GP41-specific antibody blocks cell-free HIV type 1 transcytosis through human rectal mucosa and model colonic epithelium

Journal of Immunology

Volumn 184, Issue 7, 2010, Pages 3648-3655

  Shen, Ruizhong ^a   Drelichman, Ernesto R ^c   Bimczok, Diane ^a   Ochsenbauer, Christina ^b   Kappes, John C ^b   Cannon, Jamie A ^c   Tudor, Daniela ^d   Bomsel, Morgane ^d   Smythies, Lesley E ^a   Smith, Phillip D ^a,e  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c Kentucky   (United States)

^d INSTITUT COCHIN   (France)

^e BIRMINGHAM VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; CARDIOLIPIN; CHEMOKINE RECEPTOR CCR5; DIMER; EPITOPE; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN M; MONOCLONAL ANTIBODY 2F5; MONOCLONAL ANTIBODY 7B2; MONOCLONAL ANTIBODY IS4; MONOMER; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; GP41 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; VIRUS ANTIBODY;

APICAL MEMBRANE; ARTICLE; BASOLATERAL MEMBRANE; CELL FREE SYSTEM; CELL POLARITY; CELL TYPE; COLON MUCOSA; COLUMNAR EPITHELIUM; CONTROLLED STUDY; EXPLANT; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INOCULATION; INTESTINE EPITHELIUM CELL; MEMBRANE VESICLE; MONOLAYER CULTURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RECTUM MUCOSA; TRANSCYTOSIS; VIRUS STRAIN; VIRUS TRANSMISSION; CELL STRAIN HT29; DISEASE TRANSMISSION; EPITHELIUM CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; INTESTINE MUCOSA; RECTUM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIROLOGY;

ANTI-HIV AGENTS; ANTIBODIES, VIRAL; EPITHELIAL CELLS; HIV ENVELOPE PROTEIN GP41; HIV INFECTIONS; HIV-1; HT29 CELLS; HUMANS; INTESTINAL MUCOSA; RECEPTORS, CCR5; RECTUM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 77951630373     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903346     Document Type: Article

References (68)

1. Royce, R. A., A. Sena, W. Cates, Jr., and M. S. Cohen. 1997. Sexual transmission of HIV. N. Engl. J. Med. 336: 1072-1078.
2. Wawer, M. J., R. H. Gray, N. K. Sewankambo, D. Serwadda, X. Li, O. Laeyendecker, N. Kiwanuka, G. Kigozi, M. Kiddugavu, T. Lutalo, et al. 2005. Rates of HIV-1 transmission per coital act, by stage of HIV-1 infection, in Rakai, Uganda. J. Infect. Dis. 191: 1403-1409.
3. Shattock, R. J., and J. P. Moore. 2003. Inhibiting sexual transmission of HIV-1 infection. Nat. Rev. Microbiol. 1: 25-34.
4. Bomsel, M., and A. Alfsen. 2003. Entry of viruses through the epithelial barrier: pathogenic trickery. Nat. Rev. Mol. Cell Biol. 4: 57-68.
5. Hladik, F., and M. J. McElrath. 2008. Setting the stage: host invasion by HIV. Nat. Rev. Immunol. 8: 447-457.
6. Bomsel, M. 1997. Transcytosis of infectious human immunodeficiency virus across a tight human epithelial cell line barrier. Nat. Med. 3: 42-47.
7. Bomsel, M., M. Heyman, H. Hocini, S. Lagaye, L. Belec, C. Dupont, and C. Desgranges. 1998. Intracellular neutralization of HIV transcytosis across tight epithelial barriers by anti-HIVenvelope protein dIgA or IgM. Immunity 9: 277-287. (Pubitemid 28400041)
8. Pope, M. 1999. Mucosal dendritic cells and immunodeficiency viruses. J. Infect. Dis. 179: S427-S430.
9. Hladik, F., P. Sakchalathorn, L. Ballweber, G. Lentz, M. Fialkow, D. Eschenbach, and M. J. McElrath. 2007. Initial events in establishing vaginal entry and infection by human immunodeficiency virus type-1. Immunity 26: 257-270. (Pubitemid 46329434)
10. Bobardt, M. D., U. Chatterji, S. Selvarajah, B. Van der Schueren, G. David, B. Kahn, and P. A. Gallay. 2007. Cell-free human immunodeficiency virus type 1 transcytosis through primary genital epithelial cells. J. Virol. 81: 395-405. (Pubitemid 44975178)
11. Hocini, H., P. Becquart, H. Bouhlal, N. Chomont, P. Ancuta, M. D. Kazatchkine, and L. Bélec. 2001. Active and selective transcytosis of cell-free human immunodeficiency virus through a tight polarized monolayer of human endometrial cells. J. Virol. 75: 5370-5374. (Pubitemid 32448560)
12. Alfsen, A., and M. Bomsel. 2002. HIV-1 gp41 envelope residues 650-685 exposed on native virus act as a lectin to bind epithelial cell galactosyl ceramide. J. Biol. Chem. 277: 25649-25659.
13. Alfsen, A., P. Iniguez, E. Bouguyon, and M. Bomsel. 2001. Secretory IgA specific for a conserved epitope on gp41 envelope glycoprotein inhibits epithelial transcytosis of HIV-1. J. Immunol. 166: 6257-6265. (Pubitemid 32440758)
14. + cell infection: an IgA gene and functional analysis. Mucosal Immunol. 2: 412-426.
15. Bomsel, M., C. Pastori, D. Tudor, C. Alberti, S. Garcia, D. Ferrari, A. Lazzarin, and L. Lopalco. 2007. Natural mucosal antibodies reactive with first extracellular loop of CCR5 inhibit HIV-1 transport across human epithelial cells. AIDS 21: 13-22. (Pubitemid 44912532)
16. Alfsen, A., H. Yu, A. Magerus-Chatinet, A. Schmitt, and M. Bomsel. 2005. HIV- 1-infected blood mononuclear cells form an integrin- and agrin-dependent viral synapse to induce efficient HIV-1 transcytosis across epithelial cell monolayer. Mol. Biol. Cell 16: 4267-4279.
17. Matoba, N., A. Magerus, B. C. Geyer, Y. Zhang, M. Muralidharan, A. Alfsen, C. J. Arntzen, M. Bomsel, and T. S. Mor. 2004. A mucosally targeted subunit vaccine candidate eliciting HIV-1 transcytosis-blocking Abs. Proc. Natl. Acad. Sci. USA 101: 13584-13589.
18. Wolbank, S., R. Kunert, G. Stiegler, and H. Katinger. 2003. Characterization of human class-switched polymeric (immunoglobulin M [IgM] and IgA) antihuman immunodeficiency virus type 1 antibodies 2F5 and 2G12. J. Virol. 77: 4095-4103. (Pubitemid 36350949)
19. Devito, C., K. Broliden, R. Kaul, L. Svensson, K. Johansen, P. Kiama, J. Kimani, L. Lopalco, S. Piconi, J. J. Bwayo, et al. 2000. Mucosal and plasma IgA from HIV-1-exposed uninfected individuals inhibit HIV-1 transcytosis across human epithelial cells. J. Immunol. 165: 5170-5176.
20. Hocini, H., L. Bélec, S. Iscaki, B. Garin, J. Pillot, P. Becquart, and M. Bomsel. 1997. High-level ability of secetory IgA to block HIV type 1 transcytosis: contrasting secertory IgA and IgG responses to glycoprotein 160. AIDS Res. Hum. Retroviruses. 13: 1179-1185.
21. Lewis, P., R. Nduati, J. K. Kreiss, G. C. John, B. A. Richardson, D. Mbori-Ngacha, J. Ndinya-Achola, and J. Overbaugh. 1998. Cell-free human immunodeficiency virus type 1 in breast milk. J. Infect. Dis. 177: 34-39.
22. Koulinska, I. N., E. Villamor, B. Chaplin, G. Msamanga, W. Fawzi, B. Renjifo, and M. Essex. 2006. Transmission of cell-free and cell-associated HIV-1 through breast-feeding. J. Acquir. Immune Defic. Syndr. 41: 93-99 .
23. Lehman, D. A., M. H. Chung, G. C. John-Stewart, B. A. Richardson, J. Kiarie, J. Kinuthia, and J. Overbaugh. 2008. HIV-1 persists in breast milk cells despite antiretroviral treatment to prevent mother-to-child transmission. AIDS Res. Hum. Retroviruses 22: 1475-1485.
24. Borzy, M. S., R. S. Connell, and A. A. Kiessling. 1988. Detection of human immunodeficiency virus in cell-free seminal fluid. J. Acquir. Immune Defic. Syndr. 1: 419-424.
25. Rasheed, S., Z. Li, and D. Xu. 1995. Human immunodeficiency virus load. Quantitative assessment in semen from seropositive individuals and in spiked seminal plasma. J. Reprod. Med. 40: 747-757.
26. Kiessling, A. A. 2005. Isolation of human immunodeficiency virus type 1 from semen and vaginal fluids. Methods Mol. Biol. 304: 71-86.
27. + cells. Nat. Med. 8: 150-156.
28. Chomont, N., H. Hocini, J. C. Gody, H. Bouhlal, P. Becquart, C. Krief-Bouillet, M. Kazatchkine, and L. Belec. 2008. Neutralizing monoclonal antibodies to human immunodeficiency virus type 1 do not inhibit viral transcytosis through mucosal epithelial cells. Virology 370: 246-254. (Pubitemid 350199680)
29. Li, Y., J. C. Kappes, J. A. Conway, R. W. Price, G. M. Shaw, and B. H. Hahn. 1991. Molecular characterization of human immunodeficiency virus type 1 cloned directly from uncultured human brain tissue: identification of replication-competent and -defective viral genomes. J. Virol. 65: 3973-3985.
30. Duenas-Decamp, M. J., P. J. Peters, D. Burton, and P. R. Clapham. 2009. Determinants flanking the CD4 binding loop modulate macrophage tropism of human immunodeficiency virus type 1 R5 envelopes. J. Virol. 83: 2575-2583.
31. Peters, P. J., W. M. Sullivan, M. J. Duenas-Decamp, J. Bhattacharya, C. Ankghuambom, R. Brown, K. Luzuriaga, J. Bell, P. Simmonds, J. Ball, and P. R. Clapham. 2006. Non-macrophage-tropic human immunodeficiency virus type 1 R5 envelopes predominate in blood, lymph nodes, and semen: implications for transmission and pathogenesis. J. Virol. 80: 6324-6332.
32. Peters, P. J., J. Bhattacharya, S. Hibbitts, M. T. Dittmar, G. Simmons, J. Bell, P. Simmonds, and P. R. Clapham. 2004. Biological analysis of human immunodeficiency virus type 1 R5 envelopes amplified from brain and lymph node tissues of AIDS patients with neuropathology reveals two distinct tropism phenotypes and identifies envelopes in the brain that confer an enhanced tropism and fusigenicity for macrophages. J. Virol. 78: 6915-6926.
33. Ghosh, S. K., P. N. Fultz, E. Keddie, M. S. Saag, P. M. Sharp, B. H. Hahn, and G. M. Shaw. 1993. A molecular clone of HIV-1 tropic and cytopathic for human and chimpanzee lymphocytes. Virology 194: 858-864. (Pubitemid 23192887)
34. Adachi, A., H. E. Gendelman, S. Koenig, T. Folks, R. Willey, A. Rabson, and M. A. Martin. 1986. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59: 284-291. (Pubitemid 16013975)
35. Muster, T., F. Steindl, M. Purtscher, A. Trkola, A. Klima, G. Himmler, F. Ruker, and H. Katinger. 1993. A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1. J. Virol. 67: 6642-6647. (Pubitemid 23309131)
36. Buchacher, A., R. Predl, K. Strutzenberger, W. Steinfellner, A. Trkola, M. Purtscher, G. Gruber, C. Tauer, F. Steindl, A. Jungbauer, 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. Retroviruses 10: 359-369.
37. Zhu, M., T. Olee, D. T. Le, R. A. Roubey, B. H. Hahn, V. L. Woods, Jr., and P. P. Chen. 1999. Characterization of IgG monoclonal anti-cardiolipin/ antibeta2GP1 antibodies from two patients with antiphospholipid syndrome reveals three species of antibodies. Br. J. Haematol. 105: 102-109.
38. Liao, H. X., L. L. Sutherland, S. M. Xia, M. E. Brock, R. M. Scearce, S. Vanleeuwen, S. M. Alam, M. McAdams, E. A. Weaver, Z. Camacho, et al. 2006. A group M consensus envelope glycoprotein induces antibodies that neutralize subsets of subtype B and C HIV-1 primary viruses. Virology 353: 268-282.
39. Alam, S. M., R. M. Scearce, R. J. Parks, K. Plonk, S. G. Plonk, L. L. Sutherland, M. K. Gorny, S. Zolla-Pazner, S. Vanleeuwen, M. A. Moody, et al. 2008. Human immunodeficiency virus type 1 gp41 antibodies that mask membrane proximal region epitopes: antibody binding kinetics, induction, and potential for regulation in acute infection. J. Virol. 82: 115-125.
40. Staats, H. F., S. M. Alam, R. M. Scearce, S. M. Kirwan, J. X. Zhang, W. M. Gwinn, and B. F. Haynes. 2007. In vitro and in vivo characterization of anthrax anti-protective antigen and anti-lethal factor monoclonal antibodies after passive transfer in a mouse lethal toxin challenge model to define correlates of immunity. Infect. Immun. 75: 5443-5452.
41. Driver, L. C., and M. D. Oertel. 1999. Synagis: an anti-RSV monoclonal antibody. Pediatr. Nurs. 25: 527-530.
42. Kunert, R., F. Ruker, and H. Katinger. 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. Retroviruses 14: 1115-1128.
43. Berdoz, J., C. T. Blanc, M. Reinhardt, J. P. Kraehenbuhl, and B. Corthesy. 1999. In vitro comparison of the antigen-binding and stability properties of the various molecular forms of IgA antibodies assembled and produced in CHO cells. Proc. Natl. Acad. Sci. USA 96: 3029-3034.
44. Persic, L., A. Roberts, J. Wilton, A. Cattaneo, A. Bradbury, and H. R. Hoogenboom. 1997. An integrated vector system for the eukaryotic expression of antibodies or their fragments after selection from phage display libraries. Gene 187: 9-18. (Pubitemid 27110429)
45. Shen, R., H. E. Richter, R. H. Clements, L. Novak, K. Huff, S. Sankaran-Walters, S. Dandekar, P. R. Clapham, L. E. Smythies, and P. D. Smith. 2009. Macrophages in vaginal but not in intestinal mucosa are monocyte-like and permissive to HIV-1. J. Virol. 83: 3258-3267.
46. Shen, R., L. E Smythies, R. H. Clements, L. Novak, and P. D. Smith. 2009. Dendritic cells transmit HIV-1 through human small intestinal mucosa. J. Leuk. Biol. doi:10.1189/JLB.0909605.
47. Moroney, S. M., L. C. Heller, and R. H. Widen. 2006. Evaluation of two TaqMan PCR assays for the detection of HIV-1 proviral DNA in blood samples. J. Microbiol. Methods 65: 350-353.
48. Keele, B. F., E. E. Giorgi, J. F. Salazar-Gonzalez, J. M. Decker, K. T. Pham, M. G. Salazar, C. Sun, T. Grayson, S. Wang, H. Li, et al. 2008. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc. Natl. Acad. Sci. USA 105: 7552-7557.
49. Cantin, R., S. Methot, and M. J. Tremblay. 2005. Plunder and stowaways: incorporation of cellular proteins by enveloped viruses. J. Virol. 79: 6577-6587. (Pubitemid 40677289)
50. Ho, Y. S., A. B. Abecasis, K. Theys, K. Deforche, D. E. Dwyer, M. Charleston, A. M. Vandamme, and N. K. Saksena. 2008. HIV-1 gp120 N-linked glycosylation differs between plasma and leukocyte compartments. Virol. J. 5: 14-24.
51. Sato, K., J. Aoki, N. Misawa, E. Daikoku, K. Sano, Y. Tanaka, and Y. Koyanagi. 2008. Modulation of human immunodeficiency virus type 1 infectivity through incorporation of tetraspanin proteins. J. Virol. 82: 1021-1033.
52. Pai, E. F., M. H. Klein, P. Chong, and A. Pedyczak. 2000. W. I. P. Organization. Patent number WO-00/61618.
53. Ofek, G., M. Tang, A. Sambor, H. Katinger, J. R. Mascola, R. Wyatt, and P. D. Kwong. 2004. Structure and mechanistic analysis of the anti-human immunodeficiency virus type 1 antibody 2F5 in complex with its gp41 epitope. World Intellectual Propert Organization patent WO-00/61618. J. Virol. 78: 10724-10737. (Pubitemid 39258398)
54. Cardoso, R. M., M. B. Zwick, R. L. Stanfield, R. Kunert, J. M. Binley, H. Katinger, D. R. Burton, and I. A. Wilson. 2005. Broadly neutralizing anti-HIV antibody 4E10 recognizes a helical conformation of a highly conserved fusion-associated motif in gp41. Immunity 22: 163-173.
55. Zwick, M. B., A. F. Labrijn, M. Wang, C. Spenlehauer, E. O. Saphire, J. M. Binley, J. P. Moore, G. Stiegler, H. Katinger, D. R. Burton, and P. W. Parren. 2001. Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J. Virol. 75: 10892-10905.
56. Dennison, S. M., S. M. Stewart, K. C. Stempel, H. X. Liao, B. F. Haynes, and S. M. Alam. 2009. Stable docking of neutralizing human immunodeficiency virus type 1 gp41 membrane-proximal external region monoclonal antibodies 2F5 and 4E10 is dependent on the membrane immersion depth of their epitope regions. J. Virol. 83: 10211-10223.
57. Matoba, N., T. A. Griffin, M. Mittman, J. D. Doran, A. Alfsen, D. C. Montefiori, C. V. Hanson, M. Bomsel, and T. S. Mor. 2008. Transcytosis-blocking abs elicited by an oligomeric immunogen based on the membrane proximal region of HIV-1 gp41 target non-neutralizing epitopes. Curr. HIV Res. 6: 218-229.
58. Torres, M., R. May, M. D. Scharff, and A. Casadevall. 2005. Variable-region-identical antibodies differing in isotype demonstrate differences in fine specificity and idiotype. J. Immunol. 174: 2132-2142. (Pubitemid 40223957)
59. Pritsch, O., C. Magnac, G. Dumas, J. P. Bouvet, P. Alzari, and G. Dighiero. 2000. Can isotype switch modulate antigen-binding affinity and influence clonal selection? Eur. J. Immunol. 30: 3387-3395. (Pubitemid 32005209)
60. Belec, L., P. D. Ghys, H. Hocini, J. N. Nkengasong, J. Tranchot-Diallo, M. O. Diallo, V. Ettiegne-Traore, C. Maurice, P. Becquart, M. Matta, et al. 2001. Cervicovaginal secretory antibodies to human immunodeficiency virus type 1 (HIV-1) that block viral transcytosis through tight epithelial barriers in highly exposed HIV-1-seronegative African women. J. Infect. Dis. 184: 1412-1422.
61. Ceballos, A., F. Remes Lenicov, J. Sabatte, C. Rodriguez Rodrigues, M. Cabrini, C. Jancic, S. Raiden, M. Donaldson, R. Agustin Pasqualini, Jr., C. Marin-Briggiler, et al. 2009. Spermatozoa capture HIV-1 through heparan sulfate and efficiently transmit the virus to dendritic cells. J. Exp. Med. 206: 2717-2733.
62. Mestecky, J., Z. Moldoveanu, and M. W. Russell. 2005. Immunologic uniqueness of the genital tract: challenge for vaccine development. Am. J. Reprod. Immunol. 53: 208-214.
63. Mestecky, J. 2006. Humoral immune responses to the human immunodeficiency virus type-1 (HIV-1) in the genital tract compared to other mucosal sites. J. Reprod. Immunol. 72: 1-17.
64. Moldoveanu, Z., W. Q. Huang, R. Kulhavy, M. S. Pate, and J. Mestecky. 2005. Human male genital tract secretions: both mucosal and systemic immune compartments contribute to the humoral immunity. J. Immunol. 175: 4127-4136. (Pubitemid 41292077)
65. Apodaca, G., M. Bomsel, J. Arden, P. P. Breitfeld, K. Tang, and K. E. Mostov. 1991. The polymeric immunoglobulin receptor. A model protein to study transcytosis. J. Clin. Invest. 87: 1877-1882.
66. Baba, T. W., V. Liska, R. Hofmann-Lehmann, J. Vlasak, W. Xu, S. Ayehunie, L. A. Cavacini, M. R. Posner, H. Katinger, G. Stiegler, et al. 2000. Human neutralizing monoclonal antibodies of the IgG1 subtype protect against mucosal simian-human immunodeficiency virus infection. Nat. Med. 6: 200-206.
67. Mascola, J. R., G. Stiegler, T. C. VanCott, H. Katinger, C. B. Carpenter, C. E. Hanson, H. Beary, D. Hayes, S. S. Frankel, D. L. Birx, and M. G. Lewis. 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.
68. Veazey, R. S., R. J. Shattock, M. Pope, J. C. Kirijan, J. Jones, Q. Hu, T. Ketas, P. A. Marx, P. J. Klasse, D. R. Burton, and J. P. Moore. 2003. Prevention of virus transmission to macaque monkeys by a vaginally applied monoclonal antibody to HIV-1 gp120. Nat. Med. 9: 343-346.