PCNA directs type 2 RNase H activity on DNA replication and repair substrates

Nucleic Acids Research

Volumn 39, Issue 9, 2011, Pages 3652-3666

  Bubeck, Doryen ^a   Reijns, Martin A M ^b   Graham, Stephen C ^a,c   Astell, Katy R ^b   Jones, E Yvonne ^a   Jackson, Andrew P ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b WESTERN GENERAL HOSPITAL   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXY TERMINAL TELOPEPTIDE; CYCLINE; DOUBLE STRANDED DNA; OKAZAKI FRAGMENT; PRIMER RNA; RIBONUCLEASE H; RIBONUCLEASE H2; RIBONUCLEASE H2B; RIBONUCLEOTIDE; UNCLASSIFIED DRUG;

ARCHAEOGLOBUS FULGIDUS; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA REPAIR; DNA REPLICATION; ENZYME ACTIVITY; ENZYME LOCALIZATION; ESCHERICHIA COLI; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN INTERACTION;

ARCHAEOGLOBUS FULGIDUS; CRYSTALLOGRAPHY; DNA REPAIR ENZYMES; DNA REPLICATION; HUMANS; MODELS, MOLECULAR; PEPTIDES; PROLIFERATING CELL NUCLEAR ANTIGEN; RIBONUCLEASE H;

ARCHAEA; ARCHAEOGLOBUS FULGIDUS; EUKARYOTA;

EID: 79955993911     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq980     Document Type: Article

References (60)

1. Machida, Y., Okazaki, T. and Okazaki, R. (1977) Discontinuous replication of replicative form DNA from bacteriophage phiX174. Proc. Natl Acad. Sci. USA, 74, 2776-2779. (Pubitemid 8150819)
2. Li, X. and Manley, J.L. (2005) Inactivation of the SR protein splicing factor ASF/SF2 results in genomic instability. Cell, 122, 365-378. (Pubitemid 41127139)
3. Forstemann, K. and Lingner, J. (2005) Telomerase limits the extent of base pairing between template RNA and telomeric DNA. EMBO Rep., 6, 361-366. (Pubitemid 40561629)
4. Ohtani, N., Haruki, M., Morikawa, M., Crouch, R., Itaya, M. and Kanaya, S. (1999) Identification of the genes encoding Mn2+-dependent RNase HII and Mg2+-dependent RNase HIII from Bacillus subtilis: classification of RNases H into three families. Biochemistry, 38, 605-618.
5. Cerritelli, S.M., Frolova, E.G., Feng, C., Grinberg, A., Love, P.E. and Crouch, R.J. (2003) Failure to produce mitochondrial DNA results in embryonic lethality in Rnaseh1 null mice. Mol. Cell, 11, 807-815. (Pubitemid 36385132)
6. Frank, P., Braunshofer-Reiter, C., Wintersberger, U., Grimm, R. and Büsen, W. (1998) Cloning of the cDNA encoding the large subunit of human RNase HI, a homologue of the prokaryotic RNase HII. Proc. Natl Acad. Sci. USA, 95, 12872-12877. (Pubitemid 28509490)
7. Chapados, B.R., Chai, Q., Hosfield, D.J., Qiu, J., Shen, B. and Tainer, J.A. (2001) Structural biochemistry of a type 2 RNase H: RNA primer recognition and removal during DNA replication. J. Mol. Biol., 307, 541-556. (Pubitemid 33027677)
8. Chai, Q., Qiu, J., Chapados, B. and Shen, B. (2001) Archaeoglobus fulgidus RNase HII in DNA replication: enzymological functions and activity regulation via metal cofactors. Biochem. Biophys. Res. Commun., 286, 1073-1081. (Pubitemid 32924881)
9. Nowotny, M., Gaidamakov, S.A., Ghirlando, R., Cerritelli, S.M., Crouch, R.J. and Yang, W. (2007) Structure of human RNase H1 complexed with an RNA/DNA hybrid: insight into HIV reverse transcription. Mol. Cell, 28, 264-276. (Pubitemid 47599996)
10. Eder, P.S. and Walder, J.A. (1991) Ribonuclease H from K562 human erythroleukemia cells. Purification, characterization, and substrate specificity. J. Biol. Chem., 266, 6472-6479. (Pubitemid 21906242)
11. Jeong, H.S., Backlund, P.S., Chen, H.C., Karavanov, A.A. and Crouch, R.J. (2004) RNase H2 of Saccharomyces cerevisiae is a complex of three proteins. Nucleic Acids Res., 32, 407-414. (Pubitemid 38263032)
12. Crow, Y., Leitch, A., Hayward, B., Garner, A., Parmar, R., Griffith, E., Ali, M., Semple, C., Aicardi, J., Babul-Hirji, R. et al. (2006) Mutations in genes encoding ribonuclease H2 subunits cause Aicardi-Goutiè res syndrome and mimic congenital viral brain infection. Nat. Genet., 38, 910-916. (Pubitemid 44141659)
13. Rice, G., Patrick, T., Parmar, R., Taylor, C.F., Aeby, A., Aicardi, J., Artuch, R., Montalto, S.A., Bacino, C.A., Barroso, B. et al. (2007) Clinical and molecular phenotype of Aicardi-Goutieres syndrome. Am. J. Hum. Genet., 81, 713-725. (Pubitemid 47596540)
14. Aicardi, J. and Goutieres, F. (1984) A progressive familial encephalopathy in infancy with calcifications of the basal ganglia and chronic cerebrospinal fluid lymphocytosis. Ann. Neurol., 15, 49-54. (Pubitemid 14224219)
15. Ramantani, G., Kohlhase, J., Hertzberg, C., Innes, A.M., Engel, K., Hunger, S., Borozdin, W., Mah, J.K., Ungerath, K., Walkenhorst, H. et al. (2010) Expanding the phenotypic spectrum of lupus erythematosus in aicardi-goutieres syndrome. Arthritis Rheum., 62, 1469-1477.
16. Rigby, R.E., Leitch, A. and Jackson, A.P. (2008) Nucleic acid-mediated inflammatory diseases. Bioessays, 30, 833-842.
17. Yang, Y., Lindahl, T. and Barnes, D. (2007) Trex1 exonuclease degrades ssDNA to prevent chronic checkpoint activation and autoimmune disease. Cell, 131, 873-886. (Pubitemid 350138088)
18. Burgers, P.M. (2009) Polymerase dynamics at the eukaryotic DNA replication fork. J. Biol. Chem., 284, 4041-4045.
19. Rossi, M.L. and Bambara, R.A. (2006) Reconstituted Okazaki fragment processing indicates two pathways of primer removal. J. Biol. Chem., 281, 26051-26061. (Pubitemid 44401811)
20. Turchi, J., Huang, L., Murante, R., Kim, Y. and Bambara, R. (1994) Enzymatic completion of mammalian lagging-strand DNA replication. Proc. Natl Acad. Sci. USA, 91, 9803-9807. (Pubitemid 24311896)
21. Goulian, M., Richards, S.H., Heard, C.J. and Bigsby, B.M. (1990) Discontinuous DNA synthesis by purified mammalian proteins. J. Biol. Chem., 265, 18461-18471.
22. Ishimi, Y., Claude, A., Bullock, P. and Hurwitz, J. (1988) Complete enzymatic synthesis of DNA containing the SV40 origin of replication. J. Biol. Chem., 263, 19723-19733. (Pubitemid 19016456)
23. Rydberg, B. and Game, J. (2002) Excision of misincorporated ribonucleotides in DNA by RNase H (type 2) and FEN-1 in cell-free extracts. Proc. Natl Acad. Sci. USA, 99, 16654-16659. (Pubitemid 36034028)
24. Nick McElhinny, S.A., Watts, B.E., Kumar, D., Watt, D.L., Lundstrom, E.B., Burgers, P.M., Johansson, E., Chabes, A. and Kunkel, T.A. (2010) Abundant ribonucleotide incorporation into DNA by yeast replicative polymerases. Proc. Natl Acad. Sci. USA, 107, 4949-4954.
25. Meslet-Cladiere, L., Norais, C., Kuhn, J., Briffotaux, J., Sloostra, J.W., Ferrari, E., Hubscher, U., Flament, D. and Myllykallio, H. (2007) A novel proteomic approach identifies new interaction partners for proliferating cell nuclear antigen. J. Mol. Biol., 372, 1137-1148. (Pubitemid 47381450)
26. Chon, H., Vassilev, A., DePamphilis, M., Zhao, Y., Zhang, J., Burgers, P., Crouch, R. and Cerritelli, S. (2009) Contributions of the two accessory subunits, RNASEH2B and RNASEH2C, to the activity and properties of the human RNase H2 complex. Nucleic Acids Res., 37, 96-110.
27. Gulbis, J.M., Kelman, Z., Hurwitz, J., O'Donnell, M. and Kuriyan, J. (1996) Structure of the C-terminal region of p21(WAF1/CIP1) complexed with human PCNA. Cell, 87, 297-306. (Pubitemid 26359007)
28. Maga, G. and Hubscher, U. (2003) Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J. Cell. Sci., 116, 3051-3060. (Pubitemid 37038954)
29. Montecucco, A., Rossi, R., Levin, D.S., Gary, R., Park, M.S., Motycka, T.A., Ciarrocchi, G., Villa, A., Biamonti, G. and Tomkinson, A.E. (1998) DNA ligase I is recruited to sites of DNA replication by an interaction with proliferating cell nuclear antigen: identification of a common targeting mechanism for the assembly of replication factories. EMBO J., 17, 3786-3795. (Pubitemid 28327396)
30. Garg, P. and Burgers, P.M. (2005) DNA polymerases that propagate the eukaryotic DNA replication fork. Crit. Rev. Biochem. Mol. Biol., 40, 115-128. (Pubitemid 40604979)
31. Shaban, N.M., Harvey, S., Perrino, F.W. and Hollis, T. (2010) The structure of the mammalian RNase H2 complex provides insight into RNA.NA hybrid processing to prevent immune dysfunction. J. Biol. Chem., 285, 3617-3624.
32. Hosfield, D.J., Mol, C.D., Shen, B. and Tainer, J.A. (1998) Structure of the DNA repair and replication endonuclease and exonuclease FEN-1: coupling DNA and PCNA binding to FEN-1 activity. Cell, 95, 135-146. (Pubitemid 28458031)
33. Otwinowski, Z. and Minor, W. (1997) Macromolecular Crystallography, Part A. Academic Press, New York.
34. Collaborative Computational Project, Number 4. (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr., 50, 760-763.
35. Winter, G. (2010) xia2: an expert system for macromolecular crystallography data reduction. J. Appl. Crystallogr., 43, 186-190.
36. McCoy, A.J., Grosse-Kunstleve, R.W., Storoni, L.C. and Read, R.J. (2005) Likelihood-enhanced fast translation functions. Acta Crystallogr. D Biol. Crystallogr., 61, 458-464. (Pubitemid 43934606)
37. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132. (Pubitemid 41742764)
38. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W. et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr., 66, 213-221.
39. Blanc, E., Roversi, P., Vonrhein, C., Flensburg, C., Lea, S.M. and Bricogne, G. (2004) Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr. D Biol. Crystallogr., 60, 2210-2221. (Pubitemid 41742773)
40. Smart, O., Brandl, M., Flensburg, C., Keller, P., Paciorek, W., Vonrhein, C., Womack, T. and Bricogne, G. (2008) Abstract TP139. Annual Meeting of the ACA, Knoxville, TN, 137.
41. Davis, I.W., Leaver-Fay, A., Chen, V.B., Block, J.N., Kapral, G.J., Wang, X., Murray, L.W., Arendall, W.B. III, Snoeyink, J., Richardson, J.S. et al. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res., 35, W375-W383.
42. Vagin, A.A., Steiner, R.A., Lebedev, A.A., Potterton, L., McNicholas, S., Long, F. and Murshudov, G.N. (2004) REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use. Acta Crystallogr. D Biol. Crystallogr., 60, 2184-2195. (Pubitemid 41742770)
43. Gilljam, K.M., Feyzi, E., Aas, P.A., Sousa, M.M., Muller, R., Vagbo, C.B., Catterall, T.C., Liabakk, N.B., Slupphaug, G., Drablos, F. et al. (2009) Identification of a novel, widespread, and functionally important PCNA-binding motif. J. Cell Biol., 186, 645-654.
44. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol., 372, 774-797. (Pubitemid 47321791)
45. Chapados, B., Hosfield, D., Han, S., Qiu, J., Yelent, B., Shen, B. and Tainer, J. (2004) Structural basis for FEN-1 substrate specificity and PCNA-mediated activation in DNA replication and repair. Cell, 116, 39-50. (Pubitemid 38156182)
46. Sakurai, S., Kitano, K., Yamaguchi, H., Hamada, K., Okada, K., Fukuda, K., Uchida, M., Ohtsuka, E., Morioka, H. and Hakoshima, T. (2005) Structural basis for recruitment of human flap endonuclease 1 to PCNA. EMBO J., 24, 683-693. (Pubitemid 40396099)
47. Murante, R.S., Henricksen, L.A. and Bambara, R.A. (1998) Junction ribonuclease: an activity in Okazaki fragment processing. Proc. Natl Acad. Sci. USA, 95, 2244-2249. (Pubitemid 28145926)
48. Burgers, P.M. and Yoder, B.L. (1993) ATP-independent loading of the proliferating cell nuclear antigen requires DNA ends. J. Biol. Chem., 268, 19923-19926. (Pubitemid 23278881)
49. Balakrishnan, L., Stewart, J., Polaczek, P., Campbell, J.L. and Bambara, R.A. (2010) Acetylation of Dna2 endonuclease/helicase and flap endonuclease 1 by p300 promotes DNA stability by creating long flap intermediates. J. Biol. Chem., 285, 4398-4404.
50. Leonhardt, H., Rahn, H.P., Weinzierl, P., Sporbert, A., Cremer, T., Zink, D. and Cardoso, M.C. (2000) Dynamics of DNA replication factories in living cells. J. Cell. Biol., 149, 271-280.
51. Qiu, J., Qian, Y., Frank, P., Wintersberger, U. and Shen, B. (1999) Saccharomyces cerevisiae RNase H(35) functions in RNA primer removal during lagging-strand DNA synthesis, most efficiently in cooperation with Rad27 nuclease. Mol. Cell. Biol., 19, 8361-8371. (Pubitemid 30414030)
52. Mayanagi, K., Kiyonari, S., Saito, M., Shirai, T., Ishino, Y. and Morikawa, K. (2009) Mechanism of replication machinery assembly as revealed by the DNA ligase-PCNA-DNA complex architecture. Proc. Natl Acad. Sci. USA, 106, 4647-4652.
53. Doré,A.S., Kilkenny, M.L., Jones, S.A., Oliver, A.W., Roe, S.M., Bell, S.D. and Pearl, L.H. (2006) Structure of an archaeal PCNA1-PCNA2-FEN1 complex: elucidating PCNA subunit and client enzyme specificity. Nucleic Acids Res., 34, 4515-4526. (Pubitemid 44567051)
54. Bowman, G.D., O'Donnell, M. and Kuriyan, J. (2004) Structural analysis of a eukaryotic sliding DNA clamp-clamp loader complex. Nature, 429, 724-730. (Pubitemid 38833117)
55. Ii, M. and Brill, S.J. (2005) Roles of SGS1, MUS81, and RAD51 in the repair of lagging-strand replication defects in Saccharomyces cerevisiae. Curr. Genet., 48, 213-225. (Pubitemid 41683410)
56. Chen, J.Z., Qiu, J., Shen, B. and Holmquist, G.P. (2000) Mutational spectrum analysis of RNase H(35) deficient Saccharomyces cerevisiae using fluorescence-based directed termination PCR. Nucleic Acids Res., 28, 3649-3656.
57. Henricksen, L.A., Tom, S., Liu, Y. and Bambara, R.A. (2000) Inhibition of flap endonuclease 1 by flap secondary structure and relevance to repeat sequence expansion. J. Biol. Chem., 275, 16420-16427. (Pubitemid 30398861)
58. Kao, H.I. and Bambara, R.A. (2003) The protein components and mechanism of eukaryotic Okazaki fragment maturation. Crit. Rev. Biochem. Mol. Biol., 38, 433-452. (Pubitemid 38117383)
59. Schlee, M., Hartmann, E., Coch, C., Wimmenauer, V., Janke, M., Barchet, W. and Hartmann, G. (2009) Approaching the RNA ligand for RIG-I? Immunol. Rev., 227, 66-74.
60. Rehwinkel, J. and Reise Sousa, C. (2010) RIGorous detection: exposing virus through RNA sensing. Science, 327, 284-286.