Sphingosine Kinase-1 Involves the Inhibitory Action of HIF-1α by Chlorogenic Acid in Hypoxic DU145 Cells

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2017 Feb 7

PMID 28165392

Citations 12

Authors

Myoung-Sun Lee

Seon-Ok Lee

Kyu-Ri Kim

Hyo-Jeong Lee

Affiliations

Soon will be listed here.

Abstract

Hypoxia enhances cancer development in a solid tumor. Hypoxia-inducible factor-1 α (HIF-1α) is a transcription factor that is dominantly expressed under hypoxia in solid tumor cells and is a key factor that regulates tumor. HIF-1α regulates several target genes involved in many aspects of cancer progression, including angiogenesis, metastasis, anti-apoptosis and cell proliferation as well as imparts resistance to cancer treatment. In this study, we assessed Bunge var. typical Schneider ethanol extract (CPE) for its anti-cancer effects in hypoxia-induced DU145 human prostate cancer cell line. CPE decreased the abundance of HIF-1α and sphingosine kinase-1 (SPHK-1) in hypoxia-induced prostate cancer DU145 cells. CPE decreased HIF-1α and SPHK-1 as well as SPHK-1 activity. Chlorogenic acid (CA) is one of four major compounds of CPE. Compared to CPE, CA significantly decreased the expression of HIF-1α and SPHK-1 as well as SPHK-1 activity in hypoxia-induced DU145 cells. Furthermore, CA decreased phosphorylation AKT and GSK-3β, which are associated with HIF-1α stabilization and affected SPHK-1 in a concentration-dependent manner. We confirmed the mechanism of CA-induced inhibition of HIF-1α by SPHK-1 signaling pathway using SPHK-1 siRNA and SPHK inhibitor (SKI). CA decreased the secretion and cellular expression of VEGF, thus inhibiting hypoxia-induced angiogenesis. Treatment of DU145cells with SPHK1 siRNA and CA for 48 h decreased cancer cell growth, and the inhibitory action of SPHK siRNA and CA on cell growth was confirmed by decrease in the abundance of Proliferating cell nuclear antigen (PCNA).

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References

Shin I, Lee M, Lim H, Ha H, Seo C, Kim J . An extract of Crataegus pinnatifida fruit attenuates airway inflammation by modulation of matrix metalloproteinase-9 in ovalbumin induced asthma. PLoS One. 2012; 7(9):e45734. PMC: 3448716. DOI: 10.1371/journal.pone.0045734. View

Jia X, Fu Z, Yao J, Ma H . [Effects of chlorogenic acid on the viability and HIF-1alpha mRNA expression of PC12 cells exposed to hypoxia]. Zhong Yao Cai. 2014; 36(10):1644-7. View

Cho S, Cho S, Park E, Kim B, Sohn E, Oh B . Coumestrol suppresses hypoxia inducible factor 1α by inhibiting ROS mediated sphingosine kinase 1 in hypoxic PC-3 prostate cancer cells. Bioorg Med Chem Lett. 2014; 24(11):2560-4. DOI: 10.1016/j.bmcl.2014.03.084. View

Park J, Hwang S, Park J, Lee H . Chlorogenic acid inhibits hypoxia-induced angiogenesis via down-regulation of the HIF-1α/AKT pathway. Cell Oncol (Dordr). 2015; 38(2):111-8. DOI: 10.1007/s13402-014-0216-2. View

Shen W, Qi R, Zhang J, Wang Z, Wang H, Hu C . Chlorogenic acid inhibits LPS-induced microglial activation and improves survival of dopaminergic neurons. Brain Res Bull. 2012; 88(5):487-94. DOI: 10.1016/j.brainresbull.2012.04.010. View

Kao E, Wang C, Lin W, Chu C, Tseng T . Effects of polyphenols derived from fruit of Crataegus pinnatifida on cell transformation, dermal edema and skin tumor formation by phorbol ester application. Food Chem Toxicol. 2007; 45(10):1795-804. DOI: 10.1016/j.fct.2007.03.016. View

Wu J, Peng W, Qin R, Zhou H . Crataegus pinnatifida: chemical constituents, pharmacology, and potential applications. Molecules. 2014; 19(2):1685-712. PMC: 6271784. DOI: 10.3390/molecules19021685. View

Meng Z, Tang Z, Yan Y, Guo C, Cao L, Ding G . Study on the anti-gout activity of chlorogenic acid: improvement on hyperuricemia and gouty inflammation. Am J Chin Med. 2014; 42(6):1471-83. DOI: 10.1142/S0192415X1450092X. View

Lee S, Kim J, Lee M, Lee H . Anti-cancer effect of pristimerin by inhibition of HIF-1α involves the SPHK-1 pathway in hypoxic prostate cancer cells. BMC Cancer. 2016; 16:701. PMC: 5007821. DOI: 10.1186/s12885-016-2730-2. View

10.

Jurikova T, Sochor J, Rop O, Mlcek J, Balla S, Szekeres L . Polyphenolic profile and biological activity of Chinese hawthorn (Crataegus pinnatifida BUNGE) fruits. Molecules. 2012; 17(12):14490-509. PMC: 6268084. DOI: 10.3390/molecules171214490. View

11.

Huang W, Chen W, Zhang X . Glioblastoma multiforme: Effect of hypoxia and hypoxia inducible factors on therapeutic approaches. Oncol Lett. 2016; 12(4):2283-2288. PMC: 5038353. DOI: 10.3892/ol.2016.4952. View

12.

Teraoka M, Nakaso K, Kusumoto C, Katano S, Tajima N, Yamashita A . Cytoprotective effect of chlorogenic acid against α-synuclein-related toxicity in catecholaminergic PC12 cells. J Clin Biochem Nutr. 2012; 51(2):122-7. PMC: 3432822. DOI: 10.3164/jcbn.D-11-00030. View

13.

Chen C, Pore N, Behrooz A, Ismail-Beigi F, Maity A . Regulation of glut1 mRNA by hypoxia-inducible factor-1. Interaction between H-ras and hypoxia. J Biol Chem. 2000; 276(12):9519-25. DOI: 10.1074/jbc.M010144200. View

14.

Wang T, Zhang P, Zhao C, Zhang Y, Liu H, Hu L . Prevention effect in selenite-induced cataract in vivo and antioxidative effects in vitro of Crataegus pinnatifida leaves. Biol Trace Elem Res. 2010; 142(1):106-16. DOI: 10.1007/s12011-010-8752-8. View

15.

Ramachandran S, Ient J, Gottgens E, Krieg A, Hammond E . Epigenetic Therapy for Solid Tumors: Highlighting the Impact of Tumor Hypoxia. Genes (Basel). 2015; 6(4):935-56. PMC: 4690023. DOI: 10.3390/genes6040935. View

16.

Pang C, Sheng Y, Jiang P, Wei H, Ji L . Chlorogenic acid prevents acetaminophen-induced liver injury: the involvement of CYP450 metabolic enzymes and some antioxidant signals. J Zhejiang Univ Sci B. 2015; 16(7):602-10. PMC: 4506951. DOI: 10.1631/jzus.B1400346. View

17.

Chang Q, Zuo Z, Harrison F, Sum Chow M . Hawthorn. J Clin Pharmacol. 2002; 42(6):605-12. DOI: 10.1177/00970002042006003. View

18.

Du W, Chang C, Zhang Y, Liu Y, Sun K, Wang C . High-dose chlorogenic acid induces inflammation reactions and oxidative stress injury in rats without implication of mast cell degranulation. J Ethnopharmacol. 2013; 147(1):74-83. DOI: 10.1016/j.jep.2013.01.042. View

19.

Cui T, Li J, Kayahara H, Ma L, Wu L, Nakamura K . Quantification of the polyphenols and triterpene acids in chinese hawthorn fruit by high-performance liquid chromatography. J Agric Food Chem. 2006; 54(13):4574-81. DOI: 10.1021/jf060310m. View

20.

Cho S, Lee H, Jeong S, Lee H, Kim H, Chen C . Sphingosine kinase 1 pathway is involved in melatonin-induced HIF-1α inactivation in hypoxic PC-3 prostate cancer cells. J Pineal Res. 2011; 51(1):87-93. DOI: 10.1111/j.1600-079X.2011.00865.x. View