Structure and functional dynamics characterization of the ion channel of the human respiratory syncytial virus (hRSV) small hydrophobic protein (SH) transmembrane domain by combining molecular dynamics with excited normal modes

Journal of Molecular Modeling

Volumn 22, Issue 12, 2016, Pages

  Araujo, Gabriela C ^a   Silva, Ricardo H T ^b   Scott, Luis P B ^b   Araujo, Alexandre S ^a   Souza, Fatima P ^a   de Oliveira, Ronaldo Junio ^c  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b UNIVERSIDADE FEDERAL DO ABC   (Brazil)

^c FEDERAL UNIVERSITY OF TRIÂNGULO MINEIRO   (Brazil)

Author keywords

Excited normal modes; Molecular dynamics; RSV; SH protein; Viroporin

Indexed keywords

ION CHANNEL; MEMBRANE PROTEIN; PHOSPHOLIPID; UNCLASSIFIED DRUG; VIRAL PROTEIN; VIROPORIN;

APOPTOSIS; ARTICLE; CONFORMATIONAL TRANSITION; HUMAN RESPIRATORY SYNCYTIAL VIRUS; LIPID BILAYER; MEMBRANE PERMEABILITY; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN STRUCTURE; VIRUS REPLICATION; WATER TRANSPORT; CHEMICAL PHENOMENA; CHEMISTRY; GENETICS; HUMAN; METABOLISM; PROTEIN CONFORMATION; PROTEIN DOMAIN; STRUCTURE ACTIVITY RELATION;

HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; ION CHANNELS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; STRUCTURE-ACTIVITY RELATIONSHIP; VIRAL PROTEINS;

EID: 85003766144     PISSN: 16102940     EISSN: 09485023     Source Type: Journal    
DOI: 10.1007/s00894-016-3150-6     Document Type: Article

References (50)

1. Falsey AR, Hennessey PA, Formica MA, Cox C, Walsh EE (2005) Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med 352:1749–1759. doi:10.1056/NEJMoa043951
2. Nair H, Nokes DJ, Gessner BD, Dherani M, Madhi SA, Singleton RJ et al. (2010) Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis. Lancet 375:1545–1555. doi:10.1016/S0140-6736(10)60206-1
3. Boyce TG, Mellen BG, Mitchel EF, Wright PF, Griffin MR (2000) Rates of hospitalization for respiratory syncytial virus infection among children in medicaid. J Pediatr 137:865–870. doi:10.1067/mpd.2000.110531
4. Collins PL, Hill MG, Cristina J, Grosfeld H (1996) Transcription elongation factor of respiratory syncytial virus, a nonsegmented negative-strand RNA virus. Proc Natl Acad Sci 93:81–85
5. Kochva U, Leonov H, Arkin IT (2003) Modeling the structure of the respiratory syncytial virus small hydrophobic protein by silent-mutation analysis of global searching molecular dynamics. Protein Sci Publ Protein Soc 12:2668–2674
6. Collins PL, Olmsted RA, Johnson PR (1990) The small hydrophobic protein of human respiratory syncytial virus: comparison between antigenic subgroups A and B. J Gen Virol 71(Pt 7):1571–1576
7. Olmsted RA, Collins PL (1989) The 1A protein of respiratory syncytial virus is an integral membrane protein present as multiple, structurally distinct species. J Virol 63:2019–2029
8. Collins PL, Mottet G (1993) Membrane orientation and oligomerization of the small hydrophobic protein of human respiratory syncytial virus. J Gen Virol 74(Pt 7):1445–1450
9. Jin H, Zhou H, Cheng X, Tang R, Munoz M, Nguyen N (2000) Recombinant respiratory syncytial viruses with deletions in the NS1, NS2, SH, and M2-2 genes are attenuated in vitro and in vivo. Virology 273:210–218. doi:10.1006/viro.2000.0393
10. Whitehead SS, Bukreyev A, Teng MN, Firestone CY, Claire MS, Elkins WR et al. (1999) Recombinant respiratory syncytial virus bearing a deletion of either the NS2 or SH gene is attenuated in chimpanzees. J Virol 73:3438–3442
11. Heminway BR, Yu Y, Tanaka Y, Perrine KG, Gustafson E, Bernstein JM et al. (1994) Analysis of respiratory syncytial virus F, G, and SH proteins in cell fusion. Virology 200:801–805. doi:10.1006/viro.1994.1245
12. Techaarpornkul S, Barretto N, Peeples ME (2001) Functional analysis of recombinant respiratory syncytial virus deletion mutants lacking the small hydrophobic and/or attachment glycoprotein gene. J Virol 75:6825–6834. doi:10.1128/JVI.75.15.6825-6834.2001
13. Fuentes S, Tran KC, Luthra P, Teng MN, He B (2007) Function of the respiratory syncytial virus small hydrophobic protein. J Virol 81:8361–8366. doi:10.1128/JVI.02717-06
14. He B, Lin GY, Durbin JE, Durbin RK, Lamb RA (2001) The SH integral membrane protein of the paramyxovirus simian virus 5 is required to block apoptosis in MDBK cells. J Virol 75:4068–4079. doi:10.1128/JVI.75.9.4068-4079.2001
15. Gan S-W, Tan E, Lin X, Yu D, Wang J, Tan GM-Y et al. (2012) The small hydrophobic protein of the human respiratory syncytial virus forms pentameric ion channels. J Biol Chem 287:24671–24689. doi:10.1074/jbc.M111.332791
16. Ramjeesingh M, Huan LJ, Garami E, Bear CE (1999) Novel method for evaluation of the oligomeric structure of membrane proteins. Biochem J 342:119–123
17. Gan SW, Ng L, Lin X, Gong X, Torres J (2008) Structure and ion channel activity of the human respiratory syncytial virus (hRSV) small hydrophobic protein transmembrane domain. Protein Sci Publ Protein Soc 17:813–820. doi:10.1110/ps.073366208
18. Perez M, Garcıa-Barreno B, Melero JA, Carrasco L, Guinea R (1997) Membrane permeability changes induced in escherichia coliby the sh protein of human respiratory syncytial virus. Virology 235:342–351. doi:10.1006/viro.1997.8696
19. Gonzalez ME, Carrasco L (2003) Viroporins. FEBS Lett 552:28–34
20. Rost B, Yachdav G, Liu J (2004) The PredictProtein server. Nucleic Acids Res 32:W321–W326. doi:10.1093/nar/gkh377
21. Buchan DWA, Minneci F, Nugent TCO, Bryson K, Jones DT (2013) Scalable web services for the PSIPRED protein analysis workbench. Nucleic Acids Res 41:W349–W357. doi:10.1093/nar/gkt381
22. Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinf 9:40. doi:10.1186/1471-2105-9-40
23. Berendsen HJC, van der Spoel D, van Drunen R (1995) GROMACS: a message-passing parallel molecular dynamics implementation. Comput Phys Commun 91:43–56. doi:10.1016/0010-4655(95)00042-E
24. Pronk S, Páll S, Schulz R, Larsson P, Bjelkmar P, Apostolov R et al. (2013) GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics doi:10.1093/bioinformatics/btt055.
25. Oostenbrink C, Villa A, Mark AE, van Gunsteren WF (2004) A biomolecular force field based on the free enthalpy of hydration and solvation: the GROMOS force-field parameter sets 53A5 and 53A6. J Comput Chem 25:1656–1676. doi:10.1002/jcc.20090
26. Berger O, Edholm O, Jähnig F (1997) Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys J 72:2002–2013. doi:10.1016/S0006-3495(97)78845-3
27. Berendsen HJC, Postma JPM, van Gunsteren WF, Hermans J (1981) Interaction models for water in relation to protein hydration. In: Pullman B (ed) Intermolecular forces. Springer, Netherlands, pp 331–342
28. Bussi G, Donadio D, Parrinello M (2007) Canonical sampling through velocity rescaling. J Chem Phys 126:014101. doi:10.1063/1.2408420
29. Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A, Haak JR (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81:3684–3690. doi:10.1063/1.448118
30. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG (1995) A smooth particle mesh Ewald method. J Chem Phys 103:8577–8593. doi:10.1063/1.470117
31. Nieva JL, Madan V, Carrasco L (2012) Viroporins: structure and biological functions. Nat Rev Microbiol 10:563–574. doi:10.1038/nrmicro2820
32. Murzyn K, Róg T, Pasenkiewicz-Gierula M (2005) Phosphatidylethanolamine-phosphatidylglycerol bilayer as a model of the inner bacterial membrane. Biophys J 88:1091–1103. doi:10.1529/biophysj.104.048835
33. Costa MGS, Batista PR, Bisch PM, Perahia D (2015) Exploring free energy landscapes of large conformational changes: molecular dynamics with excited normal modes. J Chem Theory Comput. doi:10.1021/acs.jctc.5b00003
34. Floquet N, Durand P, Maigret B, Badet B, Badet-Denisot M-A, Perahia D (2009) Collective motions in glucosamine-6-phosphate synthase: influence of ligand binding and role in ammonia channelling and opening of the fructose-6-phosphate binding site. J Mol Biol 385:653–664. doi:10.1016/j.jmb.2008.10.032
35. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, Karplus M (1983) CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J Comput Chem 4:187–217. doi:10.1002/jcc.540040211
36. Li Y, To J, Verdià-Baguena C, Dossena S, Surya W, Huang M et al. (2014) Inhibition of the human respiratory syncytial virus small hydrophobic protein and structural variations in a Bicelle environment. J Virol 88:11899–11914. doi:10.1128/JVI.00839-14
37. Wan S, Torres J (2011) Structural and functional aspects of the small hydrophobic (SH) protein in the human respiratory syncytial virus. In: Resch B (ed) Hum Respir Syncytial Virus Infect. InTech, doi:10.5772/28747
38. Tamm LK, Tatulian SA (1997) Infrared spectroscopy of proteins and peptides in lipid bilayers. Q Rev Biophys 30:365–429
39. Lin Y, Bright AC, Rothermel TA, He B (2003) Induction of apoptosis by paramyxovirus simian virus 5 lacking a small hydrophobic gene. J Virol 77:3371–3383. doi:10.1128/JVI.77.6.3371-3383.2003
40. Jourd’heuil D, Aspinall A, Reynolds JD, Meddings JB (1996) Membrane fluidity increases during apoptosis of sheep ileal Peyer’s patch B cells. Can J Physiol Pharmacol 74:706–711
41. Fujimoto K, Iwasaki C, Kawaguchi H, Yasugi E, Oshima M (1999) Cell membrane dynamics and the induction of apoptosis by lipid compounds. FEBS Lett 446:113–116. doi:10.1016/S0014-5793(99)00204-5
42. Wilson RL, Fuentes SM, Wang P, Taddeo EC, Klatt A, Henderson AJ et al. (2006) Function of small hydrophobic proteins of paramyxovirus. J Virol 80:1700–1709. doi:10.1128/JVI.80.4.1700-1709.2006
43. Triantafilou K, Kar S, Vakakis E, Kotecha S, Triantafilou M (2013) Human respiratory syncytial virus viroporin SH: a viral recognition pathway used by the host to signal inflammasome activation. Thorax 68:66–75. doi:10.1136/thoraxjnl-2012-202182
44. Chen I-Y, Ichinohe T (2015) Response of host inflammasomes to viral infection. Trends Microbiol 23:55–63. doi:10.1016/j.tim.2014.09.007
45. Daura X, Gademann K, Jaun B, Seebach D, van Gunsteren WF, Mark AE (1999) Peptide folding: when simulation meets experiment. Angew Chem Int Ed 38:236–240. doi:10.1002/(SICI)1521-3773(19990115)38:1/2<236::AID-ANIE236>3.0.CO;2-M
46. Li Y, Jain N, Limpanawat S, To J, Quistgaard EM, Nordlund P et al. (2015) Interaction between human BAP31 and respiratory syncytial virus small hydrophobic (SH) protein. Virology 482:105–110. doi:10.1016/j.virol.2015.03.034
47. Ambroggio EE, Separovic F, Bowie JH, Fidelio GD, Bagatolli LA (2005) Direct visualization of membrane leakage induced by the antibiotic peptides: maculatin, citropin, and aurein. Biophys J 89:1874–1881. doi:10.1529/biophysj.105.066589
48. Lang F, Föller M, Lang KS, Lang PA, Ritter M, Gulbins E et al. (2005) Ion channels in cell proliferation and apoptotic cell death. J Membr Biol 205:147–157. doi:10.1007/s00232-005-0780-5
49. Szabò I, Adams C, Gulbins E (2004) Ion channels and membrane rafts in apoptosis. Pflügers Arch Eur J Physiol 448:304–312
50. Kochva U, Leonov H, Arkin IT (2003) Modeling the structure of the respiratory syncytial virus small hydrophobic protein by silent-mutation analysis of global searching molecular dynamics. Protein Sci 12:2668–2674. doi:10.1110/ps.03151103