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Distinct prostate cancer-related mRNA cargo in extracellular vesicle subsets from prostate cell lines

BACKGROUND: Multiple types of extracellular vesicles (EVs), including microvesicles (MVs) and exosomes (EXOs), are released by all cells constituting part of the cellular EV secretome. The bioactive cargo of EVs can be shuffled between cells and consists of lipids, metabolites, proteins, and nucleic...

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Autores principales: Lázaro-Ibáñez, Elisa, Lunavat, Taral R., Jang, Su Chul, Escobedo-Lucea, Carmen, Oliver-De La Cruz, Jorge, Siljander, Pia, Lötvall, Jan, Yliperttula, Marjo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5286827/
https://www.ncbi.nlm.nih.gov/pubmed/28143451
http://dx.doi.org/10.1186/s12885-017-3087-x
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author Lázaro-Ibáñez, Elisa
Lunavat, Taral R.
Jang, Su Chul
Escobedo-Lucea, Carmen
Oliver-De La Cruz, Jorge
Siljander, Pia
Lötvall, Jan
Yliperttula, Marjo
author_facet Lázaro-Ibáñez, Elisa
Lunavat, Taral R.
Jang, Su Chul
Escobedo-Lucea, Carmen
Oliver-De La Cruz, Jorge
Siljander, Pia
Lötvall, Jan
Yliperttula, Marjo
author_sort Lázaro-Ibáñez, Elisa
collection PubMed
description BACKGROUND: Multiple types of extracellular vesicles (EVs), including microvesicles (MVs) and exosomes (EXOs), are released by all cells constituting part of the cellular EV secretome. The bioactive cargo of EVs can be shuffled between cells and consists of lipids, metabolites, proteins, and nucleic acids, including multiple RNA species from non-coding RNAs to messenger RNAs (mRNAs). In this study, we hypothesized that the mRNA cargo of EVs could differ based on the EV cellular origin and subpopulation analyzed. METHODS: We isolated MVs and EXOs from PC-3 and LNCaP prostate cancer cells by differential centrifugation and compared them to EVs derived from the benign PNT2 prostate cells. The relative mRNA levels of 84 prostate cancer-related genes were investigated and validated using quantitative reverse transcription PCR arrays. RESULTS: Based on the mRNA abundance, MVs rather than EXOs were enriched in the analyzed transcripts, providing a snapshot of the tumor transcriptome. LNCaP MVs specifically contained significantly increased mRNA levels of NK3 Homeobox 1 (NKX3-1), transmembrane protease serine 2 (TMPRSS2), and tumor protein 53 (TP53) genes, whereas PC-3 MVs carried increased mRNA levels of several genes including, caveolin-2 (CAV2), glutathione S-transferase pi 1 (GSTP1), pescadillo ribosomal biogenesis factor 1 (PES1), calmodulin regulated spectrin associated protein 1 (CAMSAP1), zinc-finger protein 185 (ZNF185), and others compared to PNT2 MVs. Additionally, ETS variant 1 (ETV1) and fatty acid synthase (FASN) mRNAs identified in LNCaP- and PC-3- derived MVs highly correlated with prostate cancer progression. CONCLUSIONS: Our study provides new understandings of the variability of the mRNA cargo of MVs and EXOs from different cell lines despite same cancer origin, which is essential to better understand the the proportion of the cell transcriptome that can be detected within EVs and to evaluate their role in disease diagnosis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12885-017-3087-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-52868272017-02-06 Distinct prostate cancer-related mRNA cargo in extracellular vesicle subsets from prostate cell lines Lázaro-Ibáñez, Elisa Lunavat, Taral R. Jang, Su Chul Escobedo-Lucea, Carmen Oliver-De La Cruz, Jorge Siljander, Pia Lötvall, Jan Yliperttula, Marjo BMC Cancer Research Article BACKGROUND: Multiple types of extracellular vesicles (EVs), including microvesicles (MVs) and exosomes (EXOs), are released by all cells constituting part of the cellular EV secretome. The bioactive cargo of EVs can be shuffled between cells and consists of lipids, metabolites, proteins, and nucleic acids, including multiple RNA species from non-coding RNAs to messenger RNAs (mRNAs). In this study, we hypothesized that the mRNA cargo of EVs could differ based on the EV cellular origin and subpopulation analyzed. METHODS: We isolated MVs and EXOs from PC-3 and LNCaP prostate cancer cells by differential centrifugation and compared them to EVs derived from the benign PNT2 prostate cells. The relative mRNA levels of 84 prostate cancer-related genes were investigated and validated using quantitative reverse transcription PCR arrays. RESULTS: Based on the mRNA abundance, MVs rather than EXOs were enriched in the analyzed transcripts, providing a snapshot of the tumor transcriptome. LNCaP MVs specifically contained significantly increased mRNA levels of NK3 Homeobox 1 (NKX3-1), transmembrane protease serine 2 (TMPRSS2), and tumor protein 53 (TP53) genes, whereas PC-3 MVs carried increased mRNA levels of several genes including, caveolin-2 (CAV2), glutathione S-transferase pi 1 (GSTP1), pescadillo ribosomal biogenesis factor 1 (PES1), calmodulin regulated spectrin associated protein 1 (CAMSAP1), zinc-finger protein 185 (ZNF185), and others compared to PNT2 MVs. Additionally, ETS variant 1 (ETV1) and fatty acid synthase (FASN) mRNAs identified in LNCaP- and PC-3- derived MVs highly correlated with prostate cancer progression. CONCLUSIONS: Our study provides new understandings of the variability of the mRNA cargo of MVs and EXOs from different cell lines despite same cancer origin, which is essential to better understand the the proportion of the cell transcriptome that can be detected within EVs and to evaluate their role in disease diagnosis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12885-017-3087-x) contains supplementary material, which is available to authorized users. BioMed Central 2017-02-01 /pmc/articles/PMC5286827/ /pubmed/28143451 http://dx.doi.org/10.1186/s12885-017-3087-x Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Lázaro-Ibáñez, Elisa
Lunavat, Taral R.
Jang, Su Chul
Escobedo-Lucea, Carmen
Oliver-De La Cruz, Jorge
Siljander, Pia
Lötvall, Jan
Yliperttula, Marjo
Distinct prostate cancer-related mRNA cargo in extracellular vesicle subsets from prostate cell lines
title Distinct prostate cancer-related mRNA cargo in extracellular vesicle subsets from prostate cell lines
title_full Distinct prostate cancer-related mRNA cargo in extracellular vesicle subsets from prostate cell lines
title_fullStr Distinct prostate cancer-related mRNA cargo in extracellular vesicle subsets from prostate cell lines
title_full_unstemmed Distinct prostate cancer-related mRNA cargo in extracellular vesicle subsets from prostate cell lines
title_short Distinct prostate cancer-related mRNA cargo in extracellular vesicle subsets from prostate cell lines
title_sort distinct prostate cancer-related mrna cargo in extracellular vesicle subsets from prostate cell lines
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5286827/
https://www.ncbi.nlm.nih.gov/pubmed/28143451
http://dx.doi.org/10.1186/s12885-017-3087-x
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