Recognition mechanism of siRNA by viral p19 suppressor of RNA silencing: A molecular dynamics study

Biophysical Journal

Volumn 96, Issue 5, 2009, Pages 1761-1769

  Xia, Zhen ^a   Zhu, Zhihong ^a   Zhu, Jun ^a   Zhou, Ruhong ^a,b,c  

^a ZHEJIANG UNIVERSITY   (China)

^b IBM T J WATSON RESEARCH CENTER   (United States)

^c Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; MUTANT PROTEIN; PROTEIN P19; SMALL INTERFERING RNA; TRYPTOPHAN; CORE PROTEIN;

ARTICLE; BASE PAIRING; BINDING AFFINITY; CONTROLLED STUDY; FORCE; GENE MUTATION; GENE SILENCING; HYDROPHOBICITY; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; NONHUMAN; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIMULATION; STRUCTURE ANALYSIS; WILD TYPE; ALGORITHM; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; GENETICS; METABOLISM; MUTATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; THERMODYNAMICS; TOMBUSVIRUS;

RNA VIRUSES; TOMBUSVIRUS;

ALGORITHMS; COMPUTER SIMULATION; HYDROPHOBICITY; MODELS, MOLECULAR; MUTANT PROTEINS; MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; RNA, SMALL INTERFERING; THERMODYNAMICS; TOMBUSVIRUS; VIRAL CORE PROTEINS;

EID: 65549103918     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2008.11.047     Document Type: Article

References (72)

1. Ahlquist, P. 2002. RNA-dependent RNA polymerases, viruses, and RNA silencing. Science. 296:1270-1273.
2. Fire, A., S. Q. Xu, M. K. Montgomery, S. A. Kostas, S. E. Driver, et al. 1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 391:806-811.
3. Novina, C. D., and P. A. Sharp. 2004. The RNAi revolution. Nature. 430:161-164.
4. Bernstein, E., A. A. Caudy, S. M. Hammond, and G. J. Hannon. 2001. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature. 409:363-366.
5. Tomari, Y., and P. D. Zamore. 2005. Perspective: machines for RNAi. Genes Dev. 19:517-529.
6. Schwarz, D. S., G. Hutvagner, T. Du, Z. S. Xu, N. Aronin, et al. 2003. Asymmetry in the assembly of the RNAi enzyme complex. Cell. 115:199-208.
7. Pham, J. W., J. L. Pellino, Y. S. Lee, R. W. Carthew, and E. J. Sontheimer. 2004. A Dicer-2-dependent 80S complex cleaves targeted mRNAs during RNAi in Drosophila. Cell. 117:83-94.
8. Matranga, C., Y. Tomari, C. Shin, D. P. Bartel, and P. D. Zamore. 2005. Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell. 123:607-620.
9. Voinnet, O. 2001. RNA silencing as a plant immune system against viruses. Trends Genet. 17:449-459.
10. Hamilton, A. J., and D. C. Baulcombe. 1999. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science. 286:950-952.
11. Li, W. X., and S. W. Ding. 2001. Viral suppressors of RNA silencing. Curr. Opin. Biotechnol. 12:150-154.
12. Baulcombe, D. 2002. Viral suppression of systemic silencing. Trends Microbiol. 10:306-308.
13. Lakatos, L., T. Csorba, V. Pantaleo, E. J. Chapman, J. C. Carrington, et al. 2006. Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. EMBO J. 25:2768-2780.
14. Qiu, W. P., J. W. Park, and H. B. Scholthof. 2002. Tombusvirus p19-mediated suppression of virus-induced gene silencing is controlled by genetic and dosage features that influence pathogenicity. Mol. Plant Microbe Interact. 15:269-280.
15. Qu, F., and T. J. Morris. 2002. Efficient infection of Nicotiana benthamiana by Tomato bushy stunt virus is facilitated by the coat protein and maintained by p19 through suppression of gene silencing. Mol. Plant Microbe Interact. 15:193-202.
16. Silhavy, D., A. Molnar, A. Lucioli, G. Szittya, C. Hornyik, et al. 2002. A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs. EMBO J. 21:3070-3080.
17. Voinnet, O. 2005. Induction and suppression of RNA silencing: insights from viral infections. Nat. Rev. Genet. 6:206-220.
18. Kasschau, K. D., and J. C. Carrington. 1998. A counter defensive strategy of plant viruses: suppression of posttranscriptional gene silencing. Cell. 95:461-470.
19. Qu, F., and T. J. Morris. 2005. Suppressors of RNA silencing encoded by plant viruses and their role in virus infection. FEBS Lett. 579:5958-5964.
20. Baulcombe, D. 2004. RNA silencing in plants. Nature. 431:356-363.
21. Omarov, R. T., J. J. Ciomperlik, and H. B. Scholthof. 2007. RNAi-associated ssRNA-specific ribonucleases in Tombusvirus P19 mutant-infected plants and evidence for a discrete siRNA-containing effector complex. Proc. Natl. Acad. Sci. USA. 104:1714-1719.
22. Vionnet, O., Y. M. Pinto, and D. C. Baulcombe. 1999. Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc. Natl. Acad. Sci. USA. 96:14147-14152.
23. Roth, B. M., G. J. Pruss, and V. B. Vance. 2004. Plant viral suppressors of RNA silencing. Virus Res. 102:97-108.
24. Anandalakshmi, R., G. J. Pruss, X. Ge, R. Marathe, A. C. Mallory, et al. 1998. A viral suppressor of gene silencing in plants. Proc. Natl. Acad. Sci. USA. 95:13079-13084.
25. Szittya, G., A. Molnar, D. Silhavy, C. Hornyik, and J. Burgyan. 2002. Short defective interfering RNAs of tombusviruses are not targeted but trigger post-transcriptional gene silencing against their helper virus. Plant Cell. 14:1-15.
26. Li, W. X., H. W. Li, R. Lu, F. Li, M. Dus, et al. 2004. Interferon antagonist proteins of influenza and vaccinia viruses are suppressors of RNA silencing. Proc. Natl. Acad. Sci. USA. 101:1350-1355.
27. Dunoyer, P., C. H. Lecellier, E. A. Parizotto, C. Himber, and O. Voinnet. 2004. Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. Plant Cell. 16:1235-1250.
28. Lecellier, C. H., P. Dunoyer, K. Arar, J. Lehmann-Che, S. Eyquem, et al. 2005. A cellular MicroRNA mediates antiviral defense in human cells. Science. 308:557-560.
29. Chapman, E. J., A. I. Prokhnevsky, K. Gopinath, V. V. Dolja, and J. C. Carrington. 2004. Viral RNA silencing suppressors inhibit the micro-RNA pathway at an intermediate step. Genes Dev. 18:1179-1186.
30. Papp, I., M. F. Mette, W. Aufsatz, L. Daxinger, S. E. Schauer, A. Ray, J. van der Winden, M. Matzke, and A. J. Matzke. 2003. Evidence for nuclear processing of plant microRNA and short-interfering RNA precursors. Plant Physiol. 132:1382-1390.
31. Lakatos, L., G. Szittya, D. Silhavy, and J. Burgyan. 2004. Molecular mechanism of RNA silencing suppression mediated by p19 protein of tombusviruses. EMBO J. 23:876-884.
32. Calabrese, J. M., and P. A. Sharp. 2006. Characterization of the short RNAs bound by the P19 suppressor of RNA silencing in mouse embryonic stem cells. RNA. 12:2092-2102.
33. Chu, M., B. Desvoyes, M. Turina, R. Noad, and H. B. Scholthof. 2000. Genetic dissection of tomato bushy stunt virus p19-protein-mediated host-dependent symptom induction and systemic invasion. Virology. 266:79-87.
34. Vargason, J. M., G. Szittya, J. Burgyan, and T. M. T. Hall. 2003. Size selective recognition of siRNA by an RNA silencing suppressor. Cell. 115:799-811.
35. Ye, K. Q., L. Malinina, and D. J. Patel. 2003. Recognition of small interfering RNA by a viral suppressor of RNA silencing. Nature. 426: 874-878.
36. Fersht, A. R., and V. Daggett. 2002. Protein folding and unfolding at atomic resolution. Cell. 108:573-582.
37. Brooks, C. L., J. N. Onuchic, and D. J. Wales. 2001. Statistical thermodynamics - taking a walk on a landscape. Science. 293:612-613.
38. Brooks, C. L., M. Gruebele, J. N. Onuchic, and P. G. Wolynes. 1998. Chemical physics of protein folding. Proc. Natl. Acad. Sci. USA. 95:11037-11038.
39. Zhou, R. H., X. H. Huang, C. J. Margulis, and B. J. Berne. 2004. Hydrophobic collapse in multidomain protein folding. Science. 305:1605-1609.
40. Liu, P., X. H. Huang, R. H. Zhou, and B. J. Berne. 2005. Observation of a dewetting transition in the collapse of the melittin tetramer. Nature. 437:159-162.
41. Snow, C. D., N. Nguyen, V. S. Pande, and M. Gruebele. 2002. Absolute comparison of simulated and experimental protein-folding dynamics. Nature. 420:102-106.
42. Garcia, A. E., and J. N. Onuchic. 2003. Folding a protein in a computer: an atomic description of the folding/unfolding of protein A. Proc. Natl. Acad. Sci. USA. 100:13898-13903.
43. Kokubo, H., and Y. Okamoto. 2004. Prediction of transmembrane helix configurations by replica-exchange simulations. Chem. Phys. Lett. 383:397-402.
44. Straub, J. E., and D. Thirumalai. 1993. Theoretical probes of conformational fluctuations in S-peptide and RNase A/3′-UMP enzyme product complex. Proteins. 15:360-373.
45. Eleftheriou, M., R. Germain, A. Royyuru, and R. Zhou. 2006. Thermal denaturing of mutant lysozyme with both OPLSAA and CHARMM force fields. J. Am. Chem. Soc. 128:13388-13395.
46. Li, X., J. Li, M. Eleftheriou, and R. Zhou. 2006. Hydration and dewetting near fluorinated superhydrophobic plates. J. Am. Chem. Soc. 128:12439-12447.
47. Tucker, M. J., R. Oyola, and F. Gai. 2006. A novel fluorescent probe for protein binding and folding studies: p-cyano-phenylalanine. Biopolymers. 83:571-576.
48. Phillips, J. C., R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, et al. 2005. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26:1781-1802.
49. Kumar, S., C. Huang, G. Zheng, E. Bohm, A. Bhatele, J. C. Phillips, H. Yu, and L. V. Kale. 2008. Scalable molecular dynamics with NAMD on Blue Gene/L. IBM.J. Res. Dev. 52:177-188.
50. Brooks, B. R., R. E. Bruccoeri, B. D. Olafson, D. J. States, S. Swaminathan, et al. 1983. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4:187-217.
51. MacKerell, A. D., Jr., N. Banavali, and N. Foloppe. 2000. Development and current status of the CHARMM force field for nucleic acids. Biopolymers. 56:257-265.
52. Mackerell, A. D., Jr., M. Feig, and C. L. Brooks, 3rd.. 2004. Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J. Comput. Chem. 25:1400-1415.
53. Jorgensen, W. L., J. Chandrasekhar, J. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935.
54. Neria, E., and M. Karplus. 1996. A position dependent friction model for solution reactions in the high friction regime: proton transfer in triosephosphate isomerase (TIM). J. Chem. Phys. 105:10812-10818.
55. Deserno, M., and C. Holm. 1998. How to mesh up Ewald sums. I. A theoretical and numerical comparison of various particle mesh routines. J. Chem. Phys. 109:7678-7693.
56. Deserno, M., and C. Holm. 1998. How to mesh up Ewald sums. II. An accurate error estimate for the particle-particle-particle-mesh algorithm. J. Chem. Phys. 109:7694-7701.
57. Deng, Y. Q., and B. Roux. 2006. Calculation of standard binding free energies: aromatic molecules in the T4 lysozyme L99A mutant. J. Chem. Theory Comput. 2:1255-1273.
58. Tirado-Rives, J., and W. L. Jorgensen. 2006. Contribution of conformer focusing to the uncertainty in predicting free energies for protein-ligand binding. J. Med. Chem. 49:5880-5884.
59. Thorpe, I. F., and C. L. Brooks, 3rd.. 2007. Molecular evolution of affinity and flexibility in the immune system. Proc. Natl. Acad. Sci. USA. 104:8821-8826.
60. Jayachandran, G., M. R. Shirts, S. Park, and V. S. Pande. 2006. Parallelized-over-parts computation of absolute binding free energy with docking and molecular dynamics. J. Chem. Phys. 125:084901.
61. Reference deleted in proof.
62. Pan, Y., D. Gao, W. Yang, H. Cho, and C. G. Zhan. 2007. Free energy perturbation (FEP) simulation on the transition states of cocaine hydrolysis catalyzed by human butyrylcholinesterase and its mutants. J. Am. Chem. Soc. 129:13537-13543.
63. Yang, W., R. Bitetti-Putzer, and M. Karplus. 2004. Free energy simulations: use of reverse cumulative averaging to determine the equilibrated region and the time required for convergence. J. Chem. Phys. 120:2618-2628.
64. Reference deleted in proof.
65. Warshel, A. 1984. Simulating the energetics and dynamics of enzymatic reactions in specificity in biological interactions. Pontificiae Academiae Scientiarum Scripta Varia. 55:60-81.
66. + by gramicidin A. Biophys. J. 56:171-182.
67. Warshel, A., P. K. Sharma, M. Kato, and W. W. Parson. 2006. Modeling electrostatic effects in proteins. Biochim. Biophys. Acta. 1764:1647-1676.
68. Mark, A. E., and W. F. van Gunsteren. 1994. Decomposition of the free energy of a system in terms of specific interactions. Implications for theoretical and experimental studies. J. Mol. Biol. 240:167-176.
69. Boresch, S., and M. Karplus. 1995. The meaning of component analysis: decomposition of the free energy in terms of specific interactions. J. Mol. Biol. 254:801-807.
70. Brady, G. P., and K. A. Sharp. 1995. Decomposition of interaction free energies in proteins and other complex systems. J. Mol. Biol. 254:77-85.
71. Bren, M., J. Florian, J. Mavri, and U. Bren. 2007. Do all pieces make a whole? Thiele cumulants and the free energy decomposition. Theor. Chem. Acc. 117:535-540.
72. Scholthof, H. B. 2006. Timeline - the Tombusvirus-encoded P19: from irrelevance to elegance. Nat. Rev. Microbiol. 4:405-411.