Resistance to ABT-737 in activated T lymphocytes: Molecular mechanisms and reversibility by inhibition of the calcineurin-NFAT pathway

Cell Death and Disease

Volumn 3, Issue 4, 2012, Pages

  Cippa P E ^a,b   Kraus, A K ^a,b   Lindenmeyer, M T ^a,b   Chen, J ^a,b   Guimezanes, A ^c   Bardwell, P D ^d   Wekerle, T ^e   Wuthrich R P ^a,b   Fehr, T ^a,b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^d ABBOTT LABORATORIES   (United States)

^e MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

ABT 737; Apoptosis; Bcl 2; T lymphocytes; Transplantation

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; CALCINEURIN; CYCLOSPORIN A; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR NFAT; ABT-737; BIPHENYL DERIVATIVE; CYCLOSPORIN; LYMPHOCYTE ANTIGEN RECEPTOR; NITROPHENOL; PIPERAZINE DERIVATIVE; SULFONAMIDE;

ALLOIMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG SENSITIVITY; FEMALE; GRAFT REJECTION; GRAFT VERSUS HOST REACTION; IMMUNE RESPONSE; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; UPREGULATION; ANIMAL; BONE MARROW TRANSPLANTATION; C57BL MOUSE; DRUG EFFECT; DRUG RESISTANCE; IMMUNOLOGY; METABOLISM; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

MURINAE;

ANIMALS; BIPHENYL COMPOUNDS; BONE MARROW TRANSPLANTATION; CALCINEURIN; CYCLOSPORINE; DRUG RESISTANCE; GRAFT VS HOST DISEASE; MICE; MICE, INBRED C57BL; NFATC TRANSCRIPTION FACTORS; NITROPHENOLS; PIPERAZINES; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; SULFONAMIDES; T-LYMPHOCYTES;

EID: 84862080324     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2012.38     Document Type: Article

References (38)

1. Vogler M, Dinsdale D, Dyer MJ, Cohen GM. Bcl-2 inhibitors: small molecules with a big impact on cancer therapy. Cell Death Differ 2009; 16: 360-367.
2. Carrington EM, Vikstrom IB, Light A, Sutherland RB, Londrigan SL, Mason KD et al. BH3 mimetics antagonizing restricted prosurvival Bcl-2 proteins represent another class of selective immune modulatory drugs. Proc Natl Acad Sci USA. 2010; 107: 10967-10971.
3. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, Belli BA et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 2005; 435: 677-681. (Pubitemid 40825512)
4. Tse C, Shoemaker AR, Adickes J, Chen J, Jin S, Johnson EF et al. ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor. Cancer Res 2008; 68: 3421-3428.
5. Wilson WH, O'Connor OA, Czuczman MS, LaCasce AS, Gerecitano JF, Leonard JP et al. Navitoclax, a targeted high-affinity inhibitor of BCL-2, in lymphoid malignancies: a phase 1 dose-escalation study of safety, pharmacokinetics, pharmacodynamics, and antitumour activity. Lancet Oncol 2010; 11: 1149-1159.
6. Del Gaizo Moore V, Schlis KD, Sallan SE, Armstrong SA, Letai A. BCL-2 dependence and ABT-737 sensitivity in acute lymphoblastic leukemia. Blood 2008; 111: 2300-2309. (Pubitemid 351451437)
7. Yecies D, Carlson NE, Deng J, Letai A. Acquired resistance to ABT-737 in lymphoma cells that up-regulate MCL-1 and BFL-1. Blood 115: 3304-3313.
8. Marsden VS, Strasser A. Control of apoptosis in the immune system: Bcl-2, BH3-only proteins and more. Annu Rev Immunol 2003; 21: 71-105. (Pubitemid 37174527)
9. Cho JH, Kim HO, Surh CD, Sprent J. T cell receptor-dependent regulation of lipid rafts controls naive CD8+ T cell homeostasis. Immunity 2010; 32: 214-226.
10. Hughes PD, Belz GT, Fortner KA, Budd RC, Strasser A, Bouillet P. Apoptosis regulators Fas and Bim cooperate in shutdown of chronic immune responses and prevention of autoimmunity. Immunity 2008; 28: 197-205. (Pubitemid 351215234)
11. Bouillet P, O'Reilly LA. CD95, BIM and T cell homeostasis. Nat Rev Immunol 2009; 9: 514-519.
12. Fischer SF, Belz GT, Strasser A. BH3-only protein Puma contributes to death of antigen-specific T cells during shutdown of an immune response to acute viral infection. Proc Natl Acad Sci USA. 2008; 105: 3035-3040. (Pubitemid 351723663)
13. Sabbagh L, Pulle G, Liu Y, Tsitsikov EN, Watts TH. ERK-dependent Bim modulation downstream of the 4-1BB-TRAF1 signaling axis is a critical mediator of CD8 T cell survival in vivo. J Immunol 2008; 180: 8093-8101.
14. Wojciechowski S, Tripathi P, Bourdeau T, Acero L, Grimes HL, Katz JD et al. Bim/Bcl-2 balance is critical for maintaining naive and memory T cell homeostasis. J Exp Med 2007; 204: 1665-1675. (Pubitemid 47048032)
15. Fehr T, Lucas CL, Kurtz J, Onoe T, Zhao G, Hogan T et al. A CD8 T cell-intrinsic role for the calcineurin-NFAT pathway for tolerance induction in vivo. Blood 2010; 115: 1280-1287.
16. Verschelde C, Walzer T, Galia P, Biemont MC, Quemeneur L, Revillard JP et al. A1/Bfl-1 expression is restricted to TCR engagement in T lymphocytes. Cell Death Differ 2003; 10: 1059-1067. (Pubitemid 37069483)
17. Gonzalez J, Orlofsky A, Prystowsky MB. A1 is a growth-permissive antiapoptotic factor mediating postactivation survival in T cells. Blood 2003; 101: 2679-2685. (Pubitemid 36857630)
18. Bardwell PD, Gu J, McCarthy D, Wallace C, Bryant S, Goess C et al. The Bcl-2 family antagonist ABT-737 significantly inhibits multiple animal models of autoimmunity J Immunol 2009; 182: 7482-7489.
19. Cippa PE, Kraus AK, Edenhofer I, Segerer S, Chen J, Hausmann M et al. The BH3-mimetic ABT-737 inhibits allogeneic immune responses. Transpl Int 2011; 24: 722-732.
20. Lawlor KE, Smith SD, van Nieuwenhuijze A, Huang DC, Wicks IP. Evaluation of the Bcl-2 family antagonist ABT-737 in collagen-induced arthritis. J Leukoc Biol 2011; 90: 819-829.
21. Al-Harbi S, Hill BT, Mazumder S, Singh K, Devecchio J, Choudhary G et al. An antiapoptotic BCL-2 family expression index predicts the response of chronic lymphocytic leukemia to ABT-737. Blood 2011; 118: 3579-3590.
22. Hamasaki A, Sendo F, Nakayama K, Ishida N, Negishi I, Hatakeyama S. Accelerated neutrophil apoptosis in mice lacking A1-a, a subtype of the bcl-2-related A1 gene J Exp Med 1998; 188: 1985-1992. (Pubitemid 28562516)
23. Cashman JR, MacDonald M, Ghirmai S, Okolowicz KJ, Sergienko E, Brown B et al. Inhibition of Bfl-1 with N-aryl maleimides. Bioorg Med Chem Lett 2010; 20: 6560-6564.
24. Matzinger P, Kamala T. Tissue-based class control: the other side of tolerance. Nat Rev Immunol 2011; 11: 221-230.
25. Aramburu J, Yaffe MB, Lopez-Rodriguez C, Cantley LC, Hogan PG, Rao A. Affinity-driven peptide selection of an NFAT inhibitor more selective than cyclosporin A. Science 1999; 285: 2129-2133. (Pubitemid 29451431)
26. Vogler M, Butterworth M, Majid A, Walewska RJ, Sun XM, Dyer MJ et al. Concurrent upregulation of BCL-XL and BCL2A1 induces approximately 1000-fold resistance to ABT-737 in chronic lymphocytic leukemia. Blood 2009; 113: 4403-4413.
27. Ulleras E, Karlberg M, Moller Westerberg C, Alfredsson J, Gerondakis S, Strasser A et al. NFAT but not NF-kappaB is critical for transcriptional induction of the prosurvival gene A1 after IgE receptor activation in mast cells. Blood 2008; 111: 3081-3089.
28. Wensveen FM, van Gisbergen KP, Derks IA, Gerlach C, Schumacher TN, van Lier RA et al. Apoptosis threshold set by Noxa and Mcl-1 after T cell activation regulates competitive selection of high-affinity clones. Immunity 32: 754-765.
29. Hotchkiss RS, Strasser A, McDunn JE, Swanson PE. Cell death. N Engl J Med. 2009; 361: 1570-1583.
30. Zamzami N, Marchetti P, Castedo M, Hirsch T, Susin SA, Masse B et al. Inhibitors of permeability transition interfere with the disruption of the mitochondrial transmembrane potential during apoptosis. FEBS Lett 1996; 384: 53-57. (Pubitemid 26114720)
31. Muller MR, A. Rao. NFAT, immunity and cancer: a transcription factor comes of age. Nat Rev Immunol 2010; 10: 645-656.
32. Sagoo P, Ali N, Garg G, Nestle FO, Lechler RI, Lombardi G. Human regulatory T cells with alloantigen specificity are more potent inhibitors of alloimmune skin graft damage than polyclonal regulatory T cells. Sci Transl Med 2011; 3: 83ra42.
33. Auphan N, Curnow J, Guimezanes A, Langlet C, Malissen B, Mellor A et al. The degree of CD8 dependence of cytolytic T cell precursors is determined by the nature of the T cell receptor (TCR) and influences negative selection in TCR-transgenic mice. Eur J Immunol 1994; 24: 1572-1577. (Pubitemid 24203763)
34. Guimezanes A, Barrett-Wilt GA, Gulden-Thompson P, Shabanowitz J, Engelhard VH, Hunt DF et al. Identification of endogenous peptides recognized by in vivo or in vitro generated alloreactive cytotoxic T lymphocytes: distinct characteristics correlated with CD8 dependence. Eur J Immunol 2001; 31: 421-432. (Pubitemid 32166596)
35. Haspot F, Fehr T, Gibbons C, Zhao G, Hogan T, Honjo T et al. Peripheral deletional tolerance of alloreactive CD8 but not CD4 T cells is dependent on the PD-1/PD-L1 pathway. Blood 2008; 112: 2149-2155.
36. Fehr T, Takeuchi Y, Kurtz J, Wekerle T, Sykes M. Early regulation of CD8 T cell alloreactivity by CD4+CD25- T cells in recipients of anti-CD154 antibody and allogeneic BMT is followed by rapid peripheral deletion of donor-reactive CD8+ T cells, precluding a role for sustained regulation. Eur J Immunol 2005; 35: 2679-2690. (Pubitemid 41404051)
37. Buferne M, Luton F, Letourneur F, Hoeveler A, Couez D, Barad M et al. Role of CD3 delta in surface expression of the TCR/CD3 complex and in activation for killing analyzed with a CD3 delta-negative cytotoxic T lymphocyte variant. J Immunol 1992; 148: 657-664.
38. Lindenmeyer MT, Eichinger F, Sen K, Anders HJ, Edenhofer I, Mattinzoli D et al. Systematic analysis of a novel human renal glomerulus-enriched gene expression dataset. PLoS One 2010; 5: e11545.