Deep sequencing reveals abundant noncanonical retroviral microRNAs in B-cell leukemia/lymphoma
Viral tumor models have significantly contributed to our understanding of oncogenic mechanisms. How transforming delta-retroviruses induce malignancy, however, remains poorly understood, especially as viral mRNA/protein are tightly silenced in tumors. Here, using deep sequencing of broad windows of...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 110; no. 6; pp. 2306 - 2311 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
05.02.2013
National Acad Sciences |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Viral tumor models have significantly contributed to our understanding of oncogenic mechanisms. How transforming delta-retroviruses induce malignancy, however, remains poorly understood, especially as viral mRNA/protein are tightly silenced in tumors. Here, using deep sequencing of broad windows of small RNA sizes in the bovine leukemia virus ovine model of leukemia/lymphoma, we provide in vivo evidence of the production of noncanonical RNA polymerase III (Pol III)-transcribed viral microRNAs in leukemic B cells in the complete absence of Pol II 5′-LTR–driven transcriptional activity. Processed from a cluster of five independent self-sufficient transcriptional units located in a proviral region dispensable for in vivo infectivity, bovine leukemia virus microRNAs represent ∼40% of all microRNAs in both experimental and natural malignancy. They are subject to strong purifying selection and associate with Argonautes, consistent with a critical function in silencing of important cellular and/or viral targets. Bovine leukemia virus microRNAs are strongly expressed in preleukemic and malignant cells in which structural and regulatory gene expression is repressed, suggesting a key role in tumor onset and progression. Understanding how Pol III-dependent microRNAs subvert cellular and viral pathways will contribute to deciphering the intricate perturbations that underlie malignant transformation. |
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| AbstractList | Viral tumor models have significantly contributed to our understanding of oncogenic mechanisms. How transforming delta-retroviruses induce malignancy, however, remains poorly understood, especially as viral mRNA/protein are tightly silenced in tumors. Here, using deep sequencing of broad windows of small RNA sizes in the bovine leukemia virus ovine model of leukemia/lymphoma, we provide in vivo evidence of the production of noncanonical RNA polymerase III (Pol III)-transcribed viral microRNAs in leukemic B cells in the complete absence of Pol II 5'-LTR-driven transcriptional activity. Processed from a cluster of five independent self-sufficient transcriptional units located in a proviral region dispensable for in vivo infectivity, bovine leukemia virus microRNAs represent ∼40% of all microRNAs in both experimental and natural malignancy. They are subject to strong purifying selection and associate with Argonautes, consistent with a critical function in silencing of important cellular and/or viral targets. Bovine leukemia virus microRNAs are strongly expressed in preleukemic and malignant cells in which structural and regulatory gene expression is repressed, suggesting a key role in tumor onset and progression. Understanding how Pol III-dependent microRNAs subvert cellular and viral pathways will contribute to deciphering the intricate perturbations that underlie malignant transformation.Viral tumor models have significantly contributed to our understanding of oncogenic mechanisms. How transforming delta-retroviruses induce malignancy, however, remains poorly understood, especially as viral mRNA/protein are tightly silenced in tumors. Here, using deep sequencing of broad windows of small RNA sizes in the bovine leukemia virus ovine model of leukemia/lymphoma, we provide in vivo evidence of the production of noncanonical RNA polymerase III (Pol III)-transcribed viral microRNAs in leukemic B cells in the complete absence of Pol II 5'-LTR-driven transcriptional activity. Processed from a cluster of five independent self-sufficient transcriptional units located in a proviral region dispensable for in vivo infectivity, bovine leukemia virus microRNAs represent ∼40% of all microRNAs in both experimental and natural malignancy. They are subject to strong purifying selection and associate with Argonautes, consistent with a critical function in silencing of important cellular and/or viral targets. Bovine leukemia virus microRNAs are strongly expressed in preleukemic and malignant cells in which structural and regulatory gene expression is repressed, suggesting a key role in tumor onset and progression. Understanding how Pol III-dependent microRNAs subvert cellular and viral pathways will contribute to deciphering the intricate perturbations that underlie malignant transformation. Viral tumor models have significantly contributed to our understanding of oncogenic mechanisms. How transforming delta-retroviruses induce malignancy, however, remains poorly understood, especially as viral mRNA/protein are tightly silenced in tumors. Here, using deep sequencing of broad windows of small RNA sizes in the bovine leukemia virus ovine model of leukemia/lymphoma, we provide in vivo evidence of the production of noncanonical RNA polymerase III (Pol III)-transcribed viral microRNAs in leukemic B cells in the complete absence of Pol II 5'-LTR-driven transcriptional activity. Processed from a cluster of five independent self-sufficient transcriptional units located in a proviral region dispensable for in vivo infectivity, bovine leukemia virus microRNAs represent ~40% of all microRNAs in both experimental and natural malignancy. They are subject to strong purifying selection and associate with Argonautes, consistent with a critical function in silencing of important cellular and/or viral targets. Bovine leukemia virus microRNAs are strongly expressed in preleukemic and malignant cells in which structural and regulatory gene expression is repressed, suggesting a key role in tumor onset and progression. Understanding how Pol III-dependent microRNAs subvert cellular and viral pathways will contribute to deciphering the intricate perturbations that underlie malignant transformation. [PUBLICATION ABSTRACT] Viral tumor models have significantly contributed to our understanding of oncogenic mechanisms. How transforming delta-retroviruses induce malignancy, however, remains poorly understood, especially as viral mRNA/protein are tightly silenced in tumors. Here, using deep sequencing of broad windows of small RNA sizes in the bovine leukemia virus ovine model of leukemia/lymphoma, we provide in vivo evidence of the production of noncanonical RNA polymerase III (Pol III)-transcribed viral microRNAs in leukemic B cells in the complete absence of Pol II 5′-LTR–driven transcriptional activity. Processed from a cluster of five independent self-sufficient transcriptional units located in a proviral region dispensable for in vivo infectivity, bovine leukemia virus microRNAs represent ∼40% of all microRNAs in both experimental and natural malignancy. They are subject to strong purifying selection and associate with Argonautes, consistent with a critical function in silencing of important cellular and/or viral targets. Bovine leukemia virus microRNAs are strongly expressed in preleukemic and malignant cells in which structural and regulatory gene expression is repressed, suggesting a key role in tumor onset and progression. Understanding how Pol III-dependent microRNAs subvert cellular and viral pathways will contribute to deciphering the intricate perturbations that underlie malignant transformation. Viral tumor models have significantly contributed to our understanding of oncogenic mechanisms. How transforming delta-retroviruses induce malignancy, however, remains poorly understood, especially as viral mRNA/protein are tightly silenced in tumors. Here, using deep sequencing of broad windows of small RNA sizes in the bovine leukemia virus ovine model of leukemia/lymphoma, we provide in vivo evidence of the production of noncanonical RNA polymerase III (Pol lll)-transcribed viral microRNAs in leukemic B cells in the complete absence of Pol II 5'-LTR-driven transcriptional activity. Processed from a cluster of five independent self-sufficient transcriptional units located in a proviral region dispensable for in vivo infectivity, bovine leukemia virus microRNAs represent ~40% of all microRNAs in both experimental and natural malignancy. They are subject to strong purifying selection and associate with Argonautes, consistent with a critical function in silencing of important cellular and/or viral targets. Bovine leukemia virus microRNAs are strongly expressed in preleukemic and malignant cells in which structural and regulatory gene expression is repressed, suggesting a key role in tumor onset and progression. Understanding how Pol III-dependent microRNAs subvert cellular and viral pathways will contribute to deciphering the intricate perturbations that underlie malignant transformation. |
| Author | Burny, Arsène Takeda, Haruko Cleuter, Yvette Durkin, Keith Georges, Michel Momont, Mélanie Mortreux, Franck Caiment, Florian Wattel, Eric Rosewick, Nicolas Vernin, Céline Van den Broeke, Anne |
| Author_xml | – sequence: 1 givenname: Nicolas surname: Rosewick fullname: Rosewick, Nicolas – sequence: 2 givenname: Mélanie surname: Momont fullname: Momont, Mélanie – sequence: 3 givenname: Keith surname: Durkin fullname: Durkin, Keith – sequence: 4 givenname: Haruko surname: Takeda fullname: Takeda, Haruko – sequence: 5 givenname: Florian surname: Caiment fullname: Caiment, Florian – sequence: 6 givenname: Yvette surname: Cleuter fullname: Cleuter, Yvette – sequence: 7 givenname: Céline surname: Vernin fullname: Vernin, Céline – sequence: 8 givenname: Franck surname: Mortreux fullname: Mortreux, Franck – sequence: 9 givenname: Eric surname: Wattel fullname: Wattel, Eric – sequence: 10 givenname: Arsène surname: Burny fullname: Burny, Arsène – sequence: 11 givenname: Michel surname: Georges fullname: Georges, Michel – sequence: 12 givenname: Anne surname: Van den Broeke fullname: Van den Broeke, Anne |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23345446$$D View this record in MEDLINE/PubMed |
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| Copyright | copyright © 1993-2008 National Academy of Sciences of the United States of America Copyright National Academy of Sciences Feb 5, 2013 |
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| Notes | http://dx.doi.org/10.1073/pnas.1213842110 SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 1Present address: Department of Toxicogenomics, Maastricht University, 6200 MD Maastricht, The Netherlands. Author contributions: M.G. and A.V.d.B. designed research; N.R., M.M., K.D., H.T., F.C., Y.C., and C.V. performed research; N.R., F.M., E.W., M.G., and A.V.d.B. analyzed data; and N.R., F.M., A.B., M.G., and A.V.d.B. wrote the paper. Edited* by Robert C. Gallo, Institute of Human Virology, University of Maryland School of Medicine, Baltimore, MD, and approved December 14, 2012 (received for review August 21, 2012) |
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| Snippet | Viral tumor models have significantly contributed to our understanding of oncogenic mechanisms. How transforming delta-retroviruses induce malignancy, however,... |
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| SubjectTerms | animal models Animals Argonaute Proteins - metabolism B lymphocytes Base Sequence Biological Sciences Bovine leukemia virus Cattle Cell Line, Tumor Cells Disease Models, Animal DNA-directed RNA polymerase Enzootic Bovine Leukosis - genetics Enzootic Bovine Leukosis - virology Gene Expression High Mobility Group Proteins - genetics High throughput nucleotide sequencing Human T-lymphotropic virus 1 - genetics Humans Leukemia Leukemia Virus, Bovine - genetics Leukemia, B-Cell - genetics Leukemia, B-Cell - veterinary Leukemia, B-Cell - virology Leukemia-Lymphoma, Adult T-Cell - genetics Leukemia-Lymphoma, Adult T-Cell - virology Lymphoma Lymphoma, B-Cell - genetics Lymphoma, B-Cell - veterinary Lymphoma, B-Cell - virology Messenger RNA MicroRNA MicroRNAs - chemistry MicroRNAs - genetics MicroRNAs - metabolism Molecular Sequence Data Nucleic Acid Conformation pathogenicity Proviruses regulator genes Ribonucleic acid RNA RNA polymerase RNA Polymerase III - metabolism RNA, Neoplasm - genetics RNA, Neoplasm - metabolism RNA, Viral - chemistry RNA, Viral - genetics RNA, Viral - metabolism Sequence Analysis, RNA Sequence Homology, Nucleic Acid Sheep Sheep Diseases - genetics Sheep Diseases - virology Terminal Repeat Sequences transcription (genetics) Tumors Viruses |
| Title | Deep sequencing reveals abundant noncanonical retroviral microRNAs in B-cell leukemia/lymphoma |
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