Mechanism of action of cyclophilin a explored by metadynamics simulations

PLoS Computational Biology

Volumn 5, Issue 3, 2009, Pages

  Leone, Vanessa ^a,b   Lattanzi, Gianluca ^c,d   Molteni, Carla ^e   Carloni, Paolo ^a,b  

^a SISSA   (Italy)

^b ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^c UNIVERSITY OF BARI   (Italy)

^d INFN SEZIONE DI BARI   (Italy)

^e KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MOLECULAR BIOLOGY; PROTEINS;

BIOLOGICAL PROCESS; CA MODEL; CAPSID PROTEINS; CYCLOPHILIN A; ISOMERISATION; MECHANISM OF ACTION; MECHANISTICS; METADYNAMICS SIMULATIONS; MODEL SUBSTRATES; TARGET PROTEINS;

ISOMERIZATION;

CAPSID PROTEIN; CYCLOPHILIN A; WATER;

ARTICLE; HUMAN IMMUNODEFICIENCY VIRUS 1; ISOMERIZATION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN STRUCTURE; SIMULATION; BINDING SITE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; ENZYME ACTIVATION; ISOMERISM; PROTEIN BINDING; ULTRASTRUCTURE;

HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE;

BINDING SITES; CAPSID PROTEINS; COMPUTER SIMULATION; CYCLOPHILIN A; ENZYME ACTIVATION; HIV-1; ISOMERISM; MODELS, CHEMICAL; MODELS, MOLECULAR; PROTEIN BINDING; WATER;

EID: 63549093762     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000309     Document Type: Article

References (60)

1. Fischer S, Dunbrack RL, Karplus M Jr (1994) Cis-trans imide isomerization of the proline dipeptide. J Am Chem Soc 116: 11931-11937.
2. Hodel A, Rice LM, Simonson T, Fox RO, Brunger AT (1995) Proline cis-trans isomerization in Staphylococcal nuclease: multi-substrate free energy perturbation calculations. Protein Sci 4: 636-654.
3. Harrar Y, Bellini C, Faure JD (2001) FKBPs: at the crossroads of folding and transduction. Trends Plant Sci 6: 426-431.
4. Wang P, Heitman J (2005) The cyclophilins. Genome Biol 6: 226.
5. Lummis SCR, Beene DL, Lee LW, Lester HA, Broadhurst RW, et al. (2005) Cis-trans isomerization at a proline opens the pore of a neurotransmitter-gated ion channel. Nature 438: 243-252.
6. Wulf G, Finn G, Suizu F, Lu KP (2005) Phosphorylation-specific prolyl isomerization: is there an underlying theme? Nat Cell Biol 7: 435-441.
7. Scarlata S, Carter C (2003) Role of HIV-1 Gag domains in virial assembly. Biochim Biophys Acta 1614: 62-72.
8. Gö thel SF, Marahiel MA (1999) Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell Mol Life Sci 55: 423-436.
9. Pastorino L, Sun A, Lu PJ, Zhou XZ, Balastik M, et al. (2006) The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-b production. Nature 440: 528-534.
10. Finkelstein AV, Ptitsyn OB (2002) Lecture 2. In: Protein Physics: A Course of Lectures. Amsterdam: Academic Press. pp 15-22.
11. van Holde KE, Jonson WC, Ho PS (1998) Biological macromolecules. In: Principles of Physical Biochemistry. Upper Saddle River, NJ: Prentice Hall. pp 2-67.
12. Bosco DA, Eisenmesser EZ, Pochapsky S, Sundquist WI, Kern D (2002) Catalysis of cis/trans isomerization in native HIV-1 capsid by human cyclophilin A. Proc Natl Acad Sci U S A 99: 5247-5252.
13. Howard BR, Vajdos FF, Li S, Sundquist WI, Hill CP (2003) Structural insights into the catalytic mechanism of cyclophilin A. Nat Struct Biol 10: 475-481.
14. Li G, Cui Q (2003) What is so special about Arg 55 in the catalysis of cyclophilin A? insights from hybrid QM/MM simulations. J Am Chem Soc 125: 15028-15038.
15. Agarwal PK, Geist A, Gorin A (2004) Protein dynamics and enzymatic catalysis: investigating the peptidyl-prolyl cis-trans isomerization activity of cyclophilin A. Biochemistry 43: 10605-10618.
16. Kofron JL, Kuzmic P, Kishore V, Colo'n-Bonilla E, Rich DH (1991) Determination of kinetic constants for peptidyl prolyl cis-trans isomerases by an improved spectrophotometric assay. Biochemistry 30: 6127-6134.
17. Kern D, Kern G, Scherer G, Fischer G, Drakenberg T (1995) Kinetic analysis of cyclophilin-catalyzed prolyl cis/trans isomerization by dynamic NMR spectroscopy. Biochemistry 34: 13594-13602.
18. Hur S, Bruice TC (2002) The mechanism of cis-trans isomerization of prolyl peptides by cyclophilin. J Am Chem Soc 124: 7303-7313.
19. Fanghänel J, Fischer G (2004) Insights into the catalytic mechanism of peptidyl prolyl cis/trans isomerases. Front Biosci 9: 3453-3478.
20. Zydowsky LD, Etzkorn FA, Chang HY, Ferguson SB, Stolz LA, et al. (1992) Active site mutants of human cyclophilin A separate peptidyl-prolyl isomerase activity from cyclosporin A binding and calcineurin inhibition. Protein Sci 1: 1092-1099.
21. Eisenmesser EZ, Bosco DA, Akke M, Kern D (2002) Enzyme dynamics during catalysis. Science 295: 1520-1523.
22. Agarwal PK (2004) Cis/trans isomerization in HIV-1 capsid protein catalyzed by cyclophilin A: insights from computational and theoretical studies. Proteins 56: 449-463.
23. Agarwal PK (2005) Role of protein dynamics in reaction rate enhancement by enzymes. J Am Chem Soc 127: 15248-15256.
24. Zhao Y, Ke H (1996) Crystal structure implies that cyclophilin predominantly catalyzes the trans to cis isomerization. Biochemistry 35: 7356-7361.
25. Fischer S, Dunbrack RL, Karplus M Jr (1994) Cis-trans imide isomerization of the proline dipeptide. J Am Chem Soc 116: 11931-11937.
26. Laio A, Parrinello M (2002) Escaping free-energy minima. Proc Natl Acad Sci U S A 99: 12562-12566.
27. Piana S, Laio A (2007) A bias-exchange approach to protein folding. J Phys Chem B 111: 4553-4559.
28. Fiorin G, Pastore A, Carloni P, Parrinello M (2006) Using metadynamics to understand the mechanism of calmodulin/target recognition at atomic detail. Biophys J 9: 2768-2777.
29. Wang JM, Cieplak P, Kollman PA (2000) How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J Comput Chem 21: 1049-1074.
30. Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, et al. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65: 712-725.
31. Bashford D, Karplus M (1990) pKa's of ionizable groups in proteins - Atomic detail from a continuum electrostatic model. Biochemistry 29: 10219-10225.
32. Gordon JC, Myers JB, Folta T, Shoja V, Heath LS, et al. (2005) H++: a server for estimating pKas and adding missing hydrogens to macromolecules. Nucleic Acids Res 33: W368-W371.
33. Kelly BN, Kyere S, Kinde I, Tang C, Howard BR, et al. (2007) Structure of the antiviral assembly inhibitor CAP-1 complex with the HIV-1 CA protein. J Mol Biol 373: 355-366.
34. Mahoney MW, Jorgensen WL (2000) A five-site model for liquid water and the reproduction of the density anomaly by rigid, nonpolarizable potential functions. J Chem Phys 112: 8910-8922.
35. Feller SE, Zhang YH, Pastor RW, Brooks BR (1995) Constant-pressure molecular-dynamics simulation: the Langevin piston method. J Chem Phys 103: 4613-4621.
36. Paterlini MG, Ferguson DM (1998) Constant temperature simulations using the Langevin equation with velocity Verlet integration. Chem Phys 236: 243-252.
37. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, et al. (1995) A smooth particle mesh Ewald method. J Chem Phys 103: 8577-8593.
38. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781-1802.
39. Metropolis N, Rosenbluth AW, Rosenbluth MN, Teller AH, Teller E (1953) Equation of state calculations by fast computing machines. J Chem Phys 21: 1087-1092.
40. Daura X, Gademann K, Jaun B, Seebach D, van Gunsteren WF, et al. (1999) Peptide folding: when simulation meets experiment. Angew Chem Int Ed Engl 38: 236-240.
41. Marinelli F, Pietrucci F, Piana S, Laio A (2008) A kinetic model of Trp-cage folding from multiple biased molecular dynamics simulations. Submitted.
42. Evans DJ, Holian BL (1985) The Nose-Hoover thermostat. J Chem Phys 83: 4069-4074.
43. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM (1997) LINCS: a linear constraint solver for molecular simulations. J Comput Chem 18: 1463-1472.
44. Lindahl E, Hess B, van der Spoel D (2001) GROMACS 3.0: a package for molecular simulation and trajectory analysis. J Mol Model 7: 306-317.
45. Berendsen HJC, Vanderspoel D, Vandrunen R (1995) GROMACS: a messagepassing parallel molecular dynamics implementation. Comput Phys Commun 91: 43-56.
46. Piana S, Laio A, Marinelli F, Van Troys M, Bourry D, et al. (2008) Predicting the effect of a point mutation on a protein fold: the villin and advillin headpieces and their Pro62Ala mutants. J Mol Biol 375: 460-470.
47. Ho BK, Coutsias EA, Seok C, Dill KA (2005) The flexibility in the proline ring couples to the protein backbone. Protein Sci 14: 1011-1018.
48. Garcia AE (1992) Large-amplitude nonlinear motions in proteins. Phys Rev Lett 68: 2696-2699.
49. Amadei A, Linssen AB, Berendsen HJ (1993) Essential dynamics of proteins. Proteins 17: 412-425.
50. Lee CT, Yang WT, Parr RG (1988) Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys Rev B 37: 785-789.
51. Becke AD (1993) Density-functional thermochemistry III. The role of exact exchange. J Chem Phys 98: 5648-5652.
52. Vosko SH, Wilk L, Nusair M (1980) Accurate spin-dependent electron liquid correlation energies for local spin density calculations: a critical analysis. Can J Phys 58: 1200-1211.
53. Stephens PJ, Devlin FJ, Chabalowski CF, Frisch MJ (1994) Ab initio calculation of vibrational absorption and circular dichroism spectra using density functional force fields. J Phys Chem 98: 11623-11627.
54. Frisch MJ, et al. (1998) GImage 98. Pittsburgh, PA: Gaussian Inc.
55. Stein RL (1993) Mechanism of enzymatic and nonenzymatic prolyl cis-trans isomerization. Adv Protein Chem 44: 1-24.
56. Eberhardt ES, Loh SN, Hinck AP, Raines RT (1992) Solvent effects on the energetics of prolyl peptide bond isomerization. J Am Chem Soc 114: 5437-5439.
57. Trzesniak D, van Gunsteren WF (2006) 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: 2544-2551.
58. Mark P, Nilsson L (2007) A molecular dynamics study of cyclophilin A free and in complex with the Ala-Pro dipeptide. Eur Biophys J 36: 213-224.
59. McDowell SE, S ̌ pačkova' N, S ̌ poner J, Walter NG (2007) Molecular dynamics simulations of RNA: an in silico single molecule approach. Biopolymers 85: 169-184.
60. Jhon JS, Kang YK (1999) Imide Cis-Trans isomerization of N-Acetyl-N9-methyl proline amide and solvent effects. J Phys Chem A 103: 5436-5439.