Recommendations for mitochondria transfer and transplantation nomenclature and characterization
Jazyk angličtina Země Německo Médium print-electronic
Typ dokumentu časopisecké články, přehledy
Grantová podpora
CAMS #1019648
Burroughs Wellcome Fund (BWF)
PubMed
39820558
DOI
10.1038/s42255-024-01200-x
PII: 10.1038/s42255-024-01200-x
Knihovny.cz E-zdroje
- MeSH
- lidé MeSH
- mitochondrie * metabolismus MeSH
- terminologie jako téma * MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Intercellular mitochondria transfer is an evolutionarily conserved process in which one cell delivers some of their mitochondria to another cell in the absence of cell division. This process has diverse functions depending on the cell types involved and physiological or disease context. Although mitochondria transfer was first shown to provide metabolic support to acceptor cells, recent studies have revealed diverse functions of mitochondria transfer, including, but not limited to, the maintenance of mitochondria quality of the donor cell and the regulation of tissue homeostasis and remodelling. Many mitochondria-transfer mechanisms have been described using a variety of names, generating confusion about mitochondria transfer biology. Furthermore, several therapeutic approaches involving mitochondria-transfer biology have emerged, including mitochondria transplantation and cellular engineering using isolated mitochondria. In this Consensus Statement, we define relevant terminology and propose a nomenclature framework to describe mitochondria transfer and transplantation as a foundation for further development by the community as this dynamic field of research continues to evolve.
Boston Children's Hospital Harvard Medical School Boston MA USA
Centro de Investigación Biomédica Facultad de Medicina Universidad de Los Andes Santiago Chile
Centro Nacional de Investigaciones Cardiovasculares Carlos 3 Madrid Spain
College of Pharmaceutical Sciences Zhejiang University Hangzhou China
Department of Biology University of Rome Tor Vergata Rome Italy
Department of Cancer Cell Biology Malaghan Institute of Medical Research Wellington New Zealand
Department of Cell Biology and Physiology Washington University School of Medicine St Louis MO USA
Department of Emergency Medicine Kindai University Faculty of Medicine Osaka Japan
Department of Emergency Medicine Northwell Health Manhassett NY USA
Department of Hematology and Oncology Graduate School of Medicine Osaka University Osaka Japan
Department of Medicine Brigham and Women's Hospital Boston MA USA
Department of Neurological Surgery University of Washington School of Medicine Seattle WA USA
Department of Pathology and Immunology Washington University School of Medicine St Louis MO USA
Department of Pharmacy 2nd Affiliated Hospital Zhejiang University School of Medicine Hangzhou China
Faculty of Science and 1st Faculty of Medicine Charles University Prague Czech Republic
Institute of Biotechnology Czech Academy of Sciences Prague Czech Republic
Mito Act Research Consortium Quito Ecuador
MitoWorld National Laboratory for Education Transformation Oakland CA USA
Montreal Neurological Institute McGill University Montreal Quebec Canada
New York State Psychiatric Institute New York NY USA
Perron Institute for Neurological and Translational Science Nedlands Western Australia Australia
School of Pharmacy and Medical Science Griffith University Southport Queensland Australia
Zobrazit více v PubMed
Monzel, A. S., Enríquez, J. A. & Picard, M. Multifaceted mitochondria: moving mitochondrial science beyond function and dysfunction. Nat. Metab. 5, 546–562 (2023). PubMed PMC
McBride, H. M., Neuspiel, M. & Wasiak, S. Mitochondria: more than just a powerhouse. Curr. Biol. 16, R551–R560 (2006). PubMed
Friedman, J. R. & Nunnari, J. Mitochondrial form and function. Nature 505, 335–343 (2014). PubMed PMC
Roger, A. J., Muñoz-Gómez, S. A. & Kamikawa, R. The origin and diversification of mitochondria. Curr. Biol. 27, R1177–r1192 (2017). PubMed
Srinivasainagendra, V. et al. Migration of mitochondrial DNA in the nuclear genome of colorectal adenocarcinoma. Genome Med. 9, 31 (2017). PubMed PMC
Geiger, O., Sanchez-Flores, A., Padilla-Gomez, J. & Degli Esposti, M. Multiple approaches of cellular metabolism define the bacterial ancestry of mitochondria. Sci. Adv. 9, eadh0066 (2023). PubMed PMC
Miao, L., Yin, Z., Knoll, A. H., Qu, Y. & Zhu, M. 1.63-billion-year-old multicellular eukaryotes from the Chuanlinggou Formation in North China. Sci. Adv. 10, eadk3208 (2024). PubMed PMC
Pennisi, E. The power of many. Science 360, 1388–1391 (2018). PubMed
Pennisi, E. Tiny fossils upend timeline of multicellular life. Science 383, 352–353 (2024). PubMed
Fukuda, H. & Kimura, A. Transfer of mitochondria into protoplasts of saccharomyces cerevisiae by mini-protoplast fusion. FEBS Lett. 113, 58–60 (1980). PubMed
Gunge, N. & Sakaguchi, K. Fusion of mitochondria with protoplasts in Saccharomyces cerevisiae. Mol. Gen. Genet 170, 243–247 (1979). PubMed
Yoshida, K. Interspecific and intraspecific mitochondria-induced cytoplasmic transformation in yeasts. Plant Cell Physiol. 20, 851–856 (1979).
Luo, Y. & Wang, W.-X. Increasing intercellular communication and directional organelle transfer in oyster hemocytes under copper stress. Environ. Sci. Technol. Lett. 10, 831–837 (2023).
Hutto, R. A. et al. Cone photoreceptors transfer damaged mitochondria to Müller glia. Cell Rep. 42, 112115 (2023). PubMed PMC
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). PubMed PMC
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). PubMed PMC
Bergthorsson, U., Adams, K. L., Thomason, B. & Palmer, J. D. Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424, 197–201 (2003). PubMed
Won, H. & Renner, S. S. Horizontal gene transfer from flowering plants to Gnetum. Proc. Natl Acad. Sci. USA 100, 10824–10829 (2003). PubMed PMC
Gurdon, C., Svab, Z., Feng, Y., Kumar, D. & Maliga, P. Cell-to-cell movement of mitochondria in plants. Proc. Natl Acad. Sci. USA 113, 3395–3400 (2016). PubMed PMC
Ferenczy, L. & MarÁZ, A. Transfer of mitochondria by protoplast fusion in Saccharomyces cerevisiae. Nature 268, 524–525 (1977). PubMed
Clark, M. A. & Shay, J. W. Mitochondrial transformation of mammalian cells. Nature 295, 605–607 (1982). PubMed
King, M. P. & Attardi, G. Injection of mitochondria into human cells leads to a rapid replacement of the endogenous mitochondrial DNA. Cell 52, 811–819 (1988). PubMed
Chomyn, A. et al. In vitro genetic transfer of protein synthesis and respiration defects to mitochondrial DNA-less cells with myopathy-patient mitochondria. Mol. Cell. Biol. 11, 2236–2244 (1991). PubMed PMC
Chomyn, A. et al. Platelet-mediated transformation of mtDNA-less human cells: analysis of phenotypic variability among clones from normal individuals–and complementation behavior of the tRNALys mutation causing myoclonic epilepsy and ragged red fibers. Am. J. Hum. Genet 54, 966–974 (1994). PubMed PMC
Manfredi, G., Thyagarajan, D., Papadopoulou, L. C., Pallotti, F. & Schon, E. A. The fate of human sperm-derived mtDNA in somatic cells. Am. J. Hum. Genet. 61, 953–960 (1997). PubMed PMC
Kulawiec, M., Owens, K. M. & Singh, K. K. mtDNA G10398A variant in African-American women with breast cancer provides resistance to apoptosis and promotes metastasis in mice. J. Hum. Genet. 54, 647–654 (2009). PubMed PMC
Katrangi, E. et al. Xenogenic transfer of isolated murine mitochondria into human rho0 cells can improve respiratory function. Rejuv. Res 10, 561–570 (2007).
Yoon, Y. G., Haug, C. L. & Koob, M. D. Interspecies mitochondrial fusion between mouse and human mitochondria is rapid and efficient. Mitochondrion 7, 223–229 (2007). PubMed
Rebbeck, C. A., Leroi, A. M. & Burt, A. Mitochondrial capture by a transmissible cancer. Science 331, 303 (2011). PubMed
Tan, A. S. et al. Mitochondrial genome acquisition restores respiratory function and tumorigenic potential of cancer cells without mitochondrial DNA. Cell Metab. 21, 81–94 (2015). PubMed
Dong, L. F. et al. Horizontal transfer of whole mitochondria restores tumorigenic potential in mitochondrial DNA-deficient cancer cells. eLife 6, e22187 (2017). PubMed PMC
Bajzikova, M. et al. Reactivation of dihydroorotate dehydrogenase-driven pyrimidine biosynthesis restores tumor growth of respiration-deficient cancer cells. Cell Metab. 29, 399–416.e310 (2019). PubMed
Lei, L. & Spradling, A. C. Mouse oocytes differentiate through organelle enrichment from sister cyst germ cells. Science 352, 95–99 (2016). PubMed PMC
Davis, C. H. et al. Transcellular degradation of axonal mitochondria. Proc. Natl Acad. Sci. USA 111, 9633–9638 (2014). PubMed PMC
Nicolás-Ávila, J. A. et al. A network of macrophages supports mitochondrial homeostasis in the heart. Cell 183, 94–109.e123 (2020). PubMed
Zhang, K. et al. TREM2hi resident macrophages protect the septic heart by maintaining cardiomyocyte homeostasis. Nat. Metab. 5, 129–146 (2023). PubMed PMC
Rosina, M. et al. Ejection of damaged mitochondria and their removal by macrophages ensure efficient thermogenesis in brown adipose tissue. Cell Metab. 34, 533–548.e512 (2022). PubMed PMC
Nicolás-Ávila, J. A., Pena-Couso, L., Muñoz-Cánoves, P. & Hidalgo, A. Macrophages, metabolism and heterophagy in the heart. Circ. Res. 130, 418–431 (2022). PubMed
Boudreau, L. H. et al. Platelets release mitochondria serving as substrate for bactericidal group IIA-secreted phospholipase A2 to promote inflammation. Blood 124, 2173–2183 (2014). PubMed PMC
Levoux, J. et al. Platelets facilitate the wound-healing capability of mesenchymal stem cells by mitochondrial transfer and metabolic reprogramming. Cell Metab. 33, 283–299.e289 (2021). PubMed
Hayakawa, K. et al. Transfer of mitochondria from astrocytes to neurons after stroke. Nature 535, 551–555 (2016). PubMed PMC
Joshi, A. U. et al. Fragmented mitochondria released from microglia trigger A1 astrocytic response and propagate inflammatory neurodegeneration. Nat. Neurosci. 22, 1635–1648 (2019). PubMed PMC
Zhou, J. et al. Astrocytic LRP1 enables mitochondria transfer to neurons and mitigates brain ischemic stroke by suppressing ARF1 lactylation. Cell Metab. 36, 2054–2068.e14 (2024). PubMed
Liu, D. et al. Regulation of blood-brain barrier integrity by Dmp1-expressing astrocytes through mitochondrial transfer. Sci. Adv. 10, eadk2913 (2024). PubMed PMC
van der Vlist, M. et al. Macrophages transfer mitochondria to sensory neurons to resolve inflammatory pain. Neuron 110, 613–626.e619 (2022). PubMed
Huang, T. et al. Efficient intervention for pulmonary fibrosis via mitochondrial transfer promoted by mitochondrial biogenesis. Nat. Commun. 14, 5781 (2023). PubMed PMC
Scozzi, D. et al. Mitochondrial damage–associated molecular patterns released by lung transplants are associated with primary graft dysfunction. Am. J. Transplant. 19, 1464–1477 (2019). PubMed PMC
Huang, T. et al. Iron oxide nanoparticles augment the intercellular mitochondrial transfer-mediated therapy. Sci. Adv. 7, eabj0534 (2021). PubMed PMC
Liang, W. et al. Mitochondria are secreted in extracellular vesicles when lysosomal function is impaired. Nat. Commun. 14, 5031 (2023). PubMed PMC
Brestoff, J. R. et al. Intercellular mitochondria transfer to macrophages regulates white adipose tissue homeostasis and is impaired in obesity. Cell Metab. 33, 270–282.e278 (2021). PubMed
Borcherding, N. et al. Dietary lipids inhibit mitochondria transfer to macrophages to divert adipocyte-derived mitochondria into blood. Cell Metab. 34, 1499–1513.e1498 (2022). PubMed PMC
Gao, J. et al. Endoplasmic reticulum mediates mitochondrial transfer within the osteocyte dendritic network. Sci. Adv. 5, eaaw7215 (2019). PubMed PMC
Suh, J. et al. Mitochondrial fragmentation and donut formation enhance mitochondrial secretion to promote osteogenesis. Cell Metab. 35, 345–360.e347 (2023). PubMed
Ding, P. et al. Mitochondria from osteolineage cells regulate myeloid cell-mediated bone resorption. Nat. Commun. 15, 5094 (2024). PubMed PMC
Yang, C. et al. Mitochondria transfer mediates stress erythropoiesis by altering the bioenergetic profiles of early erythroblasts through CD47. J. Exp. Med. 219, e20220685 (2022). PubMed PMC
Court, A. C. et al. Mitochondrial transfer from MSCs to T cells induces Treg differentiation and restricts inflammatory response. EMBO Rep. 21, e48052 (2020). PubMed PMC
Luz-Crawford, P. et al. Mesenchymal stem cell repression of Th17 cells is triggered by mitochondrial transfer. Stem Cell Res. Ther. 10, 232 (2019). PubMed PMC
Saha, T. et al. Intercellular nanotubes mediate mitochondrial trafficking between cancer and immune cells. Nat. Nanotechnol. 17, 98–106 (2022). PubMed
Kidwell, C. U. et al. Transferred mitochondria accumulate reactive oxygen species, promoting proliferation. eLife 12, e85494 (2023). PubMed PMC
Dache, Z. A. A. et al. Blood contains circulating cell-free respiratory competent mitochondria. FASEB J. 34, 3616–3630 (2020).
Crewe, C. et al. Extracellular vesicle-based interorgan transport of mitochondria from energetically stressed adipocytes. Cell Metab. 33, 1853–1868.e1811 (2021). PubMed PMC
Dong, L. F. et al. Mitochondria on the move: Horizontal mitochondrial transfer in disease and health. J. Cell Biol. 222, e202211044 (2023). PubMed PMC
Borcherding, N. & Brestoff, J. R. The power and potential of mitochondria transfer. Nature 623, 283–291 (2023). PubMed PMC
Liu, D. et al. Intercellular mitochondrial transfer as a means of tissue revitalization. Signal Transduct. Target Ther. 6, 65 (2021). PubMed PMC
Al Amir Dache, Z. & Thierry, A. R. Mitochondria-derived cell-to-cell communication. Cell Rep. 42, 112728 (2023). PubMed
McCully, J. D. et al. Injection of isolated mitochondria during early reperfusion for cardioprotection. Am. J. Physiol. Heart Circ. Physiol. 296, H94–h105 (2009). PubMed
Kaza, A. K. et al. Myocardial rescue with autologous mitochondrial transplantation in a porcine model of ischemia/reperfusion. J. Thorac. Cardiovasc. Surg. 153, 934–943 (2017). PubMed
Guariento, A. et al. Autologous mitochondrial transplantation for cardiogenic shock in pediatric patients following ischemia-reperfusion injury. J. Thorac. Cardiovasc. Surg. 162, 992–1001 (2021). PubMed
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
Norat, P. et al. Intraarterial transplantation of mitochondria after ischemic stroke reduces cerebral infarction. Stroke Vasc. Interv. Neurol. 3, e000644 (2023). PubMed PMC
McCully, J. D., del Nido, P. J. & Emani, S. M. Mitochondrial transplantation: the advance to therapeutic application and molecular modulation. Front. Cardiovasc. Med. 10, 1268814 (2023). PubMed PMC
Liu, Z., Sun, Y., Qi, Z., Cao, L. & Ding, S. Mitochondrial transfer/transplantation: an emerging therapeutic approach for multiple diseases. Cell Biosci. 12, 66 (2022). PubMed PMC
Gollihue, J. L. & Rabchevsky, A. G. Prospects for therapeutic mitochondrial transplantation. Mitochondrion 35, 70–79 (2017). PubMed PMC
Patel, S. P. et al. Delivery of mitoceuticals or respiratory competent mitochondria to sites of neurotrauma. Mitochondrion 68, 10–14 (2023). PubMed
Xu, J. et al. Targeted transplantation of engineered mitochondrial compound promotes functional recovery after spinal cord injury by enhancing macrophage phagocytosis. Bioact. Mater. 32, 427–444 (2024). PubMed
Nakamura, Y., Park, J.-H. & Hayakawa, K. Therapeutic use of extracellular mitochondria in CNS injury and disease. Exp. Neurol. 324, 113114 (2020). PubMed
Hayashida, K. et al. Exogenous mitochondrial transplantation improves survival and neurological outcomes after resuscitation from cardiac arrest. BMC Med 21, 56 (2023). PubMed PMC
Walker, M., Federico, E., Sancak, Y. & Levitt, M. R. Mitochondrial transplantation in ischemic stroke: insights from a first-in-human brain trial. Curr. Transplant. Rep. https://doi.org/10.1007/s40472-024-00428-6 (2024). DOI
Nakai, R. et al. Mitochondria transfer-based therapies reduce the morbidity and mortality of Leigh syndrome. Nat. Metab. https://doi.org/10.1038/s42255-024-01125-5 (2024). PubMed DOI
Lin, R. Z. et al. Mitochondrial transfer mediates endothelial cell engraftment through mitophagy. Nature 629, 660–668 (2024). PubMed
Nakano, T., Nakamura, Y., Park, J. H., Tanaka, M. & Hayakawa, K. Mitochondrial surface coating with artificial lipid membrane improves the transfer efficacy. Commun. Biol. 5, 745 (2022). PubMed PMC
Park, J. H. et al. O-Glc N acylation is essential for therapeutic mitochondrial transplantation. Commun. Med. 3, 169 (2023). PubMed PMC
Jacoby, E. et al. Mitochondrial augmentation of CD34 PubMed PMC
Jacoby, E. et al. Mitochondrial augmentation of hematopoietic stem cells in children with single large-scale mitochondrial DNA deletion syndromes. Sci. Transl. Med. 14, eabo3724 (2022). PubMed
Hinge, A. et al. Asymmetrically segregated mitochondria provide cellular memory of hematopoietic stem cell replicative history and drive HSC attrition. Cell Stem Cell 26, 420–430.e426 (2020). PubMed PMC
Döhla, J. et al. Metabolic determination of cell fate through selective inheritance of mitochondria. Nat. Cell Biol. 24, 148–154 (2022). PubMed PMC
Chou, S. H.-Y. et al. Extracellular mitochondria in cerebrospinal fluid and neurological recovery after subarachnoid hemorrhage. Stroke 48, 2231–2237 (2017). PubMed PMC
Cloer, C. M. et al. Mitochondrial transplant after ischemia reperfusion promotes cellular salvage and improves lung function during ex-vivo lung perfusion. J. Heart Lung Transpl. 42, 575–584 (2023).
Alway, S. E. et al. Mitochondria transplant therapy improves regeneration and restoration of injured skeletal muscle. J. Cachexia Sarcopenia Muscle 14, 493–507 (2023). PubMed PMC
Zhu, Z. et al. Photobiomodulation augments the effects of mitochondrial transplantation in the treatment of spinal cord injury in rats by facilitating mitochondrial transfer to neurons via connexin 36. Bioeng. Transl. Med. 8, e10473 (2023). PubMed
Masuzawa, A. et al. Transplantation of autologously derived mitochondria protects the heart from ischemia-reperfusion injury. Am. J. Physiol. 304, H966–H982 (2013).
Court, A. C. et al. Survival advantage of native and engineered T cells is acquired by mitochondrial transfer from mesenchymal stem cells. J. Transl. Med. 22, 868 (2024). PubMed PMC
Baldwin, J. G. et al. Intercellular nanotube-mediated mitochondrial transfer enhances T cell metabolic fitness and antitumor efficacy. Cell 187, 1–17 (2024).
Tiash, S., Brestoff, J. R. & Crewe, C. A guide to studying mitochondria transfer. Nat. Cell Biol. 25, 1551–1553 (2023). PubMed PMC
Pham, A. H., McCaffery, J. M. & Chan, D. C. Mouse lines with photo-activatable mitochondria to study mitochondrial dynamics. Genesis 50, 833–843 (2012). PubMed PMC
Los, G. V. et al. HaloTag: a novel protein labeling technology for cell imaging and protein analysis. ACS Chem. Biol. 3, 373–382 (2008). PubMed
López-Andarias, J. et al. Cell-penetrating streptavidin: a general tool for bifunctional delivery with spatiotemporal control, mediated by transport systems such as adaptive benzopolysulfane networks. J. Am. Chem. Soc. 142, 4784–4792 (2020). PubMed PMC
König, T. et al. MIROs and DRP1 drive mitochondrial-derived vesicle biogenesis and promote quality control. Nat. Cell Biol. 23, 1271–1286 (2021). PubMed
König, T. & McBride, H. M. Mitochondrial-derived vesicles in metabolism, disease, and aging. Cell Metab. 36, 21–35 (2024). PubMed
Chen, C., Li, H., Zhang, J. & Cheng, S. C. Exploring the limitations of mitochondrial dye as a genuine horizontal mitochondrial transfer surrogate. Commun. Biol. 7, 281 (2024). PubMed PMC
de Almeida, M. J., Luchsinger, L. L., Corrigan, D. J., Williams, L. J. & Snoeck, H. W. Dye-independent methods reveal elevated mitochondrial mass in hematopoietic stem cells. Cell Stem Cell 21, 725–729.e724 (2017). PubMed PMC
Patananan, A. N. et al. Pressure-driven mitochondrial transfer pipeline generates mammalian cells of desired genetic combinations and fates. Cell Rep. 33, 108562 (2020). PubMed PMC
Sercel, A. J. et al. Generating stable isolated mitochondrial recipient clones in mammalian cells using MitoPunch mitochondrial transfer. STAR Protoc. 2, 100850 (2021). PubMed PMC
Caicedo, A. et al. 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 (2015). PubMed PMC
Nzigou Mombo, B. et al. MitoCeption: transferring isolated human MSC mitochondria to glioblastoma stem cells. J. Vis. Exp. https://doi.org/10.3791/55245 (2017). PubMed DOI PMC
Sercel, A. J. et al. Stable transplantation of human mitochondrial DNA by high-throughput, pressurized isolated mitochondrial delivery. eLife 10, e63102 (2021). PubMed PMC
Dawson, E. R., Patananan, A. N., Sercel, A. J. & Teitell, M. A. Stable retention of chloramphenicol-resistant mtDNA to rescue metabolically impaired cells. Sci. Rep. 10, 14328 (2020). PubMed PMC
Chang, J. C. et al. Treatment of human cells derived from MERRF syndrome by peptide-mediated mitochondrial delivery. Cytotherapy 15, 1580–1596 (2013). PubMed
Singh, K. K., Choudhury, A. R. & Tiwari, H. K. Numtogenesis as a mechanism for development of cancer. Semin. Cancer Biol. 47, 101–109 (2017). PubMed PMC
Ljubojevic, N., Henderson, J. M. & Zurzolo, C. The ways of actin: why tunneling nanotubes are unique cell protrusions. Trends Cell Biol. 31, 130–142 (2021). PubMed
Ahmad, T. et al. Miro1 regulates intercellular mitochondrial transport & enhances mesenchymal stem cell rescue efficacy. EMBO J. 33, 994–1010 (2014). PubMed PMC
Zhang, Y. et al. iPSC-MSCs with high intrinsic MIRO1 and sensitivity to TNF-α yield efficacious mitochondrial transfer to rescue anthracycline-induced cardiomyopathy. Stem Cell Rep. 7, 749–763 (2016).
Watson, D. C. et al. GAP43-dependent mitochondria transfer from astrocytes enhances glioblastoma tumorigenicity. Nat. Cancer 4, 648–664 (2023). PubMed PMC
Liao, P. et al. Osteocyte mitochondria regulate angiogenesis of transcortical vessels. Nat. Commun. 15, 2529 (2024). PubMed PMC
Norris, R. P. Transfer of mitochondria and endosomes between cells by gap junction internalization. Traffic 22, 174–179 (2021). PubMed
Joly, E. & Hudrisier, D. What is trogocytosis and what is its purpose. Nat. Immunol. 4, 815–815 (2003). PubMed
Brukman, N. G., Uygur, B., Podbilewicz, B. & Chernomordik, L. V. How cells fuse. J. Cell Biol. 218, 1436–1451 (2019). PubMed PMC
Huang, Y. et al. TP53/p53 facilitates stress-induced exosome and protein secretion by adipocytes. Diabetes 72, 1560–1573 (2023). PubMed PMC
Welsh, J. A. et al. Minimal information for studies of extracellular vesicles (MISEV2023): From basic to advanced approaches. J. Extracell. Vesicles 13, e12404 (2024). PubMed PMC
Stephens, O. R. et al. Characterization and origins of cell-free mitochondria in healthy murine and human blood. Mitochondrion 54, 102–112 (2020). PubMed PMC
Caicedo, A. et al. The diversity and coexistence of extracellular mitochondria in circulation: a friend or foe of the immune system. Mitochondrion 58, 270–284 (2021). PubMed
Melki, I. et al. Platelets release mitochondrial antigens in systemic lupus erythematosus. Sci. Transl. Med. 13, eaav5928 (2021). PubMed
D’Acunzo, P. et al. Mitovesicles secreted into the extracellular space of brains with mitochondrial dysfunction impair synaptic plasticity. Mol. Neurodegener. 19, 34 (2024). PubMed PMC
D’Acunzo, P. et al. Mitovesicles are a novel population of extracellular vesicles of mitochondrial origin altered in Down syndrome. Sci. Adv. 7, eabe5085 (2021). PubMed PMC
Trumpff, C. et al. Stress and circulating cell-free mitochondrial DNA: a systematic review of human studies, physiological considerations, and technical recommendations. Mitochondrion 59, 225–245 (2021). PubMed PMC
Knez, J. et al. Correlates of peripheral blood mitochondrial DNA content in a general population. Am. J. Epidemiol. 183, 138–146 (2015). PubMed PMC
Roch, B. et al. Plasma derived cell-free mitochondrial DNA originates mainly from circulating cell-free mitochondria. Preprint at bioRxiv https://doi.org/10.1101/2021.09.03.458846 (2021).
Chiu, R. W. K. et al. Quantitative analysis of circulating mitochondrial DNA in plasma. Clin. Chem. 49, 719–726 (2003). PubMed
Caicedo, A. et al. Decoding the nature and complexity of extracellular mtDNA: types and implications for health and disease. Mitochondrion 75, 101848 (2024). PubMed
McArthur, K. et al. BAK/BAX macropores facilitate mitochondrial herniation and mtDNA efflux during apoptosis. Science 359, eaao6047 (2018). PubMed
McCully, J. D., Levitsky, S., Del Nido, P. J. & Cowan, D. B. Mitochondrial transplantation for therapeutic use. Clin. Transl. Med 5, 16 (2016). PubMed PMC
Herbert, M. & Turnbull, D. Progress in mitochondrial replacement therapies. Nat. Rev. Mol. Cell Biol. 19, 71–72 (2018). PubMed
Huang, P.-J. et al. Transferring xenogenic mitochondria provides neural protection against ischemic stress in ischemic rat brains. Cell Transplant. 25, 913–927 (2016). PubMed
Rossi, A. et al. Mitochondria transplantation mitigates damage in an in vitro model of renal tubular injury and in an ex vivo model of DCD renal transplantation. Ann. Surg. 278, e1313–e1326 (2023). PubMed
Yu, S. H. et al. Human umbilical cord mesenchymal stem cell-derived mitochondria (PN-101) attenuate LPS-induced inflammatory responses by inhibiting NFκB signaling pathway. BMB Rep. 55, 136–141 (2022). PubMed PMC
Lechuga-Vieco, A. V., Justo-Méndez, R. & Enríquez, J. A. Not all mitochondrial DNAs are made equal and the nucleus knows it. IUBMB Life 73, 511–529 (2021). PubMed
Lechuga-Vieco, A. V. et al. Heteroplasmy of wild-type mitochondrial DNA variants in mice causes metabolic heart disease with pulmonary hypertension and frailty. Circulation 145, 1084–1101 (2022). PubMed PMC
Gäbelein, C. G. et al. Mitochondria transplantation between living cells. PLoS Biol. 20, e3001576 (2022). PubMed PMC
Kim, M. J., Hwang, J. W., Yun, C.-K., Lee, Y. & Choi, Y.-S. Delivery of exogenous mitochondria via centrifugation enhances cellular metabolic function. Sci. Rep. 8, 3330 (2018). PubMed PMC
Coon, H. G. & Ho, C. Transformation of cultured cells to chloramphenicol resistance by purified mammalian mitochondrial DNA. Brookhaven Symp. Biol. 29, 166–177 (1977).
Fecher, C. et al. Cell-type-specific profiling of brain mitochondria reveals functional and molecular diversity. Nat. Neurosci. 22, 1731–1742 (2019). PubMed
Kuznetsov, A. V. & Margreiter, R. Heterogeneity of mitochondria and mitochondrial function within cells as another level of mitochondrial complexity. Int. J. Mol. Sci. 10, 1911–1929 (2009). PubMed PMC
Liu, X., Khouri-Farah, N., Wu, C. H. & Wu, G. Y. Targeted delivery of mitochondria to the liver in rats. J. Gastroenterol. Hepatol. 35, 2241–2247 (2020). PubMed
Ye, L. et al. Centrifugal enhancement of hepatitis C virus infection of human hepatocytes. J. Virol. Methods 148, 161–165 (2008). PubMed PMC
Guo, J., Wang, W., Yu, D. & Wu, Y. Spinoculation triggers dynamic actin and cofilin activity that facilitates HIV-1 infection of transformed and resting CD4 T cells. J. Virol. 85, 9824–9833 (2011). PubMed PMC
Harada, S. et al. Intercellular mitochondrial transfer enhances metabolic fitness and anti-tumor effects of CAR T cells. Blood 140, 2356–2357 (2022).
Suh, J. & Lee, Y.-S. Mitochondria as secretory organelles and therapeutic cargos. Exp. Mol. Med. 56, 66–85 (2024). PubMed PMC
Ippolito, L. et al. Cancer-associated fibroblasts promote prostate cancer malignancy via metabolic rewiring and mitochondrial transfer. Oncogene 38, 5339–5355 (2019). PubMed
Marlein, C. R. et al. NADPH oxidase-2 derived superoxide drives mitochondrial transfer from bone marrow stromal cells to leukemic blasts. Blood 130, 1649–1660 (2017). PubMed
Moschoi, R. et al. Protective mitochondrial transfer from bone marrow stromal cells to acute myeloid leukemic cells during chemotherapy. Blood 128, 253–264 (2016). PubMed