Effects of high intensity interval training on neuro-cardiovascular dynamic changes and mitochondrial dysfunction induced by high-fat diet in rats

Silvio R Marques Neto; Raquel C Castiglione; Teresa C B da Silva; Lorena da S Paes; Aiza Pontes; Dahienne F Oliveira; Emanuelle B Ferraz; Carla Christina Ade Caldas; José Hamilton M Nascimento; Eliete Bouskela

doi:10.1371/journal.pone.0240060

Effects of high intensity interval training on neuro-cardiovascular dynamic changes and mitochondrial dysfunction induced by high-fat diet in rats

Silvio R Marques Neto^* (Corresponding Author), Raquel C Castiglione, Teresa C B da Silva, Lorena da S Paes, Aiza Pontes, Dahienne F Oliveira, Emanuelle B Ferraz, Carla Christina Ade Caldas, José Hamilton M Nascimento, Eliete Bouskela

^*Corresponding author for this work

The Rowett Institute of Nutrition and Health

Research output: Contribution to journal › Article › peer-review

3 Citations (Scopus)

4 Downloads (Pure)

Abstract

BACKGROUND AND AIMS: Mitochondrial swelling is involved in the pathogenesis of many human diseases associated with oxidative stress including obesity. One of the strategies for prevention of deleterious effects related to obesity and overweight is engaging in regular physical activity, of which high intensity interval training (HIIT) is efficient in promoting biogenesis and improving the function of mitochondria. Therefore, our aims were to investigate the effects of HIIT on metabolic and neuro-cardiovascular dynamic control and mitochondrial swelling induced by high-fat diet (HFD).

METHODS AND RESULTS: Twenty-three male Wistar rats (60 - 80g) were divided into 4 subgroups: control (C), HIIT, HFD and HFD+HIIT. The whole experimentation period lasted for 22 weeks and HIIT sessions were performed 5 days a week during the last 4 weeks. At the end of the experiments, fasting glucose and insulin tolerance tests were performed. Cerebral microcirculation was analyzed using cortical intravital microscopy for capillary diameter and functional density. Cardiac function and ergoespirometric parameters were also investigated. Mitochondrial swelling was evaluated on brain and heart extracts. HFD promoted an increase on body adiposity (p<0.001), fasting glucose levels (p<0.001), insulin resistance index (p<0.05), cardiac hypertrophy index (p<0.05) and diastolic blood pressure (p<0.05), along with worsened cardiac function (p<0.05), reduced functional cerebral capillary density (p<0.05) and its diameter (p<0.01), and heart and brain mitochondrial function (p<0.001). HFD did not affect any ergoespirometric parameter. After 4 weeks of training, HIIT was able to improve cardiac hypertrophy index, diastolic blood pressure, cerebral functional capillary density (p<0.01) and heart and brain mitochondrial swelling (p<0.001).

CONCLUSION: In animals subjected to HFD, HIIT ameliorated both cerebral mitochondrial swelling and functional capillary density, but it did not improve cardiovascular function suggesting that the cardiovascular dysfunction elicited by HFD was not due to heart mitochondrial swelling.

Original language	English
Article number	e0240060
Number of pages	17
Journal	PloS ONE
Volume	15
Issue number	10
DOIs	https://doi.org/10.1371/journal.pone.0240060
Publication status	Published - 23 Oct 2020

Bibliographical note

This research was supported by the Brazilian National Council for Scientific and Technologic Development (CNPq) (Grant number: 474116/2008-5) and Carlos Chagas Filho Foundation for Research Support in the State of Rio de Janeiro (FAPERJ) (Grant number: E-26/ 111.732/2011), both received by Eliete Bouskela. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Data Availability Statement

All relevant data are within the paper.

Keywords

Adiposity
Animals
Blood Glucose/analysis
Blood Pressure
Cardiovascular System/pathology
Diet, High-Fat
Glucose Tolerance Test
Hemodynamics
Hypertrophy/pathology
Insulin Resistance
Male
Microcirculation
Mitochondria/physiology
Obesity/metabolism
Physical Conditioning, Animal
Rats
Rats, Wistar

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1371/journal.pone.0240060Licence: CC BY

Neto_etal_Plos_effects_of_high_VOR
this is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.https://creativecommons.org/licenses/by/4.0/
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Cite this

Marques Neto, S. R., Castiglione, R. C., da Silva, T. C. B., Paes, L. D. S., Pontes, A., Oliveira, D. F., Ferraz, E. B., Ade Caldas, C. C., Nascimento, J. H. M., & Bouskela, E. (2020). Effects of high intensity interval training on neuro-cardiovascular dynamic changes and mitochondrial dysfunction induced by high-fat diet in rats. PloS ONE, 15(10), Article e0240060. https://doi.org/10.1371/journal.pone.0240060

Marques Neto, SR, Castiglione, RC, da Silva, TCB, Paes, LDS, Pontes, A, Oliveira, DF, Ferraz, EB, Ade Caldas, CC, Nascimento, JHM & Bouskela, E 2020, 'Effects of high intensity interval training on neuro-cardiovascular dynamic changes and mitochondrial dysfunction induced by high-fat diet in rats', PloS ONE, vol. 15, no. 10, e0240060. https://doi.org/10.1371/journal.pone.0240060

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title = "Effects of high intensity interval training on neuro-cardiovascular dynamic changes and mitochondrial dysfunction induced by high-fat diet in rats",

abstract = "BACKGROUND AND AIMS: Mitochondrial swelling is involved in the pathogenesis of many human diseases associated with oxidative stress including obesity. One of the strategies for prevention of deleterious effects related to obesity and overweight is engaging in regular physical activity, of which high intensity interval training (HIIT) is efficient in promoting biogenesis and improving the function of mitochondria. Therefore, our aims were to investigate the effects of HIIT on metabolic and neuro-cardiovascular dynamic control and mitochondrial swelling induced by high-fat diet (HFD).METHODS AND RESULTS: Twenty-three male Wistar rats (60 - 80g) were divided into 4 subgroups: control (C), HIIT, HFD and HFD+HIIT. The whole experimentation period lasted for 22 weeks and HIIT sessions were performed 5 days a week during the last 4 weeks. At the end of the experiments, fasting glucose and insulin tolerance tests were performed. Cerebral microcirculation was analyzed using cortical intravital microscopy for capillary diameter and functional density. Cardiac function and ergoespirometric parameters were also investigated. Mitochondrial swelling was evaluated on brain and heart extracts. HFD promoted an increase on body adiposity (p<0.001), fasting glucose levels (p<0.001), insulin resistance index (p<0.05), cardiac hypertrophy index (p<0.05) and diastolic blood pressure (p<0.05), along with worsened cardiac function (p<0.05), reduced functional cerebral capillary density (p<0.05) and its diameter (p<0.01), and heart and brain mitochondrial function (p<0.001). HFD did not affect any ergoespirometric parameter. After 4 weeks of training, HIIT was able to improve cardiac hypertrophy index, diastolic blood pressure, cerebral functional capillary density (p<0.01) and heart and brain mitochondrial swelling (p<0.001).CONCLUSION: In animals subjected to HFD, HIIT ameliorated both cerebral mitochondrial swelling and functional capillary density, but it did not improve cardiovascular function suggesting that the cardiovascular dysfunction elicited by HFD was not due to heart mitochondrial swelling.",

keywords = "Adiposity, Animals, Blood Glucose/analysis, Blood Pressure, Cardiovascular System/pathology, Diet, High-Fat, Glucose Tolerance Test, Hemodynamics, Hypertrophy/pathology, Insulin Resistance, Male, Microcirculation, Mitochondria/physiology, Obesity/metabolism, Physical Conditioning, Animal, Rats, Rats, Wistar",

author = "{Marques Neto}, {Silvio R} and Castiglione, {Raquel C} and {da Silva}, {Teresa C B} and Paes, {Lorena da S} and Aiza Pontes and Oliveira, {Dahienne F} and Ferraz, {Emanuelle B} and {Ade Caldas}, {Carla Christina} and Nascimento, {Jos{\'e} Hamilton M} and Eliete Bouskela",

note = "This research was supported by the Brazilian National Council for Scientific and Technologic Development (CNPq) (Grant number: 474116/2008-5) and Carlos Chagas Filho Foundation for Research Support in the State of Rio de Janeiro (FAPERJ) (Grant number: E-26/ 111.732/2011), both received by Eliete Bouskela. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.",

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doi = "10.1371/journal.pone.0240060",

language = "English",

volume = "15",

journal = "PloS ONE",

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TY - JOUR

T1 - Effects of high intensity interval training on neuro-cardiovascular dynamic changes and mitochondrial dysfunction induced by high-fat diet in rats

AU - Marques Neto, Silvio R

AU - Castiglione, Raquel C

AU - da Silva, Teresa C B

AU - Paes, Lorena da S

AU - Pontes, Aiza

AU - Oliveira, Dahienne F

AU - Ferraz, Emanuelle B

AU - Ade Caldas, Carla Christina

AU - Nascimento, José Hamilton M

AU - Bouskela, Eliete

N1 - This research was supported by the Brazilian National Council for Scientific and Technologic Development (CNPq) (Grant number: 474116/2008-5) and Carlos Chagas Filho Foundation for Research Support in the State of Rio de Janeiro (FAPERJ) (Grant number: E-26/ 111.732/2011), both received by Eliete Bouskela. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

PY - 2020/10/23

Y1 - 2020/10/23

N2 - BACKGROUND AND AIMS: Mitochondrial swelling is involved in the pathogenesis of many human diseases associated with oxidative stress including obesity. One of the strategies for prevention of deleterious effects related to obesity and overweight is engaging in regular physical activity, of which high intensity interval training (HIIT) is efficient in promoting biogenesis and improving the function of mitochondria. Therefore, our aims were to investigate the effects of HIIT on metabolic and neuro-cardiovascular dynamic control and mitochondrial swelling induced by high-fat diet (HFD).METHODS AND RESULTS: Twenty-three male Wistar rats (60 - 80g) were divided into 4 subgroups: control (C), HIIT, HFD and HFD+HIIT. The whole experimentation period lasted for 22 weeks and HIIT sessions were performed 5 days a week during the last 4 weeks. At the end of the experiments, fasting glucose and insulin tolerance tests were performed. Cerebral microcirculation was analyzed using cortical intravital microscopy for capillary diameter and functional density. Cardiac function and ergoespirometric parameters were also investigated. Mitochondrial swelling was evaluated on brain and heart extracts. HFD promoted an increase on body adiposity (p<0.001), fasting glucose levels (p<0.001), insulin resistance index (p<0.05), cardiac hypertrophy index (p<0.05) and diastolic blood pressure (p<0.05), along with worsened cardiac function (p<0.05), reduced functional cerebral capillary density (p<0.05) and its diameter (p<0.01), and heart and brain mitochondrial function (p<0.001). HFD did not affect any ergoespirometric parameter. After 4 weeks of training, HIIT was able to improve cardiac hypertrophy index, diastolic blood pressure, cerebral functional capillary density (p<0.01) and heart and brain mitochondrial swelling (p<0.001).CONCLUSION: In animals subjected to HFD, HIIT ameliorated both cerebral mitochondrial swelling and functional capillary density, but it did not improve cardiovascular function suggesting that the cardiovascular dysfunction elicited by HFD was not due to heart mitochondrial swelling.

AB - BACKGROUND AND AIMS: Mitochondrial swelling is involved in the pathogenesis of many human diseases associated with oxidative stress including obesity. One of the strategies for prevention of deleterious effects related to obesity and overweight is engaging in regular physical activity, of which high intensity interval training (HIIT) is efficient in promoting biogenesis and improving the function of mitochondria. Therefore, our aims were to investigate the effects of HIIT on metabolic and neuro-cardiovascular dynamic control and mitochondrial swelling induced by high-fat diet (HFD).METHODS AND RESULTS: Twenty-three male Wistar rats (60 - 80g) were divided into 4 subgroups: control (C), HIIT, HFD and HFD+HIIT. The whole experimentation period lasted for 22 weeks and HIIT sessions were performed 5 days a week during the last 4 weeks. At the end of the experiments, fasting glucose and insulin tolerance tests were performed. Cerebral microcirculation was analyzed using cortical intravital microscopy for capillary diameter and functional density. Cardiac function and ergoespirometric parameters were also investigated. Mitochondrial swelling was evaluated on brain and heart extracts. HFD promoted an increase on body adiposity (p<0.001), fasting glucose levels (p<0.001), insulin resistance index (p<0.05), cardiac hypertrophy index (p<0.05) and diastolic blood pressure (p<0.05), along with worsened cardiac function (p<0.05), reduced functional cerebral capillary density (p<0.05) and its diameter (p<0.01), and heart and brain mitochondrial function (p<0.001). HFD did not affect any ergoespirometric parameter. After 4 weeks of training, HIIT was able to improve cardiac hypertrophy index, diastolic blood pressure, cerebral functional capillary density (p<0.01) and heart and brain mitochondrial swelling (p<0.001).CONCLUSION: In animals subjected to HFD, HIIT ameliorated both cerebral mitochondrial swelling and functional capillary density, but it did not improve cardiovascular function suggesting that the cardiovascular dysfunction elicited by HFD was not due to heart mitochondrial swelling.

KW - Adiposity

KW - Animals

KW - Blood Glucose/analysis

KW - Blood Pressure

KW - Cardiovascular System/pathology

KW - Diet, High-Fat

KW - Glucose Tolerance Test

KW - Hemodynamics

KW - Hypertrophy/pathology

KW - Insulin Resistance

KW - Male

KW - Microcirculation

KW - Mitochondria/physiology

KW - Obesity/metabolism

KW - Physical Conditioning, Animal

KW - Rats

KW - Rats, Wistar

U2 - 10.1371/journal.pone.0240060

DO - 10.1371/journal.pone.0240060

M3 - Article

C2 - 33095799

SN - 1932-6203

VL - 15

JO - PloS ONE

JF - PloS ONE

IS - 10

M1 - e0240060

ER -

Effects of high intensity interval training on neuro-cardiovascular dynamic changes and mitochondrial dysfunction induced by high-fat diet in rats

Abstract

Bibliographical note

Data Availability Statement

Keywords

UN SDGs

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