High-Carbohydrate Diet Enhanced the Anticontractile Effect of Perivascular Adipose Tissue Through Activation of Renin-Angiotensin System
The perivascular adipose tissue (PVAT) is an active endocrine organ responsible for release several substances that influence on vascular tone. Increasing evidence suggest that hyperactivation of the local renin-angiotensin system (RAS) in the PVAT plays a pivotal role in the pathogenesis of cardiom...
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Frontiers Media S.A.
2021-01-01
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| Series: | Frontiers in Physiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fphys.2020.628101/full |
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| author | Daniela Esteves Ferreira dos Reis Costa Ana Letícia Malheiros Silveira Gianne Paul Campos Natália Ribeiro Cabacinha Nóbrega Natália Ferreira de Araújo Luciano de Figueiredo Borges Luciano dos Santos Aggum Capettini Adaliene Versiani Matos Ferreira Adaliene Versiani Matos Ferreira Daniella Bonaventura |
| author_facet | Daniela Esteves Ferreira dos Reis Costa Ana Letícia Malheiros Silveira Gianne Paul Campos Natália Ribeiro Cabacinha Nóbrega Natália Ferreira de Araújo Luciano de Figueiredo Borges Luciano dos Santos Aggum Capettini Adaliene Versiani Matos Ferreira Adaliene Versiani Matos Ferreira Daniella Bonaventura |
| author_sort | Daniela Esteves Ferreira dos Reis Costa |
| collection | DOAJ |
| description | The perivascular adipose tissue (PVAT) is an active endocrine organ responsible for release several substances that influence on vascular tone. Increasing evidence suggest that hyperactivation of the local renin-angiotensin system (RAS) in the PVAT plays a pivotal role in the pathogenesis of cardiometabolic diseases. However, the local RAS contribution to the PVAT control of vascular tone during obesity is still not clear. Since the consumption of a high-carbohydrate diet (HC diet) contributes to obesity inducing a rapid and sustained increase in adiposity, so that the functional activity of PVAT could be modulated, we aimed to evaluate the effect of HC diet on the PVAT control of vascular tone and verify the involvement of RAS in this effect. For that, male Balb/c mice were fed standard or HC diet for 4 weeks. Vascular reactivity, histology, fluorescence, and immunofluorescence analysis were performed in intact thoracic aorta in the presence or absence of PVAT. The results showed that HC diet caused an increase in visceral adiposity and also in the PVAT area. Phenylephrine-induced vasoconstriction was significantly reduced in the HC group only in the presence of PVAT. The anticontractile effect of PVAT induced by HC diet was lost when aortic rings were previously incubated with angiotensin-converting enzyme inhibitor, Mas, and AT2 receptors antagonists, PI3K, nNOS, and iNOS inhibitors, hydrogen peroxide (H2O2) decomposing enzyme or non-selective potassium channels blocker. Immunofluorescence assays showed that both Mas and AT2 receptors as well as nNOS and iNOS isoforms were markedly expressed in the PVAT of the HC group. Furthermore, the PVAT from HC group also exhibited higher nitric oxide (NO) and hydrogen peroxide bioavailability. Taken together, these findings suggest that the anticontractile effect of PVAT induced by HC diet involves the signaling cascade triggered by the renin-angiotensin system through the activation of Mas and AT2 receptors, PI3K, nNOS, and iNOS, leading to increased production of nitric oxide and hydrogen peroxide, and subsequently opening of potassium channels. The contribution of PVAT during HC diet-induced obesity could be a compensatory adaptive characteristic in order to preserve the vascular function. |
| first_indexed | 2024-12-20T13:04:43Z |
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| id | doaj.art-5d0fb7b90f4e4625966fd3ef5b19bd55 |
| institution | Directory Open Access Journal |
| issn | 1664-042X |
| language | English |
| last_indexed | 2024-12-20T13:04:43Z |
| publishDate | 2021-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Physiology |
| spelling | doaj.art-5d0fb7b90f4e4625966fd3ef5b19bd552022-12-21T19:39:48ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2021-01-011110.3389/fphys.2020.628101628101High-Carbohydrate Diet Enhanced the Anticontractile Effect of Perivascular Adipose Tissue Through Activation of Renin-Angiotensin SystemDaniela Esteves Ferreira dos Reis Costa0Ana Letícia Malheiros Silveira1Gianne Paul Campos2Natália Ribeiro Cabacinha Nóbrega3Natália Ferreira de Araújo4Luciano de Figueiredo Borges5Luciano dos Santos Aggum Capettini6Adaliene Versiani Matos Ferreira7Adaliene Versiani Matos Ferreira8Daniella Bonaventura9Department of Pharmacology, Biological Sciences Institute, Federal University of Minas Gerais, Belo Horizonte, BrazilDepartment of Biochemistry and Immunology, Biological Sciences Institute, Federal University of Minas Gerais, Belo Horizonte, BrazilDepartment of Pharmacology, Biological Sciences Institute, Federal University of Minas Gerais, Belo Horizonte, BrazilDepartment of Pharmacology, Biological Sciences Institute, Federal University of Minas Gerais, Belo Horizonte, BrazilDepartment of Pharmacology, Biological Sciences Institute, Federal University of Minas Gerais, Belo Horizonte, BrazilDepartment of Biological Sciences, Morphophysiology & Pathology Sector, Federal University of São Paulo, São Paulo, BrazilDepartment of Pharmacology, Biological Sciences Institute, Federal University of Minas Gerais, Belo Horizonte, BrazilDepartment of Biochemistry and Immunology, Biological Sciences Institute, Federal University of Minas Gerais, Belo Horizonte, BrazilDepartment of Nutrition, Nursing School, Federal University of Minas Gerais, Belo Horizonte, BrazilDepartment of Pharmacology, Biological Sciences Institute, Federal University of Minas Gerais, Belo Horizonte, BrazilThe perivascular adipose tissue (PVAT) is an active endocrine organ responsible for release several substances that influence on vascular tone. Increasing evidence suggest that hyperactivation of the local renin-angiotensin system (RAS) in the PVAT plays a pivotal role in the pathogenesis of cardiometabolic diseases. However, the local RAS contribution to the PVAT control of vascular tone during obesity is still not clear. Since the consumption of a high-carbohydrate diet (HC diet) contributes to obesity inducing a rapid and sustained increase in adiposity, so that the functional activity of PVAT could be modulated, we aimed to evaluate the effect of HC diet on the PVAT control of vascular tone and verify the involvement of RAS in this effect. For that, male Balb/c mice were fed standard or HC diet for 4 weeks. Vascular reactivity, histology, fluorescence, and immunofluorescence analysis were performed in intact thoracic aorta in the presence or absence of PVAT. The results showed that HC diet caused an increase in visceral adiposity and also in the PVAT area. Phenylephrine-induced vasoconstriction was significantly reduced in the HC group only in the presence of PVAT. The anticontractile effect of PVAT induced by HC diet was lost when aortic rings were previously incubated with angiotensin-converting enzyme inhibitor, Mas, and AT2 receptors antagonists, PI3K, nNOS, and iNOS inhibitors, hydrogen peroxide (H2O2) decomposing enzyme or non-selective potassium channels blocker. Immunofluorescence assays showed that both Mas and AT2 receptors as well as nNOS and iNOS isoforms were markedly expressed in the PVAT of the HC group. Furthermore, the PVAT from HC group also exhibited higher nitric oxide (NO) and hydrogen peroxide bioavailability. Taken together, these findings suggest that the anticontractile effect of PVAT induced by HC diet involves the signaling cascade triggered by the renin-angiotensin system through the activation of Mas and AT2 receptors, PI3K, nNOS, and iNOS, leading to increased production of nitric oxide and hydrogen peroxide, and subsequently opening of potassium channels. The contribution of PVAT during HC diet-induced obesity could be a compensatory adaptive characteristic in order to preserve the vascular function.https://www.frontiersin.org/articles/10.3389/fphys.2020.628101/fullPVATobesityhigh-carbohydrate dietrenin-angiotensin systemnitric oxidehydrogen peroxide |
| spellingShingle | Daniela Esteves Ferreira dos Reis Costa Ana Letícia Malheiros Silveira Gianne Paul Campos Natália Ribeiro Cabacinha Nóbrega Natália Ferreira de Araújo Luciano de Figueiredo Borges Luciano dos Santos Aggum Capettini Adaliene Versiani Matos Ferreira Adaliene Versiani Matos Ferreira Daniella Bonaventura High-Carbohydrate Diet Enhanced the Anticontractile Effect of Perivascular Adipose Tissue Through Activation of Renin-Angiotensin System Frontiers in Physiology PVAT obesity high-carbohydrate diet renin-angiotensin system nitric oxide hydrogen peroxide |
| title | High-Carbohydrate Diet Enhanced the Anticontractile Effect of Perivascular Adipose Tissue Through Activation of Renin-Angiotensin System |
| title_full | High-Carbohydrate Diet Enhanced the Anticontractile Effect of Perivascular Adipose Tissue Through Activation of Renin-Angiotensin System |
| title_fullStr | High-Carbohydrate Diet Enhanced the Anticontractile Effect of Perivascular Adipose Tissue Through Activation of Renin-Angiotensin System |
| title_full_unstemmed | High-Carbohydrate Diet Enhanced the Anticontractile Effect of Perivascular Adipose Tissue Through Activation of Renin-Angiotensin System |
| title_short | High-Carbohydrate Diet Enhanced the Anticontractile Effect of Perivascular Adipose Tissue Through Activation of Renin-Angiotensin System |
| title_sort | high carbohydrate diet enhanced the anticontractile effect of perivascular adipose tissue through activation of renin angiotensin system |
| topic | PVAT obesity high-carbohydrate diet renin-angiotensin system nitric oxide hydrogen peroxide |
| url | https://www.frontiersin.org/articles/10.3389/fphys.2020.628101/full |
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