A broad view of scaffolding suggests that scaffolding proteins can actively control regulation and signaling of multienzyme complexes through allostery

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1834, Issue 5, 2013, Pages 820-829

  Nussinov, Ruth ^a,b   Ma, Buyong ^a   Tsai, Chung Jung ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

Allosteric; Conformational selection; Multi enzyme complex; Multi protein; Multiprotein; Population shift

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MULTIENZYME COMPLEX; SCAFFOLD PROTEIN; UBIQUITIN PROTEIN LIGASE E3;

ALLOSTERISM; CATALYSIS; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ENZYME REGULATION; ENZYME SUBUNIT; FATTY ACID SYNTHESIS; LIPID RAFT; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; REVIEW; TOPOGRAPHY; UBIQUITINATION; YEAST;

ALLOSTERIC REGULATION; CATALYTIC DOMAIN; CELL COMPARTMENTATION; PROTEINS; SIGNAL TRANSDUCTION;

EID: 84876296757     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2012.12.014     Document Type: Review

References (90)

1. R. Caspi, T. Altman, K. Dreher, C.A. Fulcher, P. Subhraveti, I.M. Keseler, A. Kothari, M. Krummenacker, M. Latendresse, L.A. Mueller, Q. Ong, S. Paley, A. Pujar, A.G. Shearer, M. Travers, D. Weerasinghe, P. Zhang, and P.D. Karp The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases Nucleic Acids Res. 40 2012 D742 D753
2. P. Romero, J. Wagg, M.L. Green, D. Kaiser, M. Krummenacker, and P.D. Karp Computational prediction of human metabolic pathways from the complete human genome Genome Biol. 6 2005 R2
3. N.M. Goodey, and S.J. Benkovic Allosteric regulation and catalysis emerge via a common route Nat. Chem. Biol. 4 2008 474 482
4. Q. Cui, and M. Karplus Allostery and cooperativity revisited Protein Sci. 17 2008 1295 1307
5. D.M. Leitner Energy flow in proteins Annu. Rev. Phys. Chem. 59 2008 233 259
6. M. Fuxreiter, I. Simon, and S. Bondos Dynamic protein-DNA recognition: beyond what can be seen Trends Biochem. Sci. 36 2011 415 423
7. B. Ma, C.J. Tsai, T. Haliloglu, and R. Nussinov Dynamic allostery: linkers are not merely flexible Structure 19 2011 907 917
8. C.J. Tsai, and R. Nussinov Gene-specific transcription activation via long-range allosteric shape-shifting Biochem. J. 439 2011 15 25
9. B. Ma, and R. Nussinov Amplification of signaling via cellular allosteric relay and protein disorder Proc. Natl. Acad. Sci. U. S. A. 106 2009 6887 6888
10. K. Gunasekaran, B. Ma, and R. Nussinov Is allostery an intrinsic property of all dynamic proteins? Proteins 57 2004 433 443
11. C.J. Tsai, A. del Sol, and R. Nussinov Allostery: absence of a change in shape does not imply that allostery is not at play J. Mol. Biol. 378 2008 1 11
12. S.R. Tzeng, and C.G. Kalodimos Protein dynamics and allostery: an NMR view Curr. Opin. Struct. Biol. 21 2011 62 67
13. A. del Sol, C.J. Tsai, B. Ma, and R. Nussinov The origin of allosteric functional modulation: multiple pre-existing pathways Structure 17 2009 1042 1050
14. J. Liu, and R. Nussinov Molecular dynamics reveal the essential role of linker motions in the function of cullin-RING E3 ligases J. Mol. Biol. 396 2010 1508 1523
15. C.J. Tsai, A. Del Sol, and R. Nussinov Protein allostery, signal transmission and dynamics: a classification scheme of allosteric mechanisms Mol. Biosyst. 5 2009 207 216
16. J.N. Pruneda, P.J. Littlefield, S.E. Soss, K.A. Nordquist, W.J. Chazin, P.S. Brzovic, and R.E. Klevit Structure of an E3:E2 Ub complex reveals an allosteric mechanism shared among RING/U-box ligases Mol. Cell 47 2012 933 942
17. S.J. Mihalik, S.F. Michaliszyn, J. de las Heras, F. Bacha, S. Lee, D.H. Chace, V.R. DeJesus, J. Vockley, and S.A. Arslanian Metabolomic profiling of fatty acid and amino acid metabolism in youth with obesity and type 2 diabetes: evidence for enhanced mitochondrial oxidation Diabetes Care 35 2012 605 611
18. T. Izard, A. Aevarsson, M.D. Allen, A.H. Westphal, R.N. Perham, A. de Kok, and W.G. Hol Principles of quasi-equivalence and Euclidean geometry govern the assembly of cubic and dodecahedral cores of pyruvate dehydrogenase complexes Proc. Natl. Acad. Sci. U. S. A. 96 1999 1240 1245
19. J.C. Holthuis, C. Ungermann, Cellular microcompartments constitute general sub-organellar functional units in cells, Biol. Chem. (in press).
20. J. Liu, and R. Nussinov Flexible cullins in cullin-RING E3 ligases allosterically regulate ubiquitination J. Biol. Chem. 286 2011 40934 40942
21. M. Leibundgut, T. Maier, S. Jenni, and N. Ban The multienzyme architecture of eukaryotic fatty acid synthases Curr. Opin. Struct. Biol. 18 2008 714 725
22. M.W. Gorna, A.J. Carpousis, and B.F. Luisi From conformational chaos to robust regulation: the structure and function of the multi-enzyme RNA degradosome Q. Rev. Biophys. 45 2012 105 145
23. A.M. van Oijen, and J.J. Loparo Single-molecule studies of the replisome Annu. Rev. Biophys. 39 2010 429 448
24. M.F. Dunn, D. Niks, H. Ngo, T.R. Barends, and I. Schlichting Tryptophan synthase: the workings of a channeling nanomachine Trends Biochem. Sci. 33 2008 254 264
25. F. Verrier, S. An, A.M. Ferrie, H. Sun, M. Kyoung, H. Deng, Y. Fang, and S.J. Benkovic GPCRs regulate the assembly of a multienzyme complex for purine biosynthesis Nat. Chem. Biol. 7 2011 909 915
26. Y. Deng, J. Gam, J.B. French, H. Zhao, S. An, and S.J. Benkovic Mapping protein-protein proximity in the purinosome J. Biol. Chem. 19 2012 38442 38448
27. K. Van Bortle, and V.G. Corces Nuclear organization and genome function Annu. Rev. Cell Dev. Biol. 28 2012 163 187
28. C.M. Agapakis, P.M. Boyle, and P.A. Silver Natural strategies for the spatial optimization of metabolism in synthetic biology Nat. Chem. Biol. 8 2012 527 535
29. K. Mohr, and E. Kostenis Signaling pathways: purinosomes under GPCR control Nat. Chem. Biol. 7 2011 860 861
30. S. An, M. Kyoung, J.J. Allen, K.M. Shokat, and S.J. Benkovic Dynamic regulation of a metabolic multi-enzyme complex by protein kinase CK2 J. Biol. Chem. 285 2010 11093 11099
31. I. Sato, Y. Obata, K. Kasahara, Y. Nakayama, Y. Fukumoto, T. Yamasaki, K.K. Yokoyama, T. Saito, and N. Yamaguchi Differential trafficking of Src, Lyn, Yes and Fyn is specified by the state of palmitoylation in the SH4 domain J. Cell Sci. 122 2009 965 975
32. A.T. Place, Z. Chen, F.R. Bakhshi, G. Liu, J.P. O'Bryan, and R.D. Minshall Cooperative role of caveolin-1 and C-terminal Src kinase binding protein in C-terminal Src kinase-mediated negative regulation of c-Src Mol. Pharmacol. 80 2011 665 672
33. T. Kanou, C. Oneyama, K. Kawahara, A. Okimura, M. Ohta, N. Ikeda, Y. Shintani, M. Okumura, and M. Okada The transmembrane adaptor Cbp/PAG1 controls the malignant potential of human non-small cell lung cancers that have c-src upregulation Mol. Cancer Res. 9 2011 103 114
34. C.S. Osborne, L. Chakalova, K.E. Brown, D. Carter, A. Horton, E. Debrand, B. Goyenechea, J.A. Mitchell, S. Lopes, W. Reik, and P. Fraser Active genes dynamically colocalize to shared sites of ongoing transcription Nat. Genet. 36 2004 1065 1071
35. L.S. Shopland, C.V. Johnson, M. Byron, J. McNeil, and J.B. Lawrence Clustering of multiple specific genes and gene-rich R-bands around SC-35 domains: evidence for local euchromatic neighborhoods J. Cell Biol. 162 2003 981 990
36. H. Sutherland, and W.A. Bickmore Transcription factories: gene expression in unions? Nat. Rev. Genet. 10 2009 457 466
37. J.A. Mitchell, and P. Fraser Transcription factories are nuclear subcompartments that remain in the absence of transcription Genes Dev. 22 2008 20 25
38. C. Ferrai, S.Q. Xie, P. Luraghi, D. Munari, F. Ramirez, M.R. Branco, A. Pombo, and M.P. Crippa Poised transcription factories prime silent uPA gene prior to activation PLoS Biol. 8 2010 e1000270
39. Y. Zheng A membranous spindle matrix orchestrates cell division Nat. Rev. Mol. Cell Biol. 11 2010 529 535
40. D. St Johnston Moving messages: the intracellular localization of mRNAs Nat. Rev. Mol. Cell Biol. 6 2005 363 375
41. J. Chen, J. Lippincott-Schwartz, and J. Liu Intracellular spatial localization regulated by the microtubule network PLoS One 7 2012 e34919
42. J. Birkenfeld, P. Nalbant, S.H. Yoon, and G.M. Bokoch Cellular functions of GEF-H1, a microtubule-regulated Rho-GEF: is altered GEF-H1 activity a crucial determinant of disease pathogenesis? Trends Cell Biol. 18 2008 210 219
43. D. Boettiger Mechanical control of integrin-mediated adhesion and signaling Curr. Opin. Cell Biol. 24 2012 592 599
44. T.A. Springer, and M.L. Dustin Integrin inside-out signaling and the immunological synapse Curr. Opin. Cell Biol. 24 2012 107 115
45. R. Nussinov, C.J. Tsai, F. Xin, and P. Radivojac Allosteric post-translational modification codes Trends Biochem. Sci. 37 2012 447 455
46. J. Monod, J. Wyman, and J.P. Changeux On the nature of allosteric transitions: a plausible model J. Mol. Biol. 12 1965 88 118
47. H. Frauenfelder, S.G. Sligar, and P.G. Wolynes The energy landscapes and motions of proteins Science 254 1991 1598 1603
48. K.A. Dill, and H.S. Chan From Levinthal to pathways to funnels Nat. Struct. Biol. 4 1997 10 19
49. H.S. Chan, and K.A. Dill Protein folding in the landscape perspective: chevron plots and non-Arrhenius kinetics Proteins 30 1998 2 33
50. C.J. Tsai, S. Kumar, B. Ma, and R. Nussinov Folding funnels, binding funnels, and protein function Protein Sci. 8 1999 1181 1190
51. C.J. Tsai, B. Ma, and R. Nussinov Folding and binding cascades: shifts in energy landscapes Proc. Natl. Acad. Sci. U. S. A. 96 1999 9970 9972
52. S. Kumar, B. Ma, C.J. Tsai, N. Sinha, and R. Nussinov Folding and binding cascades: dynamic landscapes and population shifts Protein Sci. 9 2000 10 19
53. A.T. Vaidya, C.H. Chen, J.C. Dunlap, J.J. Loros, and B.R. Crane Structure of a light-activated LOV protein dimer that regulates transcription Sci. Signal. 4 2011 ra50
54. P.S. Brzovic, A. Lissounov, D.E. Christensen, D.W. Hoyt, and R.E. Klevit A UbcH5/ubiquitin noncovalent complex is required for processive BRCA1-directed ubiquitination Mol. Cell 21 2006 873 880
55. A.D. Capili, and C.D. Lima Taking it step by step: mechanistic insights from structural studies of ubiquitin/ubiquitin-like protein modification pathways Curr. Opin. Struct. Biol. 17 2007 726 735
56. V. Bernier-Villamor, D.A. Sampson, M.J. Matunis, and C.D. Lima Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1 Cell 108 2002 345 356
57. D.M. Duda, L.A. Borg, D.C. Scott, H.W. Hunt, M. Hammel, and B.A. Schulman Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation Cell 134 2008 995 1006
58. D.M. Duda, D.C. Scott, M.F. Calabrese, E.S. Zimmerman, N. Zheng, and B.A. Schulman Structural regulation of cullin-RING ubiquitin ligase complexes Curr. Opin. Struct. Biol. 21 2011 257 264
59. S. Jackson, and Y. Xiong CRL4s: the CUL4-RING E3 ubiquitin ligases Trends Biochem. Sci. 34 2009 562 570
60. A.A. Ogunjimi, D.J. Briant, N. Pece-Barbara, C. Le Roy, G.M. Di Guglielmo, P. Kavsak, R.K. Rasmussen, B.T. Seet, F. Sicheri, and J.L. Wrana Regulation of Smurf2 ubiquitin ligase activity by anchoring the E2 to the HECT domain Mol. Cell 19 2005 297 308
61. E. Ozkan, H. Yu, and J. Deisenhofer Mechanistic insight into the allosteric activation of a ubiquitin-conjugating enzyme by RING-type ubiquitin ligases Proc. Natl. Acad. Sci. U. S. A. 102 2005 18890 18895
62. B.A. Schulman, and J.W. Harper Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways Nat. Rev. Mol. Cell Biol. 10 2009 319 331
63. E. Papaleo, N. Casiraghi, A. Arrigoni, M. Vanoni, P. Coccetti, and L. De Gioia Loop 7 of E2 enzymes: an ancestral conserved functional motif involved in the E2-mediated steps of the ubiquitination cascade PLoS One 7 2012 e40786
64. E. Papaleo, V. Ranzani, F. Tripodi, A. Vitriolo, C. Cirulli, P. Fantucci, L. Alberghina, M. Vanoni, L. De Gioia, and P. Coccetti An acidic loop and cognate phosphorylation sites define a molecular switch that modulates ubiquitin charging activity in Cdc34-like enzymes PLoS Comput. Biol. 7 2011 e1002056
65. J. Liu, and R. Nussinov The mechanism of ubiquitination in the cullin-RING E3 ligase machinery: conformational control of substrate orientation PLoS Comput. Biol. 5 2009 e1000527
66. J. Liu, and R. Nussinov Rbx1 flexible linker facilitates cullin-RING ligase function before neddylation and after deneddylation Biophys. J. 99 2010 736 744
67. N. Zheng, B.A. Schulman, L. Song, J.J. Miller, P.D. Jeffrey, P. Wang, C. Chu, D.M. Koepp, S.J. Elledge, M. Pagano, R.C. Conaway, J.W. Conaway, J.W. Harper, and N.P. Pavletich Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex Nature 416 2002 703 709
68. B.A. Schulman, A.C. Carrano, P.D. Jeffrey, Z. Bowen, E.R. Kinnucan, M.S. Finnin, S.J. Elledge, J.W. Harper, M. Pagano, and N.P. Pavletich Insights into SCF ubiquitin ligases from the structure of the Skp1-Skp2 complex Nature 408 2000 381 386
69. N. Zheng, P. Wang, P.D. Jeffrey, and N.P. Pavletich Structure of a c-Cbl-UbcH7 complex: RING domain function in ubiquitin-protein ligases Cell 102 2000 533 539
70. T. Cardozo, and M. Pagano The SCF ubiquitin ligase: insights into a molecular machine Nat. Rev. Mol. Cell Biol. 5 2004 739 751
71. G. Wu, G. Xu, B.A. Schulman, P.D. Jeffrey, J.W. Harper, and N.P. Pavletich Structure of a beta-TrCP1-Skp1-beta-catenin complex: destruction motif binding and lysine specificity of the SCF(beta-TrCP1) ubiquitin ligase Mol. Cell 11 2003 1445 1456
72. H. Dou, L. Buetow, A. Hock, G.J. Sibbet, K.H. Vousden, and D.T. Huang Structural basis for autoinhibition and phosphorylation-dependent activation of c-Cbl Nat. Struct. Mol. Biol. 19 2012 184 192
73. J. Song, J. Wang, A.A. Jozwiak, W. Hu, P.M. Swiderski, and Y. Chen Stability of thioester intermediates in ubiquitin-like modifications Protein Sci. 18 2009 2492 2499
74. D.M. Wenzel, A. Lissounov, P.S. Brzovic, and R.E. Klevit UBCH7 reactivity profile reveals parkin and HHARI to be RING/HECT hybrids Nature 474 2011 105 108
75. J.N. Pruneda, P.J. Littlefield, S.E. Soss, K.A. Nordquist, W.J. Chazin, P.S. Brzovic, and R.E. Klevit Structure of an E3:E2 approximately Ub complex reveals an allosteric mechanism shared among RING/U-box ligases Mol. Cell 47 2012 933 942
76. A.A. Yunus, and C.D. Lima Lysine activation and functional analysis of E2-mediated conjugation in the SUMO pathway Nat. Struct. Mol. Biol. 13 2006 491 499
77. D. Reverter, and C.D. Lima Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex Nature 435 2005 687 692
78. M. Tozluoglu, E. Karaca, R. Nussinov, and T. Haliloglu A mechanistic view of the role of E3 in sumoylation PLoS Comput. Biol. 6 2010
79. E. Karaca, M. Tozluoglu, R. Nussinov, and T. Haliloglu Alternative allosteric mechanisms can regulate the substrate and E2 in SUMO conjugation J. Mol. Biol. 406 2011 620 630
80. S. Maleri, Q. Ge, E.A. Hackett, Y. Wang, H.G. Dohlman, and B. Errede Persistent activation by constitutive Ste7 promotes Kss1-mediated invasive growth but fails to support Fus3-dependent mating in yeast Mol. Cell. Biol. 24 2004 9221 9238
81. M. Good, G. Tang, J. Singleton, A. Remenyi, and W.A. Lim The Ste5 scaffold directs mating signaling by catalytically unlocking the Fus3 MAP kinase for activation Cell 136 2009 1085 1097
82. M.A. Seeliger, and J. Kuriyan A MAPK scaffold lends a helping hand Cell 136 2009 994 996
83. J.G. Zalatan, S.M. Coyle, S. Rajan, S.S. Sidhu, and W.A. Lim Conformational control of the Ste5 scaffold protein insulates against MAP kinase misactivation Science 337 2012 1218 1222
84. S.M. DeWire, S. Ahn, R.J. Lefkowitz, and S.K. Shenoy Beta-arrestins and cell signaling Annu. Rev. Physiol. 69 2007 483 510
85. K. Xiao, S.K. Shenoy, K. Nobles, and R.J. Lefkowitz Activation-dependent conformational changes in {beta}-arrestin 2 J. Biol. Chem. 279 2004 55744 55753
86. R. Nussinov How do dynamic cellular signals travel long distances? Mol. Biosyst. 8 2012 22 26
87. G. Kar, O. Keskin, A. Gursoy, and R. Nussinov Allostery and population shift in drug discovery Curr. Opin. Pharmacol. 10 2010 715 722
88. Y. Pan, C.J. Tsai, B. Ma, and R. Nussinov Mechanisms of transcription factor selectivity Trends Genet. 26 2010 75 83
89. W. Shao, and M. Brown Advances in estrogen receptor biology: prospects for improvements in targeted breast cancer therapy Breast Cancer Res. 6 2004 39 52
90. J.M. Hall, and D.P. McDonnell Coregulators in nuclear estrogen receptor action: from concept to therapeutic targeting Mol. Interv. 5 2005 343 357