Caffeic acid derivatives inhibit the growth of colon cancer: Involvement of the PI3-K/Akt and AMPK signaling pathways

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Chiang, En Pei Isabel ^a   Tsai, Shu Yao ^b   Kuo, Yueh Hsiung ^b,c   Pai, Man Hui ^d   Chiu, Hsi Lin ^b,c   Rodriguez, Raymond L ^e   Tang, Feng Yao ^c  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^b ASIA UNIVERSITY   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

^d TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAFFEIC ACID DERIVATIVE; CAFFEIC ACID PHENETHYL ESTER; CAFFEIC ACID PHENYLPROPYL ESTER; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; UNCLASSIFIED DRUG; 3-PHENYLPROPYL CAFFEATE; ANTINEOPLASTIC AGENT; PHENETHYL ALCOHOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL CYCLE S PHASE; CELL PROLIFERATION; CELL SURVIVAL; CHEMOPROPHYLAXIS; COLON CANCER; DRUG EFFICACY; DRUG MECHANISM; DRUG RESPONSE; DRUG STRUCTURE; DRUG TARGETING; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; ANALOGS AND DERIVATIVES; CELL CYCLE CHECKPOINT; COLON TUMOR; DRUG EFFECTS; ENZYMOLOGY; HCT116 CELL LINE; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; CAFFEIC ACIDS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL PROLIFERATION; COLONIC NEOPLASMS; HCT116 CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; PHENYLETHYL ALCOHOL;

EID: 84903541980     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099631     Document Type: Article

References (57)

1. Siegel R, Ma J, Zou Z, Jemal A (2014) Cancer statistics, 2014. CA Cancer J Clin 64: 9-29.
2. Siegel R, Desantis C, Jemal A (2014) Colorectal cancer statistics, 2014. CA Cancer J Clin 64: 104-117.
3. Vogt PK, Kang S, Elsliger MA, Gymnopoulos M (2007) Cancer-specific mutations in phosphatidylinositol 3-kinase. Trends Biochem Sci 32: 342-349. (Pubitemid 47021415)
4. Halilovic E, She QB, Ye Q, Pagliarini R, Sellers WR, et al. (2010) PIK3CA mutation uncouples tumor growth and cyclin D1 regulation from MEK/ERK and mutant KRAS signaling. Cancer Res 70: 6804-6814.
5. Gustin JP, Karakas B, Weiss MB, Abukhdeir AM, Lauring J, et al. (2009) Knockin of mutant PIK3CA activates multiple oncogenic pathways. Proc Natl Acad Sci U S A 106: 2835-2840.
6. Kang S, Bader AG, Vogt PK (2005) Phosphatidylinositol 3-kinase mutations identified in human cancer are oncogenic. Proc Natl Acad Sci U S A 102: 802-807. (Pubitemid 40282746)
7. Wang QS, Papanikolaou A, Sabourin CL, Rosenberg DW (1998) Altered expression of cyclin D1 and cyclin-dependent kinase 4 in azoxymethane-induced mouse colon tumorigenesis. Carcinogenesis 19: 2001-2006. (Pubitemid 28521944)
8. Wolter F, Akoglu B, Clausnitzer A, Stein J (2001) Downregulation of the cyclin D1/Cdk4 complex occurs during resveratrol-induced cell cycle arrest in colon cancer cell lines. J Nutr 131: 2197-2203. (Pubitemid 32720652)
9. Hanahan D,Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674.
10. Tang F-Y, Chiang E-PI, Sun Y-C (2008) Resveratrol inhibits heregulin-beta 1-mediated matrix metalloproteinase-9 expression and cell invasion in human breast cancer cells. Journal of Nutritional Biochemistry 19: 287-294. (Pubitemid 351503761)
11. Aparicio T, Lehy T (1999) [Matrix metalloproteases in digestive pathology]. Gastroenterol Clin Biol 23: 330-341.
12. Hardie DG, Scott JW, Pan DA, Hudson ER (2003) Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett 546: 113-120. (Pubitemid 36782291)
13. Kahn BB, Alquier T, Carling D, Hardie DG (2005) AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab 1: 15-25. (Pubitemid 43960587)
14. Sato R, Goldstein JL, Brown MS (1993) Replacement of serine-871 of hamster 3-hydroxy-3-methylglutaryl-CoA reductase prevents phosphorylation by AMPactivated kinase and blocks inhibition of sterol synthesis induced by ATP depletion. Proc Natl Acad Sci U S A 90: 9261-9265. (Pubitemid 23315763)
15. Fogarty S, Hardie DG (2010) Development of protein kinase activators: AMPK as a target in metabolic disorders and cancer. Biochim Biophys Acta 1804: 581-591.
16. Baba Y, Nosho K, Shima K, Meyerhardt JA, Chan AT, et al. (2010) Prognostic significance of AMP-activated protein kinase expression and modifying effect of MAPK3/1 in colorectal cancer. Br J Cancer 103: 1025-1033.
17. Shackelford DB, Shaw RJ (2009) The LKB1-AMPK pathway: metabolism and growth control in tumour suppression. Nat Rev Cancer 9: 563-575.
18. Liu YQ, Cheng X, Guo LX, Mao C, Chen YJ, et al. (2012) Identification of an annonaceous acetogenin mimetic, AA005, as an AMPK activator and autophagy inducer in colon cancer cells. PLoS One 7: e47049.
19. Menendez JA, Lupu R (2007) Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis. Nat Rev Cancer 7: 763-777. (Pubitemid 47469806)
20. Kuchiba A, Morikawa T, Yamauchi M, Imamura Y, Liao X, et al. (2012) Body mass index and risk of colorectal cancer according to fatty acid synthase expression in the nurses' health study. J Natl Cancer Inst 104: 415-420.
21. Porstmann T, Griffiths B, Chung YL, Delpuech O, Griffiths JR, et al. (2005) PKB/Akt induces transcription of enzymes involved in cholesterol and fatty acid biosynthesis via activation of SREBP. Oncogene 24: 6465-6481. (Pubitemid 41486630)
22. Zakikhani M, Dowling RJ, Sonenberg N, Pollak MN (2008) The effects of adiponectin and metformin on prostate and colon neoplasia involve activation of AMP-activated protein kinase. Cancer Prev Res (Phila) 1: 369-375.
23. Zakikhani M, Dowling R, Fantus IG, Sonenberg N, Pollak M (2006) Metformin is an AMP kinase-dependent growth inhibitor for breast cancer cells. Cancer Res 66: 10269-10273. (Pubitemid 44799743)
24. Algire C, Amrein L, Zakikhani M, Panasci L, Pollak M (2010) Metformin blocks the stimulative effect of a high-energy diet on colon carcinoma growth in vivo and is associated with reduced expression of fatty acid synthase. Endocr Relat Cancer 17: 351-360.
25. Slattery ML, Herrick JS, Lundgreen A, Fitzpatrick FA, Curtin K, et al. (2010) Genetic variation in a metabolic signaling pathway and colon and rectal cancer risk: mTOR, PTEN, STK11, RPKAA1, PRKAG2, TSC1, TSC2, PI3K and Akt1. Carcinogenesis 31: 1604-1611.
26. Piazzon A, Vrhovsek U, Masuero D, Mattivi F, Mandoj F, et al. (2012) Antioxidant activity of phenolic acids and their metabolites: synthesis and antioxidant properties of the sulfate derivatives of ferulic and caffeic acids and of the acyl glucuronide of ferulic acid. J Agric Food Chem 60: 12312-12323.
27. Nardini M, Leonardi F, Scaccini C, Virgili F (2001) Modulation of ceramideinduced NF-kappaB binding activity and apoptotic response by caffeic acid in U937 cells: comparison with other antioxidants. Free Radic Biol Med 30: 722-733. (Pubitemid 32245578)
28. Nardini M, Pisu P, Gentili V, Natella F, Di Felice M, et al. (1998) Effect of caffeic acid on tert-butyl hydroperoxide-induced oxidative stress in U937. Free Radic Biol Med 25: 1098-1105. (Pubitemid 28558337)
29. Gocer H, Gulcin I (2011) Caffeic acid phenethyl ester (CAPE): correlation of structure and antioxidant properties. Int J Food Sci Nutr 62: 821-825.
30. Yilmaz HR, Uz E, Yucel N, Altuntas I, Ozcelik N (2004) Protective effect of caffeic acid phenethyl ester (CAPE) on lipid peroxidation and antioxidant enzymes in diabetic rat liver. J Biochem Mol Toxicol 18: 234-238. (Pubitemid 39341509)
31. Chen MF, Wu CT, Chen YJ, Keng PC, Chen WC (2004) Cell killing and radiosensitization by caffeic acid phenethyl ester (CAPE) in lung cancer cells. J Radiat Res 45: 253-260. (Pubitemid 39237128)
32. Ribeiro U Jr, Safatle-Ribeiro AV (2007) Caffeic acid phenethyl ester (CAPE) may be a promising adjuvant treatment in gastric cancer. J Clin Gastroenterol 41: 871-873.
33. Stacey DW (2003) Cyclin D1 serves as a cell cycle regulatory switch in actively proliferating cells. Curr Opin Cell Biol 15: 158-163.
34. Vivanco I, Sawyers CL (2002) The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2: 489-501. (Pubitemid 37328931)
35. Philp AJ, Campbell IG, Leet C, Vincan E, Rockman SP, et al. (2001) The phosphatidylinositol 39-kinase p85alpha gene is an oncogene in human ovarian and colon tumors. Cancer Res 61: 7426-7429. (Pubitemid 32995029)
36. Ponnurangam S, Standing D, Rangarajan P, Subramaniam D (2013) Tandutinib inhibits the Akt/mTOR signaling pathway to inhibit colon cancer growth. Mol Cancer Ther 12: 598-609.
37. Wang W, Guan KL (2009) AMP-activated protein kinase and cancer. Acta Physiol (Oxf) 196: 55-63.
38. Tang F-Y, Pai M-H, Chiang E-PI (2012) Consumption of high-fat diet induces tumor progression and epithelial-mesenchymal transition of colorectal cancer in a mouse xenograft model. Journal of Nutritional Biochemistry 23: 1302-1313.
39. Natarajan K, Singh S, Burke TR Jr, Grunberger D, Aggarwal BB (1996) Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B. Proc Natl Acad Sci U S A 93: 9090-9095. (Pubitemid 26282023)
40. Tang F-Y, Pai M-H, Kuo Y-H, Wang X-D (2012) Concomitant consumption of lycopene and fish oil inhibits tumor growth and progression in a mouse xenograft model of colon cancer. Mol Nutr Food Res 56: 1520-1531.
41. Wee S, Jagani Z, Xiang KX, Loo A, Dorsch M, et al. (2009) PI3K pathway activation mediates resistance to MEK inhibitors in KRAS mutant cancers. Cancer Res 69: 4286-4293.
42. Ramana KV, Tammali R, Srivastava SK (2010) Inhibition of aldose reductase prevents growth factor-induced G1-S phase transition through the AKT/ phosphoinositide 3-kinase/E2F-1 pathway in human colon cancer cells. Mol Cancer Ther 9: 813-824.
43. Gulhati P, Zaytseva YY, Valentino JD, Stevens PD, Kim JT, et al. (2012) Sorafenib enhances the therapeutic efficacy of rapamycin in colorectal cancers harboring oncogenic KRAS and PIK3CA. Carcinogenesis 33: 1782-1790.
44. Tang F-Y, Shih C-J, Cheng L-H, Ho H-J, Chen H-J (2008) Lycopene inhibits growth of human colon cancer cells via suppression of the Akt signaling pathway. Mol Nutr Food Res 52: 646-654.
45. Tang F-Y, Pai M-H, Wang X-D (2011) Consumption of Lycopene Inhibits the Growth and Progression of Colon Cancer in a Mouse Xenograft Model. J Agric Food Chem 59: 9011-9021.
46. Tolba MF, Esmat A, Al-Abd AM, Azab SS, Khalifa AE, et al. (2013) Caffeic acid phenethyl ester synergistically enhances docetaxel and paclitaxel cytotoxicity in prostate cancer cells. IUBMB Life 65: 716-729.
47. Lin HP, Jiang SS, Chuu CP (2012) Caffeic acid phenethyl ester causes p21 induction, Akt signaling reduction, and growth inhibition in PC-3 human prostate cancer cells. PLoS One 7: e31286.
48. Chuu CP, Lin HP, Ciaccio MF, Kokontis JM, Hause RJ Jr, et al. (2012) Caffeic acid phenethyl ester suppresses the proliferation of human prostate cancer cells through inhibition of p70S6K and Akt signaling networks. Cancer Prev Res (Phila) 5: 788-797.
49. Kuo YY, Lin HP, Huo C, Su LC, Yang J, et al. (2013) Caffeic Acid Phenethyl Ester Suppresses Proliferation and Survival of TW2.6 Human Oral Cancer Cells via Inhibition of Akt Signaling. Int J Mol Sci 14: 8801-8817.
50. Pramanik KC, Kudugunti SK, Fofaria NM, Moridani MY, Srivastava SK (2013) Caffeic acid phenethyl ester suppresses melanoma tumor growth by inhibiting PI3K/AKT/XIAP pathway. Carcinogenesis 34: 2061-2070.
51. Xiang D, Wang D, He Y, Xie J, Zhong Z, et al. (2006) Caffeic acid phenethyl ester induces growth arrest and apoptosis of colon cancer cells via the betacatenin/ T-cell factor signaling. Anticancer Drugs 17: 753-762. (Pubitemid 44310172)
52. Liao HF, Chen YY, Liu JJ, Hsu ML, Shieh HJ, et al. (2003) Inhibitory effect of caffeic acid phenethyl ester on angiogenesis, tumor invasion, and metastasis. J Agric Food Chem 51: 7907-7912.
53. Bates RC, Edwards NS, Burns GF, Fisher DE (2001) A CD44 survival pathway triggers chemoresistance via lyn kinase and phosphoinositide 3-kinase/Akt in colon carcinoma cells. Cancer Res 61: 5275-5283. (Pubitemid 32681564)
54. Weyant MJ, Carothers AM, Bertagnolli ME, Bertagnolli MM (2000) Colon cancer chemopreventive drugs modulate integrin-mediated signaling pathways. Clin Cancer Res 6: 949-956. (Pubitemid 30159353)
55. Shaw RJ, Kosmatka M, Bardeesy N, Hurley RL, Witters LA, et al. (2004) The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc Natl Acad Sci U S A 101: 3329-3335. (Pubitemid 38338195)
56. Uwai K, Osanai Y, Imaizumi T, Kanno S, Takeshita M, et al. (2008) Inhibitory effect of the alkyl side chain of caffeic acid analogues on lipopolysaccharideinduced nitric oxide production in RAW264.7 macrophages. Bioorg Med Chem 16: 7795-7803.
57. Mohan S, Patel H, Bolinaga J, Soekamto N (2013) AMP-activated protein kinase regulates L-arginine mediated cellular responses. Nutr Metab (Lond) 10: 40.