Folding of a cyclin box: Linking multitarget binding to marginal stability, oligomerization, and aggregation of the retinoblastoma tumor suppressor ab pocket domain

Journal of Biological Chemistry

Volumn 288, Issue 26, 2013, Pages 18923-18938

  Chemes, Lucía B ^a,b   Noval, María G ^a   Sánchez, Ignacio E ^b   De Prat Gay, Gonzalo ^a  

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR TRANSFORMATION; CONFORMATIONAL STABILITIES; HUMAN PAPILLOMAVIRUS; LIGAND BINDING PROPERTIES; MULTI-PROTEIN COMPLEX; RETINOBLASTOMA TUMORS; SECONDARY AND TERTIARY STRUCTURES; SIGNALING PATHWAYS;

BINDING ENERGY; LIGANDS; OLIGOMERIZATION; ONCOGENIC VIRUSES; PROTEINS; RUBIDIUM; STABILITY; STEM CELLS; TUMORS;

OLIGOMERS;

CYCLINE; PROTEIN E7; PROTEIN P53; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F;

ARTICLE; BINDING SITE; CARCINOGENESIS; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL FATE; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION; CIRCULAR DICHROISM; EUKARYOTE; FLUORESCENCE SPECTROSCOPY; GENE MUTATION; HUMAN; IN VIVO STUDY; LIGAND BINDING; MATHEMATICAL ANALYSIS; OLIGOMERIZATION; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN TARGETING; PROTEIN UNFOLDING; SIGNAL TRANSDUCTION; STEM CELL; TEMPERATURE; THERMODYNAMICS; TUMOR VIRUS; WART VIRUS;

CYCLIN FOLD; MARGINAL STABILITY; OLIGOMERIZATION; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN MISFOLDING; PROTEIN STABILITY; RETINOBLASTOMA (RB); SCAFFOLD PROTEINS; TUMOR SUPPRESSOR;

BINDING SITES; CELL DIFFERENTIATION; CIRCULAR DICHROISM; CYCLINS; DNA-BINDING PROTEINS; E2F TRANSCRIPTION FACTORS; HUMANS; LIGANDS; MODELS, MOLECULAR; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS E7 PROTEINS; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RETINOBLASTOMA PROTEIN; SIGNAL TRANSDUCTION; TEMPERATURE; TUMOR SUPPRESSOR PROTEIN P53;

EUKARYOTA; HUMAN PAPILLOMAVIRUS;

EID: 84879582466     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.467316     Document Type: Article

References (78)

1. van den Heuvel, S., and Dyson, N. J. (2008) Conserved functions of the pRB and E2F families. Nat. Rev. Mol. Cell Biol. 9, 713-724
2. Khidr, L., and Chen, P. L. (2006) RB, the conductor that orchestrates life, death and differentiation. Oncogene 25, 5210-5219 (Pubitemid 44299079)
3. Macaluso, M., Montanari, M., and Giordano, A. (2006) Rb family proteins as modulators of gene expression and new aspects regarding the interaction with chromatin remodeling enzymes. Oncogene 25, 5263-5267 (Pubitemid 44299086)
4. Sage, J. (2012) The retinoblastoma tumor suppressor and stem cell biology. Genes Dev. 26, 1409-1420
5. Cross, F. R., Buchler, N. E., and Skotheim, J. M. (2011) Evolution of networks and sequences in eukaryotic cell cycle control. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366, 3532-3544
6. Gutzat, R., Borghi, L., and Gruissem, W. (2012) Emerging roles of RETI-NOBLASTOMA-RELATED proteins in evolution and plant development. Trends Plant Sci. 17, 139-148
7. Cao, L., Peng, B., Yao, L., Zhang, X., Sun, K., Yang, X., and Yu, L. (2010) The ancient function of RB-E2F pathway: insights from its evolutionary history. Biol. Direct 5, 55
8. DeGregori, J. (2004) The Rb network. J. Cell Sci. 117, 3411-3413
9. Burkhart, D. L., and Sage, J. (2008) Cellular mechanisms of tumour suppression by the retinoblastoma gene. Nat. Rev. Cancer 8, 671-682
10. zur Hausen, H. (2009) Papillomaviruses in the causation of human cancers - a brief historical account. Virology 384, 260-265
11. McGivern, D. R., and Lemon, S. M. (2011) Virus-specific mechanisms of carcinogenesis in hepatitis C virus associated liver cancer. Oncogene 30, 1969-1983
12. Sastre-Garau, X. (2011) Merkel cell carcinoma revisited: a new example of viro-induced human tumour. Pathol. Biol. 59, 127-130
13. Lohmann, D. R. (1999) RB1 gene mutations in retinoblastoma. Hum. Mutat. 14, 283-288
14. Valverde, J. R., Alonso, J., Palacios, I., and Pestaña, A. (2005) RB1 gene mutation up-date, a meta-analysis based on 932 reported mutations available in a searchable database. BMC Genet. 6, 53
15. Sherr, C. J., and McCormick, F. (2002) The RB and p53 pathways in cancer. Cancer Cell 2, 103-112 (Pubitemid 41039110)
16. Knudsen, E. S., and Knudsen, K. E. (2008) Tailoring to RB: tumour suppressor status and therapeutic response. Nat. Rev. Cancer 8, 714-724
17. Hassler, M., Singh, S., Yue, W. W., Luczynski, M., Lakbir, R., Sanchez-Sanchez, F., Bader, T., Pearl, L. H., and Mittnacht, S. (2007) Crystal structure of the retinoblastoma protein N domain provides insight into tumor suppression, ligand interaction, and holoprotein architecture. Mol. Cell 28, 371-385 (Pubitemid 350030561)
18. Lee, J. O., Russo, A. A., and Pavletich, N. P. (1998) Structure of the retinoblastoma tumour-suppressor pocket domain bound to a peptide from HPV E7. Nature 391, 859-865 (Pubitemid 28157656)
19. Rubin, S. M., Gall, A. L., Zheng, N., and Pavletich, N. P. (2005) Structure of the Rb C-terminal domain bound to E2F1-DP1: a mechanism for phosphorylation-induced E2F release. Cell 123, 1351-1363
20. Burke, J. R., Hura, G. L., and Rubin, S. M. (2012) Structures of inactive retinoblastoma protein reveal multiple mechanisms for cell cycle control. Genes Dev. 26, 1156-1166
21. Dick, F. A. (2007) Structure-function analysis of the retinoblastoma tumor suppressor protein-is the whole a sum of its parts? Cell Div. 2, 26
22. Noble, M. E., Endicott, J. A., Brown, N. R., and Johnson, L. N. (1997) The cyclin box fold: protein recognition in cell-cycle and transcription control. Trends Biochem. Sci. 22, 482-487 (Pubitemid 27515915)
23. Gibson, T. J., Thompson, J. D., Blocker, A., and Kouzarides, T. (1994) Evidence for a protein domain superfamily shared by the cyclins, TFIIB and RB/p107. Nucleic Acids Res. 22, 946-952 (Pubitemid 24162153)
24. Isaac, C. E., Francis, S. M., Martens, A. L., Julian, L. M., Seifried, L. A., Erdmann, N., Binné, U. K., Harrington, L., Sicinski, P., Bérubé, N. G., Dyson, N. J., and Dick, F. A. (2006) The retinoblastoma protein regulates pericentric heterochromatin. Mol. Cell. Biol. 26, 3659-3671
25. Coschi, C. H., Martens, A. L., Ritchie, K., Francis, S. M., Chakrabarti, S., Berube, N. G., and Dick, F. A. (2010) Mitotic chromosome condensation mediated by the retinoblastoma protein is tumor-suppressive. Genes Dev. 24, 1351-1363
26. Lee, C., Chang, J. H., Lee, H. S., and Cho, Y. (2002) Structural basis for the recognition of the E2F transactivation domain by the retinoblastoma tumor suppressor. Genes Dev. 16, 3199-3212 (Pubitemid 36025973)
27. de Souza, R. F., Iyer, L. M., and Aravind, L. (2010) Diversity and evolution of chromatin proteins encoded by DNA viruses. Biochim. Biophys. Acta 1799, 302-318
28. Cremades, N., Sancho, J., and Freire, E. (2006) The native-state ensemble of proteins provides clues for folding, misfolding and function. Trends Biochem. Sci. 31, 494-496 (Pubitemid 44279979)
29. Gidalevitz, T., Kikis, E. A., and Morimoto, R. I. (2010) A cellular perspective on conformational disease: the role of genetic background and proteostasis networks. Curr. Opin. Struct. Biol. 20, 23-32
30. Dobson, C. M. (2003) Protein folding and misfolding. Nature 426, 884-890
31. Khoo, K. H., Mayer, S., and Fersht, A. R. (2009) Effects of stability on the biological function of p53. J. Biol. Chem. 284, 30974-30980
32. Tang, K. S., Guralnick, B. J., Wang, W. K., Fersht, A. R., and Itzhaki, L. S. (1999) Stability and folding of the tumour suppressor protein p16. J. Mol. Biol. 285, 1869-1886 (Pubitemid 29060477)
33. Joerger, A. C., and Fersht, A. R. (2008) Structural biology of the tumor suppressor p53. Annu. Rev. Biochem. 77, 557-582
34. Freed-Pastor, W. A., and Prives, C. (2012) Mutant p53: one name, many proteins. Genes Dev. 26, 1268-1286
35. Witkiewicz, A. K., Knudsen, K. E., Dicker, A. P., and Knudsen, E. S. (2011) The meaning of p16(ink4a) expression in tumors: functional significance, clinical associations and future developments. Cell Cycle 10, 2497-2503
36. Friedler, A., Veprintsev, D. B., Hansson, L. O., and Fersht, A. R. (2003) Kinetic instability of p53 core domain mutants: implications for rescue by small molecules. J. Biol. Chem. 278, 24108-24112 (Pubitemid 36830245)
37. Bullock, A. N., Henckel, J., and Fersht, A. R. (2000) Quantitative analysis of residual folding and DNA binding in mutant p53 core domain: definition of mutant states for rescue in cancer therapy. Oncogene 19, 1245-1256 (Pubitemid 30160617)
38. Wang, X., Ren, J., and Qu, X. (2008) Biophysical studies on the full-length human cyclin A2: protein stability and folding/unfolding thermodynamics. J. Phys. Chem. B 112, 8346-8353
39. Grossmann, J. G., Sharff, A. J., O'Hare, P., and Luisi, B. (2001) Molecular shapes of transcription factors TFIIB and VP16 in solution: implications for recognition. Biochemistry 40, 6267-6274 (Pubitemid 32472715)
40. Hayashi, F., Ishima, R., Liu, D., Tong, K. I., Kim, S., Reinberg, D., Bagby, S., and Ikura, M. (1998) Human general transcription factor TFIIB: conformational variability and interaction with VP16 activation domain. Biochemistry 37, 7941-7951 (Pubitemid 28307054)
41. Harbour, J. W., Luo, R. X., Dei Santi, A., Postigo, A. A., and Dean, D. C. (1999) Cdk phosphorylation triggers sequential intramolecular interactions that progressively block Rb functions as cells move through G1. Cell 98, 859-869 (Pubitemid 29446902)
42. Lamber, E. P., Beuron, F., Morris, E. P., Svergun, D. I., and Mittnacht, S. (2013) Structural insights into the mechanism of phosphoregulation of the retinoblastoma protein. PLoS One 8, e58463
43. Ang, H. C., Joerger, A. C., Mayer, S., and Fersht, A. R. (2006) Effects of common cancer mutations on stability and DNA binding of full-length p53 compared with isolated core domains. J. Biol. Chem. 281, 21934-21941 (Pubitemid 44181897)
44. Mayer, S., Rüdiger, S., Ang, H. C., Joerger, A. C., and Fersht, A. R. (2007) Correlation of levels of folded recombinant p53 in Escherichia coli with thermodynamic stability in vitro. J. Mol. Biol. 372, 268-276
45. Nichols, N. M., and Matthews, K. S. (2002) Human p53 phosphorylation mimic, S392E, increases nonspecific DNA affinity and thermal stability. Biochemistry 41, 170-178 (Pubitemid 34049392)
46. Natan, E., Baloglu, C., Pagel, K., Freund, S. M., Morgner, N., Robinson, C. V., Fersht, A. R., and Joerger, A. C. (2011) Interaction of the p53 DNA-binding domain with its N-terminal extension modulates the stability of the p53 tetramer. J. Mol. Biol. 409, 358-368
47. Chemes, L. B., Sánchez, I. E., Smal, C., and de Prat-Gay, G. (2010) Targeting mechanism of the retinoblastoma tumor suppressor by a prototypical viral oncoprotein. Structural modularity, intrinsic disorder and phosphorylation of human papillomavirus E7. FEBS J. 277, 973-988
48. Pace, C. N., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4, 2411-2423
49. Uversky, V. N. (1993) Use of fast protein size-exclusion liquid chromatography to study the unfolding of proteins which denature through the molten globule. Biochemistry 32, 13288-13298
50. Baker, B. M., and Murphy, K. P. (1996) Evaluation of linked protonation effects in protein binding reactions using isothermal titration calorimetry. Biophys. J. 71, 2049-2055 (Pubitemid 26325983)
51. Rodriguez-Larrea, D., Minning, S., Borchert, T. V., and Sanchez-Ruiz, J. M. (2006) Role of solvation barriers in protein kinetic stability. J. Mol. Biol. 360, 715-724 (Pubitemid 43975108)
52. Sanchez-Ruiz, J. M. (1992) Theoretical analysis of Lumry-Eyring models in differential scanning calorimetry. Biophys. J. 61, 921-935
53. Zlotnick, A., Johnson, J. M., Wingfield, P. W., Stahl, S. J., and Endres, D. (1999) A theoretical model successfully identifies features of hepatitis B virus capsid assembly. Biochemistry 38, 14644-14652
54. Gast, K., and Modler, A. J. (2005) in Protein Folding Handbook (Buchner, J., and Kiefhaber, T., eds) pp. 673-704, Wiley-VCH, Weinheim, Germany
55. Myers, J. K., Pace, C. N., and Scholtz, J. M. (1995) Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci. 4, 2138-2148
56. Chemes, L. B., Sánchez, I. E., and de Prat-Gay, G. (2011) Kinetic recognition of the retinoblastoma tumor suppressor by a specific protein target. J. Mol. Biol. 412, 267-284
57. Lepock, J. R., Ritchie, K. P., Kolios, M. C., Rodahl, A. M., Heinz, K. A., and Kruuv, J. (1992) Influence of transition rates and scan rate on kinetic simulations of differential scanning calorimetry profiles of reversible and irreversible protein denaturation. Biochemistry 31, 12706-12712 (Pubitemid 23016540)
58. Smal, C., Alonso, L. G., Wetzler, D. E., Heer, A., and de Prat Gay, G. (2012) Ordered self-assembly mechanism of a spherical oncoprotein oligomer triggered by zinc removal and stabilized by an intrinsically disordered domain. PLoS One 7, e36457
59. Ishimaru, D., Maia, L. F., Maiolino, L. M., Quesado, P. A., Lopez, P. C., Almeida, F. C., Valente, A. P., and Silva, J. L. (2003) Conversion of wild-type p53 core domain into a conformation that mimics a hot-spot mutant. J. Mol. Biol. 333, 443-451 (Pubitemid 37188583)
60. Bom, A. P., Freitas, M. S., Moreira, F. S., Ferraz, D., Sanches, D., Gomes, A. M., Valente, A. P., Cordeiro, Y., and Silva, J. L. (2010) The p53 core domain is a molten globule at low pH: functional implications of a partially unfolded structure. J. Biol. Chem. 285, 2857-2866
61. Gunbin, K. V., Suslov, V. V., Turnaev, I. I., Afonnikov, D. A., and Kolchanov, N. A. (2011) Molecular evolution of cyclin proteins in animals and fungi. BMC Evol. Biol. 11, 224
62. Kim, H. Y., and Cho, Y. (1997) Structural similarity between the pocket region of retinoblastoma tumour suppressor and the cyclin-box. Nat. Struct. Biol. 4, 390-395
63. Han, J. H., Batey, S., Nickson, A. A., Teichmann, S. A., and Clarke, J. (2007) The folding and evolution of multidomain proteins. Nat. Rev. Mol. Cell Biol. 8, 319-330 (Pubitemid 46474660)
64. Brockwell, D. J., and Radford, S. E. (2007) Intermediates: ubiquitous species on folding energy landscapes? Curr. Opin. Struct. Biol. 17, 30-37 (Pubitemid 46240814)
65. Silva, J. L., Cordeiro, Y., and Foguel, D. (2006) Protein folding and aggregation: two sides of the same coin in the condensation of proteins revealed by pressure studies. Biochim. Biophys. Acta 1764, 443-451
66. Xiao, S., and Raleigh, D. P. (2010) A critical assessment of putative gate-keeper interactions in the villin headpiece helical subdomain. J. Mol. Biol. 401, 274-285
67. Robertson, A. D., and Murphy, K. P. (1997) Protein structure and the energetics of protein stability. Chem. Rev. 97, 1251-1268
68. Bullock, A. N., Henckel, J., DeDecker, B. S., Johnson, C. M., Nikolova, P. V., Proctor, M. R., Lane, D. P., and Fersht, A. R. (1997) Thermodynamic stability of wild-type and mutant p53 core domain. Proc. Natl. Acad. Sci. U.S.A. 94, 14338-14342 (Pubitemid 28041374)
69. Butler, J. S., and Loh, S. N. (2006) Folding and misfolding mechanisms of the p53 DNA binding domain at physiological temperature. Protein Sci. 15, 2457-2465 (Pubitemid 44771683)
70. Butler, J. S., and Loh, S. N. (2005) Kinetic partitioning during folding of the p53 DNA binding domain. J. Mol. Biol. 350, 906-918 (Pubitemid 40943450)
71. Ano Bom, A. P., Rangel, L. P., Costa, D. C., de Oliveira, G. A., Sanches, D., Braga, C. A., Gava, L. M., Ramos, C. H., Cepeda, A. O., Stumbo, A. C., De Moura Gallo, C. V., Cordeiro, Y., and Silva, J. L. (2012) Mutant p53 aggregates into prion-like amyloid oligomers and fibrils: implications for cancer. J. Biol. Chem. 287, 28152-28162
72. Xu, J., Reumers, J., Couceiro, J. R., De Smet, F., Gallardo, R., Rudyak, S., Cornelis, A., Rozenski, J., Zwolinska, A., Marine, J. C., Lambrechts, D., Suh, Y. A., Rousseau, F., and Schymkowitz, J. (2011) Gain of function of mutant p53 by coaggregation with multiple tumor suppressors. Nat. Chem. Biol. 7, 285-295
73. Kratzke, R. A., Otterson, G. A., Hogg, A., Coxon, A. B., Geradts, J., Cowell, J. K., and Kaye, F. J. (1994) Partial inactivation of the RB product in a family with incomplete penetrance of familial retinoblastoma and benign retinal tumors. Oncogene 9, 1321-1326 (Pubitemid 24123648)
74. Park, Y., Kubo, A., Komiya, T., Coxon, A., Beebe, K., Neckers, L., Meltzer, P. S., and Kaye, F. J. (2008) Low-penetrant RB allele in small-cell cancer shows geldanamycin instability and discordant expression with mutant ras. Cell Cycle 7, 2384-2391
75. Otterson, G. A., Modi, S., Nguyen, K., Coxon, A. B., and Kaye, F. J. (1999) Temperature-sensitive RB mutations linked to incomplete penetrance of familial retinoblastoma in 12 families. Am. J. Hum. Genet. 65, 1040-1046 (Pubitemid 30462960)
76. Huh, K., Zhou, X., Hayakawa, H., Cho, J. Y., Libermann, T. A., Jin, J., Harper, J. W., and Munger, K. (2007) Human papillomavirus type 16 E7 oncoprotein associates with the cullin 2 ubiquitin ligase complex, which contributes to degradation of the retinoblastoma tumor suppressor. J. Virol. 81, 9737-9747 (Pubitemid 350067678)
77. Singh, M., Krajewski, M., Mikolajka, A., and Holak, T. A. (2005) Molecular determinants for the complex formation between the retinoblastoma protein and LXCXE sequences. J. Biol. Chem. 280, 37868-37876 (Pubitemid 41642398)
78. Tokuriki, N., and Tawfik, D. S. (2009) Protein dynamism and evolvability. Science 324, 203-207