Table of Contents
Advances in Biology
Volume 2014 (2014), Article ID 157895, 24 pages
http://dx.doi.org/10.1155/2014/157895
Review Article

Neutralization of Virus Infectivity by Antibodies: Old Problems in New Perspectives

Department of Microbiology and Immunology, Weill Cornell Medical College, Cornell University, New York, NY 10065-4896, USA

Received 30 April 2014; Accepted 12 August 2014; Published 9 September 2014

Academic Editor: Ma Luo

Copyright © 2014 P. J. Klasse. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. W. C. Koff, D. R. Burton, P. R. Johnson et al., “Accelerating next-generation vaccine development for global disease prevention,” Science, vol. 340, no. 6136, Article ID 1232910, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. P. R. Krause, S. R. Bialek, S. B. Boppana et al., “Priorities for CMV vaccine development,” Vaccine, vol. 32, no. 1, pp. 4–10, 2013. View at Publisher · View at Google Scholar
  3. S. A. Plotkin, “Immunologic correlates of protection induced by vaccination,” Pediatric Infectious Disease Journal, vol. 20, no. 1, pp. 63–75, 2001. View at Publisher · View at Google Scholar · View at Scopus
  4. S. A. Plotkin, “Correlates of vaccine-induced immunity,” Clinical Infectious Diseases, vol. 47, no. 3, pp. 401–409, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. S. A. Plotkin, “Correlates of protection induced by vaccination,” Clinical and Vaccine Immunology, vol. 17, no. 7, pp. 1055–1065, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. S. A. Plotkin, “Complex correlates of protection after vaccination,” Clinical Infectious Diseases, vol. 56, no. 10, pp. 1458–1465, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. D. R. Burton, P. Poignard, R. L. Stanfield, and I. A. Wilson, “Broadly neutralizing antibodies present new prospects to counter highly antigenically diverse viruses,” Science, vol. 337, no. 6091, pp. 183–186, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. P. J. Klasse and J. P. Moore, “Good CoP, bad CoP? Interrogating the immune responses to primate lentiviral vaccines,” Retrovirology, vol. 9, article 80, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. I. J. Amanna, N. E. Carlson, and M. K. Slifka, “Duration of humoral immunity to common viral and vaccine antigens,” New England Journal of Medicine, vol. 357, no. 19, pp. 1903–1915, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. M. K. Slifka, R. Antia, J. K. Whitmire, and R. Ahmed, “Humoral immunity due to long-lived plasma cells,” Immunity, vol. 8, no. 3, pp. 363–372, 1998. View at Publisher · View at Google Scholar · View at Scopus
  11. E. Hammarlund, M. W. Lewis, S. G. Hansen et al., “Duration of antiviral immunity after smallpox vaccination,” Nature Medicine, vol. 9, no. 9, pp. 1131–1137, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. P. J. Klasse, R. W. Sanders, A. Cerutti, and J. P. Moore, “How can HIV-type-1-Env immunogenicity be improved to facilitate antibody-based vaccine development?” AIDS Research and Human Retroviruses, vol. 28, no. 1, pp. 1–15, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. F. Klein, H. Mouquet, P. Dosenovic, J. F. Scheid, L. Scharf, and M. C. Nussenzweig, “Antibodies in HIV-1 vaccine development and therapy,” Science, vol. 341, pp. 1199–1204, 2013. View at Google Scholar
  14. D. H. Barouch and B. Korber, “HIV-1 vaccine development after STEP,” Annual Review of Medicine, vol. 61, pp. 153–167, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. N. S. Greenspan, “Dimensions of antigen recognition and levels of immunological specificity,” Advances in Cancer Research, vol. 80, pp. 147–187, 2001. View at Google Scholar · View at Scopus
  16. D. Szwajkajzer and J. Carey, “Molecular biological constraints on ligand-binding affinity and specificity,” Biopolymers, vol. 44, no. 2, pp. 181–198, 1997. View at Google Scholar · View at Scopus
  17. N. S. Greenspan, “Cohen's conjecture, Howard's hypothesis, and Ptashnes ptruth: an exploration of the relationship between affinity and specificity,” Trends in Immunology, vol. 31, no. 4, pp. 138–143, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. W. C. Koff, P. R. Johnson, D. I. Watkins et al., “HIV vaccine design: insights from live attenuated SIV vaccines,” Nature Immunology, vol. 7, no. 1, pp. 19–23, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. R. C. Desrosiers, “Prospects for live attenuated HIV,” Nature Medicine, vol. 4, p. 982, 1998. View at Google Scholar
  20. R. P. Johnson and R. C. Desrosiers, “Protective immunity induced by live attenuated simian immunodeficiency virus,” Current Opinion in Immunology, vol. 10, no. 4, pp. 436–443, 1998. View at Publisher · View at Google Scholar · View at Scopus
  21. W. H. Gerlich, “Medical virology of hepatitis B: how it began and where we are now,” Virology Journal, vol. 10, article 239, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. J. W. Wang and R. B. S. Roden, “Virus-like particles for the prevention of human papillomavirus-associated malignancies,” Expert Review of Vaccines, vol. 12, no. 2, pp. 129–141, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. J. Schiller and B. Chackerian, “Why HIV virions have low numbers of envelope spikes: implications for vaccine development,” PLoS Pathogens, vol. 10, Article ID e1004254, 2014. View at Google Scholar
  24. D. R. Burton, R. C. Desrosiers, R. W. Doms et al., “HIV vaccine design and the neutralizing antibody problem,” Nature Immunology, vol. 5, no. 3, pp. 233–236, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. B. F. Haynes, P. B. Gilbert, M. J. McElrath et al., “Immune-correlates analysis of an HIV-1 vaccine efficacy trial,” New England Journal of Medicine, vol. 366, no. 14, pp. 1275–1286, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Rerks-Ngarm, P. Pitisuttithum, S. Nitayaphan et al., “Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand,” New England Journal of Medicine, vol. 361, no. 23, pp. 2209–2220, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. D. Forthal, T. J. Hope, and G. Alter, “New paradigms for functional HIV-specific nonneutralizing antibodies,” Current Opinion in HIV and AIDS, vol. 8, no. 5, pp. 393–401, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. A. L. Schmaljohn, “Protective antiviral antibodies that lack neutralizing activity: precedents and evolution of concepts,” Current HIV Research, vol. 11, pp. 345–353, 2013. View at Google Scholar
  29. K. R. Popper, Objective Knowledge, Oxford University Press, Oxford, UK, 1972.
  30. N. J. Dimmock, “Neutralization of animal viruses,” Current Topics in Microbiology and Immunology, vol. 183, pp. 1–149, 1993. View at Google Scholar
  31. P. J. Klasse and Q. J. Sattentau, “Occupancy and mechanism in antibody-mediated neutralization of animal viruses,” Journal of General Virology, vol. 83, no. 9, pp. 2091–2108, 2002. View at Google Scholar · View at Scopus
  32. W. J. J. Finlay and J. C. Almagro, “Natural and man-made V-gene repertoires for antibody discovery,” Frontiers in Immunology, vol. 3, Article ID Article 342, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Muyldermans, “Nanobodies: natural single-domain antibodies,” Annual Review of Biochemistry, vol. 82, pp. 775–797, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. G. P. Allaway, K. L. Davis-Bruno, G. A. Beaudry et al., “Expression and characterization of CD4-IgG2, a novel heterotetramer that neutralizes primary HIV type 1 isolates,” AIDS Research and Human Retroviruses, vol. 11, no. 5, pp. 533–539, 1995. View at Publisher · View at Google Scholar · View at Scopus
  35. B. M. McDermott Jr., A. H. Rux, R. J. Eisenberg, G. H. Cohen, and V. R. Racaniello, “Two distinct binding affinities of poliovirus for its cellular receptor,” The Journal of Biological Chemistry, vol. 275, no. 30, pp. 23089–23096, 2000. View at Publisher · View at Google Scholar · View at Scopus
  36. A. P. Gounder, M. E. Wiens, S. S. Wilson, W. Lus, and J. G. Smith, “Critical determinants of human α-defensin 5 activity against non-enveloped viruses,” The Journal of Biological Chemistry, vol. 287, no. 29, pp. 24554–24562, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. S. S. Wilson, M. E. Wiens, and J. G. Smith, “Antiviral mechanisms of human defensins,” Journal of Molecular Biology, vol. 425, pp. 4965–4980, 2013. View at Google Scholar
  38. T. Du, K. Hu, J. Yang et al., “Bifunctional CD4-DC-SIGN fusion proteins demonstrate enhanced avidity to gp120 and inhibit HIV-1 infection and dissemination,” Antimicrobial Agents and Chemotherapy, vol. 56, no. 9, pp. 4640–4649, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. P. Plevka, R. Perera, J. Cardosa, R. J. Kuhn, and M. G. Rossmann, “Crystal structure of human enterovirus 71,” Science, vol. 336, no. 6086, p. 1274, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. P. Plevka, R. Perera, M. L. Yap, J. Cardosa, R. J. Kuhn, and M. G. Rossmann, “Structure of human enterovirus 71 in complex with a capsid-binding inhibitor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 14, pp. 5463–5467, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. M. G. Rossmann, Y. He, and R. J. Kuhn, “Picornavirus-receptor interactions,” Trends in Microbiology, vol. 10, no. 7, pp. 324–331, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. Y. D. Kwon, A. Finzi, X. Wu et al., “Unliganded HIV-1 gp120 core structures assume the CD4-bound conformation with regulation by quaternary interactions and variable loops,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 15, pp. 5663–5668, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. N. Madani, A. Schön, A. M. Princiotto et al., “Small-molecule CD4 mimics interact with a highly conserved pocket on HIV-1 gp120,” Structure, vol. 16, no. 11, pp. 1689–1701, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Repik and P. R. Clapham, “Plugging gp120s Cavity,” Structure, vol. 16, no. 11, pp. 1603–1604, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Schön, N. Madani, J. C. Klein et al., “Thermodynamics of binding of a low-molecular-weight CD4 mimetic to HIV-1 gp120,” Biochemistry, vol. 45, no. 36, pp. 10973–10980, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. Q. Zhao, L. Ma, S. Jiang et al., “Identification of N-phenyl-N′-(2,2,6,6-tetramethyl-piperidin-4-yl)-oxalamides as a new class of HIV-1 entry inhibitors that prevent gp120 binding to CD4,” Virology, vol. 339, no. 2, pp. 213–225, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. P. F. Lin, W. Blair, T. Wang et al., “A small molecule HIV-1 inhibitor that targets the HIV-1 envelope and inhibits CD4 receptor binding,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 19, pp. 11013–11018, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. P. L. Moore, T. Cilliers, and L. Morris, “Predicted genotypic resistance to the novel entry inhibitor, BMS-378806, among HIV-1 isolates of subtypes A to G,” AIDS, vol. 18, no. 17, pp. 2327–2330, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. Z. Si, N. Madani, J. M. Cox et al., “Small-molecule inhibitors of HIV-1 entry block receptor-induced conformational changes in the viral envelope glycoproteins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 14, pp. 5036–5041, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. R. G. Webster and W. G. Laver, “Preparation and properties of antibody directed specifically against the neuraminidase of influenza virus,” Journal of Immunology, vol. 99, no. 1, pp. 49–55, 1967. View at Google Scholar · View at Scopus
  51. D. J. DiLillo, G. S. Tan, P. Palese, and J. V. Ravetch, “Broadly neutralizing hemagglutinin stalk-specific antibodies require FcgammaR interactions for protection against influenza virus in vivo,” Nature Medicine, vol. 20, pp. 143–151, 2014. View at Google Scholar
  52. J. Feldmann and O. Schwartz, “HIV-1 virological synapse: live imaging of transmission,” Viruses, vol. 2, no. 8, pp. 1666–1680, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. V. Piguet and Q. Sattentau, “Dangerous liaisons at the virological synapse,” Journal of Clinical Investigation, vol. 114, no. 5, pp. 605–610, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. Q. J. Sattentau, “Cell-to-cell spread of retroviruses,” Viruses, vol. 2, no. 6, pp. 1306–1321, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. T. Schiffner, Q. J. Sattentau, and C. J. Duncan, “Cell-to-cell spread of HIV-1 and evasion of neutralizing antibodies,” Vaccine, vol. 31, pp. 5789–5797, 2013. View at Google Scholar
  56. M. Malbec, F. Porrot, R. Rua et al., “Broadly neutralizing antibodies that inhibit HIV-1 cell to cell transmission,” The Journal of Experimental Medicine, vol. 210, no. 13, pp. 2813–2821, 2013. View at Publisher · View at Google Scholar
  57. I. A. Abela, L. Berlinger, M. Schanz et al., “Cell-cell transmission enables HIV-1 to evade inhibition by potent CD4bs directed antibodies,” PLoS Pathogens, vol. 8, no. 4, Article ID e1002634, 2012. View at Publisher · View at Google Scholar · View at Scopus
  58. B. Mandel, “Neutralization of animal viruses,” Advances in Virus Research, vol. 23, pp. 205–268, 1978. View at Publisher · View at Google Scholar · View at Scopus
  59. E. Mehlhop, A. Fuchs, M. Engle, and M. S. Diamond, “Complement modulates pathogenesis and antibody-dependent neutralization of West Nile virus infection through a C5-independent mechanism,” Virology, vol. 393, no. 1, pp. 11–15, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. E. Mehlhop, S. Nelson, C. A. Jost et al., “Complement protein C1q reduces the stoichiometric threshold for antibody-mediated neutralization of West Nile virus,” Cell Host & Microbe, vol. 6, no. 4, pp. 381–391, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. G. T. Spear, M. Hart, G. G. Olinger, F. B. Hashemi, and M. Saifuddin, “The role of the complement system in virus infections,” Current Topics in Microbiology and Immunology, vol. 260, pp. 229–245, 2001. View at Google Scholar · View at Scopus
  62. D. N. Forthal, J. S. Gach, G. Landucci et al., “Fc-glycosylation influences Fcγ receptor binding and cell-mediated anti-hivactivity of monoclonal antibody 2G12,” The Journal of Immunology, vol. 185, no. 11, pp. 6876–6882, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. A. J. Hessell, L. Hangartner, M. Hunter et al., “Fc receptor but not complement binding is important in antibody protection against HIV,” Nature, vol. 449, no. 7158, pp. 101–104, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. B. Moldt, M. Shibata-Koyama, E. G. Rakasz et al., “A nonfucosylated variant of the anti-HIV-1 monoclonal antibody b12 has enhanced Fcγriiia-Mediated antiviral activity in vitro but does not improve protection against mucosal SHIV challenge in macaques,” Journal of Virology, vol. 86, no. 11, pp. 6189–6196, 2012. View at Publisher · View at Google Scholar · View at Scopus
  65. J. M. Bergelson and C. B. Coyne, “Picornavirus entry,” Advances in Experimental Medicine and Biology, vol. 790, pp. 24–41, 2013. View at Publisher · View at Google Scholar · View at Scopus
  66. K. N. Bossart, D. L. Fusco, and C. C. Broder, “Paramyxovirus entry,” Advances in Experimental Medicine and Biology, vol. 790, pp. 95–127, 2013. View at Publisher · View at Google Scholar · View at Scopus
  67. P. Danthi, G. H. Holm, T. Stehle, and T. S. Dermody, “Reovirus receptors, cell entry, and proapoptotic signaling,” Advances in Experimental Medicine and Biology, vol. 790, pp. 42–71, 2013. View at Publisher · View at Google Scholar · View at Scopus
  68. T. O. Edinger, M. O. Pohl, and S. Stertz, “Entry of influenza A virus: host factors and antiviral targets,” Journal of General Virology, vol. 95, pp. 263–277, 2014. View at Google Scholar
  69. C. L. Jolly and Q. J. Sattentau, “Attachment factors,” Advances in Experimental Medicine and Biology, vol. 790, pp. 1–23, 2013. View at Publisher · View at Google Scholar · View at Scopus
  70. P. J. Klasse, R. Bron, and M. Marsh, “Mechanisms of enveloped virus entry into animal cells,” Advanced Drug Delivery Reviews, vol. 34, no. 1, pp. 65–91, 1998. View at Publisher · View at Google Scholar · View at Scopus
  71. C. Krummenacher, A. Carfí, R. J. Eisenberg, and G. H. Cohen, “Entry of herpesviruses into cells: the enigma variations,” Advances in Experimental Medicine and Biology, vol. 790, pp. 178–195, 2013. View at Publisher · View at Google Scholar · View at Scopus
  72. D. Lindemann, I. Steffen, and S. Pöhlmann, “Cellular entry of retroviruses,” Advances in Experimental Medicine and Biology, vol. 790, pp. 128–149, 2013. View at Publisher · View at Google Scholar · View at Scopus
  73. B. D. Lindenbach and C. M. Rice, “The ins and outs of hepatitis C virus entry and assembly,” Nature Reviews Microbiology, vol. 11, pp. 688–700, 2013. View at Publisher · View at Google Scholar
  74. K. Lonberg Holm, R. L. Crowell, and L. Philipson, “Unrelated animal viruses share receptors,” Nature, vol. 259, no. 5545, pp. 679–681, 1976. View at Publisher · View at Google Scholar · View at Scopus
  75. L. Philipson, “Adenovirus—an eternal archetype,” Current Topics in Microbiology and Immunology, vol. 199, part 1, pp. 1–24, 1995. View at Google Scholar · View at Scopus
  76. L. Philipson and R. F. Pettersson, “The Coxsackie-Adenovirus Receptor: a new receptor in the immunoglobulin family involved in cell adhesion,” Current Topics in Microbiology and Immunology, vol. 273, pp. 87–111, 2004. View at Google Scholar · View at Scopus
  77. A. D. Regan and G. R. Whittaker, “Entry of rhabdoviruses into animal cells,” Advances in Experimental Medicine and Biology, vol. 790, pp. 167–177, 2013. View at Publisher · View at Google Scholar · View at Scopus
  78. G. Simmons, “Filovirus entry,” Advances in Experimental Medicine and Biology, vol. 790, pp. 83–94, 2013. View at Publisher · View at Google Scholar · View at Scopus
  79. X. Sun and G. R. Whittaker, “Entry of influenza virus,” Advances in Experimental Medicine and Biology, vol. 790, pp. 72–82, 2013. View at Publisher · View at Google Scholar · View at Scopus
  80. M. Suomalainen and U. F. Greber, “Uncoating of non-enveloped viruses,” Current Opinion in Virology, vol. 3, no. 1, pp. 27–33, 2013. View at Publisher · View at Google Scholar · View at Scopus
  81. T. C. Pierson and M. Kielian, “Flaviviruses: braking the entering,” Current Opinion in Virology, vol. 3, no. 1, pp. 3–12, 2013. View at Publisher · View at Google Scholar · View at Scopus
  82. P. Plattet and R. K. Plemper, “Envelope protein dynamics in paramyxovirus entry,” mBio, vol. 4, no. 4, Article ID e00413, 2013. View at Publisher · View at Google Scholar · View at Scopus
  83. G. B. Melikyan, “Common principles and intermediates of viral protein-mediated fusion: the HIV-1 paradigm,” Retrovirology, vol. 5, article 111, 2008. View at Publisher · View at Google Scholar · View at Scopus
  84. P. J. Klasse, “The molecular basis of HIV entry,” Cellular Microbiology, vol. 14, no. 8, pp. 1183–1192, 2012. View at Publisher · View at Google Scholar · View at Scopus
  85. G. B. Melikyan, “HIV entry: a game of hide-and-fuse?” Current Opinion in Virology, vol. 4, pp. 1–7, 2014. View at Google Scholar
  86. M. Marsh and A. Helenius, “Virus entry: open sesame,” Cell, vol. 124, no. 4, pp. 729–740, 2006. View at Publisher · View at Google Scholar · View at Scopus
  87. M. Marsh and R. Bron, “SFV infection in CHO cells: cell-type specific restrictions to productive virus entry at the cell surface,” Journal of Cell Science, vol. 110, part 1, pp. 95–103, 1997. View at Google Scholar · View at Scopus
  88. S. Lu, S. D. Putney, and H. L. Robinson, “Human immunodeficiency virus type 1 entry into T cells: more-rapid escape from an anti-V3 loop than from an antireceptor antibody,” Journal of Virology, vol. 66, no. 4, pp. 2547–2550, 1992. View at Google Scholar · View at Scopus
  89. S. Putney, “How antibodies block HIV infection: paths to an AIDS vaccine,” Trends in Biochemical Sciences, vol. 17, no. 5, pp. 191–196, 1992. View at Google Scholar · View at Scopus
  90. T. J. Smith, N. H. Olson, R. H. Cheng et al., “Structure of human rhinovirus complexed with Fab fragments from a neutralizing antibody,” Journal of Virology, vol. 67, no. 3, pp. 1148–1158, 1993. View at Google Scholar · View at Scopus
  91. B. Brandenburg, L. Y. Lee, M. Lakadamyali, M. J. Rust, X. Zhuang, and J. M. Hogle, “Imaging poliovirus entry in live cells,” PLoS Biology, vol. 5, no. 7, p. e183, 2007. View at Publisher · View at Google Scholar · View at Scopus
  92. A. Panjwani, M. Strauss, S. Gold et al., “Capsid protein VP4 of human rhinovirus induces membrane permeability by the formation of a size-selective multimeric pore,” PLoS Pathogens, vol. 10, no. 8, Article ID e1004294, 2014. View at Publisher · View at Google Scholar
  93. E. A. Emini, S. Y. Kao, A. J. Lewis, R. Crainic, and E. Wimmer, “Functional basis of poliovirus neutralization determined with monospecific neutralizing antibodies,” Journal of Virology, vol. 46, no. 2, pp. 466–474, 1983. View at Google Scholar · View at Scopus
  94. B. Mandel, “Characterization of type 1 poliovirus by electrophoretic analysis,” Virology, vol. 44, no. 3, pp. 554–568, 1971. View at Publisher · View at Google Scholar · View at Scopus
  95. B. Mandel, “An analysis of the physical and chemical factors involved in the reactivation of neutralized poliovirus by the method of freezing and thawing,” Virology, vol. 51, no. 2, pp. 358–369, 1973. View at Publisher · View at Google Scholar · View at Scopus
  96. B. Mandel, “Neutralization of poliovirus: a hypothesis to explain the mechanism and the one hit character of the neutralization reaction,” Virology, vol. 69, no. 2, pp. 500–510, 1976. View at Publisher · View at Google Scholar · View at Scopus
  97. R. Vrijsen, A. Mosser, and A. Boeye, “Postadsorption neutralization of poliovirus,” Journal of Virology, vol. 67, no. 6, pp. 3126–3133, 1993. View at Google Scholar · View at Scopus
  98. K. Wetz, P. Willingmann, H. Zeichhardt, and K. O. Habermehl, “Neutralization of poliovirus by polyclonal antibodies requires binding of a single IgG molecule per virion,” Archives of Virology, vol. 91, no. 3-4, pp. 207–220, 1986. View at Publisher · View at Google Scholar · View at Scopus
  99. D. R. Burton, E. O. Saphire, and P. W. H. I. Parren, “A model for neutralization of viruses based on antibody coating of the virion surface,” Current Topics in Microbiology and Immunology, vol. 260, pp. 109–143, 2001. View at Google Scholar · View at Scopus
  100. P. W. H. I. Parren, I. Mondor, D. Naniche et al., “Neutralization of human immunodeficiency virus type 1 by antibody to gp120 is determined primarily by occupancy of sites on the virion irrespective of epitope specificity,” Journal of Virology, vol. 72, no. 5, pp. 3512–3519, 1998. View at Google Scholar · View at Scopus
  101. P. Poignard, P. J. Klasse, and Q. J. Sattentau, “Antibody neutralization of HIV-1,” Immunology Today, vol. 17, no. 5, pp. 239–246, 1996. View at Publisher · View at Google Scholar · View at Scopus
  102. R. P. Ringe, R. W. Sanders, A. Yasmeen et al., “Cleavage strongly influences whether soluble HIV-1 envelope glycoprotein trimers adopt a native-like conformation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, pp. 18256–18261, 2013. View at Google Scholar
  103. R. W. Sanders, R. Derking, A. Cupo et al., “A next-generation cleaved, soluble HIV-1 Env Trimer, BG505 SOSIP.664 gp140, expresses multiple epitopes for broadly neutralizing but not non-neutralizing antibodies,” PLoS Pathogens, vol. 9, Article ID e1003618, 2013. View at Google Scholar
  104. C. Wilson, M. S. Reitz Jr., K. Aldrich et al., “The site of an immune-selected point mutation in the transmembrane protein of human immunodeficiency virus type 1 does not constitute the neutralization epitope,” Journal of Virology, vol. 64, no. 7, pp. 3240–3248, 1990. View at Google Scholar · View at Scopus
  105. P. J. Klasse, “Modeling how many envelope glycoprotein trimers per virion participate in human immunodeficiency virus infectivity and its neutralization by antibody,” Virology, vol. 369, no. 2, pp. 245–262, 2007. View at Publisher · View at Google Scholar · View at Scopus
  106. P. J. Klasse and J. P. Moore, “Quantitative model of antibody- and soluble CD4-mediated neutralization of primary isolates and T-cell line-adapted strains of human immunodeficiency virus type,” Journal of Virology, vol. 70, no. 6, pp. 3668–3677, 1996. View at Google Scholar · View at Scopus
  107. C. Magnus, O. F. Brandenberg, P. Rusert, A. Trkola, and R. R. Regoes, “Mathematical models: a key to understanding HIV envelope interactions?” Journal of Immunological Methods, vol. 398-399, pp. 1–18, 2013. View at Publisher · View at Google Scholar
  108. C. Magnus and R. R. Regoes, “Estimating the stoichiometry of HIV neutralization,” PLoS Computational Biology, vol. 6, no. 3, Article ID e1000713, 2010. View at Publisher · View at Google Scholar · View at MathSciNet · View at Scopus
  109. C. Magnus and R. R. Regoes, “Restricted occupancy models for neutralization of HIV virions and populations,” Journal of Theoretical Biology, vol. 283, pp. 192–202, 2011. View at Publisher · View at Google Scholar · View at MathSciNet · View at Scopus
  110. C. Magnus, P. Rusert, S. Bonhoeffer, A. Trkola, and R. R. Regoes, “Estimating the stoichiometry of human immunodeficiency virus entry,” Journal of Virology, vol. 83, no. 3, pp. 1523–1531, 2009. View at Publisher · View at Google Scholar · View at Scopus
  111. X. Yang, S. Kurteva, S. Lee, and J. Sodroski, “Stoichiometry of antibody neutralization of human immunodeficiency virus type 1,” Journal of Virology, vol. 79, no. 6, pp. 3500–3508, 2005. View at Publisher · View at Google Scholar · View at Scopus
  112. X. Yang, S. Kurteva, X. Ren, S. Lee, and J. Sodroski, “Stoichiometry of envelope glycoprotein trimers in the entry of human immunodeficiency virus type 1,” Journal of Virology, vol. 79, no. 19, pp. 12132–12147, 2005. View at Publisher · View at Google Scholar · View at Scopus
  113. X. Yang, S. Kurteva, X. Ren, S. Lee, and J. Sodroski, “Subunit stoichiometry of human immunodeficiency virus type 1 envelope glycoprotein trimers during virus entry into host cells,” Journal of Virology, vol. 80, no. 9, pp. 4388–4395, 2006. View at Publisher · View at Google Scholar · View at Scopus
  114. K. Schønning, O. Lund, O. S. Lund, and J. S. Hansen, “Stoichiometry of monoclonal antibody neutralization of T-cell line- adapted human immunodeficiency virus type 1,” Journal of Virology, vol. 73, no. 10, pp. 8364–8370, 1999. View at Google Scholar · View at Scopus
  115. C. R. Madeley, W. H. Allan, and A. P. Kendal, “Studies with avian influenza A viruses: serological relations of the haemagglutinin and neuraminidase antigens of ten virus isolates.,” Journal of General Virology, vol. 12, no. 2, pp. 69–78, 1971. View at Publisher · View at Google Scholar · View at Scopus
  116. M. Majer and F. Lik, “Sensitization of influenza virus A2-Singapore by antineuraminidase.,” Journal of General Virology, vol. 13, no. 2, pp. 355–356, 1971. View at Publisher · View at Google Scholar · View at Scopus
  117. H. Raux, P. Coulon, F. Lafay, and A. Flamand, “Monoclonal antibodies which recognize the acidic configuration of the rabies glycoprotein at the surface of the virion can be neutralizing,” Virology, vol. 210, no. 2, pp. 400–408, 1995. View at Publisher · View at Google Scholar · View at Scopus
  118. C. D. Rizzuto and J. G. Sodroski, “Contribution of virion ICAM-1 to human immunodeficiency virus infectivity and sensitivity to neutralization,” Journal of Virology, vol. 71, no. 6, pp. 4847–4851, 1997. View at Google Scholar · View at Scopus
  119. L. O. Arthur, J. W. Bess Jr., R. C. Sowder II et al., “Cellular proteins bound to immunodeficiency viruses: implications for pathogenesis and vaccines,” Science, vol. 258, no. 5090, pp. 1935–1938, 1992. View at Publisher · View at Google Scholar · View at Scopus
  120. M. Page, R. Quartey-Papafio, M. Robinson et al., “Complement-mediated virus infectivity neutralisation by HLA antibodies is associated with sterilising immunity to siv challenge in the macaque model for HIV/AIDS,” PLoS ONE, vol. 9, Article ID e88735, 2014. View at Google Scholar
  121. S. Ugolini, I. Mondor, P. W. H. I. Parren et al., “Inhibition of virus attachment to CD4+ target cells is a major mechanism of T cell line-adapted HIV-1 neutralization,” Journal of Experimental Medicine, vol. 186, no. 8, pp. 1287–1298, 1997. View at Publisher · View at Google Scholar · View at Scopus
  122. J. Huang, G. Ofek, L. Laub et al., “Broad and potent neutralization of HIV-1 by a gp41-specific human antibody,” Nature, vol. 491, no. 7424, pp. 406–412, 2012. View at Publisher · View at Google Scholar · View at Scopus
  123. A. S. Kim, D. P. Leaman, and M. B. Zwick, “Antibody to gp41 MPER alters functional properties of HIV-1 Env without complete neutralization,” PLoS Pathogens, vol. 10, Article ID e1004271, 2014. View at Google Scholar
  124. H. K. Steger and M. J. Root, “Kinetic dependence to HIV-1 entry inhibition,” The Journal of Biological Chemistry, vol. 281, no. 35, pp. 25813–25821, 2006. View at Publisher · View at Google Scholar · View at Scopus
  125. T. J. Smith, “Antibody interactions with rhinovirus: Lessons for mechanisms of neutralization and the role of immunity in viral evolution,” Current Topics in Microbiology and Immunology, vol. 260, pp. 1–28, 2001. View at Google Scholar · View at Scopus
  126. J. Julien, D. Sok, R. Khayat et al., “Broadly neutralizing antibody PGT121 allosterically modulates CD4 binding via recognition of the HIV-1 gp120 V3 base and multiple surrounding glycans,” PLoS Pathogens, vol. 9, no. 5, Article ID e1003342, 2013. View at Publisher · View at Google Scholar · View at Scopus
  127. N. Hashimoto and A. M. Prince, “Kinetic studies on the neutralization reaction between Japanese encephalitis virus and antiserum,” Virology, vol. 19, no. 3, pp. 261–272, 1963. View at Publisher · View at Google Scholar · View at Scopus
  128. A. M. Breschkin, J. Ahern, and D. O. White, “Antigenic determinants of influenza virus hemagglutinin VIII. Topography of the antigenic regions of influenza virus hemagglutinin determined by competitive radioimmunoassay with monoclonal antibodies,” Virology, vol. 113, no. 1, pp. 130–140, 1981. View at Publisher · View at Google Scholar · View at Scopus
  129. A. Marzi, T. Gramberg, G. Simmons et al., “DC-SIGN and DC-SIGNR interact with the glycoprotein of marburg virus and the S protein of severe acute respiratory syndrome coronavirus,” Journal of Virology, vol. 78, no. 21, pp. 12090–12095, 2004. View at Publisher · View at Google Scholar · View at Scopus
  130. P. Liu, L. D. Williams, X. Shen et al., “Capacity for infectious HIV-1 virion capture differs by envelope antibody specificity,” Journal of Virology, vol. 88, no. 9, pp. 5165–5170, 2014. View at Publisher · View at Google Scholar
  131. P. Poignard, M. Moulard, E. Golez et al., “Heterogeneity of envelope molecules expressed on primary human immunodeficiency virus type 1 particles as probed by the binding of neutralizing and nonneutralizing antibodies,” Journal of Virology, vol. 77, no. 1, pp. 353–365, 2003. View at Publisher · View at Google Scholar · View at Scopus
  132. P. Poignard, T. Fouts, D. Naniche, J. P. Moore, and Q. J. Sattentau, “Neutralizing antibodies to human immunodeficiency virus type-1 gp120 induce envelope glycoprotein subunit dissociation,” The Journal of Experimental Medicine, vol. 183, no. 2, pp. 473–484, 1996. View at Publisher · View at Google Scholar · View at Scopus
  133. C. R. Ruprecht, A. Krarup, L. Reynell et al., “MPER-specific antibodies induce gp120 shedding and irreversibly neutralize HIV-1,” Journal of Experimental Medicine, vol. 208, no. 3, pp. 439–454, 2011. View at Publisher · View at Google Scholar · View at Scopus
  134. P. J. Klasse, J. A. McKeating, M. Schutten, M. S. Reitz Jr., and M. Robert-Guroff, “An immune-selected point mutation in the transmembrane protein of n immunodeficiency virus type 1 (HXB2-Env:Ala 582(→ Thr)) decreases viral neutralization by monoclonal antibodies to the CD4-binding site,” Virology, vol. 196, no. 1, pp. 332–337, 1993. View at Publisher · View at Google Scholar · View at Scopus
  135. M. Thali, M. Charles, C. Furman et al., “Resistance to neutralization by broadly reactive antibodies to the human immunodeficiency virus type 1 gp120 glycoprotein conferred by a gp41 amino acid change,” Journal of Virology, vol. 68, no. 2, pp. 674–680, 1994. View at Google Scholar · View at Scopus
  136. S. W. Gollins and J. S. Porterfield, “A new mechanism for the neutralization of enveloped viruses by antiviral antibody,” Nature, vol. 321, no. 6067, pp. 244–246, 1986. View at Publisher · View at Google Scholar · View at Scopus
  137. K. Miyauchi, Y. Kim, O. Latinovic, V. Morozov, and G. B. Melikyan, “HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes,” Cell, vol. 137, no. 3, pp. 433–444, 2009. View at Publisher · View at Google Scholar · View at Scopus
  138. S. J. Armstrong and N. J. Dimmock, “Neutralization of influenza virus by low concentrations of hemagglutinin-specific polymeric immunoglobulin A inhibits viral fusion activity, but activation of the ribonucleoprotein is also inhibited,” Journal of Virology, vol. 66, no. 6, pp. 3823–3832, 1992. View at Google Scholar · View at Scopus
  139. S. A. Reading and N. J. Dimmock, “Neutralization of animal virus infectivity by antibody,” Archives of Virology, vol. 152, no. 6, pp. 1047–1059, 2007. View at Publisher · View at Google Scholar · View at Scopus
  140. A. H. Keeble, Z. Khan, A. Forster, and L. C. James, “TRIM21 is an IgG receptor that is structurally, thermodynamically, and kinetically conserved,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 16, pp. 6045–6050, 2008. View at Publisher · View at Google Scholar · View at Scopus
  141. D. L. Mallery, W. A. McEwan, S. R. Bidgood, G. J. Towers, C. M. Johnson, and L. C. James, “Antibodies mediate intracellular immunity through tripartite motif-containing 21 (TRIM21),” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 46, pp. 19985–19990, 2010. View at Publisher · View at Google Scholar · View at Scopus
  142. W. A. Mcewan, D. L. Mallery, D. A. Rhodes, J. Trowsdale, and L. C. James, “Intracellular antibody-mediated immunity and the role of TRIM21,” BioEssays, vol. 33, no. 11, pp. 803–809, 2011. View at Publisher · View at Google Scholar · View at Scopus
  143. W. A. McEwan, F. Hauler, C. R. Williams et al., “Regulation of virus neutralization and the persistent fraction by TRIM21,” Journal of Virology, vol. 86, no. 16, pp. 8482–8491, 2012. View at Publisher · View at Google Scholar · View at Scopus
  144. A. Kramer, T. Keitel, K. Winkler, W. Stöcklein, W. Höhne, and J. Schneider-Mergener, “Molecular basis for the binding promiscuity of an anti-p24 (HIV-1) monoclonal antibody,” Cell, vol. 91, no. 6, pp. 799–809, 1997. View at Publisher · View at Google Scholar · View at Scopus
  145. J. M. Binley, P. J. Klasse, Y. Cao et al., “Differential regulation of the antibody responses to Gag and Env proteins of human immunodeficiency virus type 1,” Journal of Virology, vol. 71, no. 4, pp. 2799–2809, 1997. View at Google Scholar · View at Scopus
  146. J. N. Weber, R. A. Weiss, and C. Roberts, “Human immunodeficiency virus infection in two cohorts of homosexual men: neutralising sera and association of anti-GAG antibody with prognosis,” The Lancet, vol. 1, no. 8525, pp. 119–121, 1987. View at Publisher · View at Google Scholar · View at Scopus
  147. O. Schwartz, V. Maréchal, B. Friguet, F. Arenzana-Seisdedos, and J. Heard, “Antiviral activity of the proteasome on incoming human immunodeficiency virus type 1,” Journal of Virology, vol. 72, no. 5, pp. 3845–3850, 1998. View at Google Scholar · View at Scopus
  148. V. Holl, M. Peressin, T. Decoville et al., “Nonneutralizing antibodies are able to inhibit human immunodeficiency virus type 1 replication in macrophages and immature dendritic cells,” Journal of Virology, vol. 80, no. 12, pp. 6177–6181, 2006. View at Publisher · View at Google Scholar · View at Scopus
  149. K. A. Dowd and T. C. Pierson, “Antibody-mediated neutralization of flaviviruses: a reductionist view,” Virology, vol. 411, no. 2, pp. 306–315, 2011. View at Publisher · View at Google Scholar · View at Scopus
  150. T. C. Pierson, D. H. Fremont, R. J. Kuhn, and M. S. Diamond, “Structural insights into the mechanisms of antibody-mediated neutralization of flavivirus infection: implications for vaccine development,” Cell Host & Microbe, vol. 4, no. 3, pp. 229–238, 2008. View at Publisher · View at Google Scholar · View at Scopus
  151. T. C. Pierson, Q. Xu, S. Nelson et al., “The stoichiometry of antibody-mediated neutralization and enhancement of West Nile virus infection,” Cell Host and Microbe, vol. 1, no. 2, pp. 135–145, 2007. View at Publisher · View at Google Scholar · View at Scopus
  152. S. B. Halstead, “Immune enhancement of viral infection,” Progress in Allergy, vol. 31, pp. 301–364, 1982. View at Google Scholar · View at Scopus
  153. S. B. Halstead, J. S. Chow, and N. J. Marchette, “Immunological enhancement of dengue virus replication,” NATURE NEW BIOL., vol. 243, no. 122, pp. 24–26, 1973. View at Google Scholar · View at Scopus
  154. S. B. Halstead and E. J. O'Rourke, “Dengue viruses and mononuclear phagocytes, I: infection enhancement by non-neutralizing antibody,” Journal of Experimental Medicine, vol. 146, no. 1, pp. 201–217, 1977. View at Publisher · View at Google Scholar · View at Scopus
  155. S. B. Halstead, J. S. Porterfield, and E. J. O'Rourke, “Enhancement of dengue virus infection in monocytes by flavivirus antisera,” American Journal of Tropical Medicine and Hygiene, vol. 29, no. 4, pp. 638–642, 1980. View at Google Scholar · View at Scopus
  156. R. Dulbecco, M. Vogt, and A. G. R. Strickland, “A study of the basic aspects of neutralization of two animal viruses, Western equine encephalitis virus and poliomyelitis virus,” Virology, vol. 2, no. 2, pp. 162–205, 1956. View at Publisher · View at Google Scholar · View at Scopus
  157. L. McLain and N. J. Dimmock, “Single- and multi-hit kinetics of immunoglobulin G neutralization of human immunodeficiency virus type 1 by monoclonal antibodies,” Journal of General Virology, vol. 75, no. 6, pp. 1457–1460, 1994. View at Publisher · View at Google Scholar · View at Scopus
  158. H. P. Taylor, S. J. Armstrong, and N. J. Dimmock, “Quantitative relationships between an influenza virus and neutralizing antibody,” Virology, vol. 159, no. 2, pp. 288–298, 1987. View at Publisher · View at Google Scholar · View at Scopus
  159. M. B. Sherman and S. C. Weaver, “Structure of the recombinant alphavirus western equine encephalitis virus revealed by cryoelectron microscopy,” Journal of Virology, vol. 84, no. 19, pp. 9775–9782, 2010. View at Publisher · View at Google Scholar · View at Scopus
  160. C. H. Andrewes and W. J. Elford, “Observations on anti-phage sera. I: “The percentage law”,” British Journal of Experimental Pathology, vol. 14, no. 6, pp. 368–376, 1933. View at Google Scholar
  161. A. J. Della-Porta and E. G. Westaway, “A multi-hit model for the neutralization of animal viruses,” Journal of General Virology, vol. 38, no. 1, pp. 1–19, 1978. View at Publisher · View at Google Scholar · View at Scopus
  162. T. Berggård, S. Linse, and P. James, “Methods for the detection and analysis of protein-protein interactions,” Proteomics, vol. 7, no. 16, pp. 2833–2842, 2007. View at Publisher · View at Google Scholar · View at Scopus
  163. L. Jason-Moller, M. Murphy, and J. Bruno, “Overview of Biacore systems and their applications,” in Current Protocols in Protein Science, vol. 19, Chapter 19, Unit 19 13, p. 13, 2006. View at Google Scholar
  164. D. Nedelkov and R. W. Nelson, “Surface plasmon resonance mass spectrometry: recent progress and outlooks,” Trends in Biotechnology, vol. 21, no. 7, pp. 301–305, 2003. View at Publisher · View at Google Scholar · View at Scopus
  165. M. Piliarik, H. Vaisocherová, and J. Homola, “Surface plasmon resonance biosensing,” Methods in Molecular Biology, vol. 503, pp. 65–88, 2009. View at Publisher · View at Google Scholar · View at Scopus
  166. R. L. Rich and D. G. Myszka, “Spying on HIV with SPR,” Trends in Microbiology, vol. 11, no. 3, pp. 124–133, 2003. View at Publisher · View at Google Scholar · View at Scopus
  167. F. Vollmer and S. Arnold, “Whispering-gallery-mode biosensing: label-free detection down to single molecules,” Nature Methods, vol. 5, no. 7, pp. 591–596, 2008. View at Publisher · View at Google Scholar · View at Scopus
  168. R. Pantophlet and D. R. Burton, “GP120: target for neutralizing HIV-1 antibodies,” Annual Review of Immunology, vol. 24, pp. 739–769, 2006. View at Publisher · View at Google Scholar · View at Scopus
  169. P. L. Earl, C. C. Broder, D. Long et al., “Native oligomeric human immunodeficiency virus type 1 envelope glycoprotein elicits diverse monoclonal antibody reactivities,” Journal of Virology, vol. 68, no. 5, pp. 3015–3026, 1994. View at Google Scholar · View at Scopus
  170. F. Gao, E. A. Weaver, Z. Lu et al., “Antigenicity and immunogenicity of a synthetic human immunodeficiency virus type 1 group M consensus envelope glycoprotein,” Journal of Virology, vol. 79, no. 2, pp. 1154–1163, 2005. View at Publisher · View at Google Scholar · View at Scopus
  171. J. M. Kovacs, J. P. Nkolola, H. Peng et al., “HIV-1 envelope trimer elicits more potent neutralizing antibody responses than monomeric gp120,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 30, pp. 12111–12116, 2012. View at Publisher · View at Google Scholar · View at Scopus
  172. P. Spearman, M. A. Lally, M. Elizaga et al., “A trimeric, V2-deleted HIV-1 envelope glycoprotein vaccine elicits potent neutralizing antibodies but limited breadth of neutralization in human volunteers,” Journal of Infectious Diseases, vol. 203, no. 8, pp. 1165–1173, 2011. View at Publisher · View at Google Scholar · View at Scopus
  173. X. Yang, J. Lee, E. M. Mahony, P. D. Kwong, R. Wyatt, and J. Sodroski, “Highly stable trimers formed by human immunodeficiency virus type 1 envelope glycoproteins fused with the trimeric motif of T4 bacteriophage fibritin,” Journal of Virology, vol. 76, no. 9, pp. 4634–4642, 2002. View at Publisher · View at Google Scholar · View at Scopus
  174. X. Yang, R. Wyatt, and J. Sodroski, “Improved elicitation of neutralizing antibodies against primary human immunodeficiency viruses by soluble stabilized envelope glycoprotein trimers,” Journal of Virology, vol. 75, no. 3, pp. 1165–1171, 2001. View at Publisher · View at Google Scholar · View at Scopus
  175. J. Julien, J. H. Lee, A. Cupo et al., “Asymmetric recognition of the HIV-1 trimer by broadly neutralizing antibody PG9,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 11, pp. 4351–4356, 2013. View at Publisher · View at Google Scholar · View at Scopus
  176. J. M. Binley, R. W. Sanders, B. Clas et al., “A recombinant human immunodeficiency virus type 1 envelope glycoprotein complex stabilized by an intermolecular disulfide bond between the gp120 and gp41 subunits is an antigenic mimic of the trimeric virion-associated structure,” Journal of Virology, vol. 74, no. 2, pp. 627–643, 2000. View at Publisher · View at Google Scholar · View at Scopus
  177. R. W. Sanders, M. Vesanen, N. Schuelke et al., “Stabilization of the soluble, cleaved, trimeric form of the envelope glycoprotein complex of human immunodeficiency virus type 1,” Journal of Virology, vol. 76, no. 17, pp. 8875–8889, 2002. View at Publisher · View at Google Scholar · View at Scopus
  178. J. M. Binley, R. W. Sanders, A. Master et al., “Enhancing the proteolytic maturation of human immunodeficiency virus type 1 envelope glycoproteins,” Journal of Virology, vol. 76, no. 6, pp. 2606–2616, 2002. View at Publisher · View at Google Scholar · View at Scopus
  179. S. Beddows, M. Franti, A. K. Dey et al., “A comparative immunogenicity study in rabbits of disulfide-stabilized, proteolytically cleaved, soluble trimeric human immunodeficiency virus type 1 gp140, trimeric cleavage-defective gp140 and monomeric gp120,” Virology, vol. 360, no. 2, pp. 329–340, 2007. View at Publisher · View at Google Scholar · View at Scopus
  180. S. Beddows, N. Schülke, M. Kirschner et al., “Evaluating the immunogenicity of a disulfide-stabilized, cleaved, trimeric form of the envelope glycoprotein complex of human immunodeficiency virus type 1,” Journal of Virology, vol. 79, no. 14, pp. 8812–8827, 2005. View at Publisher · View at Google Scholar · View at Scopus
  181. J. P. Julien, A. Cupo, D. Sok et al., “Crystal structure of a soluble cleaved HIV-1 envelope trimer,” Science, vol. 342, pp. 1477–1483, 2013. View at Publisher · View at Google Scholar
  182. D. Lyumkis, J. P. Julien, N. de Val et al., “Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer,” Science, vol. 342, no. 6165, pp. 1484–1490, 2013. View at Publisher · View at Google Scholar
  183. A. Yasmeen, R. Ringe, R. Derking et al., “Differential binding of neutralizing and non-neutralizing antibodies to native-like soluble HIV-1 Env trimers, uncleaved Env proteins, and monomeric subunits,” Retrovirology, vol. 11, article 41, 2014. View at Google Scholar
  184. P. J. Klasse and Q. J. Sattentau, “Mechanisms of virus neutralization by antibody,” Current Topics in Microbiology and Immunology, vol. 260, pp. 87–108, 2001. View at Google Scholar · View at Scopus
  185. J. S. Klein and P. J. Bjorkman, “Few and far between: how HIV may be evading antibody avidity,” PLoS Pathogens, vol. 6, no. 5, pp. 1–6, 2010. View at Publisher · View at Google Scholar · View at Scopus
  186. N. S. Greenspan, “Affinity, complementarity, cooperativity, and specificity in antibody recognition,” Current Topics in Microbiology and Immunology, vol. 260, pp. 65–85, 2001. View at Google Scholar · View at Scopus
  187. N. S. Greenspan, D. A. Dacek, and L. J. N. Cooper, “Cooperative binding of two antibodies to independent antigens by an Fc-dependent mechanism,” The FASEB Journal, vol. 3, no. 10, pp. 2203–2207, 1989. View at Google Scholar · View at Scopus
  188. C. C. LaBranche, T. L. Hoffman, J. Romano et al., “Determinants of CD4 independence for a human immunodeficiency virus type 1 variant map outside regions required for coreceptor specificity,” Journal of Virology, vol. 73, no. 12, pp. 10310–10319, 1999. View at Google Scholar · View at Scopus
  189. C. C. LaBranche, M. M. Sauter, B. S. Haggarty et al., “A single amino acid change in the cytoplasmic domain of the simian immunodeficiency virus transmembrane molecule increases envelope glycoprotein expression on infected cells,” Journal of Virology, vol. 69, no. 9, pp. 5217–5227, 1995. View at Google Scholar · View at Scopus
  190. A. N. Vzorov, K. M. Gernert, and R. W. Compans, “Multiple domains of the SIV Env protein determine virus replication efficiency and neutralization sensitivity,” Virology, vol. 332, no. 1, pp. 89–101, 2005. View at Publisher · View at Google Scholar · View at Scopus
  191. E. Yuste, J. D. Reeves, R. W. Doms, and R. C. Desrosiers, “Modulation of Env content in virions of simian immunodeficiency virus: Correlation with cell surface expression and virion infectivity,” Journal of Virology, vol. 78, no. 13, pp. 6775–6785, 2004. View at Publisher · View at Google Scholar · View at Scopus
  192. J. D. Steckbeck, I. Orlov, A. Chow et al., “Kinetic rates of antibody binding correlate with neutralization sensitivity of variant simian immunodeficiency virus strains,” Journal of Virology, vol. 79, no. 19, pp. 12311–12320, 2005. View at Publisher · View at Google Scholar · View at Scopus
  193. Q. Li, A. G. Yafal, Y. M. Lee, J. Hogle, and M. Chow, “Poliovirus neutralization by antibodies to internal epitopes of VP4 and VP1 results from reversible exposure of these sequences at physiological temperature,” Journal of Virology, vol. 68, no. 6, pp. 3965–3970, 1994. View at Google Scholar · View at Scopus
  194. E. J. Platt, M. M. Gomes, and D. Kabat, “Kinetic mechanism for HIV-1 neutralization by antibody 2G12 entails reversible glycan binding that slows cell entry,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 20, pp. 7829–7834, 2012. View at Publisher · View at Google Scholar · View at Scopus
  195. J. S. Klein, P. N. P. Gnanapragasam, R. P. Galimidi, C. P. Foglesong, A. P. West Jr., and P. J. Bjorkman, “Examination of the contributions of size and avidity to the neutralization mechanisms of the anti-HIV antibodies b12 and 4E10,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 18, pp. 7385–7390, 2009. View at Publisher · View at Google Scholar · View at Scopus
  196. A. F. Labrijn, P. Poignard, A. Raja et al., “Access of antibody molecules to the conserved coreceptor binding site on glycoprotein gp120 is sterically restricted on primary human immunodeficiency virus type 1,” Journal of Virology, vol. 77, no. 19, pp. 10557–10565, 2003. View at Publisher · View at Google Scholar · View at Scopus
  197. S. P. Layne, M. J. Merges, M. Dembo et al., “Factors underlying spontaneous inactivation and susceptibility to neutralization of human immunodeficiency virus,” Virology, vol. 189, no. 2, pp. 695–714, 1992. View at Publisher · View at Google Scholar · View at Scopus
  198. J. P. Moore, J. A. Mckeating, R. A. Weiss, and Q. J. Sattentau, “Dissociation of gp120 from HIV-1 virions induced by soluble CD4,” Science, vol. 250, no. 4984, pp. 1139–1142, 1990. View at Publisher · View at Google Scholar · View at Scopus
  199. E. J. Platt, J. P. Durnin, and D. Kabat, “Kinetic factors control efficiencies of cell entry, efficacies of entry inhibitors, and mechanisms of adaptation of human immunodeficiency virus,” Journal of Virology, vol. 79, no. 7, pp. 4347–4356, 2005. View at Publisher · View at Google Scholar · View at Scopus
  200. E. G. Westaway, “The neutralization of arboviruses, II: neutralization in heterologous virus-serum mixtures with four group B arboviruses,” Virology, vol. 26, no. 4, pp. 528–537, 1965. View at Publisher · View at Google Scholar · View at Scopus
  201. P. J. Klasse and D. R. Burton, “Antibodies to West Nile virus: a double-edged sword,” Cell Host and Microbe, vol. 1, no. 2, pp. 87–89, 2007. View at Publisher · View at Google Scholar · View at Scopus
  202. C. Herrera, P. J. Klasse, C. W. Kibler, E. Michael, J. P. Moore, and S. Beddows, “Dominant-negative effect of hetero-oligomerization on the function of the human immunodeficiency virus type 1 envelope glycoprotein complex,” Virology, vol. 351, no. 1, pp. 121–132, 2006. View at Publisher · View at Google Scholar · View at Scopus
  203. C. H. Andrewes and W. J. Elford, “Observations on anti-phage sera. II: properties of incompletely neutralized phage,” British Journal of Experimental Pathology, vol. 14, no. 6, pp. 376–383, 1933. View at Google Scholar
  204. C. Wohlfart, “Neutralization of adenoviruses: kinetics, stoichiometry, and mechanisms,” Journal of Virology, vol. 62, no. 7, pp. 2321–2328, 1988. View at Google Scholar · View at Scopus
  205. P. J. Klasse, “Neutralization of infectivity,” in Encyclopedia of Virology, Elsevier-Academic Press, 3rd edition, 2008. View at Google Scholar
  206. J. Icenogle, H. Shiwen, G. Duke, S. Gilbert, R. Rueckert, and J. Anderegg, “Neutralization of poliovirus by a monoclonal antibody: kinetics and stoichiometry,” Virology, vol. 127, no. 2, pp. 412–425, 1983. View at Publisher · View at Google Scholar · View at Scopus
  207. K. M. Murphy, Janeway's Immunobiology, New York, NY, USA, 2012.
  208. S. P. Layne, M. J. Merges, J. L. Spouge, M. Dembo, and P. L. Nara, “Blocking of human immunodeficiency virus infection depends on cell density and viral stock age,” Journal of Virology, vol. 65, no. 6, pp. 3293–3300, 1991. View at Google Scholar · View at Scopus
  209. J. Daecke, O. T. Fackler, M. T. Dittmar, and H. Kräusslich, “Involvement of clathrin-mediated endocytosis in human immunodeficiency virus type 1 entry,” Journal of Virology, vol. 79, no. 3, pp. 1581–1594, 2005. View at Publisher · View at Google Scholar · View at Scopus
  210. B. M. Dale, G. P. McNerney, D. L. Thompson et al., “Cell-to-cell transfer of HIV-1 via virological synapses leads to endosomal virion maturation that activates viral membrane fusion,” Cell Host and Microbe, vol. 10, no. 6, pp. 551–562, 2011. View at Publisher · View at Google Scholar · View at Scopus
  211. L. von Kleist, W. Stahlschmidt, H. Bulut et al., “Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition,” Cell, vol. 146, pp. 471–484, 2011. View at Google Scholar
  212. F. M. Burnet, E. V. Keogh, and D. Lush, “The immunological reactions of the filterable viruses,” The Australian Journal of Experimental Biology and Medical Science, vol. 15, no. 3, pp. 227–368, 1937. View at Publisher · View at Google Scholar
  213. R. M. Iorio and M. A. Bratt, “Neutralization of Newcastle disease virus by monoclonal antibodies to the hemagglutinin-neuraminidase glycoprotein: requirement for antibodies to four sites for complete neutralization,” Journal of Virology, vol. 51, no. 2, pp. 445–451, 1984. View at Google Scholar · View at Scopus
  214. R. M. Iorio and M. A. Bratt, “Selection of unique antigenic variants of Newcastle disease virus with neutralizing monoclonal antibodies and anti-immunoglobulin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 82, no. 20, pp. 7106–7110, 1985. View at Google Scholar · View at Scopus
  215. R. Pejchal, L. M. Walker, R. L. Stanfield et al., “Structure and function of broadly reactive antibody PG16 reveal an H3 subdomain that mediates potent neutralization of HIV-1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 25, pp. 11483–11488, 2010. View at Publisher · View at Google Scholar · View at Scopus
  216. Q. Vos, E. A. Klasen, and J. J. Haaijman, “The effect of divalent and univalent binding on antibody titration curves in solid-phase ELISA,” Journal of Immunological Methods, vol. 103, no. 1, pp. 47–54, 1987. View at Publisher · View at Google Scholar · View at Scopus
  217. R. Derking et al., submitted, 2014.
  218. S. Laal, S. Burda, M. K. Gorny, S. Karwowska, A. Buchbinder, and S. Zolla-Pazner, “Synergistic neutralization of human immunodeficiency virus type 1 by combinations of human monoclonal antibodies,” Journal of Virology, vol. 68, no. 6, pp. 4001–4008, 1994. View at Google Scholar · View at Scopus
  219. T. J. Ketas, S. Holuigue, K. Matthews, J. P. Moore, and P. J. Klasse, “Env-glycoprotein heterogeneity as a source of apparent synergy and enhanced cooperativity in inhibition of HIV-1 infection by neutralizing antibodies and entry inhibitors,” Virology, vol. 422, no. 1, pp. 22–36, 2012. View at Publisher · View at Google Scholar · View at Scopus
  220. M. C. Berenbaum, “What is synergy?” Pharmacological Reviews, vol. 41, no. 2, pp. 93–141, 1989. View at Google Scholar · View at Scopus
  221. A. V. Hill, “The combinations of haemoglobin with oxygen and with carbon monoxide. I,” Biochemical Journal, vol. 7, no. 5, pp. 471–480, 1913. View at Google Scholar
  222. A. Hoffman and A. Goldberg, “The relationship between receptor-effector unit heterogeneity and the shape of the concentration-effect profile: pharmacodynamic implications,” Journal of Pharmacokinetics and Biopharmaceutics, vol. 22, no. 6, pp. 449–468, 1994. View at Publisher · View at Google Scholar · View at Scopus
  223. J. N. Weiss, “The Hill equation revisited: uses and misuses,” The FASEB Journal, vol. 11, no. 11, pp. 835–841, 1997. View at Google Scholar · View at Scopus
  224. W. R. Greco, G. Bravo, and J. C. Parsons, “The search for synergy: a critical review from a response surface perspective,” Pharmacological Reviews, vol. 47, no. 2, pp. 331–385, 1995. View at Google Scholar · View at Scopus