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73 (2004) 39-85
2. Kironmai K.M., and Muniyappa K. Alteration of telomeric sequences and senescence caused by mutations in RAD50 of Saccharomyces cerevisiae. Genes Cell 2 (1997) 443-455
3. Pandita T.K., Pathak S., and Geard C.R. Chromosome end associations, telomeres and telomerase activity in ataxia telangiectasia cells. Cytogenet. Cell Genet. 71 (1995) 86-93
4. de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19 (2005) 2100-2110
5. Slijepcevic P. The role of DNA damage response proteins at telomeres - an "integrative" model. DNA Repair 5 (2006) 1299-1306
6. Pandita T.K., Hunt C.R., Sharma G.G., and Yang Q. Regulation of telomere movement by telomere chromatin structure. Cell Mol. Life Sci. 64 (2007) 131-138
7. Verdun R.E., and Karlseder J. Replication and protection of telomeres. Nature 447 (2007) 924-931
8. LeBel C., and Wellinger R.J. Telomeres: what's new at your end?. J. Cell Sci. 118 (2005) 2785-2788
9. Lydall D., and Whitehall S. Chromatin and the DNA damage response. DNA Repair 4 (2005) 1195-1207
10. de Lange T. T-loops and the origin of telomeres. Nature Rev. Mol. Cell Biol. 5 (2004) 323-329
11. Lin Y.C., Shih J.W., Hsu C.L., and Lin J.J. Binding and partial denaturing of G-quartet DNA by Cdc13p of Saccharomyces cerevisiae. J. Biol. Chem. 276 (2001) 47671-47674
12. Ghosal G., and Muniyappa K. Saccharomyces cerevisiae Mre11 is a high-affinity G4 DNA-binding protein and a G-rich DNA-specific endonuclease: implications for replication of telomeric DNA. Nucl. Acids Res. 33 (2005) 4692-4703
13. Frantz J.D., and Gilbert W. A novel yeast gene product, G4p1, with a specific affinity for quadruplex nucleic acids. J. Biol. Chem. 270 (1995) 20692-20697
14. Giraldo R., Suzuki M., Chapman L., and Rhodes D. Promotion of parallel DNA quadruplexes by a yeast telomere binding protein: a circular dichroism study. Proc. Natl Acad. Sci. USA 91 (1994) 7658-7662
15. Muniyappa K., Anuradha S., and Byers B. Yeast meiosis-specific protein Hop1 binds to G4 DNA and promotes its formation. Mol. Cell Biol. 20 (2000) 1361-1369
16. Liu Z., Lee A., and Gilbert W. Gene disruption of a G4-DNA-dependent nuclease in yeast leads to cellular senescence and telomere shortening. Proc. Natl Acad. Sci. USA 92 (1995) 6002-6006
17. Ritchie K.B., and Petes T. The Mre11p/Rad50p/Xrs2p complex and the Tel1p function in a single pathway for telomere maintenance in yeast. Genetics 155 (2000) 475-479
18. Boulton S.J., and Jackson S.P. Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J. 17 (1998) 1819-1828
19. Nugent C.I., Bosco G., Ross L.O., Evans S.K., Salinger A.P., Moore J.K., et al. Telomere maintenance is dependent on activities required for end repair of double-strand breaks. Curr. Biol. 8 (1998) 657-660
20. Tsukamoto Y., Taggart A.K., and Zakian V.A. The role of the Mre11-Rad50-Xrs2 complex in telomerase-mediated lengthening of Saccharomyces cerevisiae telomeres. Curr. Biol. 11 (2001) 1328-1335
21. Diede S.J., and Gottschling D.E. Exonuclease activity is required for sequence addition and Cdc13p loading at a de novo telomere. Curr. Biol. 11 (2001) 1336-1340
22. Frank C.J., Hyde M., and Greider C.W. Regulation of telomere elongation by the cyclin-dependent kinase CDK1. Mol. Cell 24 (2006) 423-432
23. Paull T.T., and Gellert M. The 3′ to 5′ exonuclease activity of Mre11 facilitates repair of DNA double-strand breaks. Mol. Cell 1 (1998) 969-979
24. Paull T.T., and Gellert M. A mechanistic basis for Mre11-directed DNA joining at microhomologies. Proc. Natl Acad. Sci. USA 97 (2000) 6409-6414
25. Trujillo K.M., Yuan S.S., Lee E.Y., and Sung P. Nuclease activities in a complex of human recombination and DNA repair factors Rad50, Mre11, and p95. J. Biol. Chem. 273 (1998) 21447-21450
26. Trujillo K.M., and Sung P. DNA structure-specific nuclease activities in the Saccharomyces cerevisiae Rad50-Mre11 complex. J. Biol. Chem. 276 (2001) 35458-35464
27. Moreau S., Ferguson J.R., and Symington L.S. The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol. Cell Biol. 19 (1999) 556-566
28. Raymond W.E., and Kleckner N. RAD50 protein of S. cerevisiae exhibits ATP-dependent DNA binding. Nucl. Acids Res. 21 (1993) 3851-3856
29. Moncalian G., Lengsfeld B., Bhaskara V., Hopfner K.P., Karcher A., Alden E., et al. The rad50 signature motif: essential to ATP binding and biological function. J. Mol. Biol. 335 (2004) 937-951
30. de Jager M., van Noort J., van Gent D.C., Dekker C., Kanaar R., and Wyman C. Human Rad50/Mre11 is a flexible complex that can tether DNA ends. Mol. Cell 8 (2001) 1129-1135
31. Hopfner K.P., Karcher A., Shin D.S., Craig L., Arthur L.M., Carney J.P., and Tainer J.A. Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101 (2000) 789-800
32. Trujillo K.M., Roh D.H., Chen L., Van Komen S., Tomkinson A., and Sung P. Yeast xrs2 binds DNA and helps target rad50 and mre11 to DNA ends. J. Biol. Chem. 278 (2003) 48957-48964
33. Nakada D., Matsumoto K., and Sugimoto K. ATM-related Tel1 associates with double-strand breaks through an Xrs2-dependent mechanism. Genes Dev. 17 (2003) 1957-1962
34. Dai Y., Kysela B., Hanakahi L.A., Manolis K., Riballo E., Stumm M., et al. Nonhomologous end joining and V(D)J recombination require an additional factor. Proc. Natl Acad. Sci. USA 100 (2003) 2462-2467
35. Clatworthy A.E., Valencia-Burton M.A., Haber J.E., and Oettinger M.A. The MRE11-RAD50-XRS2 complex, in addition to other non-homologous end-joining factors, is required for V(D)J joining in yeast. J. Biol. Chem. 280 (2005) 20247-20252
36. Maser R.S., Monsen K.J., Nelms B.E., and Petrini J.H. hMre11 and hRad50 nuclear foci are induced during the normal cellular response to DNA double-strand breaks. Mol. Cell Biol. 17 (1997) 6087-6096
37. Mirzoeva O.K., and Petrini J.H. DNA damage-dependent nuclear dynamics of the Mre11 complex. Mol. Cell Biol. 21 (2001) 281-288
38. Zhu X.D., Kuster B., Mann N., Petrini J.H., and de Lange T. Cell-cycle regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nature Genet. 25 (2000) 347-352
39. Chamankhah M., Fontanie T., and Xiao W. The Saccharomyces cerevisiae mre11(ts) allele confers a separation of DNA repair and telomere maintenance functions. Genetics 155 (2000) 569-576
40. Furuse M., Nagase Y., Tsubouchi H., Murakami-Murofushi K., Shibata T., and Ohta K. Distinct roles of two separable in vitro activities of yeast Mre11 in mitotic and meiotic recombination. EMBO J. 17 (1998) 6412-6425
41. Krogh B.O., Llorente B., Lam A., and Symington L.S. Mutations in Mre11 phosphoesterase motif I that impair Saccharomyces cerevisiae Mre11-Rad50-Xrs2 complex stability in addition to nuclease activity. Genetics 171 (2005) 1561-1570
42. Krogh B.O., and Symington L.S. Recombination proteins in yeast. Annu. Rev. Genet. 38 (2004) 233-271
43. Maringele L., and Lydall D. EXO1-dependent single-stranded DNA at telomeres activates subsets of DNA damage and spindle checkpoint pathways in budding yeast yku70Delta mutants. Genes Dev. 16 (2002) 1919-1933
44. Assenmacher N., and Hopfner K.P. MRE11/RAD50/NBS1: complex activities. Chromosoma 113 (2004) 157-166
45. Larrivee M., LeBel C., and Wellinger R.J. The generation of proper constitutive G-tails on yeast telomeres is dependent on the MRX complex. Genes Dev. 18 (2004) 1391-1396
46. Chai W., Sfeir A.J., Hoshiyama H., Shay J.W., and Wright W.E. The involvement of the Mre11/Rad50/Nbs1 complex in the generation of G-overhangs at human telomeres. EMBO Rep. 7 (2006) 225-230
47. Jackson S.P. Sensing and repairing DNA double-strand breaks. Carcinogenesis 23 (2002) 687-696
48. Valerie K., and Povirk L.F. Regulation and mechanisms of mammalian double-strand break repair. Oncogene 22 (2003) 5792-5812
49. Anderson D.E., Trujillo K.M., Sung P., and Erickson H.P. Structure of the Rad50-Mre11 DNA repair complex from Saccharomyces cerevisiae by electron microscopy. J. Biol. Chem. 276 (2001) 37027-37033
50. Chen L., Trujillo K.M., Komen S.V., Roh D.H., Krejci L., Lewis K.L., et al. Effect of amino acid substitutions in the rad50 ATP binding domain on DNA double strand break repair in yeast. J. Biol. Chem. 280 (2005) 2620-2627
51. Paull T.T., and Gellert M. Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes Dev. 13 (1999) 1276-1288
52. Roca A.I., and Cox M.M. RecA protein: structure, function, and role in recombinational DNA repair. Prog. Nucl. Acid Res. 56 (1997) 129-223
53. de Jager M., Wyman C., van Gent D.C., and Kanaar R. DNA end-binding specificity of human Rad50/Mre11 is influenced by ATP. Nucl. Acids Res. 30 (2002) 4425-4431
54. Holland I.B., and Blight M.A. ABC-ATPases, adaptable energy generators fuelling transmembrane movement of a variety of molecules in organisms from bacteria to humans. J. Mol. Biol. 293 (1999) 381-399
55. Ban C., and Yang W. Crystal structure and ATPase activity of MutL: implications for DNA repair and mutagenesis. Cell 95 (1998) 541-552
56. Webb B.L., Cox M.M., and Inman R.B. ATP hydrolysis and DNA binding by the Escherichia coli RecF protein. J. Biol. Chem. 274 (1999) 15367-15374
57. Santucci S., Bonne-Andrea C., and Clertant P. Bovine papillomavirus type 1 E1 ATPase activity does not depend on binding to DNA nor to viral E2 protein. J. Gen. Virol. 76 (1995) 1129-1140
58. Gai D., Li D., Finkielstein C.V., Ott R.D., Taneja P., Fanning E., and Chen X.S. Insights into the oligomeric states, conformational changes, and helicase activities of SV40 large tumor antigen. J. Biol. Chem. 279 (2004) 38952-38959
59. Smogorzewska A., and de Lange T. Regulation of telomerase by telomeric proteins. Annu. Rev. Biochem. 73 (2004) 177-208
60. Lundblad V. Telomere maintenance without telomerase. Oncogene 21 (2002) 522-531
61. Lee J.H., Ghirlando R., Bhaskara V., Hoffmeyer M.R., Gu J., and Paull T.T. Regulation of Mre11/Rad50 by Nbs1: effects on nucleotide-dependent DNA binding and association with ataxia-telangiectasia-like disorder mutant complexes. J. Biol. Chem. 278 (2003) 45171-45181
62. Janscak P., Garcia P.L., Hamburger F., Makuta Y., Shiraishi K., Imai Y., et al. Characterization and mutational analysis of the RecQ core of the bloom syndrome protein. J. Mol. Biol. 330 (2003) 29-42
63. Foster S.S., Zubko M.K., Guillard S., and Lydall D. MRX protects telomeric DNA at uncapped telomeres of budding yeast cdc13-1 mutants. DNA Repair 5 (2006) 840-851
64. Ghosal G., and Muniyappa K. Hoogsteen base-pairing revisited: resolving a role in normal biological processes and human diseases. Biochem. Biophys. Res. Commun. 343 (2006) 1-7
65. Maizels N. Dynamic roles for G4 DNA in the biology of eukaryotic cells. Nature Struct. Mol Biol. 13 (2006) 1055-1059
66. Sun H., Karow J.K., Hickson I.D., and Maizels N. The Bloom's syndrome helicase unwinds G4 DNA. J. Biol. Chem. 273 (1998) 27587-27592
67. Duqette M.L., Handa P., Vincent J.A., Taylor A.F., and Maizels N. Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA. Genes Dev. 18 (2004) 1618-1629
68. Nair D.T., Johnson R.E., Parkash S., Prakash L., and Aggarwal A.K. Replication by human DNA polymerase-iota occurs by Hoogsteen base-pairing. Nature 430 (2004) 377-380
69. Paeschke K., Simonsson T., Postberg J., Rhodes D., and Lipps H.J. Telomere end-binding proteins control the formation of G-quadruplex DNA structures in vivo. Nature Struct. Mol. Biol. 12 (2005) 847-854
70. Zahler A.M., Williamson J.R., Cech T.R., and Prescott D.M. Inhibition of telomerase by G-quartet DNA structures. Nature 350 (1991) 718-720
71. Chan S.W., and Blackburn E.H. New ways not to make ends meet: telomerase, DNA damage proteins and heterochromatin. Oncogene 21 (2002) 553-563
72. Craven R.J., and Petes T.D. Dependence of the regulation of telomere length on the type of subtelomeric repeats in the yeast Saccharomyces cerevisiae. Genetics 152 (1999) 1531-1541
73. Sambrook J., Fritsch E.F., and Maniatis T. Molecular Cloning: A Laboratory Manual. 2nd edit. (1989), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
74. Kironmai K.M., Muniyappa K., Friedman D.B., Hollingsworth N.M., and Byers B. DNA-binding activities of Hop1 protein, a synaptonemal complex component from Saccharomyces cerevisiae. Mol. Cell. Biol. 18 (1998) 1424-1435
75. Guhan N., and Muniyappa K. The RecA intein of Mycobacterium tuberculosis promotes cleavage of ectopic DNA sites: Implications for the dispersal of inteins in natural populations. J. Biol. Chem. 277 (2002) 40352-40361