Louis-Armstrong

Mitochondrial dysfunction in neurological disorders: Exploring mitochondrial transplantation

  • 1.

    Frey, T. G. & Mannella, C. A. The internal structure of mitochondria. Trends Biochem. Sci. 25, 319–324 (2000).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 2.

    Picard, M., Taivassalo, T., Gouspillou, G. & Hepple, R. T. Mitochondria: isolation, structure and function. J. Physiol. 589, 4413–4421 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 3.

    Rose, J. et al. Mitochondrial dysfunction in glial cells: Implications for neuronal homeostasis and survival. Toxicology 391, 109–115 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 4.

    Liu, F., Lu, J., Manaenko, A., Tang, J. & Hu, Q. Mitochondria in ischemic stroke: new insight and implications. Aging Dis. 9, 924–937 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 5.

    Briston, T. et al. Mitochondrial permeability transition pore: sensitivity to opening and mechanistic dependence on substrate availability. Sci. Rep. 7, 10492 (2017).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • 6.

    Halestrap, A. P. & Richardson, A. P. The mitochondrial permeability transition: a current perspective on its identity and role in ischaemia/reperfusion injury. J. Mol. Cell. Cardiol. 78, 129–141 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 7.

    Mylonas, C. & Kouretas, D. Lipid peroxidation and tissue damage. In Vivo 13, 295–309 (1999).

    CAS 
    PubMed 

    Google Scholar
     

  • 8.

    de Vasconcelos, N. M., Van Opdenbosch, N., Van Gorp, H., Parthoens, E. & Lamkanfi, M. Single-cell analysis of pyroptosis dynamics reveals conserved GSDMD-mediated subcellular events that precede plasma membrane rupture. Cell Death Differ. 26, 146–161 (2019).

    PubMed 
    Article 
    CAS 

    Google Scholar
     

  • 9.

    Dixon, S. J. et al. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149, 1060–1072 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 10.

    Fatokun, A. A., Dawson, V. L. & Dawson, T. M. Parthanatos: mitochondrial-linked mechanisms and therapeutic opportunities. Br. J. Pharm. 171, 2000–2016 (2014).

    CAS 
    Article 

    Google Scholar
     

  • 11.

    Gao, M. et al. Role of mitochondria in ferroptosis. Mol. Cell 73, 354–363 e353 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 12.

    Marshall, K. D. & Baines, C. P. Necroptosis: is there a role for mitochondria? Front. Physiol. 5, 323 (2014).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 13.

    DeGregorio-Rocasolano, N., Marti-Sistac, O. & Gasull, T. Deciphering the iron side of stroke: neurodegeneration at the crossroads between iron dyshomeostasis, excitotoxicity, and ferroptosis. Front. Neurosci. 13, 85 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 14.

    Do Van, B. et al. Ferroptosis, a newly characterized form of cell death in Parkinson’s disease that is regulated by PKC. Neurobiol. Dis. 94, 169–178 (2016).

    PubMed 
    Article 
    CAS 

    Google Scholar
     

  • 15.

    Lane, D. J. R., Ayton, S. & Bush, A. I. Iron and Alzheimer’s disease: an update on emerging mechanisms. J. Alzheimers Dis. 64, S379–S395 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 16.

    Xie, B. S. et al. Inhibition of ferroptosis attenuates tissue damage and improves long-term outcomes after traumatic brain injury in mice. CNS Neurosci. Ther. 25, 465–475 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 17.

    Lai, Y. et al. STYK1/NOK correlates with ferroptosis in non-small cell lung carcinoma. Biochem. Biophys. Res. Commun. 519, 659–666 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 18.

    DeHart, D. N. et al. Opening of voltage dependent anion channels promotes reactive oxygen species generation, mitochondrial dysfunction and cell death in cancer cells. Biochem. Pharm. 148, 155–162 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 19.

    Krainz, T. et al. A mitochondrial-targeted nitroxide is a potent inhibitor of ferroptosis. ACS Cent. Sci. 2, 653–659 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 20.

    Yang, W. S. et al. Regulation of ferroptotic cancer cell death by GPX4. Cell 156, 317–331 (2014).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 21.

    Azevedo, R. S. S. et al. In situ immune response and mechanisms of cell damage in central nervous system of fatal cases microcephaly by Zika virus. Sci. Rep. 8, 1 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 22.

    Slee, E. A., Adrain, C. & Martin, S. J. Executioner caspase-3, -6, and -7 perform distinct, non-redundant roles during the demolition phase of apoptosis. J. Biol. Chem. 276, 7320–7326 (2001).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 23.

    van der Bliek, A. M., Shen, Q. & Kawajiri, S. Mechanisms of mitochondrial fission and fusion. Cold Spring Harb. Perspect. Biol. 5, a011072 (2013).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 24.

    Meyer, J. N., Leuthner, T. C. & Luz, A. L. Mitochondrial fusion, fission, and mitochondrial toxicity. Toxicology 391, 42–53 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 25.

    Querfurth, H. W. & LaFerla, F. M. Alzheimer’s disease. N. Engl. J. Med. 362, 329–344 (2010).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 26.

    Patergnani, S. et al. Mitochondria in multiple sclerosis: molecular mechanisms of pathogenesis. Int. Rev. Cell Mol. Biol. 328, 49–103 (2017).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 27.

    Swerdlow, R. H. & Khan, S. M. The Alzheimer’s disease mitochondrial cascade hypothesis: an update. Exp. Neurol. 218, 308–315 (2009).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 28.

    Du, H. et al. Cyclophilin D deficiency attenuates mitochondrial and neuronal perturbation and ameliorates learning and memory in Alzheimer’s disease. Nat. Med. 14, 1097–1105 (2008).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 29.

    Rao, V. K., Carlson, E. A. & Yan, S. S. Mitochondrial permeability transition pore is a potential drug target for neurodegeneration. Biochim. Biophys. Acta 1842, 1267–1272 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 30.

    Du, H. & ShiDu Yan, S. Unlocking the door to neuronal woes in Alzheimer’s disease: abeta and mitochondrial permeability transition pore. Pharmaceuticals 3, 1936–1948 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 31.

    Tysnes, O. B. & Storstein, A. Epidemiology of Parkinson’s disease. J. Neural Transm. 124, 901–905 (2017).

    PubMed 
    Article 

    Google Scholar
     

  • 32.

    Winkler-Stuck, K. et al. Re-evaluation of the dysfunction of mitochondrial respiratory chain in skeletal muscle of patients with Parkinson’s disease. J. Neural Transm. 112, 499–518 (2005).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 33.

    Gu, M., Cooper, J. M., Taanman, J. W. & Schapira, A. H. Mitochondrial DNA transmission of the mitochondrial defect in Parkinson’s disease. Ann. Neurol. 44, 177–186 (1998).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 34.

    Ekstrand, M. I. et al. Progressive parkinsonism in mice with respiratory-chain-deficient dopamine neurons. Proc. Natl Acad. Sci. USA 104, 1325–1330 (2007).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 35.

    Klein, C. & Westenberger, A. Genetics of Parkinson’s disease. Cold Spring Harb. Perspect. Med. 2, a008888 (2012).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 36.

    Lucking, C. B. et al. Association between early-onset Parkinson’s disease and mutations in the parkin gene. N. Engl. J. Med. 342, 1560–1567 (2000).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 37.

    Gandhi, S. et al. PINK1 protein in normal human brain and Parkinson’s disease. Brain 129, 1720–1731 (2006).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 38.

    Wood-Kaczmar, A. et al. PINK1 is necessary for long term survival and mitochondrial function in human dopaminergic neurons. PLoS ONE 3, e2455 (2008).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • 39.

    Mallach, A. et al. Post mortem examination of Parkinson’s disease brains suggests decline in mitochondrial biomass, reversed by deep brain stimulation of subthalamic nucleus. FASEB J. 33, 6957–6961 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 40.

    Quintanilla, R. A. & Johnson, G. V. Role of mitochondrial dysfunction in the pathogenesis of Huntington’s disease. Brain Res. Bull. 80, 242–247 (2009).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 41.

    Lin, J. et al. Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell 119, 121–135 (2004).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 42.

    Milakovic, T. & Johnson, G. V. Mitochondrial respiration and ATP production are significantly impaired in striatal cells expressing mutant huntingtin. J. Biol. Chem. 280, 30773–30782 (2005).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 43.

    Choo, Y. S., Johnson, G. V., MacDonald, M., Detloff, P. J. & Lesort, M. Mutant huntingtin directly increases susceptibility of mitochondria to the calcium-induced permeability transition and cytochrome c release. Hum. Mol. Genet. 13, 1407–1420 (2004).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 44.

    Tellez-Nagel, I., Johnson, A. B. & Terry, R. D. Studies on brain biopsies of patients with Huntington’s chorea. J. Neuropathol. Exp. Neurol. 33, 308–332 (1974).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 45.

    Song, W. et al. Mutant huntingtin binds the mitochondrial fission GTPase dynamin-related protein-1 and increases its enzymatic activity. Nat. Med. 17, 377–382 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 46.

    Weydt, P. et al. Thermoregulatory and metabolic defects in Huntington’s disease transgenic mice implicate PGC-1alpha in Huntington’s disease neurodegeneration. Cell Metab. 4, 349–362 (2006).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 47.

    Writing Group, M. et al. Heart disease and stroke statistics-2016 update: a report from the American Heart Association. Circulation 133, e38–e360 (2016).


    Google Scholar
     

  • 48.

    Hofmeijer, J. & van Putten, M. J. Ischemic cerebral damage: an appraisal of synaptic failure. Stroke 43, 607–615 (2012).

    PubMed 
    Article 

    Google Scholar
     

  • 49.

    Dharmasaroja, P. A. Fluid intake related to brain edema in acute middle cerebral artery infarction. Transl. Stroke Res. 7, 49–53 (2016).

    PubMed 
    Article 

    Google Scholar
     

  • 50.

    Saita, S. et al. Distinct types of protease systems are involved in homeostasis regulation of mitochondrial morphology via balanced fusion and fission. Genes Cells 21, 408–424 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 51.

    Sims, N. R. & Muyderman, H. Mitochondria, oxidative metabolism and cell death in stroke. Biochim. Biophys. Acta 1802, 80–91 (2010).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 52.

    Bereiter-Hahn, J. & Voth, M. Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc. Res. Tech. 27, 198–219 (1994).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 53.

    Wang, J. et al. Mdivi-1 prevents apoptosis induced by ischemia-reperfusion injury in primary hippocampal cells via inhibition of reactive oxygen species-activated mitochondrial pathway. J. Stroke Cerebrovasc. Dis. 23, 1491–1499 (2014).

    PubMed 
    Article 

    Google Scholar
     

  • 54.

    Cowan, D. B. et al. Intracoronary delivery of mitochondria to the ischemic heart for cardioprotection. PLoS ONE 11, e0160889 (2016).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • 55.

    McCully, J. D. et al. Injection of isolated mitochondria during early reperfusion for cardioprotection. Am. J. Physiol. Heart Circ. Physiol. 296, H94–H105 (2009).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 56.

    McCully, J. D., Levitsky, S., Del Nido, P. J. & Cowan, D. B. Mitochondrial transplantation for therapeutic use. Clin. Transl. Med. 5, 16 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 57.

    Masuzawa, A. et al. Transplantation of autologously derived mitochondria protects the heart from ischemia-reperfusion injury. Am. J. Physiol. Heart Circ. Physiol. 304, H966–H982 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 58.

    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. 154, 286–289 (2017).

    PubMed 
    Article 

    Google Scholar
     

  • 59.

    Emani, S. M. & McCully, J. D. Mitochondrial transplantation: applications for pediatric patients with congenital heart disease. Transl. Pediatr. 7, 169–175 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 60.

    Zhang, Z. et al. Muscle-derived autologous mitochondrial transplantation: a novel strategy for treating cerebral ischemic injury. Behav. Brain Res. 356, 322–331 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 61.

    Liu, K. et al. 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 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 62.

    Pan, B. T. & Johnstone, R. M. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell 33, 967–978 (1983).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 63.

    Kramer-Albers, E. M. et al. Oligodendrocytes secrete exosomes containing major myelin and stress-protective proteins: trophic support for axons? Proteom. Clin. Appl 1, 1446–1461 (2007).

    Article 
    CAS 

    Google Scholar
     

  • 64.

    Simpson, R. J., Jensen, S. S. & Lim, J. W. Proteomic profiling of exosomes: current perspectives. Proteomics 8, 4083–4099 (2008).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 65.

    Puhm, F. et al. Mitochondria are a subset of extracellular vesicles released by activated monocytes and induce Type I IFN and TNF responses in endothelial cells. Circ. Res. 125, 43–52 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 66.

    Hayakawa, K. et al. Transfer of mitochondria from astrocytes to neurons after stroke. Nature 535, 551–555 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 67.

    Rustom, A., Saffrich, R., Markovic, I., Walther, P. & Gerdes, H. H. Nanotubular highways for intercellular organelle transport. Science 303, 1007–1010 (2004).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 68.

    Hayakawa, K. et al. Protective effects of endothelial progenitor cell-derived extracellular mitochondria in brain endothelium. Stem Cells 36, 1404–1410 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 69.

    Kaneko, Y. et al. Cell therapy for stroke: emphasis on optimizing safety and efficacy profile of endothelial progenitor cells. Curr. Pharm. Des. 18, 3731–3734 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 70.

    Preble, J. M. et al. Rapid isolation and purification of mitochondria for transplantation by tissue dissociation and differential filtration. J. Vis. Exp 91, e51682 (2014).


    Google Scholar
     

  • 71.

    Poot, M. et al. Analysis of mitochondrial morphology and function with novel fixable fluorescent stains. J. Histochem. Cytochem. 44, 1363–1372 (1996).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 72.

    Shi, X., Zhao, M., Fu, C. & Fu, A. Intravenous administration of mitochondria for treating experimental Parkinson’s disease. Mitochondrion 34, 91–100 (2017).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 73.

    Sun, C. et al. Endocytosis-mediated mitochondrial transplantation: transferring normal human astrocytic mitochondria into glioma cells rescues aerobic respiration and enhances radiosensitivity. Theranostics 9, 3595–3607 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 74.

    Lippert, T. & Borlongan, C. V. Prophylactic treatment of hyperbaric oxygen treatment mitigates inflammatory response via mitochondria transfer. CNS Neurosci. Ther. 25, 815–823 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 75.

    Joshi, A. U. et al. Fragmented mitochondria released from microglia trigger A1 astrocytic response and propagate inflammatory neurodegeneration. Nat. Neurosci. 22, 1635–1648 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 76.

    Robicsek, O. et al. 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 (2018).

    PubMed 
    Article 

    Google Scholar
     

  • 77.

    Yao, Y. et al. Connexin 43-mediated mitochondrial transfer of iPSC-MSCs alleviates asthma inflammation. Stem Cell Rep. 11, 1120–1135 (2018).

    CAS 
    Article 

    Google Scholar
     

  • 78.

    Partikian, A., Olveczky, B., Swaminathan, R., Li, Y. & Verkman, A. S. Rapid diffusion of green fluorescent protein in the mitochondrial matrix. J. Cell Biol. 140, 821–829 (1998).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 79.

    Gao, L., Zhang, Z., Lu, J. & Pei, G. Mitochondria are dynamically transferring between human neural cells and Alexander disease-associated GFAP mutations impair the astrocytic transfer. Front. Cell. Neurosci. 13, 316 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 80.

    Gollihue, J. L. et al. Effects of mitochondrial transplantation on bioenergetics, cellular incorporation, and functional recovery after spinal cord injury. J. Neurotrauma 35, 1800–1818 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 81.

    Kitani, T. et al. Direct human mitochondrial transfer: a novel concept based on the endosymbiotic theory. Transpl. Proc. 46, 1233–1236 (2014).

    CAS 
    Article 

    Google Scholar
     

  • 82.

    Rocca, C. J. et al. Transplantation of wild-type mouse hematopoietic stem and progenitor cells ameliorates deficits in a mouse model of Friedreich’s ataxia. Sci. Transl. Med. 9, eaaj2347 (2017).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • 83.

    Laker, R. C. et al. A novel MitoTimer reporter gene for mitochondrial content, structure, stress, and damage in vivo. J. Biol. Chem. 289, 12005–12015 (2014).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 84.

    Wilson, R. J. et al. Conditional MitoTimer reporter mice for assessment of mitochondrial structure, oxidative stress, and mitophagy. Mitochondrion 44, 20–26 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 85.

    Gollihue, J. L. & Rabchevsky, A. G. Prospects for therapeutic mitochondrial transplantation. Mitochondrion 35, 70–79 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 86.

    Islam, M. N. et al. Mitochondrial transfer from bone-marrow-derived stromal cells to pulmonary alveoli protects against acute lung injury. Nat. Med. 18, 759–765 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 87.

    Spees, J. L., Olson, S. D., Whitney, M. J. & Prockop, D. J. Mitochondrial transfer between cells can rescue aerobic respiration. Proc. Natl Acad. Sci. USA 103, 1283–1288 (2006).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 88.

    Paliwal, S., Chaudhuri, R., Agrawal, A. & Mohanty, S. Regenerative abilities of mesenchymal stem cells through mitochondrial transfer. J. Biomed. Sci. 25, 31 (2018).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • 89.

    Huang, P. J. et al. Transferring xenogenic mitochondria provides neural protection against ischemic stress in ischemic rat brains. Cell Transpl. 25, 913–927 (2016).

    CAS 
    Article 

    Google Scholar
     

  • 90.

    Hayakawa, K. et al. Extracellular mitochondria for therapy and diagnosis in acute central nervous system injury. JAMA Neurol. 75, 119–122 (2018).

    PubMed 
    Article 

    Google Scholar
     

  • 91.

    Pletjushkina, O. Y. et al. Effect of oxidative stress on dynamics of mitochondrial reticulum. Biochim. Biophys. Acta 1757, 518–524 (2006).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 92.

    Chandel, N. S. Evolution of mitochondria as signaling organelles. Cell Metab. 22, 204–206 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 93.

    Nisoli, E., Clementi, E., Moncada, S. & Carruba, M. O. Mitochondrial biogenesis as a cellular signaling framework. Biochem. Pharm. 67, 1–15 (2004).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 94.

    Scholkmann, F. Long range physical cell-to-cell signalling via mitochondria inside membrane nanotubes: a hypothesis. Theor. Biol. Med. Model. 13, 16 (2016).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • Source Article