Naringenin causes ASK1-induced apoptosis via reactive oxygen species in human pancreatic cancer cells

Food and Chemical Toxicology

Volumn 99, Issue , 2017, Pages 1-8

  Park, Hyun Jin ^a   Choi, Yong Jun ^a   Lee, Jeong Hyun ^a   Nam, Myeong Jin ^a  

^a Gachon University   (South Korea)

Author keywords

Apoptosis signal regulation kinase 1; Naringenin; Pancreatic cancer; Peroxiredoxin 1; Reactive oxygen species

Indexed keywords

APOPTOSIS SIGNAL REGULATING KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; NARINGENIN; PEROXIREDOXIN 1; PROTEIN P53; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; ANTIESTROGEN; FLAVANONE DERIVATIVE; MAP3K5 PROTEIN, HUMAN; MESSENGER RNA; P53 PROTEIN (325-355), HUMAN; PEPTIDE FRAGMENT; PEROXIREDOXIN; PRDX1 PROTEIN, HUMAN;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME INHIBITION; HOMEOSTASIS; HUMAN; HUMAN CELL; PANCREATIC CANCER CELL LINE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SNU 213 CELL LINE; TWO DIMENSIONAL ELECTROPHORESIS; UPREGULATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PANCREATIC NEOPLASMS; PATHOLOGY; PROCEDURES; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL CULTURE; TWO DIMENSIONAL GEL ELECTROPHORESIS; WESTERN BLOTTING;

APOPTOSIS; BLOTTING, WESTERN; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ESTROGEN ANTAGONISTS; FLAVANONES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE KINASE 5; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PANCREATIC NEOPLASMS; PEPTIDE FRAGMENTS; PEROXIREDOXINS; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 84995380655     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2016.11.008     Document Type: Article

References (32)

1. Birt, D.F., Hendrich, S., Wang, W., Dietary agents in cancer prevention: flavonoids and isoflavonoids. Pharmacol. Ther. 90 (2001), 157–177.
2. Burris, H.A. 3rd, Moore, M.J., Andersen, J., Green, M.R., Rothenberg, M.L., Modiano, M.R., Cripps, M.C., Portenoy, R.K., Storniolo, A.M., Tarassoff, P., Nelson, R., Dorr, F.A., Stephens, C.D., Von Hoff, D.D., Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J. Clin. Oncol. 15 (1997), 2403–2413.
3. Cathcart, R., Schwiers, E., Ames, B.N., Detection of picomole levels of hydroperoxides using a fluorescent dichlorofluorescein assay. Anal. Biochem. 134 (1983), 111–116.
4. Chen, M.F., Keng, P.C., Shau, H., Wu, C.T., Hu, Y.C., Liao, S.K., Chen, W.C., Inhibition of lung tumor growth and augmentation of radiosensitivity by decreasing peroxiredoxin I expression. Int. J. Radiat. Oncol. Biol. Phys. 64 (2006), 581–591.
5. Feng, W., Zhang, B., Cai, D.W., Zou, X.P., Therapeutic potential of histone deacetylase inhibitors in pancreatic cancer. Cancer Lett. 347 (2014), 183–190.
6. Frydoonfar, H.R., McGrath, D.R., Spigelman, A.D., The variable effect on proliferation of a colon cancer cell line by the citrus fruit flavonoid Naringenin. Colorectal disease: official J. Assoc. Coloproctology G. B. Irel. 5 (2003), 149–152.
7. Fujino, G., Noguchi, T., Matsuzawa, A., Yamauchi, S., Saitoh, M., Takeda, K., Ichijo, H., Thioredoxin and TRAF family proteins regulate reactive oxygen species-dependent activation of ASK1 through reciprocal modulation of the N-terminal homophilic interaction of ASK1. Mol. Cell. Biol. 27 (2007), 8152–8163.
8. Harmon, A.W., Patel, Y.M., Naringenin inhibits glucose uptake in MCF-7 breast cancer cells: a mechanism for impaired cellular proliferation. Breast cancer Res. Treat. 85 (2004), 103–110.
9. Hassan, M., Feyen, O., Grinstein, E., Fas-induced apoptosis of renal cell carcinoma is mediated by apoptosis signal-regulating kinase 1 via mitochondrial damage-dependent caspase-8 activation. Cell Oncol. 31 (2009), 437–456.
10. Hatkevich, T., Ramos, J., Santos-Sanchez, I., Patel, Y.M., A naringenin-tamoxifen combination impairs cell proliferation and survival of MCF-7 breast cancer cells. Exp. cell Res. 327 (2014), 331–339.
11. Hayakawa, R., Hayakawa, T., Takeda, K., Ichijo, H., Therapeutic targets in the ASK1-dependent stress signaling pathways. Proceedings of the Japan Academy. Series B. Phys. Biol. Sci. 88 (2012), 434–453.
12. Heo, H.J., Kim, D.O., Shin, S.C., Kim, M.J., Kim, B.G., Shin, D.H., Effect of antioxidant flavanone, naringenin, from Citrus junos on neuroprotection. J. Agr Food Chem. 52 (2004), 1520–1525.
13. Hollung, K., Veiseth, E., Jia, X., Faergestad, E.M., Hildrum, K.I., Application of proteomics to understand the molecular mechanisms behind meat quality. Meat Sci. 77 (2007), 97–104.
14. Jemal, A., Siegel, R., Xu, J.Q., Ward, E., Cancer statistics, 2010. Ca-Cancer J. Clin. 60 (2010), 277–300.
15. Jeon, Y.K., Yoo, D.R., Jang, Y.H., Jang, S.Y., Nam, M.J., Sulforaphane induces apoptosis in human hepatic cancer cells through inhibition of 6-phosphofructo-2-kinase/fructose-2,6-biphosphatase4, mediated by hypoxia inducible factor-1-dependent pathway. Biochim. biophysica acta 1814 (2011), 1340–1348.
16. Jeong, K.W., Lee, J., Kang, D.I., Lee, J.U., Shin, S.Y., Kim, Y., Screening of flavonoids as candidate antibiotics against Enterococcus faecalis. J. Nat. Prod. 72 (2009), 719–724.
17. Kale, A., Gawande, S., Kotwal, S., Cancer phytotherapeutics: role for flavonoids at the cellular level. Phytotherapy research. PTR 22 (2008), 567–577.
18. Kim, J.H., Bogner, P.N., Baek, S.H., Ramnath, N., Liang, P., Kim, H.R., Andrews, C., Park, Y.M., Up-regulation of peroxiredoxin 1 in lung cancer and its implication as a prognostic and therapeutic target. Clin. Cancer Res. 14 (2008), 2326–2333.
19. Kim, S.Y., Kim, T.J., Lee, K.Y., A novel function of peroxiredoxin 1 (Prx-1) in apoptosis signal-regulating kinase 1 (ASK1)-mediated signaling pathway. FEBS Lett. 582 (2008), 1913–1918.
20. Lee, J.H., Park, C.H., Jung, K.C., Rhee, H.S., Yang, C.H., Negative regulation of beta-catenin/Tcf signaling by naringenin in AGS gastric cancer cell. Biochem. Biophys. Res. Commun. 335 (2005), 771–776.
21. Ma, Q., Xie, H., Li, S., Zhang, R., Zhang, M., Wei, X., Flavonoids from the pericarps of Litchi chinensis. J. Agric. Food Chem. 62 (2014), 1073–1078.
22. Maheswari, E., Saraswathy, G.R., Santhranii, T., Hepatoprotective and antioxidant activity of N-acetyl cysteine in carbamazepine-administered rats. Indian J. Pharmacol. 46 (2014), 211–215.
23. Ou, Y.C., Kuan, Y.H., Li, J.R., Raung, S.L., Wang, C.C., Hung, Y.Y., Chen, C.J., Induction of apoptosis by luteolin involving akt inactivation in human 786-o renal cell carcinoma cells. Evid. Based Complement. Altern. Med., 2013, 2013, 109105.
24. Paredes, A., Alzuru, M., Mendez, J., Rodriguez-Ortega, M., Anti-Sindbis activity of flavanones hesperetin and naringenin. Biol. Pharm. Bull. 26 (2003), 108–109.
25. Riddell, J.R., Bshara, W., Moser, M.T., Spernyak, J.A., Foster, B.A., Gollnick, S.O., Peroxiredoxin 1 controls prostate Cancer growth through toll-like receptor 4-Dependent regulation of tumor vasculature. Cancer Res. 71 (2011), 1637–1646.
26. Ryan, P., Hynes, M.J., The kinetics and mechanisms of the reactions of iron(III) with quercetin and morin. J. Inorg. Biochem. 102 (2008), 127–136.
27. Sachdeva, S., Pant, S.C., Kushwaha, P., Bhargava, R., Flora, S.J., Sodium tungstate induced neurological alterations in rat brain regions and their response to antioxidants. Food and chemical toxicology. Int. J. Publ. Br. Ind. Biol. Res. Assoc. 82 (2015), 64–71.
28. Siegel, R., Naishadham, D., Jemal, A., Cancer statistics, 2012. Ca-Cancer J. Clin. 62 (2012), 10–29.
29. Slimestad, R., Verheul, M., Properties of chalconaringenin and rutin isolated from cherry tomatoes. J. Agric. Food Chem. 59 (2011), 3180–3185.
30. Totta, P., Acconcia, F., Leone, S., Cardillo, I., Marino, M., Mechanisms of naringenin-induced apoptotic cascade in cancer cells: involvement of estrogen receptor alpha and beta signalling. IUBMB life 56 (2004), 491–499.
31. Witkowski, P.T., Schuenadel, L., Wiethaus, J., Bourquain, D.R., Kurth, A., Nitsche, A., Cellular impedance measurement as a new tool for poxvirus titration, antibody neutralization testing and evaluation of antiviral substances. Biochem. Biophys. Res. Commun. 401 (2010), 37–41.
32. Zi, X., Feyes, D.K., Agarwal, R., Anticarcinogenic effect of a flavonoid antioxidant, silymarin, in human breast cancer cells MDA-MB 468: induction of G1 arrest through an increase in Cip1/p21 concomitant with a decrease in kinase activity of cyclin-dependent kinases and associated cyclins. Clin. Cancer Res. 4 (1998), 1055–1064.