Antitumorigenic effects of peroxisome proliferator-activated receptor-γ in non-small-cell lung cancer cells are mediated by suppression of cyclooxygenase-2 via inhibition of nuclear factor-κB

Molecular Pharmacology

Volumn 73, Issue 3, 2008, Pages 709-717

  Bren Mattison, Yvette ^a,b   Meyer, Amy M ^a   Van Putten, Vicki ^a   Li, Howard ^a   Kuhn, Katherine ^a   Stearman, Robert ^a   Weiser Evans, Mary ^a   Winn, Robert A ^a   Heasley, Lynn E ^a   Nemenoff, Raphael A ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b SPORIAN MICROSYSTEMS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOOXYGENASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CARCINOGENESIS; CELL DIFFERENTIATION; DRUG INHIBITION; DRUG MECHANISM; ENZYME REPRESSION; EPITHELIUM; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADENOCARCINOMA; ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CULTURE MEDIA; CYCLOOXYGENASE 2; DINOPROSTONE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; ENZYME INHIBITORS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; HUMANS; LUCIFERASES; LUNG NEOPLASMS; MICE; MICE, MUTANT STRAINS; MICE, TRANSGENIC; NEOPLASMS, EXPERIMENTAL; NF-KAPPA B; ORGAN CULTURE TECHNIQUES; PPAR GAMMA; PROMOTER REGIONS (GENETICS); PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; SULINDAC; TRANSFECTION; TRANSGENES;

EID: 40849140987     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.107.042002     Document Type: Article

References (39)

1. Backlund MG, Mann JR, Holla VR, Buchanan FG, Tai HH, Musiek ES, Milne GL, Katkuri S, and DuBois RN (2005) 15-Hydroxyprostaglandin dehydrogenase is down-regulated in colorectal cancer. J Biol Chem 280:3217-3223.
2. Berger J and Moller DE (2002) The mechanisms of action of PPARs. Annu Rev Med 53:409-435.
3. Blaine SA, Meyer AM, Hurteau G, Wick M, Hankin JA, Murphy RC, Dannenberg AJ, Geraci MW, Subbaramaiah K, and Nemenoff RA (2005) Targeted over-expression of mPGES-1 and elevated PGE2 production is not sufficient for lung tumorigenesis in mice. Carcinogenesis 26:209-217.
4. Bren-Mattison Y, Van Putten V, Chan D, Winn R, Geraci MW, and Nemenoff RA (2005) Peroxisome proliferator-activated receptor-gamma (PPAR(gamma)) inhibits tumorigenesis by reversing the undifferentiated phenotype of metastatic non-small-cell lung cancer cells (NSCLC). Oncogene 24:1412-1422.
5. Casibang M, Purdom S, Jakowlew S, Neckers L, Zia F, Ben-Av P, Hla T, You L, Jablons DM, and Moody TW (2001) Prostaglandin E2 and vasoactive intestinal peptide increase vascular endothelial cell growth factor mRNAs in lung cancer cells. Lung Cancer 31:203-212.
6. Corti M, Brody AR, and Harrison JH (1996) Isolation and primary culture of murine alveolar type II cells. Am J Respir Cell Mol Biol 14:309-315.
7. Debnath J, Muthuswamy SK, and Brugge JS (2003) Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30:256-268.
8. Feige JN, Gelman L, Michalik L, Desvergne B, and Wahli W (2006) From molecular action to physiological outputs: peroxisome proliferator-activated receptors are nuclear receptors at the crossroads of key cellular functions. Prog Lipid Res 45:120-159.
9. Gericke A, Munson M, and Ross AH (2006) Regulation of the PTEN phosphatase. Gene 374:1-9.
10. Han S and Roman J (2006) Rosiglitazone suppresses human lung carcinoma cell growth through PPAR{gamma}-dependent and PPAR{gamma}-independent signal pathways. Mol Cancer Ther 5:430-437.
11. Hazra S, Batra RK, Tai HH, Sharma S, Cui X, and Dubinett SM (2007) Pioglitazone and rosiglitazone decrease prostaglandin E2 in non-small-cell lung cancer cells by up-regulating 15-hydroxyprostaglandin dehydrogenase. Mol Pharmacol 71:1715-1720.
12. Heasley LE, Thaler S, Nicks M, Price B, Skorecki K, and Nemenoff RA (1997) Induction of cytosolic phospholipase A2 by oncogenic Ras in human non-small cell lung cancer. J Biol Chem 272:14501-14504.
13. Hida T, Leyton J, Makheja AN, Ben-Av P, Hla T, Martinez A, Mulshine J, Malkani S, Chung P, and Moody TW (1998) Non-small cell lung cancer cyclooxygenase activity and proliferation are inhibited by non-steroidal antiinflammatory drugs. Anticancer Res 18:775-782.
14. Horio Y, Chen A, Rice P, Roth JA, Malkinson AM, and Schrump DS (1996) Ki-ras and p53 mutations are early and late events, respectively, in urethane-induced pulmonary carcinogenesis. Mol Carcinog 17:217-223.
15. Huang C and Cabot MC (1990) Phorbol diesters stimulate the accumulation of phosphatidate, phosphatidylethanol, and diacylglycerol in three cell types. J Biol Chem 265:14858-14863.
16. Inoue H, Tanabe T, and Umesono K (2000) Feedback control of cyclooxygenase-2 expression through PPAR. J Biol Chem 275:28028-28032.
17. Keith RL, Miller YE, Hoshikawa Y, Moore MD, Gesell TL, Gao B, Malkinson AM, Golpon HA, Nemenoff RA, and Geraci MW (2002) Manipulation of pulmonary prostacyclin synthase expression prevents murine lung cancer. Cancer Res 62:734-740.
18. Keshamouni VG, Arenberg DA, Reddy RC, Newstead MJ, Anthwal S, and Standiford TJ (2005) PPAR-gamma activation inhibits angiogenesis by blocking ELR+CXC chemokine production in non-small cell lung cancer. Neoplasia 7:294-301.
19. Lee G, Elwood F, McNally J, Weiszmann J, Lindstrom M, Amaral K, Nakamura M, Miao S, Cao P, Learned RM, et al. (2002) T0070907, a selective ligand for peroxisome proliferator-activated receptor γ, functions as an antagonist of biochemical and cellular activities. J Biol Chem 277:19649- 19657.
20. Lee SY, Hur GY, Jung KH, Jung HC, Lee SY, Kim JH, Shin C, Shim JJ, In KH, Kang KH, et al. (2006) PPAR-gamma agonist increase gefitinib's antitumor activity through PTEN expression. Lung Cancer 51:297-301.
21. Lincoff AM, Wolski K, Nicholls SJ, and Nissen SE (2007) Pioglitazone and risk of cardiovascular events in patients with type 2 diabetes mellitus: a meta-analysis of randomized trials. JAMA 298:1180-1188.
22. Liu CH, Chang SH, Narko K, Trifan OC, Wu MT, Smith E, Haudenschild C, Lane TF, and Hla T (2001) Overexpression of cyclooxygenase-2 is sufficient to induce tumorigenesis in transgenic mice. J Biol Chem 276:18563- 18569.
23. Madrid LV, Wang CY, Guttridge DC, Schottelius AJ, Baldwin AS Jr, and Mayo MW (2000) Akt suppresses apoptosis by stimulating the transactivation potential of the RelA/p65 subunit of NF-kappaB. Mol Cell Biol 20:1626-1638.
24. Malkinson AM (1998) Molecular comparison of human and mouse pulmonary adenocarcinomas. Exp Lung Res 24:541-555.
25. McLemore TL, Hubbard WC, Litterst CL, Lin MC, Miller S, McMahon NA, Eggleston JC, and Boyd MR (1988) Profiles of prostaglandin biosynthesis in normal lung and tumor tissue from lung cancer patients. Cancer Res 48:3140-3147.
26. Meyer AM, Dwyer-Nield LD, Hurteau GJ, Keith RL, O'Leary E, You M, Bonventre JV, Nemenoff RA, and Malkinson AM (2004) Decreased lung tumorigenesis in mice genetically deficient in cytosolic phospholipase A2. Carcinogenesis 25:1517-1524.
27. Moody TW, Leyton J, Zakowicz H, Hida T, Kang Y, Jakowlew S, You L, Ozbun L, Zia H, Youngberg J, et al. (2001) Indomethacin reduces lung adenoma number in A/J mice. Anticancer Res 21:1749-1755.
28. Patel L, Pass I, Coxon P, Downes CP, Smith SA, and Macphee CH (2001) Tumor suppressor and anti-inflammatory actions of PPARgamma agonists are mediated via upregulation of PTEN. Curr Biol 11:764-768.
29. Reddy ST, Wadleigh DJ, and Herschman HR (2000) Transcriptional regulation of the cyclooxygenase-2 gene in activated mast cells. J Biol Chem 275:3107-3113.
30. Rigas B and Kashfi K (2005) Cancer prevention: a new era beyond cyclooxygenase-2. J Pharmacol Exp Ther 314:1-8.
31. Romashkova JA and Makarov SS (1999) NF-kappaB is a target of AKT in antiapoptotic PDGF signalling. Nature 401:86-90.
32. Sasaki H, Tanahashi M, Yukiue H, Moiriyama S, Kobayashi Y, Nakashima Y, Kaji M, Kiriyama M, Fukai I, Yamakawa Y, et al. (2002) Decreased peroxisome proliferator-activated receptor gamma gene expression was correlated with poor prognosis in patients with lung cancer. Lung Cancer 36:71-76.
33. Sizemore N, Leung S, and Stark GR (1999) Activation of phosphatidylinositol 3-kinase in response to interleukin-1 leads to phosphorylation and activation of the NF-kappaB p65/RelA subunit. Mol Cell Biol 19:4798-4805.
34. Strieter RM, Belperio JA, Burdick MD, Sharma S, Dubinett SM, and Keane MP (2004) CXC chemokines: angiogenesis, immunoangiostasis, and metastases in lung cancer. Ann N Y Acad Sci 1028:351-360.
35. Teresi RE, Shaiu CW, Chen CS, Chatterjee VK, Waite KA, and Eng C (2006) Increased PTEN expression due to transcriptional activation of PPARgamma by lovastatin and rosiglitazone. Int J Cancer 118:2390-2398.
36. Theocharis S, Kanelli H, Politi E, Margeli A, Karkandaris C, Philippides T, and Koutselinis A (2002) Expression of peroxisome proliferator activated receptor-gamma in non-small cell lung carcinoma: correlation with histological type and grade. Lung Cancer 36:249-255.
37. Van Putten V, Refaat Z, Dessev C, Blaine S, Wick M, Butterfield L, Han SY, Heasley LE, and Nemenoff RA (2001) Induction of cytosolic phospholipase A2 by oncogenic ras is mediated through the JNK and ERK pathways in rat epithelial cells. J Biol Chem 276:1226-1232.
38. Wick M, Hurteau G, Dessev C, Chan D, Geraci MW, Winn RA, Heasley LE, and Nemenoff RA (2002) Peroxisome proliferator-activated receptor-γ is a target of nonsteroidal anti-inflammatory drugs mediating cyclooxygenase- independent inhibition of lung cancer cell growth. Mol Pharmacol 62:1207-1214.
39. Xie W and Herschman HR (1995) V-src induces prostaglandin synthase 2 gene expression by activation of the c-Jun N-terminal kinase and the c-Jun transcription factor. J Biol Chem 270:27622-27628.