Angiogenesis, Inflammation & Therapeutics | Online ISSN  2207-872X
REVIEWS   (Open Access)

Mitochondria in Endothelial Dysfunction and The Relation to Cardiovascular Disease

Anastasia V Poznyak 1*, Victoria A. Khotina 2, Vasily N Sukhorukov 2, Igor A. Sobenin 2, Mikhail A. Popov 2, Anton Y. Postnov 2, and Alexander N. Orekhov 2,*

+ Author Affiliations

Journal of Angiotherapy 8(5) 1-13 https://doi.org/10.25163/angiotherapy.859557

Submitted: 05 March 2024  Revised: 01 May 2024  Published: 03 May 2024 

Abstract

Atherosclerosis is spreading more and more every year. Accordingly, more and more people suffer from this disease, especially its negative consequences. The pathogenesis of atherosclerosis involves many different mechanisms and processes. One of the players in this field is endothelial dysfunction, which captures the cells of the endothelial layer of blood vessels. Vascular dysfunction is a well-known risk factor for cardiovascular disease. Abnormalities include increased arterial stiffness as well as endothelial dysfunction associated with an atherogenic decrease in the expression and bioavailability of nitric oxide (NO). This article focuses on the evidence supporting the role of mitochondria in the maintenance of vascular function and the pathophysiology of mitochondrial-related vascular disorders. In addition, to identify possible gaps in current knowledge and find potential promising interventions, we will discuss lifestyle and nutraceutical strategies, as well as pharmaceutical treatments that improve vascular function through effects on mitochondria.

Keywords: Mitochondria, Endothelial dysfunction, Cardiovascular diseases, Mitochondrial dynamics, Therapeutic interventions

References

Alevriadou, B. R., Shanmughapriya, S., Patel, A., Stathopulos, P. B., & Madesh, M. (2017). Mitochondrial Ca2+ transport in the endothelium: regulation by ions, redox signalling and mechanical forces. Journal of the Royal Society, Interface, 14(137), 20170672. https://doi.org/10.1098/rsif.2017.0672

Arora, A., Singh, S., Bhatt, A. N., Pandey, S., Sandhir, R., & Dwarakanath, B. S. (2015). Interplay Between Metabolism and Oncogenic Process: Role of microRNAs. Translational oncogenomics, 7, 11–27. https://doi.org/10.4137/TOG.S29652

Baechler, B. L., Bloemberg, D., & Quadrilatero, J. (2019). Mitophagy regulates mitochondrial network signaling, oxidative stress, and apoptosis during myoblast differentiation. Autophagy, 15(9), 1606–1619. https://doi.org/10.1080/15548627.2019.1591672

Beckhauser, T. F., Francis-Oliveira, J., & De Pasquale, R. (2016). Reactive Oxygen Species: Physiological and Physiopathological Effects on Synaptic Plasticity. Journal of experimental neuroscience, 10(Suppl 1), 23–48. https://doi.org/10.4137/JEN.S39887

Boengler, K., Kosiol, M., Mayr, M., Schulz, R., & Rohrbach, S. (2017). Mitochondria and ageing: role in heart, skeletal muscle and adipose tissue. Journal of cachexia, sarcopenia and muscle, 8(3), 349–369. https://doi.org/10.1002/jcsm.12178

Boyman, L., Karbowski, M., & Lederer, W. J. (2020). Regulation of Mitochondrial ATP Production: Ca2+Signaling and Quality Control. Trends in molecular medicine, 26(1), 21–39. https://doi.org/10.1016/j.molmed.2019.10.007

Boyman, L., Karbowski, M., & Lederer, W. J. (2020). Regulation of Mitochondrial ATP Production: Ca2+Signaling and Quality Control. Trends in molecular medicine, 26(1), 21–39. https://doi.org/10.1016/j.molmed.2019.10.007

Byun, K., & Lee, S. (2020). The Potential Role of Irisin in Vascular Function and Atherosclerosis: A Review. International journal of molecular sciences, 21(19), 7184. https://doi.org/10.3390/ijms21197184

Carresi, C., Mollace, R., Macrì, R., Scicchitano, M., Bosco, F., Scarano, F., Coppoletta, A. R., Guarnieri, L., Ruga, S., Zito, M. C., Nucera, S., Gliozzi, M., Musolino, V., Maiuolo, J., Palma, E., & Mollace, V. (2021). Oxidative Stress Triggers Defective Autophagy in Endothelial Cells: Role in Atherothrombosis Development. Antioxidants (Basel, Switzerland), 10(3), 387. https://doi.org/10.3390/antiox10030387

Chan, S. Y., & Loscalzo, J. (2010). MicroRNA-210: a unique and pleiotropic hypoxamir. Cell cycle (Georgetown, Tex.), 9(6), 1072–1083. https://doi.org/10.4161/cc.9.6.11006

Chen, W., Yang, J., Chen, S., Xiang, H., Liu, H., Lin, D., Zhao, S., Peng, H., Chen, P., Chen, A. F., & Lu, H. (2017). Importance of mitochondrial calcium uniporter in high glucose-induced endothelial cell dysfunction. Diabetes & vascular disease research, 14(6), 494–501. https://doi.org/10.1177/1479164117723270

Chowdhury, Nafees Uddin; Tisha, Abida; Sarker, Juthika; Nath, Pulak Dev; Ahmed, Nowshin; Abdullah, Shahanshah; Farooq, Tasdik; Mahmud, Waich; Mohib, Md. Mohabbulla; Sagor, Md. Abu Taher. (2018).Targeting inducible Nitric Oxide Synthase (iNOS) in the prevention of vascular damage and cardiac inflammation in CVD. Angiotherapy, 1(2), pages 067–077.

Csiszar, A., Labinskyy, N., Pinto, J. T., Ballabh, P., Zhang, H., Losonczy, G., Pearson, K., de Cabo, R., Pacher, P., Zhang, C., & Ungvari, Z. (2009). Resveratrol induces mitochondrial biogenesis in endothelial cells. American journal of physiology. Heart and circulatory physiology, 297(1), H13–H20. https://doi.org/10.1152/ajpheart.00368.2009

Cvetkovska, M., Alber, N. A., & Vanlerberghe, G. C. (2013). The signaling role of a mitochondrial superoxide burst during stress. Plant signaling & behavior, 8(1), e22749. https://doi.org/10.4161/psb.22749

Dada, L. A., & Sznajder, J. I. (2011). Mitochondrial Ca²+ and ROS take center stage to orchestrate TNF-α-mediated inflammatory responses. The Journal of clinical investigation, 121(5), 1683–1685. https://doi.org/10.1172/JCI57748

Dalal, P. J., Muller, W. A., & Sullivan, D. P. (2020). Endothelial Cell Calcium Signaling during Barrier Function and Inflammation. The American journal of pathology, 190(3), 535–542. https://doi.org/10.1016/j.ajpath.2019.11.004

Das, G., Shravage, B. V., & Baehrecke, E. H. (2012). Regulation and function of autophagy during cell survival and cell death. Cold Spring Harbor perspectives in biology, 4(6), a008813. https://doi.org/10.1101/cshperspect.a008813

Delierneux, C., Kouba, S., Shanmughapriya, S., Potier-Cartereau, M., Trebak, M., & Hempel, N. (2020). Mitochondrial Calcium Regulation of Redox Signaling in Cancer. Cells, 9(2), 432. https://doi.org/10.3390/cells9020432

Doblado, L., Lueck, C., Rey, C., Samhan-Arias, A. K., Prieto, I., Stacchiotti, A., & Monsalve, M. (2021). Mitophagy in Human Diseases. International journal of molecular sciences, 22(8), 3903. https://doi.org/10.3390/ijms22083903

Doll, D. N., Hu, H., Sun, J., Lewis, S. E., Simpkins, J. W., & Ren, X. (2015). Mitochondrial crisis in cerebrovascular endothelial cells opens the blood-brain barrier. Stroke, 46(6), 1681–1689. https://doi.org/10.1161/STROKEAHA.115.009099

Donato, A. J., Machin, D. R., & Lesniewski, L. A. (2018). Mechanisms of Dysfunction in the Aging Vasculature and Role in Age-Related Disease. Circulation research, 123(7), 825–848. https://doi.org/10.1161/CIRCRESAHA.118.312563

Fernández, Á. F., Sebti, S., Wei, Y., Zou, Z., Shi, M., McMillan, K. L., He, C., Ting, T., Liu, Y., Chiang, W. C., Marciano, D. K., Schiattarella, G. G., Bhagat, G., Moe, O. W., Hu, M. C., & Levine, B. (2018). Disruption of the beclin 1-BCL2 autophagy regulatory complex promotes longevity in mice. Nature, 558(7708), 136–140. https://doi.org/10.1038/s41586-018-0162-7

Filippini, A., D'Amore, A., & D'Alessio, A. (2019). Calcium Mobilization in Endothelial Cell Functions. International journal of molecular sciences, 20(18), 4525. https://doi.org/10.3390/ijms20184525

Gal, R., Deres, L., Toth, K., Halmosi, R., & Habon, T. (2021). The Effect of Resveratrol on the Cardiovascular System from Molecular Mechanisms to Clinical Results. International journal of molecular sciences, 22(18), 10152. https://doi.org/10.3390/ijms221810152

Gatica, D., Chiong, M., Lavandero, S., & Klionsky, D. J. (2015). Molecular mechanisms of autophagy in the cardiovascular system. Circulation research, 116(3), 456–467. https://doi.org/10.1161/CIRCRESAHA.114.303788

Gatica, D., Chiong, M., Lavandero, S., & Klionsky, D. J. (2022). The role of autophagy in cardiovascular pathology. Cardiovascular research, 118(4), 934–950. https://doi.org/10.1093/cvr/cvab158

Germande, O., Baudrimont, M., Beaufils, F., Freund-Michel, V., Ducret, T., Quignard, J. F., Errera, M. H., Lacomme, S., Gontier, E., Mornet, S., Bejko, M., Muller, B., Marthan, R., Guibert, C., Deweirdt, J., & Baudrimont, I. (2022). NiONPs-induced alteration in calcium signaling and mitochondrial function in pulmonary artery endothelial cells involves oxidative stress and TRPV4 channels disruption. Nanotoxicology, 16(1), 29–51. https://doi.org/10.1080/17435390.2022.2030821

Gutiérrez, E., Flammer, A. J., Lerman, L. O., Elízaga, J., Lerman, A., & Fernández-Avilés, F. (2013). Endothelial dysfunction over the course of coronary artery disease. European heart journal, 34(41), 3175–3181. https://doi.org/10.1093/eurheartj/eht351

Hall, J. E., do Carmo, J. M., da Silva, A. A., Wang, Z., & Hall, M. E. (2019). Obesity, kidney dysfunction and hypertension: mechanistic links. Nature reviews. Nephrology, 15(6), 367–385. https://doi.org/10.1038/s41581-019-0145-4

Hanna, R. A., Quinsay, M. N., Orogo, A. M., Giang, K., Rikka, S., & Gustafsson, Å. B. (2012). Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 protein to selectively remove endoplasmic reticulum and mitochondria via autophagy. The Journal of biological chemistry, 287(23), 19094–19104. https://doi.org/10.1074/jbc.M111.322933

Hass, D. T., & Barnstable, C. J. (2021). Uncoupling proteins in the mitochondrial defense against oxidative stress. Progress in retinal and eye research, 83, 100941. https://doi.org/10.1016/j.preteyeres.2021.100941

He, X., Zeng, H., & Chen, J. X. (2019). Emerging role of SIRT3 in endothelial metabolism, angiogenesis, and cardiovascular disease. Journal of cellular physiology, 234(3), 2252–2265. https://doi.org/10.1002/jcp.27200

Herb, M., & Schramm, M. (2021). Functions of ROS in Macrophages and Antimicrobial Immunity. Antioxidants (Basel, Switzerland), 10(2), 313. https://doi.org/10.3390/antiox10020313

Hu, Y., Zhou, Y., Yang, Y., Tang, H., Si, Y., Chen, Z., Shi, Y., & Fang, H. (2022). Metformin Protects Against Diabetes-Induced Cognitive Dysfunction by Inhibiting Mitochondrial Fission Protein DRP1. Frontiers in pharmacology, 13, 832707. https://doi.org/10.3389/fphar.2022.832707

Jiang, Q., Yin, J., Chen, J., Ma, X., Wu, M., Liu, G., Yao, K., Tan, B., & Yin, Y. (2020). Mitochondria-Targeted Antioxidants: A Step towards Disease Treatment. Oxidative medicine and cellular longevity, 2020, 8837893. https://doi.org/10.1155/2020/8837893

Jin, J. Y., Wei, X. X., Zhi, X. L., Wang, X. H., & Meng, D. (2021). Drp1-dependent mitochondrial fission in cardiovascular disease. Acta pharmacologica Sinica, 42(5), 655–664. https://doi.org/10.1038/s41401-020-00518-y

Kim, D., Sankaramoorthy, A., & Roy, S. (2020). Downregulation of Drp1 and Fis1 Inhibits Mitochondrial Fission and Prevents High Glucose-Induced Apoptosis in Retinal Endothelial Cells. Cells, 9(7), 1662. https://doi.org/10.3390/cells9071662

Kim, I., Rodriguez-Enriquez, S., & Lemasters, J. J. (2007). Selective degradation of mitochondria by mitophagy. Archives of biochemistry and biophysics, 462(2), 245–253. https://doi.org/10.1016/j.abb.2007.03.034

Kirkman, D. L., Robinson, A. T., Rossman, M. J., Seals, D. R., & Edwards, D. G. (2021). Mitochondrial contributions to vascular endothelial dysfunction, arterial stiffness, and cardiovascular diseases. American journal of physiology. Heart and circulatory physiology, 320(5), H2080–H2100. https://doi.org/10.1152/ajpheart.00917.2020

Kluge, M. A., Fetterman, J. L., & Vita, J. A. (2013). Mitochondria and endothelial function. Circulation research, 112(8), 1171–1188. https://doi.org/10.1161/CIRCRESAHA.111.300233

Kluge, M. A., Fetterman, J. L., & Vita, J. A. (2013). Mitochondria and endothelial function. Circulation research, 112(8), 1171–1188. https://doi.org/10.1161/CIRCRESAHA.111.300233

Kumar, V., & Jurkunas, U. V. (2021). Mitochondrial Dysfunction and Mitophagy in Fuchs Endothelial Corneal Dystrophy. Cells, 10(8), 1888. https://doi.org/10.3390/cells10081888

Kupis, W., Palyga, J., Tomal, E., & Niewiadomska, E. (2016). The role of sirtuins in cellular homeostasis. Journal of physiology and biochemistry, 72(3), 371–380. https://doi.org/10.1007/s13105-016-0492-6

Liu, L., Li, Y., Wang, J., Zhang, D., Wu, H., Li, W., Wei, H., Ta, N., Fan, Y., Liu, Y., Wang, X., Wang, J., Pan, X., Liao, X., Zhu, Y., & Chen, Q. (2021). Mitophagy receptor FUNDC1 is regulated by PGC-1α/NRF1 to fine tune mitochondrial homeostasis. EMBO reports, 22(3), e50629. https://doi.org/10.15252/embr.202050629

Man, A., Li, H., & Xia, N. (2019). The Role of Sirtuin1 in Regulating Endothelial Function, Arterial Remodeling and Vascular Aging. Frontiers in physiology, 10, 1173. https://doi.org/10.3389/fphys.2019.01173

Martino, E., Balestrieri, A., Anastasio, C., Maione, M., Mele, L., Cautela, D., Campanile, G., Balestrieri, M. L., & D'Onofrio, N. (2022). SIRT3 Modulates Endothelial Mitochondrial Redox State during Insulin Resistance. Antioxidants (Basel, Switzerland), 11(8), 1611. https://doi.org/10.3390/antiox11081611

McLachlan, J., Beattie, E., Murphy, M. P., Koh-Tan, C. H., Olson, E., Beattie, W., Dominiczak, A. F., Nicklin, S. A., & Graham, D. (2014). Combined therapeutic benefit of mitochondria-targeted antioxidant, MitoQ10, and angiotensin receptor blocker, losartan, on cardiovascular function. Journal of hypertension, 32(3), 555–564. https://doi.org/10.1097/HJH.0000000000000054

McMackin, C. J., Widlansky, M. E., Hamburg, N. M., Huang, A. L., Weller, S., Holbrook, M., Gokce, N., Hagen, T. M., Keaney, J. F., Jr, & Vita, J. A. (2007). Effect of combined treatment with alpha-Lipoic acid and acetyl-L-carnitine on vascular function and blood pressure in patients with coronary artery disease. Journal of clinical hypertension (Greenwich, Conn.), 9(4), 249–255. https://doi.org/10.1111/j.1524-6175.2007.06052.x

Md. Fakruddin, Md. Asaduzzaman Shishir, Kumkum Rahman Mouree, Shamsuddin Sultan Khan. (2020). Environmental and physiological angiogenesis in causing CVD with oxidative pattern, Journal of angiotherpay, 6(2), 2129.

Mensah, G. A., Wei, G. S., Sorlie, P. D., Fine, L. J., Rosenberg, Y., Kaufmann, P. G., Mussolino, M. E., Hsu, L. L., Addou, E., Engelgau, M. M., & Gordon, D. (2017). Decline in Cardiovascular Mortality: Possible Causes and Implications. Circulation research, 120(2), 366–380. https://doi.org/10.1161/CIRCRESAHA.116.309115

Mongirdiene, A., Skrodenis, L., Varoneckaite, L., Mierkyte, G., & Gerulis, J. (2022). Reactive Oxygen Species Induced Pathways in Heart Failure Pathogenesis and Potential Therapeutic Strategies. Biomedicines, 10(3), 602. https://doi.org/10.3390/biomedicines10030602

Morciano, G., Marchi, S., Morganti, C., Sbano, L., Bittremieux, M., Kerkhofs, M., Corricelli, M., Danese, A., Karkucinska-Wieckowska, A., Wieckowski, M. R., Bultynck, G., Giorgi, C., & Pinton, P. (2018). Role of Mitochondria-Associated ER Membranes in Calcium Regulation in Cancer-Specific Settings. Neoplasia (New York, N.Y.), 20(5), 510–523. https://doi.org/10.1016/j.neo.2018.03.005

Münzel, T., Camici, G. G., Maack, C., Bonetti, N. R., Fuster, V., & Kovacic, J. C. (2017). Impact of Oxidative Stress on the Heart and Vasculature: Part 2 of a 3-Part Series. Journal of the American College of Cardiology, 70(2), 212–229. https://doi.org/10.1016/j.jacc.2017.05.035

Negri, S., Faris, P., & Moccia, F. (2021). Reactive Oxygen Species and Endothelial Ca2+ Signaling: Brothers in Arms or Partners in Crime?. International journal of molecular sciences, 22(18), 9821. https://doi.org/10.3390/ijms22189821

Nita, M., & Grzybowski, A. (2016). The Role of the Reactive Oxygen Species and Oxidative Stress in the Pathomechanism of the Age-Related Ocular Diseases and Other Pathologies of the Anterior and Posterior Eye Segments in Adults. Oxidative medicine and cellular longevity, 2016, 3164734. https://doi.org/10.1155/2016/3164734

Okutsu, M., Yamada, M., Tokizawa, K., Marui, S., Suzuki, K., Lira, V. A., & Nagashima, K. (2021). Regular exercise stimulates endothelium autophagy via IL-1 signaling in ApoE deficient mice. FASEB journal : official publication of the Federation of American Societies for Experimental Biology, 35(7), e21698. https://doi.org/10.1096/fj.202002790RR. FASEB J. 2021;35(7):e21698. doi:10.1096/fj.202002790RR

Pagano, G., Pallardó, F. V., Lyakhovich, A., Tiano, L., Fittipaldi, M. R., Toscanesi, M., & Trifuoggi, M. (2020). Aging-Related Disorders and Mitochondrial Dysfunction: A Critical Review for Prospect Mitoprotective Strategies Based on Mitochondrial Nutrient Mixtures. International journal of molecular sciences, 21(19), 7060. https://doi.org/10.3390/ijms21197060

Pan, M., Han, Y., Basu, A., Dai, A., Si, R., Willson, C., Balistrieri, A., Scott, B. T., & Makino, A. (2018). Overexpression of hexokinase 2 reduces mitochondrial calcium overload in coronary endothelial cells of type 2 diabetic mice. American journal of physiology. Cell physiology, 314(6), C732–C740. https://doi.org/10.1152/ajpcell.00350.2017

Peng, S., Grace, M. S., Gondin, A. B., Retamal, J. S., Dill, L., Darby, W., Bunnett, N. W., Abogadie, F. C., Carbone, S. E., Tigani, T., Davis, T. P., Poole, D. P., Veldhuis, N. A., & McIntyre, P. (2020). The transient receptor potential vanilloid 4 (TRPV4) ion channel mediates protease activated receptor 1 (PAR1)-induced vascular hyperpermeability. Laboratory investigation; a journal of technical methods and pathology, 100(8), 1057–1067. https://doi.org/10.1038/s41374-020-0430-7

Peoples, J. N., Saraf, A., Ghazal, N., Pham, T. T., & Kwong, J. Q. (2019). Mitochondrial dysfunction and oxidative stress in heart disease. Experimental & molecular medicine, 51(12), 1–13. https://doi.org/10.1038/s12276-019-0355-7

Perrone, D., Fuggetta, M. P., Ardito, F., Cottarelli, A., De Filippis, A., Ravagnan, G., De Maria, S., & Lo Muzio, L. (2017). Resveratrol (3,5,4'-trihydroxystilbene) and its properties in oral diseases. Experimental and therapeutic medicine, 14(1), 3–9. https://doi.org/10.3892/etm.2017.4472

Pickrell, A. M., & Youle, R. J. (2015). The roles of PINK1, parkin, and mitochondrial fidelity in Parkinson's disease. Neuron, 85(2), 257–273. https://doi.org/10.1016/j.neuron.2014.12.007

Pinton, P., Giorgi, C., Siviero, R., Zecchini, E., & Rizzuto, R. (2008). Calcium and apoptosis: ER-mitochondria Ca2+ transfer in the control of apoptosis. Oncogene, 27(50), 6407–6418. https://doi.org/10.1038/onc.2008.308

Rakovic, A., Shurkewitsch, K., Seibler, P., Grünewald, A., Zanon, A., Hagenah, J., Krainc, D., & Klein, C. (2013). Phosphatase and tensin homolog (PTEN)-induced putative kinase 1 (PINK1)-dependent ubiquitination of endogenous Parkin attenuates mitophagy: study in human primary fibroblasts and induced pluripotent stem cell-derived neurons. The Journal of biological chemistry, 288(4), 2223–2237. https://doi.org/10.1074/jbc.M112.391680

Ray, A., Jaiswal, A., Dutta, J., Singh, S., & Mabalirajan, U. (2020). A looming role of mitochondrial calcium in dictating the lung epithelial integrity and pathophysiology of lung diseases. Mitochondrion, 55, 111–121. https://doi.org/10.1016/j.mito.2020.09.004

Rius-Pérez, S., Torres-Cuevas, I., Millán, I., Ortega, Á. L., & Pérez, S. (2020). PGC-1α, Inflammation, and Oxidative Stress: An Integrative View in Metabolism. Oxidative medicine and cellular longevity, 2020, 1452696. https://doi.org/10.1155/2020/1452696

Rizzuto, R., Marchi, S., Bonora, M., Aguiari, P., Bononi, A., De Stefani, D., Giorgi, C., Leo, S., Rimessi, A., Siviero, R., Zecchini, E., & Pinton, P. (2009). Ca(2+) transfer from the ER to mitochondria: when, how and why. Biochimica et biophysica acta, 1787(11), 1342–1351. https://doi.org/10.1016/j.bbabio.2009.03.015

Sanchis-Gomar, F., Perez-Quilis, C., Leischik, R., & Lucia, A. (2016). Epidemiology of coronary heart disease and acute coronary syndrome. Annals of translational medicine, 4(13), 256. https://doi.org/10.21037/atm.2016.06.33

Schwalm, J. D., McKee, M., Huffman, M. D., & Yusuf, S. (2016). Resource Effective Strategies to Prevent and Treat Cardiovascular Disease. Circulation, 133(8), 742–755. https://doi.org/10.1161/CIRCULATIONAHA.115.008721

Shenouda, S. M., Widlansky, M. E., Chen, K., Xu, G., Holbrook, M., Tabit, C. E., Hamburg, N. M., Frame, A. A., Caiano, T. L., Kluge, M. A., Duess, M. A., Levit, A., Kim, B., Hartman, M. L., Joseph, L., Shirihai, O. S., & Vita, J. A. (2011). Altered mitochondrial dynamics contributes to endothelial dysfunction in diabetes mellitus. Circulation, 124(4), 444–453. https://doi.org/10.1161/CIRCULATIONAHA.110.014506

Tanpradit, N., Chatdarong, K., & Comizzoli, P. (2016). Carbonyl cyanide 4-(trifluoromethoxy)phenylhydrazone (FCCP) pre-exposure ensures follicle integrity during in vitro culture of ovarian tissue but not during cryopreservation in the domestic cat model. Journal of assisted reproduction and genetics, 33(12), 1621–1631. https://doi.org/10.1007/s10815-016-0810-5

Tanwar, J., Singh, J. B., & Motiani, R. K. (2021). Molecular machinery regulating mitochondrial calcium levels: The nuts and bolts of mitochondrial calcium dynamics. Mitochondrion, 57, 9–22. https://doi.org/10.1016/j.mito.2020.12.001

Tilokani, L., Nagashima, S., Paupe, V., & Prudent, J. (2018). Mitochondrial dynamics: overview of molecular mechanisms. Essays in biochemistry, 62(3), 341–360. https://doi.org/10.1042/EBC20170104

Timm, K. N., & Tyler, D. J. (2020). The Role of AMPK Activation for Cardioprotection in Doxorubicin-Induced Cardiotoxicity. Cardiovascular drugs and therapy, 34(2), 255–269. https://doi.org/10.1007/s10557-020-06941-x

Ungvari, Z., Tarantini, S., Donato, A. J., Galvan, V., & Csiszar, A. (2018). Mechanisms of Vascular Aging. Circulation research, 123(7), 849–867. https://doi.org/10.1161/CIRCRESAHA.118.311378

Vaka, R., Deer, E., & LaMarca, B. (2022). Is Mitochondrial Oxidative Stress a Viable Therapeutic Target in Preeclampsia?. Antioxidants (Basel, Switzerland), 11(2), 210. https://doi.org/10.3390/antiox11020210

Yaniv, Y., Spurgeon, H. A., Ziman, B. D., & Lakatta, E. G. (2013). Ca²+/calmodulin-dependent protein kinase II (CaMKII) activity and sinoatrial nodal pacemaker cell energetics. PloS one, 8(2), e57079. https://doi.org/10.1371/journal.pone.0057079

Yim, W. W., & Mizushima, N. (2020). Lysosome biology in autophagy. Cell discovery, 6, 6. https://doi.org/10.1038/s41421-020-0141-7

Youle, R. J., & van der Bliek, A. M. (2012). Mitochondrial fission, fusion, and stress. Science (New York, N.Y.), 337(6098), 1062–1065. https://doi.org/10.1126/science.1219855

Yu, E. P., & Bennett, M. R. (2016). The role of mitochondrial DNA damage in the development of atherosclerosis. Free radical biology & medicine, 100, 223–230. https://doi.org/10.1016/j.freeradbiomed.2016.06.011

Zhang, J., Xiang, H., Liu, J., Chen, Y., He, R. R., & Liu, B. (2020). Mitochondrial Sirtuin 3: New emerging biological function and therapeutic target. Theranostics, 10(18), 8315–8342. https://doi.org/10.7150/thno.45922

Zhou, J., Wang, H., Shen, R., Fang, J., Yang, Y., Dai, W., Zhu, Y., & Zhou, M. (2018). Mitochondrial-targeted antioxidant MitoQ provides neuroprotection and reduces neuronal apoptosis in experimental traumatic brain injury possibly via the Nrf2-ARE pathway. American journal of translational research, 10(6), 1887–1899.

Zhuan, B., Wang, X., Wang, M. D., Li, Z. C., Yuan, Q., Xie, J., & Yang, Z. (2020). Hypoxia induces pulmonary artery smooth muscle dysfunction through mitochondrial fragmentation-mediated endoplasmic reticulum stress. Aging, 12(23), 23684–23697. https://doi.org/10.18632/aging.103892

Zorov, D. B., Vorobjev, I. A., Popkov, V. A., Babenko, V. A., Zorova, L. D., Pevzner, I. B., Silachev, D. N., Zorov, S. D., Andrianova, N. V., & Plotnikov, E. Y. (2019). Lessons from the Discovery of Mitochondrial Fragmentation (Fission): A Review and Update. Cells, 8(2), 175. https://doi.org/10.3390/cells8020175

Zuo, Z., Jing, K., Wu, H., Wang, S., Ye, L., Li, Z., Yang, C., Pan, Q., Liu, W. J., & Liu, H. F. (2020). Mechanisms and Functions of Mitophagy and Potential Roles in Renal Disease. Frontiers in physiology, 11, 935. https://doi.org/10.3389/fphys.2020.00935

PDF
Full Text
Export Citation

View Dimensions


View Plumx



View Altmetric



7
Save
0
Citation
523
View
1
Share