15-Deoxy-Δ12,14-prostaglandin J2 induces apoptosis in human malignant B cells: An effect associated with inhibition of NF-κB activity and down-regulation of antiapoptotic proteins

Blood

Volumn 105, Issue 4, 2005, Pages 1750-1758

  Piva, Roberta ^b   Gianferretti, Patrizia ^b   Ciucci, Alessandra ^b   Taulli, Riccardo ^b   Belardo, Giuseppe ^b   Santoro, M Gabriella ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

15 DEOXY DELTA12,14 PROSTAGLANDIN J2; ANTIAPOPTOTIC PROTEIN; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE; CASPASE 8; CASPASE 9; CELLULAR INHIBITOR OF APOPTOSIS PROTEIN 1; CELLULAR INHIBITOR OF APOPTOSIS PROTEIN 2; CYCLOPENTENONE DERIVATIVE; FLICE INHIBITORY PROTEIN; GENE PRODUCT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NUCLEAR FACTOR KAPPA BETA P65; P65 PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEASOME INHIBITOR; PROTEIN; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; B LYMPHOCYTE; BURKITT LYMPHOMA; CANCER CELL; CARCINOGENESIS; CELL SURVIVAL; CONTROLLED STUDY; DNA BINDING; DOWN REGULATION; DRUG EFFECT; ENZYME ACTIVATION; ENZYME ACTIVITY; FLOW CYTOMETRY; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; INFLAMMATION; LENTIVIRINAE; MULTIPLE MYELOMA; PRIORITY JOURNAL; REGULATORY MECHANISM; RNA INTERFERENCE;

EID: 13544263219     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2004-04-1360     Document Type: Article

References (70)

1. Straus DS, Glass CK. Cyclopentenone prostaglandins: new insights on biological activities and cellular targets. Med Res Rev. 2001;21:185-210.
2. Gilroy DW, Colville-Nash PR, Willis D, Chivers J, Paul-Clark MJ, Willoughby DA. Inducible cyclooxygenase may have anti-inflammatory properties. Nat Med. 1999;5:698-701.
3. Santoro MG. Antiviral activity of cyclopentenone prostanoids. Trends Microbiol. 1997;5:276-281.
4. Santoro MG, Benedetto A, Jaffe BM. Prostaglandin A1 induces differentiation in Friend erythroleukemia cells. Prostaglandins. 1979;17:719-727.
5. Santoro MG, Crisari A, Benedetto A, Amici C. Modulation of the growth of a human erythroleukemic cell line (K562) by prostaglandins: antiproliferative action of prostaglandin A. Cancer Res. 1986;46:6073-6077.
6. Clay CE, Namen AM, Atsumi G, et al. Influence of J series prostaglandins on apoptosis and tumorigenesis of breast cancer cells. Carcinogenesis. 1999;20:1905-1911.
7. Butler R, Mitchell SH, Tindall DJ, Young CY. Non-apoptotic cell death associated with S-phase arrest of prostate cancer cells via the peroxisome proliferator-activated receptor gamma ligand, 15-deoxy-delta12,14-prostaglandin J2. Cell Growth Differ. 2000;11:49-61.
8. Shimada T, Kojima K, Yoshiura K, Hiraishi H, Terano A. Characteristics of the peroxisome proliferator activated receptor gamma (PPARgamma) ligand induced apoptosis in colon cancer cells. Gut. 2002;50:658-664.
9. Tsubouchi Y, Sano H, Kawahito Y, et al. Inhibition of human lung cancer cell growth by the peroxisome proliferator-activated receptor-gamma agonists through induction of apoptosis. Biochem Biophys Res Commun. 2000;270:400-405.
10. Zander T, Kraus JA, Grammes C, et al. Induction of apoptosis in human and rat glioma by agonists of the nuclear receptor PPARgamma. J Neurochem. 2002;81:1052-1060.
11. Liu JD, Lin SY, Ho YS, et al. Involvement of c-jun N-terminal kinase activation in 15-deoxy-delta12,14-prostaglandin J2-and prostaglandin A1-induced apoptosis in AGS gastric epithelial cells. Mol Carcinog. 2003;37:16-24.
12. Mossner R, Schulz U, Kruger U, et al. Agonists of peroxisome proliferator-activated receptor gamma inhibit cell growth in malignant melanoma. J Invest Dermatol. 2002;119:576-582.
13. Laurora S, Pizzimenti S, Briatore F, et al. Peroxisome proliferator-activated receptor ligands affect growth- related gene expression in human leukemic cells. J Pharmacol Exp Ther. 2003;305:932-942.
14. Padilla J, Leung E, Phipps RP. Human B lymphocytes and B lymphomas express PPAR-gamma and are killed by PPAR-gamma agonists. Clin Immunol. 2002;103:22-33.
15. Nencioni A, Lauber K, Grunebach F, et al. Cyclopentenone prostaglandins induce lymphocyte apoptosis by activating the mitochondrial apoptosis pathway independent of external death receptor signaling. J Immunol. 2003;171:5148-5156.
16. Kliewer SA, Lenhard JM, Willson TM, Patel I, Morris DC, Lehmann JM. A prostaglandin J2 metabolite binds peroxisome proliferator-activated receptor gamma and promotes adipocyte differentiation. Cell. 1995;83:813-819.
17. Boyault S, Simonin MA, Bianchi A, et al. 15-Deoxy-delta12,14-PGJ2, but not troglitazone, modulates IL-1beta effects in human chondrocytes by inhibiting NF-kappaB and AP-1 activation pathways. FEBS Lett. 2001;501:24-30.
18. Ward C, Dransfield I, Murray J, Farrow SN, Haslett C, Rossi AG. Prostaglandin D2 and its metabolites induce caspase-dependent granulocyte apoptosis that is mediated via inhibition of I kappa B alpha degradation using a peroxisome proliferator-activated receptor-gamma-independent mechanism. J Immunol. 2002;168:6232-6243.
19. Rossi A, Kapahi P, Natoli G, et al. Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IkappaB kinase. Nature. 2000;403:103-108.
20. Li Q, Verma IM. NF-kappaB regulation in the immune system. Nat Rev Immunol. 2002;2:725-734.
21. Karin M, Lin A. NF-kappaB at the crossroads of life and death. Nat Immunol. 2002;3:221-227.
22. Santoro MG, Rossi A, Amici C. NF-kappaB and virus infection: who controls whom. Embo J. 2003;22:2552-2560.
23. Karin M, Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu Rev Immunol. 2000;18:621-663.
24. Karin M, Cao Y, Greten FR, Li ZW. NF-kappaB in cancer: from innocent bystander to major culprit. Nat Rev Cancer. 2002;2:301-310.
25. Guttridge DC, Albanese C, Reuther JY, Pestell RG, Baldwin AS Jr. NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol Cell Biol. 1999;19:5785-5799.
26. Duyao MP, Kessler DJ, Spicer DB, et al. Transactivation of the c-myc promoter by human T cell leukemia virus type 1 tax is mediated by NF kappa B. J Biol Chem. 1992;267:16288-16291.
27. Rayet B, Gelinas C. Aberrant rel/nfkb genes and activity in human cancer. Oncogene. 1999;18:6938-6947.
28. Baldwin AS Jr. Series introduction: the transcription factor NF-kappaB and human disease. J Clin Invest. 2001;107:3-6.
29. Bargou RC, Emmerich F, Krappmann D, et al. Constitutive nuclear factor-kappaB-RelA activation is required for proliferation and survival of Hodgkin's disease tumor cells. J Clin Invest. 1997;100:2961-2969.
30. Pham LV, Tamayo AT, Yoshimura LC, et al. A CD40 signalosome anchored in lipid rafts leads to constitutive activation of NF-kappaB and autonomous cell growth in B cell lymphomas. Immunity. 2002;16:37-50.
31. Davis RE, Brown KD, Siebenlist U, Staudt LM. Constitutive nuclear factor kappaB activity is required for survival of activated B cell-like diffuse large B cell lymphoma cells. J Exp Med. 2001;194:1861-1874.
32. Ni H, Ergin M, Huang Q, et al. Analysis of expression of nuclear factor kappa B (NF-kappa B) in multiple myeloma: downregulation of NF-kappa B induces apoptosis. Br J Haematol. 2001;115:279-286.
33. Orlowski RZ, Eswara JR, Lafond-Walker A, Grever MR, Orlowski M, Dang CV. Tumor growth inhibition induced in a murine model of human Burkitt's lymphoma by a proteasome inhibitor. Cancer Res. 1998;58:4342-4348.
34. Tiscornia G, Tergaonkar V, Galimi F, Verma IM. CRE recombinase-inducible RNA interference mediated by lentiviral vectors. Proc Natl Acad Sci U S A. 2004;101:7347-7351.
35. Zabel U, Schreck R, Baeuerle PA. DNA binding of purified transcription factor NF-kappa B: affinity, specificity, Zn2+ dependence, and differential half-site recognition. J Biol Chem. 1991;266:252-260.
36. Mosser DD, Theodorakis NG, Morimoto RI. Coordinate changes in heat shock element-binding activity and HSP70 gene transcription rates in human cells. Mol Cell Biol. 1988;8:4736-4744.
37. DiDonato JA, Hayakawa M, Rothwarf DM, Zandi E, Karin M. A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB. Nature. 1997;388:548-554.
38. Ghosh S, May MJ, Kopp EB. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol. 1998;16:225-260.
39. Rossi A, Elia G, Santoro MG. Inhibition of nuclear factor kappa B by prostaglandin A1: an effect associated with heat shock transcription factor activation. Proc Natl Acad Sci U S A. 1997;94:746-750.
40. Straus DS, Pascual G, Li M, et al. 15-deoxy-delta 12,14-prostaglandin J2 inhibits multiple steps in the NF-kappa B signaling pathway. Proc Natl Acad Sci USA. 2000;97:4844-4849.
41. Amici C, Belardo G, Rossi A, Santoro MG. Activation of I kappa B kinase by herpes simplex virus type 1: a novel target for anti-herpetic therapy. J Biol Chem. 2001;276:28759-28766.
42. Rovin BH, Lu L, Cosio A. Cyclopentenone prostaglandins inhibit cytokine-induced NF-kappaB activation and chemokine production by human mesangial cells. J Am Soc Nephrol. 2001;12:1659-1667.
43. Rossi A, Elia G, Santoro MG. 2-Cyclopenten-1-one, a new inducer of heat shock protein 70 with antiviral activity. J Biol Chem. 1996;271:32192-32196.
44. Mitsiades N, Mitsiades CS, Poulaki V, et al. Biologic sequelae of nuclear factor-kappaB blockade in multiple myeloma: therapeutic applications. Blood. 2002;99:4079-4086.
45. Chen Y, Morrow JD, Roberts LJ II. Formation of reactive cyclopentenone compounds in vivo as products of the isoprostane pathway. J Biol Chem. 1999;274:10863-10868.
46. Roberts LJ II, Morrow JD. Products of the isoprostane pathway: unique bioactive compounds and markers of lipid peroxidation. Cell Mol Life Sci. 2002;59:808-820.
47. Beg AA, Sha WC, Bronson RT, Ghosh S, Baltimore D. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappa B. Nature. 1995;376:167-170.
48. Kessler DJ, Spicer DB, La Rosa FA, Sonenshein GE. A novel NF-kappa B element within exon 1 of the murine c-mycgene. Oncogene. 1992;7:2447-2453.
49. La Rosa FA, Pierce JW, Sonenshein GE. Differential regulation of the c-myc oncogene promoter by the NF-kappa B rel family of transcription factors. Mol Cell Biol. 1994;14:1039-1044.
50. Kanda K, Hu HM, Zhang L, Grandchamps J, Boxer LM. NF-kappa B activity is required for the deregulation of c-myc expression by the immunoglobulin heavy chain enhancer. J Biol Chem. 2000;275:32338-32346.
51. Feinman R, Koury J, Thames M, Barlogie B, Epstein J, Siegel DS. Role of NF-kappaB in the rescue of multiple myeloma cells from glucocorticoid-induced apoptosis by bcl-2. Blood. 1999;93:3044-3052.
52. Hideshima T, Richardson P, Chauhan D, et al. The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells. Cancer Res. 2001;61:3071-3076.
53. Hideshima T, Chauhan D, Richardson P, et al. NF-kappa B as a therapeutic target in multiple myeloma. J Biol Chem. 2002;277:16639-16647.
54. Bharti AC, Donato N, Singh S, Aggarwal BB. Curcumin (diferuloylmethane) down-regulates the constitutive activation of nuclear factor-kappa B and IkappaBalpha kinase in human multiple myeloma cells, leading to suppression of proliferation and induction of apoptosis. Blood. 2003;101:1053-1062.
55. Padilla J, Kaur K, Cao HJ, Smith TJ, Phipps RP. Peroxisome proliferator activator receptor-gamma agonists and 15-deoxy-Delta(12,14)(12,14)-PGJ(2) induce apoptosis in normal and malignant B-lineage cells. J Immunol. 2000;165:6941-6948.
56. Clay CE, Monjazeb A, Thorburn J, Chilton FH, High KP. 15-Deoxy-delta12,14-prostaglandin J2-induced apoptosis does not require PPARgamma in breast cancer cells. J Lipid Res. 2002;43:1818-1828.
57. Nikitakis NG, Siavash H, Hebert C, Reynolds MA, Hamburger AW, Sauk JJ. 15-PGJ2, but not thiazolidinediones, inhibits cell growth, induces apoptosis, and causes downregulation of Stat3 in human oral SCCa cells. Br J Cancer. 2002;87:1396-1403.
58. Nencioni A, Lauber K, Grunebach F, et al. Cyclopentenone prostaglandins induce caspase activation and apoptosis in dendritic cells by a PPAR-gamma-independent mechanism: regulation by inflammatory and T cell-derived stimuli. Exp Hematol. 2002;30:1020-1028.
59. Mitsiades N, Mitsiades CS, Poulaki V, et al. Molecular sequelae of proteasome inhibition in human multiple myeloma cells. Proc Natl Acad Sci U S A. 2002;99:14374-14379.
60. Hideshima T, Mitsiades C, Akiyama M, et al. Molecular mechanisms mediating antimyeloma activity of proteasome inhibitor PS-341. Blood. 2003;101:1530-1534.
61. Hideshima T, Richardson P, Anderson KC. Novel therapeutic approaches for multiple myeloma. Immunol Rev. 2003;194:164-176.
62. Cherney BW, Bhatia KG, Sgadari C, et al. Role of the p53 tumor suppressor gene in the tumorigenicity of Burkitt's lymphoma cells. Cancer Res. 1997;57:2508-2515.
63. Liu Q, Hilsenbeck S, Gazitt Y. Arsenic trioxide-induced apoptosis in myeloma cells: p53-dependent G1 or G2/M cell cycle arrest, activation of caspase-8 or caspase-9, and synergy with APO2/TRAIL. Blood. 2003;101:4078-4087.
64. Lee JH, Kim HS, Jeong SY, Kim IK. Induction of p53 and apoptosis by delta 12-PGJ2 in human hepatocarcinoma SK-HEP-1 cells. FEBS Lett. 1995;368:348-352.
65. Ohtani-Fujita N, Minami S, Mimaki S, Dao S, Sakai T. p53-Independent activation of the gadd45 promoter by Delta12-prostaglandin J2. Biochem Biophys Res Commun. 1998;251:648-652.
66. Donato NJ, Wu JY, Zhang L, Kantarjian H, Talpaz M. Down-regulation of interleukin-3/granulocyte-macrophage colony-stimulating factor receptor beta-chain in BCR-ABL(+) human leukemic cells: association with loss of cytokine-mediated Stat-5 activation and protection from apoptosis after BCR-ABL inhibition. Blood. 2001;97:2846-2853.
67. Shaulian E, Karin M. AP-1 as a regulator of cell life and death. Nat Cell Biol. 2002;4:E131-E136.
68. Vivanco I, Sawyers CL. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat Rev Cancer. 2002;2:489-501.
69. Shield MJ. Novel applications of misoprostol. Pharmacol Ther. 1995;65:125-147.
70. Vane J, O'Grady J. Therapeutic applications of prostaglandins. Sevenoaks, United Kingdom: Edward Arnold, Hodder Stroughton Publishers; 1993.