Neutralizing igG at the portal of infection mediates protection against vaginal simian/human immunodeficiency virus challenge

Journal of Virology

Volumn 87, Issue 21, 2013, Pages 11603-11616

  Klein, Katja ^a   Veazey, Ronald S ^b   Warrier, Ranjit ^d   Hraber, Peter ^e   Doyle Meyers, Lara A ^b   Buffa, Viviana ^a   Liao, Hua Xin ^c   Haynes, Barton F ^c   Shaw, George M ^d   Shattock, Robin J ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e LOS ALAMOS NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN F(AB')2 FRAGMENT; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; NEUTRALIZING ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; IMMUNOGLOBULIN G;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DETECTION; ANTIVIRAL ACTIVITY; ARTICLE; BODY WEIGHT; DRUG BLOOD LEVEL; DRUG DISTRIBUTION; DRUG POTENCY; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN TISSUE; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; TARGET CELL; UTERINE CERVIX; VAGINITIS; VIRUS IMMUNITY; ANIMAL; DOSE RESPONSE; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; SEXUALLY TRANSMITTED DISEASE; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; TREATMENT OUTCOME; SEXUALLY TRANSMITTED DISEASES;

ANIMALS; ANTIBODIES, NEUTRALIZING; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; HIV ANTIBODIES; HIV-1; HUMANS; IMMUNOGLOBULIN G; MACACA MULATTA; SEXUALLY TRANSMITTED DISEASES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; TREATMENT OUTCOME;

EID: 84886902378     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01361-13     Document Type: Article

References (79)

1. Haase AT. 2005. Perils at mucosal front lines for HIV and SIV and their hosts. Nat. Rev. Immunol. 5:783-792.
2. Baba TW, Liska V, Hofmann-Lehmann R, Vlasak J, Xu W, Ayehunie S, Cavacini LA, Posner MR, Katinger H, Stiegler G, Bernacky BJ, Rizvi TA, Schmidt R, Hill LR, Keeling ME, Lu Y, Wright JE, Chou TC, Ruprecht RM. 2000. Human neutralizing monoclonal antibodies of the IgG1 subtype protect against mucosal simian-human immunodeficiency virus infection. Nat. Med. 6:200-206.
3. Hessell AJ, Rakasz EG, Poignard P, Hangartner L, Landucci G, Forthal DN, KoffWC, Watkins DI, Burton DR. 2009. Broadly neutralizing human anti-HIV antibody 2G12 is effective in protection against mucosal SHIV challenge even at low serum neutralizing titers. PLoS Pathog. 5:e1000433.
4. Mascola JR, Lewis MG, Stiegler G, Harris D, VanCott TC, Hayes D, Louder MK, Brown CR, Sapan CV, Frankel SS, Lu Y, Robb ML, Katinger H, Birx DL. 1999. Protection of macaques against pathogenic simian/human immunodeficiency virus 89.6PD by passive transfer of neutralizing antibodies. J. Virol. 73:4009-4018.
5. Mascola JR, Stiegler G, VanCott TC, Katinger H, Carpenter CB, Hanson CE, Beary H, Hayes D, Frankel SS, Birx DL, Lewis MG. 2000. Protection of macaques against vaginal transmission of a pathogenic HIV- 1/SIV chimeric virus by passive infusion of neutralizing antibodies. Nat. Med. 6:207-210.
6. Parren PW, Marx PA, Hessell AJ, Luckay A, Harouse J, Cheng-Mayer C, Moore JP, Burton DR. 2001. Antibody protects macaques against vaginal challenge with a pathogenic R5 simian/human immunodeficiency virus at serum levels giving complete neutralization in vitro. J. Virol. 75: 8340-8347.
7. Xu W, Hofmann-Lehmann R, McClure HM, Ruprecht RM. 2002. Passive immunization with human neutralizing monoclonal antibodies: correlates of protective immunity against HIV. Vaccine 20:1956-1960.
8. Burton DR, Hessell AJ, Keele BF, Klasse PJ, Ketas TA, Moldt B, Dunlop DC, Poignard P, Doyle LA, Cavacini L, Veazey RS, Moore JP. 2011. Limited or no protection by weakly or nonneutralizing antibodies against vaginal SHIV challenge of macaques compared with a strongly neutralizing antibody. Proc. Natl. Acad. Sci. U. S. A. 108:11181-11186.
9. Moog C, Dereuddre-Bosquet N, Teillaud JL, Biedma ME, Holl V, VanHam G, Heyndrickx L, Van Dorsselaer V, Katinger D, Vcelar B, Zolla-Pazner S, Mangeot I, Kelly C, Shattock RJ, Le Grand R. 2013. Protective effect of vaginal application of neutralizing and nonneutralizing inhibitory antibodies against vaginal SHIV challenge in macaques. Mucosal Immunol. [Epub ahead of print.]
10. Veazey RS, Shattock RJ, Pope M, Kirijan JC, Jones J, Hu Q, Ketas T, Marx PA, Klasse PJ, Burton DR, Moore JP. 2003. Prevention of virus transmission to macaque monkeys by a vaginally applied monoclonal antibody to HIV-1 gp120. Nat. Med. 9:343-346.
11. Buchacher A, Predl R, Strutzenberger K, Steinfellner W, Trkola A, Purtscher M, Gruber G, Tauer C, Steindl F, Jungbauer A, et al. 1994. Generation of human monoclonal antibodies against HIV-1 proteins; electrofusion and Epstein-Barr virus transformation for peripheral blood lymphocyte immortalization. AIDS Res. Hum. Retrovir. 10:359-369.
12. Burton DR, Pyati J, Koduri R, Sharp SJ, Thornton GB, Parren PW, Sawyer LS, Hendry RM, Dunlop N, Nara PL, Lamacchia M, Garratty E, Stiehm ER, Bryson YJ, Cao Y, Moore JP, Ho DD, Barbas CF, III. 1994. Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 266:1024-1027.
13. Stiegler G, Kunert R, Purtscher M, Wolbank S, Voglauer R, Steindl F, Katinger H. 2001. A potent cross-clade neutralizing human monoclonal antibody against a novel epitope on gp41 of human immunodeficiency virus type 1. AIDS Res. Hum. Retrovir. 17:1757-1765.
14. Walker LM, Phogat SK, Chan-Hui PY, Wagner D, Phung P, Goss JL, Wrin T, Simek MD, Fling S, Mitcham JL, Lehrman JK, Priddy FH, Olsen OA, Frey SM, Hammond PW, Kaminsky S, Zamb T, Moyle M, KoffWC, Poignard P, Burton DR. 2009. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326:285-289.
15. Wu X, Yang ZY, Li Y, Hogerkorp CM, Schief WR, Seaman MS, Zhou T, Schmidt SD, Wu L, Xu L, Longo NS, McKee K, O'Dell S, Louder MK, WycuffDL, Feng Y, Nason M, Doria-Rose N, Connors M, Kwong PD, Roederer M, Wyatt RT, Nabel GJ, Mascola JR. 2010. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329:856-861.
16. Mazanec MB, Nedrud JG, Kaetzel CS, Lamm ME. 1993. A three-tiered view of the role of IgA in mucosal defense. Immunol. Today 14:430-435.
17. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, Paris R, Premsri N, Namwat C, de Souza M, Adams E, Benenson M, Gurunathan S, Tartaglia J, McNeil JG, Francis DP, Stablein D, Birx DL, Chunsuttiwat S, Khamboonruang C, Thongcharoen P, Robb ML, Michael NL, Kunasol P, Kim JH. 2009. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361: 2209-2220.
18. Haynes BF, Gilbert PB, McElrath MJ, Zolla-Pazner S, Tomaras GD, Alam SM, Evans DT, Montefiori DC, Karnasuta C, Sutthent R, Liao HX, DeVico AL, Lewis GK, Williams C, Pinter A, Fong Y, Janes H, DeCamp A, Huang Y, Rao M, Billings E, Karasavvas N, Robb ML, Ngauy V, de Souza MS, Paris R, Ferrari G, Bailer RT, Soderberg KA, Andrews C, Berman PW, Frahm N, De Rosa SC, Alpert MD, Yates NL, Shen X, Koup RA, Pitisuttithum P, Kaewkungwal J, Nitayaphan S, Rerks-Ngarm S, Michael NL, Kim JH. 2012. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N. Engl. J. Med. 366:1275-1286.
19. Kunert R, Steinfellner W, Purtscher M, Assadian A, Katinger H. 2000. Stable recombinant expression of the anti HIV-1 monoclonal antibody 2F5 after IgG3/IgG1 subclass switch in CHO cells. Biotechnol. Bioeng. 67:97-103.
20. Binley JM, Wrin T, Korber B, Zwick MB, Wang M, Chappey C, Stiegler G, Kunert R, Zolla-Pazner S, Katinger H, Petropoulos CJ, Burton DR. Comprehensive cross-clade neutralization analysis of a panel of anti- human immunodeficiency virus type 1 monoclonal antibodies. J. Virol. 78:13232-13252.
21. Chakrabarti BK, Walker LM, Guenaga JF, Ghobbeh A, Poignard P, Burton DR, Wyatt RT. 2011. Direct antibody access to the HIV-1 membrane- proximal external region positively correlates with neutralization sensitivity. J. Virol. 85:8217-8226.
22. Alam SM, Morelli M, Dennison SM, Liao HX, Zhang R, Xia SM, Rits-Volloch S, Sun L, Harrison SC, Haynes BF, Chen B. 2009. Role of HIV membrane in neutralization by two broadly neutralizing antibodies. Proc. Natl. Acad. Sci. U. S. A. 106:20234-20239.
23. Frey G, Peng H, Rits-Volloch S, Morelli M, Cheng Y, Chen B. 2008. A fusion-intermediate state of HIV-1 gp41 targeted by broadly neutralizing antibodies. Proc. Natl. Acad. Sci. U. S. A. 105:3739-3744.
24. Guenaga J, Wyatt RT. 2012. Structure-guided alterations of the gp41-directed HIV-1 broadly neutralizing antibody 2F5 reveal new properties regarding its neutralizing function. PLoS Pathog. 8:e1002806.
25. Holl V, Hemmerter S, Burrer R, Schmidt S, Bohbot A, Aubertin AM, Moog C. 2004. Involvement of Fc gamma RI (CD64) in the mechanism of HIV-1 inhibition by polyclonal IgG purified from infected patients in cultured monocyte-derived macrophages. J. Immunol. 173:6274-6283.
26. Holl V, Peressin M, Decoville T, Schmidt S, Zolla-Pazner S, Aubertin AM, Moog C. 2006. Nonneutralizing antibodies are able to inhibit human immunodeficiency virus type 1 replication in macrophages and immature dendritic cells. J. Virol. 80:6177-6181.
27. Holl V, Peressin M, Schmidt S, Decoville T, Zolla-Pazner S, Aubertin AM, Moog C. 2006. Efficient inhibition of HIV-1 replication in human immature monocyte-derived dendritic cells by purified anti-HIV-1 IgG without induction of maturation. Blood 107:4466-4474.
28. Perez LG, Zolla-Pazner S, Montefiori DC. 2013. Antibody-dependent, FcgammaRI-mediated neutralization of HIV-1 in TZM-bl cells occurs independently of phagocytosis. J. Virol. 87:5287-5290.
29. Tudor D, Bomsel M. 2011. The broadly neutralizing HIV-1 IgG 2F5 elicits gp41-specific antibody-dependent cell cytotoxicity in a FcgammaRI- dependent manner. AIDS 25:751-759.
30. Chakrabarti BK, Pancera M, Phogat S, O'Dell S, McKee K, Guenaga J, Robinson J, Mascola J, Wyatt RT. 2011. HIV type 1 Env precursor cleavage state affects recognition by both neutralizing and nonneutralizing gp41 antibodies. AIDS Res. Hum. Retrovir. 27:877-887.
31. Bomsel M, Heyman M, Hocini H, Lagaye S, Belec L, Dupont C, Desgranges C. 1998. Intracellular neutralization of HIV transcytosis across tight epithelial barriers by anti-HIV envelope protein dIgA or IgM. Immunity 9:277-287.
32. Shen R, Drelichman ER, Bimczok D, Ochsenbauer C, Kappes JC, Cannon JA, Tudor D, Bomsel M, Smythies LE, Smith PD. 2010. GP41-specific antibody blocks cell-free HIV type 1 transcytosis through human rectal mucosa and model colonic epithelium. J. Immunol. 184:3648-3655.
33. Liao HX, Levesque MC, Nagel A, Dixon A, Zhang R, Walter E, Parks R, Whitesides J, Marshall DJ, Hwang KK, Yang Y, Chen X, Gao F, Munshaw S, Kepler TB, Denny T, Moody MA, Haynes BF. 2009. High-throughput isolation of immunoglobulin genes from single human B cells and expression as monoclonal antibodies. J. Virol. Methods 158: 171-179.
34. Nicely NI, Dennison SM, Spicer L, Scearce RM, Kelsoe G, Ueda Y, Chen H, Liao HX, Alam SM, Haynes BF. 2010. Crystal structure of a nonneutralizing antibody to the HIV-1 gp41 membrane-proximal external region. Nat. Struct. Mol. Biol. 17:1492-1494.
35. Ofek G, Tang M, Sambor A, Katinger H, Mascola JR, Wyatt R, Kwong PD. 2004. Structure and mechanistic analysis of the anti-human immunodeficiency virus type 1 antibody 2F5 in complex with its gp41 epitope. J. Virol. 78:10724-10737.
36. Kunert R, Ruker F, Katinger H. 1998. Molecular characterization of five neutralizing anti-HIV type 1 antibodies: identification of nonconventional D segments in the human monoclonal antibodies 2G12 and 2F5. AIDS Res. Hum. Retrovir. 14:1115-1128.
37. Johnson V, Byington R. 1990. Quantitative assay for virus infectivity: infectivity assay (virus yield assay), p 71-76. In Aldovini A, Walker BD (ed), Techniques in HIV research. Stockton Press, New York, NY.
38. Balzarini J, Van Laethem K, Hatse S, Froeyen M, Peumans W, Van Damme E, Schols D. 2005. Carbohydrate-binding agents cause deletions of highly conserved glycosylation sites in HIV GP120: a new therapeutic concept to hit the Achilles heel of HIV. J. Biol. Chem. 280:41005-41014.
39. Fletcher P, Kiselyeva Y, Wallace G, Romano J, Griffin G, Margolis L, Shattock R. 2005. The nonnucleoside reverse transcriptase inhibitor UC- 781 inhibits human immunodeficiency virus type 1 infection of human cervical tissue and dissemination by migratory cells. J. Virol. 79:11179-11186.
40. Greenhead P, Hayes P, Watts PS, Laing KG, Griffin GE, Shattock RJ. Parameters of human immunodeficiency virus infection of human cervical tissue and inhibition by vaginal virucides. J. Virol. 74:5577-5586.
41. Hu Q, Frank I, Williams V, Santos JJ, Watts P, Griffin GE, Moore JP, Pope M, Shattock RJ. 2004. Blockade of attachment and fusion receptors inhibits HIV-1 infection of human cervical tissue. J. Exp. Med. 199:1065-1075.
42. National Research Council. 1996. Guide for the care and use of laboratory animals. National Academy Press, Washington, DC.
43. Marx PA, Spira AI, Gettie A, Dailey PJ, Veazey RS, Lackner AA, Mahoney CJ, Miller CJ, Claypool LE, Ho DD, Alexander NJ. 1996. Progesterone implants enhance SIV vaginal transmission and early virus load. Nat. Med. 2:1084-1089.
44. Keele BF, Li H, Learn GH, Hraber P, Giorgi EE, Grayson T, Sun C, Chen Y, Yeh WW, Letvin NL, Mascola JR, Nabel GJ, Haynes BF, Bhattacharya T, Perelson AS, Korber BT, Hahn BH, Shaw GM. 2009. Low-dose rectal inoculation of rhesus macaques by SIVsmE660 or SIVmac251 recapitulates human mucosal infection by HIV-1. J. Exp. Med. 206:1117-1134.
45. Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, Middel J, Cornelissen IL, Nottet HS, KewalRamani VN, Littman DR, Figdor CG, van Kooyk Y. 2000. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100: 587-597.
46. Izquierdo-Useros N, Lorizate M, Puertas MC, Rodriguez-Plata MT, Zangger N, Erikson E, Pino M, Erkizia I, Glass B, Clotet B, Keppler OT, Telenti A, Krausslich HG, Martinez-Picado J. 2012. Siglec-1 is a novel dendritic cell receptor that mediates HIV-1 trans-infection through recognition of viral membrane gangliosides. PLoS Biol. 10:e1001448.
47. Puryear WB, Akiyama H, Geer SD, Ramirez NP, Yu X, Reinhard BM, Gummuluru S. 2013. Interferon-inducible mechanism of dendritic cellmediated HIV-1 dissemination is dependent on Siglec-1/CD169. PLoS Pathog. 9:e1003291.
48. Parrish NF, Gao F, Li H, Giorgi EE, Barbian HJ, Parrish EH, Zajic L, Iyer SS, Decker JM, Kumar A, Hora B, Berg A, Cai F, Hopper J, Denny TN, Ding H, Ochsenbauer C, Kappes JC, Galimidi RP, West AP, Jr, Bjorkman PJ, Wilen CB, Doms RW, O'Brien M, Bhardwaj N, Borrow P, Haynes BF, Muldoon M, Theiler JP, Korber B, Shaw GM, Hahn BH. Phenotypic properties of transmitted founder HIV-1. Proc. Natl. Acad. Sci. U. S. A. 110:6626-6633.
49. Abrahams MR, Anderson JA, Giorgi EE, Seoighe C, Mlisana K, Ping LH, Athreya GS, Treurnicht FK, Keele BF, Wood N, Salazar-Gonzalez JF, Bhattacharya T, Chu H, Hoffman I, Galvin S, Mapanje C, Kazembe P, Thebus R, Fiscus S, Hide W, Cohen MS, Karim SA, Haynes BF, Shaw GM, Hahn BH, Korber BT, Swanstrom R, Williamson C. 2009. Quantitating the multiplicity of infection with human immunodeficiency virus type 1 subtype C reveals a non-Poisson distribution of transmitted variants. J. Virol. 83:3556-3567.
50. Haaland RE, Hawkins PA, Salazar-Gonzalez J, Johnson A, Tichacek A, Karita E, Manigart O, Mulenga J, Keele BF, Shaw GM, Hahn BH, Allen SA, Derdeyn CA, Hunter E. 2009. Inflammatory genital infections mitigate a severe genetic bottleneck in heterosexual transmission of subtype A and C HIV-1. PLoS Pathog. 5:e1000274.
51. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, Salazar MG, Sun C, Grayson T, Wang S, Li H, Wei X, Jiang C, Kirchherr JL, Gao F, Anderson JA, Ping LH, Swanstrom R, Tomaras GD, Blattner WA, Goepfert PA, Kilby JM, Saag MS, Delwart EL, Busch MP, Cohen MS, Montefiori DC, Haynes BF, Gaschen B, Athreya GS, Lee HY, Wood N, Seoighe C, Perelson AS, Bhattacharya T, Korber BT, Hahn BH, Shaw GM. 2008. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc. Natl. Acad. Sci. U. S. A. 105:7552-7557.
52. Salazar-Gonzalez JF, Salazar MG, Keele BF, Learn GH, Giorgi EE, Li H, Decker JM, Wang S, Baalwa J, Kraus MH, Parrish NF, Shaw KS, Guffey MB, Bar KJ, Davis KL, Ochsenbauer-Jambor C, Kappes JC, Saag MS, Cohen MS, Mulenga J, Derdeyn CA, Allen S, Hunter E, Markowitz M, Hraber P, Perelson AS, Bhattacharya T, Haynes BF, Korber BT, Hahn BH, Shaw GM. 2009. Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J. Exp. Med. 206:1273-1289.
53. Lee HY, Giorgi EE, Keele BF, Gaschen B, Athreya GS, Salazar-Gonzalez JF, Pham KT, Goepfert PA, Kilby JM, Saag MS, Delwart EL, Busch MP, Hahn BH, Shaw GM, Korber BT, Bhattacharya T, Perelson AS. 2009. Modeling sequence evolution in acute HIV-1 infection. J. Theor. Biol. 261:341-360.
54. Wolbank S, Kunert R, Stiegler G, Katinger H. 2003. Characterization of human class-switched polymeric (immunoglobulin M [IgM] and IgA) anti-human immunodeficiency virus type 1 antibodies 2F5 and 2G12. J. Virol. 77:4095-4103.
55. Tudor D, Yu H, Maupetit J, Drillet AS, Bouceba T, Schwartz-Cornil I, Lopalco L, Tuffery P, Bomsel M. 2012. Isotype modulates epitope specificity, affinity, and antiviral activities of anti-HIV-1 human broadly neutralizing 2F5 antibody. Proc. Natl. Acad. Sci. U. S. A. 109:12680-12685.
56. Perez LG, Costa MR, Todd CA, Haynes BF, Montefiori DC. 2009. Utilization of immunoglobulin G Fc receptors by human immunodeficiency virus type 1: a specific role for antibodies against the membraneproximal external region of gp41. J. Virol. 83:7397-7410.
57. Peressin M, Holl V, Schmidt S, Decoville T, Mirisky D, Lederle A, Delaporte M, Xu K, Aubertin AM, Moog C. 2011. HIV-1 replication in Langerhans and interstitial dendritic cells is inhibited by neutralizing and Fc-mediated inhibitory antibodies. J. Virol. 85:1077-1085.
58. Su B, Xu K, Lederle A, Peressin M, Biedma ME, Laumond G, Schmidt S, Decoville T, Proust A, Lambotin M, Holl V, Moog C. 2012. Neutralizing antibodies inhibit HIV-1 transfer from primary dendritic cells to autologous CD4 T lymphocytes. Blood 120:3708-3717.
59. Merbah M, Arakelyan A, Edmonds T, Ochsenbauer C, Kappes JC, Shattock RJ, Grivel JC, Margolis LB. 2012. HIV-1 expressing the envelopes of transmitted/founder or control/reference viruses have similar infection patterns of CD4 T-cells in human cervical tissue ex vivo. PLoS One 7:e50839.
60. Bazin-Redureau MI, Renard CB, Scherrmann JM. 1997. Pharmacokinetics of heterologous and homologous immunoglobulin G, F(ab=)2 and Fab after intravenous administration in the rat. J. Pharm. Pharmacol. 49:277-281.
61. Sedlacek HH, Gronski P, Hofstaetter T, Kanzy EJ, Schorlemmer HU, Seiler FR. 1983. The biological properties of immunoglobulin G and its split products [F(ab=)2 and Fab]. Klin. Wochenschr. 61:723-736.
62. Covell DG, Barbet J, Holton OD, Black CD, Parker RJ, Weinstein JN. Pharmacokinetics of monoclonal immunoglobulin G1, F(ab=)2, and Fab= in mice. Cancer Res. 46:3969-3978.
63. Ghetie V, Hubbard JG, Kim JK, Tsen MF, Lee Y, Ward ES. 1996. Abnormally short serum half-lives of IgG in beta 2-microglobulindeficient mice. Eur. J. Immunol. 26:690-696.
64. Israel EJ, Taylor S, Wu Z, Mizoguchi E, Blumberg RS, Bhan A, Simister NE. 1997. Expression of the neonatal Fc receptor, FcRn, on human intestinal epithelial cells. Immunology 92:69-74.
65. Israel EJ, Wilsker DF, Hayes KC, Schoenfeld D, Simister NE. 1996. Increased clearance of IgG in mice that lack beta 2-microglobulin: possible protective role of FcRn. Immunology 89:573-578.
66. Junghans RP, Anderson CL. 1996. The protection receptor for IgG catabolism is the beta2-microglobulin-containing neonatal intestinal transport receptor. Proc. Natl. Acad. Sci. U. S. A. 93:5512-5516.
67. Zhu X, Meng G, Dickinson BL, Li X, Mizoguchi E, Miao L, Wang Y, Robert C, Wu B, Smith PD, Lencer WI, Blumberg RS. 2001. MHC class I-related neonatal Fc receptor for IgG is functionally expressed in monocytes, intestinal macrophages, and dendritic cells. J. Immunol. 166:3266-3276.
68. Dall'Acqua WF, Woods RM, Ward ES, Palaszynski SR, Patel NK, Brewah YA, Wu H, Kiener PA, Langermann S. 2002. Increasing the affinity of a human IgG1 for the neonatal Fc receptor: biological consequences. J. Immunol. 169:5171-5180.
69. Armbruster C, Stiegler GM, Vcelar BA, Jager W, Koller U, Jilch R, Ammann CG, Pruenster M, Stoiber H, Katinger HW. 2004. Passive immunization with the anti-HIV-1 human monoclonal antibody (hMAb) 4E10 and the hMAb combination 4E10/2F5/2G12. J. Antimicrob. Chemother. 54:915-920.
70. Junghans RP. 1997. Finally! The Brambell receptor (FcRB). Mediator of transmission of immunity and protection from catabolism for IgG. Immunol. Res. 16:29-57.
71. Li Z, Palaniyandi S, Zeng R, Tuo W, Roopenian DC, Zhu X. 2011. Transfer of IgG in the female genital tract byMHCclass I-related neonatal Fc receptor (FcRn) confers protective immunity to vaginal infection. Proc. Natl. Acad. Sci. U. S. A. 108:4388-4393.
72. Derdeyn CA, Decker JM, Bibollet-Ruche F, Mokili JL, Muldoon M, Denham SA, Heil ML, Kasolo F, Musonda R, Hahn BH, Shaw GM, Korber BT, Allen S, Hunter E. 2004. Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission. Science 303:2019-2022.
73. Chomont N, Hocini H, Gody JC, Bouhlal H, Becquart P, Krief-Bouillet C, Kazatchkine M, Belec L. 2008. Neutralizing monoclonal antibodies to human immunodeficiency virus type 1 do not inhibit viral transcytosis through mucosal epithelial cells. Virology 370:246-254.
74. Garg A, Balthasar JP. 2007. Physiologically-based pharmacokinetic (PBPK) model to predict IgG tissue kinetics in wild-type and FcRnknockout mice. J. Pharmacokinet. Pharmacodyn. 34:687-709.
75. Raux M, Finkielsztejn L, Salmon-Ceron D, Bouchez H, Excler JL, Dulioust E, Grouin JM, Sicard D, Blondeau C. 2000. IgG subclass distribution in serum and various mucosal fluids of HIV type 1-infected subjects. AIDS Res. Hum. Retrovir. 16:583-594.
76. Hessell AJ, Hangartner L, Hunter M, Havenith CE, Beurskens FJ, Bakker JM, Lanigan CM, Landucci G, Forthal DN, Parren PW, Marx PA, Burton DR. 2007. Fc receptor but not complement binding is important in antibody protection against HIV. Nature 449:101-104.
77. Pudney J, Quayle AJ, Anderson DJ. 2005. Immunological microenvironments in the human vagina and cervix: mediators of cellular immunity are concentrated in the cervical transformation zone. Biol. Reprod. 73: 1253-1263.
78. Moldt B, Shibata-Koyama M, Rakasz EG, Schultz N, Kanda Y, Dunlop DC, Finstad SL, Jin C, Landucci G, Alpert MD, Dugast AS, Parren PW, Nimmerjahn F, Evans DT, Alter G, Forthal DN, Schmitz JE, Iida S, Poignard P, Watkins DI, Hessell AJ, Burton DR. 2012. A nonfucosylated variant of the anti-HIV-1 monoclonal antibody b12 has enhanced FcgammaRIIIa- mediated antiviral activity in vitro but does not improve protection against mucosal SHIV challenge in macaques. J. Virol. 86:6189-6196.
79. Huang J, Ofek G, Laub L, Louder MK, Doria-Rose NA, Longo NS, Imamichi H, Bailer RT, Chakrabarti B, Sharma SK, Alam SM, Wang T, Yang Y, Zhang B, Migueles SA, Wyatt R, Haynes BF, Kwong PD, Mascola JR, Connors M. 2012. Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 491:406-412.