Multi-Carotenoids at Physiological Levels Inhibit VEGF-Induced Tube Formation of Endothelial Cells and the Possible Mechanisms of Action Both In Vitro and Ex Vivo

References

• Folkman J: Angiogenesis. Annu Rev Med 57, 1–18, 2006.
   PubMed Web of Science ®Google Scholar
• Folkman J: Tumor angiogenesis: therapeutic implications. N Engl J Med 285, 1182–1186, 1971.
   PubMed Web of Science ®Google Scholar
• Folkman J: Fundamental concepts of the angiogenic process. Curr Mol Med 3, 643–651, 2003.
   PubMed Web of Science ®Google Scholar
• Ferrara N, and Kerbel RS: Angiogenesis as a therapeutic target. Nature 438, 967–974, 2005.
   PubMed Web of Science ®Google Scholar
• Carmeliet P, and Jain RK: Angiogenesis in cancer and other diseases. Nature 407, 249–257, 2000.
   PubMed Web of Science ®Google Scholar
• Chuang CH, Liu CH, Lu TJ, and Hu ML: Suppression of alpha-tocopherol ether-linked acetic acid in VEGF-induced angiogenesis and the possible mechanisms in human umbilical vein endothelial cells. Toxicol Appl Pharmacol 281, 310–316, 2014.
   PubMed Web of Science ®Google Scholar
• Stetler-Stevenson WG: Matrix metalloproteinases in angiogenesis: a moving target for therapeutic intervention. J Clin Invest 103, 1237–1241, 1999.
   PubMed Web of Science ®Google Scholar
• Park SL, Won SY, Song JH, Lee SY, Kim WJ, et al.: Esculetin inhibits VEGF-induced angiogenesis both in vitro and in vivo. Am J Chin Med 44, 61–76, 2016.
   PubMed Web of Science ®Google Scholar
• Prager GW, Breuss JM, Steurer S, Mihaly J, and Binder BR: Vascular endothelial growth factor (VEGF) induces rapid prourokinase (pro-uPA) activation on the surface of endothelial cells. Blood 103, 955–962, 2004.
   PubMed Web of Science ®Google Scholar
• Breuss JM, and Uhrin P: VEGF-initiated angiogenesis and the uPA/uPAR system. Cell Adh Migr 6, 535–615, 2012.
   PubMed Web of Science ®Google Scholar
• Elgass S, Cooper A, and Chopra M: Lycopene inhibits angiogenesis in human umbilical vein endothelial cells and rat aortic rings. Br J Nutr 108, 431–439, 2012.
   PubMed Web of Science ®Google Scholar
• Chen ML, Lin YH, Yang CM, and Hu ML: Lycopene inhibits angiogenesis both in vitro and in vivo by inhibiting MMP-2/uPA system through VEGFR2-mediated PI3K-Akt and ERK/p38 signaling pathways. Mol Nutr Food Res 56, 889–899, 2012.
   PubMed Web of Science ®Google Scholar
• Guruvayoorappan C, and Kuttan G: Beta-carotene inhibits tumor-specific angiogenesis by altering the cytokine profile and inhibits the nuclear translocation of transcription factors in B16F-10 melanoma cells. Integr Cancer Ther 6, 258–270, 2007.
   PubMed Web of Science ®Google Scholar
• Chew BP, Brown CM, Park JS, and Mixter PF: dietary lutein inhibits mouse mammary tumor growth by regulating angiogenesis and apoptosis. Anticancer Res 23, 3333–3339, 2003.
   PubMed Web of Science ®Google Scholar
• Stahl W, Junghans A, de Boer B, Driomina ES, Briviba K, et al.: Carotenoid mixtures protect multilamellar liposomes against oxidative damage: synergistic effects of lycopene and lutein. FEBS Lett 427, 305–308, 1998.
   PubMed Web of Science ®Google Scholar
• Del Giudice R, Petruk G, Raiola A, Barone A, Monti DM, et al.: Carotenoids in fresh and processed tomato (Solanum lycopersicum) fruits protect cells from oxidative stress injury. J Sci Food Agric 97, 1616–1623, 2017.
   PubMed Web of Science ®Google Scholar
• Chen HY, Yang CM, Chen JY, Yueh TC, and Hu ML: Multicarotenoids at physiological levels inhibit metastasis in human hepatocarcinoma SK-Hep-1 cells. Nutr Cancer 67, 676–686, 2015.
   PubMed Web of Science ®Google Scholar
• Nishino H, Murakoshic M, Tokudad H, and Satomid Y: Cancer prevention by carotenoids. Arch Biochem Biophys 483, 165–168, 2009.
   PubMed Web of Science ®Google Scholar
• Murakoshi M, Nishino H, Satomi Y, Takayasu J, Hasegawa T, et al.: Potent preventive action of alpha-carotene against carcinogenesis: spontaneous liver carcinogenesis and promoting stage of lung and skin carcinogenesis in mice are suppressed more effectively by alpha-carotene than by beta-carotene. Cancer Res 52, 6583–6587, 1992.
   PubMed Web of Science ®Google Scholar
• Lin YJ, Chien YW, Yang SH, and Cheng HH: Fruits and stir-fried vegetables increase plasma carotenoids in young adults. Asia Pac J Clin Nutr 16, 616–623, 2007.
   PubMed Web of Science ®Google Scholar
• Tucker KL, Chen H, Vogel S, Wilson PW, Schaefer EJ, et al.: Carotenoid intakes, assessed by dietary questionnaire, are associated with plasma carotenoid concentrations in an elderly population. J Nutr 129, 438–445, 1999.
   PubMed Web of Science ®Google Scholar
• Pierce JP, Natarajan L, Sun S, Al-Delaimy W, Flatt SW, et al.: Increases in plasma carotenoid concentrations in response to a major dietary change in the women's healthy eating and living study. Cancer Epidemiol Biomarkers Prev 15, 1886–1892, 2006.
   PubMed Web of Science ®Google Scholar
• Lin CY, Huang CS, and Hu ML: The use of fetal bovine serum as delivery vehicle to improve the uptake and stability of lycopene in cell culture 505 studies. Br J Nutr 98, 226–232, 2007.
   PubMed Web of Science ®Google Scholar
• Yang CM, Zhou YJ, Wang RJ, and Hu ML: Anti-angiogenic effects and mechanisms of polysaccharides from Antrodia cinnamomea with different molecular weights. J Ethnopharmacol 123, 407–412, 2009.
   PubMed Web of Science ®Google Scholar
• Repesh LA: A new in vitro assay for quantitating tumor cell invasion. Invasion Metastasis 9, 192–208, 1989.
   PubMedGoogle Scholar
• Yang CM, Liu YZ, Liao JW, and Hu ML: The in vitro and in vivo anti-metastatic efficacy of oxythiamine and the possible mechanisms of action. Clin Exp Metastasis 27, 341–349, 2010.
   PubMed Web of Science ®Google Scholar
• Go RS, and Owen WG: The rat aortic ring assay for in vitro study of angiogenesis. Methods Mol Med 85, 59–64, 2003.
   PubMedGoogle Scholar
• Omar HA, Arafa el-SA, Salama SA, Arab HH, Wu CH, et al.: OSU-A9 inhibits angiogenesis in human umbilical vein endothelial cells via disrupting Akt-NF-κB and MAPK signaling pathways. Toxicol Appl Pharmacol 272, 616–624, 2013.
   PubMed Web of Science ®Google Scholar
• Snoek-van Beurden PA, and Von den Hoff JW: Zymographic techniques for the analysis of matrix metalloproteinases and their inhibitors. BioTechniques 38, 73–83, 2005.
   PubMed Web of Science ®Google Scholar
• Donnini S, Morbidelli L, Taraboletti G, and Ziche M: ERK1-2 and p38 MAPK regulate MMP/TIMP balance and function in response to thrombospondin-1 fragments in the microvascular endothelium. Life Sci 74, 2975–2985, 2004.
   PubMed Web of Science ®Google Scholar
• Haas TL: Endothelial cell regulation of matrix metalloproteinases. Can J Physiol Pharmacol 83, 1–7, 2005.
   PubMed Web of Science ®Google Scholar
• Pepper MS: Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arterioscler Thromb Vasc Biol 21, 1104–1117, 2001.
   PubMed Web of Science ®Google Scholar
• Wagner S, Fueller T, Hummel V, Rieckmann P, and Tonn JC: Influence of VEGF-R2 inhibition on MMP secretion and motility of microvascular human cerebral endothelial cells (HCEC). J Neurooncol 62, 221–231, 2003.
   PubMed Web of Science ®Google Scholar
• Binder BR, Mihaly J, and Prager GW: uPAR-uPA-PAI-1 interactions and signaling: a vascular biologist's view. Thromb Haemost 97, 336–342, 2007.
   PubMed Web of Science ®Google Scholar
• Gualandris A, Lopez Conejo T, Giunciuglio D, Albini A, Sabini E, et al.: Urokinase-type plasminogen activator overexpression enhances the invasive capacity of endothelial cells. Microvasc Res 53, 254–260, 1997.
   PubMed Web of Science ®Google Scholar
• Nykjaer A, Conese M, Christensen EI, Olson D, Cremona O, et al.: Recycling of the urokinase receptor upon internalization of the uPA:serpin complexes. EMBO J 16, 2610–2620, 1997.
   PubMed Web of Science ®Google Scholar
• Shibuya M: Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis. J Biochem Mol Biol 39, 469–478, 2006.
   PubMedGoogle Scholar
• Tammela T, Enholm B, Alitalo K, and Paavonen K: The biology of vascular endothelial growth factors. Cardiovasc Res 65, 550–563, 2005.
   PubMed Web of Science ®Google Scholar
• Lamalice L, Houle F, and Huot J: Phosphorylation of Tyr1214 within VEGFR-2 triggers the recruitment of Nck and activation of Fyn leading to SAPK2/p38 activation and endothelial cell migration in response to VEGF. J Biol Chem 281, 34009–34020, 2006.
   PubMed Web of Science ®Google Scholar
• Chu LY, Ramakrishnan DP, and Silverstein RL: Silverstein, Thrombospondin-1 modulates VEGF signaling via CD36 by recruiting SHP-1 to VEGFR2 complex in microvascular endothelial cells. Blood 122, 1822–1832, 2013.
   PubMed Web of Science ®Google Scholar
• Gruszecki WI, and Strzałka K: Carotenoids as modulators of lipid membrane physical properties. Biochim Biophys Acta 1740, 108–115, 2005.
   PubMed Web of Science ®Google Scholar
• Subczynski WK, Markowska E, and Sielewiesiuk J: Spin-label studies on phosphatidylcholine-polar carotenoid membranes: effects of alkylchain length and unsaturation. Biochim Biophys Acta 1150, 173–181, 1993.
   PubMed Web of Science ®Google Scholar
• Strzalka K, and Gruszecki WI: Effect of beta-carotene on structural and dynamic properties of model phosphatidylcholine membranes: I. An EPR spin label study. Biochim Biophys Acta 1194, 138–142, 1994.
   PubMed Web of Science ®Google Scholar
• Colavitti R, Pani G, Bedogni B, Anzevino R, Borrello S, et al.: Reactive oxygen species as downstream mediators of angiogenic signaling by vascular endothelial growth factor receptor-2/KDR. J Biol Chem 277, 3101–3108, 2002.
   PubMed Web of Science ®Google Scholar
• Simons M, Gordon E, and Claesson-Welsh L: Mechanisms and regulation of endothelial VEGF receptor signalling. Nat Rev Mol Cell Biol 17, 611–625, 2016.
   PubMed Web of Science ®Google Scholar
• Lemmon MA, and Schlessinger J: Cell signaling by receptor tyrosine kinases. Cell 141, 1117–1134, 2010.
   PubMed Web of Science ®Google Scholar
• Michaud DS, Feskanich D, Rimm EB, Colditz GA, Speizer FE, et al.: Intake of specific carotenoids and risk of lung cancer in 2 prospective US cohorts. Am J Clin Nutr 72, 990–997, 2000.
   PubMed Web of Science ®Google Scholar
• Eliassen AH, Hendrickson SJ, Brinton LA, Buring JE, Campos H, et al.: Circulating carotenoids and risk of breast cancer: pooled analysis of eight prospective studies. J Natl Cancer Inst 104, 1905–1916, 2012.
   PubMed Web of Science ®Google Scholar
• Gaziano JM, Manson JE, Branch LG, Colditz GA, Willett WC, et al.: A prospective study of consumption of carotenoids in fruits and vegetables and decreased cardiovascular mortality in the elderly. Ann Epidemiol 5, 255–260, 1995.
   PubMedGoogle Scholar
• Liu RH: Potential synergy of phytochemicals in cancer prevention: mechanism of action. J Nutr 134, 3479S–3485S, 2004.
   PubMed Web of Science ®Google Scholar