Activation of PPARγ by curcumin inhibits Moser cell growth and mediates suppression of gene expression of cyclin D1 and EGFR

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 288, Issue 3 51-3, 2005, Pages

  Chen, Anping ^a   Xu, Jianye ^a  

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

Author keywords

Chemoprevention; Colon cancer; Gene expression; Phytochemicals; Receptors

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CURCUMIN; CYCLIN D1; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PD 68235; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA ANTAGONIST; RECEPTOR BLOCKING AGENT; SP 650012; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CELL DIFFERENTIATION; CELL GROWTH; COLORECTAL CANCER; DOSE RESPONSE; DRUG MECHANISM; GENE EXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TRANSACTIVATION;

ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL PROLIFERATION; COLONIC NEOPLASMS; CURCUMIN; CYCLIN D1; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION; HUMANS; IMMUNOPRECIPITATION; JNK MITOGEN-ACTIVATED PROTEIN KINASES; L-LACTATE DEHYDROGENASE; PHOSPHORYLATION; PLASMIDS; PPAR GAMMA; RECEPTOR, EPIDERMAL GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; TRANSFECTION; TYROSINE;

EID: 13844306722     PISSN: 01931857     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpgi.00209.2004     Document Type: Article

References (63)

1. Aggarwal BB, Kumar A, and Bharti AC. Anticancer potential of curcumin: preclinical and clinical studies. Anticancer Res 23: 363-398, 2003.
2. Ammon HP and Wahl MA. Pharmacology of Curcuma longa. Planta Med 57: 1-7, 1991.
3. Arteaga CL. Epidermal growth factor receptor dependence in human tumors: more than just expression? Oncologist 7, Suppl 4: 31-39, 2002.
4. Auwerx J. PPARγ the ultimate thrifty gene. Diabetologia 42: 1033-1049, 1999.
5. Bogazzi F, Ultimieri F, Raggi F, Russo D, Vanacore R, Guida C, Brogioni S, Cosci C, Gasperi M, Bartalena L, and Martino E. Growth hormone inhibits apoptosis in human colonic cancer cell lines: antagonistic effects of peroxisome proliferator activated receptor-γ ligands. Endocrinology 145: 3353-3362, 2004.
6. Brockman JA, Gupta RA, and Dubois RN. Activation of PPARγ leads to inhibition of anchorage-independent growth of human colorectal cancer cells. Gastroenterology 115: 1049-1055, 1998.
7. Camp HS, Chaudhry A, and Leff T. A novel potent antagonist of peroxisome proliferator-activated receptor-γ blocks adipocyte differentiation but does not revert the phenotype of terminally differentiated adipocytes. Endocrinology 142: 3207-3213, 2001.
8. Camp HS and Tafuri SR. Regulation of peroxisome proliferator-activated receptor-γ activity by mitogen-activated protein kinase. J Biol Chem 272: 10811-10816, 1997.
9. Camp HS, Tafuri SR, and Leff T. c-Jun N-terminal kinase phosphorylates peroxisome proliferator-activated receptor-γ1 and negatively regulates its transcriptional activity. Endocrinology 140: 392-397, 1999.
10. Chauhan DP. Chemotherapeutic potential of curcumin for colorectal cancer. Curr Pharm Des 8: 1695-1706, 2002.
11. Chen A and Davis BH. UV irradiation activates JNK and increases αI(I)-collagen gene expression in rat hepatic stellate cells. J Biol Chem 274: 158-164, 1999.
12. Chen A and Davis BH. The DNA binding protein BTEB mediates acetaldehyde-induced, jun N-terminal kinase-dependent αI(I)-collagen gene expression in rat hepatic stellate cells. Mol Cell Biol 20: 2818-2826, 2000.
13. 3 stimulates activator protein-1-dependent Caco-2 cell differentiation. J Biol Chem 274: 35505-35513, 1999.
14. Chen A, Zhang L, Xu J, and Tang Jun. The antioxidant (-)- epigallocatechin-3-gallate inhibits activated hepatic stellate cell growth and suppresses acetaldehyde-induced gene expression. Biochem J 368: 695-704, 2002.
15. Chen H, Zhang ZS, Zhang YL, and Zhou DY. Curcumin inhibits cell proliferation by interfering with the cell cycle and inducing apoptosis in colon carcinoma cells. Anticancer Res 19: 3675-3680, 1999.
16. Chen YR and Tan TH. Inhibition of-the c-Jun N-terminal kinase (JNK) signaling pathway by curcumin. Oncogens 17: 173-178, 1998.
17. Ciardiello F and Tortora G. Epidermal growth factor receptor (EGFR) as a target in cancer therapy: understanding the role of receptor expression and other molecular determinants that could influence the response to anti-EGFR drugs. Eur J Cancer 39: 1348-1354, 2003.
18. Dancey JE and Freidlin B. Targeting epidermal growth factor receptor-are we missing the mark? Lancet 362: 62-64, 2003.
19. Dorai T, Gehani N, and Katz A. Therapeutic potential of curcumin in human prostate cancer. II. Curcumin inhibits tyrosine kinase activity of epidermal growth factor receptor and depletes the protein. Mol Uml 4: 1-6, 2000.
20. Fajas L, Auboeuf D, Raspe E, Schoonjans K, Lefebvre AM, Saladin R, Najib J, Laville M, Fruchart JC, Deeb S, Vidal-Puig A, Flier J, Briggs MR, Staels B, Vidal H, and Auwerx J. The organization, promoter analysis, and expression of the human PPARγ gene. J Biol Chem 272: 18779-18789, 1997.
21. Fajas L, Fruchart JC, and Auwerx J. PPARγ3 mRNA: a distinct PPARγ mRNA subtype transcribed from an independent promoter. FEBS Lett 438: 55-60, 1998.
22. Forman BM, Chen J, and Evans RM. The peroxisome proliferator-activated receptors: ligands and activators. Ann NY Acad Sci 804: 266-275, 1996.
23. Green S and Wahli W. Peroxisome proliferator-activated receptors: finding the orphan a home. Mol Cell Endocrinol 100: 149-153, 1994.
24. Gupta RA, Brockman JA, Sarraf P, Willson TM, and DuBois RN. Target genes of peroxisome proliferator-activated receptor-γ in colorectal cancer cells. J Biol Chem 276: 29681-29687, 2001.
25. Hazra S, Xiong S, Wang J, Rippe R, Chatterjee VK, and Tsukamoto H. PPARγ induces a phenotypic switch from activated to quiescent hepatic stellate cells. J Biol Chem 279: 11392-11401, 2003.
26. Jobin C, Bradham CA, Russo MP, Juma B, Narula AS, Brenner DA, and Sartor RB. Curcumin blocks cytokine-mediated NF-κ activation and proinflammatory gene expression by inhibiting inhibitory factor I-κB kinase activity. J Immunol 163: 3474-3483, 1999.
27. Kawamori T, Lubet R, Steele VE, Kelloff GJ, Kaskey RB, Rao CV, and Reddy BS. Chemopreventive effect of curcumin, a naturally occurring anti-inflammatory agent, during the promotion/progression stages of colon cancer. Cancer Res 59: 597-601, 1999.
28. Kenny FS, Hui R, Musgrove EA, Gee JM, Blarney RW, Nicholson RI, Sutherland RL, and Robertson JF. Overexpression of cyclin D1 messenger RNA predicts for poor prognosis in estrogen receptor-positive breast cancer. Clin Cancer Res 5: 2069-2076, 1999.
29. Kitamura S, Miyazaki Y, Shinomura Y, Kondo S, Kanayama S, and Matsuzawa Y. Peroxisome proliferator-activated receptor-γ induces growth arrest and differentiation markers of human colon cancer cells. Jpn J Cancer Res 90: 75-80, 1999.
30. Korutla L, Cheung JY, Mendelsohn J, and Kumar R. Inhibition of ligand-induced activation of epidermal growth factor receptor tyrosine phosphorylation by curcumin. Carcinogenesis 16: 1741-1745, 1995.
31. Korutla L and Kumar R. Inhibitory effect of curcumin on epidermal growth factor receptor kinase activity in A431 cells. Blochim Biophys Acta 1224: 597-600, 1994.
32. Kubota T, Koshizuka K, Williamson EA, Asou H, Said JW, Holden S, Miyoshi I, and Koeffler HP. Ligand for peroxisome proliferator-activated receptor-γ (troglitazone) has potent antitumor effect against human prostate cancer both in vitro and in vivo. Cancer Res 58: 3344-3352, 1998.
33. Kue PF, Taub JS, Harrington LB, Polakiewicz RD, Ullrich A, and Daaka Y. Lysophosphatidic acid-regulated mitogenic ERK signaling in androgen-insensitive prostate cancer PC-3 cells. Int J Cancer 102: 572-579, 2002.
34. Lefebvre AM, Chen I, Desreumaux P, Najib J, Fruchart JC, Geboes K, Briggs M, Heyman R, and Auwerx J. Activation of the peroxisome proliferator-activated receptor-γ promotes the development of colon tumors in C57BL/6J-APCMin/+ mice. Nat Med 4: 1053-1057, 1998.
35. Levine AE, McRae LJ, Hamilton DA, Brattain DE, Yeoman LC, and Brattain MG. Identification of endogenous inhibitory growth factors from a human colon carcinoma cell line. Cancer Res 45: 2248-2254, 1985.
36. Lin JK, Chen YC, Huang YT, and Lin-Shiau SY. Suppression of protein kinase C and nuclear oncogene expression as possible molecular mechanisms of cancer chemoprevention by apigenin and curcumin. J Cell Biochem Suppl 28-29: 39-48, 1997.
37. Liu Z and Armant DR. Lysophosphatidic acid regulates murine blastocyst development by transactivation of receptors for heparin-binding EGF-like growth factor. Exp Cell Res 296: 317-326, 2004.
38. Lukas J, Bartkova J, and Bartek J. Convergence of mitogenic signalling cascades from diverse classes of receptors at the cyclin D-cyclin-dependent kinase-pRb-controlled G1 checkpoint. Mol Cell Biol 16: 6917-6925, 1996.
39. Mansen A, Guardiola-Diaz H, Rafter J, Branting C, and Gustafsson JA. Expression of the peroxisome proliferator-activated receptor (PPAR) in the mouse colonie mucosa. Biochem Biophys Res Commun 222; 844-851, 1996.
40. McCarthy KJ, Routh RE, Shaw W, Walsh K, Welbourne TC, and Johnson JH. Troglitazone halts diabetic glomerulosclerosis by blockade of mesangial expansion. Kidney Int 58: 2341-2350, 2000.
41. McIntyre TM, Pontsler AV, Suva AR, St Hilaire A, Xu Y, Hinshaw JC, Zimmerman GA, Hama K, Aoki J, Arai H, and Prestwich GD. Identification of an intracellular receptor for lysophosphatidic acid (LPA): LPA is a transcellular PPARγ agonist. Proc Natl Acad Sci USA 100: 131-136, 2003.
42. Mohan R, Sivak J, Ashton P, Russo LA, Pham BQ, Kasahara N, Raizman MB, and Fini ME. Curcuminoids inhibit the angiogenic response stimulated by fibroblast growth factor-2, including expression of matrix metalloproteinase gelatinase B. J Biol Chem 275: 10405-10412, 2000.
43. Mohandas KM and Desai DC. Epidemiology of digestive tract cancers in India. V. Large and small bowel. Indian J Gastroenterol 18: 118-121, 1999.
44. Moragoda L, Jaszewski R, and Majumdar AP. Curcumin induced modulation of cell cycle and apoptosis in gastric and colon cancer cells. Anticancer Res 21: 873-878, 2001.
45. Mukhopadhyay A, Banerjee S, Stafford LJ, Xia C, Liu M, and Aggarwal BB. Curcumin-induced suppression of cell proliferation correlates with down-regulation of cyclin D1 expression and CDK4-mediated retinoblastoma protein phosphorylation. Oncogene 21: 8852-8861, 2002.
46. Pan MH, Huang TM, and Lin JK. Biotransformation of curcumin through reduction and glucuronidation in mice. Drug Metab Dispos 27: 486-494, 1999.
47. Pestell RG, Albsjnese C, Reutens AT, Segall JE, Lee RJ, and Arnold A. The cyclins and cyclin-dependent kinase inhibitors in hormonal regulation of proliferation and differentiation. Endocr Rev 20: 501-534, 1999.
48. Plummer SM, Holloway KA, Manson MM, Munks RJ, Kaptein A, Farrow S, and Howells L. Inhibition of cyclo-oxygenase 2 expression in colon cells by the chemopreventive agent curcumin involves inhibition of NF-κB activation via the NIK/IKK signalling complex. Oncogene 18: 6013-6020, 1999.
49. Roberts-Thomson SJ. Peroxisome proliferator-activated receptors in tumorigenesis: targets of tumour promotion and treatment. Immunol Cell Biol 78: 436-441, 2000.
50. Routh RE, Johnson JH, and McCarthy KJ. Troglitazone suppresses the secretion of type I collagen by mesangial cells in vitro. Kidney Int 61: 1365-1376, 2002.
51. Saez E, Tontonoz P, Nelson MC, Alvarez JG, Ming UT, Baird SM, Thomazy VA, and Evans RM. Activators of the nuclear receptor PPARγ enhance colon polyp formation. Nat Med 4: 1058-1061, 1998.
52. Salomon DS, Brandt R, Ciardiello F, and Normanno N. Epidermal growth factor-related peptides and their receptors in human malignancies. Crit Rev Oncol Hematol 19: 183-232, 1995.
53. Sarraf P, Mueller E, Jones D, King FJ, DeAngelo DJ, Partridge JB, Holden SA, Chen LB, Singer S, Fletcher C, and Spiegelman BM. Differentiation and reversal of malignant changes in colon cancer through PPARγ. Nat Med 4: 1046-1052, 1998.
54. Sarraf P, Mueller E, Smith WM, Wright HM, Kum JB, Aaltonen LA, de la Chapelle A, Spiegelman BM, and Eng C. Loss-of-function mutations in PPAR-γ associated with human colon cancer. Mol Cell 3: 799-804, 1999.
55. Schmittgen TD, Zakrajsek BA, Mills AG, Gorn V, Singer MJ, and Reed MW. Quantitative reverse transcription-polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Anal Biochem 285: 194-204, 2000.
56. Shishodia S, Potdar P, Gairola CG, and Aggarwal BB. Curcumin (diferuloylmethane) down-regulates cigarette smoke-induced NF-κB activation through inhibition of IκBα kinase in human lung epithelial cells: correlation with suppression of COX-2, MMP-9 and cyclin D1. Carcinogenesis 24: 1269-1279, 2003.
57. Squires MS, Hudson EA, Howells L, Sale S, Honghton CE, Jones JL, Fox LH, Dickens M, Prigent SA, and Manson MM. Relevance of mitogen activated protein kinase (MAPK) and phosphotidylinositol-3-kinase/protein kiuase B (PI3K/PKB) pathways to induction of apoptosis by curcumin in breast cells. Biochem Pharmacol 65: 361-376, 2003.
58. Surh YJ. Cancer chemoprevention with dietary phytochemicals. Nat Rev Cancer 3: 768-780, 2003.
59. Tontonoz P, Nagy L, Alvarez JG, Thomazy VA, and Evans RM. PPARγ promotes monocyte/macrophage differentiation and uptake of oxidized LDL. Cell 93: 241-252, 1998.
60. Wang C, Fu M, D'Amico M, Albanese C, Zhou JN, Brownlee M, Lisanti MP, Chatterjee VK, Lazar MA, and Pestell RG. Inhibition of cellular proliferation through IκB kinase-independent and peroxisome proliferator-activated receptors-γ-dependent repression of cyclin D1. Mol Cell Biol 21: 3057-3070, 2001.
61. Wang C, Pattabiraman N, Zhou JN, Fu M, Sakamaki T, Albanese C, Li Z, Wu K, Hulit J, Neumeister P, Novikoff PM, Brownlee M, Scherer PE, Jones JG, Whitney KD, Donehower LA, Harris EL, Rohan T, Johns DC, and Pestell RG. Cyclin D1 repression of peroxisome proliferator-activated receptor-γ expression and transactivation. Mol Cell Biol 23: 6159-6173, 2003.
62. Xu J, Fu Y, and Chen A. Activation of peroxisome proliferator-activated receptor-γ contributes to the inhibitory effects of curcumin on rat hepatic stellate cell growth. Am J Physiol Gastrointest Liver Physiol 285: G20-G30, 2003.
63. Yarden Y and Sliwkowski MX. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2: 127-137, 2001.