Table 1.

Overview of donor/acceptor cells (types of cells) involved in mitochondrial transfer

Donor cellsAcceptor cellsType of transferReferences
Rat neuroendocrine pheochromocytoma cells Rat neuroendocrine pheochromocytoma cells TNTs Rustom et al., 2004  
Human embryonic kidney cells Human embryonic kidney cells TNTs Rustom et al., 2004  
Normal rat kidney cells Normal rat kidney cells TNTs Rustom et al., 2004  
Rat neonatal CMs Human endothelial progenitor cells Nanotubes Koyanagi et al., 2005  
Human macrophage Human macrophages TNTs Onfelt et al., 2006  
Human MSCs Human alveolar adenocarcinoma cells TNTs Spees et al., 2006  
Human skin fibroblast Human alveolar adenocarcinoma cells TNTs Spees et al., 2006  
Human MSCs Rat CM Nanotubes Plotnikov et al., 2008  
Rat MSCs Rat lung ECs Cx43-based intercellular gap junctional communication Otsu et al., 2009  
MSCs Rat cardiomyoblasts Nanotubes Cselenyak et al., 2010  
Rat kidney renal tubular cells Human MSCs TNTs and gap junctions Plotnikov et al., 2010  
Human MSCs Rat kidney renal tubular cells TNTs and gap junctions Plotnikov et al., 2010  
Mouse endothelial progenitor cells Human umbilical vein ECs TNTs Yasuda et al., 2010  
Human adipose-derived stem cells Mouse CMs Partial cell fusion Acquistapace et al., 2011  
Human proximal tubular epithelial cells Human proximal tubular epithelial cells TNT-like structures Domhan et al., 2011  
Rat ventricular CMs Rat fibroblasts Nanotubes He et al., 2011  
Rat ventricular CMs Rat ventricular CMs Nanotubes He et al., 2011  
Rat fibroblasts Rat fibroblasts Nanotubes He et al., 2011  
Rat fibroblasts Rat ventricular CMs Nanotubes He et al., 2011  
Rat hippocampal astrocytes Rat hippocampal astrocytes TNTs Wang et al., 2011  
Human MSCs Human osteosarcoma cells Partial cell fusion Cho et al., 2012  
Mouse BM-derived stromal cells Mouse BM-derived stromal cells Cx43-containing gap junctional channels, nanotubes, MVs Islam et al., 2012  
Human BM-derived stromal cells Human BM-derived stromal cells Cx43-containing gap junctional channels, nanotubes, MVs Islam et al., 2012  
Mouse BM-derived stromal cells* Mouse alveolar epithelial cell* Cx43-containing gap junctional channels, nanotubes, MVs Islam et al., 2012  
Human BM-derived stromal cells* Mouse alveolar epithelial cell* Cx43-containing gap junctional channels, nanotubes, MVs Islam et al., 2012  
Human pleural mesothelioma cells Human pleural mesothelioma cells TNTs Lou et al., 2012  
Human MSCs Human vascular smooth muscle cells TNTs Vallabhaneni et al., 2012  
Human vascular smooth muscle cells Human MSCs TNTs Vallabhaneni et al., 2012  
Human retinal pigment epithelial cells Human retinal pigment epithelial cells TNTs Witting et al., 2012) 
Human ECs Human ovarian cancer cells TNTs Pasquier et al., 2013  
Human ECs Human breast cancer cells TNTs Pasquier et al., 2013  
MSC* Bronchial epithelial cells* TNTs Ahmad et al., 2014  
Platelets Neutrophils ECVs Boudreau et al., 2014  
Murine neuronal cells* Murine glial cells* Protrusions Davis et al., 2014  
MSCs* Lung epithelial cells* TNTs Li et al., 2014  
MSCs Human umbilical vein ECs TNTs Li et al., 2014  
Human multipotent MSCs Rat neuronal cells Intercellular contacts Babenko et al., 2015  
Human multipotent MSCs Rat glial cells Intercellular contacts Babenko et al., 2015  
Breast cancer cells Breast cancer cells n.s. Jayaprakash et al., 2015  
Normal fibroblast cells Normal fibroblast cells n.s. Jayaprakash et al., 2015  
Human MSCs  Macrophages MVs Phinney et al., 2015  
Human MSCs*  Macrophages* MVs Phinney et al., 2015  
Pheochromocytoma cells Pheochromocytoma cells TNTs Okafo et al., 2017  
MSCs Rat cardiomyoblasts TNTs Han et al., 2016  
Astrocytes* Neuronal cells* Extracellular mitochondrial particles Hayakawa et al., 2016  
MSCs* Lung alveolar macrophages* TNTs Jackson et al., 2016a, b  
MSCs Corneal epithelial cells TNTs Jiang et al., 2016  
Mouse sister germ cells Mouse oocytes Microtubes Lei and Spradling, 2016  
BM stromal cells Acute myeloid leukemic cells Endocytosis Moschoi et al., 2016  
BM stromal cells* Acute myeloid leukemic cells* Endocytosis Moschoi et al., 2016  
MSCs* Murine CMs* TNTs Zhang et al., 2016  
MSCs Murine CMs TNTs Zhang et al., 2016  
MSCs MERRF cybrid cells n.s. Chuang et al., 2017  
Malignant urothelial carcinoma cells Non-malignant urinary papillary urothelial tumor cells TNTs Lu et al., 2017  
Human MSCs Human CMs n.s. Mahrouf-Yorgov et al., 2017  
Human MSCs Human ECs n.s. Mahrouf-Yorgov et al., 2017  
Human CMs Human MSCs n.s. Mahrouf-Yorgov et al., 2017  
Human ECs Human MSCs n.s. Mahrouf-Yorgov et al., 2017  
BM stromal cells* Acute myeloid leukemia cells* TNTs Marlein et al., 2017  
Mesenchymal stromal cells* Macrophages* EVs Morrison et al., 2017  
Human healthy astrocytes Human stressed astrocytes TNTs Rostami et al., 2017  
Human multipotent MSCs Rat astrocytes TNTs Babenko et al., 2018  
Human multipotent MSCs Neuron-like PC12 pheochromocytoma ρ0 cells TNTs Babenko et al., 2018  
MSCs Neural stem cells Actin-based intercellular structures Boukelmoune et al., 2018  
Monkey kidney cells Monkey kidney cells TNTs Guo et al., 2018  
Porcine alveolar macrophages Porcine alveolar macrophages TNTs Guo et al., 2018  
Porcine umbilical cord MSCs  Porcine alveolar macrophages TNTs Guo et al., 2018  
Endothelial progenitor cells Brain ECs Endothelial progenitor cell–derived mitochondrial particles Hayakawa et al., 2018  
Myeloid-derived regulatory cells T Cells ECVs Hough et al., 2018  
Cardiac myofibroblasts Cardiomyocytes Nanotubes Shen et al., 2018  
T cell acute lymphoblastic leukemia cells MSCs TNTs Wang e al., 2018  
MSCs T Cell acute lymphoblastic leukemia cells TNTs Wang et al., 2018  
Human induced pluripotent stem cell–derived MSCs Human bronchial epithelium cells TNTs (Cx43 mediated) Yao et al., 2018  
Human induced pluripotent stem cell–derived MSCs* Murine epithelial cells* TNTs (Cx43 mediated) Yao et al., 2018  
Scattered tubular-like cells Tubular epithelial cells ECVs Zou et al., 2018  
MSCs Acute lymphoblastic leukemia cells TNTs Burt et al., 2019  
BM MSCs  Human ECs TNTs Feng et al., 2019  
Human astrocytes Human astrocytes n.s. Gao et al., 2019  
Human neuronal cells Human astrocytes n.s. Gao et al., 2019  
Cancer-associated fibroblasts Prostate cancer cells Cellular bridges Ippolito et al., 2019  
Cancer-associated fibroblasts* Prostate cancer cells* Cellular bridges Ippolito et al., 2019  
BM-derived MSCs Proximal tubular epithelial cells n.s. Konari et al., 2019  
BM-derived MSCs* Proximal tubular epithelial cells* n.s. Konari et al., 2019  
Rat MSCs Rat neurons Gap junction intercellular communication Li et al., 2019  
Rat MSCs* Rat neurons* Gap junction intercellular communication Li et al., 2019  
Astrocytes Primary rat neuronal cells n.s. Lippert and Borlongan, 2019  
BM stromal cells MM cells TNTs Marlein et al., 2019  
BM stromal cells Hematopoietic stem cells Gap junction Mistry et al., 2019  
BM stromal cells* Hematopoietic stem cells* Gap junction Mistry et al., 2019  
Astrocytes Neurons n.s. English et al., 2020  
Murine hematopoietic stem and progenitor cells* Murine mesenchymal stromal cells* Cell-contact dependent, Cx43-mediated Golan et al., 2020  
Murine CMs* Murine macrophages* Cardiomyocyte-derived exophers (subcellular particles) Nocolas-Avila et al., 2020  
Mesenchymal stromal cells Islet β cells TNTs Rackham et al., 2020  
Murine white adipocytes* Murine macrophages* n.s. Brestoff et al., 2021  
Human MSCs Injured alveolar epithelial cells  Cx43-containing gap junctional channels Huang et al., 2021  
Platelets MSCs Dynamin-dependent clathrin-mediated endocytosis Levoux et al., 2021  
Platelets* MSCs* Dynamin-dependent clathrin-mediated endocytosis Levoux et al., 2021  
BM stromal cells Myeloma cells TNTs and partial cell fusion Matula et al., 2021  
Myeloma cells BM stromal cells TNTs and partial cell fusion Matula et al., 2021  
Murine ovarian follicles Murine ovarian follicles Gap junction internalization Norris, 2021  
Glioblastoma stem cells Glioblastoma stem cells TNTs Pinto et al., 2021  
3D-glioblastoma organoids 3D-glioblastoma organoids TNTs Pinto et al., 2021  
Human breast epithelial cancer cells Human breast epithelial cancer cells ECVs Rabas et al., 2021  
Murine high-metastatic lung carcinoma cells Murine low-metastatic lung carcinoma cells ECVs Takenaga et al., 2021  
Murine low-metastatic lung carcinoma cells Murine high-metastatic lung carcinoma cells ECVs Takenaga et al., 2021  
Murine high-metastatic lung carcinoma cells* Murine low-metastatic lung carcinoma cells and cancer-associated fibroblasts* ECVs Takenaga et al., 2021  
MSCs Neurons Cell-to-cell contact Tseng et al., 2021  
Human glioblastoma cells Human primary astrocytes TNTs Valdebenito et al., 2021  
Human neurons Human astrocytes TNTs Lampinen et al., 2022  
Murine neurons Murine astrocytes TNTs Lampinen et al., 2022  
Murine brown adipocytes* Murine adipocytes* ECVs Rosina et al., 2022  
Effector immune cells Breast cancer cells TNTs Saha et al., 2022  
T cells* Lung carcinoma cells* TNTs Saha et al., 2022  
T cells* Melanoma cells* TNTs Saha et al., 2022  
Donor cellsAcceptor cellsType of transferReferences
Rat neuroendocrine pheochromocytoma cells Rat neuroendocrine pheochromocytoma cells TNTs Rustom et al., 2004  
Human embryonic kidney cells Human embryonic kidney cells TNTs Rustom et al., 2004  
Normal rat kidney cells Normal rat kidney cells TNTs Rustom et al., 2004  
Rat neonatal CMs Human endothelial progenitor cells Nanotubes Koyanagi et al., 2005  
Human macrophage Human macrophages TNTs Onfelt et al., 2006  
Human MSCs Human alveolar adenocarcinoma cells TNTs Spees et al., 2006  
Human skin fibroblast Human alveolar adenocarcinoma cells TNTs Spees et al., 2006  
Human MSCs Rat CM Nanotubes Plotnikov et al., 2008  
Rat MSCs Rat lung ECs Cx43-based intercellular gap junctional communication Otsu et al., 2009  
MSCs Rat cardiomyoblasts Nanotubes Cselenyak et al., 2010  
Rat kidney renal tubular cells Human MSCs TNTs and gap junctions Plotnikov et al., 2010  
Human MSCs Rat kidney renal tubular cells TNTs and gap junctions Plotnikov et al., 2010  
Mouse endothelial progenitor cells Human umbilical vein ECs TNTs Yasuda et al., 2010  
Human adipose-derived stem cells Mouse CMs Partial cell fusion Acquistapace et al., 2011  
Human proximal tubular epithelial cells Human proximal tubular epithelial cells TNT-like structures Domhan et al., 2011  
Rat ventricular CMs Rat fibroblasts Nanotubes He et al., 2011  
Rat ventricular CMs Rat ventricular CMs Nanotubes He et al., 2011  
Rat fibroblasts Rat fibroblasts Nanotubes He et al., 2011  
Rat fibroblasts Rat ventricular CMs Nanotubes He et al., 2011  
Rat hippocampal astrocytes Rat hippocampal astrocytes TNTs Wang et al., 2011  
Human MSCs Human osteosarcoma cells Partial cell fusion Cho et al., 2012  
Mouse BM-derived stromal cells Mouse BM-derived stromal cells Cx43-containing gap junctional channels, nanotubes, MVs Islam et al., 2012  
Human BM-derived stromal cells Human BM-derived stromal cells Cx43-containing gap junctional channels, nanotubes, MVs Islam et al., 2012  
Mouse BM-derived stromal cells* Mouse alveolar epithelial cell* Cx43-containing gap junctional channels, nanotubes, MVs Islam et al., 2012  
Human BM-derived stromal cells* Mouse alveolar epithelial cell* Cx43-containing gap junctional channels, nanotubes, MVs Islam et al., 2012  
Human pleural mesothelioma cells Human pleural mesothelioma cells TNTs Lou et al., 2012  
Human MSCs Human vascular smooth muscle cells TNTs Vallabhaneni et al., 2012  
Human vascular smooth muscle cells Human MSCs TNTs Vallabhaneni et al., 2012  
Human retinal pigment epithelial cells Human retinal pigment epithelial cells TNTs Witting et al., 2012) 
Human ECs Human ovarian cancer cells TNTs Pasquier et al., 2013  
Human ECs Human breast cancer cells TNTs Pasquier et al., 2013  
MSC* Bronchial epithelial cells* TNTs Ahmad et al., 2014  
Platelets Neutrophils ECVs Boudreau et al., 2014  
Murine neuronal cells* Murine glial cells* Protrusions Davis et al., 2014  
MSCs* Lung epithelial cells* TNTs Li et al., 2014  
MSCs Human umbilical vein ECs TNTs Li et al., 2014  
Human multipotent MSCs Rat neuronal cells Intercellular contacts Babenko et al., 2015  
Human multipotent MSCs Rat glial cells Intercellular contacts Babenko et al., 2015  
Breast cancer cells Breast cancer cells n.s. Jayaprakash et al., 2015  
Normal fibroblast cells Normal fibroblast cells n.s. Jayaprakash et al., 2015  
Human MSCs  Macrophages MVs Phinney et al., 2015  
Human MSCs*  Macrophages* MVs Phinney et al., 2015  
Pheochromocytoma cells Pheochromocytoma cells TNTs Okafo et al., 2017  
MSCs Rat cardiomyoblasts TNTs Han et al., 2016  
Astrocytes* Neuronal cells* Extracellular mitochondrial particles Hayakawa et al., 2016  
MSCs* Lung alveolar macrophages* TNTs Jackson et al., 2016a, b  
MSCs Corneal epithelial cells TNTs Jiang et al., 2016  
Mouse sister germ cells Mouse oocytes Microtubes Lei and Spradling, 2016  
BM stromal cells Acute myeloid leukemic cells Endocytosis Moschoi et al., 2016  
BM stromal cells* Acute myeloid leukemic cells* Endocytosis Moschoi et al., 2016  
MSCs* Murine CMs* TNTs Zhang et al., 2016  
MSCs Murine CMs TNTs Zhang et al., 2016  
MSCs MERRF cybrid cells n.s. Chuang et al., 2017  
Malignant urothelial carcinoma cells Non-malignant urinary papillary urothelial tumor cells TNTs Lu et al., 2017  
Human MSCs Human CMs n.s. Mahrouf-Yorgov et al., 2017  
Human MSCs Human ECs n.s. Mahrouf-Yorgov et al., 2017  
Human CMs Human MSCs n.s. Mahrouf-Yorgov et al., 2017  
Human ECs Human MSCs n.s. Mahrouf-Yorgov et al., 2017  
BM stromal cells* Acute myeloid leukemia cells* TNTs Marlein et al., 2017  
Mesenchymal stromal cells* Macrophages* EVs Morrison et al., 2017  
Human healthy astrocytes Human stressed astrocytes TNTs Rostami et al., 2017  
Human multipotent MSCs Rat astrocytes TNTs Babenko et al., 2018  
Human multipotent MSCs Neuron-like PC12 pheochromocytoma ρ0 cells TNTs Babenko et al., 2018  
MSCs Neural stem cells Actin-based intercellular structures Boukelmoune et al., 2018  
Monkey kidney cells Monkey kidney cells TNTs Guo et al., 2018  
Porcine alveolar macrophages Porcine alveolar macrophages TNTs Guo et al., 2018  
Porcine umbilical cord MSCs  Porcine alveolar macrophages TNTs Guo et al., 2018  
Endothelial progenitor cells Brain ECs Endothelial progenitor cell–derived mitochondrial particles Hayakawa et al., 2018  
Myeloid-derived regulatory cells T Cells ECVs Hough et al., 2018  
Cardiac myofibroblasts Cardiomyocytes Nanotubes Shen et al., 2018  
T cell acute lymphoblastic leukemia cells MSCs TNTs Wang e al., 2018  
MSCs T Cell acute lymphoblastic leukemia cells TNTs Wang et al., 2018  
Human induced pluripotent stem cell–derived MSCs Human bronchial epithelium cells TNTs (Cx43 mediated) Yao et al., 2018  
Human induced pluripotent stem cell–derived MSCs* Murine epithelial cells* TNTs (Cx43 mediated) Yao et al., 2018  
Scattered tubular-like cells Tubular epithelial cells ECVs Zou et al., 2018  
MSCs Acute lymphoblastic leukemia cells TNTs Burt et al., 2019  
BM MSCs  Human ECs TNTs Feng et al., 2019  
Human astrocytes Human astrocytes n.s. Gao et al., 2019  
Human neuronal cells Human astrocytes n.s. Gao et al., 2019  
Cancer-associated fibroblasts Prostate cancer cells Cellular bridges Ippolito et al., 2019  
Cancer-associated fibroblasts* Prostate cancer cells* Cellular bridges Ippolito et al., 2019  
BM-derived MSCs Proximal tubular epithelial cells n.s. Konari et al., 2019  
BM-derived MSCs* Proximal tubular epithelial cells* n.s. Konari et al., 2019  
Rat MSCs Rat neurons Gap junction intercellular communication Li et al., 2019  
Rat MSCs* Rat neurons* Gap junction intercellular communication Li et al., 2019  
Astrocytes Primary rat neuronal cells n.s. Lippert and Borlongan, 2019  
BM stromal cells MM cells TNTs Marlein et al., 2019  
BM stromal cells Hematopoietic stem cells Gap junction Mistry et al., 2019  
BM stromal cells* Hematopoietic stem cells* Gap junction Mistry et al., 2019  
Astrocytes Neurons n.s. English et al., 2020  
Murine hematopoietic stem and progenitor cells* Murine mesenchymal stromal cells* Cell-contact dependent, Cx43-mediated Golan et al., 2020  
Murine CMs* Murine macrophages* Cardiomyocyte-derived exophers (subcellular particles) Nocolas-Avila et al., 2020  
Mesenchymal stromal cells Islet β cells TNTs Rackham et al., 2020  
Murine white adipocytes* Murine macrophages* n.s. Brestoff et al., 2021  
Human MSCs Injured alveolar epithelial cells  Cx43-containing gap junctional channels Huang et al., 2021  
Platelets MSCs Dynamin-dependent clathrin-mediated endocytosis Levoux et al., 2021  
Platelets* MSCs* Dynamin-dependent clathrin-mediated endocytosis Levoux et al., 2021  
BM stromal cells Myeloma cells TNTs and partial cell fusion Matula et al., 2021  
Myeloma cells BM stromal cells TNTs and partial cell fusion Matula et al., 2021  
Murine ovarian follicles Murine ovarian follicles Gap junction internalization Norris, 2021  
Glioblastoma stem cells Glioblastoma stem cells TNTs Pinto et al., 2021  
3D-glioblastoma organoids 3D-glioblastoma organoids TNTs Pinto et al., 2021  
Human breast epithelial cancer cells Human breast epithelial cancer cells ECVs Rabas et al., 2021  
Murine high-metastatic lung carcinoma cells Murine low-metastatic lung carcinoma cells ECVs Takenaga et al., 2021  
Murine low-metastatic lung carcinoma cells Murine high-metastatic lung carcinoma cells ECVs Takenaga et al., 2021  
Murine high-metastatic lung carcinoma cells* Murine low-metastatic lung carcinoma cells and cancer-associated fibroblasts* ECVs Takenaga et al., 2021  
MSCs Neurons Cell-to-cell contact Tseng et al., 2021  
Human glioblastoma cells Human primary astrocytes TNTs Valdebenito et al., 2021  
Human neurons Human astrocytes TNTs Lampinen et al., 2022  
Murine neurons Murine astrocytes TNTs Lampinen et al., 2022  
Murine brown adipocytes* Murine adipocytes* ECVs Rosina et al., 2022  
Effector immune cells Breast cancer cells TNTs Saha et al., 2022  
T cells* Lung carcinoma cells* TNTs Saha et al., 2022  
T cells* Melanoma cells* TNTs Saha et al., 2022  
*

in vivo work

Note: TNTs, nanotubes, protrusions, microtubes, actin-based intercellular structures, cellular bridges—types of filamentous tubes that function as intercellular bridges. n.s., not specified in original paper.

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