pH-dependent molecular dynamics of vesicular stomatitis virus glycoprotein G

Proteins: Structure, Function and Bioinformatics

Volumn 80, Issue 11, 2012, Pages 2601-2613

  Rücker, Pia ^a   Wieninger, Silke A ^b   Ullmann, G Matthias ^b   Sticht, Heinrich ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF BAYREUTH   (Germany)

Author keywords

Biophysical simulation; Computational biology; Protein structure; Protonation; Viral fusion

Indexed keywords

THROMBOSPONDIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENDOSOME; MOLECULAR DYNAMICS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE; VESICULAR STOMATITIS VIRUS;

GLYCOPROTEINS; HYDROGEN-ION CONCENTRATION; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTONS; VESICULAR STOMATITIS; VESICULAR STOMATITIS INDIANA VIRUS; VIRAL FUSION PROTEINS;

VESICULAR STOMATITIS VIRUS;

EID: 84867204197     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24145     Document Type: Article

References (44)

1. Helenius A, Kartenbeck J, Simons K, Fries E. On the entry of Semliki forest virus into BHK-21 cells. J Cell Biol 1980; 84: 404-420.
2. White J, Helenius A. pH-dependent fusion between the Semliki forest virus membrane and liposomes. Proc Natl Acad Sci USA 1980; 77: 3273-3277.
3. Harrison SC. Viral membrane fusion. Nat Struct Mol Biol 2008; 15: 690-698.
4. Kamman RL, Go KG, Muskiet FA, Stomp GP, Van Dijk P, Berendsen HJ. Proton spin relaxation studies of fatty tissue and cerebral white matter. Magn Reson Imaging 1984; 2: 211-220.
5. Backovic M, Jardetzky TS. Class III viral membrane fusion proteins. Curr Opin Struct Biol 2009; 19: 189-196.
6. Da Poian AT, Carneiro FA, Stauffer F. Viral membrane fusion: is glycoprotein G of rhabdoviruses a representative of a new class of viral fusion proteins? Braz J Med Biol Res 2005; 38: 813-823.
7. Harrison SC. The pH sensor for flavivirus membrane fusion. J Cell Biol 2008; 183: 177-179.
8. Kampmann T, Mueller DS, Mark AE, Young PR, Kobe B. The role of histidine residues in low-pH-mediated viral membrane fusion. Structure 2006; 14: 1481-1487.
9. Maeda T, Ohnishi S. Activation of influenza virus by acidic media causes hemolysis and fusion of erythrocytes. FEBS Lett 1980; 122: 283-287.
10. Roche S, Gaudin Y. Characterization of the equilibrium between the native and fusion-inactive conformation of rabies virus glycoprotein indicates that the fusion complex is made of several trimers. Virology 2002; 297: 128-135.
11. Skehel JJ, Bayley PM, Brown EB, Martin SR, Waterfield MD, White JM, Wilson IA, Wiley DC. Changes in the conformation of influenza virus hemagglutinin at the pH optimum of virus-mediated membrane fusion. Proc Natl Acad Sci USA 1982; 79: 968-972.
12. Roche S, Bressanelli S, Rey FA, Gaudin Y. Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 2006; 313: 187-191.
13. Roche S, Rey FA, Gaudin Y, Bressanelli S. Structure of the prefusion form of the vesicular stomatitis virus glycoprotein G. Science 2007; 315: 843-848.
14. Carneiro FA, Stauffer F, Lima CS, Juliano MA, Juliano L, Da Poian AT. Membrane fusion induced by vesicular stomatitis virus depends on histidine protonation. J Biol Chem 2003; 278: 13789-13794.
15. Roche S, Albertini AA, Lepault J, Bressanelli S, Gaudin Y. Structures of vesicular stomatitis virus glycoprotein: membrane fusion revisited. Cell Mol Life Sci 2008; 65: 1716-1728.
16. Bashford D. An object-oriented programming suite for electrostatic effects in biological molecules: an experience report on the MEAD project Scientific Computing in Object-Oriented Parallel Environments. In: Scientific computing in object-oriented parallel environments. Ishikawa Y, Oldehoeft R, Reynders J, Tholburn M, editors. Vol. 1343. Berlin: Springer; 1997. pp 233-240.
17. Bashford D, Gerwert K. Electrostatic calculations of the pKa values of ionizable groups in bacteriorhodopsin. J Mol Biol 1992; 224: 473-486.
18. Ullmann GM, Knapp EW. Electrostatic models for computing protonation and redox equilibria in proteins. Eur Biophys J 1999; 28: 533-551.
19. Case DA, Cheatham T, Darden T, Gohlke H, Luo R, Merz KM, Onufriev A, Simmerling C, Wang B, Woods R. The Amber biomolecular simulation programs. J Comput Chem 2005; 26: 1668-1688.
20. Case DA, Darden TA, Cheatham TE, III, Simmerling CL, Wang J, Duke RE, Luo R, Merz KM, Pearlman DA, Crowley M, Walker RC, Zhang W, Wang B, Hayik S, Roitberg A, Seabra G, Wong KF, Paesani F, Wu X, Brozell S, Tsui V, Gohlke H, Yang L, Tan C, Mongan J, Hornak V, Cui G, Beroza P, Mathews DH, Schafmeister C, Ross WS, Kollman PA. AMBER 9. San Francisco, CA: University of California; 2006.
21. Pearlman DA, Case DA, Caldwell JW, Ross WS, Cheatham TE, III, DeBolt S, Ferguson D, Seibel G, Kollman P. AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Comput Phys Commun 1995; 91: 1-41.
22. Cheatham TE, III, Cieplak P, Kollman PA. A modified version of the Cornell et al. force field with improved sugar pucker phases and helical repeat. J Biomol Struct Dyn 1999; 16: 845-862.
23. Cornell WD, Cieplak P, Bayly CI, Gould IR, Merz KMJ, Ferguson DM, Spellmeyer DC, Fox T, Caldwell JW, Kollman PA. A second generation force field for the simulation of proteins, nucleic acids and organic molecules. J Am Chem Soc 1995; 117: 5179-5197.
24. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. Comparison of simple potential functions for simulating liquid water. J Chem Phys 1983; 79: 926-935.
25. Darden TA, York DM, Pedersen LG. Particle mesh Ewald. An N.log(N) method for Ewald sums in large systems. J Chem Phys 1993; 98: 10089-10092.
26. Dirauf P, Meiselbach H, Sticht H. Effects of the V82A and I54V mutations on the dynamics and ligand binding properties of HIV-1 protease. J Mol Model 2010; 16: 1577-1583.
27. Meiselbach H, Horn AH, Harrer T, Sticht H. Insights into amprenavir resistance in E35D HIV-1 protease mutation from molecular dynamics and binding free-energy calculations. J Mol Model 2007; 13: 297-304.
28. Wartha F, Horn AHC, Meiselbach H, Sticht H. Molecular dynamics simulations of HIV-1 protease suggest different mechanisms contributing to drug resistance. J Chem Theory Comput 2005; 1: 315-324.
29. Ryckaert JP, Ciccotti G, Berendsen HJC. Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 1977; 23: 327-341.
30. Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics. J Mol Graph 1996; 14: 33-38, 27-38.
31. Tripos. Sybyl 7.3. St. Louis, Missouri: Tripos; 1991-2008.
32. Accelrys. DS ViewerPro Suite 6.0. San Diego, CA: Accelrys; 2005.
33. Case D, Darden T, Cheatham TI, Simmerling C, Wang J, Duke R, Luo R, Crowley M, Walker R, Zhang W, Merz K, Wang B, Hayik S, Roitberg A, Seabra G, Kolossváry I, Wong K, Paesani F, Vanicek J, Wu X, Brozell S, Steinbrecher T, Gohlke H, Yang L, Tan C, Mongan J, Hornak V, Cui G, Mathews D, Seetin M, Sagui C, Babin V, Kollman P. AMBER 10. San Francisco: University of California, CA; 2008.
34. Onufriev A, Bashford D, Case DA. Exploring protein native states and large-scale conformational changes with a modified generalized born model. Proteins 2004; 55: 383-394.
35. Sitkoff D, Lockhart DJ, Sharp KA, Honig B. Calculation of electrostatic effects at the amino terminus of an α-helix. Biophys J 1994; 67: 2251-2260.
36. a values in proteins-a theoretical analysis of protonation energies with practical consequences for enzymatic reactions. J Phys Chem B 2010; 114: 1994-2003.
37. Gorecki A, Szypowski M, Dlugosz M, Trylska J. RedMD-reduced molecular dynamics package. J Comput Chem 2009; 30: 2364-2373.
38. Mueller DS, Kampmann T, Yennamalli R, Young PR, Kobe B, Mark AE. Histidine protonation and the activation of viral fusion proteins. Biochem Soc Trans 2008; 36: 43-45.
39. Li Y, Drone C, Sat E, Ghosh HP. Mutational analysis of the vesicular stomatitis virus glycoprotein G for membrane fusion domains. J Virol 1993; 67: 4070-4077.
40. Shokralla S, He Y, Wanas E, Ghosh HP. Mutations in a carboxy-terminal region of vesicular stomatitis virus glycoprotein G that affect membrane fusion activity. Virology 1998; 242: 39-50.
41. Nelson S, Poddar S, Lin TY, Pierson TC. Protonation of individual histidine residues is not required for the pH-dependent entry of west Nile virus: evaluation of the "histidine switch" hypothesis. J Virol 2009; 83: 12631-12635.
42. Cui Q, Li G, Ma J, Karplus M. A normal mode analysis of structural plasticity in the biomolecular motor F(1)-ATPase. J Mol Biol 2004; 340: 345-372.
43. Kleinekathofer U, Isralewitz B, Dittrich M, Schulten K. Domain motion of individual F(1)-ATPase βeta-subunits during unbiased molecular dynamics simulations. J Phys Chem A 2011; 115: 7267-7274.
44. Gaudin Y, Raux H, Flamand A, Ruigrok RW. Identification of amino acids controlling the low-pH-induced conformational change of rabies virus glycoprotein. J Virol 1996; 70: 7371-7378.