Targeting antigen to Clec9A primes follicular Th cell memory responses capable of robust recall

Journal of Immunology

Volumn 195, Issue 3, 2015, Pages 1006-1014

  Kato, Yu ^a   Zaid, Ali ^a   Davey, Gayle M ^a   Mueller, Scott N ^a   Nutt, Stephen L ^a,b   Zotos, Dimitra ^a,b   Tarlinton, David M ^a,b   Shortman, Ken ^a,b   Lahoud, Mireille H ^c,d   Heath, William R ^a   Caminschi, Irina ^a,c  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c MACFARLANE BURNET INSTITUTE FOR MEDICAL RESEARCH AND PUBLIC HEALTH   (Australia)

^d MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CHEMOKINE RECEPTOR CXCR5; GLYCOPROTEIN D; IMMUNOGLOBULIN G1; INTERLEUKIN 21; LYMPHOCYTE RECEPTOR; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CLEC9A; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN BCL 6; PROTEIN CLEC9A; UNCLASSIFIED DRUG; ANTIGEN; BCL6 PROTEIN, MOUSE; BLR1 PROTEIN, MOUSE; CLEC9A PROTEIN, MOUSE; DNA BINDING PROTEIN; GLYCOPROTEIN D, HUMAN HERPESVIRUS 1; IL21R PROTEIN, MOUSE; IMMUNOGLOBULIN RECEPTOR; INTERLEUKIN 21 RECEPTOR ALPHA; INTERLEUKIN DERIVATIVE; LECTIN; OVALBUMIN; PDCD1 PROTEIN, MOUSE; VIRUS ENVELOPE PROTEIN;

ANIMAL EXPERIMENT; ANTIBODY PRODUCTION; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DRUG POTENCY; FOLLICULAR HELPER T LYMPHOCYTE; GERMINAL CENTER; HELPER CELL; HERPES SIMPLEX VIRUS 1; IMMUNOLOGICAL MEMORY; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; VACCINATION; ADOPTIVE TRANSFER; ANIMAL; B LYMPHOCYTE; BIOSYNTHESIS; C57BL MOUSE; CELL DIFFERENTIATION; CYTOLOGY; DENDRITIC CELL; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; TRANSPLANTATION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS; B-LYMPHOCYTES; CELL DIFFERENTIATION; DENDRITIC CELLS; DNA-BINDING PROTEINS; GERMINAL CENTER; IMMUNOLOGIC MEMORY; INTERLEUKIN-21 RECEPTOR ALPHA SUBUNIT; INTERLEUKINS; LECTINS, C-TYPE; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OVALBUMIN; PROGRAMMED CELL DEATH 1 RECEPTOR; RECEPTORS, CXCR5; RECEPTORS, IMMUNOLOGIC; T-LYMPHOCYTES, HELPER-INDUCER; VIRAL ENVELOPE PROTEINS;

EID: 84937690110     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500767     Document Type: Article

References (61)

1. Pooley, J. L., W. R. Heath, and K. Shortman. 2001. Cutting edge: intravenous soluble antigen is presented to CD4 T cells by CD8- dendritic cells, but crosspresented to CD8 T cells by CD8+ dendritic cells. J. Immunol. 166: 5327-5330.
2. den Haan, J. M., S. M. Lehar, and M. J. Bevan. 2000. CD8+ but not CD82dendritic cells cross-prime cytotoxic T cells in vivo. J. Exp. Med. 192: 1685-1696.
3. Smith, C. M., G. T. Belz, N. S. Wilson, J. A. Villadangos, K. Shortman, F. R. Carbone, and W. R. Heath. 2003. Cutting edge: conventional CD8 alpha+ dendritic cells are preferentially involved in CTL priming after footpad infection with herpes simplex virus-1. J. Immunol. 170: 4437-4440.
4. Belz, G. T., C. M. Smith, D. Eichner, K. Shortman, G. Karupiah, F. R. Carbone, and W. R. Heath. 2004. Cutting edge: conventional CD8 alpha+ dendritic cells are generally involved in priming CTL immunity to viruses. J. Immunol. 172: 1996-2000.
5. Dudziak, D., A. O. Kamphorst, G. F. Heidkamp, V. R. Buchholz, C. Trumpfheller, S. Yamazaki, C. Cheong, K. Liu, H.-W. Lee, C. G. Park, et al. 2007. Differential antigen processing by dendritic cell subsets in vivo. Science 315: 107-111.
6. Schnorrer, P., G. M. N. Behrens, N. S. Wilson, J. L. Pooley, C. M. Smith, D. El-Sukkari, G. Davey, F. Kupresanin, M. Li, E. Maraskovsky, et al. 2006. The dominant role of CD8+ dendritic cells in cross-presentation is not dictated by antigen capture. Proc. Natl. Acad. Sci. USA 103: 10729-10734.
7. Hochrein, H., M. O'Keeffe, T. Luft, S. Vandenabeele, R. J. Grumont, E. Maraskovsky, and K. Shortman. 2000. Interleukin (IL)-4 is a major regulatory cytokine governing bioactive IL-12 production by mouse and human dendritic cells. J. Exp. Med. 192: 823-833.
8. Maldonado-López, R., T. De Smedt, P. Michel, J. Godfroid, B. Pajak, C. Heirman, K. Thielemans, O. Leo, J. Urbain, and M. Moser. 1999. CD8alpha+ and CD8alpha- subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J. Exp. Med. 189: 587-592.
9. Pulendran, B., J. L. Smith, G. Caspary, K. Brasel, D. Pettit, E. Maraskovsky, and C. R. Maliszewski. 1999. Distinct dendritic cell subsets differentially regulate the class of immune response in vivo. Proc. Natl. Acad. Sci. USA 96: 1036-1041.
10. Bonifaz, L., D. Bonnyay, K. Mahnke, M. Rivera, M. C. Nussenzweig, and R. M. Steinman. 2002. Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance. J. Exp. Med. 196: 1627-1638.
11. Bonifaz, L. C., D. P. Bonnyay, A. Charalambous, D. I. Darguste, S. Fujii, H. Soares, M. K. Brimnes, B. Moltedo, T. M. Moran, and R. M. Steinman. 2004. In vivo targeting of antigens to maturing dendritic cells via the DEC-205 receptor improves T cell vaccination. J. Exp. Med. 199: 815-824.
12. Hawiger, D., K. Inaba, Y. Dorsett, M. Guo, K. Mahnke, M. Rivera, J. V. Ravetch, R. M. Steinman, and M. C. Nussenzweig. 2001. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J. Exp. Med. 194: 769-779.
13. Mahnke, K., Y. Qian, J. Knop, and A. H. Enk. 2003. Induction of CD4+/CD25+ regulatory T cells by targeting of antigens to immature dendritic cells. Blood 101: 4862-4869.
14. Caminschi, I., A. I. Proietto, F. Ahmet, S. Kitsoulis, J. Shin Teh, J. C. Y. Lo, A. Rizzitelli, L. Wu, D. Vremec, S. L. H. van Dommelen, et al. 2008. The dendritic cell subtype-restricted C-type lectin Clec9A is a target for vaccine enhancement. Blood 112: 3264-3273.
15. Joffre, O. P., D. Sancho, S. Zelenay, A. M. Keller, and C. Reis e Sousa. 2010. Efficient and versatile manipulation of the peripheral CD4+ T-cell compartment by antigen targeting to DNGR-1/CLEC9A. Eur. J. Immunol. 40: 1255-1265.
16. Lahoud, M. H., F. Ahmet, S. Kitsoulis, S. S. Wan, D. Vremec, C.-N. Lee, B. Phipson, W. Shi, G. K. Smyth, A. M. Lew, et al. 2011. Targeting antigen to mouse dendritic cells via Clec9A induces potent CD4 T cell responses biased toward a follicular helper phenotype. J. Immunol. 187: 842-850.
17. Li, J., F. Ahmet, L. C. Sullivan, A. G. Brooks, S. J. Kent, R. De Rose, A. M. Salazar, C. Reis e Sousa, K. Shortman, M. H. Lahoud, et al. 2015. Antibodies targeting Clec9A promote strong humoral immunity without adjuvant in mice and non-human primates. Eur. J. Immunol. 45: 854-864.
18. Idoyaga, J., C. Cheong, K. Suda, N. Suda, J. Y. Kim, H. Lee, C. G. Park, and R. M. Steinman. 2008. Cutting edge: langerin/CD207 receptor on dendritic cells mediates efficient antigen presentation on MHC I and II products in vivo. J. Immunol. 180: 3647-3650.
19. Idoyaga, J., A. Lubkin, C. Fiorese, M. H. Lahoud, I. Caminschi, Y. Huang, A. Rodriguez, B. E. Clausen, C. G. Park, C. Trumpfheller, and R. M. Steinman. 2011. Comparable T helper 1 (Th1) and CD8 T-cell immunity by targeting HIV gag p24 to CD8 dendritic cells within antibodies to Langerin, DEC205, and Clec9A. Proc. Natl. Acad. Sci. USA 108: 2384-2389.
20. Lahoud, M. H., A. I. Proietto, F. Ahmet, S. Kitsoulis, L. Eidsmo, L. Wu, P. Sathe, S. Pietersz, H. W. Chang, I. D. Walker, et al. 2009. The C-type lectin Clec12A present on mouse and human dendritic cells can serve as a target for antigen delivery and enhancement of antibody responses. J. Immunol. 182: 7587-7594.
21. Sancho, D., D. Mourão-Sá, O. P. Joffre, O. Schulz, N. C. Rogers, D. J. Pennington, J. R. Carlyle, and C. Reis e Sousa. 2008. Tumor therapy in mice via antigen targeting to a novel, DC-restricted C-type lectin. J. Clin. Invest. 118: 2098-2110.
22. Soares, H., H. Waechter, N. Glaichenhaus, E. Mougneau, H. Yagita, O. Mizenina, D. Dudziak, M. C. Nussenzweig, and R. M. Steinman. 2007. A subset of dendritic cells induces CD4+ T cells to produce IFN-gamma by an IL-12-independent but CD70-dependent mechanism in vivo. J. Exp. Med. 204: 1095-1106.
23. Boscardin, S. B., J. C. R. Hafalla, R. F. Masilamani, A. O. Kamphorst, H. A. Zebroski, U. Rai, A. Morrot, F. Zavala, R. M. Steinman, R. S. Nussenzweig, and M. C. Nussenzweig. 2006. Antigen targeting to dendritic cells elicits long-lived T cell help for antibody responses. J. Exp. Med. 203: 599-606.
24. Loschko, J., A. Schlitzer, D. Dudziak, I. Drexler, N. Sandholzer, C. Bourquin, W. Reindl, and A. B. Krug. 2011. Antigen delivery to plasmacytoid dendritic cells via BST2 induces protective T cell-mediated immunity. J. Immunol. 186: 6718-6725.
25. Park, H. Y., A. Light, M. H. Lahoud, I. Caminschi, D. M. Tarlinton, and K. Shortman. 2013. Evolution of B cell responses to Clec9A-targeted antigen. J. Immunol. 191: 4919-4925.
26. Kretschmer, K., I. Apostolou, D. Hawiger, K. Khazaie, M. C. Nussenzweig, and H. von Boehmer. 2005. Inducing and expanding regulatory T cell populations by foreign antigen. Nat. Immunol. 6: 1219-1227.
27. Pereira, J. P., L. M. Kelly, Y. Xu, and J. G. Cyster. 2009. EBI2 mediates B cell segregation between the outer and centre follicle. Nature 460: 1122-1126.
28. Gatto, D., D. Paus, A. Basten, C. R. Mackay, and R. Brink. 2009. Guidance of B cells by the orphan G protein-coupled receptor EBI2 shapes humoral immune responses. Immunity 31: 259-269.
29. Victora, G. D., T. A. Schwickert, D. R. Fooksman, A. O. Kamphorst, M. Meyer-Hermann, M. L. Dustin, and M. C. Nussenzweig. 2010. Germinal center dynamics revealed by multiphoton microscopy with a photoactivatable fluorescent reporter. Cell 143: 592-605.
30. Chappell, C. P., K. E. Draves, N. V. Giltiay, and E. A. Clark. 2012. Extrafollicular B cell activation by marginal zone dendritic cells drives T celldependent antibody responses. J. Exp. Med. 209: 1825-1840.
31. Gatto, D., K. Wood, I. Caminschi, D. Murphy-Durland, P. Schofield, D. Christ, G. Karupiah, and R. Brink. 2013. The chemotactic receptor EBI2 regulates the homeostasis, localization and immunological function of splenic dendritic cells. Nat. Immunol. 14: 446-453.
32. Corbett, A. J., I. Caminschi, B. S. McKenzie, J. L. Brady, M. D. Wright, P. L. Mottram, P. M. Hogarth, A. N. Hodder, Y. Zhan, D. M. Tarlinton, et al. 2005. Antigen delivery via two molecules on the CD8- dendritic cell subset induces humoral immunity in the absence of conventional "danger". Eur. J. Immunol. 35: 2815-2825.
33. Crotty, S. 2011. Follicular helper CD4 T cells (TFH). Annu. Rev. Immunol. 29: 621-663.
34. Barnden, M. J., J. Allison, W. R. Heath, and F. R. Carbone. 1998. Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and betachain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 76: 34-40.
35. Bedoui, S., P. G. Whitney, J. Waithman, L. Eidsmo, L. Wakim, I. Caminschi, R. S. Allan, M. Wojtasiak, K. Shortman, F. R. Carbone, et al. 2009. Crosspresentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat. Immunol. 10: 488-495.
36. Lüthje, 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.
37. Ozaki, K., R. Spolski, C. G. Feng, C.-F. Qi, J. Cheng, A. Sher, H. C. Morse, III, C. Liu, P. L. Schwartzberg, and W. J. Leonard. 2002. A critical role for IL-21 in regulating immunoglobulin production. Science 298: 1630-1634.
38. van Lint, A., M. Ayers, A. G. Brooks, R. M. Coles, W. R. Heath, and F. R. Carbone. 2004. Herpes simplex virus-specific CD8+ T cells can clear established lytic infections from skin and nerves and can partially limit the early spread of virus after cutaneous inoculation. J. Immunol. 172: 392-397.
39. 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 Protocol C Principal Investigators. 2013. Human circulating PD-1+CXCR3-CXCR5+ memory Tfh cells are highly functional and correlate with broadly neutralizing HIV antibody responses. Immunity 39: 758-769.
40. Liu, X., X. Yan, B. Zhong, R. I. Nurieva, A. Wang, X. Wang, N. Martin-Orozco, Y. Wang, S. H. Chang, E. Esplugues, et al. 2012. Bcl6 expression specifies the T follicular helper cell program in vivo. J. Exp. Med. 209: 1841-1852, S1-S24.
41. 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.
42. Hale, J. S., B. Youngblood, D. R. Latner, A. U. R. 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.
43. Gebhardt, T., P. G. Whitney, A. Zaid, L. K. Mackay, A. G. Brooks, W. R. Heath, F. R. Carbone, and S. N. Mueller. 2011. Different patterns of peripheral migration by memory CD4+ and CD8+ T cells. Nature 477: 216-219.
44. MacLeod, M. K. L., A. McKee, F. Crawford, J. White, J. Kappler, and P. Marrack. 2008. CD4 memory T cells divide poorly in response to antigen because of their cytokine profile. Proc. Natl. Acad. Sci. USA 105: 14521-14526.
45. Johnston, R. J., A. C. Poholek, D. DiToro, I. Yusuf, D. Eto, B. Barnett, A. L. Dent, J. Craft, and S. Crotty. 2009. Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science 325: 1006-1010.
46. Yu, D., S. Rao, L. M. Tsai, S. K. Lee, Y. He, E. L. Sutcliffe, M. Srivastava, M. Linterman, L. Zheng, N. Simpson, et al. 2009. The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment. Immunity 31: 457-468.
47. 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.
48. Nakayamada, S., Y. Kanno, H. Takahashi, D. Jankovic, K. T. Lu, T. A. Johnson, H. W. Sun, G. Vahedi, O. Hakim, R. Handon, et al. 2011. Early Th1 cell differentiation is marked by a Tfh cell-like transition. Immunity 35: 919-931.
49. Szabo, S. J., S. T. Kim, G. L. Costa, X. Zhang, C. G. Fathman, and L. H. Glimcher. 2000. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100: 655-669.
50. Linterman, M. A., R. J. Rigby, R. K. Wong, D. Yu, R. Brink, J. L. Cannons, P. L. Schwartzberg, M. C. Cook, G. D. Walters, and C. G. Vinuesa. 2009. Follicular helper T cells are required for systemic autoimmunity. J. Exp. Med. 206: 561-576.
51. Lee, S. K., R. J. Rigby, D. Zotos, L. M. Tsai, S. Kawamoto, J. L. Marshall, R. R. Ramiscal, T. D. Chan, D. Gatto, R. Brink, et al. 2011. B cell priming for extrafollicular antibody responses requires Bcl-6 expression by T cells. J. Exp. Med. 208: 1377-1388.
52. Yi, T., and J. G. Cyster. 2013. EBI2-mediated bridging channel positioning supports splenic dendritic cell homeostasis and particulate antigen capture. eLife 2: e00757.
53. Balázs, M., F. Martin, T. Zhou, and J. Kearney. 2002. Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity 17: 341-352.
54. Idoyaga, J., N. Suda, K. Suda, C. G. Park, and R. M. Steinman. 2009. Antibody to Langerin/CD207 localizes large numbers of CD8a+ dendritic cells to the marginal zone of mouse spleen. Proc. Natl. Acad. Sci. USA 106: 1524-1529.
55. Dorner, B. G., M. B. Dorner, X. Zhou, C. Opitz, A. Mora, S. Güttler, A. Hutloff, H. W. Mages, K. Ranke, M. Schaefer, et al. 2009. Selective expression of the chemokine receptor XCR1 on cross-presenting dendritic cells determines cooperation with CD8+ T cells. Immunity 31: 823-833.
56. Hartung, E., M. Becker, A. Bachem, N. Reeg, A. Jäkel, A. Hutloff, H. Weber, C. Weise, C. Giesecke, V. Henn, et al. 2015. Induction of potent CD8 T cell cytotoxicity by specific targeting of antigen to cross-presenting dendritic cells in vivo via murine or human XCR1. J. Immunol. 194: 1069-1079.
57. Coffey, F., B. Alabyev, and T. Manser. 2009. Initial clonal expansion of germinal center B cells takes place at the perimeter of follicles. Immunity 30: 599-609.
58. Kerfoot, S. M., G. Yaari, J. R. Patel, K. L. Johnson, D. G. Gonzalez, S. H. Kleinstein, and A. M. Haberman. 2011. Germinal center B cell and T follicular helper cell development initiates in the interfollicular zone. Immunity 34: 947-960.
59. Ahmed, R., and D. Gray. 1996. Immunological memory and protective immunity: understanding their relation. Science 272: 54-60.
60. Pepper, M., A. J. Pagán, B. Z. Igyártó, J. J. Taylor, and M. K. Jenkins. 2011. Opposing signals from the Bcl6 transcription factor and the interleukin-2 receptor generate T helper 1 central and effector memory cells. Immunity 35: 583-595.
61. MacLeod, M. K. L., A. David, A. S. McKee, F. Crawford, J. W. Kappler, and P. Marrack. 2011. Memory CD4 T cells that express CXCR5 provide accelerated help to B cells. J. Immunol. 186: 2889-2896.