Nipah virion entry kinetics, composition, and conformational changes determined by enzymatic virus-like particles and new flow virometry tools

Journal of Virology

Volumn 88, Issue 24, 2014, Pages 14197-14206

  Landowski, Matthew ^a   Dabundo, Jeffrey ^a   Liu, Qian ^a   Nicola, Anthony V ^a   Aguilar, Hector C ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LACTAMASE; CHIMERIC PROTEIN; EPHRIN B2; EPHRIN B3; VIRUS ENVELOPE PROTEIN; VIRUS GLYCOPROTEIN; VIROSOME;

ARTICLE; CELL FUSION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; EMBRYO; FLOW MEASUREMENT; FLOW VIROMETRY; HUMAN; HUMAN CELL; MEMBRANE FUSION; NIPAH VIRUS; NONHUMAN; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR BINDING; VIRION; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS MUTANT; VIRUS PARTICLE; VIRUS RELEASE; CELL LINE; METABOLISM; PHYSIOLOGY; PROCEDURES; VIROLOGY;

CELL LINE; HUMANS; NIPAH VIRUS; VIRION; VIROLOGY; VIROSOMES; VIRUS INTERNALIZATION;

EID: 84911478785     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01632-14     Document Type: Article

References (55)

1. Eaton BT, Broder CC, Middleton D, Wang LF. 2006. Hendra and Nipah viruses: different and dangerous. Nat. Rev. Microbiol. 4:23-35. http://dx.doi.org/10.1038/nrmicro1323.
2. Lamb RA, Paterson RG, Jardetzky TS. 2006. Paramyxovirus membrane fusion: lessons from the F andHNatomic structures. Virology 344:30-37. http://dx.doi.org/10.1016/j.virol.2005.09.007.
3. White JM, Delos SE, Brecher M, Schornberg K. 2008. Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit. Rev. Biochem. Mol. Biol. 43:189-219. http://dx.doi.org/10.1080/10409230802058320.
4. Hsu VP, Hossain MJ, Parashar UD, Ali MM, Ksiazek TG, Kuzmin I, Niezgoda M, Rupprecht C, Bresee J, Breiman RF. 2004. Nipah virus encephalitis reemergence, Bangladesh. Emerg. Infect. Dis. 10:2082-2087. http://dx.doi.org/10.3201/eid1012.040701.
5. Lam SK. 2003. Nipah virus-a potential agent of bioterrorism? Antiviral Res. 57:113-119. http://dx.doi.org/10.1016/S0166-3542(02)00204-8.
6. Bonaparte MI, Dimitrov AS, Bossart KN, Crameri G, Mungall BA, Bishop KA, Choudhry V, Dimitrov DS, Wang LF, Eaton BT, Broder CC. 2005. Ephrin-B2 ligand is a functional receptor for Hendra virus and Nipah virus. Proc. Natl. Acad. Sci. U. S. A. 102:10652-10657. http://dx.doi.org/10.1073/pnas.0504887102.
7. Negrete OA, Levroney EL, Aguilar HC, Bertolotti-Ciarlet A, Nazarian R, Tajyar S, Lee B. 2005. EphrinB2 is the entry receptor for Nipah virus, an emergent deadly paramyxovirus. Nature 436:401-405. http://dx.doi.org/10.1038/nature03838.
8. Negrete OA, Wolf MC, Aguilar HC, Enterlein S, Wang W, Muhlberger E, Su SV, Bertolotti-Ciarlet A, Flick R, Lee B. 2006. Two key residues in ephrinB3 are critical for its use as an alternative receptor for Nipah virus. PLoS Pathog. 2:e7. http://dx.doi.org/10.1371/journal.ppat.0020007.
9. Chua KB, Bellini WJ, Rota PA, Harcourt BH, Tamin A, Lam SK, Ksiazek TG, Rollin PE, Zaki SR, Shieh W, Goldsmith CS, Gubler DJ, Roehrig JT, Eaton B, Gould AR, Olson J, Field H, Daniels P, Ling AE, Peters CJ, Anderson LJ, Mahy BW. 2000. Nipah virus: a recently emergent deadly paramyxovirus. Science 288:1432-1435. http://dx.doi.org/10.1126/science.288.5470.1432.
10. Luby SP, Hossain MJ, Gurley ES, Ahmed BN, Banu S, Khan SU, Homaira N, Rota PA, Rollin PE, Comer JA, Kenah E, Ksiazek TG, Rahman M. 2009. Recurrent zoonotic transmission of Nipah virus into humans, Bangladesh, 2001-2007. Emerg. Infect. Dis. 15:1229-1235. http://dx.doi.org/10.3201/eid1508.081237.
11. Luby SP, Rahman M, Hossain MJ, Blum LS, Husain MM, Gurley E, Khan R, Ahmed BN, Rahman S, Nahar N, Kenah E, Comer JA, Ksiazek TG. 2006. Foodborne transmission of Nipah virus, Bangladesh. Emerg. Infect. Dis. 12:1888-1894. http://dx.doi.org/10.3201/eid1212.060732.
12. Aguilar HC, Iorio RM. 2012. Henipavirus membrane fusion and viral entry. Curr. Top. Microbiol. Immunol. 359:79-94. http://dx.doi.org/10.1007/82_2012_200.
13. Dutch RE. 2010. Entry and fusion of emerging paramyxoviruses. PLoS Pathog. 6:e1000881. http://dx.doi.org/10.1371/journal.ppat.1000881.
14. Lamb RA, Jardetzky TS. 2007. Structural basis of viral invasion: lessons from paramyxovirus F. Curr. Opin. Struct. Biol. 17:427-436. http://dx.doi.org/10.1016/j.sbi.2007.08.016.
15. Aloia RC, Tian HR, Jensen FC. 1993. Lipid-composition and fluidity of the human-immunodeficiency-virus envelope and host-cell plasmamembranes. Proc. Natl. Acad. Sci. U. S. A. 90:5181-5185. http://dx.doi.org/10.1073/pnas.90.11.5181.
16. Nguyen DH, Hildreth JEK. 2000. Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. J. Virol. 74:3264-3272. http://dx.doi.org/10.1128/JVI.74.7.3264-3272.2000.
17. Aguilar HC, Lee B. 2011. Emerging paramyxoviruses: molecular mechanisms and antiviral strategies. Expert Rev. Mol. Med. 13:e6. http://dx.doi.org/10.1017/S1462399410001754.
18. Cathomen T, Mrkic B, Spehner D, Drillien R, Naef R, Pavlovic J, Aguzzi A, Billeter MA, Cattaneo R. 1998. A matrix-less measles virus is infectious and elicits extensive cell fusion: consequences for propagation in the brain. EMBO J. 17:3899-3908. http://dx.doi.org/10.1093/emboj/17.14.3899.
19. Money VA, McPhee HK, Mosely JA, Sanderson JM, Yeo RP. 2009. Surface features of a Mononegavirales matrix protein indicate sites of membrane interaction. Proc. Natl. Acad. Sci. U. S. A. 106:4441-4446. http://dx.doi.org/10.1073/pnas.0805740106.
20. Takimoto T, Murti KG, Bousse T, Scroggs RA, Portner A. 2001. Role of matrix and fusion proteins in budding of Sendai virus. J. Virol. 75:11384-11391. http://dx.doi.org/10.1128/JVI.75.23.11384-11391.2001.
21. Takimoto T, Portner A. 2004. Molecular mechanism of paramyxovirus budding. Virus Res. 106:133-145. http://dx.doi.org/10.1016/j.virusres.2004.08.010.
22. Harrison MS, Sakaguchi T, Schmitt AP. 2010. Paramyxovirus assembly and budding: building particles that transmit infections. Int. J. Biochem. Cell Biol. 42:1416-1429. http://dx.doi.org/10.1016/j.biocel.2010.04.005.
23. Ciancanelli MJ, Basler CF. 2006. Mutation of YMYL in the Nipah virus matrix protein abrogates budding and alters subcellular localization. J. Virol. 80:12070-12078. http://dx.doi.org/10.1128/JVI.01743-06.
24. Patch JR, Crameri G, Wang LF, Eaton BT, Broder CC. 2007. Quantitative analysis of Nipah virus proteins released as virus-like particles reveals central role for the matrix protein. Virol. J. 4:1. http://dx.doi.org/10.1186/1743-422X-4-1.
25. Patch JR, Han Z, McCarthy SE, Yan L, Wang LF, Harty RN, Broder CC. 2008. The YPLGVG sequence of the Nipah virus matrix protein is required for budding. Virol. J. 5:137. http://dx.doi.org/10.1186/1743-422X-5-137.
26. Wang YE, Park A, Lake M, Pentecost M, Torres B, Yun TE, Wolf MC, Holbrook MR, Freiberg AN, Lee B. 2010. Ubiquitin-regulated nuclearcytoplasmic trafficking of the Nipah virus matrix protein is important for viral budding. PLoS Pathog. 6:e1001186. http://dx.doi.org/10.1371/journal.ppat.1001186.
27. Wolf MC, Wang Y, Freiberg AN, Aguilar HC, Holbrook MR, Lee B. 2009. A catalytically and genetically optimized beta-lactamase-matrix based assay for sensitive, specific, and higher throughput analysis of native henipavirus entry characteristics. Virol. J. 6:119. http://dx.doi.org/10.1186/1743-422X-6-119.
28. Zlokarnik G, Negulescu PA, Knapp TE, Mere L, Burres N, Feng LX, Whitney M, Roemer K, Tsien RY. 1998. Quantitation of transcription and clonal selection of single living cells with beta-lactamase as reporter. Science 279:84-88. http://dx.doi.org/10.1126/science.279.5347.84.
29. Cavrois M, de Noronha C, Greene WC. 2002. A sensitive and specific enzyme-based assay detecting HIV-1 virion fusion in primary T lymphocytes. Nat. Biotechnol. 20:1151-1154. http://dx.doi.org/10.1038/nbt745.
30. Lu X, Liu Q, Benavides-Montano JA, Nicola AV, Aston DE, Rasco BA, Aguilar HC. 2013. Detection of receptor-induced glycoprotein conformational changes on enveloped virions by using confocal micro-Raman spectroscopy. J. Virol. 87:3130-3142. http://dx.doi.org/10.1128/JVI.03220-12.
31. Negrete OA, Chu D, Aguilar HC, Lee B. 2007. Single amino acid changes in the Nipah and Hendra virus attachment glycoproteins distinguish ephrinb2 from ephrinb3 usage. J. Virol. 81:10804-10814. http://dx.doi.org/10.1128/JVI.00999-07.
32. Liu Q, Stone JA, Bradel-Tretheway B, Dabundo J, Montano JAB, Santos-Montanez J, Biering SB, Nicola AV, Iorio RM, Lu XN, Aguilar HC. 2013. Unraveling a three-step spatiotemporal mechanism of triggering of receptor-induced Nipah virus fusion and cell entry. PLoS Pathog. 9(11):e1003770. http://dx.doi.org/10.1371/journal.ppat.1003770.
33. Aguilar HC, Aspericueta V, Robinson LR, Aanensen KE, Lee B. 2010. A quantitative and kinetic fusion protein-triggering assay can discern distinct steps in the Nipah virus membrane fusion cascade. J. Virol. 84:8033-8041. http://dx.doi.org/10.1128/JVI.00469-10.
34. Aguilar HC, Ataman ZA, Aspericueta V, Fang AQ, Stroud M, Negrete OA, Kammerer RA, Lee B. 2009. A novel receptor-induced activation site in the Nipah virus attachment glycoprotein (G) involved in triggering the fusion glycoprotein (F). J. Biol. Chem. 284:1628-1635. http://dx.doi.org/10.1074/jbc.M807469200.
35. Cardone G, Brecher M, Fontana J, Winkler DC, Butan C, White JM, Steven AC. 2012. Visualization of the two-step fusion process of the retrovirus avian sarcoma/leukosis virus by cryo-electron tomography. J. Virol. 86:12129-12137. http://dx.doi.org/10.1128/JVI.01880-12.
36. Dollery SJ, Delboy MG, Nicola AV. 2010. Low pH-induced conformational change in herpes simplex virus glycoprotein B. J. Virol. 84:3759-3766. http://dx.doi.org/10.1128/JVI.02573-09.
37. Dollery SJ, Wright CC, Johnson DC, Nicola AV. 2011. Low-pHdependent changes in the conformation and oligomeric state of the prefusion form of herpes simplex virus glycoprotein B are separable from fusion activity. J. Virol. 85:9964-9973. http://dx.doi.org/10.1128/JVI.05291-11.
38. He L, Piper A, Meilleur F, Hernandez R, Heller WT, Brown DT. 2012. Conformational changes in Sindbis virus induced by decreased pH are revealed by small-angle neutron scattering. J. Virol. 86:1982-1987. http://dx.doi.org/10.1128/JVI.06569-11.
39. Tran EEH, Borgnia MJ, Kuybeda O, Schauder DM, Bartesaghi A, Frank GA, Sapiro G, Milne JLS, Subramaniam S. 2012. Structural mechanism of trimeric HIV-1 envelope glycoprotein activation. PLoS Pathog. 8:e1002797. http://dx.doi.org/10.1371/journal.ppat.1002797.
40. Aguilar HC, Matreyek KA, Filone CM, Hashimi ST, Levroney EL, Negrete OA, Bertolotti-Ciarlet A, Choi DY, McHardy I, Fulcher JA, Su SV, Wolf MC, Kohatsu L, Baum LG, Lee B. 2006. N-glycans on Nipah virus fusion protein protect against neutralization but reduce membrane fusion and viral entry. J. Virol. 80:4878-4889. http://dx.doi.org/10.1128/JVI.80.10.4878-4889.2006.
41. Levroney EL, Aguilar HC, Fulcher JA, Kohatsu L, Pace KE, Pang M, Gurney KB, Baum LG, Lee B. 2005. Novel innate immune functions for galectin-1: galectin-1 inhibits cell fusion by Nipah virus envelope glycoproteins and augments dendritic cell secretion of proinflammatory cytokines. J. Immunol. 175:413-420. http://dx.doi.org/10.4049/jimmunol.175.1.413.
42. Niwa H, Yamamura K, Miyazaki J. 1991. Efficient selection for highexpression transfectants with a novel eukaryotic vector. Gene 108:193-199. http://dx.doi.org/10.1016/0378-1119(91)90434-D.
43. Aguilar HC, Matreyek KA, Choi DY, Filone CM, Young S, Lee B. 2007. Polybasic KKR motif in the cytoplasmic tail of Nipah virus fusion protein modulates membrane fusion by inside-out signaling. J. Virol. 81:4520-4532. http://dx.doi.org/10.1128/JVI.02205-06.
44. Biering SB, Huang A, Vu AT, Robinson LR, Bradel-Tretheway B, Choi E, Lee B, Aguilar HC. 2012. N-glycans on the Nipah virus attachment glycoprotein modulate fusion and viral entry as they protect against antibody neutralization. J. Virol. 86:11991-12002. http://dx.doi.org/10.1128/JVI.01304-12.
45. Tscherne DM, Manicassamy B, Garcia-Sastre A. 2010. An enzymatic virus-like particle assay for sensitive detection of virus entry. J. Virol. Methods 163:336-343. http://dx.doi.org/10.1016/j.jviromet.2009.10.020.
46. Whitman SD, Dutch RE. 2007. Surface density of the Hendra G protein modulates Hendra F protein-promoted membrane fusion: role for Hendra G protein trafficking and degradation. Virology 363:419-429. http://dx.doi.org/10.1016/j.virol.2007.01.029.
47. McKinnell JA, Saag MS. 2009. Novel drug classes: entry inhibitors [enfuvirtide, chemokine (C-C motif) receptor 5 antagonists]. Curr. Opin. HIV AIDS 4:513-517. http://dx.doi.org/10.1097/COH.0b013e328331d3d 0.
48. Poveda E, Briz V, Soriano V. 2005. Enfuvirtide, the first fusion inhibitor to treat HIV infection. AIDS Rev. 7:139-147.
49. Russell CJ, Jardetzky TS, Lamb RA. 2001. Membrane fusion machines of paramyxoviruses: capture of intermediates of fusion. EMBO J. 20:4024-4034. http://dx.doi.org/10.1093/emboj/20.15.4024.
50. Iorio RM, Mahon PJ. 2008. Paramyxoviruses: different receptors- different mechanisms of fusion. Trends Microbiol. 16:135-137. http://dx.doi.org/10.1016/j.tim.2008.01.006.
51. Albertini AA, Merigoux C, Libersou S, Madiona K, Bressanelli S, Roche S, Lepault J, Melki R, Vachette P, Gaudin Y. 2012. Characterization of monomeric intermediates during VSV glycoprotein structural transition. PLoS Pathog. 8:e1002556. http://dx.doi.org/10.1371/journal.ppat.1002556.
52. Li L, Jose J, Xiang Y, Kuhn RJ, Rossmann MG. 2010. Structural changes of envelope proteins during alphavirus fusion. Nature 468:705-708. http://dx.doi.org/10.1038/nature09546.
53. Yin HS, Paterson RG, Wen X, Lamb RA, Jardetzky TS. 2005. Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proc. Natl. Acad. Sci. U. S. A. 102:9288-9293. http://dx.doi.org/10.1073/pnas.0503989102.
54. Rossman JS, Jing XH, Leser GP, Lamb RA. 2010. Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 142:902-913. http://dx.doi.org/10.1016/j.cell.2010.08.029.
55. Walpita P, Barr J, Sherman M, Basler CF, Wang L. 2011. Vaccine potential of Nipah virus-like particles. PLoS One 6:e18437. http://dx.doi.org/10.1371/journal.pone.0018437.