p21 Exploits Residue Tyr151 as a Tether for High-Affinity PCNA Binding

Biochemistry

Volumn 54, Issue 22, 2015, Pages 3483-3493

  Kroker, Alice J ^a   Bruning, John B ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINDING ENERGY; CELL PROLIFERATION; CELLS; CYTOLOGY; DNA; HYDROGEN BONDS; HYDROPHOBICITY; MOBILE SECURITY; PEPTIDES; PROTEINS; TETHERLINES;

BINDING AFFINITIES; CELL CYCLE CONTROL; COCRYSTAL STRUCTURE; CONSENSUS SEQUENCE; ENTROPY AND ENTHALPIES; HYDROPHOBIC CAVITIES; ISOTHERMAL TITRATION CALORIMETRY; PROLIFERATING CELL NUCLEAR ANTIGENS;

BINS;

CYCLINE; HYDROXYL GROUP; PROTEIN P21; CDKN1A PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; PEPTIDE; PROTEIN BINDING; TYROSINE;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENTHALPY; ENTROPY; HYDROGEN BOND; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; PRIORITY JOURNAL; X RAY CRYSTALLOGRAPHY; AMINO ACID SUBSTITUTION; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MISSENSE MUTATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SUBSTITUTION; CRYSTALLOGRAPHY, X-RAY; CYCLIN-DEPENDENT KINASE INHIBITOR P21; HUMANS; MUTATION, MISSENSE; PEPTIDES; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; TYROSINE;

EID: 84935894063     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b00241     Document Type: Article

References (52)

1. Moldovan, G. L., Pfander, B., and Jentsch, S. (2007) PCNA, the maestro of the replication fork Cell 129 (4) 665 - 679
2. Mailand, N., Gibbs-Seymour, I., and Bekker-Jensen, S. (2013) Regulation of PCNA-protein interactions for genome stability Nat. Rev. Mol. Cell Biol. 14 (5) 269 - 282
3. Bruning, J. B. and Shamoo, Y. (2004) Structural and thermodynamic analysis of human PCNA with peptides derived from DNA polymerase-δ p66 subunit and flap endonuclease-1 Structure 12 (12) 2209 - 2219
4. De Biasio, A. and Blanco, F. J. (2013) Proliferating cell nuclear antigen structure and interactions: Too many partners for one dancer? Adv. Protein Chem. Struct. Biol. 91, 1 - 36
5. Krishna, T. S., Kong, X. P., Gary, S., Burgers, P. M., and Kuriyan, J. (1994) Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA Cell 79 (7) 1233 - 1243
6. 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 (2) 297 - 306
7. Maga, G. and Hubscher, U. (2003) Proliferating cell nuclear antigen (PCNA): A dancer with many partners J. Cell Sci. 116 (Part 15) 3051 - 3060
8. Dieckman, L. M., Freudenthal, B. D., and Washington, M. T. (2012) PCNA Structure and Function: Insights from Structures of PCNA Complexes and Post-translationally Modified PCNA Subcell. Biochem. 62, 281 - 299
9. Georgescu, R. E., Kim, S. S., Yurieva, O., Kuriyan, J., Kong, X. P., and O'Donnell, M. (2008) Structure of a sliding clamp on DNA Cell 132 (1) 43 - 54
10. Warbrick, E., Lane, D. P., Glover, D. M., and Cox, L. S. (1995) A small peptide inhibitor of DNA replication defines the site of interaction between the cyclin-dependent kinase inhibitor p21WAF1 and proliferating cell nuclear antigen Curr. Biol. 5 (3) 275 - 282
11. Warbrick, E. (1998) PCNA binding through a conserved motif BioEssays 20 (3) 195 - 199
12. 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., Krokan, H. E., and Otterlei, M. (2009) Identification of a novel, widespread, and functionally important PCNA-binding motif J. Cell Biol. 186 (5) 645 - 654
13. De Biasio, A., Campos-Olivas, R., Sanchez, R., Lopez-Alonso, J. P., Pantoja-Uceda, D., Merino, N., Villate, M., Martin-Garcia, J. M., Castillo, F., Luque, I., and Blanco, F. J. (2012) Proliferating cell nuclear antigen (PCNA) interactions in solution studied by NMR PLoS One 7 (11) e48390
14. Zheleva, D. I., Zhelev, N. Z., Fischer, P. M., Duff, S. V., Warbrick, E., Blake, D. G., and Lane, D. P. (2000) A quantitative study of the in vitro binding of the C-terminal domain of p21 to PCNA: Affinity, stoichiometry, and thermodynamics Biochemistry 39 (25) 7388 - 7397
15. Punchihewa, C., Inoue, A., Hishiki, A., Fujikawa, Y., Connelly, M., Evison, B., Shao, Y., Heath, R., Kuraoka, I., Rodrigues, P., Hashimoto, H., Kawanishi, M., Sato, M., Yagi, T., and Fujii, N. (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 (17) 14289 - 14300
16. Hishiki, A., Hashimoto, H., Hanafusa, T., Kamei, K., Ohashi, E., Shimizu, T., Ohmori, H., and Sato, M. (2009) Structural basis for novel interactions between human translesion synthesis polymerases and proliferating cell nuclear antigen J. Biol. Chem. 284 (16) 10552 - 10560
17. Bubeck, D., Reijns, M. A., Graham, S. C., Astell, K. R., Jones, E. Y., and Jackson, A. P. (2011) PCNA directs type 2 RNase H activity on DNA replication and repair substrates Nucleic Acids Res. 39 (9) 3652 - 3666
18. Miyachi, K., Fritzler, M. J., and Tan, E. M. (1978) Autoantibody to a nuclear antigen in proliferating cells J. Immunol. 121 (6) 2228 - 2234
19. Bravo, R., Fey, S. J., Bellatin, J., Larsen, P. M., Arevalo, J., and Celis, J. E. (1981) Identification of a nuclear and of a cytoplasmic polypeptide whose relative proportions are sensitive to changes in the rate of cell proliferation Exp. Cell Res. 136 (2) 311 - 319
20. Naryzhny, S. N. and Lee, H. (2007) Characterization of proliferating cell nuclear antigen (PCNA) isoforms in normal and cancer cells: There is no cancer-associated form of PCNA FEBS Lett. 581 (25) 4917 - 4920
21. Sakakura, C., Hagiwara, A., Tsujimoto, H., Ozaki, K., Sakakibara, T., Oyama, T., Ogaki, M., and Takahashi, T. (1994) Inhibition of gastric cancer cell proliferation by antisense oligonucleotides targeting the messenger RNA encoding proliferating cell nuclear antigen Br. J. Cancer 70 (6) 1060 - 1066
22. Actis, M., Inoue, A., Evison, B., Perry, S., Punchihewa, C., and Fujii, N. (2013) Small molecule inhibitors of PCNA/PIP-box interaction suppress translesion DNA synthesis Bioorg. Med. Chem. 21, 1972 - 1977
23. Cayrol, C., Knibiehler, M., and Ducommun, B. (1998) p21 binding to PCNA causes G1 and G2 cell cycle arrest in p53-deficient cells Oncogene 16 (3) 311 - 320
24. Dillehay, K. L., Lu, S., and Dong, Z. (2014) Anti-tumor effects of a novel small molecule targeting PCNA chromatin association in prostate cancer Mol. Cancer Ther. 2817 - 2826
25. Gu, L., Smith, S., Li, C., Hickey, R. J., Stark, J. M., Fields, G. B., Lang, W. H., Sandoval, J. A., and Malkas, L. H. (2014) A PCNA-Derived Cell Permeable Peptide Selectively Inhibits Neuroblastoma Cell Growth PLoS One 9 (4) e94773
26. Inoue, A., Kikuchi, S., Hishiki, A., Shao, Y., Heath, R., Evison, B. J., Actis, M., Canman, C. E., Hashimoto, H., and Fujii, N. (2014) A Small Molecule Inhibitor of Monoubiquitinated Proliferating Cell Nuclear Antigen (PCNA) Inhibits Repair of Interstrand DNA Cross-link, Enhances DNA Double Strand Break, and Sensitizes Cancer Cells to Cisplatin J. Biol. Chem. 289 (10) 7109 - 7120
27. Massodi, I., Bidwell, G. L., III, and Raucher, D. (2005) Evaluation of cell penetrating peptides fused to elastin-like polypeptide for drug delivery J. Controlled Release 108 (2-3) 396 - 408
28. 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 (6) 811 - 819
29. Kortemme, T. and Baker, D. (2002) A simple physical model for binding energy hot spots in protein-protein complexes Proc. Natl. Acad. Sci. U.S.A. 99 (22) 14116 - 14121
30. Kortemme, T., Kim, D. E., and Baker, D. (2004) Computational alanine scanning of protein-protein interfaces Sci. STKE 2004 (219) 1 - 8
31. Leslie, A. G. and Powell, H. R. (2007) Processing Diffraction Data with Mosflm. In Evolving Methods for Macromolecular Crystallography, Vol. 245, pp 41 - 51, Springer, Berlin.
32. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments Acta Crystallogr. D67 (Part 4) 235 - 242
33. Cowieson, N. P., Aragao, D., Clift, M., Ericsson, D. J., Gee, C., Harrop, S. J., Mudie, N., Panjikar, S., Price, J. R., Riboldi-Tunnicliffe, A., Williamson, R., and Caradoc-Davies, T. (2015) MX1: A bending-magnet crystallography beamline serving both chemical and macromolecular crystallography communities at the Australian Synchrotron J. Synchrotron Radiat. 22 (Part 1) 187 - 190
34. McPhillips, T. M., McPhillips, S. E., Chiu, H. J., Cohen, A. E., Deacon, A. M., Ellis, P. J., Garman, E., Gonzalez, A., Sauter, N. K., Phizackerley, R. P., Soltis, S. M., and Kuhn, P. (2002) Blu-Ice and the Distributed Control System: Software for data acquisition and instrument control at macromolecular crystallography beamlines J. Synchrotron Radiat. 9 (Part 6) 401 - 406
35. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40 (Part 4) 658 - 674
36. 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., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D66 (Part 2) 213 - 221
37. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot Acta Crystallogr. D66 (Part 4) 486 - 501
38. Chen, V. B., Arendall, W. B., III, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: All-atom structure validation for macromolecular crystallography Acta Crystallogr. D66 (Part 1) 12 - 21
39. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, W. B., Snoeyink, J., Richardson, J. S., and Richardson, D. C. (2007) MolProbity: All-atom contacts and structure validation for proteins and nucleic acids Nucleic Acids Res. 35 (Web Server Issue) W375 - W383
40. Kontopidis, G., Wu, S. Y., Zheleva, D. I., Taylor, P., McInnes, C., Lane, D. P., Fischer, P. M., and Walkinshaw, M. D. (2005) Structural and biochemical studies of human proliferating cell nuclear antigen complexes provide a rationale for cyclin association and inhibitor design Proc. Natl. Acad. Sci. U.S.A. 102 (6) 1871 - 1876
41. Dundas, J., Ouyang, Z., Tseng, J., Binkowski, A., Turpaz, Y., and Liang, J. (2006) CASTp: Computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues Nucleic Acids Res. 34 (Web Server Issue) W116 - W118
42. Fridman, Y., Gur, E., Fleishman, S. J., and Aharoni, A. (2013) Computational protein design suggests that human PCNA-partner interactions are not optimized for affinity Proteins 81 (2) 341 - 348
43. Kanagaraj, R., Saydam, N., Garcia, P. L., Zheng, L., and Janscak, P. (2006) Human RECQ5β helicase promotes strand exchange on synthetic DNA structures resembling a stalled replication fork Nucleic Acids Res. 34 (18) 5217 - 5231
44. Hamajima, N., Johmura, Y., Suzuki, S., Nakanishi, M., and Saitoh, S. (2013) Increased Protein Stability of CDKN1C Causes a Gain-of-Function Phenotype in Patients with IMAGe Syndrome PLoS One 8 (9) e75137
45. Cazzalini, O., Perucca, P., Mocchi, R., Sommatis, S., Prosperi, E., and Stivala, L. A. (2014) DDB2 association with PCNA is required for its degradation after UV-induced DNA damage Cell Cycle 13 (2) 240 - 248
46. Chen, X., Paudyal, S. C., Chin, R. I., and You, Z. (2013) PCNA promotes processive DNA end resection by Exo1 Nucleic Acids Res. 41, 9325 - 9338
47. Howlett, N. G., Harney, J. A., Rego, M. A., Kolling, F. W. t., and Glover, T. W. (2009) Functional interaction between the Fanconi Anemia D2 protein and proliferating cell nuclear antigen (PCNA) via a conserved putative PCNA interaction motif J. Biol. Chem. 284 (42) 28935 - 28942
48. Bacquin, A., Pouvelle, C., Siaud, N., Perderiset, M., Salome-Desnoulez, S., Tellier-Lebegue, C., Lopez, B., Charbonnier, J. B., and Kannouche, P. L. (2013) The helicase FBH1 is tightly regulated by PCNA via CRL4(Cdt2)-mediated proteolysis in human cells Nucleic Acids Res. 41 (13) 6501 - 6513
49. Parker, A., Gu, Y., Mahoney, W., Lee, S. H., Singh, K. K., and Lu, A. L. (2001) Human homolog of the MutY repair protein (hMYH) physically interacts with proteins involved in long patch DNA base excision repair J. Biol. Chem. 276 (8) 5547 - 5555
50. Banks, D., Wu, M., Higa, L. A., Gavrilova, N., Quan, J., Ye, T., Kobayashi, R., Sun, H., and Zhang, H. (2006) L2DTL/CDT2 and PCNA interact with p53 and regulate p53 polyubiquitination and protein stability through MDM2 and CUL4A/DDB1 complexes Cell Cycle 5 (15) 1719 - 1729
51. Shibata, E., Dar, A., and Dutta, A. (2014) CRL4Cdt2 E3 Ubiquitin Ligase and PCNA Cooperate to Degrade Thymine DNA Glycosylase in S-phase J. Biol. Chem. 289, 23056 - 23064
52. Park, J. M., Yang, S. W., Yu, K. R., Ka, S. H., Lee, S. W., Seol, J. H., Jeon, Y. J., and Chung, C. H. (2014) Modification of PCNA by ISG15 plays a crucial role in termination of error-prone translesion DNA synthesis Mol. Cell 54 (4) 626 - 638