Vaccine induction of lymph node-resident simian immunodeficiency virus Env-specific T follicular helper cells in rhesus macaques

Journal of Immunology

Volumn 196, Issue 4, 2016, Pages 1700-1710

  Vargas Inchaustegui, Diego A ^a   Demers, Andrew ^b   Shaw, Julia M ^a   Kang, Guobin ^b   Ball, David ^a   Tuero, Iskra ^a   Musich, Thomas ^a   Mohanram, Venkatramanan ^a   Demberg, Thorsten ^a   Karpova, Tatiana S ^a   Li, Qingsheng ^b   Robert Guroff, Marjorie ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF NEBRASKA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; INTERLEUKIN 21; MIFAMURTIDE; MONOMER; OLIGOMER; RECOMBINANT GLYCOPROTEIN GP 120; RECOMBINANT GLYCOPROTEIN GP 140; RECOMBINANT PROTEIN; SIMIAN IMMUNODEFICIENCY VIRUS VACCINE; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY SECRETING CELL; ARTICLE; B LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELL POPULATION; CONTROLLED STUDY; ENVELOPE GENE; FEMALE; GAG GENE; GERMINAL CENTER; HELPER CELL; HUMAN ADENOVIRUS 5; LYMPH NODE; LYMPH NODE BIOPSY; MALE; NEF GENE; NONHUMAN; PRIORITY JOURNAL; REV GENE; RHESUS MONKEY; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VACCINATION; VIRUS GENE; VIRUS REPLICATION; ANIMAL; CONFOCAL MICROSCOPY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY;

ANIMALS; B-LYMPHOCYTES; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE PRODUCTS, ENV; GERMINAL CENTER; IMMUNOHISTOCHEMISTRY; LYMPH NODES; MACACA MULATTA; MICROSCOPY, CONFOCAL; SAIDS VACCINES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84958555153     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1502137     Document Type: Article

References (48)

1. Plotkin, S. A. 2010. Correlates of protection induced by vaccination. Clin. Vaccine Immunol. 17: 1055-1065.
2. Plotkin, S. A. 1999. Vaccination against the major infectious diseases. C. R. Acad. Sci. III 322: 943-951.
3. Klein, F., H. Mouquet, P. Dosenovic, J. F. Scheid, L. Scharf, and M. C. Nussenzweig. 2013. Antibodies in HIV-1 vaccine development and therapy. Science 341: 1199-1204.
4. McGuire, A. T., A. M. Dreyer, S. Carbonetti, A. Lippy, J. Glenn, J. F. Scheid, H. Mouquet, and L. Stamatatos. 2014. HIV antibodies. Antigen modification regulates competition of broad and narrow neutralizing HIV antibodies. Science 346: 1380-1383.
5. Stamatatos, L., L. Morris, D. R. Burton, and J. R. Mascola. 2009. Neutralizing antibodies generated during natural HIV-1 infection: good news for an HIV-1 vaccine? Nat. Med. 15: 866-870.
6. Baumjohann, D., S. Preite, A. Reboldi, F. Ronchi, K. M. Ansel, A. Lanzavecchia, and F. Sallusto. 2013. Persistent antigen and germinal center B cells sustain T follicular helper cell responses and phenotype. Immunity 38: 596-605.
7. Crotty, S. 2011. Follicular helper CD4 T cells (TFH). Annu. Rev. Immunol. 29: 621-663.
8. Nurieva, R. I., Y. Chung, G. J. Martinez, X. O. Yang, S. Tanaka, T. D. Matskevitch, Y. H. Wang, and C. Dong. 2009. Bcl6 mediates the development of T follicular helper cells. Science 325: 1001-1005.
9. Nutt, S. L., and D. M. Tarlinton. 2011. Germinal center B and follicular helper T cells: siblings, cousins or just good friends? Nat. Immunol. 12: 472-477.
10. Glatman Zaretsky, A., J. J. Taylor, I. L. King, F. A. Marshall, M. Mohrs, and E. J. Pearce. 2009. T follicular helper cells differentiate from Th2 cells in response to helminth antigens. J. Exp. Med. 206: 991-999.
11. Fahey, L. M., E. B. Wilson, H. Elsaesser, C. D. Fistonich, D. B. McGavern, and D. G. Brooks. 2011. Viral persistence redirects CD4 T cell differentiation toward T follicular helper cells. J. Exp. Med. 208: 987-999.
12. Fairfax, K. C., B. Everts, E. Amiel, A. M. Smith, G. Schramm, H. Haas, G. J. Randolph, J. J. Taylor, and E. J. Pearce. 2015. IL-4-secreting secondary T follicular helper (Tfh) cells arise from memory T cells, not persisting Tfh cells, through a B cell-dependent mechanism. J. Immunol. 194: 2999-3010.
13. Hale, J. S., B. Youngblood, D. R. Latner, A. U. Mohammed, L. Ye, R. S. Akondy, T. Wu, S. S. Iyer, and R. Ahmed. 2013. Distinct memory CD4+ T cells with commitment to T follicular helper-and T helper 1-cell lineages are generated after acute viral infection. Immunity 38: 805-817.
14. Nurieva, R. I., Y. Chung, D. Hwang, X. O. Yang, H. S. Kang, L. Ma, Y. H. Wang, S. S. Watowich, A. M. Jetten, Q. Tian, and C. Dong. 2008. Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 29: 138-149.
15. Hale, J. S., and R. Ahmed. 2015. Memory T follicular helper CD4 T cells. Front. Immunol. 6: 16.
16. Fukazawa, Y., R. Lum, A. A. Okoye, H. Park, K. Matsuda, J. Y. Bae, S. I. Hagen, R. Shoemaker, C. Deleage, C. Lucero, et al. 2015. B cell follicle sanctuary permits persistent productive simian immunodeficiency virus infection in elite controllers. Nat. Med. 21: 132-139.
17. Fukazawa, Y., H. Park, M. J. Cameron, F. Lefebvre, R. Lum, N. Coombes, E. Mahyari, S. I. Hagen, J. Y. Bae, M. D. Reyes, III, et al. 2012. Lymph node T cell responses predict the efficacy of live attenuated SIV vaccines. Nat. Med. 18: 1673-1681.
18. Klatt, N. R., C. L. Vinton, R. M. Lynch, L. A. Canary, J. Ho, P. A. Darrah, J. D. Estes, R. A. Seder, S. L. Moir, and J. M. Brenchley. 2011. SIV infection of rhesus macaques results in dysfunctional T-and B-cell responses to neo and recall Leishmania major vaccination. Blood 118: 5803-5812.
19. Connick, E., J. M. Folkvord, K. T. Lind, E. G. Rakasz, B. Miles, N. A. Wilson, M. L. Santiago, K. Schmitt, E. B. Stephens, H. O. Kim, et al. 2014. Compartmentalization of simian immunodeficiency virus replication within secondary lymphoid tissues of rhesus macaques is linked to disease stage and inversely related to localization of virus-specific CTL. J. Immunol. 193: 5613-5625.
20. Connick, E., T. Mattila, J. M. Folkvord, R. Schlichtemeier, A. L. Meditz, M. G. Ray, M. D. McCarter, S. Mawhinney, A. Hage, C. White, and P. J. Skinner. 2007. CTL fail to accumulate at sites of HIV-1 replication in lymphoid tissue. J. Immunol. 178: 6975-6983.
21. Lindqvist, M., J. van Lunzen, D. Z. Soghoian, B. D. Kuhl, S. Ranasinghe, G. Kranias, M. D. Flanders, S. Cutler, N. Yudanin, M. I. Muller, et al. 2012. Expansion of HIV-specific T follicular helper cells in chronic HIV infection. J. Clin. Invest. 122: 3271-3280.
22. Perreau, M., A. L. Savoye, E. De Crignis, J. M. Corpataux, R. Cubas, E. K. Haddad, L. De Leval, C. Graziosi, and G. Pantaleo. 2013. Follicular helper T cells serve as the major CD4 T cell compartment for HIV-1 infection, replication, and production. J. Exp. Med. 210: 143-156.
23. Hong, J. J., P. K. Amancha, K. Rogers, A. A. Ansari, and F. Villinger. 2012. Spatial alterations between CD4(+) T follicular helper, B, and CD8(+) T cells during simian immunodeficiency virus infection: T/B cell homeostasis, activation, and potential mechanism for viral escape. J. Immunol. 188: 3247-3256.
24. Petrovas, C., T. Yamamoto, M. Y. Gerner, K. L. Boswell, K. Wloka, E. C. Smith, D. R. Ambrozak, N. G. Sandler, K. J. Timmer, X. Sun, et al. 2012. CD4 T follicular helper cell dynamics during SIV infection. J. Clin. Invest. 122: 3281-3294.
25. Petrovas, C., and R. A. Koup. 2014. T follicular helper cells and HIV/SIVspecific antibody responses. Curr. Opin. HIV AIDS 9: 235-241.
26. Morgan, C., M. Marthas, C. Miller, A. Duerr, C. Cheng-Mayer, R. Desrosiers, J. Flores, N. Haigwood, S. L. Hu, R. P. Johnson, et al. 2008. The use of nonhuman primate models in HIV vaccine development. PLoS Med. 5: e173.
27. Xu, H., X. Wang, A. A. Lackner, and R. S. Veazey. 2014. PD-1(HIGH) follicular CD4 T helper cell subsets residing in lymph node germinal centers correlate with B cell maturation and IgG production in rhesus macaques. Front. Immunol. 5: 85.
28. Onabajo, O. O., J. George, M. G. Lewis, and J. J. Mattapallil. 2013. Rhesus macaque lymph node PD-1(hi)CD4+ T cells express high levels of CXCR5 and IL-21 and display a CCR7(lo)ICOS+Bcl6+ T-follicular helper (Tfh) cell phenotype. PLoS One 8: e59758.
29. Shi, S., S. Seki, T. Matano, and H. Yamamoto. 2013. IL-21-producer CD4+ T cell kinetics during primary simian immunodeficiency virus infection. Microbes Infect. 15: 697-707.
30. Yamamoto, T., R. M. Lynch, R. Gautam, R. Matus-Nicodemos, S. D. Schmidt, K. L. Boswell, S. Darko, P. Wong, Z. Sheng, C. Petrovas, et al. 2015. Quality and quantity of TFH cells are critical for broad antibody development in SHIVAD8 infection. Sci. Transl. Med. 7: 298ra120.
31. Blackburn, M. J., M. Zhong-Min, F. Caccuri, K. McKinnon, L. Schifanella, Y. Guan, G. Gorini, D. Venzon, C. Fenizia, N. Binello, et al. 2015. Regulatory and helper follicular T cells and antibody avidity to simian immunodeficiency virus glycoprotein 120. J. Immunol. 195: 3227-3236.
32. Tuero, I., V. Mohanram, T. Musich, L. Miller, D. A. Vargas-Inchaustegui, T. Demberg, D. Venzon, I. Kalisz, V. S. Kalyanaraman, R. Pal, et al. 2015. Mucosal B cells are associated with delayed SIV acquisition in vaccinated female but not male rhesus macaques following SIVmac251 rectal challenge. PLoS Pathog. 11: e1005101.
33. Vargas-Inchaustegui, D. A., P. Xiao, A. E. Hogg, T. Demberg, K. McKinnon, D. Venzon, E. Brocca-Cofano, J. Dipasquale, E. M. Lee, L. Hudacik, et al. 2013. Immune targeting of PD-1(hi) expressing cells during and after antiretroviral therapy in SIV-infected rhesus macaques. Virology 447: 274-284.
34. Sommer, C. S. C., U. Kothe, and F. A. Hamprecht. 2011. ilastik: Interactive Learning and Segmentation Toolkit. Eighth IEEE International Symposium on Biomedical Imaging (ISBI): 230-Interactive Learning and Segmentation Toolkit. Eighth IEEE International Symposium on Biomedical Imaging (ISBI): 230.
35. Ma, C. S., S. Suryani, D. T. Avery, A. Chan, R. Nanan, B. Santner-Nanan, E. K. Deenick, and S. G. Tangye. 2009. Early commitment of naïve human CD4 (+) T cells to the T follicular helper (T(FH)) cell lineage is induced by IL-12. Immunol. Cell Biol. 87: 590-600.
36. Bannard, O., R. M. Horton, C. D. Allen, J. An, T. Nagasawa, and J. G. Cyster. 2013. Germinal center centroblasts transition to a centrocyte phenotype according to a timed program and depend on the dark zone for effective selection. Immunity 39: 912-924.
37. De Silva, N. S., and U. Klein. 2015. Dynamics of B cells in germinal centres. Nat. Rev. Immunol. 15: 137-148.
38. Crotty, S. 2015. A brief history of T cell help to B cells. Nat. Rev. Immunol. 15: 185-189.
39. Nojima, T., K. Haniuda, T. Moutai, M. Matsudaira, S. Mizokawa, I. Shiratori, T. Azuma, and D. Kitamura. 2011. In-vitro derived germinal centre B cells differentially generate memory B or plasma cells in vivo. Nat. Commun. 2: 465.
40. Schmitt, N., S. E. Bentebibel, and H. Ueno. 2014. Phenotype and functions of memory Tfh cells in human blood. Trends Immunol. 35: 436-442.
41. Suh, W. K. 2015. Life of T follicular helper cells. Mol. Cells 38: 195-201.
42. Patterson, L. J., S. Kuate, M. Daltabuit-Test, Q. Li, P. Xiao, K. McKinnon, J. DiPasquale, A. Cristillo, D. Venzon, A. Haase, and M. Robert-Guroff. 2012. Replicating adenovirus-simian immunodeficiency virus (SIV) vectors efficiently prime SIV-specific systemic and mucosal immune responses by targeting myeloid dendritic cells and persisting in rectal macrophages, regardless of immunization route. Clin. Vaccine Immunol. 19: 629-637.
43. Lofano, G., F. Mancini, G. Salvatore, R. Cantisani, E. Monaci, C. Carrisi, S. Tavarini, C. Sammicheli, S. Rossi Paccani, E. Soldaini, et al. 2015. Oil-inwater emulsion MF59 increases germinal center B cell differentiation and persistence in response to vaccination. J. Immunol. 195: 1617-1627.
44. Mastelic Gavillet, B., C. S. Eberhardt, F. Auderset, F. Castellino, A. Seubert, J. S. Tregoning, P. H. Lambert, E. de Gregorio, G. Del Giudice, and C. A. Siegrist. 2015. MF59 mediates its B cell adjuvanticity by promoting T follicular helper cells and thus germinal center responses in adult and early life. J. Immunol. 194: 4836-4845.
45. Moon, J. J., H. Suh, A. V. Li, C. F. Ockenhouse, A. Yadava, and D. J. Irvine. 2012. Enhancing humoral responses to a malaria antigen with nanoparticle vaccines that expand Tfh cells and promote germinal center induction. Proc. Natl. Acad. Sci. USA 109: 1080-1085.
46. Hollister, K., Y. Chen, S. Wang, H. Wu, A. Mondal, N. Clegg, S. Lu, and A. Dent. 2014. The role of follicular helper T cells and the germinal center in HIV-1 gp120 DNA prime and gp120 protein boost vaccination. Hum. Vaccin. Immunother. 10: 1985-1992.
47. Addo, M. M., and M. Altfeld. 2014. Sex-based differences in HIV type 1 pathogenesis. J. Infect. Dis. 209(Suppl 3): S86-S92.
48. Klein, S. L. 2012. Sex influences immune responses to viruses, and efficacy of prophylaxis and treatments for viral diseases. BioEssays 34: 1050-1059.