Intragenic antagonistic roles of protein and circRNA in tumorigenesis

Jlenia Guarnerio; Yang Zhang; Giulia Cheloni; Riccardo Panella; Jesse Mae Katon; Mark Simpson; Akinobu Matsumoto; Antonella Papa; Cristian Loretelli; Andreas Petri; Sakari Kauppinen; Cassandra Garbutt; Gunnlaugur Petur Nielsen; Vikram Deshpande; Mireia Castillo-Martin; Carlos Cordon-Cardo; Spentzos Dimitrios; John G Clohessy; Mona Batish; Pier Paolo Pandolfi

doi:10.1038/s41422-019-0192-1

Intragenic antagonistic roles of protein and circRNA in tumorigenesis

Jlenia Guarnerio, Yang Zhang, Giulia Cheloni, Riccardo Panella, Jesse Mae Katon, Mark Simpson, Akinobu Matsumoto, Antonella Papa, Cristian Loretelli, Andreas Petri, Sakari Kauppinen, Cassandra Garbutt, Gunnlaugur Petur Nielsen, Vikram Deshpande, Mireia Castillo-Martin, Carlos Cordon-Cardo, Spentzos Dimitrios, John G Clohessy, Mona Batish, Pier Paolo Pandolfi

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

106 Citationer (Scopus)

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.

Originalsprog	Engelsk
Tidsskrift	Cell Research
Vol/bind	29
Udgave nummer	8
Sider (fra-til)	628-640
Antal sider	13
ISSN	1001-0602
DOI	https://doi.org/10.1038/s41422-019-0192-1
Status	Udgivet - 1 aug. 2019

Bibliografisk note

Korrektion til artiklen:
Guarnerio, J., Zhang, Y., Cheloni, G. et al. Author Correction: Intragenic antagonistic roles of protein and circRNA in tumorigenesis. Cell Res 30, 188 (2020). https://doi.org/10.1038/s41422-019-0262-4

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https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6796857/pdf/41422_2019_Article_192.pdf

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Citationsformater

Guarnerio, J., Zhang, Y., Cheloni, G., Panella, R., Mae Katon, J., Simpson, M., Matsumoto, A., Papa, A., Loretelli, C., Petri, A., Kauppinen, S., Garbutt, C., Petur Nielsen, G., Deshpande, V., Castillo-Martin, M., Cordon-Cardo, C., Dimitrios, S., Clohessy, J. G., Batish, M., & Pandolfi, P. P. (2019). Intragenic antagonistic roles of protein and circRNA in tumorigenesis. Cell Research, 29(8), 628-640. https://doi.org/10.1038/s41422-019-0192-1

@article{3c8db78fd30e40ed853d850a019956c3,

title = "Intragenic antagonistic roles of protein and circRNA in tumorigenesis",

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.",

author = "Jlenia Guarnerio and Yang Zhang and Giulia Cheloni and Riccardo Panella and {Mae Katon}, Jesse and Mark Simpson and Akinobu Matsumoto and Antonella Papa and Cristian Loretelli and Andreas Petri and Sakari Kauppinen and Cassandra Garbutt and {Petur Nielsen}, Gunnlaugur and Vikram Deshpande and Mireia Castillo-Martin and Carlos Cordon-Cardo and Spentzos Dimitrios and Clohessy, {John G} and Mona Batish and Pandolfi, {Pier Paolo}",

note = "Correction to this article: Guarnerio, J., Zhang, Y., Cheloni, G. et al. Author Correction: Intragenic antagonistic roles of protein and circRNA in tumorigenesis. Cell Res 30, 188 (2020). https://doi.org/10.1038/s41422-019-0262-4",

year = "2019",

month = aug,

day = "1",

doi = "10.1038/s41422-019-0192-1",

language = "English",

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journal = "Cell Research",

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Guarnerio, J, Zhang, Y, Cheloni, G, Panella, R, Mae Katon, J, Simpson, M, Matsumoto, A, Papa, A, Loretelli, C, Petri, A , Kauppinen, S, Garbutt, C, Petur Nielsen, G, Deshpande, V, Castillo-Martin, M, Cordon-Cardo, C, Dimitrios, S, Clohessy, JG, Batish, M & Pandolfi, PP 2019, 'Intragenic antagonistic roles of protein and circRNA in tumorigenesis', Cell Research, bind 29, nr. 8, s. 628-640. https://doi.org/10.1038/s41422-019-0192-1

TY - JOUR

T1 - Intragenic antagonistic roles of protein and circRNA in tumorigenesis

AU - Guarnerio, Jlenia

AU - Zhang, Yang

AU - Cheloni, Giulia

AU - Panella, Riccardo

AU - Mae Katon, Jesse

AU - Simpson, Mark

AU - Matsumoto, Akinobu

AU - Papa, Antonella

AU - Loretelli, Cristian

AU - Petri, Andreas

AU - Kauppinen, Sakari

AU - Garbutt, Cassandra

AU - Petur Nielsen, Gunnlaugur

AU - Deshpande, Vikram

AU - Castillo-Martin, Mireia

AU - Cordon-Cardo, Carlos

AU - Dimitrios, Spentzos

AU - Clohessy, John G

AU - Batish, Mona

AU - Pandolfi, Pier Paolo

N1 - Correction to this article: Guarnerio, J., Zhang, Y., Cheloni, G. et al. Author Correction: Intragenic antagonistic roles of protein and circRNA in tumorigenesis. Cell Res 30, 188 (2020). https://doi.org/10.1038/s41422-019-0262-4

PY - 2019/8/1

Y1 - 2019/8/1

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85067884091&partnerID=8YFLogxK

U2 - 10.1038/s41422-019-0192-1

DO - 10.1038/s41422-019-0192-1

M3 - Journal article

C2 - 31209250

SN - 1001-0602

VL - 29

SP - 628

EP - 640

JO - Cell Research

JF - Cell Research

IS - 8

ER -

Intragenic antagonistic roles of protein and circRNA in tumorigenesis

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