Cyclosporine-resistant, Rab27a-independent mobilization of intracellular preformed CD40 ligand mediates antigen-specific T cell help in vitro

Journal of Immunology

Volumn 187, Issue 2, 2011, Pages 626-634

  Koguchi, Yoshinobu ^a   Gardell, Jennifer L ^a   Thauland, Timothy J ^a   Parker, David C ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN INHIBITOR; CD40 LIGAND; CD70 ANTIGEN; CYCLOSPORIN; RAB27A PROTEIN; TACROLIMUS;

ANIMAL CELL; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE ACTIVATION; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; MOLECULAR DYNAMICS; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; PURIFICATION; T LYMPHOCYTE; TH1 CELL; UPREGULATION;

ANIMALS; ANTIGEN-PRESENTING CELLS; CD40 LIGAND; CELLS, CULTURED; CYCLOSPORINE; CYTOPLASMIC GRANULES; DRUG RESISTANCE; EPITOPES, T-LYMPHOCYTE; INTRACELLULAR FLUID; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, NUDE; MICE, TRANSGENIC; RAB GTP-BINDING PROTEINS; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 79960537726     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1004083     Document Type: Article

References (64)

1. Parker, D. C. 1993. T cell-dependent B cell activation. Annu. Rev. Immunol. 11: 331-360.
2. van Kooten, C., and J. Banchereau. 2000. CD40-CD40 ligand. J. Leukoc. Biol. 67: 2-17.
3. McHeyzer-Williams, L. J., and M. G. McHeyzer-Williams. 2005. Antigen-specific memory B cell development. Annu. Rev. Immunol. 23: 487-513.
4. Williams, M. A., and M. J. Bevan. 2007. Effector and memory CTL differentiation. Annu. Rev. Immunol. 25: 171-192.
5. Murphy, K. M., P. Travers, and M. Walport. 2008. Janeway's Immunobiology. Garland Science/ Taylor & Francis Group, New York.
6. + memory T cells contains preformed CD40 ligand that is rapidly but transiently expressed on their surface after activation through the T cell receptor complex. J. Exp. Med. 181: 1293-1301.
7. + T cells and is quickly expressed on the cell surface in an antigen-specific manner. Blood 110: 2520-2527.
8. Okada, T., M. J. Miller, I. Parker, M. F. Krummel, M. Neighbors, S. B. Hartley, A. O'Garra, M. D. Cahalan, and J. G. Cyster. 2005. Antigen-engaged B cells undergo chemotaxis toward the T zone and form motile conjugates with helper T cells. PLoS Biol. 3: e150.
9. Allen, C. D., T. Okada, H. L. Tang, and J. G. Cyster. 2007. Imaging of germinal center selection events during affinity maturation. Science 315: 528-531.
10. Qi, 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.
11. Matheu, M. P., C. Beeton, A. Garcia, V. Chi, S. Rangaraju, O. Safrina, K. Monaghan, M. I. Uemura, D. Li, S. Pal, et al. 2008. Imaging of effector memory T cells during a delayed-type hypersensitivity reaction and suppression by Kv1.3 channel block. Immunity 29: 602-614.
12. Cannons, J. L., H. Qi, K. T. Lu, M. Dutta, J. Gomez-Rodriguez, J. Cheng, E. K. Wakeland, R. N. Germain, and P. L. Schwartzberg. 2010. Optimal germinal center responses require a multistage T cell:B cell adhesion process involving integrins, SLAM-associated protein, and CD84. Immunity 32: 253-265.
13. Blott, E. J., and G. M. Griffiths. 2002. Secretory lysosomes. Nat. Rev. Mol. Cell Biol. 3: 122-131.
14. Stinchcombe, J. C., G. Bossi, S. Booth, and G. M. Griffiths. 2001. The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity 15: 751-761.
15. Jenkins, M. R., and G. M. Griffiths. 2010. The synapse and cytolytic machinery of cytotoxic T cells. Curr. Opin. Immunol. 22: 308-313.
16. Thauland, T. J., and D. C. Parker. 2010. Diversity in immunological synapse structure. Immunology 131: 466-472.
17. Yellin, M. J., K. Sippel, G. Inghirami, L. R. Covey, J. J. Lee, J. Sinning, E. A. Clark, L. Chess, and S. Lederman. 1994. CD40 molecules induce down-modulation and endocytosis of T cell surface T cell-B cell activating molecule/CD40-L: potential role in regulating helper effector function. J. Immunol. 152: 598-608. (Pubitemid 24072963)
18. Stinchcombe, J. C., D. C. Barral, E. H. Mules, S. Booth, A. N. Hume, L. M. Machesky, M. C. Seabra, and G. M. Griffiths. 2001. Rab27a is required for regulated secretion in cytotoxic T lymphocytes. J. Cell Biol. 152: 825-834.
19. Oxenius, A., M. F. Bachmann, R. M. Zinkernagel, and H. Hengartner. 1998. Virus-specific MHC-class II-restricted TCR-transgenic mice: effects on humoral and cellular immune responses after viral infection. Eur. J. Immunol. 28: 390-400.
20. Sokol, C. L., G. M. Barton, A. G. Farr, and R. Medzhitov. 2008. A mechanism for the initiation of allergen-induced T helper type 2 responses. Nat. Immunol. 9: 310-318.
21. + T cells to effector cells. Eur. J. Immunol. 36: 1093-1103.
22. Son, Y. I., S. Egawa, T. Tatsumi, R. E. Redlinger, Jr., P. Kalinski, and T. Kanto. 2002. A novel bulk-culture method for generating mature dendritic cells from mouse bone marrow cells. J. Immunol. Methods 262: 145-157. (Pubitemid 34450739)
23. Fuleihan, R., N. Ramesh, A. Horner, D. Ahern, P. J. Belshaw, D. G. Alberg, I. Stamenkovic, W. Harmon, and R. S. Geha. 1994. Cyclosporin A inhibits CD40 ligand expression in T lymphocytes. J. Clin. Invest. 93: 1315-1320.
24. Kawakami, K., and D. C. Parker. 1993. Antigen and helper T lymphocytes activate B lymphocytes by distinct signaling pathways. Eur. J. Immunol. 23: 77-84.
25. + T helper cell effector functions. Blood 115: 2989-2997.
26. Borst, J., J. Hendriks, and Y. Xiao. 2005. CD27 and CD70 in T cell and B cell activation. Curr. Opin. Immunol. 17: 275-281.
27. + T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281: 65-78.
28. Van den Eertwegh, A. J., R. J. Noelle, M. Roy, D. M. Shepherd, A. Aruffo, J. A. Ledbetter, W. J. Boersma, and E. Claassen. 1993. In vivo CD40-gp39 interactions are essential for thymus-dependent humoral immunity, I: In vivo expression of CD40 ligand, cytokines, and antibody production delineates sites of cognate T-B cell interactions. J. Exp. Med. 178: 1555-1565.
29. Han, S., K. Hathcock, B. Zheng, T. B. Kepler, R. Hodes, and G. Kelsoe. 1995. Cellular interaction in germinal centers: roles of CD40 ligand and B7-2 in established germinal centers. J. Immunol. 155: 556-567.
30. Takahashi, Y., P. R. Dutta, D. M. Cerasoli, and G. Kelsoe. 1998. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl, V: Affinity maturation develops in two stages of clonal selection. J. Exp. Med. 187: 885-895.
31. Paus, D., T. G. Phan, T. D. Chan, S. Gardam, A. Basten, and R. Brink. 2006. Antigen recognition strength regulates the choice between extrafollicular plasma cell and germinal center B cell differentiation. J. Exp. Med. 203: 1081-1091.
32. O'Connor, B. P., L. A. Vogel, W. Zhang, W. Loo, D. Shnider, E. F. Lind, M. Ratliff, R. J. Noelle, and L. D. Erickson. 2006. Imprinting the fate of antigen-reactive B cells through the affinity of the B cell receptor. J. Immunol. 177: 7723-7732.
33. Chan, T. D., D. Gatto, K. Wood, T. Camidge, A. Basten, and R. Brink. 2009. Antigen affinity controls rapid T-dependent antibody production by driving the expansion rather than the differentiation or extrafollicular migration of early plasmablasts. J. Immunol. 183: 3139-3149.
34. Harwood, N. E., and F. D. Batista. 2008. New insights into the early molecular events underlying B cell activation. Immunity 28: 609-619.
35. Cyster, J. G. 2010. Shining a light on germinal center B cells. Cell 143: 503-505.
36. Depoil, D., R. Zaru, M. Guiraud, A. Chauveau, J. Harriague, G. Bismuth, C. Utzny, S. Müller, and S. Valitutti. 2005. Immunological synapses are versatile structures enabling selective T cell polarization. Immunity 22: 185-194. (Pubitemid 40255710)
37. Allen, C. D., T. Okada, and J. G. Cyster. 2007. Germinal-center organization and cellular dynamics. Immunity 27: 190-202.
38. Reinhardt, R. L., H. E. Liang, and R. M. Locksley. 2009. Cytokine-secreting follicular T cells shape the antibody repertoire. Nat. Immunol. 10: 385-393.
39. Ozaki, K., R. Spolski, R. Ettinger, H. P. Kim, G. Wang, C. F. Qi, P. Hwu, D. J. Shaffer, S. Akilesh, D. C. Roopenian, et al. 2004. Regulation of B cell differentiation and plasma cell generation by IL-21, a novel inducer of Blimp-1 and Bcl-6. J. Immunol. 173: 5361-5371. (Pubitemid 39392119)
40. Linterman, M. A., L. Beaton, D. Yu, R. R. Ramiscal, M. Srivastava, J. J. Hogan, N. K. Verma, M. J. Smyth, R. J. Rigby, and C. G. Vinuesa. 2010. IL-21 acts directly on B cells to regulate Bcl-6 expression and germinal center responses. J. Exp. Med. 207: 353-363.
41. Zotos, D., J. M. Coquet, Y. Zhang, A. Light, K. D'Costa, A. Kallies, L. M. Corcoran, D. I. Godfrey, K. M. Toellner, M. J. Smyth, et al. 2010. IL-21 regulates germinal center B cell differentiation and proliferation through a B cell-intrinsic mechanism. J. Exp. Med. 207: 365-378.
42. Calame, K. L., K. I. Lin, and C. Tunyaplin. 2003. Regulatory mechanisms that determine the development and function of plasma cells. Annu. Rev. Immunol. 21: 205-230.
43. Saito, M., J. Gao, K. Basso, Y. Kitagawa, P. M. Smith, G. Bhagat, A. Pernis, L. Pasqualucci, and R. Dalla-Favera. 2007. A signaling pathway mediating downregulation of BCL6 in germinal center B cells is blocked by BCL6 gene alterations in B cell lymphoma. Cancer Cell 12: 280-292. (Pubitemid 47333420)
44. 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.
45. Erickson, L. D., B. G. Durell, L. A. Vogel, B. P. O'Connor, M. Cascalho, T. Yasui, H. Kikutani, and R. J. Noelle. 2002. Short-circuiting long-lived humoral immunity by the heightened engagement of CD40. J. Clin. Invest. 109: 613-620.
46. Bolduc, A., E. Long, D. Stapler, M. Cascalho, T. Tsubata, P. A. Koni, and M. Shimoda. 2010. Constitutive CD40L expression on B cells prematurely terminates germinal center response and leads to augmented plasma cell production in T cell areas. J. Immunol. 185: 220-230.
47. Kishi, Y., Y. Aiba, T. Higuchi, K. Furukawa, T. Tokuhisa, T. Takemori, and T. Tsubata. 2010. Augmented antibody response with premature germinal center regression in CD40L transgenic mice. J. Immunol. 185: 211-219.
48. Polo, J. M., W. Ci, J. D. Licht, and A. Melnick. 2008. Reversible disruption of BCL6 repression complexes by CD40 signaling in normal and malignant B cells. Blood 112: 644-651.
49. Ci, W., J. M. Polo, and A. Melnick. 2008. B-cell lymphoma 6 and the molecular pathogenesis of diffuse large B-cell lymphoma. Curr. Opin. Hematol. 15: 381-390.
50. He, J. S., D. E. Gong, and H. L. Ostergaard. 2010. Stored Fas ligand, a mediator of rapid CTL-mediated killing, has a lower threshold for response than degranulation or newly synthesized Fas ligand. J. Immunol. 184: 555-563.
51. Damdinsuren, B., Y. Zhang, A. Khalil, W. H. Wood, III, K. G. Becker, M. J. Shlomchik, and R. Sen. 2010. Single round of antigen receptor signaling programs naive B cells to receive T cell help. Immunity 32: 355-366.
52. MacDonald, K. P., Y. Nishioka, P. E. Lipsky, and R. Thomas. 1997. Functional CD40 ligand is expressed by T cells in rheumatoid arthritis. J. Clin. Invest. 100: 2404-2414.
53. Yi, Y., M. McNerney, and S. K. Datta. 2000. Regulatory defects in Cbl and mitogen-activated protein kinase (extracellular signal-related kinase) pathways cause persistent hyperexpression of CD40 ligand in human lupus T cells. J. Immunol. 165: 6627-6634.
54. Katsiari, C. G., S. N. Liossis, A. M. Dimopoulos, D. V. Charalambopoulo, M. Mavrikakis, and P. P. Sfikakis. 2002. CD40L overexpression on T cells and monocytes from patients with systemic lupus erythematosus is resistant to calcineurin inhibition. Lupus 11: 370-378.
55. Mathur, R. K., A. Awasthi, P. Wadhone, B. Ramanamurthy, and B. Saha. 2004. Reciprocal CD40 signals through p38MAPK and ERK-1/2 induce counteracting immune responses. Nat. Med. 10: 540-544.
56. Guarda, G., C. Dostert, F. Staehli, K. Cabalzar, R. Castillo, A. Tardivel, P. Schneider, and J. Tschopp. 2009. T cells dampen innate immune responses through inhibition of NLRP1 and NLRP3 inflammasomes. Nature 460: 269-273.
57. Kornbluth, R. S. 2007. An adaptive route to innate immunity? Blood 110: 2221-2222.
58. + T cells. Cell Immunol. 257: 69-79.
59. Bossi, G., and G. M. Griffiths. 1999. Degranulation plays an essential part in regulating cell surface expression of Fas ligand in T cells and natural killer cells. Nat. Med. 5: 90-96.
60. He, J. S., and H. L. Ostergaard. 2007. CTLs contain and use intracellular stores of FasL distinct from cytolytic granules. J. Immunol. 179: 2339-2348.
61. Keller, A. M., T. A. Groothuis, E. A. Veraar, M. Marsman, L. Maillette de Buy Wenniger, H. Janssen, J. Neefjes, and J. Borst. 2007. Costimulatory ligand CD70 is delivered to the immunological synapse by shared intracellular trafficking with MHC class II molecules. Proc. Natl. Acad. Sci. USA 104: 5989-5994.
62. Johnson, S., Y. Zhan, R. M. Sutherland, A. M. Mount, S. Bedoui, J. L. Brady, E. M. Carrington, L. E. Brown, G. T. Belz, W. R. Heath, and A. M. Lew. 2009. Selected Toll-like receptor ligands and viruses promote helper-independent cytotoxic T cell priming by upregulating CD40L on dendritic cells. Immunity 30: 218-227.
63. Henn, V., J. R. Slupsky, M. Gräfe, I. Anagnostopoulos, R. Förster, G. Müller-Berghaus, and R. A. Kroczek. 1998. CD40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells. Nature 391: 591-594.
64. Otterdal, K., C. Smith, E. Oie, T. M. Pedersen, A. Yndestad, E. Stang, K. Endresen, N. O. Solum, P. Aukrust, and J. K. Damås. 2006. Platelet-derived LIGHT induces inflammatory responses in endothelial cells and monocytes. Blood 108: 928-935.