Conformational plasticity of an enzyme during catalysis: Intricate coupling between cyclophilin a dynamics and substrate turnover

Biophysical Journal

Volumn 104, Issue 1, 2013, Pages 216-226

  McGowan, Lauren C ^a   Hamelberg, Donald ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHILIN A; TRYPTOPHAN;

ARTICLE; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; HUMAN; HYDROGEN BOND; METABOLISM; PRINCIPAL COMPONENT ANALYSIS; PROBABILITY; PROTEIN CONFORMATION;

BIOCATALYSIS; CATALYTIC DOMAIN; CYCLOPHILIN A; HUMANS; HYDROGEN BONDING; MODELS, MOLECULAR; PRINCIPAL COMPONENT ANALYSIS; PROBABILITY; PROTEIN CONFORMATION; SUBSTRATE SPECIFICITY; TRYPTOPHAN;

EID: 84872151410     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.11.3815     Document Type: Article

References (75)

1. D.K. Srivastava, and S.A. Bernhard Metabolite transfer via enzyme-enzyme complexes Science 234 1986 1081 1086 (Pubitemid 17206186)
2. S.P. Jackson, and J. Bartek The DNA-damage response in human biology and disease Nature 461 2009 1071 1078
3. S. Nagata Apoptosis by death factor Cell 88 1997 355 365 (Pubitemid 27131377)
4. R.J. Davis Signal transduction by the JNK group of MAP kinases Cell 103 2000 239 252
5. W.L. Miller Early steps in androgen biosynthesis: from cholesterol to DHEA Baillieres Clin. Endocrinol. Metab. 12 1998 67 81 (Pubitemid 28495390)
6. P.C. Babbitt, and J.A. Gerlt Understanding enzyme superfamilies. Chemistry as the fundamental determinant in the evolution of new catalytic activities J. Biol. Chem. 272 1997 30591 30594 (Pubitemid 27527485)
7. S.W. May Applications of oxidoreductases Curr. Opin. Biotechnol. 10 1999 370 375 (Pubitemid 29373952)
8. R. Wolfenden, and M.J. Snider The depth of chemical time and the power of enzymes as catalysts Acc. Chem. Res. 34 2001 938 945
9. D.A. Kraut, K.S. Carroll, and D. Herschlag Challenges in enzyme mechanism and energetics Annu. Rev. Biochem. 72 2003 517 571 (Pubitemid 36934521)
10. A. Warshel Computer simulations of enzyme catalysis: methods, progress, and insights Annu. Rev. Biophys. Biomol. Struct. 32 2003 425 443 (Pubitemid 37056236)
11. D. Hamelberg, and J.A. McCammon Mechanistic insight into the role of transition-state stabilization in cyclophilin A J. Am. Chem. Soc. 131 2009 147 152
12. D. Hamelberg, T. Shen, and J.A. McCammon Phosphorylation effects on cis/trans isomerization and the backbone conformation of serine-proline motifs: accelerated molecular dynamics analysis J. Am. Chem. Soc. 127 2005 1969 1974 (Pubitemid 40229179)
13. P. Wang, and J. Heitman The cyclophilins Genome Biol. 6 2005 226
14. J. Dornan, P. Taylor, and M.D. Walkinshaw Structures of immunophilins and their ligand complexes Curr. Top. Med. Chem. 3 2003 1392 1409
15. T.L. Davis, and J.R. Walker S. Dhe-Paganon Structural and biochemical characterization of the human cyclophilin family of peptidyl-prolyl isomerases PLoS Biol. 8 2010 e1000439
16. G. Fischer Chemical aspects of peptide bond isomerization Chem. Soc. Rev. 29 2000 119 127
17. C. Dugave, and L. Demange Cis-trans isomerization of organic molecules and biomolecules: implications and applications Chem. Rev. 103 2003 2475 2532
18. C. Grathwohl, and K. Wüthrich NMR studies of the rates of proline cis-trans isomerization in oligopeptides Biopolymers 20 1981 2623 2633
19. R.K. Harrison, and R.L. Stein Substrate specificities of the peptidyl prolyl cis-trans isomerase activities of cyclophilin and FK-506 binding protein: evidence for the existence of a family of distinct enzymes Biochemistry 29 1990 3813 3816 (Pubitemid 20151288)
20. P.A.M. Schmidpeter, and G. Jahreis F.X. Schmid Prolyl isomerases show low sequence specificity toward the residue following the proline Biochemistry 50 2011 4796 4803
21. B. Sherry, and G. Zybarth M. Bukrinsky Role of cyclophilin A in the uptake of HIV-1 by macrophages and T lymphocytes Proc. Natl. Acad. Sci. USA 95 1998 1758 1763 (Pubitemid 28103467)
22. D. Braaten, and J. Luban Cyclophilin A regulates HIV-1 infectivity, as demonstrated by gene targeting in human T cells EMBO J. 20 2001 1300 1309 (Pubitemid 32233970)
23. F.F. Vajdos, and S. Yoo C.P. Hill Crystal structure of cyclophilin A complexed with a binding site peptide from the HIV-1 capsid protein Protein Sci. 6 1997 2297 2307 (Pubitemid 27490740)
24. U. Chatterji, and M. Bobardt P. Gallay The isomerase active site of cyclophilin A is critical for hepatitis C virus replication J. Biol. Chem. 284 2009 16998 17005
25. J. Zheng, and J.E. Koblinski C.V. Clevenger Prolyl isomerase cyclophilin A regulation of Janus-activated kinase 2 and the progression of human breast cancer Cancer Res. 68 2008 7769 7778
26. K.N. Brazin, and R.J. Mallis A.H. Andreotti Regulation of the tyrosine kinase Itk by the peptidyl-prolyl isomerase cyclophilin A Proc. Natl. Acad. Sci. USA 99 2002 1899 1904 (Pubitemid 34168986)
27. J. Lee, and S.S. Kim An overview of cyclophilins in human cancers J. Int. Med. Res. 38 2010 1561 1574
28. D.A. Bosco, and E.Z. Eisenmesser D. Kern Catalysis of cis/trans isomerization in native HIV-1 capsid by human cyclophilin A Proc. Natl. Acad. Sci. USA 99 2002 5247 5252 (Pubitemid 34411534)
29. E.Z. Eisenmesser, and O. Millet D. Kern Intrinsic dynamics of an enzyme underlies catalysis Nature 438 2005 117 121 (Pubitemid 41599831)
30. S.C.L. Kamerlin, and A. Warshel At the dawn of the 21st century: is dynamics the missing link for understanding enzyme catalysis? Proteins 78 2010 1339 1375
31. J. Fanghänel, and G. Fischer Insights into the catalytic mechanism of peptidyl prolyl cis/trans isomerases Front. Biosci. 9 2004 3453 3478
32. R.K. Harrison, and R.L. Stein Mechanistic studies of peptidyl prolyl cis-trans isomerase: evidence for catalysis by distortion Biochemistry 29 1990 1684 1689 (Pubitemid 20074707)
33. G. Li, and Q. Cui What is so special about Arg 55 in the catalysis of cyclophilin A? Insights from hybrid QM/MM simulations J. Am. Chem. Soc. 125 2003 15028 15038 (Pubitemid 37509666)
34. R. Wolfenden Enzyme catalysis: conflicting requirements of substrate access and transition state affinity Mol. Cell. Biochem. 3 1974 207 211
35. D.A. Case, and T.A. Darden P.A. Kollman AMBER 10 2008 University of California San Francisco, CA
36. W. Jorgensen, and J. Chandrasekhar M. Klein Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79 1983 926 935
37. V. Hornak, and R. Abel C. Simmerling Comparison of multiple AMBER force fields and development of improved protein backbone parameters Proteins 65 2006 712 725 (Pubitemid 44583220)
38. W.D. Cornell, and P. Cieplak P.A. Kollman A second generation force field for the simulation of proteins, nucleic acids, and organic molecules J. Am. Chem. Soc. 117 1995 5179 5197
39. U. Doshi, and D. Hamelberg Reoptimization of the AMBER force field parameters for peptide bond (ω) torsions using accelerated molecular dynamics J. Phys. Chem. B 113 2009 16590 16595
40. J.S. Fraser, and M.W. Clarkson T. Alber Hidden alternative structures of proline isomerase essential for catalysis Nature 462 2009 669 673
41. D. Trzesniak, and W.F. van Gunsteren Catalytic mechanism of cyclophilin as observed in molecular dynamics simulations: pathway prediction and reconciliation of x-ray crystallographic and NMR solution data Protein Sci. 15 2006 2544 2551 (Pubitemid 44771691)
42. L.D. Zydowsky, and F.A. Etzkorn C.T. Walsh Active site mutants of human cyclophilin A separate peptidyl-prolyl isomerase activity from cyclosporin A binding and calcineurin inhibition Protein Sci. 1 1992 1092 1099 (Pubitemid 23016423)
43. J.L. Kofron, and P. Kuzmic D.H. Rich Determination of kinetic constants for peptidyl prolyl cis-trans isomerases by an improved spectrophotometric assay Biochemistry 30 1991 6127 6134
44. J.-P. Ryckaert, G. Ciccotti, and H.J.C. Berendsen Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes J. Comput. Phys. 23 1977 327 341
45. A. Toukmaji, and C. Sagui T. Darden Efficient particle-mesh Ewald based approach to fixed and induced dipolar interactions J. Chem. Phys. 113 2000 10913 10927 (Pubitemid 32087579)
46. C. Sagui, L.G. Pedersen, and T.A. Darden Towards an accurate representation of electrostatics in classical force fields: efficient implementation of multipolar interactions in biomolecular simulations J. Chem. Phys. 120 2004 73 87
47. T. Darden, D. York, and L. Pedersen Particle mesh Ewald: an Nṡlog(N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
48. D. Hamelberg, J. Mongan, and J.A. McCammon Accelerated molecular dynamics: a promising and efficient simulation method for biomolecules J. Chem. Phys. 120 2004 11919 11929
49. T. Shen, and D. Hamelberg A statistical analysis of the precision of reweighting-based simulations J. Chem. Phys. 129 2008 034103 034109
50. M.A. Balsera, and W. Wriggers K. Schulten Principal component analysis and long time protein dynamics J. Phys. Chem. 100 1996 2567 2572 (Pubitemid 126793208)
51. G.G. Maisuradze, A. Liwo, and H.A. Scheraga Principal component analysis for protein folding dynamics J. Mol. Biol. 385 2009 312 329
52. J. Numata, M. Wan, and E.W. Knapp Conformational entropy of biomolecules: beyond the quasi-harmonic approximation Genome Informatics 18 2007 192 205
53. S. Hayward, A. Kitao, and N. Gō Harmonic and anharmonic aspects in the dynamics of BPTI: a normal mode analysis and principal component analysis Protein Sci. 3 1994 936 943 (Pubitemid 24170073)
54. L. Skjaerven, A. Martinez, and N. Reuter Principal component and normal mode analysis of proteins; a quantitative comparison using the GroEL subunit Proteins 79 2011 232 243
55. P.A. Kollman, and I. Massova T.E. Cheatham 3rd Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models Acc. Chem. Res. 33 2000 889 897 (Pubitemid 32056774)
56. T. Hou, and J. Wang W. Wang Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations J. Chem. Inf. Model. 51 2011 69 82
57. C.-J. Tsai, B. Ma, and R. Nussinov Folding and binding cascades: shifts in energy landscapes Proc. Natl. Acad. Sci. USA 96 1999 9970 9972 (Pubitemid 29422488)
58. D.D. Boehr, R. Nussinov, and P.E. Wright The role of dynamic conformational ensembles in biomolecular recognition Nat. Chem. Biol. 5 2009 789 796
59. P. Csermely, R. Palotai, and R. Nussinov Induced fit, conformational selection and independent dynamic segments: an extended view of binding events Trends Biochem. Sci. 35 2010 539 546
60. B. Ma, and R. Nussinov Enzyme dynamics point to stepwise conformational selection in catalysis Curr. Opin. Chem. Biol. 14 2010 652 659
61. D.E. Koshland Application of a theory of enzyme specificity to protein synthesis Proc. Natl. Acad. Sci. USA 44 1958 98 104
62. G.G. Hammes, Y.-C. Chang, and T.G. Oas Conformational selection or induced fit: a flux description of reaction mechanism Proc. Natl. Acad. Sci. USA 106 2009 13737 13741
63. H.-X. Zhou From induced fit to conformational selection: a continuum of binding mechanism controlled by the timescale of conformational transitions Biophys. J. 98 2010 L15 L17
64. P.K. Agarwal Enzymes: an integrated view of structure, dynamics and function Microb. Cell Fact. 5 2006 2
65. D. Kern, and G. Kern T. Drakenberg Kinetic analysis of cyclophilin-catalyzed prolyl cis/trans isomerization by dynamic NMR spectroscopy Biochemistry 34 1995 13594 13602
66. P.K. Agarwal Role of protein dynamics in reaction rate enhancement by enzymes J. Am. Chem. Soc. 127 2005 15248 15256 (Pubitemid 41547393)
67. A. Ramanathan, and P.K. Agarwal Evolutionarily conserved linkage between enzyme fold, flexibility, and catalysis PLoS Biol. 9 2011 e1001193
68. P.K. Agarwal, A. Geist, and A. Gorin Protein dynamics and enzymatic catalysis: investigating the peptidyl-prolyl cis-trans isomerization activity of cyclophilin A Biochemistry 43 2004 10605 10618 (Pubitemid 39096703)
69. H.-Y. Yeh, and P.H. Klesius Channel catfish, Ictalurus punctatus, cyclophilin A and B cDNA characterization and expression analysis Vet. Immunol. Immunopathol. 121 2008 370 377 (Pubitemid 351163402)
70. D.J. Bergsma, and C. Eder M.A. Levy The cyclophilin multigene family of peptidyl-prolyl isomerases. Characterization of three separate human isoforms J. Biol. Chem. 266 1991 23204 23214 (Pubitemid 21908781)
71. U. Doshi, and L.C. McGowan D. Hamelberg Resolving the complex role of enzyme conformational dynamics in catalytic function Proc. Natl. Acad. Sci. USA 109 2012 5699 5704
72. A. Warshel, and P.K. Sharma M.H. Olsson Electrostatic basis for enzyme catalysis Chem. Rev. 106 2006 3210 3235 (Pubitemid 44376933)
73. M.E. Cardenas, E. Lim, and J. Heitman Mutations that perturb cyclophilin A ligand binding pocket confer cyclosporin A resistance in Saccharomyces cerevisiae J. Biol. Chem. 270 1995 20997 21002
74. D.A. Bosco, and E.Z. Eisenmesser D. Kern Dissecting the microscopic steps of the cyclophilin A enzymatic cycle on the biological HIV-1 capsid substrate by NMR J. Mol. Biol. 403 2010 723 738
75. M. Gastmans, G. Volckaert, and Y. Engelborghs Tryptophan microstate reshuffling upon the binding of cyclosporin A to human cyclophilin A Proteins 35 1999 464 474 (Pubitemid 29264843)