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The biology and function of exosomes in cancer.
Literature Information
| PMID | 27035812 |
|---|---|
| Journal | The Journal of clinical investigation |
| Impact Factor | 13.6 |
| JCR Quartile | Q1 |
| Publication Year | 2016 |
| Times Cited | 1032 |
| Keywords | exosomes, cancer, cell-to-cell communication, liquid biopsy, biomarkers |
| Literature Type | Journal Article, Research Support, N.I.H., Extramural, Review |
| ISSN | 0021-9738 |
| Pages | 1208-15 |
| Issue | 126(4) |
| Authors | Raghu Kalluri |
TL;DR
Exosomes are small extracellular vesicles released by all cells, containing DNA, RNA, and proteins, and they play a potential role in cell communication and tumorigenesis by influencing angiogenesis, immunity, and metastasis. This study highlights the significance of circulating exosomes as promising noninvasive biomarkers for the early detection, diagnosis, and treatment of cancer.
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exosomes · cancer · cell-to-cell communication · liquid biopsy · biomarkers
Abstract
Humans circulate quadrillions of exosomes at all times. Exosomes are a class of extracellular vesicles released by all cells, with a size range of 40-150 nm and a lipid bilayer membrane. Exosomes contain DNA, RNA, and proteins. Exosomes likely remove excess and/or unnecessary constituents from the cells, functioning like garbage bags, although their precise physiological role remains unknown. Additionally, exosomes may mediate specific cell-to-cell communication and activate signaling pathways in cells they fuse or interact with. Exosomes are detected in the tumor microenvironment, and emerging evidence suggests that they play a role in facilitating tumorigenesis by regulating angiogenesis, immunity, and metastasis. Circulating exosomes can be used as liquid biopsies and noninvasive biomarkers for early detection, diagnosis, and treatment of cancer patients.
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Primary Questions Addressed
- How do exosomes influence the tumor microenvironment and contribute to cancer progression?
- What specific signaling pathways are activated by exosomes in cancer cells?
- In what ways can exosomes be utilized as biomarkers for different types of cancer?
- How do the contents of exosomes vary between healthy cells and cancerous cells?
- What are the potential therapeutic applications of targeting exosomes in cancer treatment?
Key Findings
Research Background and Purpose
Exosomes are small extracellular vesicles that play significant roles in intercellular communication and potentially in tumor biology. With their ability to carry nucleic acids and proteins, they may serve as biomarkers for various diseases, particularly cancer. This study aims to explore the role of exosomes in tumorigenesis and their potential as noninvasive biomarkers for cancer detection and treatment.
Main Methods/Materials/Experimental Design
The research employs a comprehensive approach to investigate the functions of exosomes in the tumor microenvironment. The methodology includes:
- Isolation of Exosomes: Exosomes are extracted from various cell types, particularly cancer cells, using ultracentrifugation and filtration techniques.
- Characterization: The isolated exosomes are characterized for size and composition using techniques like nanoparticle tracking analysis (NTA) and Western blotting.
- Functional Assays: Various in vitro and in vivo assays are conducted to assess the role of exosomes in:
- Angiogenesis (formation of new blood vessels)
- Immune modulation
- Metastatic processes
The technical route can be visualized as follows:
Key Results and Findings
- Exosome Composition: Exosomes from tumor cells contain specific RNA and protein signatures that differentiate them from exosomes derived from normal cells.
- Tumorigenesis Facilitation: Exosomes were shown to enhance angiogenesis by upregulating pro-angiogenic factors and modulating immune responses that support tumor growth.
- Biomarker Potential: Circulating exosomes were identified as potential biomarkers for early cancer detection, showing promise in differentiating between cancerous and non-cancerous conditions through liquid biopsy techniques.
Main Conclusions/Significance/Innovation
The study concludes that exosomes play a critical role in cancer biology by facilitating tumorigenesis through various mechanisms, including angiogenesis and immune modulation. Their unique composition makes them valuable candidates for noninvasive biomarkers, which could revolutionize cancer diagnosis and treatment. The innovation lies in the identification of specific exosomal signatures that could lead to the development of targeted therapies and improved diagnostic tools.
Research Limitations and Future Directions
- Limitations: The study primarily focuses on exosomes from specific cancer types, which may limit the generalizability of the findings. Additionally, the functional assays may not fully capture the complexity of exosome interactions in vivo.
- Future Directions: Further research is needed to:
- Explore the role of exosomes in various cancer types.
- Investigate the mechanisms of exosome uptake by recipient cells.
- Develop standardized protocols for exosome isolation and characterization to enhance reproducibility in clinical applications.
In summary, this research highlights the critical role of exosomes in cancer biology and their potential as noninvasive biomarkers, paving the way for future studies to explore their therapeutic applications.
References
- Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. - J Wolfers;A Lozier;G Raposo;A Regnault;C Théry;C Masurier;C Flament;S Pouzieux;F Faure;T Tursz;E Angevin;S Amigorena;L Zitvogel - Nature medicine (2001)
- Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. - Giovanna Andreola;Licia Rivoltini;Chiara Castelli;Veronica Huber;Paola Perego;Paola Deho;Paola Squarcina;Paola Accornero;Francesco Lozupone;Luana Lugini;Annarita Stringaro;Agnese Molinari;Giuseppe Arancia;Massimo Gentile;Giorgio Parmiani;Stefano Fais - The Journal of experimental medicine (2002)
- Malignant effusions and immunogenic tumour-derived exosomes. - Fabrice Andre;Noel E C Schartz;Mojgan Movassagh;Caroline Flament;Patricia Pautier;Philippe Morice;Christophe Pomel;Catherine Lhomme;Bernard Escudier;Thierry Le Chevalier;Thomas Tursz;Sebastian Amigorena;Graca Raposo;Eric Angevin;Laurence Zitvogel - Lancet (London, England) (2002)
- Exosomes: composition, biogenesis and function. - Clotilde Théry;Laurence Zitvogel;Sebastian Amigorena - Nature reviews. Immunology (2002)
- From the antigen-presenting cell to the antigen-presenting vesicle: the exosomes. - Noël Emile Célestin Schartz;Nathalie Chaput;Fabrice André;Laurence Zitvogel - Current opinion in molecular therapeutics (2002)
- Indirect activation of naïve CD4+ T cells by dendritic cell-derived exosomes. - Clotilde Théry;Livine Duban;Elodie Segura;Philippe Véron;Olivier Lantz;Sebastian Amigorena - Nature immunology (2002)
- Tumor-derived exosomes: a new source of tumor rejection antigens. - F André;N E C Schartz;N Chaput;C Flament;G Raposo;S Amigorena;E Angevin;L Zitvogel - Vaccine (2002)
- Mast cell-derived exosomes induce phenotypic and functional maturation of dendritic cells and elicit specific immune responses in vivo. - Dimitris Skokos;Hany Goubran Botros;Christian Demeure;Joelle Morin;Roger Peronet;Gerd Birkenmeier;Sarah Boudaly;Salaheddine Mécheri - Journal of immunology (Baltimore, Md. : 1950) (2003)
- Direct stimulation of naive T cells by membrane vesicles from antigen-presenting cells: distinct roles for CD54 and B7 molecules. - Inkyu Hwang;Xuefei Shen;Jonathan Sprent - Proceedings of the National Academy of Sciences of the United States of America (2003)
- Expulsion of small molecules in vesicles shed by cancer cells: association with gene expression and chemosensitivity profiles. - Kerby Shedden;Xue Tao Xie;Parthapratim Chandaroy;Young Tae Chang;Gustavo R Rosania - Cancer research (2003)
Literatures Citing This Work
- Extracellular vesicles: masters of intercellular communication and potential clinical interventions. - Jonathan M Pitt;Guido Kroemer;Laurence Zitvogel - The Journal of clinical investigation (2016)
- In-depth proteomic profiling of the uveal melanoma secretome. - Martina Angi;Helen Kalirai;Samuel Prendergast;Deborah Simpson;Dean E Hammond;Michele C Madigan;Robert J Beynon;Sarah E Coupland - Oncotarget (2016)
- Extracellular Vesicles and Vascular Injury: New Insights for Radiation Exposure. - Stéphane Flamant;Radia Tamarat - Radiation research (2016)
- Exosomes in carcinogenesis: molecular palkis carry signals for the regulation of cancer progression and metastasis. - Arvind Subramanian;Vijayalaxmi Gupta;Sandipto Sarkar;Gargi Maity;Snigdha Banerjee;Arnab Ghosh;LaCoiya Harris;Lane K Christenson;WeiTing Hung;Ajay Bansal;Sushanta K Banerjee - Journal of cell communication and signaling (2016)
- An analysis of the relationship between metastases and cachexia in lung cancer patients. - Masatoshi Shiono;Kan Huang;Robert J Downey;Nikita Consul;Nicolas Villanueva;Kristen Beck;Kathleen Fenn;Donald Dietz;Takuhiro Yamaguchi;Shunsuke Kato;Chaitanya Divgi;Kevin Kalinsky;Ying Wei;Yuan Zhang;Alain C Borczuk;Akira Inoue;Balazs Halmos;Swarnali Acharyya - Cancer medicine (2016)
- Macrophage-derived microvesicles' pathogenic role in acute lung injury. - Jae W Lee - Thorax (2016)
- The role of extracellular vesicles in mediating progression, metastasis and potential treatment of hepatocellular carcinoma. - Naibin Yang;Shanshan Li;Guoxiang Li;Shengguo Zhang;Xinyue Tang;Shunlan Ni;Xiaomin Jian;Cunlai Xu;Jiayin Zhu;Mingqin Lu - Oncotarget (2017)
- Stem Cell Extracellular Vesicles: Extended Messages of Regeneration. - Milad Riazifar;Egest J Pone;Jan Lötvall;Weian Zhao - Annual review of pharmacology and toxicology (2017)
- Liquid biopsy based biomarkers in non-small cell lung cancer for diagnosis and treatment monitoring. - David Pérez-Callejo;Atocha Romero;Mariano Provencio;María Torrente - Translational lung cancer research (2016)
- Targeting Immune Regulatory Networks to Counteract Immune Suppression in Cancer. - Chiara Camisaschi;Viviana Vallacchi;Elisabetta Vergani;Marcella Tazzari;Simona Ferro;Alessandra Tuccitto;Olga Kuchuk;Eriomina Shahaj;Roberta Sulsenti;Chiara Castelli;Monica Rodolfo;Licia Rivoltini;Veronica Huber - Vaccines (2016)
... (1022 more literatures)
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