Proteostasis in epicardial versus subcutaneous adipose tissue in heart failure subjects with and without diabetes
Cardiovascular diseases (CVDs) are leading cause of death and primary cause of morbidity and mortality in diabetic population. Epicardial adipose tissue (EAT) covers the heart's surface and is a source of biomolecules regulating heart and blood vessel physiology. The protective activation of th...
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| Published in | Biochimica et biophysica acta. Molecular basis of disease Vol. 1864; no. 6; pp. 2183 - 2198 |
|---|---|
| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Netherlands
Elsevier B.V
01.06.2018
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0925-4439 1879-260X |
| DOI | 10.1016/j.bbadis.2018.03.025 |
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| Abstract | Cardiovascular diseases (CVDs) are leading cause of death and primary cause of morbidity and mortality in diabetic population. Epicardial adipose tissue (EAT) covers the heart's surface and is a source of biomolecules regulating heart and blood vessel physiology. The protective activation of the unfolded protein response (UPR) and autophagy allows the cardiomyocyte reticular network to restore energy and/or nutrient homeostasis and to avoid cell death. However, an excessive or prolonged UPR activation can trigger cell death. UPR activation is an early event of diabetic cardiomyopathies and deregulated autophagy is associated with CVDs.
An upregulation of UPR markers (glucose-regulated protein 78 KDa, glucose-regulated protein 94 KDa, inositol-requiring enzyme 1α, protein kinase RNA-like ER kinase and CCAAT/−enhancer-binding protein homologous protein (CHOP) gene) in EAT compared to subcutaneous adipose tissue (SAT), was observed as well as the UPR-related apoptosis marker caspase-4/procaspase-4 ratio but not in CHOP protein levels. Additionally, levels of ubiquitin and ubiquitinated proteins were decreased in EAT. Moreover, upregulation of autophagy markers (5′ adenosine monophosphate-activated protein kinase, mechanistic target of rapamycin, Beclin 1, microtubule-associated protein light chain 3-II, lysosome-associated membrane protein 2, and PTEN-induced putative kinase 1) was observed, as well as an increase in the apoptotic Bim but not the ratio between Bim and the anti-apoptotic Bcl-2 in EAT. Diabetic patients show alterations in UPR activation markers but not in autophagy or apoptosis markers.
UPR and autophagy are increased in EAT compared to SAT, opening doors to the identification of early biomarkers for cardiomyopathies and novel therapeutic targets.
•Epicardial adipose tissue has increased ER stress compared to subcutaneous adipose tissue from the same patients•Diabetic patients have slightly increase of ER stress in adipose tissue compared to non-diabetic patients•Epicardial adipose tissue has increased autophagy compared to subcutaneous adipose tissue from the same patients |
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| AbstractList | Cardiovascular diseases (CVDs) are leading cause of death and primary cause of morbidity and mortality in diabetic population. Epicardial adipose tissue (EAT) covers the heart's surface and is a source of biomolecules regulating heart and blood vessel physiology. The protective activation of the unfolded protein response (UPR) and autophagy allows the cardiomyocyte reticular network to restore energy and/or nutrient homeostasis and to avoid cell death. However, an excessive or prolonged UPR activation can trigger cell death. UPR activation is an early event of diabetic cardiomyopathies and deregulated autophagy is associated with CVDs.
An upregulation of UPR markers (glucose-regulated protein 78 KDa, glucose-regulated protein 94 KDa, inositol-requiring enzyme 1α, protein kinase RNA-like ER kinase and CCAAT/-enhancer-binding protein homologous protein (CHOP) gene) in EAT compared to subcutaneous adipose tissue (SAT), was observed as well as the UPR-related apoptosis marker caspase-4/procaspase-4 ratio but not in CHOP protein levels. Additionally, levels of ubiquitin and ubiquitinated proteins were decreased in EAT. Moreover, upregulation of autophagy markers (5' adenosine monophosphate-activated protein kinase, mechanistic target of rapamycin, Beclin 1, microtubule-associated protein light chain 3-II, lysosome-associated membrane protein 2, and PTEN-induced putative kinase 1) was observed, as well as an increase in the apoptotic Bim but not the ratio between Bim and the anti-apoptotic Bcl-2 in EAT. Diabetic patients show alterations in UPR activation markers but not in autophagy or apoptosis markers.
UPR and autophagy are increased in EAT compared to SAT, opening doors to the identification of early biomarkers for cardiomyopathies and novel therapeutic targets. Cardiovascular diseases (CVDs) are leading cause of death and primary cause of morbidity and mortality in diabetic population. Epicardial adipose tissue (EAT) covers the heart's surface and is a source of biomolecules regulating heart and blood vessel physiology. The protective activation of the unfolded protein response (UPR) and autophagy allows the cardiomyocyte reticular network to restore energy and/or nutrient homeostasis and to avoid cell death. However, an excessive or prolonged UPR activation can trigger cell death. UPR activation is an early event of diabetic cardiomyopathies and deregulated autophagy is associated with CVDs. An upregulation of UPR markers (glucose-regulated protein 78 KDa, glucose-regulated protein 94 KDa, inositol-requiring enzyme 1α, protein kinase RNA-like ER kinase and CCAAT/−enhancer-binding protein homologous protein (CHOP) gene) in EAT compared to subcutaneous adipose tissue (SAT), was observed as well as the UPR-related apoptosis marker caspase-4/procaspase-4 ratio but not in CHOP protein levels. Additionally, levels of ubiquitin and ubiquitinated proteins were decreased in EAT. Moreover, upregulation of autophagy markers (5′ adenosine monophosphate-activated protein kinase, mechanistic target of rapamycin, Beclin 1, microtubule-associated protein light chain 3-II, lysosome-associated membrane protein 2, and PTEN-induced putative kinase 1) was observed, as well as an increase in the apoptotic Bim but not the ratio between Bim and the anti-apoptotic Bcl-2 in EAT. Diabetic patients show alterations in UPR activation markers but not in autophagy or apoptosis markers. UPR and autophagy are increased in EAT compared to SAT, opening doors to the identification of early biomarkers for cardiomyopathies and novel therapeutic targets. •Epicardial adipose tissue has increased ER stress compared to subcutaneous adipose tissue from the same patients•Diabetic patients have slightly increase of ER stress in adipose tissue compared to non-diabetic patients•Epicardial adipose tissue has increased autophagy compared to subcutaneous adipose tissue from the same patients Cardiovascular diseases (CVDs) are leading cause of death and primary cause of morbidity and mortality in diabetic population. Epicardial adipose tissue (EAT) covers the heart's surface and is a source of biomolecules regulating heart and blood vessel physiology. The protective activation of the unfolded protein response (UPR) and autophagy allows the cardiomyocyte reticular network to restore energy and/or nutrient homeostasis and to avoid cell death. However, an excessive or prolonged UPR activation can trigger cell death. UPR activation is an early event of diabetic cardiomyopathies and deregulated autophagy is associated with CVDs.BACKGROUNDCardiovascular diseases (CVDs) are leading cause of death and primary cause of morbidity and mortality in diabetic population. Epicardial adipose tissue (EAT) covers the heart's surface and is a source of biomolecules regulating heart and blood vessel physiology. The protective activation of the unfolded protein response (UPR) and autophagy allows the cardiomyocyte reticular network to restore energy and/or nutrient homeostasis and to avoid cell death. However, an excessive or prolonged UPR activation can trigger cell death. UPR activation is an early event of diabetic cardiomyopathies and deregulated autophagy is associated with CVDs.An upregulation of UPR markers (glucose-regulated protein 78 KDa, glucose-regulated protein 94 KDa, inositol-requiring enzyme 1α, protein kinase RNA-like ER kinase and CCAAT/-enhancer-binding protein homologous protein (CHOP) gene) in EAT compared to subcutaneous adipose tissue (SAT), was observed as well as the UPR-related apoptosis marker caspase-4/procaspase-4 ratio but not in CHOP protein levels. Additionally, levels of ubiquitin and ubiquitinated proteins were decreased in EAT. Moreover, upregulation of autophagy markers (5' adenosine monophosphate-activated protein kinase, mechanistic target of rapamycin, Beclin 1, microtubule-associated protein light chain 3-II, lysosome-associated membrane protein 2, and PTEN-induced putative kinase 1) was observed, as well as an increase in the apoptotic Bim but not the ratio between Bim and the anti-apoptotic Bcl-2 in EAT. Diabetic patients show alterations in UPR activation markers but not in autophagy or apoptosis markers.RESULTSAn upregulation of UPR markers (glucose-regulated protein 78 KDa, glucose-regulated protein 94 KDa, inositol-requiring enzyme 1α, protein kinase RNA-like ER kinase and CCAAT/-enhancer-binding protein homologous protein (CHOP) gene) in EAT compared to subcutaneous adipose tissue (SAT), was observed as well as the UPR-related apoptosis marker caspase-4/procaspase-4 ratio but not in CHOP protein levels. Additionally, levels of ubiquitin and ubiquitinated proteins were decreased in EAT. Moreover, upregulation of autophagy markers (5' adenosine monophosphate-activated protein kinase, mechanistic target of rapamycin, Beclin 1, microtubule-associated protein light chain 3-II, lysosome-associated membrane protein 2, and PTEN-induced putative kinase 1) was observed, as well as an increase in the apoptotic Bim but not the ratio between Bim and the anti-apoptotic Bcl-2 in EAT. Diabetic patients show alterations in UPR activation markers but not in autophagy or apoptosis markers.UPR and autophagy are increased in EAT compared to SAT, opening doors to the identification of early biomarkers for cardiomyopathies and novel therapeutic targets.CONCLUSIONUPR and autophagy are increased in EAT compared to SAT, opening doors to the identification of early biomarkers for cardiomyopathies and novel therapeutic targets. |
| Author | Lourenço, N. Carvalho, E. Fonseca, A.C. Burgeiro, A. Antunes, M. Carvalho, L. Espinoza, D. |
| AuthorAffiliation | 6 Department of Geriatrics, University of Arkansas for Medical Sciences, Little Rock, Arkansas 72202, United States 2 Institute of Pathology, Faculty of Medicine, University of Coimbra, 3004-517 Coimbra, Portugal 3 Centre for Informatics and Systems of the University of Coimbra (CISUC), Department of Informatics Engineering, University of Coimbra, Portugal 1 Center of Neuroscience and Cell Biology, University of Coimbra, 3004-504 Coimbra, Portugal 7 Arkansas Children's Research Institute, Little Rock, Arkansas 72202, United States 5 The Portuguese Diabetes Association (APDP), 1250-203 Lisbon, Portugal 4 Cardiothoracic Surgery Unit at the Coimbra University Hospital Centre, Praceta Prof. Mota Pinto, 3000-075 Coimbra, Portugal |
| AuthorAffiliation_xml | – name: 6 Department of Geriatrics, University of Arkansas for Medical Sciences, Little Rock, Arkansas 72202, United States – name: 2 Institute of Pathology, Faculty of Medicine, University of Coimbra, 3004-517 Coimbra, Portugal – name: 1 Center of Neuroscience and Cell Biology, University of Coimbra, 3004-504 Coimbra, Portugal – name: 7 Arkansas Children's Research Institute, Little Rock, Arkansas 72202, United States – name: 3 Centre for Informatics and Systems of the University of Coimbra (CISUC), Department of Informatics Engineering, University of Coimbra, Portugal – name: 5 The Portuguese Diabetes Association (APDP), 1250-203 Lisbon, Portugal – name: 4 Cardiothoracic Surgery Unit at the Coimbra University Hospital Centre, Praceta Prof. Mota Pinto, 3000-075 Coimbra, Portugal |
| Author_xml | – sequence: 1 givenname: A. surname: Burgeiro fullname: Burgeiro, A. organization: Center of Neuroscience and Cell Biology, University of Coimbra, 3004-504 Coimbra, Portugal – sequence: 2 givenname: A.C. surname: Fonseca fullname: Fonseca, A.C. organization: Center of Neuroscience and Cell Biology, University of Coimbra, 3004-504 Coimbra, Portugal – sequence: 3 givenname: D. surname: Espinoza fullname: Espinoza, D. organization: Center of Neuroscience and Cell Biology, University of Coimbra, 3004-504 Coimbra, Portugal – sequence: 4 givenname: L. surname: Carvalho fullname: Carvalho, L. organization: Institute of Pathology, Faculty of Medicine, University of Coimbra, 3004-517 Coimbra, Portugal – sequence: 5 givenname: N. surname: Lourenço fullname: Lourenço, N. organization: Centre for Informatics and Systems of the University of Coimbra (CISUC), Department of Informatics Engineering, University of Coimbra, Portugal – sequence: 6 givenname: M. surname: Antunes fullname: Antunes, M. organization: Cardiothoracic Surgery Unit at the Coimbra University Hospital Centre, Praceta Prof. Mota Pinto, 3000-075 Coimbra, Portugal – sequence: 7 givenname: E. surname: Carvalho fullname: Carvalho, E. email: ecarvalh@cnc.uc.pt organization: Center of Neuroscience and Cell Biology, University of Coimbra, 3004-504 Coimbra, Portugal |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29625179$$D View this record in MEDLINE/PubMed |
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| Keywords | Bcl-2 FFA BECN1 GRP SAT LVEF DM PERK Autophagy Epicardial adipose tissue Endoplasmic reticulum stress GADD153 NDM UPR mTOR CHOP LC3 BMI NYHA Heart failure Lamp2 MS Bim CAD ECF ER PVDF p62 ECL CVD ERAD CCS PINK1 AT IRE1α AMPK EAT ULK1 NCAD mTORC1 HF LVSF Apoptosis |
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| Notes | ObjectType-Article-2 SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 23 Contribution of each author: MA provided samples. AB, ACF, DE and EC collected samples. AB, ACF and DE performed experiments. LC performed histochemical analyses. NL performed statistical analyses. ACF prepared figures. AB and ACF drafted manuscript. AB, ACF and EC edited and revised manuscript. AB, ACF and EC designed research. AB, ACF, DE, LC, NL, MA and EC approved final version of the manuscript. |
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| SubjectTerms | Aged Apoptosis Autophagy Biomarkers Diabetes Mellitus - metabolism Diabetes Mellitus - pathology Diabetic Cardiomyopathies - diagnosis Diabetic Cardiomyopathies - metabolism Diabetic Cardiomyopathies - pathology Endoplasmic Reticulum - pathology Endoplasmic Reticulum Stress Epicardial adipose tissue Female Heart failure Heart Failure - diagnosis Heart Failure - metabolism Heart Failure - pathology Humans Male Myocytes, Cardiac - pathology Pericardium - cytology Pericardium - metabolism Pericardium - pathology Proteostasis Subcutaneous Fat - cytology Subcutaneous Fat - metabolism Unfolded Protein Response |
| Title | Proteostasis in epicardial versus subcutaneous adipose tissue in heart failure subjects with and without diabetes |
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