Differences in glycoprotein complex receptor binding site accessibility prompt poor cross-reactivity of neutralizing antibodies between closely related arenaviruses

Journal of Virology

Volumn 91, Issue 7, 2017, Pages

  Brouillette, Rachel B ^a   Phillips, Elisabeth K ^a   Ayithan, Natarajan ^a   Maury, Wendy ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Arenavirus; Clade B viruses; Glycoprotein; GPC; Jun n virus; Machupo virus; Neutralizing antibodies; New World arenavirus

Indexed keywords

CHIMERIC PROTEIN; EPITOPE; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG; VIRUS ANTIBODY; VIRUS GLYCOPROTEIN; VIRUS GLYCOPROTEIN 1; NEUTRALIZING ANTIBODY; PROTEIN BINDING; VIRUS ANTIGEN; VIRUS FUSION PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CONTROLLED STUDY; CROSS REACTION; FEMALE; JUNIN VIRUS; MACHUPO VIRUS; MOUSE; NEW WORLD ARENAVIRUS; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; SEQUENCE ANALYSIS; VIRION; VIRUS INTERFERENCE; VIRUS NEUTRALIZATION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CHLOROCEBUS AETHIOPS; COMPARATIVE STUDY; HEK293 CELL LINE; HUMAN; IMMUNOLOGY; SPECIES DIFFERENCE; VERO CELL LINE;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; BINDING SITES; CERCOPITHECUS AETHIOPS; CROSS REACTIONS; HEK293 CELLS; HUMANS; JUNIN VIRUS; MICE; PROTEIN BINDING; SPECIES SPECIFICITY; VERO CELLS; VIRAL FUSION PROTEINS;

EID: 85015248230     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01454-16     Document Type: Article

References (49)

1. Irwin NR, Bayerlova M, Missa O, Martinkova N. 2012. Complex patterns of host switching in New World arenaviruses. Mol Ecol 21:4137-4150. https://doi.org/10.1111/j.1365-294X.2012.05663.x.
2. Wulff H, Lange JV, Webb PA. 1978. Interrelationships among arenaviruses measured by indirect immunofluorescence. Intervirology 9:344-350. https://doi.org/10.1159/000148956.
3. Radoshitzky SR, Bao Y, Buchmeier MJ, Charrel RN, Clawson AN, Clegg CS, DeRisi JL, Emonet S, Gonzalez JP, Kuhn JH, Lukashevich IS, Peters CJ, Romanowski V, Salvato MS, Stenglein MD, de la Torre JC. 2015. Past, present, and future of arenavirus taxonomy. Arch Virol 160:1851-1874. https://doi.org/10.1007/s00705-015-2418-y.
4. Wang W, Zhou Z, Zhang L, Wang S, Xiao G. 2016. Structure-function relationship of the mammarenavirus envelope glycoprotein. Virol Sin 31:380-394. https://doi.org/10.1007/s12250-016-3815-4.
5. Casals J, Buckley SM, Cedeno R. 1975. Antigenic properties of the arenaviruses. Bull World Health Organ 52:421-427.
6. Gschwender H, Lehmann-Grube F. 1973. Antigenic properties of the LCM virus: virion and complement-fixing antigen, p 25-35. In Lymphocytic choriomeningitis virus and other arenaviruses. Springer, Berlin, Germany.
7. Buchmeier MJ, Gee SR, Rawls WE. 1977. Antigens of Pichinde virus. I. Relationship of soluble antigens derived from infected BHK-21 cells to the structural components of the virion. J Virol 22:175-186.
8. Cresta B, Padula P, de Martinez Segovia M. 1980. Biological properties of Junin virus proteins. I. Identification of the immunogenic glycoprotein. Intervirology 13:284-288.
9. Buchmeier MJ, Lewicki HA, Tomori O, Oldstone MBA. 1981. Monoclonal antibodies to lymphocytic choriomeningitis and pichinde viruses: Generation, characterization, and cross-reactivity with other arenaviruses. Virology 113:73-85. https://doi.org/10.1016/0042-6822(81)90137-9.
10. Bruno-Lobo GG, Bruno-Lobo M, Johnson KM, Webb PA, de Paola D. 1968. Pathogenesis of Junin virus infection in the infant hamster. An Microbiol 15:11-33.
11. Rowe WP, Pugh WE, Webb PA, Peters CJ. 1970. Serological relationship of the Tacaribe complex of viruses to lymphocytic choriomeningitis virus. J Virol 5:289-292.
12. Johnson KM, Webb PA, Justines G. 1973. Biology of TaCaribe-complex viruses, p 241-258. In Lehmann-Grube F (ed), Lymphocytic choriomeningitis virus and other arenaviruses: symposium held at the Heinrich-Pette-Institut für Experimentelle Virologie und Immunologie, Universität Hamburg, October 16-18. Springer, Berlin, Germany.
13. Casals J. 1975. Arenaviruses. Yale J Biol Med 48:115-140.
14. Calisher CH, Tzianabos T, Lord RD, Coleman PH. 1970. Tamiami virus, a new member of the TaCaribe group. Am J Trop Med Hyg 19:520-526.
15. Johnson KM, Halstead SB, Cohen SN. 1967. Hemorrhagic fevers of Southeast Asia and South America: a comparative appraisal. Prog Med Virol 9:105-158.
16. Berge TO. 1975. International catalogue of arboviruses. U.S. Department of Health, Education, and Welfare, Washington, DC.
17. Trapido H, Sanmartin C. 1971. Pichinde virus, a new virus of the Tacaribe group from Colombia. Am J Trop Med Hyg 20:631-641.
18. Buckley SM, Casals J. 1970. Lassa fever, a new virus disease of man from West Africa. III. Isolation and characterization of the virus. Am J Trop Med Hyg 19:680-691.
19. Dutko F, Pfau C. 1978. Arenavirus defective interfering particles mask the cell-killing potential of standard virus. J Gen Virol 38:195-208. https://doi.org/10.1099/0022-1317-38-2-195.
20. Monath TP. 1973. Lassa fever. Trop Doctor 3:155-161. https://doi.org/10.1177/004947557300300404.
21. Sengupta S, Rawls WE. 1979. Pseudotypes of vesicular stomatitis virus and Pichinde virus. J Gen Virol 42:141-148. https://doi.org/10.1099/0022-1317-42-1-141.
22. Howard CR, Lewicki H, Allison L, Salter M, Buchmeier MJ. 1985. Properties and characterization of monoclonal antibodies to Tacaribe virus. J Gen Virol 66(Pt 7):1383-1395. https://doi.org/10.1099/0022-1317-66-7-1383.
23. Smadel JE, Wall MJ. 1940. A soluble antigen of lymphocytic choriomeningitis. II. Independence of anti-soluble substance antibodies and neutralizing antibodies, and the role of soluble antigen and inactive virus in immunity to infection. J Exp Med 72:389-405.
24. Rutter G, Gschwender H. 1973. Antigenic alteration of cells in vitro infected with LCM virus, p 51-59. In Lymphocytic choriomeningitis virus and other arenaviruses. Springer, Berlin, Germany.
25. Abraham J, Corbett KD, Farzan M, Choe H, Harrison SC. 2010. Structural basis for receptor recognition by New World hemorrhagic fever arenaviruses. Nat Struct Mol Biol 17:438-444. https://doi.org/10.1038/nsmb.1772.
26. Mahmutovic S, Clark L, Levis SC, Briggiler AM, Enria DA, Harrison SC, Abraham J. 2015. Molecular basis for antibody-mediated neutralization of New World hemorrhagic fever mammarenaviruses. Cell Host Microbe 18:705-713. https://doi.org/10.1016/j.chom.2015.11.005.
27. Radoshitzky SR, Abraham J, Spiropoulou CF, Kuhn JH, Nguyen D, Li W, Nagel J, Schmidt PJ, Nunberg JH, Andrews NC, Farzan M, Choe H. 2007. Transferrin receptor 1 is a cellular receptor for New World haemorrhagic fever arenaviruses. Nature 446:92-96. https://doi.org/10.1038/nature05539.
28. Schmidt AG, Therkelsen MD, Stewart S, Kepler TB, Liao HX, Moody MA, Haynes BF, Harrison SC. 2015. Viral receptor-binding site antibodies with diverse germline origins. Cell 161:1026-1034. https://doi.org/10.1016/j.cell.2015.04.028.
29. Xu R, Krause JC, McBride R, Paulson JC, Crowe JE, Jr, Wilson IA. 2013. A recurring motif for antibody recognition of the receptor-binding site of influenza hemagglutinin. Nat Struct Mol Biol 20:363-370. https://doi.org/10.1038/nsmb.2500.
30. Scheid JF, Mouquet H, Ueberheide B, Diskin R, Klein F, Oliveira TY, Pietzsch J, Fenyo D, Abadir A, Velinzon K, Hurley A, Myung S, Boulad F, Poignard P, Burton DR, Pereyra F, Ho DD, Walker BD, Seaman MS, Bjorkman PJ, Chait BT, Nussenzweig MC. 2011. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333:1633-1637. https://doi.org/10.1126/science.1207227.
31. Zhou T, Georgiev I, Wu X, Yang ZY, Dai K, Finzi A, Kwon YD, Scheid JF, Shi W, Xu L, Yang Y, Zhu J, Nussenzweig MC, Sodroski J, Shapiro L, Nabel GJ, Mascola JR, Kwong PD. 2010. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329:811-817. https://doi.org/10.1126/science.1192819.
32. Chen Z, Fischer ER, Kouiavskaia D, Hansen BT, Ludtke SJ, Bidzhieva B, Makiya M, Agulto L, Purcell RH, Chumakov K. 2013. Cross-neutralizing human anti-poliovirus antibodies bind the recognition site for cellular receptor. Proc Natl Acad Sci U S A 110:20242-20247. https://doi.org/10.1073/pnas.1320041110.
33. Takada A, Robison C, Goto H, Sanchez A, Murti KG, Whitt MA, Kawaoka Y. 1997. A system for functional analysis of Ebola virus glycoprotein. Proc Natl Acad Sci U S A 94:14764-14769. https://doi.org/10.1073/pnas .94.26.14764.
34. Iha K. 2013. Pseudotyped vesicular stomatitis virus for analysis of entry of arenaviruses and its application to serodiagnosis of Argentine hemorrhagic fever. PhD dissertation. University of Tokyo, Tokyo, Japan.
35. Golden JW, Maes P, Kwilas SA, Ballantyne J, Hooper JW. 2016. Glycoprotein-specific antibodies produced by DNA vaccination protect guinea pigs from lethal Argentine and Venezuelan hemorrhagic fever. J Virol 90:3515-3529. https://doi.org/10.1128/JVI.02969-15.
36. Sanchez A, Pifat DY, Kenyon RH, Peters CJ, McCormick JB, Kiley MP. 1989. Junin virus monoclonal antibodies: characterization and cross-reactivity with other arenaviruses. J Gen Virol 70:1125-1132. https://doi.org/10.1099/0022-1317-70-5-1125.
37. Zeitlin L, Geisbert JB, Deer DJ, Fenton KA, Bohorov O, Bohorova N, Goodman C, Kim D, Hiatt A, Pauly MH, Velasco J, Whaley KJ, Altmann F, Gruber C, Steinkellner H, Honko AN, Kuehne AI, Aman MJ, Sahandi S, Enterlein S, Zhan X, Enria D, Geisbert TW. 2016. Monoclonal antibody therapy for Junin virus infection. Proc Natl Acad Sci U S A 113: 4458-4463. https://doi.org/10.1073/pnas.1600996113.
38. York J, Berry JD, Stroher U, Li Q, Feldmann H, Lu M, Trahey M, Nunberg JH. 2010. An antibody directed against the fusion peptide of Junin virus envelope glycoprotein GPC inhibits pH-induced membrane fusion. J Virol 84:6119-6129. https://doi.org/10.1128/JVI.02700-09.
39. York J, Romanowski V, Lu M, Nunberg JH. 2004. The signal peptide of the Junin arenavirus envelope glycoprotein is myristoylated and forms an essential subunit of the mature G1-G2 complex. J Virol 78:10783-10792. https://doi.org/10.1128/JVI.78.19.10783-10792.2004.
40. Purtscher M, Trkola A, Gruber G, Buchacher A, Predl R, Steindl F, Tauer C, Berger R, Barrett N, Jungbauer A, Katinger H. 1994. A broadly neutralizing human monoclonal antibody against gp41 of human immunodeficiency virus type 1. AIDS Res Hum Retroviruses 10:1651-1658. https://doi.org/10.1089/aid.1994.10.1651.
41. Gorny MK, Zolla-Pazner S. 2000. Recognition by human monoclonal antibodies of free and complexed peptides representing the prefusogenic and fusogenic forms of human immunodeficiency virus type 1 gp41. J Virol 74:6186-6192. https://doi.org/10.1128/JVI.74.13.6186-6192.2000.
42. Martin VK, Droniou-Bonzom ME, Reignier T, Oldenburg JE, Cox AU, Cannon PM. 2010. Investigation of clade B New World arenavirus tropism by using chimeric GP1 proteins. J Virol 84:1176-1182. https://doi.org/10.1128/JVI.01625-09.
43. Albarino CG, Bird BH, Chakrabarti AK, Dodd KA, Flint M, Bergeron E, White DM, Nichol ST. 2011. The major determinant of attenuation in mice of the Candid1 vaccine for Argentine hemorrhagic fever is located in the G2 glycoprotein transmembrane domain. J Virol 85:10404-10408. https://doi.org/10.1128/JVI.00856-11.
44. Coughlin MM, Prabhakar BS. 2012. Neutralizing human monoclonal antibodies to severe acute respiratory syndrome coronavirus: target, mechanism of action, and therapeutic potential. Rev Med Virol 22:2-17. https://doi.org/10.1002/rmv.706.
45. Dias JM, Kuehne AI, Abelson DM, Bale S, Wong AC, Halfmann P, Muhammad MA, Fusco ML, Zak SE, Kang E, Kawaoka Y, Chandran K, Dye JM, Saphire EO. 2011. A shared structural solution for neutralizing ebolaviruses. Nat Struct Mol Biol 18:1424-1427. https://doi.org/10.1038/nsmb.2150.
46. Bale S, Dias J, Fusco M, Hashiguchi T, Wong A, Liu T, Keuhne A, Li S, Woods V, Chandran K. 2012. Structural basis for differential neutralization of ebolaviruses. Viruses 4:447-470. https://doi.org/10.3390/v4040447.
47. Bruns M, Cihak J, Muller G, Lehmann-Grube F. 1983. Lymphocytic choriomeningitis virus. VI. Isolation of a glycoprotein mediating neutralization. Virology 130:247-251.
48. Parekh BS, Buchmeier MJ. 1986. Proteins of lymphocytic choriomeningitis virus: antigenic topography of the viral glycoproteins. Virology 153:168-178. https://doi.org/10.1016/0042-6822(86)90020-6.
49. Ruo S, Mitchell S, Kiley M, Roumillat L, Fisher-Hoch S, McCormick J. 1991. Antigenic relatedness between arenaviruses defined at the epitope level by monoclonal antibodies. J Gen Virol 72:549-555. https://doi.org/10.1099/0022-1317-72-3-549.