Tumor exosomes induce tunneling nanotubes in lipid raft-enriched regions of human mesothelioma cells
Tunneling nanotubes (TnTs) are long, non-adherent, actin-based cellular extensions that act as conduits for transport of cellular cargo between connected cells. The mechanisms of nanotube formation and the effects of the tumor microenvironment and cellular signals on TnT formation are unknown. In th...
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Published in | Experimental cell research Vol. 323; no. 1; pp. 178 - 188 |
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Main Authors | , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
Elsevier Inc
15.04.2014
Elsevier BV |
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Abstract | Tunneling nanotubes (TnTs) are long, non-adherent, actin-based cellular extensions that act as conduits for transport of cellular cargo between connected cells. The mechanisms of nanotube formation and the effects of the tumor microenvironment and cellular signals on TnT formation are unknown. In the present study, we explored exosomes as potential mediators of TnT formation in mesothelioma and the potential relationship of lipid rafts to TnT formation. Mesothelioma cells co-cultured with exogenous mesothelioma-derived exosomes formed more TnTs than cells cultured without exosomes within 24–48h; and this effect was most prominent in media conditions (low-serum, hyperglycemic medium) that support TnT formation (1.3–1.9-fold difference). Fluorescence and electron microscopy confirmed the purity of isolated exosomes and revealed that they localized predominantly at the base of and within TnTs, in addition to the extracellular environment. Time-lapse microscopic imaging demonstrated uptake of tumor exosomes by TnTs, which facilitated intercellular transfer of these exosomes between connected cells. Mesothelioma cells connected via TnTs were also significantly enriched for lipid rafts at nearly a 2-fold higher number compared with cells not connected by TnTs. Our findings provide supportive evidence of exosomes as potential chemotactic stimuli for TnT formation, and also lipid raft formation as a potential biomarker for TnT-forming cells.
•Exosomes derived from malignant cells can stimulate an increased rate in the formation of tunneling nanotubes.•Tunneling nanotubes can serve as conduits for intercellular transfer of these exosomes.•Most notably, exosomes derived from benign mesothelial cells had no effect on nanotube formation.•Cells forming nanotubes were enriched in lipid rafts at a greater number compared with cells not forming nanotubes.•Our findings suggest causal and potentially synergistic association of exosomes and tunneling nanotubes in cancer. |
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AbstractList | Tunneling nanotubes (TnTs) are long, non-adherent, actin-based cellular extensions that act as conduits for transport of cellular cargo between connected cells. The mechanisms of nanotube formation and the effects of the tumor microenvironment and cellular signals on TnT formation are unknown. In the present study, we explored exosomes as potential mediators of TnT formation in mesothelioma and the potential relationship of lipid rafts to TnT formation. Mesothelioma cells co-cultured with exogenous mesothelioma-derived exosomes formed more TnTs than cells cultured without exosomes within 24-48 hours; and this effect was most prominent in media conditions (low-serum, hyperglycemic medium) that support TnT formation (1.3-1.9-fold difference). Fluorescence and electron microscopy confirmed the purity of isolated exosomes and revealed that they localized predominantly at the base of and within TnTs, in addition to the extracellular environment. Time-lapse microscopic imaging demonstrated uptake of tumor exosomes by TnTs, which facilitated intercellular transfer of these exosomes between connected cells. Mesothelioma cells connected via TnTs were also significantly enriched for lipid rafts at nearly a 2-fold higher number compared with cells not connected by TnTs. Our findings provide supportive evidence of exosomes as potential chemotactic stimuli for TnT formation, and also lipid raft formation as a potential biomarker for TnT-forming cells. Tunneling nanotubes (TnTs) are long, non-adherent, actin-based cellular extensions that act as conduits for transport of cellular cargo between connected cells. The mechanisms of nanotube formation and the effects of the tumor microenvironment and cellular signals on TnT formation are unknown. In the present study, we explored exosomes as potential mediators of TnT formation in mesothelioma and the potential relationship of lipid rafts to TnT formation. Mesothelioma cells co-cultured with exogenous mesothelioma-derived exosomes formed more TnTs than cells cultured without exosomes within 24-48 h; and this effect was most prominent in media conditions (low-serum, hyperglycemic medium) that support TnT formation (1.3-1.9-fold difference). Fluorescence and electron microscopy confirmed the purity of isolated exosomes and revealed that they localized predominantly at the base of and within TnTs, in addition to the extracellular environment. Time-lapse microscopic imaging demonstrated uptake of tumor exosomes by TnTs, which facilitated intercellular transfer of these exosomes between connected cells. Mesothelioma cells connected via TnTs were also significantly enriched for lipid rafts at nearly a 2-fold higher number compared with cells not connected by TnTs. Our findings provide supportive evidence of exosomes as potential chemotactic stimuli for TnT formation, and also lipid raft formation as a potential biomarker for TnT-forming cells. Tunneling nanotubes (TnTs) are long, non-adherent, actin-based cellular extensions that act as conduits for transport of cellular cargo between connected cells. The mechanisms of nanotube formation and the effects of the tumor microenvironment and cellular signals on TnT formation are unknown. In the present study, we explored exosomes as potential mediators of TnT formation in mesothelioma and the potential relationship of lipid rafts to TnT formation. Mesothelioma cells co-cultured with exogenous mesothelioma-derived exosomes formed more TnTs than cells cultured without exosomes within 24–48h; and this effect was most prominent in media conditions (low-serum, hyperglycemic medium) that support TnT formation (1.3–1.9-fold difference). Fluorescence and electron microscopy confirmed the purity of isolated exosomes and revealed that they localized predominantly at the base of and within TnTs, in addition to the extracellular environment. Time-lapse microscopic imaging demonstrated uptake of tumor exosomes by TnTs, which facilitated intercellular transfer of these exosomes between connected cells. Mesothelioma cells connected via TnTs were also significantly enriched for lipid rafts at nearly a 2-fold higher number compared with cells not connected by TnTs. Our findings provide supportive evidence of exosomes as potential chemotactic stimuli for TnT formation, and also lipid raft formation as a potential biomarker for TnT-forming cells. •Exosomes derived from malignant cells can stimulate an increased rate in the formation of tunneling nanotubes.•Tunneling nanotubes can serve as conduits for intercellular transfer of these exosomes.•Most notably, exosomes derived from benign mesothelial cells had no effect on nanotube formation.•Cells forming nanotubes were enriched in lipid rafts at a greater number compared with cells not forming nanotubes.•Our findings suggest causal and potentially synergistic association of exosomes and tunneling nanotubes in cancer. Tunneling nanotubes (TnTs) are long, non-adherent, actin-based cellular extensions that act as conduits for transport of cellular cargo between connected cells. The mechanisms of nanotube formation and the effects of the tumor microenvironment and cellular signals on TnT formation are unknown. In the present study, we explored exosomes as potential mediators of TnT formation in mesothelioma and the potential relationship of lipid rafts to TnT formation. Mesothelioma cells co-cultured with exogenous mesothelioma-derived exosomes formed more TnTs than cells cultured without exosomes within 24–48 h; and this effect was most prominent in media conditions (low-serum, hyperglycemic medium) that support TnT formation (1.3–1.9-fold difference). Fluorescence and electron microscopy confirmed the purity of isolated exosomes and revealed that they localized predominantly at the base of and within TnTs, in addition to the extracellular environment. Time-lapse microscopic imaging demonstrated uptake of tumor exosomes by TnTs, which facilitated intercellular transfer of these exosomes between connected cells. Mesothelioma cells connected via TnTs were also significantly enriched for lipid rafts at nearly a 2-fold higher number compared with cells not connected by TnTs. Our findings provide supportive evidence of exosomes as potential chemotactic stimuli for TnT formation, and also lipid raft formation as a potential biomarker for TnT-forming cells. - Highlights: • Exosomes derived from malignant cells can stimulate an increased rate in the formation of tunneling nanotubes. • Tunneling nanotubes can serve as conduits for intercellular transfer of these exosomes. • Most notably, exosomes derived from benign mesothelial cells had no effect on nanotube formation. • Cells forming nanotubes were enriched in lipid rafts at a greater number compared with cells not forming nanotubes. • Our findings suggest causal and potentially synergistic association of exosomes and tunneling nanotubes in cancer. Tunneling nanotubes (TnTs) are long, non-adherent, actin-based cellular extensions that act as conduits for transport of cellular cargo between connected cells. The mechanisms of nanotube formation and the effects of the tumor microenvironment and cellular signals on TnT formation are unknown. In the present study, we explored exosomes as potential mediators of TnT formation in mesothelioma and the potential relationship of lipid rafts to TnT formation. Mesothelioma cells co-cultured with exogenous mesothelioma-derived exosomes formed more TnTs than cells cultured without exosomes within 24-48h; and this effect was most prominent in media conditions (low-serum, hyperglycemic medium) that support TnT formation (1.3-1.9-fold difference). Fluorescence and electron microscopy confirmed the purity of isolated exosomes and revealed that they localized predominantly at the base of and within TnTs, in addition to the extracellular environment. Time-lapse microscopic imaging demonstrated uptake of tumor exosomes by TnTs, which facilitated intercellular transfer of these exosomes between connected cells. Mesothelioma cells connected via TnTs were also significantly enriched for lipid rafts at nearly a 2-fold higher number compared with cells not connected by TnTs. Our findings provide supportive evidence of exosomes as potential chemotactic stimuli for TnT formation, and also lipid raft formation as a potential biomarker for TnT-forming cells. [PUBLICATION ABSTRACT] |
Author | Moreira, André L. Thayanithy, Venugopal Babatunde, Victor Steer, Clifford J. Downey, Robert J. Oh, Sanghoon Fujisawa, Sho Moore, Malcolm A.S. Barlas, Afsar Ke, Xu Lou, Emil Dickson, Elizabeth L. Manova-Todorova, Katia Wong, Phillip Romin, Yevgeniy Subramanian, Subbaya |
AuthorAffiliation | 7 Departments of Medicine and Genetics, Cell Biology and Development, University of Minnesota, Minneapolis, Minnesota 55455, USA 2 Moore Laboratory, Department of Cell Biology, Sloan-Kettering Institute, Memorial Sloan-Kettering Cancer Center, New York, New York, 10021, USA 4 Molecular Cytology, Memorial Sloan-Kettering Cancer Center, New York, New York, 10021, USA 6 Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York, 10021, USA 5 Department of Pathology, Memorial Sloan-Kettering Cancer Center, New York, New York, 10021, USA 3 Department of Obstetrics & Gynecology, Division of Gynecologic Oncology, University of Minnesota, Minneapolis, Minnesota 55455, USA 1 Department of Medicine, Division of Hematology, Oncology and Transplantation, University of Minnesota, Minneapolis, Minnesota 55455, USA 8 Department of Surgery, University of Minnesota, Minneapolis, Minnesota 55455, USA |
AuthorAffiliation_xml | – name: 4 Molecular Cytology, Memorial Sloan-Kettering Cancer Center, New York, New York, 10021, USA – name: 2 Moore Laboratory, Department of Cell Biology, Sloan-Kettering Institute, Memorial Sloan-Kettering Cancer Center, New York, New York, 10021, USA – name: 7 Departments of Medicine and Genetics, Cell Biology and Development, University of Minnesota, Minneapolis, Minnesota 55455, USA – name: 8 Department of Surgery, University of Minnesota, Minneapolis, Minnesota 55455, USA – name: 1 Department of Medicine, Division of Hematology, Oncology and Transplantation, University of Minnesota, Minneapolis, Minnesota 55455, USA – name: 6 Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York, 10021, USA – name: 3 Department of Obstetrics & Gynecology, Division of Gynecologic Oncology, University of Minnesota, Minneapolis, Minnesota 55455, USA – name: 5 Department of Pathology, Memorial Sloan-Kettering Cancer Center, New York, New York, 10021, USA |
Author_xml | – sequence: 1 givenname: Venugopal surname: Thayanithy fullname: Thayanithy, Venugopal organization: Department of Medicine, Division of Hematology, Oncology and Transplantation, University of Minnesota, Minneapolis, MN 55455, USA – sequence: 2 givenname: Victor surname: Babatunde fullname: Babatunde, Victor organization: Moore Laboratory, Department of Cell Biology, Sloan-Kettering Institute, Memorial Sloan-Kettering Cancer Center, New York, NY 10021, USA – sequence: 3 givenname: Elizabeth L. surname: Dickson fullname: Dickson, Elizabeth L. organization: Department of Obstetrics & Gynecology, Division of Gynecologic Oncology, University of Minnesota, Minneapolis, MN 55455, USA – sequence: 4 givenname: Phillip surname: Wong fullname: Wong, Phillip organization: Department of Medicine, Division of Hematology, Oncology and Transplantation, University of Minnesota, Minneapolis, MN 55455, USA – sequence: 5 givenname: Sanghoon surname: Oh fullname: Oh, Sanghoon organization: Molecular Cytology, Memorial Sloan-Kettering Cancer Center, New York, NY 10021, USA – sequence: 6 givenname: Xu surname: Ke fullname: Ke, Xu organization: Molecular Cytology, Memorial Sloan-Kettering Cancer Center, New York, NY 10021, USA – sequence: 7 givenname: Afsar surname: Barlas fullname: Barlas, Afsar organization: Molecular Cytology, Memorial Sloan-Kettering Cancer Center, New York, NY 10021, USA – sequence: 8 givenname: Sho surname: Fujisawa fullname: Fujisawa, Sho organization: Molecular Cytology, Memorial Sloan-Kettering Cancer Center, New York, NY 10021, USA – sequence: 9 givenname: Yevgeniy surname: Romin fullname: Romin, Yevgeniy organization: Molecular Cytology, Memorial Sloan-Kettering Cancer Center, New York, NY 10021, USA – sequence: 10 givenname: André L. surname: Moreira fullname: Moreira, André L. organization: Department of Pathology, Memorial Sloan-Kettering Cancer Center, New York, NY 10021, USA – sequence: 11 givenname: Robert J. surname: Downey fullname: Downey, Robert J. organization: Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, NY 10021, USA – sequence: 12 givenname: Clifford J. surname: Steer fullname: Steer, Clifford J. organization: Departments of Medicine and Genetics, Cell Biology and Development, University of Minnesota, Minneapolis, MN 55455, USA – sequence: 13 givenname: Subbaya surname: Subramanian fullname: Subramanian, Subbaya organization: Department of Surgery, University of Minnesota, Minneapolis, MN 55455, USA – sequence: 14 givenname: Katia surname: Manova-Todorova fullname: Manova-Todorova, Katia organization: Molecular Cytology, Memorial Sloan-Kettering Cancer Center, New York, NY 10021, USA – sequence: 15 givenname: Malcolm A.S. surname: Moore fullname: Moore, Malcolm A.S. organization: Moore Laboratory, Department of Cell Biology, Sloan-Kettering Institute, Memorial Sloan-Kettering Cancer Center, New York, NY 10021, USA – sequence: 16 givenname: Emil surname: Lou fullname: Lou, Emil email: emil-lou@umn.edu organization: Department of Medicine, Division of Hematology, Oncology and Transplantation, University of Minnesota, Minneapolis, MN 55455, USA |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24468420$$D View this record in MEDLINE/PubMed https://www.osti.gov/biblio/22395889$$D View this record in Osti.gov |
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Keywords | RT SMACs Tunneling nanotubes Mesothelioma Lipid rafts CTCF MAPK Exosomes ATCC Intercellular transfer MPs FBS mTOR AMPK TnTs Intercellular communication nm DIC ELISA |
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SubjectTerms | 60 APPLIED LIFE SCIENCES ACTIN Biological Transport - physiology CATTLE Cell Communication - physiology Cell Culture Techniques Cell Line, Tumor ENZYME IMMUNOASSAY ENZYMES Exosomes Exosomes - metabolism FLUORESCENCE Humans Intercellular communication Intercellular transfer Lipid rafts LIPIDS Lung cancer Membrane Microdomains - metabolism Mesothelioma Mesothelioma - metabolism NANOTUBES NEOPLASMS Signal Transduction Tumor Microenvironment Tunneling nanotubes |
Title | Tumor exosomes induce tunneling nanotubes in lipid raft-enriched regions of human mesothelioma cells |
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