Reduced plakoglobin increases the risk of sodium current defects and atrial conduction abnormalities in response to androgenic anabolic steroid abuse
Androgenic anabolic steroids (AAS) are commonly abused by young men. Male sex and increased AAS levels are associated with earlier and more severe manifestation of common cardiac conditions, such as atrial fibrillation, and rare ones, such as arrhythmogenic right ventricular cardiomyopathy (ARVC). C...
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| Published in | The Journal of physiology Vol. 602; no. 18; pp. 4409 - 4436 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
Wiley Subscription Services, Inc
01.09.2024
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0022-3751 1469-7793 1469-7793 |
| DOI | 10.1113/JP284597 |
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| Abstract | Androgenic anabolic steroids (AAS) are commonly abused by young men. Male sex and increased AAS levels are associated with earlier and more severe manifestation of common cardiac conditions, such as atrial fibrillation, and rare ones, such as arrhythmogenic right ventricular cardiomyopathy (ARVC). Clinical observations suggest a potential atrial involvement in ARVC. Arrhythmogenic right ventricular cardiomyopathy is caused by desmosomal gene defects, including reduced plakoglobin expression. Here, we analysed clinical records from 146 ARVC patients to identify that ARVC is more common in males than females. Patients with ARVC also had an increased incidence of atrial arrhythmias and P wave changes. To study desmosomal vulnerability and the effects of AAS on the atria, young adult male mice, heterozygously deficient for plakoglobin (Plako+/−), and wild type (WT) littermates were chronically exposed to 5α‐dihydrotestosterone (DHT) or placebo. The DHT increased atrial expression of pro‐hypertrophic, fibrotic and inflammatory transcripts. In mice with reduced plakoglobin, DHT exaggerated P wave abnormalities, atrial conduction slowing, sodium current depletion, action potential amplitude reduction and the fall in action potential depolarization rate. Super‐resolution microscopy revealed a decrease in NaV1.5 membrane clustering in Plako+/− atrial cardiomyocytes after DHT exposure. In summary, AAS combined with plakoglobin deficiency cause pathological atrial electrical remodelling in young male hearts. Male sex is likely to increase the risk of atrial arrhythmia, particularly in those with desmosomal gene variants. This risk is likely to be exaggerated further by AAS use.
Key points
Androgenic male sex hormones, such as testosterone, might increase the risk of atrial fibrillation in patients with arrhythmogenic right ventricular cardiomyopathy (ARVC), which is often caused by desmosomal gene defects (e.g. reduced plakoglobin expression).
In this study, we observed a significantly higher proportion of males who had ARVC compared with females, and atrial arrhythmias and P wave changes represented a common observation in advanced ARVC stages.
In mice with reduced plakoglobin expression, chronic administration of 5α‐dihydrotestosterone led to P wave abnormalities, atrial conduction slowing, sodium current depletion and a decrease in membrane‐localized NaV1.5 clusters.
5α‐Dihydrotestosterone, therefore, represents a stimulus aggravating the pro‐arrhythmic phenotype in carriers of desmosomal mutations and can affect atrial electrical function.
figure legend Atrial arrhythmias (AA) can be a clinical manifestation of advanced arrhythmogenic right ventricular cardiomyopathy (ARVC), and a male preponderance can be observed. Patients with ARVC show atrial conduction abnormalities on ECG. In a murine experimental ARVC model, low expression of the ARVC‐associated protein plakoglobin (Plako+/−) combined with androgenic anabolic steroid (male sex hormone) exposure led to ECG P wave abnormalities. This was combined with reduced sodium channel (NaV1.5) clustering and decreased peak Na+ current, leading to atrial conduction abnormalities, a substrate for arrhythmias. |
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| AbstractList | Androgenic anabolic steroids (AAS) are commonly abused by young men. Male sex and increased AAS levels are associated with earlier and more severe manifestation of common cardiac conditions, such as atrial fibrillation, and rare ones, such as arrhythmogenic right ventricular cardiomyopathy (ARVC). Clinical observations suggest a potential atrial involvement in ARVC. Arrhythmogenic right ventricular cardiomyopathy is caused by desmosomal gene defects, including reduced plakoglobin expression. Here, we analysed clinical records from 146 ARVC patients to identify that ARVC is more common in males than females. Patients with ARVC also had an increased incidence of atrial arrhythmias and P wave changes. To study desmosomal vulnerability and the effects of AAS on the atria, young adult male mice, heterozygously deficient for plakoglobin (Plako+/−), and wild type (WT) littermates were chronically exposed to 5α‐dihydrotestosterone (DHT) or placebo. The DHT increased atrial expression of pro‐hypertrophic, fibrotic and inflammatory transcripts. In mice with reduced plakoglobin, DHT exaggerated P wave abnormalities, atrial conduction slowing, sodium current depletion, action potential amplitude reduction and the fall in action potential depolarization rate. Super‐resolution microscopy revealed a decrease in NaV1.5 membrane clustering in Plako+/− atrial cardiomyocytes after DHT exposure. In summary, AAS combined with plakoglobin deficiency cause pathological atrial electrical remodelling in young male hearts. Male sex is likely to increase the risk of atrial arrhythmia, particularly in those with desmosomal gene variants. This risk is likely to be exaggerated further by AAS use.
Key points
Androgenic male sex hormones, such as testosterone, might increase the risk of atrial fibrillation in patients with arrhythmogenic right ventricular cardiomyopathy (ARVC), which is often caused by desmosomal gene defects (e.g. reduced plakoglobin expression).
In this study, we observed a significantly higher proportion of males who had ARVC compared with females, and atrial arrhythmias and P wave changes represented a common observation in advanced ARVC stages.
In mice with reduced plakoglobin expression, chronic administration of 5α‐dihydrotestosterone led to P wave abnormalities, atrial conduction slowing, sodium current depletion and a decrease in membrane‐localized NaV1.5 clusters.
5α‐Dihydrotestosterone, therefore, represents a stimulus aggravating the pro‐arrhythmic phenotype in carriers of desmosomal mutations and can affect atrial electrical function.
figure legend Atrial arrhythmias (AA) can be a clinical manifestation of advanced arrhythmogenic right ventricular cardiomyopathy (ARVC), and a male preponderance can be observed. Patients with ARVC show atrial conduction abnormalities on ECG. In a murine experimental ARVC model, low expression of the ARVC‐associated protein plakoglobin (Plako+/−) combined with androgenic anabolic steroid (male sex hormone) exposure led to ECG P wave abnormalities. This was combined with reduced sodium channel (NaV1.5) clustering and decreased peak Na+ current, leading to atrial conduction abnormalities, a substrate for arrhythmias. Androgenic anabolic steroids (AAS) are commonly abused by young men. Male sex and increased AAS levels are associated with earlier and more severe manifestation of common cardiac conditions, such as atrial fibrillation, and rare ones, such as arrhythmogenic right ventricular cardiomyopathy (ARVC). Clinical observations suggest a potential atrial involvement in ARVC. Arrhythmogenic right ventricular cardiomyopathy is caused by desmosomal gene defects, including reduced plakoglobin expression. Here, we analysed clinical records from 146 ARVC patients to identify that ARVC is more common in males than females. Patients with ARVC also had an increased incidence of atrial arrhythmias and P wave changes. To study desmosomal vulnerability and the effects of AAS on the atria, young adult male mice, heterozygously deficient for plakoglobin (Plako+/−), and wild type (WT) littermates were chronically exposed to 5α‐dihydrotestosterone (DHT) or placebo. The DHT increased atrial expression of pro‐hypertrophic, fibrotic and inflammatory transcripts. In mice with reduced plakoglobin, DHT exaggerated P wave abnormalities, atrial conduction slowing, sodium current depletion, action potential amplitude reduction and the fall in action potential depolarization rate. Super‐resolution microscopy revealed a decrease in NaV1.5 membrane clustering in Plako+/− atrial cardiomyocytes after DHT exposure. In summary, AAS combined with plakoglobin deficiency cause pathological atrial electrical remodelling in young male hearts. Male sex is likely to increase the risk of atrial arrhythmia, particularly in those with desmosomal gene variants. This risk is likely to be exaggerated further by AAS use.Key pointsAndrogenic male sex hormones, such as testosterone, might increase the risk of atrial fibrillation in patients with arrhythmogenic right ventricular cardiomyopathy (ARVC), which is often caused by desmosomal gene defects (e.g. reduced plakoglobin expression).In this study, we observed a significantly higher proportion of males who had ARVC compared with females, and atrial arrhythmias and P wave changes represented a common observation in advanced ARVC stages.In mice with reduced plakoglobin expression, chronic administration of 5α‐dihydrotestosterone led to P wave abnormalities, atrial conduction slowing, sodium current depletion and a decrease in membrane‐localized NaV1.5 clusters.5α‐Dihydrotestosterone, therefore, represents a stimulus aggravating the pro‐arrhythmic phenotype in carriers of desmosomal mutations and can affect atrial electrical function. Androgenic anabolic steroids (AAS) are commonly abused by young men. Male sex and increased AAS levels are associated with earlier and more severe manifestation of common cardiac conditions, such as atrial fibrillation, and rare ones, such as arrhythmogenic right ventricular cardiomyopathy (ARVC). Clinical observations suggest a potential atrial involvement in ARVC. Arrhythmogenic right ventricular cardiomyopathy is caused by desmosomal gene defects, including reduced plakoglobin expression. Here, we analysed clinical records from 146 ARVC patients to identify that ARVC is more common in males than females. Patients with ARVC also had an increased incidence of atrial arrhythmias and P wave changes. To study desmosomal vulnerability and the effects of AAS on the atria, young adult male mice, heterozygously deficient for plakoglobin (Plako+/-), and wild type (WT) littermates were chronically exposed to 5α-dihydrotestosterone (DHT) or placebo. The DHT increased atrial expression of pro-hypertrophic, fibrotic and inflammatory transcripts. In mice with reduced plakoglobin, DHT exaggerated P wave abnormalities, atrial conduction slowing, sodium current depletion, action potential amplitude reduction and the fall in action potential depolarization rate. Super-resolution microscopy revealed a decrease in NaV1.5 membrane clustering in Plako+/- atrial cardiomyocytes after DHT exposure. In summary, AAS combined with plakoglobin deficiency cause pathological atrial electrical remodelling in young male hearts. Male sex is likely to increase the risk of atrial arrhythmia, particularly in those with desmosomal gene variants. This risk is likely to be exaggerated further by AAS use. KEY POINTS: Androgenic male sex hormones, such as testosterone, might increase the risk of atrial fibrillation in patients with arrhythmogenic right ventricular cardiomyopathy (ARVC), which is often caused by desmosomal gene defects (e.g. reduced plakoglobin expression). In this study, we observed a significantly higher proportion of males who had ARVC compared with females, and atrial arrhythmias and P wave changes represented a common observation in advanced ARVC stages. In mice with reduced plakoglobin expression, chronic administration of 5α-dihydrotestosterone led to P wave abnormalities, atrial conduction slowing, sodium current depletion and a decrease in membrane-localized NaV1.5 clusters. 5α-Dihydrotestosterone, therefore, represents a stimulus aggravating the pro-arrhythmic phenotype in carriers of desmosomal mutations and can affect atrial electrical function.Androgenic anabolic steroids (AAS) are commonly abused by young men. Male sex and increased AAS levels are associated with earlier and more severe manifestation of common cardiac conditions, such as atrial fibrillation, and rare ones, such as arrhythmogenic right ventricular cardiomyopathy (ARVC). Clinical observations suggest a potential atrial involvement in ARVC. Arrhythmogenic right ventricular cardiomyopathy is caused by desmosomal gene defects, including reduced plakoglobin expression. Here, we analysed clinical records from 146 ARVC patients to identify that ARVC is more common in males than females. Patients with ARVC also had an increased incidence of atrial arrhythmias and P wave changes. To study desmosomal vulnerability and the effects of AAS on the atria, young adult male mice, heterozygously deficient for plakoglobin (Plako+/-), and wild type (WT) littermates were chronically exposed to 5α-dihydrotestosterone (DHT) or placebo. The DHT increased atrial expression of pro-hypertrophic, fibrotic and inflammatory transcripts. In mice with reduced plakoglobin, DHT exaggerated P wave abnormalities, atrial conduction slowing, sodium current depletion, action potential amplitude reduction and the fall in action potential depolarization rate. Super-resolution microscopy revealed a decrease in NaV1.5 membrane clustering in Plako+/- atrial cardiomyocytes after DHT exposure. In summary, AAS combined with plakoglobin deficiency cause pathological atrial electrical remodelling in young male hearts. Male sex is likely to increase the risk of atrial arrhythmia, particularly in those with desmosomal gene variants. This risk is likely to be exaggerated further by AAS use. KEY POINTS: Androgenic male sex hormones, such as testosterone, might increase the risk of atrial fibrillation in patients with arrhythmogenic right ventricular cardiomyopathy (ARVC), which is often caused by desmosomal gene defects (e.g. reduced plakoglobin expression). In this study, we observed a significantly higher proportion of males who had ARVC compared with females, and atrial arrhythmias and P wave changes represented a common observation in advanced ARVC stages. In mice with reduced plakoglobin expression, chronic administration of 5α-dihydrotestosterone led to P wave abnormalities, atrial conduction slowing, sodium current depletion and a decrease in membrane-localized NaV1.5 clusters. 5α-Dihydrotestosterone, therefore, represents a stimulus aggravating the pro-arrhythmic phenotype in carriers of desmosomal mutations and can affect atrial electrical function. Androgenic anabolic steroids (AAS) are commonly abused by young men. Male sex and increased AAS levels are associated with earlier and more severe manifestation of common cardiac conditions, such as atrial fibrillation, and rare ones, such as arrhythmogenic right ventricular cardiomyopathy (ARVC). Clinical observations suggest a potential atrial involvement in ARVC. Arrhythmogenic right ventricular cardiomyopathy is caused by desmosomal gene defects, including reduced plakoglobin expression. Here, we analysed clinical records from 146 ARVC patients to identify that ARVC is more common in males than females. Patients with ARVC also had an increased incidence of atrial arrhythmias and P wave changes. To study desmosomal vulnerability and the effects of AAS on the atria, young adult male mice, heterozygously deficient for plakoglobin (Plako ), and wild type (WT) littermates were chronically exposed to 5α-dihydrotestosterone (DHT) or placebo. The DHT increased atrial expression of pro-hypertrophic, fibrotic and inflammatory transcripts. In mice with reduced plakoglobin, DHT exaggerated P wave abnormalities, atrial conduction slowing, sodium current depletion, action potential amplitude reduction and the fall in action potential depolarization rate. Super-resolution microscopy revealed a decrease in Na 1.5 membrane clustering in Plako atrial cardiomyocytes after DHT exposure. In summary, AAS combined with plakoglobin deficiency cause pathological atrial electrical remodelling in young male hearts. Male sex is likely to increase the risk of atrial arrhythmia, particularly in those with desmosomal gene variants. This risk is likely to be exaggerated further by AAS use. KEY POINTS: Androgenic male sex hormones, such as testosterone, might increase the risk of atrial fibrillation in patients with arrhythmogenic right ventricular cardiomyopathy (ARVC), which is often caused by desmosomal gene defects (e.g. reduced plakoglobin expression). In this study, we observed a significantly higher proportion of males who had ARVC compared with females, and atrial arrhythmias and P wave changes represented a common observation in advanced ARVC stages. In mice with reduced plakoglobin expression, chronic administration of 5α-dihydrotestosterone led to P wave abnormalities, atrial conduction slowing, sodium current depletion and a decrease in membrane-localized Na 1.5 clusters. 5α-Dihydrotestosterone, therefore, represents a stimulus aggravating the pro-arrhythmic phenotype in carriers of desmosomal mutations and can affect atrial electrical function. |
| Author | Syeda, Fahima Hepburn, Claire Gkoutos, Georgios V. Steeds, Richard Wright, Thomas Sommerfeld, Laura C. O'Shea, Christopher Pavlovic, Davor Holmes, Andrew P. Fabritz, Larissa Witten, Anika Kew, Tania Cardoso, Victor R. Broadway‐Stringer, Sophie Lavery, Gareth G. Yu, Ting Y. Kirchhof, Paulus Kavanagh, Deirdre M. O'Reilly, Molly Kulle, Alexandra Arlt, Wiebke Fortmueller, Lisa Menon, Priyanka R. Pike, Jeremy M. Stoll, Monika Kabir, S. Nashitha Lutz, Susanne Gehmlich, Katja Aljehani, Areej |
| Author_xml | – sequence: 1 givenname: Laura C. orcidid: 0000-0001-9837-8770 surname: Sommerfeld fullname: Sommerfeld, Laura C. organization: Standort Hamburg/Kiel/Lübeck – sequence: 2 givenname: Andrew P. orcidid: 0000-0001-9270-9401 surname: Holmes fullname: Holmes, Andrew P. organization: University of Birmingham – sequence: 3 givenname: Ting Y. surname: Yu fullname: Yu, Ting Y. organization: Research and Training Centre in Physical Sciences for Health – sequence: 4 givenname: Christopher orcidid: 0000-0003-3030-7364 surname: O'Shea fullname: O'Shea, Christopher organization: Research and Training Centre in Physical Sciences for Health – sequence: 5 givenname: Deirdre M. orcidid: 0000-0003-1531-6617 surname: Kavanagh fullname: Kavanagh, Deirdre M. organization: University of Birmingham – sequence: 6 givenname: Jeremy M. orcidid: 0000-0003-4163-0335 surname: Pike fullname: Pike, Jeremy M. organization: University of Birmingham – sequence: 7 givenname: Thomas surname: Wright fullname: Wright, Thomas organization: University of Birmingham – sequence: 8 givenname: Fahima orcidid: 0000-0002-0277-2552 surname: Syeda fullname: Syeda, Fahima organization: University of Birmingham – sequence: 9 givenname: Areej orcidid: 0009-0005-5502-3618 surname: Aljehani fullname: Aljehani, Areej organization: University of Birmingham – sequence: 10 givenname: Tania surname: Kew fullname: Kew, Tania organization: University of Birmingham – sequence: 11 givenname: Victor R. orcidid: 0000-0002-9588-6304 surname: Cardoso fullname: Cardoso, Victor R. organization: University of Birmingham – sequence: 12 givenname: S. Nashitha orcidid: 0000-0003-1811-8683 surname: Kabir fullname: Kabir, S. Nashitha organization: University of Birmingham – sequence: 13 givenname: Claire orcidid: 0000-0003-2651-9583 surname: Hepburn fullname: Hepburn, Claire organization: University of Birmingham – sequence: 14 givenname: Priyanka R. orcidid: 0000-0001-9541-7180 surname: Menon fullname: Menon, Priyanka R. organization: University of Birmingham – sequence: 15 givenname: Sophie orcidid: 0000-0003-1657-5442 surname: Broadway‐Stringer fullname: Broadway‐Stringer, Sophie organization: University of Birmingham – sequence: 16 givenname: Molly orcidid: 0000-0003-1936-5838 surname: O'Reilly fullname: O'Reilly, Molly organization: University of Birmingham – sequence: 17 givenname: Anika orcidid: 0000-0002-8245-7105 surname: Witten fullname: Witten, Anika organization: University of Münster – sequence: 18 givenname: Lisa orcidid: 0000-0003-1222-8830 surname: Fortmueller fullname: Fortmueller, Lisa organization: University of Münster – sequence: 19 givenname: Susanne orcidid: 0000-0002-0554-8070 surname: Lutz fullname: Lutz, Susanne organization: University Medical Center Göttingen – sequence: 20 givenname: Alexandra orcidid: 0000-0002-4411-6879 surname: Kulle fullname: Kulle, Alexandra organization: University Hospital Schleswig‐Holstein, Campus Kiel – sequence: 21 givenname: Georgios V. orcidid: 0000-0002-2061-091X surname: Gkoutos fullname: Gkoutos, Georgios V. organization: MRC Health Data Research UK (HDR), Midlands Site – sequence: 22 givenname: Davor orcidid: 0000-0002-3171-3551 surname: Pavlovic fullname: Pavlovic, Davor organization: University of Birmingham – sequence: 23 givenname: Wiebke orcidid: 0000-0001-5106-9719 surname: Arlt fullname: Arlt, Wiebke organization: London UK & Institute of Clinical Sciences, Faculty of Medicine, Imperial College – sequence: 24 givenname: Gareth G. orcidid: 0000-0001-5794-748X surname: Lavery fullname: Lavery, Gareth G. organization: Birmingham Health Partners – sequence: 25 givenname: Richard orcidid: 0000-0001-5687-2535 surname: Steeds fullname: Steeds, Richard organization: University Hospitals Birmingham NHS Foundation Trust – sequence: 26 givenname: Katja orcidid: 0000-0003-4019-1844 surname: Gehmlich fullname: Gehmlich, Katja organization: University of Birmingham – sequence: 27 givenname: Monika orcidid: 0000-0002-2711-4281 surname: Stoll fullname: Stoll, Monika organization: Maastricht University – sequence: 28 givenname: Paulus orcidid: 0000-0002-1881-0197 surname: Kirchhof fullname: Kirchhof, Paulus organization: University Heart & Vascular Center Hamburg, University Medical Center Hamburg‐Eppendorf – sequence: 29 givenname: Larissa orcidid: 0000-0002-9241-1733 surname: Fabritz fullname: Fabritz, Larissa email: l.fabritz@uke.de organization: University Heart & Vascular Center Hamburg, University Medical Center Hamburg‐Eppendorf |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38345865$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_1113_JP286706 crossref_primary_10_1242_jcs_262041 |
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| Issue | 18 |
| Keywords | conduction velocity arrhythmogenic right ventricular cardiomyopathy desmosome testosterone cardiac atria NaV1.5 |
| Language | English |
| License | Attribution 2024 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society. |
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| Notes | Handling Editors: Peter Kohl & Ramona Emig This article was first published as a preprint. Sommerfeld LC, Holmes AP, Yu TY, O'Shea C, Kavanagh DM, Pike JM, Wright T, Syeda F, Aljehani A, Kew T, Cardoso VR, Kabir SN, Hepburn C, Menon PM, Broadway‐Stringer S, O'Reilly M, Witten A, Fortmueller L, Lutz S, Kulle A, Gkoutos GV, Pavlovic D, Arlt W, Lavery GG, Steeds R, Gehmlich K, Stoll M, Kirchhof P, Fabritz L. 2022. Male sex hormone and reduced plakoglobin jointly impair atrial conduction and cardiac sodium currents. bioRxiv. https://doi.org/10.1113/JP284597#support‐information‐section The peer review history is available in the Supporting Information section of this article https://doi.org/10.1101/2022.06.03.494748 . ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 |
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Androgenic anabolic steroid abuse and the cardiovascular system publication-title: Handbook of Experimental Pharmacology – ident: e_1_2_5_97_1 doi: 10.1371/journal.pone.0099178 – ident: e_1_2_5_4_1 doi: 10.1155/2014/451520 |
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| Snippet | Androgenic anabolic steroids (AAS) are commonly abused by young men. Male sex and increased AAS levels are associated with earlier and more severe... |
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| SubjectTerms | Action potential Action Potentials - drug effects Adult Anabolic Agents - pharmacology Anabolic Androgenic Steroids Androgens - pharmacology Animals Arrhythmia arrhythmogenic right ventricular cardiomyopathy Arrhythmogenic Right Ventricular Dysplasia - genetics Arrhythmogenic Right Ventricular Dysplasia - metabolism Arrhythmogenic Right Ventricular Dysplasia - physiopathology Cardiac arrhythmia cardiac atria Cardiomyocytes Cardiomyopathy Catenin Conduction conduction velocity Depolarization desmosome Dihydrotestosterone Dihydrotestosterone - pharmacology Female Fibrillation gamma Catenin - genetics gamma Catenin - metabolism Heart Atria - drug effects Heart Atria - metabolism Heart Atria - physiopathology Humans Male Males Membrane potential Mice Mice, Inbred C57BL NaV1.5 Phenotypes Sex differences Sex hormones Sodium Sodium channels (voltage-gated) Steroid hormones Testosterone Ventricle Young Adult |
| Title | Reduced plakoglobin increases the risk of sodium current defects and atrial conduction abnormalities in response to androgenic anabolic steroid abuse |
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