Startseite The therapeutic potential of mitochondrial transplantation for the treatment of neurodegenerative disorders
Artikel
Lizenziert
Nicht lizenziert Erfordert eine Authentifizierung

The therapeutic potential of mitochondrial transplantation for the treatment of neurodegenerative disorders

  • César Espino De la Fuente-Muñoz und Clorinda Arias EMAIL logo
Veröffentlicht/Copyright: 7. Dezember 2020
Veröffentlichen auch Sie bei De Gruyter Brill

Abstract

Mitochondrial activity is essential to support neural functions, and changes in the integrity and activity of the mitochondria can contribute to synaptic damage and neuronal death, especially in degenerative diseases associated with age, such as Alzheimer’s and Parkinson’s disease. Currently, different approaches are used to treat these conditions, and one strategy under research is mitochondrial transplantation. For years, mitochondria have been shown to be transferred between cells of different tissues. This process has allowed several attempts to develop transplantation schemes by isolating functional mitochondria and introducing them into damaged tissue in particular to counteract the harmful effects of myocardial ischemia. Recently, mitochondrial transfer between brain cells has also been reported, and thus, mitochondrial transplantation for disorders of the nervous system has begun to be investigated. In this review, we focus on the relevance of mitochondria in the nervous system, as well as some mitochondrial alterations that occur in neurodegenerative diseases associated with age. In addition, we describe studies that have performed mitochondrial transplantation in various tissues, and we emphasize the advances in mitochondrial transplantation aimed at treating diseases of the nervous system.


Corresponding author: Clorinda Arias, Departamento de Medicina Genómica y Toxicología Ambiental, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, AP 70-228, 04510, Ciudad de México, México, E-mail:

Funding source: Fundación Miguel Alemán, A.C., UNAM, DGAPA, PAPIIT

Award Identifier / Grant number: IN20231

  1. Author contribution: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: This work was supported by Fundación Miguel Alemán, A.C., UNAM, DGAPA, PAPIIT grant number, IN20231.

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

References

Adami, P.V.M., Quijano, C., Magnani, N., Galeano, P., Evelson, P., Cassina, A., Do Carmo, S., Leal, M.C., Castaño, E.M., Cuello, A.C., et al. (2017). Synaptosomal bioenergetic defects are associated with cognitive impairment in a transgenic rat model of early Alzheimer’s disease. J. Cerebr. Blood Flow Metabol. 37: 69–84.10.1177/0271678X15615132Suche in Google Scholar PubMed PubMed Central

Ahmad, T., Aggarwal, K., Pattnaik, B., Mukherjee, S., Sethi, T., Tiwari, B.K., Kumar, M., Micheal, A., Mabalirajan, U., Ghosh, B., et al. (2013). Computational classification of mitochondrial shapes reflects stress and redox state. Cell Death Dis. 4: e461–e461. https://doi.org/10.1038/cddis.2012.213.Suche in Google Scholar PubMed PubMed Central

Ahmad, T., Mukherjee, S., Pattnaik, B., Kumar, M., Singh, S., Kumar, M., Rehman, R., Tiwari, B.K., Jha, K.A., Barhanpurkar, A.P., et al. (2014). Miro1 regulates intercellular mitochondrial transport & amp: enhances mesenchymal stem cell rescue efficacy. EMBO J. 33. https://doi.org/10.1002/embj.201386030.Suche in Google Scholar PubMed PubMed Central

Al Amir Dache, Z., Otandault, A., Tanos, R., Pastor, B., Meddeb, R., Sanchez, C., Arena, G., Lasorsa, L., Bennett, A., Grange, T., et al. (2020). Blood contains circulating cell-free respiratory competent mitochondria. Faseb. J. 34: 3616–3630. https://doi.org/10.1096/fj.201901917rr.Suche in Google Scholar

Alikhani, N., Ankarcrona, M., and Glaser, E. (2009). Mitochondria and Alzheimer’s disease: amyloid-β peptide uptake and degradation by the presequence protease. hPreP. J. Bioenerg. Biomembr. 41: 447–451, https://doi.org/10.1007/s10863-009-9244-4.Suche in Google Scholar PubMed

Alikhani, N., Guo, L., Yan, S., Du, H., Pinho, C.M., Chen, J.X., Glaser, E., and Yan, S.S. (2011). Decreased proteolytic activity of the mitochondrial amyloid-β degrading enzyme, PreP peptidasome, in alzheimer’s disease brain mitochondria. J. Alzheim. Dis. 27: 75–87. https://doi.org/10.3233/jad-2011-101716.Suche in Google Scholar

Baek, S.H., Park, S.J., Jeong, J.I., Kim, S.H., Han, J.J.-W.W., Kyung, J.W., Baik, S.-H.H., Choi, Y., Choi, B.Y., Park, J.S., et al. (2017). Inhibition of Drp1 ameliorates synaptic depression, Aβ deposition, and cognitive impairment in an alzheimer’s disease model. J. Neurosci. 37: 5099–5110. https://doi.org/10.1523/jneurosci.2385-16.2017.Suche in Google Scholar

Berridge, M.V., McConnell, M.J., Grasso, C., Bajzikova, M., Kovarova, J., and Neuzil, J. (2016). Horizontal transfer of mitochondria between mammalian cells: beyond co-culture approaches, current opinion in genetics and development. Elsevier Current Trends.https://doi.org/10.1016/j.gde.2016.04.003.Suche in Google Scholar PubMed

Bertero, E., Maack, C., and O’Rourke, B. (2018). Mitochondrial transplantation in humans: “magical” cure or cause for concern? J. Clin. Invest. 128: 5191–5194. https://doi.org/10.1172/jci124944.Suche in Google Scholar

Bertero, E., O’Rourke, B., and Maack, C. (2020). Mitochondria do not survive calcium overload during transplantation. Circ. Res.https://doi.org/10.1161/CIRCRESAHA.119.316291.Suche in Google Scholar PubMed PubMed Central

Bukoreshtliev, N.V., Wang, X., Hodneland, E., Gurke, S., Barroso, J.F.V., and Gerdes, H.H. (2009). Selective block of tunneling nanotube (TNT) formation inhibits intercellular organelle transfer between PC12 cells. FEBS Lett. 583: 1481–1488. https://doi.org/10.1016/j.febslet.2009.03.065.Suche in Google Scholar PubMed

Burté, F., Carelli, V., Chinnery, P.F., and Yu-Wai-Man, P. (2015). Disturbed mitochondrial dynamics and neurodegenerative disorders. Nat. Rev. Neurol. 11: 11–24, https://doi.org/10.1038/nrneurol.2014.228.Suche in Google Scholar PubMed

Chandel, N.S. (2014). Mitochondria as signaling organelles. BMC Biol. 12:34, https://doi.org/10.1186/1741-7007-12-34.Suche in Google Scholar PubMed PubMed Central

Chang, J.C., Chang, H.S., Wu, Y.C., Cheng, W.L., Lin, T.T., Chang, H.J., Kuo, S.J., Chen, S.T., and Liu, C.S. (2019). Mitochondrial transplantation regulates antitumour activity chemoresistance and mitochondrial dynamics in breast cancer. J. Exp. Clin. Cancer Res 38. https://doi.org/10.1186/s13046-019-1028-z.Suche in Google Scholar PubMed PubMed Central

Chang, J.C., Hoel, F., Liu, K.H., Wei, Y.H., Cheng, F.C., Kuo, S.J., Tronstad, K.J., and Liu, C.S. (2017). Peptide-mediated delivery of donor mitochondria improves mitochondrial function and cell viability in human cybrid cells with the MELAS A3243G mutation. Sci. Rep. 7: 10710. https://doi.org/10.1038/s41598-017-10870-5.Suche in Google Scholar PubMed PubMed Central

Chang, J.C., Wu, S.L., Liu, K.H., Chen, Y.H., Chuang, C.S, Cheng, F.C., Su, H.L., Wei, Y.H., Kuo, S.J., and Liu, C.S. (2016). Allogeneic/xenogeneic transplantation of peptide-labeled mitochondria in Parkinson’s disease: restoration of mitochondria functions and attenuation of 6-hydroxydopamine-induced neurotoxicity. Transl. Res. 170: 40–56e3. https://doi.org/10.1016/j.trsl.2015.12.003.Suche in Google Scholar PubMed

Chen, H., and Chan, D.C. (2009). Mitochondrial dynamics-fusion, fission, movement, and mitophagy-in neurodegenerative diseases. Hum. Mol. Genet. 18: R169–R176. https://doi.org/10.1093/hmg/ddp326.Suche in Google Scholar PubMed PubMed Central

Chen, H., McCaffery, J.M., and Chan, D.C. (2007). Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell 130: 548–562. https://doi.org/10.1016/j.cell.2007.06.026.Suche in Google Scholar PubMed

Chou, S.H.Y.H.-Y., Lan, J., Esposito, E., Ning, M.M., Balaj, L., Ji, X., Lo, E.H., and Hayakawa, K. (2017). Extracellular mitochondria in cerebrospinal fluid and neurological recovery after subarachnoid hemorrhage. Stroke 48: 2231–2237. https://doi.org/10.1161/strokeaha.117.017758.Suche in Google Scholar PubMed PubMed Central

Clark, M.A., and Shay, J.W. (1982). Mitochondrial transformation of mammalian cells. Nature 295: 605–607. https://doi.org/10.1038/295605a0.Suche in Google Scholar PubMed

Cowan, D.B., Yao, R., Akurathi, V., Snay, E.R., Thedsanamoorthy, J.K., Zurakowski, D., Ericsson, M., Friehs, I., Wu, Y., Levitsky, S., et al. (2016). Intracoronary delivery of mitochondria to the ischemic heart for cardioprotection. PLoS One 11: e0160889. https://doi.org/10.1371/journal.pone.0160889.Suche in Google Scholar PubMed PubMed Central

Davis, C.O., Kim, K.-Y., Bushong, E.A., Mills, E.A., Boassa, D., Shih, T., Kinebuchi, M., Phan, S., Zhou, Y., Bihlmeyer, N.A., et al. (2014). Transcellular degradation of axonal mitochondria. Proc. Natl. Acad. Sci. U.S.A. 111: 9633–9638. https://doi.org/10.1073/pnas.1404651111.Suche in Google Scholar PubMed PubMed Central

Devi, L., Raghavendran, V., Prabhu, B.M., Avadhani, N.G., and Anandatheerthavarada, H.K. (2008). Mitochondrial import and accumulation of α-synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson disease brain. J. Biol. Chem. 283: 9089–9100. https://doi.org/10.1074/jbc.m710012200.Suche in Google Scholar

Divakaruni, S.S., Van Dyke, A.M., Chandra, R., LeGates, T.A., Contreras, M., Dharmasri, P.A., Higgs, H.N., Lobo, M.K., Thompson, S.M., and Blanpied, T.A. (2018). Long-term potentiation requires a rapid burst of dendritic mitochondrial fission during induction. Neuron 100: 860–875, e7. https://doi.org/10.1016/j.neuron.2018.09.025.Suche in Google Scholar PubMed PubMed Central

Doulamis, I.P., Guariento, A., Duignan, T., Orfany, A., Kido, T., Zurakowski, D., del Nido, P.J., and McCully, J.D. (2019). Mitochondrial transplantation for myocardial protection in diabetic hearts. Eur. J. Cardio. Thorac. Surg. 57: 836–845. https://doi.org/10.1093/ejcts/ezz326.Suche in Google Scholar PubMed

Du, F., Yu, Q., Yan, S., Hu, G., Lue, L.F., Walker, D.G., Wu, L., Yan, S.F., Tieu, K., and Yan, S.S. (2017). PINK1 signalling rescues amyloid pathology and mitochondrial dysfunction in Alzheimer’s disease. Brain 140: 3233–3251. https://doi.org/10.1093/brain/awx258.Suche in Google Scholar PubMed PubMed Central

Du, H., Guo, L., Yan, S., Sosunov, A.A., McKhann, G.M., and ShiDu Yan, S. (2010). Early deficits in synaptic mitochondria in an Alzheimer’s disease mouse model. Proc. Natl. Acad. Sci. U.S.A. 107: 18670–18675. https://doi.org/10.1073/pnas.1006586107.Suche in Google Scholar PubMed PubMed Central

Dupont, M., Souriant, S., Lugo-Villarino, G., Maridonneau-Parini, I., and Vérollet, C. (2018). Tunneling nanotubes: intimate communication between myeloid cells. Front. Immunol. 9:43, https://doi.org/10.3389/fimmu.2018.00043.Suche in Google Scholar PubMed PubMed Central

Emani, S.M., and McCully, J.D. (2018). Mitochondrial transplantation: applications for pediatric patients with congenital heart disease: AME Publishing Company, Translational Pediatrics, https://doi.org/10.21037/tp.2018.02.02.Suche in Google Scholar PubMed PubMed Central

Emani, S.M., Piekarski, B.L., Harrild, D., del Nido, P.J., and McCully, J.D. (2017). Autologous mitochondrial transplantation for dysfunction after ischemia-reperfusion injury. J. Thorac. Cardiovasc. Surg. 154: 286–289. https://doi.org/10.1016/j.jtcvs.2017.02.018.Suche in Google Scholar PubMed

Erecinska, M., Cherian, S., and Silver, I.A. (2004). Energy metabolism in mammalian brain during development. Prog. Neurobiol. 73: 397–445, https://doi.org/10.1016/j.pneurobio.2004.06.003.Suche in Google Scholar PubMed

Falchi, A.M., Sogos, V., Saba, F., Piras, M., Congiu, T., and Piludu, M. (2013). Astrocytes shed large membrane vesicles that contain mitochondria, lipid droplets and ATP. Histochem. Cell Biol. 139: 221–231. https://doi.org/10.1007/s00418-012-1045-x.Suche in Google Scholar PubMed

Falkevall, A., Alikhani, N., Bhushan, S., Pavlov, P.F., Busch, K., Johnson, K.A., Eneqvist, T., Tjernberg, L., Ankarcrona, M., and Glaser, E. (2006). Degradation of the amyloid β-protein by the novel mitochondrial peptidasome. PreP. J. Biol. Chem. 281: 29096–29104. https://doi.org/10.1074/jbc.m602532200.Suche in Google Scholar PubMed

Fang, E.F., Hou, Y., Palikaras, K., Adriaanse, B.A., Kerr, J.S., Yang, B., Lautrup, S., Hasan-Olive, M.M., Caponio, D., Dan, X., et al. (2019). Mitophagy inhibits amyloid-β and tau pathology and reverses cognitive deficits in models of Alzheimer’s disease. Nat. Neurosci. 1. https://doi.org/10.1038/s41593-018-0332-9.Suche in Google Scholar PubMed PubMed Central

Fu, A., Hou, Y., Yu, Z., Zhao, Z., and Liu, Z. (2019). Healthy mitochondria inhibit the metastatic melanoma in lungs. Int. J. Biol. Sci. 15: 2707–2718. https://doi.org/10.7150/ijbs.38104.Suche in Google Scholar PubMed PubMed Central

Gao, L., Zhang, Z., Lu, J., and Pei, G. (2019). Mitochondria are dynamically transferring between human neural cells and alexander disease-associated GFAP mutations impair the astrocytic transfer. Front. Cell. Neurosci. 13: 316. https://doi.org/10.3389/fncel.2019.00316.Suche in Google Scholar PubMed PubMed Central

Giorgi, C., Agnoletto, C., Bononi, A., Bonora, M., de Marchi, E., Marchi, S., Missiroli, S., Patergnani, S., Poletti, F., Rimessi, A., et al. (2012). Mitochondrial calcium homeostasis as potential target for mitochondrial medicine. Mitochondrion 12: 77–85, https://doi.org/10.1016/j.mito.2011.07.004.Suche in Google Scholar PubMed PubMed Central

Gollihue, J.L., Patel, S.P., Eldahan, K.C., Cox, D.H., Donahue, R.R., Taylor, B.K., Sullivan, P.G., and Rabchevsky, A.G. (2018). Effects of mitochondrial transplantation on bioenergetics, cellular incorporation, and functional recovery after spinal cord injury. J. Neurotrauma 35: 1800–1818. https://doi.org/10.1089/neu.2017.5605.Suche in Google Scholar PubMed PubMed Central

Gollihue, J.L., Patel, S.P., Mashburn, C., Eldahan, K.C., Sullivan, P.G., and Rabchevsky, A.G. (2017). Optimization of mitochondrial isolation techniques for intraspinal transplantation procedures. J. Neurosci. Methods 287: 1–12. https://doi.org/10.1016/j.jneumeth.2017.05.023.Suche in Google Scholar PubMed PubMed Central

Gollihue, J.L., and Rabchevsky, A.G. (2017). Prospects for therapeutic mitochondrial transplantation. Mitochondrion 35: 70–79, https://doi.org/10.1016/j.mito.2017.05.007.Suche in Google Scholar PubMed PubMed Central

Golpich, M., Amini, E., Mohamed, Z., Azman Ali, R., Mohamed Ibrahim, N., and Ahmadiani, A. (2017). Mitochondrial dysfunction and biogenesis in neurodegenerative diseases: pathogenesis and treatment. CNS Neurosci. Ther. 23: 5–22, https://doi.org/10.1111/cns.12655.Suche in Google Scholar PubMed PubMed Central

Grossman, L.I., Wildman, D.E., Schmidt, T.R., and Goodman, M. (2004). Accelerated evolution of the electron transport chain in anthropoid primates. Trends Genet. 20: 578–585, https://doi.org/10.1016/j.tig.2004.09.002.Suche in Google Scholar PubMed

Grünewald, A., Rygiel, K.A., Hepplewhite, P.D., Morris, C.M., Picard, M., and Turnbull, D.M. (2016). Mitochondrial DNA depletion in respiratory chain-deficient Parkinson disease neurons. Ann. Neurol. 79: 366–378. https://doi.org/10.1002/ana.24571.Suche in Google Scholar PubMed PubMed Central

Gureev, A.P., Popov, V.N., and Starkov, A.A. (2020). Crosstalk between the mTOR and Nrf2/ARE signaling pathways as a target in the improvement of long-term potentiation. Exp. Neurol.https://doi.org/10.1016/j.expneurol.2020.113285.Suche in Google Scholar PubMed PubMed Central

Hara, Y., Yuk, F., Puri, R., Janssen, W.G.M., Rapp, P.R., and Morrison, J.H. (2014). Presynaptic mitochondrial morphology in monkey prefrontal cortex correlates with working memory and is improved with estrogen treatment. Proc. Natl. Acad. Sci. U.S.A. 111: 486–491. https://doi.org/10.1073/pnas.1311310110.Suche in Google Scholar PubMed PubMed Central

Hayakawa, K., Chan, S.J., Mandeville, E.T., Park, J.H., Bruzzese, M., Montaner, J., Arai, K., Rosell, A., and Lo, E.H. (2018). Protective effects of endothelial progenitor cell-derived extracellular mitochondria in brain endothelium. Stem Cells. 36: 1404–1410. https://doi.org/10.1002/stem.2856.Suche in Google Scholar PubMed PubMed Central

Hayakawa, K., Esposito, E., Wang, X., Terasaki, Y., Liu, Y., Xing, C., Ji, X., and Lo, E.H. (2016). Transfer of mitochondria from astrocytes to neurons after stroke. Nature 535: 551–555. https://doi.org/10.1038/nature18928.Suche in Google Scholar PubMed PubMed Central

He, K., Shi, X., Zhang, X., Dang, S., Ma, X., Liu, F., Xu, M., Lv, Z., Han, D., Fang, X., et al. (2011). Long-distance intercellular connectivity between cardiomyocytes and cardiofibroblasts mediated by membrane nanotubes. Cardiovasc. Res. 92: 39–47. https://doi.org/10.1093/cvr/cvr189.Suche in Google Scholar PubMed

Hirai, K., Aliev, G., Nunomura, A., Fujioka, H., Russell, R.L., Atwood, C.S., Johnson, A.B., Kress, Y., Vinters, H.V., Tabaton, M., et al. (2001). Mitochondrial abnormalities in Alzheimer’s disease. J. Neurosci. 21: 3017–3023. https://doi.org/10.1523/jneurosci.21-09-03017.2001.Suche in Google Scholar PubMed PubMed Central

Holm, M.M., Kaiser, J., and Schwab, M.E. (2018). Extracellular vesicles: multimodal envoys in neural maintenance and repair. Trends Neurosci. 41: 360–372, https://doi.org/10.1016/j.tins.2018.03.006.Suche in Google Scholar PubMed

Huang, P.J., Kuo, C.C., Lee, H.C., Shen, C.I., Cheng, F.C., Wu, S.F., Chang, J.C., Pan, H.C., Lin, S.Z., Liu, C.S., et al. (2016). Transferring xenogenic mitochondria provides neural protection against ischemic stress in ischemic rat brains. Cell Transplant. 25: 913–927. https://doi.org/10.3727/096368915x689785.Suche in Google Scholar

Islam, M.N., Das, S.R., Emin, M.T., Wei, M., Sun, L., Westphalen, K., Rowlands, D.J., Quadri, S.K., Bhattacharya, S., and Bhattacharya, J. (2012). Mitochondrial transfer from bone-marrow-derived stromal cells to pulmonary alveoli protects against acute lung injury. Nat. Med. 18: 759–765. https://doi.org/10.1038/nm.2736.Suche in Google Scholar PubMed PubMed Central

Jagmag, S.A., Tripathi, N., Shukla, S.D., Maiti, S., and Khurana, S. (2016). Evaluation of models of Parkinson’s disease. Front. Neurosci. 9: 503, https://doi.org/10.3389/fnins.2015.00503.Suche in Google Scholar PubMed PubMed Central

Jin, H., Kanthasamy, A., Ghosh, A., Anantharam, V., Kalyanaraman, B., and Kanthasamy, A.G. (2014). Mitochondria-targeted antioxidants for treatment of Parkinson’s disease: preclinical and clinical outcomes. Biochim. Biophys. Acta (BBA) – Mol. Basis Dis. 1842: 1282–1294, https://doi.org/10.1016/j.bbadis.2013.09.007.Suche in Google Scholar PubMed PubMed Central

Joshi, A.U., Minhas, P.S., Liddelow, S.A., Haileselassie, B., Andreasson, K.I., Dorn, G.W., and Mochly-Rosen, D. (2019). Fragmented mitochondria released from microglia trigger A1 astrocytic response and propagate inflammatory neurodegeneration. Nat. Neurosci. 22: 1635–1648. https://doi.org/10.1038/s41593-019-0486-0.Suche in Google Scholar PubMed PubMed Central

Kandimalla, R., Manczak, M., Fry, D., Suneetha, Y., Sesaki, H., and Reddy, P.H. (2016). Reduced dynamin-related protein 1 protects against phosphorylated Tau-induced mitochondrial dysfunction and synaptic damage in Alzheimer’s disease. Hum. Mol. Genet. 25: 4881–4897. https://doi.org/10.1093/hmg/ddw312.Suche in Google Scholar PubMed PubMed Central

Kang, J.S., Tian, J.H., Pan, P.Y., Zald, P., Li, C., Deng, C., and Sheng, Z.H. (2008). Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation. Cell 132: 137–148. https://doi.org/10.1016/j.cell.2007.11.024.Suche in Google Scholar PubMed PubMed Central

Katrangi, E., D’Souza, G., Boddapati, S.V., Kulawiec, M., Singh, K.K., Bigger, B., and Weissig, V. (2007). Xenogenic transfer of isolated murine mitochondria into human ρ0 cells can improve respiratory function. Rejuvenation Res. 10: 561–570. https://doi.org/10.1089/rej.2007.0575.Suche in Google Scholar PubMed

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. (2017). Myocardial rescue with autologous mitochondrial transplantation in a porcine model of ischemia/reperfusion. J Thoracic Cardiovasc Surg. Mosby: 934–943. https://doi.org/10.1016/j.jtcvs.2016.10.077.Suche in Google Scholar PubMed

Keller, K.E., Bradley, J.M., Sun, Y.Y., Yang, Y.F., and Acott, T.S. (2017). Tunneling nanotubes are novel cellular structures that communicate signals between trabecular meshwork cells. Investig. Ophthalmol. Vis. Sci. 58: 5298–5307. https://doi.org/10.1167/iovs.17-22732.Suche in Google Scholar PubMed PubMed Central

Kesner, E.E., Saada-Reich, A., and Lorberboum-Galski, H. (2016). Characteristics of mitochondrial transformation into human cells. Sci. Rep. 6. https://doi.org/10.1038/srep26057.Suche in Google Scholar PubMed PubMed Central

Khamsi, R. (2004). Energetic cells may have boosted the brain. Nature. https://doi.org/10.1038/news041122-5.Suche in Google Scholar

Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., Yokochi, M., Mizuno, Y., and Shimizu, N. (1998). Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392: 605–608. https://doi.org/10.1038/33416.Suche in Google Scholar PubMed

Koyanagi, M., Brandes, R.P., Haendeler, J., Zeiher, A.M., and Dimmeler, S. (2005). Cell-to-cell connection of endothelial progenitor cells with cardiac myocytes by nanotubes: a novel mechanism for cell fate changes?. Circ. Res. 96: 1039–1041. https://doi.org/10.1161/01.res.0000168650.23479.0c.Suche in Google Scholar

Kuo, C.C., Su, H.L., Chang, T.L., Chiang, C.Y., Sheu, M.L., Cheng, F.C., Chen, C.J., Sheehan, J., and Pan, H.C. (2017). Prevention of axonal degeneration by perineurium injection of mitochondria in a sciatic nerve crush injury model. Neurosurgery 80: 475–488. https://doi.org/10.1093/neuros/nyw090.Suche in Google Scholar PubMed

Laird, M.D., Clerc, P., Polster, B.M., and Fiskum, G. (2013). Augmentation of normal and glutamate-impaired neuronal respiratory capacity by exogenous alternative biofuels. Transl. Stroke Res. 4: 643–651. https://doi.org/10.1007/s12975-013-0275-0.Suche in Google Scholar PubMed PubMed Central

Levy, M., Faas, G.C., Saggau, P., Craigen, W.J., and Sweatt, J.D. (2003). Mitochondrial regulation of synaptic plasticity in the hippocampus. J. Biol. Chem. 278: 17727–17734. https://doi.org/10.1074/jbc.m212878200.Suche in Google Scholar

Li, X., Zhang, Y., Yeung, S.C., Liang, Y., Liang, X., Ding, Y., Ip, M.S.M., Tse, H.-F., Mak, J.C.W., and Lian, Q. (2014). Mitochondrial transfer of induced pluripotent stem cell–derived mesenchymal stem cells to airway epithelial cells attenuates cigarette smoke–induced damage. Am. J. Respir. Cell Mol. Biol. 51: 455–465. https://doi.org/10.1165/rcmb.2013-0529oc.Suche in Google Scholar

Li, Z., Okamoto, K.I., Hayashi, Y., and Sheng, M. (2004). The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119: 873–887. https://doi.org/10.1016/j.cell.2004.11.003.Suche in Google Scholar PubMed

Lin, M.-Y., and Sheng, Z.-H. (2015). Regulation of mitochondrial transport in neurons. Exp. Cell Res. 334: 35–44. https://doi.org/10.1016/j.yexcr.2015.01.004.Suche in Google Scholar PubMed PubMed Central

Liu, K., Guo, L., Zhou, Z., Pan, M., and Yan, C. (2019). Mesenchymal stem cells transfer mitochondria into cerebral microvasculature and promote recovery from ischemic stroke. Microvasc. Res. 123: 74–80. https://doi.org/10.1016/j.mvr.2019.01.001.Suche in Google Scholar PubMed

Liu, K., Ji, K., Guo, L., Wu, W., Lu, H., Shan, P., and Yan, C. (2014). Mesenchymal stem cells rescue injured endothelial cells in an in vitro ischemia-reperfusion model via tunneling nanotube like structure-mediated mitochondrial transfer. Microvasc. Res. 92: 10–18. https://doi.org/10.1016/j.mvr.2014.01.008.Suche in Google Scholar PubMed

Manczak, M., Calkins, M.J., and Reddy, P.H. (2011). Impaired mitochondrial dynamics and abnormal interaction of amyloid beta with mitochondrial protein Drp1 in neurons from patients with Alzheimer’s disease: implications for neuronal damage. Hum. Mol. Genet. 20: 2495–2509. https://doi.org/10.1093/hmg/ddr139.Suche in Google Scholar PubMed PubMed Central

Mandal, A., and Drerup, C.M. (2019). Axonal transport and mitochondrial function in neurons. Front. Cell. Neurosci. 13:373, https://doi.org/10.3389/fncel.2019.00373.Suche in Google Scholar PubMed PubMed Central

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. (2013). Transplantation of autologously derived mitochondria protects the heart from ischemia-reperfusion injury. AJP Hear. Circ. Physiol. 304: H966–H982. https://doi.org/10.1152/ajpheart.00883.2012.Suche in Google Scholar PubMed PubMed Central

McCully, J.D., Cowan, D.B., Emani, S.M., and del Nido, P.J. (2017). Mitochondrial transplantation: from animal models to clinical use in humans. Mitochondrion 34: 127–134, https://doi.org/10.1016/j.mito.2017.03.004.Suche in Google Scholar PubMed

McCully, J.D., Cowan, D.B., Pacak, C.A., Toumpoulis, I.K., Dayalan, H., and Levitsky, S. (2009). Injection of isolated mitochondria during early reperfusion for cardioprotection. Am. J. Physiol. Heart Circ. Physiol. 296: H94–H105. https://doi.org/10.1152/ajpheart.00567.2008.Suche in Google Scholar PubMed PubMed Central

McCully, J.D., Emani, S.M., and Del Nido, P.J. (2020). Letter by McCully et al Regarding Article, “Mitochondria do not survive calcium overload. Circ. Res.https://doi.org/10.1161/CIRCRESAHA.120.316832.Suche in Google Scholar PubMed

Melentijevic, I., Toth, M.L., Arnold, M.L., Guasp, R.J., Harinath, G., Nguyen, K.C., Taub, D., Parker, J.A., Neri, C., Gabel, C.V., et al. (2017). C. elegans neurons jettison protein aggregates and mitochondria under neurotoxic stress. Nature 542: 367–371. https://doi.org/10.1038/nature21362.Suche in Google Scholar PubMed PubMed Central

Miliotis, S., Nicolalde, B., Ortega, M., Yepez, J., and Caicedo, A. (2019). Forms of extracellular mitochondria and their impact in health. Mitochondrion.10.1016/j.mito.2019.02.002Suche in Google Scholar PubMed

Morris, M.C., Depollier, J., Mery, J., Heitz, F., and Divita, G. (2001). A peptide carrier for the delivery of biologically active proteins into mammalian cells. Nat. Biotechnol. 19: 1173–1176. https://doi.org/10.1038/nbt1201-1173.Suche in Google Scholar PubMed

Morrison, T.J., Jackson, M.V., Cunningham, E.K., Kissenpfennig, A., McAuley, D.F., O’Kane, C.M., and Krasnodembskaya, A.D. (2017). Mesenchymal stromal cells modulate macrophages in clinically relevant lung injury models by extracellular vesicle mitochondrial transfer. Am. J. Respir. Crit. Care Med. 196: 1275–1286. https://doi.org/10.1164/rccm.201701-0170oc.Suche in Google Scholar

Moschoi, R., Imbert, V., Nebout, M., Chiche, J., Mary, D., Prebet, T., Saland, E., Castellano, R., Pouyet, L., Collette, Y., et al. (2016). Protective mitochondrial transfer from bone marrow stromal cells to acute myeloid leukemic cells during chemotherapy. Blood 128: 253–264. https://doi.org/10.1182/blood-2015-07-655860.Suche in Google Scholar PubMed

Moskowitzova, K., Liu, K., Shin, B., Ramirez-Barbieri, G.F., Guariento, A., Blitzer, D., Cowan, D.B., Thedsanamoorthy, J.K., Yao, R., Orfany, A., et al. (2018). Mitochondrial transplantation prolongs cold preservation time in murine cardiac transplantation. J. Hear Lung Transplant. 37: S22–S23. https://doi.org/10.1016/j.healun.2018.01.033.Suche in Google Scholar

Moskowitzova, K., Shin, B., Liu, K., Ramirez-Barbieri, G., Guariento, A., Blitzer, D., Thedsanamoorthy, J.K., Yao, R., Snay, E.R., Inkster, J.A.H., et al. (2019). Mitochondrial transplantation prolongs cold ischemia time in murine heart transplantation 38, 92–99. https://doi.org/10.1016/j.healun.2018.09.025.Suche in Google Scholar PubMed PubMed Central

Mossmann, D., Vögtle, F.N., Taskin, A.A., Teixeira, P.F., Ring, J., Burkhart, J.M., Burger, N., Pinho, C.M., Tadic, J., Loreth, D., et al. (2014). Amyloid-β peptide induces mitochondrial dysfunction by inhibition of preprotein maturation. Cell Metabol. 20: 662–669. https://doi.org/10.1016/j.cmet.2014.07.024.Suche in Google Scholar PubMed

Murray, L.M.A., and Krasnodembskaya, A.D. (2019). Concise review: intercellular communication via organelle transfer in the biology and therapeutic applications of stem cells. Stem Cells. 37: 14–25. https://doi.org/10.1002/stem.2922.Suche in Google Scholar PubMed

Murthy, V.N., and Camilli, P. De. (2003). Cell biology of the presynaptic Terminal. Annu. Rev. Neurosci. 26: 701–728. https://doi.org/10.1146/annurev.neuro.26.041002.131445.Suche in Google Scholar PubMed

Nakamura, K., Nemani, V.M., Azarbal, F., Skibinski, G., Levy, J.M., Egami, K., Munishkina, L., Zhang, J., Gardner, B., Wakabayashi, J., et al. (2011). Direct membrane association drives mitochondrial fission by the Parkinson disease-associated protein α-synuclein. J. Biol. Chem. 286: 20710–20726. https://doi.org/10.1074/jbc.m110.213538.Suche in Google Scholar

Nakamura, K., Nemani, V.M., Wallender, E.K., Kaehlcke, K., Ott, M., and Edwards, R.H. (2008). Optical reporters for the conformation of α-synuclein reveal a specific interaction with mitochondria. J. Neurosci. 28: 12305–12317. https://doi.org/10.1523/jneurosci.3088-08.2008.Suche in Google Scholar PubMed PubMed Central

Nguyen, P.V., Marin, L., and Atwood, H.L. (1997). Synaptic physiology and mitochondrial function in crayfish tonic and phasic motor neurons. J. Neurophysiol. 78: 281–294. https://doi.org/10.1152/jn.1997.78.1.281.Suche in Google Scholar PubMed

Nicolás-Ávila, J.A., Lechuga-Vieco, A.V., Esteban-Martínez, L., Sánchez-Díaz, M., Díaz-García, E., Santiago, D.J., Rubio-Ponce, A., Li, J.L., Balachander, A., Quintana, J.A., et al. (2020). A network of macrophages supports mitochondrial homeostasis in the heart. Cell, https://doi.org/10.1016/j.cell.2020.08.031.Suche in Google Scholar PubMed

Pacak, C.A., Preble, J.M., Kondo, H., Seibel, P., Levitsky, S., del Nido, P.J., Cowan, D.B., and McCully, J.D. (2015). Actin-dependent mitochondrial internalization in cardiomyocytes: evidence for rescue of mitochondrial function. Biol. Open 4: 622–626. https://doi.org/10.1242/bio.201511478.Suche in Google Scholar PubMed PubMed Central

Park, J.-S.S., Davis, R.L., and Sue, C.M. (2018). Mitochondrial dysfunction in Parkinson’s disease: new mechanistic insights and therapeutic perspectives. Curr. Neurol. Neurosci. Rep. 18: 21. https://doi.org/10.1007/s11910-018-0829-3.Suche in Google Scholar PubMed PubMed Central

Pepe, S., Marasco, S.F., Haas, S.J., Sheeran, F.L., Krum, H., and Rosenfeldt, F.L. (2007). Coenzyme Q10 in cardiovascular disease. Mitochondrion 7 Suppl: S154–S167, https://doi.org/10.1016/j.mito.2007.02.005.Suche in Google Scholar PubMed

Perkins, G.A., Tjong, J., Brown, J.M., Poquiz, P.H., Scott, R.T., Kolson, D.R., Ellisman, M.H., and Spirou, G.A. (2010). The micro-architecture of mitochondria at active zones: electron tomography reveals novel anchoring scaffolds and cristae structured for high-rate metabolism. J. Neurosci. 30: 1015–1026. https://doi.org/10.1523/jneurosci.1517-09.2010.Suche in Google Scholar

Picard, M., and McEwen, B.S. (2014). Mitochondria impact brain function and cognition. Proc. Natl. Acad. Sci. U.S.A. 111: 7–8. https://doi.org/10.1073/pnas.1321881111.Suche in Google Scholar PubMed PubMed Central

Pickrell, A.M., Huang, C.H., Kennedy, S.R., Ordureau, A., Sideris, D.P., Hoekstra, J.G., Harper, J.W., and Youle, R.J. (2015). Endogenous parkin preserves dopaminergic substantia nigral neurons following mitochondrial DNA mutagenic stress. Neuron 87: 371–381. https://doi.org/10.1016/j.neuron.2015.06.034.Suche in Google Scholar PubMed PubMed Central

Piel, D.A., Gruber, P.J., Weinheimer, C.J., Courtois, M.R., Robertson, C.M., Coopersmith, C.M., Deutschman, C.S., and Levy, R.J. (2007). Mitochondrial resuscitation with exogenous cytochrome c in the septic heart. Crit. Care Med. 35: 2120–2127. https://doi.org/10.1097/01.ccm.0000278914.85340.fe.Suche in Google Scholar PubMed

Plotnikov, E.Y., Khryapenkova, T.G., Galkina, S.I., Sukhikh, G.T., and Zorov, D.B. (2010). Cytoplasm and organelle transfer between mesenchymal multipotent stromal cells and renal tubular cells in co-culture. Exp. Cell Res. 316: 2447–2455. https://doi.org/10.1016/j.yexcr.2010.06.009.Suche in Google Scholar PubMed

Poewe, W., Seppi, K., Tanner, C.M., Halliday, G.M., Brundin, P., Volkmann, J., Schrag, A.E., and Lang, A.E. (2017). Parkinson disease. Nat. Rev. Dis. Prim. 3: 1–21. https://doi.org/10.1038/nrdp.2017.13.Suche in Google Scholar PubMed

Pontzer, H., Brown, M.H., Raichlen, D.A., Dunsworth, H., Hare, B., Walker, K., Luke, A., Dugas, L.R., Durazo-Arvizu, R., Schoeller, D., et al. (2016). Metabolic acceleration and the evolution of human brain size and life history. Nature 533: 390–392. https://doi.org/10.1038/nature17654.Suche in Google Scholar PubMed PubMed Central

Preble, J.M., Pacak, C.A., Kondo, H., MacKay, A.A., Cowan, D.B., and McCully, J.D. (2014). Rapid isolation and purification of mitochondria for transplantation by tissue dissociation and differential filtration. J. Vis. Exp.: e51682. https://doi.org/10.3791/51682.Suche in Google Scholar PubMed PubMed Central

Querfurth, H.W., and LaFerla, F.M. (2010). Alzheimer’s disease. N. Engl. J. Med. 362: 329–344. https://doi.org/10.1056/nejmra0909142.Suche in Google Scholar

Ramirez-Barbieri, G., Moskowitzova, K., Shin, B., Blitzer, D., Orfany, A., Guariento, A., Iken, K., Friehs, I., Zurakowski, D., del Nido, P.J., et al. (2018). Alloreactivity and allorecognition of syngeneic and allogeneic mitochondria. Mitochondrion 46: 103–115. https://doi.org/10.1016/j.mito.2018.03.002.Suche in Google Scholar PubMed

Rangaraju, V., Calloway, N., and Ryan, T.A. (2014). Activity-driven local ATP synthesis is required for synaptic function. Cell 156: 825–835. https://doi.org/10.1016/j.cell.2013.12.042.Suche in Google Scholar PubMed PubMed Central

Rangaraju, V., Lauterbach, M., and Schuman, E.M. (2019a). Spatially stable mitochondrial compartments fuel local translation during plasticity. Cell 176: 73–84.e15. https://doi.org/10.1016/j.cell.2018.12.013.Suche in Google Scholar PubMed

Rangaraju, V., Lewis, T.L., Hirabayashi, Y., Bergami, M., Motori, E., Cartoni, R., Kwon, S.K., and Courchet, J. (2019b). Pleiotropic mitochondria: the influence of mitochondria on neuronal development and disease. J. Neurosci. 39: 8200–8208. https://doi.org/10.1523/jneurosci.1157-19.2019.Suche in Google Scholar PubMed PubMed Central

Raoof, A.R., Vlist, M.V.D., Willemen, H.L.D.M., and Prado, J. (2020). Macrophages transfer mitochondria to sensory neurons to resolve inflammatory pain. bioRxiv. https://doi.org/10.1101/2020.02.12.940445.Suche in Google Scholar

Rizzuto, R. (2001). Intracellular Ca2+ pools in neuronal signalling. Curr. Opin. Neurobiol. 11: 306–311, https://doi.org/10.1016/s0959-4388(00)00212-9.Suche in Google Scholar PubMed

Robey, R.B., and Hay, N. (2006). Mitochondrial hexokinases, novel mediators of the antiapoptotic effects of growth factors and Akt. Oncogene 25: 4683–4696, https://doi.org/10.1038/sj.onc.1209595.Suche in Google Scholar PubMed

Robicsek, O., Ene, H.M., Karry, R., Ytzhaki, O., Asor, E., McPhie, D., Cohen, B.M., Ben-Yehuda, R., Weiner, I., and Ben-Shachar, D. (2018). Isolated mitochondria transfer improves neuronal differentiation of schizophrenia-derived induced pluripotent stem cells and rescues deficits in a rat model of the disorder. Schizophr. Bull. 44: 432–442. https://doi.org/10.1093/schbul/sbx077.Suche in Google Scholar PubMed PubMed Central

Roushandeh, A.M., Kuwahara, Y., and Roudkenar, M.H. (2019). Mitochondrial transplantation as a potential and novel master key for treatment of various incurable diseases. Cytotechnology 71: 647–663. https://doi.org/10.1007/s10616-019-00302-9.Suche in Google Scholar PubMed PubMed Central

Ruan, L., Zhou, C., Jin, E., Kucharavy, A., Zhang, Y., Wen, Z., Florens, L., and Li, R. (2017). Cytosolic proteostasis through importing of misfolded proteins into mitochondria. Nature 543: 443–446. https://doi.org/10.1038/nature21695.Suche in Google Scholar PubMed PubMed Central

Rustom, A., Saffrich, R., Markovic, I., Walther, P., and Gerdes, H.-H. (2004). Nanotubular highways for intercellular organelle transport. Science 303: 1007–1010. https://doi.org/10.1126/science.1093133.Suche in Google Scholar PubMed

Sarter, M., and Parikh, V. (2005). Choline transporters, cholinergic transmission and cognition. Nat. Rev. Neurosci. 6: 48–56, https://doi.org/10.1038/nrn1588.Suche in Google Scholar PubMed

Saxton, W.M., and Hollenbeck, P.J. (2012). The axonal transport of mitochondria. J. Cell Sci. 125: 2095–2104. https://doi.org/10.1242/jcs.053850.Suche in Google Scholar PubMed PubMed Central

Scarffe, L.A., Stevens, D.A., Dawson, V.L., and Dawson, T.M. (2014). Parkin and PINK1: much more than mitophagy. Trends Neurosci. 37: 315–324. https://doi.org/10.1016/j.tins.2014.03.004.Suche in Google Scholar PubMed PubMed Central

Schwarz, T.L. (2013). Mitochondrial trafficking in neurons. Cold Spring Harb. Perspect. Biol 5. https://doi.org/10.1101/cshperspect.a011304.Suche in Google Scholar PubMed PubMed Central

Scott, I., and Youle, R.J. (2010). Mitochondrial fission and fusion. Essays Biochem. 47: 85–98. https://doi.org/10.1042/bse0470085.Suche in Google Scholar PubMed PubMed Central

Sharpley, M.S., Marciniak, C., Eckel-Mahan, K., McManus, M., Crimi, M., Waymire, K., Lin, C.S., Masubuchi, S., Friend, N., Koike, M., et al. (2012). Heteroplasmy of mouse mtDNA is genetically unstable and results in altered behavior and cognition. Cell 151: 333–343. https://doi.org/10.1016/j.cell.2012.09.004.Suche in Google Scholar PubMed PubMed Central

Shi, X., Zhao, M., Fu, C., and Fu, A. (2017). Intravenous administration of mitochondria for treating experimental Parkinson’s disease. Mitochondrion 34: 91–100. https://doi.org/10.1016/j.mito.2017.02.005.Suche in Google Scholar PubMed

Shin, B., Cowan, D.B., Emani, S.M., del Nido, P.J., and McCully, J.D. (2017). Mitochondrial transplantation in myocardial ischemia and reperfusion injury Advances in experimental medicine and biology. Cham: Springer, 595–619 https://doi.org/10.1007/978-3-319-55330-6_31.Suche in Google Scholar 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. (2019). A novel biological strategy for myocardial protection by intracoronary delivery of mitochondria: safety and efficacy. JACC Basic to Transl. Sci. 4: 871–888. https://doi.org/10.1016/j.jacbts.2019.08.007.Suche in Google Scholar PubMed PubMed Central

Silver, I., and Erecińska, M. (1998). Oxygen and ion concentrations in normoxic and hypoxic brain cells. Adv. Exp. Med. Biol. 454: 7–16. https://doi.org/10.1007/978-1-4615-4863-8_2.Suche in Google Scholar PubMed

Sisakhtnezhad, S., and Khosravi, L. (2015). Emerging physiological and pathological implications of tunneling nanotubes formation between cells. Eur. J. Cell Biol. 94: 429–443, https://doi.org/10.1016/j.ejcb.2015.06.010.Suche in Google Scholar PubMed

Smith, G.M., and Gallo, G. (2018). The role of mitochondria in axon development and regeneration. Dev. Neurobiol. 78: 221–237, https://doi.org/10.1002/dneu.22546.Suche in Google Scholar PubMed PubMed Central

Song, X., Hu, W., Yu, H., Wang, H., Zhao, Y, Korngold, R., and Zhao, Yong. (2020). Existence of circulating mitochondria in human and animal peripheral blood. Int. J. Mol. Sci. 21: 2122. https://doi.org/10.3390/ijms21062122.Suche in Google Scholar PubMed PubMed Central

Sorrentino, V., Romani, M., Mouchiroud, L., Beck, J.S., Zhang, H., D’Amico, D., Moullan, N., Potenza, F., Schmid, A.W., Rietsch, S., et al. (2017). Enhancing mitochondrial proteostasis reduces amyloid-β proteotoxicity. Nature 552: 187–193. https://doi.org/10.1038/nature25143.Suche in Google Scholar PubMed PubMed Central

Spees, J.L., Olson, S.D., Whitney, M.J., and Prockop, D.J. (2006). Mitochondrial transfer between cells can rescue aerobic respiration. Proc. Natl. Acad. Sci. U.S.A. 103: 1283–1288. https://doi.org/10.1073/pnas.0510511103.Suche in Google Scholar PubMed PubMed Central

Suen, D.F., Norris, K.L., and Youle, R.J. (2008). Mitochondrial dynamics and apoptosis. Genes Dev. 22: 1577–1590. https://doi.org/10.1101/gad.1658508.Suche in Google Scholar PubMed PubMed Central

Sun, C., Liu, X., Wang, B., Wang, Z., Liu, Y., Di, C., Si, J., Li, H., Wu, Q., Xu, D., et al. (2019). Endocytosis-mediated mitochondrial transplantation: transferring normal human astrocytic mitochondria into glioma cells rescues aerobic respiration and enhances radiosensitivity. Theranostics 9: 3595–3607. https://doi.org/10.7150/thno.33100.Suche in Google Scholar PubMed PubMed Central

Sun, T., Qiao, H., Pan, P.Y., Chen, Y., and Sheng, Z.H. (2013). Motile axonal mitochondria contribute to the variability of presynaptic strength. Cell Rep. 4: 413–419. https://doi.org/10.1016/j.celrep.2013.06.040.Suche in Google Scholar PubMed PubMed Central

Tachibana, M., Sparman, M., Sritanaudomchai, H., Ma, H., Clepper, L., Woodward, J., Li, Y., Ramsey, C., Kolotushkina, O., and Mitalipov, S. (2009). Mitochondrial gene replacement in primate offspring and embryonic stem cells. Nature 461: 367–372. https://doi.org/10.1038/nature08368.Suche in Google Scholar PubMed PubMed Central

Tanaka, D., Nakada, K., Takao, K., Ogasawara, E., Kasahara, A., Sato, A., Yonekawa, H., Miyakawa, T., and Hayashi, J.I. (2008). Normal mitochondrial respiratory function is essential for spatial remote memory in mice. Mol. Brain 1: 21. https://doi.org/10.1186/1756-6606-1-21.Suche in Google Scholar PubMed PubMed Central

Todorova, V., and Blokland, A. (2016). Mitochondria and synaptic plasticity in the mature and aging nervous system. Curr. Neuropharmacol. 15: 166–173. https://doi.org/10.2174/1570159x14666160414111821.Suche in Google Scholar PubMed PubMed Central

Torralba, D., Baixauli, F., and Sánchez-Madrid, F. (2016). Mitochondria know No boundaries: mechanisms and functions of intercellular mitochondrial transfer. Front. Cell Dev. Biol. 4: 107. https://doi.org/10.3389/fcell.2016.00107.Suche in Google Scholar PubMed PubMed Central

Tseng, N., Lambie, S.C., Huynh, C.Q., Sanford, B., Patel, M., Herson, P.S., and Ormond, D.R. (2020). Mitochondrial transfer from mesenchymal stem cells improves neuronal metabolism after oxidant injury in vitro: the role of Miro1. J. Cerebr. Blood Flow Metabol. 271678X20928147, https://doi.org/10.1177/0271678x20928147.Suche in Google Scholar

Verstreken, P., Ly, C.V., Venken, K.J.T., Koh, T.-W.W., Zhou, Y., and Bellen, H.J. (2005). Synaptic Mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 47: 365–378. https://doi.org/10.1016/j.neuron.2005.06.018.Suche in Google Scholar PubMed

Wang, L., Guo, L., Lu, L., Sun, H., Shao, M., Beck, S.J., Li, L., Ramachandran, J., Du, Y., and Du, H. (2016). Synaptosomal mitochondrial dysfunction in 5xFAD mouse model of Alzheimer’s disease. PLoS One 11: e0150441. https://doi.org/10.1371/journal.pone.0150441.Suche in Google Scholar PubMed PubMed Central

Wang, X., Bukoreshtliev, N.V., and Gerdes, H.H. (2012). Developing neurons form transient nanotubes facilitating electrical coupling and calcium signaling with distant astrocytes. PLoS One 7 https://doi.org/10.1371/journal.pone.0047429.Suche in Google Scholar PubMed PubMed Central

Wang, X., Su, B., Lee, H.-g. H., Li, X., Perry, G., Smith, M., and Zhu, X. (2009). Impaired balance of mitochondrial fission and fusion in Alzheimer’s disease. J. Neurosci. 29: 9090–9103. https://doi.org/10.1523/jneurosci.1357-09.2009.Suche in Google Scholar PubMed PubMed Central

Wang, X., Su, B., Siedlak, S.L., Moreira, P.I., Fujioka, H., Wang, Y., Casadesus, G., and Zhu, X. (2008). Amyloid-beta overproduction causes abnormal mitochondrial dynamics via differential modulation of mitochondrial fission/fusion proteins. Proc. Natl. Acad. Sci. U.S.A. 105: 19318–19323. https://doi.org/10.1073/pnas.0804871105.Suche in Google Scholar PubMed PubMed Central

Wang, Y., Ni, J., Gao, C., Xie, L., Zhai, L., Cui, G., and Yin, X. (2019). Mitochondrial transplantation attenuates lipopolysaccharide- induced depression-like behaviors. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 93: 240–249. https://doi.org/10.1016/j.pnpbp.2019.04.010.Suche in Google Scholar PubMed

Wu, T.H., Sagullo, E., Case, D., Zheng, X., Li, Y., Hong, J.S., Teslaa, T., Patananan, A.N., McCaffery, J.M., Niazi, K., et al. (2016). Mitochondrial transfer by photothermal nanoblade restores metabolite profile in mammalian cells. Cell Metabol. 23: 921–929. https://doi.org/10.1016/j.cmet.2016.04.007.Suche in Google Scholar PubMed PubMed Central

Yao, J., Irwin, R.W., Zhao, L., Nilsen, J., Hamilton, R.T., and Brinton, R.D. (2009). Mitochondrial bioenergetic deficit precedes Alzheimer’s pathology in female mouse model of Alzheimer’s disease. Proc. Natl. Acad. Sci. U.S.A. 106: 14670–14675. https://doi.org/10.1073/pnas.0903563106.Suche in Google Scholar PubMed PubMed Central

Yao, Y., Fan, X.L., Jiang, D., Zhang, Y., Li, X., Xu, Z.B., Fang, S.B, Chiu, S., Tse, H.F., Lian, Q., et al. (2018). Connexin 43-mediated mitochondrial transfer of iPSC-MSCs alleviates asthma inflammation. Stem Cell Rep 11: 1120–1135. https://doi.org/10.1016/j.stemcr.2018.09.012.Suche in Google Scholar PubMed PubMed Central

Youle, R.J., and van der Bliek, A.M. (2012). Mitochondrial fission, fusion, and stress. Science 337: 1062–1065. https://doi.org/10.1126/science.1219855.Suche in Google Scholar PubMed PubMed Central

Zhang, B., Gao, Y., Li, Q., Sun, D., Dong, X., Li, X., Xin, W., and Zhang, J. (2020). Effects of brain-derived mitochondria on the function of neuron and vascular endothelial cell after traumatic brain injury. World Neurosurg 138. https://doi.org/10.1016/j.wneu.2019.11.172.Suche in Google Scholar PubMed

Zhang, L., Trushin, S., Christensen, T.A., Bachmeier, B.V., Gateno, B., Schroeder, A., Yao, J., Itoh, K., Sesaki, H., Poon, W.W., et al. (2016). Altered brain energetics induces mitochondrial fission arrest in Alzheimer’s Disease. Sci. Rep. 6: 18725. https://doi.org/10.1038/srep18725.Suche in Google Scholar PubMed PubMed Central

Zhang, Z., Ma, Z., Yan, C., Pu, K., Wu, M., Bai, J., Li, Y., and Wang, Q. (2019). Muscle-derived autologous mitochondrial transplantation: a novel strategy for treating cerebral ischemic injury. Behav. Brain Res. 356: 322–331. https://doi.org/10.1016/j.bbr.2018.09.005.Suche in Google Scholar PubMed

Zhao, Y., Jiang, Z., Delgado, E., Li, H., Zhou, H., Hu, W., Perez-Basterrechea, M., Janostakova, A., Tan, Q., Wang, J., et al. (2017). Platelet-derived mitochondria display embryonic stem cell markers and improve pancreatic islet b-cell function in humans. Stem Cells Transl. Med. 6: 1684–1697. https://doi.org/10.1002/sctm.17-0078.Suche in Google Scholar PubMed PubMed Central

Zhao, Z., Yu, Z., Hou, Y., Zhang, L., and Fu, A. (2020). Improvement of cognitive and motor performance with mitotherapy in aged mice. Int. J. Biol. Sci. 16: 849–858. https://doi.org/10.7150/ijbs.40886.Suche in Google Scholar PubMed PubMed Central

Zheng, Y.R., Zhang, X.N., and Chen, Z. (2019). Mitochondrial transport serves as a mitochondrial quality control strategy in axons: implications for central nervous system disorders. CNS Neurosci. Ther. 25: 876–886, https://doi.org/10.1111/cns.13122.Suche in Google Scholar PubMed PubMed Central

Zorov, D.B., Juhaszova, M., and Sollott, S.J. (2014). Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol. Rev. 94: 909–50. https://doi.org/10.1152/physrev.00026.2013.Suche in Google Scholar PubMed PubMed Central

Zozina, V.I., Covantev, S., Goroshko, O.A., Krasnykh, L.M., and Kukes, V.G. (2018). Coenzyme Q10 in cardiovascular and metabolic diseases: current state of the problem. Curr. Cardiol. Rev. 14: 164–174. https://doi.org/10.2174/1573403x14666180416115428.Suche in Google Scholar PubMed PubMed Central

Received: 2020-07-08
Accepted: 2020-09-29
Published Online: 2020-12-07
Published in Print: 2021-02-23

© 2020 Walter de Gruyter GmbH, Berlin/Boston

Heruntergeladen am 21.9.2025 von https://www.degruyterbrill.com/document/doi/10.1515/revneuro-2020-0068/html?lang=de
Button zum nach oben scrollen