Intragenic antagonistic roles of protein and circRNA in tumorigenesis

circRNAs arise from back splicing events during mRNA processing, and when deregulated can play an active role in cancer. Here we characterize a new circRNA (circPOK) encoded by the Zbtb7a gene (also kown as POKEMON , LRF ) in the context of mesenchymal tumor progression. circPOK functions as a non-c...

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Published inCell research Vol. 29; no. 8; pp. 628 - 640
Main Authors Guarnerio, Jlenia, Zhang, Yang, Cheloni, Giulia, Panella, Riccardo, Mae Katon, Jesse, Simpson, Mark, Matsumoto, Akinobu, Papa, Antonella, Loretelli, Cristian, Petri, Andreas, Kauppinen, Sakari, Garbutt, Cassandra, Nielsen, Gunnlaugur Petur, Deshpande, Vikram, Castillo-Martin, Mireia, Cordon-Cardo, Carlos, Dimitrios, Spentzos, Clohessy, John G., Batish, Mona, Pandolfi, Pier Paolo
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.08.2019
Nature Publishing Group
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Online AccessGet full text
ISSN1001-0602
1748-7838
1748-7838
DOI10.1038/s41422-019-0192-1

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Abstract circRNAs arise from back splicing events during mRNA processing, and when deregulated can play an active role in cancer. Here we characterize a new circRNA (circPOK) encoded by the Zbtb7a gene (also kown as POKEMON , LRF ) in the context of mesenchymal tumor progression. circPOK functions as a non-coding proto-oncogenic RNA independently and antithetically to its linear transcript counterpart, which acts as a tumor suppressor by encoding the Pokemon transcription factor. We find that circPOK regulates pro-proliferative and pro-angiogenic factors by co-activation of the ILF2/3 complex. Importantly, the expression of Pokemon protein and circRNA is aberrantly uncoupled in cancer through differential post-transcriptional regulation. Thus, we identify a novel type of genetic unit, the iRegulon, that yields biochemically distinct RNA products, circular and linear, with diverse and antithetical functions. Our findings further expand the cellular repertoire towards the control of normal biological outputs, while aberrant expression of such components may underlie disease pathogenesis including cancer.
AbstractList circRNAs arise from back splicing events during mRNA processing, and when deregulated can play an active role in cancer. Here we characterize a new circRNA (circPOK) encoded by the Zbtb7a gene (also kown as POKEMON , LRF ) in the context of mesenchymal tumor progression. circPOK functions as a non-coding proto-oncogenic RNA independently and antithetically to its linear transcript counterpart, which acts as a tumor suppressor by encoding the Pokemon transcription factor. We find that circPOK regulates pro-proliferative and pro-angiogenic factors by co-activation of the ILF2/3 complex. Importantly, the expression of Pokemon protein and circRNA is aberrantly uncoupled in cancer through differential post-transcriptional regulation. Thus, we identify a novel type of genetic unit, the iRegulon, that yields biochemically distinct RNA products, circular and linear, with diverse and antithetical functions. Our findings further expand the cellular repertoire towards the control of normal biological outputs, while aberrant expression of such components may underlie disease pathogenesis including cancer.
circRNAs arise from back splicing events during mRNA processing, and when deregulated can play an active role in cancer. Here we characterize a new circRNA (circPOK) encoded by the Zbtb7a gene (also kown as POKEMON, LRF) in the context of mesenchymal tumor progression. circPOK functions as a non-coding proto-oncogenic RNA independently and antithetically to its linear transcript counterpart, which acts as a tumor suppressor by encoding the Pokemon transcription factor. We find that circPOK regulates pro-proliferative and pro-angiogenic factors by co-activation of the ILF2/3 complex. Importantly, the expression of Pokemon protein and circRNA is aberrantly uncoupled in cancer through differential post-transcriptional regulation. Thus, we identify a novel type of genetic unit, the iRegulon, that yields biochemically distinct RNA products, circular and linear, with diverse and antithetical functions. Our findings further expand the cellular repertoire towards the control of normal biological outputs, while aberrant expression of such components may underlie disease pathogenesis including cancer.
circRNAs arise from back splicing events during mRNA processing, and when deregulated can play an active role in cancer. Here we characterize a new circRNA (circPOK) encoded by the Zbtb7a gene (also kown as POKEMON, LRF) in the context of mesenchymal tumor progression. circPOK functions as a non-coding proto-oncogenic RNA independently and antithetically to its linear transcript counterpart, which acts as a tumor suppressor by encoding the Pokemon transcription factor. We find that circPOK regulates pro-proliferative and pro-angiogenic factors by co-activation of the ILF2/3 complex. Importantly, the expression of Pokemon protein and circRNA is aberrantly uncoupled in cancer through differential post-transcriptional regulation. Thus, we identify a novel type of genetic unit, the iRegulon, that yields biochemically distinct RNA products, circular and linear, with diverse and antithetical functions. Our findings further expand the cellular repertoire towards the control of normal biological outputs, while aberrant expression of such components may underlie disease pathogenesis including cancer.circRNAs arise from back splicing events during mRNA processing, and when deregulated can play an active role in cancer. Here we characterize a new circRNA (circPOK) encoded by the Zbtb7a gene (also kown as POKEMON, LRF) in the context of mesenchymal tumor progression. circPOK functions as a non-coding proto-oncogenic RNA independently and antithetically to its linear transcript counterpart, which acts as a tumor suppressor by encoding the Pokemon transcription factor. We find that circPOK regulates pro-proliferative and pro-angiogenic factors by co-activation of the ILF2/3 complex. Importantly, the expression of Pokemon protein and circRNA is aberrantly uncoupled in cancer through differential post-transcriptional regulation. Thus, we identify a novel type of genetic unit, the iRegulon, that yields biochemically distinct RNA products, circular and linear, with diverse and antithetical functions. Our findings further expand the cellular repertoire towards the control of normal biological outputs, while aberrant expression of such components may underlie disease pathogenesis including cancer.
Author Deshpande, Vikram
Garbutt, Cassandra
Dimitrios, Spentzos
Loretelli, Cristian
Cordon-Cardo, Carlos
Castillo-Martin, Mireia
Kauppinen, Sakari
Nielsen, Gunnlaugur Petur
Pandolfi, Pier Paolo
Clohessy, John G.
Batish, Mona
Petri, Andreas
Guarnerio, Jlenia
Panella, Riccardo
Zhang, Yang
Mae Katon, Jesse
Cheloni, Giulia
Simpson, Mark
Papa, Antonella
Matsumoto, Akinobu
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  organization: Cancer Research Institute, Beth Israel Deaconess Cancer Center, Departments of Medicine and Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School
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Snippet circRNAs arise from back splicing events during mRNA processing, and when deregulated can play an active role in cancer. Here we characterize a new circRNA...
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SubjectTerms 14/32
38
38/77
631/67/327
631/67/68
64/60
96/31
Alternative Splicing - genetics
Angiogenesis
Animals
Biomedical and Life Sciences
Cancer
Carcinogenesis - genetics
Cell Biology
Cell Line, Tumor
Deregulation
DNA-Binding Proteins - genetics
DNA-Binding Proteins - metabolism
Exons
Gene Expression Regulation, Neoplastic
Gene Knockout Techniques
Gene regulation
HEK293 Cells
Humans
Life Sciences
Mesenchymal Stem Cells - metabolism
Mesenchyme
Mice
Mice, Inbred C57BL
Mice, Knockout
mRNA processing
Non-coding RNA
Pathogenesis
Post-transcription
Proteins
Proto-Oncogenes - genetics
Ribonucleic acid
RNA
RNA, Circular - genetics
RNA, Small Interfering - genetics
Sarcoma - genetics
Sarcoma - pathology
Splicing
Transcription Factors - genetics
Transcription Factors - metabolism
Transfection
Tumor suppressor genes
Tumorigenesis
Tumors
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Title Intragenic antagonistic roles of protein and circRNA in tumorigenesis
URI https://link.springer.com/article/10.1038/s41422-019-0192-1
https://www.ncbi.nlm.nih.gov/pubmed/31209250
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