A novel mechanism for regulating the activity of proliferating cell nuclear antigen by a small protein

Nucleic Acids Research

Volumn 42, Issue 9, 2014, Pages 5776-5789

  Li, Zhuo ^a   Huang, Richard Y C ^a,b   Yopp, Daniel C ^c   Hileman, Travis H ^c   Santangelo, Thomas J ^c   Hurwitz, Jerard ^d   Hudgens, Jeffrey W ^a,b   Kelman, Zvi ^a,b  

^a UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

^c OHIO STATE UNIVERSITY   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLINE; MESYLIC ACID METHYL ESTER; MITOMYCIN; PROTEIN INHIBITOR; THERMOCOCCALES INHIBITOR OF PROLIFERATING CELL NUCLEAR ANTIGEN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; DEUTERIUM HYDROGEN EXCHANGE; ESCHERICHIA COLI; GEL PERMEATION CHROMATOGRAPHY; IN VITRO STUDY; MASS SPECTROMETRY; METHANOTHERMOBACTER THERMAUTOTROPHICUS; MOLECULAR CLONING; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN PURIFICATION; REGULATORY MECHANISM; SITE DIRECTED MUTAGENESIS; SOUTHERN BLOTTING; THERMOCOCCUS KODAKARENSIS; TRIMERIZATION; ULTRAVIOLET RADIATION;

AMINO ACID SUBSTITUTION; ARCHAEAL PROTEINS; DEUTERIUM EXCHANGE MEASUREMENT; DNA POLYMERASE II; FLAP ENDONUCLEASES; KINETICS; MICROBIAL VIABILITY; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; THERMOCOCCUS;

EID: 84901363936     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku239     Document Type: Article

References (52)

1. Vivona, J.B. and Kelman, Z. (2003) The diverse spectrum of sliding clamp interacting proteins. FEBS Lett., 546, 167-172. (Pubitemid 36782405
2. Moldovan, G.L., Pfander, B. and Jentsch, S. (2007) PCNA, the maestro of the replication fork. Cell, 129, 665-679. (Pubitemid 46802385
3. Stoimenov, I. and Helleday, T. (2009) PCNA on the crossroad of cancer. Biochem. Soc. Trans., 37, 605-613.
4. Jeruzalmi, D., O'Donnell, M. and Kuriyan, J. (2002) Clamp loaders and sliding clamps. Curr. Opin. Struct. Biol., 12, 217-224.
5. Indiani, C. and O'Donnell, M. (2006) The replication clamp-loading machine at work in the three domains of life. Nat. Rev. Mol. Cell Biol., 7, 751-761.
6. Kelman, Z. and Hurwitz, J. (1998) Protein-PCNA interactions: A DNA-scanning mechanism? Trends Biochem. Sci., 23, 236-238.
7. Winter, J.A. and Bunting, K.A. (2012) Rings in the extreme: PCNA interactions and adaptations in the archaea. Archaea, 2012, 951010.
8. Yao, N.Y. and O'Donnell, M. (2012) The RFC clamp loader: Structure and function. Subcell Biochem., 62, 259-279.
9. Warbrick, E. (1998) PCNA binding through a conserved motif. Bioessays, 20, 195-199.
10. Warbrick, E., Heatherington, W., Lane, D.P. and Glover, D.M. (1998) PCNA binding proteins in Drosophila melanogaster: The analysis of a conserved PCNA binding domain. Nucleic Acids Res., 26, 3925-3932. (Pubitemid 28401341
11. Gulbis, J.M., Kelman, Z., Hurwitz, J., O'Donnell, M. and Kuriyan, J. (1996) Structure of the C-Terminal region of p21WAF1/CIP1 complexed with human PCNA. Cell, 87, 297-306. (Pubitemid 26359007
12. Xu, H., Zhang, P., Liu, L. and Lee, M.Y. (2001) A novel PCNA-binding motif identified by the panning of a random peptide display library. Biochemistry, 40, 4512-4520.
13. Haracska, L., Acharya, N., Unk, I., Johnson, R.E., Hurwitz, J., Prakash, L. and Prakash, S. (2005) A single domain in human DNA polymerase-mediates interaction with PCNA: Implications for translesion DNA synthesis. Mol. Cell. Biol., 25, 1183-1190.
14. Kelman, Z., Zuo, S., Arroyo, M.P., Wang, T.S. and Hurwitz, J. (1999) The C-Terminal region of Schizosaccaromyces pombe proliferating cell nuclear antigen is essential for DNA polymerase activity. Proc. Natl. Acad. Sci. U.S.A., 96, 9515-9520.
15. Gomes, X.V. and Burgers, P.M. (2000) Two modes of FEN1 binding to PCNA regulated by DNA. EMBO J., 19, 3811-3821. (Pubitemid 30462138
16. 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.
17. Kelman, Z. and O'Donnell, M. (1995) Structural and functional similarities of prokaryotic and eukaryotic DNA polymerase sliding clamps. Nucleic Acids Res., 23, 3613-3620.
18. Dalrymple, B.P., Kongsuwan, K., Wijffels, G., Dixon, N.E. and Jennings, P.A. (2001) A universal protein-protein interaction motif in the eubacterial DNA replication and repair systems. Proc. Natl. Acad. Sci. U.S.A., 98, 11627-11632.
19. Kurz, M., Dalrymple, B., Wijffels, G. and Kongsuwan, K. (2004) Interaction of the sliding clamp beta-subunit and Hda, a DnaA-related protein. J. Bacteriol., 186, 3508-3515. (Pubitemid 38661548
20. Ladner, J.E., Pan, M., Hurwitz, J. and Kelman, Z. (2011) Crystal structures of two active proliferating cell nuclear antigens (PCNAs) encoded by Thermococcus kodakaraensis. Proc. Natl. Acad. Sci. U.S.A., 108, 2711-2716.
21. Pan, M., Santangelo, T.J., Cübonövá, L., Li, Z., Metangmo, H., Ladner, J., Hurwitz, J., Reeve, J.N. and Kelman, Z. (2013) Thermococcus kodakarensis has two functional PCNA homologues but only one is required for viability. Extremophiles, 17, 453-461.
22. Kuba, Y., Ishino, S., Yamagami, T., Tokuhara, M., Kanai, T., Fujikane, R., Daiyasu, H., Atomi, H. and Ishino, Y. (2012) Comparative analyses of the two proliferating cell nuclear antigens from the hyperthermophilic archaeon, Thermococcus kodakarensis. Genes Cells, 17, 923-937.
23. Pan, M., Kelman, L.M. and Kelman, Z. (2011) The archaeal PCNA proteins. Biochem. Soc. Trans., 39, 20-24.
24. Li, Z., Santangelo, T.J., Cübonövá, L., Reeve, J.N. and Kelman, Z. (2010) Affinity purification of an archaeal DNA replication protein network. MBio, 1, e00221-00210.
25. Shen, Y., Musti, K., Hiramoto, M., Kikuchi, H., Kawarabayashi, Y. and Matsui, I. (2001) Invariant Asp-1122 and Asp-1124 are essential residues for polymerization catalysis of family D DNA polymerase from Pyrococcus horikoshii. J. Biol. Chem., 276, 27376-27383.
26. Chemnitz Galal, W., Pan, M., Kelman, Z. and Hurwitz, J. (2012) Characterization of the DNA primase complex isolated from the archaeon, Thermococcus kodakaraensis. J. Biol. Chem., 287, 16209-16219.
27. Kelman, Z. and Hurwitz, J. (2000) A unique organization of the protein subunits of the DNA polymerase clamp loader in the archaeon Methanobacterium thermoautotrophicum DH. J. Biol. Chem., 275, 7327-7336.
28. Shin, J.-H., Jiang, Y., Grabowski, B., Hurwitz, J. and Kelman, Z. (2003) Substrate requirements for duplex DNA translocation by the eukaryal and archaeal minichromosome maintenance helicases. J. Biol. Chem., 278, 49053-49062.
29. Hileman, T.H. and Santangelo, T.J. (2012) Genetics techniques for Thermococcus kodakarensis. Front. Microbiol., 3, 195.
30. Sato, T., Fukui, T., Atomi, H. and Imanaka, T. (2005) Improved and versatile transformation system allowing multiple genetic manipulations of the hyperthermophilic archaeon Thermococcus kodakaraensis. Appl. Environ. Microbiol., 71, 3889-3899.
31. Santangelo, T.J., Cubonova, L. and Reeve, J.N. (2010) Thermococcus kodakarensis genetics: TK1827-encoded beta-glycosidase, new positive-selection protocol, and targeted and repetitive deletion technology. Appl. Environ. Microbiol., 76, 1044-1152.
32. Cubonova, L., Katano, M., Kanai, T., Atomi, H., Reeve, J.N. and Santangelo, T.J. (2012) An archaeal histone is required for transformation of Thermococcus kodakarensis. J. Bacteriol., 194, 6864-6674.
33. Cübonövá, L., Richardson, T., Burkhart, B.W., Kelman, Z., Reeve, J.N., Connolly, B.A. and Santangelo, T.J. (2013) Archaeal DNA polymerase D but not DNA polymerase B is required for genome replication in Thermococcus kodakarensis. J. Bacteriol., 195, 2322-2328.
34. Pascal, B.D., Willis, S., Lauer, J.L., Landgraf, R.R., West, G.M., Marciano, D., Novick, S., Goswami, D., Chalmers, M.J. and Griffin, P.R. (2012) HDX workbench: Software for the analysis of H/D exchange MS data. J. Am. Soc. Mass Spectrom., 23, 1512-1521.
35. Press, W.H. (2007) Numerical Recipes : The Art of Scientific Computing. 3rd edn. Cambridge University Press, Cambridge, UK; New York.
36. Hubscher, U. and Seo, Y.S. (2001) Replication of the lagging strand: A concert of at least 23 polypeptides. Mol. Cells, 12, 149-157.
37. Balakrishnan, L. and Bambara, R.A. (2013) Okazaki fragment metabolism. Cold Spring Harb. Perspect. Biol., 5, a010173.
38. 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.
39. 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.
40. Rand, K.D., Zehl, M., Jensen, O.N. and Jorgensen, T.J. (2009) Protein hydrogen exchange measured at single-residue resolution by electron transfer dissociation mass spectrometry. Anal. Chem., 81, 5577-5584.
41. Fang, J., Engen, J.R. and Beuning, P.J. (2011) Escherichia coli processivity clamp beta from DNA polymerase III is dynamic in solution. Biochemistry, 50, 5958-5968.
42. Englander, S.W. (2006) Hydrogen exchange and mass spectrometry: A historical perspective. J. Am. Soc. Mass Spectrom., 17, 1481-1489.
43. Chalmers, M.J., Busby, S.A., Pascal, B.D., West, G.M. and Griffin, P.R. (2011) Differential hydrogen/deuterium exchange mass spectrometry analysis of protein-ligand interactions. Expert Rev. Proteomics, 8, 43-59.
44. Huang, R.Y., Garai, K., Frieden, C. and Gross, M.L. (2011) Hydrogen/deuterium exchange and electron-Transfer dissociation mass spectrometry determine the interface and dynamics of apolipoprotein E oligomerization. Biochemistry, 50, 9273-9282.
45. Huang, R.Y., Wen, J., Blankenship, R.E. and Gross, M.L. (2012) Hydrogen-deuterium exchange mass spectrometry reveals the interaction of Fenna-Matthews-Olson protein and chlorosome CsmA protein. Biochemistry, 51, 187-193.
46. Jackson, S.P. and Durocher, D. (2013) Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell, 49, 795-807.
47. Gibbs, E., Kelman, Z., Gulbis, J.M., O'Donnell, M., Kuriyan, J., Burgers, P.M.J. and Hurwitz, J. (1997) The influence of the proliferating cell nuclear antigen-interacting domain of p21CIP1 on DNA synthesis catalyzed by the human and Saccharomyces cerevisiae polymerase d holoenzymes. J. Biol. Chem., 272, 2373-2381.
48. Kennelly, P.J. (2003) Archaeal protein kinases and protein phosphatases: Insights from genomics and biochemistry. Biochem. J., 370, 373-389.
49. Maupin-Furlow, J.A. (2013) Ubiquitin-like proteins and their roles in archaea. Trends Microbiol., 21, 31-38.
50. Miyachi, K., Fritzler, M.J. and Tan, E.M. (1978) Autoantibody to a nuclear antigen in proliferating cells. J. Immun., 121, 2228-2234. (Pubitemid 9075187
51. Tan, Z., Wortman, M., Dillehay, K.L., Seibel, W.L., Evelyn, C.R., Smith, S.J., Malkas, L.H., Zheng, Y., Lu, S. and Dong, Z. (2012) Small-molecule targeting of proliferating cell nuclear antigen chromatin association inhibits tumor cell growth. Mol. Pharmacol., 81, 811-819.
52. Punchihewa, C., Inoue, A., Hishiki, A., Fujikawa, Y., Connelly, M., Evison, B., Shao, Y., Heath, R., Kuraoka, I., Rodrigues, P. et al. (2012) Identification of small molecule proliferating cell nuclear antigen (PCNA) inhibitor that disrupts interactions with PIP-box proteins and inhibits DNA replication. J. Biol. Chem., 287, 14289-14300.