Quercetin glucosides promote ischemia-induced angiogenesis, but do not promote tumor growth

Life Sciences

Volumn 93, Issue 22, 2013, Pages 814-819

  Sumi, Makoto ^a,b   Tateishi, Norifumi ^c   Shibata, Hiroshi ^c   Ohki, Takao ^b   Sata, Masataka ^a,d  

^a UNIVERSITY OF TOKYO   (Japan)

^b JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c Suntory Wellness Limited Research Center   (Japan)

^d UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

Angiogenesis; Collateral; Flavonoids; NO; Quercetin glucosides

Indexed keywords

ANGIOGENESIS INHIBITOR; CARBOXYMETHYLCELLULOSE; CD31 ANTIGEN; GLUCOSIDE; QUERCETIN DERIVATIVE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; CAPILLARY DENSITY; CONTROLLED STUDY; DRUG EFFECT; FEEDING; FEMORAL ARTERY; HINDLIMB; IMMUNOHISTOCHEMISTRY; ISCHEMIA; LIMB BLOOD FLOW; MALE; MOUSE; NONHUMAN; TISSUE DOPPLER IMAGING; TUMOR GROWTH;

ANGIOGENESIS; COLLATERAL; FLAVONOIDS; NO; QUERCETIN GLUCOSIDES;

ANGIOGENESIS INDUCING AGENTS; ANIMALS; ANTIOXIDANTS; CAPILLARIES; CYTOKINES; DISEASE MODELS, ANIMAL; GLUCOSIDES; HINDLIMB; ISCHEMIA; MALE; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, MUTANT STRAINS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE SYNTHASE TYPE III; QUERCETIN;

MURINAE; MUS;

EID: 84887233301     PISSN: 00243205     EISSN: 18790631     Source Type: Journal    
DOI: 10.1016/j.lfs.2013.09.005     Document Type: Article

References (40)

1. A. Ahmad, M.M. Khan, M.N. Hoda, S.S. Raza, M.B. Khan, and H. Javed Quercetin protects against oxidative stress associated damages in a rat model of transient focal cerebral ischemia and reperfusion Neurochem Res 36 2011 1360 1371
2. A. Aicher, C. Heeschen, C. Mildner-Rihm, C. Urbich, C. Ihling, and K. Technau-Ihling Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells Nat Med 9 2003 1370 1376 (Pubitemid 37466185)
3. T. Akiyama, T. Washino, T. Yamada, T. Koda, and T. Maitani Constituents of enzymatically modified isoquercitrin and enzymatically modified rutin (extract) J Food Hyg Soc Jpn 41 2000 54 60 (Pubitemid 30190980)
4. Y.H. Aldebasi, A.H. Rahmani, A.A. Khan, and S.M. Aly The effect of vascular endothelial growth factor in the progression of bladder cancer and diabetic retinopathy Int J Clin Exp Med 6 2013 239 251
5. K. Amano, H. Matsubara, O. Iba, M. Okigaki, S. Fujiyama, and T. Imada Enhancement of ischemia-induced angiogenesis by eNOS overexpression Hypertension 41 2003 156 162 (Pubitemid 36056808)
6. M. Arras, W.D. Ito, D. Scholz, B. Winkler, J. Schaper, and W. Schaper Monocyte activation in angiogenesis and collateral growth in the rabbit hindlimb J Clin Invest 101 1998 40 50 (Pubitemid 28058901)
7. S. Attanasio, and G. Schaer Therapeutic angiogenesis for the management of refractory angina: current concepts Cardiovasc Ther 29 2011 e1 e11
8. M. Billinger, P. Kloos, F.R. Eberli, S. Windecker, B. Meier, and C. Seiler Physiologically assessed coronary collateral flow and adverse cardiac ischemic events: a follow-up study in 403 patients with coronary artery disease J Am Coll Cardiol 40 2002 1545 1550 (Pubitemid 35253630)
9. T. Couffinhal, M. Silver, M. Kearney, A. Sullivan, B. Witzenbichler, and M. Magner Impaired collateral vessel development associated with reduced expression of vascular endothelial growth factor in ApoE -/- mice Circulation 99 1999 3188 3198 (Pubitemid 29289086)
10. S. Dai, Y. He, H. Zhang, L. Yu, T. Wan, and Z. Xu Endothelial-specific expression of mitochondrial thioredoxin promotes ischemia-mediated arteriogenesis and angiogenesis Arterioscler Thromb Vasc Biol 29 2009 495 502
11. N.H. Daud, C.S. Aung, A.K. Hewavitharana, A.S. Wilkinson, J.T. Pierson, and S.J. Roberts-Thomson Mango extracts and the mango component mangiferin promote endothelial cell migration J Agric Food Chem 58 2010 5181 5186
12. J.H. de Vries, P.L. Janssen, P.C. Hollman, W.A. van Staveren, and M.B. Katan Consumption of quercetin and kaempferol in free-living subjects eating a variety of diets Cancer Lett 114 1997 141 144 (Pubitemid 27140095)
13. J. Duarte, R. Perez-Palencia, F. Vargas, M.A. Ocete, F. Perez-Vizcaino, and A. Zarzuelo Antihypertensive effects of the flavonoid quercetin in spontaneously hypertensive rats Br J Pharmacol 133 2001 117 124 (Pubitemid 32500458)
14. M. Erden Inal, and A. Kahraman The protective effect of flavonol quercetin against ultraviolet a induced oxidative stress in rats Toxicology 154 2000 21 29
15. J. Folkman Seminars in medicine of the Beth Israel Hospital, Boston. Clinical applications of research on angiogenesis N Engl J Med 333 1995 1757 1763
16. S. Freedman, and J.M. Isner Therapeutic angiogenesis for ischemic cardiovascular disease J Mol Cell Cardiol 33 2001 379 393 (Pubitemid 32538996)
17. M.G. Hertog, E.J. Feskens, P.C. Hollman, M.B. Katan, and D. Kromhout Dietary antioxidant flavonoids and risk of coronary heart disease: the Zutphen elderly study Lancet 342 1993 1007 1011 (Pubitemid 23314801)
18. P.L. Huang, Z. Huang, H. Mashimo, K.D. Bloch, M.A. Moskowitz, and J.A. Bevan Hypertension in mice lacking the gene for endothelial nitric oxide synthase Nature 377 1995 239 242
19. G.S. Kelly Quercetin. Monograph Altern Med Rev 16 2011 172 194
20. P.G. Li, L. Sun, X. Han, S. Ling, W.T. Gan, and J.W. Xu Quercetin induces rapid eNOS phosphorylation and vasodilation by an Akt-independent and PKA-dependent mechanism Pharmacology 89 2012 220 228
21. T. Makino, R. Shimizu, M. Kanemaru, Y. Suzuki, M. Moriwaki, and H. Mizukami Enzymatically modified isoquercitrin, alpha-oligoglucosyl quercetin 3-O-glucoside, is absorbed more easily than other quercetin glycosides or aglycone after oral administration in rats Biol Pharm Bull 32 2009 2034 2040
22. T. Makino, M. Kanemaru, S. Okuyama, R. Shimizu, H. Tanaka, and H. Mizukami Anti-allergic effects of enzymatically modified isoquercitrin (alpha-oligoglucosyl quercetin 3-O-glucoside), quercetin 3-O-glucoside, alpha-oligoglucosyl rutin, and quercetin, when administered orally to mice J Nat Med 67 2013 881 886
23. T. Murohara, T. Asahara, M. Silver, C. Bauters, H. Masuda, and C. Kalka Nitric oxide synthase modulates angiogenesis in response to tissue ischemia J Clin Invest 101 1998 2567 2578 (Pubitemid 28270451)
24. T. Murohara, B. Witzenbichler, I. Spyridopoulos, T. Asahara, B. Ding, and A. Sullivan Role of endothelial nitric oxide synthase in endothelial cell migration Arterioscler Thromb Vasc Biol 19 1999 1156 1161 (Pubitemid 29227632)
25. T. Natori, M. Sata, M. Washida, Y. Hirata, R. Nagai, and M. Makuuchi G-CSF stimulates angiogenesis and promotes tumor growth: potential contribution of bone marrow-derived endothelial progenitor cells Biochem Biophys Res Commun 297 2002 1058 1061 (Pubitemid 35230360)
26. P. Pratheeshkumar, A. Budhraja, Y.O. Son, X. Wang, Z. Zhang, and S. Ding Quercetin inhibits angiogenesis mediated human prostate tumor growth by targeting VEGFR-2 regulated AKT/mTOR/P70S6K signaling pathways PLoS One 7 2012 e47516
27. J. Robak, and R.J. Gryglewski Flavonoids are scavengers of superoxide anions Biochem Pharmacol 37 1988 837 841 (Pubitemid 18058453)
28. L. Rossig, B. Fichtlscherer, K. Breitschopf, J. Haendeler, A.M. Zeiher, and A. Mulsch Nitric oxide inhibits caspase-3 by S-nitrosation in vivo J Biol Chem 274 1999 6823 6826
29. C. Ruegg, and N. Mutter Anti-angiogenic therapies in cancer: achievements and open questions Bull Cancer 94 2007 753 762 (Pubitemid 47605603)
30. E.I. Salim, M. Kaneko, H. Wanibuchi, K. Morimura, and S. Fukushima Lack of carcinogenicity of enzymatically modified isoquercitrin in F344/DuCrj rats Food Chem Toxicol 42 2004 1949 1969 (Pubitemid 39421496)
31. M. Sanchez, M. Galisteo, R. Vera, I.C. Villar, A. Zarzuelo, and J. Tamargo Quercetin downregulates nadph oxidase, increases enos activity and prevents endothelial dysfunction in spontaneously hypertensive rats J Hypertens 24 2006 75 84 (Pubitemid 41818091)
32. M. Sata, M. Kakoki, D. Nagata, H. Nishimatsu, E. Suzuki, and T. Aoyagi Adrenomedullin and nitric oxide inhibit human endothelial cell apoptosis via a cyclic GMP-independent mechanism Hypertension 36 2000 83 88 (Pubitemid 30602157)
33. M. Sata, H. Nishimatsu, E. Suzuki, S. Sugiura, M. Yoshizumi, and Y. Ouchi Endothelial nitric oxide synthase is essential for the HMG-CoA reductase inhibitor cerivastatin to promote collateral growth in response to ischemia FASEB J 15 2001 2530 2532
34. M. Sata, H. Nishimatsu, J. Osuga, K. Tanaka, N. Ishizaka, and S. Ishibashi Statins augment collateral growth in response to ischemia but they do not promote cancer and atherosclerosis Hypertension 43 2004 1214 1220 (Pubitemid 38691742)
35. C. Seiler The human coronary collateral circulation Eur J Clin Invest 40 2010 465 476
36. Y. Shen, K.D. Croft, J.M. Hodgson, R. Kyle, I.L. Lee, and Y. Wang Quercetin and its metabolites improve vessel function by inducing eNOS activity via phosphorylation of AMPK Biochem Pharmacol 84 2012 1036 1044
37. S.A. Stacker, C. Caesar, M.E. Baldwin, G.E. Thornton, R.A. Williams, and R. Prevo VEGF-D promotes the metastatic spread of tumor cells via the lymphatics Nat Med 7 2001 186 191 (Pubitemid 32148485)
38. E. Van Belle, A. Rivard, D. Chen, M. Silver, S. Bunting, and N. Ferrara Hypercholesterolemia attenuates angiogenesis but does not preclude augmentation by angiogenic cytokines Circulation 96 1997 2667 2674 (Pubitemid 27451360)
39. N. van Royen, J.J. Piek, I. Buschmann, I. Hoefer, M. Voskuil, and W. Schaper Stimulation of arteriogenesis; a new concept for the treatment of arterial occlusive disease Cardiovasc Res 49 2001 543 553 (Pubitemid 32146417)
40. Y. Yamamoto, and E. Oue Antihypertensive effect of quercetin in rats fed with a high-fat high-sucrose diet Biosci Biotechnol Biochem 70 2006 933 939