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Review

Blocking Costimulatory Pathways: Prospects for Inducing Transplantation Tolerance

Bert Verbinnen1 University Hospital Gasthuisberg, Catholic University of Leuven, Leuven, Belgium
,
Stefaan W Van Gool1 University Hospital Gasthuisberg, Catholic University of Leuven, Leuven, Belgium
&
Jan L Ceuppens† Clinical Immunology, UZ Gasthuisberg, Herestraat 49, 3000Leuven, Belgium.Tel.: +32 1634 3805 Fax: +32 1634 [email protected]
Pages 497-509 | Published online: 16 Jul 2010

Bibliography

  • Starr TK , JamesonSC, HogquistKA: Positive and negative selection of T cells.Annu. Rev. Immunol.21 , 139–176 (2003).
  • Alam SM , TraversPJ, WungJLet al.: T-cell-receptor affinity and thymocyte positive selection.Nature381(6583) , 616–620 (1996).
  • Kappler JW , RoehmN, MarrackP: T cell tolerance by clonal elimination in the thymus.Cell49(2) , 273–280 (1987).
  • Redmond WL , ShermanLA: Peripheral tolerance of CD8 T lymphocytes.Immunity22(3) , 275–284 (2005).
  • Romagnani S : Regulation of the T cell response.Clin. Exp. Allergy36(11) , 1357–1366 (2006).
  • Schwartz RH : T cell anergy.Annu. Rev. Immunol.21 , 305–334 (2003).
  • Lamb JR , SkidmoreBJ, GreenN, ChillerJM, FeldmannM: Induction of tolerance in influenza virus-immune T lymphocyte clones with synthetic peptides of influenza hemagglutinin.J. Exp. Med.157(5) , 1434–1447 (1983).
  • Quill H , SchwartzRH: Stimulation of normal inducer T cell clones with antigen presented by purified Ia molecules in planar lipid membranes: specific induction of a long-lived state of proliferative nonresponsiveness.J. Immunol.138(11) , 3704–3712 (1987).
  • Frauwirth KA , ThompsonCB: Activation and inhibition of lymphocytes by costimulation.J. Clin. Invest.109(3) , 295–299 (2002).
  • Powell JD : The induction and maintenance of T cell anergy.Clin. Immunol.120(3) , 239–246 (2006).
  • Greenwald RJ , FreemanGJ, SharpeAH: The B7 family revisited.Annu. Rev. Immunol.23 , 515–548 (2005).
  • Sharpe AH , FreemanGJ: The B7-CD28 superfamily.Nat. Rev. Immunol.2(2) , 116–126 (2002).
  • Nurieva RI : Regulation of immune and autoimmune responses by ICOS-B7h interaction.Clin. Immunol.115(1) , 19–25 (2005).
  • Fife BT , BluestoneJA: Control of peripheral T-cell tolerance and autoimmunity via the CTLA-4 and PD-1 pathways.Immunol. Rev.224 , 166–182 (2008).
  • Holmberg D , CilioCM, LundholmM, MottaV: CTLA-4 (CD152) and its involvement in autoimmune disease.Autoimmunity38(3) , 225–233 (2005).
  • Butte MJ , KeirME, PhamduyTB, SharpeAH, FreemanGJ: Programmed death-1 ligand 1 interacts specifically with the B7–1 costimulatory molecule to inhibit T cell responses.Immunity27(1) , 111–122 (2007).
  • Croft M : Co-stimulatory members of the TNFR family: keys to effective T-cell immunity?Nat. Rev. Immunol.3(8) , 609–620 (2003).
  • Rocha B , GrandienA, FreitasAA: Anergy and exhaustion are independent mechanisms of peripheral T cell tolerance.J. Exp. Med.181(3) , 993–1003 (1995).
  • Zajac AJ , BlattmanJN, Murali-KrishnaKet al.: Viral immune evasion due to persistence of activated T cells without effector function.J. Exp. Med.188(12) , 2205–2213 (1998).
  • Singh NJ , ChenC, SchwartzRH: The impact of T cell intrinsic antigen adaptation on peripheral immune tolerance.PLoS Biol.4(11) , e340- (2006).
  • Kronenberg M , RudenskyA: Regulation of immunity by self-reactive T cells.Nature435(7042) , 598–604 (2005).
  • Sakaguchi S , YamaguchiT, NomuraT, OnoM: Regulatory T cells and immune tolerance.Cell133(5) , 775–787 (2008).
  • Tang Q , BluestoneJA: The Foxp3+ regulatory T cell: a jack of all trades, master of regulation.Nat. Immunol.9(3) , 239–244 (2008).
  • Roncarolo MG , GregoriS, BattagliaM, BacchettaR, FleischhauerK, LevingsMK: Interleukin-10-secreting type 1 regulatory T cells in rodents and humans.Immunol. Rev.212 , 28–50 (2006).
  • Cottrez F , GrouxH: Specialization in tolerance: innate CD(4+)CD(25+) versus acquired Tr1 and Th3 regulatory T cells.Transplantation77(1 Suppl.) , S12–S15 (2004).
  • Sakaguchi S , SakaguchiN, AsanoM, ItohM, TodaM: Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor α-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases.J. Immunol.155(3) , 1151–1164 (1995).
  • Suri-Payer E , AmarAZ, ThorntonAM, ShevachEM: CD4+CD25+ T cells inhibit both the induction and effector function of autoreactive T cells and represent a unique lineage of immunoregulatory cells.J. Immunol.160(3) , 1212–1218 (1998).
  • Fontenot JD , GavinMA, RudenskyAY: Foxp3 programs the development and function of CD4+CD25+ regulatory T cells.Nat. Immunol.4(4) , 330–336 (2003).
  • Hori S , NomuraT, SakaguchiS: Control of regulatory T cell development by the transcription factor Foxp3.Science299(5609) , 1057–1061 (2003).
  • Brunkow ME , JefferyEW, HjerrildKAet al.: Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse.Nat. Genet.27(1) , 68–73 (2001).
  • Wildin RS , RamsdellF, PeakeJet al.: X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy.Nat. Genet.27(1) , 18–20 (2001).
  • Bennett CL , ChristieJ, RamsdellFet al.: The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3.Nat. Genet.27(1) , 20–21 (2001).
  • Collison LW , WorkmanCJ, KuoTTet al.: The inhibitory cytokine IL-35 contributes to regulatory T-cell function.Nature450(7169) , 566–569 (2007).
  • O‘Garra A , VieiraP: Regulatory T cells and mechanisms of immune system control.Nat. Med.10(8) , 801–805 (2004).
  • Groux H , O‘GarraA, BiglerMet al.: A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis.Nature389(6652) , 737–742 (1997).
  • Barrat FJ , CuaDJ, BoonstraAet al.: In vitro generation of interleukin 10-producing regulatory CD4+ T cells is induced by immunosuppressive drugs and inhibited by T helper type 1 (Th1)- and Th2-inducing cytokines.J. Exp. Med.195(5) , 603–616 (2002).
  • Steinbrink K , WolflM, JonuleitH, KnopJ, EnkAH: Induction of tolerance by IL-10-treated dendritic cells.J. Immunol.159(10) , 4772–4780 (1997).
  • Sato K , YamashitaN, BabaM, MatsuyamaT: Modified myeloid dendritic cells act as regulatory dendritic cells to induce anergic and regulatory T cells.Blood101(9) , 3581–3589 (2003).
  • Ito T , YangM, WangYHet al.: Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand.J. Exp. Med.204(1) , 105–115 (2007).
  • Chen W , JinW, HardegenNet al.: Conversion of peripheral CD4+.J. Exp. Med.198(12) , 1875–1886 (2003).
  • Fantini MC , BeckerC, MonteleoneG, PalloneF, GallePR, NeurathMF: Cutting edge: TGF-β induces a regulatory phenotype in CD4+.J. Immunol.172(9) , 5149–5153 (2004).
  • Coombes JL , SiddiquiKR, Arancibia-CarcamoCVet al.: A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-β and retinoic acid-dependent mechanism.J. Exp. Med.204(8) , 1757–1764 (2007).
  • Linsley PS , BradyW, UrnesM, GrosmaireLS, DamleNK, LedbetterJA: CTLA-4 is a second receptor for the B cell activation antigen B7.J. Exp. Med.174(3) , 561–569 (1991).
  • Lenschow DJ , ZengY, ThistlethwaiteJRet al.: Long-term survival of xenogeneic pancreatic islet grafts induced by CTLA4lg.Science257(5071) , 789–792 (1992).
  • Turka LA , LinsleyPS, LinHet al.: T-cell activation by the CD28 ligand B7 is required for cardiac allograft rejection in vivo.Proc. Natl Acad. Sci. USA89(22) , 11102–11105 (1992).
  • Lin H , BollingSF, LinsleyPSet al.: Long-term acceptance of major histocompatibility complex mismatched cardiac allografts induced by CTLA4Ig plus donor-specific transfusion.J. Exp. Med.178(5) , 1801–1806 (1993).
  • Pearson TC , AlexanderDZ, WinnKJ, LinsleyPS, LowryRP, LarsenCP: Transplantation tolerance induced by CTLA4-Ig.Transplantation57(12) , 1701–1706 (1994).
  • Cavinato RA , CasiraghiF, AzzolliniNet al.: Pretransplant donor peripheral blood mononuclear cells infusion induces transplantation tolerance by generating regulatory T cells.Transplantation79(9) , 1034–1039 (2005).
  • Larsen CP , ElwoodET, AlexanderDZet al.: Long-term acceptance of skin and cardiac allografts after blocking CD40 and CD28 pathways.Nature381(6581) , 434–438 (1996).
  • Levisetti MG , PadridPA, SzotGLet al.: Immunosuppressive effects of human CTLA4Ig in a non-human primate model of allogeneic pancreatic islet transplantation.J. Immunol.159(11) , 5187–5191 (1997).
  • Kirk AD , HarlanDM, ArmstrongNNet al.: CTLA4-Ig and anti-CD40 ligand prevent renal allograft rejection in primates.Proc. Natl Acad. Sci. USA94(16) , 8789–8794 (1997).
  • Birsan T , HausenB, HigginsJPet al.: Treatment with humanized monoclonal antibodies against CD80 and CD86 combined with sirolimus prolongs renal allograft survival in cynomolgus monkeys.Transplantation75(12) , 2106–2113 (2003).
  • Kirk AD , TadakiDK, CelnikerAet al.: Induction therapy with monoclonal antibodies specific for CD80 and CD86 delays the onset of acute renal allograft rejection in non-human primates.Transplantation72(3) , 377–384 (2001).
  • Larsen CP , AlexanderDZ, HollenbaughDet al.: CD40–gp39 interactions play a critical role during allograft rejection. Suppression of allograft rejection by blockade of the CD40–gp39 pathway.Transplantation61(1) , 4–9 (1996).
  • Hancock WW , SayeghMH, ZhengXG, PeachR, LinsleyPS, TurkaLA: Costimulatory function and expression of CD40 ligand, CD80, and CD86 in vascularized murine cardiac allograft rejection.Proc. Natl Acad. Sci. USA93(24) , 13967–13972 (1996).
  • Markees TG , PhillipsNE, GordonEJet al.: Long-term survival of skin allografts induced by donor splenocytes and anti-CD154 antibody in thymectomized mice requires CD4+ T cells, interferon-γ, and CTLA4.J. Clin. Invest.101(11) , 2446–2455 (1998).
  • Larsen CP , PearsonTC: The CD40 pathway in allograft rejection, acceptance, and tolerance.Curr. Opin. Immunol.9(5) , 641–647 (1997).
  • Sebille F , VanhoveB, SoulillouJP: Mechanisms of tolerance induction: blockade of co-stimulation.Philos. Trans. R. Soc. Lond. B. Biol. Sci.356(1409) , 649–657 (2001).
  • Larsen CP , PearsonTC, AdamsABet al.: Rational development of LEA29Y (belatacept), a high-affinity variant of CTLA4-Ig with potent immunosuppressive properties.Am. J. Transplant.5(3) , 443–453 (2005).
  • Vincenti F , LarsenC, DurrbachAet al.: Costimulation blockade with belatacept in renal transplantation.N. Engl. J. Med.353(8) , 770–781 (2005).
  • Sidiropoulos PI , BoumpasDT: Lessons learned from anti-CD40L treatment in systemic lupus erythematosus patients.Lupus13(5) , 391–397 (2004).
  • Andre P , PrasadKS, DenisCVet al.: CD40L stabilizes arterial thrombi by a β3 integrin-dependent mechanism.Nat. Med.8(3) , 247–252 (2002).
  • Inwald DP , McDowallA, PetersMJ, CallardRE, KleinNJ: CD40 is constitutively expressed on platelets and provides a novel mechanism for platelet activation.Circ. Res.92(9) , 1041–1048 (2003).
  • Adams AB , ShirasugiN, JonesTRet al.: Development of a chimeric anti-CD40 monoclonal antibody that synergizes with LEA29Y to prolong islet allograft survival.J. Immunol.174(1) , 542–550 (2005).
  • Haanstra KG , RingersJ, SickEAet al.: Prevention of kidney allograft rejection using anti-CD40 and anti-CD86 in primates.Transplantation75(5) , 637–643 (2003).
  • Harada H , SalamaAD, ShoMet al.: The role of the ICOS-B7h T cell costimulatory pathway in transplantation immunity.J. Clin. Invest.112(2) , 234–243 (2003).
  • Kashizuka H , ShoM, NomiTet al.: Role of the ICOS-B7h costimulatory pathway in the pathophysiology of chronic allograft rejection.Transplantation79(9) , 1045–1050 (2005).
  • Guillonneau C , AubryV, RenaudinKet al.: Inhibition of chronic rejection and development of tolerogenic T cells after ICOS–ICOSL and CD40–CD40L co-stimulation blockade.Transplantation80(4) , 546–554 (2005).
  • Nabeyama K , YasunamiY, ToyofukuAet al.: Beneficial effects of costimulatory blockade with anti-inducible costimulator antibody in conjunction with CTLA4Ig on prevention of islet xenograft rejection from rat to mouse.Transplantation78(11) , 1590–1596 (2004).
  • Zhang QW , RabantM, SchenkA, ValujskikhA: ICOS-dependent and -independent functions of memory CD4 T cells in allograft rejection.Am. J. Transplant.8(3) , 497–506 (2008).
  • Curry AJ , ChikweJ, SmithXGet al.: OX40 (CD134) blockade inhibits the co-stimulatory cascade and promotes heart allograft survival.Transplantation78(6) , 807–814 (2004).
  • Demirci G , AmanullahF, KewalaramaniRet al.: Critical role of OX40 in CD28 and CD154-independent rejection.J. Immunol.172(3) , 1691–1698 (2004).
  • Yuan X , SalamaAD, DongVet al.: The role of the CD134-CD134 ligand costimulatory pathway in alloimmune responses in vivo.J. Immunol.170(6) , 2949–2955 (2003).
  • Van Gool SW , VermeirenJ, RafiqK, LorrK, De Boer M, Ceuppens JL: Blocking CD40 – CD154 and CD80/CD86 – CD28 during primary allogeneic stimulation results in T cell anergy and high IL-10 production. Eur. J. Immunol.29(8) , 2367–2375 (1999).
  • Vermeiren J , CeuppensJL, VanGMet al.: Human T cell activation by costimulatory signal-deficient allogeneic cells induces inducible costimulator-expressing anergic T cells with regulatory cell activity.J. Immunol.172(9) , 5371–5378 (2004).
  • Coenen JJ , KoenenHJ, van Rijssen E, Hilbrands LB, Joosten I: Tolerizing effects of co-stimulation blockade rest on functional dominance of CD4+CD25+ regulatory T cells. Transplantation79(2) , 147–156 (2005).
  • Wekerle T , SayeghMH, HillJet al.: Extrathymic T cell deletion and allogeneic stem cell engraftment induced with costimulatory blockade is followed by central T cell tolerance.J. Exp. Med.187(12) , 2037–2044 (1998).
  • Wells AD , LiXC, LiYet al.: Requirement for T-cell apoptosis in the induction of peripheral transplantation tolerance.Nat. Med.5(11) , 1303–1307 (1999).
  • Kurtz J , ItoH, WekerleT, ShafferJ, SykesM: Mechanisms involved in the establishment of tolerance through costimulatory blockade and BMT: lack of requirement for CD40L-mediated signaling for tolerance or deletion of donor-reactive CD4+ cells.Am. J. Transplant.1(4) , 339–349 (2001).
  • Verbinnen B , BilliauAD, VermeirenJet al.: Contribution of regulatory T cells and effector T cell deletion in tolerance induction by costimulation blockade.J. Immunol.181(2) , 1034–1042 (2008).
  • Bigenzahn S , BlahaP, KoporcZet al.: The role of non-deletional tolerance mechanisms in a murine model of mixed chimerism with costimulation blockade.Am. J. Transplant.5(6) , 1237–1247 (2005).
  • Quezada SA , BennettK, BlazarBR, RudenskyAY, SakaguchiS, NoelleRJ: Analysis of the underlying cellular mechanisms of anti-CD154-induced graft tolerance: the interplay of clonal anergy and immune regulation.J. Immunol.175(2) , 771–779 (2005).
  • Friedline RH , BrownDS, NguyenHet al.: CD4+ regulatory T cells require CTLA-4 for the maintenance of systemic tolerance.J. Exp. Med.206(2) , 421–434 (2009).
  • Wing K , OnishiY, Prieto-MartinPet al.: CTLA-4 control over Foxp3+ regulatory T cell function.Science322(5899) , 271–275 (2008).
  • Judge TA , WuZ, ZhengXG, SharpeAH, SayeghMH, TurkaLA: The role of CD80, CD86, and CTLA4 in alloimmune responses and the induction of long-term allograft survival.J. Immunol.162(4) , 1947–1951 (1999).
  • Coenen JJ , KoenenHJ, vanRE, BoonL, JoostenI, HilbrandsLB: CTLA-4 engagement and regulatory CD4+CD25+ T cells independently control CD8+-mediated responses under costimulation blockade.J. Immunol.176(9) , 5240–5246 (2006).
  • Tsai MK , HoHN, ChienHF, Ou-YangP, LeeCJ, LeePH: The role of B7 ligands (CD80 and CD86) in CD152-mediated allograft tolerance: a crosscheck hypothesis.Transplantation77(1) , 48–54 (2004).
  • Poirier N , AzimzadehAM, ZhangTet al.: Inducing CTLA-4-dependent immune regulation by selective CD28 blockade promotes regulatory T cells in organ transplantation.Sci. Transl. Med.2(17) , 17RA10 (2010).
  • Finger EB , BluestoneJA: When ligand becomes receptor – tolerance via B7 signaling on DCs.Nat. Immunol.3(11) , 1056–1057 (2002).
  • Puccetti P , GrohmannU: IDO and regulatory T cells: a role for reverse signalling and non-canonical NF-κB activation.Nat. Rev. Immunol.7(10) , 817–823 (2007).
  • Fallarino F , GrohmannU, VaccaCet al.: T cell apoptosis by tryptophan catabolism.Cell Death Differ.9(10) , 1069–1077 (2002).
  • Grohmann U , OrabonaC, FallarinoFet al.: CTLA-4-Ig regulates tryptophan catabolism in vivo.Nat. Immunol.3(11) , 1097–1101 (2002).
  • Seveno C , CoulonF, HaspotFet al.: Induction of regulatory cells and control of cellular but not vascular rejection by costimulation blockade in hamster-to-rat heart xenotransplantation.Xenotransplantation14(1) , 25–33 (2007).
  • Pree I , BigenzahnS, FuchsDet al.: CTLA4Ig promotes the induction of hematopoietic chimerism and tolerance independently of Indoleamine-2,3-dioxygenase.Transplantation83(5) , 663–667 (2007).
  • Francisco LM , SalinasVH, BrownKEet al.: PD-L1 regulates the development, maintenance, and function of induced regulatory T cells.J. Exp. Med.206(13) , 3015–3029 (2009).
  • Chen M , XiaoX, DemirciG, LiXC: OX40 controls islet allograft tolerance in CD154 deficient mice by regulating FOXP3+ Tregs.Transplantation85(11) , 1659–1662 (2008).
  • Ito T , WangYH, DuramadOet al.: OX40 ligand shuts down IL-10-producing regulatory T cells.Proc. Natl Acad. Sci. USA103(35) , 13138–13143 (2006).
  • Vu MD , XiaoX, GaoWet al.: OX40 costimulation turns off Foxp3+ Tregs.Blood110(7) , 2501–2510 (2007).
  • Wekerle T , SykesM: Mixed chimerism and transplantation tolerance.Annu. Rev. Med.52 , 353–370 (2001).
  • Jacobsen N , TaaningE, LadefogedJ, KristensenJK, PedersenFK: Tolerance to an HLA-B,DR disparate kidney allograft after bone-marrow transplantation from same donor.Lancet343(8900) , 800 (1994).
  • Sorof JM , KoerperMA, PortaleAA, PotterD, DeSantesK, CowanM: Renal transplantation without chronic immunosuppression after T cell-depleted, HLA-mismatched bone marrow transplantation.Transplantation59(11) , 1633–1635 (1995).
  • Svendsen UG , AggestrupS, HeilmannCet al.: Transplantation of a lobe of lung from mother to child following previous transplantation with maternal bone marrow.J. Heart Lung Transplant.18(4) , 388–390 (1999).
  • Wekerle T , KurtzJ, ItoHet al.: Allogeneic bone marrow transplantation with co-stimulatory blockade induces macrochimerism and tolerance without cytoreductive host treatment.Nat. Med.6(4) , 464–469 (2000).
  • Miller DM , ThornleyTB, PearsonTet al.: TLR agonists prevent the establishment of allogeneic hematopoietic chimerism in mice treated with costimulation blockade.J. Immunol.182(9) , 5547–5559 (2009).
  • Seung E , MordesJP, RossiniAA, GreinerDL: Hematopoietic chimerism and central tolerance created by peripheral-tolerance induction without myeloablative conditioning.J. Clin. Invest.112(5) , 795–808 (2003).

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