CoChat
Sign Up
Cited by 171Mitochondrial Function and PathologyAutophagy in Disease and TherapyExtracellular vesicles in disease

Inter and Intracellular mitochondrial trafficking in health and disease

Open access
Shanmughapriya, Santhanam, Langford, Dianne, Natarajaseenivasan, Kalimuthusamy·2020·Ageing Research Reviews
DOI 10.1016/j.arr.2020.101128PMC PMC7484258
Open this paper in CoChat — free account

Abstract

Neurons and glia maintain central nervous system (CNS) homeostasis through diverse mechanisms of intra- and intercellular signaling. Some of these interactions include the exchange of soluble factors between cells via direct cell-to-cell contact for both short and long-distance transfer of biological materials. Transcellular transfer of mitochondria has emerged as a key example of this communication. This transcellular transfer of mitochondria are dynamically involved in the cellular and tissue response to CNS injury and play beneficial roles in recovery. This review highlights recent research addressing the cause and effect of intra- and intercellular mitochondrial transfer with a specific focus on the future of mitochondrial transplantation therapy. We believe that mitochondrial transfer plays a crucial role during bioenergetic crisis/deficit, but the quality, quantity and mode of mitochondrial transfer determines the protective capacity for the receiving cells. Mitochondrial transplantation is a new treatment paradigm and will overcome the major bottleneck of traditional approach of correcting mitochondria-related disorders.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.arr.2020.101128

Cites

21 of 21 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 187

  1. Abounit S, Zurzolo C, 2012 Wiring through tunneling nanotubes--from electrical signals to organelle transfer. J Cell Sci 125, 1089– 1098. 22399801
  2. Ahmad T, Mukherjee S, Pattnaik B, Kumar M, Singh S, Kumar M, Rehman R, Tiwari BK, Jha KA, Barhanpurkar AP, Wani MR, Roy SS, Mabalirajan U, Ghosh B, Agrawal A, 2014 Miro1 regulates intercellular mitochondrial transport & enhances mesenchymal stem cell rescue efficacy. EMBO J 33, 994– 1010. 24431222 PMC4193933
  3. Al Amir Dache Z, Otandault A, Tanos R, Pastor B, Meddeb R, Sanchez C, Arena G, Lasorsa L, Bennett A, Grange T, El Messaoudi S, Mazard T, Prevostel C, Thierry AR, 2020 Blood contains circulating cell-free respiratory competent mitochondria. FASEB J 34, 3616– 3630. 31957088
  4. Araki T, 1977 Freezing injury in mitochondrial membranes. II. Degradation of phospholipid in rabbit liver mitochondria during freezing and storage at low temperatures. Cryobiology 14, 151– 159. 558866
  5. Aspenstrom P, Ruusala A, Pacholsky D, 2007 Taking Rho GTPases to the next level: the cellular functions of atypical Rho GTPases. Exp Cell Res 313, 3673– 3679. 17850788
  6. Babenko VA, Silachev DN, Zorova LD, Pevzner IB, Khutornenko AA, Plotnikov EY, Sukhikh GT, Zorov DB, 2015 Improving the Post-Stroke Therapeutic Potency of Mesenchymal Multipotent Stromal Cells by Cocultivation With Cortical Neurons: The Role of Crosstalk Between Cells. Stem Cells Transl Med 4, 1011– 1020. 26160961 PMC4542870
  7. Baughman JM, Perocchi F, Girgis HS, Plovanich M, Belcher-Timme CA, Sancak Y, Bao XR, Strittmatter L, Goldberger O, Bogorad RL, Koteliansky V, Mootha VK, 2011 Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 476, 341– 345. 21685886 PMC3486726
  8. Beck M, Brickley K, Wilkinson HL, Sharma S, Smith M, Chazot PL, Pollard S, Stephenson FA, 2002 Identification, molecular cloning, and characterization of a novel GABAA receptor-associated protein, GRIF-1. J Biol Chem 277, 30079– 30090. 12034717
  9. Berridge MV, Neuzil J, 2017 The mobility of mitochondria: Intercellular trafficking in health and disease. Clin Exp Pharmacol Physiol 44 Suppl 1, 15– 20. 28409855
  10. Berridge MV, Schneider RT, McConnell MJ, 2016 Mitochondrial Transfer from Astrocytes to Neurons following Ischemic Insult: Guilt by Association? Cell Metab 24, 376– 378. 27626198
  11. Bertero E, Maack C, O’Rourke B, 2018 Mitochondrial transplantation in humans: “magical” cure or cause for concern? J Clin Invest 128, 5191– 5194. 30371508 PMC6264628
  12. Birsa N, Norkett R, Higgs N, Lopez-Domenech G, Kittler JT, 2013 Mitochondrial trafficking in neurons and the role of the Miro family of GTPase proteins. Biochem Soc Trans 41, 1525– 1531. 24256248
  13. Bock FJ, Tait SWG, 2020 Mitochondria as multifaceted regulators of cell death. Nat Rev Mol Cell Biol 21, 85– 100. 31636403
  14. Bozi LH, Bechara LR, Dos Santos AF, Campos JC, 2016 Mitochondrial-derived vesicles: a new player in cardiac mitochondrial quality control. J Physiol 594, 6077– 6078. 27800623 PMC5088229
  15. Bragoszewski P, Turek M, Chacinska A, 2017 Control of mitochondrial biogenesis and function by the ubiquitin-proteasome system. Open Biol 7. PMC5413908 28446709
  16. Braschi E, Goyon V, Zunino R, Mohanty A, Xu L, McBride HM, 2010 Vps35 mediates vesicle transport between the mitochondria and peroxisomes. Curr Biol 20, 1310– 1315. 20619655
  17. Brickley K, Smith MJ, Beck M, Stephenson FA, 2005 GRIF-1 and OIP106, members of a novel gene family of coiled-coil domain proteins: association in vivo and in vitro with kinesin. J Biol Chem 280, 14723– 14732. 15644324
  18. Brickley K, Stephenson FA, 2011 Trafficking kinesin protein (TRAK)-mediated transport of mitochondria in axons of hippocampal neurons. J Biol Chem 286, 18079– 18092. 21454691 PMC3093881
  19. Bukoreshtliev NV, Wang X, Hodneland E, Gurke S, Barroso JF, Gerdes HH, 2009 Selective block of tunneling nanotube (TNT) formation inhibits intercellular organelle transfer between PC12 cells. FEBS Lett 583, 1481– 1488. 19345217
  20. Cadete VJ, Deschenes S, Cuillerier A, Brisebois F, Sugiura A, Vincent A, Turnbull D, Picard M, McBride HM, Burelle Y, 2016 Formation of mitochondrial-derived vesicles is an active and physiologically relevant mitochondrial quality control process in the cardiac system. J Physiol 594, 5343– 5362. 27311616 PMC5023710
  21. Cai Q, Gerwin C, Sheng ZH, 2005 Syntabulin-mediated anterograde transport of mitochondria along neuronal processes. J Cell Biol 170, 959– 969. 16157705 PMC1804288
  22. Caicedo A, Fritz V, Brondello JM, Ayala M, Dennemont I, Abdellaoui N, de Fraipont F, Moisan A, Prouteau CA, Boukhaddaoui H, Jorgensen C, Vignais ML, 2015 MitoCeption as a new tool to assess the effects of mesenchymal stem/stromal cell mitochondria on cancer cell metabolism and function. Sci Rep 5, 9073. 25766410 PMC4358056
  23. Chan NC, Salazar AM, Pham AH, Sweredoski MJ, Kolawa NJ, Graham RL, Hess S, Chan DC, 2011 Broad activation of the ubiquitin-proteasome system by Parkin is critical for mitophagy. Hum Mol Genet 20, 1726– 1737. 21296869 PMC3071670
  24. Chang CY, Liang MZ, Chen L, 2019 Current progress of mitochondrial transplantation that promotes neuronal regeneration. Transl Neurodegener 8, 17. 31210929 PMC6567446
  25. Chang DT, Honick AS, Reynolds IJ, 2006 Mitochondrial trafficking to synapses in cultured primary cortical neurons. J Neurosci 26, 7035– 7045. 16807333 PMC6673923
  26. Chang DT, Reynolds IJ, 2006 Differences in mitochondrial movement and morphology in young and mature primary cortical neurons in culture. Neuroscience 141, 727– 736. 16797853
  27. Chang JC, Wu SL, Liu KH, Chen YH, Chuang CS, Cheng FC, Su HL, Wei YH, Kuo SJ, Liu CS, 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– 56 e43. 26730494
  28. Chen YM, Gerwin C, Sheng ZH, 2009 Dynein light chain LC8 regulates syntaphilin-mediated mitochondrial docking in axons. J Neurosci 29, 9429– 9438. 19641106 PMC6666546
  29. Chien L, Liang MZ, Chang CY, Wang C, Chen L, 2018 Mitochondrial therapy promotes regeneration of injured hippocampal neurons. Biochim Biophys Acta Mol Basis Dis 1864, 3001– 3012. 29913215
  30. Chinnery HR, Pearlman E, McMenamin PG, 2008 Cutting edge: Membrane nanotubes in vivo: a feature of MHC class II+ cells in the mouse cornea. J Immunol 180, 5779– 5783. 18424694 PMC3392179
  31. Cowan DB, Yao R, Thedsanamoorthy JK, Zurakowski D, Del Nido PJ, McCully JD, 2017 Transit and integration of extracellular mitochondria in human heart cells. Sci Rep 7, 17450. 29234096 PMC5727261
  32. Csordas G, Weaver D, Hajnoczky G, 2018 Endoplasmic Reticulum-Mitochondrial Contactology: Structure and Signaling Functions. Trends Cell Biol 28, 523– 540. 29588129 PMC6005738
  33. Dai Y, Zheng K, Clark J, Swerdlow RH, Pulst SM, Sutton JP, Shinobu LA, Simon DK, 2014 Rapamycin drives selection against a pathogenic heteroplasmic mitochondrial DNA mutation. Hum Mol Genet 23, 637– 647. 24101601 PMC3888257
  34. De Stefani D, Raffaello A, Teardo E, Szabo I, Rizzuto R, 2011 A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476, 336– 340. 21685888 PMC4141877
  35. Diaz-Vegas A, Sanchez-Aguilera P, Krycer JR, Morales PE, Monsalves-Alvarez M, Cifuentes M, Rothermel BA, Lavandero S, 2020 Is mitochondrial dysfunction a common root of noncommunicable chronic diseases? Endocr Rev. PMC7255501 32179913
  36. El-Hattab AW, Zarante AM, Almannai M, Scaglia F, 2017 Therapies for mitochondrial diseases and current clinical trials. Mol Genet Metab 122, 1– 9. PMC5773113 28943110
  37. Emani SM, Piekarski BL, Harrild D, Del Nido PJ, McCully JD, 2017 Autologous mitochondrial transplantation for dysfunction after ischemia-reperfusion injury. J Thorac Cardiovasc Surg 154, 286– 289. 28283239
  38. Evans WH, Martin PE, 2002 Gap junctions: structure and function (Review). Mol Membr Biol 19, 121– 136. 12126230
  39. Falchi AM, Sogos V, Saba F, Piras M, Congiu T, Piludu M, 2013 Astrocytes shed large membrane vesicles that contain mitochondria, lipid droplets and ATP. Histochem Cell Biol 139, 221– 231. 23108569
  40. Fransson A, Ruusala A, Aspenstrom P, 2003 Atypical Rho GTPases have roles in mitochondrial homeostasis and apoptosis. J Biol Chem 278, 6495– 6502. 12482879
  41. Fransson S, Ruusala A, Aspenstrom P, 2006 The atypical Rho GTPases Miro-1 and Miro-2 have essential roles in mitochondrial trafficking. Biochem Biophys Res Commun 344, 500– 510. 16630562
  42. Fu A, Shi X, Zhang H, Fu B, 2017 Mitotherapy for Fatty Liver by Intravenous Administration of Exogenous Mitochondria in Male Mice. Front Pharmacol 8, 241. 28536524 PMC5422541
  43. Glancy B, Hartnell LM, Combs CA, Femnou A, Sun J, Murphy E, Subramaniam S, Balaban RS, 2017 Power Grid Protection of the Muscle Mitochondrial Reticulum. Cell Rep 19, 487– 496. 28423313 PMC5490369
  44. Glater EE, Megeath LJ, Stowers RS, Schwarz TL, 2006 Axonal transport of mitochondria requires milton to recruit kinesin heavy chain and is light chain independent. J Cell Biol 173, 545– 557. 16717129 PMC2063864
  45. Godlewski J, Krichevsky AM, Johnson MD, Chiocca EA, Bronisz A, 2015 Belonging to a network--microRNAs, extracellular vesicles, and the glioblastoma microenvironment. Neuro Oncol 17, 652– 662. 25301812 PMC4482852
  46. Gollihue JL, Patel SP, Eldahan KC, Cox DH, Donahue RR, Taylor BK, Sullivan PG, Rabchevsky AG, 2018a Effects of Mitochondrial Transplantation on Bioenergetics, Cellular Incorporation, and Functional Recovery after Spinal Cord Injury. J Neurotrauma 35, 1800– 1818. 29648982 PMC6053898
  47. Gollihue JL, Patel SP, Rabchevsky AG, 2018b Mitochondrial transplantation strategies as potential therapeutics for central nervous system trauma. Neural Regen Res 13, 194– 197. 29557359 PMC5879881
  48. Gollihue JL, Rabchevsky AG, 2017 Prospects for therapeutic mitochondrial transplantation. Mitochondrion 35, 70– 79. 28533168 PMC5518605
  49. Gong YN, Crawford JC, Heckmann BL, Green DR, 2019 To the edge of cell death and back. FEBS J 286, 430– 440. 30506628 PMC6361675
  50. Gorska-Andrzejak J, Stowers RS, Borycz J, Kostyleva R, Schwarz TL, Meinertzhagen IA, 2003 Mitochondria are redistributed in Drosophila photoreceptors lacking milton, a kinesin-associated protein. J Comp Neurol 463, 372– 388. 12836173
  51. Gousset K, Schiff E, Langevin C, Marijanovic Z, Caputo A, Browman DT, Chenouard N, de Chaumont F, Martino A, Enninga J, Olivo-Marin JC, Mannel D, Zurzolo C, 2009 Prions hijack tunnelling nanotubes for intercellular spread. Nat Cell Biol 11, 328– 336. 19198598
  52. Granatiero V, De Stefani D, Rizzuto R, 2017 Mitochondrial Calcium Handling in Physiology and Disease. Adv Exp Med Biol 982, 25– 47. 28551780
  53. Grishin A, Li H, Levitan ES, Zaks-Makhina E, 2006 Identification of gamma-aminobutyric acid receptor-interacting factor 1 (TRAK2) as a trafficking factor for the K+ channel Kir2.1. J Biol Chem 281, 30104– 30111. 16895905
  54. Guescini M, Genedani S, Stocchi V, Agnati LF, 2010 Astrocytes and Glioblastoma cells release exosomes carrying mtDNA. J Neural Transm (Vienna) 117, 1– 4. 19680595
  55. Guo X, Macleod GT, Wellington A, Hu F, Panchumarthi S, Schoenfield M, Marin L, Charlton MP, Atwood HL, Zinsmaier KE, 2005 The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses. Neuron 47, 379– 393. 16055062
  56. Haghnia M, Cavalli V, Shah SB, Schimmelpfeng K, Brusch R, Yang G, Herrera C, Pilling A, Goldstein LS, 2007 Dynactin is required for coordinated bidirectional motility, but not for dynein membrane attachment. Mol Biol Cell 18, 2081– 2089. 17360970 PMC1877108
  57. Han H, Hu J, Yan Q, Zhu J, Zhu Z, Chen Y, Sun J, Zhang R, 2016 Bone marrow-derived mesenchymal stem cells rescue injured H9c2 cells via transferring intact mitochondria through tunneling nanotubes in an in vitro simulated ischemia/reperfusion model. Mol Med Rep 13, 1517– 1524. 26718099 PMC4732861
  58. Harris JJ, Jolivet R, Attwell D, 2012 Synaptic energy use and supply. Neuron 75, 762– 777. 22958818
  59. Hayakawa K, Bruzzese M, Chou SH, Ning M, Ji X, Lo EH, 2018a Extracellular Mitochondria for Therapy and Diagnosis in Acute Central Nervous System Injury. JAMA Neurol 75, 119– 122. 29159397 PMC8305970
  60. Hayakawa K, Chan SJ, Mandeville ET, Park JH, Bruzzese M, Montaner J, Arai K, Rosell A, Lo EH, 2018b Protective Effects of Endothelial Progenitor Cell-Derived Extracellular Mitochondria in Brain Endothelium. Stem Cells 36, 1404– 1410. 29781122 PMC6407639
  61. Hayakawa K, Esposito E, Wang X, Terasaki Y, Liu Y, Xing C, Ji X, Lo EH, 2016 Transfer of mitochondria from astrocytes to neurons after stroke. Nature 535, 551– 555. 27466127 PMC4968589
  62. Hervera A, De Virgiliis F, Palmisano I, Zhou L, Tantardini E, Kong G, Hutson T, Danzi MC, Perry RB, Santos CXC, Kapustin AN, Fleck RA, Del Rio JA, Carroll T, Lemmon V, Bixby JL, Shah AM, Fainzilber M, Di Giovanni S, 2018 Reactive oxygen species regulate axonal regeneration through the release of exosomal NADPH oxidase 2 complexes into injured axons. Nat Cell Biol 20, 307– 319. 29434374
  63. Heyck M, Bonsack B, Zhang H, Sadanandan N, Cozene B, Kingsbury C, Lee JY, Borlongan CV, 2019 Highlight article: The brain and eye: Treating cerebral and retinal ischemia through mitochondrial transfer. Exp Biol Med (Maywood) 244, 1485– 1492. 31604382 PMC6900702
  64. Hirokawa N, Niwa S, Tanaka Y, 2010 Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron 68, 610– 638. 21092854
  65. Hollenbeck PJ, 1996 The pattern and mechanism of mitochondrial transport in axons. Front Biosci 1, d91– 102. 9159217
  66. Hollenbeck PJ, 2005 Mitochondria and neurotransmission: evacuating the synapse. Neuron 47, 331– 333. 16055057 PMC2538582
  67. Hollenbeck PJ, Saxton WM, 2005 The axonal transport of mitochondria. J Cell Sci 118, 5411– 5419. 16306220 PMC1533994
  68. Huang L, Nakamura Y, Lo EH, Hayakawa K, 2019 Astrocyte Signaling in the Neurovascular Unit After Central Nervous System Injury. Int J Mol Sci 20. PMC6358919 30642007
  69. Huang PJ, Kuo CC, Lee HC, Shen CI, Cheng FC, Wu SF, Chang JC, Pan HC, Lin SZ, Liu CS, Su HL, 2016 Transferring Xenogenic Mitochondria Provides Neural Protection Against Ischemic Stress in Ischemic Rat Brains. Cell Transplant 25, 913– 927. 26555763
  70. Hubley MJ, Locke BR, Moerland TS, 1996 The effects of temperature, pH, and magnesium on the diffusion coefficient of ATP in solutions of physiological ionic strength. Biochim Biophys Acta 1291, 115– 121. 8898871
  71. Iadecola C, Nedergaard M, 2007 Glial regulation of the cerebral microvasculature. Nat Neurosci 10, 1369– 1376. 17965657
  72. Jackson MV, Morrison TJ, Doherty DF, McAuley DF, Matthay MA, Kissenpfennig A, O’Kane CM, Krasnodembskaya AD, 2016 Mitochondrial Transfer via Tunneling Nanotubes is an Important Mechanism by Which Mesenchymal Stem Cells Enhance Macrophage Phagocytosis in the In Vitro and In Vivo Models of ARDS. Stem Cells 34, 2210– 2223. 27059413 PMC4982045
  73. Jakobs S, 2006 High resolution imaging of live mitochondria. Biochim Biophys Acta 1763, 561– 575. 16750866
  74. Jin H, Kanthasamy A, Ghosh A, Anantharam V, Kalyanaraman B, Kanthasamy AG, 2014 Mitochondria-targeted antioxidants for treatment of Parkinson’s disease: preclinical and clinical outcomes. Biochim Biophys Acta 1842, 1282– 1294. 24060637 PMC3961561
  75. Kanai Y, Okada Y, Tanaka Y, Harada A, Terada S, Hirokawa N, 2000 KIF5C, a novel neuronal kinesin enriched in motor neurons. J Neurosci 20, 6374– 6384. 10964943 PMC6772948
  76. Kang JS, Tian JH, Pan PY, Zald P, Li C, Deng C, Sheng ZH, 2008 Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation. Cell 132, 137– 148. 18191227 PMC2259239
  77. Karki S, Holzbaur EL, 1999 Cytoplasmic dynein and dynactin in cell division and intracellular transport. Curr Opin Cell Biol 11, 45– 53. 10047518
  78. Kaza AK, Wamala I, Friehs I, Kuebler JD, Rathod RH, Berra I, Ericsson M, Yao R, Thedsanamoorthy JK, Zurakowski D, Levitsky S, Del Nido PJ, Cowan DB, McCully JD, 2017 Myocardial rescue with autologous mitochondrial transplantation in a porcine model of ischemia/reperfusion. J Thorac Cardiovasc Surg 153, 934– 943. 27938904
  79. Kesner EE, Saada-Reich A, Lorberboum-Galski H, 2016 Characteristics of Mitochondrial Transformation into Human Cells. Sci Rep 6, 26057. 27184109 PMC4868981
  80. Khakh BS, Beaumont V, Cachope R, Munoz-Sanjuan I, Goldman SA, Grantyn R, 2017 Unravelling and Exploiting Astrocyte Dysfunction in Huntington’s Disease. Trends Neurosci 40, 422– 437. 28578789 PMC5706770
  81. Khakh BS, Sofroniew MV, 2015 Diversity of astrocyte functions and phenotypes in neural circuits. Nat Neurosci 18, 942– 952. 26108722 PMC5258184
  82. King SJ, Schroer TA, 2000 Dynactin increases the processivity of the cytoplasmic dynein motor. Nat Cell Biol 2, 20– 24. 10620802
  83. Kirk E, Chin LS, Li L, 2006 GRIF1 binds Hrs and is a new regulator of endosomal trafficking. J Cell Sci 119, 4689– 4701. 17062640
  84. Koyanagi M, Brandes RP, Haendeler J, Zeiher AM, 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. 15879310
  85. Langford GM, 2002 Myosin-V, a versatile motor for short-range vesicle transport. Traffic 3, 859– 865. 12453149
  86. Li X, Zhang Y, Yeung SC, Liang Y, Liang X, Ding Y, Ip MS, Tse HF, Mak JC, 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. 24738760
  87. Lippert T, Borlongan CV, 2019 Prophylactic treatment of hyperbaric oxygen treatment mitigates inflammatory response via mitochondria transfer. CNS Neurosci Ther 25, 815– 823. 30972972 PMC6630002
  88. Liu CS, Chang JC, Kuo SJ, Liu KH, Lin TT, Cheng WL, Chuang SF, 2014a Delivering healthy mitochondria for the therapy of mitochondrial diseases and beyond. Int J Biochem Cell Biol 53, 141– 146. 24842105
  89. Liu F, Lu J, Manaenko A, Tang J, Hu Q, 2018 Mitochondria in Ischemic Stroke: New Insight and Implications. Aging Dis 9, 924– 937. 30271667 PMC6147588
  90. Liu K, Guo L, Zhou Z, Pan M, Yan C, 2019 Mesenchymal stem cells transfer mitochondria into cerebral microvasculature and promote recovery from ischemic stroke. Microvasc Res 123, 74– 80. 30611747
  91. Liu K, Ji K, Guo L, Wu W, Lu H, Shan P, Yan C, 2014b 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. 24486322
  92. Lyamzaev KG, Nepryakhina OK, Saprunova VB, Bakeeva LE, Pletjushkina OY, Chernyak BV, Skulachev VP, 2008 Novel mechanism of elimination of malfunctioning mitochondria (mitoptosis): formation of mitoptotic bodies and extrusion of mitochondrial material from the cell. Biochim Biophys Acta 1777, 817– 825. 18433711
  93. Macaskill AF, Rinholm JE, Twelvetrees AE, Arancibia-Carcamo IL, Muir J, Fransson A, Aspenstrom P, Attwell D, Kittler JT, 2009 Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 61, 541– 555. 19249275 PMC2670979
  94. Macheiner T, Fengler VH, Agreiter M, Eisenberg T, Madeo F, Kolb D, Huppertz B, Ackbar R, Sargsyan K, 2016 Magnetomitotransfer: An efficient way for direct mitochondria transfer into cultured human cells. Sci Rep 6, 35571. 27767193 PMC5073296
  95. Maeda A, Fadeel B, 2014 Mitochondria released by cells undergoing TNF-alpha-induced necroptosis act as danger signals. Cell Death Dis 5, e1312. 24991764 PMC4123071
  96. Mandal A, Drerup CM, 2019 Axonal Transport and Mitochondrial Function in Neurons. Front Cell Neurosci 13, 373. 31447650 PMC6696875
  97. Marchi S, Patergnani S, Missiroli S, Morciano G, Rimessi A, Wieckowski MR, Giorgi C, Pinton P, 2018 Mitochondrial and endoplasmic reticulum calcium homeostasis and cell death. Cell Calcium 69, 62– 72. 28515000
  98. Masuzawa A, Black KM, Pacak CA, Ericsson M, Barnett RJ, Drumm C, Seth P, Bloch DB, Levitsky S, Cowan DB, McCully JD, 2013 Transplantation of autologously derived mitochondria protects the heart from ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 304, H966– 982. 23355340 PMC3625892
  99. McCully JD, Emani SM, Del Nido PJ, 2020 Letter by McCully et al Regarding Article, “Mitochondria Do Not Survive Calcium Overload”. Circ Res 126, e56– e57. 32271682
  100. McCully JD, Levitsky S, Del Nido PJ, Cowan DB, 2016 Mitochondrial transplantation for therapeutic use. Clin Transl Med 5, 16. 27130633 PMC4851669
  101. McLelland GL, Soubannier V, Chen CX, McBride HM, Fon EA, 2014 Parkin and PINK1 function in a vesicular trafficking pathway regulating mitochondrial quality control. EMBO J 33, 282– 295. 24446486 PMC3989637
  102. Melkov A, Abdu U, 2018 Regulation of long-distance transport of mitochondria along microtubules. Cell Mol Life Sci 75, 163– 176. 28702760 PMC11105322
  103. Miller KE, Sheetz MP, 2004 Axonal mitochondrial transport and potential are correlated. J Cell Sci 117, 2791– 2804. 15150321
  104. Mishra P, Chan DC, 2014 Mitochondrial dynamics and inheritance during cell division, development and disease. Nat Rev Mol Cell Biol 15, 634– 646. 25237825 PMC4250044
  105. Mistry JJ, Marlein CR, Moore JA, Hellmich C, Wojtowicz EE, Smith JGW, Macaulay I, Sun Y, Morfakis A, Patterson A, Horton RH, Divekar D, Morris CJ, Haestier A, Di Palma F, Beraza N, Bowles KM, Rushworth SA, 2019 ROS-mediated PI3K activation drives mitochondrial transfer from stromal cells to hematopoietic stem cells in response to infection. Proc Natl Acad Sci U S A 116, 24610– 24619. 31727843 PMC6900710
  106. Morris RL, Hollenbeck PJ, 1993 The regulation of bidirectional mitochondrial transport is coordinated with axonal outgrowth. J Cell Sci 104 (Pt 3), 917– 927. 8314882
  107. Morrison TJ, Jackson MV, Cunningham EK, Kissenpfennig A, McAuley DF, O’Kane CM, Krasnodembskaya AD, 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. 28598224 PMC5694830
  108. Morshed M, Hlushchuk R, Simon D, Walls AF, Obata-Ninomiya K, Karasuyama H, Djonov V, Eggel A, Kaufmann T, Simon HU, Yousefi S, 2014 NADPH oxidase-independent formation of extracellular DNA traps by basophils. J Immunol 192, 5314– 5323. 24771850
  109. Moschoi R, Imbert V, Nebout M, Chiche J, Mary D, Prebet T, Saland E, Castellano R, Pouyet L, Collette Y, Vey N, Chabannon C, Recher C, Sarry JE, Alcor D, Peyron JF, Griessinger E, 2016 Protective mitochondrial transfer from bone marrow stromal cells to acute myeloid leukemic cells during chemotherapy. Blood 128, 253– 264. 27257182
  110. Nakajima A, Kurihara H, Yagita H, Okumura K, Nakano H, 2008 Mitochondrial Extrusion through the cytoplasmic vacuoles during cell death. J Biol Chem 283, 24128– 24135. 18593703 PMC3259776
  111. Nakamura Y, Park JH, Hayakawa K, 2020 Therapeutic use of extracellular mitochondria in CNS injury and disease. Exp Neurol 324, 113114. 31734316 PMC6980730
  112. Neuspiel M, Schauss AC, Braschi E, Zunino R, Rippstein P, Rachubinski RA, Andrade-Navarro MA, McBride HM, 2008 Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers. Curr Biol 18, 102– 108. 18207745
  113. Nicholls DG, Budd SL, 2000 Mitochondria and neuronal survival. Physiol Rev 80, 315– 360. 10617771
  114. Nukala VN, Singh IN, Davis LM, Sullivan PG, 2006 Cryopreservation of brain mitochondria: a novel methodology for functional studies. J Neurosci Methods 152, 48– 54. 16246427
  115. Oeding SJ, Majstrowicz K, Hu XP, Schwarz V, Freitag A, Honnert U, Nikolaus P, Bahler M, 2018 Identification of Miro1 and Miro2 as mitochondrial receptors for myosin XIX. J Cell Sci 131. 30111583
  116. Ohno N, Kidd GJ, Mahad D, Kiryu-Seo S, Avishai A, Komuro H, Trapp BD, 2011 Myelination and axonal electrical activity modulate the distribution and motility of mitochondria at CNS nodes of Ranvier. J Neurosci 31, 7249– 7258. 21593309 PMC3139464
  117. Otsu K, Das S, Houser SD, Quadri SK, Bhattacharya S, Bhattacharya J, 2009 Concentration-dependent inhibition of angiogenesis by mesenchymal stem cells. Blood 113, 4197– 4205. 19036701 PMC2676081
  118. Ouyang YB, Xu L, Lu Y, Sun X, Yue S, Xiong XX, Giffard RG, 2013 Astrocyte-enriched miR-29a targets PUMA and reduces neuronal vulnerability to forebrain ischemia. Glia 61, 1784– 1794. 24038396 PMC3810393
  119. Pacak CA, Preble JM, Kondo H, Seibel P, Levitsky S, Del Nido PJ, Cowan DB, McCully JD, 2015 Actin-dependent mitochondrial internalization in cardiomyocytes: evidence for rescue of mitochondrial function. Biol Open 4, 622– 626. 25862247 PMC4434813
  120. Paliwal S, Chaudhuri R, Agrawal A, Mohanty S, 2018 Regenerative abilities of mesenchymal stem cells through mitochondrial transfer. J Biomed Sci 25, 31. 29602309 PMC5877369
  121. Pallafacchina G, Zanin S, Rizzuto R, 2018 Recent advances in the molecular mechanism of mitochondrial calcium uptake. F1000Res 7. PMC6263489 30555683
  122. Paolicelli RC, Bergamini G, Rajendran L, 2019 Cell-to-cell Communication by Extracellular Vesicles: Focus on Microglia. Neuroscience 405, 148– 157. 29660443
  123. Park JS, Davis RL, Sue CM, 2018 Mitochondrial Dysfunction in Parkinson’s Disease: New Mechanistic Insights and Therapeutic Perspectives. Curr Neurol Neurosci Rep 18, 21. 29616350 PMC5882770
  124. Pasquier J, Guerrouahen BS, Al Thawadi H, Ghiabi P, Maleki M, Abu-Kaoud N, Jacob A, Mirshahi M, Galas L, Rafii S, Le Foll F, Rafii A, 2013 Preferential transfer of mitochondria from endothelial to cancer cells through tunneling nanotubes modulates chemoresistance. J Transl Med 11, 94. 23574623 PMC3668949
  125. Patananan AN, Wu TH, Chiou PY, Teitell MA, 2016 Modifying the Mitochondrial Genome. Cell Metab 23, 785– 796. 27166943 PMC4864607
  126. Pilling AD, Horiuchi D, Lively CM, Saxton WM, 2006 Kinesin-1 and Dynein are the primary motors for fast transport of mitochondria in Drosophila motor axons. Mol Biol Cell 17, 2057– 2068. 16467387 PMC1415296
  127. Pitt JM, Kroemer G, Zitvogel L, 2016 Extracellular vesicles: masters of intercellular communication and potential clinical interventions. J Clin Invest 126, 1139– 1143. 27035805 PMC4811136
  128. Popkov VA, Plotnikov EY, Silachev DN, Zorova LD, Pevzner IB, Jankauskas SS, Zorov SD, Andrianova NV, Babenko VA, Zorov DB, 2017 Bacterial Therapy and Mitochondrial Therapy. Biochemistry (Mosc) 82, 1549– 1556. 29486705
  129. Porter KR, Claude A, Fullam EF, 1945 A Study of Tissue Culture Cells by Electron Microscopy: Methods and Preliminary Observations. J Exp Med 81, 233– 246. 19871454 PMC2135493
  130. Quintero OA, DiVito MM, Adikes RC, Kortan MB, Case LB, Lier AJ, Panaretos NS, Slater SQ, Rengarajan M, Feliu M, Cheney RE, 2009 Human Myo19 is a novel myosin that associates with mitochondria. Curr Biol 19, 2008– 2013. 19932026 PMC2805763
  131. Ramirez-Barbieri G, Moskowitzova K, Shin B, Blitzer D, Orfany A, Guariento A, Iken K, Friehs I, Zurakowski D, Del Nido PJ, McCully JD, 2019 Alloreactivity and allorecognition of syngeneic and allogeneic mitochondria. Mitochondrion 46, 103– 115. 29588218
  132. Rintoul GL, Filiano AJ, Brocard JB, Kress GJ, Reynolds IJ, 2003 Glutamate decreases mitochondrial size and movement in primary forebrain neurons. J Neurosci 23, 7881– 7888. 12944518 PMC6740596
  133. Robicsek O, Ene HM, Karry R, Ytzhaki O, Asor E, McPhie D, Cohen BM, Ben-Yehuda R, Weiner I, 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. 28586483 PMC5814822
  134. Rocca CJ, Goodman SM, Dulin JN, Haquang JH, Gertsman I, Blondelle J, Smith JLM, Heyser CJ, Cherqui S, 2017 Transplantation of wild-type mouse hematopoietic stem and progenitor cells ameliorates deficits in a mouse model of Friedreich’s ataxia. Sci Transl Med 9. PMC5735830 29070698
  135. Rogers RS, Bhattacharya J, 2013 When cells become organelle donors. Physiology (Bethesda) 28, 414– 422. 24186936
  136. Roushandeh AM, Kuwahara Y, Roudkenar MH, 2019 Mitochondrial transplantation as a potential and novel master key for treatment of various incurable diseases. Cytotechnology 71, 647– 663. 30706303 PMC6465382
  137. Russo E, Nguyen H, Lippert T, Tuazon J, Borlongan CV, Napoli E, 2018 Mitochondrial targeting as a novel therapy for stroke. Brain Circ 4, 84– 94. 30450413 PMC6187947
  138. Rustom A, Saffrich R, Markovic I, Walther P, Gerdes HH, 2004 Nanotubular highways for intercellular organelle transport. Science 303, 1007– 1010. 14963329
  139. Sansone P, Savini C, Kurelac I, Chang Q, Amato LB, Strillacci A, Stepanova A, Iommarini L, Mastroleo C, Daly L, Galkin A, Thakur BK, Soplop N, Uryu K, Hoshino A, Norton L, Bonafe M, Cricca M, Gasparre G, Lyden D, Bromberg J, 2017 Packaging and transfer of mitochondrial DNA via exosomes regulate escape from dormancy in hormonal therapy-resistant breast cancer. Proc Natl Acad Sci U S A 114, E9066– E9075. 29073103 PMC5664494
  140. Saotome M, Safiulina D, Szabadkai G, Das S, Fransson A, Aspenstrom P, Rizzuto R, Hajnoczky G, 2008 Bidirectional Ca2+-dependent control of mitochondrial dynamics by the Miro GTPase. Proc Natl Acad Sci U S A 105, 20728– 20733. 19098100 PMC2634948
  141. Sato M, Sato K, 2011 Degradation of paternal mitochondria by fertilization-triggered autophagy in C. elegans embryos. Science 334, 1141– 1144. 21998252
  142. Saxton WM, Hollenbeck PJ, 2012 The axonal transport of mitochondria. J Cell Sci 125, 2095– 2104. 22619228 PMC3656622
  143. Schwarz TL, 2013 Mitochondrial trafficking in neurons. Cold Spring Harb Perspect Biol 5. PMC3660831 23732472
  144. Sena LA, Chandel NS, 2012 Physiological roles of mitochondrial reactive oxygen species. Mol Cell 48, 158– 167. 23102266 PMC3484374
  145. Sheng ZH, 2014 Mitochondrial trafficking and anchoring in neurons: New insight and implications. J Cell Biol 204, 1087– 1098. 24687278 PMC3971748
  146. Shi X, Zhao M, Fu C, Fu A, 2017 Intravenous administration of mitochondria for treating experimental Parkinson’s disease. Mitochondrion 34, 91– 100. 28242362
  147. Shin B, Saeed MY, Esch JJ, Guariento A, Blitzer D, Moskowitzova K, Ramirez-Barbieri G, Orfany A, Thedsanamoorthy JK, Cowan DB, Inkster JA, Snay ER, Staffa SJ, Packard AB, Zurakowski D, Del Nido PJ, McCully JD, 2019 A Novel Biological Strategy for Myocardial Protection by Intracoronary Delivery of Mitochondria: Safety and Efficacy. JACC Basic Transl Sci 4, 871– 888. 31909298 PMC6938990
  148. Singh A, Kukreti R, Saso L, Kukreti S, 2019 Oxidative Stress: A Key Modulator in Neurodegenerative Diseases. Molecules 24. PMC6514564 31013638
  149. Sinha P, Islam MN, Bhattacharya S, Bhattacharya J, 2016 Intercellular mitochondrial transfer: bioenergetic crosstalk between cells. Curr Opin Genet Dev 38, 97– 101. 27235808 PMC5067171
  150. Soubannier V, McLelland GL, Zunino R, Braschi E, Rippstein P, Fon EA, McBride HM, 2012a A vesicular transport pathway shuttles cargo from mitochondria to lysosomes. Curr Biol 22, 135– 141. 22226745
  151. Soubannier V, Rippstein P, Kaufman BA, Shoubridge EA, McBride HM, 2012b Reconstitution of mitochondria derived vesicle formation demonstrates selective enrichment of oxidized cargo. PLoS One 7, e52830. 23300790 PMC3530470
  152. Spees JL, Olson SD, Whitney MJ, Prockop DJ, 2006 Mitochondrial transfer between cells can rescue aerobic respiration. Proc Natl Acad Sci U S A 103, 1283– 1288. 16432190 PMC1345715
  153. Stefanatos R, Sanz A, 2018 The role of mitochondrial ROS in the aging brain. FEBS Lett 592, 743– 758. 29106705
  154. Stowers RS, Megeath LJ, Gorska-Andrzejak J, Meinertzhagen IA, Schwarz TL, 2002 Axonal transport of mitochondria to synapses depends on milton, a novel Drosophila protein. Neuron 36, 1063– 1077. 12495622
  155. Suen DF, Narendra DP, Tanaka A, Manfredi G, Youle RJ, 2010 Parkin overexpression selects against a deleterious mtDNA mutation in heteroplasmic cybrid cells. Proc Natl Acad Sci U S A 107, 11835– 11840. 20547844 PMC2900690
  156. Sugiura A, McLelland GL, Fon EA, McBride HM, 2014 A new pathway for mitochondrial quality control: mitochondrial-derived vesicles. EMBO J 33, 2142– 2156. 25107473 PMC4282503
  157. Sun X, Wang Y, Zhang J, Tu J, Wang XJ, Su XD, Wang L, Zhang Y, 2012 Tunneling-nanotube direction determination in neurons and astrocytes. Cell Death Dis 3, e438. 23222508 PMC3542613
  158. Szabadkai G, Simoni AM, Bianchi K, De Stefani D, Leo S, Wieckowski MR, Rizzuto R, 2006 Mitochondrial dynamics and Ca2+ signaling. Biochim Biophys Acta 1763, 442– 449. 16750865
  159. Szymanski J, Janikiewicz J, Michalska B, Patalas-Krawczyk P, Perrone M, Ziolkowski W, Duszynski J, Pinton P, Dobrzyn A, Wieckowski MR, 2017 Interaction of Mitochondria with the Endoplasmic Reticulum and Plasma Membrane in Calcium Homeostasis, Lipid Trafficking and Mitochondrial Structure. Int J Mol Sci 18. PMC5536064 28726733
  160. Tan AS, Baty JW, Dong LF, Bezawork-Geleta A, Endaya B, Goodwin J, Bajzikova M, Kovarova J, Peterka M, Yan B, Pesdar EA, Sobol M, Filimonenko A, Stuart S, Vondrusova M, Kluckova K, Sachaphibulkij K, Rohlena J, Hozak P, Truksa J, Eccles D, Haupt LM, Griffiths LR, Neuzil J, Berridge MV, 2015 Mitochondrial genome acquisition restores respiratory function and tumorigenic potential of cancer cells without mitochondrial DNA. Cell Metab 21, 81– 94. 25565207
  161. Tomasi D, Wang GJ, Volkow ND, 2013 Energetic cost of brain functional connectivity. Proc Natl Acad Sci U S A 110, 13642– 13647. 23898179 PMC3746878
  162. Trias E, Barbeito L, Yamanaka K, 2018 Phenotypic heterogeneity of astrocytes in motor neuron disease. Clin Exp Neuroimmunol 9, 225– 234. 30555538 PMC6282976
  163. Unuma K, Aki T, Funakoshi T, Hashimoto K, Uemura K, 2015 Extrusion of mitochondrial contents from lipopolysaccharide-stimulated cells: Involvement of autophagy. Autophagy 11, 1520– 1536. 26102061 PMC4590602
  164. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO, 2007 Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9, 654– 659. 17486113
  165. Valenci I, Yonai L, Bar-Yaacov D, Mishmar D, Ben-Zvi A, 2015 Parkin modulates heteroplasmy of truncated mtDNA in Caenorhabditis elegans. Mitochondrion 20, 64– 70. 25462019
  166. van Spronsen M, Mikhaylova M, Lipka J, Schlager MA, van den Heuvel DJ, Kuijpers M, Wulf PS, Keijzer N, Demmers J, Kapitein LC, Jaarsma D, Gerritsen HC, Akhmanova A, Hoogenraad CC, 2013 TRAK/Milton motor-adaptor proteins steer mitochondrial trafficking to axons and dendrites. Neuron 77, 485– 502. 23395375
  167. Voloboueva LA, Suh SW, Swanson RA, Giffard RG, 2007 Inhibition of mitochondrial function in astrocytes: implications for neuroprotection. J Neurochem 102, 1383– 1394. 17488276 PMC3175820
  168. Wallace DC, 2018 Mitochondrial genetic medicine. Nat Genet 50, 1642– 1649. 30374071
  169. Wang W, Karamanlidis G, Tian R, 2016 Novel targets for mitochondrial medicine. Sci Transl Med 8, 326rv323. PMC4819426 26888432
  170. Wang X, Gerdes HH, 2011 Long-distance electrical coupling via tunneling nanotubes. Biochim Biophys Acta 1818, 2082– 2086. 21930113
  171. Wang X, Schwarz TL, 2009 The mechanism of Ca2+ -dependent regulation of kinesin-mediated mitochondrial motility. Cell 136, 163– 174. 19135897 PMC2768392
  172. Wang X, Winter D, Ashrafi G, Schlehe J, Wong YL, Selkoe D, Rice S, Steen J, LaVoie MJ, Schwarz TL, 2011 PINK1 and Parkin target Miro for phosphorylation and degradation to arrest mitochondrial motility. Cell 147, 893– 906. 22078885 PMC3261796
  173. Wang XF, Cynader MS, 2001 Pyruvate released by astrocytes protects neurons from copper-catalyzed cysteine neurotoxicity. J Neurosci 21, 3322– 3331. 11331361 PMC6762471
  174. Waterman-Storer CM, Karki S, Holzbaur EL, 1995 The p150Glued component of the dynactin complex binds to both microtubules and the actin-related protein centractin (Arp-1). Proc Natl Acad Sci U S A 92, 1634– 1638. 7878030 PMC42574
  175. Webber E, Li L, Chin LS, 2008 Hypertonia-associated protein Trak1 is a novel regulator of endosome-to-lysosome trafficking. J Mol Biol 382, 638– 651. 18675823 PMC2575741
  176. Weihofen A, Thomas KJ, Ostaszewski BL, Cookson MR, Selkoe DJ, 2009 Pink1 forms a multiprotein complex with Miro and Milton, linking Pink1 function to mitochondrial trafficking. Biochemistry 48, 2045– 2052. 19152501 PMC2693257
  177. Wu TH, Sagullo E, Case D, Zheng X, Li Y, Hong JS, TeSlaa T, Patananan AN, McCaffery JM, Niazi K, Braas D, Koehler CM, Graeber TG, Chiou PY, Teitell MA, 2016 Mitochondrial Transfer by Photothermal Nanoblade Restores Metabolite Profile in Mammalian Cells. Cell Metab 23, 921– 929. 27166949 PMC5062745
  178. Yamaguchi R, Andreyev A, Murphy AN, Perkins GA, Ellisman MH, Newmeyer DD, 2007 Mitochondria frozen with trehalose retain a number of biological functions and preserve outer membrane integrity. Cell Death Differ 14, 616– 624. 16977331
  179. Yang H, Borg TK, Ma Z, Xu M, Wetzel G, Saraf LV, Markwald R, Runyan RB, Gao BZ, 2016 Biochip-based study of unidirectional mitochondrial transfer from stem cells to myocytes via tunneling nanotubes. Biofabrication 8, 015012. 26844857
  180. Yang Z, Steele DS, 2000 Effects of cytosolic ATP on spontaneous and triggered Ca2+-induced Ca2+ release in permeabilised rat ventricular myocytes. J Physiol 523 Pt 1, 29– 44. 10673543 PMC2269793
  181. Yao Y, Fan XL, Jiang D, Zhang Y, Li X, Xu ZB, Fang SB, Chiu S, Tse HF, Lian Q, Fu QL, 2018 Connexin 43-Mediated Mitochondrial Transfer of iPSC-MSCs Alleviates Asthma Inflammation. Stem Cell Reports 11, 1120– 1135. 30344008 PMC6234920
  182. Yi M, Weaver D, Hajnoczky G, 2004 Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J Cell Biol 167, 661– 672. 15545319 PMC2172592
  183. Yousefi S, Gold JA, Andina N, Lee JJ, Kelly AM, Kozlowski E, Schmid I, Straumann A, Reichenbach J, Gleich GJ, Simon HU, 2008 Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense. Nat Med 14, 949– 953. 18690244
  184. Yun SP, Kam TI, Panicker N, Kim S, Oh Y, Park JS, Kwon SH, Park YJ, Karuppagounder SS, Park H, Kim S, Oh N, Kim NA, Lee S, Brahmachari S, Mao X, Lee JH, Kumar M, An D, Kang SU, Lee Y, Lee KC, Na DH, Kim D, Lee SH, Roschke VV, Liddelow SA, Mari Z, Barres BA, Dawson VL, Lee S, Dawson TM, Ko HS, 2018 Block of A1 astrocyte conversion by microglia is neuroprotective in models of Parkinson’s disease. Nat Med 24, 931– 938. 29892066 PMC6039259
  185. Zappulli V, Friis KP, Fitzpatrick Z, Maguire CA, Breakefield XO, 2016 Extracellular vesicles and intercellular communication within the nervous system. J Clin Invest 126, 1198– 1207. 27035811 PMC4811121
  186. Zhang Z, Ma Z, Yan C, Pu K, Wu M, Bai J, Li Y, Wang Q, 2019 Muscle-derived autologous mitochondrial transplantation: A novel strategy for treating cerebral ischemic injury. Behav Brain Res 356, 322– 331. 30213662
  187. Zhu XH, Qiao H, Du F, Xiong Q, Liu X, Zhang X, Ugurbil K, Chen W, 2012 Quantitative imaging of energy expenditure in human brain. Neuroimage 60, 2107– 2117. 22487547 PMC3325488

Cited by

Sorted by citations

Authors
Shanmughapriya, S., Langford, D., & Natarajaseenivasan, K.
Affiliations
  • Pennsylvania State University (US)
  • Temple University (US)
  • Bharathidasan University (IN)
Corresponding author
Natarajaseenivasan, Kalimuthusamy
ORCID
Venue
Ageing Research Reviews
Publisher
Elsevier BV
Published
2020-09
Volume
62
Pages
101128
ISSN
1568-1637 (ISSN-L)
DOI
10.1016/j.arr.2020.101128
PMC
PMC7484258
OpenAlex
W3045291713
Cited by
171
References
21
Citations by year
2026: 30 · 2025: 35 · 2024: 44 · 2023: 24 · 2022: 18 · 2021: 18 · 2020: 2
FWCI
1.51
Type
journal article
Language
en
Open access
Licence
Locations
  • Ageing Research Reviews (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institutes of Health (R01 MH107340, K99/R00 4R00HL138268-03)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
  • Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
Keywords
mitochondrial trafficking, intercellular communication, mitochondrial quality control, mitochondrial disease
MeSH terms
Cell Movement, Central Nervous System, Humans, Mitochondria, Neurons, Protein Transport

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review