Pioglitazone, a PPARγ agonist, inhibits growth and invasion of human hepatocellular carcinoma via blockade of the rage signaling

Molecular Carcinogenesis

Volumn 54, Issue 12, 2015, Pages 1584-1595

  Yang, Yuan ^a,b   Zhao, Ling Hao ^a   Huang, Bo ^c   Wang, Ruo Yu ^a   Yuan, Sheng Xian ^a   Tao, Qi Fei ^a   Xu, Yong ^d   Sun, Han Yong ^a   Lin, Chuan ^a   Zhou, Wei Ping ^a,b  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b National Innovation Alliance for Hepatitis and Liver Cancer   (China)

^c SUZHOU MUNICIPAL HOSPITAL   (China)

^d Shanghai Personal Biotechnology Limited Company   (China)

Author keywords

Growth; Hepatocellular carcinoma; Invasion; Pioglitazone; RAGE

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; ANTINEOPLASTIC AGENT; COLLAGEN TYPE 4; CYCLIN D1; GELATINASE A; HIGH MOBILITY GROUP B1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; KI 67 ANTIGEN; LAMININ; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIOGLITAZONE; SMALL INTERFERING RNA; 2,4 THIAZOLIDINEDIONE DERIVATIVE; MITOGEN ACTIVATED PROTEIN KINASE; MOK PROTEIN, HUMAN; TUMOR ANTIGEN;

ADULT; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CANCER SIZE; CANCER STAGING; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL GROWTH; CELL INVASION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; DRUG EFFECT; FEMALE; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LYMPH VESSEL METASTASIS; MALE; MIDDLE AGED; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TISSUE MICROARRAY; TUMOR INVASION; UPREGULATION; AGONISTS; ANTAGONISTS AND INHIBITORS; CARCINOMA, HEPATOCELLULAR; DRUG EFFECTS; HEPG2 CELL LINE; LIVER NEOPLASMS; METABOLISM; PREVENTION AND CONTROL; TUMOR CELL LINE;

ANTIGENS, NEOPLASM; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; MALE; MIDDLE AGED; MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASM INVASIVENESS; PPAR GAMMA; SIGNAL TRANSDUCTION; THIAZOLIDINEDIONES;

EID: 84944576851     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.22231     Document Type: Article

References (41)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011; 61:69-90.
2. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010; 127:2893-2917.
3. Sterenczak KA, Joetzke AE, Willenbrock S, et al. High-mobility group B1 (HMGB1) and receptor for advanced glycation end-products (RAGE) expression in canine lymphoma. Anticancer Res 2010; 30:5043-5048.
4. Sterenczak KA, Kleinschmidt S, Wefstaedt P, et al. Quantitative PCR and immunohistochemical analyses of HMGB1 and RAGE expression in canine disseminated histiocytic sarcoma (malignant histiocytosis). Anticancer Res 2011; 31:1541-1548.
5. Kang R, Tang D, Schapiro NE, et al. The receptor for advanced glycation end products (RAGE) sustains autophagy and limits apoptosis, promoting pancreatic tumor cell survival. Cell Death Differ 2010; 17:666-676.
6. Heijmans J, Büller NV, Hoff E, et al. Rage signalling promotes intestinal tumourigenesis. Oncogene 2013; 32:1202-1206.
7. DiNorcia J, Moroziewicz DN, Ippagunta N, et al. RAGE signaling significantly impacts tumorigenesis and hepatic tumor growth in murine models of colorectal carcinoma. J Gastrointest Surg 2010; 14:1680-1690.
8. Liang H, Zhong Y, Zhou S, Peng L. Knockdown of RAGE expression inhibits colorectal cancer cell invasion and suppresses angiogenesis in vitro and in vivo. Cancer Lett 2011; 313:91-98.
9. Elangovan I, Thirugnanam S, Chen A, et al. Targeting receptor for advanced glycation end products (RAGE) expression induces apoptosis and inhibits prostate tumor growth. Biochem Biophys Res Commun 2012; 417:1133-1138.
10. Knapp P, Jarzabek K, Błachnio A, Zbroch T. The role of peroxisome proliferator-activated receptors (PPAR) in carcinogenesis. Ginekol Pol 2006; 77:643-651.
11. Li H, Sorenson AL, Poczobutt J, et al. Activation of PPARγ in myeloid cells promotes lung cancer progression and metastasis. PLoS One 2011; 6:e28133.
12. Al-Taie OH, Graf T, Illert B, et al. Differential effects of PPARgamma activation by the oral antidiabetic agent pioglitazone in Barrett's carcinoma in vitro and in vivo. J Gastroenterol 2009; 44:919-929.
13. Li MY, Yuan H, Ma LT, et al. Roles of peroxisome proliferator-activated receptor-alpha and -gamma in the development of non-small cell lung cancer. Am J Respir Cell Mol Biol 2010; 43:674-683.
14. Choi IK, Kim YH, Kim JS, Seo JH. PPAR-gamma ligand promotes the growth of APC-mutated HT-29 human colon cancer cells in vitro and in vivo. Invest New Drugs 2008; 26:283-288.
15. Grommes C, Landreth GE, Sastre M, et al. Inhibition of in vivo glioma growth and invasion by peroxisome proliferator-activated receptor gamma agonist treatment. Mol Pharmacol 2006; 70:1524-1533.
16. Shigeto T, Yokoyama Y, Xin B, Mizunuma H. Peroxisome proliferator-activated receptor alpha and gamma ligands inhibit the growth of human ovarian cancer. Oncol Rep 2007; 18:833-840.
17. Takano S, Kubota T, Nishibori H, et al. Pioglitazone, a ligand for peroxisome proliferator-activated receptor-gamma acts as an inhibitor of colon cancer liver metastasis. Anticancer Res 2008; 28:3593-3599.
18. Grommes C, Conway DS, Alshekhlee A, Barnholtz-Sloan JS. Inverse association of PPARγ agonists use and high grade glioma development. J Neurooncol 2010; 100:233-239.
19. Jiao L, Taylor PR, Weinstein SJ, et al. Advanced glycation end products, soluble receptor for advanced glycation end products, and risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev 2011; 20:1430-1438.
20. Jiao L, Weinstein SJ, Albanes D, et al. Evidence that serum levels of the soluble receptor for advanced glycation end products are inversely associated with pancreatic cancer risk: A prospective study. Cancer Res 2011; 71:3582-3589.
21. Bartling B, Hofmann HS, Sohst A, et al. Prognostic potential and tumor growth-inhibiting effect of plasma advanced glycation end products in non-small cell lung carcinoma. Mol Med 2011; 17:980-989.
22. Takino J, Yamagishi S, Takeuchi M. Glycer-AGEs-RAGE signaling enhances the angiogenic potential of hepatocellular carcinoma by upregulating VEGF expression. World J Gastroenterol 2012; 18:1781-1788.
23. Mizumoto S, Takahashi J, Sugahara K. Receptor for advanced glycation end products (RAGE) functions as receptor for specific sulfated glycosaminoglycans, and anti-RAGE antibody or sulfated glycosaminoglycans delivered in vivo inhibit pulmonary metastasis of tumor cells. J Biol Chem 2012; 287:18985-18994.
24. Yaser AM, Huang Y, Zhou RR, et al. The Role of Receptor for Advanced Glycation End Products (RAGE) in the proliferation of hepatocellular carcinoma. Int J Mol Sci 2012; 13:5982-5997.
25. Cha HJ, Kim J, Hong SM, et al. Overexpression of renal tumor antigen is associated with tumor invasion and poor prognosis of hepatocellular carcinoma. Ann Surg Oncol 2012; 19(Suppl 3):S404-S411.
26. Ueno T, Teraoka N, Takasu S, et al. Suppressive effect of pioglitazone, a PPARgamma ligand, on azoxymethane-induced colon aberrant crypt foci in KK-Ay Mice. Asian Pac J Cancer Prev 2012; 13:4067-4073.
27. Dobson ME, Diallo-Krou E, Grachtchouk V, et al. Pioglitazone induces a proadipogenic antitumor response in mice with PAX8-PPARgamma fusion protein thyroid carcinoma. Endocrinology 2011; 152:4455-4465.
28. Li MY, Kong AW, Yuan H, et al. Pioglitazone prevents smoking carcinogen-induced lung tumor development in mice. Curr Cancer Drug Targets 2012; 12:597-606.
29. Shim J, Kim BH, Kim YI, et al. The peroxisome proliferator-activated receptor gamma ligands, pioglitazone and 15-deoxy-Delta(12, 14)-prostaglandin J(2), have antineoplastic effects against hepatitis B virus-associated hepatocellular carcinoma cells. Int J Oncol 2010; 36:223-231.
30. Motomura W, Takahashi N, Nagamine M, et al. Growth arrest by troglitazone is mediated by p27Kip1 accumulation, which results from dual inhibition of proteasome activity and Skp2 expression in human hepatocellular carcinoma cells. Int J Cancer 2004; 108:41-46.
31. Rumi MA, Sato H, Ishihara S, et al. Peroxisome proliferator-activated receptor gamma ligand-induced growth inhibition of human hepatocellular carcinoma. Br J Cancer 2001; 84:1640-1647.
32. Al-Alem L, Southard RC, Kilgore MW, Curry TE. Specific thiazolidinediones inhibit ovarian cancer cell line proliferation and cause cell cycle arrest in a PPARγ independent manner. PLoS ONE 2011; 6:e16179.
33. Nemenoff R. Activation of PPARγ in myeloid cells promotes lung cancer progression and metastasis. Oncoimmunology 2012; 1:403-404.
34. Yoshizawa K, Cioca DP, Kawa S, et al. Peroxisome proliferator-activated receptor gamma ligand troglitazone induces cell cycle arrest and apoptosis of hepatocellular carcinoma cell lines. Cancer 2002; 95:2243-2251.
35. Wang G, Han D, Zhang Y, et al. A novel hypothesis: Up-regulation of HO-1 by activation of PPARγ inhibits HMGB1-RAGE signaling pathway and ameliorates the development of ALI/ARDS. J Thorac Dis 2013; 5:706-710.
36. Choi J, Lee MK, Oh KH, et al. Interaction effect between the receptor for advanced glycation end products (RAGE) and high-mobility group box-1 (HMGB-1) for the migration of a squamous cell carcinoma cell line. Tumori 2011; 97:196-202.
37. Lin L, Zhong K, Sun Z, Wu G, Ding G. Receptor for advanced glycation end products (RAGE) partially mediates HMGB1-ERKs activation in clear cell renal cell carcinoma. J Cancer Res Clin Oncol 2012; 138:11-22.
38. He Q, You H, Li XM, Liu TH, Wang P, Wang BE. HMGB1 promotes the synthesis of pro-IL-1β and pro-IL-18 by activation of p38 MAPK and NF-κB through receptors for advanced glycation end-products in macrophages. Asian Pac J Cancer Prev 2012; 13:1365-1370.
39. Chen RC, Yi PP, Zhou RR, et al. The role of HMGB1-RAGE axis in migration and invasion of hepatocellular carcinoma cell lines. Mol Cell Biochem 2014; 390:271-280.
40. Ueda J, Kajita M, Suenaga N, Fujii K, Seiki M. Sequence-specific silencing of MT1-MMP expression suppresses tumor cell migration and invasion: Importance of MT1-MMP as a therapeutic target for invasive tumors. Oncogene 2003; 22:8716-8722.
41. Zhang J, Zhu JS, Zhou Z, Chen WX, Chen NW. Inhibitory effects of ethyl pyruvate administration on human gastric cancer growth via regulation of the HMGB1-RAGE and Akt pathways in vitro and in vivo. Oncol Rep 2012; 27:1511-1519.