The BRAF Pseudogene Functions as a Competitive Endogenous RNA and Induces Lymphoma In Vivo
Research over the past decade has suggested important roles for pseudogenes in physiology and disease. In vitro experiments demonstrated that pseudogenes contribute to cell transformation through several mechanisms. However, in vivo evidence for a causal role of pseudogenes in cancer development is...
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Published in | Cell Vol. 161; no. 2; pp. 319 - 332 |
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Main Authors | , , , , , , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Elsevier Inc
09.04.2015
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Subjects | |
Online Access | Get full text |
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Abstract | Research over the past decade has suggested important roles for pseudogenes in physiology and disease. In vitro experiments demonstrated that pseudogenes contribute to cell transformation through several mechanisms. However, in vivo evidence for a causal role of pseudogenes in cancer development is lacking. Here, we report that mice engineered to overexpress either the full-length murine B-Raf pseudogene Braf-rs1 or its pseudo “CDS” or “3′ UTR” develop an aggressive malignancy resembling human diffuse large B cell lymphoma. We show that Braf-rs1 and its human ortholog, BRAFP1, elicit their oncogenic activity, at least in part, as competitive endogenous RNAs (ceRNAs) that elevate BRAF expression and MAPK activation in vitro and in vivo. Notably, we find that transcriptional or genomic aberrations of BRAFP1 occur frequently in multiple human cancers, including B cell lymphomas. Our engineered mouse models demonstrate the oncogenic potential of pseudogenes and indicate that ceRNA-mediated microRNA sequestration may contribute to the development of cancer.
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•The BRAF pseudogene functions as a ceRNA for BRAF in humans and mice•Braf-rs1 overexpression promotes B cell lymphoma in mice•Silencing of BRAFP1 affects MAPK signaling and proliferation of human cancer cells•Genomic gains and aberrant expression of BRAFP1 are found in various human cancers
The in vivo evidence for the regulatory activity of pseudogenes has been lacking, and their role in disease progression has been correlative. This study now shows that transgenic expression of the BRAF pseudogene induces a malignancy in mice resembling human diffuse large B cell lymphoma, establishing its oncogenic function. |
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AbstractList | Research over the past decade has suggested important roles for pseudogenes in physiology and disease. In vitro experiments demonstrated that pseudogenes contribute to cell transformation through several mechanisms. However, in vivo evidence for a causal role of pseudogenes in cancer development is lacking. Here, we report that mice engineered to overexpress either the full-length murine B-Raf pseudogene Braf-rs1 or its pseudo "CDS" or "3' UTR" develop an aggressive malignancy resembling human diffuse large B cell lymphoma. We show that Braf-rs1 and its human ortholog, BRAFP1, elicit their oncogenic activity, at least in part, as competitive endogenous RNAs (ceRNAs) that elevate BRAF expression and MAPK activation in vitro and in vivo. Notably, we find that transcriptional or genomic aberrations of BRAFP1 occur frequently in multiple human cancers, including B cell lymphomas. Our engineered mouse models demonstrate the oncogenic potential of pseudogenes and indicate that ceRNA-mediated microRNA sequestration may contribute to the development of cancer. Research over the past decade has suggested important roles for pseudogenes in physiology and disease. In vitro experiments demonstrated that pseudogenes contribute to cell transformation through several mechanisms. However, in vivo evidence for a causal role of pseudogenes in cancer development is lacking. Here, we report that mice engineered to overexpress either the full-length murine B-Raf pseudogene Braf-rs1 or its pseudo “CDS” or “3′ UTR” develop an aggressive malignancy resembling human diffuse large B cell lymphoma. We show that Braf-rs1 and its human ortholog, BRAFP1, elicit their oncogenic activity, at least in part, as competitive endogenous RNAs (ceRNAs) that elevate BRAF expression and MAPK activation in vitro and in vivo. Notably, we find that transcriptional or genomic aberrations of BRAFP1 occur frequently in multiple human cancers, including B cell lymphomas. Our engineered mouse models demonstrate the oncogenic potential of pseudogenes and indicate that ceRNA-mediated microRNA sequestration may contribute to the development of cancer. [Display omitted] •The BRAF pseudogene functions as a ceRNA for BRAF in humans and mice•Braf-rs1 overexpression promotes B cell lymphoma in mice•Silencing of BRAFP1 affects MAPK signaling and proliferation of human cancer cells•Genomic gains and aberrant expression of BRAFP1 are found in various human cancers The in vivo evidence for the regulatory activity of pseudogenes has been lacking, and their role in disease progression has been correlative. This study now shows that transgenic expression of the BRAF pseudogene induces a malignancy in mice resembling human diffuse large B cell lymphoma, establishing its oncogenic function. Research over the past decade has suggested important roles for pseudogenes in physiology and disease. In vitro experiments demonstrated that pseudogenes contribute to cell transformation through several mechanisms. However, in vivo evidence for a causal role of pseudogenes in cancer development is lacking. Here we report that mice engineered to overexpress either the full-length murine B-Raf pseudogene, Braf-rs1 , or its pseudo “CDS” or “3’UTR” develop an aggressive malignancy resembling human diffuse large B-cell lymphoma. We show that Braf-rs1 and its human ortholog, BRAFP1 , elicit their oncogenic activity, at least in part, as competitive endogenous RNAs (ceRNAs) that elevate BRAF expression and MAPK activation in vitro and in vivo . Notably, we find that transcriptional or genomic aberrations of BRAFP1 occur frequently in multiple human cancers including B-cell lymphomas. Our engineered mouse models demonstrate the oncogenic potential of pseudogenes, and indicate that ceRNA-mediated microRNA sequestration may contribute to the development of cancer. |
Author | Reschke, Markus Shipp, Margaret A. Adams, David J. Rodig, Scott J. Sjoberg, Marcela Wu, David Velasco-Herrera, Martin Del Castillo Ruocco, Anna Bothmer, Anne Keane, Thomas M. Ng, Christopher Chiarle, Roberto Léopold, Valentine Seitzer, Nina Chapuy, Bjoern Elemento, Olivier Verma, Akanksha Fung, Jacqueline Tay, Yvonne Pandolfi, Pier Paolo Ala, Ugo Langellotto, Fernanda Karreth, Florian A. |
AuthorAffiliation | 3 Experimental Cancer Genetics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, CB10 1HH, UK 7 Department of Pathology, Brigham and Women’s Hospital, Boston, MA 02115, USA 1 Cancer Research Institute, Beth Israel Deaconess Cancer Center, Department of Medicine and Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA 6 Department of Pathology, Children’s Hospital and Harvard Medical School, Boston, MA 02115, USA 5 Meyer Cancer Center, Weill Cornell Medical College, New York, NY 10021 8 Department of Molecular Biotechnology and Health Sciences, University of Torino, Torino, Italy 4 Department of Physiology and Biophysics, Institute for Computational Biomedicine, Weill Cornell Medical College, New York, NY 10021 2 Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02115, USA |
AuthorAffiliation_xml | – name: 4 Department of Physiology and Biophysics, Institute for Computational Biomedicine, Weill Cornell Medical College, New York, NY 10021 – name: 3 Experimental Cancer Genetics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, CB10 1HH, UK – name: 5 Meyer Cancer Center, Weill Cornell Medical College, New York, NY 10021 – name: 7 Department of Pathology, Brigham and Women’s Hospital, Boston, MA 02115, USA – name: 2 Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02115, USA – name: 1 Cancer Research Institute, Beth Israel Deaconess Cancer Center, Department of Medicine and Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA – name: 8 Department of Molecular Biotechnology and Health Sciences, University of Torino, Torino, Italy – name: 6 Department of Pathology, Children’s Hospital and Harvard Medical School, Boston, MA 02115, USA |
Author_xml | – sequence: 1 givenname: Florian A. surname: Karreth fullname: Karreth, Florian A. organization: Cancer Research Institute, Beth Israel Deaconess Cancer Center, Department of Medicine and Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA – sequence: 2 givenname: Markus surname: Reschke fullname: Reschke, Markus organization: Cancer Research Institute, Beth Israel Deaconess Cancer Center, Department of Medicine and Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA – sequence: 3 givenname: Anna surname: Ruocco fullname: Ruocco, Anna organization: Cancer Research Institute, Beth Israel Deaconess Cancer Center, Department of Medicine and Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA – sequence: 4 givenname: Christopher surname: Ng fullname: Ng, Christopher organization: Cancer Research Institute, Beth Israel Deaconess Cancer Center, Department of Medicine and Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA – sequence: 5 givenname: Bjoern surname: Chapuy fullname: Chapuy, Bjoern organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02115, USA – sequence: 6 givenname: Valentine surname: Léopold fullname: Léopold, Valentine organization: Cancer Research Institute, Beth Israel Deaconess Cancer Center, Department of Medicine and Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA – sequence: 7 givenname: Marcela surname: Sjoberg fullname: Sjoberg, Marcela organization: Experimental Cancer Genetics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton CB10 1HH, UK – sequence: 8 givenname: Thomas M. surname: Keane fullname: Keane, Thomas M. organization: Experimental Cancer Genetics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton CB10 1HH, UK – sequence: 9 givenname: Akanksha surname: Verma fullname: Verma, Akanksha organization: Department of Physiology and Biophysics, Institute for Computational Biomedicine, Weill Cornell Medical College, New York, NY 10021, USA – sequence: 10 givenname: Ugo surname: Ala fullname: Ala, Ugo organization: Cancer Research Institute, Beth Israel Deaconess Cancer Center, Department of Medicine and Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA – sequence: 11 givenname: Yvonne surname: Tay fullname: Tay, Yvonne organization: Cancer Research Institute, Beth Israel Deaconess Cancer Center, Department of Medicine and Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA – sequence: 12 givenname: David surname: Wu fullname: Wu, David organization: Meyer Cancer Center, Weill Cornell Medical College, New York, NY 10021, USA – sequence: 13 givenname: Nina surname: Seitzer fullname: Seitzer, Nina organization: Cancer Research Institute, Beth Israel Deaconess Cancer Center, Department of Medicine and Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA – sequence: 14 givenname: Martin Del Castillo surname: Velasco-Herrera fullname: Velasco-Herrera, Martin Del Castillo organization: Experimental Cancer Genetics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton CB10 1HH, UK – sequence: 15 givenname: Anne surname: Bothmer fullname: Bothmer, Anne organization: Cancer Research Institute, Beth Israel Deaconess Cancer Center, Department of Medicine and Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA – sequence: 16 givenname: Jacqueline surname: Fung fullname: Fung, Jacqueline organization: Cancer Research Institute, Beth Israel Deaconess Cancer Center, Department of Medicine and Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA – sequence: 17 givenname: Fernanda surname: Langellotto fullname: Langellotto, Fernanda organization: Department of Pathology, Children’s Hospital and Harvard Medical School, Boston, MA 02115, USA – sequence: 18 givenname: Scott J. surname: Rodig fullname: Rodig, Scott J. organization: Department of Pathology, Brigham and Women’s Hospital, Boston, MA 02115, USA – sequence: 19 givenname: Olivier surname: Elemento fullname: Elemento, Olivier organization: Department of Physiology and Biophysics, Institute for Computational Biomedicine, Weill Cornell Medical College, New York, NY 10021, USA – sequence: 20 givenname: Margaret A. surname: Shipp fullname: Shipp, Margaret A. organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02115, USA – sequence: 21 givenname: David J. surname: Adams fullname: Adams, David J. organization: Experimental Cancer Genetics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton CB10 1HH, UK – sequence: 22 givenname: Roberto surname: Chiarle fullname: Chiarle, Roberto organization: Department of Pathology, Children’s Hospital and Harvard Medical School, Boston, MA 02115, USA – sequence: 23 givenname: Pier Paolo surname: Pandolfi fullname: Pandolfi, Pier Paolo email: ppandolf@bidmc.harvard.edu organization: Cancer Research Institute, Beth Israel Deaconess Cancer Center, Department of Medicine and Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25843629$$D View this record in MEDLINE/PubMed |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Author Contribution F.A.K. and P.P.P conceived and designed the study. F.A.K., M.R., A.R., Y.T., D.W., N.S. and A.B., performed experiments, and F.A.K., M.R. and P.P.P analyzed most data. C.N., J.F. and F.L. carried out immunohistochemistry. U.A. performed miRNA predictions. R.C. and S.J.R. evaluated histopathology of tumors and advised on immunohistochemical validation. M.S., T.M.K., M.D.C.VH. and D.J.A. performed RNAseq analysis. B.C. and M.A.S. provided human samples and cell lines. A.V. and O.E. analyzed BRAFP1 expression in human RNAseq data. F.A.K. and P.P.P. wrote the manuscript with contributions from all authors. |
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Snippet | Research over the past decade has suggested important roles for pseudogenes in physiology and disease. In vitro experiments demonstrated that pseudogenes... Research over the past decade has suggested important roles for pseudogenes in physiology and disease. In vitro experiments demonstrated that pseudogenes... Research over the past decade has suggested important roles for pseudogenes in physiology and disease. In vitro experiments demonstrated that pseudogenes... |
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SubjectTerms | Animals Base Sequence Humans Lymphoma, Large B-Cell, Diffuse - genetics Lymphoma, Large B-Cell, Diffuse - metabolism Mice Molecular Sequence Data Proto-Oncogene Proteins B-raf - genetics Proto-Oncogene Proteins B-raf - metabolism Pseudogenes RNA - metabolism |
Title | The BRAF Pseudogene Functions as a Competitive Endogenous RNA and Induces Lymphoma In Vivo |
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