Natural Bioactive Compounds As Protectors Of Mitochondrial Dysfunction In Cardiovascular Diseases And Aging
Abstract
1. Introduction
2. Oxidative Stress in Cardiovascular Diseases
3. Mitochondrial Dysfunction in CVD
4. Mitochondrial Dysfunction in Aging: Crossing Point with CVD?
5. Bioactive Compounds with Mitochondrial Protective Function
6. Conclusions
Funding
Conflicts of Interest
References
- Nichols, M.; Townsend, N.; Wilson, L.; Bhatnagar, P.; Wickramasinghe, K.; Rayner, M. Cardiovascular disease in Europe: Epidemiological update 2016. Eur. Hear. J. 2016, 37, 3232–3245. [Google Scholar]
- Alwan, A. Global Status Report on Noncommunicable Diseases 2010; World Health Organization: Geneva, Switzerland, 2011. [Google Scholar]
- Gensini, G.F.; Comeglio, M.; Colella, A. Classical risk factors and emerging elements in the risk profile for coronary artery disease. Eur. Heart J. 1998, 19, 53–61. [Google Scholar]
- Abbott, R.D.; McGee, D. The Framingham Study, Section 37: The probability of developing certain cardiovascular diseases in eight years at specified values of some characteristics. NIH Publ. 1987, 1987, 87–2284. [Google Scholar]
- Salas-Salvadó, J.; Becerra-Tomás, N.; García-Gavilán, J.F.; Bulló, M.; Barrubés, L. Mediterranean Diet and Cardiovascular Disease Prevention: What Do We Know? Prog. Cardiovasc. Dis. 2018. [Google Scholar] [CrossRef]
- Bowen, K.J.; Sullivan, V.K.; Kris-Etherton, P.M.; Petersen, K.S. Nutrition and Cardiovascular Disease—An Update. Curr. Atheroscler. Rep. 2018, 20, 8. [Google Scholar] [CrossRef]
- Fuentes, Q.E.; Fuentes, Q.F.; Andrés, V.; Pello, O.M.; de Mora, J.F.; Palomo, G.I. Role of platelets as mediators that link inflammation and thrombosis in atherosclerosis. Platelets 2013, 24, 255–262. [Google Scholar] [CrossRef]
- Naghavi, M.; Libby, P.; Falk, E.; Casscells, S.W.; Litovsky, S.; Rumberger, J.; Badimon, J.J.; Stefanadis, C.; Moreno, P.; Pasterkamp, G. From vulnerable plaque to vulnerable patient a call for new definitions and risk assessment strategies: Part I. Circulation 2003, 108, 1664–1672. [Google Scholar] [CrossRef]
- Krötz, F.; Sohn, H.Y.; Gloe, T.; Zahler, S.; Riexinger, T.; Schiele, T.M.; Becker, B.F.; Theisen, K.; Klauss, V.; Pohl, U. NAD [P] H oxidase–dependent platelet superoxide anion release increases platelet recruitment. Blood 2002, 100, 917–924. [Google Scholar] [CrossRef]
- Walsh, T.G.; Berndt, M.C.; Carrim, N.; Cowman, J.; Kenny, D.; Metharom, P. The role of Nox1 and Nox2 in GPVI-dependent platelet activation and thrombus formation. Redox Biol. 2014, 2, 178–186. [Google Scholar] [CrossRef]
- Siasos, G.; Tsigkou, V.; Kosmopoulos, M.; Theodosiadis, D.; Simantiris, S.; Tagkou, N.; Tsimpiktsioglou, A.; Stampouloglou, P.; Oikonomou, E.; Mourouzis, K.; et al. Mitochondria and cardiovascular diseases-from pathophysiology to treatment. Ann. Transl. Med. 2018, 6, 1–22. [Google Scholar] [CrossRef]
- Kanaan, G.N.; Harper, M.E. Cellular redox dysfunction in the development of cardiovascular diseases. Biochim. Biophys. Acta 2017, 1861, 2822–2829. [Google Scholar] [CrossRef]
- Watson, R.R.; Schönlau, F. Nutraceutical and antioxidant effects of a delphinidin-rich maqui berry extract Delphinol®: A review. Minerva Cardioangiol. 2015, 63, 1–12. [Google Scholar]
- Luo, Y.; Shang, P.; Li, D. Luteolin: A Flavonoid that Has Multiple Cardio-Protective Effects and Its Molecular Mechanisms. Front. Pharmacol. 2017, 8, 692. [Google Scholar] [CrossRef]
- Rossman, M.J.; Santos-Parker, J.R.; Steward, C.A.C.; Bispham, N.Z.; Cuevas, L.M.; Rosenberg, H.L.; Woodward, K.A.; Chonchol, M.; Gioscia-Ryan, R.A.; Murphy, M.P.; et al. Chronic Supplementation With a Mitochondrial Antioxidant [MitoQ] Improves Vascular Function in Healthy Older Adults. Hypertension 2018, 71, 1056–1063. [Google Scholar] [CrossRef]
- Papaharalambus, C.A.; Griendling, K.K. Basic mechanisms of oxidative stress and reactive oxygen species in cardiovascular injury. Trends Cardiovasc. Med. 2007, 17, 48–54. [Google Scholar] [CrossRef]
- Virdis, A.; Duranti, E.; Taddei, S. Oxidative stress and vascular damage in hypertension: Role of angiotensin II. Int. J. Hypertens. 2011, 2011, 1–7. [Google Scholar] [CrossRef]
- Keaney, J.F., Jr.; Larson, M.G.; Vasan, R.S.; Wilson, P.W.; Lipinska, I.; Corey, D.; Massaro, J.M.; Sutherland, P.; Vita, J.A.; Benjamin, E.J. Obesity and systemic oxidative stress: Clinical correlates of oxidative stress in the Framingham Study. Arterioscler. Thromb. Vasc. Biol. 2003, 23, 434–439. [Google Scholar] [CrossRef]
- Yang, R.-L.; Shi, Y.-H.; Hao, G.; Li, W.; Le, G.-W. Increasing Oxidative Stress with Progressive Hyperlipidemia in Human: Relation between Malondialdehyde and Atherogenic Index. J. Clin. Biochem. Nutr. 2008, 43, 154–158. [Google Scholar] [CrossRef]
- Otani, H. Oxidative Stress as Pathogenesis of Cardiovascular Risk Associated with Metabolic Syndrome. Antioxid. Redox Signal. 2010, 15, 1911–1926. [Google Scholar] [CrossRef]
- Schulz, E.; Gori, T.; Münzel, T. Oxidative stress and endothelial dysfunction in hypertension. Hypertens. Res. 2011, 34, 665–673. [Google Scholar] [CrossRef]
- Sandoo, A.; Van Zanten, J.J.V.; Metsios, G.S.; Carroll, D.; Kitas, G.D. The Endothelium and Its Role in Regulating Vascular Tone. Open Cardiovasc. Med. J. 2010, 4, 302–312. [Google Scholar] [CrossRef]
- Galley, H.F.; Webster, N.R. Physiology of the endothelium. Br. J. Anaesth. 2004, 93, 105–113. [Google Scholar] [CrossRef]
- Touyz, R.M.; Briones, A.M. Reactive oxygen species and vascular biology: Implications in human hypertension. Hypertens. Res. 2011, 34, 5–14. [Google Scholar] [CrossRef]
- Chrissobolis, S. Oxidative stress and endothelial dysfunction in cerebrovascular disease. Front. Biosci. 2011, 16, 1733. [Google Scholar] [CrossRef]
- Badimon, L.; Vilahur, G. Thrombosis formation on atherosclerotic lesions and plaque rupture. J. Intern. Med. 2014, 276, 618–632. [Google Scholar] [CrossRef]
- Gimbrone, M.A.; García-Cardeña, G. Endothelial Cell Dysfunction and the Pathobiology of Atherosclerosis. Circ. Res. 2016, 118, 620–636. [Google Scholar] [CrossRef]
- Wachowicz, B.; Olas, B.; Zbikowska, H.M.; Buczyński, A. Generation of reactive oxygen species in blood platelets. Platelets 2002, 13, 175–182. [Google Scholar] [CrossRef]
- Qiao, J.; Arthur, J.F.; Gardiner, E.E.; Andrews, R.K.; Zeng, L.; Xu, K. Regulation of platelet activation and thrombus formation by reactive oxygen species. Redox Biol. 2018, 14, 126–130. [Google Scholar] [CrossRef]
- Incalza, M.A.; D’Oria, R.; Natalicchio, A.; Perrini, S.; Laviola, L.; Giorgino, F. Oxidative stress and reactive oxygen species in endothelial dysfunction associated with cardiovascular and metabolic diseases. Vasc. Pharmacol. 2018, 100, 1–19. [Google Scholar] [CrossRef]
- Sirker, A.; Zhang, M.; Shah, A.M. NADPH oxidases in cardiovascular disease: Insights from in vivo models and clinical studies. Basic Res. Cardiol. 2011, 106, 735–747. [Google Scholar] [CrossRef]
- Virdis, A.; Bacca, A.; Colucci, R.; Duranti, E.; Fornai, M.; Materazzi, G.; Ippolito, C.; Bernardini, N.; Blandizzi, C.; Bernini, G.; et al. Endothelial Dysfunction in Small Arteries of Essential Hypertensive Patients: Role of Cyclooxygenase-2 in Oxidative Stress Generation. Hypertension 2013, 62, 337–344. [Google Scholar] [CrossRef] [PubMed]
- Higgins, P.; Dawson, J.; Lees, K.R.; McArthur, K.; Quinn, T.J.; Walters, M.R. Xanthine Oxidase Inhibition For The Treatment Of Cardiovascular Disease: A Systematic Review and Meta-Analysis. Cardiovasc. Ther. 2011, 30, 217–226. [Google Scholar] [CrossRef] [PubMed]
- Rochette, L.; Lorin, J.; Zeller, M.; Guilland, J.-C.; Lorgis, L.; Cottin, Y.; Vergely, C. Nitric oxide synthase inhibition and oxidative stress in cardiovascular diseases: Possible therapeutic targets? Pharmacol. Ther. 2013, 140, 239–257. [Google Scholar] [CrossRef] [PubMed]
- Walters, J.W.; Amos, D.; Ray, K.; Santanam, N. Mitochondrial redox status as a target for cardiovascular disease. Curr. Opin. Pharmacol. 2016, 27, 50–55. [Google Scholar] [CrossRef]
- Vásquez-Trincado, C.; García-Carvajal, I.; Pennanen, C.; Parra, V.; Hill, J.A.; Rothermel, B.A.; Lavandero, S. Mitochondrial dynamics, mitophagy and cardiovascular disease. J. Physiol. 2015, 594, 509–525. [Google Scholar] [CrossRef]
- Ballinger, S.W. Mitochondrial dysfunction in cardiovascular disease. Free. Radic. Boil. Med. 2005, 38, 1278–1295. [Google Scholar] [CrossRef]
- Dikalov, S. Crosstalk between mitochondria and NADPH oxidases. Free. Radic. Boil. Med. 2011, 51, 1289–1301. [Google Scholar] [CrossRef]
- Brandes, R.P.; Weissmann, N.; Schröder, K. NADPH oxidases in cardiovascular disease. Free. Radic. Boil. Med. 2010, 49, 687–706. [Google Scholar] [CrossRef]
- Gray, S.P.; Di Marco, E.; Okabe, J.; Szyndralewiez, C.; Heitz, F.; Montezano, A.C.; de Haan, J.B.; Koulis, C.; El-Osta, A.; Andrews, K.L.; et al. NADPH oxidase 1 plays a key role in diabetes mellitus-accelerated atherosclerosis. Circulation 2013, 127, 1888–1902. [Google Scholar] [CrossRef]
- Gimenez, M.; Schickling, B.M.; Lopes, L.R.; Miller, F.J., Jr. Nox1 in cardiovascular diseases: Regulation and pathophysiology. Clin. Sci. 2016, 130, 151–165. [Google Scholar] [CrossRef]
- Judkins, C.P.; Diep, H.; Broughton, B.R.; Mast, A.E.; Hooker, E.U.; Miller, A.A.; Selemidis, S.; Dusting, G.J.; Sobey, C.G.; Drummond, G.R. Direct evidence of a role for Nox2 in superoxide production, reduced nitric oxide bioavailability, and early atherosclerotic plaque formation in ApoE-/- mice. Am. J. Physiol. Circ. Physiol. 2010, 298, H24–H32. [Google Scholar] [CrossRef] [PubMed]
- Quesada, I.M.; Lucero, A.; Amaya, C.; Meijles, D.N.; Cifuentes, M.E.; Pagano, P.J.; Castro, C. Selective inactivation of NADPH oxidase 2 causes regression of vascularization and the size and stability of atherosclerotic plaques. Atherosclerosis 2015, 242, 469–475. [Google Scholar] [CrossRef] [PubMed]
- Fulton, D.J.R.; Barman, S.A. Clarity on the Isoform Specific Roles of NADPH-oxidases [Nox] and Nox4 in Atherosclerosis. Arter. Thromb. Vasc. Boil. 2016, 36, 579–581. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Gray, S.P.; Di Marco, E.; Kennedy, K.; Chew, P.; Okabe, J.; El-Osta, A.; Calkin, A.C.; Biessen, E.A.; Touyz, R.M.; Cooper, M.E.; et al. Reactive Oxygen Species Can Provide Atheroprotection via NOX4-Dependent Inhibition of Inflammation and Vascular Remodeling. Arter. Thromb. Vasc. Boil. 2016, 36, 295–307. [Google Scholar] [CrossRef] [PubMed]
- Montezano, A.C.; Tsiropoulou, S.; Dulak-Lis, M.; Harvey, A.; Camargo, L.D.L.; Touyz, R.M. Redox signaling, Nox5 and vascular remodeling in hypertension. Curr. Opin. Nephrol. Hypertens. 2015, 24, 425–433. [Google Scholar] [CrossRef] [PubMed]
- Montezano, A.; Harvey, A.; Rios, F.; Beatie, W.; McPherson, L.; Thomson, J.; Holterman, C.E.; Kennedy, C.; Touyz, R.M. 151 Nox5 induces vascular dysfunction and arterial remodelling independently of blood pressure elevation in ang ii-infused nox5-expressing mice. Heart 2017, 103, A111. [Google Scholar] [CrossRef]
- Mitchell, J.A.; Warner, T.D. COX isoforms in the cardiovascular system: Understanding the activities of non-steroidal anti-inflammatory drugs. Nat. Rev. Drug Discov. 2006, 5, 75–86. [Google Scholar] [CrossRef]
- Sellers, R.S.; Radi, Z.A.; Khan, N.K. Pathophysiology of Cyclooxygenases in Cardiovascular Homeostasis. Veter-Pathology 2010, 47, 601–613. [Google Scholar] [CrossRef]
- Fitzpatrick, F.A. Cyclooxygenase enzymes: Regulation and function. Curr. Pharm. Des. 2004, 10, 577–588. [Google Scholar] [CrossRef]
- Mitchell, J.A.; Kirkby, N.S. Eicosanoids, prostacyclin and cyclooxygenase in the cardiovascular system. Br. J. Pharmacol. 2018, 176, 1038–1050. [Google Scholar] [CrossRef]
- Zweier, J.L.; Talukder, M.H. The role of oxidants and free radicals in reperfusion injury. Cardiovasc. Res. 2006, 70, 181–190. [Google Scholar] [CrossRef] [PubMed]
- Nomura, J.; Busso, N.; Ives, A.; Matsui, C.; Tsujimoto, S.; Shirakura, T.; Tamura, M.; Kobayashi, T.; So, A.; Yamanaka, Y. Xanthine Oxidase Inhibition by Febuxostat Attenuates Experimental Atherosclerosis in Mice. Sci. Rep. 2014, 4, 4554. [Google Scholar] [CrossRef] [PubMed]
- Patetsios, P.; Song, M.; Shutze, W.P.; Pappas, C.; Rodino, W.; Ramirez, J.A.; Panetta, T.F. Identification of uric acid and xanthine oxidase in atherosclerotic plaque. Am. J. Cardiol. 2001, 88, 188–191. [Google Scholar] [CrossRef]
- Kohagura, K.; Tana, T.; Higa, A.; Yamazato, M.; Ishida, A.; Nagahama, K.; Sakima, A.; Iseki, K.; Ohya, Y. Effects of xanthine oxidase inhibitors on renal function and blood pressure in hypertensive patients with hyperuricemia. Hypertens. Res. 2016, 39, 593. [Google Scholar] [CrossRef] [PubMed]
- Lei, J.; Vodovotz, Y.; Tzeng, E.; Billiar, T.R. Nitric oxide, a protective molecule in the cardiovascular system. Nitric Oxide 2013, 35, 175–185. [Google Scholar] [CrossRef] [PubMed]
- Godo, S.; Shimokawa, H. Divergent roles of endothelial nitric oxide synthases system in maintaining cardiovascular homeostasis. Free Radic. Boil. Med. 2017, 109, 4–10. [Google Scholar] [CrossRef]
- Förstermann, U. Nitric oxide and oxidative stress in vascular disease. Pflügers Arch.-Eur. J. Physiol. 2010, 459, 923–939. [Google Scholar] [CrossRef]
- Li, L.; Chen, W.; Rezvan, A.; Jo, H.; Harrison, D.G. Tetrahydrobiopterin deficiency and nitric oxide synthase uncoupling contribute to atherosclerosis induced by disturbed flow. Arter. Thromb. Vasc. Boil. 2011, 31, 1547–1554. [Google Scholar] [CrossRef]
- Zhang, M.; Wen, J.; Wang, X.; Xiao, C. High‑dose folic acid improves endothelial function by increasing tetrahydrobiopterin and decreasing homocysteine levels. Mol. Med. Rep. 2014, 10, 1609–1613. [Google Scholar] [CrossRef]
- Sun, N.; Finkel, T. Cardiac mitochondria: A surprise about size. J. Mol. Cell. Cardiol. 2015, 82, 213–215. [Google Scholar] [CrossRef]
- Dai, D.-F.; Rabinovitch, P.S.; Ungvari, Z. Mitochondria and Cardiovascular Aging. Circ. Res. 2012, 110. [Google Scholar] [CrossRef] [PubMed]
- Liesa, M.; Shirihai, O.S. Mitochondrial Dynamics in the Regulation of Nutrient Utilization and Energy Expenditure. Cell Metab. 2013, 17, 491–506. [Google Scholar] [CrossRef] [PubMed]
- Chistiakov, D.A.; Shkurat, T.P.; Melnichenko, A.A.; Grechko, A.V.; Orekhov, A.N. The role of mitochondrial dysfunction in cardiovascular disease: A brief review. Ann. Med. 2018, 50, 121–127. [Google Scholar] [CrossRef] [PubMed]
- Ong, S.-B.; Hausenloy, D.J. Mitochondrial morphology and cardiovascular disease. Cardiovasc. Res. 2010, 88, 16–29. [Google Scholar] [CrossRef]
- Sharp, W.W.; Fang, Y.H.; Han, M.; Zhang, H.J.; Hong, Z.; Banathy, A.; Morrow, E.; Ryan, J.J.; Archer, S.L. Dynamin-related protein 1 [Drp1]-mediated diastolic dysfunction in myocardial ischemia-reperfusion injury: Therapeutic benefits of Drp1 inhibition to reduce mitochondrial fission. FASEB J. 2013, 28, 316–326. [Google Scholar] [CrossRef]
- Karbowski, M.; Lee, Y.-J.; Gaume, B.; Jeong, S.-Y.; Frank, S.; Nechushtan, A.; Santel, A.; Fuller, M.; Smith, C.L.; Youle, R.J. Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J. Cell Biol. 2002, 159, 931–938. [Google Scholar] [CrossRef]
- Vendrov, A.E.; Vendrov, K.C.; Smith, A.; Yuan, J.; Sumida, A.; Robidoux, J.; Runge, M.S.; Madamanchi, N.R. NOX4 NADPH oxidase-dependent mitochondrial oxidative stress in aging-associated cardiovascular disease. Antioxid. Redox Signal. 2015, 23, 1389–1409. [Google Scholar] [CrossRef]
- Twig, G.; Elorza, A.; Molina, A.J.; Mohamed, H.; Wikstrom, J.D.; Walzer, G.; Stiles, L.; Haigh, S.E.; Katz, S.; Las, G.; et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 2008, 27, 433–446. [Google Scholar] [CrossRef]
- Suárez-Rivero, J.M.; Villanueva-Paz, M.; de la Cruz-Ojeda, P.; de la Mata, M.; Cotán, D.; Oropesa-Ávila, M.; de Lavera, I.; Álvarez-Córdoba, M.; Luzón-Hidalgo, R.; Sánchez-Alcázar, J.A. Mitochondrial Dynamics in Mitochondrial Diseases. Diseases 2017, 5, 1. [Google Scholar] [CrossRef]
- Chouchani, E.T.; Pell, V.R.; James, A.M.; Work, L.M.; Saeb-Parsy, K.; Frezza, C.; Krieg, T.; Murphy, M.P. A Unifying Mechanism for Mitochondrial Superoxide Production during Ischemia-Reperfusion Injury. Cell Metab. 2016, 23, 254–263. [Google Scholar] [CrossRef]
- Kalogeris, T.; Bao, Y.; Korthuis, R.J. Mitochondrial reactive oxygen species: A double edged sword in ischemia/reperfusion vs preconditioning. Redox Biol. 2014, 2, 702–714. [Google Scholar] [CrossRef] [PubMed]
- Li, Q.; Zhang, T.; Wang, J.; Zhang, Z.; Zhai, Y.; Yang, G.-Y.; Sun, X. Rapamycin attenuates mitochondrial dysfunction via activation of mitophagy in experimental ischemic stroke. Biophys. Res. Commun. 2014, 444, 182–188. [Google Scholar] [CrossRef] [PubMed]
- Yu, P.; Zhang, J.; Yu, S.; Luo, Z.; Hua, F.; Yuan, L.; Zhou, Z.; Liu, Q.; Du, X.; Chen, S.; et al. Protective Effect of Sevoflurane Postconditioning against Cardiac Ischemia/Reperfusion Injury via Ameliorating Mitochondrial Impairment, Oxidative Stress and Rescuing Autophagic Clearance. PLoS ONE 2015, 10, e0134666. [Google Scholar] [CrossRef]
- Zhou, H.; Zhang, Y.; Hu, S.; Shi, C.; Zhu, P.; Ma, Q.; Jin, Q.; Cao, F.; Tian, F.; Chen, Y. Melatonin protects cardiac microvasculature against ischemia/reperfusion injury via suppression of mitochondrial fission-VDAC1-HK2-mPTP-mitophagy axis. J. Pineal Res. 2017, 63, e12413. [Google Scholar] [CrossRef] [PubMed]
- Hasan, P.; Saotome, M.; Ikoma, T.; Iguchi, K.; Kawasaki, H.; Iwashita, T.; Hayashi, H.; Maekawa, Y. Mitochondrial fission protein, dynamin-related protein 1, contributes to the promotion of hypertensive cardiac hypertrophy and fibrosis in Dahl-salt sensitive rats. J. Mol. Cell. Cardiol. 2018, 121, 103–106. [Google Scholar] [CrossRef] [PubMed]
- Pennanen, C.; Parra, V.; López-Crisosto, C.; Morales, P.E.; Del Campo, A.; Gutierrez, T.; Rivera-Mejías, P.; Kuzmicic, J.; Chiong, M.; Zorzano, A.; et al. Mitochondrial fission is required for cardiomyocyte hypertrophy mediated by a Ca2+-calcineurin signaling pathway. J. Cell Sci. 2014, 127, 2659–2671. [Google Scholar] [CrossRef]
- Rosca, M.G.; Hoppel, C.L. Mitochondrial dysfunction in heart failure. Heart Fail. Rev. 2013, 18, 607–622. [Google Scholar] [CrossRef]
- Okonko, D.O.; Shah, A.M. Mitochondrial dysfunction and oxidative stress in CHF. Nat. Rev. Cardiol. 2014, 12, 6. [Google Scholar] [CrossRef]
- Akhmedov, A.; Camici, G.G.; Lüscher, T.F.; Savarese, G. Molecular mechanism of endothelial and vascular aging: Implications for cardiovascular disease. Eur. Heart J. 2015, 36, 3392–3403. [Google Scholar]
- Sallam, N.; Laher, I. Exercise Modulates Oxidative Stress and Inflammation in Aging and Cardiovascular Diseases. Oxidative Med. Cell. Longev. 2016, 2016, 32. [Google Scholar] [CrossRef]
- Lakatta, E.G. Arterial and cardiac aging: Major shareholders in cardiovascular disease enterprises. Circulation 2003, 107, 490–497. [Google Scholar] [CrossRef] [PubMed]
- North, B.J.; Sinclair, D.A. The intersection between aging and cardiovascular disease. Circ. Res. 2012, 110, 1097–1108. [Google Scholar] [CrossRef] [PubMed]
- Cui, H.; Kong, Y.; Zhang, H. Oxidative stress, mitochondrial dysfunction, and aging. J. Signal Transduct. 2011, 2012, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Camici, G.G.; Liberale, L. Aging: The next cardiovascular disease? Eur. Heart J. 2017, 38, 1621–1623. [Google Scholar] [CrossRef]
- Sun, N.; Youle, R.J.; Finkel, T. The Mitochondrial Basis of Aging. Mol. Cell 2016, 61, 654–666. [Google Scholar] [CrossRef]
- Kauppila, T.E.S.; Kauppila, J.H.K.; Larsson, N.G. Mammalian Mitochondria and Aging: An Update. Cell Metab. 2017, 25, 57–71. [Google Scholar] [CrossRef]
- Kim, I.; Rodriguez-Enriquez, S.; Lemasters, J.J. Selective degradation of mitochondria by mitophagy. Arch. Biochem. Biophys. 2007, 462, 245–253. [Google Scholar] [CrossRef]
- Lopez-Lluch, G.; Irusta, P.M.; Navas, P.; de Cabo, R. Mitochondrial biogenesis and healthy aging. Exp. Gerontol. 2008, 43, 813–819. [Google Scholar] [CrossRef]
- Srivastava, S. The Mitochondrial Basis of Aging and Age-Related Disorders. Genes 2017, 8, 398. [Google Scholar] [CrossRef]
- Payne, B.A.; Chinnery, P.F. Mitochondrial dysfunction in aging: Much progress but many unresolved questions. Biochim. Biophys. Acta. 2015, 1847, 1347–1353. [Google Scholar] [CrossRef]
- Williams, S.L.; Huang, J.; Edwards, Y.J.; Ulloa, R.H.; Dillon, L.M.; Prolla, T.A.; Vance, J.M.; Moraes, C.T.; Züchner, S. The mtDNA mutation spectrum of the progeroid Polg mutator mouse includes abundant control region multimers. Cell Metab. 2010, 12, 675–682. [Google Scholar] [CrossRef] [PubMed]
- Sivitz, W.I.; Yorek, M.A. Mitochondrial dysfunction in diabetes: From molecular mechanisms to functional significance and therapeutic opportunities. Antioxid. Redox Signal. 2010, 12, 537–577. [Google Scholar] [CrossRef] [PubMed]
- Hsu, C.-C.; Tseng, L.-M.; Lee, H.-C. Role of mitochondrial dysfunction in cancer progression. Exp. Boil. Med. 2016, 241, 1281–1295. [Google Scholar] [CrossRef] [PubMed]
- Johri, A.; Beal, M.F. Mitochondrial dysfunction in neurodegenerative diseases. Biochim. Biophys. Acta 1998, 1366, 211–223. [Google Scholar] [CrossRef] [PubMed]
- Li, D.; Wang, P.; Luo, Y.; Zhao, M.; Chen, F. Health benefits of anthocyanins and molecular mechanisms: Update from recent decade. Crit. Rev. Food Sci. Nutr. 2017, 57, 1729–1741. [Google Scholar] [CrossRef] [PubMed]
- Skates, E.; Overall, J.; DeZego, K.; Wilson, M.; Esposito, D.; Lila, M.A.; Komarnytsky, S. Berries containing anthocyanins with enhanced methylation profiles are more effective at ameliorating high fat diet-induced metabolic damage. Food Chem. Toxicol. 2018, 111, 445–453. [Google Scholar] [CrossRef] [PubMed]
- Lagoa, R.; Graziani, I.; Lopez-Sanchez, C.; Garcia-Martinez, V.; Gutierrez-Merino, C. Complex I and cytochrome c are molecular targets of flavonoids that inhibit hydrogen peroxide production by mitochondria. Biochim. Biophys. Acta 2011, 1807, 1562–1572. [Google Scholar] [CrossRef]
- Silva, F.S.G.; Simoes, R.F.; Couto, R.; Oliveira, P.J. Targeting mitochondria in cardiovascular diseases. Curr. Pharm. Des. 2016, 22, 5698–5717. [Google Scholar] [CrossRef]
- Davidson, S.M.; Duchen, M.R. Endothelial mitochondria: Contributing to vascular function and disease. Circ. Res. 2007, 100, 1128–1141. [Google Scholar] [CrossRef]
- Borutaite, V.; Toleikis, A.; Brown, G.C. In the eye of the storm: Mitochondrial damage during heart and brain ischaemia. FEBS J. 2013, 280, 4999–5014. [Google Scholar] [CrossRef]
- Xie, X.; Zhao, R.; Shen, G.X. Impact of Cyanidin-3-Glucoside on Glycated LDL-Induced NADPH Oxidase Activation, Mitochondrial Dysfunction and Cell Viability in Cultured Vascular Endothelial Cells. Int. J. Mol. Sci. 2012, 13, 15867–15880. [Google Scholar] [CrossRef] [PubMed]
- Skemiene, K.; Liobikas, J.; Borutaite, V. Anthocyanins as substrates for mitochondrial complex I—Protective effect against heart ischemic injury. FEBS J. 2015, 282, 963–971. [Google Scholar] [CrossRef] [PubMed]
- Testai, L. Flavonoids and mitochondrial pharmacology: A new paradigm for cardioprotection. Life Sci. 2015, 135, 68–76. [Google Scholar] [CrossRef] [PubMed]
- Liobikas, J.; Skemiene, K.; Trumbeckaite, S.; Borutaite, V. Anthocyanins in cardioprotection: A path through mitochondria. Pharmacol. Res. 2016, 113, 808–815. [Google Scholar] [CrossRef] [PubMed]
- Boengler, K.; Hilfiker-Kleiner, D.; Heusch, G.; Schulz, R. Inhibition of permeability transition pore opening by mitochondrial STAT3 and its role in myocardial ischemia/reperfusion. Basic Res. Cardiol. 2010, 105, 771–785. [Google Scholar] [CrossRef] [PubMed]
- Mendez, D.L.; Akey, I.V.; Akey, C.W.; Kranz, R.G.; Akey, I.V. Oxidized or reduced cytochrome c and axial ligand variants all form the apoptosome in vitro. Biochemistry 2017, 56, 2766–2769. [Google Scholar] [CrossRef]
- Zaidi, S.; Hassan, M.I.; Islam, A.; Ahmad, F. The role of key residues in structure, function, and stability of cytochrome-c. Cell. Mol. Life Sci. 2014, 71, 229–255. [Google Scholar] [CrossRef]
- Skemiene, K.; Rakauskaite, G.; Trumbeckaite, S.; Liobikas, J.; Brown, G.C.; Borutaite, V. Anthocyanins block ischemia-induced apoptosis in the perfused heart and support mitochondrial respiration potentially by reducing cytosolic cytochrome c. Int. J. Biochem. Cell Boil. 2013, 45, 23–29. [Google Scholar] [CrossRef]
- Škėmienė, K.; Jablonskienė, G.; Liobikas, J.; Borutaitė, V. Protecting the heart against ischemia/reperfusion-induced necrosis and apoptosis: The effect of anthocyanins. Medicina 2013, 49, 15. [Google Scholar] [CrossRef]
- Esper, R.J.; Nordaby, R.A.; Vilariño, J.O.; Paragano, A.; Cacharrón, J.L.; Machado, R.A. Endothelial dysfunction: A comprehensive appraisal. Cardiovasc. Diabetol. 2006, 5, 4. [Google Scholar] [CrossRef]
- Jin, X.; Yi, L.; Chen, M.L.; Chen, C.Y.; Chang, H.; Zhang, T.; Wang, L.; Zhu, J.D.; Zhang, Q.Y.; Mi, M.T. Delphinidin-3-glucoside protects against oxidized low-density lipoprotein-induced mitochondrial dysfunction in vascular endothelial cells via the sodium-dependent glucose transporter SGLT1. PLoS ONE 2013, 8, e68617. [Google Scholar] [CrossRef] [PubMed]
- Xie, X.; Zhao, R.; Shen, G.X. Influence of Delphinidin-3-glucoside on Oxidized Low-Density Lipoprotein-Induced Oxidative Stress and Apoptosis in Cultured Endothelial Cells. J. Agric. Food Chem. 2012, 60, 1850–1856. [Google Scholar] [CrossRef] [PubMed]
- Fernandes, I.; Faria, A.; Calhau, C.; De Freitas, V.; Mateus, N. Bioavailability of anthocyanins and derivatives. J. Funct. Foods 2014, 7, 54–66. [Google Scholar] [CrossRef]
- Cassidy, A. Berry anthocyanin intake and cardiovascular health. Mol. Asp. Med. 2018, 61, 76–82. [Google Scholar] [CrossRef]
- Cassidy, A.; Minihane, A.-M. The role of metabolism [and the microbiome] in defining the clinical efficacy of dietary flavonoids1. Am. J. Clin. Nutr. 2016, 105, 10–22. [Google Scholar] [CrossRef]
- Cassidy, A.; Mukamal, K.J.; Liu, L.; Franz, M.; Eliassen, A.H.; Rimm, E.B. A high anthocyanin intake is associated with a reduced risk of myocardial infarction in young and middle-aged women. Circulation 2013, 127, 188–196. [Google Scholar] [CrossRef]
- Mink, P.J.; Scrafford, C.G.; Barraj, L.M.; Harnack, L.; Hong, C.-P.; Nettleton, J.A.; Jacobs, D.R. Flavonoid intake and cardiovascular disease mortality: A prospective study in postmenopausal women. Am. J. Clin. Nutr. 2007, 85, 895–909. [Google Scholar] [CrossRef]
- Wallace, T.C. Anthocyanins in Cardiovascular Disease1. Adv. Nutr. 2011, 2, 1–7. [Google Scholar] [CrossRef]
- Paixão, J.; Dinis, T.C.P.; Almeida, L.M. Dietary anthocyanins protect endothelial cells against peroxynitrite-induced mitochondrial apoptosis pathway and Bax nuclear translocation: An in vitro approach. Apoptosis 2011, 16, 976–989. [Google Scholar] [CrossRef]
- Paixão, J.; Dinis, T.C.; Almeida, L.M. Malvidin-3-glucoside protects endothelial cells up-regulating endothelial NO synthase and inhibiting peroxynitrite-induced NF-kB activation. Chem. Interact. 2012, 199, 192–200. [Google Scholar] [CrossRef]
- Thomson, R.H. Distribution of naturally occurring quinones. Pharm. World Sci. 1991, 13, 70–73. [Google Scholar] [CrossRef] [PubMed]
- Cape, J.L.; Bowman, M.K.; Kramer, D.M. Computation of the redox and protonation properties of quinones: Towards the prediction of redox cycling natural products. Phytochemistry 2006, 67, 1781–1788. [Google Scholar] [CrossRef] [PubMed]
- Zhu, B.-Q.; Zhou, H.-Z.; Teerlink, J.R.; Karliner, J.S. Pyrroloquinoline Quinone [PQQ] Decreases Myocardial Infarct Size and Improves Cardiac Function in Rat Models of Ischemia and Ischemia/Reperfusion. Cardiovasc. Drugs Ther. 2004, 18, 421–431. [Google Scholar] [CrossRef] [PubMed]
- Weng, X.C.; Gordon, M.H. Antioxidant activity of quinones extracted from tanshen [Salvia miltiorrhiza Bunge]. J. Agric. Food Chem. 1992, 40, 1331–1336. [Google Scholar] [CrossRef]
- Tao, R.; Karliner, J.S.; Simonis, U.; Zheng, J.; Zhang, J.; Honbo, N.; Alano, C.C. Pyrroloquinoline Quinone Preserves Mitochondrial Function and Prevents Oxidative Injury in Adult Rat Cardiac Myocytes. Biochem. Biophys. Res. Commun. 2007, 363, 257–262. [Google Scholar] [CrossRef][Green Version]
- Severina, I.I.; Severin, F.F.; Korshunova, G.A.; Sumbatyan, N.V.; Ilyasova, T.M.; Simonyan, R.A.; Rogov, A.G.; Trendeleva, T.A.; Zvyagilskaya, R.A.; Dugina, V.B.; et al. In search of novel highly active mitochondria-targeted antioxidants: Thymoquinone and its cationic derivatives. FEBS Lett. 2013, 587, 2018–2024. [Google Scholar] [CrossRef]
- Kumar, A.; Singh, R.; Saxena, M.; Niaz, M.; Joshi, S.; Chattopadhyay, P.; Mechirova, V.; Pella, D.; Fedacko, J. Effect of carni Q-gel [ubiquinol and carnitine] on cytokines in patients with heart failure in the Tishcon study. Acta Cardiol. 2007, 62, 349–354. [Google Scholar] [CrossRef]
- Zhu, B.-Q.; Simonis, U.; Cecchini, G.; Zhou, H.-Z.; Li, L.; Teerlink, J.R.; Karliner, J.S. Comparison of Pyrroloquinoline Quinone and/or Metoprolol on Myocardial Infarct Size and Mitochondrial Damage in a Rat Model of Ischemia/Reperfusion Injury. J. Cardiovasc. Pharmacol. Ther. 2006, 11, 119–128. [Google Scholar] [CrossRef]
- Schneider-Stock, R.; Fakhoury, I.H.; Zaki, A.M.; El-Baba, C.O.; Gali-Muhtasib, H.U. Thymoquinone: Fifty years of success in the battle against cancer models. Drug Discov. Today 2014, 19, 18–30. [Google Scholar] [CrossRef]
- Nagi, M.N.; Al-Shabanah, O.A.; Hafez, M.M.; Sayed-Ahmed, M.M. Thymoquinone supplementation attenuates cyclophosphamide-induced cardiotoxicity in rats. J. Biochem. Mol. Toxicol. 2011, 25, 135–142. [Google Scholar] [CrossRef]
- Kocak, C.; Kocak, F.E.; Akcilar, R.; Isiklar, O.O.; Kocak, H.; Bayat, Z.; Simsek, H.; Taser, F.; Altuntas, I.; Akcılar, R. Molecular and biochemical evidence on the protective effects of embelin and carnosic acid in isoproterenol-induced acute myocardial injury in rats. Life Sci. 2016, 147, 15–23. [Google Scholar] [CrossRef] [PubMed]
- Shabana, A.; El-Menyar, A.; Asim, M.; Al-Azzeh, H.; Al Thani, H. Cardiovascular benefits of black cumin [Nigella sativa]. Cardiovasc. Toxicol. 2013, 13, 9–21. [Google Scholar] [CrossRef] [PubMed]
- Berlin, J. Plant cell cultures—A future source of natural products? Endeavour 1984, 8, 5–8. [Google Scholar] [CrossRef]
- Kelso, G.F.; Porteous, C.M.; Coulter, C.V.; Hughes, G.; Porteous, W.K.; Ledgerwood, E.C.; Smith, R.A.; Murphy, M.P. Selective targeting of a redox-active ubiquinone to mitochondria within cells: Antioxidant and antiapoptotic properties. J. Biol. Chem. 2001, 276, 4588–4596. [Google Scholar] [CrossRef]
- Colucci, W.S. Molecular and Cellular Mechanisms of Myocardial Failure. Am. J. Cardiol. 1997, 80, 15L–25L. [Google Scholar] [CrossRef]
- Ferrara, N.; Abete, P.; Ambrosio, G.; Landino, P.; Caccese, P.; Cirillo, P.; Oradei, A.; Littarru, G.P.; Chiariello, M.; Rengo, F. Protective role of chronic ubiquinone administration on acute cardiac oxidative stress. J. Pharmacol. Exp. Ther. 1995, 274, 858–865. [Google Scholar]
- Kumar, A.; Kaur, H.; Devi, P.; Mohan, V. Role of coenzyme Q10 [CoQ10] in cardiac disease, hypertension and Meniere-like syndrome. Pharmacol. Ther. 2009, 124, 259–268. [Google Scholar] [CrossRef]
- ElBaky, N.A.A.; El-Orabi, N.F.; Fadda, L.M.; Abd-Elkader, O.H.; Ali, H.M. Role of N-Acetylcysteine and Coenzyme Q10 in the Amelioration of Myocardial Energy Expenditure and Oxidative Stress, Induced by Carbon Tetrachloride Intoxication in Rats. Dose-Response 2018, 16, 1559325818790158. [Google Scholar] [CrossRef]
- Flowers, N.; Hartley, L.; Todkill, D.; Stranges, S.; Rees, K. Co-enzyme Q10 supplementation for the primary prevention of cardiovascular disease. Cochrane Database Syst. Rev. 2014. [Google Scholar] [CrossRef]
- de Frutos, F.; Gea, A.; Hernandez-Estefania, R.; Rabago, G. Prophylactic treatment with coenzyme Q10 in patients undergoing cardiac surgery: Could an antioxidant reduce complications? A systematic review and meta-analysis. Interact. Cardiovasc. Thorac. Surg. 2015, 20, 254–259. [Google Scholar] [CrossRef]
- Alehagen, U.; Alexander, J.; Aaseth, J. Supplementation with Selenium and Coenzyme Q10 Reduces Cardiovascular Mortality in Elderly with Low Selenium Status. A Secondary Analysis of a Randomised Clinical Trial. PLoS ONE 2016, 11, e0157541. [Google Scholar] [CrossRef]
- Madmani, M.E.; Yusuf Solaiman, A.; Tamr Agha, K.; Madmani, Y.; Shahrour, Y.; Essali, A.; Kadro, W. Coenzyme Q10 for heart failure. Cochrane Database Syst. Rev. 2014. [Google Scholar] [CrossRef]
- Mortensen, S.A.; Rosenfeldt, F.; Kumar, A.; Dolliner, P.; Filipiak, K.J.; Pella, D.; Alehagen, U.; Steurer, G.; Littarru, G.P. The Effect of Coenzyme Q10 on Morbidity and Mortality in Chronic Heart Failure: Results From Q-SYMBIO: A Randomized Double-Blind Trial. JACC Heart Fail. 2014, 2, 641–649. [Google Scholar] [CrossRef]
- Sharma, S. Isothiocyanates in Heterocyclic Synthesis. Sulfur Rep. 1989, 8, 327–454. [Google Scholar] [CrossRef]
- Fahey, J.W.; Zalcmann, A.T.; Talalay, P. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 2001, 56, 5–51. [Google Scholar] [CrossRef]
- De Figueiredo, S.M.; Filho, S.A.V.; Nogueira-Machado, J.A.; Caligiorne, R.B. The anti-oxidant properties of isothiocyanates: A review. Recent Pat. Endocr. Metab. Immune Drug Discov. 2013, 7, 213–225. [Google Scholar] [CrossRef]
- Dinkova-Kostova, A.T.; Kostov, R.V. Glucosinolates and isothiocyanates in health and disease. Trends Mol. Med. 2012, 18, 337–347. [Google Scholar] [CrossRef]
- Smith, R.E.; Tran, K.; Smith, C.C.; McDonald, M.; Shejwalkar, P.; Hara, K. The Role of the Nrf2/ARE Antioxidant System in Preventing Cardiovascular Diseases. Diseases 2016, 4, 34. [Google Scholar] [CrossRef]
- Shokeir, A.A.; Barakat, N.; Hussein, A.M.; Awadalla, A.; Harraz, A.M.; Khater, S.; Hemmaid, K.; Kamal, A.I. Activation of Nrf2 by ischemic preconditioning and sulforaphane in renal ischemia/reperfusion injury: A comparative experimental study. Physiol. Res. 2015, 64, 313–323. [Google Scholar]
- Gillespie, S.; Holloway, P.M.; Becker, F.; Rauzi, F.; Vital, S.A.; Taylor, K.A.; Stokes, K.Y.; Emerson, M.; Gavins, F.N.E. The isothiocyanate sulforaphane modulates platelet function and protects against cerebral thrombotic dysfunction. Br. J. Pharmacol. 2018. [Google Scholar] [CrossRef]
- Armah, C.N.; Derdemezis, C.; Traka, M.H.; Dainty, J.R.; Doleman, J.F.; Saha, S.; Leung, W.; Potter, J.F.; Lovegrove, J.A.; Mithen, R.F. Diet rich in high glucoraphanin broccoli reduces plasma LDL cholesterol: Evidence from randomised controlled trials. Mol. Nutr. Food Res. 2015, 59, 918–926. [Google Scholar] [CrossRef]
- Mirmiran, P.; Bahadoran, Z.; Golzarand, M.; Zojaji, H.; Azizi, F. A comparative study of broccoli sprouts powder and standard triple therapy on cardiovascular risk factors following H.pylori eradication: A randomized clinical trial in patients with type 2 diabetes. J. Diabetes Metab. Disord. 2014, 13, 64. [Google Scholar] [CrossRef]
- Ma, T.; Zhu, D.; Chen, D.; Zhang, Q.; Dong, H.; Wu, W.; Lu, H.; Wu, G. Sulforaphane, a Natural Isothiocyanate Compound, Improves Cardiac Function and Remodeling by Inhibiting Oxidative Stress and Inflammation in a Rabbit Model of Chronic Heart Failure. Med Sci. Monit. 2018, 24, 1473–1483. [Google Scholar] [CrossRef]
- Galuppo, M.; Giacoppo, S.; Iori, R.; De Nicola, G.R.; Milardi, D.; Bramanti, P.; Mazzon, E. 4[alpha-L-rhamnosyloxy]-benzyl isothiocyanate, a bioactive phytochemical that defends cerebral tissue and prevents severe damage induced by focal ischemia/reperfusion. J. Biol. Regul. Homeost. Agents 2015, 29, 343–356. [Google Scholar]
- Ho, J.-N.; Yoon, H.-G.; Park, C.-S.; Kim, S.; Jun, W.; Choue, R.; Lee, J. Isothiocyanates Ameliorate the Symptom of Heart Dysfunction and Mortality in a Murine AIDS Model by Inhibiting Apoptosis in the Left Ventricle. J. Med. Food 2012, 15, 781–787. [Google Scholar] [CrossRef]
- Jang, Y.J.; Park, B.; Lee, H.-W.; Park, H.J.; Koo, H.J.; Kim, B.O.; Sohn, E.-H.; Um, S.H.; Pyo, S. Sinigrin attenuates the progression of atherosclerosis in ApoE −/− mice fed a high-cholesterol diet potentially by inhibiting VCAM-1 expression. Chem. Interact. 2017, 272, 28–36. [Google Scholar] [CrossRef]
- López-Otín, C.; Blasco, M.A.; Partridge, L.; Serrano, M.; Kroemer, G. The Hallmarks of Aging. Cell 2013, 153, 1194–1217. [Google Scholar] [CrossRef]
- Katsuumi, G.; Shimizu, I.; Yoshida, Y.; Minamino, T. Vascular Senescence in Cardiovascular and Metabolic Diseases. Front. Cardiovasc. Med. 2018, 5, 18. [Google Scholar] [CrossRef]
- Gallage, S.; Gil, J. Mitochondrial Dysfunction Meets Senescence. Trends Biochem. Sci. 2016, 41, 207–209. [Google Scholar] [CrossRef]
- Childs, B.G.; Li, H.; van Deursen, J.M. Senescent cells: A therapeutic target for cardiovascular disease. J. Clin. Investig. 2018, 128, 1217–1228. [Google Scholar] [CrossRef]
- Walaszczyk, A.; Dookun, E.; Redgrave, R.; Tual-Chalot, S.; Victorelli, S.; Spyridopoulos, I.; Owens, A.; Arthur, H.M.; Passos, J.F.; Richardson, G.D. Pharmacological clearance of senescent cells improves survival and recovery in aged mice following acute myocardial infarction. Aging Cell 2019, 18, e12945. [Google Scholar] [CrossRef] [PubMed]
- Shimizu, I.; Minamino, T. Cellular senescence in cardiac diseases. J. Cardiol. 2019. [Google Scholar] [CrossRef] [PubMed]
- Xu, M.; Pirtskhalava, T.; Farr, J.N.; Weigand, B.M.; Palmer, A.K.; Weivoda, M.M.; Inman, C.L.; Ogrodnik, M.B.; Hachfeld, C.M.; Fraser, D.G.; et al. Senolytics Improve Physical Function and Increase Lifespan in Old Age. Nat. Med. 2018, 24, 1246–1256. [Google Scholar] [CrossRef] [PubMed]
- Kirkland, J.L.; Tchkonia, T.; Zhu, Y.; Niedernhofer, L.J.; Robbins, P.D. The Clinical Potential of Senolytic Drugs. J. Am. Geriatr. Soc. 2017, 65, 2297–2301. [Google Scholar] [CrossRef]
- Li, W.; Qin, L.; Feng, R.; Hu, G.; Sun, H.; He, Y.; Zhang, R. Emerging senolytic agents derived from natural products. Mech. Ageing Dev. 2019, 181, 1–6. [Google Scholar] [CrossRef]
- Formica, J.; Regelson, W. Review of the biology of quercetin and related bioflavonoids. Food Chem. Toxicol. 1995, 33, 1061–1080. [Google Scholar] [CrossRef]
- Egert, S.; Bosy-Westphal, A.; Seiberl, J.; Kürbitz, C.; Settler, U.; Plachta-Danielzik, S.; Wagner, A.E.; Frank, J.; Schrezenmeir, J.; Rimbach, G.; et al. Quercetin reduces systolic blood pressure and plasma oxidised low-density lipoprotein concentrations in overweight subjects with a high-cardiovascular disease risk phenotype: A double-blinded, placebo-controlled cross-over study. Br. J. Nutr. 2009, 102, 1065–1074. [Google Scholar] [CrossRef]
- Rivera, L.; Morón, R.; Sanchez, M.; Zarzuelo, A.; Galisteo, M. Quercetin Ameliorates Metabolic Syndrome and Improves the Inflammatory Status in Obese Zucker Rats. Obesity 2008, 16, 2081–2087. [Google Scholar] [CrossRef]
- Erdman, J.W., Jr.; Balentine, D.; Arab, L.; Beecher, G.; Dwyer, J.T.; Folts, J.; Harnly, J.; Hollman, P.; Keen, C.L.; Mazza, G.; et al. Flavonoids and heart health: Proceedings of the ILSI North America flavonoids workshop, May 31–June 1, 2005, Washington, DC. J. Nutr. 2007, 137, 718S–737S. [Google Scholar] [CrossRef]
- De Oliveira, M.R.; Nabavi, S.M.; Braidy, N.; Setzer, W.N.; Ahmed, T.; Nabavi, S.F. Quercetin and the mitochondria: A mechanistic view. Biotechnol. Adv. 2016, 34, 532–549. [Google Scholar] [CrossRef]
- Hubbard, G.P.; Wolffram, S.; Lovegrove, J.A.; Gibbins, J.M. Ingestion of quercetin inhibits platelet aggregation and essential components of the collagen-stimulated platelet activation pathway in humans. J. Thromb. Haemost. 2004, 2, 2138–2145. [Google Scholar] [CrossRef]
- Sanchez, M.; Lodi, F.; Vera, R.; Villar, I.C.; Cogolludo, A.; Jimenez, R.; Moreno, L.; Romero, M.; Tamargo, J.; Perez-Vizcaino, F.; et al. Quercetin and isorhamnetin prevent endothelial dysfunction, superoxide production, and overexpression of p47phox induced by angiotensin II in rat aorta. J. Nutr. 2007, 137, 910–915. [Google Scholar] [CrossRef]
- Shen, Y.; Ward, N.C.; Hodgson, J.M.; Puddey, I.B.; Wang, Y.; Zhang, D.; Maghzal, G.J.; Stocker, R.; Croft, K.D. Dietary quercetin attenuates oxidant-induced endothelial dysfunction and atherosclerosis in apolipoprotein E knockout mice fed a high-fat diet: A critical role for heme oxygenase-1. Free Radic. Boil. Med. 2013, 65, 908–915. [Google Scholar] [CrossRef]
- Edwards, R.L.; Lyon, T.; Litwin, S.E.; Rabovsky, A.; Symons, J.D.; Jalili, T. Quercetin reduces blood pressure in hypertensive subjects. J. Nutr. 2007, 137, 2405–2411. [Google Scholar] [CrossRef]
- Jing, Z.; Wang, Z.; Li, X.; Li, X.; Cao, T.; Bi, Y.; Zhou, J.; Chen, X.; Yu, D.; Zhu, L.; et al. Protective Effect of Quercetin on Posttraumatic Cardiac Injury. Sci. Rep. 2016, 6, 30812. [Google Scholar] [CrossRef]
- Chen, Y.-W.; Chou, H.-C.; Lin, S.-T.; Chen, Y.-H.; Chang, Y.-J.; Chen, L.; Chan, H.-L. Cardioprotective Effects of Quercetin in Cardiomyocyte under Ischemia/Reperfusion Injury. Evid. -Based Complement. Altern. Med. 2013, 2013, 1–16. [Google Scholar] [CrossRef]
- Khan, N.; Syed, D.N.; Ahmad, N.; Mukhtar, H. Fisetin: A Dietary Antioxidant for Health Promotion. Antioxid. Redox Signal. 2012, 19, 151–162. [Google Scholar] [CrossRef]
- Dolan, K.; Wirtz, A.L.; Moazen, B.; Ndeffo-Mbah, M.; Galvani, A.; Kinner, S.A.; Courtney, R.; McKee, M.; Amon, J.J.; Maher, L.; et al. Global burden of HIV, viral hepatitis, and tuberculosis in prisoners and detainees. Lancet 2016, 388, 1089–1102. [Google Scholar] [CrossRef]
- Sun, X.; Ma, X.; Li, Q.; Yang, Y.; Xu, X.; Sun, J.; Yu, M.; Cao, K.; Yang, L.; Yang, G.; et al. Anti‑cancer effects of fisetin on mammary carcinoma cells via regulation of the PI3K/Akt/mTOR pathway: In Vitro and in vivo studies. Int. J. Mol. Med. 2018, 42, 811–820. [Google Scholar] [CrossRef]
- Pal, H.C.; Pearlman, R.L.; Afaq, F. Fisetin and Its Role in Chronic Diseases. Adv. Exp. Med. Biol. 2016, 928, 213–244. [Google Scholar]
- Yousefzadeh, M.J.; Zhu, Y.; McGowan, S.J.; Angelini, L.; Fuhrmann-Stroissnigg, H.; Xu, M.; Ling, Y.Y.; Melos, K.I.; Pirtskhalava, T.; Inman, C.L.; et al. Fisetin is a senotherapeutic that extends health and lifespan. EBioMedicine 2018, 36, 18–28. [Google Scholar] [CrossRef]
- Kwak, S.; Ku, S.-K.; Bae, J.-S. Fisetin inhibits high-glucose-induced vascular inflammation in vitro and in vivo. Inflamm. Res. 2014, 63, 779–787. [Google Scholar] [CrossRef]
- Lee, S.E.; Jeong, S.I.; Yang, H.; Park, Y.S.; Park, C.-S.; Jin, Y.-H.; Park, C.; Jin, Y. Fisetin induces Nrf2-mediated HO-1 expression through PKC-δ and p38 in human umbilical vein endothelial cells. J. Cell. Biochem. 2011, 112, 2352–2360. [Google Scholar] [CrossRef]
- Shanmugam, K.; Ravindran, S.; Kurian, G.A.; Rajesh, M. Fisetin Confers Cardioprotection against Myocardial Ischemia Reperfusion Injury by Suppressing Mitochondrial Oxidative Stress and Mitochondrial Dysfunction and Inhibiting Glycogen Synthase Kinase 3β Activity. Oxidative Med. Cell. Longev. 2018, 2018, 1–16. [Google Scholar] [CrossRef]
- Juhaszova, M.; Zorov, D.B.; Yaniv, Y.; Nuss, H.B.; Wang, S.; Sollott, S.J. Role of glycogen synthase kinase-3beta in cardioprotection. Circ. Res. 2009, 104, 1240–1252. [Google Scholar] [CrossRef]
- Chatterjee, A.; Dutta, C.P. Alkaloids of Piper longum Linn. I. Structure and synthesis of piperlongumine and piperlonguminine. Tetrahedron 1967, 23, 1769–1781. [Google Scholar] [CrossRef]
- Iwashita, M.; Oka, N.; Ohkubo, S.; Saito, M.; Nakahata, N. Piperlongumine, a constituent of Piper longum L.; inhibits rabbit platelet aggregation as a thromboxane A[2] receptor antagonist. Eur. J. Pharmacol. 2007, 570, 38–42. [Google Scholar] [CrossRef]
- Yuan, H.; Houck, K.L.; Tian, Y.; Bharadwaj, U.; Hull, K.; Zhou, Z.; Zhou, M.; Wu, X.; Tweardy, D.J.; Romo, D.; et al. Piperlongumine Blocks JAK2-STAT3 to Inhibit Collagen-Induced Platelet Reactivity Independent of Reactive Oxygen Species†. PLoS ONE 2015, 10, e0143964. [Google Scholar] [CrossRef]
- Zhou, Z.; Gushiken, F.C.; Bolgiano, D.; Salsbery, B.J.; Aghakasiri, N.; Jing, N.; Wu, X.; Vijayan, K.V.; Rumbaut, R.E.; Adachi, R.; et al. Signal transducer and activator of transcription 3 [STAT3] regulates collagen-induced platelet aggregation independently of its transcription factor activity. Circulation 2013, 127, 476–485. [Google Scholar] [CrossRef]
- Son, D.J.; Kim, S.Y.; Han, S.S.; Kim, C.W.; Kumar, S.; Park, B.S.; Lee, S.E.; Yun, Y.P.; Jo, H.; Park, Y.H. Piperlongumine inhibits atherosclerotic plaque formation and vascular smooth muscle cell proliferation by suppressing PDGF receptor signaling. Biophys. Res. Commun. 2012, 427, 349–354. [Google Scholar] [CrossRef]
- Bezerra, D.P.; Pessoa, C.; de Moraes, M.O.; Saker-Neto, N.; Silveira, E.R.; Costa-Lotufo, L.V. Overview of the therapeutic potential of piplartine [piperlongumine]. Eur. J. Pharm. Sci. 2013, 48, 453–463. [Google Scholar] [CrossRef] [PubMed]
- Salabei, J.K.; Hill, B.G. Mitochondrial fission induced by platelet-derived growth factor regulates vascular smooth muscle cell bioenergetics and cell proliferation. Redox Biol. 2013, 1, 542–551. [Google Scholar] [CrossRef] [PubMed]
Pathology/Model | Compound | Effect | Reference |
---|---|---|---|
Hearth ischemia | Delphinidin-3-glucoside and Cyanidin-3-glucoside | Reduction of cytosolic cyt c directly and rapidly | [109] |
Pre-perfusion of hearts | Cyanidin-3-glucoside | Prevention of ischemia-induced caspase activation | [109] |
Pre-perfusion of hearts | Delphinidin-3-glucoside and Cyanidin-3-glucoside | Support of mitochondrial state 4 respiration even in the presence of exogenous cyt c | [109] |
Ischemia and other diseases involving mitochondrial complex I dysfunction | Delfinidin-3-glucósido (Dp3G) y la cianidina-3-glucósido (Cy3G) | Action as electron acceptors in complex I-mediated oxidation of NADH | [103] |
Endothelial dysfunction | Cyanidin- delphinidin- and pelargonidin-3-glucoside | Inhibition of several crucial signaling cascades, upstream and downstream of mitochondria. | [120] |
Endothelial dysfunction | Malvidin-3-glucoside | NO balance and in inhibition of pro-inflammatory signaling pathways | [121] |
Pathology/Model | Compound | Effect | Reference |
---|---|---|---|
Cardiac failure | Pyrroloquinoline quinone | Antioxidant activity in cardiac myocytes through its action as a free radical scavenger | [126] |
Cardiac failure | Thymoquinone | Reduction of oxidative stress and improvement of mitochondrial function through increasing ATP production in cardiac myocytes | [131] |
Cardiac failure | Ubiquinone | Increase of the transport of electrons from organic substrates to oxygen in the respiratory chain of mitochondria | [138] |
Pathology | Compound | Effect | Reference |
---|---|---|---|
Renal ischemia/reperfusion | Sulforaphane | Enhancement of the expression of Nrf2, HO-1, and NQO-1, attenuation of the expression of inflammatory and apoptotic markers | [150] |
Photo-induced thrombosis model | Sulforaphane | Reduction of LPS-mediated enhancement of thrombus formation in the cerebral microcirculation | [151] |
Cerebral ischemia/reperfusion | Glucomoringin-isothiocyanate | Reduction of TNF-alpha release, NFκBp65 nuclear translocation, markers of inflammation and oxidative stress | [155] |
Murine AIDS model with heart dysfunction | Sulforaphane | Inhibition of apoptosis by increasing the Bcl-2/Bax ratio; Suppression of the expression of inducible nitric oxide synthase and inactivation of the cytoplasmic nuclear factor κB | [156] |
Murine AIDS model with heart dysfunction | Benzyl Isothiocyanate | Inhibition of apoptosis by increasing the Bcl-2/Bax ratio | [156] |
Murine AIDS model with heart dysfunction | Phenethylisothiocyante | Inhibition of apoptosis by increasing the Bcl-2/Bax ratio; Suppression of the expression of inducible nitric oxide synthase and inactivation of cytoplasmic nuclear factor κB | [156] |
Atherogenic murine model ApoE knockout | Sinigrin | Reduction in serum concentrations of LDH, TC, LDL, and pro-inflammatory cytokines. Attenuated mRNA expression of adhesion molecules [VCAM-1 and others] and chemokines | [157] |
Pathology/Model | Compound | Effect | Reference |
---|---|---|---|
Endothelial dysfunction model of thoracic aortae cell from male Wistar rats | Quercetin | Prevention of overexpression of the p47phox subunit of NOX. A decrease in O2- production. Increase of bioavailability of NO | [173] |
Posttraumatic cardiac dysfunction in H9c2 cells | Quercetin | Suppression of TNF-α increase of ROS overproduction and Ca2+ overload in cardiomyocytes | [176] |
Ischemic/reperfusion model in H9C2 cells | Quercetin | Reduction of activity and activation of Src kinase, STAT3, caspase 9 and Bax. Decrease of intracellular ROS production, and expression of inducible MnSOD. | [177]. |
HUVECS endothelial cells in a hyperglycemic model | Fisetin | Induction of apoptosis in senescent cells without affecting cell proliferation. | [183] |
HUVECS cells | Fisetin | Increase in the transcription activity of Nfr2, mainly HO-1 expression. | [184] |
Myocardial ischemia-reperfusion injury [Langendorff isolated heart perfusion system] | Fisetin | Decrease of mitochondrial oxidative stress and mitochondrial dysfunction mediated by inhibition of glycogen synthase kinase 3β | [185] |
Human platelets from healthy donors | Piperlongumine | Inhibition of collagen-induced platelet aggregation, calcium influx, CD62p expression, microparticles formation, and thrombus formation. | [189] |
In vivo murine model of accelerated atherosclerosis | Piperlongumine | Reduction of atherosclerotic plaque formation, the proliferation of endothelial cells and induction of NF-κB activation, mediated by platelet-derived growth factor BB [PDGF-BB]- inhibiton. | [191]. |
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Arauna, D.; Furrianca, M.; Espinosa-Parrilla, Y.; Fuentes, E.; Alarcón, M.; Palomo, I. Natural Bioactive Compounds As Protectors Of Mitochondrial Dysfunction In Cardiovascular Diseases And Aging. Molecules 2019, 24, 4259. https://doi.org/10.3390/molecules24234259
Arauna D, Furrianca M, Espinosa-Parrilla Y, Fuentes E, Alarcón M, Palomo I. Natural Bioactive Compounds As Protectors Of Mitochondrial Dysfunction In Cardiovascular Diseases And Aging. Molecules. 2019; 24(23):4259. https://doi.org/10.3390/molecules24234259
Chicago/Turabian StyleArauna, Diego, María Furrianca, Yolanda Espinosa-Parrilla, Eduardo Fuentes, Marcelo Alarcón, and Iván Palomo. 2019. "Natural Bioactive Compounds As Protectors Of Mitochondrial Dysfunction In Cardiovascular Diseases And Aging" Molecules 24, no. 23: 4259. https://doi.org/10.3390/molecules24234259
APA StyleArauna, D., Furrianca, M., Espinosa-Parrilla, Y., Fuentes, E., Alarcón, M., & Palomo, I. (2019). Natural Bioactive Compounds As Protectors Of Mitochondrial Dysfunction In Cardiovascular Diseases And Aging. Molecules, 24(23), 4259. https://doi.org/10.3390/molecules24234259