Detection of receptor-induced glycoprotein conformational changes on enveloped virions by using confocal micro-raman spectroscopy

Journal of Virology

Volumn 87, Issue 6, 2013, Pages 3130-3142

  Lu, Xiaonan ^a,b   Liu, Qian ^b   Benavides Montano, Javier A ^b,c   Nicola, Anthony V ^b   Aston, D Eric ^d   Rasco, Barbara A ^b   Aguilar, Hector C ^b  

^a TIANJIN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c UNIVERSIDAD NACIONAL DE COLOMBIA   (Colombia)

^d UNIVERSITY OF IDAHO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASSEMBLY MATRIX PROTEIN; EPHRIN B2; EPHRIN B3; MATRIX PROTEIN; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; VIRUS GLYCOPROTEINS F; VIRUS GLYCOPROTEINS G;

ANIMAL CELL; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; FEASIBILITY STUDY; MEMBRANE FUSION; NIPAH VIRUS; NONHUMAN; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAMAN SPECTROMETRY; RECEPTOR BINDING; REPRODUCIBILITY; SIGNAL TRANSDUCTION; TEMPERATURE; VESICULAR STOMATITIS VIRUS; VIRION; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS LIKE AGENT;

HUMANS; NIPAH VIRUS; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTORS, VIRUS; SPECTRUM ANALYSIS, RAMAN; VIRAL ENVELOPE PROTEINS; VIRION; VIROLOGY; VIRUS ATTACHMENT;

EID: 84874734792     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03220-12     Document Type: Article

References (80)

1. 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.
2. Dollery SJ, Delboy MG, Nicola AV. 2010. Low pH-induced conformational change in herpes simplex virus glycoprotein B. J. Virol. 84:3759- 3766.
3. 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.
4. 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.
5. 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. doi:10.1371/journal.ppat.1002797.
6. 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.
7. Eaton BT, Broder CC, Middleton D, Wang LF. 2006. Hendra and Nipah viruses: different and dangerous. Nat. Rev. Microbiol. 4:23-35.
8. Lamb RA, Paterson RG, Jardetzky TS. 2006. Paramyxovirus membrane fusion: lessons from the F andHNatomic structures. Virology 344:30 -37.
9. Aguilar HC, Iorio RM. 2012. Henipavirus membrane fusion and viral entry. Curr. Top. Microbiol. Immunol. 359:79 -94.
10. 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. doi:10.1371/journal.ppat.1002556.
11. Li L, Jose J, Xiang Y, Kuhn RJ, Rossmann MG. 2010. Structural changes of envelope proteins during alphavirus fusion. Nature 468:705-708.
12. Russell CJ, Jardetzky TS, Lamb RA. 2001. Membrane fusion machines of paramyxoviruses: capture of intermediates of fusion. EMBO J. 20:4024- 4034.
13. 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.
14. 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.
15. Goldsmith CS, Miller SE. 2009. Modern uses of electron microscopy for detection of viruses. Clin. Microbiol. Rev. 22:552-563.
16. Mahony JB. 2008. Detection of respiratory viruses by molecular methods. Clin. Microbiol. Rev. 21:716 -747.
17. Leland DS, Ginocchio CC. 2007. Role of cell culture for virus detection in the age of technology. Clin. Microbiol. Rev. 20:49 -78.
18. Harry DJ, Jennings MB, Yee J, Carlson JR. 1989. Antigen detection for human immunodeficiency virus. Clin. Microbiol. Rev. 2:241-249.
19. Lu X, Rasco BA, Kang DH, Jabal JM, Aston DE, Konkel ME. 2011. Infrared and Raman spectroscopic studies of the antimicrobial effects of garlic concentrates and diallyl constituents on foodborne pathogens. Anal. Chem. 83:4137- 4146.
20. Tuma R. 2005. Raman spectroscopy of proteins: from peptides to large assemblies. J. Raman Spectrosc. 36:307-319.
21. Alexander TA. 2008. Development of methodology based on commercialized SERS-active substrates for rapid discrimination of Poxviridae virions. Anal. Chem. 80:2817-2825.
22. Hoang V, Tripp RA, Rota P, Dluhy RA. 2010. Identification of individual genotypes of measles virus using surface enhanced Raman spectroscopy. Analyst 135:3103-3109.
23. Driskell JD, Zhu Y, Kirkwood CD, Zhao Y, Dluhy RA, Tripp RA. 2010. Rapid and sensitive detection of rotavirus molecular signatures using surface enhanced Raman spectroscopy. PLoS One 5:e10222. doi:10.1371 /journal.pone.0010222.
24. Shanmukh S, Jones L, Driskell J, Zhao Y, Dluhy R, Tripp RA. 2006. Rapid and sensitive detection of respiratory virus molecular signatures using a silver nanorod array SERS substrate. Nano Lett. 6:2630 -2636.
25. Shanmukh S, Jones L, Zhao YP, Driskell JD, Tripp RA, Dluhy RA. 2008. Identification and classification of respiratory syncytial virus (RSV) strains by surface-enhanced Raman spectroscopy and multivariate statistical techniques. Anal. Bioanal. Chem. 390:1551-1555.
26. Cialla D, Deckert-Gaudig T, Budich C, Laue M, Moller R, Naumann D, Deckert V, Popp J. 2009. Raman to the limit: tip-enhanced Raman spectroscopic investigations of a single tobacco mosaic virus. J. Raman Spectrosc. 40:240 -243.
27. Hermann P, Hermelink A, Lausch V, Holland G, Moller L, Bannert N, Naumann D. 2011. Evaluation of tip-enhanced Raman spectroscopy for characterizing different virus strains. Analyst 136:1148 -1152.
28. 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.
29. 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.
30. Bossart KN, Wang LF, Eaton BT, Broder CC. 2001. Functional expression and membrane fusion tropism of the envelope glycoproteins of Hendra virus. Virology 290:121-135.
31. Bossart KN, Wang LF, Flora MN, Chua KB, Lam SK, Eaton BT, Broder CC. 2002. Membrane fusion tropism and heterotypic functional activities of the Nipah virus and Hendra virus envelope glycoproteins. J. Virol. 76:11186 -11198.
32. 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.
33. 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.
34. 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.
35. 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. doi:10.1371/journal.ppat.0020007.
36. 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.
37. Lu X, Huang Q, Miller WG, Aston DE, Xu J, Xue F, Zhang H, Rasco BA, Wang S, Konkel ME. 2012. Comprehensive detection and discrimination of Campylobacter species by use of confocal micro-Raman spectroscopy and multilocus sequence typing. J. Clin. Microbiol. 50:2932- 2946.
38. 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. doi:10.1186/1743-422X -6-119.
39. 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.
40. Bocklitz T, Walter A, Hartmann K, Rosch P, Popp J. 2011. How to pre-process Raman spectra for reliable and stable models? Anal. Chim. Acta 704:47-56.
41. Lieber CA, Mahadevan-Jansen A. 2003. Automated method for subtraction of fluorescence from biological Raman spectra. Appl. Spectrosc. 57: 1363-1367.
42. Ashton L, Johannessen C, Goodacre R. 2011. The importance of protonation in the investigation of protein phosphorylation using Raman spectroscopy and Raman optical activity. Anal. Chem. 83:7978 -7983.
43. Brewster VL, Ashton L, Goodacre R. 2011. Monitoring the glycosylation status of proteins using Raman spectroscopy. Anal. Chem. 83:6074-6081.
44. De Maesschalck R, Jouan-Rimbaud D, Massart DL. 2000. The Mahalanobis distance. Chemometr. Intell. Lab. 50:1-18.
45. Li JF, Hibbert DB, Fuller S, Cattle J, Way CP. 2005. Comparison of spectra using a Bayesian approach. An argument using oil spills as an example. Anal. Chem. 77:639-644.
46. Hamel L, Brown CW. 2012. Bayesian probability approach to feature significance for infrared spectra of bacteria. Appl. Spectrosc. 66:48 -59.
47. Shreve J, Schneider H, Soysal O. 2011. A methodology for comparing classification methods through the assessment of model stability and validity in variable selection. Decis. Support Syst. 52:247-257.
48. Noda I. 1993. Generalized 2-dimensional correlation method applicable to infrared, Raman, and other types of spectroscopy. Appl. Spectrosc. 47:1329 -1336.
49. 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. doi:10.1186/1743 -422X-4-1.
50. 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. doi:10.1186/1743-422X-5-137.
51. 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. doi:10.1371/journal.ppat.1001186.
52. Markosyan RM, Cohen FS, Melikyan GB. 2003. HIV-1 envelope proteins complete their folding into six-helix bundles immediately after fusion pore formation. Mol. Biol. Cell 14:926 -938.
53. Mzoughi O, Gaston F, Granados GC, Lakhdar-Ghazal F, Giralt E, Bahraoui E. 2010. Fusion intermediates of HIV-1 gp41 as targets for antibody production: design, synthesis, and HR1-HR2 complex purification and characterization of generated antibodies. ChemMedChem 5:1907-1918.
54. 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.
55. Poveda E, Briz V, Soriano V. 2005. Enfuvirtide, the first fusion inhibitor to treat HIV infection. AIDS Rev. 7:139 -147.
56. Iorio RM, Mahon PJ. 2008. Paramyxoviruses: different receptors- different mechanisms of fusion. Trends Microbiol. 16:135-137.
57. Zhu F, Isaacs NW, Hecht L, Tranter GE, Barron LD. 2006. Raman optical activity of proteins, carbohydrates and glycoproteins. Chirality 18: 103-115.
58. Blanch EW, Hecht L, Day LA, Pederson DM, Barron LD. 2001. Tryptophan absolute stereochemistry in viral coat proteins from Raman optical activity. J. Am. Chem. Soc. 123:4863- 4864.
59. Blanch EW, Hecht L, Syme CD, Volpetti V, Lomonossoff GP, Nielsen K, Barron LD. 2002. Molecular structures of viruses from Raman optical activity. J. Gen. Virol. 83:2593-2600.
60. Blanch EW, McColl IH, Hecht L, Nielsen K, Barron LD. 2004. Structural characterization of proteins and viruses using Raman optical activity. Vib. Spectrosc. 35:87-92.
61. Blanch EW, Robinson DJ, Hecht L, Barron LD. 2001. A comparison of the solution structures of tobacco rattle and tobacco mosaic viruses from Raman optical activity. J. Gen. Virol. 82:1499 -1502.
62. McColl IH, Blanch EW, Hecht L, Barron LD. 2004. A study of alphahelix hydration in polypeptides, proteins, and viruses using vibrational Raman optical activity. J. Am. Chem. Soc. 126:8181- 8188.
63. Zhu F, Isaacs NW, Hecht L, Barron LD. 2005. Polypeptide and carbohydrate structure of an intact glycoprotein from Raman optical activity. J. Am. Chem. Soc. 127:6142- 6143.
64. Arboleda PH, Loppnow GR. 2000. Raman spectroscopy as a discovery tool in carbohydrate chemistry. Anal. Chem. 72:2093-2098.
65. Kinalwa MN, Blanch EW, Doig AJ. 2010. Accurate determination of protein secondary structure content from Raman and Raman optical activity spectra. Anal. Chem. 82:6347- 6349.
66. McColl IH, Blanch EW, Gill AC, Rhie AG, Ritchie MA, Hecht L, Nielsen K, Barron LD. 2003. A new perspective on beta-sheet structures using vibrational Raman optical activity: from poly(L-lysine) to the prion protein. J. Am. Chem. Soc. 125:10019 -10026.
67. Zhu F, Isaacs NW, Hecht L, Barron LD. 2005. Raman optical activity: a tool for protein structure analysis. Structure 13:1409 -1419.
68. Lednev IK, Karnoup AS, Sparrow MC, Asher SA. 1999. Alpha-helix peptide folding and unfolding activation barriers: a nanosecond UV resonance Raman study. J. Am. Chem. Soc. 121:8074-8086.
69. Tsuboi M, Suzuki M, Overman SA, Thomas GJ. 2000. Intensity of the polarized Raman band at 1340-1345 cm(-1) as an indicator of protein alpha-helix orientation: application to Pf1 filamentous virus. Biochemistry 39:2677-2684.
70. Jarvis RM, Blanch EW, Golovanov AP, Screen J, Goodacre R. 2007. Quantification of casein phosphorylation with conformational interpretation using Raman spectroscopy. Analyst 132:1053-1060.
71. Sundararajan N, Mao DQ, Chan S, Koo TW, Su X, Sun L, Zhang JW, Sung KB, Yamakawa M, Gafken PR, Randolph T, McLerran D, Feng ZD, Berlin AA, Roth MB. 2006. Ultrasensitive detection and characterization of posttranslational modifications using surface-enhanced Raman spectroscopy. Anal. Chem. 78:3543-3550.
72. Kikuchi GE, Baker SA, Merajver SD, Coligan JE, Levine M, Glorioso JC, Nairn R. 1987. Purification and structural characterization of herpes simplex virus glycoprotein C. Biochemistry 26:424-431.
73. Negri P, Chen GJ, Kage A, Nitsche A, Naumann D, Xu BQ, Dluhy RA. 2012. Direct optical detection of viral nucleoprotein binding to an antiinfluenza aptamer. Anal. Chem. 84:5501-5508.
74. Negri P, Kage A, Nitsche A, Naumann D, Dluhy RA. 2011. Detection of viral nucleoprotein binding to anti-influenza aptamers via SERS. Chem. Commun. (Camb.) 47:8635- 8637.
75. Balakrishnan G, Weeks CL, Ibrahim M, Soldatova AV, Spiro TG. 2008. Protein dynamics from time resolved UV Raman spectroscopy. Curr. Opin. Struct. Biol. 18:623- 629.
76. Ashton L, Dusting J, Imomoh E, Balabani S, Blanch EW. 2010. Susceptibility of different proteins to flow-induced conformational changes monitored with Raman spectroscopy. Biophys. J. 98:707-714.
77. Lippert JL, Lindsay RM, Schultz R. 1981. Laser Raman characterization of conformational changes in sarcoplasmic reticulum induced by temperature, Ca2+, and Mg2+ J. Biol. Chem. 256:2411-2416.
78. Singhal K, Kalkan AK. 2010. Surface-enhanced Raman scattering captures conformational changes of single photoactive yellow protein molecules under photoexcitation. J. Am. Chem. Soc. 132:429-431.
79. Delrue I, Verzele D, Madder A, Nauwynck HJ. 2012. Inactivated virus vaccines from chemistry to prophylaxis: merits, risks and challenges. Expert Rev. Vaccines 11:695-719.
80. Van Reeth K, Ma W. Swine influenza virus vaccines: to change or not to change-that's the question. Curr. Top. Microbiol. Immunol., in press.