Extracellular RNA in oncogenesis, metastasis and drug resistance

Extracellular vesicles and nanoparticles (EVPs) are now recognized as a novel form of cell–cell communication. All cells release a wide array of heterogeneous EVPs with distinct protein, lipid, and RNA content, dependent on the pathophysiological state of the donor cell. The overall cargo content in...

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Main Authors: Hannah Nelson, Sherman Qu, Jeffrey L. Franklin, Qi Liu, Heather H. Pua, Kasey C. Vickers, Alissa M. Weaver, Robert J. Coffey, James G. Patton
Format: Article
Language:English
Published: Taylor & Francis Group 2024-12-01
Series:RNA Biology
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Online Access:https://www.tandfonline.com/doi/10.1080/15476286.2024.2385607
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author Hannah Nelson
Sherman Qu
Jeffrey L. Franklin
Qi Liu
Heather H. Pua
Kasey C. Vickers
Alissa M. Weaver
Robert J. Coffey
James G. Patton
author_facet Hannah Nelson
Sherman Qu
Jeffrey L. Franklin
Qi Liu
Heather H. Pua
Kasey C. Vickers
Alissa M. Weaver
Robert J. Coffey
James G. Patton
author_sort Hannah Nelson
collection DOAJ
description Extracellular vesicles and nanoparticles (EVPs) are now recognized as a novel form of cell–cell communication. All cells release a wide array of heterogeneous EVPs with distinct protein, lipid, and RNA content, dependent on the pathophysiological state of the donor cell. The overall cargo content in EVPs is not equivalent to cellular levels, implying a regulated pathway for selection and export. In cancer, release and uptake of EVPs within the tumour microenvironment can influence growth, proliferation, invasiveness, and immune evasion. Secreted EVPs can also have distant, systemic effects that can promote metastasis. Here, we review current knowledge of EVP biogenesis and cargo selection with a focus on the role that extracellular RNA plays in oncogenesis and metastasis. Almost all subtypes of RNA have been identified in EVPs, with miRNAs being the best characterized. We review the roles of specific miRNAs that have been detected in EVPs and that play a role in oncogenesis and metastasis.
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publishDate 2024-12-01
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series RNA Biology
spelling doaj-art-0149ce03e8b64eb8b051c0b241d310772025-08-20T02:39:08ZengTaylor & Francis GroupRNA Biology1547-62861555-85842024-12-0121180581910.1080/15476286.2024.2385607Extracellular RNA in oncogenesis, metastasis and drug resistanceHannah Nelson0Sherman Qu1Jeffrey L. Franklin2Qi Liu3Heather H. Pua4Kasey C. Vickers5Alissa M. Weaver6Robert J. Coffey7James G. Patton8Department of Biological Sciences, Vanderbilt University and Vanderbilt University Medical Center, Nashville, TN, USADepartment of Biological Sciences, Vanderbilt University and Vanderbilt University Medical Center, Nashville, TN, USACenter for Extracellular Vesicle Research, Vanderbilt University School of Medicine, Nashville, TN, USACenter for Extracellular Vesicle Research, Vanderbilt University School of Medicine, Nashville, TN, USACenter for Extracellular Vesicle Research, Vanderbilt University School of Medicine, Nashville, TN, USACenter for Extracellular Vesicle Research, Vanderbilt University School of Medicine, Nashville, TN, USACenter for Extracellular Vesicle Research, Vanderbilt University School of Medicine, Nashville, TN, USACenter for Extracellular Vesicle Research, Vanderbilt University School of Medicine, Nashville, TN, USADepartment of Biological Sciences, Vanderbilt University and Vanderbilt University Medical Center, Nashville, TN, USAExtracellular vesicles and nanoparticles (EVPs) are now recognized as a novel form of cell–cell communication. All cells release a wide array of heterogeneous EVPs with distinct protein, lipid, and RNA content, dependent on the pathophysiological state of the donor cell. The overall cargo content in EVPs is not equivalent to cellular levels, implying a regulated pathway for selection and export. In cancer, release and uptake of EVPs within the tumour microenvironment can influence growth, proliferation, invasiveness, and immune evasion. Secreted EVPs can also have distant, systemic effects that can promote metastasis. Here, we review current knowledge of EVP biogenesis and cargo selection with a focus on the role that extracellular RNA plays in oncogenesis and metastasis. Almost all subtypes of RNA have been identified in EVPs, with miRNAs being the best characterized. We review the roles of specific miRNAs that have been detected in EVPs and that play a role in oncogenesis and metastasis.https://www.tandfonline.com/doi/10.1080/15476286.2024.2385607extracellular vesiclesnanoparticlesRNACancerTumor microenviromentmetastasis
spellingShingle Hannah Nelson
Sherman Qu
Jeffrey L. Franklin
Qi Liu
Heather H. Pua
Kasey C. Vickers
Alissa M. Weaver
Robert J. Coffey
James G. Patton
Extracellular RNA in oncogenesis, metastasis and drug resistance
RNA Biology
extracellular vesicles
nanoparticles
RNA
Cancer
Tumor microenviroment
metastasis
title Extracellular RNA in oncogenesis, metastasis and drug resistance
title_full Extracellular RNA in oncogenesis, metastasis and drug resistance
title_fullStr Extracellular RNA in oncogenesis, metastasis and drug resistance
title_full_unstemmed Extracellular RNA in oncogenesis, metastasis and drug resistance
title_short Extracellular RNA in oncogenesis, metastasis and drug resistance
title_sort extracellular rna in oncogenesis metastasis and drug resistance
topic extracellular vesicles
nanoparticles
RNA
Cancer
Tumor microenviroment
metastasis
url https://www.tandfonline.com/doi/10.1080/15476286.2024.2385607
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AT shermanqu extracellularrnainoncogenesismetastasisanddrugresistance
AT jeffreylfranklin extracellularrnainoncogenesismetastasisanddrugresistance
AT qiliu extracellularrnainoncogenesismetastasisanddrugresistance
AT heatherhpua extracellularrnainoncogenesismetastasisanddrugresistance
AT kaseycvickers extracellularrnainoncogenesismetastasisanddrugresistance
AT alissamweaver extracellularrnainoncogenesismetastasisanddrugresistance
AT robertjcoffey extracellularrnainoncogenesismetastasisanddrugresistance
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