Mechanisms of nuclear content loading to exosomes
Nuclear-derived exosomes generated by micronuclear collapse provide an accurate snapshot of genomic features in ovarian cancer. Exosome cargoes are highly varied and include proteins, small RNAs, and genomic DNA (gDNA). The presence of gDNA suggests that different intracellular compartments contribu...
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| Published in | Science advances Vol. 5; no. 11; p. eaax8849 |
|---|---|
| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Association for the Advancement of Science
01.11.2019
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| Subjects | |
| Online Access | Get full text |
| ISSN | 2375-2548 2375-2548 |
| DOI | 10.1126/sciadv.aax8849 |
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| Abstract | Nuclear-derived exosomes generated by micronuclear collapse provide an accurate snapshot of genomic features in ovarian cancer.
Exosome cargoes are highly varied and include proteins, small RNAs, and genomic DNA (gDNA). The presence of gDNA suggests that different intracellular compartments contribute to exosome loading, resulting in distinct exosome subpopulations. However, the loading of gDNA and other nuclear contents into exosomes (nExo) remains poorly understood. Here, we identify the relationship between cancer cell micronuclei (MN), which are markers of genomic instability, and nExo formation. Imaging flow cytometry analyses reveal that 10% of exosomes derived from cancer cells and <1% of exosomes derived from blood and ascites from patients with ovarian cancer carry nuclear contents. Treatment with genotoxic drugs resulted in increased MN and nExos both in vitro and in vivo. We observed that multivesicular body precursors and exosomal markers, such as the tetraspanins, directly interact with MN. Collectively, this work provides new insights related to nExos, which have implications for cancer biomarker development. |
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| AbstractList | Nuclear-derived exosomes generated by micronuclear collapse provide an accurate snapshot of genomic features in ovarian cancer.
Exosome cargoes are highly varied and include proteins, small RNAs, and genomic DNA (gDNA). The presence of gDNA suggests that different intracellular compartments contribute to exosome loading, resulting in distinct exosome subpopulations. However, the loading of gDNA and other nuclear contents into exosomes (nExo) remains poorly understood. Here, we identify the relationship between cancer cell micronuclei (MN), which are markers of genomic instability, and nExo formation. Imaging flow cytometry analyses reveal that 10% of exosomes derived from cancer cells and <1% of exosomes derived from blood and ascites from patients with ovarian cancer carry nuclear contents. Treatment with genotoxic drugs resulted in increased MN and nExos both in vitro and in vivo. We observed that multivesicular body precursors and exosomal markers, such as the tetraspanins, directly interact with MN. Collectively, this work provides new insights related to nExos, which have implications for cancer biomarker development. Exosome cargoes are highly varied and include proteins, small RNAs, and genomic DNA (gDNA). The presence of gDNA suggests that different intracellular compartments contribute to exosome loading, resulting in distinct exosome subpopulations. However, the loading of gDNA and other nuclear contents into exosomes (nExo) remains poorly understood. Here, we identify the relationship between cancer cell micronuclei (MN), which are markers of genomic instability, and nExo formation. Imaging flow cytometry analyses reveal that 10% of exosomes derived from cancer cells and <1% of exosomes derived from blood and ascites from patients with ovarian cancer carry nuclear contents. Treatment with genotoxic drugs resulted in increased MN and nExos both in vitro and in vivo. We observed that multivesicular body precursors and exosomal markers, such as the tetraspanins, directly interact with MN. Collectively, this work provides new insights related to nExos, which have implications for cancer biomarker development. Exosome cargoes are highly varied and include proteins, small RNAs, and genomic DNA (gDNA). The presence of gDNA suggests that different intracellular compartments contribute to exosome loading, resulting in distinct exosome subpopulations. However, the loading of gDNA and other nuclear contents into exosomes (nExo) remains poorly understood. Here, we identify the relationship between cancer cell micronuclei (MN), which are markers of genomic instability, and nExo formation. Imaging flow cytometry analyses reveal that 10% of exosomes derived from cancer cells and <1% of exosomes derived from blood and ascites from patients with ovarian cancer carry nuclear contents. Treatment with genotoxic drugs resulted in increased MN and nExos both in vitro and in vivo. We observed that multivesicular body precursors and exosomal markers, such as the tetraspanins, directly interact with MN. Collectively, this work provides new insights related to nExos, which have implications for cancer biomarker development.Exosome cargoes are highly varied and include proteins, small RNAs, and genomic DNA (gDNA). The presence of gDNA suggests that different intracellular compartments contribute to exosome loading, resulting in distinct exosome subpopulations. However, the loading of gDNA and other nuclear contents into exosomes (nExo) remains poorly understood. Here, we identify the relationship between cancer cell micronuclei (MN), which are markers of genomic instability, and nExo formation. Imaging flow cytometry analyses reveal that 10% of exosomes derived from cancer cells and <1% of exosomes derived from blood and ascites from patients with ovarian cancer carry nuclear contents. Treatment with genotoxic drugs resulted in increased MN and nExos both in vitro and in vivo. We observed that multivesicular body precursors and exosomal markers, such as the tetraspanins, directly interact with MN. Collectively, this work provides new insights related to nExos, which have implications for cancer biomarker development. |
| Author | Oliphint, Paul Allen Song, Xingzhi Laurent, Louise C. Clise-Dwyer, Karen De Hoff, Peter Zhang, Jianhua Sood, Anil K. O’Halloran, Theresa J. Burks, Jared K. Villar-Prados, Alejandro Yokoi, Akira Morey, Robert Liu, Jinsong Roszik, Jason |
| Author_xml | – sequence: 1 givenname: Akira orcidid: 0000-0003-0789-5102 surname: Yokoi fullname: Yokoi, Akira organization: Department of Gynecologic Oncology and Reproductive Medicine, University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 2 givenname: Alejandro orcidid: 0000-0001-6900-3267 surname: Villar-Prados fullname: Villar-Prados, Alejandro organization: Department of Gynecologic Oncology and Reproductive Medicine, University of Texas MD Anderson Cancer Center, Houston, TX, USA., Department of Medicine, Stanford University, Stanford, CA, USA – sequence: 3 givenname: Paul Allen orcidid: 0000-0001-9713-5574 surname: Oliphint fullname: Oliphint, Paul Allen organization: Department of Molecular Biosciences and Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, TX, USA – sequence: 4 givenname: Jianhua orcidid: 0000-0001-5412-9860 surname: Zhang fullname: Zhang, Jianhua organization: Department of Genomic Medicine, University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 5 givenname: Xingzhi surname: Song fullname: Song, Xingzhi organization: Department of Genomic Medicine, University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 6 givenname: Peter surname: De Hoff fullname: De Hoff, Peter organization: Department of Obstetrics, Gynecology, and Reproductive Sciences, University of California, San Diego, La Jolla, CA, USA – sequence: 7 givenname: Robert surname: Morey fullname: Morey, Robert organization: Department of Obstetrics, Gynecology, and Reproductive Sciences, University of California, San Diego, La Jolla, CA, USA., Bioinformatics and Systems Biology Graduate Program, University of California, San Diego, La Jolla, CA, USA – sequence: 8 givenname: Jinsong surname: Liu fullname: Liu, Jinsong organization: Department of Pathology, University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 9 givenname: Jason orcidid: 0000-0002-4561-6170 surname: Roszik fullname: Roszik, Jason organization: Department of Genomic Medicine, University of Texas MD Anderson Cancer Center, Houston, TX, USA., Department of Melanoma Medical Oncology, University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 10 givenname: Karen surname: Clise-Dwyer fullname: Clise-Dwyer, Karen organization: Section of Transplant Immunology, Department of Stem Cell Transplantation and Cellular Therapy, University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 11 givenname: Jared K. orcidid: 0000-0002-6173-9074 surname: Burks fullname: Burks, Jared K. organization: Department of Leukemia and Division of Cancer Medicine, University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 12 givenname: Theresa J. surname: O’Halloran fullname: O’Halloran, Theresa J. organization: Department of Molecular Biosciences and Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, TX, USA – sequence: 13 givenname: Louise C. orcidid: 0000-0002-2095-7534 surname: Laurent fullname: Laurent, Louise C. organization: Department of Obstetrics, Gynecology, and Reproductive Sciences, University of California, San Diego, La Jolla, CA, USA., Bioinformatics and Systems Biology Graduate Program, University of California, San Diego, La Jolla, CA, USA – sequence: 14 givenname: Anil K. orcidid: 0000-0003-4242-1762 surname: Sood fullname: Sood, Anil K. organization: Department of Gynecologic Oncology and Reproductive Medicine, University of Texas MD Anderson Cancer Center, Houston, TX, USA., Center for RNA Interference and Non-Coding RNA, University of Texas MD Anderson Cancer Center, Houston, TX, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31799396$$D View this record in MEDLINE/PubMed |
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| Copyright | Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). 2019 The Authors |
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| Snippet | Nuclear-derived exosomes generated by micronuclear collapse provide an accurate snapshot of genomic features in ovarian cancer.
Exosome cargoes are highly... Exosome cargoes are highly varied and include proteins, small RNAs, and genomic DNA (gDNA). The presence of gDNA suggests that different intracellular... |
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| SubjectTerms | Biomarkers, Tumor - metabolism Cancer Cell Biology Cell Line, Tumor DNA - genetics DNA Copy Number Variations - genetics DNA Damage - drug effects DNA Damage - genetics Exosomes - metabolism Female Humans Micronuclei, Chromosome-Defective Ovarian Neoplasms - genetics SciAdv r-articles Tetraspanins - metabolism |
| Title | Mechanisms of nuclear content loading to exosomes |
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