Reshaping the past: Strategies for modulating T-cell memory immune responses

Clinical Immunology

Volumn 122, Issue 1, 2007, Pages 1-12

  Ndejembi, Modesta P ^a   Tang, Anita L ^a   Farber, Donna L ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Alloimmunity; Autoimmunity; Immune memory; Immunosuppresssion; Regulation; T lymphocyte

Indexed keywords

ALEFACEPT; ALEMTUZUMAB; BASILIXIMAB; CD134 ANTIGEN; CD28 ANTIGEN; CD3 ANTIBODY; CD40 ANTIGEN; CD40 LIGAND; CD40 LIGAND MONOCLONAL ANTIBODY; CYCLOSPORIN A; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; DACLIZUMAB; FINGOLIMOD; INDUCIBLE COSTIMULATOR LIGAND; INTERLEUKIN 2; LIGAND; LYMPHOCYTE ANTIBODY; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY OX40; OKT 3; PEPTIDE DERIVATIVE; RAPAMYCIN; TACROLIMUS; THYMOCYTE ANTIBODY; UNCLASSIFIED DRUG;

ALLERGIC ENCEPHALOMYELITIS; AUTOIMMUNE DISEASE; CELL COMPARTMENTALIZATION; CELL HETEROGENEITY; CLINICAL TRIAL; DIABETES MELLITUS; DRUG MECHANISM; ENTERITIS; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; KIDNEY GRAFT REJECTION; KIDNEY TRANSPLANTATION; LOW DRUG DOSE; LYMPHOCYTE ACTIVATION; LYMPHOID TISSUE; MEMORY T LYMPHOCYTE; NONHUMAN; PRIORITY JOURNAL; PSORIASIS; SHORT SURVEY; T CELL DEPLETION; THROMBOEMBOLISM;

ANIMALS; HUMANS; IMMUNOLOGIC MEMORY; MODELS, IMMUNOLOGICAL; T-LYMPHOCYTES;

EID: 33845878796     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2006.06.012     Document Type: Short Survey

References (148)

1. 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. 164 (2000) 2338-2346
2. London C.A., Lodge M.P., and Abbas A.K. Functional responses and costimulator dependence of memory CD4+ T cells. J. Immunol. 164 (2000) 265-272
3. 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 APC types including resting B cells. J. Immunol. 152 (1994) 2675-2685
4. 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 401 (1999) 708-712
5. Bingaman A.W., Patke D.S., Mane V.R., Ahmadzadeh M., Ndejembi M., Bartlett S.T., and Farber D.L. Novel phenotypes and migratory properties distinguish memory CD4 T cell subsets in lymphoid and lung tissue. Eur. J. Immunol. 35 (2005) 3173-3186
6. Bingaman A.W., and Farber D.L. Memory T cells in transplantation: generation, function, and potential role in rejection. Am. J. Transp. 4 (2004) 846-852
7. Cho B.K., Rao V.P., Ge Q., Eisen H.N., and Chen J. Homeostasis-stimulated proliferation drives naive T cells to differentiate directly into memory T cells. J. Exp. Med. 192 (2000) 549-556
8. Murali-Krishna K., and Ahmed R. Cutting edge: naive T cells masquerading as memory cells. J. Immunol. 165 (2000) 1733-1737
9. Ge Q., Hu H., Eisen H.N., and Chen J. Different contributions of thymopoiesis and homeostasis-driven proliferation to the reconstitution of naive and memory T cell compartments. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 2989-2994
10. Tanchot C., Le Campion A., Leaument S., Dautigny N., and Lucas B. Naive CD4+ lymphocytes convert to anergic or memory-like cells in T cell-deprived recipients. Eur. J. Immunol. 31 (2001) 2256-2265
11. Wu Z., Bensinger S.J., Zhang J., Chen C., Yuan X., Huang X., Markmann J.F., Kassaee A., Rosengard B.R., Hancock W.W., Sayegh M.H., and Turka L.A. Homeostatic proliferation is a barrier to transplantation tolerance. Nat. Med. 10 (2004) 87-92
12. Hamilton S.E., Wolkers M.C., Schoenberger S.P., and Jameson S.C. The generation of protective memory-like CD8+ T cells during homeostatic proliferation requires CD4+ T cells. Nat. Immunol. 7 (2006) 475-481
13. Moulton V.R., and Farber D.L. Committed to memory: lineage choices for activated T cells. Trends Immunol. 27 (2006) 261-267
14. Croxford J.L., Anger H.A., and Miller S.D. Viral delivery of an epitope from Haemophilus influenzae induces central nervous system autoimmune disease by molecular mimicry. J. Immunol. 174 (2005) 907-917
15. Croxford J.L., Olson J.K., Anger H.A., and Miller S.D. Initiation and exacerbation of autoimmune demyelination of the central nervous system via virus-induced molecular mimicry: implications for the pathogenesis of multiple sclerosis. J. Virol. 79 (2005) 8581-8590
16. Sospedra M., Zhao Y., zur Hausen H., Muraro P.A., Hamashin C., de Villiers E.M., Pinilla C., and Martin R. Recognition of conserved amino acid motifs of common viruses and its role in autoimmunity. PLoS Pathog. 1 (2005) e41
17. Baccala R., and Theofilopoulos A.N. The new paradigm of T-cell homeostatic proliferation-induced autoimmunity. Trends Immunol. 26 (2005) 5-8
18. Kawakami N., Odoardi F., Ziemssen T., Bradl M., Ritter T., Neuhaus O., Lassmann H., Wekerle H., and Flugel A. Autoimmune CD4+ T cell memory: lifelong persistence of encephalitogenic T cell clones in healthy immune repertoires. J. Immunol. 175 (2005) 69-81
19. Austin L.M., Ozawa M., Kikuchi T., Walters I.B., and Krueger J.G. The majority of epidermal T cells in Psoriasis vulgaris lesions can produce type 1 cytokines, interferon-gamma, interleukin-2, and tumor necrosis factor-alpha, defining TC1 (cytotoxic T lymphocyte) and TH1 effector populations: a type 1 differentiation bias is also measured in circulating blood T cells in psoriatic patients. J. Invest. Dermatol. 113 (1999) 752-759
20. Friedrich M., Krammig S., Henze M., Docke W.D., Sterry W., and Asadullah K. Flow cytometric characterization of lesional T cells in psoriasis: intracellular cytokine and surface antigen expression indicates an activated, memory/effector type 1 immunophenotype. Arch. Dermatol. Res. 292 (2000) 519-521
21. Kohem C.L., Brezinschek R.I., Wisbey H., Tortorella C., Lipsky P.E., and Oppenheimer-Marks N. Enrichment of differentiated CD45RBdim,CD27- memory T cells in the peripheral blood, synovial fluid, and synovial tissue of patients with rheumatoid arthritis. Arthritis Rheum. 39 (1996) 844-854
22. Fasth A.E., Cao D., van Vollenhoven R., Trollmo C., and Malmstrom V. CD28nullCD4+ T cells-characterization of an effector memory T-cell population in patients with rheumatoid arthritis. Scand. J. Immunol. 60 (2004) 199-208
23. Burns J., Bartholomew B., and Lobo S. Isolation of myelin basic protein-specific T cells predominantly from the memory T-cell compartment in multiple sclerosis. Ann. Neurol. 45 (1999) 33-39
24. Okuda Y., Okuda M., Apatoff B.R., and Posnett D.N. The activation of memory CD4(+) T cells and CD8(+) T cells in patients with multiple sclerosis. J. Neurol. Sci. 235 (2005) 11-17
25. Lovett-Racke A.E., Trotter J.L., Lauber J., Perrin P.J., June C.H., and Racke M.K. Decreased dependence of myelin basic protein-reactive T cells on CD28-mediated costimulation in multiple sclerosis patients. A marker of activated/memory T cells. J. Clin. Invest. 101 (1998) 725-730
26. Ellis C.N., and Krueger G.G. Treatment of chronic plaque psoriasis by selective targeting of memory effector T lymphocytes. N. Engl. J. Med. 345 (2001) 248-255
27. Gordon K.B., Vaishnaw A.K., O'Gorman J., Haney J., and Menter A. Treatment of psoriasis with alefacept: correlation of clinical improvement with reductions of memory T-cell counts. Arch. Dermatol. 139 (2003) 1563-1570
28. Neidhart M., Fehr K., Pataki F., and Michel B.A. The levels of memory (CD45RA-, RO+) CD4+ and CD8+ peripheral blood T-lymphocytes correlate with IgM rheumatoid factors in rheumatoid arthritis. Rheunatol. Int. 15 (1996) 201-209
29. Reijonen H., Novak E.J., Kochik S., Heninger A., Liu A.W., Kwok W.W., and Nepom G.T. Detection of GAD65-specific T-cells by major histocompatibility complex class II tetramers in type 1 diabetic patients and at-risk subjects. Diabetes 51 (2002) 1375-1382
30. Beeton C., and Chandy K.G. Potassium channels, memory T cells, and multiple sclerosis. Neuroscientist 11 (2005) 550-562
31. 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. 163 (1999) 2267-2275
32. Augustine J.J., Siu D.S., Clemente M.J., Schulak J.A., Heeger P.S., and Hricik D.E. Pre-transplant IFN-gamma ELISPOTs are associated with post-transplant renal function in African American renal transplant recipients. Am. J. Transp. 5 (2005) 1971-1975
33. Gebauer B.S., Hricik D.E., Atallah A., Bryan K., Riley J., Tary-Lehmann M., Greenspan N.S., Dejelo C., Boehm B.O., Hering B.J., and Heeger P.S. Evolution of the enzyme-linked immunosorbent spot assay for post-transplant alloreactivity as a potentially useful immune monitoring tool. Am. J. Transp. 2 (2002) 857-866
34. Pearl J.P., Parris J., Hale D.A., Hoffmann S.C., Bernstein W.B., McCoy K.L., Swanson S.J., Mannon R.B., Roederer M., and Kirk A.D. Immunocompetent T-cells with a memory-like phenotype are the dominant cell type following antibody-mediated T-cell depletion. Am. J. Transp. 5 (2005) 465-474
35. 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. Transp. 2 (2002) 501-509
36. Bonnefoy-Berard N., Vincent C., and Revillard J.P. Antibodies against functional leukocyte surface molecules in polyclonal antilymphocyte and antithymocyte globulins. Transplantation 51 (1991) 669-673
37. Knechtle S.J., Pirsch J.D., Fechner J. J.H., Becker B.N., Friedl A., Colvin R.B., Lebeck L.K., Chin L.T., Becker Y.T., Odorico J.S., D'Alessandro A.M., Kalayoglu M., Hamawy M.M., Hu H., Bloom D.D., and Sollinger H.W. Campath-1H induction plus rapamycin monotherapy for renal transplantation: results of a pilot study. Am. J. Transp. 3 (2003) 722-730
38. Bonnefoy-Berard N., and Revillard J.P. Mechanisms of immunosuppression induced by antithymocyte globulins and OKT3. J. Heart Lung Transp. 15 (1996) 435-442
39. Genestier L., Fournel S., Flacher M., Assossou O., and RevillardN. Bonnefoy-Berard J.P. Induction of Fas (Apo-1, CD95)-mediated apoptosis of activated lymphocytes by polyclonal antithymocyte globulins. Blood 91 (1998) 2360-2368
40. Preville X., Flacher M., LeMauff B., Beauchard S., Davelu P., Tiollier J., and Revillard J.P. Mechanisms involved in antithymocyte globulin immunosuppressive activity in a nonhuman primate model. Transplantation 71 (2001) 460-468
41. Neujahr D.C., Chen C., Huang X., Markmann J.F., Cobbold S., Waldmann H., Sayegh M.H., Hancock W.W., and Turka L.A. Accelerated memory cell homeostasis during T cell depletion and approaches to overcome it. J. Immunol. 176 (2006) 4632-4639
42. Cox A.L., Thompson S.A.J., Jones J.L., Robertson V.H., Hale G., Waldmann H., Compston D.A.S., and Coles A.J. Lymphocyte homeostasis following therapeutic lymphocyte depletion in multiple sclerosis. Eur. J. Immunol. 35 (2005) 3332-3342
43. Jendro M.C., Ganten T., Matteson E.L., Weyand C.M., and Goronzy J.J. Emergence of oligoclonal T cell populations following therapeutic T cell depletion in rheumatoid arthritis. Arthritis Rheum. 38 (1995) 1242-1251
44. Kuhns M.S., Davis M.M., and Garcia K.C. Deconstructing the form and function of the TCR/CD3 complex. Immunity 24 (2006) 133-139
45. Andris F., Denanglaire S., de Mattia F., Urbain J., and Leo O. Naive T cells are resistant to anergy induction by anti-CD3 antibodies. J. Immunol. 173 (2004) 3201-3208
46. Hirsch R., Eckhaus M., Auchincloss Jr. H., Sachs D.H., and Bluestone J.A. Effects of in vivo administration of anti-T3 monoclonal antibody on T cell function in mice. I. Immunosuppression of transplantation responses. J. Immunol. 140 (1988) 3766-3772
47. Li B., Wang H., Dai J., Ji J., Qian W., Zhang D., Hou S., and Guo Y. Construction and characterization of a humanized anti-human CD3 monoclonal antibody 12F6 with effective immunoregulation functions. Immunology 116 (2005) 487-498
48. Ceuppens J.L., Bloemmen F.J., and Van Wauwe J.P. T cell unresponsiveness to the mitogenic activity of OKT3 antibody results from a deficiency of monocyte Fc gamma receptors for murine IgG2a and inability to cross-link the T3-Ti complex. J. Immunol. 135 (1985) 3882-3886
49. Suthanthiran M., Fotino M., Riggio R.R., Cheigh J.S., and Stenzel K.H. OKT3-associated adverse reactions: mechanistic basis and therapeutic options. Am. J. Kidney Dis. 14 (1989) 39-44
50. Chang T.W., Testa D., Kung P.C., Perry L., Dreskin H.J., and Goldstein G. Cellular origin and interactions involved in gamma-interferon production induced by OKt3 monoclonal antibody. J. Immunol. 128 (1982) 585-589
51. Gaston R.S., Deierhoi M.H., Patterson T., Prasthofer E., Julian B.A., Barber W.H., Laskow D.A., Diethelm A.G., and Curtis J.J. OKT3 first-dose reaction: association with T cell subsets and cytokine release. Kidney Int. 39 (1991) 141-148
52. Thistlethwaite Jr. J.R., Stuart J.K., Mayes J.T., Gaber A.O., Woodle S., Buckingham M.R., and Stuart F.P. Complications and monitoring of OKT3 therapy. Am. J. Kidney Dis. 11 (1988) 112-119
53. Alegre M.L., Collins A.M., Pulito V.L., Brosius R.A., Olson W.C., Zivin R.A., Knowles R., Thistlethwaite J.R., Jolliffe L.K., and Bluestone J.A. Effect of a single amino acid mutation on the activating and immunosuppressive properties of a "humanized" OKT3 monoclonal antibody. J. Immunol. 148 (1992) 3461-3468
54. Herold K.C., Hagopian W., Auger J.A., Poumian-Ruiz E., Taylor L., Donaldson D., Gitelman S.E., Harlan D.M., Xu D., Zivin R.A., and Bluestone J.A. Anti-CD3 monoclonal antibody in new-onset type 1 diabetes mellitus. N. Engl. J. Med. 346 (2002) 1692-1698
55. Herold K.C., Burton J.B., Francois F., Poumian-Ruiz E., Glandt M., and Bluestone J.A. Activation of human T cells by FcR nonbinding anti-CD3 mAb, hOKT3gamma1(Ala-Ala). J. Clin. Invest. 111 (2003) 409-418
56. Ahmadzadeh M., and Farber D.L. Functional plasticity of an antigen-specific memory CD4 T cell population. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 11802-11807
57. Dudley M.E., Wunderlich J.R., Robbins P.F., Yang J.C., Hwu P., Schwartzentruber D.J., Topalian S.L., Sherry R., Restifo N.P., Hubicki A.M., Robinson M.R., Raffeld M., Duray P., Seipp C.A., Rogers-Freezer L., Morton K.E., Mavroukakis S.A., White D.E., and Rosenberg S.A. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298 (2002) 850-854
58. Levine B.L., Bernstein W.B., Aronson N.E., Schlienger K., Cotte J., Perfetto S., Humphries M.J., Ratto-Kim S., Birx D.L., Steffens C., Landay A., Carroll R.G., and June C.H. Adoptive transfer of costimulated CD4+ T cells induces expansion of peripheral T cells and decreased CCR5 expression in HIV infection. Nat. Med. 8 (2002) 47-53
59. Patke D.S., Ahmadzadeh M., Bingaman A.W., and Farber D.L. Anti-CD3 priming generates heterogeneous antigen-specific memory CD4 T cells. Clin. Immunol. 117 (2005) 125-132
60. Dooms H., Kahn E., Knoechel B., and Abbas A.K. IL-2 induces a competitive survival advantage in T lymphocytes. J. Immunol. 172 (2004) 5973-5979
61. Williams M.A., Tyznik A.J., and Bevan M.J. Interleukin-2 signals during priming are required for secondary expansion of CD8(+) memory T cells. Nature 441 (2006) 890-893
62. Dai Z., Konieczny B.T., and Lakkis F.G. The dual role of IL-2 in the generation and maintenance of CD8+ memory T cells. J. Immunol. 165 (2000) 3031-3036
63. Schreiber S.L., and Crabtree G.R. The mechanism of action of cyclosporin A and FK506. Immunol. Today 13 (1992) 136-142
64. Sehgal S.N. Rapamune (RAPA, rapamycin, sirolimus): mechanism of action immunosuppressive effect results from blockade of signal transduction and inhibition of cell cycle progression. Clin. Biochem. 31 (1998) 335-340
65. Flanagan W.M., and Crabtree G.R. Rapamycin inhibits p34cdc2 expression and arrests T lymphocyte proliferation at the G1/S transition. Ann. N. Y. Acad. Sci. 696 (1993) 31-37
66. Koenen H.J., Michielsen E.C., Verstappen J., Fasse E., and Joosten I. Superior T-cell suppression by rapamycin and FK506 over rapamycin and cyclosporine A because of abrogated cytotoxic T-lymphocyte induction, impaired memory responses, and persistent apoptosis. Transplantation 75 (2003) 1581-1590
67. Chandok M.R., and Farber D.L. Signaling control of memory T cell generation and function. Semin. Immunol. 16 (2004) 285-293
68. Farber D.L., Acuto O., and Bottomly K. Differential TCR-mediated signaling in naive and memory CD4 T cells. Eur. J. Immunol. 27 (1997) 2094-2101
69. Hussain S.F., Anderson C.F., and Farber D.L. Differential SLP-76 expression and TCR-mediated signaling in effector and memory CD4 T cells. J. Immunol. 168 (2002) 1557-1565
70. Church A.C. Clinical advances in therapies targeting the interleukin-2 receptor. Q. J. Med. 96 (2003) 91-102
71. Patke D.S., and Farber D.L. Modulation of memory CD4 T cell function and survival potential by altering the strength of the recall stimulus. J. Immunol. 174 (2005) 5433-5443
72. Ku C.C., Murakami M., Sakamoto A., Kappler J., and Marrack P. Control of homeostasis of CD8+ memory T cells by opposing cytokines. Science 288 (2000) 675-678
73. Kohm A.P., McMahon J.S., Podojil J.R., Begolka W.S., DeGutes M., Kasprowicz D.J., Ziegler S.F., and Miller S.D. Cutting edge: anti-CD25 monoclonal antibody injection results in the functional inactivation, not depletion, of CD4+CD25+ T regulatory cells. J. Immunol. 176 (2006) 3301-3305
74. Dai Z., Li Q., Wang Y., Gao G., Diggs L.S., Tellides G., and Lakkis F.G. CD4+CD25+ regulatory T cells suppress allograft rejection mediated by memory CD8+ T cells via a CD30-dependent mechanism. J. Clin. Invest. 113 (2004) 310-317
75. Bretscher P., and Cohn M. A theory of self-nonself discrimination. Science 169 (1970) 1042-1049
76. Lafferty K.J., and Woolnough J. The origin and mechanism of the allograft reaction. Immunol. Rev. 35 (1977) 231-262
77. Salomon B., and Bluestone J.A. Complexities of CD28/B7: CTLA-4 costimulatory pathways in autoimmunity and transplantation. Annu. Rev. Immunol. 19 (2001) 225-252
78. Bluestone J.A., St Clair E.W., and Turka L.A. CTLA4Ig: bridging the basic immunology with clinical application. Immunity 24 (2006) 233-238
79. Murali-Krishna K., Altman J.D., Suresh M., Sourdive D.J., Zajac A.J., Miller J.D., Slansky J., and Ahmed R. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 8 (1998) 177-187
80. Metz D.P., Farber D.L., Taylor T., and Bottomly K. Differential role of CTLA-4 in regulation of resting memory versus naive CD4 T cell activation. J. Immunol. 161 (1998) 5855-5861
81. Linsley P.S., Wallace P.M., Johnson J., Gibson M.G., Greene J.L., Ledbetter J.A., Singh C., and Tepper M.A. Immunosuppression in vivo by a soluble form of the CTLA-4 T cell activation molecule. Science 257 (1992) 792-795
82. Wells A.D., Gudmundsdottir H., and Turka L.A. Following the fate of individual T cells throughout activation and clonal expansion. Signals from T cell receptor and CD28 differentially regulate the induction and duration of a proliferative response. J. Clin. Invest. 100 (1997) 3173-3183
83. Lin H., Bolling S.F., Linsley P.S., Wei R.Q., Gordon D., Thompson C.B., and Turka L.A. Long-term acceptance of major histocompatibility complex mismatched cardiac allografts induced by CTLA4Ig plus donor-specific transfusion. J. Exp. Med. 178 (1993) 1801-1806
84. Pearson T.C., Alexander D.Z., Winn K.J., Linsley P.S., Lowry R.P., and Larsen C.P. Transplantation tolerance induced by CTLA4-Ig. Transplantation 57 (1994) 1701-1706
85. Finck B.K., Linsley P.S., and Wofsy D. Treatment of murine lupus with CTLA4Ig. Science 265 (1994) 1225-1227
86. Khoury S.J., Akalin E., Chandraker A., Turka L.A., Linsley P.S., Sayegh M.H., and Hancock W.W. CD28-B7 costimulatory blockade by CTLA4Ig prevents actively induced experimental autoimmune encephalomyelitis and inhibits Th1 but spares Th2 cytokines in the central nervous system. J. Immunol. 155 (1995) 4521-4524
87. Kremer J.M., Westhovens R., Leon M., Di Giorgio E., Alten R., Steinfeld S., Russell A., Dougados M., Emery P., Nuamah I.F., Williams G.R., Becker J.C., Hagerty D.T., and Moreland L.W. Treatment of rheumatoid arthritis by selective inhibition of T-cell activation with fusion protein CTLA4Ig. N. Engl. J. Med. 349 (2003) 1907-1915
88. Abrams J.R., Lebwohl M.G., Guzzo C.A., Jegasothy B.V., Goldfarb M.T., Goffe B.S., Menter A., Lowe N.J., Krueger G., Brown M.J., Weiner R.S., Birkhofer M.J., Warner G.L., Berry K.K., Linsley P.S., Krueger J.G., Ochs H.D., Kelley S.L., and Kang S. CTLA4Ig-mediated blockade of T-cell costimulation in patients with psoriasis vulgaris. J. Clin. Invest. 103 (1999) 1243-1252
89. Ndejembi M.P., Patke D.S., Bingaman A.W., and Farber D.L. CTLA4-Ig inhibits IL-2 production and in-vivo expansion of antigen-stimulated memory CD4 T cells. Clin. Immunol. 115 (2005) S219-S220
90. Ndejembi M.P., Patke D.S., Bingaman A.W., and Farber D.L. CTLA4-Ig treatment promotes loss of antigen-activated effector memory CD4 T cells. Arthritis Rheum. 52 (2005) S492
91. Larsen C.P., Pearson T.C., Adams A.B., Tso P., Shirasugi N., Strobertm E., Anderson D., Cowan S., Price K., Naemura J., Emswiler J., Greene J., Turk L.A., Bajorath J., Townsend R., Hagerty D., Linsley P.S., and Peach R.J. Rational development of LEA29Y (belatacept), a high-affinity variant of CTLA4-Ig with potent immunosuppressive properties. Am. J. Transp. 5 (2005) 443-453
92. Larsen C.P., Knechtle S.J., Adams A.B., Pearson T.C., and Kirk A.D. A new look at blockade of T cell costimulation: A therapeutic strategy for long-term maintenance immunosuppression. Am. J. Transp. 6 (2006) 876-883
93. Vincenti F., Larsen C., Durrbach A., Wekerle T., Nashan B., Blancho G., Lang P., Grinyo J., Halloran P.F., Solez K., Hagerty D., Levy E., Zhou W., Natarajan K., and Charpentier B. Costimulation blockade with belatacept in renal transplantation. N. Engl. J. Med. 353 (2005) 770-781
94. Yoshinaga S.K., Whoriskey J.S., Khare S.D., Sarmiento U., Guo J., Horan T., Shih G., Zhang M., Coccia M.A., Kohno T., Tafuri-Bladt A., Brankow D., Campbell P., Chang D., Chiu L., Dai T., Duncan G., Elliott G.S., Hui A., McCabe S.M., Scully S., Shahinian A., Shaklee C.L., Van G., Mak T.W., et al. T-cell co-stimulation through B7RP-1 and ICOS. Nature 402 (1999) 827-832
95. Greenwald R.J., Freeman G.J., and Sharpe A.H. The B7 family revisited. Annu. Rev. Immunol. 23 (2005) 515-548
96. Hutloff A., Dittrich A.M., Beier K.C., Eljaschewitsch B., Kraft R., Anagnostopoulos I., and Kroczek R.A. ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature 397 (1999) 263-266
97. Khayyamian S., Hutloff A., Buchner K., Grafe M., Henn V., Kroczek R.A., and Mages H.W. ICOS-ligand, expressed on human endothelial cells, costimulates Th1 and Th2 cytokine secretion by memory CD4+ T cells. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 6198-6203
98. Rottman J.B., Smith T., Tonra J.R., Ganley K., Bloom T., Silva R., Pierce B., Gutierrez-Ramos J.C., Ozkaynak E., and Coyle A.J. The costimulatory molecule ICOS plays an important role in the immunopathogenesis of EAE. Nat. Immunol. 2 (2001) 605-611
99. Iwai H., Kozono Y., Hirose S., Akiba H., Yagita H., Okumura K., Kohsaka H., Miyasaka N., and Azuma M. Amelioration of collagen-induced arthritis by blockade of inducible costimulator-B7 homologous protein costimulation. J. Immunol. 169 (2002) 4332-4339
100. Ozkaynak E., Gao W., Shemmeri N., Wang C., Gutierrez-Ramos J.C., Amaral J., Qin S., Rottman J.B., Coyle A.J., and Hancock W.W. Importance of ICOS-B7RP-1 costimulation in acute and chronic allograft rejection. Nat. Immunol. 2 (2001) 591-596
101. Kashizuka H., Sho M., Nomi T., Ikeda N., Kuzumoto Y., Akashi S., Tsurui Y., Mizuno T., Kanehiro H., Yagita H., Nakajima Y., and Sayegh M.H. Role of the ICOS-B7h costimulatory pathway in the pathophysiology of chronic allograft rejection. Transplantation 79 (2005) 1045-1050
102. Vu M.D., Clarkson M.R., Yagita H., Turka L.A., Sayegh M.H., and Li X.C. Critical, but conditional, role of OX40 in memory T cell-mediated rejection. J. Immunol. 176 (2006) 1394-1401
103. Chambers C.A., Sullivan T.J., and Allison J.P. Lymphoproliferation in CTLA-4-deficient mice is mediated by costimulation-dependent activation of CD4+ T cells. Immunity 7 (1997) 885-895
104. Anton van der Merwe P., Davis S.J., Shaw A.S., and Dustin M.L. Cytoskeletal polarization and redistribution of cell-surface molecules during T cell antigen recognition. Semin. Immunol. 12 (2000) 5-21
105. Linsley P.S., Brady W., Urnes M., Grosmaire L.S., Damle N.K., and Ledbetter J.A. CTLA-4 is a second receptor for the B cell activation antigen B7. J. Exp. Med. 174 (1991) 561-569
106. Ueda H., Howson J.M., Esposito L., Heward J., Snook H., Chamberlain G., Rainbow D.B., Hunter K.M., Smith A.N., Di Genova G., Herr M.H., Dahlman I., Payne F., Smyth D., Lowe C., Twells R.C., Howlett S., Healy B., Nutland S., Rance H.E., Everett V., Smink L.J., Lam A.C., Cordell H.J., Walker N.M., Bordin C., Hulme J., Motzo C., Cucca F., Hess J.F., Metzker M.L., Rogers J., Gregory S., Allahabadia A., Nithiyananthan R., Tuomilehto-Wolf E., Tuomilehto J., Bingley P., Gillespie K.M., Undlien D.E., Ronningen K.S., Guja C., Ionescu-Tirgoviste C., Savage D.A., Maxwell A.P., Carson D.J., Patterson C.C., Franklyn J.A., Clayton D.G., Peterson L.B., Wicker L.S., Todd J.A., and Gough S.C. Association of the T-cell regulatory gene CTLA4 with susceptibility to autoimmune disease. Nature 423 (2003) 506-511
107. Rodriguez M.R., Nunez-Roldan A., Aguilar F., Valenzuela A., Garcia A., and Gonzalez-Escribano M.F. Association of the CTLA4 3′ untranslated region polymorphism with the susceptibility to rheumatoid arthritis. Hum. Immunol. 63 (2002) 76-81
108. Fecteau S., Basadonna G.P., Freitas A., Ariyan C., Sayegh M.H., and Rothstein D.M. CTLA-4 up-regulation plays a role in tolerance mediated by CD45. Nat. Immunol. 2 (2001) 58-63
109. Chemnitz J.M., Parry R.V., Nichols K.E., June C.H., and Riley J.L. SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T cell activation. J. Immunol. 173 (2004) 945-954
110. Liang S.C., Latchman Y.E., Buhlmann J.E., Tomczak M.F., Horwitz B.H., Freeman G.J., and Sharpe A.H. Regulation of PD-1, PD-L1, and PD-L2 expression during normal and autoimmune responses. Eur. J. Immunol. 33 (2003) 2706-2716
111. Carter L., Fouser L.A., Jussif J., Fitz L., Deng B., Wood C.R., Collins M., Honjo T., Freeman G.J., and Carreno B.M. PD-1:PD-L inhibitory pathway affects both CD4(+) and CD8(+) T cells and is overcome by IL-2. Eur. J. Immunol. 32 (2002) 634-643
112. Yamazaki T., Akiba H., Iwai H., Matsuda H., Aoki M., Tanno Y., Shin T., Tsuchiya H., Pardoll D.M., Okumura K., Azuma M., and Yagita H. Expression of programmed death 1 ligands by murine T cells and APC. J. Immunol. 169 (2002) 5538-5545
113. Nishimura H., Nose M., Hiai H., Minato N., and Honjo T. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 11 (1999) 141-151
114. Salama A.D., Chitnis T., Imitola J., Ansari M.J., Akiba H., Tushima F., Azuma M., Yagita H., Sayegh M.H., and Khoury S.J. Critical role of the programmed death-1 (PD-1) pathway in regulation of experimental autoimmune encephalomyelitis. J. Exp. Med. 198 (2003) 71-78
115. Barber D.L., Wherry E.J., Masopust D., Zhu B., Allison J.P., Sharpe A.H., Freeman G.J., and Ahmed R. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439 (2006) 682-687
116. Nakazawa A., Dotan I., Brimnes J., Allez M., Shao L., Tsushima F., Azuma M., and Mayer L. The expression and function of costimulatory molecules B7H and B7-H1 on colonic epithelial cells. Gastroenterology 126 (2004) 1347-1357
117. Hatachi S., Iwai Y., Kawano S., Morinobu S., Kobayashi M., Koshiba M., Saura R., Kurosaka M., Honjo T., and Kumagai S. CD4+ PD-1+ T cells accumulate as unique anergic cells in rheumatoid arthritis synovial fluid. J. Rheumatol. 30 (2003) 1410-1419
118. Cayabyab M., Phillips J.H., and Lanier L.L. CD40 preferentially costimulates activation of CD4+ T lymphocytes. J. Immunol. 152 (1994) 1523-1531
119. Bingaman A.W., Ha J., Durham M.M., Waitze S.Y., Tucker-Burden C., Cowan S.R., Pearson T.C., and Larsen C.P. Analysis of the CD40 and CD28 pathways on alloimmune responses by CD4+ T cells in vivo. Transplantation 72 (2001) 1286-1292
120. 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. 169 (2002) 4667-4673
121. MacLeod M., Kwakkenbos M.J., Crawford A., Brown S., Stockinger B., Schepers K., Schumacher T., and Gray D. CD4 memory T cells survive and proliferate but fail to differentiate in the absence of CD40. J. Exp. Med. 203 (2006) 897-906
122. Larsen C.P., Knechtle S.J., Adams A., Pearson T., and Kirk A.D. A new look at blockade of T-cell costimulation: a therapeutic strategy for long-term maintenance immunosuppression. Am. J. Transp. 6 (2006) 876-883
123. Haanstra K.G., Sick E.A., Ringers J., Wubben J.A., Kuhn E.M., Boon L., and Jonker M. Costimulation blockade followed by a 12-week period of cyclosporine A facilitates prolonged drug-free survival of rhesus monkey kidney allografts. Transplantation 79 (2005) 1623-1626
124. Salek-Ardakani S., Song J., Halteman B.S., Jember A.G., Akiba H., Yagita H., and Croft M. OX40 (CD134) controls memory T helper 2 cells that drive lung inflammation. J. Exp. Med. 198 (2003) 315-324
125. Gramaglia I., Jember A., Pippig S.D., Weinberg A.D., Killeen N., and Croft M. The OX40 costimulatory receptor determines the development of CD4 memory by regulating primary clonal expansion. J. Immunol. 165 (2000) 3043-3050
126. Rogers P.R., Song J., Gramaglia I., Killeen N., and Croft M. OX40 promotes Bcl-xL and Bcl-2 expression and is essential for long-term survival of CD4 T cells. Immunity 15 (2001) 445-455
127. Evans D.E., Prell R.A., Thalhofer C.J., Hurwitz A.A., and Weinberg A.D. Engagement of OX40 enhances antigen-specific CD4(+) T cell mobilization/memory development and humoral immunity: comparison of alphaOX-40 with alphaCTLA-4. J. Immunol. 167 (2001) 6804-6811
128. Hendriks J., Xiao Y., Rossen J.W., van der Sluijs K.F., Sugamura K., Ishii N., and Borst J. During viral infection of the respiratory tract, CD27, 4-1BB, and OX40 collectively determine formation of CD8+ memory T cells and their capacity for secondary expansion. J. Immunol. 175 (2005) 1665-1676
129. Weinberg A.D., Wallin J.J., Jones R.E., Sullivan T.J., Bourdette D.N., Vandenbark A.A., and Offner H. Target organ-specific up-regulation of the MRC OX-40 marker and selective production of Th1 lymphokine mRNA by encephalitogenic T helper cells isolated from the spinal cord of rats with experimental autoimmune encephalomyelitis. J. Immunol. 152 (1994) 4712-4721
130. Tittle T.V., Weinberg A.D., Steinkeler C.N., and Maziarz R.T. Expression of the T-cell activation antigen, OX-40, identifies alloreactive T cells in acute graft-versus-host disease. Blood 89 (1997) 4652-4658
131. Brugnoni D., Bettinardi A., Malacarne F., Airo P., and Cattaneo R. CD134/OX40 expression by synovial fluid CD4+ T lymphocytes in chronic synovitis. Br. J. Rheumatol. 37 (1998) 584-585
132. Higgins L.M., McDonald S.A., Whittle N., Crockett N., Shields J.G., and MacDonald T.T. Regulation of T cell activation in vitro and in vivo by targeting the OX40-OX40 ligand interaction: amelioration of ongoing inflammatory bowel disease with an OX40-IgG fusion protein, but not with an OX40 ligand-IgG fusion protein. J. Immunol. 162 (1999) 486-493
133. Salek-Ardakani S., and Croft M. Regulation of CD4 T cell memory by OX40 (CD134). Vaccine 24 (2006) 872-883
134. Kreuwel H.T., Aung S., Silao C., and Sherman L.A. Memory CD8(+) T cells undergo peripheral tolerance. Immunity 17 (2002) 73-81
135. Wei C.H., Trenney R., Sanchez-Alavez M., Marquardt K., Woodland D.L., Henriksen S.J., and Sherman L.A. Tissue-resident memory CD8+ T cells can be deleted by soluble, but not cross-presented antigen. J. Immunol. 175 (2005) 6615-6623
136. Mirshahidi S., Huang C.T., and Sadegh-Nasseri S. Anergy in peripheral memory CD4(+) T cells induced by low avidity engagement of T cell receptor. J. Exp. Med. 194 (2001) 719-731
137. Mallone R., Kochik S.A., Reijonen H., Carson B., Ziegler S.F., Kwok W.W., and Nepom G.T. Functional avidity directs T-cell fate in autoreactive CD4+ T cells. Blood 106 (2005) 2798-2805
138. Steinman L. Immune therapy for autoimmune diseases. Science 305 (2004) 212-216
139. Semnani R.T., Nutman T.B., Hochman P., Shaw S., and van Seventer G.A. Costimulation by purified intercellular adhesion molecule 1 and lymphocyte function-associated antigen 3 induces distinct proliferation, cytokine and cell surface antigen profiles in human "naive" and "memory" CD4 T cells. J. Exp. Med. 180 (1994) 2125-2135
140. Sanders M.E., Makgoba M.W., Sharrow S.O., Stephany D., Springer T.A., Young H.A., and Shaw S. Human memory T lymphocytes express increased levels of three cell adhesion molecules (LFA-3, CD2, and LFA-1) and three other molecules (UCHL1, CDw29, and Pgp-1) and have enhanced IFN-γ production. J. Immunol. 140 (1988) 1401-1407
141. da Silva A.J., Brickelmaier M., Majeau G.R., Li Z., Su L., Hsu Y.M., and Hochman P.S. Alefacept, an immunomodulatory recombinant LFA-3/IgG1 fusion protein, induces CD16 signaling and CD2/CD16-dependent apoptosis of CD2(+) cells. J. Immunol. 168 (2002) 4462-4471
142. Majeau G.R., Meier W., Jimmo B., Kioussis D., and Hochman P.S. Mechanism of lymphocyte function-associated molecule 3-Ig fusion proteins inhibition of T cell responses. Structure/function analysis in vitro and in human CD2 transgenic mice. J. Immunol. 152 (1994) 2753-2767
143. Schmitz A., Sankaranarayanan A., Azam P., Schmidt-Lassen K., Homerick D., Hansel W., and Wulff H. Design of PAP-1, a selective small molecule Kv1.3 blocker, for the suppression of effector memory T cells in autoimmune diseases. Mol. Pharmacol. 68 (2005) 1254-1270
144. Rus H., Pardo C.A., Hu L., Darrah E., Cudrici C., Niculescu T., Niculescu F., Mullen K.M., Allie R., Guo L., Wulff H., Beeton C., Judge S.I., Kerr D.A., Knaus H.G., Chandy K.G., and Calabresi P.A. The voltage-gated potassium channel Kv1.3 is highly expressed on inflammatory infiltrates in multiple sclerosis brain. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 11094-11099
145. Matloubian M., Lo C.G., Cinamon G., Lesneski M.J., Xu Y., Brinkmann V., Allende M.L., Proia R.L., and Cyster J.G. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427 (2004) 355-360
146. Pinschewer D.D., Ochsenbein A.F., Odermatt B., Brinkmann V., Hengartner H., and Zinkernagel R.M. FTY720 immunosuppression impairs effector T cell peripheral homing without affecting induction, expansion, and memory. J. Immunol. 164 (2000) 5761-5770
147. Zhang Q., Chen Y., Fairchild R.L., Heeger P.S., and Valujskikh A. Lymphoid sequestration of alloreactive memory CD4 T cells promotes cardiac allograft survival. J. Immunol. 176 (2006) 770-777
148. Fujii R., Kanai T., Nemoto Y., Makita S., Oshima S., Okamoto R., Tsuchiya K., Totsuka T., and Watanabe M. FTY720 suppresses CD4+CD44highCD62L- effector memory T cell-mediated colitis. Am. J. Physiol.: Gastrointest. Liver Physiol. 291 (2006) G267-G274