Regulatory T cells can prevent memory CD8 + T-cell-mediated rejection following polymorphonuclear cell depletion

European Journal of Immunology

Volumn 40, Issue 11, 2010, Pages 3107-3116

  Jones, Nick D ^a   Brook, Matthew O ^a   Carvalho Gaspar, Manuela ^a   Luo, Shiqao ^a   Wood, Kathryn J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Memory; Mouse; Tolerance; Transplantation; Treg

Indexed keywords

ALLOANTIGEN; CXCL1 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCLONAL ANTIBODY; PERFORIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD3+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CYTOKINE PRODUCTION; FLOW CYTOMETRY; GRAFT REJECTION; IMMUNOHISTOCHEMISTRY; IMMUNOSUPPRESSIVE TREATMENT; LYMPHOCYTIC INFILTRATION; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; SKIN ALLOGRAFT; T CELL DEPLETION; ALLOTRANSPLANTATION; ANIMAL; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LEUKAPHERESIS; MOUSE MUTANT; NEUTROPHIL; PATHOLOGY; SKIN TRANSPLANTATION;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; GRAFT REJECTION; IMMUNOLOGIC MEMORY; LEUKOCYTE REDUCTION PROCEDURES; MICE; MICE, KNOCKOUT; NEUTROPHILS; SKIN TRANSPLANTATION; T-LYMPHOCYTES, REGULATORY; TRANSPLANTATION, HOMOLOGOUS;

EID: 79952108804     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201040671     Document Type: Article

References (44)

1. Azzawi, M., Hasleton, P. S., Geraghty, P. J., Yonan, N., Krysiak, P., El-Gammal, A., Deiraniya, A. K. and Hutchinson, I. V., RANTES chemokine expression is related to acute cardiac cellular rejection and infiltration by CD45RO T-lymphocytes and macrophages. J. Heart Lung Transplant. 1998. 17: 881-887.
2. Ibrahim, S., Dawson, D. V., Van Trigt, P. and Sanfilippo, F., Differential infiltration by CD45RO and CD45RA subsets of T cells associated with human heart allograft rejection. Am. J. Pathol. 1993. 142: 1794-1803.
3. Ibrahim, S., Dawson, D. V. and Sanfilippo, F., Predominant infiltration of rejecting human renal allografts with T cells expressing CD8 and CD45RO. Transplantation 1995. 59: 724-728.
4. Dollinger, M. M., Howie, S. E., Plevris, J. N., Graham, A. M., Hayes, P. C. and Harrison, D. J., Intrahepatic proliferation of 'naïve' and 'memory' T cells during liver allograft rejection: primary immune response within the allograft. FASEB J. 1998. 12: 939-947.
5. Reinke, P., Fietze, E., Docke, W. D., Kern, F., Ewert, R. and Volk, H. D., Late acute rejection in long-term renal allograft recipients. Diagnostic and predictive value of circulating activated T cells. Transplantation 1994. 58: 35-41.
6. Heeger, P. S., Greenspan, N. S., Kuhlenschmidt, S., Dejelo, C., Hricik, D. E., Schulak, J. A. and Tary-Lehmann, M., Pretransplant frequency of donor-specific, IFN-gamma-producing lymphocytes is a manifestation of immunologic memory and correlates with the risk of posttransplant rejection episodes. J. Immunol. 1999. 163: 2267-2275.
7. Trzonkowski, P., Zilvetti, M., Friend, P. and Wood, K. J., Recipient memory-like lymphocytes remain unresponsive to graft antigens after CAMPATH-1H induction with reduced maintenance immunosuppression. Transplantation 2006. 82: 1342-1351.
8. Pearl, J. P., Parris, J., Hale, D. A., Hoffmann, S. C., Bernstein, W. B., McCoy, K. L., Swanson, S. J. et al., Immunocompetent T-cells with a memory-like phenotype are the dominant cell type following antibody-mediated T-cell depletion. Am. J. Transplant. 2005. 5: 465-474.
9. Yang, J., Brook, M. O., Carvalho-Gaspar, M., Zhang, J., Ramon, H. E., Sayegh, M. H., Wood, K. J. et al., Allograft rejection mediated by memory T cells is resistant to regulation. Proc. Natl. Acad. Sci. USA 2007. 104: 19954-19959.
10. Wu, Z., Bensinger, S. J., Zhang, J., Chen, C., Yuan, X., Huang, X., Markmann, J. F. et al., Homeostatic proliferation is a barrier to transplantation tolerance. Nat. Med. 2004. 10: 87-92.
11. Zhai, Y., Meng, L., Gao, F., Busuttil, R. W. and Kupiec-Weglinski, J. W., Allograft rejection by primed/memory CD8+ T cells is CD154 blockade resistant: therapeutic implications for sensitized transplant recipients. J. Immunol. 2002. 169: 4667-4673.
12. Valujskikh, A., Pantenburg, B. and Heeger, P. S., Primed allospecific T cells prevent the effects of costimulatory blockade on prolonged cardiac allograft survival in mice. Am. J. Transplant. 2002. 2: 501-509.
13. Adams, A. B., Williams, M. A., Jones, T. R., Shirasugi, N., Durham, M. M., Kaech, S. M., Wherry, E. J. et al., Heterologous immunity provides a potent barrier to transplantation tolerance. J. Clin. Invest. 2003. 111: 1887-1895.
14. Jones, N. D., Carvalho-Gaspar, M., Luo, S., Brook, M. O., Martin, L. and Wood, K. J., Effector and memory CD8+ T cells can be generated in response to alloantigen independently of CD4+ T cell help. J. Immunol. 2006. 176: 2316-2323.
15. Tang, A. L., Bingaman, A. W., Kadavil, E. A., Leeser, D. B. and Farber, D. L., Generation and functional capacity of polyclonal alloantigen-specific memory CD4 T cells. Am. J. Transplant. 2006. 6: 1275-1284.
16. Kingsley, C. I., Karim, M., Bushell, A. R. and Wood, K. J., CD25+CD4+ regulatory T cells prevent graft rejection: CTLA-4 and IL-10-dependent immunoregulation of alloresponses. J. Immunol. 2002. 168: 1080-1086.
17. Carvalho-Gaspar, M., Jones, N. D., Luo, S., Martin, L., Brook, M. O. and Wood, K. J., Location and time-dependent control of rejection by regulatory T cells culminates in a failure to generate memory T cells. J. Immunol. 2008. 180: 6640-6648.
18. Adams, A. B., Pearson, T. C. and Larsen, C. P., Heterologous immunity: an overlooked barrier to tolerance. Immunol. Rev. 2003. 196: 147-160.
19. Sachs, D. H., Tolerance: of mice and men. J. Clin. Invest. 2003. 111: 1819-1821.
20. Tanchot, C., Lemonnier, F. A., Perarnau, B., Freitas, A. A. and Rocha, B., Differential requirements for survival and proliferation of CD8 naive or memory T cells. Science 1997. 276: 2057-2062.
21. + T cells following immunization. Eur. J. Immunol. 1995. 25: 1755-1759.
22. Rogers, P. R., Dubey, C. and Swain, S. L., Qualitative changes accompany memory T cell generation: faster, more effective responses at lower doses of antigen. J. Immunol. 2000. 164: 2338-2346.
23. Croft, M., Bradley, L. M. and Swain, S. L., Naive versus memory CD4 T cell response to antigen. Memory cells are less dependent on accessory cell costimulation and can respond to many antigen-presenting cell types including resting B cells. J. Immunol. 1994. 152: 2675-2685.
24. Kambayashi, T., Assarsson, E., Lukacher, A. E., Ljunggren, H. G. and Jensen, P. E., Memory CD8+ T cells provide an early source of IFN-gamma. J. Immunol. 2003. 170: 2399-2408.
25. Barber, D. L., Wherry, E. J. and Ahmed, R., Cutting edge: rapid in vivo killing by memory CD8 T cells. J. Immunol. 2003. 171: 27-31.
26. Zhang, Q. W., Kish, D. D. and Fairchild, R. L., Absence of allograft ICAM-1 attenuates alloantigen-specific T cell priming, but not primed T cell trafficking into the graft, to mediate acute rejection. J. Immunol. 2003. 170: 5530-5537.
27. + T cells to antigen stimulation in vivo. Nat. Immunol. 2000. 1: 47-53.
28. Sallusto, F., Lenig, D., Forster, R., Lipp, M. and Lanzavecchia, A., Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999. 401: 708-712.
29. Sallusto, F., Kremmer, E., Palermo, B., Hoy, A., Ponath, P., Qin, S., Forster, R. et al., Switch in chemokine receptor expression upon TCR stimulation reveals novel homing potential for recently activated T cells. Eur. J. Immunol. 1999. 29: 2037-2045.
30. Fitzhugh, D. J., Naik, S., Wright Caughman, S. and Hwang, S. T., C-C chemokine receptor 6 is essential for arrest of a subset of memory T cells on activated dermal microvascular endothelial cells under physiologic flow conditions in vitro. J. Immunol. 2000. 165: 6677-6681.
31. Schenk, A. D., Nozaki, T., Rabant, M., Valujskikh, A. and Fairchild, R. L., Donor-reactive CD8 memory T cells infiltrate cardiac allografts within 24-h posttransplant in naive recipients. Am. J. Transplant. 2008. 8: 1652-1661.
32. Engeman, T., Gorbachev, A. V., Kish, D. D. and Fairchild, R. L., The intensity of neutrophil infiltration controls the number of antigen-primed CD8 T cells recruited into cutaneous antigen challenge sites. J. Leukoc. Biol. 2004. 76: 941-949.
33. Waaga, A.-M., Gasser, M., Kist-van Holthe, J. E., Najafian, N., Muller, A., Vella, J. P., Womer, K. L. et al., Regulatory functions of self-restricted MHC class II allopeptide-specific Th2 clones in vivo. J. Clin. Invest. 2001. 107: 909-916.
34. Schenk, S., Kish, D. D., He, C., El-Sawy, T., Chiffoleau, E., Chen, C., Wu, Z. et al., Alloreactive T cell responses and acute rejection of single class II MHC-disparate heart allografts are under strict regulation by CD4+CD25+ T cells. J. Immunol. 2005. 174: 3741-3748.
35. Belperio, J. A., Keane, M. P., Burdick, M. D., Gomperts, B. N., Xue, Y. Y., Hong, K., Mestas, J. et al., CXCR2/CXCR2 ligand biology during lung transplant ischemia-reperfusion injury. J. Immunol. 2005. 175: 6931-6939.
36. Mehrad, B., Strieter, R. M., Moore, T. A., Tsai, W. C., Lira, S. A. and Standiford, T. J., CXC chemokine receptor-2 ligands are necessary components of neutrophil-mediated host defense in invasive pulmonary aspergillosis. J. Immunol. 1999. 163: 6086-6094.
37. Chou, A.-H., Tsai, H.-F., Lin, L.-L., Hsieh, S.-L., Hsu, P.-I. and Hsu, P.-N., Enhanced proliferation and increased IFN-production in T cells by signal transduced through TNF-related apoptosis-inducing ligand. J. Immunol. 2001. 167: 1347-1352.
38. Li, L., Huang, L., Vergis, A. L., Ye, H., Bajwa, A., Narayan, V., Strieter, R. M. et al., IL-17 produced by neutrophils regulates IFN-gamma-mediated neutrophil migration in mouse kidney ischemia-reperfusion injury. J. Clin. Invest. 120: 331-342.
39. El-Sawy, T., Belperio, J. A., Strieter, R. M., Remick, D. G. and Fairchild, R. L., Inhibition of polymorphonuclear leukocyte-mediated graft damage synergizes with short-term costimulatory blockade to prevent cardiac allograft rejection. Circulation 2005. 112: 320-331.
40. Lin, C. Y., Graca, L., Cobbold, S. P. and Waldmann, H., Dominant transplantation tolerance impairs CD8+ T cell function but not expansion. Nat. Immunol. 2002. 3: 1208-1213.
41. Sponaas, A. M., Tomlinson, P. D., Antoniou, J., Auphan, N., Langlet, C., Malissen, B., Schmitt-Verhulst, A. M. and Mellor, A. L., Induction of tolerance to self MHC class I molecules expressed under the control of milk protein or B-globin gene promoters. Int. Immunol. 1994. 6: 277-287.
42. Hua, C., Boyer, C., Guimezanes, A., Albert, F. and Schmitt-Verhulst, A.-M., Analysis of T cell activation requirements with the use of alloantigens or an anti-clonotypic monoclonal antibody. J. Immunol. 1986. 136: 1927-1936.
43. Carvalho-Gaspar, M., Billing, J. S., Spriewald, B. M. and Wood, K. J., Chemokine gene expression during allograft rejection: Comparison of two quantitative PCR techniques. J. Immunol. Methods 2005. 301: 41-52.
44. Livak, K. J. and Schmittgen, T. D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001. 25: 402-408.