Kaempferol inhibits cell proliferation and glycolysis in esophagus squamous cell carcinoma via targeting EGFR signaling pathway

Tumor Biology

Volumn 37, Issue 8, 2016, Pages 10247-10256

  Yao, Shihua ^a,b   Wang, Xiaowei ^b   Li, Chunguang ^b   Zhao, Tiejun ^b   Jin, Hai ^b   Fang, Wentao ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

EGFR; Esophagus squamous cell carcinoma; Glycolysis; Hexokinase 2; Kaempferol

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; HEXOKINASE; KAEMPFEROL; LACTIC ACID; PROTEIN HEXOKINASE 2; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; EGFR PROTEIN, HUMAN; KAEMPFEROL DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CELL CYCLE G0 PHASE; CELL CYCLE REGULATION; CELL PROLIFERATION; CLONOGENESIS; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; DOWNSTREAM PROCESSING; DRUG TARGETING; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; FEMALE; FLOW CYTOMETRY; G1 PHASE CELL CYCLE CHECKPOINT; GLUCOSE TRANSPORT; GLYCOLYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; SIGNAL TRANSDUCTION; TUMOR CELL; TUMOR XENOGRAFT; ANIMAL; BAGG ALBINO MOUSE; DRUG EFFECTS; DRUG SCREENING; ESOPHAGUS TUMOR; IMMUNOHISTOCHEMISTRY; METABOLISM; PATHOLOGY; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE; WESTERN BLOTTING;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL PROLIFERATION; ESOPHAGEAL NEOPLASMS; FEMALE; FLOW CYTOMETRY; GLYCOLYSIS; HUMANS; IMMUNOHISTOCHEMISTRY; KAEMPFEROLS; MICE; MICE, INBRED BALB C; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84983613474     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-016-4912-6     Document Type: Article

References (46)

1. Domper Arnal MJ, Ferrandez Arenas A, Lanas Arbeloa A. Esophageal cancer: risk factors, screening and endoscopic treatment in western and eastern countries. World J Gastroenterol. 2015;21:7933–43.
2. Enzinger PC, Mayer RJ. Esophageal cancer. N Engl J Med. 2003;349:2241–52.
3. Somerset SM, Johannot L. Dietary flavonoid sources in Australian adults. Nutr Cancer. 2008;60:442–9.
4. Seifried HE, Anderson DE, Fisher EI, Milner JA. A review of the interaction among dietary antioxidants and reactive oxygen species. J Nutr Biochem. 2007;18:567–79.
5. Azevedo C, Correia-Branco A, Araujo JR, Guimaraes JT, Keating E, Martel F. The chemopreventive effect of the dietary compound kaempferol on the mcf-7 human breast cancer cell line is dependent on inhibition of glucose cellular uptake. Nutr Cancer. 2015;67:504–13.
6. Diantini A, Subarnas A, Lestari K, Halimah E, Susilawati Y, Supriyatna, et al. Kaempferol-3-O-rhamnoside isolated from the leaves of Schima wallichii Korth. inhibits MCF-7 breast cancer cell proliferation through activation of the caspase cascade pathway. Oncol Lett. 2012;3:1069–72.
7. Huang WW, Tsai SC, Peng SF, Lin MW, Chiang JH, Chiu YJ, et al. Kaempferol induces autophagy through ampk and akt signaling molecules and causes g2/m arrest via downregulation of cdk1/cyclin b in sk-hep-1 human hepatic cancer cells. Int J Oncol. 2013;42:2069–77.
8. Mylonis I, Lakka A, Tsakalof A, Simos G. The dietary flavonoid kaempferol effectively inhibits hif-1 activity and hepatoma cancer cell viability under hypoxic conditions. Biochem Biophys Res Commun. 2010;398:74–8.
9. Cho HJ, Park JH. Kaempferol induces cell cycle arrest in ht-29 human colon cancer cells. J Cancer Prev. 2013;18:257–63.
10. Lee HS, Cho HJ, Yu R, Lee KW, Chun HS, Park JH. Mechanisms underlying apoptosis-inducing effects of kaempferol in ht-29 human colon cancer cells. Int J Mol Sci. 2014;15:2722–37.
11. Luo H, Rankin GO, Liu L, Daddysman MK, Jiang BH, Chen YC. Kaempferol inhibits angiogenesis and vegf expression through both hif dependent and independent pathways in human ovarian cancer cells. Nutr Cancer. 2009;61:554–63.
12. Luo H, Rankin GO, Li Z, Depriest L, Chen YC. Kaempferol induces apoptosis in ovarian cancer cells through activating p53 in the intrinsic pathway. Food Chem. 2011;128:513–9.
13. Halimah E, Diantini A, Destiani DP, Pradipta IS, Sastramihardja HS, Lestari K, et al. Induction of caspase cascade pathway by kaempferol-3-rhamnoside in lncap prostate cancer cell lines. Biomed Rep. 2015;3:115–7.
14. Wu LY, Lu HF, Chou YC, Shih YL, Bau DT, Chen JC, et al. Kaempferol induces DNA damage and inhibits DNA repair associated protein expressions in human promyelocytic leukemia hl-60 cells. Am J Chin Med. 2015;43:365–82.
15. Song W, Dang Q, Xu D, Chen Y, Zhu G, Wu K, et al. Kaempferol induces cell cycle arrest and apoptosis in renal cell carcinoma through egfr/p38 signaling. Oncol Rep. 2014;31:1350–6.
16. Huang WW, Chiu YJ, Fan MJ, Lu HF, Yeh HF, Li KH, et al. Kaempferol induced apoptosis via endoplasmic reticulum stress and mitochondria-dependent pathway in human osteosarcoma u-2 os cells. Mol Nutr Food Res. 2010;54:1585–95.
17. Filomeni G, Desideri E, Cardaci S, Graziani I, Piccirillo S, Rotilio G, et al. Carcinoma cells activate amp-activated protein kinase-dependent autophagy as survival response to kaempferol-mediated energetic impairment. Autophagy. 2010;6:202–16.
18. Luo H, Rankin GO, Juliano N, Jiang BH, Chen YC. Kaempferol inhibits vegf expression and in vitro angiogenesis through a novel erk-nfkappab-cmyc-p21 pathway. Food Chem. 2012;130:321–8.
19. Ganapathy-Kanniappan S, Geschwind JF. Tumor glycolysis as a target for cancer therapy: progress and prospects. Mol Cancer. 2013;12:152.
20. Wilson JE. Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function. J Exp Biol. 2003;206:2049–57.
21. Mathupala SP, Rempel A, Pedersen PL. Glucose catabolism in cancer cells. Isolation, sequence, and activity of the promoter for type II hexokinase. J Biol Chem. 1995;270:16918–25.
22. Suh DH, Kim MA, Kim H, Kim MK, Kim HS, Chung HH, et al. Association of overexpression of hexokinase II with chemoresistance in epithelial ovarian cancer. Clin Exp Med. 2014;14:345–53.
23. Rho M, Kim J, Jee CD, Lee YM, Lee HE, Kim MA, et al. Expression of type 2 hexokinase and mitochondria-related genes in gastric carcinoma tissues and cell lines. Anticancer Res. 2007;27:251–8.
24. Palmieri D, Fitzgerald D, Shreeve SM, Hua E, Bronder JL, Weil RJ, et al. Analyses of resected human brain metastases of breast cancer reveal the association between up-regulation of hexokinase 2 and poor prognosis. Mol Cancer Res: MCR. 2009;7:1438–45.
25. Fonteyne P, Casneuf V, Pauwels P, Van Damme N, Peeters M, Dierckx R, et al. Expression of hexokinases and glucose transporters in treated and untreated oesophageal adenocarcinoma. Histol Histopathol. 2009;24:971–7.
26. Peng SY, Lai PL, Pan HW, Hsiao LP, Hsu HC. Aberrant expression of the glycolytic enzymes aldolase b and type II hexokinase in hepatocellular carcinoma are predictive markers for advanced stage, early recurrence and poor prognosis. Oncol Rep. 2008;19:1045–53.
27. Ogawa H, Nagano H, Konno M, Eguchi H, Koseki J, Kawamoto K, et al. The combination of the expression of hexokinase 2 and pyruvate kinase m2 is a prognostic marker in patients with pancreatic cancer. Mol Clin Oncol. 2015;3:563–71.
28. Hamabe A, Yamamoto H, Konno M, Uemura M, Nishimura J, Hata T, et al. Combined evaluation of hexokinase 2 and phosphorylated pyruvate dehydrogenase-e1alpha in invasive front lesions of colorectal tumors predicts cancer metabolism and patient prognosis. Cancer Sci. 2014;105:1100–8.
29. Wang J, Yu JM, Jing SW, Guo Y, Wu YJ, Li N, et al. Relationship between egfr over-expression and clinicopathologic characteristics in squamous cell carcinoma of the esophagus: a meta-analysis. Asian Pac J Cancer Prev: APJCP. 2014;15:5889–93.
30. Aichler M, Motschmann M, Jutting U, Luber B, Becker K, Ott K, et al. Epidermal growth factor receptor (egfr) is an independent adverse prognostic factor in esophageal adenocarcinoma patients treated with cisplatin-based neoadjuvant chemotherapy. Oncotarget. 2014;5:6620–32.
31. Gates MA, Tworoger SS, Hecht JL, De Vivo I, Rosner B, Hankinson SE. A prospective study of dietary flavonoid intake and incidence of epithelial ovarian cancer. Int J Cancer J Int Cancer. 2007;121:2225–32.
32. Nothlings U, Murphy SP, Wilkens LR, Henderson BE, Kolonel LN. Flavonols and pancreatic cancer risk: the multiethnic cohort study. Am J Epidemiol. 2007;166:924–31.
33. Garcia-Closas R, Gonzalez CA, Agudo A, Riboli E. Intake of specific carotenoids and flavonoids and the risk of gastric cancer in Spain. Cancer Causes Control: CCC. 1999;10:71–5.
34. Bobe G, Sansbury LB, Albert PS, Cross AJ, Kahle L, Ashby J, et al. Dietary flavonoids and colorectal adenoma recurrence in the polyp prevention trial. Cancer Epidemiol, Biomarkers Prev: Publ Am Assoc Cancer Res, Cosponsored Am Soc Prev Oncol. 2008;17:1344–53.
35. Zhang Q, Zhao XH, Wang ZJ. Cytotoxicity of flavones and flavonols to a human esophageal squamous cell carcinoma cell line (kyse-510) by induction of g2/m arrest and apoptosis. Toxicol In Vitro: Int J Published Assoc BIBRA. 2009;23:797–807.
36. Pastorino JG, Shulga N, Hoek JB. Mitochondrial binding of hexokinase II inhibits bax-induced cytochrome c release and apoptosis. J Biol Chem. 2002;277:7610–8.
37. Majewski N, Nogueira V, Bhaskar P, Coy PE, Skeen JE, Gottlob K, et al. Hexokinase-mitochondria interaction mediated by akt is required to inhibit apoptosis in the presence or absence of bax and bak. Mol Cell. 2004;16:819–30.
38. Krasnov GS, Dmitriev AA, Lakunina VA, Kirpiy AA, Kudryavtseva AV. Targeting vdac-bound hexokinase II: a promising approach for concomitant anti-cancer therapy. Expert Opin Ther Targets. 2013;17:1221–33.
39. Xie F, Su M, Qiu W, Zhang M, Guo Z, Su B, et al. Kaempferol promotes apoptosis in human bladder cancer cells by inducing the tumor suppressor, pten. Int J Mol Sci. 2013;14:21215–26.
40. Law AA, Collie-Duguid ES, Smith TA. Influence of resistance to 5-fluorouracil and tomudex on [18f]fdg incorporation, glucose transport and hexokinase activity. Int J Oncol. 2012;41:378–82.
41. Jiang JX, Gao S, Pan YZ, Yu C, Sun CY. Overexpression of microrna-125b sensitizes human hepatocellular carcinoma cells to 5-fluorouracil through inhibition of glycolysis by targeting hexokinase II. Mol Med Rep. 2014;10:995–1002.
42. Peng Q, Zhou J, Zhou Q, Pan F, Zhong D, Liang H. Silencing hexokinase II gene sensitizes human colon cancer cells to 5-fluorouracil. Hepato-Gastroenterology. 2009;56:355–60.
43. Makinoshima H, Takita M, Matsumoto S, Yagishita A, Owada S, Esumi H, et al. Epidermal growth factor receptor (egfr) signaling regulates global metabolic pathways in egfr-mutated lung adenocarcinoma. J Biol Chem. 2014;289:20813–23.
44. De Rosa V, Iommelli F, Monti M, Fonti R, Votta G, Stoppelli MP, et al. Reversal of Warburg effect and reactivation of oxidative phosphorylation by differential inhibition of egfr signaling pathways in non-small cell lung cancer. Clin Cancer Res: Off J Am Assoc Cancer Res. 2015;21:5110–20.
45. Chen GQ, Tang CF, Shi XK, Lin CY, Fatima S, Pan XH, et al. Halofuginone inhibits colorectal cancer growth through suppression of akt/mtorc1 signaling and glucose metabolism. Oncotarget. 2015;6:24148–62.
46. Zhuo B, Li Y, Li Z, Qin H, Sun Q, Zhang F, et al. Pi3k/akt signaling mediated hexokinase-2 expression inhibits cell apoptosis and promotes tumor growth in pediatric osteosarcoma. Biochem Biophys Res Commun. 2015;464:401–6.