Resveratrol at anti-angiogenesis/anticancer concentrations suppresses protein kinase G signaling and decreases IAPs expression in HUVECs

Anticancer Research

Volumn 35, Issue 1, 2015, Pages 273-282

  Wong, Janica C ^a,b,c   Fiscus, Ronald R ^a,c  

^a ROSEMAN UNIVERSITY OF HEALTH SCIENCES   (United States)

^b UNIVERSITY OF NEVADA   (United States)

^c NEVADA CANCER INSTITUTE   (United States)

Author keywords

Angiogenesis; HUVECs; Inhibitor of Apoptosis Proteins (IAPs); Protein kinase G (PKG); Resveratrol

Indexed keywords

CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; INHIBITOR OF APOPTOSIS PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN 1; INHIBITOR OF APOPTOSIS PROTEIN 2; LIVIN; MESSENGER RNA; NITRIC OXIDE; RESVERATROL; VASODILATOR STIMULATED PHOSPHOPROTEIN; X LINKED INHIBITOR OF APOPTOSIS; ANGIOGENESIS INHIBITOR; ISOENZYME; STILBENE DERIVATIVE;

ANGIOGENESIS; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UMBILICAL VEIN ENDOTHELIAL CELL; WESTERN BLOTTING; APOPTOSIS; CELL CULTURE; CELL MOTION; CELL PROLIFERATION; DRUG EFFECTS; DRUG SCREENING; GENE EXPRESSION; GENETICS; METABOLISM; SIGNAL TRANSDUCTION;

ANGIOGENESIS INHIBITORS; APOPTOSIS; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CYCLIC GMP-DEPENDENT PROTEIN KINASES; DRUG SCREENING ASSAYS, ANTITUMOR; GENE EXPRESSION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; ISOENZYMES; SIGNAL TRANSDUCTION; STILBENES;

EID: 84920479717     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (27)

1. Aggarwal BB, Bhardwaj A, Aggarwal RS, Seeram NP, Shishodia S and Takada Y: Role of resveratrol in prevention and therapy of cancer: preclinical and clinical studies. Anticancer Res 24: 2783-2840, 2004.
2. Brunner F, Schmidt K, Nielsen EB and Mayer B: Novel guanylyl cyclase inhibitor potently inhibits cyclic GMP accumulation in endothelial cells and relaxation of bovine pulmonary artery. J Pharmacol Exp Ther 277: 48-53, 1996.
3. Chan GH and Fiscus RR: Exaggerated production of nitric oxide (NO) and increases in inducible NO-synthase mRNA levels induced by the pro-inflammatory cytokine interleukin-1beta in vascular smooth muscle cells of elderly rats. Exp Gerontol 39: 387-394, 2004.
4. Chen LK, Qiang PF, Xu QP, Zhao YH, Dai F and Zhang L: Trans-3, 4, 5, 4'-tetramethoxystilbene, a resveratrol analog, potently inhibits angiogenesis in vitro and in vivo. Acta pharmacologica Sinica 34: 1174-1182, 2013.
5. Cudmore M, Ahmad S, Al-Ani B, Hewett P, Ahmed S and Ahmed A: VEGF-E activates endothelial nitric oxide synthase to induce angiogenesis via cGMP and PKG-independent pathways. Biochem Biophys Res Commun 345: 1275-1282, 2006.
6. Draijer R, Vaandrager AB, Nolte C, de Jonge HR, Walter U and van Hinsbergh VW: Expression of cGMP-dependent protein kinase I and phosphorylation of its substrate, vasodilatorstimulated phosphoprotein, in human endothelial cells of different origin. Circ Res 77: 897-905, 1995.
7. Ekshyyan VP, Hebert VY, Khandelwal A and Dugas TR: Resveratrol inhibits rat aortic vascular smooth muscle cell proliferation via estrogen receptor dependent nitric oxide production. J Cardiovasc Pharmacol 50: 83-93, 2007.
8. Farrand L, Byun S, Kim JY, Im-Aram A, Lee J, Lim S, Lee KW, Suh JY, Lee HJ and Tsang BK: Piceatannol Enhances Cisplatin Sensitivity in Ovarian Cancer via Modulation of p53, X-linked Inhibitor of Apoptosis Protein (XIAP), and Mitochondrial Fission. J Biol Chem 288: 23740-23750, 2013.
9. Fiscus RR: Involvement of cyclic GMP and protein kinase G in the regulation of apoptosis and survival in neural cells. Neurosignals 11: 175-190, 2002.
10. Fiscus RR and Johlfs MG: Protein kinase G (PKG): Involvement in promoting neural cell survival, proliferation, synaptogenesis and synaptic plasticity and the use of new ultrasensitive capillary-electrophoresis-based methodology for measuring PKG expression and molecular actions. In: Protein Kinase Technologies, in the series NEUROMETHODS Mukai H (ed.): Springer, pp. 319-348, 2012.
11. Fiscus RR, Leung EL, Wong JC and Johlfs MG: Nitric Oxide/Protein Kinase G-Iα Promotes c-Src Activation, Proliferation and Chemoresistance in Ovarian Cancer. In: Ovarian Cancer - Basic Science Perspective (Farghaly S ed.): Intech Open Access Publisher, pp. 315-334, 2012.
12. Fiscus RR, Yuen JP, Chan SL, Kwong JH and Chew SB: Nitric oxide and cyclic GMP as pro- and anti-apoptotic agents. J Card Surg 17: 336-339, 2002.
13. Fukumura D, Gohongi T, Kadambi A, Izumi Y, Ang J, Yun CO, Buerk DG, Huang PL and Jain RK: Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc Natl Acad Sci USA 98: 2604-2609, 2001.
14. 2+ signaling, ERK 1/2 activation, mitogenesis and vasodilator production. J Endocrinol 182: 485-499, 2004.
15. Hood J and Granger HJ: Protein kinase G mediates vascular endothelial growth factor-induced Raf-1 activation and proliferation in human endothelial cells. J Biol Chem 273: 23504-23508, 1998.
16. Jaffe EA, Nachman RL, Becker CG and Minick CR: Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J Clin Invest 52: 2745-2756, 1973.
17. Koika V, Zhou Z, Vasileiadis I, Roussos C, Finetti F, Monti M, Morbidelli L and Papapetropoulos A: PKG-I inhibition attenuates vascular endothelial growth factor-stimulated angiogenesis. Vascul Pharmacol 53: 215-222, 2010.
18. Lee HR, Kim J, Park J, Ahn S, Jeong E and Park H: FERM domain promotes resveratrol-induced apoptosis in endothelial cells via inhibition of NO production. Biochem Biophys Res Commun 441: 891-896, 2013.
19. Leung EL, Wong JC, Johlfs MG, Tsang BK and Fiscus RR: Protein kinase G type Ialpha activity in human ovarian cancer cells significantly contributes to enhanced Src activation and DNA synthesis/cell proliferation. Mol Cancer Res 8: 578-591, 2010.
20. Morgan DM: Isolation and culture of human umbilical vein endothelial cells. Methods Mol Med 2: 101-109, 1996.
21. Pyriochou A, Beis D, Koika V, Potytarchou C, Papadimitriou E, Zhou Z and Papapetropoulos A: Soluble guanylyl cyclase activation promotes angiogenesis. J Pharmacol Exp Ther 319: 663-671, 2006.
22. Wallerath T, Deckert G, Ternes T, Anderson H, Li H, Witte K and Forstermann U: Resveratrol, a polyphenolic phytoalexin present in red wine, enhances expression and activity of endothelial nitric oxide synthase. Circulation 106: 1652-1658, 2002.
23. Wang H, Zhou H, Zou Y, Liu Q, Guo C, Gao G, Shao C and Gong Y: Resveratrol modulates angiogenesis through the GSK3beta/beta-catenin/TCF-dependent pathway in human endothelial cells. Biochem Pharmacol 80: 1386-1395, 2010.
24. Wong JC, Bathina M and Fiscus RR: Cyclic GMP/protein kinase G type-Ialpha (PKG-Ialpha) signaling pathway promotes CREB phosphorylation and maintains higher c-IAP1, livin, survivin and Mcl-1 expression and the inhibition of PKG-Ialpha kinase activity synergizes with cisplatin in non-small cell lung cancer cells. J Cell Biochem 113: 3587-3598, 2012.
25. Wong JC and Fiscus RR: Essential roles of the nitric oxide (no)/cGMP/protein kinase G type-Ialpha (PKG-Ialpha) signaling pathway and the atrial natriuretic peptide (ANP)/cGMP/PKGIalpha autocrine loop in promoting proliferation and cell survival of OP9 bone marrow stromal cells. J Cell Biochem 112: 829- 839, 2011.
26. Xia N, Strand S, Schlufter F, Siuda D, Reifenberg G, Kleinert H, Forstermann U and Li H: Role of SIRT1 and FOXO factors in eNOS transcriptional activation by resveratrol. Nitric Oxide 32: 29-35, 2013.
27. Ziche M and Morbidelli L: Nitric oxide and angiogenesis. J Neurooncol 50: 139-148, 2000.