Carnosic acid inhibits STAT3 signaling and induces apoptosis through generation of ROS in human colon cancer HCT116 cells

Molecular Carcinogenesis

Volumn 55, Issue 6, 2016, Pages 1096-1110

  Kim, Do Hee ^a   Park, Ki Woong ^b   Chae, In Gyeong ^b   Kundu, Juthika ^b   Kim, Eun Hee ^c   Kundu, Joydeb Kumar ^b   Chun, Kyung Soo ^b  

^a Seoul National University   (South Korea)

^b Keimyung University   (South Korea)

^c CHA University   (South Korea)

Author keywords

Apoptosis; Carnosic acid; Colon cancer; Reactive oxygen species; Signal transducer and activator of transcription 3

Indexed keywords

ACETYLCYSTEINE; ANTINEOPLASTIC AGENT; BUTHIONINE SULFOXIMINE; CARNOSIC ACID; CASPASE 3; CASPASE 9; CYCLIN D1; CYCLIN D2; CYCLIN D3; DNA; JANUS KINASE 2; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MDM2; PROTEIN P53; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; STAT3 PROTEIN; SURVIVIN; ABIETANE DERIVATIVE; STAT3 PROTEIN, HUMAN;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CELL VIABILITY; COLORECTAL CANCER; CONTROLLED STUDY; DNA BINDING; ENZYME ACTIVATION; GENE ACTIVITY; GENE PRODUCT; HCT116 CELL LINE; HT 29 CELL LINE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REPORTER GENE; SIGNAL TRANSDUCTION; CELL PROLIFERATION; CELL SURVIVAL; COLONIC NEOPLASMS; DRUG EFFECTS; GENE EXPRESSION REGULATION; HCT 116 CELL LINE; HT-29 CELL LINE; METABOLISM; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; COLONIC NEOPLASMS; DITERPENES, ABIETANE; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HT29 CELLS; HUMANS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 84936805532     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.22353     Document Type: Article

References (46)

1. Merika E, Saif MW, Katz A, Syrigos K, Morse M. Review. Colon cancer vaccines: An update. In Vivo 2010; 24:607-628.
2. Chung MY, Lim TG, Lee KW. Molecular mechanisms of chemopreventive phytochemicals against gastroenterological cancer development. World J Gastroenterol 2013; 19:984-993.
3. Block G, Patterson B, Subar A, Fruit . Vegetables, and cancer prevention: A review of the epidemiological evidence. Nutr Cancer 1992; 18:1-29.
4. Pesakhov S, Khanin M, Studzinski GP, Danilenko M. Distinct combinatorial effects of the plant polyphenols curcumin, carnosic acid, and silibinin on proliferation and apoptosis in acute myeloid leukemia cells. Nutr Cancer 2010; 62:811-824.
5. Yu YM, Lin CH, Chan HC, Tsai HD. Carnosic acid reduces cytokine-induced adhesion molecules expression and monocyte adhesion to endothelial cells. Eur J Nutr 2009; 48:101-106.
6. Barni MV, Carlini MJ, Cafferata EG, Puricelli L, Moreno S. Carnosic acid inhibits the proliferation and migration capacity of human colorectal cancer cells. Oncol Rep 2012; 27:1041-1048.
7. Hanahan D, Weinberg RA. Hallmarks of cancer: The next generation. Cell 2011; 144:646-674.
8. Elumalai P, Gunadharini DN, Senthilkumar K, et al. Induction of apoptosis in human breast cancer cells by nimbolide through extrinsic and intrinsic pathway. Toxicol Lett 2012; 215:131-142.
9. Neergheen VS, Bahorun T, Taylor EW, Jen LS, Aruoma OI. Targeting specific cell signaling transduction pathways by dietary and medicinal phytochemicals in cancer chemoprevention. Toxicology 2010; 278:229-241.
10. Burz C, Berindan-Neagoe I, Balacescu O, Irimie A. Apoptosis in cancer: Key molecular signaling pathways and therapy targets. Acta Oncol 2009; 48:811-821.
11. Aggarwal BB, Takada Y, Oommen OV. From chemoprevention to chemotherapy: Common targets and common goals. Expert Opin Investig Drugs 2004; 13:1327-1338.
12. Lau GK, Ye D. STAT3 implicated in the development of colon cancer: A step closer for targeted therapy?. Gastroenterology 2010; 139:353-355.
13. Lin L, Liu A, Peng Z, et al. STAT3 is necessary for proliferation and survival in colon cancer-initiating cells. Cancer Res 2011; 71:7226-7237.
14. Slattery ML, Lundgreen A, Kadlubar SA, Bondurant KL, Wolff RK. JAK/STAT/SOCS-signaling pathway and colon and rectal cancer. Mol Carcinog 2013; 52:155-166.
15. Bowman T, Garcia R, Turkson J, Jove R. STATs in oncogenesis. Oncogene 2000; 19:2474-2488.
16. Brierley MM, Fish EN. Stats: Multifaceted regulators of transcription. J Interferon Cytokine Res 2005; 25:733-744.
17. Johnston PA, Grandis JR. STAT3 signaling: Anticancer strategies and challenges. Mol Interv 2011; 11:18-26.
18. Kundu J, Wahab SM, Kundu JK, et al. Tob1 induces apoptosis and inhibits proliferation, migration and invasion of gastric cancer cells by activating Smad4 and inhibiting betacatenin signaling. Int J Oncol 2012; 41:839-848.
19. Kundu JK, Shin YK, Kim SH, Surh YJ. Resveratrol inhibits phorbol ester-induced expression of COX-2 and activation of NF-kappaB in mouse skin by blocking IkappaB kinase activity. Carcinogenesis 2006; 27:1465-1474.
20. Janicke RU, Ng P, Sprengart ML, Porter AG. Caspase-3 is required for alpha-fodrin cleavage but dispensable for cleavage of other death substrates in apoptosis. J Biol Chem 1998; 273:15540-15545.
21. Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 1993; 74:609-619.
22. Kadowaki H, Nishitoh H, Urano F, et al. Amyloid beta induces neuronal cell death through ROS-mediated ASK1 activation. Cell Death Differ 2005; 12:19-24.
23. Ngo SN, Williams DB, Head RJ. Rosemary and cancer prevention: Preclinical perspectives. Crit Rev Food Sci Nutr 2011; 51:946-954.
24. Park M, Han J, Lee CS, Soo BH, Lim KM, Ha H. Carnosic acid, a phenolic diterpene from rosemary, prevents UV-induced expression of matrix metalloproteinases in human skin fibroblasts and keratinocytes. Exp Dermatol 2013; 22:336-341.
25. Xiang Q, Liu Z, Wang Y, et al. Carnosic acid attenuates lipopolysaccharide-induced liver injury in rats via fortifying cellular antioxidant defense system. Food Chem Toxicol 2013; 53:1-9.
26. Kar S, Palit S, Ball WB, Das PK. Carnosic acid modulates Akt/IKK/NF-kappaB signaling by PP2A and induces intrinsic and extrinsic pathway mediated apoptosis in human prostate carcinoma PC-3 cells. Apoptosis 2012; 17:735-747.
27. Cherbonnel-Lasserre C, Dosanjh MK. Suppression of apoptosis by overexpression of Bcl-2 or Bcl-xL promotes survival and mutagenesis after oxidative damage. Biochimie 1997; 79:613-617.
28. Valassiadou KE, Stefanaki K, Tzardi M, et al. Immunohistochemical expression of p53, bcl-2, mdm2 and waf1/p21 proteins in colorectal adenocarcinomas. Anticancer Res 1997; 17:2571-2576.
29. Bonnotte B, Favre N, Moutet M, et al. Bcl-2-mediated inhibition of apoptosis prevents immunogenicity and restores tumorigenicity of spontaneously regressive tumors. J Immunol 1998; 161:1433-1438.
30. Miyashita T, Reed JC. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 1995; 80:293-299.
31. Kim DH, Kundu JK, Surh YJ. Redox modulation of p53: Mechanisms and functional significance. Mol Carcinog 2011; 50:222-234.
32. Rigatti MJ, Verma R, Belinsky GS, Rosenberg DW, Giardina C. Pharmacological inhibition of Mdm2 triggers growth arrest and promotes DNA breakage in mouse colon tumors and human colon cancer cells. Mol Carcinog 2012; 51:363-378.
33. Miyashita T, Krajewski S, Krajewska M, et al. Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 1994; 9:1799-1805.
34. Lotem J, Peled-Kamar M, Groner Y, Sachs L. Cellular oxidative stress and the control of apoptosis by wild-type p53, cytotoxic compounds, and cytokines. Proc Natl Acad Sci USA 1996; 93:9166-9171.
35. Satoh T, McKercher SR, Lipton SA. Nrf2/ARE-mediated antioxidant actions of pro-electrophilic drugs. Free Radic Biol Med 2013; 65:645-657.
36. Masuda M, Suzui M, Yasumatu R, et al. Constitutive activation of signal transducers and activators of transcription 3 correlates with cyclin D1 overexpression and may provide a novel prognostic marker in head and neck squamous cell carcinoma. Cancer Res 2002; 62:3351-3355.
37. Corvinus FM, Orth C, Moriggl R, et al. Persistent STAT3 activation in colon cancer is associated with enhanced cell proliferation and tumor growth. Neoplasia 2005; 7:545-555.
38. Lin Q, Lai R, Chirieac LR, et al. Constitutive activation of JAK3/STAT3 in colon carcinoma tumors and cell lines: Inhibition of JAK3/STAT3 signaling induces apoptosis and cell cycle arrest of colon carcinoma cells. Am J Pathol 2005; 167:969-980.
39. Li L, Shaw PE. A STAT3 dimer formed by inter-chain disulphide bridging during oxidative stress. Biochem Biophys Res Commun 2004; 322:1005-1011.
40. Laird AD, Li G, Moss KG, et al. Src family kinase activity is required for signal tranducer and activator of transcription 3 and focal adhesion kinase phosphorylation and vascular endothelial growth factor signaling in vivo and for anchorage-dependent and -independent growth of human tumor cells. Mol Cancer Ther 2003; 2:461-469.
41. Kanda N, Seno H, Konda Y, et al. STAT3 is constitutively activated and supports cell survival in association with survivin expression in gastric cancer cells. Oncogene 2004; 23:4921-4929.
42. Dixit D, Sharma V, Ghosh S, Koul N, Mishra PK, Sen E. Manumycin inhibits STAT3, telomerase activity, and growth of glioma cells by elevating intracellular reactive oxygen species generation. Free Radic Biol Med 2009; 47:364-374.
43. Liu Y, Wang L, Wu Y, et al. Pterostilbene exerts antitumor activity against human osteosarcoma cells by inhibiting the JAK2/STAT3 signaling pathway. Toxicology 2013; 304:120-131.
44. Tai J, Cheung S, Wu M, Hasman D. Antiproliferation effect of Rosemary (Rosmarinus officinalis) on human ovarian cancer cells in vitro. Phytomedicine: International journal of phytotherapy and phytopharmacology 2012; 19:436-443.
45. Selvendiran K, Ahmed S, Dayton A, et al. HO-3867, a curcumin analog, sensitizes cisplatin-resistant ovarian carcinoma, leading to therapeutic synergy through STAT3 inhibition. Cancer Biol Ther 2011; 12:837-845.
46. Das R, Bhattacharya K, Samanta SK, Pal BC, Mandal C. Improved chemosensitivity in cervical cancer to cisplatin: Synergistic activity of mahanine through STAT3 inhibition. Cancer letters 2014; 351:81-90.