The adaptor protein Miro1 modulates horizontal transfer of mitochondria in mouse melanoma models
Summary: Recent research has shown that mtDNA-deficient cancer cells (ρ0 cells) acquire mitochondria from tumor stromal cells to restore respiration, facilitating tumor formation. We investigated the role of Miro1, an adaptor protein involved in movement of mitochondria along microtubules, in this p...
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2025-01-01
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author | Jaromir Novak Zuzana Nahacka Gabriela L. Oliveira Petra Brisudova Maria Dubisova Sarka Dvorakova Sona Miklovicova Marketa Dalecka Verena Puttrich Lenka Grycova Silvia Magalhaes-Novais Catarina Mendes Correia Jennifer Levoux Ludek Stepanek Jan Prochazka David Svec David Pajuelo Reguera Guillermo Lopez-Domenech Renata Zobalova Radek Sedlacek Mikkel G. Terp Payam A. Gammage Zdenek Lansky Josef Kittler Paulo J. Oliveira Henrik J. Ditzel Michael V. Berridge Anne-Marie Rodriguez Stepana Boukalova Jakub Rohlena Jiri Neuzil |
author_facet | Jaromir Novak Zuzana Nahacka Gabriela L. Oliveira Petra Brisudova Maria Dubisova Sarka Dvorakova Sona Miklovicova Marketa Dalecka Verena Puttrich Lenka Grycova Silvia Magalhaes-Novais Catarina Mendes Correia Jennifer Levoux Ludek Stepanek Jan Prochazka David Svec David Pajuelo Reguera Guillermo Lopez-Domenech Renata Zobalova Radek Sedlacek Mikkel G. Terp Payam A. Gammage Zdenek Lansky Josef Kittler Paulo J. Oliveira Henrik J. Ditzel Michael V. Berridge Anne-Marie Rodriguez Stepana Boukalova Jakub Rohlena Jiri Neuzil |
author_sort | Jaromir Novak |
collection | DOAJ |
description | Summary: Recent research has shown that mtDNA-deficient cancer cells (ρ0 cells) acquire mitochondria from tumor stromal cells to restore respiration, facilitating tumor formation. We investigated the role of Miro1, an adaptor protein involved in movement of mitochondria along microtubules, in this phenomenon. Inducible Miro1 knockout (Miro1KO) mice markedly delayed tumor formation after grafting ρ0 cancer cells. Miro1KO mice with fluorescently labeled mitochondria revealed that this delay was due to hindered mitochondrial transfer from the tumor stromal cells to grafted B16 ρ0 cells, which impeded recovery of mitochondrial respiration and tumor growth. Miro1KO led to the perinuclear accumulation of mitochondria and impaired mobility of the mitochondrial network. In vitro experiments revealed decreased association of mitochondria with microtubules, compromising mitochondrial transfer via tunneling nanotubes (TNTs) in mesenchymal stromal cells. Here we show the role of Miro1 in horizontal mitochondrial transfer in mouse melanoma models in vivo and its involvement with TNTs. |
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institution | Kabale University |
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language | English |
publishDate | 2025-01-01 |
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spelling | doaj-art-85fb633a244e4576a0814bf2863768862025-01-11T06:41:12ZengElsevierCell Reports2211-12472025-01-01441115154The adaptor protein Miro1 modulates horizontal transfer of mitochondria in mouse melanoma modelsJaromir Novak0Zuzana Nahacka1Gabriela L. Oliveira2Petra Brisudova3Maria Dubisova4Sarka Dvorakova5Sona Miklovicova6Marketa Dalecka7Verena Puttrich8Lenka Grycova9Silvia Magalhaes-Novais10Catarina Mendes Correia11Jennifer Levoux12Ludek Stepanek13Jan Prochazka14David Svec15David Pajuelo Reguera16Guillermo Lopez-Domenech17Renata Zobalova18Radek Sedlacek19Mikkel G. Terp20Payam A. Gammage21Zdenek Lansky22Josef Kittler23Paulo J. Oliveira24Henrik J. Ditzel25Michael V. Berridge26Anne-Marie Rodriguez27Stepana Boukalova28Jakub Rohlena29Jiri Neuzil30Institute of Biotechnology, Czech Academy of Sciences, 252 50 Prague-West, Czech Republic; Faculty of Science, Charles University, 128 00 Prague, Czech RepublicInstitute of Biotechnology, Czech Academy of Sciences, 252 50 Prague-West, Czech Republic; Corresponding authorInstitute of Biotechnology, Czech Academy of Sciences, 252 50 Prague-West, Czech Republic; NC-UC, Center for Neuroscience and Cell Biology, University of Coimbra, 3060-197 Cantanhede, Portugal; CIBB, Centre for Innovative Biomedicine and Biotechnology, University of Coimbra, 3060-197 Cantanhede, Portugal; Institute for Interdisciplinary Research, Doctoral Program in Experimental Biology and Biomedicine (PDBEB), University of Coimbra, 3060-197 Cantanhede, PortugalInstitute of Biotechnology, Czech Academy of Sciences, 252 50 Prague-West, Czech Republic; Faculty of Science, Charles University, 128 00 Prague, Czech RepublicInstitute of Biotechnology, Czech Academy of Sciences, 252 50 Prague-West, Czech Republic; Faculty of Science, Charles University, 128 00 Prague, Czech RepublicInstitute of Biotechnology, Czech Academy of Sciences, 252 50 Prague-West, Czech RepublicInstitute of Biotechnology, Czech Academy of Sciences, 252 50 Prague-West, Czech Republic; Faculty of Science, Charles University, 128 00 Prague, Czech RepublicFaculty of Science, Charles University, 128 00 Prague, Czech RepublicInstitute of Biotechnology, Czech Academy of Sciences, 252 50 Prague-West, Czech RepublicInstitute of Biotechnology, Czech Academy of Sciences, 252 50 Prague-West, Czech RepublicInstitute of Biotechnology, Czech Academy of Sciences, 252 50 Prague-West, Czech Republic; Czech Center for Phenogenomic, Institute of Molecular Genetics, Czech Academy of Sciences, 252 50 Vestec, Czech RepublicCancer Research UK Scotland Institute, Glasgow G61 1BD, UKSorbonne University, Institute of Biology Paris-Seine, 75005 Paris, FranceCzech Center for Phenogenomic, Institute of Molecular Genetics, Czech Academy of Sciences, 252 50 Vestec, Czech RepublicCzech Center for Phenogenomic, Institute of Molecular Genetics, Czech Academy of Sciences, 252 50 Vestec, Czech RepublicInstitute of Biotechnology, Czech Academy of Sciences, 252 50 Prague-West, Czech RepublicCzech Center for Phenogenomic, Institute of Molecular Genetics, Czech Academy of Sciences, 252 50 Vestec, Czech RepublicDepartment of Neuroscience, Physiology and Pharmacology, University College London, Gower Street, London WC1E 6BT, UKInstitute of Biotechnology, Czech Academy of Sciences, 252 50 Prague-West, Czech RepublicCzech Center for Phenogenomic, Institute of Molecular Genetics, Czech Academy of Sciences, 252 50 Vestec, Czech RepublicInstitute of Molecular Medicine, University of Southern Denmark, 5000 Odense, DenmarkCancer Research UK Scotland Institute, Glasgow G61 1BD, UK; School of Cancer Sciences, University of Glasgow, Glasgow G61 1BD, UKInstitute of Biotechnology, Czech Academy of Sciences, 252 50 Prague-West, Czech RepublicDepartment of Neuroscience, Physiology and Pharmacology, University College London, Gower Street, London WC1E 6BT, UKNC-UC, Center for Neuroscience and Cell Biology, University of Coimbra, 3060-197 Cantanhede, Portugal; CIBB, Centre for Innovative Biomedicine and Biotechnology, University of Coimbra, 3060-197 Cantanhede, PortugalInstitute of Molecular Medicine, University of Southern Denmark, 5000 Odense, Denmark; Department of Oncology, Odense University Hospital, 5000 Odense, DenmarkMalaghan Institute of Medical Research, Wellington 6012, New ZealandSorbonne University, Institute of Biology Paris-Seine, 75005 Paris, France; University Paris-Est Créteil, INSERM, IMRB, 94010 Créteil, FranceInstitute of Biotechnology, Czech Academy of Sciences, 252 50 Prague-West, Czech Republic; Faculty of Science, Charles University, 128 00 Prague, Czech RepublicInstitute of Biotechnology, Czech Academy of Sciences, 252 50 Prague-West, Czech RepublicInstitute of Biotechnology, Czech Academy of Sciences, 252 50 Prague-West, Czech Republic; Faculty of Science, Charles University, 128 00 Prague, Czech Republic; School of Pharmacy and Medical Science, Griffith University, Southport, QLD 4222, Australia; 1st Faculty of Medicine, Charles University, 121 08 Prague, Czech Republic; Corresponding authorSummary: Recent research has shown that mtDNA-deficient cancer cells (ρ0 cells) acquire mitochondria from tumor stromal cells to restore respiration, facilitating tumor formation. We investigated the role of Miro1, an adaptor protein involved in movement of mitochondria along microtubules, in this phenomenon. Inducible Miro1 knockout (Miro1KO) mice markedly delayed tumor formation after grafting ρ0 cancer cells. Miro1KO mice with fluorescently labeled mitochondria revealed that this delay was due to hindered mitochondrial transfer from the tumor stromal cells to grafted B16 ρ0 cells, which impeded recovery of mitochondrial respiration and tumor growth. Miro1KO led to the perinuclear accumulation of mitochondria and impaired mobility of the mitochondrial network. In vitro experiments revealed decreased association of mitochondria with microtubules, compromising mitochondrial transfer via tunneling nanotubes (TNTs) in mesenchymal stromal cells. Here we show the role of Miro1 in horizontal mitochondrial transfer in mouse melanoma models in vivo and its involvement with TNTs.http://www.sciencedirect.com/science/article/pii/S2211124724015055CP: CancerCP: Cell biology |
spellingShingle | Jaromir Novak Zuzana Nahacka Gabriela L. Oliveira Petra Brisudova Maria Dubisova Sarka Dvorakova Sona Miklovicova Marketa Dalecka Verena Puttrich Lenka Grycova Silvia Magalhaes-Novais Catarina Mendes Correia Jennifer Levoux Ludek Stepanek Jan Prochazka David Svec David Pajuelo Reguera Guillermo Lopez-Domenech Renata Zobalova Radek Sedlacek Mikkel G. Terp Payam A. Gammage Zdenek Lansky Josef Kittler Paulo J. Oliveira Henrik J. Ditzel Michael V. Berridge Anne-Marie Rodriguez Stepana Boukalova Jakub Rohlena Jiri Neuzil The adaptor protein Miro1 modulates horizontal transfer of mitochondria in mouse melanoma models Cell Reports CP: Cancer CP: Cell biology |
title | The adaptor protein Miro1 modulates horizontal transfer of mitochondria in mouse melanoma models |
title_full | The adaptor protein Miro1 modulates horizontal transfer of mitochondria in mouse melanoma models |
title_fullStr | The adaptor protein Miro1 modulates horizontal transfer of mitochondria in mouse melanoma models |
title_full_unstemmed | The adaptor protein Miro1 modulates horizontal transfer of mitochondria in mouse melanoma models |
title_short | The adaptor protein Miro1 modulates horizontal transfer of mitochondria in mouse melanoma models |
title_sort | adaptor protein miro1 modulates horizontal transfer of mitochondria in mouse melanoma models |
topic | CP: Cancer CP: Cell biology |
url | http://www.sciencedirect.com/science/article/pii/S2211124724015055 |
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