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Metagenomic and metatranscriptomic analysis of human prostate microbiota from patients with prostate cancer

BACKGROUND: Prostate cancer (PCa) is the most common malignant neoplasm among men in many countries. Since most precancerous and cancerous tissues show signs of inflammation, chronic bacterial prostatitis has been hypothesized to be a possible etiology. However, establishing a causal relationship be...

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Autores principales: Feng, Ye, Ramnarine, Varune Rohan, Bell, Robert, Volik, Stanislav, Davicioni, Elai, Hayes, Vanessa M., Ren, Shancheng, Collins, Colin C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6379980/
https://www.ncbi.nlm.nih.gov/pubmed/30777011
http://dx.doi.org/10.1186/s12864-019-5457-z
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author Feng, Ye
Ramnarine, Varune Rohan
Bell, Robert
Volik, Stanislav
Davicioni, Elai
Hayes, Vanessa M.
Ren, Shancheng
Collins, Colin C.
author_facet Feng, Ye
Ramnarine, Varune Rohan
Bell, Robert
Volik, Stanislav
Davicioni, Elai
Hayes, Vanessa M.
Ren, Shancheng
Collins, Colin C.
author_sort Feng, Ye
collection PubMed
description BACKGROUND: Prostate cancer (PCa) is the most common malignant neoplasm among men in many countries. Since most precancerous and cancerous tissues show signs of inflammation, chronic bacterial prostatitis has been hypothesized to be a possible etiology. However, establishing a causal relationship between microbial inflammation and PCa requires a comprehensive analysis of the prostate microbiome. The aim of this study was to characterize the microbiome in prostate tissue of PCa patients and investigate its association with tumour clinical characteristics as well as host expression profiles. RESULTS: The metagenome and metatranscriptome of tumour and the adjacent benign tissues were assessed in 65 Chinese radical prostatectomy specimens. Escherichia, Propionibacterium, Acinetobacter and Pseudomonas were abundant in both metagenome and metatranscriptome, thus constituting the core of the prostate microbiome. The biodiversity of the microbiomes could not be differentiated between the matched tumour/benign specimens or between the tumour specimens of low and high Gleason Scores. The expression profile of ten Pseudomonas genes was strongly correlated with that of eight host small RNA genes; three of the RNA genes may negatively associate with metastasis. Few viruses could be identified from the prostate microbiomes. CONCLUSIONS: This is the first study of the human prostate microbiome employing an integrated metagenomics and metatranscriptomics approach. In this Chinese cohort, both metagenome and metatranscriptome analyses showed a non-sterile microenvironment in the prostate of PCa patients, but we did not find links between the microbiome and local progression of PCa. However, the correlated expression of Pseudomonas genes and human small RNA genes may provide tantalizing preliminary evidence that Pseudomonas infection may impede metastasis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5457-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-63799802019-02-28 Metagenomic and metatranscriptomic analysis of human prostate microbiota from patients with prostate cancer Feng, Ye Ramnarine, Varune Rohan Bell, Robert Volik, Stanislav Davicioni, Elai Hayes, Vanessa M. Ren, Shancheng Collins, Colin C. BMC Genomics Research Article BACKGROUND: Prostate cancer (PCa) is the most common malignant neoplasm among men in many countries. Since most precancerous and cancerous tissues show signs of inflammation, chronic bacterial prostatitis has been hypothesized to be a possible etiology. However, establishing a causal relationship between microbial inflammation and PCa requires a comprehensive analysis of the prostate microbiome. The aim of this study was to characterize the microbiome in prostate tissue of PCa patients and investigate its association with tumour clinical characteristics as well as host expression profiles. RESULTS: The metagenome and metatranscriptome of tumour and the adjacent benign tissues were assessed in 65 Chinese radical prostatectomy specimens. Escherichia, Propionibacterium, Acinetobacter and Pseudomonas were abundant in both metagenome and metatranscriptome, thus constituting the core of the prostate microbiome. The biodiversity of the microbiomes could not be differentiated between the matched tumour/benign specimens or between the tumour specimens of low and high Gleason Scores. The expression profile of ten Pseudomonas genes was strongly correlated with that of eight host small RNA genes; three of the RNA genes may negatively associate with metastasis. Few viruses could be identified from the prostate microbiomes. CONCLUSIONS: This is the first study of the human prostate microbiome employing an integrated metagenomics and metatranscriptomics approach. In this Chinese cohort, both metagenome and metatranscriptome analyses showed a non-sterile microenvironment in the prostate of PCa patients, but we did not find links between the microbiome and local progression of PCa. However, the correlated expression of Pseudomonas genes and human small RNA genes may provide tantalizing preliminary evidence that Pseudomonas infection may impede metastasis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5457-z) contains supplementary material, which is available to authorized users. BioMed Central 2019-02-18 /pmc/articles/PMC6379980/ /pubmed/30777011 http://dx.doi.org/10.1186/s12864-019-5457-z Text en © The Author(s). 2019 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
Feng, Ye
Ramnarine, Varune Rohan
Bell, Robert
Volik, Stanislav
Davicioni, Elai
Hayes, Vanessa M.
Ren, Shancheng
Collins, Colin C.
Metagenomic and metatranscriptomic analysis of human prostate microbiota from patients with prostate cancer
title Metagenomic and metatranscriptomic analysis of human prostate microbiota from patients with prostate cancer
title_full Metagenomic and metatranscriptomic analysis of human prostate microbiota from patients with prostate cancer
title_fullStr Metagenomic and metatranscriptomic analysis of human prostate microbiota from patients with prostate cancer
title_full_unstemmed Metagenomic and metatranscriptomic analysis of human prostate microbiota from patients with prostate cancer
title_short Metagenomic and metatranscriptomic analysis of human prostate microbiota from patients with prostate cancer
title_sort metagenomic and metatranscriptomic analysis of human prostate microbiota from patients with prostate cancer
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6379980/
https://www.ncbi.nlm.nih.gov/pubmed/30777011
http://dx.doi.org/10.1186/s12864-019-5457-z
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