Harnessing programmed cell death as a therapeutic strategy in rheumatic diseases

Nature Reviews Rheumatology

Volumn 7, Issue 3, 2011, Pages 152-160

  Ramaswamy, Madhu ^a   Deng, Min ^a   Siegel, Richard M ^a  

^a NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 8; COMPLEMENT COMPONENT C1Q; DEATH RECEPTOR; FAS LIGAND; METHOTREXATE; PROTEIN BCL 2; RITUXIMAB; TOCILIZUMAB; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR;

APOPTOSIS; ARTICLE; DRUG MECHANISM; DRUG TARGETING; GENETIC DISORDER; HUMAN; IMMUNE SYSTEM; IMMUNOPATHOGENESIS; IMMUNOREGULATION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RHEUMATIC DISEASE; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; AUTOIMMUNE DISEASES; CASPASES; HUMANS; MODELS, ANIMAL; RHEUMATIC DISEASES;

EID: 79952438496     PISSN: 17594790     EISSN: 17594804     Source Type: Journal    
DOI: 10.1038/nrrheum.2010.225     Document Type: Article

References (106)

1. Ferguson, T. A. & Griffith, T. S. A vision of cel death: Fas ligand and immune privilege 10 years later. Immunol. Rev. 213, 228-238 (2006). (Pubitemid 44401504)
2. Griffith, T. S., Brunner, T., Fletcher, S. M., Green, D. R. & Ferguson, T. A. Fas ligand? induced apoptosis as a mechanism of immune privilege. Science 270, 1189-1192 (1995).
3. Kirshner, J. R., Karpova, A. Y., Kops, M. & Howley, P M. Identification of TRAIL as an interferon regulatory factor 3 transcriptional target. J. Virol. 79, 9320-9324 (2005). (Pubitemid 40934844)
4. Siegel, R. M. Caspases at the crossroads of mmune-cell life and death. Nat Rev. Immunol. 6, 308-317 (2006).
5. Kischkel, F C et al. Cytotoxicitydependent APO-1 (Fas/CD95)associated proteins form a deathinducing signaling complex (DISC) with the receptor. EMBO J. 14, 5579-5588 (1995)
6. Peter, M. E. & Krammer, P H. The CD95(APO1/Fas) DISC and beyond. Cell Death Differ. 10, 26-35 (2003).
7. Micheau, O. The long form of FLIP is an activator of caspase-8 at the Fas death-inducing signaling complex. J. Biol. Chem. 277, 45162-45171 (2002). (Pubitemid 36159119)
8. Zhang, N. & He, Y W. An essential role for c-FLIP in the efficient development of mature T lymphocytes. J. Exp. Med. 202, 395-404 (2005). (Pubitemid 41126957)
9. Budd, R., Yeh, W. & Tschopp, J. cFLIP regulation of lymphocyte activation and development. Nat Rev. Immunol. 6, 196-204 (2006). (Pubitemid 43290989)
10. Scaffidi, C et al. Two CD95 (APO1/Fas) signaling pathways. EMBO J. 17, 1675-1687 (1998). (Pubitemid 28119121)
11. Shell, S. et al. Let7 expression defines two differentiation stages of cancer. Proc. Natl Acad. Sci. USA 104, 11400-11405 (2007). (Pubitemid 47175152)
12. Ramaswamy M. & Siegel, R. M. A FAScinating receptor in self-tolerance. Immunity 26, 545-547 (2007). (Pubitemid 46756356)
13. Siegel, R. M., Chan, F K., Chun, H. J. & Lenardo, M. J. The multifaceted role of Fas signaling in immune cell homeostasis and autoimmunity Nat Immunol. 1, 469-474 (2000).
14. Strasser, A., Jost, P J. & Nagata, S. The many roles of FAS receptor signaling in the immune system. Immunity 30, 180-192 (2009).
15. Chen, L. et al. CD95 promotes tumour growth. Nature 465, 492-496 (2010).
16. Letellier, E. et al. CD95ligand on peripheral myeloid cells activates Syk kinase to trigger their recruitment to the inflammatory site. Immunity 32, 240-252 (2010).
17. + Tcell memory via TRAILmediated activation-induced cell death. Nature 434, 88-93 (2005). (Pubitemid 40349390)
18. Takeda, K. et al. Critical role for tumor necrosis factor-related apoptosis-inducing ligand in mmune surveillance against tumor development. J. Exp. Med. 195, 161-169 (2002). (Pubitemid 34461260)
19. Micheau, O. & Tschopp, J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114, 181-190 (2003). (Pubitemid 36936912)
20. Vince, J. E. et al. TweAK-FN14 signaling induces lysosomal degradation of a cIAP1-TRAF2 complex to sensitize tumor cells to TNFα. J. Cell Biol. 182, 171-184 (2008). (Pubitemid 352008630)
21. Ashwell, J. D. TweAKing death. J. Cell Biol. 182, 15-17 (2008). (Pubitemid 352008616)
22. Ashkenazi, A. & Dixit, V. M. Apoptosis control by death and decoy receptors. Curr. Opin. Cell Biol. 11, 255-260 (1999) (Pubitemid 29164042)
23. Marsden, v. S. & Strasser, A. Control of apoptosis in the immune system: Bcl2, BH3 only proteins and more. Annu. Rev. Immunol. 21, 71-105 (2003). (Pubitemid 37174527)
24. Youle, R. J. & Strasser, A. The BCL2 protein family: opposing activities that mediate cel death. Nat Rev. Mol. Cell Biol. 9, 47-59 (2008).
25. Strasser, A. The role of BH3only proteins in the mmune system. Nat Rev. Immunol. 5, 189-200 (2005). (Pubitemid 40364821)
26. Luo, X., Budihardjo, I., Zou, H., Slaughter, C & Wang, X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cel surface death receptors. Cell 94, 481-490 (1998). (Pubitemid 28391864)
27. Li, H., Zhu, H., Xu, C J. & Yuan, J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94, 491-501 (1998). (Pubitemid 28391865)
28. Srinivasula, S. M. et al. A conserved XIAP interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature 410, 112-116 (2001). (Pubitemid 32225846)
29. Green, D. R. & Kroemer, G. The pathophysiology of mitochondrial cell death. Science 305, 626-629 (2004). (Pubitemid 39006738)
30. Hildeman, D. A., Zhu, Y., Mitchell, T C., Kappler, J. & Marrack, P Molecular mechanisms of activated T cell death in vivo. Curr. Opin. Immunol. 14, 354-359 (2002). (Pubitemid 34327978)
31. Bouillet, P et al. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 286, 1735-1738 (1999). (Pubitemid 129515880)
32. + T cell contraction. Immunity 28, 218-230 (2008). (Pubitemid 351215232)
33. Hutcheson, J. et al. Combined deficiency of proapoptotic regulators Bim and Fas results in the early onset of systemic autoimmunity. Immunity 28, 206-217 (2008). (Pubitemid 351215233)
34. Hughes, P D. et al. Apoptosis regulators Fas and Bim cooperate in shutdown of chronic immune responses and prevention of autoimmunity. Immunity 28, 197-205 (2008). (Pubitemid 351215234)
35. Hornung, F., Zheng, L. & Lenardo, M. J. Maintenance of clonotype specificity in CD95/Apo-1/Fas-mediated apoptosis of mature T lymphocytes. J. Immunol. 159, 3816-3822 (1997). (Pubitemid 127469637)
36. Ramaswamy, M. et al. Cutting edge: Rac GTPases sensitize activated T cells to die via Fas. J. Immunol. 179, 6384-6388 (2007).
37. Muppidi, J. R. & Siegel, R. M. Ligand independent redistribution of Fas (CD95) into ipid rafts mediates clonotypic T cell death. Nat Immunol. 5, 182-189 (2004). (Pubitemid 38208360)
38. Vandenabeele, P, Vanden Berghe, T & Festjens, N. Caspase inhibitors promote alternative cell death pathways. Sci. STKE 2006, pe44 (2006).
39. Kroemer, G. et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 16, 3-11 (2009).
40. Declercq, W., Vanden Berghe, T & Vandenabeele, P RIP kinases at the crossroads of cell death and survival. Cell 138, 229-232 (2009).
41. Degterev, A. et al. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem. Biol. 4, 313-321 (2008). (Pubitemid 351550892)
42. Kroemer, G. & Levine, B. Autophagic cell death: the story of a misnomer. Nat Rev. Mol. Cell Biol. 9, 1004-1010 (2008).
43. Bell, B. D. et al. FADD and caspase-8 control the outcome of autophagic signaling in proliferating T cells. Proc. Natl Acad. Sci. USA 105, 16677-16682 (2008).
44. Green, D. R., Ferguson, T., Zitvogel, L & Kroemer, G. Immunogenic and tolerogenic cel death. Nat Rev. Immunol. 9, 353-363 (2009)
45. Fadok, V. A. et al. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGe2, and PAF J. Clin. Invest 101, 890-898 (1998). (Pubitemid 28096086)
46. Torchinsky, M. B., Garaude, J., Martin, A. P & Blander, J. M. Innate immune recognition of infected apoptotic cells directs TH17 cel differentiation. Nature 458, 78-82 (2009).
47. Botto, M. et al. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet 19, 56-59 (1998). (Pubitemid 28242023)
48. Bowness, P et al. Hereditary C1q deficiency and systemic lupus erythematosus. QJM 87, 455-464 (1994). (Pubitemid 24243465)
49. Lu, Q. & Lemke, G. Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro 3 family. Science 293, 306-311 (2001). (Pubitemid 32694748)
50. Hanayama, R. et al. Autoimmune disease and mpaired uptake of apoptotic cells in MFGe8 deficient mice. Science 304, 1147-1150 (2004). (Pubitemid 38661849)
51. Cook, H. T & Botto, M. Mechanisms of disease: the complement system and the pathogenesis of systemic lupus erythematosus. Nat. Clin. Pract Rheumatol. 2, 330-337 (2006). (Pubitemid 43842262)
52. Cohen, P. L. & Eisenberg, R. A. Lpr and gld: single gene models of systemic autoimmunity and lymphoproliferative disease. Annu. Rev. Immunol. 9, 243-269 (1991).
53. Stranges, P B. et al. elimination of antigen presenting cells and autoreactive T cells by fas contributes to prevention of autoimmunity. Immunity 26, 629-641 (2007). (Pubitemid 46756349)
54. Straus, S. E., Sneller, M., Lenardo, M. J., Puck, J. M. & Strober, W. An inherited disorder of lymphocyte apoptosis: the autoimmune lymphoproliferative syndrome. Ann. Intern. Med. 130, 591-601 (1999). (Pubitemid 29169388)
55. Drappa, J., Vaishnaw, A. K., Sullivan, K. E., Chu, J. L. & Elkon, K. B. Fas gene mutations in the Canale-Smith syndrome, an inherited lymphoproliferative disorder associated with autoimmunity. N. Engl. J. Med. 335, 1643-1649 (1996). (Pubitemid 26392729)
56. Fisher, G. H. et al. Dominant interfering Fas gene mutations impair apoptosis in a human autoimmune lymphoproliferative syndrome. Cell 81, 935-946 (1995).
57. Chun, H. J. et al. Pleiotropic defects in lymphocyte activation caused by caspase-8 mutations lead to human immunodeficiency. Nature 419, 395-399 (2002).
58. Pope, R. M. Apoptosis as a therapeutic tool in rheumatoid arthritis. Nat Rev. Immunol. 2, 527-535 (2002). (Pubitemid 37328744)
59. Perlman, H. et al. FLICe-inhibitory protein expression during macrophage differentiation confers resistance to fasmediated apoptosis. J. Exp. Med. 190, 1679-1688 (1999). (Pubitemid 30002349)
60. Liu, H. et al. TNFαinduced apoptosis of macrophages following inhibition of NFκB: a central role for disruption of mitochondria. J. Immunol. 172, 1907-1915 (2004). (Pubitemid 38116841)
61. Kovacs, B., Vassilopoulos, D., vogelgesang, S. A. & Tsokos, G. C Defective CD3mediated cel death in activated T cells from patients with systemic lupus erythematosus: role of decreased intracellular TNFα. Clin. Immunol. Immunopathol. 81, 293-302 (1996). (Pubitemid 26414559)
62. Liossis, S. N., Ding, X. Z., Dennis, G. J. & Tsokos, G. C Altered pattern of TCR/CD3 mediated proteintyrosyl phosphorylation in T cells from patients with systemic lupus erythematosus. Deficient expression of the T cell receptor zeta chain. J. Clin. Invest 101, 1448-1457 (1998). (Pubitemid 28166843)
63. Emlen, W., Niebur, J. & Kadera, R. Accelerated in vitro apoptosis of lymphocytes from patients with systemic lupus erythematosus. J. Immunol. 152, 3685-3692 (1994). (Pubitemid 24098067)
64. Baumann, I. et al. Impaired uptake of apoptotic cells into tingible body macrophages in germinal centers of patients with systemic lupus erythematosus. Arthritis Rheum. 46, 191-201 (2002). (Pubitemid 34121664)
65. Korb, L. C & Ahearn, J. M. C1q binds directly and specifically to surface blebs of apoptotic human keratinocytes: complement deficiency and systemic lupus erythematosus revisited. J. Immunol. 158, 4525-4528 (1997). (Pubitemid 127483768)
66. Carroll, M. C The role of complement in B cell activation and tolerance. Adv. Immunol. 74, 61-88 (2000).
67. Viorritto, I. C., Nikolov, N. P & Siegel, R. M. Autoimmunity versus tolerance: can dying cells tip the balance? Clin. Immunol. 122, 125-134 (2007). (Pubitemid 46073889)
68. Mouquet, H. et al. B-cell depletion mmunotherapy in pemphigus: effects on cellular and humoral immune responses. J. Invest Dermatol. 128, 2859-2869 (2008).
69. Zhou, X., Hu, W. & Qin, X. The role of complement in the mechanism of action of rituximab for B-cell lymphoma: implications for therapy. Oncologist 13, 954-966 (2008).
70. Ayroldi, E. et al. Interleukin-6 (IL-6) prevents activation-induced cell death: IL-2-independent inhibition of Fas/fasL expression and cell death. Blood 92, 4212-4219 (1998). (Pubitemid 28544337)
71. Haga, S. et al. Stat3 protects against Fas induced liver injury by redoxdependent and independent mechanisms. J. Clin. Invest 112, 989-998 (2003). (Pubitemid 38056314)
72. Kovalovich, K. et al. Interleukin6 protects against Fasmediated death by establishing a critical level of antiapoptotic hepatic proteins FLIP, Bcl2, and BclxL J. Biol. Chem. 276, 26605-26613 (2001)
73. Rigby, W. F Drug insight: different mechanisms of action of tumor necrosis factor antagonists\passiveaggressive behavior? Nat Clin. Pract Rheumatol. 3, 227-233 (2007). (Pubitemid 46860407)
74. van den Brande, J. M. et al. Infliximab but not etanercept induces apoptosis in lamina propria T lymphocytes from patients with Crohn's disease. Gastroenterology 124, 1774-1785 (2003).
75. Present, D. H. et al. Infliximab for the treatment of fistulas in patients with Crohn's disease. N. Engl. J. Med. 340, 1398-1405 (1999) (Pubitemid 29205403)
76. Sandborn, w. J. et al. etanercept for active Crohn's disease: a randomized, doubleblind, placebocontrolled trial. Gastroenterology 121, 1088-1094 (2001) (Pubitemid 33022088)
77. Chiang, E. Y et al. Targeted depletion of lymphotoxinαexpressing TH1 and TH17 cells inhibits autoimmune disease. Nat Med. 15, 766-773 (2009).
78. Distelhorst, C W. Recent insights into the mechanism of glucocorticosteroidinduced apoptosis. Cell Death Differ. 9, 6-19 (2002). (Pubitemid 34071989)
79. Strauss, G., Osen, W. & Debatin, K. M. Induction of apoptosis and modulation of activation and effector function in T cells by mmunosuppressive drugs. Clin. Exp. Immunol. 128, 255-266 (2002). (Pubitemid 34534038)
80. Herman, S., Zurgil, N. & Deutsch, M. Low dose methotrexate induces apoptosis with reactive oxygen species involvement in T lymphocytic cel ines to a greater extent than in monocytic lines. Inflamm. Res. 54, 273-280 (2005). (Pubitemid 41185488)
81. + T cell subpopulations. Immunol. Invest 33, 351-362 (2004). (Pubitemid 39299320)
82. Patel, M. P, Masood, A., Patel, P S. & Chanan Khan, A. A. Targeting the Bcl-2. Curr. Opin. Oncol. 21, 516-523 (2009).
83. Oltersdorf, T. et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435, 677-681 (2005). (Pubitemid 40825512)
84. Konopleva, M. et al. Mechanisms of apoptosis sensitivity and resistance to the BH3 mimetic ABT-737 in acute myeloid leukemia. Cancer Cell 10, 375-388 (2006). (Pubitemid 44693472)
85. Van Delft, M. F. et al. The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized. Cancer Cell 10, 389-399 (2006).
86. Bardwell, P D. et al. The Bcl-2 family antagonist ABT-737 significantly inhibits multiple animal models of autoimmunity. J. Immunol. 182, 7482-7489 (2009).
87. Kobayashi, T et al. Novel gene therapy for rheumatoid arthritis by FADD gene transfer: induction of apoptosis of rheumatoid synoviocytes but not chondrocytes. Gene Ther. 7, 527-533 (2000). (Pubitemid 30156568)
88. Palao, G. et al. Down-regulation of FLIP sensitizes rheumatoid synovial fibroblasts to Fas-mediated apoptosis. Arthritis Rheum. 50, 2803-2810 (2004). (Pubitemid 39209517)
89. Mourich, D. v. et al. Antisense targeting of cFLIP sensitizes activated T cells to undergo apoptosis and desensitizes responses to contact dermatitis. J. Invest. Dermatol. 129, 1945-1953 (2009).
90. Jonsson, H., Allen, P. & Peng, S. L. Inflammatory arthritis requires Foxo3a to prevent Fas ligand-induced neutrophil apoptosis. Nat Med. 11, 666-671 (2005). (Pubitemid 40868308)
91. Nagata, S. & Golstein, P The Fas death factor. Science 267, 1449-1456 (1995).
92. Xu, Y et al. Fc gamma Rs modulate cytotoxicity of anti-Fas antibodies: implications for agonistic antibody-based therapeutics. J. Immunol. 171, 562-568 (2003). (Pubitemid 36871362)
93. Schneider, P et al. Conversion of membrane bound Fas(CD95) ligand to its soluble form is associated with downregulation of its proapoptotic activity and loss of liver toxicity. J. Exp. Med. 187, 1205-1213 (1998). (Pubitemid 28189110)
94. Holler, N. et al. Two adjacent trimeric Fas ligands are required for Fas signaling and formation of a deathinducing signaling complex. Mol. Cell. Biol. 23, 1428-1440 (2003). (Pubitemid 36177050)
95. Verbrugge, I. et al. Combining radiotherapy with APO010 in cancer treatment. Clin. Cancer Res. 15, 2031-2038 (2009).
96. Samel, D. et al. Generation of a FasLbased proapoptotic fusion protein devoid of systemic toxicity due to cellsurface antigenrestricted activation. J. Biol. Chem. 278, 32077-32082 (2003) (Pubitemid 37048396)
97. Bremer, E., Ten Cate, B., Samplonius, D. F., De Leij, L. F & Helfrich, W. CD7-restricted activation of Fasmediated apoptosis: a novel therapeutic approach for acute T-cell leukemia. Blood 107, 2863-2870 (2006).
98. Okamoto, K. et al. Induction of apoptosis in the rheumatoid synovium by Fas ligand gene transfer. Gene Ther. 5, 331-338 (1998). (Pubitemid 28138238)
99. Zhang, H. et al. Amelioration of collagen? induced arthritis by CD95 (Apo-1/Fas)ligand gene transfer. J. Clin. Invest. 100, 1951-1957 (1997). (Pubitemid 27459348)
100. Varfolomeev, E. et al. X chromosome-linked inhibitor of apoptosis regulates cell death induction by proapoptotic receptor agonists. J. Biol. Chem. 284, 34553-34560 (2009).
101. Varfolomeev, E. et al. IAP antagonists induce autoubiquitination of c-IAPs, NFκB activation, and TNFαdependent apoptosis. Cell 131, 669-681 (2007). (Pubitemid 350087204)
102. + T cells due to enhanced Fas signaling complex formation and association with lipid raft microdomains. doi:10.1038/cdd.2010.155.
103. + central memory T cells. J. Exp. Med. 204, 79-91 (2007). (Pubitemid 46148759)
104. Combadiere, B., Reis E, Sousa, C., Germain, R. N. & Lenardo, M. J. Selective induction of apoptosis in mature T lymphocytes by variant T cell receptor ligands. J. Exp. Med. 187, 349-355 (1998). (Pubitemid 28080064)
105. Nikolov, N. P. et al. Systemic autoimmunity and defective Fas ligand secretion in the absence of the wiskott-Aldrich syndrome protein. Blood 116, 740-747 (2010).
106. Schungel, S. et al. The strength of the Fas ligand signal determines whether hepatocytes act as type 1 or type 2 cells in murine livers. Hepatology 50, 1558-1566 (2009).