Induction of endoplasmic reticulum stress response by TZD18, a novel dual ligand for peroxisome proliferator-activated receptor α/γ, in human breast cancer cells

Molecular Cancer Therapeutics

Volumn 8, Issue 8, 2009, Pages 2296-2307

  Zang, Chuanbing ^a   Liu, Hongyu ^a   Bertz, Janina ^a   Possinger, Kurt ^a   Koeffler, H Phillip ^b   Elstner, Elena ^a   Eucker, Jan ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2,4 THIAZOLIDINEDIONE DERIVATIVE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ACTIVATING TRANSCRIPTION FACTOR 4; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CASPASE 3; CASPASE 8; CASPASE 9; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN BAK; PROTEIN BAX; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; TZD 18; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER INHIBITION; CELL DEATH; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BREAST NEOPLASMS; CELL LINE, TUMOR; ENDOPLASMIC RETICULUM; FEMALE; HUMANS; LIGANDS; PHENYL ETHERS; PPAR ALPHA; PPAR GAMMA; RNA, SMALL INTERFERING; THIAZOLIDINEDIONES; TRANSCRIPTION FACTOR CHOP; UP-REGULATION;

EID: 68849130149     PISSN: 15357163     EISSN: None     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-09-0347     Document Type: Article

References (50)

1. Grimaldi PA. The roles of PPARs in adipocyte differentiation. Prog Lipid Res 2001;40:269-81.
2. Picard F, Auwerx J. PPAR(γ) and glucose homeostasis. Annu Rev Nutr 2002;22:167-97.
3. Straus DS, Glass CK. Anti-inflammatory actions of PPAR ligands: new insights on cellular and molecular mechanisms. Trends Immunol 2007;28:551-8.
4. Michalik L, Desvergne B, Wahli W. Peroxisome-proliferator-activated receptors and cancers: complex stories. Nat Rev Cancer 2004;4:61-70.
5. Krishnan A, Nair SA, Pillai MR. Biology of PPAR γ in cancer: a critical review on existing lacunae. Curr Mol Med 2007;7:532-40.
6. Elstner E, Mueller C, Koshizuka K, et al. Ligands for peroxisome proliferator-activated receptorgamma and retinoic acid receptor inhibit growth and induce apoptosis of human breast cancer cells in vitro and in BNX mice. Proc Natl Acad Sci U S A 1998;95:8806-11.
7. Elstner E, Williamson EA, Zang C, et al. Novel therapeutic approach: ligands for PPARgamma and retinoid receptors induce apoptosis in bcl-2-positive human breast cancer cells. Breast Cancer Res Treat 2002;74:155-65.
8. Fenner MH, Elstner E. Peroxisome proliferator-activated receptor-γ ligands for the treatment of breast cancer. Expert Opin Investig Drugs 2005;14:557-68.
9. Kim KY, Kim SS, Cheon HG. Differential anti-proliferative actions of peroxisome proliferator-activated receptor-γ agonists in MCF-7 breast cancer cells. Biochem Pharmacol 2006;72:530-40.
10. Posch MG, Zang C, Mueller W, Lass U, Von Deimling A, Elstner E. Somatic mutations in peroxisome proliferator-activated receptor-γ are rare events in human cancer cells. Med Sci Monit 2004;10:BR250-4.
11. Suchanek KM, May FJ, Robinson JA, et al. Peroxisome proliferator- activated receptor α in the human breast cancer cell lines MCF-7 and MDA-MB-231. Mol Carcinog 2002;34:165-71.
12. Liu H, Zang C, Fenner MH, et al. Growth inhibition and apoptosis in human Philadelphia chromosome-positive lymphoblastic leukemia cell lines by treatment with the dual PPARα/γ ligand TZD18. Blood 2006;107:3683-92.
13. Bocca C, Bozzo F, Martinasso G, Canuto RA, Miglietta A. Involvement of PPARα in the growth inhibitory effect of arachidonic acid on breast cancer cells. Br J Nutr 2008:1-12.
14. Saidi SA, Holland CM, Charnock-Jones DS, Smith SK. In vitro and in vivo effects of the PPAR-α agonists fenofibrate and retinoic acid in endometrial cancer. Mol Cancer 2006;5:13.
15. Liu DC, Zang CB, Liu HY, Possinger K, Fan SG, Elstner E. A novel PPAR α/γ dual agonist inhibits cell growth and induces apoptosis in human glioblastoma T98G cells. Acta Pharmacol Sin 2004;25:1312-9.
16. Zang C, Liu H, Waechter M, et al. Dual PPAR α/γ ligand TZD18 either alone or in combination with imatinib inhibits proliferation and induces apoptosis of human CML cell lines. Cell Cycle 2006;5:2237-43.
17. Gardner OS, Shiau CW, Chen CS, Graves LM. Peroxisome proliferator- activated receptor γ-independent activation of p38 MAPK by thiazolidine-diones involves calcium/calmodulin-dependent protein kinase II and protein kinase R: correlation with endoplasmic reticulum stress. J Biol Chem 2005;280:10109-18.
18. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007;8:519-29.
19. Kim R, Emi M, Tanabe K, Murakami S. Role of the unfolded protein response in cell death. Apoptosis 2006;11:5-13.
20. Szegezdi E, Logue SE, Gorman AM, Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep 2006;7:880-5.
21. Zang C, Liu H, Posch MG, et al. Peroxisome proliferator-activated receptor γligands induce growth inhibition and apoptosis of human B lymphocytic leukemia. Leuk Res 2004;28:387-97.
22. Lin JH, Li H, Yasumura D, et al. IRE1 signaling affects cell fate during the unfolded protein response. Science 2007;318:944-9.
23. Melichar B, Konopleva M, Hu W, Melicharova K, Andreeff M, Freedman RS. Growth-inhibitory effect of a novel synthetic triterpenoid, 2-cyano-3,12- dioxoolean-1,9-dien-28-oic acid, on ovarian carcinoma cell lines not dependent on peroxisome proliferator-activated receptor-γ expression. Gynecol Oncol 2004;93:149-54.
24. Yamaguchi H, Wang HG. CHOP is involved in endoplasmic reticulum stress-induced apoptosis by enhancing DR5 expression in human carcinoma cells. J Biol Chem 2004;279:45495-502.
25. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 2001;21:1249-59.
26. Janicke RU, Sprengart ML, Wati MR, Porter AG. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem 1998;273:9357-60.
27. Jiang CC, Chen LH, Gillespie S, et al. Inhibition of MEK sensitizes human melanoma cells to endoplasmic reticulum stress-induced apoptosis. Cancer Res 2007;67:9750-61.
28. Chen CL, Lin CF, Chang WT, Huang WC, Teng CF, Lin YS. Ceramide induces p38 MAPK and JNK activation through a mechanism involving a thioredoxin- interacting protein-mediated pathway. Blood 2008;111:4365-75.
29. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001;107:881-91.
30. Lee AH, Iwakoshi NN, Glimcher LH. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 2003;23:7448-59.
31. Thuerauf DJ, Morrison L, Glembotski CC. Opposing roles for ATF6α and ATF6β in endoplasmic reticulum stress response gene induction. J Biol Chem 2004;279:21078-84.
32. Luo S, Baumeister P, Yang S, Abcouwer SF, Lee AS. Induction of Grp78/BiP by translational block: activation of the Grp78 promoter by ATF4 through and upstream ATF/CRE site independent of the endoplasmic reticulum stress elements. J Biol Chem 2003;278:37375-85.
33. Harding HP, Novoa I, Zhang Y, et al. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 2000;6:1099-108.
34. Yeh TC, Chiang PC, Li TK, et al. Genistein induces apoptosis in human hepatocellular carcinomas via interaction of endoplasmic reticulum stress and mitochondrial insult. Biochem Pharmacol 2007;73:782-92.
35. Kim SH, Hwang CI, Juhnn YS, Lee JH, Park WY, Song YS. GADD153 mediates celecoxib-induced apoptosis in cervical cancer cells. Carcinogenesis 2007;28:223-31.
36. Zinszner H, Kuroda M, Wang X, et al. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 1998;12:982-95.
37. Matsumoto M, Minami M, Takeda K, Sakao Y, Akira S. Ectopic expression of CHOP (GADD153) induces apoptosis in M1 myeloblastic leukemia cells. FEBS Lett 1996;395:143-7.
38. Kim DG, You KR, Liu MJ, Choi YK, Won YS. GADD153-mediated anticancer effects of N-(4-hydroxyphenyl)retinamide on human hepatoma cells. J Biol Chem 2002;277:38930-8.
39. Lei P, Abdelrahim M, Safe S. 1,1-Bis(3′-indolyl)-1-(p-substituted phenyl)methanes inhibit ovarian cancer cell growth through peroxisome proliferator-activated receptor-dependent and independent pathways. Mol Cancer Ther 2006;5:2324-36.
40. Sun SY, Liu X, Zou W, Yue P, Marcus AI, Khuri FR. The farnesyltransferase inhibitor lonafarnib induces CCAAT/enhancer-binding protein homologous protein-dependent expression of death receptor 5, leading to induction of apoptosis in human cancer cells. J Biol Chem 2007;282:18800-9.
41. Murakami Y, Aizu-Yokota E, Sonoda Y, Ohta S, Kasahara T. Suppression of endoplasmic reticulum stress-induced caspase activation and cell death by the overexpression of Bcl-xL or Bcl-2. J Biochem 2007;141:401-10.
42. Zong WX, Li C, Hatzivassiliou G, et al. Bax and Bakcan localize to the endoplasmic reticulum to initiate apoptosis. J Cell Biol 2003;162:59-69.
43. Takeda K, Matsuzawa A, Nishitoh H, Ichijo H. Roles of MAPKKK ASK1 in stress-induced cell death. Cell Struct Funct 2003;28:23-9.
44. Wang XZ, Ron D. Stress-induced phosphorylation and activation of the transcription factor CHOP (GADD153) by p38 MAP Kinase. Science 1996;272:1347-9.
45. Zou W, Yue P, Khuri FR, Sun SY. Coupling of endoplasmic reticulum stress to CDDO-Me-induced up-regulation of death receptor 5 via a CHOP-dependent mechanism involving JNK activation. Cancer Res 2008;68:7484-92.
46. Dhanasekaran DN, Reddy EP. JNK signaling in apoptosis. Oncogene 2008;27:6245-51.
47. Thornton TM, Rincon M. Non-classical p38 map kinase functions: cell cycle checkpoints and survival. Int J Biol Sci 2009;5:44-51.
48. Arai K, Lee SR, van Leyen K, Kurose H, Lo EH. Involvement of ERK MAP kinase in endoplasmic reticulum stress in SH-SY5Y human neuroblastoma cells. J Neurochem 2004;89:232-9.
49. Joo JH, Liao G, Collins JB, Grissom SF, Jetten AM. Farnesol-induced apoptosis in human lung carcinoma cells is coupled to the endoplasmic reticulum stress response. Cancer Res 2007;67:7929-36.
50. Mebratu Y, Tesfaigzi Y. How ERK1/2 activation controls cell proliferation and cell death is subcellular localization the answer? Cell Cycle 2009;8.