Probing the functions of the paramyxovirus glycoproteins F and HN with a panel of synthetic antibodies

Journal of Virology

Volumn 88, Issue 20, 2014, Pages 11713-11725

  Welch, Brett D ^a   Paduch, Marcin ^b   Leser, George P ^a   Bergman, Zachary ^a   Kors, Christopher A ^a   Paterson, Reay G ^a   Jardetzky, Theodore S ^c   Kossiakoff, Anthony A ^b   Lamb, Robert A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; SIALIDASE; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; VIRUS GLYCOPROTEIN F; VIRUS GLYCOPROTEIN HN; GLYCOPROTEIN; VIRUS ANTIGEN; VIRUS PROTEIN;

ANIMAL CELL; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; MOLECULAR RECOGNITION; NONHUMAN; PARAINFLUENZA VIRUS 5; PARAMYXOVIRUS; PEPTIDE LIBRARY; PHAGE DISPLAY; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; PROTEIN REFOLDING; RECEPTOR BINDING; SURFACE PLASMON RESONANCE; VIRUS CELL INTERACTION; VIRUS NEUTRALIZATION; WILD TYPE; ANIMAL; ANTIBODY SPECIFICITY; CELL LINE; ELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOLOGY; PARAMYXOVIRIDAE; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS;

ANIMALS; ANTIBODIES; ANTIBODY SPECIFICITY; ANTIGENS, VIRAL; CELL LINE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME-LINKED IMMUNOSORBENT ASSAY; GLYCOPROTEINS; HUMANS; MICROSCOPY, ELECTRON; PARAMYXOVIRIDAE; VIRAL PROTEINS;

EID: 84907432523     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01707-14     Document Type: Article

References (69)

1. Lamb RA, Parks GD. 2013. Paramyxoviridae: The viruses and their replication, p 957-995. Knipe DM, Howley PM, Cohen JI, Griffin DE, Lamb RA, Martin MA, Rancaniello VR, Roizman B (ed), Fields virology, 6th ed, vol 1. Lippincott Williams & Wilkins, Philadelphia, PA.
2. Bowden TA, Aricescu AR, Gilbert RJ, Grimes JM, Jones EY, Stuart DI. 2008. Structural basis of Nipah and Hendra virus attachment to their cell-surface receptor ephrin-B2. Nat. Struct. Mol. Biol. 15:567-572. http: //dx.doi.org/10.1038/nsmb.1435.
3. Colf LA, Juo ZS, Garcia KC. 2007. Structure of the measles virus hemagglutinin. Nat. Struct. Mol. Biol. 14:1227-1228. http://dx.doi.org/10.1038/nsmb1342.
4. Crennell S, Takimoto T, Portner A, Taylor G. 2000. Crystal structure of the multifunctional paramyxovirus hemagglutinin-neuraminidase. Nat. Struct. Biol. 7:1068-1074. http://dx.doi.org/10.1038/81002.
5. Hashiguchi T, Kajikawa M, Maita N, Takeda M, Kuroki K, Sasaki K, Kohda D, Yanagi Y, Maenaka K. 2007. Crystal structure of measles virus hemagglutinin provides insight into effective vaccines. Proc. Natl. Acad. Sci. U. S. A. 104:19535-19540. http://dx.doi.org/10.1073/pnas.0707830104.
6. Lawrence MC, Borg NA, Streltsov VA, Pilling PA, Epa VC, Varghese JN, McKimm-Breschkin JL, Colman PM. 2004. Structure of the haemagglutinin-neuraminidase from human parainfluenza virus type III. J. Mol. Biol. 335:1343-1357. http://dx.doi.org/10.1016/j.jmb.2003.11.032.
7. Xu K, Rajashankar KR, Chan YP, Himanen JP, Broder CC, Nikolov DB. 2008. Host cell recognition by the henipaviruses: crystal structures of the Nipah G attachment glycoprotein and its complex with ephrin-B3. Proc. Natl. Acad. Sci. U. S. A. 105:9953-9958. http://dx.doi.org/10.1073/pnas.0804797105.
8. Yuan P, Thompson T, Wurzburg BA, Paterson RG, Lamb RA, Jardetzky TS. 2005. Structural studies of the parainfluenza virus 5 hemagglutinin-neuraminidase tetramer in complex with its receptor, sialyllactose. Structure 13:803-815. http://dx.doi.org/10.1016/j.str.2005.02.019.
9. Bowden TA, Crispin M, Harvey DJ, Jones EY, Stuart DI. 2010. Dimeric architecture of the Hendra virus attachment glycoprotein: evidence for a conserved mode of assembly. J. Virol. 84:6208-6217. http://dx.doi.org/10.1128/JVI.00317-10.
10. Yuan P, Paterson RG, Leser GP, Lamb RA, Jardetzky TS. 2012. Structure of the Ulster strain Newcastle disease virus hemagglutininneuraminidase reveals auto-inhibitory interactions associated with low virulence. PLoS Pathog. 8:e1002855. http://dx.doi.org/10.1371/journal.ppat.1002855.
11. Santiago C, Celma ML, Stehle T, Casasnovas JM. 2010. Structure of the measles virus hemagglutinin bound to the CD46 receptor. Nat. Struct. Mol. Biol. 17:124-129. http://dx.doi.org/10.1038/nsmb.1726.
12. Yuan P, Swanson KA, Leser GP, Paterson RG, Lamb RA, Jardetzky TS. 2011. Structure of the Newcastle disease virus hemagglutininneuraminidase (HN) ectodomain reveals a four-helix bundle stalk. Proc. Natl. Acad. Sci. U. S. A. 108:14920-14925. http://dx.doi.org/10.1073/pnas.1111691108.
13. Bowden TA, Crispin M, Harvey DJ, Aricescu AR, Grimes JM, Jones EY, Stuart DI. 2008. Crystal structure and carbohydrate analysis of Nipah virus attachment glycoprotein: a template for antiviral and vaccine design. J. Virol. 82:11628-11636. http://dx.doi.org/10.1128/JVI.01344-08.
14. Yuan P, Leser GP, Demeler B, Lamb RA, Jardetzky TS. 2008. Domain architecture and oligomerization properties of the paramyxovirus PIV 5 hemagglutinin-neuraminidase (HN) protein. Virology 378:282-291. http://dx.doi.org/10.1016/j.virol.2008.05.023.
15. Ng DT, Hiebert SW, Lamb RA. 1990. Different roles of individual Nlinked oligosaccharide chains in folding, assembly, and transport of the simian virus 5 hemagglutinin-neuraminidase. Mol. Cell. Biol. 10:1989-2001.
16. Bossart KN, Crameri G, Dimitrov AS, Mungall BA, Feng YR, Patch JR, Choudhary A, Wang LF, Eaton BT, Broder CC. 2005. Receptor binding, fusion inhibition, and induction of cross-reactive neutralizing antibodies by a soluble G glycoprotein of Hendra virus. J. Virol. 79:6690-6702. http: //dx.doi.org/10.1128/JVI.79.11.6690-6702.2005.
17. Brindley MA, Plemper RK. 2010. Blue native PAGE and biomolecular complementation reveal a tetrameric or higher-order oligomer organization of the physiological measles virus attachment protein H. J. Virol. 84:12174-12184. http://dx.doi.org/10.1128/JVI.01222-10.
18. Bose S, Welch BD, Kors CA, Yuan P, Jardetzky TS, Lamb RA. 2011. Structure and mutagenesis of the parainfluenza virus 5 hemagglutinin-neuraminidase stalk domain reveals a four-helix bundle and the role of the stalk in fusion promotion. J. Virol. 85:12855-12866. http://dx.doi.org/10.1128/JVI.06350-11.
19. Bishop KA, Hickey AC, Khetawat D, Patch JR, Bossart KN, Zhu Z, Wang LF, Dimitrov DS, Broder CC. 2008. Residues in the stalk domain of the Hendra virus G glycoprotein modulate conformational changes associated with receptor binding. J. Virol. 82:11398-11409. http://dx.doi.org/10.1128/JVI.02654-07.
20. Deng R, Wang Z, Mirza AM, Iorio RM. 1995. Localization of a domain on the paramyxovirus attachment protein required for the promotion of cellular fusion by its homologous fusion protein spike. Virology 209:457-469. http://dx.doi.org/10.1006/viro.1995.1278.
21. Deng R, Wang Z, Mahon PJ, Marinello M, Mirza A, Iorio RM. 1999. Mutations in the Newcastle disease virus hemagglutinin-neuraminidase protein that interfere with its ability to interact with the homologous F protein in the promotion of fusion. Virology 253:43-54. http://dx.doi.org /10.1006/viro.1998.9501.
22. Melanson VR, Iorio RM. 2004. Amino acid substitutions in the F-specific domain in the stalk of the Newcastle disease virus HN protein modulate fusion and interfere with its interaction with the F protein. J. Virol. 78: 13053-13061. http://dx.doi.org/10.1128/JVI.78.23.13053-13061.2004.
23. Lee JK, Prussia A, Paal T, White LK, Snyder JP, Plemper RK. 2008. Functional interaction between paramyxovirus fusion and attachment proteins. J. Biol. Chem. 283:16561-16572. http://dx.doi.org/10.1074/jbc.M801018200.
24. Paal T, Brindley MA, St Clair C, Prussia A, Gaus D, Krumm SA, Snyder JP, Plemper RK. 2009. Probing the spatial organization of measles virus fusion complexes. J. Virol. 83:10480-10493. http://dx.doi.org/10.1128 /JVI.01195-09.
25. Stone-Hulslander J, Morrison TG. 1999. Mutational analysis of heptad repeats in the membrane-proximal region of Newcastle disease virus HN protein. J. Virol. 73:3630-3637.
26. Takimoto T, Taylor GL, Connaris HC, Crennell SJ, Portner A. 2002. Role of the hemagglutinin-neuraminidase protein in the mechanism of paramyxovirus-cell membrane fusion. J. Virol. 76:13028-13033. http://dx.doi.org/10.1128/JVI.76.24.13028-13033.2002.
27. Yao Q, Hu X, Compans RW. 1997. Association of the parainfluenza virus fusion and hemagglutinin-neuraminidase glycoproteins on cell surfaces. J. Virol. 71:650-656.
28. Plemper RK, Hammond AL, Gerlier D, Fielding AK, Cattaneo R. 2002. Strength of envelope protein interaction modulates cytopathicity of measles virus. J. Virol. 76:5051-5061. http://dx.doi.org/10.1128/JVI.76.10.5051-5061.2002.
29. 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.
30. Welch BD, Yuan P, Bose S, Kors CA, Lamb RA, Jardetzky TS. 2013. Structure of the parainfluenza virus 5 (PIV5) hemagglutininneuraminidase (HN) ectodomain. PLoS Pathog. 9:e1003534. http://dx.doi.org/10.1371/journal.ppat.1003534.
31. Harrison SC. 2008. Viral membrane fusion. Nat. Struct. Mol. Biol. 15: 690-698. http://dx.doi.org/10.1038/nsmb.1456.
32. Yin HS, Wen X, Paterson RG, Lamb RA, Jardetzky TS. 2006. Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature 439:38-44. http://dx.doi.org/10.1038/nature04322.
33. Welch BD, Liu Y, Kors CA, Leser GP, Jardetzky TS, Lamb RA. 2012. Structure of the cleavage-activated prefusion form of the parainfluenza virus 5 fusion protein. Proc. Natl. Acad. Sci. U. S. A. 109:16672-16677. http://dx.doi.org/10.1073/pnas.1213802109.
34. McLellan JS, Chen M, Leung S, Graepel KW, Du X, Yang Y, Zhou T, Baxa U, Yasuda E, Beaumont T, Kumar A, Modjarrad K, Zheng Z, Zhao M, Xia N, Kwong PD, Graham BS. 2013. Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Science 340:1113-1117. http://dx.doi.org/10.1126/science.1234914.
35. Wen X, Krause JC, Leser GP, Cox RG, Lamb RA, Williams JV, Crowe JE, Jr, Jardetzky TS. 2012. Structure of the human metapneumovirus fusion protein with neutralizing antibody identifies a pneumovirus antigenic site. Nat. Struct. Mol. Biol. 19:461-463. http://dx.doi.org/10.1038 /nsmb.2250.
36. Yin H-S, 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.
37. McLellan JS, Yang Y, Graham BS, Kwong PD. 2011. Structure of respiratory syncytial virus fusion glycoprotein in the postfusion conformation reveals preservation of neutralizing antigenic sites. J. Virol. 85:7788-7796. http://dx.doi.org/10.1128/JVI.00555-11.
38. Swanson K, Wen X, Leser GP, Paterson RG, Lamb RA, Jardetzky TS. 2010. Structure of the Newcastle disease virus F protein in the post-fusion conformation. Virology 402:372-379. http://dx.doi.org/10.1016/j.virol.2010.03.050.
39. Swanson KA, Settembre EC, Shaw CA, Dey AK, Rappuoli R, Mandl CW, Dormitzer PR, Carfi A. 2011. Structural basis for immunization with postfusion respiratory syncytial virus fusion F glycoprotein (RSV F) to elicit high neutralizing antibody titers. Proc. Natl. Acad. Sci. U. S. A. 108:9619-9624. http://dx.doi.org/10.1073/pnas.1106536108.
40. Kim YH, Donald JE, Grigoryan G, Leser GP, Fadeev AY, Lamb RA, DeGrado WF. 2011. Capture and imaging of a prehairpin fusion intermediate of the paramyxovirus PIV5. Proc. Natl. Acad. Sci. U. S. A. 108: 20992-20997. http://dx.doi.org/10.1073/pnas.1116034108.
41. Bose S, Zokarkar A, Welch BD, Leser GP, Jardetzky TS, Lamb RA. 2012. Fusion activation by a headless parainfluenza virus 5 hemagglutininneuraminidase stalk suggests a modular mechanism for triggering. Proc. Natl. Acad. Sci. U. S. A. 109:E2625-E2634. http://dx.doi.org/10.1073/pnas.1213813109.
42. Ader N, Brindley MA, Avila M, Origgi FC, Langedijk J, Orvell C, Vandevelde M, Zurbriggen A, Plemper RK, Plattet P. 2012. Structural rearrangements of the central region of the morbillivirus attachment protein stalk domain trigger F protein refolding for membrane fusion. J. Biol. Chem. 287:16324-16334. http://dx.doi.org/10.1074/jbc.M112.342493.
43. Navaratnarajah CK, Negi S, Braun W, Cattaneo R. 2012. Membrane fusion triggering: three modules with different structure and function in the upper half of the measles virus attachment protein stalk. J. Biol. Chem. 287:38543-38551. http://dx.doi.org/10.1074/jbc.M112.410563.
44. Navaratnarajah CK, Oezguen N, Rupp L, Kay L, Leonard VH, Braun W, Cattaneo R. 2011. The heads of the measles virus attachment protein move to transmit the fusion-triggering signal. Nat. Struct. Mol. Biol. 18: 128-134. http://dx.doi.org/10.1038/nsmb.1967.
45. Sugrue RJ, Bahadur G, Zambon MC, Hall-Smith M, Douglas AR, Hay AJ. 1990. Specific structural alteration of the influenza haemagglutinin by amantadine. EMBO J. 9:3469-3476.
46. Sanchez-San Martin C, Sosa H, Kielian M. 2008. A stable prefusion intermediate of the alphavirus fusion protein reveals critical features of class II membrane fusion. Cell Host Microbe 4:600-608. http://dx.doi.org /10.1016/j.chom.2008.10.012.
47. Waning DL, Russell CJ, Jardetzky TS, Lamb RA. 2004. Activation of a paramyxovirus fusion protein is modulated by inside-out signaling from the cytoplasmic tail. Proc. Natl. Acad. Sci. U. S. A. 101:9217-9222. http: //dx.doi.org/10.1073/pnas.0403339101.
48. Connolly SA, Leser GP, Yin HS, Jardetzky TS, Lamb RA. 2006. Refolding of a paramyxovirus F protein from prefusion to postfusion conformations observed by liposome binding and electron microscopy. Proc. Natl. Acad. Sci. U. S. A. 103:17903-17908. http://dx.doi.org/10.1073/pnas.0608678103.
49. Koide S, Sidhu SS. 2009. The importance of being tyrosine: lessons in molecular recognition from minimalist synthetic binding proteins. ACS Chem. Biol. 4:325-334. http://dx.doi.org/10.1021/cb800314v.
50. Koide A, Gilbreth RN, Esaki K, Tereshko V, Koide S. 2007. Highaffinity single-domain binding proteins with a binary-code interface. Proc. Natl. Acad. Sci. U. S. A. 104:6632-6637. http://dx.doi.org/10.1073/pnas.0700149104.
51. Fellouse FA, Barthelemy PA, Kelley RF, Sidhu SS. 2006. Tyrosine plays a dominant functional role in the paratope of a synthetic antibody derived from a four amino acid code. J. Mol. Biol. 357:100-114. http://dx.doi.org /10.1016/j.jmb.2005.11.092.
52. Fellouse FA, Esaki K, Birtalan S, Raptis D, Cancasci VJ, Koide A, Jhurani P, Vasser M, Wiesmann C, Kossiakoff AA, Koide S, Sidhu SS. 2007. High-throughput generation of synthetic antibodies from highly functional minimalist phage-displayed libraries. J. Mol. Biol. 373:924-940. http://dx.doi.org/10.1016/j.jmb.2007.08.005.
53. Koellhoffer JF, Chen G, Sandesara RG, Bale S, Saphire EO, Chandran K, Sidhu SS, Lai JR. 2012. Two synthetic antibodies that recognize and neutralize distinct proteolytic forms of the Ebola virus envelope glycoprotein. Chembiochem. 13:2549-2557. http://dx.doi.org/10.1002/cbic.201200493.
54. Paduch M, Koide A, Uysal S, Rizk SS, Koide S, Kossiakoff AA. 2013. Generating conformation-specific synthetic antibodies to trap proteins in selected functional states. Methods 60:3-14. http://dx.doi.org/10.1016/j.ymeth.2012.12.010.
55. Miller KR, Koide A, Leung B, Fitzsimmons J, Yoder B, Yuan H, Jay M, Sidhu SS, Koide S, Collins EJ. 2012. T cell receptor-like recognition of tumor in vivo by synthetic antibody fragment. PLoS One 7:e43746. http: //dx.doi.org/10.1371/journal.pone.0043746.
56. Tonikian R, Zhang Y, Boone C, Sidhu SS. 2007. Identifying specificity profiles for peptide recognition modules from phage-displayed peptide libraries. Nat. Protoc. 2:1368-1386. http://dx.doi.org/10.1038/nprot.2007.151.
57. Iorio RM, Bratt MA. 1983. Monoclonal antibodies to Newcastle disease virus: delineation of four antigenic sites on the HN glycoprotein. J. Virol. 48:440-450.
58. Iorio RM, Bratt MA. 1984. Monoclonal antibodies as functional probes of the HN glycoprotein of Newcastle disease virus: antigenic separation of the hemagglutinating and neuraminidase sites. J. Immunol. 133:2215-2219.
59. Iorio RM, Bratt MA. 1985. Selection of unique antigenic variants of Newcastle disease virus with neutralizing monoclonal antibodies and antiimmunoglobulin. Proc. Natl. Acad. Sci. U. S. A. 82:7106-7110. http://dx.doi.org/10.1073/pnas.82.20.7106.
60. Iorio RM, Lawton KA, Nicholson PM, Bratt MA. 1984. Monoclonal antibodies identify a strain-specific antigenic site on the HN glycoprotein of Newcastle disease virus strain Australia-Victoria. Virus Res. 1:513-525. http://dx.doi.org/10.1016/0168-1702(84)90009-1.
61. Randall RE, Young DF, Goswami KKA, Russell WC. 1987. Isolation and characterization of monoclonal antibodies to simian virus 5 and their use in revealing antigenic differences between human, canine and simian isolates. J. Gen. Virol. 68:2769-2780. http://dx.doi.org/10.1099/0022-1317-68-11-2769.
62. Bose S, Heath CM, Shah PA, Alayyoubi M, Jardetzky TS, Lamb RA. 2013. Mutations in the parainfluenza virus 5 fusion (F) protein reveal domains important for fusion triggering and metastability. J. Virol. 87: 13520-13531. http://dx.doi.org/10.1128/JVI.02123-13.
63. Bose S, Song AS, Jardetzky TS, Lamb RA. 2014. Fusion activation through attachment protein stalk domains indicates a conserved core mechanism of paramyxovirus entry into cells. J. Virol. 88:3925-3941. http://dx.doi.org/10.1128/JVI.03741-13.
64. 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.
65. Brindley MA, Takeda M, Plattet P, Plemper RK. 2012. Triggering the measles virus membrane fusion machinery. Proc. Natl. Acad. Sci. U. S. A. 109:E3018-E3027. http://dx.doi.org/10.1073/pnas.1210925109.
66. Liu Q, Stone JA, Bradel-Tretheway B, Dabundo J, Benavides-Montano JA, Santos-Montanez J, Biering SB, Nicola AV, Iorio RM, Lu X, Aguilar HC. 2013. Unraveling a three-step spatiotemporal mechanism of triggering of receptor-induced Nipah virus fusion and cell entry. PLoS Pathog. 9:e1003770. http://dx.doi.org/10.1371/journal.ppat.1003770.
67. Brindley MA, Suter R, Schestak I, Kiss G, Wright ER, Plemper RK. 2013. A stabilized headless measles virus attachment protein stalk efficiently triggers membrane fusion. J. Virol. 87:11693-11703. http://dx.doi.org/10.1128/JVI.01945-13.
68. Yuasa T, Kawano M, Tabata N, Nishio M, Kusagawa S, Komada H, Matsumura H, Ito Y, Tsurudome M. 1995. A cell fusion-inhibiting monoclonal antibody binds to the presumed stalk domain of the human parainfluenza type 2 virus hemagglutinin-neuraminidase protein. Virology 206:1117-1125. http://dx.doi.org/10.1006/viro.1995.1035.
69. Bimanns S, Rusu M, Wriggers W. 2011. Using Sculptor and Situs for simultaneous assembly of atomic components into low-resolution shapes. J. Struct. Biol. 173:428-435. http://dx.doi.org/10.1016/j.jsb.2010.11.002.