Activation of PPARγ is required for curcumin to induce apoptosis and to inhibit the expression of extracellular matrix genes in hepatic stellate cells in vitro

Biochemical Journal

Volumn 384, Issue 1, 2004, Pages 149-157

  Zheng, Shizhong ^a,b   Chen, Anping ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b NANJING MEDICAL UNIVERSITY   (China)

Author keywords

Apoptosis; Extracellular matrix; Hepatic fibrosis; Hepatic stellate cell; Peroxisome proliferator activated receptor (PPAR ); Phytochemical

Indexed keywords

ACTIVATION ANALYSIS; CELLS; ENZYMES; GENES; PIGMENTS;

CELL PROLIFERATION; EXTRACELLULAR MATRIX; LIVER FIBROGENESIS;

ENZYME INHIBITION;

CURCUMIN; PD 68235; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; UNCLASSIFIED DRUG; CYCLIN D1; ENZYME INHIBITOR; NITRO DERIVATIVE; PD 068235; TGFB1 PROTEIN, RAT; THIAZOLE DERIVATIVE; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL PROLIFERATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FIBROGENESIS; GENE EXPRESSION; GENE EXPRESSION REGULATION; LIVER CELL; LIVER FIBROSIS; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; STELLATE CELL; ANIMAL; CHEMISTRY; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; FLOW CYTOMETRY; GENETICS; LIVER; METABOLISM; METHODOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALIA;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; CURCUMIN; CYCLIN D1; ENZYME INHIBITORS; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; LIVER; MALE; NITRO COMPOUNDS; PPAR GAMMA; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; THIAZOLES; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

EID: 9444252295     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20040928     Document Type: Article

References (54)

1. Friedman, S. L. (2000) Molecular regulation of hepatic fibrosis, an integrated cellular response to tissue injury. J. Biol. Chem. 275, 2247-2250
2. Schuppan, D., Atkinson, J., Ruehl, M. and Riecken, E. O. (1995) Alcohol and liver fibrosis - pathobiochemistry and treatment. Z. Gastroenterol. 33, 546-550
3. Dooley, S., Delvoux, B., Lahme, B., Mangasser-Stephan, K. and Gressner, A. M. (2000) Modulation of transforming growth factor beta response and signaling during transdifferentiation of rat hepatic stellate cells to myofibroblasts. Hepatology 31, 1094-1106
4. Friedman, S. L., Yamasaki, G. and Wong, L. (1994) Modulation of transforming growth factor beta receptors of rat lipocytes during the hepatic wound healing response. Enhanced binding and reduced gene expression accompany cellular activation in culture and in vivo. J. Biol. Chem. 269, 10551-10558
5. Chen, A. (2002) Acetaldehyde stimulates the activation of latent transforming growth factor-beta1 and induces expression of the type II receptor of the cytokine in rat cultured hepatic stellate cells. Biochem. J. 368, 683-693
6. Nakamura, T., Sakata, R., Ueno, T., Sata, M. and Ueno, H. (2000) Inhibition of transforming growth factor beta prevents progression of liver fibrosis and enhances hepatocyte regeneration in dimethylnitrosamine-treated rats. Hepatology 32, 247-255
7. Qi, Z., Atsuchi, N., Ooshima, A., Takeshita, A. and Ueno, H. (1999) Blockade of type beta transforming growth factor signaling prevents liver fibrosis and dysfunction in the rat. Proc. Natl. Acad. Sci. U.S.A. 96, 2345-2349
8. Ueno, H., Sakamoto, T., Nakamura, T., Qi, Z., Astuchi, N., Takeshita, A., Shimizu, K. and Ohashi, H. (2000) A soluble transforming growth factor beta receptor expressed in muscle prevents liver fibrogenesis and dysfunction in rats. Hum. Gene Ther. 11, 33-42
9. Iredale, J. P., Benyon, R. C., Pickering, J., McCullen, M., Northrop, M., Pawley, S., Hovell, C. and Arthur, M. J. (1998) Mechanisms of spontaneous resolution of rat liver fibrosis. Hepatic stellate cell apoptosis and reduced hepatic expression of metalloproteinase inhibitors. J. Clin. Invest. 102, 538-549
10. Houseknecht, K. L., Cole, B. M. and Steele, P. J. (2002) Peroxisome proliferator-activated receptor gamma (PPARgamma) and its ligands: a review. Dornest. Anim. Endocrinol. 22, 1-23
11. Takashima, T., Fujiwara, Y., Higuchi, K., Arakawa, T., Yano, Y., Hasuma, T. and Otani, S. (2001) PPAR-gamma ligands inhibit growth of human esophageal adenocarcinoma cells through induction of apoptosis, cell cycle arrest and reduction of ornithine decarboxylase activity. Int. J. Oncol. 19, 465-471
12. Tontonoz, P., Singer, S., Forman, B. M., Sarraf, P., Fletcher, J. A., Fletcher, C. D., Brun, R. P., Mueller, E., Altiok, S., Oppenheim, H. et al. (1997) Terminal differentiation of human liposarcoma cells induced by ligands for peroxisome proliferator-activated receptor gamma and the retinoid X receptor. Proc. Natl. Acad. Sci. U.S.A. 94, 237-241
13. Galli, A., Crabb, D., Price, D., Ceni, E., Salzano, R., Surrenti, C. and Casini, A. (2000) Peroxisome proliferator-activated receptor gamma transcriptional regulation is involved in platelet-derived growth factor-induced proliferation of human hepatic stellate cells. Hepatology 31, 101-108
14. Miyahara, T., Schrum, L., Rippe, R., Xiong, S., Yee, Jr, H. F., Motomura, K., Anania, F. A., Willson, T. M. and Tsukamoto, H. (2000) Peroxisome proliferator-activated receptors and hepatic stellate cell activation. J. Biol. Chem. 275, 35715-35722
15. Marra, F., Efsen, E., Romanelli, R. G., Caligiuri, A., Pastacaldi, S., Batignani, G., Bonacchi, A., Caporale, R., Laffi, G., Pinzani, M. and Gentilini, P. (2000) Ligands of peroxisome proliferator-activated receptor gamma modulate profibrogenic and proinflammatory actions in hepatic stellate cells. Gastroenterology 119, 466-478
16. Galli, A., Crabb, D. W., Ceni, E., Salzano, R., Mello, T., Svegliati-Baroni, G., Ridolfi, F., Trozzi, L., Surrenti, C. and Casini, A. (2002) Antidiabetic thiazolidinediones inhibit collagen synthesis and hepatic stellate cell activation in vivo and in vitro. Gastroenterology 122, 1924-1940
17. Hazra, S., Xiong, S., Wang, J., Rippe, R., Chatterjee, V. K. and Tsukamoto, H. (2003) PPARgamma induces a phenotypic switch from activated to quiescent hepatic stellate cells. J. Biol. Chem. 279, 11392-11401
18. Ruby, A. J., Kuttan, G., Babu, K. D., Rajasekharan, K. N. and Kuttan, R. (1995) Anti-tumour and antioxidant activity of natural curcuminoids. Cancer Lett. 94, 79-83
19. Sreejayan, R. M. N. (1994) Curcuminoids as potent inhibitors of lipid peroxidation. J. Pharm. Pharmacol. 46, 1013-1016
20. Brouet, I. and Ohshima, H. (1995) Curcumin, an anti-tumour promoter and anti-inflammatory agent, inhibits induction of nitric oxide synthase in activated macrophages. Biochem. Biophys. Res. Commun. 206, 533-540
21. Joe, B. and Lokesh, B. R. (1994) Role of capsaicin, curcumin and dietary n-3 fatty acids in lowering the generation of reactive oxygen species in rat peritoneal macrophages. Biochim. Biophys. Acta 1224, 255-263
22. Liu, J. Y., Lin, S. J. and Lin, J. K. (1993) Inhibitory effects of curcumin on protein kinase C activity induced by 12-O-tetradecanoyl-phorbol-13- acetate in NIH 3T3 cells. Carcinogenesis 14, 857-861
23. Singh, S. and Aggarwal, B. B. (1995) Activation of transcription factor NF-kappa B is suppressed by curcumin (diferuloylmethane). J. Biol. Chem. 270, 24995-25000
24. Chuang, S. E., Cheng, A. L., Lin, J. K. and Kuo, M. L. (2000) Inhibition by curcumin of diethylnitrosamine-induced hepatic hyperplasia, inflammation, cellular gene products and cell-cycle-related proteins in rats. Food Chem. Toxicol. 38, 991-995
25. Xu, J., Fu, Y. and Chen, A. (2003) Activation of peroxisome proliferator-activated receptor-gamma contributes to the inhibitory effects of curcumin on rat hepatic stellate cell growth. Am. J. Physiol. Gastrointest. Liver Physiol. 285, G20-G30
26. Chen, A., Beno, D. W. A. and Davis, B. H. (1996) Suppression of stellate cell type I collagen gene expression involves AP-2 transmodulation of nuclear factor-1-dependent gene transcription. J. Biol. Chem. 271, 25994-25998
27. Camp, H. S., Chaudhry, A. and Leff, T. (2001) A novel potent antagonist of peroxisome proliferator-activated receptor gamma blocks adipocyte differentiation but does not revert the phenotype of terminally differentiated adipocytes. Endocrinology 142, 3207-3213
28. Schmittgen, T. D., Zakrajsek, B. A., Mills, A. G., Gorn, V., Singer, M. J. and Reed, M. W. (2000) Quantitative reverse transcription-polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Anal. Biochem. 285, 194-204
29. Ji, C., Casinghino, S., McCarthy, T. L. and Centrella, M. (1996) Cloning, characterization, and expression of the transforming growth factor-beta type I receptor promoter in fetal rat bone cells. J. Cell. Biochem. 63, 478-490
30. Bae, H. W., Geiser, A. G., Kim, D. H., Chung, M. T., Burmester, J. K., Sporn, M. B., Roberts, A. B. and Kim, S. J. (1995) Characterization of the promoter region of the human transforming growth factor-beta type II receptor gene. J. Biol. Chem. 270, 29460-29468
31. Wang, C., Pattabiraman, N., Zhou, J. N., Fu, M., Sakamaki, T., Albanese, C., Li, Z., Wu, K., Hulit, J., Neumeister, P. et al. (2003) Cyclin D1 repression of peroxisome proliferator-activated receptor gamma expression and transactivation. Mol. Cell. Biol. 23, 6159-6173
32. De Bleser, P. J., Niki, T., Rogiers, V. and Geerts, A. (1997) Transforming growth factor-beta gene expression in normal and fibrotic rat liver. J. Hepatol. 26, 886-893
33. McIntyre, T. M., Pontsler, A. V., Silva, A. R., St Hilaire, A., Xu, Y., Hinshaw, J. C., Zimmerman, G. A., Hama, K., Aoki, J., Arai, H. and Prestwich, G. D. (2003) Identification of an intracellular receptor for lysophosphatidic acid (LPA): LPA is a transcellular PPARgamma agonist. Proc. Natl. Acad. Sci. U.S.A. 100, 131-136
34. Dennis, P. A. and Rifkin, D. B. (1991) Cellular activation of latent transforming growth factor beta requires binding to the cation-independent mannose 6-phosphate/insulin-like growth factor type II receptor. Proc. Natl. Acad. Sci. U.S.A. 88, 580-584
35. Massague, J. and Chen, Y. G. (2000) Controlling TGF-beta signaling. Genes Dev. 14, 627-644
36. Ignotz, R. A. and Massague, J. (1986) Transforming growth factor-beta stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. J. Biol. Chem. 261, 4337-4345
37. Czaja, M. J., Weiner, F. R., Flanders, K. C., Giambrone, M. A., Wind, R., Biempica, L. and Zern, M. A. (1989) In vitro and in vivo association of transforming growth factor-beta 1 with hepatic fibrosis. J. Cell Biol. 108, 2477-2482
38. Moragoda, L., Jaszewski, R. and Majumdar, A. P. (2001) Curcumin induced modulation of cell cycle and apoptosis in gastric and colon cancer cells. Anticancer Res. 21, 873-878
39. Mukhopadhyay, A., Banerjee, S., Stafford, L. J., Xia, C., Liu, M. and Aggarwal, B. B. (2002) Curcumin-induced suppression of cell proliferation correlates with down-regulation of cyclin D1 expression and CDK4-mediated retinoblastoma protein phosphorylation. Oncogene 21, 8852-8861
40. Shishodia, S., Potdar, P., Gairola, C. G. and Aggarwal, B. B. (2003) Curcumin (diferuloylmethane) down-regulates cigarette smoke-induced NF-kappaB activation through inhibition of IkappaBalpha kinase in human lung epithelial cells: correlation with suppression of COX-2, MMP-9 and cyclin D1. Carcinogenesis 24, 1269-1279
41. Wang, C., Fu, M., D'Amico, M., Albanese, C., Zhou, J. N., Brownlee, M., Lisanti, M. P., Chatterjee, V. K., Lazar, M. A. and Pestell, R. G. (2001) Inhibition of cellular proliferation through IkappaB kinase-independent and peroxisome proliferator-activated receptor gamma-dependent repression of cyclin D1. Mol. Cell. Biol. 21, 3057-3070
42. Sarraf, P., Mueller, E., Jones, D., King, F. J., DeAngelo, D. J., Partridge, J. B., Holden, S. A., Chen, L. B., Singer, S., Fletcher, C. and Spiegelman, B. M. (1998) Differentiation and reversal of malignant changes in colon cancer through PPARgamma. Nat. Med. 4, 1046-1052
43. Sporn, M. B., Suh, N. and Mangelsdorf, D. J. (2001) Prospects for prevention and treatment of cancer with selective PPARgamma modulators (SPARMs). Trends Mol. Med. 7, 395-400
44. Chen, G. G., Lee, J. F., Wang, S. H., Chan, U. P., Ip, P. C. and Lau, W. Y. (2002) Apoptosis induced by activation of peroxisome-proliferator activated receptor-gamma is associated with Bcl-2 and NF-kappaB in human colon cancer. Life Sci. 70, 2631-2646
45. Butts, B. D., Tran, N. L. and Briehl, M. M. (2004) Identification of a functional peroxisome proliferator activated receptor response element in the 3′ untranslated region of the human bcl-2 gene. Int. J. Oncol. 24, 1305-1310
46. Paradis, V., Dargere, D., Bonvoust, F., Vidaud, M., Segarini, P. and Bedossa, P. (2002) Effects and regulation of connective tissue growth factor on hepatic stellate cells. Lab. Invest. 82, 767-774
47. Garcia-Trevijano, E. R., Iraburu, M. J., Fontana, L., Dominguez-Rosales, J. A., Auster, A., Covarrubias-Pinedo, A. and Rojkind, M. (1999) Transforming growth factor betal induces the expression of alpha1 (I) procollagen mRNA by a hydrogen peroxide-C/EBPbeta-dependent mechanism in rat hepatic stellate cells. Hepatology 29, 960-970
48. Isshiki, K., Haneda, M., Koya, D., Maeda, S., Sugimoto, T. and Kikkawa, R. (2000) Thiazolidinedione compounds ameliorate glomerular dysfunction independent of their insulin-sensitizing action in diabetic rats. Diabetes 49, 1022-1032
49. Ghosh, A. K., Bhattacharyya, S., Lakos, G., Chen, S. J., Mori, Y. and Varga, J. (2004) Disruption of transforming growth factor beta signaling and profibrotic responses in normal skin fibroblasts by peroxisome proliferator-activated receptor gamma. Arthritis Rheum. 50, 1305-1318
50. Subbaramaiah, K., Lin, D. T., Hart, J. C. and Dannenberg, A. J. (2001) Peroxisome proliferator-activated receptor gamma ligands suppress the transcriptional activation of cyclpoxygehase-2. Evidence for involvement of activator protein-1 and CREB-binding prqtein/p300. J. Biol. Chem. 276, 12440-12448
51. De Vos, P., Lefebvre, A. M., Miller, S. G., Guerre-Millo, M., Wong, K., Saladin, R., Hamann, L. G., Staels, B., Briggs, M. R. and Auwerx, J. (1996) Thiazolidinediones repress ob gene expression in rodents via activation of peroxisome proliferator-activated receptor gamma. J. Clin. Invest. 98, 1004-1009
52. Schihner, S., Dellas, C., Schröder, M., Heinlein, C. A., Chang, C., Fischer, J. and Knepel, W. (2002) Repression of glucagon gene transcription by peroxisome proliferator-activated receptor gamma through inhibition of Pax6 transcriptional activity. J. Biol. Chem. 277, 1941-1948
53. Fu, M., Zhang, J., Zhu, X., Myles, D. E., Willson, T. M., Liu, X. and Chen, Y. E. (2001) Peroxisome proliferator-activated receptor gamma inhibits transforming growth factor beta-induced connective tissue growth factor expression in human aortic smooth muscle cells by interfering with Smad3. J. Biol. Chem. 276, 45888-45894
54. Fu, M., Zhang, J., Lin, Y., Zhu, X., Zhao, L., Ahmad, M., Ehrengruber, M. U. and Chen, Y. E. (2003) Early stimulation and late inhibition of peroxisome proliferator-activated receptor gamma (PPAR gamma) gene expression by transforming growth factor beta in human aortic smooth muscle cells: role of early growth-response factor-1 (Egr-1), activator protein 1 (AP1) and Smads. Biochem. J. 370, 1019-1025