Quaking Inhibits Doxorubicin-Mediated Cardiotoxicity Through Regulation of Cardiac Circular RNA Expression
RBPs (RNA-binding proteins) have been described to be expressed and regulated in various organs including the heart. Little is known about the role of RBPs in heart failure induced by the chemotherapy drug doxorubicin and their interaction with circular RNAs. We aimed to identify key RBPs involved i...
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| Vydáno v: | Circulation research Ročník 122; číslo 2; s. 246 |
|---|---|
| Hlavní autoři: | , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
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United States
19.01.2018
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| Témata: | |
| ISSN: | 1524-4571, 1524-4571 |
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| Abstract | RBPs (RNA-binding proteins) have been described to be expressed and regulated in various organs including the heart. Little is known about the role of RBPs in heart failure induced by the chemotherapy drug doxorubicin and their interaction with circular RNAs.
We aimed to identify key RBPs involved in doxorubicin-mediated heart failure and to elucidate their function.
Global transcriptome profiling from murine myocardium exposed to doxorubicin identified 5 differentially expressed RBPs. Expression of the RBP QKI (Quaking) in response to doxorubicin was strongly downregulated in rodent cardiomyocytes and human induced pluripotent stem cell-derived cardiomyocytes in vitro and in vivo in mice. Knockdown of
in primary cardiomyocytes increased apoptosis and atrophy after treatment with doxorubicin, whereas lentiviral mediated overexpression of
inhibited the doxorubicin-induced apoptosis in cardiomyocytes. In vivo, AAV9 (adeno-associated virus serotype 9)-mediated cardiac overexpression of
prevented cardiac apoptosis and cardiac atrophy induced by doxorubicin and improved cardiac function. Mechanistically, by lentiviral-based overexpression and CRISPR/Cas9-mediated silencing of
, we identified regulated expression of specific circular RNAs derived from
(Titin),
(Formin homology 2 domain containing 3), and
(Striatin, calmodulin-binding protein 3). Moreover, inhibition of
-derived circular RNA increased the susceptibility of cardiomyocytes to doxorubicin.
We here show that overexpression of
strongly attenuates the toxic effect of doxorubicin via regulating a set of circular RNAs.
is, thus, an interesting target molecule to combat doxorubicin-induced cardiotoxicity. |
|---|---|
| AbstractList | RBPs (RNA-binding proteins) have been described to be expressed and regulated in various organs including the heart. Little is known about the role of RBPs in heart failure induced by the chemotherapy drug doxorubicin and their interaction with circular RNAs.
We aimed to identify key RBPs involved in doxorubicin-mediated heart failure and to elucidate their function.
Global transcriptome profiling from murine myocardium exposed to doxorubicin identified 5 differentially expressed RBPs. Expression of the RBP QKI (Quaking) in response to doxorubicin was strongly downregulated in rodent cardiomyocytes and human induced pluripotent stem cell-derived cardiomyocytes in vitro and in vivo in mice. Knockdown of
in primary cardiomyocytes increased apoptosis and atrophy after treatment with doxorubicin, whereas lentiviral mediated overexpression of
inhibited the doxorubicin-induced apoptosis in cardiomyocytes. In vivo, AAV9 (adeno-associated virus serotype 9)-mediated cardiac overexpression of
prevented cardiac apoptosis and cardiac atrophy induced by doxorubicin and improved cardiac function. Mechanistically, by lentiviral-based overexpression and CRISPR/Cas9-mediated silencing of
, we identified regulated expression of specific circular RNAs derived from
(Titin),
(Formin homology 2 domain containing 3), and
(Striatin, calmodulin-binding protein 3). Moreover, inhibition of
-derived circular RNA increased the susceptibility of cardiomyocytes to doxorubicin.
We here show that overexpression of
strongly attenuates the toxic effect of doxorubicin via regulating a set of circular RNAs.
is, thus, an interesting target molecule to combat doxorubicin-induced cardiotoxicity. RBPs (RNA-binding proteins) have been described to be expressed and regulated in various organs including the heart. Little is known about the role of RBPs in heart failure induced by the chemotherapy drug doxorubicin and their interaction with circular RNAs.RATIONALERBPs (RNA-binding proteins) have been described to be expressed and regulated in various organs including the heart. Little is known about the role of RBPs in heart failure induced by the chemotherapy drug doxorubicin and their interaction with circular RNAs.We aimed to identify key RBPs involved in doxorubicin-mediated heart failure and to elucidate their function.OBJECTIVEWe aimed to identify key RBPs involved in doxorubicin-mediated heart failure and to elucidate their function.Global transcriptome profiling from murine myocardium exposed to doxorubicin identified 5 differentially expressed RBPs. Expression of the RBP QKI (Quaking) in response to doxorubicin was strongly downregulated in rodent cardiomyocytes and human induced pluripotent stem cell-derived cardiomyocytes in vitro and in vivo in mice. Knockdown of Qki in primary cardiomyocytes increased apoptosis and atrophy after treatment with doxorubicin, whereas lentiviral mediated overexpression of Qki5 inhibited the doxorubicin-induced apoptosis in cardiomyocytes. In vivo, AAV9 (adeno-associated virus serotype 9)-mediated cardiac overexpression of Qki5 prevented cardiac apoptosis and cardiac atrophy induced by doxorubicin and improved cardiac function. Mechanistically, by lentiviral-based overexpression and CRISPR/Cas9-mediated silencing of Qki5, we identified regulated expression of specific circular RNAs derived from Ttn (Titin), Fhod3 (Formin homology 2 domain containing 3), and Strn3 (Striatin, calmodulin-binding protein 3). Moreover, inhibition of Ttn-derived circular RNA increased the susceptibility of cardiomyocytes to doxorubicin.METHODS AND RESULTSGlobal transcriptome profiling from murine myocardium exposed to doxorubicin identified 5 differentially expressed RBPs. Expression of the RBP QKI (Quaking) in response to doxorubicin was strongly downregulated in rodent cardiomyocytes and human induced pluripotent stem cell-derived cardiomyocytes in vitro and in vivo in mice. Knockdown of Qki in primary cardiomyocytes increased apoptosis and atrophy after treatment with doxorubicin, whereas lentiviral mediated overexpression of Qki5 inhibited the doxorubicin-induced apoptosis in cardiomyocytes. In vivo, AAV9 (adeno-associated virus serotype 9)-mediated cardiac overexpression of Qki5 prevented cardiac apoptosis and cardiac atrophy induced by doxorubicin and improved cardiac function. Mechanistically, by lentiviral-based overexpression and CRISPR/Cas9-mediated silencing of Qki5, we identified regulated expression of specific circular RNAs derived from Ttn (Titin), Fhod3 (Formin homology 2 domain containing 3), and Strn3 (Striatin, calmodulin-binding protein 3). Moreover, inhibition of Ttn-derived circular RNA increased the susceptibility of cardiomyocytes to doxorubicin.We here show that overexpression of Qki5 strongly attenuates the toxic effect of doxorubicin via regulating a set of circular RNAs. Qki5 is, thus, an interesting target molecule to combat doxorubicin-induced cardiotoxicity.CONCLUSIONSWe here show that overexpression of Qki5 strongly attenuates the toxic effect of doxorubicin via regulating a set of circular RNAs. Qki5 is, thus, an interesting target molecule to combat doxorubicin-induced cardiotoxicity. |
| Author | Streckfuß-Bömeke, Katrin Fiedler, Jan Thum, Thomas Milting, Hendrik Gupta, Shashi Kumar Garg, Ankita Bär, Christian Chatterjee, Shambhabi Foinquinos, Ariana |
| Author_xml | – sequence: 1 givenname: Shashi Kumar surname: Gupta fullname: Gupta, Shashi Kumar email: gupta.shashi@mh-hannover.de, thum.thomas@mh-hannover.de organization: From the Institute of Molecular and Translational Therapeutic Strategies (S.K.G., A.G., C.B., S.C., A.F., J.F., T.T.) and Excellence Cluster REBIRTH (T.T.), Hannover Medical School, Germany; Herz- und Diabeteszentrum NRW, Universitätsklinikum der Ruhr Universität Bochum, Erich und Hanna Klessmann-Institute for Cardiovascular Research and Development, Bad Oeynhausen, Germany (H.M.); Clinic for Cardiology and Pneumology, Stem Cell Laboratory, University Medical Center, Gottingen, Germany (K.S.-B.); DZHK (German Center for Cardiovascular Research) Partner site Göttingen, Germany (K.S.-B.); and National Heart and Lung Institute, Imperial College London, United Kingdom (T.T.). gupta.shashi@mh-hannover.de thum.thomas@mh-hannover.de – sequence: 2 givenname: Ankita surname: Garg fullname: Garg, Ankita organization: From the Institute of Molecular and Translational Therapeutic Strategies (S.K.G., A.G., C.B., S.C., A.F., J.F., T.T.) and Excellence Cluster REBIRTH (T.T.), Hannover Medical School, Germany; Herz- und Diabeteszentrum NRW, Universitätsklinikum der Ruhr Universität Bochum, Erich und Hanna Klessmann-Institute for Cardiovascular Research and Development, Bad Oeynhausen, Germany (H.M.); Clinic for Cardiology and Pneumology, Stem Cell Laboratory, University Medical Center, Gottingen, Germany (K.S.-B.); DZHK (German Center for Cardiovascular Research) Partner site Göttingen, Germany (K.S.-B.); and National Heart and Lung Institute, Imperial College London, United Kingdom (T.T.) – sequence: 3 givenname: Christian surname: Bär fullname: Bär, Christian organization: From the Institute of Molecular and Translational Therapeutic Strategies (S.K.G., A.G., C.B., S.C., A.F., J.F., T.T.) and Excellence Cluster REBIRTH (T.T.), Hannover Medical School, Germany; Herz- und Diabeteszentrum NRW, Universitätsklinikum der Ruhr Universität Bochum, Erich und Hanna Klessmann-Institute for Cardiovascular Research and Development, Bad Oeynhausen, Germany (H.M.); Clinic for Cardiology and Pneumology, Stem Cell Laboratory, University Medical Center, Gottingen, Germany (K.S.-B.); DZHK (German Center for Cardiovascular Research) Partner site Göttingen, Germany (K.S.-B.); and National Heart and Lung Institute, Imperial College London, United Kingdom (T.T.) – sequence: 4 givenname: Shambhabi surname: Chatterjee fullname: Chatterjee, Shambhabi organization: From the Institute of Molecular and Translational Therapeutic Strategies (S.K.G., A.G., C.B., S.C., A.F., J.F., T.T.) and Excellence Cluster REBIRTH (T.T.), Hannover Medical School, Germany; Herz- und Diabeteszentrum NRW, Universitätsklinikum der Ruhr Universität Bochum, Erich und Hanna Klessmann-Institute for Cardiovascular Research and Development, Bad Oeynhausen, Germany (H.M.); Clinic for Cardiology and Pneumology, Stem Cell Laboratory, University Medical Center, Gottingen, Germany (K.S.-B.); DZHK (German Center for Cardiovascular Research) Partner site Göttingen, Germany (K.S.-B.); and National Heart and Lung Institute, Imperial College London, United Kingdom (T.T.) – sequence: 5 givenname: Ariana surname: Foinquinos fullname: Foinquinos, Ariana organization: From the Institute of Molecular and Translational Therapeutic Strategies (S.K.G., A.G., C.B., S.C., A.F., J.F., T.T.) and Excellence Cluster REBIRTH (T.T.), Hannover Medical School, Germany; Herz- und Diabeteszentrum NRW, Universitätsklinikum der Ruhr Universität Bochum, Erich und Hanna Klessmann-Institute for Cardiovascular Research and Development, Bad Oeynhausen, Germany (H.M.); Clinic for Cardiology and Pneumology, Stem Cell Laboratory, University Medical Center, Gottingen, Germany (K.S.-B.); DZHK (German Center for Cardiovascular Research) Partner site Göttingen, Germany (K.S.-B.); and National Heart and Lung Institute, Imperial College London, United Kingdom (T.T.) – sequence: 6 givenname: Hendrik surname: Milting fullname: Milting, Hendrik organization: From the Institute of Molecular and Translational Therapeutic Strategies (S.K.G., A.G., C.B., S.C., A.F., J.F., T.T.) and Excellence Cluster REBIRTH (T.T.), Hannover Medical School, Germany; Herz- und Diabeteszentrum NRW, Universitätsklinikum der Ruhr Universität Bochum, Erich und Hanna Klessmann-Institute for Cardiovascular Research and Development, Bad Oeynhausen, Germany (H.M.); Clinic for Cardiology and Pneumology, Stem Cell Laboratory, University Medical Center, Gottingen, Germany (K.S.-B.); DZHK (German Center for Cardiovascular Research) Partner site Göttingen, Germany (K.S.-B.); and National Heart and Lung Institute, Imperial College London, United Kingdom (T.T.) – sequence: 7 givenname: Katrin surname: Streckfuß-Bömeke fullname: Streckfuß-Bömeke, Katrin organization: From the Institute of Molecular and Translational Therapeutic Strategies (S.K.G., A.G., C.B., S.C., A.F., J.F., T.T.) and Excellence Cluster REBIRTH (T.T.), Hannover Medical School, Germany; Herz- und Diabeteszentrum NRW, Universitätsklinikum der Ruhr Universität Bochum, Erich und Hanna Klessmann-Institute for Cardiovascular Research and Development, Bad Oeynhausen, Germany (H.M.); Clinic for Cardiology and Pneumology, Stem Cell Laboratory, University Medical Center, Gottingen, Germany (K.S.-B.); DZHK (German Center for Cardiovascular Research) Partner site Göttingen, Germany (K.S.-B.); and National Heart and Lung Institute, Imperial College London, United Kingdom (T.T.) – sequence: 8 givenname: Jan surname: Fiedler fullname: Fiedler, Jan organization: From the Institute of Molecular and Translational Therapeutic Strategies (S.K.G., A.G., C.B., S.C., A.F., J.F., T.T.) and Excellence Cluster REBIRTH (T.T.), Hannover Medical School, Germany; Herz- und Diabeteszentrum NRW, Universitätsklinikum der Ruhr Universität Bochum, Erich und Hanna Klessmann-Institute for Cardiovascular Research and Development, Bad Oeynhausen, Germany (H.M.); Clinic for Cardiology and Pneumology, Stem Cell Laboratory, University Medical Center, Gottingen, Germany (K.S.-B.); DZHK (German Center for Cardiovascular Research) Partner site Göttingen, Germany (K.S.-B.); and National Heart and Lung Institute, Imperial College London, United Kingdom (T.T.) – sequence: 9 givenname: Thomas surname: Thum fullname: Thum, Thomas email: gupta.shashi@mh-hannover.de, thum.thomas@mh-hannover.de organization: From the Institute of Molecular and Translational Therapeutic Strategies (S.K.G., A.G., C.B., S.C., A.F., J.F., T.T.) and Excellence Cluster REBIRTH (T.T.), Hannover Medical School, Germany; Herz- und Diabeteszentrum NRW, Universitätsklinikum der Ruhr Universität Bochum, Erich und Hanna Klessmann-Institute for Cardiovascular Research and Development, Bad Oeynhausen, Germany (H.M.); Clinic for Cardiology and Pneumology, Stem Cell Laboratory, University Medical Center, Gottingen, Germany (K.S.-B.); DZHK (German Center for Cardiovascular Research) Partner site Göttingen, Germany (K.S.-B.); and National Heart and Lung Institute, Imperial College London, United Kingdom (T.T.). gupta.shashi@mh-hannover.de thum.thomas@mh-hannover.de |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29133306$$D View this record in MEDLINE/PubMed |
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| Keywords | heart failure RNA-binding protein cardiotoxicity noncoding RNA doxorubicin |
| Language | English |
| License | 2017 The Authors. |
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| PublicationTitle | Circulation research |
| PublicationTitleAlternate | Circ Res |
| PublicationYear | 2018 |
| References | 29348242 - Circ Res. 2018 Jan 19;122(2):188-190 |
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| Snippet | RBPs (RNA-binding proteins) have been described to be expressed and regulated in various organs including the heart. Little is known about the role of RBPs in... |
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| SubjectTerms | Animals Antibiotics, Antineoplastic - toxicity Cardiotoxicity - genetics Cardiotoxicity - metabolism Doxorubicin - toxicity Gene Expression Mice Mice, Inbred C57BL Myocytes, Cardiac - drug effects Myocytes, Cardiac - metabolism Random Allocation RNA - biosynthesis RNA - genetics RNA-Binding Proteins - biosynthesis RNA-Binding Proteins - genetics |
| Title | Quaking Inhibits Doxorubicin-Mediated Cardiotoxicity Through Regulation of Cardiac Circular RNA Expression |
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