Cinnamaldehyde-induced apoptosis in human hepatoma PLC/PRF/5 cells involves the mitochondrial death pathway and is sensitive to inhibition by cyclosporin A and z-VAD-fmk

Anti-Cancer Agents in Medicinal Chemistry

Volumn 13, Issue 10, 2013, Pages 1565-1574

  Lin, Liang Tzung ^a,b   Tai, Chen Jei ^a,c   Chang, Shun Pang ^d   Chen, Jin Liang ^e   Wu, Shu Jing ^e   Lin, Chun Ching ^d  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^b IWK HEALTH CENTRE   (Canada)

^c TAIPEI MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^e CHIA NAN UNIVERSITY OF PHARMACY AND SCIENCE   (Taiwan)

Author keywords

Apoptosis; Cinnamaldehyde; Cyclosporin A; Hepatoma; Mitochondria; ROS; z VAD fmk

Indexed keywords

CASPASE INHIBITOR; CINNAMALDEHYDE; CYCLOSPORIN A; CYTOCHROME C; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; X LINKED INHIBITOR OF APOPTOSIS;

APOPTOSIS; ARTICLE; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; PROTEIN EXPRESSION; WESTERN BLOTTING;

ACROLEIN; AMINO ACID CHLOROMETHYL KETONES; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CASPASE 3; CELL LINE, TUMOR; CYCLOSPORINE; CYTOCHROMES C; GENE EXPRESSION REGULATION, NEOPLASTIC; HEPATOCYTES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL PROTEINS; POLY(ADP-RIBOSE) POLYMERASES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 84898974038     PISSN: 18715206     EISSN: 18755992     Source Type: Journal    
DOI: 10.2174/18715206113139990144     Document Type: Article

References (54)

1. Agostini, M.; Tucci, P.; Melino, G. Cell death pathology: perspective for human diseases. Biochem Biophys Res Commun, 2011, 414(3), 451-455.
2. Elmore, S. Apoptosis: a review of programmed cell death. Toxicol. Pathol., 2007, 35(4), 495-516.
3. Chalah, A.; Khosravi-Far, R. The mitochondrial death pathway. Adv. Exp. Med. Biol., 2008, 615, 25-45.
4. Green, D.R.; Kroemer, G. The pathophysiology of mitochondrial cell death. Science, 2004, 305(5684), 626-629.
5. Karbowski, M. Mitochondria on guard: role of mitochondrial fusion and fission in the regulation of apoptosis. Adv. Exp. Med. Biol., 2010, 687, 131-142.
6. Bao, Q.; Shi, Y. Apoptosome: a platform for the activation of initiator caspases. Cell Death Differ., 2007, 14(1), 56-65.
7. Salvesen, G.S.; Riedl, S.J. Caspase mechanisms. Adv. Exp. Med. Biol., 2008, 615, 13-23.
8. Galluzzi, L.; Joza, N.; Tasdemir, E.; Maiuri, M.C.; Hengartner, M.; Abrams, J.M.; Tavernarakis, N.; Penninger, J.; Madeo, F.; Kroemer, G. No death without life: vital functions of apoptotic effectors. Cell Death Differ., 2008, 15(7), 1113-1123.
9. Launay, S.; Hermine, O.; Fontenay, M.; Kroemer, G.; Solary, E.; Garrido, C. Vital functions for lethal caspases. Oncogene, 2005, 24(33), 5137-5148.
10. Gyrd-Hansen, M.; Meier, P. IAPs: from caspase inhibitors to modulators of NF-kappaB, inflammation and cancer. Nat. Rev. Cancer, 2010, 10(8), 561-574.
11. Peng, Y.; Sun, H.; Lu, J.; Liu, L.; Cai, Q.; Shen, R.; Yang, C.Y.; Yi, H.; Wang, S. Bivalent Smac mimetics with a diazabicyclic core as highly potent antagonists of XIAP and cIAP1/2 and novel anticancer agents. J. Med. Chem., 2012, 55(1), 106-114.
12. Reuter, S.; Prasad, S.; Phromnoi, K.; Ravindran, J.; Sung, B.; Yadav, V.R.; Kannappan, R.; Chaturvedi, M.M.; Aggarwal, B.B. Thiocolchicoside exhibits anticancer effects through downregulation of NF-kappaB pathway and its regulated gene products linked to inflammation and cancer. Cancer Prev. Res. (Phila), 2010, 3(11), 1462-1472.
13. Lou, Z.Q.; Qin, B. Species Systematization and Quality Evaluation of Commonly Used Chinese Traditional Drugs; Beijing University Medical Press: Beijing, China, 1995.
14. Jayaprakasha, G.K.; Rao, L.J. Chemistry, biogenesis, and biological activities of Cinnamomum zeylanicum. Crit. Rev. Food Sci. Nutr., 2011, 51(6), 547-562.
15. He, Z.D.; Qiao, C.F.; Han, Q.B.; Cheng, C.L.; Xu, H.X.; Jiang, R.W.; But, P.P.; Shaw, P.C. Authentication and quantitative analysis on the chemical profile of cassia bark (cortex cinnamomi) by high-pressure liquid chromatography. J. Agric. Food Chem., 2005, 53(7), 2424-2428.
16. Burt, S. Essential oils: their antibacterial properties and potential applications in foods--a review. Int. J. Food Microbiol., 2004, 94(3), 223-253.
17. Amalaradjou, M.A.; Baskaran, S.A.; Ramanathan, R.; Johny, A.K.; Charles, A.S.; Valipe, S.R.; Mattson, T.; Schreiber, D.; Juneja, V.K.; Mancini, R.; Venkitanarayanan, K. Enhancing the thermal destruction of Escherichia coli O157:H7 in ground beef patties by trans-cinnamaldehyde. Food Microbiol., 2010, 27(6), 841-844.
18. Wei, Q.Y.; Xiong, J.J.; Jiang, H.; Zhang, C.; Wen, Y. The antimicrobial activities of the cinnamaldehyde adducts with amino acids. Int. J. Food Microbiol., 2011, 150(2-3), 164-170.
19. Kollanoor-Johny, A.; Mattson, T.; Baskaran, S.A.; Amalaradjou, M.A.; Babapoor, S.; March, B.; Valipe, S.; Darre, M.; Hoagland, T.; Schreiber, D.; Khan, M.I.; Donoghue, A.; Donoghue, D.; Venkitanarayanan, K. Reduction of Salmonella enterica Serovar Enteritidis Colonization in 20-Day-Old Broiler Chickens by the Plant-Derived Compounds trans-Cinnamaldehyde and Eugenol. Appl. Environ. Microbiol., 2012, 78(8), 2981-2987.
20. King, A.A.; Shaughnessy, D.T.; Mure, K.; Leszczynska, J.; Ward, W.O.; Umbach, D.M.; Xu, Z.; Ducharme, D.; Taylor, J.A.; Demarini, D.M.; Klein, C.B. Antimutagenicity of cinnamaldehyde and vanillin in human cells: Global gene expression and possible role of DNA damage and repair. Mutat. Res., 2007, 616(1-2), 60-69.
21. Hayashi, K.; Imanishi, N.; Kashiwayama, Y.; Kawano, A.; Terasawa, K.; Shimada, Y.; Ochiai, H. Inhibitory effect of cinnamaldehyde, derived from Cinnamomi cortex, on the growth of influenza A/PR/8 virus in vitro and in vivo. Antiviral Res., 2007, 74(1), 1-8.
22. Ding, Y.; Qiu, L.; Zhao, G.; Xu, J.; Wang, S. Influence of cinnamaldehyde on viral myocarditis in mice. Am. J. Med. Sci., 2010, 340(2), 114-120.
23. Youn, H.S.; Lee, J.K.; Choi, Y.J.; Saitoh, S.I.; Miyake, K.; Hwang, D.H.; Lee, J.Y. Cinnamaldehyde suppresses toll-like receptor 4 activation mediated through the inhibition of receptor oligomerization. Biochem. Pharmacol., 2008, 75(2), 494-502.
24. Kim, B.H.; Lee, Y.G.; Lee, J.; Lee, J.Y.; Cho, J.Y. Regulatory effect of cinnamaldehyde on monocyte/macrophage-mediated inflammatory responses. Mediators Inflamm., 2010, 2010, 529359.
25. Chao, L.K.; Hua, K.F.; Hsu, H.Y.; Cheng, S.S.; Lin, I.F.; Chen, C.J.; Chen, S.T.; Chang, S.T. Cinnamaldehyde inhibits proinflammatory cytokines secretion from monocytes/macrophages through suppression of intracellular signaling. Food Chem. Toxicol., 2008, 46(1), 220-231.
26. Ka, H.; Park, H.J.; Jung, H.J.; Choi, J.W.; Cho, K.S.; Ha, J.; Lee, K.T. Cinnamaldehyde induces apoptosis by ROS-mediated mitochondrial permeability transition in human promyelocytic leukemia HL-60 cells. Cancer Lett., 2003, 196(2), 143-152.
27. Ng, L.T.; Wu, S.J. Antiproliferative Activity of Cinnamomum cassia Constituents and Effects of Pifithrin-Alpha on Their Apoptotic Signaling Pathways in Hep G2 Cells. Evid. Based Complement. Alternat. Med., 2011, 2011, 492148.
28. Wu, S.J.; Ng, L.T.; Lin, C.C. Cinnamaldehyde-induced apoptosis in human PLC/PRF/5 cells through activation of the proapoptotic Bcl-2 family proteins and MAPK pathway. Life Sci., 2005, 77(8), 938-951.
29. Kwon, H.K.; Hwang, J.S.; So, J.S.; Lee, C.G.; Sahoo, A.; Ryu, J.H.; Jeon, W.K.; Ko, B.S.; Im, C.R.; Lee, S.H.; Park, Z.Y.; Im, S.H. Cinnamon extract induces tumor cell death through inhibition of NFkappaB and AP1. BMC Cancer, 2010, 10, 392.
30. Bruyere, C.; Genovese, S.; Lallemand, B.; Ionescu-Motatu, A.; Curini, M.; Kiss, R.; Epifano, F. Growth inhibitory activities of oxyprenylated and non-prenylated naturally occurring phenylpropanoids in cancer cell lines. Bioorg. Med. Chem. Lett., 2011, 21(14), 4174-4179.
31. Duessel, S.; Heuertz, R.M.; Ezekiel, U.R. Growth inhibition of human colon cancer cells by plant compounds. Clin. Lab Sci., 2008, 21(3), 151-157.
32. Imai, T.; Yasuhara, K.; Tamura, T.; Takizawa, T.; Ueda, M.; Hirose, M.; Mitsumori, K. Inhibitory effects of cinnamaldehyde on 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone-induced lung carcinogenesis in rasH2 mice. Cancer Lett., 2002, 175(1), 9-16.
33. Nakamura, M.; Nagano, H.; Sakon, M.; Yamamoto, T.; Ota, H.; Wada, H.; Damdinsuren, B.; Noda, T.; Marubashi, S.; Miyamoto, A.; Takeda, Y.; Umeshita, K.; Nakamori, S.; Dono, K.; Monden, M. Role of the Fas/FasL pathway in combination therapy with interferon-alpha and fluorouracil against hepatocellular carcinoma in vitro. J. Hepatol., 2007, 46(1), 77-88.
34. Wu, S.J.; Ng, L.T. MAPK inhibitors and pifithrin-alpha block cinnamaldehyde-induced apoptosis in human PLC/PRF/5 cells. Food Chem. Toxicol., 2007, 45(12), 2446-2453.
35. Usta, J.; Kreydiyyeh, S.; Bajakian, K.; Nakkash-Chmaisse, H. In vitro effect of eugenol and cinnamaldehyde on membrane potential and respiratory chain complexes in isolated rat liver mitochondria. Food Chem. Toxicol., 2002, 40(7), 935-940.
36. Kim, D.H.; Kim, C.H.; Kim, M.S.; Kim, J.Y.; Jung, K.J.; Chung, J.H.; An, W.G.; Lee, J.W.; Yu, B.P.; Chung, H.Y. Suppression of age-related inflammatory NF-kappaB activation by cinnamaldehyde. Biogerontology, 2007, 8(5), 545-554.
37. Wu, S.J.; Ng, L.T.; Lin, C.C. Effects of vitamin E on the cinnamaldehyde-induced apoptotic mechanism in human PLC/PRF/5 cells. Clin. Exp. Pharmacol. Physiol., 2004, 31(11), 770-776.
38. Ferlini, C.; Scambia, G. Assay for apoptosis using the mitochondrial probes, Rhodamine123 and 10-N-nonyl acridine orange. Nat. Protoc., 2007, 2(12), 3111-3114.
39. Bai, J.; Cederbaum, A.I. Overexpression of CYP2E1 in mitochondria sensitizes HepG2 cells to the toxicity caused by depletion of glutathione. J. Biol. Chem., 2006, 281(8), 5128-5136.
40. Solaini, G.; Sgarbi, G.; Lenaz, G.; Baracca, A. Evaluating mitochondrial membrane potential in cells. Biosci. Rep., 2007, 27(1-3), 11-21.
41. Ferlini, C.; Biselli, R.; Nisini, R.; Fattorossi, A. Rhodamine 123: a useful probe for monitoring T cell activation. Cytometry, 1995, 21(3), 284-293.
42. Chen, L.B. Mitochondrial membrane potential in living cells. Annu. Rev. Cell Biol., 1988, 4, 155-181.
43. Boulares, A.H.; Zoltoski, A.J.; Contreras, F.J.; Yakovlev, A.G.; Yoshihara, K.; Smulson, M.E. Regulation of DNAS1L3 endonuclease activity by poly(ADP-ribosyl)ation during etoposideinduced apoptosis. Role of poly(ADP-ribose) polymerase-1 cleavage in endonuclease activation. J. Biol. Chem., 2002, 277(1), 372-378.
44. Kroemer, G.; Galluzzi, L.; Brenner, C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev., 2007, 87(1), 99-163.
45. Orrenius, S.; Gogvadze, V.; Zhivotovsky, B. Mitochondrial oxidative stress: implications for cell death. Ann. Rev. Pharmacol. Toxicol., 2007, 47, 143-183.
46. Daiber, A. Redox signaling (cross-talk) from and to mitochondria involves mitochondrial pores and reactive oxygen species. Biochim. Biophys. Acta, 2010, 1797(6-7), 897-906.
47. Zorov, D.B.; Filburn, C.R.; Klotz, L.O.; Zweier, J.L.; Sollott, S.J. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J. Exp. Med., 2000, 192(7), 1001-1014.
48. Feng, R.; Han, J.; Ziegler, J.; Yang, M.; Castranova, V. Apaf-1 deficiency confers resistance to ultraviolet-induced apoptosis in mouse embryonic fibroblasts by disrupting reactive oxygen species amplification production and mitochondrial pathway. Free Radic Biol. Med., 2012, 52(5), 889-897.
49. Chen, Q.; Gong, B.; Almasan, A. Distinct stages of cytochrome c release from mitochondria: evidence for a feedback amplification loop linking caspase activation to mitochondrial dysfunction in genotoxic stress induced apoptosis. Cell Death Differ., 2000, 7(2), 227-233.
50. Slee, E.A.; Keogh, S.A.; Martin, S.J. Cleavage of BID during cytotoxic drug and UV radiation-induced apoptosis occurs downstream of the point of Bcl-2 action and is catalysed by caspase-3: a potential feedback loop for amplification of apoptosisassociated mitochondrial cytochrome c release. Cell Death Differ., 2000, 7(6), 556-565.
51. Adams, J.M.; Cory, S. Life-or-death decisions by the Bcl-2 protein family. Trends Biochem Sci., 2001, 26(1), 61-66.
52. Kakkar, P.; Singh, B.K. Mitochondria: a hub of redox activities and cellular distress control. Mol. Cell Biochem., 2007, 305(1-2), 235-253.
53. Scorrano, L.; Korsmeyer, S.J. Mechanisms of cytochrome c release by proapoptotic BCL-2 family members. Biochem. Biophys Res. Commun., 2003, 304(3), 437-444.
54. Shen, H.M.; Liu, Z.G. JNK signaling pathway is a key modulator in cell death mediated by reactive oxygen and nitrogen species. Free Radic Biol. Med., 2006, 40(6), 928-939.