Mitochondrial Dysfunction in Cardiac Diseases and Therapeutic Strategies
Abstract
:1. Introduction
2. Mitochondrial Function in Mammalian Cardiac Development
2.1. Embryonic Stage
2.2. Postnatal Stage
2.3. Mitochondrial Function in the Adult Heart
2.4. Mitochondrial Adaptations with Age
3. Mitochondrial Dysfunction in Cardiovascular Diseases
3.1. Mitochondrial Cardiomyopathy
3.1.1. Hypertrophic Cardiomyopathy
3.1.2. Dilated Cardiomyopathy
3.2. Congenital Heart Disease
3.3. Coronary Artery Disease
3.4. Myocardial Ischemia–Reperfusion Injury
3.5. Heart Failure
3.6. Drug-Induced Cardiac Toxicity
Dysfunctional Mitochondrial Component | Molecules | CVD | Ref. |
---|---|---|---|
ATP | DYRK1B, PGC-1α | HF | [133] |
Autophagy, Anti-proliferative | Verapamil | DIC | [156] |
Complex I | Ndufa7 | HCM | [89] |
Complex I | NDUFB11 | HCM | [90] |
Complex I | S100a8/a9 | IR injury | [127] |
Complex I | AKAP1 | HF | [132] |
Complex IV | MRPS14 | HCM | [91] |
Complex IV | Cyclooxygenase-2 | DIC | [143] |
Complex I and IV | TK2 | HCM | [97] |
Complex IV, OXPHOS | Risperidone | DIC | [147] |
ETC | ELAC2 | HCM | [92] |
ETC | SRCAP complex | CHD | [21] |
ETC | Zotepine, Aripiprazole, Quetiapine, Risperidone, Clozapine | DIC | [146] |
ETC, ROS | Profilin, Profilin-SIRT3 | CAD | [119] |
ETC, Mitochondrial protein synthesis | Quinidine | DIC | [153] |
MtDNA | ATP6, CYTB, ND5, ND4, and ND2 | CHD | [110] |
MtDNA | Replication defects | CHD | [113] |
MtDNA | PCSK9 | IR injury | [159] |
Mt-tRNA | M.8306T>C | MCM | [88] |
Mt-tRNA | M.3243A>G | MCM | [88] |
Mt-tRNA | M.4317A>G | MCM | [88] |
Mt-tRNA | GTPBP3 | HCM | [102] |
Mt-tRNA | 3302A>G, 295A>G, 4435A>G, 5655T>C, 12201T>C, 14692A>G, 15927G>A | DCM | [105] |
Mitochondrial morphology | MFN1/2 | DCM | [49] |
Mitochondrial morphology | DOX | DIC | [140] |
Organelle | TAZ | DCM | [93] |
Organelle | DNAJC19 | DCM | [94] |
Organelle | ATO | DIC | [141] |
Organelle | Antiarrhythmic drugs | DIC | [152] |
Organelle | MtDNA, MtRNA | DCM | [109] |
Organelle | Mitochondrial density and ATP | Cyanotic CHD | [111] |
Organelle | Defects in mitochondrial maturation | HLHS | [114] |
Organelle | Mt-tRNA | DCM | [116,117] |
OXPHOS | Vasodilators | DIC | [150] |
OXPHOS | M.8812A>G, M.10320G>A | DCM | [107] |
ETC, mPTP | CK2α | IR injury | [125] |
ROS | NLRP3 | HF | [130] |
ROS | NSAIDs | DIC | [142] |
4. Current Therapeutic Medications and Strategies
4.1. Mitochondrially Targeted Therapeutic Drugs
4.1.1. Drugs Targeting Mitochondrial Complexes
4.1.2. Drugs Targeting Mitochondrial Redox State
4.1.3. Drugs Targeting Mitochondrial Permeability Transition Pore
4.1.4. Drugs Targeting Mitochondrial Dynamics
4.2. Mitochondrially Targeted Gene Therapy Strategies
4.2.1. Mitochondrial Genome Editing
4.2.2. Ectopic Expression of Mitochondrial Proteins
4.2.3. Mitochondrial Replacement Therapy
4.2.4. Mitochondrial Transplantation
Drugs/Therapy | Mitochondrial Target | Disease | Therapeutic Mechanism | Ref. |
---|---|---|---|---|
Elamipretide | ETC | BTHS | Increasing mitochondrial oxygen flux, complex I and IV | [168,169,170] |
OP2113 | ROS/H2O2 | IR injury | Specific blockade of ROS/H2O2 production | [179,180] |
Idebenone | ETC/ROS | FRDA/HCM/AMI | Increasing ATP synthesis; ROS-AMPK-mTOR axis | [181,182,183] |
Carvedilol | OXPHOS | DIC | Lower troponin levels | [185,186,187] |
Mito-TEMPOL | OXPHOS | DIC | Scavenging oxygen free radicals | [189,190,191,228] |
Propofol | OXPHOS | IR injury | Transcriptional activation of mitochondrial protein LRPPRC | [193] |
Diazoxide | OXPHOS | CVD | Turn on ATP-sensitive potassium channel (KATP)and reduces ROS and Ca2+-induced swelling | [194] |
CsA | The mPTP | IR injury | Inhibition of mPTP | [197] |
The mPTP | The mPTP | IR injury | Improves CaCl2-induced mitochondrial swelling | [198] |
TRO40303 | The mPTP | AMI | Delayed mPTP opening. | [199,200] |
Ranolazine | The mPTP | Arrhythmia | Delayed mPTP opening; improved complex I | [202] |
Mdivi-1 | Dynamics | HF | Inhibition of DRP1 | [206] |
Dynasore | Dynamics | IR injury | Improved survival and viability | [207] |
BGP-15 | Dynamics | CVD | Increasing OPA1 | [209] |
SAMβA | Dynamics | HF | Inhibits the interaction of MFN1 with βIIPKC | [210] |
Trimetazidine | Dynamics | Angina pectoris | Improves mitochondrial structural and functional damage | [211] |
PCSK9-siRNA | Autophagy | IR injury | Inhibition of autophagy | [126] |
β-hydroxybutyric acid | Acetylation/inflammation | HFpEF | β-Hydroxybutyric acid targets mitochondrial hyperacetylation | [130] |
MitoTALENs | MtDNA | CVD | Targeting mutant loci and suppressing mutant gene replication | [212,213] |
CRISPR/Cas9 | MtDNA | CVD | Gene editing | [214] |
5. Discussion and Outlook
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Panda, P.; Verma, H.K.; Lakkakula, S.; Merchant, N.; Kadir, F.; Rahman, S.; Jeffree, M.S.; Lakkakula, B.V.K.S.; Rao, P.V. Biomarkers of Oxidative Stress Tethered to Cardiovascular Diseases. Oxidative Med. Cell. Longev. 2022, 2022, 9154295. [Google Scholar] [CrossRef] [PubMed]
- Katona, M.; Bartók, Á.; Nichtova, Z.; Csordás, G.; Berezhnaya, E.; Weaver, D.; Ghosh, A.; Várnai, P.; Yule, D.I.; Hajnóczky, G. Capture at the ER-mitochondrial contacts licenses IP(3) receptors to stimulate local Ca2+ transfer and oxidative metabolism. Nat. Commun. 2022, 13, 6779. [Google Scholar] [CrossRef] [PubMed]
- Suski, J.; Lebiedzinska, M.; Bonora, M.; Pinton, P.; Duszynski, J.; Wieckowski, M.R. Relation Between Mitochondrial Membrane Potential and ROS Formation. Methods Mol. Biol. 2018, 1782, 357–381. [Google Scholar] [CrossRef]
- Nguyen, B.Y.; Ruiz-Velasco, A.; Bui, T.; Collins, L.; Wang, X.; Liu, W. Mitochondrial function in the heart: The insight into mechanisms and therapeutic potentials. Br. J. Pharmacol. 2019, 176, 4302–4318. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Q.; Sun, Q.; Zhou, L.; Liu, K.; Jiao, K. Complex Regulation of Mitochondrial Function During Cardiac Development. J. Am. Heart Assoc. 2019, 8, e012731. [Google Scholar] [CrossRef]
- Martin, O.J.; Lai, L.; Soundarapandian, M.M.; Leone, T.C.; Zorzano, A.; Keller, M.P.; Attie, A.D.; Muoio, D.M.; Kelly, D.P. A role for peroxisome proliferator-activated receptor γ coactivator-1 in the control of mitochondrial dynamics during postnatal cardiac growth. Circ. Res. 2014, 114, 626–636. [Google Scholar] [CrossRef] [PubMed]
- Murray, T.V.; Ahmad, A.; Brewer, A.C. Reactive oxygen at the heart of metabolism. Trends Cardiovasc. Med. 2014, 24, 113–120. [Google Scholar] [CrossRef]
- Drenckhahn, J.D. Heart development: Mitochondria in command of cardiomyocyte differentiation. Dev. Cell 2011, 21, 392–393. [Google Scholar] [CrossRef]
- Cho, S.W.; Park, J.S.; Heo, H.J.; Park, S.W.; Song, S.; Kim, I.; Han, Y.M.; Yamashita, J.K.; Youm, J.B.; Han, J.; et al. Dual modulation of the mitochondrial permeability transition pore and redox signaling synergistically promotes cardiomyocyte differentiation from pluripotent stem cells. J. Am. Heart Assoc. 2014, 3, e000693. [Google Scholar] [CrossRef]
- Hom, J.R.; Quintanilla, R.A.; Hoffman, D.L.; de Mesy Bentley, K.L.; Molkentin, J.D.; Sheu, S.S.; Porter, G.A., Jr. The permeability transition pore controls cardiac mitochondrial maturation and myocyte differentiation. Dev. Cell 2011, 21, 469–478. [Google Scholar] [CrossRef]
- Cao, X.; Chen, Y. Mitochondria and calcium signaling in embryonic development. Semin. Cell Dev. Biol. 2009, 20, 337–345. [Google Scholar] [CrossRef] [PubMed]
- Rowe, G.C.; Jiang, A.; Arany, Z. PGC-1 coactivators in cardiac development and disease. Circ. Res. 2010, 107, 825–838. [Google Scholar] [CrossRef] [PubMed]
- Arany, Z.; He, H.; Lin, J.; Hoyer, K.; Handschin, C.; Toka, O.; Ahmad, F.; Matsui, T.; Chin, S.; Wu, P.H.; et al. Transcriptional coactivator PGC-1 alpha controls the energy state and contractile function of cardiac muscle. Cell Metab. 2005, 1, 259–271. [Google Scholar] [CrossRef] [PubMed]
- Leone, T.C.; Lehman, J.J.; Finck, B.N.; Schaeffer, P.J.; Wende, A.R.; Boudina, S.; Courtois, M.; Wozniak, D.F.; Sambandam, N.; Bernal-Mizrachi, C.; et al. PGC-1alpha deficiency causes multi-system energy metabolic derangements: Muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol. 2005, 3, e101. [Google Scholar] [CrossRef] [PubMed]
- Zhang, D.; Li, Y.; Heims-Waldron, D.; Bezzerides, V.; Guatimosim, S.; Guo, Y.; Gu, F.; Zhou, P.; Lin, Z.; Ma, Q.; et al. Mitochondrial Cardiomyopathy Caused by Elevated Reactive Oxygen Species and Impaired Cardiomyocyte Proliferation. Circ. Res. 2018, 122, 74–87. [Google Scholar] [CrossRef]
- Kasahara, A.; Cipolat, S.; Chen, Y.; Dorn, G.W., 2nd; Scorrano, L. Mitochondrial fusion directs cardiomyocyte differentiation via calcineurin and Notch signaling. Science 2013, 342, 734–737. [Google Scholar] [CrossRef]
- Ballard, A.; Zeng, R.; Zarei, A.; Shao, C.; Cox, L.; Yan, H.; Franco, A.; Dorn, G.W., 2nd; Faccio, R.; Veis, D.J. The tethering function of mitofusin2 controls osteoclast differentiation by modulating the Ca2+-NFATc1 axis. J. Biol. Chem. 2020, 295, 6629–6640. [Google Scholar] [CrossRef]
- de Brito, O.M.; Scorrano, L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 2008, 456, 605–610. [Google Scholar] [CrossRef] [PubMed]
- Zhao, K.; Huang, X.; Zhao, W.; Lu, B.; Yang, Z. LONP1-mediated mitochondrial quality control safeguards metabolic shifts in heart development. Development 2022, 149, dev200458. [Google Scholar] [CrossRef]
- Zhao, B.; Chen, Y.; Jiang, N.; Yang, L.; Sun, S.; Zhang, Y.; Wen, Z.; Ray, L.; Liu, H.; Hou, G.; et al. Znhit1 controls intestinal stem cell maintenance by regulating H2A.Z incorporation. Nat. Commun. 2019, 10, 1071. [Google Scholar] [CrossRef]
- Xu, M.; Yao, J.; Shi, Y.; Yi, H.; Zhao, W.; Lin, X.; Yang, Z. The SRCAP chromatin remodeling complex promotes oxidative metabolism during prenatal heart development. Development 2021, 148, dev199026. [Google Scholar] [CrossRef]
- Bishop, S.P.; Zhou, Y.; Nakada, Y.; Zhang, J. Changes in Cardiomyocyte Cell Cycle and Hypertrophic Growth During Fetal to Adult in Mammals. J. Am. Heart Assoc. 2021, 10, e017839. [Google Scholar] [CrossRef] [PubMed]
- Yan, H.; Rao, X.; Wang, R.; Zhu, S.; Liu, R.; Zheng, X. Cell Cycle Withdrawal Limit the Regenerative Potential of Neonatal Cardiomyocytes. Cardiovasc. Eng. Technol. 2021, 12, 475–484. [Google Scholar] [CrossRef] [PubMed]
- Kannan, S.; Kwon, C. Regulation of cardiomyocyte maturation during critical perinatal window. J. Physiol. 2020, 598, 2941–2956. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.; Bleck, C.K.; Glancy, B. 3D mitochondrial remodeling during postnatal heart development. FASEB J. 2022, 36, R6223. [Google Scholar] [CrossRef]
- Padula, S.L.; Velayutham, N.; Yutzey, K.E. Transcriptional Regulation of Postnatal Cardiomyocyte Maturation and Regeneration. Int. J. Mol. Sci. 2021, 22, 3288. [Google Scholar] [CrossRef] [PubMed]
- Piquereau, J.; Novotova, M.; Fortin, D.; Garnier, A.; Ventura-Clapier, R.; Veksler, V.; Joubert, F. Postnatal development of mouse heart: Formation of energetic microdomains. J. Physiol. 2010, 588, 2443–2454. [Google Scholar] [CrossRef]
- Sakamoto, T.; Matsuura, T.R.; Wan, S.; Ryba, D.M.; Kim, J.U.; Won, K.J.; Lai, L.; Petucci, C.; Petrenko, N.; Musunuru, K.; et al. A Critical Role for Estrogen-Related Receptor Signaling in Cardiac Maturation. Circ. Res. 2020, 126, 1685–1702. [Google Scholar] [CrossRef]
- Gong, G.; Song, M.; Csordas, G.; Kelly, D.P.; Matkovich, S.J.; Dorn, G.W., 2nd. Parkin-mediated mitophagy directs perinatal cardiac metabolic maturation in mice. Science 2015, 350, aad2459. [Google Scholar] [CrossRef]
- Sánchez-Díaz, M.; Nicolás-Ávila, J.; Cordero, M.D.; Hidalgo, A. Mitochondrial Adaptations in the Growing Heart. Trends Endocrinol. Metab. 2020, 31, 308–319. [Google Scholar] [CrossRef]
- Qiao, X.; Jia, S.; Ye, J.; Fang, X.; Zhang, C.; Cao, Y.; Xu, C.; Zhao, L.; Zhu, Y.; Wang, L.; et al. PTPIP51 regulates mouse cardiac ischemia/reperfusion through mediating the mitochondria-SR junction. Sci. Rep. 2017, 7, 45379. [Google Scholar] [CrossRef] [PubMed]
- Mishra, J.; Camara, A.K.S. Mitochondrial Calcium Handling in Isolated Mitochondria from a Guinea Pig Heart. Methods Mol. Biol. 2022, 2497, 97–106. [Google Scholar] [CrossRef] [PubMed]
- Zorov, D.B.; Juhaszova, M.; Sollott, S.J. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol. Rev. 2014, 94, 909–950. [Google Scholar] [CrossRef]
- Cadenas, S. Mitochondrial uncoupling, ROS generation and cardioprotection. Biochim. Biophys. Acta Bioenerg. 2018, 1859, 940–950. [Google Scholar] [CrossRef]
- Fernandez-Vizarra, E.; Zeviani, M. Mitochondrial disorders of the OXPHOS system. FEBS Lett. 2021, 595, 1062–1106. [Google Scholar] [CrossRef] [PubMed]
- Yang, Y.; Wang, W.; Tian, Y.; Shi, J. Sirtuin 3 and mitochondrial permeability transition pore (mPTP): A systematic review. Mitochondrion 2022, 64, 103–111. [Google Scholar] [CrossRef] [PubMed]
- Barthélémy, C.; Ogier de Baulny, H.; Diaz, J.; Cheval, M.A.; Frachon, P.; Romero, N.; Goutieres, F.; Fardeau, M.; Lombès, A. Late-onset mitochondrial DNA depletion: DNA copy number, multiple deletions, and compensation. Ann. Neurol. 2001, 49, 607–617. [Google Scholar] [CrossRef]
- Kopajtich, R.; Nicholls, T.J.; Rorbach, J.; Metodiev, M.D.; Freisinger, P.; Mandel, H.; Vanlander, A.; Ghezzi, D.; Carrozzo, R.; Taylor, R.W.; et al. Mutations in GTPBP3 cause a mitochondrial translation defect associated with hypertrophic cardiomyopathy, lactic acidosis, and encephalopathy. Am. J. Hum. Genet. 2014, 95, 708–720. [Google Scholar] [CrossRef]
- Vilardo, E.; Rossmanith, W. Molecular insights into HSD10 disease: Impact of SDR5C1 mutations on the human mitochondrial RNase P complex. Nucleic Acids Res. 2015, 43, 5112–5119. [Google Scholar] [CrossRef]
- Hochberg, I.; Demain, L.A.M.; Richer, J.; Thompson, K.; Urquhart, J.E.; Rea, A.; Pagarkar, W.; Rodríguez-Palmero, A.; Schlüter, A.; Verdura, E.; et al. Bi-allelic variants in the mitochondrial RNase P subunit PRORP cause mitochondrial tRNA processing defects and pleiotropic multisystem presentations. Am. J. Hum. Genet. 2021, 108, 2195–2204. [Google Scholar] [CrossRef]
- Ng, M.Y.W.; Wai, T.; Simonsen, A. Quality control of the mitochondrion. Dev. Cell 2021, 56, 881–905. [Google Scholar] [CrossRef] [PubMed]
- Fan, H.; He, Z.; Huang, H.; Zhuang, H.; Liu, H.; Liu, X.; Yang, S.; He, P.; Yang, H.; Feng, D. Mitochondrial Quality Control in Cardiomyocytes: A Critical Role in the Progression of Cardiovascular Diseases. Front. Physiol. 2020, 11, 252. [Google Scholar] [CrossRef] [PubMed]
- Tahrir, F.G.; Langford, D.; Amini, S.; Mohseni Ahooyi, T.; Khalili, K. Mitochondrial quality control in cardiac cells: Mechanisms and role in cardiac cell injury and disease. J. Cell. Physiol. 2019, 234, 8122–8133. [Google Scholar] [CrossRef] [PubMed]
- Boyman, L.; Karbowski, M.; Lederer, W.J. Regulation of Mitochondrial ATP Production: Ca2+ Signaling and Quality Control. Trends Mol. Med. 2020, 26, 21–39. [Google Scholar] [CrossRef]
- Wang, Y.P.; Sharda, A.; Xu, S.N.; van Gastel, N.; Man, C.H.; Choi, U.; Leong, W.Z.; Li, X.; Scadden, D.T. Malic enzyme 2 connects the Krebs cycle intermediate fumarate to mitochondrial biogenesis. Cell Metab. 2021, 33, 1027–1041.e1028. [Google Scholar] [CrossRef]
- Jin, J.Y.; Wei, X.X.; Zhi, X.L.; Wang, X.H.; Meng, D. Drp1-dependent mitochondrial fission in cardiovascular disease. Acta Pharmacol. Sin. 2021, 42, 655–664. [Google Scholar] [CrossRef]
- Chang, Y.W.; Song, Z.H.; Chen, C.C. FAK regulates cardiomyocyte mitochondrial fission and function through Drp1. FEBS J. 2022, 289, 1897–1910. [Google Scholar] [CrossRef]
- Cao, Y.P.; Zheng, M. Mitochondrial dynamics and inter-mitochondrial communication in the heart. Arch. Biochem. Biophys. 2019, 663, 214–219. [Google Scholar] [CrossRef]
- Chen, Y.; Liu, Y.; Dorn, G.W., 2nd. Mitochondrial fusion is essential for organelle function and cardiac homeostasis. Circ. Res. 2011, 109, 1327–1331. [Google Scholar] [CrossRef]
- Franco, A.; Walton, C.E.; Dang, X. Mitochondria Clumping vs. Mitochondria Fusion in CMT2A Diseases. Life 2022, 12, 2110. [Google Scholar] [CrossRef]
- Ishihara, N.; Nomura, M.; Jofuku, A.; Kato, H.; Suzuki, S.O.; Masuda, K.; Otera, H.; Nakanishi, Y.; Nonaka, I.; Goto, Y.; et al. Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat. Cell Biol. 2009, 11, 958–966. [Google Scholar] [CrossRef] [PubMed]
- Song, M.; Franco, A.; Fleischer, J.A.; Zhang, L.; Dorn, G.W., 2nd. Abrogating Mitochondrial Dynamics in Mouse Hearts Accelerates Mitochondrial Senescence. Cell Metab. 2017, 26, 872–883.e875. [Google Scholar] [CrossRef] [PubMed]
- Wu, L.; Wang, L.; Du, Y.; Zhang, Y.; Ren, J. Mitochondrial quality control mechanisms as therapeutic targets in doxorubicin-induced cardiotoxicity. Trends Pharmacol. Sci. 2023, 44, 34–49. [Google Scholar] [CrossRef]
- Khuanjing, T.; Palee, S.; Kerdphoo, S.; Jaiwongkam, T.; Anomasiri, A.; Chattipakorn, S.C.; Chattipakorn, N. Donepezil attenuated cardiac ischemia/reperfusion injury through balancing mitochondrial dynamics, mitophagy, and autophagy. Transl. Res. 2021, 230, 82–97. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Zhu, Y.; Zhou, Q.; Yan, Y.; Qu, J.; Ye, H. Heat shock protein 70 expression protects against sepsis-associated cardiomyopathy by inhibiting autophagy. Hum. Exp. Toxicol. 2021, 40, 735–741. [Google Scholar] [CrossRef]
- Chi, R.F.; Li, L.; Wang, A.L.; Yang, H.; Xi, J.; Zhu, Z.F.; Wang, K.; Li, B.; Yang, L.G.; Qin, F.Z.; et al. Enhanced oxidative stress mediates pathological autophagy and necroptosis in cardiac myocytes in pressure overload induced heart failure in rats. Clin. Exp. Pharmacol. Physiol. 2022, 49, 60–69. [Google Scholar] [CrossRef]
- Forte, M.; Bianchi, F.; Cotugno, M.; Marchitti, S.; De Falco, E.; Raffa, S.; Stanzione, R.; Di Nonno, F.; Chimenti, I.; Palmerio, S.; et al. Pharmacological restoration of autophagy reduces hypertension-related stroke occurrence. Autophagy 2020, 16, 1468–1481. [Google Scholar] [CrossRef]
- Wang, M.; Shah, A.M. Age-associated pro-inflammatory remodeling and functional phenotype in the heart and large arteries. J. Mol. Cell. Cardiol. 2015, 83, 101–111. [Google Scholar] [CrossRef]
- Steenman, M.; Lande, G. Cardiac aging and heart disease in humans. Biophys. Rev. 2017, 9, 131–137. [Google Scholar] [CrossRef]
- Miyamoto, S. Autophagy and cardiac aging. Cell Death Differ. 2019, 26, 653–664. [Google Scholar] [CrossRef]
- Mendoza, A.; Karch, J. Keeping the beat against time: Mitochondrial fitness in the aging heart. Front. Aging 2022, 3, 951417. [Google Scholar] [CrossRef] [PubMed]
- Chen, G.; Kroemer, G.; Kepp, O. Mitophagy: An Emerging Role in Aging and Age-Associated Diseases. Front. Cell Dev. Biol. 2020, 8, 200. [Google Scholar] [CrossRef]
- Maxwell, K.N.; Fisher, E.A.; Breslow, J.L. Overexpression of PCSK9 accelerates the degradation of the LDLR in a post-endoplasmic reticulum compartment. Proc. Natl. Acad. Sci. USA 2005, 102, 2069–2074. [Google Scholar] [CrossRef] [PubMed]
- Sun, N.; Yun, J.; Liu, J.; Malide, D.; Liu, C.; Rovira, I.I.; Holmström, K.M.; Fergusson, M.M.; Yoo, Y.H.; Combs, C.A.; et al. Measuring In Vivo Mitophagy. Mol. Cell 2015, 60, 685–696. [Google Scholar] [CrossRef]
- Short, K.R.; Nair, K.S. Mechanisms of sarcopenia of aging. J. Endocrinol. Investig. 1999, 22, 95–105. [Google Scholar]
- Kujoth, G.C.; Hiona, A.; Pugh, T.D.; Someya, S.; Panzer, K.; Wohlgemuth, S.E.; Hofer, T.; Seo, A.Y.; Sullivan, R.; Jobling, W.A.; et al. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 2005, 309, 481–484. [Google Scholar] [CrossRef] [PubMed]
- Chen, T.; He, J.; Huang, Y.; Zhao, W. The generation of mitochondrial DNA large-scale deletions in human cells. J. Hum. Genet. 2011, 56, 689–694. [Google Scholar] [CrossRef]
- Guo, X.; Xu, W.; Zhang, W.; Pan, C.; Thalacker-Mercer, A.E.; Zheng, H.; Gu, Z. High-frequency and functional mitochondrial DNA mutations at the single-cell level. Proc. Natl. Acad. Sci. USA 2023, 120, e2201518120. [Google Scholar] [CrossRef]
- Lu, C.Y.; Lee, H.C.; Fahn, H.J.; Wei, Y.H. Oxidative damage elicited by imbalance of free radical scavenging enzymes is associated with large-scale mtDNA deletions in aging human skin. Mutat. Res. 1999, 423, 11–21. [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]
- El’darov Ch, M.; Vays, V.B.; Vangeli, I.M.; Kolosova, N.G.; Bakeeva, L.E. Morphometric Examination of Mitochondrial Ultrastructure in Aging Cardiomyocytes. Biochemistry 2015, 80, 604–609. [Google Scholar] [CrossRef] [PubMed]
- Zhao, L.; Zou, X.; Feng, Z.; Luo, C.; Liu, J.; Li, H.; Chang, L.; Wang, H.; Li, Y.; Long, J.; et al. Evidence for association of mitochondrial metabolism alteration with lipid accumulation in aging rats. Exp. Gerontol. 2014, 56, 3–12. [Google Scholar] [CrossRef] [PubMed]
- Picca, A.; Calvani, R.; Coelho-Júnior, H.J.; Marzetti, E. Mitophagy: At the heart of mitochondrial quality control in cardiac aging and frailty. Exp. Gerontol. 2021, 153, 111508. [Google Scholar] [CrossRef] [PubMed]
- Dai, D.F.; Chiao, Y.A.; Marcinek, D.J.; Szeto, H.H.; Rabinovitch, P.S. Mitochondrial oxidative stress in aging and healthspan. Longev. Healthspan 2014, 3, 6. [Google Scholar] [CrossRef]
- de Almeida, A.; de Oliveira, J.; da Silva Pontes, L.V.; de Souza Júnior, J.F.; Gonçalves, T.A.F.; Dantas, S.H.; de Almeida Feitosa, M.S.; Silva, A.O.; de Medeiros, I.A. ROS: Basic Concepts, Sources, Cellular Signaling, and its Implications in Aging Pathways. Oxidative Med. Cell. Longev. 2022, 2022, 1225578. [Google Scholar] [CrossRef]
- Li, W.W.; Wang, H.J.; Tan, Y.Z.; Wang, Y.L.; Yu, S.N.; Li, Z.H. Reducing lipofuscin accumulation and cardiomyocytic senescence of aging heart by enhancing autophagy. Exp. Cell Res. 2021, 403, 112585. [Google Scholar] [CrossRef]
- Sithara, T.; Drosatos, K. Metabolic Complications in Cardiac Aging. Front. Physiol. 2021, 12, 669497. [Google Scholar] [CrossRef]
- Picca, A.; Mankowski, R.T.; Burman, J.L.; Donisi, L.; Kim, J.S.; Marzetti, E.; Leeuwenburgh, C. Mitochondrial quality control mechanisms as molecular targets in cardiac ageing. Nat. Rev. Cardiol. 2018, 15, 543–554. [Google Scholar] [CrossRef]
- Lima, T.; Li, T.Y.; Mottis, A.; Auwerx, J. Pleiotropic effects of mitochondria in aging. Nat. Aging 2022, 2, 199–213. [Google Scholar] [CrossRef]
- Wu, Z.; Senchuk, M.M.; Dues, D.J.; Johnson, B.K.; Cooper, J.F.; Lew, L.; Machiela, E.; Schaar, C.E.; DeJonge, H.; Blackwell, T.K.; et al. Mitochondrial unfolded protein response transcription factor ATFS-1 promotes longevity in a long-lived mitochondrial mutant through activation of stress response pathways. BMC Biol. 2018, 16, 147. [Google Scholar] [CrossRef]
- Wiley, C.D.; Velarde, M.C.; Lecot, P.; Liu, S.; Sarnoski, E.A.; Freund, A.; Shirakawa, K.; Lim, H.W.; Davis, S.S.; Ramanathan, A.; et al. Mitochondrial Dysfunction Induces Senescence with a Distinct Secretory Phenotype. Cell Metab. 2016, 23, 303–314. [Google Scholar] [CrossRef]
- Yang, Y.; Gao, H.; Zhou, H.; Liu, Q.; Qi, Z.; Zhang, Y.; Zhang, J. The role of mitochondria-derived peptides in cardiovascular disease: Recent updates. Biomed. Pharmacother. 2019, 117, 109075. [Google Scholar] [CrossRef]
- Ikonomidis, I.; Katogiannis, K.; Kyriakou, E.; Taichert, M.; Katsimaglis, G.; Tsoumani, M.; Andreadou, I.; Maratou, E.; Lambadiari, V.; Kousathana, F.; et al. β-Amyloid and mitochondrial-derived peptide-c are additive predictors of adverse outcome to high-on-treatment platelet reactivity in type 2 diabetics with revascularized coronary artery disease. J. Thromb. Thrombolysis 2020, 49, 365–376. [Google Scholar] [CrossRef]
- Yen, K.; Wan, J.; Mehta, H.H.; Miller, B.; Christensen, A.; Levine, M.E.; Salomon, M.P.; Brandhorst, S.; Xiao, J.; Kim, S.J.; et al. Humanin Prevents Age-Related Cognitive Decline in Mice and is Associated with Improved Cognitive Age in Humans. Sci. Rep. 2018, 8, 14212. [Google Scholar] [CrossRef]
- Lee, C.; Zeng, J.; Drew, B.G.; Sallam, T.; Martin-Montalvo, A.; Wan, J.; Kim, S.J.; Mehta, H.; Hevener, A.L.; de Cabo, R.; et al. The mitochondrial-derived peptide MOTS-c promotes metabolic homeostasis and reduces obesity and insulin resistance. Cell Metab. 2015, 21, 443–454. [Google Scholar] [CrossRef]
- Wachoski-Dark, E.; Zhao, T.; Khan, A.; Shutt, T.E.; Greenway, S.C. Mitochondrial Protein Homeostasis and Cardiomyopathy. Int. J. Mol. Sci. 2022, 23, 3353. [Google Scholar] [CrossRef]
- Campbell, T.; Slone, J.; Huang, T. Mitochondrial Genome Variants as a Cause of Mitochondrial Cardiomyopathy. Cells 2022, 11, 2835. [Google Scholar] [CrossRef]
- Ding, Y.; Gao, B.; Huang, J. Mitochondrial Cardiomyopathy: The Roles of mt-tRNA Mutations. J. Clin. Med. 2022, 11, 6431. [Google Scholar] [CrossRef]
- Shi, X.; Zhang, Y.; Chen, R.; Gong, Y.; Zhang, M.; Guan, R.; Rotstein, O.D.; Liu, X.; Wen, X.Y. ndufa7 plays a critical role in cardiac hypertrophy. J. Cell. Mol. Med. 2020, 24, 13151–13162. [Google Scholar] [CrossRef]
- Reinson, K.; Kovacs-Nagy, R.; Õiglane-Shlik, E.; Pajusalu, S.; Nõukas, M.; Wintjes, L.T.; van den Brandt, F.C.A.; Brink, M.; Acker, T.; Ahting, U.; et al. Diverse phenotype in patients with complex I deficiency due to mutations in NDUFB11. Eur. J. Med. Genet. 2019, 62, 103572. [Google Scholar] [CrossRef]
- Jackson, C.B.; Huemer, M.; Bolognini, R.; Martin, F.; Szinnai, G.; Donner, B.C.; Richter, U.; Battersby, B.J.; Nuoffer, J.M.; Suomalainen, A.; et al. A variant in MRPS14 (uS14m) causes perinatal hypertrophic cardiomyopathy with neonatal lactic acidosis, growth retardation, dysmorphic features and neurological involvement. Hum. Mol. Genet. 2019, 28, 639–649. [Google Scholar] [CrossRef]
- Saoura, M.; Powell, C.A.; Kopajtich, R.; Alahmad, A.; Al-Balool, H.H.; Albash, B.; Alfadhel, M.; Alston, C.L.; Bertini, E.; Bonnen, P.E.; et al. Mutations in ELAC2 associated with hypertrophic cardiomyopathy impair mitochondrial tRNA 3’-end processing. Hum. Mutat. 2019, 40, 1731–1748. [Google Scholar] [CrossRef]
- Dudek, J.; Maack, C. Barth syndrome cardiomyopathy. Cardiovasc. Res. 2017, 113, 399–410. [Google Scholar] [CrossRef]
- Al Tuwaijri, A.; Alyafee, Y.; Alharbi, M.; Ballow, M.; Aldrees, M.; Alam, Q.; Sleiman, R.A.; Umair, M.; Alfadhel, M. Novel homozygous pathogenic mitochondrial DNAJC19 variant in a patient with dilated cardiomyopathy and global developmental delay. Mol. Genet. Genomic. Med. 2022, 10, e1969. [Google Scholar] [CrossRef]
- Ranjbarvaziri, S.; Kooiker, K.B.; Ellenberger, M.; Fajardo, G.; Zhao, M.; Vander Roest, A.S.; Woldeyes, R.A.; Koyano, T.T.; Fong, R.; Ma, N.; et al. Altered Cardiac Energetics and Mitochondrial Dysfunction in Hypertrophic Cardiomyopathy. Circulation 2021, 144, 1714–1731. [Google Scholar] [CrossRef]
- Nomura, S.; Satoh, M.; Fujita, T.; Higo, T.; Sumida, T.; Ko, T.; Yamaguchi, T.; Tobita, T.; Naito, A.T.; Ito, M.; et al. Cardiomyocyte gene programs encoding morphological and functional signatures in cardiac hypertrophy and failure. Nat. Commun. 2018, 9, 4435. [Google Scholar] [CrossRef]
- Mazurova, S.; Magner, M.; Kucerova-Vidrova, V.; Vondrackova, A.; Stranecky, V.; Pristoupilova, A.; Zamecnik, J.; Hansikova, H.; Zeman, J.; Tesarova, M.; et al. Thymidine kinase 2 and alanyl-tRNA synthetase 2 deficiencies cause lethal mitochondrial cardiomyopathy: Case reports and review of the literature. Cardiol. Young 2017, 27, 936–944. [Google Scholar] [CrossRef]
- Yip, M.C.J.; Savickas, S.; Gygi, S.P.; Shao, S. ELAC1 Repairs tRNAs Cleaved during Ribosome-Associated Quality Control. Cell Rep. 2020, 30, 2106–2114.e2105. [Google Scholar] [CrossRef]
- Brzezniak, L.K.; Bijata, M.; Szczesny, R.J.; Stepien, P.P. Involvement of human ELAC2 gene product in 3’ end processing of mitochondrial tRNAs. RNA Biol. 2011, 8, 616–626. [Google Scholar] [CrossRef]
- Haack, T.B.; Kopajtich, R.; Freisinger, P.; Wieland, T.; Rorbach, J.; Nicholls, T.J.; Baruffini, E.; Walther, A.; Danhauser, K.; Zimmermann, F.A.; et al. ELAC2 mutations cause a mitochondrial RNA processing defect associated with hypertrophic cardiomyopathy. Am. J. Hum. Genet. 2013, 93, 211–223. [Google Scholar] [CrossRef]
- Migunova, E.; Theophilopoulos, J.; Mercadante, M.; Men, J.; Zhou, C.; Dubrovsky, E.B. ELAC2/RNaseZ-linked cardiac hypertrophy in Drosophila melanogaster. Dis. Model. Mech. 2021, 14, 1754–8403. [Google Scholar] [CrossRef] [PubMed]
- Chen, D.; Zhang, Z.; Chen, C.; Yao, S.; Yang, Q.; Li, F.; He, X.; Ai, C.; Wang, M.; Guan, M.X. Deletion of Gtpbp3 in zebrafish revealed the hypertrophic cardiomyopathy manifested by aberrant mitochondrial tRNA metabolism. Nucleic Acids Res. 2019, 47, 5341–5355. [Google Scholar] [CrossRef] [PubMed]
- Orellana, E.A.; Siegal, E.; Gregory, R.I. tRNA dysregulation and disease. Nat. Rev. Genet. 2022, 23, 651–664. [Google Scholar] [CrossRef]
- Martínez-Reyes, I.; Chandel, N.S. Mitochondrial TCA cycle metabolites control physiology and disease. Nat. Commun. 2020, 11, 102. [Google Scholar] [CrossRef]
- Qi, Y.; Wu, Z.; Bai, Y.; Jiao, Y.; Li, P. Screening for Mitochondrial tRNA Mutations in 318 Patients with Dilated Cardiomyopathy. Hum. Hered. 2022, 87, 1–11. [Google Scholar] [CrossRef]
- Arbustini, E.; Diegoli, M.; Fasani, R.; Grasso, M.; Morbini, P.; Banchieri, N.; Bellini, O.; Dal Bello, B.; Pilotto, A.; Magrini, G.; et al. Mitochondrial DNA mutations and mitochondrial abnormalities in dilated cardiomyopathy. Am. J. Pathol. 1998, 153, 1501–1510. [Google Scholar] [CrossRef]
- Govindaraj, P.; Rani, B.; Sundaravadivel, P.; Vanniarajan, A.; Indumathi, K.P.; Khan, N.A.; Dhandapany, P.S.; Rani, D.S.; Tamang, R.; Bahl, A.; et al. Mitochondrial genome variations in idiopathic dilated cardiomyopathy. Mitochondrion 2019, 48, 51–59. [Google Scholar] [CrossRef]
- Long, P.A.; Evans, J.M.; Olson, T.M. Exome sequencing establishes diagnosis of Alström syndrome in an infant presenting with non-syndromic dilated cardiomyopathy. Am. J. Med. Genet. A 2015, 167a, 886–890. [Google Scholar] [CrossRef]
- Ziemann, M.; Wu, W.; Deng, X.L.; Du, X.J. Transcriptomic Analysis of Dysregulated Genes of the nDNA-mtDNA Axis in a Mouse Model of Dilated Cardiomyopathy. Front. Genet. 2022, 13, 921610. [Google Scholar] [CrossRef]
- Abaci, N.; Arıkan, M.; Tansel, T.; Sahin, N.; Cakiris, A.; Pacal, F.; Sırma Ekmekci, S.; Gök, E.; Üstek, D. Mitochondrial mutations in patients with congenital heart defects by next generation sequencing technology. Cardiol. Young 2015, 25, 705–711. [Google Scholar] [CrossRef]
- Ucar, Z.; Akbaba, T.H.; Aydinoglu, A.T.; Onder, S.C.; Balci-Peynircioglu, B.; Demircin, M.; Balci-Hayta, B. Mitochondrial Dysfunction in Cyanotic Congenital Heart Disease: A Promising Therapeutic Approach for the Future. Pediatr. Cardiol. 2022, 43, 1870–1878. [Google Scholar] [CrossRef]
- Hinton, R.B.; Ware, S.M. Heart Failure in Pediatric Patients with Congenital Heart Disease. Circ. Res. 2017, 120, 978–994. [Google Scholar] [CrossRef]
- Karamanlidis, G.; Bautista-Hernandez, V.; Fynn-Thompson, F.; Del Nido, P.; Tian, R. Impaired mitochondrial biogenesis precedes heart failure in right ventricular hypertrophy in congenital heart disease. Circ. Heart Fail. 2011, 4, 707–713. [Google Scholar] [CrossRef]
- Liu, X.; Yagi, H.; Saeed, S.; Bais, A.S.; Gabriel, G.C.; Chen, Z.; Peterson, K.A.; Li, Y.; Schwartz, M.C.; Reynolds, W.T.; et al. The complex genetics of hypoplastic left heart syndrome. Nat. Genet. 2017, 49, 1152–1159. [Google Scholar] [CrossRef]
- Willcox, J.A.L.; Geiger, J.T.; Morton, S.U.; McKean, D.; Quiat, D.; Gorham, J.M.; Tai, A.C.; DePalma, S.; Bernstein, D.; Brueckner, M.; et al. Neither cardiac mitochondrial DNA variation nor copy number contribute to congenital heart disease risk. Am. J. Hum. Genet. 2022, 109, 961–966. [Google Scholar] [CrossRef]
- Jia, Z.; Wang, X.; Qin, Y.; Xue, L.; Jiang, P.; Meng, Y.; Shi, S.; Wang, Y.; Qin Mo, J.; Guan, M.X. Coronary heart disease is associated with a mutation in mitochondrial tRNA. Hum. Mol. Genet. 2013, 22, 4064–4073. [Google Scholar] [CrossRef]
- Zhang, Z.; Liu, M.; He, J.; Zhang, X.; Chen, Y.; Li, H. Maternally inherited coronary heart disease is associated with a novel mitochondrial tRNA mutation. BMC Cardiovasc. Disord. 2019, 19, 293. [Google Scholar] [CrossRef]
- Figley, M.D.; Bieri, G.; Kolaitis, R.M.; Taylor, J.P.; Gitler, A.D. Profilin 1 associates with stress granules and ALS-linked mutations alter stress granule dynamics. J. Neurosci. 2014, 34, 8083–8097. [Google Scholar] [CrossRef]
- Paszek, E.; Zajdel, W.; Rajs, T.; Żmudka, K.; Legutko, J.; Kleczyński, P. Profilin 1 and Mitochondria-Partners in the Pathogenesis of Coronary Artery Disease? Int. J. Mol. Sci. 2021, 22, 1100. [Google Scholar] [CrossRef]
- Escobar, E. Hypertension and coronary heart disease. J. Hum. Hypertens. 2002, 16 (Suppl. S1), S61–S63. [Google Scholar] [CrossRef]
- Kumarasamy, S.; Gopalakrishnan, K.; Shafton, A.; Nixon, J.; Thangavel, J.; Farms, P.; Joe, B. Mitochondrial polymorphisms in rat genetic models of hypertension. Mamm. Genome 2010, 21, 299–306. [Google Scholar] [CrossRef] [PubMed]
- Robert, P.; Nguyen, P.M.C.; Richard, A.; Grenier, C.; Chevrollier, A.; Munier, M.; Grimaud, L.; Proux, C.; Champin, T.; Lelièvre, E.; et al. Protective role of the mitochondrial fusion protein OPA1 in hypertension. FASEB J. 2021, 35, e21678. [Google Scholar] [CrossRef] [PubMed]
- Xu, H.X.; Cui, S.M.; Zhang, Y.M.; Ren, J. Mitochondrial Ca2+ regulation in the etiology of heart failure: Physiological and pathophysiological implications. Acta Pharmacol. Sin. 2020, 41, 1301–1309. [Google Scholar] [CrossRef]
- Ding, Z.; Wang, X.; Liu, S.; Shahanawaz, J.; Theus, S.; Fan, Y.; Deng, X.; Zhou, S.; Mehta, J.L. PCSK9 expression in the ischaemic heart and its relationship to infarct size, cardiac function, and development of autophagy. Cardiovasc. Res. 2018, 114, 1738–1751. [Google Scholar] [CrossRef]
- Zhou, H.; Zhu, P.; Wang, J.; Zhu, H.; Ren, J.; Chen, Y. Pathogenesis of cardiac ischemia reperfusion injury is associated with CK2α-disturbed mitochondrial homeostasis via suppression of FUNDC1-related mitophagy. Cell Death Differ. 2018, 25, 1080–1093. [Google Scholar] [CrossRef]
- Huang, G.; Lu, X.; Duan, Z.; Zhang, K.; Xu, L.; Bao, H.; Xiong, X.; Lin, M.; Li, C.; Li, Y.; et al. PCSK9 Knockdown Can Improve Myocardial Ischemia/Reperfusion Injury by Inhibiting Autophagy. Cardiovasc. Toxicol. 2022, 22, 951–961. [Google Scholar] [CrossRef]
- Li, Y.; Chen, B.; Yang, X.; Zhang, C.; Jiao, Y.; Li, P.; Liu, Y.; Li, Z.; Qiao, B.; Bond Lau, W.; et al. S100a8/a9 Signaling Causes Mitochondrial Dysfunction and Cardiomyocyte Death in Response to Ischemic/Reperfusion Injury. Circulation 2019, 140, 751–764. [Google Scholar] [CrossRef]
- Zhou, B.; Tian, R. Mitochondrial dysfunction in pathophysiology of heart failure. J. Clin. Investig. 2018, 128, 3716–3726. [Google Scholar] [CrossRef]
- Butts, B.; Gary, R.A.; Dunbar, S.B.; Butler, J. The Importance of NLRP3 Inflammasome in Heart Failure. J. Card. Fail. 2015, 21, 586–593. [Google Scholar] [CrossRef]
- Deng, Y.; Xie, M.; Li, Q.; Xu, X.; Ou, W.; Zhang, Y.; Xiao, H.; Yu, H.; Zheng, Y.; Liang, Y.; et al. Targeting Mitochondria-Inflammation Circuit by β-Hydroxybutyrate Mitigates HFpEF. Circ. Res. 2021, 128, 232–245. [Google Scholar] [CrossRef]
- Sheeran, F.L.; Pepe, S. Posttranslational modifications and dysfunction of mitochondrial enzymes in human heart failure. Am. J. Physiol. Endocrinol. Metab. 2016, 311, E449–E460. [Google Scholar] [CrossRef] [PubMed]
- Qi, B.; He, L.; Zhao, Y.; Zhang, L.; He, Y.; Li, J.; Li, C.; Zhang, B.; Huang, Q.; Xing, J.; et al. Akap1 deficiency exacerbates diabetic cardiomyopathy in mice by NDUFS1-mediated mitochondrial dysfunction and apoptosis. Diabetologia 2020, 63, 1072–1087. [Google Scholar] [CrossRef]
- Zhuang, L.; Jia, K.; Chen, C.; Li, Z.; Zhao, J.; Hu, J.; Zhang, H.; Fan, Q.; Huang, C.; Xie, H.; et al. DYRK1B-STAT3 Drives Cardiac Hypertrophy and Heart Failure by Impairing Mitochondrial Bioenergetics. Circulation 2022, 145, 829–846. [Google Scholar] [CrossRef] [PubMed]
- Tang, X.; Wang, Z.; Hu, S.; Zhou, B. Assessing Drug-Induced Mitochondrial Toxicity in Cardiomyocytes: Implications for Preclinical Cardiac Safety Evaluation. Pharmaceutics 2022, 14, 1313. [Google Scholar] [CrossRef] [PubMed]
- Brandão, S.R.; Reis-Mendes, A.; Domingues, P.; Duarte, J.A.; Bastos, M.L.; Carvalho, F.; Ferreira, R.; Costa, V.M. Exploring the aging effect of the anticancer drugs doxorubicin and mitoxantrone on cardiac mitochondrial proteome using a murine model. Toxicology 2021, 459, 152852. [Google Scholar] [CrossRef]
- Mamoshina, P.; Rodriguez, B.; Bueno-Orovio, A. Toward a broader view of mechanisms of drug cardiotoxicity. Cell Rep. Med. 2021, 2, 100216. [Google Scholar] [CrossRef]
- Huang, J.; Wu, R.; Chen, L.; Yang, Z.; Yan, D.; Li, M. Understanding Anthracycline Cardiotoxicity from Mitochondrial Aspect. Front. Pharmacol. 2022, 13, 811406. [Google Scholar] [CrossRef]
- Zamorano, J.L.; Lancellotti, P.; Rodriguez Muñoz, D.; Aboyans, V.; Asteggiano, R.; Galderisi, M.; Habib, G.; Lenihan, D.J.; Lip, G.Y.H.; Lyon, A.R.; et al. 2016 ESC Position Paper on cancer treatments and cardiovascular toxicity developed under the auspices of the ESC Committee for Practice Guidelines: The Task Force for cancer treatments and cardiovascular toxicity of the European Society of Cardiology (ESC). Eur. Heart J. 2016, 37, 2768–2801. [Google Scholar] [CrossRef]
- Varricchi, G.; Ameri, P.; Cadeddu, C.; Ghigo, A.; Madonna, R.; Marone, G.; Mercurio, V.; Monte, I.; Novo, G.; Parrella, P.; et al. Antineoplastic Drug-Induced Cardiotoxicity: A Redox Perspective. Front. Physiol. 2018, 9, 167. [Google Scholar] [CrossRef]
- Babaei, H.; Razmaraii, N.; Assadnassab, G.; Mohajjel Nayebi, A.; Azarmi, Y.; Mohammadnejad, D.; Azami, A. Ultrastructural and Echocardiographic Assessment of Chronic Doxorubicin-Induced Cardiotoxicity in Rats. Arch. Razi Inst. 2020, 75, 55–62. [Google Scholar] [CrossRef]
- Vineetha, V.P.; Soumya, R.S.; Raghu, K.G. Phloretin ameliorates arsenic trioxide induced mitochondrial dysfunction in H9c2 cardiomyoblasts mediated via alterations in membrane permeability and ETC complexes. Eur. J. Pharmacol. 2015, 754, 162–172. [Google Scholar] [CrossRef]
- Salimi, A.; Neshat, M.R.; Naserzadeh, P.; Pourahmad, J. Mitochondrial Permeability Transition Pore Sealing Agents and Antioxidants Protect Oxidative Stress and Mitochondrial Dysfunction Induced by Naproxen, Diclofenac and Celecoxib. Drug Res. 2019, 69, 598–605. [Google Scholar] [CrossRef] [PubMed]
- Atashbar, S.; Jamali, Z.; Khezri, S.; Salimi, A. Celecoxib decreases mitochondrial complex IV activity and induces oxidative stress in isolated rat heart mitochondria: An analysis for its cardiotoxic adverse effect. J. Biochem. Mol. Toxicol. 2022, 36, e22934. [Google Scholar] [CrossRef] [PubMed]
- Wu, C.S.; Tsai, Y.T.; Tsai, H.J. Antipsychotic drugs and the risk of ventricular arrhythmia and/or sudden cardiac death: A nation-wide case-crossover study. J. Am. Heart Assoc. 2015, 4, e001568. [Google Scholar] [CrossRef] [PubMed]
- Anglin, R.; Rosebush, P.; Mazurek, M. Psychotropic medications and mitochondrial toxicity. Nat. Rev. Neurosci. 2012, 13, 650. [Google Scholar] [CrossRef]
- Cikánková, T.; Fišar, Z.; Bakhouche, Y.; Ľupták, M.; Hroudová, J. In vitro effects of antipsychotics on mitochondrial respiration. Naunyn-Schmiedeberg’s Arch. Pharmacol. 2019, 392, 1209–1223. [Google Scholar] [CrossRef]
- Beauchemin, M.; Geguchadze, R.; Guntur, A.R.; Nevola, K.; Le, P.T.; Barlow, D.; Rue, M.; Vary, C.P.H.; Lary, C.W.; Motyl, K.J.; et al. Exploring mechanisms of increased cardiovascular disease risk with antipsychotic medications: Risperidone alters the cardiac proteomic signature in mice. Pharmacol. Res. 2020, 152, 104589. [Google Scholar] [CrossRef]
- Edinoff, A.N.; Ellis, E.D.; Nussdorf, L.M.; Hill, T.W.; Cornett, E.M.; Kaye, A.M.; Kaye, A.D. Antipsychotic Polypharmacy-Related Cardiovascular Morbidity and Mortality: A Comprehensive Review. Neurol. Int. 2022, 14, 294–309. [Google Scholar] [CrossRef]
- Finsterer, J.; Zarrouk-Mahjoub, S. Mitochondrial toxicity of cardiac drugs and its relevance to mitochondrial disorders. Expert Opin. Drug Metab. Toxicol. 2015, 11, 15–24. [Google Scholar] [CrossRef]
- Daiber, A.; Münzel, T. Organic Nitrate Therapy, Nitrate Tolerance, and Nitrate-Induced Endothelial Dysfunction: Emphasis on Redox Biology and Oxidative Stress. Antioxid. Redox Signal. 2015, 23, 899–942. [Google Scholar] [CrossRef]
- Münzel, T. Recent findings on nitrates: Their action, bioactivation and development of tolerance. Dtsch. Med. Wochenschr. 2008, 133, 2277–2282. [Google Scholar] [CrossRef]
- Agarwal, A.K.; Rao, S.S. Effect of quinidine on kidney biochemistry and function in male Sprague-Dawley rats. Food Chem. Toxicol. 1995, 33, 203–207. [Google Scholar] [CrossRef] [PubMed]
- Bachmann, E.; Weber, E.; Zbinden, G. Biochemical mechanisms of quinidine cardiotoxicity. J. Cardiovasc. Pharmacol. 1986, 8, 826–831. [Google Scholar] [CrossRef] [PubMed]
- Kawasaki, C.; Kawasaki, T.; Ogata, M.; Sata, T.; Chaudry, I.H. Lidocaine enhances apoptosis and suppresses mitochondrial functions of human neutrophil in vitro. J. Trauma 2010, 68, 401–408. [Google Scholar] [CrossRef] [PubMed]
- Serviddio, G.; Bellanti, F.; Giudetti, A.M.; Gnoni, G.V.; Capitanio, N.; Tamborra, R.; Romano, A.D.; Quinto, M.; Blonda, M.; Vendemiale, G.; et al. Mitochondrial oxidative stress and respiratory chain dysfunction account for liver toxicity during amiodarone but not dronedarone administration. Free Radic. Biol. Med. 2011, 51, 2234–2242. [Google Scholar] [CrossRef] [PubMed]
- Salabei, J.K.; Balakumaran, A.; Frey, J.C.; Boor, P.J.; Treinen-Moslen, M.; Conklin, D.J. Verapamil stereoisomers induce antiproliferative effects in vascular smooth muscle cells via autophagy. Toxicol. Appl. Pharmacol. 2012, 262, 265–272. [Google Scholar] [CrossRef] [PubMed]
- Haeusler, I.L.; Chan, X.H.S.; Guérin, P.J.; White, N.J. The arrhythmogenic cardiotoxicity of the quinoline and structurally related antimalarial drugs: A systematic review. BMC Med. 2018, 16, 200. [Google Scholar] [CrossRef]
- Connolly, S.J. Evidence-based analysis of amiodarone efficacy and safety. Circulation 1999, 100, 2025–2034. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Li, X.; Liu, S.; Brickell, A.N.; Zhang, J.; Wu, Z.; Zhou, S.; Ding, Z. PCSK9 regulates pyroptosis via mtDNA damage in chronic myocardial ischemia. Basic Res. Cardiol. 2020, 115, 66. [Google Scholar] [CrossRef]
- Brown, D.A.; Perry, J.B.; Allen, M.E.; Sabbah, H.N.; Stauffer, B.L.; Shaikh, S.R.; Cleland, J.G.; Colucci, W.S.; Butler, J.; Voors, A.A.; et al. Expert consensus document: Mitochondrial function as a therapeutic target in heart failure. Nat. Rev. Cardiol. 2017, 14, 238–250. [Google Scholar] [CrossRef]
- Andreux, P.A.; Houtkooper, R.H.; Auwerx, J. Pharmacological approaches to restore mitochondrial function. Nat. Rev. Drug Discov. 2013, 12, 465–483. [Google Scholar] [CrossRef] [PubMed]
- Kang, E.; Wu, J.; Gutierrez, N.M.; Koski, A.; Tippner-Hedges, R.; Agaronyan, K.; Platero-Luengo, A.; Martinez-Redondo, P.; Ma, H.; Lee, Y.; et al. Mitochondrial replacement in human oocytes carrying pathogenic mitochondrial DNA mutations. Nature 2016, 540, 270–275. [Google Scholar] [CrossRef] [PubMed]
- Xu, J.; Du, W.; Zhao, Y.; Lim, K.; Lu, L.; Zhang, C.; Li, L. Mitochondria targeting drugs for neurodegenerative diseases-Design, mechanism and application. Acta Pharm. Sin. B 2022, 12, 2778–2789. [Google Scholar] [CrossRef] [PubMed]
- Birk, A.V.; Chao, W.M.; Bracken, C.; Warren, J.D.; Szeto, H.H. Targeting mitochondrial cardiolipin and the cytochrome c/cardiolipin complex to promote electron transport and optimize mitochondrial ATP synthesis. Br. J. Pharmacol. 2014, 171, 2017–2028. [Google Scholar] [CrossRef]
- Dai, W.; Shi, J.; Gupta, R.C.; Sabbah, H.N.; Hale, S.L.; Kloner, R.A. Bendavia, a mitochondria-targeting peptide, improves postinfarction cardiac function, prevents adverse left ventricular remodeling, and restores mitochondria-related gene expression in rats. J. Cardiovasc. Pharmacol. 2014, 64, 543–553. [Google Scholar] [CrossRef]
- Sabbah, H.N.; Gupta, R.C.; Kohli, S.; Wang, M.; Hachem, S.; Zhang, K. Chronic Therapy with Elamipretide (MTP-131), a Novel Mitochondria-Targeting Peptide, Improves Left Ventricular and Mitochondrial Function in Dogs With Advanced Heart Failure. Circ. Heart Fail. 2016, 9, e002206. [Google Scholar] [CrossRef]
- Obi, C.; Smith, A.T.; Hughes, G.J.; Adeboye, A.A. Targeting mitochondrial dysfunction with elamipretide. Heart Fail. Rev. 2022, 27, 1925–1932. [Google Scholar] [CrossRef]
- Chatfield, K.C.; Sparagna, G.C.; Chau, S.; Phillips, E.K.; Ambardekar, A.V.; Aftab, M.; Mitchell, M.B.; Sucharov, C.C.; Miyamoto, S.D.; Stauffer, B.L. Elamipretide Improves Mitochondrial Function in the Failing Human Heart. JACC Basic Transl. Sci. 2019, 4, 147–157. [Google Scholar] [CrossRef]
- Daubert, M.A.; Yow, E.; Dunn, G.; Marchev, S.; Barnhart, H.; Douglas, P.S.; O’Connor, C.; Goldstein, S.; Udelson, J.E.; Sabbah, H.N. Novel Mitochondria-Targeting Peptide in Heart Failure Treatment: A Randomized, Placebo-Controlled Trial of Elamipretide. Circ. Heart Fail. 2017, 10, e004389. [Google Scholar] [CrossRef]
- Reid Thompson, W.; Hornby, B.; Manuel, R.; Bradley, E.; Laux, J.; Carr, J.; Vernon, H.J. A phase 2/3 randomized clinical trial followed by an open-label extension to evaluate the effectiveness of elamipretide in Barth syndrome, a genetic disorder of mitochondrial cardiolipin metabolism. Genet. Med. 2021, 23, 471–478. [Google Scholar] [CrossRef]
- El-Mir, M.Y.; Nogueira, V.; Fontaine, E.; Avéret, N.; Rigoulet, M.; Leverve, X. Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I. J. Biol. Chem. 2000, 275, 223–228. [Google Scholar] [CrossRef] [PubMed]
- Owen, M.R.; Doran, E.; Halestrap, A.P. Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain. Biochem. J. 2000, 348 Pt 3, 607–614. [Google Scholar] [CrossRef] [PubMed]
- Ma, T.; Tian, X.; Zhang, B.; Li, M.; Wang, Y.; Yang, C.; Wu, J.; Wei, X.; Qu, Q.; Yu, Y.; et al. Low-dose metformin targets the lysosomal AMPK pathway through PEN2. Nature 2022, 603, 159–165. [Google Scholar] [CrossRef] [PubMed]
- Sardu, C.; Paolisso, P.; Sacra, C.; Mauro, C.; Minicucci, F.; Portoghese, M.; Rizzo, M.R.; Barbieri, M.; Sasso, F.C.; D’Onofrio, N.; et al. Effects of Metformin Therapy on Coronary Endothelial Dysfunction in Patients with Prediabetes with Stable Angina and Nonobstructive Coronary Artery Stenosis: The CODYCE Multicenter Prospective Study. Diabetes Care 2019, 42, 1946–1955. [Google Scholar] [CrossRef]
- Ong, S.B.; Dongworth, R.K.; Cabrera-Fuentes, H.A.; Hausenloy, D.J. Role of the MPTP in conditioning the heart—Translatability and mechanism. Br. J. Pharmacol. 2015, 172, 2074–2084. [Google Scholar] [CrossRef]
- Protti, A.; Lecchi, A.; Fortunato, F.; Artoni, A.; Greppi, N.; Vecchio, S.; Fagiolari, G.; Moggio, M.; Comi, G.P.; Mistraletti, G.; et al. Metformin overdose causes platelet mitochondrial dysfunction in humans. Crit. Care 2012, 16, R180. [Google Scholar] [CrossRef]
- Stewart, S.; Lesnefsky, E.J.; Chen, Q. Reversible blockade of electron transport with amobarbital at the onset of reperfusion attenuates cardiac injury. Transl. Res. 2009, 153, 224–231. [Google Scholar] [CrossRef]
- Aldakkak, M.; Stowe, D.F.; Chen, Q.; Lesnefsky, E.J.; Camara, A.K. Inhibited mitochondrial respiration by amobarbital during cardiac ischaemia improves redox state and reduces matrix Ca2+ overload and ROS release. Cardiovasc. Res. 2008, 77, 406–415. [Google Scholar] [CrossRef]
- Detaille, D.; Pasdois, P.; Sémont, A.; Dos Santos, P.; Diolez, P. An old medicine as a new drug to prevent mitochondrial complex I from producing oxygen radicals. PLoS ONE 2019, 14, e0216385. [Google Scholar] [CrossRef]
- Dai, W.; Amoedo, N.D.; Perry, J.; Le Grand, B.; Boucard, A.; Carreno, J.; Zhao, L.; Brown, D.A.; Rossignol, R.; Kloner, R.A. Effects of OP2113 on Myocardial Infarct Size and No Reflow in a Rat Myocardial Ischemia/Reperfusion Model. Cardiovasc. Drugs Ther. 2022, 36, 217–227. [Google Scholar] [CrossRef]
- Rustin, P.; Rötig, A.; Munnich, A.; Sidi, D. Heart hypertrophy and function are improved by idebenone in Friedreich’s ataxia. Free Radic. Res. 2002, 36, 467–469. [Google Scholar] [CrossRef] [PubMed]
- Kearney, M.; Orrell, R.W.; Fahey, M.; Brassington, R.; Pandolfo, M. Pharmacological treatments for Friedreich ataxia. Cochrane Database Syst. Rev. 2016, 2016, Cd007791. [Google Scholar] [CrossRef] [PubMed]
- Perry, J.B.; Davis, G.N.; Allen, M.E.; Makrecka-Kuka, M.; Dambrova, M.; Grange, R.W.; Shaikh, S.R.; Brown, D.A. Cardioprotective effects of idebenone do not involve ROS scavenging: Evidence for mitochondrial complex I bypass in ischemia/reperfusion injury. J Mol. Cell. Cardiol. 2019, 135, 160–171. [Google Scholar] [CrossRef] [PubMed]
- Li, D.; Zhang, G.; Wang, Z.; Guo, J.; Liu, Y.; Lu, Y.; Qin, Z.; Xu, Y.; Cao, C.; Wang, B.; et al. Idebenone attenuates ferroptosis by inhibiting excessive autophagy via the ROS-AMPK-mTOR pathway to preserve cardiac function after myocardial infarction. Eur. J. Pharmacol. 2023, 943, 175569. [Google Scholar] [CrossRef] [PubMed]
- Pereira, G.C.; Silva, A.M.; Diogo, C.V.; Carvalho, F.S.; Monteiro, P.; Oliveira, P.J. Drug-induced cardiac mitochondrial toxicity and protection: From doxorubicin to carvedilol. Curr. Pharm. Des. 2011, 17, 2113–2129. [Google Scholar] [CrossRef]
- Avila, M.S.; Ayub-Ferreira, S.M.; de Barros Wanderley, M.R., Jr.; das Dores Cruz, F.; Gonçalves Brandão, S.M.; Rigaud, V.O.C.; Higuchi-Dos-Santos, M.H.; Hajjar, L.A.; Kalil Filho, R.; Hoff, P.M.; et al. Carvedilol for Prevention of Chemotherapy-Related Cardiotoxicity: The CECCY Trial. J. Am. Coll. Cardiol. 2018, 71, 2281–2290. [Google Scholar] [CrossRef]
- Forrester, M.B. Pediatric carvedilol ingestions reported to Texas poison centers, 2000 to 2008. Pediatr. Emerg. Care 2010, 26, 730–732. [Google Scholar] [CrossRef]
- Xun, Z.; Rivera-Sánchez, S.; Ayala-Peña, S.; Lim, J.; Budworth, H.; Skoda, E.M.; Robbins, P.D.; Niedernhofer, L.J.; Wipf, P.; McMurray, C.T. Targeting of XJB-5-131 to mitochondria suppresses oxidative DNA damage and motor decline in a mouse model of Huntington’s disease. Cell Rep. 2012, 2, 1137–1142. [Google Scholar] [CrossRef]
- Trnka, J.; Blaikie, F.H.; Smith, R.A.; Murphy, M.P. A mitochondria-targeted nitroxide is reduced to its hydroxylamine by ubiquinol in mitochondria. Free Radic. Biol. Med. 2008, 44, 1406–1419. [Google Scholar] [CrossRef]
- Trnka, J.; Blaikie, F.H.; Logan, A.; Smith, R.A.; Murphy, M.P. Antioxidant properties of MitoTEMPOL and its hydroxylamine. Free Radic. Res. 2009, 43, 4–12. [Google Scholar] [CrossRef]
- Dickey, J.S.; Gonzalez, Y.; Aryal, B.; Mog, S.; Nakamura, A.J.; Redon, C.E.; Baxa, U.; Rosen, E.; Cheng, G.; Zielonka, J.; et al. Mito-tempol and dexrazoxane exhibit cardioprotective and chemotherapeutic effects through specific protein oxidation and autophagy in a syngeneic breast tumor preclinical model. PLoS ONE 2013, 8, e70575. [Google Scholar] [CrossRef] [PubMed]
- Silva, F.S.; Simoes, R.F.; Couto, R.; Oliveira, P.J. Targeting Mitochondria in Cardiovascular Diseases. Curr. Pharm. Des. 2016, 22, 5698–5717. [Google Scholar] [CrossRef]
- Zhang, Q.; Cai, S.; Guo, L.; Zhao, G. Propofol induces mitochondrial-associated protein LRPPRC and protects mitochondria against hypoxia in cardiac cells. PLoS ONE 2020, 15, e0238857. [Google Scholar] [CrossRef]
- Lucas, A.M.; Caldas, F.R.; da Silva, A.P.; Ventura, M.M.; Leite, I.M.; Filgueiras, A.B.; Silva, C.G.; Kowaltowski, A.J.; Facundo, H.T. Diazoxide prevents reactive oxygen species and mitochondrial damage, leading to anti-hypertrophic effects. Chem. Biol. Interact. 2017, 261, 50–55. [Google Scholar] [CrossRef] [PubMed]
- Deja, M.A.; Malinowski, M.; Gołba, K.S.; Kajor, M.; Lebda-Wyborny, T.; Hudziak, D.; Domaradzki, W.; Szurlej, D.; Bończyk, A.; Biernat, J.; et al. Diazoxide protects myocardial mitochondria, metabolism, and function during cardiac surgery: A double-blind randomized feasibility study of diazoxide-supplemented cardioplegia. J. Thorac. Cardiovasc. Surg. 2009, 137, 997–1004, 1004e1001-1002. [Google Scholar] [CrossRef] [PubMed]
- Naryzhnaya, N.V.; Maslov, L.N.; Oeltgen, P.R. Pharmacology of mitochondrial permeability transition pore inhibitors. Drug Dev. Res. 2019, 80, 1013–1030. [Google Scholar] [CrossRef] [PubMed]
- Cung, T.T.; Morel, O.; Cayla, G.; Rioufol, G.; Garcia-Dorado, D.; Angoulvant, D.; Bonnefoy-Cudraz, E.; Guérin, P.; Elbaz, M.; Delarche, N.; et al. Cyclosporine before PCI in Patients with Acute Myocardial Infarction. N. Engl. J. Med. 2015, 373, 1021–1031. [Google Scholar] [CrossRef]
- Panel, M.; Ahmed-Belkacem, A.; Ruiz, I.; Guichou, J.F.; Pawlotsky, J.M.; Ghaleh, B.; Morin, D. A Phenyl-Pyrrolidine Derivative Reveals a Dual Inhibition Mechanism of Myocardial Mitochondrial Permeability Transition Pore, Which Is Limited by Its Myocardial Distribution. J. Pharmacol. Exp. Ther. 2021, 376, 348–357. [Google Scholar] [CrossRef]
- Schaller, S.; Paradis, S.; Ngoh, G.A.; Assaly, R.; Buisson, B.; Drouot, C.; Ostuni, M.A.; Lacapere, J.J.; Bassissi, F.; Bordet, T.; et al. TRO40303, a new cardioprotective compound, inhibits mitochondrial permeability transition. J. Pharmacol. Exp. Ther. 2010, 333, 696–706. [Google Scholar] [CrossRef]
- Schaller, S.; Michaud, M.; Latyszenok, V.; Robert, F.; Hocine, M.; Arnoux, T.; Gabriac, M.; Codoul, H.; Bourhane, A.; de Bellefois, I.C.; et al. TRO40303, a mitochondrial-targeted cytoprotective compound, provides protection in hepatitis models. Pharmacol. Res. Perspect 2015, 3, e00144. [Google Scholar] [CrossRef]
- Le Lamer, S.; Paradis, S.; Rahmouni, H.; Chaimbault, C.; Michaud, M.; Culcasi, M.; Afxantidis, J.; Latreille, M.; Berna, P.; Berdeaux, A.; et al. Translation of TRO40303 from myocardial infarction models to demonstration of safety and tolerance in a randomized Phase I trial. J. Transl. Med. 2014, 12, 38. [Google Scholar] [CrossRef] [PubMed]
- Aldakkak, M.; Camara, A.K.; Heisner, J.S.; Yang, M.; Stowe, D.F. Ranolazine reduces Ca2+ overload and oxidative stress and improves mitochondrial integrity to protect against ischemia reperfusion injury in isolated hearts. Pharmacol. Res. 2011, 64, 381–392. [Google Scholar] [CrossRef] [PubMed]
- Aung, L.H.H.; Jumbo, J.C.C.; Wang, Y.; Li, P. Therapeutic potential and recent advances on targeting mitochondrial dynamics in cardiac hypertrophy: A concise review. Mol. Ther. Nucleic Acids 2021, 25, 416–443. [Google Scholar] [CrossRef] [PubMed]
- Archer, S.L. Mitochondrial dynamics--mitochondrial fission and fusion in human diseases. N. Engl. J. Med. 2013, 369, 2236–2251. [Google Scholar] [CrossRef] [PubMed]
- Quiles, J.M.; Gustafsson, Å.B. The role of mitochondrial fission in cardiovascular health and disease. Nat. Rev. Cardiol. 2022, 19, 723–736. [Google Scholar] [CrossRef] [PubMed]
- Ong, S.B.; Subrayan, S.; Lim, S.Y.; Yellon, D.M.; Davidson, S.M.; Hausenloy, D.J. Inhibiting mitochondrial fission protects the heart against ischemia/reperfusion injury. Circulation 2010, 121, 2012–2022. [Google Scholar] [CrossRef]
- Gao, D.; Zhang, L.; Dhillon, R.; Hong, T.T.; Shaw, R.M.; Zhu, J. Dynasore protects mitochondria and improves cardiac lusitropy in Langendorff perfused mouse heart. PLoS ONE 2013, 8, e60967. [Google Scholar] [CrossRef]
- Yu, H.Y.; Guo, Y.H.; Gao, W. Mitochondrial fusion protein Mfn2 and cardiovascular diseases. Sheng Li Ke Xue Jin Zhan 2010, 41, 11–16. [Google Scholar]
- Szabo, A.; Sumegi, K.; Fekete, K.; Hocsak, E.; Debreceni, B.; Setalo, G., Jr.; Kovacs, K.; Deres, L.; Kengyel, A.; Kovacs, D.; et al. Activation of mitochondrial fusion provides a new treatment for mitochondria-related diseases. Biochem. Pharmacol. 2018, 150, 86–96. [Google Scholar] [CrossRef]
- Ferreira, J.C.B.; Campos, J.C.; Qvit, N.; Qi, X.; Bozi, L.H.M.; Bechara, L.R.G.; Lima, V.M.; Queliconi, B.B.; Disatnik, M.H.; Dourado, P.M.M.; et al. A selective inhibitor of mitofusin 1-βIIPKC association improves heart failure outcome in rats. Nat. Commun. 2019, 10, 329. [Google Scholar] [CrossRef]
- Shu, H.; Hang, W.; Peng, Y.; Nie, J.; Wu, L.; Zhang, W.; Wang, D.W.; Zhou, N. Trimetazidine Attenuates Heart Failure by Improving Myocardial Metabolism via AMPK. Front. Pharmacol. 2021, 12, 707399. [Google Scholar] [CrossRef] [PubMed]
- Bacman, S.R.; Kauppila, J.H.K.; Pereira, C.V.; Nissanka, N.; Miranda, M.; Pinto, M.; Williams, S.L.; Larsson, N.G.; Stewart, J.B.; Moraes, C.T. MitoTALEN reduces mutant mtDNA load and restores tRNA(Ala) levels in a mouse model of heteroplasmic mtDNA mutation. Nat. Med. 2018, 24, 1696–1700. [Google Scholar] [CrossRef]
- Gammage, P.A.; Viscomi, C.; Simard, M.L.; Costa, A.S.H.; Gaude, E.; Powell, C.A.; Van Haute, L.; McCann, B.J.; Rebelo-Guiomar, P.; Cerutti, R.; et al. Genome editing in mitochondria corrects a pathogenic mtDNA mutation in vivo. Nat. Med. 2018, 24, 1691–1695. [Google Scholar] [CrossRef]
- Jo, A.; Ham, S.; Lee, G.H.; Lee, Y.I.; Kim, S.; Lee, Y.S.; Shin, J.H.; Lee, Y. Efficient Mitochondrial Genome Editing by CRISPR/Cas9. BioMed Res. Int. 2015, 2015, 305716. [Google Scholar] [CrossRef] [PubMed]
- Manfredi, G.; Fu, J.; Ojaimi, J.; Sadlock, J.E.; Kwong, J.Q.; Guy, J.; Schon, E.A. Rescue of a deficiency in ATP synthesis by transfer of MTATP6, a mitochondrial DNA-encoded gene, to the nucleus. Nat. Genet. 2002, 30, 394–399. [Google Scholar] [CrossRef] [PubMed]
- Lavie, J.; Serrat, R.; Bellance, N.; Courtand, G.; Dupuy, J.W.; Tesson, C.; Coupry, I.; Brice, A.; Lacombe, D.; Durr, A.; et al. Mitochondrial morphology and cellular distribution are altered in SPG31 patients and are linked to DRP1 hyperphosphorylation. Hum. Mol. Genet. 2017, 26, 674–685. [Google Scholar] [CrossRef]
- Aryamvally, A.; Myers, M.F.; Huang, T.; Slone, J.; Pilipenko, V.; Hartmann, J.E. Mitochondrial replacement therapy: Genetic counselors’ experiences, knowledge, and opinions. J. Genet. Couns. 2021, 30, 828–837. [Google Scholar] [CrossRef]
- Tachibana, M.; Sparman, M.; Sritanaudomchai, H.; Ma, H.; Clepper, L.; Woodward, J.; Li, Y.; Ramsey, C.; Kolotushkina, O.; Mitalipov, S. Mitochondrial gene replacement in primate offspring and embryonic stem cells. Nature 2009, 461, 367–372. [Google Scholar] [CrossRef]
- Sharma, H.; Singh, D.; Mahant, A.; Sohal, S.K.; Kesavan, A.K.; Samiksha. Development of mitochondrial replacement therapy: A review. Heliyon 2020, 6, e04643. [Google Scholar] [CrossRef]
- Guariento, A.; Blitzer, D.; Doulamis, I.; Shin, B.; Moskowitzova, K.; Orfany, A.; Ramirez-Barbieri, G.; Staffa, S.J.; Zurakowski, D.; Del Nido, P.J.; et al. Preischemic autologous mitochondrial transplantation by intracoronary injection for myocardial protection. J. Thorac. Cardiovasc. Surg. 2020, 160, e15–e29. [Google Scholar] [CrossRef]
- Kaza, A.K.; Wamala, I.; Friehs, I.; Kuebler, J.D.; Rathod, R.H.; Berra, I.; Ericsson, M.; Yao, R.; Thedsanamoorthy, J.K.; Zurakowski, D.; et al. Myocardial rescue with autologous mitochondrial transplantation in a porcine model of ischemia/reperfusion. J. Thorac. Cardiovasc. Surg. 2017, 153, 934–943. [Google Scholar] [CrossRef] [PubMed]
- Wilkins, H.M.; Carl, S.M.; Swerdlow, R.H. Cytoplasmic hybrid (cybrid) cell lines as a practical model for mitochondriopathies. Redox Biol. 2014, 2, 619–631. [Google Scholar] [CrossRef] [PubMed]
- Lee, S.E.; Kang, Y.C.; Kim, Y.; Kim, S.; Yu, S.H.; Park, J.H.; Kim, I.H.; Kim, H.Y.; Han, K.; Lee, H.K.; et al. Preferred Migration of Mitochondria toward Cells and Tissues with Mitochondrial Damage. Int. J. Mol. Sci. 2022, 23, 15734. [Google Scholar] [CrossRef] [PubMed]
- Shin, B.; Saeed, M.Y.; Esch, J.J.; Guariento, A.; Blitzer, D.; Moskowitzova, K.; Ramirez-Barbieri, G.; Orfany, A.; Thedsanamoorthy, J.K.; Cowan, D.B.; et al. A Novel Biological Strategy for Myocardial Protection by Intracoronary Delivery of Mitochondria: Safety and Efficacy. JACC Basic Transl. Sci. 2019, 4, 871–888. [Google Scholar] [CrossRef]
- Masuzawa, A.; Black, K.M.; Pacak, C.A.; Ericsson, M.; Barnett, R.J.; Drumm, C.; Seth, P.; Bloch, D.B.; Levitsky, S.; Cowan, D.B.; et al. Transplantation of autologously derived mitochondria protects the heart from ischemia-reperfusion injury. Am J. Physiol. Heart Circ. Physiol. 2013, 304, H966–H982. [Google Scholar] [CrossRef]
- Blitzer, D.; Guariento, A.; Doulamis, I.P.; Shin, B.; Moskowitzova, K.; Barbieri, G.R.; Orfany, A.; Del Nido, P.J.; McCully, J.D. Delayed Transplantation of Autologous Mitochondria for Cardioprotection in a Porcine Model. Ann. Thorac. Surg. 2020, 109, 711–719. [Google Scholar] [CrossRef]
- Emani, S.M.; Piekarski, B.L.; Harrild, D.; Del Nido, P.J.; McCully, J.D. Autologous mitochondrial transplantation for dysfunction after ischemia-reperfusion injury. J. Thorac. Cardiovasc. Surg. 2017, 154, 286–289. [Google Scholar] [CrossRef]
- Ramalingam, A.; Budin, S.B.; Mohd Fauzi, N.; Ritchie, R.H.; Zainalabidin, S. Targeting mitochondrial reactive oxygen species-mediated oxidative stress attenuates nicotine-induced cardiac remodeling and dysfunction. Sci. Rep. 2021, 11, 13845. [Google Scholar] [CrossRef]
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Huang, Y.; Zhou, B. Mitochondrial Dysfunction in Cardiac Diseases and Therapeutic Strategies. Biomedicines 2023, 11, 1500. https://doi.org/10.3390/biomedicines11051500
Huang Y, Zhou B. Mitochondrial Dysfunction in Cardiac Diseases and Therapeutic Strategies. Biomedicines. 2023; 11(5):1500. https://doi.org/10.3390/biomedicines11051500
Chicago/Turabian StyleHuang, Yafei, and Bingying Zhou. 2023. "Mitochondrial Dysfunction in Cardiac Diseases and Therapeutic Strategies" Biomedicines 11, no. 5: 1500. https://doi.org/10.3390/biomedicines11051500
APA StyleHuang, Y., & Zhou, B. (2023). Mitochondrial Dysfunction in Cardiac Diseases and Therapeutic Strategies. Biomedicines, 11(5), 1500. https://doi.org/10.3390/biomedicines11051500