Oleuropein aglycone attenuates the pro-angiogenic phenotype of senescent fibroblasts: A functional study in endothelial cells

Journal of Functional Foods

Volumn 53, Issue , 2019, Pages 219-226

  Margheri, Francesca ^a   Menicacci, Beatrice ^a,b   Laurenzana, Anna ^a   Del Rosso, Mario ^a   Fibbi, Gabriella ^a   Cipolleschi, Maria Grazia ^a   Ruzzolini, Jessica ^a   Nediani, Chiara ^a   Mocali, Alessandra ^a   Giovannelli, Lisa ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF SIENA   (Italy)

Author keywords

ECFC; hMVEC; Oleuropein; SASP; Senescent fibroblasts

Indexed keywords

EID: 85059150009     PISSN: 17564646     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jff.2018.12.026     Document Type: Article

References (48)

1. Bayram, B., Ozcelik, B., Grimm, S., Roeder, T., Schrader, C., Ernst, I., Rimbach, G., A diet rich in olive oil phenolics reduces oxidative stress in the heart of SAMP8 mice by induction of Nrf2-dependent gene expression. Rejuvenation Research 15:1 (2012), 71–81, 10.1089/rej.2011.1245.
2. Bergers, G., Brekken, R., McMahon, G., Vu, T.H., Itoh, T., Tamaki, K., Hanahan, D., Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nature Cell Biology 2 (2000), 737–744.
3. Breuss, J.M., Uhrin, P., VEGF-initiated angiogenesis and the uPA/uPAR system. Cell Adhesion and Migration 6 (2012), 535–540, 10.4161/cam.22243.
4. Calabriso, N., Massaro, M., Scoditti, E., D'Amore, S., Gnoni, A., Pellegrino, M., Carluccio, M.A., Extra virgin olive oil rich in polyphenols modulates VEGF-induced angiogenic responses by preventing NADPH oxidase activity and expression. Journal of Nutritional Biochemistry 28 (2016), 19–29, 10.1016/j.jnutbio.2015.09.026.
5. Campisi, J., Aging, cellular senescence, and cancer. Annual Review of Physiology 75 (2013), 685–705, 10.1146/annurev-physiol-030212-183653.
6. Casamenti, F., Stefani, M., Olive polyphenols: New promising agents to combat aging-associated neurodegeneration. Expert Review of Neurotherapeutics 17:4 (2017), 345–358, 10.1080/14737175.2017.1245617.
7. Chun, T.H., Sabeh, F., Ota, I., Murphy, H., McDonagh, K.T., Holmbeck, K., Weiss, S.J., MT1-MMP-dependent neovessel formation within the confines of the three-dimensional extracellular matrix. The Journal of Cell Biology 167 (2004), 757–767.
8. Coppé, J.P., Patil, C.K., Rodier, F., Sun, Y., Muñoz, D.P., Goldstein, J., Campisi, J., Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biology 6 (2008), 2853–2868, 10.1371/journal.pbio.0060301.
9. Davalos, A.R., Coppe, J.P., Campisi, J., Desprez, P.Y., Senescent cells as a source of inflammatory factors for tumor progression. Cancer Metastasis Reviews 29:2 (2010), 273–283, 10.1007/s10555-010-9220-9.
10. de Bock, M., Thorstensen, E.B., Derraik, J.G.B., Henderson, H.V., Hofman, P.L., Cutfield, W.S., Human absorption and metabolism of oleuropein and hydroxytyrosol ingested as olive (Olea europaea L.) leaf extract. Molecular Nutrition & Food Research 57 (2013), 2079–2085, 10.1002/mnfr.201200795.
11. Huang, P.H., Chen, Y.H., Wang, C.H., Chen, J.S., Tsai, H.Y., Lin, F.Y., Lin, S.J., Matrix metalloproteinase-9 is essential for ischemia-induced neovascularization by modulating bone marrow-derived endothelial progenitor cells. Arteriosclerosis Thrombosis and Vascular Biology 29:8 (2009), 1179–1184, 10.1161/ATVBAHA.109.189175.
12. Koziol, A., Martín-Alonso, M., Clemente, C., Gonzalo, P., Arroyo, A.G., Site-specific cellular functions of MT1-MMP. European Journal of Cell Biology 91:11–12 (2012), 889–895, 10.1016/j.ejcb.2012.07.003.
13. Ksiazek, K., Jörres, A., Witowski, J., Senescence induces a proangiogenic switch in human peritoneal mesothelial cells. Rejuvenation Research 11:3 (2008), 681–683, 10.1089/rej.2008.0736.
14. Laurenzana, A., Fibbi, G., Margheri, F., Biagioni, A., Luciani, C., Del Rosso, M., Chillà, A., Endothelial progenitor cells in sprouting angiogenesis: proteases pave the way. Current Molecular Medicine 15:7 (2015), 606–620.
15. Leri, M., Oropesa-Nuñez, R., Canale, C., Raimondi, S., Giorgetti, S., Bruzzone, E., Bucciantini, M., Oleuropein aglycone: A polyphenol with different targets against amyloid toxicity. Biochimica Biophysica Acta 1862 (2018), 1432–1442, 10.1016/j.bbagen.2018.03.023.
16. Li, A., Dubey, S., Varney, M.L., Dave, B.J., Singh, R.K., Il-8 directly enhanced endothelial cell survival, proliferation, and matrix metalloproteinases production and regulated angiogenesis. The Journal of Immunology 170 (2003), 3369–3376.
17. Lijnen, H.R., Matrix metalloproteinases and cellular fibrinolytic activity. Biochemistry 67 (2002), 107–115.
18. Liston, D.R., Davis, M., Clinically relevant concentrations of anticancer drugs: a guide for nonclinical studies. Clinical Cancer Research 23 (2017), 3489–3498, 10.1158/1078-0432.CCR-16-3083.
19. Liu, J., Huang, J., Yao, W.Y., Ben, Q.W., Chen, D.F., He, X.Y., Yuan, Y.Z., The origins of vascularization in tumors. Frontiers in Bioscience 17 (2012), 2559–2565.
20. Luccarini, I., Pantano, D., Nardiello, P., Cavone, L., Lapucci, A., Miceli, C., Casamenti, F., The polyphenol oleuropein aglycone modulates the PARP1-SIRT1 interplay: an in vitro and in vivo study. Journal of Alzheimers Disease 54:2 (2016), 737–750, 10.3233/JAD-160471.
21. Margheri, F., Chillà, A., Laurenzana, A., Serratì, S., Mazzanti, B., Saccardi, R., Fibbi, G., Endothelial progenitor cell-dependent angiogenesis requires localization of the full-length form of uPAR in caveolae. Blood 118:13 (2011), 3743–3755, 10.1182/blood-2011-02-338681.
22. Margheri, F., Serratì, S., Lapucci, A., Chillà, A., Bazzichi, L., Bombardieri, S., Del Rosso, M., Modulation of the angiogenic phenotype of normal and systemic sclerosis endothelial cells by gain-loss of function of pentraxin 3 and matrix metalloproteinase 12. Arthritis Rheum 62:8 (2010), 2488–2498, 10.1002/art.27522.
23. Menendez, J.A., Joven, J., Aragonès, G., Barrajón-Catalán, E., Beltrán-Debón, R., Borrás-Linares, I., Segura-Carretero, A., Xenohormetic and anti-aging activity of secoiridoid polyphenols present in extra virgin olive oil: A new family of gerosuppressant agents. Cell Cycle 12:4 (2013), 555–578.
24. Menicacci, B., Cipriani, C., Margheri, F., Mocali, A., Giovannelli, L., Modulation of the senescence-associated inflammatory phenotype in human fibroblasts by olive phenols. International Journal of Molecular Sciences, 18(11), 2017, E2275, 10.3390/ijms18112275.
25. Menicacci, B., Laurenzana, A., Chillà, A., Margheri, F., Peppicelli, S., Tanganelli, E., Mocali, A., Chronic resveratrol treatment inhibits MRC5 fibroblast SASP-related protumoral effects on melanoma cells. The Journals of Gerontology Series A 72:9 (2017), 1187–1195, 10.1093/gerona/glw336.
26. Menicacci, B., Margheri, F., Laurenzana, A., Chillà, A., Del Rosso, M., Giovannelli, L., Mocali, A., Chronic resveratrol treatment reduces the pro-angiogenic effect of human fibroblast “Senescent Associated Secretory Phenotype” (SASP) on endothelial colony forming cells: The role of IL8. The Journals of Gerontology Series A, 2018, 10.1093/Gerona/gly175.
27. Miceli, C., Santin, Y., Manzella, N., Coppini, R., Berti, A., Stefani, M., Nediani, C., Oleuropein aglycone protects against MAO-A-induced autophagy impairment and cardiomyocyte death through activation of TFEB. Oxidative Medicine and Cellular Longevity, 26, 2018, 8067592, 10.1155/2018/8067592.
28. Oliveras-López, M.J., Berná, G., Jurado-Ruiz, E., López-García de la Serrana, H., Martín, F., Consumption of extra-virgin olive oil rich in phenolic compounds has beneficial antioxidant effects in healthy human adults. Journal of Functional Foods 10 (2014), 475–484.
29. Ortiz-Montero, P., Londoño-Vallejo, A., Vernot, J.P., Senescence-associated IL-6 and IL-8 cytokines induce a self- and cross-reinforced senescence/inflammatory milieu strengthening tumorigenic capabilities in the MCF-7 breast cancer cell line. Cell Communication Signalling, 15(1), 2017, 17.
30. Palmieri, D., Aliakbarian, B., Casazza, A.A, Ferrari, N., Spinella, G., Pane, B., Palombo, D., Effects of polyphenol extract from olive pomace on anoxia-induced endothelial dysfunction. Microvascular Research 83:3 (2012), 281–289, 10.1016/j.mvr.2012.02.010.
31. Parkinson, L., Cicerale, S., The health benefiting mechanisms of virgin olive oil phenolic compounds. Molecules, 21(12), 2016, E1734, 10.3390/molecules21121734.
32. Pepper, M.S., Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arteriosclerosis Thrombosis and Vascular Biology 21 (2001), 1104–1117.
33. Piroddi, M., Albini, A., Fabiani, R., Giovannelli, L., Luceri, C., Natella, F., Galli, F., Nutrigenomics of extra-virgin olive oil: A review. Biofactors 43:1 (2017), 17–41, 10.1002/biof.1318.
34. Pitozzi, V., Jacomelli, M., Catelan, D., Servili, M., Taticchi, A., Biggeri, A., Giovannelli, L., Long-term dietary extra-virgin olive oil rich in polyphenols reverses age-related dysfunctions in motor coordination and contextual memory in mice: Role of oxidative stress. Rejuvenation Research 15:6 (2012), 601–612, 10.1089/rej.2012.1346.
35. Pitozzi, V., Mocali, A., Laurenzana, A., Giannoni, E., Cifola, I., Battaglia, C., Giovannelli, L., Chronic resveratrol treatment ameliorates cell adhesion and mitigates the inflammatory phenotype in senescent human fibroblasts. The Journals of Gerontology Series A 68:4 (2013), 371–381, 10.1093/gerona/gls183.
36. Rigacci, S., Olive oil phenols as promising multi-targeting agents against Alzheimer's disease. Advances in Experimental Medicine and Biology 863 (2015), 1–20.
37. Rigacci, S., Miceli, C., Nediani, C., Berti, A., Cascella, R., Pantano, D., Stefani, M., Oleuropein aglycone induces autophagy via the AMPK/mTOR signalling pathway: A mechanistic insight. Oncotarget 6:34 (2015), 35344–35357.
38. Rigacci, S., Stefani, M., Nutraceutical properties of olive oil polyphenols. An itinerary from cultured cells through animal models to humans. International Journal of Molecular Sciences, 17(6), 2016, E843, 10.3390/ijms17060843.
39. Ruzzolini, J., Peppicelli, S., Andreucci, E., Bianchini, F., Scardigli, A., Romani, Calorini, L., Oleuropein, the main polyphenol of Olea europaea leaf extract, has an anti cancer effect on human BRAF melanoma cells and potentiates the cytotoxicity of current chemotherapies. Nutrients, 10, 2018, 1950, 10.3390/nu10121950.
40. Scoditti, E., Calabriso, N., Massaro, M., Pellegrino, M., Storelli, C., Martines, G., 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. Archives of Biochemistry and Biophysics 527:2 (2012), 81–89, 10.1016/j.abb.2012.05.003.
41. Senger, D.R., Davis, G.E., Angiogenesis. Cold Spring Harbor Perspectives in Biology, 3, 2011, a005090, 10.1101/cshperspect.a005090.
42. Souza, P.A.L., Marcadenti, A., Portal, V.L., Effects of olive oil phenolic compounds on inflammation in the prevention and treatment of coronary artery disease. Nutrients, 9(10), 2017, E1087, 10.3390/nu9101087.
43. Terzuoli, E., Donnini, S., Giachetti, A., Iñiguez, M.A., Fresno, M., Melillo, G., Ziche, M., Inhibition of hypoxia inducible factor-1alpha by dihydroxyphenylethanol, a product from olive oil, blocks microsomal prostaglandin-E synthase-1/vascular endothelial growth factor expression and reduces tumor angiogenesis. Clinical Cancer Research 16:16 (2010), 4207–4216, 10.1158/1078-0432.CCR-10-0156.
44. Van Hinsbergh, V.W., Engelse, M.A., Quax, P.H., Pericellular proteases in angiogenesis and vasculogenesis. Arteriosclerosis Thrombosis and Vascular Biology 26 (2006), 716–728, 10.1161/01.ATV.0000209518.58252.17.
45. Vegran, F., Boidot, R., Michiels, C., Sonveaux, P., Feron, O., Lactate influx through the endothelial cell monocarboxylate transporter mct1 supports an nf-kappab/il-8 pathway that drives tumor angiogenesis. Cancer Research 71 (2011), 2550–2560, 10.1158/0008-5472.CAN-10-2828.
46. Vissers, M.N., Zock, P.L., Roodenburg, A.J., Leenen, R., Katan, M.B., Olive oil phenols are absorbed in humans. The Journal of Nutrition 132 (2002), 409–417.
47. Wu, Y., Dai, J., Schmuckler, N.G., Bakdash, N., Yoder, M.C., Overall, C.M., Colman, R.W., Cleaved high molecular weight kininogen inhibits tube formation of endothelial progenitor cells via suppression of matrix metalloproteinase 2. Journal of Thrombosis and Haemostasis 8:1 (2010), 185–193, 10.1111/j.1538-7836.2009.03662.x.
48. Xing, F., Saidou, J., Watabe, K., Cancer associated fibroblasts (CAFs) in tumor microenvironment. Frontiers in Bioscience 15 (2010), 166–179.