Live simian immunodeficiency virus vaccine correlate of protection: Local antibody production and concentration on the path of virus entry

Journal of Immunology

Volumn 193, Issue 6, 2014, Pages 3113-3125

  Li, Qingsheng ^a,o   Zeng, Ming ^a,p   Duan, Lijie ^a   Voss, James E ^b,c   Smith, Anthony J ^a,q   Pambuccian, Stefan ^a   Shang, Liang ^a   Wietgrefe, Stephen ^a   Southern, Peter J ^a   Reilly, Cavan S ^d   Skinner, Pamela J ^e   Zupancic, Mary L ^a   Carlis, John V ^f   Piatak, Michael ^g   Waterman, Diane ^h   Reeves, R Keith ^i,j   Masek Hammerman, Katherine ^i,j   Derdeyn, Cynthia A ^k   Alpert, Michael D ⁱ   Evans, David T ^i,r   Kohler, Heinz ^l   Müller, Sybille ^m   Robinson, James ⁿ   Lifson, Jeffrey D ^g   Burton, Dennis R ^b,c   Johnson, R Paul ^c,i,s   Haase, Ashley T ^a   more..

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

^e UNIVERSITY OF MINNESOTA   (United States)

^f University of Minnesota   (United States)

^g SAIC FREDERICK INC   (United States)

^h ZeptoMetrix Corporation   (United States)

ⁱ HARVARD MEDICAL SCHOOL   (United States)

^j MASSACHUSETTS GENERAL HOSPITAL   (United States)

^k EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^l UNIVERSITY OF KENTUCKY   (United States)

^m Immpheron Incorporated   (United States)

ⁿ TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^o UNIVERSITY OF NEBRASKA   (United States)

^p UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^q Manipal Education Americas   (United States)

^r UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^s EMORY UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR; GLYCOPROTEIN GP 41; IMMUNOGLOBULIN G ANTIBODY; SIMIAN IMMUNODEFICIENCY VIRUS VACCINE; IMMUNOGLOBULIN G; LIVE VACCINE; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; CONTROLLED STUDY; DRUG MEGADOSE; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; LYMPH FOLLICLE; NEWBORN; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; RHESUS MONKEY; VACCINATION; VAGINA EPITHELIUM; VIRUS ENTRY; VIRUS LOAD; VIRUS TRANSMISSION; ANIMAL; BIOSYNTHESIS; HIV INFECTIONS; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; MUCOSA; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; UTERINE CERVIX; VAGINA; VIROLOGY;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY FORMATION; CERVIX UTERI; FEMALE; HIV ENVELOPE PROTEIN GP41; HIV INFECTIONS; HIV-1; IMMUNOGLOBULIN G; MACACA MULATTA; MUCOUS MEMBRANE; SAIDS VACCINES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VACCINATION; VACCINES, ATTENUATED; VAGINA;

EID: 84926498205     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400820     Document Type: Article

References (47)

1. Haase, A. T. 2010. Targeting early infection to prevent HIV-1 mucosal transmission. Nature 464: 217-223.
2. Quinn, T. C., and J. Overbaugh. 2005. HIV/AIDS in women: an expanding epidemic. Science 308: 1582-1583.
3. Daniel, M. D., F. Kirchhoff, S. C. Czajak, P. K. Sehgal, and R. C. Desrosiers. 1992. Protective effects of a live attenuated SIV vaccine with a deletion in the nef gene. Science 258: 1938-1941.
4. Johnson, R. P. 1999. Live attenuated AIDS vaccines: hazards and hopes. Nat. Med. 5: 154-155.
5. Koff, W. C., P. R. Johnson, D. I. Watkins, D. R. Burton, J. D. Lifson, K. J. Hasenkrug, A. B. McDermott, A. Schultz, T. J. Zamb, R. Boyle, and R. C. Desrosiers. 2006. HIV vaccine design: insights from live attenuated SIV vaccines. Nat. Immunol. 7: 19-23.
6. Reynolds, M. R., A. M. Weiler, K. L. Weisgrau, S. M. Piaskowski, J. R. Furlott, J. T. Weinfurter, M. Kaizu, T. Soma, E. J. León, C. MacNair, et al. 2008. Macaques vaccinated with live-attenuated SIV control replication of heterologous virus. J. Exp. Med. 205: 2537-2550.
7. Reynolds, M. R., A. M. Weiler, S. M. Piaskowski, H. L. Kolar, A. J. Hessell, M. Weiker, K. L. Weisgrau, E. J. León, W. E. Rogers, R. Makowsky, et al. 2010. Macaques vaccinated with simian immunodeficiency virus SIVmac239δ nef delay acquisition and control replication after repeated low-dose heterologous SIV challenge. J. Virol. 84: 9190-9199.
8. Connor, R. I., D. C. Montefiori, J. M. Binley, J. P. Moore, S. Bonhoeffer, A. Gettie, E. A. Fenamore, K. E. Sheridan, D. D. Ho, P. J. Dailey, and P. A. Marx. 1998. Temporal analyses of virus replication, immune responses, and efficacy in rhesus macaques immunized with a live, attenuated simian immunodeficiency virus vaccine. J. Virol. 72: 7501-7509.
9. Roopenian, D. C., and S. Akilesh. 2007. FcRn: the neonatal Fc receptor comes of age. Nat. Rev. Immunol. 7: 715-725.
10. Miller, C. J., Q. Li, K. Abel, E.-Y. Kim, Z.-M. Ma, S. Wietgrefe, L. La Franco-Scheuch, L. Compton, L. Duan, M. D. Shore, et al. 2005. Propagation and dissemination of infection after vaginal transmission of simian immunodeficiency virus. [Published erratum appears in 2005 J. Virol. 79: 11552.] J. Virol. 79: 9217-9227.
11. Li, Q., J. D. Estes, P. M. Schlievert, L. Duan, A. J. Brosnahan, P. J. Southern, C. S. Reilly, M. L. Peterson, N. Schultz-Darken, K. G. Brunner, et al. 2009. Glycerol monolaurate prevents mucosal SIV transmission. Nature 458: 1034-1038.
12. + T cells. Science 286: 1353-1357.
13. Zeng, M., A. J. Smith, S. W. Wietgrefe, P. J. Southern, T. W. Schacker, C. S. Reilly, J. D. Estes, G. F. Burton, G. Silvestri, J. D. Lifson, et al. 2011. Cumulative mechanisms of lymphoid tissue fibrosis and T cell depletion in HIV- 1 and SIV infections. J. Clin. Invest. 121: 998-1008.
14. Salisch, N. C., D. E. Kaufmann, A. S. Awad, R. K. Reeves, D. P. Tighe, Y. Li, M. Piatak, Jr., J. D. Lifson, D. T. Evans, F. Pereyra, et al. 2010. Inhibitory TCR coreceptor PD-1 is a sensitive indicator of low-level replication of SIV and HIV-1 J. Immunol. 184: 476-487.
15. Kozlowski, P. A., R. M. Lynch, R. R. Patterson, S. Cu-Uvin, T. P. Flanigan, and M. R. Neutra. 2000. Modified wick method using Weck-Cel sponges for collection of human rectal secretions and analysis of mucosal HIV antibody. J. Acquir. Immune Defic. Syndr. 24: 297-309.
16. Caffrey, M., M. Cai, J. Kaufman, S. J. Stahl, P. T. Wingfield, D. G. Covell, A. M. Gronenborn, and G. M. Clore. 1998. Three-dimensional solution structure of the 44 kDa ectodomain of SIV gp41. EMBO J. 17: 4572-4584.
17. Freissmuth, D., A. Hiltgartner, C. Stahl-Hennig, D. Fuchs, K. Tenner-Racz, P. Racz, K. Uberla, A. Strasak, M. P. Dierich, H. Stoiber, and B. Falkensammer. 2010. Analysis of humoral immune responses in rhesus macaques vaccinated with attenuated SIVmac239Deltanef and challenged with pathogenic SIVmac251. J. Med. Primatol. 39: 97-111.
18. Means, R. E., T. Greenough, and R. C. Desrosiers. 1997. Neutralization sensitivity of cell culture-passaged simian immunodeficiency virus. J. Virol. 71: 7895-7902.
19. Shen, R., E. R. Drelichman, D. Bimczok, C. Ochsenbauer, J. C. Kappes, J. A. Cannon, D. Tudor, M. Bomsel, L. E. Smythies, and P. D. Smith. 2010. GP41-specific antibody blocks cell-free HIV type 1 transcytosis through human rectal mucosa and model colonic epithelium. J. Immunol. 184: 3648-3655.
20. Antohe, F., L. RǍdulescu, A. Gafencu, V. Gheţie, and M. Simionescu. 2001. Expression of functionally active FcRn and the differentiated bidirectional transport of IgG in human placental endothelial cells. Hum. Immunol. 62: 93-105.
21. Maidji, E., S. McDonagh, O. Genbacev, T. Tabata, and L. Pereira. 2006. Maternal antibodies enhance or prevent cytomegalovirus infection in the placenta by neonatal Fc receptor-mediated transcytosis. Am. J. Pathol. 168: 1210-1226.
22. Pinter, A., W. J. Honnen, S. A. Tilley, C. Bona, H. Zaghouani, M. K. Gorny, and S. Zolla-Pazner. 1989. Oligomeric structure of gp41, the transmembrane protein of human immunodeficiency virus type 1. J. Virol. 63: 2674-2679.
23. Zolla-Pazner, S., M. K. Gorny, W. J. Honnen, and A. Pinter. 1989. Reinterpretation of human immunodeficiency virus western blot patterns. N. Engl. J. Med. 320: 1280-1281.
24. Parekh, B. S., C. P. Pau, T. C. Granade, M. Rayfield, K. M. De Cock, H. Gayle, G. Schochetman, and J. R. George. 1991. Oligomeric nature of transmembrane glycoproteins of HIV-2: procedures for their efficient dissociation and preparation of Western blots for diagnosis. AIDS 5: 1009-1013.
25. Cole, K. S., M. Alvarez, D. H. Elliott, H. Lam, E. Martin, T. Chau, K. Micken, J. L. Rowles, J. E. Clements, M. Murphey-Corb, et al. 2001. Characterization of neutralization epitopes of simian immunodeficiency virus (SIV) recognized by rhesus monoclonal antibodies derived from monkeys infected with an attenuated SIV strain. Virology 290: 59-73.
26. Sanderson, R. D., P. Lalor, and M. Bernfield. 1989. B lymphocytes express and lose syndecan at specific stages of differentiation. Cell Regul. 1: 27-35.
27. Smedts, F., F. Ramaekers, S. Troyanovsky, M. Pruszczynski, H. Robben, B. Lane, I. Leigh, F. Plantema, and P. Vooijs. 1992. Basal-cell keratins in cervical reserve cells and a comparison to their expression in cervical intraepithelial neoplasia. Am. J. Pathol. 140: 601-612.
28. Martens, J. E., F. M. Smedts, D. Ploeger, T. J. Helmerhorst, F. C. Ramaekers, J. W. Arends, and A. H. Hopman. 2009. Distribution pattern and marker profile show two subpopulations of reserve cells in the endocervical canal. Int. J. Gynecol. Pathol. 28: 381-388.
29. Li, Z., S. Palaniyandi, R. Zeng, W. Tuo, D. C. Roopenian, and X. Zhu. 2011. Transfer of IgG in the female genital tract by MHC class I-related neonatal Fc receptor (FcRn) confers protective immunity to vaginal infection. Proc. Natl. Acad. Sci. USA 108: 4388-4393.
30. Tsuge, S., Y. Mizutani, K. Matsuoka, T. Sawasaki, Y. Endo, K. Naruishi, H. Maeda, S. Takashiba, K. Shiogama, K. Inada, and Y. Tsutsumi. 2011. Specific in situ visualization of plasma cells producing antibodies against Porphyromonas gingivalis in gingival radicular cyst: application of the enzyme-labeled antigen method. J. Histochem. Cytochem. 59: 673-689.
31. Moore, P. L., E. T. Crooks, L. Porter, P. Zhu, C. S. Cayanan, H. Grise, P. Corcoran, M. B. Zwick, M. Franti, L. Morris, et al. 2006. Nature of nonfunctional envelope proteins on the surface of human immunodeficiency virus type 1. J. Virol. 80: 2515-2528.
32. Zolla-Pazner, S. 2004. Identifying epitopes of HIV-1 that induce protective antibodies. Nat. Rev. Immunol. 4: 199-210.
33. Xu, J.-Y., M. K. Gorny, T. Palker, S. Karwaska, and S. Zolla-Pazner. 1991. Epitope mapping of two immunodominant domains of gp41, the transmembrane protein of HIV-1. Using ten human monoclonal antibodies. J. Virol. 65: 4832-4838.
34. Nakanishi, Y., B. Lu, C. Gerard, and A. Iwasaki. 2009. CD8(+) T lymphocyte mobilization to virus-infected tissue requires CD4(+) T-cell help. Nature 462: 510-513.
35. Burton, D. R., A. J. Hessell, B. F. Keele, P. J. Klasse, T. A. Ketas, B. Moldt, D. C. Dunlop, P. Poignard, L. A. Doyle, L. Cavacini, et al. 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. USA 108: 11181-11186.
36. Bai, Y., L. Ye, D. B. Tesar, H. Song, D. Zhao, P. J. Björkman, D. C. Roopenian, and X. Zhu. 2011. Intracellular neutralization of viral infection in polarized epithelial cells by neonatal Fc receptor (FcRn)-mediated IgG transport. Proc. Natl. Acad. Sci. USA 108: 18406-18411.
37. Burrer, R., S. Haessig-Einius, A.-M. Aubertin, and C. Moog. 2005. Neutralizing as well as non-neutralizing polyclonal immunoglobulin (Ig)G from infected patients capture HIV-1 via antibodies directed against the principal immunodominant domain of gp41. Virology 333: 102-113.
38. Shingai, M., Y. Nishimura, F. Klein, H. Mouquet, O. K. Donau, R. Plishka, A. Buckler-White, M. Seaman, M. Piatak, Jr., J. D. Lifson, et al. 2013. Antibodymediated immunotherapy of macaques chronically infected with SHIV suppresses viraemia. Nature 503: 277-280.
39. Hope, T. J. 2011. Moving ahead an HIV vaccine: to neutralize or not, a key HIV vaccine question. Nat. Med. 17: 1195-1197.
40. Bomsel, M., D. Tudor, A. S. Drillet, A. Alfsen, Y. Ganor, M. G. Roger, N. Mouz, M. Amacker, A. Chalifour, L. Diomede, et al. 2011. Immunization with HIV-1 gp41 subunit virosomes induces mucosal antibodies protecting nonhuman primates against vaginal SHIV challenges. Immunity 34: 269-280.
41. Shang, L., A. J. Smith, L. Duan, K. E. Perkey, L. Qu, S. Wietgrefe, M. Zupancic, P. J. Southern, K. Masek-Hammerman, R. K. Reeves, et al. 2014. NK cell responses to SIV vaginal exposure in naive and vaccinated rhesus macaques. J. Immunol. 193: 277-284.
42. Ye, L., R. Zeng, Y. Bai, D. C. Roopenian, and X. Zhu. 2011. Efficient mucosal vaccination mediated by the neonatal Fc receptor. Nat. Biotechnol. 29: 158-163.
43. Lu, L., S. Palaniyandi, R. Zeng, Y. Bai, X. Liu, Y. Wang, C. D. Pauza, D. C. Roopenian, and X. Zhu. 2011. A neonatal Fc receptor-targeted mucosal vaccine strategy effectively induces HIV-1 antigen-specific immunity to genital infection. J. Virol. 85: 10542-10553.
44. Shin, H., and A. Iwasaki. 2012. A vaccine strategy that protects against genital herpes by establishing local memory T cells. Nature 491: 463-467.
45. Sasikala-Appukuttan, A. K., H. O. Kim, N. J. Kinzel, J. J. Hong, A. J. Smith, R. Wagstaff, C. Reilly, M. Piatak, Jr., J. D. Lifson, R. K. Reeves, et al. 2013. Location and dynamics of the immunodominant CD8 T cell response to SIVDnef immunization and SIVmac251 vaginal challenge. PLoS ONE.
46. Baba, T. W., Y. S. Jeong, D. Pennick, R. Bronson, M. F. Greene, and R. M. Ruprecht. 1995. Pathogenicity of live, attenuated SIV after mucosal infection of neonatal macaques. Science 267: 1820-1825.
47. Baba, T. W., V. Liska, A. H. Khimani, N. B. Ray, P. J. Dailey, D. Penninck, R. Bronson, M. F. Greene, H. M. McClure, L. N. Martin, and R. M. Ruprecht. 1999. Live attenuated, multiply deleted simian immunodeficiency virus causes AIDS in infant and adult macaques. Nat. Med. 5: 194-203.