Thio-Cl-IB-MECA, a novel A3 adenosine receptor agonist, suppresses angiogenesis by regulating PI3K/AKT/mTOR and ERK signaling in endothelial cells

Biochemical and Biophysical Research Communications

Volumn 437, Issue 1, 2013, Pages 79-86

  Kim, Gi Dae ^a   Oh, Jedo ^a   Jeong, Lak Shin ^b   Lee, Sang Kook ^a  

^a Seoul National University   (South Korea)

^b Ewha Womans University   (South Korea)

Author keywords

Anti angiogenesis; Cl IB MECA; EB; Endothelial cells; ERK; HUVECs; IB MECA; MES; PECAM; PI3K; PI3K AKT mTOR; Thio Cl IB MECA

Indexed keywords

2 CHLORO N6 (3 IODOBENZYL) 4' THIOADENOSINE 5' N METHYLURONAMIDE; ADENOSINE RECEPTOR STIMULATING AGENT; ANGIOGENESIS INHIBITOR; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL VIABILITY; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; MICROVASCULATURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; WESTERN BLOTTING;

2-CHLORO-N(6)-(3-IODOBENZYL)-4′-THIOADENOSINE-5′-N-METHYLURONAMIDE; 2-CHLORO-N(6)-(3-IODOBENZYL)-ADENOSINE-5′-N-METHYLCARBOXAMIDE; A(3) ADENOSINE RECEPTOR; A(3)AR; ANTI-ANGIOGENESIS; CL-IB-MECA; EB; EMBRYOID BODY; ENDOTHELIAL CELLS; ERK; EXTRACELLULAR SIGNAL-REGULATED KINASE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUVECS; IB-MECA; MES; MOUSE EMBRYONIC STEM; N(6)-(3-IODOBENZYL)ADENOSINE-5′-N-METHYLURONAMIDE; PECAM; PHOSPHATIDYLINOSITOL-3-KINASE; PI3K; PI3K/AKT/MTOR; PLATELET/ENDOTHELIAL CELL ADHESION MOLECULE; THIO-CL-IB-MECA;

ADENOSINE; ADENOSINE A3 RECEPTOR AGONISTS; ANIMALS; ANTIGENS, CD31; BIOLOGICAL MARKERS; CELL MOVEMENT; CELL PROLIFERATION; EMBRYOID BODIES; EMBRYONIC STEM CELLS; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84880506278     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2013.06.040     Document Type: Article

References (34)

1. Fredholm B.B., AP I.J., Jacobson K.A., Linden J., Muller C.E. International Union of Basic and Clinical Pharmacology. LXXXI. Nomenclature and classification of adenosine receptors-an update. Pharmacol. Rev. 2011, 63:1-34.
2. Carmeliet P., Jain R.K. Angiogenesis in cancer and other diseases. Nature 2000, 407:249-257.
3. Kim S.J., Min H.Y., Chung H.J., Park E.J., Hong J.Y., Kang Y.J., Shin D.H., Jeong L.S., Lee S.K. Inhibition of cell proliferation through cell cycle arrest and apoptosis by thio-Cl-IB-MECA, a novel A3 adenosine receptor agonist, in human lung cancer cells. Cancer Lett. 2008, 264:309-315.
4. Kim H., Kang J.W., Lee S., Choi W.J., Jeong L.S., Yang Y., Hong J.T., Yoon do Y. A3 adenosine receptor antagonist, truncated Thio-Cl-IB-MECA, induces apoptosis in T24 human bladder cancer cells. Anticancer Res. 2010, 30:2823-2830.
5. Lee E.J., Min H.Y., Chung H.J., Park E.J., Shin D.H., Jeong L.S., Lee S.K. A novel adenosine analog, thio-Cl-IB-MECA, induces G0/G1 cell cycle arrest and apoptosis in human promyelocytic leukemia HL-60 cells. Biochem. Pharmacol. 2005, 70:918-924.
6. Fernandez P., Jara C., Aguilera V., Caviedes L., Diaz F., Radojkovic C., Veas C., Lamperti L., Escudero C., Aguayo C. Adenosine A(2)A and A(3) receptors are involved in the human endothelial progenitor cells migration. J. Cardiovasc. Pharmacol. 2012, 59:397-404.
7. Platts S.H., Duling B.R. Adenosine A3 receptor activation modulates the capillary endothelial glycocalyx. Circ. Res. 2004, 94:77-82.
8. Feoktistov I., Goldstein A.E., Ryzhov S., Zeng D., Belardinelli L., Voyno-Yasenetskaya T., Biaggioni I. Differential expression of adenosine receptors in human endothelial cells: role of A2B receptors in angiogenic factor regulation. Circ. Res. 2002, 90:531-538.
9. Feoktistov I., Ryzhov S., Goldstein A.E., Biaggioni I. Mast cell-mediated stimulation of angiogenesis: cooperative interaction between A2B and A3 adenosine receptors. Circ. Res. 2003, 92:485-492.
10. Fidler I.J., Ellis L.M. The implications of angiogenesis for the biology and therapy of cancer metastasis. Cell 1994, 79:185-188.
11. Xu Z., Fang S., Zuo Y., Zhang Y., Cheng R., Wang Q., Yang Z., Cai W., Ma J., Yang X., Gao G. Combination of pigment epithelium-derived factor with radiotherapy enhances the antitumor effects on nasopharyngeal carcinoma by downregulating vascular endothelial growth factor expression and angiogenesis. Cancer Sci. 2011, 102:1789-1798.
12. Merighi S., Benini A., Mirandola P., Gessi S., Varani K., Leung E., Maclennan S., Borea P.A. A3 adenosine receptor activation inhibits cell proliferation via phosphatidylinositol 3-kinase/Akt-dependent inhibition of the extracellular signal-regulated kinase 1/2 phosphorylation in A375 human melanoma cells. J. Biol. Chem. 2005, 280:19516-19526.
13. Jeong L.S., Jin D.Z., Kim H.O., Shin D.H., Moon H.R., Gunaga P., Chun M.W., Kim Y.C., Melman N., Gao Z.G., Jacobson K.A. N6-substituted D-4'-thioadenosine-5'-methyluronamides: potent and selective agonists at the human A3 adenosine receptor. J. Med. Chem. 2003, 46:3775-3777.
14. Kim G.D., Bae S.Y., Park H.J., Bae K., Lee S.K. Honokiol inhibits vascular vessel formation of mouse embryonic stem cell-derived endothelial cells via the suppression of PECAM and MAPK/mTOR signaling pathway. Cell. Physiol. Biochem. 2012, 30:758-770.
15. Kim G.D., Kim G.J., Seok J.H., Chung H.M., Chee K.M., Rhee G.S. Differentiation of endothelial cells derived from mouse embryoid bodies: a possible in vitro vasculogenesis model. Toxicol. Lett. 2008, 180:166-173.
16. Kim G.D., Rhee G.S., Chung H.M., Chee K.M., Kim G.J. Cytotoxicity of 5-fluorouracil: Effect on endothelial differentiation via cell cycle inhibition in mouse embryonic stem cells. Toxicol. In Vitro 2009, 23:719-727.
17. Yi T., Yi Z., Cho S.G., Luo J., Pandey M.K., Aggarwal B.B., Liu M. Gambogic acid inhibits angiogenesis and prostate tumor growth by suppressing vascular endothelial growth factor receptor 2 signaling. Cancer Res. 2008, 68:1843-1850.
18. Kubota Y., Kleinman H.K., Martin G.R., Lawley T.J. Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J. Cell Biol. 1988, 107:1589-1598.
19. Baker M., Robinson S.D., Lechertier T., Barber P.R., Tavora B., D'Amico G., Jones D.T., Vojnovic B., Hodivala-Dilke K. Use of the mouse aortic ring assay to study angiogenesis. Nat. Protoc. 2012, 7:89-104.
20. Gu A., Tsark W., Holmes K.V., Shively J.E. Role of Ceacam1 in VEGF induced vasculogenesis of murine embryonic stem cell-derived embryoid bodies in 3D culture. Exp. Cell Res. 2009, 315:1668-1682.
21. Kruger E.A., Duray P.H., Tsokos M.G., Venzon D.J., Libutti S.K., Dixon S.C., Rudek M.A., Pluda J., Allegra C., Figg W.D. Endostatin inhibits microvessel formation in the ex vivo rat aortic ring angiogenesis assay. Biochem. Biophys. Res. Commun. 2000, 268:183-191.
22. Wartenberg M., Gunther J., Hescheler J., Sauer H. The embryoid body as a novel in vitro assay system for antiangiogenic agents. Lab. Invest. 1998, 78:1301-1314.
23. Karar J., Maity A. PI3K/AKT/mTOR pathway in angiogenesis. Front. Mol. Neurosci. 2011, 4:51.
24. Fishman P., Madi L., Bar-Yehuda S., Barer F., Del Valle L., Khalili K. Evidence for involvement of Wnt signaling pathway in IB-MECA mediated suppression of melanoma cells. Oncogene 2002, 21:4060-4064.
25. Madi L., Bar-Yehuda S., Barer F., Ardon E., Ochaion A., Fishman P. A3 adenosine receptor activation in melanoma cells: association between receptor fate and tumor growth inhibition. J. Biol. Chem. 2003, 278:42121-42130.
26. Chung H., Jung J.Y., Cho S.D., Hong K.A., Kim H.J., Shin D.H., Kim H., Kim H.O., Shin D.H., Lee H.W., Jeong L.S., Kong G. The antitumor effect of LJ-529, a novel agonist to A3 adenosine receptor, in both estrogen receptor-positive and estrogen receptor-negative human breast cancers. Mol. Cancer Ther. 2006, 5:685-692.
27. Descamps B., Emanueli C. Vascular differentiation from embryonic stem cells: novel technologies and therapeutic promises. Vascul. Pharmacol. 2012, 56:267-279.
28. Tabruyn S.P., Griffioen A.W. Molecular pathways of angiogenesis inhibition. Biochem. Biophys. Res. Commun. 2007, 355:1-5.
29. Cho D.H., Choi Y.J., Jo S.A., Ryou J., Kim J.Y., Chung J., Jo I. Troglitazone acutely inhibits protein synthesis in endothelial cells via a novel mechanism involving protein phosphatase 2A-dependent p70 S6 kinase inhibition. Am. J. Physiol. Cell Physiol. 2006, 291:C317-326.
30. Yap T.A., Garrett M.D., Walton M.I., Raynaud F., de Bono J.S., Workman P. Targeting the PI3K-AKT-mTOR pathway: progress, pitfalls, and promises. Curr. Opin. Pharmacol. 2008, 8:393-412.
31. Boutros T., Chevet E., Metrakos P. Mitogen-activated protein (MAP) kinase/MAP kinase phosphatase regulation: roles in cell growth, death, and cancer. Pharmacol. Rev. 2008, 60:261-310.
32. Xia Z., Dickens M., Raingeaud J., Davis R.J., Greenberg M.E. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 1995, 270:1326-1331.
33. Brambilla R., Cattabeni F., Ceruti S., Barbieri D., Franceschi C., Kim Y.C., Jacobson K.A., Klotz K.N., Lohse M.J., Abbracchio M.P. Activation of the A3 adenosine receptor affects cell cycle progression and cell growth. Naunyn Schmiedebergs Arch. Pharmacol. 2000, 361:225-234.
34. Takahashi K., Mitsui K., Yamanaka S. Role of ERas in promoting tumour-like properties in mouse embryonic stem cells. Nature 2003, 423:541-545.