Identification of continuous human B-cell epitopes in the VP35, VP40, nucleoprotein and glycoprotein of ebola virus

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Becquart, Pierre ^a,b   Mahlakõiv, Tanel ^b   Nkoghe, Dieudonné ^b   Leroy, Eric M ^a,b  

^a INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^b CENTRE INTERNATIONAL DE RECHERCHES MÉDICALES DE FRANCEVILLE   (Gabon)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; IMMUNOGLOBULIN G; PROTEIN VP35; PROTEIN VP40; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; VIRUS NUCLEOPROTEIN; VIRUS PROTEIN; CORE PROTEIN; GLYCOPROTEIN; NUCLEOPROTEIN; NUCLEOPROTEIN VP35, EBOLA VIRUS; NUCLEOPROTEIN VP40, EBOLA VIRUS;

ADOLESCENT; ADULT; ANTIGEN ANTIBODY REACTION; ANTIGEN DETECTION; ANTIGEN SPECIFICITY; ARTICLE; ASYMPTOMATIC INFECTION; B LYMPHOCYTE; CHILD; CLINICAL FEATURE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISEASE COURSE; EBOLA VIRUS; EPIDEMIC; ETHNIC GROUP; GABON; GABONESE; HEMORRHAGIC FEVER; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNOREACTIVITY; MAJOR CLINICAL STUDY; NONHUMAN; PROTEIN DOMAIN; PROTEIN STRUCTURE; PROTEIN SUBUNIT; RESIDENTIAL HOME; RNA VIRUS INFECTION; SCHOOL CHILD; SEROLOGY; SERUM; SURVIVOR; SYMPTOM; VIRUS ASSEMBLY; VIRUS CELL INTERACTION; VIRUS RELEASE; AMINO ACID SEQUENCE; BLOOD; CHEMISTRY; EBOLAVIRUS; FEMALE; GENETICS; HEMORRHAGIC FEVER, EBOLA; IMMUNOLOGY; MALE; MOLECULAR GENETICS; SEROTYPE; VIROLOGY;

ADOLESCENT; ADULT; AMINO ACID SEQUENCE; B-LYMPHOCYTES; CHILD; DISEASE OUTBREAKS; EBOLAVIRUS; EPITOPES; FEMALE; GABON; GLYCOPROTEINS; HEMORRHAGIC FEVER, EBOLA; HUMANS; MALE; MOLECULAR SEQUENCE DATA; NUCLEOPROTEINS; SEROGROUP; VIRAL CORE PROTEINS;

EID: 84902590090     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096360     Document Type: Article

References (73)

1. Kuhn JH, Jahrling PB (2010) Clarification and guidance on the proper usage of virus and virus species names. Arch Virol 155: 445-453.
2. Feldmann H, Klenk HD, Sanchez A (1993) Molecular biology and evolution of filoviruses. Arch Virol Suppl 7: 81-100.
3. Sanchez A, Khan AS, Zaki S, Nabel GJ, Kziazeck TG, et al. (2001) Filoridae: Marburg and Ebola viruses. In: Knipe DS., Howley, P.M., Griffin, D.E., Lamb, R.A., Martin, M.A., Roizman, B., Straus, S.E., editor. Fields Virology Lippincott Williams and Wilkins, Philadelphia, PA. pp. 1279-1304.
4. (1978) Ebola haemorrhagic fever in Sudan, 1976. Report of a WHO/International Study Team. Bull World Health Organ 56: 247-270.
5. Khan AS, Tshioko FK, Heymann DL, Le Guenno B, Nabeth P, et al. (1999) The reemergence of Ebola hemorrhagic fever, Democratic Republic of the Congo, 1995. Commission de Lutte contre les Epidemies a Kikwit. J Infect Dis 179 Suppl 1: S76-86.
6. Georges AJ, Leroy EM, Renaut AA, Benissan CT, Nabias RJ, et al. (1999) Ebola hemorrhagic fever outbreaks in Gabon, 1994-1997: epidemiologic and health control issues. J Infect Dis 179 Suppl 1: S65-75. (Pubitemid 29091385)
7. Leroy EM, Rouquet P, Formenty P, Souquiere S, Kilbourne A, et al. (2004) Multiple Ebola virus transmission events and rapid decline of central African wildlife. Science 303: 387-390. (Pubitemid 38095781)
8. Leroy EM, Baize S, Volchkov VE, Fisher-Hoch SP, Georges-Courbot MC, et al. (2000) Human asymptomatic Ebola infection and strong inflammatory response. Lancet 355: 2210-2215. (Pubitemid 30394329)
9. Leroy EM, Baize S, Debre P, Lansoud-Soukate J, Mavoungou E (2001) Early immune responses accompanying human asymptomatic Ebola infections. Clin Exp Immunol 124: 453-460. (Pubitemid 32701707)
10. Baize S, Leroy EM, Georges AJ, Georges-Courbot MC, Capron M, et al. (2002) Inflammatory responses in Ebola virus-infected patients. Clin Exp Immunol 128: 163-168. (Pubitemid 34451194)
11. Bradfute SB, Warfield KL, Bavari S (2008) Functional CD8+ T cell responses in lethal Ebola virus infection. J Immunol 180: 4058-4066.
12. Baize S, Leroy EM, Georges-Courbot MC, Capron M, Lansoud-Soukate J, et al. (1999) Defective humoral responses and extensive intravascular apoptosis are associated with fatal outcome in Ebola virus-infected patients. Nat Med 5: 423-426. (Pubitemid 29180581)
13. Ksiazek TG, West CP, Rollin PE, Jahrling PB, Peters CJ (1999) ELISA for the detection of antibodies to Ebola viruses. J Infect Dis 179 Suppl 1: S192-198. (Pubitemid 29091402)
14. Onyango CO, Opoka ML, Ksiazek TG, Formenty P, Ahmed A, et al. (2007) Laboratory diagnosis of Ebola hemorrhagic fever during an outbreak in Yambio, Sudan, 2004. J Infect Dis 196 Suppl 2: S193-198. (Pubitemid 351417260)
15. Wauquier N, Becquart P, Gasquet C, Leroy EM (2009) Immunoglobulin G in Ebola outbreak survivors, Gabon. Emerg Infect Dis 15: 1136-1137.
16. Ksiazek TG, Rollin PE, Williams AJ, Bressler DS, Martin ML, et al. (1999) Clinical virology of Ebola hemorrhagic fever (EHF): virus, virus antigen, and IgG and IgM antibody findings among EHF patients in Kikwit, Democratic Republic of the Congo, 1995. J Infect Dis 179 Suppl 1: S177-187. (Pubitemid 29091400)
17. Becquart P, Wauquier N, Mahlakoiv T, Nkoghe D, Padilla C, et al. (2010) High prevalence of both humoral and cellular immunity to Zaire ebolavirus among rural populations in Gabon. PLoS One 5: e9126.
18. Maruyama T, Rodriguez LL, Jahrling PB, Sanchez A, Khan AS, et al. (1999) Ebola virus can be effectively neutralized by antibody produced in natural human infection. J Virol 73: 6024-6030. (Pubitemid 29274889)
19. Volchkov V, Volchkova V, Eckel C, Klenk HD, Bouloy M, et al. (1997) Emergence of subtype Zaire Ebola virus in Gabon. Virology 232: 139-144. (Pubitemid 27244471)
20. Leroy EM, Souquiere S, Rouquet P, Drevet D (2002) Re-emergence of ebola haemorrhagic fever in Gabon. Lancet 359: 712. (Pubitemid 34203784)
21. Lee JE, Fusco ML, Hessell AJ, Oswald WB, Burton DR, et al. (2008) Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor. Nature 454: 177-182. (Pubitemid 351969896)
22. Wilson JA, Hevey M, Bakken R, Guest S, Bray M, et al. (2000) Epitopes involved in antibody-mediated protection from Ebola virus. Science 287: 1664-1666. (Pubitemid 30127770)
23. Shahhosseini S, Das D, Qiu X, Feldmann H, Jones SM, et al. (2007) Production and characterization of monoclonal antibodies against different epitopes of Ebola virus antigens. J Virol Methods 143: 29-37. (Pubitemid 46802822)
24. Dye JM, Herbert AS, Kuehne AI, Barth JF, Muhammad MA, et al. (2012) Postexposure antibody prophylaxis protects nonhuman primates from filovirus disease. Proc Natl Acad Sci U S A 109: 5034-5039.
25. Elliott LH, Kiley MP, McCormick JB (1985) Descriptive analysis of Ebola virus proteins. Virology 147: 169-176. (Pubitemid 16200579)
26. Geisbert TW, Jahrling PB (1995) Differentiation of filoviruses by electron microscopy. Virus Res 39: 129-150. (Pubitemid 26054781)
27. Harty RN, Brown ME, Wang G, Huibregtse J, Hayes FP (2000) A PPxY motif within the VP40 protein of Ebola virus interacts physically and functionally with a ubiquitin ligase: implications for filovirus budding. Proc Natl Acad Sci U S A 97: 13871-13876.
28. Panchal RG, Ruthel G, Kenny TA, Kallstrom GH, Lane D, et al. (2003) In vivo oligomerization and raft localization of Ebola virus protein VP40 during vesicular budding. Proc Natl Acad Sci U S A 100: 15936-15941. (Pubitemid 38021093)
29. Johnson RF, Bell P, Harty RN (2006) Effect of Ebola virus proteins GP, NP and VP35 on VP40 VLP morphology. Virol J 3: 31.
30. Noda T, Sagara H, Suzuki E, Takada A, Kida H, et al. (2002) Ebola virus VP40 drives the formation of virus-like filamentous particles along with GP. J Virol 76: 4855-4865. (Pubitemid 34441691)
31. Dessen A, Forest E, Volchkov V, Dolnik O, Klenk HD, et al. (2000) Crystallization and preliminary X-ray analysis of the matrix protein from Ebola virus. Acta Crystallogr D Biol Crystallogr 56: 758-760. (Pubitemid 30392573)
32. Dessen A, Volchkov V, Dolnik O, Klenk HD, Weissenhorn W (2000) Crystal structure of the matrix protein VP40 from Ebola virus. EMBO J 19: 4228-4236. (Pubitemid 30623733)
33. Jasenosky LD, Neumann G, Lukashevich I, Kawaoka Y (2001) Ebola virus VP40-induced particle formation and association with the lipid bilayer. J Virol 75: 5205-5214. (Pubitemid 32448543)
34. Bornholdt ZA, Noda T, Abelson DM, Halfmann P, Wood MR, et al. (2013) Structural rearrangement of ebola virus VP40 begets multiple functions in the virus life cycle. Cell 154: 763-774.
35. Ruigrok RW, Schoehn G, Dessen A, Forest E, Volchkov V, et al. (2000) Structural characterization and membrane binding properties of the matrix protein VP40 of Ebola virus. J Mol Biol 300: 103-112.
36. Razumov IA, Belanov EF, Bukreev AA, Kazachinkskaia EI (1998) [Monoclonal antibodies to Marburg virus proteins and their immunochemical characteristics]. Vopr Virusol 43: 274-279.
37. Yang ZY, Duckers HJ, Sullivan NJ, Sanchez A, Nabel EG, et al. (2000) Identification of the Ebola virus glycoprotein as the main viral determinant of vascular cell cytotoxicity and injury. Nat Med 6: 886-889. (Pubitemid 30644746)
38. Feldmann H, Volchkov VE, Volchkova VA, Stroher U, Klenk HD (2001) Biosynthesis and role of filoviral glycoproteins. J Gen Virol 82: 2839-2848. (Pubitemid 33107496)
39. Yonezawa A, Cavrois M, Greene WC (2005) Studies of ebola virus glycoprotein-mediated entry and fusion by using pseudotyped human immunodeficiency virus type 1 virions: involvement of cytoskeletal proteins and enhancement by tumor necrosis factor alpha. J Virol 79: 918-926. (Pubitemid 40053875)
40. Takada A, Ebihara H, Feldmann H, Geisbert TW, Kawaoka Y (2007) Epitopes required for antibody-dependent enhancement of Ebola virus infection. J Infect Dis 196 Suppl 2: S347-356. (Pubitemid 351417281)
41. Takada A, Ebihara H, Jones S, Feldmann H, Kawaoka Y (2007) Protective efficacy of neutralizing antibodies against Ebola virus infection. Vaccine 25: 993-999. (Pubitemid 44937459)
42. Qiu X, Fernando L, Melito PL, Audet J, Feldmann H, et al. (2012) Ebola GP-specific monoclonal antibodies protect mice and guinea pigs from lethal Ebola virus infection. PLoS Negl Trop Dis 6: e1575.
43. Maruyama T, Parren PW, Sanchez A, Rensink I, Rodriguez LL, et al. (1999) Recombinant human monoclonal antibodies to Ebola virus. J Infect Dis 179 Suppl 1: S235-239. (Pubitemid 29091407)
44. Parren PW, Geisbert TW, Maruyama T, Jahrling PB, Burton DR (2002) Pre- and postexposure prophylaxis of Ebola virus infection in an animal model by passive transfer of a neutralizing human antibody. J Virol 76: 6408-6412. (Pubitemid 34556338)
45. Oswald WB, Geisbert TW, Davis KJ, Geisbert JB, Sullivan NJ, et al. (2007) Neutralizing antibody fails to impact the course of Ebola virus infection in monkeys. PLoS Pathog 3: e9.
46. Marzi A, Yoshida R, Miyamoto H, Ishijima M, Suzuki Y, et al. (2012) Protective efficacy of neutralizing monoclonal antibodies in a nonhuman primate model of Ebola hemorrhagic fever. PLoS One 7: e36192.
47. Sanchez A, Trappier SG, Mahy BW, Peters CJ, Nichol ST (1996) The virion glycoproteins of Ebola viruses are encoded in two reading frames and are expressed through transcriptional editing. Proc Natl Acad Sci U S A 93: 3602-3607. (Pubitemid 26125667)
48. Volchkov VE, Becker S, Volchkova VA, Ternovoj VA, Kotov AN, et al. (1995) GP mRNA of Ebola virus is edited by the Ebola virus polymerase and by T7 and vaccinia virus polymerases. Virology 214: 421-430.
49. Reynard O, Borowiak M, Volchkova VA, Delpeut S, Mateo M, et al. (2009) Ebolavirus glycoprotein GP masks both its own epitopes and the presence of cellular surface proteins. J Virol 83: 9596-9601.
50. Francica JR, Varela-Rohena A, Medvec A, Plesa G, Riley JL, et al. (2010) Steric shielding of surface epitopes and impaired immune recognition induced by the ebola virus glycoprotein. PLoS Pathog 6: e1001098.
51. Wang CC, Chen JR, Tseng YC, Hsu CH, Hung YF, et al. (2009) Glycans on influenza hemagglutinin affect receptor binding and immune response. Proc Natl Acad Sci U S A 106: 18137-18142.
52. Klenk HD, Feldmann H (2001) Symposium on Marburg and Ebola viruses. Virus Res 80: 117-123. (Pubitemid 32971950)
53. Olal D, Kuehne AI, Bale S, Halfmann P, Hashiguchi T, et al. (2012) Structure of an antibody in complex with its mucin domain linear epitope that is protective against Ebola virus. J Virol 86: 2809-2816.
54. Simmons G, Wool-Lewis RJ, Baribaud F, Netter RC, Bates P (2002) Ebola virus glycoproteins induce global surface protein down-modulation and loss of cell adherence. J Virol 76: 2518-2528. (Pubitemid 34150720)
55. Sullivan NJ, Peterson M, Yang ZY, Kong WP, Duckers H, et al. (2005) Ebola virus glycoprotein toxicity is mediated by a dynamin-dependent protein-trafficking pathway. J Virol 79: 547-553. (Pubitemid 39648407)
56. Manicassamy B, Wang J, Jiang H, Rong L (2005) Comprehensive analysis of ebola virus GP1 in viral entry. J Virol 79: 4793-4805. (Pubitemid 40464230)
57. Kaletsky RL, Simmons G, Bates P (2007) Proteolysis of the Ebola virus glycoproteins enhances virus binding and infectivity. J Virol 81: 13378-13384. (Pubitemid 350247834)
58. Francica JR, Matukonis MK, Bates P (2009) Requirements for cell rounding and surface protein down-regulation by Ebola virus glycoprotein. Virology 383: 237-247.
59. Dowling W, Thompson E, Badger C, Mellquist JL, Garrison AR, et al. (2007) Influences of glycosylation on antigenicity, immunogenicity, and protective efficacy of ebola virus GP DNA vaccines. J Virol 81: 1821-1837. (Pubitemid 46214455)
60. Kuhn JH, Radoshitzky SR, Guth AC, Warfield KL, Li W, et al. (2006) Conserved receptor-binding domains of Lake Victoria marburgvirus and Zaire ebolavirus bind a common receptor. J Biol Chem 281: 15951-15958. (Pubitemid 43848488)
61. Brindley MA, Hughes L, Ruiz A, McCray PB Jr., Sanchez A, et al. (2007) Ebola virus glycoprotein 1: identification of residues important for binding and postbinding events. J Virol 81: 7702-7709. (Pubitemid 47047855)
62. Changula K, Yoshida R, Noyori O, Marzi A, Miyamoto H, et al. (2013) Mapping of conserved and species-specific antibody epitopes on the Ebola virus nucleoprotein. Virus Res 176: 83-90.
63. Rowe AK, Bertolli J, Khan AS, Mukunu R, Muyembe-Tamfum JJ, et al. (1999) Clinical, virologic, and immunologic follow-up of convalescent Ebola hemorrhagic fever patients and their household contacts, Kikwit, Democratic Republic of the Congo. Commission de Lutte contre les Epidemies a Kikwit. J Infect Dis 179 Suppl 1: S28-35. (Pubitemid 29091380)
64. Sobarzo A, Groseth A, Dolnik O, Becker S, Lutwama JJ, et al. (2013) Profile and persistence of the virus-specific neutralizing humoral immune response in human survivors of Sudan ebolavirus (Gulu). J Infect Dis 208: 299-309.
65. Sobarzo A, Ochayon DE, Lutwama JJ, Balinandi S, Guttman O, et al. (2013) Persistent immune responses after Ebola virus infection. N Engl J Med 369: 492-493.
66. Frank R (2002) The SPOT-synthesis technique. Synthetic peptide arrays on membrane supports-principles and applications. J Immunol Methods 267: 13-26.
67. Barlow DJ, Edwards MS, Thornton JM (1986) Continuous and discontinuous protein antigenic determinants. Nature 322: 747-748. (Pubitemid 16074126)
68. Van Regenmortel MHV (1996) Mapping Epitope Structure and Activity: From One-Dimensional Prediction to Four-Dimensional Description of Antigenic Specificity. Methods 9: 465-472.
69. Toyoda H, Kumada T, Kiriyama S, Sone Y, Tanikawa M, et al. (2005) Changes in hepatitis C virus (HCV) antibody status in patients with chronic hepatitis C after eradication of HCV infection by interferon therapy. Clin Infect Dis 40: e49-54.
70. Linde A, Fridell E, Dahl H, Andersson J, Biberfeld P, et al. (1990) Effect of primary Epstein-Barr virus infection on human herpesvirus 6, cytomegalovirus, and measles virus immunoglobulin G titers. J Clin Microbiol 28: 211-215. (Pubitemid 20050922)
71. Georges-Courbot MC, Sanchez A, Lu CY, Baize S, Leroy E, et al. (1997) Isolation and phylogenetic characterization of Ebola viruses causing different outbreaks in Gabon. Emerg Infect Dis 3: 59-62. (Pubitemid 127433640)
72. Leroy EM, Baize S, Mavoungou E, Apetrei C (2002) Sequence analysis of the GP, NP, VP40 and VP24 genes of Ebola virus isolated from deceased, surviving and asymptomatically infected individuals during the 1996 outbreak in Gabon: comparative studies and phylogenetic characterization. J Gen Virol 83: 67-73. (Pubitemid 34030811)
73. Wittmann TJ, Biek R, Hassanin A, Rouquet P, Reed P, et al. (2007) Isolates of Zaire ebolavirus from wild apes reveal genetic lineage and recombinants. Proc Natl Acad Sci U S A 104: 17123-17127. (Pubitemid 350211002)