IL-15 induces alloreactive CD28- Memory CD8 T cell proliferation and CTLA4-Ig resistant memory CD8 T cell activation

American Journal of Transplantation

Volumn 14, Issue 6, 2014, Pages 1277-1289

  Traitanon, O ^a,b   Gorbachev, A ^a   Bechtel, J J ^a   Keslar, K S ^a   Baldwin III, W M ^a,c   Poggio, E D ^a   Fairchild, R L ^a,c  

^a LERNER RESEARCH INSTITUTE   (United States)

^b THAMMASAT UNIVERSITY   (Thailand)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

belatacept; Costimulation; cytokines cytokine receptors; immunosuppressant; T cell biology

Indexed keywords

ABATACEPT; ALLOANTIGEN; CD28 ANTIGEN; CTLA 4IG; GAMMA INTERFERON; INTERLEUKIN 15; INTERLEUKIN 2; INTERLEUKIN 7; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4;

ADULT; AGED; ARTICLE; B LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; KIDNEY ALLOGRAFT; KIDNEY GRAFT; KIDNEY GRAFT REJECTION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE SUBPOPULATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MEMORY T LYMPHOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; TISSUE INJURY; CYTOLOGY; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MIXED LYMPHOCYTE CULTURE; PHYSIOLOGY;

ANTIGENS, CD28; CD8-POSITIVE T-LYMPHOCYTES; CTLA-4 ANTIGEN; HUMANS; IMMUNOLOGIC MEMORY; INTERLEUKIN-15; LYMPHOCYTE ACTIVATION; LYMPHOCYTE CULTURE TEST, MIXED;

EID: 84901356055     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.12719     Document Type: Article

References (63)

1. Augustine JJ, Siu DS, Clemente MJ, Schulak JA, Heeger PS, Hricik DE., Pre-transplant IFN-gamma ELISPOTs are associated with post-transplant renal function in African American renal transplant recipients. Am J Transplant 2005; 5: 1971-1975. (Pubitemid 41039873)
2. Heeger PS, Greenspan NS, Kuhlenschmidt S, et al. Pretransplant frequency of donor-specific, IFN-gamma-producing lymphocytes is a manifestation of immunologic memory and correlates with the risk of post-transplant rejection episodes. J Immunol 1999; 163: 2267-2275. (Pubitemid 29382237)
3. Adams AB, Williams MR, Jones TR, et al. Heterologous immunity provides a potent barrier to transplantation tolerance. J Clin Invest 2003; 111: 1887-1895. (Pubitemid 38057733)
4. Ford ML, Kirk AD, Larsen CP., Donor-reactive T-cell stimulation history and precursor frequency: Barriers to tolerance induction. Transplantation 2009; 87: S69-S74.
5. Ford ML, Larsen CP., Overcoming the memory barrier in tolerance induction: Molecular mimicry and functional heterogeneity among pathogen-specific T-cell populations. Curr Opin Organ Transplant 2010; 15: 405-410.
6. Welsh RM, Markees TG, Woda BA, et al. Virus-induced abrogation of transplantation tolerance induced by donor-specific transfusion and anti-CD154 antibody. J Virol 2000; 74: 2210-2218. (Pubitemid 30091475)
7. - cells are induced by antigen and evolve through extensive rounds of division. Int Immunol 1999; 11: 1027-1033. (Pubitemid 29338743)
8. + T subsets with distinctive replicative history and partial effector functions. Blood 2003; 102: 1779-1787. (Pubitemid 37022574)
9. - compartment. Blood 2001; 98: 2817-2827.
10. + T cells contain greatly expanded functional virus-specific memory CTL clones. J Immunol 1999; 162: 7569-7577. (Pubitemid 29277739)
11. + T cell response. J Immunol 2002; 168: 5455-5464. (Pubitemid 34556123)
12. Boucher N, Dufeu-Duchesne T, Vicaut E, Farge D, Effros RB, Schachter F., CD28 expression in T cell aging and human longevity. Exp Gerontol 1998; 33: 267-282. (Pubitemid 28196407)
13. Czesnikiewicz-Guzik M, Lee WW, Cui D, et al. T cell subset-specific susceptibility to aging. Clin Immunol 2008; 127: 107-118.
14. + T-cell repertoire, which may be the basis for an imbalance in the cytokine production profile in elderly persons. J Virol 2005; 79: 3675-3683. (Pubitemid 40327955)
15. - T lymphocytes: Antigenic and functional properties. J Immunol 1993; 150: 1147-1159. (Pubitemid 23127405)
16. - lymphocytes during aging. Exp Gerontol 2004; 39: 539-544. (Pubitemid 38402080)
17. + T cell subset: Age-associated expansion and shift from memory to naive phenotype. J Immunol 1999; 162: 3327-3335. (Pubitemid 29313581)
18. Posnett DN, Sinha R, Kabak S, Russo C., Clonal populations of T cells in normal elderly humans: The T cell equivalent to "benign monoclonal gammapathy." J Exp Med 1994; 179: 609-618.
19. + T cells. Hum Immunol 2002; 63: 1000-1009. (Pubitemid 35231683)
20. - and IL-12/IL-15-mediated signaling. Mech Ageing Dev 2002; 123: 1389-1402. (Pubitemid 35247434)
21. - T cells in patients with chronic kidney graft rejection. Transplant Proc 2003; 35: 2902-2904. (Pubitemid 38102085)
22. Studer SM, George MP, Zhu X, et al. CD28 down-regulation on CD4 T cells is a marker for graft dysfunction in lung transplant recipients. Am J Respir Crit Care Med 2008; 178: 765-773.
23. + lymphocyte populations in long-term drug-free tolerance and chronic rejection in human kidney graft recipients. J Am Soc Nephrol 2006; 17: 294-304.
24. Durrbach A, Pestana JM, Pearson T, et al. A phase III study of Belatacept versus cyclosporine in kidney transplants from extended criteria donors (BENEFIT-EXT Study). Am J Transplant 2010; 10: 547-557.
25. Vincenti F, Charpentier B, Vanrenterghem Y, et al. A phase III study of belatacept-based immunosuppression regimens versus cyclosporine in renal transplant recipients (BENEFIT Study). Am J Transplant 2010; 10: 535-546.
26. Schenk AD, Gorbacheva V, Rabant M, Fairchild RL, Valujskikh A., Effector functions of donor-reactive CD8 memory T cells are dependent on ICOS induced during division in cardiac grafts. Am J Transplant 2009; 9: 64-73.
27. Schenk AD, Nozaki T, Rabant M, Valujskikh A, Fairchild RL., Donor-reactive CD8 memory T cells infiltrate cardiac allografts within 24-h posttransplant in naive recipients. Am J Transplant 2008; 8: 1652-1661.
28. Setoguchi K, Hattori Y, Iida S, Baldwin WM III, Fairchild RL., Endogenous memory CD8 T cells are activated within cardiac allografts without mediating rejection. Am J Transplant 2013; 13: 2293-2307.
29. Poggio ED, Clemente M, Hricik DE, Heeger PS., Panel of reactive T cells as a measurement of primed cellular alloimmunity in kidney transplant candidates. J Am Soc Nephrol 2006; 17: 564-572.
30. Livak KJ, Schmittgen TD., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001; 25: 402-408. (Pubitemid 34164012)
31. Surh CD, Sprent J., Homeostasis of naive and memory T cells. Immunity 2008; 29: 848-862.
32. + T cells in vivo by IL-15. Immunity 1998; 8: 591-599. (Pubitemid 28264750)
33. Aktas E, Kucuksezer UC, Bilgic S, Erten G, Deniz G., Relationship between CD107a expression and cytotoxic activity. Cell Immunol 2009; 254: 149-154.
34. + T cells by a flow cytometric assay for degranulation. J Immunol Methods 2003; 281: 65-78. (Pubitemid 37324571)
35. + memory T cells mediated by IL-15 and its induced cytokines. J Immunol 2006; 177: 7802-7810. (Pubitemid 44846296)
36. Budagian V, Bulanova E, Paus R, Bulfone-Paus S., IL-15/IL-15 receptor biology: A guided tour through an expanding universe. Cytokine Growth Factor Rev 2006; 17: 259-280. (Pubitemid 44038618)
37. Di Sabatino A, Calarota SA, Vidali F, Macdonald TT, Corazza GR., Role of IL-15 in immune-mediated and infectious diseases. Cytokine Growth Factor Rev 2011; 22: 19-33.
38. Li XC, Demirci G, Ferrari-Lacraz S, et al. IL-15 and IL-2: A matter of life and death for T cells in vivo. Nat Med 2001; 7: 114-118. (Pubitemid 32095650)
39. Ma A, Koka R, Burkett P., Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu Rev Immunol 2006; 24: 657-679.
40. + memory pool. J Clin Invest 2005; 115: 1177-1187. (Pubitemid 40629036)
41. Fehniger TA, Caligiuri MA., Interleukin-15: Biology and relevance to human disease. Blood 2001; 97: 14-32. (Pubitemid 32061238)
42. Bamford RN, Grant AJ, Burton JD, et al. The interleukin (IL) 2 receptor beta chin is shared by IL-2 and a cytokine, provisionally designated IL-T, that stimulates T-cell proliferation and the induction of lymphokine-activated killer cells. Proc Natl Acad Sci USA 1994; 91: 4940-4944.
43. Burton JD, Bamford RN, Peters C, et al. A lymphokine, provisionally designated interleukin T and produced by a human adult T-cell leukemia line, stimulates T-cell proliferation and the induction of lymphokine-activated killer cells. Proc Natl Acad Sci USA 1994; 91: 4935-4939. (Pubitemid 24177765)
44. Kawamura T, Koka R, Ma A, Kumar V., Differential roles for IL-15 alpha-chain in NK cell development and Ly-49 induction. J Immunol 2003; 171: 5085-5090. (Pubitemid 37432790)
45. Ku CC, Murakami M, Sakamoto A, Kappler J, Marrack P., Control of homeostasis of CD8+ memory T cells by opposing cytokines. Science 2000; 288: 675-678. (Pubitemid 30241571)
46. Ajjan RA, Watson PF, Weetman AP., Detection of IL-12, IL-13, and IL-15 messenger ribonucleic acid in the thyroid of patients with autoimmune thyroid disease. J Clin Endocrinol Metab 1997; 82: 666-669. (Pubitemid 27068648)
47. Bhorade SM, Yu A, Vigneswaran WT, Alex CG, Garrity ER., Elevation of interleukin-15 protein expression in bronchoalveolar fluid in acute lung allograft rejection. Chest 2007; 131: 533-538. (Pubitemid 46280416)
48. Manfro RC, Roy-Chaudhury P, Zheng XX, et al. Interleukin-15 gene transcripts are present in rejecting islet allografts. Transplant Proc 1997; 29: 1077-1078. (Pubitemid 27126097)
49. Pavlakis M, Strehlau J, Lipman M, Shapiro M, Maslinksi W, Strom TB., Intragraft IL-15 transcripts are increased in human renal allograft rejection. Transplantation 1996; 62: 543-545. (Pubitemid 26295833)
50. Reksten TR, Jonsson MV, Szyszko EA, Brun JG, Jonsson R, Brokstad KA., Cytokine and autoantibody profiling related to histopathological features in primary Sjogren's syndrome. Rheumatology 2009; 48: 1102-1106.
51. Robertson H, Kirby JA., Post-transplant renal tubulitis: The recruitment, differentiation, and persistence of intra-epithelial T cells. Am J Transplant 2003; 3: 3-10. (Pubitemid 36306816)
52. Wang WL, Yao MY, Jin J, et al. Increased expression of non-interleukin-2 T cell growth factors and their implications during liver allograft rejection in rats. J Gastroenterol Hepatol 2007; 22: 1141-1147. (Pubitemid 47019862)
53. Weiler M, Rogashev B, Einbinder T, et al. Interleukin-15, a leukocyte activator and growth factor, is produced by cortical tubular epithelial cells. J Am Soc Nephrol 1998; 9: 1194-1201. (Pubitemid 28283882)
54. Ferrari-Lacraz S, Zheng XX, Kim YS, et al. An antagonist IL-15/Fc protein prevents costimulation blockade-resistant rejection. J Immunol 2001; 167: 3478-3485. (Pubitemid 32852594)
55. + T cells resistant to costimulatory blockade are controlled by an antagonist interleukin-15/Fc protein. Transplantation 2006; 82: 1510-1517. (Pubitemid 44967635)
56. Koulmanda M, Qipo A, Fan Z, et al. Prolonged survival of allogeneic islets in cynomolgus monkeys after short-term triple therapy. Am J Transplant 2012; 12: 1296-1302.
57. - T cells in healthy ageing people, including centenarians. Immunology 1966; 88: 501-507.
58. Su CA, Iida S, Abe T, Fairchild RL., Endogenous memory CD8 T cells directly mediate cardiac allograft rejection. Am J Transplant 2014; 14: 568-579.
59. + T cells with innate-like capacity to lyse vascular endothelium in granulomatosis with polyangiitis (Wegener's). Arth Rheum 2011; 63: 2116-2126.
60. -) natural killer cell extravasation into human endometrium. Biol Reprod 2013; 89: 1-7.
61. Vincenti F, Larsen CP, Alberu J, et al. Three-year outcomes from BENEFIT, a randomized, active-controlled, parallel-group study in adult kidney transplant recipients. Am J Transplant 2012; 12: 210-217.
62. Bryl E, Vallejo AN, Weyand CM, Goronzy JJ., Down-regulation of CD28 expression by TNF-α. J Immunol 2001; 167: 3231-3238.
63. Lewis D, Merched-Sauvage EM, Goronzy JJ, Weyand CM, Vallejo AN., Tumor necrosis factor-α and CD80 modulate CD28 expression through a similar mechanism of T-cell receptor-independent inhibition of transcription. J Biol Chem 2004; 279: 29130-29138. (Pubitemid 38915785)