Protective antiviral antibodies that lack neutralizing activity: Precedents and evolution of concepts

Current HIV Research

Volumn 11, Issue 5, 2013, Pages 345-353

  Schmaljohn, Alan L ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

ADCC; Antibody; Non neutralizing antibodies; Passive immunity; Virus

Indexed keywords

EPITOPE; GLYCOPROTEIN E1; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; IMMUNOGLOBULIN CLASS; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G3; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; NONSTRUCTURAL PROTEIN 1; PALIVIZUMAB; POLYCLONAL ANTIBODY; PROTECTIVE NON NEUTRALIZING ANTIBODY; PROTEIN A33R; PROTEIN L1R; SUBUNIT VACCINE; UNCLASSIFIED DRUG; VACCINIA GROWTH FACTOR; VIRUS ANTIBODY; VIRUS ANTIGEN; VIRUS PROTEIN;

ALPHA VIRUS; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; COMPLEMENT DEPENDENT CYTOTOXICITY; CYTOMEGALOVIRUS; EBOLA VIRUS; FLAVIVIRUS; HUMAN IMMUNODEFICIENCY VIRUS; INFLUENZA VIRUS; META ANALYSIS (TOPIC); PASSIVE IMMUNIZATION; POXVIRUS; RESPIRATORY SYNCYTIAL VIRUS INFECTION; SINDBIS VIRUS; VACCINIA VIRUS; VESICULAR STOMATITIS VIRUS; VIRION; VIRUS INFECTION; VIRUS NEUTRALIZATION; VIRUS RESISTANCE; WEST NILE FLAVIVIRUS; YELLOW FEVER FLAVIVIRUS;

ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; HUMANS; IMMUNITY, INNATE; VIRAL VACCINES; VIRUS DISEASES;

EID: 84888990148     PISSN: 1570162X     EISSN: 18734251     Source Type: Journal    
DOI: 10.2174/1570162X113116660057     Document Type: Article

References (65)

1. Beers SA, Chan CHT, French RR, Cragg MS, Glennie MJ. CD20 as a Target for Therapeutic Type I and II Monoclonal Antibodies. Semin Hematol 2010; 47(2): 107-14.
2. Golay J, Introna M. Mechanism of action of therapeutic monoclonal antibodies: Promises and pitfalls of in vitro and in vivo assays. Arch Biochem Biophys 2012; 526(2): 146-53.
3. Dimitrov DS, Marks JD. Therapeutic Antibodies: Current State and Future Trends-Is a Paradigm Change Coming Soon? Methods Mol Biol Clifton Nj 2009; 525: 1-27.
4. Burnett JC, Henchal EA, Schmaljohn AL, Bavari S. The evolving field of biodefence: therapeutic developments and diagnostics. Nat Rev Drug Discov 2005; 4(4): 281-97.
5. Webster RG, Brown LE, Laver WG. Antigenic and biological characterization of influenza virus neuraminidase (N2) with monoclonal antibodies. Virology 1984; 135(1): 30-42.
6. Dimmock NJ. Mechanisms of Neutralization of Animal Viruses. J Gen Virol 1984; 65(6): 1015-22.
7. Hangartner L, Zinkernagel RM, Hengartner H. Antiviral antibody responses: the two extremes of a wide spectrum. Nat Rev 2006; 6(3): 231-43.
8. Reading SA, Dimmock NJ. Neutralization of animal virus infectivity by antibody. Arch Virol 2007; 152(6): 1047-59.
9. Peiris JSM, Gordon S, Unkeless JC, Porterfield JS. Monoclonal anti-Fc receptor IgG blocks antibody enhancement of viral replication in macrophages. Nature 1981; 289(5794): 189-91.
10. Zinkernagel RM, Althage A. Antiviral protection by virus-immune cytotoxic T cells: infected target cells are lysed before infectious virus progeny is assembled. J Exp Med 1977; 145(3): 644-51.
11. Sissons JGP, Oldstone MBA. Antibody-Mediated Destruction of Virus-Infected Cells. In: Henry G. Kunkel and Frank J. Dixon, editor. Adv. Immunol. [Internet]. Academic Press; 1980 [cited 2013 Apr 18]. p. 209-60. Available from: http://www. sciencedir ect. com/science/article/pii/S0065277608600450.
12. Appleyard G, Hapel AJ, Boulter EA. An Antigenic Difference between Intracellular and Extracellular Rabbitpox Virus. J Gen Virol 1971; 13(1): 9-17.
13. Griffin DE, Johnson RT. Role of the Immune Response in Recovery from Sindbis Virus Encephalitis in Mice. J Immunol 1977; 118(3): 1070-5.
14. Perrin LH, Zinkernagel RM, Oldstone MBA. Immune response in humans after vaccination with vaccinia virus: generation of a virusspecific cytotoxic activity by human peripheral lymphocytes. J Exp Med 1977; 146(4): 949-69.
15. Köhler G, Milstein C. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 1975; 256(5517): 495-7.
16. Koprowski H, Gerhard W, Croce CM. Production of antibodies against influenza virus by somatic cell hybrids between mouse myeloma and primed spleen cells. Proc Natl Acad Sci USA 1977; 74(7): 2985-8.
17. Yewdell JW, Webster RG, Gerhard WU. Antigenic variation in three distinct determinants of an influenza type A haemagglutinin molecule. Nature 1979; 279(5710): 246-8.
18. Lefrancois L, Lyles DS. The interaction of antibody with the major surface glycoprotein of vesicular stornatitis virus II. Monoclonal antibodies to nonneutralizing and cross-reactive epitopes of Indiana and New Jersey serotypes. Virology 1982; 121(1): 168-74.
19. Mathews JH, Roehrig JT. Determination of the protective epitopes on the glycoproteins of Venezuelan equine encephalomyelitis virus by passive transfer of monoclonal antibodies. J Immunol 1982; 129(6): 2763-7.
20. Schmaljohn AL, Johnson ED, Dalrymple JM, Cole GA. Nonneutralizing monoclonal antibodies can prevent lethal alphavirus encephalitis. Nature 1982; 297(5861): 70-2.
21. Dalrymple JM, Schlesinger S, Russell PK. Antigenic characterization of two Sindbis envelope glycoproteins separated by isoelectric focusing. Virology 1976; 69(1): 93-103.
22. Gould EA, Buckley A, Barrett ADT, Cammack N. Neutralizing (54K) and Non-neutralizing (54K and 48K) Monoclonal Antibodies against Structural and Non-structural Yellow Fever Virus Proteins Confer Immunity in Mice. J Gen Virol 1986; 67(3): 591-5.
23. Schlesinger JJ, Brandriss MW, Walsh EE. Protection against 17D yellow fever encephalitis in mice by passive transfer of monoclonal antibodies to the nonstructural glycoprotein gp48 and by active immunization with gp48. J Immunol 1985; 135(4): 2805-9.
24. Lefrancois L. Protection against lethal viral infection by neutralizing and nonneutralizing monoclonal antibodies: distinct mechanisms of action in vivo. J Virol 1984; 51(1): 208-14.
25. Cohen ME, Xiao Y, Eisenberg RJ, Cohen GH, Isaacs SN. Antibody against Extracellular Vaccinia Virus (EV) Protects Mice through Complement and Fc Receptors. PloS One 2011; 6(6): e20597.
26. Kim M, Yang H, Kim S-K, et al. Biochemical and Functional Analysis of Smallpox Growth Factor (SPGF) and Anti-SPGF Monoclonal Antibodies. J Biol Chem 2004; 279(24): 25838-48.
27. Hooper JW, Custer DM, Schmaljohn CS, Schmaljohn AL. DNA vaccination with vaccinia virus L1R and A33R genes protects mice against a lethal poxvirus challenge. Virology 2000; 266(2): 329-39.
28. Carragher DM, Kaminski DA, Moquin A, Hartson L, Randall TD. A Novel Role for Non-Neutralizing Antibodies against Nucleoprotein in Facilitating Resistance to Influenza Virus. J Immunol 2008; 181(6): 4168-76.
29. Wilson JA, Hevey M, Bakken R, et al. Epitopes involved in antibody-mediated protection from Ebola virus. Science 2000; 287(5458): 1664-6.
30. Chung KM, Thompson BS, Fremont DH, Diamond MS. Antibody recognition of cell surface-associated NS1 triggers Fc-gamma receptor-mediated phagocytosis and clearance of West Nile Virusinfected cells. J Virol 2007; 81(17): 9551-5.
31. Iacono-Connors LC, Smith JF, Ksiazek TG, Kelley CL, Schmaljohn CS. Characterization of Langat virus antigenic determinants defined by monoclonal antibodies to E, NS1 and preM and identification of a protective, non-neutralizing preMspecific monoclonal antibody. Virus Res 1996; 43(2): 125-36.
32. Guan Y, Pazgier M, Sajadi MM, et al. Diverse specificity and effector function among human antibodies to HIV-1 envelope glycoprotein epitopes exposed by CD4 binding. Proc Natl Acad Sci USA 2013; 110(1): E69-E78.
33. Haynes BF, Gilbert PB, McElrath MJ, et al. Immune-Correlates Analysis of an HIV-1 Vaccine Efficacy Trial. N Engl J Med 2012; 366(14): 1275-86.
34. Schlesinger JJ, Chapman S. Neutralizing F(ab)2 fragments of protective monoclonal antibodies to yellow fever virus (YF) envelope protein fail to protect mice against lethal YF encephalitis. J Gen Virol 1995; 76(1): 217-20.
35. Lefrancois L. Protection against lethal viral infection by neutralizing and nonneutralizing monoclonal antibodies: distinct mechanisms of action in vivo. J Virol 1984; 51(1): 208-14.
36. Schmaljohn AL, Kokubun KM, Cole GA. Protective monoclonal antibodies define maturational and pH-dependent antigenic changes in Sindbis virus E1 glycoprotein. Virology 1983; 130(1): 144-54.
37. Hernandez R, Paredes A. Sindbis virus as a model for studies of conformational changes in a metastable virus and the role of conformational changes in in vitro antibody neutralisation. Rev Med Virol 2009; 19(5): 257-72.
38. Parker MD, Buckley MJ, Melanson VR, Glass PJ, Norwood D, Hart MK. Antibody to the E3 glycoprotein protects mice against lethal venezuelan equine encephalitis virus infection. J Virol 2010; 84(24): 12683-90.
39. Brecher M, Schornberg KL, Delos SE, Fusco ML, Saphire EO, White JM. Cathepsin Cleavage Potentiates the Ebola Virus Glycoprotein To Undergo a Subsequent Fusion-Relevant Conformational Change. J Virol 2012; 86(1): 364-72.
40. Laliberte JP, Weisberg AS, Moss B. The Membrane Fusion Step of Vaccinia Virus Entry Is Cooperatively Mediated by Multiple Viral Proteins and Host Cell Components. PloS Pathog 2011; 7(12): e1002446.
41. Hooper JW, Thompson E, Wilhelmsen C, et al. Smallpox DNA vaccine protects nonhuman primates against lethal monkeypox. J Virol 2004; 78(9): 4433-43.
42. Galmiche MC, Goenaga J, Wittek R, Rindisbacher L. Neutralizing and Protective Antibodies Directed against Vaccinia Virus Envelope Antigens. Virology 1999; 254(1): 71-80.
43. Moss B. Smallpox vaccines: targets of protective immunity. Immunol Rev 2011; 239(1): 8-26.
44. Lustig S, Fogg C, Whitbeck JC, Eisenberg RJ, Cohen GH, Moss B. Combinations of Polyclonal or Monoclonal Antibodies to Proteins of the Outer Membranes of the Two Infectious Forms of Vaccinia Virus Protect Mice against a Lethal Respiratory Challenge. J Virol 2005; 79(21): 13454-62.
45. Wilson JA, Hevey M, Bakken R, et al. Epitopes involved in antibody-mediated protection from Ebola virus. Science 2000; 287(5458): 1664-6.
46. Stec DS, Waddell A, Schmaljohn CS, Cole GA, Schmaljohn AL. Antibody-selected variation and reversion in Sindbis virus neutralization epitopes. J Virol 1986; 57(3): 715-20.
47. Vogt MR, Dowd KA, Engle M, et al. Poorly Neutralizing Cross-Reactive Antibodies against the Fusion Loop of West Nile Virus Envelope Protein Protect In Vivo via Fcγ Receptor and Complement-Dependent Effector Mechanisms. J Virol 2011; 85(22): 11567-80.
48. Burton DR, Poignard P, Stanfield RL, Wilson IA. Broadly Neutralizing Antibodies Present New Prospects to Counter Highly Antigenically Diverse Viruses. Science 2012; 337(6091): 183-6.
49. Su H-P, Golden JW, Gittis AG, Hooper JW, Garboczi DN. Structural basis for the binding of the neutralizing antibody, 7D11, to the poxvirus L1 protein. Virology 2007; 368(2): 331-41.
50. Sylte MJ, Suarez DL. Influenza Neuraminidase as a Vaccine Antigen. In: Compans RW, Orenstein WA, editors. Vaccines Pandemic Influ. [Internet]. Springer Berlin Heidelberg; 2009 [cited 2013 Apr 11]. p. 227-41. Available from: http://link. springer. com/chapter/10. 1007/978-3-540-92165-3β12.
51. Hessell AJ, Hangartner L, Hunter M, et al. Fc receptor but not complement binding is important in antibody protection against HIV. Nature 2007; 449(7158): 101-4.
52. Koenig HC, Sutherland A, Izurieta HS, McGonagle D. Application of the immunological disease continuum to study autoimmune and other inflammatory events after vaccination. Vaccine 2011; 29(5): 913-9.
53. Guzman MG, Alvarez M, Halstead SB. Secondary infection as a risk factor for dengue hemorrhagic fever/dengue shock syndrome: an historical perspective and role of antibody-dependent enhancement of infection. Arch. Virol. [Internet]. 2013 Mar 8 [cited 2013 Apr 23]; Available from: http://link. springer. com/content/pdf/10. 1007%2Fs00705-013-1645-3. pdf.
54. Ehlinger EP, Webster EM, Kang HH, et al. Maternal Cytomegalovirus-Specific Immune Responses and Symptomatic Postnatal Cytomegalovirus Transmission in Very Low-Birth-Weight Preterm Infants. J Infect Dis 2011; 204(11): 1672-82.
55. Manley K, Anderson J, Yang F, et al. Human Cytomegalovirus Escapes a Naturally Occurring Neutralizing Antibody by Incorporating It into Assembling Virions. Cell Host Microbe 2011; 10(3): 197-209.
56. Mouquet H, Nussenzweig MC. Polyreactive antibodies in adaptive immune responses to viruses. Cell Mol Life Sci 2011; 69(9): 1435-45.
57. Stapleton NM, Andersen JT, Stemerding AM, et al. Competition for FcRn-mediated transport gives rise to short half-life of human IgG3 and offers therapeutic potential. Nat Commun 2011; 2: 599.
58. Plotkin SA. Complex Correlates of Protection After Vaccination. Clin. Infect. Dis. [Internet]. 2013 Feb 5 [cited 2013 Apr 26]; Available from: http://cid. oxfordjournals. org/content/early/2013/03/05/cid. cit048.
59. Sullivan NJ, Martin JE, Graham BS, Nabel GJ. Correlates of protective immunity for Ebola vaccines: implications for regulatory approval by the animal rule. Nat Rev Microbiol 2009; 7(5): 393-400.
60. Ovsyannikova IG, Poland GA. Vaccinomics: Current Findings, Challenges and Novel Approaches for Vaccine Development. Aaps J 2011; 13(3): 438-44.
61. Regenmortel MHVV. Requirements for empirical immunogenicity trials, rather than structure-based design, for developing an effective HIV vaccine. Arch Virol 2012; 157(1): 1-20.
62. Meerten T van, Rijn RS van, Hol S, Hagenbeek A, Ebeling SB. Complement-Induced Cell Death by Rituximab Depends on CD20 Expression Level and Acts Complementary to Antibody-Dependent Cellular Cytotoxicity. Clin Cancer Res 2006; 12(13): 4027-35.
63. Schlesinger JJ, Brandriss MW, Cropp CB, Monath TP. Protection against yellow fever in monkeys by immunization with yellow fever virus nonstructural protein NS1. J Virol 1986; 60(3): 1153-5.
64. Yokomori K, Baker SC, Stohlman SA, Lai MM. Hemagglutininesterase-specific monoclonal antibodies alter the neuropathogenicity of mouse hepatitis virus. J Virol 1992; 66(5): 2865-74.
65. Hangartner L, Zellweger RM, Giobbi M, et al. Nonneutralizing antibodies binding to the surface glycoprotein of lymphocytic choriomeningitis virus reduce early virus spread. J Exp Med 2006; 203(8): 2033-42.