SOP-GPU: Accelerating biomolecular simulations in the centisecond timescale using graphics processors

Proteins: Structure, Function and Bioinformatics

Volumn 78, Issue 14, 2010, Pages 2984-2999

  Zhmurov, A ^a,b   Dima, R I ^c   Kholodov, Y ^b   Barsegov, V ^a,b  

^a University of Massachusetts Lowell   (United States)

^b MOSCOW INSTITUTE OF PHYSICS AND TECHNOLOGY   (Russian Federation)

^c UNIVERSITY OF CINCINNATI   (United States)

Author keywords

Biomolecular assemblies; Coarse grained models; Dynamic force spectroscopy; Force extension curves; Graphics processing units; Langevin dynamics

Indexed keywords

ARTICLE; ATOMIC FORCE MICROSCOPY; DYNAMIC FORCE SPECTROSCOPY; ELECTRON MICROSCOPY; GRAPHIC PROCESSING UNIT; INFORMATION PROCESSING; MICROPROCESSOR; OPTICAL TWEEZERS; PRIORITY JOURNAL; PROTEIN PROCESSING; SELF ORGANIZED POLYMER MODEL; SIMULATION;

ALGORITHMS; BIOMECHANICS; COMPUTER GRAPHICS; COMPUTER SIMULATION; FIBRINOGEN; HUMANS; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; PROTEIN FOLDING; SYNAPTOTAGMIN I;

EID: 77958019726     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22824     Document Type: Article

References (89)

1. Stossel TP, Condeelis J, Cooley L, Hartwig JH, Noegel A, Schleicher M, Shapiro SS, Filamins as integrators of cell mechanics and signalling. Nat Rev Mol Cell Biol 2001;2:138-145.
2. Johnson CP, Tang HY, Carag C, Speicher DW, Discher DE. Forced unfolding of proteins within cells. Science 2007;317:663-666.
3. Paul R, Heil P, Spatz JP, Schwarz US. Propagation of mechanical stress through the actin cytoskeleton toward focal adhesions: model and experiment. Biophys J 2008;94:1470-1482.
4. Leckband D. Nanomechanics of adhesion proteins. Curr Opin Struct Biol 2004;14:523-530.
5. McEver RP. Selectins: lectins that initiate cell adhesion under flow. Curr Opin Cell Biol 2002;14:581-586.
6. Marshall BT, Long M, Piper JW, Yago T, McEver RP, Zhu C. Direct observation of catch bonds involving cell-adhesion molecules. Nature 2003;423:190-193.
7. Barsegov V, Thirumalai D. Dynamics of unbinding of cell adhesion molecules: Transition from catch to slip bonds. Proc Natl Acad Sci USA 2005;102:1835-1839.
8. Weisel JW. The mechanical properties of fibrin for basic scientists and clinicians. Biophys Chem 2004;112:267-276.
9. Weisel JW. Enigmas of blood clot elasticity. Science 2008;320:456-457.
10. Lord ST. Fibrinogen and fibrin: scaffold proteins in hemostasis. Curr Opin Hematol 2007;14:236-241.
11. Falvo MR, Washburn S, Superfine R, Finch M, Brooks Jr FP, Chi V, Taylor RM II. Manipulation of individual viruses: friction and mechanical properties. Biophys J 1997;72:1396-1403.
12. Uetrecht C, Verslius C, Watts NR, Roos WH, Wuite GJL, Wingfield PT, Steven AC, Heck AJ. High-resolution mass spectrometry of viral assemblies: molecular composition and stability of dimorphic hepatitis b virus capsids. Proc Natl Acad Sci USA 2008;105: 9216-9220.
13. Kuznetsov YG, Daijogo S, Zhou J, Semler BL, McPherson A. Atomic force microscopy analysis of icosahedral virus RNA. J Mol Biol 2007;347:41-52.
14. Kol N, Shi Y, Tsvitov M, Barlam D, Shneck RZ, Kay MS, Rousso I. A stiffness switch in human immunodeficiency virus. Biophys J 2007;92:1777-1783.
15. Ivanovska IL, de Pablo PJ, Ibarra B, Sgalari G, MacKintosh FC, Carrascosa JL, Schmidt CF, Wuite GJL. Bacteriophage capsids: tough nanoshells with complex elastic properties. Proc Natl Acad Sci USA 2004;101:7600-7605.
16. Ivanovska I, Wuite G, Joensson B, Evilevitch A. Internal DNA pressure modifies stability of WT phage. Proc Natl Acad Sci USA 2007;104:9603-9608.
17. Steven AC, BHJ, Cheng N, Trus BL, Conway JF. Virus maturation: dynamics and mechanism of a stabilizing structural transition that leads to infectivity. Curr Opin Struct Biol 2005;15:227-236.
18. Carrion-Vazquez M, Li H, Lu H, Marszalek PE, Oberhauser AF, Fernandez JM. The mechanical stability of ubiquitin is linkage dependent. Nat Struct Biol 2003;10:738-743.
19. Schwaiger I, Sattler C, Hostetter DR, Rief M. The myosin coiledcoil is a trully elastic protein structure. Nature Mat 2002;1:232-235.
20. Brujic J, Hermans RI, Walther KA, Fernandez JM. Single-molecule force spectroscopy reveals signatures of glassy dynamics in the energy landscape of ubiquitin. Nature Phys 2006;2:282-286.
21. Brown AEX, Litvinov RI, Discher DE, Weisel JW. Forced unfolding of coiled-coils in fibrinogen by single-molecule AFM. Biophys J 2007;92:L39-L41.
22. Smith DE, Tans SJ, Smith SB, Grimes S, Anderson DL, Bustamante C. The bacteriophage φ 29 portal motor can package DNA against a large internal force. Nature 2001;413:748-752.
23. Roos WH, Ivanovska IL, Evilevitch A, Wuite GJL. Viral capsids: Mechanical characteristics, genome packaging and delivery mechanisms. Cell Mol Life Sci 2007;64:1484-1497.
24. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, Karplus M. CHARMM: a programm for macromolecular energy, minimization, and dynamics calculations. J Comp Chem 1983;4:187-217.
25. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kalé L, Schulten K. Scalable molecular dynamics with NAMD. J Comp Chem 2005;26:1781-1802.
26. Berendsen HJC, van der Spoel D, van Drunen R. GROMACS: a message-passing parallel molecular dynamics implementation. Comp Phys Commun 1995;91:43-56.
27. Isralewitz B, Gao M, Schulten K. Steered molecular dynamics and mechanical functions of proteins. Curr Opin Struct Biol 2001;11: 224-230.
28. Stone JE, Phillips JC, Freddolino PL, Hardy DJ, Trabuco LG, Schulten K. Accelerating molecular modeling applications with graphical processors. J Comp Chem 2007;28:2618-2640.
29. Freddolino PL, Liu F, Gruebele M, Schulten K. Ten-microsecond MD simulation of a fast-folding WW domain. Biophys J 2008;94: L75-L77.
30. Zink M, Grubmueller H. Mechanical properties of the icosahedral shell of southern bean mosaic virus: A molecular dynamics study. Biophys J 2009;96:1767-1777.
31. AMD. ATI Stream Computing Technical Overview. AMD; Sunnyvale, CA, 2009.
32. NVIDIA. NVIDIA CUDA Programming Guide, 2.3.1 ed. NVIDIA; Santa Clara, CA, 2009.
33. NVIDIA. NVIDIA CUDA C Programming Best Practices Guide, 2.3 ed. NVIDIA; Santa Clara, CA, 2009.
34. Munshi A. Khronos OpenCL Working Group The OpenCL Specification, 1.0 ed. Beaverton, OR. Publisher-Khronos Group, 2009.
35. Anderson AG, Goddard WA, III, Schroder P. QuantumMonte Carlo on graphical processing units. Comp Phys Commun 2007;177:298-306.
36. Yasuda K. Two-electron integral evaluation on the graphics processor unit. J Comput Chem 2007;29:334-342.
37. Yasuda K. Accelerating density functional calculations with graphics processing Unit. J Chem Theor Comput 2008;4:1230-1236.
38. Ufimtsev IS, Martinez TJ. Quantum chemistry on graphics processing units. Strategies for two-electron integral evaluation. J Chem Theor Comput 2008;4:222-231.
39. Vogt L, Olivares-Amaya R, Kermes S, Shao Y, Amador-Bedolla C, AspuruGuzik A. Accelerating resolution-of-the-identity secondorder Moller-Plesset quantum chemistry calculations with graphical processing units. J Phys Chem A 2008;112:2049-2057.
40. Rodrigues CI, Hardy DJ, Stone JE, Schulten K, Hwu W-MW. GPU acceleration of cutoff pair potentials for molecular modeling applications. CF 008: Proceedings of the 5th conference on computing frontiers, New York, NY, USA. ACM; 2008;273-282.
41. Phillips JC, Stone JE, Schulten K. Adapting a message-driven parallel application to GPU-accelerated clusters. SC '08: Proceedings of the 2008ACM/IEEE conference on supercomputing, Piscataway, NJ, USA: IEEE Press; 20pp. 1-9.
42. Friedrichs MS, Eastman P, Vaidyanathan V, Houston M, Legrand S, Beberg AL, Ensign DL, Bruins CM, Pande VS. Accelerating molecular dynamic simulation on Graphics Processing Units. J Comput Chem 2009;30:864-872.
43. Harvey MJ, Giupponi G, Fabritilis GD. ACEMD: accelerating biomolecular dynamics in the microsecond time scale. J Chem Theory Comput 2009;5:1632-1639.
44. Harvey MJ, Fabritilis GD. An implementation of the smooth Particle Mesh Ewald method on GPU hardware. J Chem Theory Comput 2009;5:2371-2377.
45. Davis JE, Ozsoy A, Patel S, Taufer M. Towards large-scale molecular dynamics simulations on graphics processors. BICoB '09: Proceedings of the 1st international conference on bioinformatics and computational biology, Berlin, Heidelberg. Springer-Verlag: New York, NY, 2009;176-186.
46. van Meel JA, Arnold A, Frenkel D, Zwart SFP, Belleman R. Harvesting graphics power for MD simulations. Mol Simul 2008;34:259-266.
47. Anderson JA, Lorentz CD, Travesset A. General purpose molecular dynamics simulations fully implemented on graphics processing units. J Comp Phys 2008;227:5342-5359.
48. Tozzini V. Coarse-grained models for proteins. Curr Opin Struct Biol 2005;15:144-150.
49. Clementi C, Nymeyer H, Onuchic JN. Toplogical and energetic factors: what determines the structural details of the transition state ensemble and "en-route" intermediates for protein folding?. J Mol Biol 2000;298:937-953.
50. Veitshans T, Klimov D, Thirumalai D. Protein folding kinetics: timescales, pathways and energy landscapes in terms of sequencedependent properties. Folding and Design 1997;2:1-22.
51. Klimov DK, Thirumalai D. Native topology determines forceinduced unfolding pathways in globular proteins. Proc Natl Acad Sci USA 2000;97:7254-7259.
52. Hyeon C, Dima RI, Thirumalai D. Pathways and kinetic barriers in mechanical unfolding and refolding of RNA and proteins. Structure 2006;14:1633-1645.
53. Mickler M, Dima RI, Dietz H, Hyeon C, Thirumalai D, Rief M. Revealing the bifurcation in the unfolding pathways of GFP using single molecule experiments and simulations. Proc Natl Acad Sci USA 2007;104:20268-20273.
54. Dima RI, Joshi H. Probing the origin of tubulin rigidity with molecular simulations. Proc Natl Acad Sci USA 2008.
55. Hyeon C, Onuchic JN. Internal strain regulates the nucleotide binding site of the kinesin leading head. Proc Natl Acad Sci USA 2007;104:2175-2180.
56. Lin JC, Thirumalai D. Relative stability of helices determines the folding landscape of adenine riboswitch aptamers. J Am Chem Soc 2008;130:14080-14084.
57. Hyeon C, Lorimer GH, Thirumalai D. Dynamics of allosteric transitions in GroEL. Proc Natl Acad Sci USA 2006;103:18939-18944.
58. Chen J, Dima RI, Thirumalai D. Allosteric communication in dihydrofolate reductase: signaling network and pathways for closed to occluded transition and back. J Mol Biol 2007;374:250-266.
59. Hyeon C, Jennings PA, Adams JA, Onuchic JN. Ligand-induced global transitions in the catalytic domain of protein kinase A. Proc Natl Acad Sci USA 2009;106:3023-3028.
60. Tehver R, Thirumalai D. Rigor to post-rigor transition in myosin V: Link between the dynamics and the supporting architecture. Structure 2010;18:471-481.
61. Kirk DB, Wen-Mei WH. Programming Massively Parallel Processors: a hands-on approach. Morgan Kaufmann: Burlington, MA; 2010.
62. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Sindyalov IN, Bourne PE. The protein databank. Nucleic Acids Res 2000;28:235-242.
63. Levesque D, Verlet L, Kürkijarvi J. Computer "experiments" on classical fluids. IV. Transport properties and time-correlation functions of the Lennard-Jones liquid near its triple point. Phys Rev A 1973;7:1690-1700.
64. Box GEP, Miller ME. A note on the generation of normal random deviates. Ann Math Stat 1958;29:610-611.
65. Nguyen H, editor. GPU Gems Addison-Wesley; Boston, MA; 2008.
66. Carrillo-Tripp M, Shepherd CM, Borelli IA, Venkataraman S, Lander G, Natarajan P, Johnson JE, Brooks ICL, Reddy VS. VIPERdb2: an enhanced and web API enabled relational database for structural virology. Nucl Acid Res 2009;37:D436-D442.
67. Ferguson N, Johnson CM, Macias M, Oschkinat H, Fersht AR. Ultrafast folding of WW domains without structured aromatic clusters in the denatured state. Proc Natl Acad Sci USA 2001;98:13002-13007.
68. Karanicolas J, Brooks CL. Structural basis for biphasic kinetics in the folding of the WW domain from a formin-binding proteins: lessons for protein design? Proc Natl Acad Sci USA 2003;100:3954-3959.
69. Ermak DL, McCammon JA. Brownian dynamics with hydrodynamic interactions. J Chem Phys 1978;69:1352-1360.
70. Rief M, Gautel M, Oesterhelt F, Fernandez JM, Gaub HE. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 1997;276:1109-1112.
71. Carrion-Vazquez M, Oberhauser AF, Fisher TE, Marszalek PE, Li H, Fernandez JM. Mechanical design of proteins studied by single-molecule force spectroscopy and protein engineering. Prog Biophys Mol Biol 2000;74:63-91.
72. Martens S, Kozlov MM, McMahon HT. How synaptotagmin promotes membrane fusion. Science 2007;316:1205-1208.
73. Fuson KL, Ma L, Sutton RB, Oberhauser AF. The C2 domains of human synaptotagmin 1 have distinct mechanical properties. Biophys J 2009;96:1083-1090.
74. Yang J, Wang Y, Chen Y. GPU accelerated molecular dynamics simulations of thermal conductivities. J Comp Phys 2007;221:799-804.
75. NVIDIA. NVIDIA'S Next generation CUDA Compute Architecture: Fermi, 1.1 ed. NVIDIA; Santa Clara, CA, 2009.
76. Marszalek P, Lu H, Li H, Carrion-Vazquez M, Oberhauser A, Schulten K, Fernandez J. Mechanical unfolding intermediates in titin modules. Nature 1999;402:100-103.
77. Michel JP, Ivanovska IL, Gibbons MM, Klug WS, Knobler CM, Wuite GJL, Schmidt CF. Nanoindentation studies of full and empty viral capsids and the effects of capsid protein mutations on elasticity and strength. Proc Natl Acad Sci USA 2006;103:6184-6189.
78. Barsegov V, Morrison G, Thirumalai D. Role of internal chain dynamics on the rupture kinetics of adhesive contacts. Phys Rev Lett 2008;100:248102-248105.
79. Barsegov V, Klimov DK, Thirumalai D. Mapping the energy landscape of biomolecules using single molecule force correlation spectroscopy: theory and applications. Biophys J 2006;90:3827-3841.
80. Bura E, Klimov DK, Barsegov V. Analyzing forced unfolding of protein tandems by ordered variates, 1: independent unfolding times. Biophys J 2007;93:1100-1115.
81. Bell GI. Models for the specific adhesion of cells to cells. Science. 1978;200:618-627.
82. Evans E, Ritchie K. Dynamic strength of molecular adhesion bonds. Biophys J 1997;72:1541-1555.
83. Hummer G, Szabo A. Kinetics from nonequilibrium single-molecule pulling experiments. Biophys J 2003;85:5-15.
84. Dudko OK, Hummer G, Szabo A. Theory, analysis, and interpretation of single-molecule force spectroscopy experiments. Proc Natl Acad Sci USA 2008;105:15755-15760.
85. Hyeon C, Thirumalai D. Forced-unfolding and force-quench refolding of RNA hairpins. Biophys J 2006;90:3410-3427.
86. Hyeon C, Thirumalai D. Measuring the energy landscape roughness and the transition state location of biomolecules using single molecule mechanical unfolding experiments. J Phys Cond Matt 2007;19:113101-113128.
87. Zwanzig R. Nonequilibrium statistical mechanics. Oxford, U.K: Oxford University Press: 2001.
88. Hanggi P, Talkner P, Borkovec M. Reaction-rate theory: fifty years after Kramers. Rev Mod Phys 1990;62:251-341.
89. Lu H, Schulten K. Steered molecular dynamics simulations of force-induced protein domain unfolding. Proteins 1999;35:453-463.