The Strength in Breakdown: Understanding Mitophagy and Its Implications in Cardiovascular Diseases

Anastasia V. Poznyak; Alexey V. Churov; 3; Natalia V. Elizova; Tatiana Ivanovna Kovyanova; 2; Vasily N. Sukhorukov; 4; Alexander N. Orekhov; 4*

doi:10.25163/angiotherapy.879718

Angiogenesis, Inflammation & Therapeutics | Online ISSN 2207-872X

REVIEWS (Open Access)

The Strength in Breakdown: Understanding Mitophagy and Its Implications in Cardiovascular Diseases

Anastasia V. Poznyak ¹*, Alexey V. Churov ^2,3, Natalia V. Elizova ², Tatiana Ivanovna Kovyanova ^1,2, Vasily N. Sukhorukov ^3,4, Alexander N. Orekhov ^3,4*

+ Author Affiliations

Journal of Angiotherapy 8 (7) 1-14 https://doi.org/10.25163/angiotherapy.879718

Submitted: 10 May 2024 Revised: 15 July 2024 Published: 17 July 2024

Abstract

Mitophagy, the selective autophagy of mitochondria, plays a crucial role in maintaining cellular homeostasis by ensuring the quality and quantity of functional mitochondria. This process is essential for cellular health, as dysfunctional mitochondria can lead to severe pathological conditions, including cardiovascular disorders, cancer, and neurodegenerative diseases. Impaired mitophagy may result in abnormal mitochondrial morphology and DNA mutations, contributing to the progression of these ailments. Therefore, understanding the mechanisms regulating mitophagy and its implications in pathological contexts is of great importance. This review paper provides an in-depth exploration of the mechanisms of mitophagy and its role in maintaining mitochondrial quality. It summarizes the most recent findings in the field, particularly focusing on the implications of defective mitophagy in cardiovascular disorders. The study delves into the connections between impaired mitophagy and the development of atherosclerosis, ischemic heart disease, cardiomyopathies, hypertension, and peripheral vascular disease. Moreover, it discusses the various regulatory proteins and processes involved in mitophagy, presenting a comprehensive overview of the intricate network governing this crucial cellular process. By shedding light on the intricate mechanisms involved in mitophagy and its role in addressing cardiovascular disorders, this review paper paves the way for potential therapeutic targets aimed at mitigating mitochondrial dysfunction-related ailments. The identification of pathways and proteins associated with mitophagy provides valuable insights into potential interventions that could prevent or effectively treat these disorders. However, it also highlights the existing uncertainties and the need for further in-depth exploration to fully comprehend the complexity of mitophagy regulation and its broader implications in cellular health.

Keywords: mitophagy; mitochondria; atherosclerosis; CVD.

References

Alam, M., Ali, S., Mohammad, T., Hasan, G. M., Yadav, D. K., & Hassan, M. I. (2021). B Cell Lymphoma 2: A Potential Therapeutic Target for Cancer Therapy. International journal of molecular sciences, 22(19), 10442. https://doi.org/10.3390/ijms221910442

Bennett, M. R., Sinha, S., & Owens, G. K. (2016). Vascular Smooth Muscle Cells in Atherosclerosis. Circulation research, 118(4), 692–702. https://doi.org/10.1161/CIRCRESAHA.115.306361

Brandt, M. M., Nguyen, I. T. N., Krebber, M. M., van de Wouw, J., Mokry, M., Cramer, M. J., Duncker, D. J., Verhaar, M. C., Joles, J. A., & Cheng, C. (2019). Limited synergy of obesity and hypertension, prevalent risk factors in onset and progression of heart failure with preserved ejection fraction. Journal of cellular and molecular medicine, 23(10), 6666–6678. https://doi.org/10.1111/jcmm.14542

Cahill, T. J., Leo, V., Kelly, M., Stockenhuber, A., Kennedy, N. W., Bao, L., Cereghetti, G. M., Harper, A. R., Czibik, G., Liao, C., Bellahcene, M., Steeples, V., Ghaffari, S., Yavari, A., Mayer, A., Poulton, J., Ferguson, D. J., Scorrano, L., Hettiarachchi, N. T., Peers, C., … Ashrafian, H. (2015). Resistance of Dynamin-related Protein 1 Oligomers to Disassembly Impairs Mitophagy, Resulting in Myocardial Inflammation and Heart Failure. The Journal of biological chemistry, 290(43), 25907–25919. https://doi.org/10.1074/jbc.M115.665695

Calderón-Sánchez, E. M., Falcón, D., Martín-Bórnez, M., Ordoñez, A., & Smani, T. (2021). Urocortin Role in Ischemia Cardioprotection and the Adverse Cardiac Remodeling. International journal of molecular sciences, 22(22), 12115. https://doi.org/10.3390/ijms222212115

Checkouri, E., Blanchard, V., & Meilhac, O. (2021). Macrophages in Atherosclerosis, First or Second Row Players?. Biomedicines, 9(9), 1214. https://doi.org/10.3390/biomedicines9091214

Choubey, V., Zeb, A., & Kaasik, A. (2021). Molecular Mechanisms and Regulation of Mammalian Mitophagy. Cells, 11(1), 38. https://doi.org/10.3390/cells11010038

Chu, C. T., Ji, J., Dagda, R. K., Jiang, J. F., Tyurina, Y. Y., Kapralov, A. A., Tyurin, V. A., Yanamala, N., Shrivastava, I. H., Mohammadyani, D., Wang, K. Z. Q., Zhu, J., Klein-Seetharaman, J., Balasubramanian, K., Amoscato, A. A., Borisenko, G., Huang, Z., Gusdon, A. M., Cheikhi, A., Steer, E. K., … Kagan, V. E. (2013). Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells. Nature cell biology, 15(10), 1197–1205. https://doi.org/10.1038/ncb2837

Diao, R. Y., & Gustafsson, Å. B. (2022). Mitochondrial quality surveillance: mitophagy in cardiovascular health and disease. American journal of physiology. Cell physiology, 322(2), C218–C230. https://doi.org/10.1152/ajpcell.00360.2021

Fan, H., He, Z., Huang, H., Zhuang, H., Liu, H., Liu, X., Yang, S., He, P., Yang, H., & Feng, D. (2020). Mitochondrial Quality Control in Cardiomyocytes: A Critical Role in the Progression of Cardiovascular Diseases. Frontiers in physiology, 11, 252. https://doi.org/10.3389/fphys.2020.00252

Fritsch, L. E., Moore, M. E., Sarraf, S. A., & Pickrell, A. M. (2020). Ubiquitin and Receptor-Dependent Mitophagy Pathways and Their Implication in Neurodegeneration. Journal of molecular biology, 432(8), 2510–2524. https://doi.org/10.1016/j.jmb.2019.10.015

Funai, K., Summers, S. A., & Rutter, J. (2020). Reign in the membrane: How common lipids govern mitochondrial function. Current opinion in cell biology, 63, 162–173. https://doi.org/10.1016/j.ceb.2020.01.006

Gao, P., Yang, W., & Sun, L. (2020). Mitochondria-Associated Endoplasmic Reticulum Membranes (MAMs) and Their Prospective Roles in Kidney Disease. Oxidative medicine and cellular longevity, 2020, 3120539. https://doi.org/10.1155/2020/3120539

Gollmer, J., Zirlik, A., & Bugger, H. (2020). Mitochondrial Mechanisms in Diabetic Cardiomyopathy. Diabetes & metabolism journal, 44(1), 33–53. https://doi.org/10.4093/dmj.2019.0185

Gurusamy, N., Lekli, I., Gorbunov, N. V., Gherghiceanu, M., Popescu, L. M., & Das, D. K. (2009). Cardioprotection by adaptation to ischaemia augments autophagy in association with BAG-1 protein. Journal of cellular and molecular medicine, 13(2), 373–387. https://doi.org/10.1111/j.1582-4934.2008.00495.x

Gustafsson A. B. (2011). Bnip3 as a dual regulator of mitochondrial turnover and cell death in the myocardium. Pediatric cardiology, 32(3), 267–274. https://doi.org/10.1007/s00246-010-9876-5

Haas, T. L., Lloyd, P. G., Yang, H. T., & Terjung, R. L. (2012). Exercise training and peripheral arterial disease. Comprehensive Physiology, 2(4), 2933–3017. https://doi.org/10.1002/cphy.c110065

Hall, A. R., Burke, N., Dongworth, R. K., & Hausenloy, D. J. (2014). Mitochondrial fusion and fission proteins: novel therapeutic targets for combating cardiovascular disease. British journal of pharmacology, 171(8), 1890–1906. https://doi.org/10.1111/bph.12516

Harrison D. G. (2013). The mosaic theory revisited: common molecular mechanisms coordinating diverse organ and cellular events in hypertension. Journal of the American Society of Hypertension : JASH, 7(1), 68–74. https://doi.org/10.1016/j.jash.2012.11.007

Hill, B. G., Benavides, G. A., Lancaster, J. R., Jr, Ballinger, S., Dell'Italia, L., Jianhua, Z., & Darley-Usmar, V. M. (2012). Integration of cellular bioenergetics with mitochondrial quality control and autophagy. Biological chemistry, 393(12), 1485–1512. https://doi.org/10.1515/hsz-2012-0198

Hsiao, Y. T., Shimizu, I., Wakasugi, T., Yoshida, Y., Ikegami, R., Hayashi, Y., Suda, M., Katsuumi, G., Nakao, M., Ozawa, T., Izumi, D., Kashimura, T., Ozaki, K., Soga, T., & Minamino, T. (2021). Cardiac mitofusin-1 is reduced in non-responding patients with idiopathic dilated cardiomyopathy. Scientific reports, 11(1), 6722. https://doi.org/10.1038/s41598-021-86209-y

Jaminon, A., Reesink, K., Kroon, A., & Schurgers, L. (2019). The Role of Vascular Smooth Muscle Cells in Arterial Remodeling: Focus on Calcification-Related Processes. International journal of molecular sciences, 20(22), 5694. https://doi.org/10.3390/ijms20225694

Jiang, B., Zhou, X., Yang, T., Wang, L., Feng, L., Wang, Z., Xu, J., Jing, W., Wang, T., Su, H., Yang, G., & Zhang, Z. (2023). The role of autophagy in cardiovascular disease: Cross-interference of signaling pathways and underlying therapeutic targets. Frontiers in cardiovascular medicine, 10, 1088575. https://doi.org/10.3389/fcvm.2023.1088575

Jin, Q., Li, R., Hu, N., Xin, T., Zhu, P., Hu, S., Ma, S., Zhu, H., Ren, J., & Zhou, H. (2018). DUSP1 alleviates cardiac ischemia/reperfusion injury by suppressing the Mff-required mitochondrial fission and Bnip3-related mitophagy via the JNK pathways. Redox biology, 14, 576–587. https://doi.org/10.1016/j.redox.2017.11.004

Jin, S. M., & Youle, R. J. (2012). PINK1- and Parkin-mediated mitophagy at a glance. Journal of cell science, 125(Pt 4), 795–799. https://doi.org/10.1242/jcs.093849

Kagan, V. E., Chu, C. T., Tyurina, Y. Y., Cheikhi, A., & Bayir, H. (2014). Cardiolipin asymmetry, oxidation and signaling. Chemistry and physics of lipids, 179, 64–69. https://doi.org/10.1016/j.chemphyslip.2013.11.010

Kagan, V. E., Jiang, J., Huang, Z., Tyurina, Y. Y., Desbourdes, C., Cottet-Rousselle, C., Dar, H. H., Verma, M., Tyurin, V. A., Kapralov, A. A., Cheikhi, A., Mao, G., Stolz, D., St Croix, C. M., Watkins, S., Shen, Z., Li, Y., Greenberg, M. L., Tokarska-Schlattner, M., Boissan, M., … Schlattner, U. (2016). NDPK-D (NM23-H4)-mediated externalization of cardiolipin enables elimination of depolarized mitochondria by mitophagy. Cell death and differentiation, 23(7), 1140–1151. https://doi.org/10.1038/cdd.2015.160

Kaludercic, N., Maiuri, M. C., Kaushik, S., Fernández, Á. F., de Bruijn, J., Castoldi, F., Chen, Y., Ito, J., Mukai, R., Murakawa, T., Nah, J., Pietrocola, F., Saito, T., Sebti, S., Semenzato, M., Tsansizi, L., Sciarretta, S., & Madrigal-Matute, J. (2020). Comprehensive autophagy evaluation in cardiac disease models. Cardiovascular research, 116(3), 483–504. https://doi.org/10.1093/cvr/cvz233

Kim, S., Lee, W., & Cho, K. (2021). P62 Links the Autophagy Pathway and the Ubiquitin-Proteasome System in Endothelial Cells during Atherosclerosis. International journal of molecular sciences, 22(15), 7791. https://doi.org/10.3390/ijms22157791

Klanova, M., & Klener, P. (2020). BCL-2 Proteins in Pathogenesis and Therapy of B-Cell Non-Hodgkin Lymphomas. Cancers, 12(4), 938. https://doi.org/10.3390/cancers12040938

Kny, M., & Fielitz, J. (2022). Hidden Agenda - The Involvement of Endoplasmic Reticulum Stress and Unfolded Protein Response in Inflammation-Induced Muscle Wasting. Frontiers in immunology, 13, 878755. https://doi.org/10.3389/fimmu.2022.878755

Li, G., Li, J., Shao, R., Zhao, J., & Chen, M. (2021). FUNDC1: A Promising Mitophagy Regulator at the Mitochondria-Associated Membrane for Cardiovascular Diseases. Frontiers in cell and developmental biology, 9, 788634. https://doi.org/10.3389/fcell.2021.788634

Li, Y., Ge, J., Yin, Y., Yang, R., Kong, J., & Gu, J. (2022). Upregulated miR-206 Aggravates Deep Vein Thrombosis by Regulating GJA1-Mediated Autophagy of Endothelial Progenitor Cells. Cardiovascular therapeutics, 2022, 9966306. https://doi.org/10.1155/2022/9966306

Li, Y., Zheng, W., Lu, Y., Zheng, Y., Pan, L., Wu, X., Yuan, Y., Shen, Z., Ma, S., Zhang, X., Wu, J., Chen, Z., & Zhang, X. (2021). BNIP3L/NIX-mediated mitophagy: molecular mechanisms and implications for human disease. Cell death & disease, 13(1), 14. https://doi.org/10.1038/s41419-021-04469-y

Lin, J., Duan, J., Wang, Q., Xu, S., Zhou, S., & Yao, K. (2022). Mitochondrial Dynamics and Mitophagy in Cardiometabolic Disease. Frontiers in cardiovascular medicine, 9, 917135. https://doi.org/10.3389/fcvm.2022.917135

Liu, M., & Wu, Y. (2022). Role of Mitophagy in Coronary Heart Disease: Targeting the Mitochondrial Dysfunction and Inflammatory Regulation. Frontiers in cardiovascular medicine, 9, 819454. https://doi.org/10.3389/fcvm.2022.819454

Marinkovic, M., Šprung, M., & Novak, I. (2021). Dimerization of mitophagy receptor BNIP3L/NIX is essential for recruitment of autophagic machinery. Autophagy, 17(5), 1232–1243. https://doi.org/10.1080/15548627.2020.1755120

Marzetti, E., Csiszar, A., Dutta, D., Balagopal, G., Calvani, R., & Leeuwenburgh, C. (2013). Role of mitochondrial dysfunction and altered autophagy in cardiovascular aging and disease: from mechanisms to therapeutics. American journal of physiology. Heart and circulatory physiology, 305(4), H459–H476. https://doi.org/10.1152/ajpheart.00936.2012

Matsui, Y., Takagi, H., Qu, X., Abdellatif, M., Sakoda, H., Asano, T., Levine, B., & Sadoshima, J. (2007). Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circulation research, 100(6), 914–922. https://doi.org/10.1161/01.RES.0000261924.76669.36

Meissner, C., Lorenz, H., Hehn, B., & Lemberg, M. K. (2015). Intramembrane protease PARL defines a negative regulator of PINK1- and PARK2/Parkin-dependent mitophagy. Autophagy, 11(9), 1484–1498. https://doi.org/10.1080/15548627.2015.1063763

Morciano, G., Patergnani, S., Bonora, M., Pedriali, G., Tarocco, A., Bouhamida, E., Marchi, S., Ancora, G., Anania, G., Wieckowski, M. R., Giorgi, C., & Pinton, P. (2020). Mitophagy in Cardiovascular Diseases. Journal of clinical medicine, 9(3), 892. https://doi.org/10.3390/jcm9030892

Mullen, T. D., Hannun, Y. A., & Obeid, L. M. (2012). Ceramide synthases at the centre of sphingolipid metabolism and biology. The Biochemical journal, 441(3), 789–802. https://doi.org/10.1042/BJ20111626

Park, G. H., Park, J. H., & Chung, K. C. (2021). Precise control of mitophagy through ubiquitin proteasome system and deubiquitin proteases and their dysfunction in Parkinson's disease. BMB reports, 54(12), 592–600. https://doi.org/10.5483/BMBRep.2021.54.12.107

Picca, A., Mankowski, R. T., Burman, J. L., Donisi, L., Kim, J. S., Marzetti, E., & Leeuwenburgh, C. (2018). Mitochondrial quality control mechanisms as molecular targets in cardiac ageing. Nature reviews. Cardiology, 15(9), 543–554. https://doi.org/10.1038/s41569-018-0059-z

Popov L. D. (2022). Mitochondrial-derived vesicles: Recent insights. Journal of cellular and molecular medicine, 26(12), 3323–3328. https://doi.org/10.1111/jcmm.17391

Prieto Huarcaya, S., Drobny, A., Marques, A. R. A., Di Spiezio, A., Dobert, J. P., Balta, D., Werner, C., Rizo, T., Gallwitz, L., Bub, S., Stojkovska, I., Belur, N. R., Fogh, J., Mazzulli, J. R., Xiang, W., Fulzele, A., Dejung, M., Sauer, M., Winner, B., Rose-John, S., … Zunke, F. (2022). Recombinant pro-CTSD (cathepsin D) enhances SNCA/α-Synuclein degradation in α-Synucleinopathy models. Autophagy, 18(5), 1127–1151. https://doi.org/10.1080/15548627.2022.2045534

Pyo, J. O., Yoo, S. M., Ahn, H. H., Nah, J., Hong, S. H., Kam, T. I., Jung, S., & Jung, Y. K. (2013). Overexpression of Atg5 in mice activates autophagy and extends lifespan. Nature communications, 4, 2300. https://doi.org/10.1038/ncomms3300

Razani, B., Feng, C., Coleman, T., Emanuel, R., Wen, H., Hwang, S., Ting, J. P., Virgin, H. W., Kastan, M. B., & Semenkovich, C. F. (2012). Autophagy links inflammasomes to atherosclerotic progression. Cell metabolism, 15(4), 534–544. https://doi.org/10.1016/j.cmet.2012.02.011

Saito, T., & Sadoshima, J. (2015). Molecular mechanisms of mitochondrial autophagy/mitophagy in the heart. Circulation research, 116(8), 1477–1490. https://doi.org/10.1161/CIRCRESAHA.116.303790

Schieber, M. N., Hasenkamp, R. M., Pipinos, I. I., Johanning, J. M., Stergiou, N., DeSpiegelaere, H. K., Chien, J. H., & Myers, S. A. (2017). Muscle strength and control characteristics are altered by peripheral artery disease. Journal of vascular surgery, 66(1), 178–186.e12. https://doi.org/10.1016/j.jvs.2017.01.051

Schirone, L., Forte, M., D'Ambrosio, L., Valenti, V., Vecchio, D., Schiavon, S., Spinosa, G., Sarto, G., Petrozza, V., Frati, G., & Sciarretta, S. (2022). An Overview of the Molecular Mechanisms Associated with Myocardial Ischemic Injury: State of the Art and Translational Perspectives. Cells, 11(7), 1165. https://doi.org/10.3390/cells11071165

Sharma, M. D., Nguyen, A. V., Brown, S., & Robbins, R. J. (2017). Cardiovascular Disease in Acromegaly. Methodist DeBakey cardiovascular journal, 13(2), 64–67. https://doi.org/10.14797/mdcj-13-2-64

Shi, R. Y., Zhu, S. H., Li, V., Gibson, S. B., Xu, X. S., & Kong, J. M. (2014). BNIP3 interacting with LC3 triggers excessive mitophagy in delayed neuronal death in stroke. CNS neuroscience & therapeutics, 20(12), 1045–1055. https://doi.org/10.1111/cns.12325

Shiiba, I., Takeda, K., Nagashima, S., Ito, N., Tokuyama, T., Yamashita, S. I., Kanki, T., Komatsu, T., Urano, Y., Fujikawa, Y., Inatome, R., & Yanagi, S. (2021). MITOL promotes cell survival by degrading Parkin during mitophagy. EMBO reports, 22(3), e49097. https://doi.org/10.15252/embr.201949097

Su, X., Zhou, M., Li, Y., An, N., Yang, F., Zhang, G., Xu, L., Chen, H., Wu, H., & Xing, Y. (2022). Mitochondrial Damage in Myocardial Ischemia/Reperfusion Injury and Application of Natural Plant Products. Oxidative medicine and cellular longevity, 2022, 8726564. https://doi.org/10.1155/2022/8726564

Sun, S., Hou, H., Ma, G., Ma, Q., Li, N., Zhang, L., Dong, C., Cao, M., Tam, K. Y., Ying, Z., & Wang, H. (2022). The interaction between E3 ubiquitin ligase Parkin and mitophagy receptor PHB2 links inner mitochondrial membrane ubiquitination to efficient mitophagy. The Journal of biological chemistry, 298(12), 102704. https://doi.org/10.1016/j.jbc.2022.102704

Terešak, P., Lapao, A., Subic, N., Boya, P., Elazar, Z., & Simonsen, A. (2022). Regulation of PRKN-independent mitophagy. Autophagy, 18(1), 24–39. https://doi.org/10.1080/15548627.2021.18882441

Tong, M., Saito, T., Zhai, P., Oka, S. I., Mizushima, W., Nakamura, M., Ikeda, S., Shirakabe, A., & Sadoshima, J. (2019). Mitophagy Is Essential for Maintaining Cardiac Function During High Fat Diet-Induced Diabetic Cardiomyopathy. Circulation research, 124(9), 1360–1371. https://doi.org/10.1161/CIRCRESAHA.118.314607

Tuleta, I., & Frangogiannis, N. G. (2021). Fibrosis of the diabetic heart: Clinical significance, molecular mechanisms, and therapeutic opportunities. Advanced drug delivery reviews, 176, 113904. https://doi.org/10.1016/j.addr.2021.113904

Underwood, P. C., & Adler, G. K. (2013). The renin angiotensin aldosterone system and insulin resistance in humans. Current hypertension reports, 15(1), 59–70. https://doi.org/10.1007/s11906-012-0323-2

Vasam, G., Nadeau, R., Cadete, V. J. J., Lavallée-Adam, M., Menzies, K. J., & Burelle, Y. (2021). Proteomics characterization of mitochondrial-derived vesicles under oxidative stress. FASEB journal : official publication of the Federation of American Societies for Experimental Biology, 35(4), e21278. https://doi.org/10.1096/fj.202002151R

Villa, E., Proïcs, E., Rubio-Patiño, C., Obba, S., Zunino, B., Bossowski, J. P., Rozier, R. M., Chiche, J., Mondragón, L., Riley, J. S., Marchetti, S., Verhoeyen, E., Tait, S. W. G., & Ricci, J. E. (2017). Parkin-Independent Mitophagy Controls Chemotherapeutic Response in Cancer Cells. Cell reports, 20(12), 2846–2859. https://doi.org/10.1016/j.celrep.2017.08.087

Vos, M., Dulovic-Mahlow, M., Mandik, F., Frese, L., Kanana, Y., Haissatou Diaw, S., Depperschmidt, J., Böhm, C., Rohr, J., Lohnau, T., König, I. R., & Klein, C. (2021). Ceramide accumulation induces mitophagy and impairs β-oxidation in PINK1 deficiency. Proceedings of the National Academy of Sciences of the United States of America, 118(43), e2025347118. https://doi.org/10.1073/pnas.2025347118

Wan, W., Hua, F., Fang, P., Li, C., Deng, F., Chen, S., Ying, J., & Wang, X. (2022). Regulation of Mitophagy by Sirtuin Family Proteins: A Vital Role in Aging and Age-Related Diseases. Frontiers in aging neuroscience, 14, 845330. https://doi.org/10.3389/fnagi.2022.845330

Wang, C., & Wang, X. (2015). The interplay between autophagy and the ubiquitin-proteasome system in cardiac proteotoxicity. Biochimica et biophysica acta, 1852(2), 188–194. https://doi.org/10.1016/j.bbadis.2014.07.028

Wang, S., Zhao, Z., Feng, X., Cheng, Z., Xiong, Z., Wang, T., Lin, J., Zhang, M., Hu, J., Fan, Y., Reiter, R. J., Wang, H., & Sun, D. (2018). Melatonin activates Parkin translocation and rescues the impaired mitophagy activity of diabetic cardiomyopathy through Mst1 inhibition. Journal of cellular and molecular medicine, 22(10), 5132–5144. https://doi.org/10.1111/jcmm.13802

Wang, X. L., Feng, S. T., Wang, Y. T., Yuan, Y. H., Li, Z. P., Chen, N. H., Wang, Z. Z., & Zhang, Y. (2022). Mitophagy, a Form of Selective Autophagy, Plays an Essential Role in Mitochondrial Dynamics of Parkinson's Disease. Cellular and molecular neurobiology, 42(5), 1321–1339. https://doi.org/10.1007/s10571-021-01039-w

Wolf G. (2006). Renal injury due to renin-angiotensin-aldosterone system activation of the transforming growth factor-beta pathway. Kidney international, 70(11), 1914–1919. https://doi.org/10.1038/sj.ki.5001846

Xie, W., Zhang, L., Luo, W., Zhai, Z., Wang, C., & Shen, Y. H. (2020). AKT2 regulates endothelial-mediated coagulation homeostasis and promotes intrathrombotic recanalization and thrombus resolution in a mouse model of venous thrombosis. Journal of thrombosis and thrombolysis, 50(1), 98–111. https://doi.org/10.1007/s11239-020-02112-9

Yoo, S. M., & Jung, Y. K. (2018). A Molecular Approach to Mitophagy and Mitochondrial Dynamics. Molecules and cells, 41(1), 18–26. https://doi.org/10.14348/molcells.2018.2277

Yu, B. B., Zhi, H., Zhang, X. Y., Liang, J. W., He, J., Su, C., Xia, W. H., Zhang, G. X., & Tao, J. (2019). Mitochondrial dysfunction-mediated decline in angiogenic capacity of endothelial progenitor cells is associated with capillary rarefaction in patients with hypertension via downregulation of CXCR4/JAK2/SIRT5 signaling. EBioMedicine, 42, 64–75. https://doi.org/10.1016/j.ebiom.2019.03.031

Zhang W. (2020). The mitophagy receptor FUN14 domain-containing 1 (FUNDC1): A promising biomarker and potential therapeutic target of human diseases. Genes & diseases, 8(5), 640–654. https://doi.org/10.1016/j.gendis.2020.08.011

Zhang, Y., Wang, C., Zhou, J., Sun, A., Hueckstaedt, L. K., Ge, J., & Ren, J. (2017). Complex inhibition of autophagy by mitochondrial aldehyde dehydrogenase shortens lifespan and exacerbates cardiac aging. Biochimica et biophysica acta. Molecular basis of disease, 1863(8), 1919–1932. https://doi.org/10.1016/j.bbadis.2017.03.016

Zhou, X., Hu, X., Xie, J., Xu, C., Xu, W., & Jiang, H. (2012). Exogenous high-mobility group box 1 protein injection improves cardiac function after myocardial infarction: involvement of Wnt signaling activation. Journal of biomedicine & biotechnology, 2012, 743879. https://doi.org/10.1155/2012/743879

PDF
Abstract
Export Citation

View Dimensions

View Plumx

View Altmetric

Save

0
Citation

377
View

Share