Polyphenol-based nutraceuticals for the control of angiogenesis: Analysis of the critical issues for human use

Pharmacological Research

Volumn 111, Issue , 2016, Pages 384-393

  Morbidelli, Lucia ^a  

^a UNIVERSITY OF SIENA   (Italy)

Author keywords

Angiogenesis; Cancer therapy; Endothelial cell; Growth factor receptor; Nutraceutical; Phytochemical

Indexed keywords

CURCUMIN; ELLAGIC ACID; EPIGALLOCATECHIN GALLATE; FISETIN; FLAVONOID; GENISTEIN; GINSENOSIDE; HYDROXYTYROSOL; LICOCHALCONE A; LUTEOLIN; PHENOL DERIVATIVE; POLYPHENOL; QUERCETIN; RESVERATROL; STILBENE DERIVATIVE; TERPENOID DERIVATIVE; WITHAFERIN A; XANTHOHUMOL; ANGIOGENESIS INHIBITOR;

ANGIOGENESIS; ANTIANGIOGENIC ACTIVITY; CONCENTRATION RESPONSE; DRUG BIOAVAILABILITY; DRUG EFFICACY; DRUG FORMULATION; DRUG MECHANISM; DRUG SAFETY; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; DIETARY SUPPLEMENT; DRUG EFFECTS; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; VASCULARIZATION;

ANGIOGENESIS INHIBITORS; ANIMALS; DIETARY SUPPLEMENTS; HUMANS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; POLYPHENOLS;

EID: 84978388207     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2016.07.011     Document Type: Review

References (158)

1. [1] Carmeliet, P., Jain, R.K., Angiogenesis in cancer and other diseases. Nature 407:6801 (2000), 249–257.
2. [2] Carmeliet, P., Angiogenesis in health and disease. Nat. Med. 9:6 (2003), 653–660.
3. [3] Khurana, R., Simons, M., Martin, J.F., Zachary, I.C., Role of angiogenesis in cardiovascular disease: a critical appraisal. Circulation 112:12 (2005), 1813–1824.
4. [4] Chung, A.S., Ferrara, N., Developmental and pathological angiogenesis. Annu. Rev. Cell Dev. Biol. 27 (2011), 563–584.
5. [5] Folkman, J., Fighting cancer by attacking its blood supply. Sci. Am. 275:3 (1996), 150–154.
6. [6] Ferrara, N., Kerbel, R.S., Angiogenesis as a therapeutic target. Nature 438:7070 (2005), 967–974.
7. [7] Al-Husein, B., Abdalla, M., Trepte, M., Deremer, D.L., Somanath, P.R., Antiangiogenic therapy for cancer: an update. Pharmacotherapy 32:12 (2012), 1095–1111.
8. [8] Kubota, Y., Tumor angiogenesis and anti-angiogenic therapy. Keio J. Med. 61:2 (2012), 47–56.
9. [9] Welti, J., Loges, S., Dimmeler, S., Carmeliet, P., Recent molecular discoveries in angiogenesis and antiangiogenic therapies in cancer. J. Clin. Invest. 123:8 (2013), 3190–3200.
10. [10] Hoeben, A., Landuyt, B., Highley, M.S., Wildiers, H., Van Oosterom, A.T., De Bruijn, E.A., Vascular endothelial growth factor and angiogenesis. Pharmacol. Rev. 56:4 (2004), 549–580.
11. [11] Weis, S.M., Cheresh, D.A., Tumor angiogenesis: molecular pathways and therapeutic targets. Nat. Med. 17:11 (2011), 1359–1370.
12. [12] Amadio, M., Govoni, S., Pascale, A., Targeting VEGF in eye neovascularization: what's new?: A comprehensive review on current therapies and oligonucleotide-based interventions under development. Pharmacol. Res. 103 (2016), 253–269.
13. [13] Malecic, N., Young, H.S., Novel investigational vascular endothelial growth factor (VEGF) receptor antagonists for psoriasis. Expert Opin. Investig. Drugs 25:4 (2016), 455–462.
14. [14] Marinaccio, C., Nico, B., Maiorano, E., Specchia, G., Ribatti, D., Insights in hodgkin lymphoma angiogenesis. Leuk. Res. 38:8 (2014), 857–861.
15. [15] Papa, A., Zaccarelli, E., Caruso, D., Vici, P., Benedetti Panici, P., Tomao, F., Targeting angiogenesis in endometrial cancer-new agents for tailored treatments. Expert Opin. Investig. Drugs 25:1 (2016), 31–49.
16. [16] Xu, L., Stevens, J., Hilton, M.B., Seaman, S., Conrads, T.P., Veenstra, T.D., Logsdon, D., Morris, H., Swing, D.A., Patel, N.L., Kalen, J., Haines, D.C., Zudaire, E., St Croix, B., COX-2 inhibition potentiates antiangiogenic cancer therapy and prevents metastasis in preclinical models. Sci. Transl. Med., 6(242), 2014 (242).
17. [17] E, J., Xing, J., Gong, H., He, J., Zhang, W., Combine MEK inhibition with PI3 K/mTOR inhibition exert inhibitory tumor growth effect on KRAS and PIK3 CA mutation CRC xenografts due to reduced expression of VEGF and matrix metallopeptidase-9. Tumour Biol. 36:2 (2015), 1091–1097.
18. [18] Norioka, K., Mitaka, T., Mochizuki, Y., Hara, M., Kawagoe, M., Nakamura, H., Interaction of interleukin-1 and interferon-gamma on fibroblast growth factor-induced angiogenesis. Jpn. J. Cancer Res. 85:5 (1994), 522–529.
19. [19] Cassinelli, G., Lanzi, C., Supino, R., Pratesi, G., Zuco, V., Laccabue, D., Cuccuru, G., Bombardelli, E., Zunino, F., Cellular bases of the antitumor activity of the novel taxane IDN 5109 (BAY59-8862) on hormone-refractory prostate cancer. Clin. Cancer Res. 8:8 (2002), 2647–2654.
20. [20] Hotchkiss, K.A., Ashton, A.W., Mahmood, R., Russell, R.G., Sparano, J.A., Schwartz, E.L., Inhibition of endothelial cell function in vitro and angiogenesis in vivo by docetaxel (Taxotere): association with impaired repositioning of the microtubule organizing center. Mol. Cancer Ther. 1:13 (2002), 1191–1200.
21. [21] Zhang, D., Hedlund, E.M., Lim, S., Chen, F., Zhang, Y., Sun, B., Cao, Y., Antiangiogenic agents significantly improve survival in tumor-bearing mice by increasing tolerance to chemotherapy-induced toxicity. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 4117–4122.
22. [22] Gillies, R.J., Verduzco, D., Gatenby, R.A., Evolutionary dynamics of carcinogenesis and why targeted therapy does not work. Nat. Rev. Cancer 12 (2012), 487–493.
23. [23] Ishak, R.S., Aad, S.A., Kyei, A., Farhat, F.S., Cutaneous manifestations of anti-angiogenic therapy in oncology: review with focus on VEGF inhibitors. Crit. Rev. Oncol. Hematol. 90:2 (2014), 152–164.
24. [24] Morbidelli, L., Donnini, S., Ziche, M., Targeting endothelial cell metabolism for cardio-protection from the toxicity of antitumor agents. Cardio Oncol., 2, 2016, 3.
25. [25] Recio, M.C., Andujar, I., Rios, J.L., Anti-inflammatory agents from plants: progress and potential. Curr. Med. Chem. 19:14 (2012), 2088–2103.
26. [26] Cowan, M.M., Plant products as antimicrobial agents. Clin. Microbiol. Rev. 12:4 (1999), 564–582.
27. [27] Sagar, S.M., Yance, D., Wong, R.K., Natural health products that inhibit angiogenesis: a potential source for investigational new agents to treat cancer-Part 1. Curr. Oncol. 13:1 (2006), 14–26.
28. [28] Wen, W., Lu, J., Zhang, K., Chen, S., Grape seed extract inhibits angiogenesis via suppression of the vascular endothelial growth factor receptor signaling pathway. Cancer Prev. Res. (Phila.) 1:7 (2008), 554–561.
29. [29] Wang, Z., Dabrosin, C., Yin, X., Fuster, M.M., Arreola, A., Rathmell, W.K., Generali, D., Nagaraju, G.P., El-Rayes, B., Ribatti, D., Chen, Y.C., Honoki, K., Fujii, H., Georgakilas, A.G., Nowsheen, S., Amedei, A., Niccolai, E., Amin, A., Ashraf, S.S., Helferich, B., Yang, X., Guha, G., Bhakta, D., Ciriolo, M.R., Aquilano, K., Chen, S., Halicka, D., Mohammed, S.I., Azmi, A.S., Bilsland, A., Keith, W.N., Jensen, L.D., Broad targeting of angiogenesis for cancer prevention and therapy. Semin. Cancer Biol. 35:Suppl (2015), S224–S243.
30. [30] Hanahan, D., Weinberg, R.A., Hallmarks of cancer: the next generation. Cell 144:5 (2011), 646–674.
31. [31] Finetti, F., Solito, R., Morbidelli, L., Giachetti, A., Ziche, M., Donnini, S., Prostaglandin E2 regulates angiogenesis via activation of fibroblast growth factor receptor-1. J. Biol. Chem. 283:4 (2008), 2139–2146.
32. [32] Donnini, S., Finetti, F., Terzuoli, E., Bazzani, L., Ziche, M., Targeting PGE2 signaling in tumor progression and angiogenesis. Forum Immunopathol. Dis. Ther. 5:3 (2014), 173–182.
33. [33] Liu, R.H., Health benefits of fruit and vegetables are from additive and synergistic combinations of phytochemicals. Am. J. Clin. Nutr. 78:Suppl. 3 (2003), 517S–520S.
34. [34] Tomé-Carneiro, J., Visioli, F., Polyphenol-based nutraceuticals for the prevention and treatment of cardiovascular disease: review of human evidence. Phytomedicine, 2015 pii: S0944-7113(15)00363-3.
35. [35] Huang, W.Y., Cai, Y.Z., Zhang, Y., Natural phenolic compounds from medicinal herbs and dietary plants: potential use for cancer prevention. Nutr. Cancer 62:1 (2010), 1–20.
36. [36] Coucha, M., Elshaer, S.L., Eldahshan, W.S., Mysona, B.A., El-Remessy, A.B., Molecular mechanisms of diabetic retinopathy: potential therapeutic targets. Middle East Afr. J. Ophthalmol. 22:2 (2015), 135–144.
37. [37] Sak, K., Chemotherapy and dietary phytochemical agents. Chemother. Res. Pract., 2012, 2012, 282570.
38. [38] Wang, C.Z., Luo, X., Zhang, B., Song, W.X., Ni, M., Mehendale, S., Xie, J.T., Aung, H.H., He, T.C., Yuan, C.S., Notoginseng enhances anti-cancer effect of 5-fluorouracil on human colorectal cancer cells. Cancer Chemother. Pharmacol. 60:1 (2007), 69–79.
39. [39] Singh, B.N., Singh, B.R., Sarma, B.K., Singh, H.B., Potential chemoprevention of N-nitrosodiethylamine-induced hepatocarcinogenesis by polyphenolics from Acacia nilotica bark. Chem. Biol. Interact. 181 (2009), 20–28.
40. [40] Singh, B.N., Shankar, S., Srivastava, R.K., Green tea catechin, epigallocatechin-3-gallate (EGCG): mechanisms, perspectives and clinical applications. Biochem. Pharmacol. 82 (2011), 1807–1821.
41. [41] Singh, B.N., Singh, H.B., Singh, A., Naqvi, A.H., Singh, B.R., Dietary phytochemicals alter epigenetic events and signaling pathways for inhibition of metastasis cascade: phytoblockers of metastasis cascade. Cancer Metastasis Rev. 33:1 (2014), 41–85.
42. [42] Desai, A.G., Qazi, G.N., Ganju, R.K., El-Tamer, M., Singh, J., Saxena, A.K., Bhat, H.K., Medicinal plants and cancer chemoprevention. Curr. Drug Metab. 9:7 (2008), 581–591.
43. [43] Sagar, S.M., Yance, D., Wong, R.K., Natural health products that inhibit angiogenesis: a potential source for investigational new agents to treat cancer—Part 1. Curr. Oncol. 13:1 (2006), 14–26.
44. [44] Larrosa, M., Lodovici, M., Morbidelli, L., Dolara, P., Hydrocaffeic and p-coumaric acids, natural phenolic compounds, inhibit UV-B damage in WKD human conjunctival cells in vitro and rabbit eye in vivo. Free Radic. Res. 42:10 (2008), 903–910.
45. [45] Lodovici, M., Caldini, S., Morbidelli, L., Akpan, V., Ziche, M., Dolara, P., Protective effect of 4-coumaric acid from UVB ray damage in the rabbit eye. Toxicology 255:1–2 (2009), 1–5.
46. [46] Naksuriya, O., Okonogi, S., Schiffelers, R.M., Hennink, W.E., Curcumin nanoformulations: a review of pharmaceutical properties and preclinical studies and clinical data related to cancer treatment. Biomaterials 35:10 (2014), 3365–3383.
47. [47] Aggarwal, B.B., Gupta, S.C., Sung, B., Curcumin: an orally bioavailable blocker of TNF and other pro-inflammatory biomarkers. Br. J. Pharmacol. 169:8 (2013), 1672–1692.
48. [48] Arbiser, J.L., Klauber, N., Rohan, R., van Leeuwen, R., Huang, M.T., Fisher, C., Flynn, E., Byers, H.R., Curcumin is an in vivo inhibitor of angiogenesis. Mol. Med. 4:6 (1998), 376–383.
49. [49] Hong, J.H., Ahn, K.S., Bae, E., Jeon, S.S., Choi, H.Y., The effects of curcumin on the invasiveness of prostate cancer in vitro and in vivo. Prostate Cancer Prostatic Dis. 9:2 (2006), 147–152.
50. [50] Yoysungnoen, P., Wirachwong, P., Bhattarakosol, P., Niimi, H., Patumraj, S., Effects of curcumin on tumor angiogenesis and biomarkers, COX-2 and VEGF, in hepatocellular carcinoma cell-implanted nude mice. Clin. Hemorheol. Microcirc. 34:1-2 (2006), 109–115.
51. [51] Hasima, N.1, Aggarwal, B.B., Cancer-linked targets modulated by curcumin. Int. J. Biochem. Mol. Biol. 3:4 (2012), 328–351.
52. [52] Bimonte, S., Barbieri, A., Palma, G., Rea, D., Luciano, A., D'Aiuto, M., Arra, C., Izzo, F., Dissecting the role of curcumin in tumour growth and angiogenesis in mouse model of human breast cancer. Biomed. Res. Int., 2015, 2015, 878134.
53. [53] Terzuoli, E., Donnini, S., Giachetti, A., Iñiguez, M.A., Fresno, M., Melillo, G., Ziche, M., Inhibition of hypoxia inducible factor-1 alpha by dihydroxyphenylethanol, a product from olive oil, blocks microsomal prostaglandin-E synthase-1/vascular endothelial growth factor expression and reduces tumor angiogenesis. Clin. Cancer Res. 16:16 (2010), 4207–4216.
54. [54] Terzuoli, E., Giachetti, A., Ziche, M., Donnini, S., Hydroxytyrosol, a product from olive oil, reduces colon cancer growth by enhancing epidermal growth factor receptor degradation. Mol. Nutr. Food Res. 60:3 (2016), 519–529.
55. [55] Scoditti, E., Calabriso, N., Massaro, M., Pellegrino, M., Storelli, C., Martines, G., De Caterina, R., Carluccio, M.A., Mediterranean diet polyphenols reduce inflammatory angiogenesis through MMP-9 and COX-2 inhibition in human vascular endothelial cells: a potentially protective mechanism in atherosclerotic vascular disease and cancer. Arch. Biochem. Biophys. 527:2 (2012), 81–89.
56. [56] Lamy, S., Ouanouki, A., Béliveau, R., Desrosiers, R.R., Olive oil compounds inhibit vascular endothelial growth factor receptor-2 phosphorylation. Exp. Cell Res. 322:1 (2014), 89–98.
57. [57] Manach, C., Scalbert, A., Morand, C., Remesy, C., Jimenez, L., Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr. 79:5 (2004), 727–747.
58. [58] Berrino, F., Mediterranean diet and its association with reduced invasive breast cancer risk. JAMA Oncol 2:4 (2016), 535–536.
59. [59] Visioli, F., The resveratrol fiasco. Pharmacol. Res., 90, 2014, 87.
60. [60] Tang, P.C., Ng, Y.F., Ho, S., Gyda, M., Chan, S.W., Resveratrol and cardiovascular health-promising therapeutic or hopeless illusion. Pharmacol. Res. 90 (2014), 88–115.
61. [61] Shukla, Y., Singh, R., Resveratrol and cellular mechanisms of cancer prevention. Ann. N. Y. Acad. Sci. 1215 (2011), 1–8.
62. [62] Garvin, S., Ollinger, K., Dabrosin, C., Resveratrol induces apoptosis and inhibits angiogenesis in human breast cancer xenografts in vivo. Cancer Lett. 231 (2006), 113–122.
63. [63] Bishayee, A., Cancer prevention and treatment with resveratrol: from rodent studies to clinical trials. Cancer Prev. Res. (Phila.) 2 (2009), 409–418.
64. [64] Cao, Z., Fang, J., Xia, C., Shi, X., Jiang, B.H., trans-3,4,5'-Trihydroxystibene inhibits hypoxia-inducible factor 1 alpha and vascular endothelial growth factor expression in human ovarian cancer cells. Clin. Cancer Res. 10:15 (2004), 5253–5263.
65. [65] Brakenhielm, E., Cao, R., Cao, Y., Suppression of angiogenesis, tumor growth, and wound healing by resveratrol, a natural compound in red wine and grapes. FASEB J. 15:10 (2001), 1798–1800.
66. [66] Liu, Z., Li, Y., Yang, R., Effects of resveratrol on vascular endothelial growth factor expression in osteosarcoma cells and cell proliferation. Oncol. Lett. 4:4 (2012), 837–839.
67. [67] Bishayee, A., Cancer prevention and treatment with resveratrol: from rodent studies to clinical trials. Cancer Prev. Res. (Phila.) 2:5 (2009), 409–418.
68. [68] Bishayee, A., Politis, T., Darvesh, A.S., Resveratrol in the chemoprevention and treatment of hepatocellular carcinoma. Cancer Treat. Rev. 36:1 (2010), 43–53.
69. [69] Srivastava, R.K., Unterman, T.G., Shankar, S., FOXO transcription factors and VEGF neutralizing antibody enhance antiangiogenic effects of resveratrol. Mol. Cell. Biochem. 337 (2010), 201–212.
70. [70] Lin, M.T., Yen, M.L., Lin, C.Y., Kuo, M.L., Inhibition of vascular endothelial growth factor-induced angiogenesis by resveratrol through interruption of Src-dependent vascular endothelial cadherin tyrosine phosphorylation. Mol. Pharmacol. 64 (2003), 1029–1036.
71. [71] Yu, H., Pan, C., Zhao, S., et al. Resveratrol inhibits tumor necrosis factor-alpha- mediated matrix metalloproteinase-9 expression and invasion of human hepatocellular carcinoma cells. Biomed. Pharmacother. 62 (2008), 366–372.
72. [72] Kimura, Y., Sumiyoshi, M., Baba, K., Antitumor activities of synthetic and natural stilbenes through antiangiogenic action. Cancer Sci. 99 (2008), 2083–2096.
73. [73] van Meeteren, M.E., Hendriks, J.J., Dijkstra, C.D., van Tol, E.A., Dietary compounds prevent oxidative damage and nitric oxide production by cells involved in demyelinating disease. Biochem. Pharmacol. 67 (2004), 967–975.
74. [74] Igura, K., Ohta, T., Kuroda, Y., Kaji, K., Resveratrol and quercetin inhibit angiogenesis in vitro. Cancer Lett. 171 (2001), 11–16.
75. [75] Tan, W.F., Lin, L.P., Li, M.H., Zhang, Y.X., Tong, Y.G., Xiao, D., Quercetin, Ding J., a dietary-derived flavonoid, possesses antiangiogenic potential. Eur. J. Pharmacol. 459 (2003), 255–262.
76. [76] Chiesi, M., Schwaller, R., Inhibition of constitutive endothelial NO-synthase activity by tannin and quercetin. Biochem. Pharmacol. 49:4 (1995), 495–501.
77. [77] Li, F., Bai, Y., Zhao, M., Huang, L., Li, S., Li, X., Chen, Y., Quercetin inhibits vascular endothelial growth factor-induced choroidal and retinal angiogenesis in vitro. Ophthalmic Res. 53:3 (2015), 109–116.
78. [78] Zhao, D., Qin, C., Fan, X., Li, Y., Gu, B., Inhibitory effects of quercetin on angiogenesis in larval zebrafish and human umbilical vein endothelial cells. Eur. J. Pharmacol. 723 (2014), 360–367.
79. [79] Lin, C., Wu, M., Dong, J., Quercetin-4'-O-β-D-glucopyranoside (QODG) inhibits angiogenesis by suppressing VEGFR2-mediated signaling in zebrafish and endothelial cells. PLoS One, 7(2), 2012, e31708.
80. [80] Jackson, S.J., Venema, R.C., Quercetin inhibits eNOS, microtubule polymerization, and mitotic progression in bovine aortic endothelial cells. J. Nutr. 136:5 (2006), 1178–1184.
81. [81] Xiao, X., Shi, D., Liu, L., Wang, J., Xie, X., Kang, T., Deng, W., Quercetin suppresses cyclooxygenase-2 expression and angiogenesis through inactivation of P300 signaling. PLoS One, 6(8), 2011, e22934.
82. [82] Yang, F., Jiang, X., Song, L., Wang, H., Mei, Z., Xu, Z., Xing, N., Quercetin inhibits angiogenesis through thrombospondin-1 upregulation to antagonize human prostate cancer PC-3 cell growth in vitro and in vivo. Oncol. Rep. 35:3 (2016), 1602–1610.
83. [83] Pratheeshkumar, P., Budhraja, A., Son, Y.O., Wang, X., Zhang, Z., Ding, S., Wang, L., Hitron, A., Lee, J.C., Xu, M., Chen, G., Luo, J., Shi, X., Quercetin inhibits angiogenesis mediated human prostate tumor growth by targeting VEGFR- 2 regulated AKT/mTOR/P70S6K signaling pathways. PLoS One, 7(10), 2012, e47516.
84. [84] Li, F., Bai, Y., Zhao, M., Huang, L., Li, S., Li, X., Chen, Y., Quercetin inhibits vascular endothelial growth factor-induced choroidal and retinal angiogenesis in vitro. Ophthalmic Res. 53:3 (2015), 109–116.
85. [85] Tsai, S.H., Liang, Y.C., Lin-Shiau, S.Y., Lin, J.K., Suppression of TNFalpha-mediated NFkappaB activity by myricetin and other flavonoids through downregulating the activity of IKK in ECV304 cells. J. Cell. Biochem. 74 (1999), 606–615.
86. [86] Suh, Y., Afaq, F., Johnson, J.J., Mukhtar, H., A plant flavonoid fisetin induces apoptosis in colon cancer cells by inhibition of COX2 and Wnt/EGFR/NF-kappaB-signaling pathways. Carcinogenesis 30 (2009), 300–307.
87. [87] Bagli, E., Stefaniotou, M., Morbidelli, L., Ziche, M., Psillas, K., Murphy, C., Fotsis, T., Luteolin inhibits vascular endothelial growth factor-induced angiogenesis; inhibition of endothelial cell survival and proliferation by targeting phosphatidylinositol 3'-kinase activity. Cancer Res. 64:21 (2004), 7936–7946.
88. [88] Fotsis, T., Pepper, M., Adlercreutz, H., Fleischmann, G., Hase, T., Montesano, R., Schweigerer, L., Genistein, a dietary-derived inhibitor of in vitro angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 90:7 (1993), 2690–2694.
89. [89] Koroma, B.M., de Juan, E. Jr., Phosphotyrosine inhibition and control of vascular endothelial cell proliferation by genistein. Biochem. Pharmacol. 48:4 (1994), 809–818.
90. [90] Banerjee, S., Li, Y., Wang, Z., Sarkar, F.H., Multi-targeted therapy of cancer by genistein. Cancer Lett. 269 (2008), 226–242.
91. [91] Kang, X., Jin, S., Zhang, Q., Antitumor and antiangiogenic activity of soy phytoestrogen on 7,12-dimethylbenz(a)anthracene-induced mammary tumors following ovariectomy in Sprague-Dawley rats. J. Food Sci. 74 (2009), H237–42.
92. [92] Farina, H.G., Pomies, M., Alonso, D.F., Gomez, D.E., Antitumor and antiangiogenic activity of soy isoflavone genistein in mouse models of melanoma and breast cancer. Oncol. Rep. 16 (2006), 885–891.
93. [93] Jung, Y.D., Kim, M.S., Shin, B.A., Chay, K.O., Ahn, B.W., Liu, W., Bucana, C.D., Gallick, G.E., Ellis, L.M., EGCG, a major component of green tea, inhibits tumour growth by inhibiting VEGF induction in human colon carcinoma cells. Br. J. Cancer 84:6 (2001), 844–850.
94. [94] Cao, Y., Cao, R., Angiogenesis inhibited by drinking tea. Nature, 398, 1999, 381.
95. [95] Sartippour, M.R., Shao, Z.M., Heber, D., Beatty, P., Zhang, L., Liu, C., Ellis, L., Liu, W., Go, V.L., Brooks, M.N., Green tea inhibits vascular endothelial growth factor (VEGF) induction in human breast cancer cells. J. Nutr. 132:8 (2002), 2307–2311.
96. [96] Masuda, M., Suzui, M., Lim, J.T., Deguchi, A., Soh, J.W., Weinstein, I.B., Epigallocatechin-3-gallate decreases VEGF production in head and neck and breast carcinoma cells by inhibiting EGFR-related pathways of signal transduction. J. Exp. Ther. Oncol. 2:6 (2002), 350–359.
97. [97] Leong, H., Mathur, P.S., Greene, G.L., Green tea catechins inhibit angiogenesis through suppression of STAT3 activation. Breast Cancer Res. Treat. 117 (2009), 505–515.
98. [98] Maeda-Yamamoto, M., Kawahara, H., Tahara, N., Tsuji, K., Hara, Y., Isemura, M., Effects of tea polyphenols on the invasion and matrix metalloproteinases activities of human fibrosarcoma HT1080 cells. J. Agric. Food Chem. 47:6 (1999), 2350–2354.
99. [99] Ramos, S., Effects of dietary flavonoids on apoptotic pathways related to cancer chemoprevention. J. Nutr. Biochem. 18 (2007), 427–442.
100. [100] Yang, H., Sun, D.K., Chen, D., Cui, Q.C., Gu, Y.Y., Jiang, T., Chen, W., Wan, S.B., Dou, Q.P., Antitumor activity of novel fluorosubstituted (−)-epigallocatechin-3-gallate analogs. Cancer Lett. 292 (2010), 48–53.
101. [101] Slivova, V., Zaloga, G., DeMichele, S.J., Mukerji, P., Huang, Y.S., Siddiqui, R., Harvey, K., Valachovicova, T., Sliva, D., Green tea polyphenols modulate secretion of urokinase plasminogen activator (uPA) and inhibit invasive behavior of breast cancer cells. Nutr. Cancer 52 (2005), 66–73.
102. [102] Sen, T., Moulik, S., Dutta, A., Choudhury, P.R., Banerji, A., Das, S., Roy, M., Chatterjee, A., Multifunctional effect of epigallocatechin-3-gallate (EGCG) in downregulation of gelatinase-A(MMP-2) in human breast cancer cell line MCF-7. Life Sci. 84 (2009), 194–204.
103. [103] Lin, J.K., Liang, Y.C., Lin-Shiau, S.Y., Cancer chemoprevention by tea polyphenols through mitotic signal transduction blockade. Biochem. Pharmacol. 58 (1999), 911–915.
104. [104] Jung, Y.D., Kim, M.S., Shin, B.A., Chay, K.O., Ahn, B.W., Liu, W., Bucana, C.D., Gallick, G.E., Ellis, L.M., EGCG, a major component of green tea, inhibits tumour growth by inhibiting VEGF induction in human colon carcinoma cells. Br. J. Cancer 84 (2001), 844–850.
105. [105] Khan, N., Adhami, V.M., Mukhtar, H., Review: green tea polyphenols in chemo-prevention of prostate cancer: preclinical and clinical studies. Nutr. Cancer 61 (2009), 836–841.
106. [106] Yang, C.S., Wang, X., Lu, G., Picinich, S.C., Cancer prevention by tea: animal studies, molecular mechanisms and human relevance. Nat. Rev. Cancer 9 (2009), 429–439.
107. [107] Hastak, K., Gupta, S., Ahmad, N., Agarwal, M.K., Agarwal, M.L., Mukhtar, H., Role of p53 and NF-kappaB in epigallocatechin-3-gallate-induced apoptosis of LNCaP cells. Oncogene 22 (2003), 4851–4859.
108. [108] Gu, J.W., Makey, K.L., Tucker, K.B., Chinchar, E., Mao, X., Pei, I., Thomas, E.Y., Miele, L.E.G.C.G., a major green tea catechin suppresses breast tumor angiogenesis and growth via inhibiting the activation of HIF-1α and NF-kB, and VEGF expression. Vasc. Cell, 5, 2013, 9.
109. [109] Du, G.J., Zhang, Z., Wen, X.D., Yu, C., Calway, T., Yuan, C.S., Wang, C.Z., Epigallocatechin Gallate (EGCG) is the most effective cancer chemopreventive polyphenol in green tea. Nutrients 4 (2012), 1679–1691.
110. [110] Mackenzie, G.G., Adamo, A.M., Decker, N.P., Oteiza, P.I., Dimeric procyanidin B2 inhibits constitutively active NF-kappaB in Hodgkin's lymphoma cells independently of the presence of IkappaB mutations. Biochem. Pharmacol. 75 (2008), 1461–1471.
111. [111] Kenny, T.P., Keen, C.L., Jones, P., Kung, H.J., Schmitz, H.H., Gershwin, M.E., Cocoa procyanidins inhibit proliferation and angiogenic signals in human dermal microvascular endothelial cells following stimulation by low-level H2O2. Exp. Biol. Med. (Maywood) 229 (2004), 765–771.
112. [112] Liu, Y., Gao, X., Deeb, D., Arbab, A.S., Dulchavsky, S.A., Gautam, S.C., Anticancer agent xanthohumol inhibits IL-2 induced signaling pathways involved in T cell proliferation. J. Exp. Ther. Oncol. 10 (2012), 1–8.
113. [113] Kim, Y.H., Shin, E.K., Kim, D.H., Lee, H.H., Park, J.H., Kim, J.K., Antiangiogenic effect of licochalcone A. Biochem. Pharmacol. 80 (2010), 1152–1159.
114. [114] Kwon, G.T., Cho, H.J., Chung, W.Y., Park, K.K., Moon, A., Park, J.H., Isoliquiritigenin inhibits migration and invasion of prostate cancer cells: possible mediation by decreased JNK/AP-1 signaling. J. Nutr. Biochem. 20 (2009), 663–676.
115. [115] Mochizuki, M., Yoo, Y.C., Matsuzawa, K., Sato, K., Saiki, I., Tono-oka, S., Samukawa, K., Azuma, I., Inhibitory effect of tumor metastasis in mice by saponins, ginsenoside-Rb2, 20(R)- and 20(S)-ginsenoside-Rg3, of red ginseng. Biol. Pharm. Bull. 18:9 (1995), 1197–1202.
116. [116] Sato, K., Mochizuki, M., Saiki, I., Yoo, Y.C., Samukawa, K., Azuma, I., Inhibition of tumor angiogenesis and metastasis by a saponin of Panax ginseng, ginsenoside-Rb2. Biol. Pharm. Bull. 17:5 (1994), 635–639.
117. [117] Morisaki, N., Watanabe, S., Tezuka, M., Zenibayashi, M., Shiina, R., Koyama, N., Kanzaki, T., Saito, Y., Mechanism of angiogenic effects of saponin from ginseng Radix rubra in human umbilical vein endothelial cells. Br. J. Pharmacol. 115:7 (1995), 1188–1193.
118. [118] Yang, H., Shi, G., Dou, Q.P., The tumor proteasome is a primary target for the natural anticancer compound Withaferin A isolated from Indian winter cherry. Mol. Pharmacol. 71 (2007), 426–437.
119. [119] Mohan, R., Hammers, H.J., Bargagna-Mohan, P., Zhan, X.H., Herbstritt, C.J., Ruiz, A., Zhang, L., Hanson, A.D., Conner, B.P., Rougas, J., Pribluda vs. Withaferin A is a potent inhibitor of angiogenesis. Angiogenesis 7 (2004), 115–122.
120. [120] Jayaprakasam, B., Zhang, Y., Seeram, N.P., Nair, M.G., Growth inhibition of human tumor cell lines by withanolides from Withania somnifera leaves. Life Sci. 74 (2003), 125–132.
121. [121] Park, J.S., Chew, B.P., Wong, T.S., Dietary lutein from marigold extract inhibits mammary tumor development in BALB/c mice. J. Nutr. 128 (1998), 1650–1656.
122. [122] Krinsky, N.I., Johnson, E.J., Carotenoid actions and their relation to health and disease. Mol. Aspects Med. 26 (2005), 459–516.
123. [123] Bertl, E., Bartsch, H., Gerhauser, C., Inhibition of angiogenesis and endothelial cell functions are novel sulforaphane-mediated mechanisms in chemo-prevention. Mol. Cancer Ther. 5 (2006), 575–585.
124. [124] Kowshik, J., Giri, H., Kishore, T.K., Kesavan, R., Vankudavath, R.N., Reddy, G.B., Dixit, M., Nagini, S., Ellagic acid inhibits VEGF/VEGFR2, PI3K/Akt and MAPK signaling cascades in the hamster cheek pouch carcinogenesis model. Anticancer Agents Med. Chem. 14:9 (2014), 1249–1260.
125. [125] Haraguchi, T., Kayashima, T., Okazaki, Y., Inoue, J., Mineo, S., Matsubara, K., Sakaguchi, E., Yanaka, N., Kato, N., Cecal succinate elevated by some dietary polyphenols may inhibit colon cancer cell proliferation and angiogenesis. J. Agric. Food Chem. 62:24 (2014), 5589–5594.
126. [126] Guruvayoorappan, C., Kuttan, G., Amentoflavone inhibits experimental tumor metastasis through a regulatory mechanism involving MMP-2, MMP-9, prolyl hydroxylase, lysyl oxidase, VEGF, ERK-1, ERK-2, STAT-1, NM23 and cytokines in lung tissues of C57BL/6 mice. Immunopharmacol. Immunotoxicol. 30 (2008), 711–727.
127. [127] Tarallo, V., Lepore, L., Marcellini, M., Dal Piaz, F., Tudisco, L., Ponticelli, S., Lund, F.W., Roepstorff, P., Orlandi, A., Pisano, C., et al. The biflavonoid amentoflavone inhibits neovascularization preventing the activity of proangiogenic vascular endothelial growth factors. J. Biol. Chem. 286 (2011), 19641–19651.
128. [128] Mousa, A.S., Mousa, S.A., Anti-angiogenesis efficacy of the garlic ingredient alliin and antioxidants: role of nitric oxide and p53. Nutr. Cancer 53:1 (2005), 104–110.
129. [129] Yi, L., Su, Q., Molecular mechanisms for the anti-cancer effects of diallyl disulfide. Food Chem. Toxicol. 57 (2013), 362–370.
130. [130] Eok-Cheon, K., Jeong-Ki, M., Tae-Yoon, K., Shin-Jeong, L., Hyun-Ok, Y., Sanghwa, H., Young-Myeong, K., Young-Guen, K., 6-Gingerol, a pungent ingredient of ginger, inhibits angiogenesis in vitro and in vivo. Biochem. Biophys. Res. Commun. 335 (2005), 300–308.
131. [131] Kanjoormana, M., Kuttan, G., Antiangiogenic activity of ursolic acid. Integr. Cancer Ther. 9 (2010), 224–235.
132. [132] Kim, H.N., Kim, H., Kong, J., Bae, S., Kim, Y., Lee, N., Cho, B.J., Lee, S.K., Kim, H.R., Hwang, Y.I., Kang, J.S., Lee, W.J., Vitamin C down-regulates VEGF production in B16F10 murine melanoma cells via the suppression of p42/44 MAPK activation. J. Cell. Biochem. 112 (2011), 894–901.
133. [133] Malafa, M.P., Fokum, F.D., Smith, L., Louis, A., Inhibition of angiogenesis and promotion of melanoma dormancy by vitamin E succinate. Ann. Surg. Oncol. 9 (2002), 1023–1032.
134. [134] Saha, S.K., Khuda-Bukhsh, A.R., Molecular approaches towards development of purified natural products and their structurally known derivatives as efficient anti-cancer drugs: current trends. Eur. J. Pharmacol. 714:1–3 (2013), 239–248.
135. [135] Mori, M., Supuran, C.T., Editorial: challenging organic syntheses and pharmacological applications of natural products and their derivatives. Curr. Pharm. Des. 21:38 (2015), 5451–5452.
136. [136] Ravishankar, D., Watson, K.A., Boateng, S.Y., Green, R.J., Greco, F., Osborn, H.M., Exploring quercetin and luteolin derivatives as antiangiogenic agents. Eur. J. Med. Chem. 97 (2015), 259–274.
137. [137] Manach, C., Scalbert, A., Morand, C., Remesy, C., Jimenez, L., Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr. 79:5 (2004), 727–747.
138. [138] Siddiqui, I.A., Adhami, V.M., Bharali, D.J., Hafeez, B.B., Asim, M., Khwaja, S.I., Ahmad, N., Cui, H., Mousa, S.A., Mukhtar, H., Introducing nanochemoprevention as a novel approach for cancer control: proof of principle with green tea polyphenol epigallocatechin-3-gallate. Cancer Res. 69:5 (2009), 1712–1716.
139. [139] Wang, L., Li, H., Wang, S., Liu, R., Wu, Z., Wang, C., Wang, Y., Chen, M., Enhancing the antitumor activity of berberine hydrochloride by solid lipid nanoparticle encapsulation. AAPS PharmSciTech 15:4 (2014), 834–844.
140. [140] Luo, H., Jiang, B., Li, B., Li, Z., Jiang, B.H., Chen, Y.C., Kaempferol nanoparticles achieve strong and selective inhibition of ovarian cancer cell viability. Int. J. Nanomed. 7 (2012), 3951–3959.
141. [141] Gou, M., Men, K., Shi, H., Xiang, M., Zhang, J., Song, J., Long, J., Wan, Y., Luo, F., Zhao, X., Qian, Z., Curcumin-loaded biodegradable polymeric micelles for colon cancer therapy in vitro and in vivo. Nanoscale 3:4 (2011), 1558–1567.
142. [142] Jain, A.K., Thanki, K., Jain, S., Co-encapsulation of tamoxifen and quercetin in polymeric nanoparticles: implications on oral bioavailability, antitumor efficacy, and drug-induced toxicity. Mol. Pharm. 10:9 (2013), 3459–3474.
143. [143] Narayanan, S., Mony, U., Vijaykumar, D.K., Koyakutty, M., Paul-Prasanth, B., Menon, D., Sequential release of epigallocatechin gallate and paclitaxel from PLGA-casein core/shell nanoparticles sensitizes drug-resistant breast cancer cells. Nanomedicine 11 (2015), 1399–1406.
144. [144] Gao, X., Wang, B., Wei, X., Men, K., Zheng, F., Zhou, Y., Zheng, Y., Gou, M., Huang, M., Guo, G., Huang, N., Qian, Z., Wei, Y., Anticancer effect and mechanism of polymer micelle-encapsulated quercetin on ovarian cancer. Nanoscale 4:22 (2012), 7021–7030.
145. [145] Long, Q., Xiel, Y., Huang, Y., Wu, Q., Zhang, H., Xiong, S., Liu, Y., Chen, L., Wei, Y., Zhao, X., Gong, C., Induction of apoptosis and inhibition of angiogenesis by PEGylated liposomal quercetin in both cisplatin-sensitive and cisplatin-resistant ovarian cancers. J. Biomed. Nanotechnol. 9:6 (2013), 965–975.
146. [146] Miura, T., Yuan, L., Sun, B., Fujii, H., Yoshida, M., Wakame, K., Kosuna, K., Isoflavone aglycone produced by culture of soybean extracts with basidiomycetes and its anti-angiogenic activity. Biosci. Biotechnol. Biochem. 66 (2002), 2626–2631.
147. [147] deVere White, R.W., Tsodikov, A., Stapp, E.C., Soares, S.E., Fujii, H., Hackman, R.M., Effects of a high dose, aglycone-rich soy extract on prostate-specific antigen and serum isoflavone concentrations in men with localized prostate cancer. Nutr. Cancer 62:8 (2010), 1036–1043.
148. [148] Donnini, S., Finetti, F., Lusini, L., Morbidelli, L., Cheynier, V., Barron, D., Williamson, G., Waltenberger, J., Ziche, M., Divergent effects of quercetin conjugates on angiogenesis. Br. J. Nutr. 95:5 (2006), 1016–1023.
149. [149] Bergers, G., Hanahan, D., Modes of resistance to anti-angiogenic therapy. Nat. Rev. Cancer 8 (2008), 592–603.
150. [150] Forssell, J., Oberg, A., Henriksson, M.L., Stenling, R., Jung, A., Palmqvist, R., High macrophage infiltration along the tumor front correlates with improved survival in colon cancer. Clin. Cancer Res. 13 (2007), 1472–1479.
151. [151] Garaude, J., Kent, A., van Rooijen, N., Blander, J.M., Simultaneous targeting of toll-and nod-like receptors induces effective tumor-specific immune responses. Sci. Transl. Med., 4, 2012 (120ra116).
152. [152] Mocanu, M.-M., Nagy, P., Szöll̋osi, J., Chemoprevention of breast cancer by dietary polyphenols. Molecules 20 (2015), 22578–22620.
153. [153] Zhou, J.R., Yu, L., Zhong, Y., Blackburn, G.L., Soy phytochemicals and tea bioactive components synergistically inhibit androgen-sensitive human prostate tumors in mice. J. Nutr. 133 (2003), 516–521.
154. [154] Zhou, J.R., Yu, L., Mai, Z., Blackburn, G.L., Combined inhibition of estrogen-dependent human breast carcinoma by soy and tea bioactive components in mice. Int. J. Cancer 108 (2004), 8–14.
155. [155] Bisacchi, D., Benelli, R., Vanzetto, C., Ferrari, N., Tosetti, F., Albini, A., Anti-angiogenesis and angioprevention: mechanisms, problems and perspectives. Cancer Detect. Prev. 27 (2003), 229–238.
156. [156] Rossi, T., Gallo, C., Bassani, B., Canali, S., Albini, A., Bruno, A., Drink your prevention: beverages with cancer preventive phytochemicals. Pol. Arch. Med. Wewn. 124:12 (2014), 713–722.
157. [157] Faruque, L.I., Lin, M., Battistella, M., Wiebe, N., Reiman, T., Hemmelgarn, B., Thomas, C., Tonelli, M., Systematic review of the risk of adverse outcomes associated with vascular endothelial growth factor inhibitors for the treatment of cancer. PLoS One, 9(7), 2014, e101145.
158. [158] Chatterjee, S., Bhattacharjee, B., Use of natural molecules as anti-angiogenic inhibitors for vascular endothelial growth factor receptor. Bioinformation 8:25 (2012), 1249–1254.