Circulating CXCR5+PD-1+response predicts influenza vaccine antibody responses in young adults but not elderly adults

Journal of Immunology

Volumn 193, Issue 7, 2014, Pages 3528-3537

  Herati, Ramin Sedaghat ^a   Reuter, Morgan A ^a   Dolfi, Douglas V ^a,b   Mansfield, Kathleen D ^a,b   Aung, Htin ^c,d   Badwan, Osama Z ^c,d   Kurupati, Raj K ^e   Kannan, Senthil ^e   Ertl, Hildegund ^e   Schmader, Kenneth E ^f,g   Betts, Michael R ^a   Canaday, David H ^c,d   Wherry, E John ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b JANSSEN RESEARCH AND DEVELOPMENT   (Belgium)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

^d LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

^e WISTAR INSTITUTE   (United States)

^f DUKE UNIVERSITY MEDICAL CENTER   (United States)

^g DURHAM VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD38 ANTIGEN; CHEMOKINE RECEPTOR CXCR5; CYTOKINE; ICOS PROTEIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN M; IMMUNOGLOBULIN M ANTIBODY; INFLUENZA VACCINE; INTERLEUKIN 21; KI 67 ANTIGEN; PROGRAMMED DEATH 1 RECEPTOR; UNCLASSIFIED DRUG; VIRUS ANTIBODY; CXCR5 PROTEIN, HUMAN; PDCD1 PROTEIN, HUMAN;

ADULT; AGED; AGING; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE RESPONSE; HELPER CELL; HUMAN; HUMAN CELL; IMMUNOGLOBULIN PRODUCTION; IN VITRO STUDY; INFLUENZA; INFLUENZA VACCINATION; PREDICTION; PROTEIN EXPRESSION; T FOLLICULAR HELPER CELL; VIRUS STRAIN; YOUNG ADULT; AGE; B LYMPHOCYTE; BLOOD; CLINICAL TRIAL; COMPARATIVE STUDY; CYTOLOGY; DRUG EFFECT; FEMALE; GERMINAL CENTER; IMMUNOLOGY; MALE; METABOLISM; MULTICENTER STUDY;

ADULT; AGE FACTORS; AGING; ANTIBODIES, VIRAL; ANTIBODY FORMATION; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; FEMALE; GERMINAL CENTER; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INFLUENZA VACCINES; MALE; PROGRAMMED CELL DEATH 1 RECEPTOR; RECEPTORS, CXCR5;

EID: 84907200998     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302503     Document Type: Article

References (64)

1. Osterholm, M. T ., N. S. Kelley, A. Sommer, and E. A. Belongia. 2012. Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect. Dis. 12: 36-44.
2. Goodwin, K., C. Vi boud, and L. Simonsen. 2006. Antibody response to influenza vaccination in the elderly: a quantitative review. Vaccine 24: 1159-1169.
3. Jackson, L., M. L. Jackson, C. H. Phillips, J. Benoit, D. Cole, T. A. K. Koepel, H. Q. Mclean, J. K. Meece, S. K. Strey, E. Maria, et al; Centers for Disease Control and Prevention (CDC) . 2013. Interim adjusted estimates of seasonal influenza vaccine effectiveness-United States, February 2013. MMWR Morb. Mortal. Wkly. Rep. 62: 119-123.
4. Talbot, H. K., M. R. Griffin, Q. Chen, Y. Zhu, J. V.Williams, and K. M. Edwards. 2011. Effectiveness of seasonal vaccine in preventing confirmed influenzaassociated hospitalizations in community dwelling old er adults. J. Infect. Dis. 203: 500-508.
5. Thompson,W.W., M. R. Moore, E.Weintraub, P.-Y. Cheng, X. Jin, C. B. Bridges, J. S. Bresee, and D. K. Shay. 2009. Estimating influenza-associated deaths in the United States. Am. J. Public Health 99(Suppl 2): S225-S230.
6. Haynes, L., and S. L. Swain. 2006. Why aging T cells fail: implications for vaccination. Immunity 24: 663-666.
7. Moro-Garcí a, M. A., R. Alonso-Arias, and C. López-Larrea. 2013. When Aging Reaches CD4+ T-Cells: Phenotypic and Functional Changes. Front. Immunol. 4: 107.
8. Goronzy, J. J., and C. M . Weyand. 2013. Understanding immunosenescence to improve responses to vaccines. Nat. Immunol. 14: 428-436.
9. World Health Organization Influenza (seasonal): 1-3., Available at, http://www.who.int/mediacentre/factsheets/fs211/en/, Accessed June 1,2014.
10. McCullers, J. A., and V. C. Huber. 2012. Correlates of vaccine protection from influenza and its complications. Hum. Vaccin. Immunother. 8: 34-44.
11. Ohmit, S. E., J. G. Petrie, R. T. Cross, E. Johnson, and A. S. Monto. 2011. Influenza hemagglutination-inhibition antibody titer as a correlate of vaccineinduced protection. J. Infect. Dis. 204: 1879 -1885.
12. Jiang, N., J. He, J. A. Weinstein, L. Penland, S. Sasaki, X. S. He, C. L. Dekker, N.-Y. Zheng, M. Huang, M. Sullivan, et al. 2013. Lineage structur e of the human antibody repertoire in response to influenza vaccination. Sci. Transl. Med. 5: 171ra19.
13. Sasaki, S., M. Sullivan, C. F. Narvaez, T. H. Holmes, D. Furman, N. Y. Zheng, M. Nishtala, J. Wrammert, K. Smith, J. A. James, et al. 2011. Limited efficacy of inactivated influenza vaccine in elderly individuals is associated with decreased production of vaccine-specific antibodies. J. Clin. Invest. 121: 3109-3119.
14. Pereira, L. F., A. P. D. de Souza, T. J. Borges, and C. Bonorino. 2011. Impaired in vivo CD4+ T cell expansion and differentiation in aged mice is not solely due to T cell defects: decreased stimulation by aged d endritic cells. Mech. Ageing Dev. 132: 187-194.
15. Crotty, S. 2011. Follicular helper CD4 T cells (TFH). Annu. Rev. Immunol. 29: 621-663.
16. Schaerli, P., K. Willimann, A. B. Lang, M. Lipp, P. Loetscher, and B. Moser. 2000. CXC chemokine receptor 5 expression defines follicular homing T cells with B cell helper function. J. Exp. Med. 192: 1553-1562.
17. Schaerli, P., P. Loetscher, and B. Moser. 2001. Cutting edge: induction of follicular homing precedes effector Th cell development. J. Immunol. 167: 6082-6086.
18. Ansel, K. M., L. J. McHeyzer-Williams, V. N. Ngo, M. G. McHeyzer-Williams, and J. G. Cyster. 1999. In vivo-activated CD4 T cells upregulate CXC chemokine receptor 5 and reprogram their response to lymphoid chemokines. J. Exp. Med. 190: 1123-1134.
19. Booth, C., K. C. Gilmour, P. Veys, A. R. Gennery, M. A. Slatter, H. Chapel, P. T. Heath, C. G. Steward, O. Smith, A. O'Meara, et al. 2011. X-linked lymphoproliferative disease due to SAP/SH2D1A deficiency: a multicenter study on the manifestations, management and outcome of the disease. [Published erratum appears in 2011. Blood 118: 5060]. Blood 117: 53-62.
20. Hu, J., C. Havenar-Daughton, and S. Crotty. 2013. Modulation of SAP dependent T:B cell interactions as a strategy to improve vaccination. Curr. Opin. Virol. 3: 363-370.
21. Kroenke, M. A., D. Eto, M. Locci, M. Cho, T. Davidson, E. K. Haddad, and S. Crotty. 2012. Bcl6 and Maf cooperate to instruct human follicular helper CD4 T cell differentiation. J. Immunol. 188: 3734-3744.
22. Q i, H., J. L. Cannons, F. Klauschen, P. L. Schwartzberg, and R. N. Germain. 2008. SAP-controlled T-B cell interactions underlie germinal centre formation. Nature 455: 764-769.
23. Choi, Y. S., D. Eto, J. A. Yang, C. Lao, and S. Crotty. 2013. Cutting edge: STAT1 is required for IL-6-mediated Bcl6 induction for early follicular helper cell differentiation. J. Immunol. 190: 3049-3053.
24. Eto , D., C. Lao, D. DiToro, B. Barnett, T. C. Escobar, R. Kageyama, I. Yusuf, and S. Crotty. 2011. IL-21 and IL-6 are critical for different aspects of B cell immunity and redundantly induce optimal follicular helper CD4 T cell (Tfh) differentiation. PLoS ONE 6: e17739.
25. 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 naï ve human CD4(+) T cells to the T follicular helper (T(FH)) cell lineage is induced by IL-12. Immunol. Cell Biol. 87: 590-600.
26. Ma, C. S., S. Pittaluga, D. T. Avery, N. J. Hare, I. Maric, A. D. Klion, K. E. Nichols, and S. G. Tangye. 2006. Selective generation of functional somatically mutated IgM+CD27+, but not Ig isotype-switched, memory B cells in X-linked lymphoproliferative disease. J. Clin. Invest. 116: 322-333 .
27. Akiba, H., K. Takeda, Y. Kojima, Y. Usui, N. Harada, T. Yamazaki, J. Ma, K. Tezuka, H. Yagita, and K. Okumura. 2005. The role of ICOS in the CXCR5+ follicular B helper T cell maintenance in vivo. J. Immunol. 175: 2340-2348.
28. Bossaller, L., J. Burger, R. Draeger, B. Grimbacher, R. K noth, A. Plebani, A. Durandy, U. Baumann, M. Schlesier, A. A. Welcher, et al. 2006. ICOS deficiency is associated with a severe reduction of CXCR5+CD4 germinal center Th cells. J. Immunol. 177: 4927-4932.
29. 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 follic ular helper cells in chronic HIV infection. J. Clin. Invest. 122: 3271-3280.
30. Cubas R. A.,J. C. Mudd,A. L. Savoye,M. Perreau,J. van Grevenynghe,T. Metcalf,E. Connick,A. Meditz, G. J. Freeman, G. Abesada-Terk, Jr., et al., 2013. Inadequate T follicular cell help impairs B cell immunity during HIV infection. Nat. Med., 19, 494-499.
31. Chevalier, N., D. Jarrossay, E. Ho, D. T. Avery, C. S. Ma, D. Yu, F. Sallusto, S. G. Tangye, and C. R. Mackay. 2011. CXCR5 expressing human central memory CD4 T cells and their relevance for humoral immune responses. J. Immunol. 186: 5556-5568.
32. Morita, R., N. Schmitt, S. E. Bentebibel, R. Ranganathan, L. Bourdery, G. Zurawski, E. Foucat, M. Dullaers, S. Oh, N. Sabzghabaei, et al. 2011. Human blood CXCR5(+)CD4(+) T cells are cou nterparts of T follicular cells and contain specific subsets that differentially support antibody secretion. Immunity 34: 108-121.
33. Rasheed, A.-U., H.-P. Rahn, F. Sallusto, M. Lipp, and G. Müller. 2006. Follicular B helper T cell activity is confined to CXCR5(hi)ICOS(hi) CD4 T cells and is independent of CD57 expression. Eur. J. Immunol. 36: 1892-1903.
34. Simpson, N., P. A. Gatenby, A. Wilson, S. Malik, D. A. Fulcher, S. G. Tangye, H. Manku, T. J. Vyse, G. Roncador, G. A. Huttley, et al. 2010. Expansion of circulating T cells resembling follicular helper T cells is a fixed phenotype that identifies a subset of seve re systemic lupus erythematosus. Arthritis Rheum. 62: 234-244.
35. Romme Christensen, J., L. Börnsen, R. Ratzer, F. Piehl, M. Khademi, T. Olsson, P. S. Sørensen, and F. Sellebjerg. 2013. System ic inflammation in progressive multiple sclerosis involves follicular T-helper, Th17-and activated B-cells and correlates with progression. PLoS ONE 8: e57820.
36. Bentebibel, S., S. Lopez, G. Obermoser, N. Sc hmitt, C. Mueller, C. Harrod, E. Flano, A. Mejias, R. A. Albrecht, D. Blankenship, et al. 2013. Induction of ICOS+CXCR3+CXCR5+ TH cells correlates with antibody responses to influenza vaccination. Sci. Transl. Med. 5: 176ra32.
37. Locci, M., C. Havenar-Daughton, E. Landais, J. Wu, M. A. Kroenke, C. L. Arlehamn, L. F. Su, R. Cubas, M. M. Davis, A. Sette, et al; International AIDS Vaccine Initiative Pr otocol C Principal Investigators. 2013. Human circulating PD-+1CXCR3-CXCR5+ memory Tfh cells are highly functional and correlate with broadly neutralizing HIV antibody responses. Immunity 39: 758-769.
38. Spensieri, F., E. Borgogni, L. Zedda, M. Bardelli, F. Buricchi, G. Volpini, E. Fragapane, S. Tavarini, O. Finco, R. Rappuoli, et al. 2013. Human circulating influenza-CD4+ ICOS1+IL-21+ T cells expand after vaccination, exert h elper function, and predict antibody responses. Proc. Natl. Acad. Sci. USA 110: 14330-14335.
39. WHO Global Influenza Surveillance Network. 2011. Manual for the Laboratory Diagnosis and Virological Surveillance of Influenza. WHO Press, Geneva, Switzerland.
40. Choi, Y. S., R. Kageyama, D. Eto, T. C. Escobar, R. J. Johnston, L. Monticelli, C. Lao, and S. Crotty. 2011. ICOS receptor instructs T follicular help er cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6. Immunity 34: 932-946.
41. 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.
42. L üthje, K., A. Kallies, Y. Shimohakamada, G. T. Belz, A. Light, D. M. Tarlinton, and S. L. Nutt. 2012. The development and fate of follicular helper T cells defined by an IL-21 reporter mouse. Nat. Immunol. 13: 491-498.
43. Li, X., H. Miao, A. Henn, D. J. Topham, H.Wu, M. S. Zand, and T. R. Mosmann. 2012. Ki-67 expression reveals strong, transient influenza specific CD4 T cell responses after adult vaccination. Vac cine 30: 4581-4584.
44. Soares, A., L. Govender, J. Hughes, W. Mavakla, M. de Kock, C. Barnard, B. Pienaar, E. Janse van Rensburg, G. Jacobs, G. Khomba, et al. 2010. Novel appl ication of Ki67 to quantify antigen-specific in vitro lymphoproliferation. J. Immunol. Methods 362: 43-50.
45. Miller, J. D., R. G. van der Most, R. S. Akondy, J. T. Glidewell, S. Albott, D. Masopust, K. Murali-Krishna, P. L. Mahar, S. Edupuganti, S. Lalor, et al. 2008. Human effector and memory CD8+ T cell responses to smallpox and yellow fever vaccines. Immunity 28: 710-722.
46. Pallikkuth, S., A. Parmigiani, S. Y. Silva, V. K. George, M. Fischl, R. Pahwa, and S. Pahwa. 2012. Impaired peripheral blood T-follicular helper cell function in HIV-infected nonresponders to the 2009 H1N1/09 vaccine. Blood 120: 985-993.
47. Cox, R. J., K. A. Brokstad, M. A. Zuckerman, J. M. Wood, L. R. Haaheim, and J. S. Oxford. 1994. An early humoral immune response in peripheral blood following parenteral inactivated influenza vaccination. Vaccine 12: 993-999.
48. el-Madhun, A. S., R. J. Cox, A. S øreide, J. Olofsson, and L. R. Haaheim. 1998. Systemic and mucosal immune responses in young children and adults after parenteral influenza vaccination. J. Infect. Dis. 178: 933-939.
49. Remarque, E. J., J. M. de Jong, R. J. van der Klis, N. Masurel, and G. J. Ligthart. 1999. Dose-dependent antibody response to influenza H1N1 vaccine component in elderly nursing home patients. Exp. Gerontol. 34: 109-115.
50. Kuilman, T., C. Michaloglou, L. C. W. Vredeveld, S. Douma, R. van Doorn, C. J. Desmet, L. A. Aarden, W. J. Mooi, and D. S. Peeper. 2008. Oncogeneinduced senescence relayed by an interleukin-dependent inflammatory network. Cell 133: 1019-1031.
51. Kogut, I., J. L. Scholz, M. P. Cancro, and J. C. Cambier. 2012. B cell maintenance and function in aging. Semin. Immunol. 24: 342-349.
52. Parmigiani, A., M. L. Alcaide, R. Freguja, S. Pallikkuth, D. Frasca, M. A. Fischl, and S. Pahwa. 2013. Impaired antibody response to influenza vaccine in HIVinfected and uninfected aging women is associated with immune activation and inflammation. PLoS ONE 8: e79816.
53. He, J., L. M. Tsai, Y. A. Leong, X. Hu, C. S. Ma, N. Chevalier, X. Sun, K. Vandenberg, S. Rockman, Y. Ding, et al. 2013. Circulating precursor CCR7(lo)PD-1(hi) CXCR5+ CD4+ T cells indicate Tfh cell activity an d promote antibody responses upon antigen reexposure. Immunity 39: 770-781.
54. Buonfiglio, D., M. Bragardo, S. Bonissoni, V. Redoglia, R. Cauda, S. Zupo, V. L. Burgio, H. Wolff, K. Franssila, G. G aidano, et al. 1999. Characterization of a novel human surface molecule selectively expressed by mature thymocytes, activated T cells and subsets of T cell lymphomas. Eur. J. Immunol. 29: 2863-2874.
55. Buonfiglio, D., M. Bragardo, V. Redoglia, R. Vaschetto, F. Bottarel, S. Bonissoni, T. Bensi, C. Mezzatesta, C. A. Janeway, Jr., and U. Dianzani. 2000. The T cell activation molecule H4 and th e CD28-like molecule ICOS are identical. Eur. J. Immunol. 30: 3463-3467.
56. Allman, D., A. Jain, A. Dent, R. R. Maile, T. Selvaggi, M. R. Kehry, and L. M. Staudt. 1996. BCL-6 expression during B-cell activation. Blood 87: 5257-5268.
57. Niu, H., B. H. Ye, and R. Dalla-Favera. 1998. Antigen receptor signaling induces MAP kinase-mediated phosphorylation and degradation of the BCL-6 transcription factor. Genes Dev. 12: 1953-1961.
58. Gross, P. A., C. Russo, S. Dran, P. Cataruozolo, G. Munk, and S. C. Lancey. 1997. Time to earliest peak serum antibody response to influenza vaccine in the elderly. Clin. Diagn. Lab. Immunol. 4: 491-492.
59. Miller, M. S., T. J. Gardner, F. Krammer, L. C. Aguado, D. Tortorella, C. F. Basler, and P. Palese. 2013. Neutralizing Ant ibodies Against Previously Encountered Influenza Virus Strains Increase over Time: A Longitudinal Analysis. Sci. Transl. Med. 5: 198ra107.
60. Roti, M., J. Yang, D. Berger, L. Huston, E. A. James, and W. W. Kwok. 2008. Healthy human subjects have CD4+ T cells directed against H5N1 influenza virus. J. Immunol. 180: 1758-1768.
61. Weber, J. P., F. Fuhrmann, and A. Hutloff. 2012. T-follicular he lper cells survive as long-term memory cells. Eur. J. Immunol. 42: 1981- 1988.
62. Marinova, E., S. Han, and B. Zheng. 2006. Human germinal center T cells are unique Th cells with high propensity for apoptosis induction. Int. Immunol. 18: 1337-1345.
63. Trautmann, L., L. Janbazian, N. Chomont, E. A. Said, S. Gimmig, B. Bessette, M. R. Boulassel, E. Delwart, H. Sepulveda, R. S. Balder as, et al. 2006. Upregulation of PD-1 expression on HIV-specific CD8+ T cells leads to reversible immune dysfunction. Nat. Med. 12: 1198-1202.
64. Blackman, M. A., and D. L. Woodland. 2011. The narrowing of the CD8 T cell repertoire in old age. Curr. Opin. Immunol. 23: 537-542.