Cyclopentenone Prostaglandins Induce Lymphocyte Apoptosis by Activating the Mitochondrial Apoptosis Pathway Independent of External Death Receptor Signaling

Journal of Immunology

Volumn 171, Issue 10, 2003, Pages 5148-5156

  Nencioni, Alessio ^a,b   Lauber, Kirsten ^a   Grünebach, Frank ^a   Van Parijs, Luk ^b   Denzlinger, Claudio ^a   Wesselborg, Sebastian ^a   Brossart, Peter ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

15 DEOXY DELTA12,14 PROSTAGLANDIN J2; ACETYLCYSTEINE; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE 8; CASPASE INHIBITOR; CELL DEATH RECEPTOR; CELL RECEPTOR; CYCLOPENTANONE DERIVATIVE; CYTOCHROME C; FAS ANTIGEN; KETONE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR AGONIST; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROSTAGLANDIN; PROSTAGLANDIN D2 DERIVATIVE; PROTEIN BCL 2; PROTEIN BCL X; REACTIVE OXYGEN METABOLITE; THIAZOLIDINE DERIVATIVE; UNCLASSIFIED DRUG;

ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; ENZYME ACTIVATION; ENZYME RELEASE; FAS ASSOCIATED DEATH DOMAIN; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOMODULATION; LEUKEMIA CELL LINE; LYMPHOCYTE; LYMPHOCYTE PROLIFERATION; MEMBRANE POTENTIAL; MITOCHONDRION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DOMAIN; RECEPTOR BLOCKING; SIGNAL TRANSDUCTION; T CELL LEUKEMIA;

EID: 0242412240     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.171.10.5148     Document Type: Article

References (68)

1. 2. J. Biol. Chem. 258:11713.
2. 2 metabolite generated during inflammatory processes. J. Biol. Chem. 277:10459.
3. Gilroy, D. W., P. R. Colville-Nash, D. Willis, J. Chivers, M. J. Paul-Clark, and D. A. Willoughby. 1999. Inducible cyclooxygenase may have anti-inflammatory properties. Nat. Med. 55:698.
4. Willoughby, D. A., A. R. Moore, and P. R. Collville-Nash. 2000. Cyclopentenone prostaglandins: new allies in the war on inflammation. Nat. Med. 6:137.
5. Ricote, M., A. C. Li, T. M. Willson, C. J. Kelly, and C. K. Glass. 1998. The peroxisome proliferator-activated receptor-γ is a negative regulator of macrophage activation. Nature 391:79.
6. 2 integrin-dependent oxidative burst: involvement of a mechanism distinct from peroxisome proliferator-activated receptor γ ligation. J. Immunol. 163:6187.
7. Jiang, C., A. T. Ting, and B. Seed. 1998. PPAR-γ agonists inhibit production of monocyte inflammatory cytokines. Nature 391:82.
8. Yang, X. Y., L. H. Wang, T. Chen, D. R. Hodge, J. H. Resau, L. DaSilva, and W. L. Ferrar. 2000. Activation of human T-lymphocytes is inhibited by peroxisome proliferator-activated receptor γ (PPARγ) agonists. J. Biol. Chem. 275:4541.
9. Clark, R. B., D. Bishop-Bailey, T. Estrada-Hernandez, T. Hla, L. Puddington, and S. J. Padula. 2000. The nuclear receptor PPARγ and immunoregulation: PPARγ mediates inhibition of helper T cell responses. J. Immunol. 164:1364.
10. Harris, S. G., and R. P. Phipps. 2001. The nuclear receptor PPARγ is expressed by mouse T-lymphocytes and PPARγ agonists induce apoptosis. Eur. J. Immunol. 31:1098.
11. 2, and peroxisome proliferator activated receptor-γ agonists induce apoptosis in transformed, but not normal, human T lineage cells. Immunology 105:23.
12. Wang, Y. L., K. A. Frauwirth, S. M. Rangwala, M. A. Lazar, and C. B. Thompson. 2002. Thiazolidinedione activation of peroxisome proliferator-activated receptor γ can enhance mitochondrial potential and promote cell survival. J. Biol. Chem. 277:31781.
13. 2 inhibits CD95 ligand gene expression in T lymphocytes: interference with promoter activation via peroxisome proliferator-activated receptor-γ-independent mechanisms. J. Immunol. 170:4578.
14. + lymphocytes. J. Immunol. 165:1743.
15. 2 metabolite binds peroxisome proliferator-activated receptor γ and promotes adipocyte differentiation. Cell 83:813.
16. Desvergne, B., and W. Wahli. 1999. Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr. Rev. 20:649.
17. Tontonoz, P., E. Hu, and B. M. Spiegelman. 1994. Stimulation of adipogenesis in fibroblasts by PPARγ2, a lipid-activated transcription factor. Cell 79:1147.
18. Barak, Y., M. C. Nelson, E. S. Ong, Y. Z. Jones, P. Ruiz-Lozano, K. R. Chien, A. Koder, and R. M. Evans. 1999. PPAR-γ is required for placental, cardiac, and adipose tissue development. Mol. Cell 4:585.
19. Greene, M. E., B. Blumberg, O. W. McBride, H. F. Yi, K. Kronquist, K. Kwan, L. Hsieh, G. Greene, and S. D. Nimer. 1995. Isolation of the human peroxisome proliferator activated receptor-γ cDNA: expression in hematopoietic cells and chromosomal mapping. Gene Expression 4:281.
20. Tontonoz, P., L. Nagy, J. G. Alvarez, V. A. Thomazy, and R. M. Evans. 1998. PPARγ promotes monocyte/macrophage differentiation and uptake of oxidized LDL. Cell 93:241.
21. Nencioni, A., F. Grunebach, A. Zobywlaski, C. Denzlinger, W. Brugger, and P. Brossart. 2002. Dendritic cell immunogenicity is regulated by peroxisome proliferator-activated receptor γ. J. Immunol. 169:1228.
22. Nencioni, A., K. Lauber, F. Grunebach, W. Brugger, C. Denzlinger, S. Wesselborg, and P. Brossart. 2002. Cyclopentenone prostaglandins induce caspase activation and apoptosis in dendritic cells by a PPAR-γ-independent mechanism: regulation by inflammatory and T cell-derived stimuli. Exp. Hematol. 30:1020.
23. Gosset, P., A. S. Charbonnier, P. Delerive, J. Fontaine, B. Staels, J. Pestel, A. B. Tonnel, and F. Trottein. 2001. Peroxisome proliferator-activated receptor γ activators affect the maturation of human monocyte-derived dendritic cells. Eur. J. Immunol. 31:2857.
24. Su, C. G., X. Wen, S. T. Bailey, W. Jiang, S. M. Rangwala, S. A. Keilbaugh, A. Flanigan, S. Murthy, M. A. Lazar, and G. D. Wu. 1999. A novel therapy for colitis utilizing PPAR-γ ligands to inhibit the epithelial inflammatory response. J. Clin. Invest. 104:383.
25. Tanaka, T., H. Kohno, S. Yoshitani, S. Takashima, A. Okumura, A. Murakami, and M. Hosokawa. 2001. Ligand for peroxisome proliferator-activated receptors α and γ inhibit chemically induced colitis and formation of aberrant crypt foci in rats. Cancer Res. 61:2424.
26. 2 induces synoviocyte apoptosis and suppresses adjuvant-induced arthritis in rats. J. Clin. Invest. 106:189.
27. 2. J. Biol. Chem. 274:17042.
28. Chinetti, G., S. Griglio, M. Antonucci, I. P. Torra, P. Delerive, Z. Majd, J. C. Fruchart, J. Chapman, J. Najib, and B. Staels. 1998. Activation of proliferator-activated receptors α and γ induces apoptosis of human monocyte-derived macrophages. J. Biol. Chem. 273:25573.
29. Göke, R., A. Göke, B. Göke, and Y. Chen. 2000. Regulation of TRAIL-induced apoptosis by transcription factors. Cell. Immunol. 201:77.
30. 2 induce apoptosis in normal and malignant B-lineage cells. J. Immunol. 165:6941.
31. 2 inhibits multiple steps in the NF-κB signaling pathway. Proc. Natl. Acad. Sci. USA 97:4844.
32. Rossi, A., P. Kapahi, G. Natoli, T. Takahashi, Y. Chen, M. Karin, and M. G. Santoro. 2000. Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IκB kinase. Nature 403:103.
33. 2 inhibition of NF-κB-DNA binding through covalent modification of the p50 subunit. J. Biol. Chem. 276:35530.
34. Straus, D. S., and C. K. Glass. 2001. Cyclopentenone prostaglandins: new insights on biological activities and cellular targets. Med. Res. Rev. 21:185.
35. Wang, C. Y., M. W. Mayo, R. G. Korneluk, D. V. Goeddel, and A. S. Baldwin. 1998. NF-κB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281:1680.
36. Mullally, J. E., P. J. Moos, K. Edes, and F. A. Fitzpatrick. 2001. Cyclopentenone prostaglandins of the J series inhibit the ubiquitin isopeptidase activity of the proteasome pathway. J. Biol. Chem. 276:30366.
37. Hortelano, S., A. Castrillo, A. M. Alvarez, and L. Bosca. 2000. Contribution of cyclopentenone prostaglandins to the resolution of inflammation through the potentiation of apoptosis in activated macrophages. J. Immunol. 165:6525.
38. 2 induces apoptosis of human hepatic myofibroblasts: a pathway involving oxidative stress independently of peroxisome-proliferator-activated receptors. J. Biol. Chem. 276:38152.
39. Kondo, M., T. Oya-Ito, T. Kumagai, T. Osawa, and K. Uchida. 2001. Cyclopentenone prostaglandins as potential inducers of intracellular oxidative stress. J. Biol. Chem. 276:12076.
40. Krammer, P. H. 2000. CD95's deathly mission in the immune system. Nature 407:789.
41. Schulze-Osthoff, K., D. Ferrari, M. Los, S. Wesselborg, and M. E. Peter. 1998. Apoptosis signaling by death receptors. Eur. J. Biochem. 254:439.
42. Los, M., S. Wesselborg, and K. Schulze-Osthoff. 1999. The role of caspases in development, immunity, and apoptotic signal transduction: lessons from knockout mice. Immunity 10:629.
43. Hengartner, M. O. 2000. The biochemistry of apoptosis. Nature 407:770.
44. Li, H., H. Zhu, C. J. Xu, and J. Yuan. 1998. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94:491.
45. Luo, X., I. Budihardjo, H. Zou, C. Slaughter, and X. Wang. 1998. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94:481.
46. Adams, J. M., and S. Cory. 1998. The Bcl-2 protein family: arbiters of cell survival. Science 281:1322.
47. Kluck, R. M., E. Bossy-Wetzel, D. R. Green, and D. D. Newmeyer. 1997. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275:1132.
48. Yang, J., X. Liu, K. Bhalla, C. N. Kim, A. M. Ibrado, J. Cai, T. I. Peng, D. P. Jones, and X. Wang. 1997. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275:1129.
49. Engels, I. H., A. Stepczynska, C. Stroh, K. Lauber, C. Berg, R. Schwenzer, H. Wajant, R. U. Janicke, A. G. Porter, C. Belka, et al. 2000. Caspase-8/FLICE functions as an executioner caspase in anticancer drug-induced apoptosis. Oncogene 19:4563.
50. Stepczynska, A., K. Lauber, I. H. Engels, O. Janssen, D. Kabelitz, S. Wesselborg, and K. Schulze-Osthoff. 2001. Staurosporine and conventional anticancer drugs induce overlapping, yet distinct pathways of apoptosis and caspase activation. Oncogene 20:1193.
51. Wesselborg, S., I. H. Engels, E. Rossmann, M. Los, and K. Schulze-Osthoff. 1999. Anticancer drugs induce caspase-8/FLICE activation in the absence of CD95 receptor/ligand interaction. Blood 9:3053.
52. Nicoletti, I., G. Migliorati, M. C. Pagliacci, F. Grignani, and C. Riccardi. 1991. A rapid and simple method for measuring thymocytes apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 139:271.
53. Lauber, K., H. A. Appel, S. F. Schlosser, M. Gregor, K. Schulze-Osthoff, and S. Wesselborg. 2001. The adapter protein apoptotic protease-activating factor-1 (Apaf-1) is proteolytically processed during apoptosis. J. Biol. Chem. 276:29772.
54. Castedo, M., K. Ferri, T. Roumier, D. Metivier, N. Zamzami, and G. Kroemer. 2002. Quantitation of mitochondrial alterations associated with apoptosis. J. Immunol. Methods 265:39.
55. Takeyama, N., S. Miki, A. Hirakawa, and T. Tanaka. 2002. Role of the mitochondrial permeability transition and cytochrome c release in hydrogen peroxide-induced apoptosis. Exp. Cell. Res. 274:16.
56. Van Parijs, L., and A. K. Abbas. 1998. Homeostasis and self-tolerance in the immune system: turning lymphocytes off. Science 280:243.
57. Van Parijs, L., Y. Refaeli, J. D. Lord, B. H. Nelson, A. K. Abbas, and D. Baltimore. 1999. Uncoupling IL-2 signals that regulate T cell proliferation, survival, and Fas-mediated activation-induced cell death. Immunity 11:281.
58. L and Bfl-1. J. Immunol. 169:4882.
59. L and RAG genes are induced and the response to IL-2 enhanced in EμEBNA-1 transgenic mouse lymphocytes. Oncogene 21:5182.
60. 2+ fluxes. Proc. Natl. Acad. Sci. USA 91:6569.
61. Lassus, P., X. Opitz-Araya, and Y. Lazebnik. 2002. Requirement for caspase-2 in stress-induced apoptosis before mitochondrial permeabilization. Science 297:1352.
62. Jaattela, M., and J. Tschopp. 2003. Caspase-independent cell death in T lymphocytes. Nat. Immunol. 4:416.
63. 2 formation and characterization of its synthetases in various tissues of adult rats. Arch. Biochem. Biophys. 279:521.
64. 2 production is likely antigen presenting cells. J. Immunol. 143:2982.
65. Van Parijs, L., D. A. Peterson, and A. K. Abbas. 1998. The Fas/Fas ligand pathway and Bcl-2 regulate T cell responses to model self and foreign antigens. Immunity 8:265.
66. Boise, L. H., P. J. Noel, and C. B. Thompson. 1995. CD28 and apoptosis. Curr. Opin. Immunol. 7:620.
67. Singer, G. G., and A. K. Abbas. 1994. The fas antigen is involved in peripheral but not thymic deletion of T lymphocytes in T cell receptor transgenic mice. Immunity 1:365.
68. Zheng, L., G. Fisher, R. E. Miller, J. Peschon, D. H. Lynch, and M. J. Lenardo. 1995. Induction of apoptosis in mature T cells by tumour necrosis factor. Nature 377:348.