Decreased T follicular regulatory cell/T follicular helper cell (TFH) in simian immunodeficiency virus-infected rhesus macaques may contribute to accumulation of TFH in chronic infection

Journal of Immunology

Volumn 195, Issue 7, 2015, Pages 3237-3247

  Chowdhury, Ankita ^a   Del Rio, Perla Maria Estrada ^a,b   Tharp, Greg K ^a   Trible, Ronald P ^a   Amara, Rama R ^a   Chahroudi, Ann ^a   Reyes Teran, Gustavo ^b   Bosinger, Steven E ^a   Silvestri, Guido ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUTO NACIONAL DE ENFERMEDADES RESPIRATORIAS   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; CD4 ANTIGEN; CHEMOKINE RECEPTOR CXCR5; DNA VACCINE; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 21; PROTEIN BCL 6; TRANSCRIPTION FACTOR FOXP3; FORKHEAD TRANSCRIPTION FACTOR; INTERLEUKIN DERIVATIVE; REPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CRYOPRESERVATION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HELPER CELL; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; INFECTION; LYMPHOCYTE COUNT; LYMPHOCYTE PROLIFERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHESUS MONKEY; RNA SEQUENCE; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; THYROID FOLLICLE CELL; ANIMAL; B LYMPHOCYTE; BIOSYNTHESIS; CELL PROLIFERATION; CYTOLOGY; GENETIC TRANSCRIPTION; GENETICS; GERMINAL CENTER; HUMORAL IMMUNITY; IMMUNOLOGY; NUCLEOTIDE SEQUENCE; SEQUENCE ANALYSIS; SIMIAN IMMUNODEFICIENCY VIRUS; VIROLOGY;

ANIMALS; B-LYMPHOCYTES; BASE SEQUENCE; CELL PROLIFERATION; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GERMINAL CENTER; IMMUNITY, HUMORAL; INTERLEUKIN-10; INTERLEUKINS; LYMPHOCYTE COUNT; MACACA MULATTA; PROTO-ONCOGENE PROTEINS C-BCL-6; REPRESSOR PROTEINS; SEQUENCE ANALYSIS, RNA; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY; TRANSCRIPTION, GENETIC;

EID: 84942456010     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402701     Document Type: Article

References (36)

1. Pissani, F., and H. Streeck. 2014. Emerging concepts on T follicular helper cell dynamics in HIV infection. Trends Immunol. 35: 278-286.
2. Corti, D., and A. Lanzavecchia. 2013. Broadly neutralizing antiviral antibodies. Annu. Rev. Immunol. 31: 705-742.
3. Murphy, M. K., L. Yue, R. Pan, S. Boliar, A. Sethi, J. Tian, K. Pfafferot, E. Karita, S. A. Allen, E. Cormier, et al. 2013. Viral escape from neutralizing antibodies in early subtype A HIV-1 infection drives an increase in autologous neutralization breadth. PLoS Pathog. 9: e1003173.
4. Crotty, S. 2011. Follicular helper CD4 T cells (TFH). Annu. Rev. Immunol. 29: 621-663.
5. Pratama, A., and C. G. Vinuesa. 2014. Control of TFH cell numbers: why and how? Immunol. Cell Biol. 92: 40-48.
6. Yang, X., J. Yang, Y. Chu, Y. Xue, D. Xuan, S. Zheng, and H. Zou. 2014. T follicular helper cells and regulatory B cells dynamics in systemic lupus erythematosus. PLoS One 9: e88441.
7. Ma, C. S., and E. K. Deenick. 2014. Human T follicular helper (Tfh) cells and disease. Immunol. Cell Biol. 92: 64-71.
8. Vinuesa, C. G. 2012. HIV and T follicular helper cells: a dangerous relationship. J. Clin. Invest. 122: 3059-3062.
9. 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.
10. 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.
11. Petrovas, C., and R. A. Koup. 2014. T follicular helper cells and HIV/SIVspecific antibody responses. Curr. Opin. HIV AIDS 9: 235-241.
12. Chung, Y., S. Tanaka, F. Chu, R. I. Nurieva, G. J. Martinez, S. Rawal, Y. H. Wang, H. Lim, J. M. Reynolds, X. H. Zhou, et al. 2011. Follicular regulatory T cells expressing Foxp3 and Bcl-6 suppress germinal center reactions. Nat. Med. 17: 983-988.
13. Linterman, M. A., W. Pierson, S. K. Lee, A. Kallies, S. Kawamoto, T. F. Rayner, M. Srivastava, D. P. Divekar, L. Beaton, J. J. Hogan, et al. 2011. Foxp3+ follicular regulatory T cells control the germinal center response. Nat. Med. 17: 975-982.
14. Lai, L., S. Kwa, P. A. Kozlowski, D. C. Montefiori, G. Ferrari, W. E. Johnson, V. Hirsch, F. Villinger, L. Chennareddi, P. L. Earl, et al. 2011. Prevention of infection by a granulocyte-macrophage colony-stimulating factor co-expressing DNA/modified vaccinia Ankara simian immunodeficiency virus vaccine. J. Infect. Dis. 204: 164-173.
15. Ortiz, A. M., N. R. Klatt, B. Li, Y. Yi, B. Tabb, X. P. Hao, L. Sternberg, B. Lawson, P. M. Carnathan, E. M. Cramer, et al. 2011. Depletion of CD4+ T cells abrogates post-peak decline of viremia in SIV-infected rhesus macaques. J. Clin. Invest. 121: 4433-4445.
16. Cartwright, E. K., C. S. McGary, B. Cervasi, L. Micci, B. Lawson, S. T. Elliott, R. G. Collman, S. E. Bosinger, M. Paiardini, T. H. Vanderford, et al. 2014. Divergent CD4+ T memory stem cell dynamics in pathogenic and nonpathogenic simian immunodeficiency virus infections. J. Immunol. 192: 4666-4673.
17. Vanderford, T. H., C. Slichter, K. A. Rogers, B. O. Lawson, R. Obaede, J. Else, F. Villinger, S. E. Bosinger, and G. Silvestri. 2012. Treatment of SIV-infected sooty mangabeys with a type-I IFN agonist results in decreased virus replication without inducing hyperimmune activation. Blood 119: 5750-5757.
18. Klatt, N. R., E. Shudo, A. M. Ortiz, J. C. Engram, M. Paiardini, B. Lawson, M. D. Miller, J. Else, I. Pandrea, J. D. Estes, et al. 2010. CD8+ lymphocytes control viral replication in SIVmac239-infected rhesus macaques without decreasing the lifespan of productively infected cells. PLoS Pathog. 6: e1000747.
19. Sandler, N. G., S. E. Bosinger, J. D. Estes, R. T. Zhu, G. K. Tharp, E. Boritz, D. Levin, S. Wijeyesinghe, K. N. Makamdop, G. Q. del Prete, et al. 2014. Type I interferon responses in rhesus macaques prevent SIV infection and slow disease progression. Nature 511: 601-605.
20. Dobin, A., C. A. Davis, F. Schlesinger, J. Drenkow, C. Zaleski, S. Jha, P. Batut, M. Chaisson, and T. R. Gingeras. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29: 15-21.
21. Trapnell, C., D. G. Hendrickson, M. Sauvageau, L. Goff, J. L. Rinn, and L. Pachter. 2013. Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat. Biotechnol. 31: 46-53.
22. Vinuesa, C. G., and J. G. Cyster. 2011. How T cells earn the follicular rite of passage. Immunity 35: 671-680.
23. Alexander, C. M., L. T. Tygrett, A. W. Boyden, K. L. Wolniak, K. L. Legge, and T. J. Waldschmidt. 2011. T regulatory cells participate in the control of germinal centre reactions. Immunology 133: 452-468.
24. Wollenberg, I., A. Agua-Doce, A. Hernández, C. Almeida, V. G. Oliveira, J. Faro, and L. Graca. 2011. Regulation of the germinal center reaction by Foxp3 + follicular regulatory T cells. J. Immunol. 187: 4553-4560.
25. Wing, J. B., and S. Sakaguchi. 2014. Foxp3+ T(reg) cells in humoral immunity. Int. Immunol. 26: 61-69.
26. Liu, W., A. L. Putnam, Z. Xu-Yu, G. L. Szot, M. R. Lee, S. Zhu, P. A. Gottlieb, P. Kapranov, T. R. Gingeras, B. Fazekas de St Groth, et al. 2006. CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells. J. Exp. Med. 203: 1701-1711.
27. Seddiki, N., B. Santner-Nanan, J. Martinson, J. Zaunders, S. Sasson, A. Landay, M. Solomon, W. Selby, S. I. Alexander, R. Nanan, et al. 2006. Expression of interleukin (IL)-2 and IL-7 receptors discriminates between human regulatory and activated T cells. J. Exp. Med. 203: 1693-1700.
28. Dunham, R. M., B. Cervasi, J. M. Brenchley, H. Albrecht, A. Weintrob, B. Sumpter, J. Engram, S. Gordon, N. R. Klatt, I. Frank, et al. 2008. CD127 and CD25 expression defines CD4+ T cell subsets that are differentially depleted during HIV infection. J. Immunol. 180: 5582-5592.
29. Getnet, D., J. F. Grosso, M. V. Goldberg, T. J. Harris, H. R. Yen, T. C. Bruno, N. M. Durham, E. L. Hipkiss, K. J. Pyle, S. Wada, et al. 2010. A role for the transcription factor Helios in human CD4(+)CD25(+) regulatory T cells. Mol. Immunol. 47: 1595-1600.
30. Ray, J. P., H. D. Marshall, B. J. Laidlaw, M. M. Staron, S. M. Kaech, and J. Craft. 2014. Transcription factor STAT3 and type I interferons are corepressive insulators for differentiation of follicular helper and T helper 1 cells. Immunity 40: 367-377.
31. Blackburn, M. J., M. Zhong-Min, F. Caccuri, K. McKinnon, L. Schifanella, Y. Guan, G. Gorini, D. Venzon, C. Fenizia, N. Binello, S. N. Gordon, C. J. Miller, G. Franchini, and M. Vaccari. 2015. Regulatory and helper follicular T cells and antibody avidity to simian immunodeficiency virus glycoprotein 120. J. Immunol. 195: 3227-3236.
32. Sage, P. T., L. M. Francisco, C. V. Carman, and A. H. Sharpe. 2013. The receptor PD-1 controls follicular regulatory T cells in the lymph nodes and blood. Nat. Immunol. 14: 152-161.
33. Birzele, F., T. Fauti, H. Stahl, M. C. Lenter, E. Simon, D. Knebel, A. Weith, T. Hildebrandt, and D. Mennerich. 2011. Next-generation insights into regulatory T cells: expression profiling and FoxP3 occupancy in Human. Nucleic Acids Res. 39: 7946-7960.
34. Moreno-Fernandez, M. E., W. Zapata, J. T. Blackard, G. Franchini, and C. A. Chougnet. 2009. Human regulatory T cells are targets for human immunodeficiency Virus (HIV) infection, and their susceptibility differs depending on the HIV type 1 strain. J. Virol. 83: 12925-12933.
35. Brenchley, J. M., B. J. Hill, D. R. Ambrozak, D. A. Price, F. J. Guenaga, J. P. Casazza, J. Kuruppu, J. Yazdani, S. A. Migueles, M. Connors, et al. 2004. T-cell subsets that harbor human immunodeficiency virus (HIV) in vivo: implications for HIV pathogenesis. J. Virol. 78: 1160-1168.
36. Brenchley, J. M., C. Vinton, B. Tabb, X. P. Hao, E. Connick, M. Paiardini, J. D. Lifson, G. Silvestri, and J. D. Estes. 2012. Differential infection patterns of CD4+ T cells and lymphoid tissue viral burden distinguish progressive and nonprogressive lentiviral infections. Blood 120: 4172-4181.