Chlorogenic acid inhibits hypoxia-induced angiogenesis via down-regulation of the HIF-1α/AKT pathway

Cellular Oncology

Volumn 38, Issue 2, 2015, Pages 111-118

  Park, Jin Ju ^a   Hwang, Su Jung ^a   Park, Ji Hyeon ^b   Lee, Hyo Jong ^a  

^a Inje University   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

Angiogenesis; Chlorogenic acid; HIF 1; VEGF

Indexed keywords

ANTINEOPLASTIC AGENT; CHLOROGENIC ACID; HIF1A PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROTEIN KINASE B;

ANIMAL; C57BL MOUSE; CELL HYPOXIA; DOWN REGULATION; DRUG EFFECTS; HUMAN; IMMUNOHISTOCHEMISTRY; METABOLISM; MOUSE; NEOVASCULARIZATION (PATHOLOGY); PATHOPHYSIOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR CELL LINE; WESTERN BLOTTING;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CELL HYPOXIA; CELL LINE, TUMOR; CHLOROGENIC ACID; DOWN-REGULATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PATHOLOGIC; PROTO-ONCOGENE PROTEINS C-AKT; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 84939969985     PISSN: 22113428     EISSN: 22113436     Source Type: Journal    
DOI: 10.1007/s13402-014-0216-2     Document Type: Article

References (45)

1. O. Thews, T. Wolloscheck, W. Dillenburg, S. Kraus, D.K. Kelleher, M.A. Konerding, P. Vaupel, Microenvironmental adaptation of experimental tumours to chronic vs acute hypoxia. Br. J. Cancer 91, 1181–1189 (2004)
2. H.J. Lee, C.H. Jeong, J.H. Cha, K.W. Kim, PKC-delta inhibitors sustain self-renewal of mouse embryonic stem cells under hypoxia in vitro. Exp. Mol. Med. 42, 294–301 (2010)
3. L. Ostergaard, A. Tietze, T. Nielsen, K.R. Drasbek, K. Mouridsen, S.N. Jespersen, M.R. Horsman, The relationship between tumor blood flow, angiogenesis, tumor hypoxia, and aerobic glycolysis. Cancer Res. 73, 5618–5624 (2013)
4. M. Hou, J. Cui, J. Liu, F. Liu, R. Jiang, K. Liu, Y. Wang, L. Yin, W. Liu, B. Yu, Angiopoietin-like 4 confers resistance to hypoxia/serum deprivation-induced apoptosis through PI3K/Akt and ERK1/2 signaling pathways in mesenchymal stem cells. PLoS One 9, e85808 (2014)
5. Y. Zheng, Y. Ni, X. Huang, Z. Wang, W. Han, Overexpression of HIF-1alpha indicates a poor prognosis in tongue carcinoma and may be associated with tumour metastasis. Oncol. Lett. 5, 1285–1289 (2013)
6. M. Yan, M. Rayoo, E.A. Takano, K.C. Investigators, S.B. Fox, BRCA1 tumours correlate with a HIF-1alpha phenotype and have a poor prognosis through modulation of hydroxylase enzyme profile expression. Br. J. Cancer 101, 1168–1174 (2009)
7. X.B. Wan, X.J. Fan, M.Y. Chen, J. Xiang, P.Y. Huang, L. Guo, X.Y. Wu, J. Xu, Z.J. Long, Y. Zhao, W.H. Zhou, H.Q. Mai, Q. Liu, M.H. Hong, Elevated Beclin 1 expression is correlated with HIF-1alpha in predicting poor prognosis of nasopharyngeal carcinoma. Autophagy 6, 395–404 (2010)
8. J.Y. Park, H.J. Jung, I. Seo, B.K. Jha, S.I. Suh, M.H. Suh, W.K. Baek, Translational suppression of HIF-1alpha by miconazole through the mTOR signaling pathway. Cell. Oncol. 37, 269–279 (2014)
9. X.S. Huang, TLC densitometry of chlorogenic acid in granules of Artemisia capillaris in the treatment of jaundice. Zhong Yao Tong Bao 10, 30–32 (1985)
10. A. Nugroho, S.C. Lim, S. Karki, J.S. Choi, H.J. Park, Simultaneous quantification and validation of new peroxynitrite scavengers from Artemisia iwayomogi. Pharm. Biol. 4, 1–9 (2014)
11. B.C. Cheng, X.Q. Ma, H.Y. Kwan, K.W. Tse, H.H. Cao, T. Su, X. Shu, Z.Z. Wu, Z.L. Yu, A herbal formula consisting of Rosae Multiflorae Fructus and Lonicerae Japonicae Flos inhibits inflammatory mediators in LPS-stimulated RAW 264.7 macrophages. J. Ethnopharmacol. 153, 922–927 (2014)
12. W.Y. Du, C. Chang, Y. Zhang, Y.Y. Liu, K. Sun, C.S. Wang, M.X. Wang, Y. Liu, F. Wang, J.Y. Fan, P.T. Li, J.Y. Han, High-dose chlorogenic acid induces inflammation reactions and oxidative stress injury in rats without implication of mast cell degranulation. J. Ethnopharmacol. 147, 74–83 (2013)
13. S. Bhattacharyya, S. Majhi, B.P. Saha, P.K. Mukherjee, Chlorogenic acid-phospholipid complex improve protection against UVA induced oxidative stress. J. Photochem. Photobiol. B 130, 293–298 (2014)
14. M. Teraoka, K. Nakaso, C. Kusumoto, S. Katano, N. Tajima, A. Yamashita, T. Zushi, S. Ito, T. Matsura, Cytoprotective effect of chlorogenic acid against α-synuclein-related toxicity in catecholaminergic PC12 cells. J. Clin. Biochem. Nutr. 51, 122–127 (2012)
15. W. Shen, R. Qi, J. Zhang, Z. Wang, H. Wang, C. Hu, Y. Zhao, M. Bie, Y. Wang, Y. Fu, M. Chen, D. Lu, Chlorogenic acid inhibits LPS-induced microglial activation and improves survival of dopaminergic neurons. Brain Res. Bull. 88, 487–494 (2012)
16. S.J. Hwang, Y.W. Kim, Y. Park, H.J. Lee, K.W. Kim, Anti-inflammatory effects of chlorogenic acid in lipopolysaccharide-stimulated RAW 264.7 cells. Inflamm. Res. 63, 81–90 (2014)
17. L. Yang, J. Zhang, C. Wang, X. Qin, Q. Yu, Y. Zhou, J. Liu, Interaction between 8-hydroxyquinoline ruthenium(II) complexes and basic fibroblast growth factors (bFGF): inhibiting angiogenesis and tumor growth through ERK and AKT signaling pathways. Metallomics 6, 518–531 (2014)
18. G.D. Kim, J. Oh, L.S. Jeong, S.K. Lee, Thio-Cl-IB-MECA, a novel A(3) adenosine receptor agonist, suppresses angiogenesis by regulating PI3K/AKT/mTOR and ERK signaling in endothelial cells. Biochem. Biophys. Res. Commun. 437, 79–86 (2013)
19. D. Sun, Y. Liu, Q. Yu, Y. Zhou, R. Zhang, X. Chen, A. Hong, J. Liu, The effects of luminescent ruthenium(II) polypyridyl functionalized selenium nanoparticles on bFGF-induced angiogenesis and AKT/ERK signaling. Biomaterials 34, 171–180 (2013)
20. S. Kan, W.M. Cheung, Y. Zhou, W.S. Ho, Enhancement of doxorubicin cytotoxicity by tanshinone IIA in HepG2 human hepatoma cells. Planta Med. 80, 70–76 (2014)
21. S.R. Gundala, C. Yang, N. Lakshminarayana, G. Asif, M.V. Gupta, S. Shamsi, R. Aneja, Polar biophenolics in sweet potato greens extract synergize to inhibit prostate cancer cell proliferation and in vivo tumor growth. Carcinogenesis 34, 2039–2049 (2013)
22. Y.J. Liu, C.Y. Zhou, C.H. Qiu, X.M. Lu, Y.T. Wang, Chlorogenic acid induced apoptosis and inhibition of proliferation in human acute promyelocytic leukemia HL60 cells. Mol. Med. Rep. 8, 1106–1110 (2013)
23. J.S. Yang, C.W. Liu, Y.S. Ma, S.W. Weng, N.Y. Tang, S.H. Wu, B.C. Ji, C.Y. Ma, Y.C. Ko, S. Funayama, C.L. Kuo, Chlorogenic acid induces apoptotic cell death in U937 leukemia cells through caspase- and mitochondria-dependent pathways. In Vivo 26, 971–978 (2012)
24. E. Burgos-Moron, J.M. Calderon-Montano, M.L. Orta, N. Pastor, C. Perez-Guerrero, C. Austin, S. Mateos, M. Lopez-Lazaro, The coffee constituent chlorogenic acid induces cellular DNA damage and formation of topoisomerase I- and II-DNA complexes in cells. J. Agric. Food Chem. 60, 7384–7391 (2012)
25. Q. Wang, Q. Chen, M. He, P. Mir, J. Su, Q. Yang, Inhibitory effect of antioxidant extracts from various potatoes on the proliferation of human colon and liver cancer cells. Nutr. Cancer 63, 1044–1052 (2011)
26. C. Narayan, A. Kumar, Antineoplastic and immunomodulatory effect of polyphenolic components of Achyranthes aspera (PCA) extract on urethane induced lung cancer in vivo. Mol. Biol. Rep. 41, 179–191 (2014)
27. M. Cichocki, M. Dalek, M. Szamalek, W. Baer-Dubowska, Naturally occurring phenolic acids modulate TPA-induced activation of EGFR, AP-1, and STATs in mouse epidermis. Nutr. Cancer 66, 308–314 (2014)
28. S.D. Young, R.P. Hill, Effects of reoxygenation on cells from hypoxic regions of solid tumors: anticancer drug sensitivity and metastatic potential. J. Natl. Cancer Inst. 82, 371–380 (1990)
29. J.D. Chapman, The detection and measurement of hypoxic cells in solid tumors. Cancer 54, 2441–2449 (1984)
30. C. Kim, H.G. Yu, J. Sohn, The anti-angiogenic effect of chlorogenic acid on choroidal neovascularization. Korean J. Ophthalmol. 24, 163–168 (2010)
31. J.Y. Shin, J. Sohn, K.H. Park, Chlorogenic acid decreases retinal vascular hyperpermeability in diabetic rat model. J. Korean Med. Sci. 28, 608–613 (2013)
32. D. Bagdas, B. Cam Etoz, S. Inan Ozturkoglu, N. Cinkilic, M.O. Ozyigit, Z. Gul, N. Isbil Buyukcoskun, K. Ozluk, M.S. Gurun, Effects of systemic chlorogenic acid on random-pattern dorsal skin flap survival in diabetic rats. Biol. Pharm. Bull. 37, 361–370 (2014)
33. W.C. Chen, S.S. Liou, T.F. Tzeng, S.L. Lee, I.M. Liu, Effect of topical application of chlorogenic acid on excision wound healing in rats. Planta Med. 79, 616–621 (2013)
34. J. Fensterle, B. Aicher, I. Seipelt, M. Teifel, J. Engel, Current view on the mechanism of action of perifosine in cancer. Anti Cancer Agents Med. Chem. 14, 629–635 (2014)
35. P. Bhoopathi, B. Gorantla, G.S. Sailaja, C.S. Gondi, M. Gujrati, J.D. Klopfenstein, J.S. Rao, SPARC overexpression inhibits cell proliferation in neuroblastoma and is partly mediated by tumor suppressor protein PTEN and AKT. PLoS One 7, e36093 (2012)
36. Y.J. Cheng, J.W. Tsai, K.C. Hsieh, Y.C. Yang, Y.J. Chen, M.S. Huang, S.S. Yuan, Id1 promotes lung cancer cell proliferation and tumor growth through Akt-related pathway. Cancer Lett. 307, 191–199 (2011)
37. S.L. Locatelli, A. Giacomini, A. Guidetti, L. Cleris, R. Mortarini, A. Anichini, A.M. Gianni, C. Carlo-Stella, Perifosine and sorafenib combination induces mitochondrial cell death and antitumor effects in NOD/SCID mice with Hodgkin lymphoma cell line xenografts. Leukemia 27, 1677–1687 (2013)
38. R. Voltan, C. Celeghini, E. Melloni, P. Secchiero, G. Zauli, Perifosine plus nutlin-3 combination shows a synergistic anti-leukaemic activity. Br. J. Haematol. 148, 957–961 (2010)
39. R.L. Vinall, K. Hwa, P. Ghosh, C.X. Pan, P.N. Lara Jr., R.W. de Vere White, Combination treatment of prostate cancer cell lines with bioactive soy isoflavones and perifosine causes increased growth arrest and/or apoptosis. Clin. Cancer Res. 13, 6204–6216 (2007)
40. P. Wang, L. Han, H. Shen, P. Wang, C. Lv, G. Zhao, J. Niu, L. Xue, Q.J. Wang, T. Tong, J. Chen, Protein kinase D1 is essential for Ras-induced senescence and tumor suppression by regulating senescence-associated inflammation. Proc. Natl. Acad. Sci. U. S. A. 111, 7683–7688 (2014)
41. A.E. Harvey, L.M. Lashinger, D. Hays, L.M. Harrison, K. Lewis, S.M. Fischer, S.D. Hursting, Calorie restriction decreases murine and human pancreatic tumor cell growth, nuclear factor-kappaB activation, and inflammation-related gene expression in an insulin-like growth factor-1-dependent manner. PLoS One 9, e94151 (2014)
42. H.J. Lee, B.J. Ahn, M.W. Shin, J.H. Choi, K.W. Kim, Ninjurin1: a potential adhesion molecule and its role in inflammation and tissue remodeling. Mol. Cells 29, 223–227 (2010)
43. J. Shan, J. Fu, Z. Zhao, X. Kong, H. Huang, L. Luo, Z. Yin, Chlorogenic acid inhibits lipopolysaccharide-induced cyclooxygenase-2 expression in RAW264.7 cells through suppressing NF-kappaB and JNK/AP-1 activation. Int. Immunopharmacol. 9, 1042–1048 (2009)
44. N. Yun, J.W. Kang, S.M. Lee, Protective effects of chlorogenic acid against ischemia/reperfusion injury in rat liver: molecular evidence of its antioxidant and anti-inflammatory properties. J. Nutr. Biochem. 23, 1249–1255 (2012)
45. Y. Sato, S. Itagaki, T. Kurokawa, J. Ogura, M. Kobayashi, T. Hirano, M. Sugawara, K. Iseki, In vitro and in vivo antioxidant properties of chlorogenic acid and caffeic acid. Int. J. Pharm. 403, 136–138 (2011)