The ATPase activity of MLH1 is required to orchestrate DNA double-strand breaks and end processing during class switch recombination

Journal of Experimental Medicine

Volumn 209, Issue 4, 2012, Pages 671-678

  Chahwan, Richard ^a   van Oers, Johanna M M ^a   Avdievich, Elena ^a   Zhao, Chunfang ^a   Edelmann, Winfried ^a   Scharff, Matthew D ^a   Roa, Sergio Roa ^a,b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF NAVARRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DOUBLE STRANDED DNA; ENDONUCLEASE; PROTEIN MLH1; MLH1 PROTEIN, MOUSE; NUCLEAR PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; DNA STRAND BREAKAGE; ENZYME ACTIVITY; ENZYME ANALYSIS; GENE REARRANGEMENT; GENE TARGETING; GENETIC RECOMBINATION; MISMATCH REPAIR; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; ANIMAL; B LYMPHOCYTE; DNA END JOINING REPAIR; DNA REPAIR; DOUBLE STRANDED DNA BREAK; GENETICS; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; SOMATIC HYPERMUTATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADENOSINE TRIPHOSPHATASES; ANIMALS; B-LYMPHOCYTES; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; DNA REPAIR; IMMUNOGLOBULIN CLASS SWITCHING; MICE; NUCLEAR PROTEINS; RECOMBINATION, GENETIC; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN;

EID: 84861740928     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20111531     Document Type: Article

References (42)

1. Avdievich, E., C. Reiss, S.J. Scherer, Y. Zhang, S.M. Maier, B. Jin, H. Hou Jr., A. Rosenwald, H. Riedmiller, R. Kucherlapati, et al. 2008. Distinct effects of the recurrent Mlh1G67R mutation on MMR functions, cancer, and meiosis. Proc. Natl. Acad. Sci. USA. 105:4247-4252. http://dx.doi.org/10.1073/pnas.0800276105
2. Ban, C., M. Junop, and W. Yang. 1999. Transformation of MutL by ATP binding and hydrolysis: a switch in DNA mismatch repair. Cell. 97:85-97. http://dx.doi.org/10.1016/S0092-8674(00)80717-5
3. Bergerat, A., B. de Massy, D. Gadelle, P.C. Varoutas, A. Nicolas, and P. Forterre. 1997. An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature. 386:414-417. http://dx.doi.org/10.1038/386414a0
4. Bothmer, A., D.F. Robbiani, M. Di Virgilio, S.F. Bunting, I.A. Klein, N. Feldhahn, J. Barlow, H.T. Chen, D. Bosque, E. Callen, et al. 2011. Regulation of DNA end joining, resection, and immunoglobulin class switch recombination by 53BP1. Mol. Cell. 42:319-329. http://dx.doi.org/10.1016/j.molcel.2011.03.019
5. Cannavo, E., B. Gerrits, G. Marra, R. Schlapbach, and J. Jiricny. 2007. Characterization of the interactome of the human MutL homologues MLH1, PMS1, and PMS2. J. Biol. Chem. 282:2976-2986. http://dx.doi.org/10.1074/jbc.M609989200
6. Chahwan, R., W. Edelmann, M.D. Scharff, and S. Roa. 2011. Mismatchmediated error prone repair at the immunoglobulin genes. Biomed. Pharmacother. 65:529-536. http://dx.doi.org/10.1016/j.biopha.2011.09.001
7. Dutta, R., and M. Inouye. 2000. GHKL, an emergent ATPase/kinase superfamily. Trends Biochem. Sci. 25:24-28. http://dx.doi.org/10.1016/S0968-0004(99)01503-0
8. Eccleston, J., C. Yan, K. Yuan, F.W. Alt, and E. Selsing. 2011. Mismatch repair proteins MSH2, MLH1, and EXO1 are important for class-switch recombination events occurring in B cells that lack nonhomologous end joining. J. Immunol. 186:2336-2343. http://dx.doi.org/10.4049/jimmunol.1003104
9. Edelmann, W., P.E. Cohen, M. Kane, K. Lau, B. Morrow, S. Bennett, A. Umar, T. Kunkel, G. Cattoretti, R. Chaganti, et al. 1996. Meiotic pachytene arrest in MLH1-deficient mice. Cell. 85:1125-1134. http://dx.doi.org/10.1016/S0092-8674(00)81312-4
10. Ehrenstein, M.R., C. Rada, A.M. Jones, C. Milstein, and M.S. Neuberger. 2001. Switch junction sequences in PMS2-deficient mice reveal a microhomology-mediated mechanism of Ig class switch recombination. Proc. Natl. Acad. Sci. USA. 98:14553-14558. http://dx.doi.org/10.1073/pnas.241525998
11. Genschel, J., and P. Modrich. 2009. Functions of MutLalpha, replication protein A (RPA), and HMGB1 in 5α-directed mismatch repair. J. Biol. Chem. 284:21536-21544. http://dx.doi.org/10.1074/jbc.M109.021287
12. Hu, X., M. Machius, and W. Yang. 2003. Monovalent cation dependence and preference of GHKL ATPases and kinases. FEBS Lett. 544:268-273. http://dx.doi.org/10.1016/S0014-5793(03)00519-2
13. Iyer, R.R., A. Pluciennik, V. Burdett, and P.L. Modrich. 2006. DNA mismatch repair: functions and mechanisms. Chem. Rev. 106:302-323. http://dx.doi.org/10.1021/cr0404794
14. Jiricny, J. 2006. The multifaceted mismatch-repair system. Nat. Rev. Mol. Cell Biol. 7:335-346. http://dx.doi.org/10.1038/nrm1907
15. Johnson, J.R., N. Erdeniz, M. Nguyen, S. Dudley, and R.M. Liskay. 2010. Conservation of functional asymmetry in the mammalian MutLα ATPase. DNA Repair (Amst.). 9:1209-1213. http://dx.doi.org/10.1016/j.dnarep.2010.08.006
16. Kim, N., G. Bozek, J.C. Lo, and U. Storb. 1999. Different mismatch repair deficiencies all have the same effects on somatic hypermutation: Intact primary mechanism accompanied by secondary modifications. J. Exp. Med. 190:21-30. http://dx.doi.org/10.1084/jem.190.1.21
17. Kotnis, A., L. Du, C. Liu, S.W. Popov, and Q. Pan-Hammarström. 2009. Nonhomologous end joining in class switch recombination: the beginning of the end. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364:653-665. http://dx.doi.org/10.1098/rstb.2008.0196
18. Kuang, F.L., Z. Luo, and M.D. Scharff. 2009. H3 trimethyl K9 and H3 acetyl K9 chromatin modifications are associated with class switch recombination. Proc. Natl. Acad. Sci. USA. 106:5288-5293. http://dx.doi.org/10.1073/pnas.0901368106
19. Kunkel, T.A., and D.A. Erie. 2005. DNA mismatch repair. Annu. Rev. Biochem. 74:681-710. http://dx.doi.org/10.1146/annurev.biochem.74.082803.133243
20. Lieber, M.R. 2010. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem. 79:181-211. http://dx.doi.org/10.1146/annurev.biochem.052308.093131
21. MacCarthy, T., S. Roa, M.D. Scharff, and A. Bergman. 2009. SHMTool: a webserver for comparative analysis of somatic hypermutation datasets. DNA Repair (Amst.). 8:137-141. http://dx.doi.org/10.1016/j.dnarep.2008.09.006
22. Maul, R.W., H. Saribasak, S.A. Martomo, R.L. McClure, W. Yang, A. Vaisman, H.S. Gramlich, D.G. Schatz, R. Woodgate, D.M. Wilson III, and P.J. Gearhart. 2011. Uracil residues dependent on the deaminase AID in immunoglobulin gene variable and switch regions. Nat. Immunol. 12:70-76. http://dx.doi.org/10.1038/ni.1970
23. Péron, S., A. Metin, P. Gardès, M.A. Alyanakian, E. Sheridan, C.P. Kratz, A. Fischer, and A. Durandy. 2008. Human PMS2 deficiency is associated with impaired immunoglobulin class switch recombination. J. Exp. Med. 205:2465-2472. http://dx.doi.org/10.1084/jem.20080789
24. Phung, Q.H., D.B. Winter, R. Alrefai, and P.J. Gearhart. 1999. Hypermutation in Ig V genes from mice deficient in the MLH1 mismatch repair protein. J. Immunol. 162:3121-3124.
25. Pillon, M.C., J.J. Lorenowicz, M. Uckelmann, A.D. Klocko, R.R. Mitchell, Y.S. Chung, P. Modrich, G.C. Walker, L.A. Simmons, P. Friedhoff, and A. Guarné. 2010. Structure of the endonuclease domain of MutL: unlicensed to cut. Mol. Cell. 39:145-151. http://dx.doi.org/10.1016/j.molcel.2010.06.027
26. Polosina, Y.Y., and C.G. Cupples. 2010. MutL: conducting the cell's response to mismatched and misaligned DNA. Bioessays. 32:51-59. http://dx.doi.org/10.1002/bies.200900089
27. Raevaara, T.E., M.K. Korhonen, H. Lohi, H. Hampel, E. Lynch, K.E. Lönnqvist, E. Holinski-Feder, C. Sutter, W. McKinnon, S. Duraisamy, et al. 2005. Functional significance and clinical phenotype of nontruncating mismatch repair variants of MLH1. Gastroenterology. 129:537-549.
28. Ramachandran, S., R. Chahwan, R.M. Nepal, D. Frieder, S. Panier, S. Roa, A. Zaheen, D. Durocher, M.D. Scharff, and A. Martin. 2010. The RNF8/RNF168 ubiquitin ligase cascade facilitates class switch recombination. Proc. Natl. Acad. Sci. USA. 107:809-814. http://dx.doi.org/10.1073/pnas.0913790107
29. Räschle, M., P. Dufner, G. Marra, and J. Jiricny. 2002. Mutations within the hMLH1 and hPMS2 subunits of the human MutLalpha mismatch repair factor affect its ATPase activity, but not its ability to interact with hMut-Salpha. J. Biol. Chem. 277:21810-21820. http://dx.doi.org/10.1074/jbc.M108787200
30. Roa, S., Z. Li, J.U. Peled, C. Zhao, W. Edelmann, and M.D. Scharff. 2010. MSH2/MSH6 complex promotes error-free repair of AID-induced dU:G mispairs as well as error-prone hypermutation of A:T sites. PLoS ONE. 5:e11182. http://dx.doi.org/10.1371/journal.pone.0011182
31. Rogakou, E.P., C. Boon, C. Redon, and W.M. Bonner. 1999. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146:905-916. http://dx.doi.org/10.1083/jcb.146.5.905
32. Sacho, E.J., F.A. Kadyrov, P. Modrich, T.A. Kunkel, and D.A. Erie. 2008. Direct visualization of asymmetric adenine-nucleotide-induced conformational changes in MutL alpha. Mol. Cell. 29:112-121. http://dx.doi.org/10.1016/j.molcel.2007.10.030
33. Schrader, C.E., W. Edelmann, R. Kucherlapati, and J. Stavnezer. 1999. Reduced isotype switching in splenic B cells from mice deficient in mismatch repair enzymes. J. Exp. Med. 190:323-330. http://dx.doi.org/10.1084/jem.190.3.323
34. Schrader, C.E., J.E. Guikema, E.K. Linehan, E. Selsing, and J. Stavnezer. 2007. Activation-induced cytidine deaminase-dependent DNA breaks in class switch recombination occur during G1 phase of the cell cycle and depend upon mismatch repair. J. Immunol. 179:6064-6071.
35. Shah, S.N., S.E. Hile, and K.A. Eckert. 2010. Defective mismatch repair, microsatellite mutation bias, and variability in clinical cancer phenotypes. Cancer Res. 70:431-435. http://dx.doi.org/10.1158/0008-5472. CAN-09-3049
36. Spampinato, C., and P. Modrich. 2000. The MutL ATPase is required for mismatch repair. J. Biol. Chem. 275:9863-9869. http://dx.doi.org/10.1074/jbc.275.13.9863
37. Stavnezer, J. 2011. Complex regulation and function of activation-induced cytidine deaminase. Trends Immunol. 32:194-201. http://dx.doi.org/10.1016/j.it.2011.03.003
38. Stavnezer, J., A. Björkman, L. Du, A. Cagigi, and Q. Pan-Hammarström. 2010. Mapping of switch recombination junctions, a tool for studying DNA repair pathways during immunoglobulin class switching. Adv. Immunol. 108:45-109. http://dx.doi.org/10.1016/B978-0-12-380995-7.00003-3
39. Steele, E.J. 2009. Mechanism of somatic hypermutation: critical analysis of strand biased mutation signatures at A:T and G:C base pairs. Mol. Immunol. 46:305-320. http://dx.doi.org/10.1016/j.molimm.2008.10.021
40. Tomer, G., A.B. Buermeyer, M.M. Nguyen, and R.M. Liskay. 2002. Contribution of human mlh1 and pms2 ATPase activities to DNA mismatch repair. J. Biol. Chem. 277:21801-21809. http://dx.doi.org/10.1074/jbc.M111342200
41. van Oers, J.M., S. Roa, U. Werling, Y. Liu, J. Genschel, H. Hou Jr., R.S. Sellers, P. Modrich, M.D. Scharff, and W. Edelmann. 2010. PMS2 endonuclease activity has distinct biological functions and is essential for genome maintenance. Proc. Natl. Acad. Sci. USA. 107:13384-13389. http://dx.doi.org/10.1073/pnas.1008589107
42. Yan, C.T., C. Boboila, E.K. Souza, S. Franco, T.R. Hickernell, M. Murphy, S. Gumaste, M. Geyer, A.A. Zarrin, J.P. Manis, et al. 2007. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature. 449:478-482. http://dx.doi.org/10.1038/nature06020