In vitro reconstitution of RNA primer removal in Archaea reveals the existence of two pathways

Biochemical Journal

Volumn 447, Issue 2, 2012, Pages 271-280

  Henneke, Ghislaine ^a,b,c  

^a Centre National de la Recherche Scientifique   (France)

^b UNIVERSITÉ DE BRETAGNE OCCIDENTALE   (France)

^c CNRS   (France)

Author keywords

Archaea; DNA ligase; DNA polymerase; Nuclease; Okazaki fragment

Indexed keywords

DNA DIRECTED DNA POLYMERASE BETA; DNA DIRECTED DNA POLYMERASE DELTA; DNA LIGASE I; ESTERASE; FLAP ENDONUCLEASE 1; LIGASE; OKAZAKI FRAGMENT; PRIMER RNA; RECOMBINANT PROTEIN; RIBONUCLEASE H; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DNA CLEAVAGE; DNA FLANKING REGION; DNA REPLICATION; DNA SYNTHESIS; ENZYME MECHANISM; ENZYME RECONSTITUTION; ENZYME SPECIFICITY; IN VITRO STUDY; LIGATION; NONHUMAN; PRIORITY JOURNAL; PYROCOCCUS ABYSSI;

DNA; DNA REPLICATION; FLAP ENDONUCLEASES; PYROCOCCUS ABYSSI; RIBONUCLEASE H; RNA; RNA POLYMERASE II;

PYROCOCCUS ABYSSI;

EID: 84866865361     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20120959     Document Type: Article

References (47)

1. Waga, S. and Stillman, B. (1994) Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro. Nature 369, 207-212 (Pubitemid 24154796)
2. Pursell, Z. F., Isoz, I., Lundstrom, E. B., Johansson, E. and Kunkel, T. A. (2007) Yeast DNA polymerase epsilon participates in leading-strand DNA replication. Science 317, 127-130 (Pubitemid 47056472)
3. Nick McElhinny, S. A., Gordenin, D. A., Stith, C. M., Burgers, P. M. and Kunkel, T. A. (2008) Division of labor at the eukaryotic replication fork. Mol. Cell 30, 137-144 (Pubitemid 351626683)
4. Anderson, S. and DePamphilis, M. L. (1979) Metabolism of Okazaki fragments during simian virus 40 DNA replication. J. Biol. Chem. 254, 11495-11504
5. 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)
6. Ayyagari, R., Gomes, X. V., Gordenin, D. A. and Burgers, P. M. (2003) Okazaki fragment maturation in yeast. I. Distribution of functions between FEN1 and DNA2. J. Biol. Chem. 278, 1618-1625 (Pubitemid 36801392)
7. Maga, G., Villani, G., Tillement, V., Stucki, M., Locatelli, G. A., Frouin, I., Spadari, S. and Hubscher, U. (2001) Okazaki fragment processing: modulation of the strand displacement activity of DNA polymerase δ by the concerted action of replication protein A, proliferating cell nuclear antigen, and flap endonuclease-1. Proc. Natl. Acad. Sci. U.S.A. 98, 14298-14303 (Pubitemid 33121386)
8. Tishkoff, D. X., Filosi, N., Gaida, G. M. and Kolodner, R. D. (1997) A novel mutation avoidance mechanism dependent on S. cerevisiae RAD27 is distinct from DNA mismatch repair. Cell 88, 253-263 (Pubitemid 28015874)
9. Bae, S. H., Bae, K. H., Kim, J. A. and Seo, Y. S. (2001) RPA governs endonuclease switching during processing of Okazaki fragments in eukaryotes. Nature 412, 456-461
10. Bae, S. H. and Seo, Y. S. (2000) Characterization of the enzymatic properties of the yeast dna2 helicase/endonuclease suggests a new model for Okazaki fragment processing. J. Biol. Chem. 275, 38022-38031
11. Budd, M. E. and Campbell, J. L. (1997) A yeast replicative helicase, Dna2 helicase, interacts with yeast FEN-1 nuclease in carrying out its essential function. Mol. Cell. Biol. 17, 2136-2142 (Pubitemid 27133299)
12. Kang, H. Y., Choi, E., Bae, S. H., Lee, K. H., Gim, B. S., Kim, H. D., Park, C., MacNeill, S. A. and Seo, Y. S. (2000) Genetic analyses of Schizosaccharomyces pombe dna2+ reveal that dna2 plays an essential role in Okazaki fragment metabolism. Genetics 155, 1055-1067 (Pubitemid 30463418)
13. Zheng, L., Zhou, M., Guo, Z., Lu, H., Qian, L., Dai, H., Qiu, J., Yakubovskaya, E., Bogenhagen, D. F., Demple, B. and Shen, B. (2008) Human DNA2 is a mitochondrial nuclease/helicase for efficient processing of DNA replication and repair intermediates. Mol. Cell 32, 325-336
14. 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)
15. 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
16. Matsunaga, F., Norais, C., Forterre, P. and Myllykallio, H. (2003) Identification of short 'eukaryotic' Okazaki fragments synthesized from a prokaryotic replication origin. EMBO Rep. 4, 154-158 (Pubitemid 36322156)
17. Desogus, G., Onesti, S., Brick, P., Rossi, M. and Pisani, F. M. (1999) Identification and characterization of a DNA primase from the hyperthermophilic archaeon Methanococcus jannaschii. Nucleic Acids Res. 27, 4444-4450 (Pubitemid 29533186)
18. Lao-Sirieix, S. H. and Bell, S. D. (2004) The heterodimeric primase of the hyperthermophilic archaeon Sulfolobus solfataricus possesses DNA and RNA primase, polymerase and 3- -terminal nucleotidyl transferase activities. J. Mol. Biol. 344, 1251-1263
19. Le Breton, M., Henneke, G., Norais, C., Flament, D., Myllykallio, H., Querellou, J. and Raffin, J. P. (2007) The heterodimeric primase from the euryarchaeon Pyrococcus abyssi: a multifunctional enzyme for initiation and repair? J. Mol. Biol. 374, 1172-1185 (Pubitemid 350130258)
20. Liu, L., Komori, K., Ishino, S., Bocquier, A. A., Cann, I. K., Kohda, D. and Ishino, Y. (2001) The archaeal DNA primase: biochemical characterization of the p41-p46 complex from Pyrococcus furiosus. J. Biol. Chem. 276, 45484-45490
21. Matsui, E., Nishio, M., Yokoyama, H., Harata, K., Darnis, S. and Matsui, I. (2003) Distinct domain functions regulating de novo DNA synthesis of thermostable DNA primase from hyperthermophile Pyrococcus horikoshii. Biochemistry 42, 14968-14976 (Pubitemid 37553527)
22. Henneke, G., Flament, D., Hubscher, U., Querellou, J. and Raffin, J. P. (2005) The hyperthermophilic euryarchaeota Pyrococcus abyssi likely requires the two DNA polymerases D and B for DNA replication. J. Mol. Biol. 350, 53-64 (Pubitemid 40804731)
23. Rouillon, C., Henneke, G., Flament, D., Querellou, J. and Raffin, J. P. (2007) DNA polymerase switching on homotrimeric PCNA at the replication fork of the Euryarchaea Pyrococcus abyssi. J. Mol. Biol. 369, 343-355 (Pubitemid 46678054)
24. Berquist, B. R., DasSarma, P. and DasSarma, S. (2007) Essential and non-essential DNA replication genes in the model halophilic Archaeon, Halobacterium sp. NRC-1. BMC Genet. 8, 31
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. Zhang, C., Guo, L., Deng, L., Wu, Y., Liang, Y., Huang, L. and She, Q. (2010) Revealing the essentiality of multiple archaeal pcna genes using a mutant propagation assay based on an improved knockout method. Microbiology 156, 3386-3397
27. Castrec, B., Rouillon, C., Henneke, G., Flament, D., Querellou, J. and Raffin, J. P. (2009) Binding to PCNA in euryarchaeal DNA replication requires two PIP motifs for DNA polymerase D and one PIP motif for DNA polymerase B. J. Mol. Biol. 394, 209-218
28. Tang, X. F., Shen, Y., Matsui, E. and Matsui, I. (2004) Domain topology of the DNA polymerase D complex from a hyperthermophilic archaeon Pyrococcus horikoshii. Biochemistry 43, 11818-11827 (Pubitemid 39277628)
29. Tori, K., Kimizu, M., Ishino, S. and Ishino, Y. (2007) DNA polymerases BI and D from the hyperthermophilic archaeon Pyrococcus furiosus both bind to proliferating cell nuclear antigen with their C-terminal PIP-box motifs. J. Bacteriol. 189, 5652-5657 (Pubitemid 47206412)
30. Cann, I. K., Ishino, S., Nomura, N., Sako, Y. and Ishino, Y. (1999) Two family B DNA polymerases from Aeropyrum pernix, an aerobic hyperthermophilic crenarchaeote. J. Bacteriol. 181, 5984-5992 (Pubitemid 29459908)
31. Iwai, T., Kurosawa, N., Itoh, Y. H., Kimura, N. and Horiuchi, T. (2000) Sequence analysis of three family B DNA polymerases from the thermoacidophilic crenarchaeon Sulfurisphaera ohwakuensis. DNA Res. 7, 243-251
32. Daimon, K., Kawarabayasi, Y., Kikuchi, H., Sako, Y. and Ishino, Y. (2002) Three proliferating cell nuclear antigen-like proteins found in the hyperthermophilic archaeon Aeropyrum pernix : interactions with the two DNA polymerases. J. Bacteriol. 184, 687-694 (Pubitemid 34150215)
33. Dionne, I., Nookala, R. K., Jackson, S. P., Doherty, A. J. and Bell, S. D. (2003) A heterotrimeric PCNA in the hyperthermophilic archaeon Sulfolobus solfataricus. Mol. Cell 11, 275-282 (Pubitemid 36126608)
34. Dore, 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)
35. Beattie, T. R. and Bell, S. D. (2012) Coordination of multiple enzyme activities by a single PCNA in archaeal Okazaki fragment maturation. EMBO J. 31, 1556-1567
36. Kiyonari, S., Takayama, K., Nishida, H. and Ishino, Y. (2006) Identification of a novel binding motif in Pyrococcus furiosus DNA ligase for the functional interaction with proliferating cell nuclear antigen. J. Biol. Chem. 281, 28023-28032 (Pubitemid 44414515)
37. 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. U.S.A. 106, 4647-4652
38. Erauso, G., Reysenbach, A. L., Godfroy, A., Meunier, J. R., Crump, B., Partensky, F., Baross, J. A., Marteinsson, V., Barbier, G., Pace, N. R. and Prieur, D. (1993) Pyrococcus abyssi sp. nov., a new hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Arch. Microbiol. 160, 338-349 (Pubitemid 23290214)
39. Cohen, G. N., Barbe, V., Flament, D., Galperin, M., Heilig, R., Lecompte, O., Poch, O., Prieur, D., Querellou, J., Ripp, R. et al. (2003) An integrated analysis of the genome of the hyperthermophilic archaeon Pyrococcus abyssi. Mol. Microbiol. 47, 1495-1512 (Pubitemid 36363335)
40. Gueguen, Y., Rolland, J. L., Lecompte, O., Azam, P., Le Romancer, G., Flament, D., Raffin, J. P. and Dietrich, J. (2001) Characterization of two DNA polymerases from the hyperthermophilic euryarchaeon Pyrococcus abyssi. Eur. J. Biochem. 268, 5961-5969 (Pubitemid 33079333)
41. Henneke, G., Gueguen, Y., Flament, D., Azam, P., Querellou, J., Dietrich, J., Hubscher, U. and Raffin, J. P. (2002) Replication Factor C from the hyperthermophilic archaeon Pyrococcus abyssi does not need ATP hydrolysis for clamp-loading and contains a functionally conserved RFC PCNA-binding domain. J. Mol. Biol. 323, 795-810 (Pubitemid 35341056)
42. Palud, A., Villani, G., L'Haridon, S., Querellou, J., Raffin, J. P. and Henneke, G. (2008) Intrinsic properties of the two replicative DNA polymerases of Pyrococcus abyssi in replicating abasic sites: possible role in DNA damage tolerance? Mol. Microbiol. 70, 746-761
43. Le Laz, S., Le Goaziou, A. and Henneke, G. (2010) Structure-specific nuclease activities of Pyrococcus abyssi RNase HII. J. Bacteriol. 192, 3689-3698
44. Jin, Y. H., Obert, R., Burgers, P. M., Kunkel, T. A., Resnick, M. A. and Gordenin, D. A. (2001) The 3'→5' exonuclease of DNA polymerase δ can substitute for the 5' flap endonuclease Rad27/Fen1 in processing Okazaki fragments and preventing genome instability. Proc. Natl. Acad. Sci. U.S.A. 98, 5122-5127 (Pubitemid 32397093)
45. Mossi, R., Ferrari, E. and Hubscher, U. (1998) DNA ligase I selectively affects DNA synthesis by DNA polymerases δ and ε suggesting differential functions in DNA replication and repair. J. Biol. Chem. 273, 14322-14330 (Pubitemid 28319148)
46. Creze, C., Ligabue, A., Laurent, S., Lestini, R., Laptenok, S. P., Khun, J., Vos, M. H., Czjzek, M., Myllykallio, H. and Flament, D. (2012) Modulation of the Pyrococcus abyssi NucS endonuclease activity by replication clamp at functional and structural levels. J. Biol. Chem. 287, 15648-15660
47. Zheng, L. and Shen, B. (2011) Okazaki fragment maturation: nucleases take centre stage. J. Mol. Cell Biol. 3, 23-30