LFA-1 antagonism inhibits early infiltration of endogenous memory CD8 T cells into cardiac allografts and donor-reactive T cell priming

American Journal of Transplantation

Volumn 11, Issue 5, 2011, Pages 923-935

  Setoguchi, K ^a,b   Schenk, A D ^a,c   Ishii, D ^a   Hattori, Y ^a   Baldwin III, W M ^a,c   Tanabe, K ^b   Fairchild, R L ^a,c  

^a LERNER RESEARCH INSTITUTE   (United States)

^b TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

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

Author keywords

acute allograft rejection; Acute cellular rejection; adhesion molecules; alloreactive T cells; leukocyte infiltration; memory CD8+ T cells

Indexed keywords

ANTIBODY; CXCL1 CHEMOKINE; CXCL9 CHEMOKINE; CYTOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INDUCIBLE COSTIMULATOR MOLECULE; INTERLEUKIN 1BETA; INTERLEUKIN 6; LYMPHOCYTE ANTIBODY; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1 ANTIBODY; MONOCLONAL ANTIBODY; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DONOR REACTIVE T CELL PRIMING; DRUG EFFICACY; GENE EXPRESSION; GRAFT RECIPIENT; GRAFT SURVIVAL; HEART TRANSPLANTATION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC INFILTRATION; MALE; MEMORY T LYMPHOCYTE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; ORGAN DONOR; PRIORITY JOURNAL; SPLEEN;

ANIMALS; ANTIBODIES, MONOCLONAL; CD8-POSITIVE T-LYMPHOCYTES; FLOW CYTOMETRY; HEART TRANSPLANTATION; IMMUNOHISTOCHEMISTRY; IMMUNOLOGIC MEMORY; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MALE; MICE; MICE, INBRED C57BL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES; TRANSPLANTATION, HOMOLOGOUS;

EID: 79955544000     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2011.03492.x     Document Type: Article

References (62)

1. Lechler RI, Sykes M, Thomson AW, Turka LA,. Organ transplantation-how much of the promise has been realized Nat Med 2005; 11: 605-613. (Pubitemid 40868300)
2. El-Sawy T, Fahmy NM, Fairchild RL,. Chemokines: Directing leukocyte infitration into allografts. Curr Opin Immunol 2002; 14: 562-568.
3. Hancock WW,. Chemokine receptor-dependent alloresponses. Immunol Rev 2003; 196: 37-50. (Pubitemid 37468102)
4. Sayegh MH, Remuzzi G,. Clinical update: Immunosuppression minimization. Lancet 2007; 369: 1676-1678.
5. Amano H, Bickerstaff A, Orosz CG, Novick AC, Toma H, Fairchild RL,. Absence of recipient CCR5 promotes early and increased allospecific antibody responses to cardiac allografts. J Immunol 2005; 174: 6499-6508. (Pubitemid 40663845)
6. Kwun J, Hazinedaroglu SM, Schadde E, et al,. Unaltered graft survival and intragraft lymphocytes infiltration in the cardiac allograft of CxcR3-/- mouse recipients. Am J Transplant 2008; 8: 1593-1603.
7. Rosenblum JM, Zhang QW, Siu G, et al,. CXCR3 antagonism impairs the development of donor-reactive, IFN-gamma-producing effectors and prolongs allograft survival. Transplantation 2009; 87: 360-369.
8. Zerwes H-G, Li, Kovarik J, et al,. The chemokine receptor Cxcr3 is not essential for acute cardiac allograft rejection in mice and rats. Am J Transplant 2008; 8: 1604-1613.
9. Nicolls MR, Gill RG,. LFA-1 (CD11a) as a therapeutic target. Am J Transplant 2006; 6: 27-36. (Pubitemid 43382197)
10. Chou YK, Edwards DM, Weinberg AD, et al,. Activation pathways implicate anti-HLA-DP and anti-LFA-1 antibodies as lead candidates for intervention in chronic berylliosis. J Immunol 2005; 174: 4316-4324. (Pubitemid 40396014)
11. Freiberg BA, Kupfer H, Maslanik W, et al,. Staging and resetting T cell activation in SMACs. Nat Immunol 2002; 3: 911-917. (Pubitemid 35154003)
12. Gorochov G, Gross G, Waks T, Eshhar Z,. Anti-leukocyte function-associated antigen-1 antibodies inhibit T cell activation following low-avidity and adhesion-independent interactions. Immunology 1993; 79: 548-555. (Pubitemid 23246890)
13. Grakoui A, Bromley SK, Sumen C, et al,. The immunological synapse: A molecular machine controlling T cell activation. Science 2002; 285: 221-227.
14. Lee K-H, Holdorf AD, Dustin ML, Chan AC, Allen PM, Shaw AS,. T cell receptor signaling precedes immunological synapse formation. Science 2002; 295: 1539-1542. (Pubitemid 34174012)
15. Rutigliano JA, Johnson TR, Hollinger TN, Fischer JE, Aung S, Graham BS,. Treatment with anti-LFA-1 delays the CD8+ cytotoxic -T-lymphocyte response and viral clearance in mice with primary respiratory syncytial virus infection. J Virol 2004; 78: 3014-3023. (Pubitemid 38314359)
16. Springer TA, Dustin ML, Kishimoto TK, Marlin SD,. The lympyhocyte function-associated LFA-1, CD2, and LFA-3 molecules: Cell adhesion receptors of the immune system. Annu Rev Immunol 1987; 107: 223-252.
17. Isobe M, Yagita H, Okumura K, Ihara A,. Specific acceptance of cardiac allograft after treatment with antibodies to ICAM-1 and LFA-1. Science 1992; 255: 1125-1129.
18. Lunsford KE, Koester MA, Eiring AM, Horne PH, Gao D, Bumgartner GL,. Targeting LFA-1 and CD154 suppresses the in vivo activation and development of cytolytic (CD4-independent) CD8+ T cells. J Immunol 2005; 175: 7855-7866. (Pubitemid 41798346)
19. Metzler B, Gfeller P, Bigaud M, et al,. Combinations of anti-LFA-1, everolimus, anti-CD40 ligand, and allogeneic bone marrow induce central transplantation tolerance through hemopoietic chimerism, including protection from chronic heart allograft rejection. J Immunol 2004; 173: 7025-7036. (Pubitemid 39541092)
20. Murakawa T, Kerklo MM, Zamora MR, et al,. Simultaneous LFA-1 and CD40 ligand antagonism prevents airway remodeling in orthotopic airway transplantation: Implications for the role of respiratory epithelium as a modulator of fibrosis. J Immunol 2005; 174: 3869-3879. (Pubitemid 40395959)
21. Nicolls MR, Coulombe M, Beilke J, Gelhaus HC, Gill RG,. CD4-dependent generation of dominant transplantation tolerance induced by simultaneous perturbation of CD154 and LFA-1 pathways. J Immunol 2002; 169: 4831-4839. (Pubitemid 35217146)
22. NIcolls MR, Coulombe M, Yang H, Bolwerk A, Gill RG,. Anti-LFA-1 therapy induces long-term islet allograft acceptance in the absence of IFN-γ or IL-4. J Immunol 2000; 164: 3627-3634. (Pubitemid 30169816)
23. Page AJ, Ford ML, Kirk AD,. Memory T cell-specific therapeutics in organ transplantation. Curr Opin Organ Transplant 2009; 14: 643-649.
24. Valujskikh A,. Targeting T cell memory: Where do we stand Curr Opin Organ Transplant 2008; 13: 344-349.
25. Adams AB, Pearson TC, Larsen CP,. Heterologous immunity: An overlooked barrier to tolerance. Immunol Rev 2003; 196: 147-160. (Pubitemid 37468109)
26. Brehm MA, Markees TG, Daniels KA, Greiner DL, Rossini AA, Welsh RM,. Direct visualization of cross-reactive effector and memory allo-specific CD8 T cells generated in response to viral infections. J Immunol 2003; 170: 4077-4086. (Pubitemid 36428170)
27. Selin LK, Brehm MA, Naumov YN, et al,. Memory of mice and men: CD8+ T cell cross-reactivity and heterlogous immunity. Immunol Rev 2006; 211: 164-181. (Pubitemid 43882970)
28. 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)
29. Heeger PS, Greenspan NS, Kuhlenschmidt S, et al,. Pretransplant frequency of donor-specific, IFN-gamma-producing lymphcytes is a manifestation of immunologic memory and correlates with the risk of post-transplant rejection episodes. J Immunol 1999; 163: 2267-2275. (Pubitemid 29382237)
30. 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)
31. Chen Y, Heeger PS, Valujskikh A,. In vivo helper functions of alloreactive memory CD4+ T cells remain intact despite donor-specific transfusion and anti-CD40 ligand therapy. J Immunol 2004; 172: 5456-5466. (Pubitemid 38542046)
32. Koyama I, Nadazdin O, Boskovic S, et al,. Depletion of CD8 memory T cells for induction of tolerance of a previously transplanted kidney allograft. Am J Transplant 2007; 7: 1055-1061. (Pubitemid 46643090)
33. 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)
34. Zhang Q, Chen Y, Fairchild RL, Heeger PS, Valujskikh A,. Lymphoid sequestration of alloreactive memory CD4 T cells promotes cardiac allograft survival. J Immunol 2006; 176: 770-777. (Pubitemid 43099673)
35. 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.
36. 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.
37. Louis S, Audrain M, Cantarovich D, et al,. Long-term cell monitoring of kidney recipients after an antilymphocyte globulin induction with and without steroids. Transplantation 2007; 83: 712-721. (Pubitemid 46569188)
38. Weaver TA, Charafeddine AH, Agarwal A, et al,. Alefacept promotes co-stimulation blockade based allograft survival in nonhuman primates. Nat Med 2009; 15: 746-749.
39. Fischer A, Durandy A, Sterkers G, Griscelli C,. Role of the LFA-1 molecule in cellular interactions required for antibody production in humans. J Immunol 1986; 136: 3198-3203. (Pubitemid 16113899)
40. Howard DR, Eaves AC, Takei F,. Lymphocyte function-associated antigen (LFA-1) is involved in B cell activation. J Immunol 1986; 136: 4013-4018. (Pubitemid 16123044)
41. Lee WT, Vitetta ES,. The differential expression of homing and adhesion molecules on virgin and memory T cells in the mouse. Cell Immunol 1991; 132: 215-222.
42. Moy VT, Brian AA,. Signaling by lymphocyte function-associated antigen 1 (LFA-1) in B cells: Enhanced antigen presentation after stimulation through LFA-1. J Exp Med 1992; 175: 1-7.
43. Sanders ME, Makgoba MW, Sharrow SO, et al,. Human memory T lymphocytes express increases levels of three cell adhsion molecules (LFA-3, CD2, and LFA-1) and three other molecules (UCHL1, CDw29, and Pgp-1) and have enhanced IFN-gamma production. J Immunol 1988; 140: 1401-1407.
44. Corry RJ, Winn HJ, Russell PS,. Primarily vascularized allografts of hearts in mice. Transplantation 1973; 16: 343-350.
45. Afanasyeva M, Georgakopoulos D, Belardi DF, et al,. Quantitative analysis of myocardial inflammation by flow cytometry in murine autoimmune myocarditis: Correlation with cardiac function. Am J Pathol 2004; 164: 807-815. (Pubitemid 38235463)
46. Murata K, Fox-Talbot K, Qian Z, et al,. Synergistic depostion of C4d by complement-activating and non-activating antibodies in cardiac transplants. Am J Transplant 2007; 7: 2605-2614. (Pubitemid 47561614)
47. El-Sawy T, Belperio JA, Strieter RM, Remick DG, Fairchild RL,. Inhibition of polymorphonuclear leukocyte-mediated graft damage synergizes with short-term costimulatory blockade to prevent cardiac allograft rejection. Circulation 2005; 112: 320-331. (Pubitemid 41022072)
48. El-Sawy T, Miura M, Fairchild R,. Early T cell response to allografts occurring prior to alloantigen priming up-regulates innate mediated inflammation and graft necrosis. Am J Pathol 2004; 165: 147-157. (Pubitemid 38821822)
49. Nozaki T, Amano H, Bickerstaff A, et al,. Antibody-mediated rejection of cardiac allografts in CCR5-deficient recipients. J Immunol 2007; 179: 5238-5245.
50. LaRosa DF, Rahman AH, Turka LA,. The innate immune system in allograft rejection and tolerance. J Immunol 2007; 178: 7503-7509. (Pubitemid 46898016)
51. Burrows SR, Khanna R, Burrows JM, Moss DJ,. An alloresponse in humans is dominated by cytotoxic T lymphocytes (CTL) cross-reactive with a single Epstein-Barr virus CTL epitope: Implications for graft-versus-host disease. J Exp Med 1994; 179: 1155-1161. (Pubitemid 24091774)
52. Morita K, Miura M, Paolone DR, et al,. Early chemokine cascades in murine cardiac grafts regulate T cell recruitment and progression of acute allograft rejection. J Immunol 2001; 167: 2979-2984. (Pubitemid 32768935)
53. Chang JT, Palanivel Vr, Kinjyo I, et al,. Asymmetric T lymphocyte division in the initiation of adaptive immune responses. Science 2007; 315: 1687-1691. (Pubitemid 46515618)
54. Mempel TR, Henrickson SE, von Andrian UH,. T cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 2004; 427: 154-159. (Pubitemid 38094955)
55. Sabatos CA, Doh J, Chakravarti S, et al,. A synaptic basis for paracrine interleukin-2 signaling during homotypic T cell interaction. Immunity 2008; 29: 238-248.
56. Stemberger C, Huster KM, Koffler M, et al,. A single naive CD8+ T cell precursor can develop into diverse effector and memory subsets. Immunity 2007; 27: 985-997. (Pubitemid 50014865)
57. Owens T,. A role for adhesion molecules in contact-dependent T help for B cells. Eur J Immunol 1991; 21: 979-983.
58. Rayat GR, Gill RG,. Indefinite survival of neonatal porcine islet xenografts by simultaneous targeting of LFA-1 and CD154 or CD45RB. Diabetes 2005; 54: 443-451.
59. Gottlieb AB, Hamilton T, Caro I, Kwon P, Compton PG, Leonardi CL,. Long-term continuous efalizumab therapy in patients with moderate to severe chronic plaque psoriasis: Updated results from an ongoing trial. J Am Acad Dermatol 2006; 54: S154-S163. (Pubitemid 43238298)
60. Lebwohl M, Tyring SK, Hamilton TK, et al,. A novel targeted T cell modulator, efalizumab, for plaque psoriasis. N Engl J Med 2003; 349: 2004-2013 (Pubitemid 37448923)
61. Posselt AM, Bellin MD, Tavakol M, et al,. Islet transplantation in type 1 diabetics using an immunosuppressive protocol based on the anti-LFA-1 antibody efalizumab. Am J Transplant 2010; 10: 1870-1880.
62. Vincenti F, Mendez R, Pescovitz M, et al,. A phase I/II randomized open-label multicenter trial of efalizumab, a humanized anti-CD11a, anti-LFA-1 in renal transplantation. Am J Transplant 2007; 7: 1770-1777. (Pubitemid 46905435)