Kinetic recognition of the retinoblastoma tumor suppressor by a specific protein target

Journal of Molecular Biology

Volumn 412, Issue 2, 2011, Pages 267-284

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

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

intrinsically disordered proteins; LxCxE motif; phosphorylation; retinoblastoma protein; viral oncoprotein

Indexed keywords

PROTEIN E7; RETINOBLASTOMA BINDING PROTEIN; VIRUS PROTEIN;

ARTICLE; CANCER INHIBITION; CELL CYCLE REGULATION; GENE EXPRESSION; HUMAN PAPILLOMAVIRUS TYPE 16; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIMIAN VIRUS 40; TUMOR SUPPRESSOR GENE;

HUMAN PAPILLOMAVIRUS;

EID: 80052021703     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.07.015     Document Type: Article

References (84)

1. Chinnam M., and Goodrich D.W. RB1, development, and cancer Curr. Top. Dev. Biol. 94 2011 129 169
2. Longworth M.S., and Dyson N.J. pRb, a local chromatin organizer with global possibilities Chromosoma 119 2010 1 11
3. van den Heuvel S., and Dyson N.J. Conserved functions of the pRB and E2F families Nat. Rev., Mol. Cell Biol. 9 2008 713 724
4. Burkhart D.L., and Sage J. Cellular mechanisms of tumour suppression by the retinoblastoma gene Nat. Rev., Cancer 8 2008 671 682
5. Howley P.M., and Livingston D.M. Small DNA tumor viruses: large contributors to biomedical sciences Virology 384 2009 256 259
6. Morris E.J., and Dyson N.J. Retinoblastoma protein partners Adv. Cancer Res. 82 2001 1 54 (Pubitemid 32613381)
7. DeGregori J. The Rb network J. Cell Sci. 117 2004 3411 3413
8. Isaac C.E., Francis S.M., Martens A.L., Julian L.M., Seifried L.A., and Erdmann N. The retinoblastoma protein regulates pericentric heterochromatin Mol. Cell. Biol. 26 2006 3659 3671
9. Xiao B., Spencer J., Clements A., Ali-Khan N., Mittnacht S., and Broceno C. Crystal structure of the retinoblastoma tumor suppressor protein bound to E2F and the molecular basis of its regulation Proc. Natl Acad. Sci. USA 100 2003 2363 2368 (Pubitemid 36297504)
10. Lee C., Chang J.H., Lee H.S., and Cho Y. Structural basis for the recognition of the E2F transactivation domain by the retinoblastoma tumor suppressor Genes Dev. 16 2002 3199 3212 (Pubitemid 36025973)
11. Singh M., Krajewski M., Mikolajka A., and Holak T.A. Molecular determinants for the complex formation between the retinoblastoma protein and LXCXE sequences J. Biol. Chem. 280 2005 37868 37876 (Pubitemid 41642398)
12. Dick F.A. Structure-function analysis of the retinoblastoma tumor suppressor protein-is the whole a sum of its parts? Cell Div. 2 2007 26
13. Burke J.R., Deshong A.J., Pelton J.G., and Rubin S.M. Phosphorylation-induced conformational changes in the retinoblastoma protein inhibit E2F transactivation domain binding J. Biol. Chem. 285 2010 16286 16293
14. Rubin S.M., Gall A.L., Zheng N., and Pavletich N.P. Structure of the Rb C-terminal domain bound to E2F1-DP1: a mechanism for phosphorylation-induced E2F release Cell 123 2005 1093 1106 (Pubitemid 41785423)
15. de Souza R.F., Iyer L.M., and Aravind L. Diversity and evolution of chromatin proteins encoded by DNA viruses Biochim. Biophys. Acta 1799 2009 302 318
16. Kehn K., Fuente Cde L., Strouss K., Berro R., Jiang H., and Brady J. The HTLV-I Tax oncoprotein targets the retinoblastoma protein for proteasomal degradation Oncogene 24 2005 525 540 (Pubitemid 40188558)
17. Munakata T., Nakamura M., Liang Y., Li K., and Lemon S.M. Down-regulation of the retinoblastoma tumor suppressor by the hepatitis C virus NS5B RNA-dependent RNA polymerase Proc. Natl Acad. Sci. USA 102 2005 18159 18164 (Pubitemid 41798518)
18. Forng R.Y., and Atreya C.D. Mutations in the retinoblastoma protein-binding LXCXE motif of rubella virus putative replicase affect virus replication J. Gen. Virol. 80 1999 327 332 (Pubitemid 29095191)
19. Davey N.E., Trave G., and Gibson T.J. How viruses hijack cell regulation Trends Biochem. Sci. 36 2011 159 169
20. Lee J.O., Russo A.A., and Pavletich N.P. Structure of the retinoblastoma tumour-suppressor pocket domain bound to a peptide from HPV E7 Nature 391 1998 859 865 (Pubitemid 28157656)
21. Kim H.Y., Ahn B.Y., and Cho Y. Structural basis for the inactivation of retinoblastoma tumor suppressor by SV40 large T antigen EMBO J. 20 2001 295 304 (Pubitemid 32099125)
22. Ferreon J.C., Martinez-Yamout M.A., Dyson H.J., and Wright P.E. Structural basis for subversion of cellular control mechanisms by the adenoviral E1A oncoprotein Proc. Natl Acad. Sci. USA 106 2009 13260 13265
23. Liu X., and Marmorstein R. Structure of the retinoblastoma protein bound to adenovirus E1A reveals the molecular basis for viral oncoprotein inactivation of a tumor suppressor Genes Dev. 21 2007 2711 2716 (Pubitemid 350070718)
24. Dyson N., Guida P., McCall C., and Harlow E. Adenovirus E1A makes two distinct contacts with the retinoblastoma protein J. Virol. 66 1992 4606 4611
25. Patrick D.R., Oliff A., and Heimbrook D.C. Identification of a novel retinoblastoma gene product binding site on human papillomavirus type 16 E7 protein J. Biol. Chem. 269 1994 6842 6850 (Pubitemid 24191078)
26. Block C., Janknecht R., Herrmann C., Nassar N., and Wittinghofer A. Quantitative structure-activity analysis correlating Ras/Raf interaction in vitro to Raf activation in vivo Nat. Struct. Biol. 3 1996 244 251 (Pubitemid 26081707)
27. Kiel C., and Serrano L. Cell type-specific importance of ras-c-raf complex association rate constants for MAPK signaling Sci. Signal. 2 2009 ra38
28. Schreiber G. Kinetic studies of protein-protein interactions Curr. Opin. Struct. Biol. 12 2002 41 47 (Pubitemid 34142719)
29. Phelps W.C., Yee C.L., Munger K., and Howley P.M. The human papillomavirus type 16 E7 gene encodes transactivation and transformation functions similar to those of adenovirus E1A Cell 53 1988 539 547
30. Banerjee N.S., Genovese N.J., Noya F., Chien W.M., Broker T.R., and Chow L.T. Conditionally activated E7 proteins of high-risk and low-risk human papillomaviruses induce S phase in postmitotic, differentiated human keratinocytes J. Virol. 80 2006 6517 6524 (Pubitemid 43927453)
31. Garcia-Alai M.M., Alonso L.G., and de Prat-Gay G. The N-terminal module of HPV16 E7 is an intrinsically disordered domain that confers conformational and recognition plasticity to the oncoprotein Biochemistry 46 2007 10405 10412 (Pubitemid 47417236)
32. Uversky V.N., Roman A., Oldfield C.J., and Dunker A.K. Protein intrinsic disorder and human papillomaviruses: increased amount of disorder in E6 and E7 oncoproteins from high risk HPVs J. Proteome Res. 5 2006 1829 1842 (Pubitemid 44232696)
33. Alonso L.G., Garcia-Alai M.M., Nadra A.D., Lapena A.N., Almeida F.L., Gualfetti P., and Prat-Gay G.D. High-risk (HPV16) human papillomavirus E7 oncoprotein is highly stable and extended, with conformational transitions that could explain its multiple cellular binding partners Biochemistry 41 2002 10510 10518
34. Liu X., Clements A., Zhao K., and Marmorstein R. Structure of the human papillomavirus E7 oncoprotein and its mechanism for inactivation of the retinoblastoma tumor suppressor J. Biol. Chem. 281 2006 578 586 (Pubitemid 43671221)
35. Ohlenschlager O., Seiboth T., Zengerling H., Briese L., Marchanka A., and Ramachandran R. Solution structure of the partially folded high-risk human papilloma virus 45 oncoprotein E7 Oncogene 25 2006 5953 5959 (Pubitemid 44477289)
36. Chemes L.B., Sanchez I.E., Smal C., and de Prat-Gay G. 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 2010 973 988
37. Rechsteiner M., and Rogers S.W. PEST sequences and regulation by proteolysis Trends Biochem. Sci. 21 1996 267 271 (Pubitemid 26228278)
38. Dick F.A., and Dyson N.J. Three regions of the pRB pocket domain affect its inactivation by human papillomavirus E7 proteins J. Virol. 76 2002 6224 6234 (Pubitemid 34556318)
39. Chan H.M., Smith L., and La Thangue N.B. Role of LXCXE motif-dependent interactions in the activity of the retinoblastoma protein Oncogene 20 2001 6152 6163 (Pubitemid 32964427)
40. Munger K., Yee C.L., Phelps W.C., Pietenpol J.A., Moses H.L., and Howley P.M. Biochemical and biological differences between E7 oncoproteins of the high- and low-risk human papillomavirus types are determined by amino-terminal sequences J. Virol. 65 1991 3943 3948
41. Huang P.S., Patrick D.R., Edwards G., Goodhart P.J., Huber H.E., and Miles L. Protein domains governing interactions between E2F, the retinoblastoma gene product, and human papillomavirus type 16 E7 protein Mol. Cell. Biol. 13 1993 953 960 (Pubitemid 23040261)
42. Heck D.V., Yee C.L., Howley P.M., and Munger K. Efficiency of binding the retinoblastoma protein correlates with the transforming capacity of the E7 oncoproteins of the human papillomaviruses Proc. Natl Acad. Sci. USA 89 1992 4442 4446
43. Xue B., Williams R.W., Oldfield C.J., Goh G.K., Dunker A.K., and Uversky V.N. Viral disorder or disordered viruses: do viral proteins possess unique features? Protein Pept. Lett. 17 2010 932 951
44. Chemes, L. B., Sánchez, I.E., Alonso, L.G. & de Prat-Gay, G. (2011). Intrinsic Disorder in the human papillomavirus E7 protein. In Flexible Viruses: Structural Disorder within Viral Proteins (Longhi, S., Uversky, V.N., ed.), pp. in press. John Wiley and Sons.
45. Shoemaker B.A., Portman J.J., and Wolynes P.G. Speeding molecular recognition by using the folding funnel: the fly-casting mechanism Proc. Natl Acad. Sci. USA 97 2000 8868 8873 (Pubitemid 30626639)
46. Helt A.M., and Galloway D.A. Mechanisms by which DNA tumor virus oncoproteins target the Rb family of pocket proteins Carcinogenesis 24 2003 159 169 (Pubitemid 36277627)
47. Magnaghi-Jaulin L., Groisman R., Naguibneva I., Robin P., Lorain S., and Le Villain J.P. Retinoblastoma protein represses transcription by recruiting a histone deacetylase Nature 391 1998 601 605 (Pubitemid 28157604)
48. Stokes P.H., Thompson L.S., Marianayagam N.J., and Matthews J.M. Dimerization of CtIP may stabilize in vivo interactions with the Retinoblastoma-pocket domain Biochem. Biophys. Res. Commun. 354 2007 197 202 (Pubitemid 46123219)
49. Dick F.A., Sailhamer E., and Dyson N.J. Mutagenesis of the pRB pocket reveals that cell cycle arrest functions are separable from binding to viral oncoproteins Mol. Cell. Biol. 20 2000 3715 3727 (Pubitemid 30243917)
50. MacLellan W.R., Xiao G., Abdellatif M., and Schneider M.D. A novel Rb- and p300-binding protein inhibits transactivation by MyoD Mol. Cell. Biol. 20 2000 8903 8915 (Pubitemid 32245921)
51. Miyake S., Sellers W.R., Safran M., Li X., Zhao W., and Grossman S.R. Cells degrade a novel inhibitor of differentiation with E1A-like properties upon exiting the cell cycle Mol. Cell. Biol. 20 2000 8889 8902 (Pubitemid 32245920)
52. Joerger A.C., and Fersht A.R. Structural biology of the tumor suppressor p53 Annu. Rev. Biochem. 77 2008 557 582
53. Clements A., Johnston K., Mazzarelli J.M., Ricciardi R.P., and Marmorstein R. Oligomerization properties of the viral oncoproteins adenovirus E1A and human papillomavirus E7 and their complexes with the retinoblastoma protein Biochemistry 39 2000 16033 16045 (Pubitemid 32038266)
54. Sheinerman F.B., Norel R., and Honig B. Electrostatic aspects of protein-protein interactions Curr. Opin. Struct. Biol. 10 2000 153 159 (Pubitemid 30198940)
55. Vindigni A., White C.E., Komives E.A., and Di Cera E. Energetics of thrombin-thrombomodulin interaction Biochemistry 36 1997 6674 6681 (Pubitemid 27242325)
56. Grucza R.A., Bradshaw J.M., Mitaxov V., and Waksman G. Role of electrostatic interactions in SH2 domain recognition: salt-dependence of tyrosyl-phosphorylated peptide binding to the tandem SH2 domain of the Syk kinase and the single SH2 domain of the Src kinase Biochemistry 39 2000 10072 10081 (Pubitemid 30663028)
57. Fersht A.R., Matouschek A., and Serrano L. The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding J. Mol. Biol. 224 1992 771 782
58. Chien W.M., Parker J.N., Schmidt-Grimminger D.C., Broker T.R., and Chow L.T. Casein kinase II phosphorylation of the human papillomavirus-18 E7 protein is critical for promoting S-phase entry Cell Growth Differ. 11 2000 425 435 (Pubitemid 30644366)
59. Phelps W.C., Munger K., Yee C.L., Barnes J.A., and Howley P.M. Structure-function analysis of the human papillomavirus type 16 E7 oncoprotein J. Virol. 66 1992 2418 2427
60. Genovese N.J., Banerjee N.S., Broker T.R., and Chow L.T. Casein kinase II motif-dependent phosphorylation of human papillomavirus E7 protein promotes p130 degradation and S-phase induction in differentiated human keratinocytes J. Virol. 82 2008 4862 4873 (Pubitemid 351657048)
61. Munger K., Werness B.A., Dyson N., Phelps W.C., Harlow E., and Howley P.M. Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product EMBO J. 8 1989 4099 4105 (Pubitemid 20066852)
62. Hassler M., Singh S., Yue W.W., Luczynski M., Lakbir R., and Sanchez-Sanchez F. Crystal structure of the retinoblastoma protein N domain provides insight into tumor suppression, ligand interaction, and holoprotein architecture Mol. Cell 28 2007 371 385 (Pubitemid 350030561)
63. Schreiber G., and Fersht A.R. Interaction of barnase with its polypeptide inhibitor barstar studied by protein engineering Biochemistry 32 1993 5145 5150 (Pubitemid 23162083)
64. Myles T., Le Bonniec B.F., Betz A., and Stone S.R. Electrostatic steering and ionic tethering in the formation of thrombin-hirudin complexes: the role of the thrombin anion-binding exosite-I Biochemistry 40 2001 4972 4979 (Pubitemid 32332543)
65. Kiel C., Selzer T., Shaul Y., Schreiber G., and Herrmann C. Electrostatically optimized Ras-binding Ral guanine dissociation stimulator mutants increase the rate of association by stabilizing the encounter complex Proc. Natl Acad. Sci. USA 101 2004 9223 9228 (Pubitemid 38812856)
66. Gianni S., Engstrom A., Larsson M., Calosci N., Malatesta F., and Eklund L. The kinetics of PDZ domain-ligand interactions and implications for the binding mechanism J. Biol. Chem. 280 2005 34805 34812 (Pubitemid 41504614)
67. Stewart R.C., and Van Bruggen R. Association and dissociation kinetics for CheY interacting with the P2 domain of CheA J. Mol. Biol. 336 2004 287 301 (Pubitemid 38111177)
68. Zhang Y., Wavreille A.S., Kunys A.R., and Pei D. The SH2 domains of inositol polyphosphate 5-phosphatases SHIP1 and SHIP2 have similar ligand specificity but different binding kinetics Biochemistry 48 2009 11075 11083
69. Radic Z., Kirchhoff P.D., Quinn D.M., McCammon J.A., and Taylor P. Electrostatic influence on the kinetics of ligand binding to acetylcholinesterase. Distinctions between active center ligands and fasciculin J. Biol. Chem. 272 1997 23265 23277 (Pubitemid 27392463)
70. Rihs H.P., Jans D.A., Fan H., and Peters R. The rate of nuclear cytoplasmic protein transport is determined by the casein kinase II site flanking the nuclear localization sequence of the SV40 T-antigen EMBO J. 10 1991 633 639 (Pubitemid 21905517)
71. Whalen S.G., Marcellus R.C., Barbeau D., and Branton P.E. Importance of the Ser-132 phosphorylation site in cell transformation and apoptosis induced by the adenovirus type 5 E1A protein J. Virol. 70 1996 5373 5383 (Pubitemid 26240711)
72. Grove T.Z., Cortajarena A.L., and Regan L. Ligand binding by repeat proteins: natural and designed Curr. Opin. Struct. Biol. 18 2008 507 515
73. Remenyi A., Good M.C., and Lim W.A. Docking interactions in protein kinase and phosphatase networks Curr. Opin. Struct. Biol. 16 2006 676 685 (Pubitemid 44827730)
74. Mittag T., Kay L.E., and Forman-Kay J.D. Protein dynamics and conformational disorder in molecular recognition J. Mol. Recognit. 23 2009 105 116
75. Uversky V.N. Multitude of binding modes attainable by intrinsically disordered proteins: a portrait gallery of disorder-based complexes Chem. Soc. Rev. 40 2010 1623 1634
76. Ferreiro D.U., Hegler J.A., Komives E.A., and Wolynes P.G. On the role of frustration in the energy landscapes of allosteric proteins Proc. Natl Acad. Sci. USA 108 2011 3499 3503
77. Balog E.R.M., Burke J.R., Hura G.L., and Rubin S.M. Crystal structure of the unliganded retinoblastoma protein pocket domain Proteins: Struct., Funct., Bioinf. 79 2011 2010 2014
78. Sugase K., Dyson H.J., and Wright P.E. Mechanism of coupled folding and binding of an intrinsically disordered protein Nature 447 2007 1021 1025 (Pubitemid 46975749)
79. Turjanski A.G., Gutkind J.S., Best R.B., and Hummer G. Binding-induced folding of a natively unstructured transcription factor PLoS Comput. Biol. 4 2008 e1000060
80. Whitford P.C., Onuchic J.N., and Wolynes P.G. Energy landscape along an enzymatic reaction trajectory: hinges or cracks? HFSP J. 2 2008 61 64
81. Pace C.N., Vajdos F., Fee L., Grimsley G., and Gray T. How to measure and predict the molar absorption coefficient of a protein Protein Sci. 4 1995 2411 2423
82. Hermanson G.T. Bioconjugate Techniques 1996 Academic Press San Diego, CA
83. Malatesta F. The study of bimolecular reactions under non-pseudo-first order conditions Biophys. Chem. 116 2005 251 256 (Pubitemid 40962453)
84. Chi C.N., Bach A., Engstrom A., Wang H., Stromgaard K., Gianni S., and Jemth P. A sequential binding mechanism in a PDZ domain Biochemistry 48 2009 7089 7097