Combined training increases thermogenic fat activity in patients with overweight and type 2 diabetes

Ivan Luiz Padilha Bonfante; Milena Monfort-Pires; Renata Garbellini Duft; Keryma Chaves da Silva Mateus; José Carlos de Lima Júnior; Joice Cristina dos Santos Trombeta; Enrico Antonio Rautenberg Finardi; Diego Trevisan Brunelli; Joseane Morari; Jéssica Aparecida Barbosa de Lima; Maria Luisa Bellotto; Thiago Matos Ferreira de Araújo; Celso Darío Ramos; Mara Patricia Traina Chacon-Mikahil; Licio Augusto Velloso; Cláudia Regina Cavaglieri

doi:10.1038/s41366-022-01086-3

Combined training increases thermogenic fat activity in patients with overweight and type 2 diabetes

Ivan Luiz Padilha Bonfante^* (Corresponding Author), Milena Monfort-Pires, Renata Garbellini Duft, Keryma Chaves da Silva Mateus, José Carlos de Lima Júnior, Joice Cristina dos Santos Trombeta, Enrico Antonio Rautenberg Finardi, Diego Trevisan Brunelli, Joseane Morari, Jéssica Aparecida Barbosa de Lima, Maria Luisa Bellotto, Thiago Matos Ferreira de Araújo, Celso Darío Ramos, Mara Patricia Traina Chacon-Mikahil, Licio Augusto Velloso, Cláudia Regina Cavaglieri^* (Corresponding Author)

^*Corresponding author for this work

The Rowett Institute of Nutrition and Health

University of Campinas

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

9 Citations (Scopus)

Abstract

Background
Exercise is an important strategy in the management of diabetes. Experimental studies have shown that exercise acts, at least in part, by inducing the production of myokines that improve metabolic control and activate brown/beige adipose tissue depots. Combined training (CT) is recommended by the major diabetes guidelines due to its metabolic and cardiovascular benefits, however, its impact on brown/beige adipose tissue activities has never been tested in humans with overweight and type 2 diabetes (T2D). Here, we evaluated the effects of 16-week combined training (CT) program on brown adipose tissue activity; browning and autophagy markers, and serum pro-thermogenic/inflammatory inducers in patients with overweight and T2D.

Methods
Thirty-four patients with overweight and T2D were assigned to either a control group (CG) or a combined training group (CTG) in a randomized and controlled study. Functional/fitness parameters, anthropometry/body composition parameters, blood hormone/biochemical parameters, thermogenic/autophagic gene expression in subcutaneous adipose tissue were evaluated before and at the end of the intervention. In addition, cold-induced 18-Fluoroxyglucose Positron Emission Computed Tomography (18F-FDG PET/CT) was performed in the training group before and after the end of the intervention.

Results
CT increased cervical/supraclavicular brown adipose tissue (BAT) thermogenic activity (p = 0.03) as well as in perirenal adipose tissue (p = 0.02). In addition, CT increased the expression of genes related to thermogenic profile (TMEM26: + 95%, p = 0.04; and EPSTI1: + 26%, p = 0.03) and decreased autophagic genes (ULK1: −15%, p = 0.04; LC3: −5%, p = 0.02; and ATG4: −22%, p < 0.001) in subcutaneous adipose tissue. There were positive correlations between Δ% BAT activity with Δ% of post training energy expenditure cold exposure, HDL-c, IL4, adiponectin, irisin, meteorin-like, and TMEM26 and ZIC1 genes, besides negative correlations with LDL-c, total cholesterol and C-reactive protein.

Conclusion
This is the first evidence of the beneficial actions of CT on adipose tissue thermogenic activity in humans, and it adds important support for the recommendation of CT as a strategy in the management of diabetes.

Original language	English
Pages (from-to)	1145-1154
Number of pages	9
Journal	International Journal of Obesity
Volume	46
Early online date	16 Feb 2022
DOIs	https://doi.org/10.1038/s41366-022-01086-3
Publication status	Published - Jun 2022

Bibliographical note

ILPB thank Luiz Carlos Bonfante (In memoriam). The authors thank the participants; Obesity and Comorbidities Research Center—University of Campinas; Clinics Hospital—University of Campinas; Faculty of Physical Education—University of Campinas; Nuclear Medicine and collaborators team of Clinics Hospital—University of Campinas; Integrated Teaching, Research and Extension Laboratory—School of Physical Education—University of Campinas; Bárbara J. Amorim, Sergio Brunetto, Edna Brunetto, Natália Tobar, Antonio Calixto and Marcela Reymond Simões for your contribution in technical support.

Data Availability Statement

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

UN SDGs

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

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Cite this

Bonfante, I. L. P., Monfort-Pires, M., Duft, R. G., Mateus, K. C. D. S., Júnior, J. C. D. L., Trombeta, J. C. D. S., Finardi, E. A. R., Brunelli, D. T., Morari, J., Lima, J. A. B. D., Bellotto, M. L., Araújo, T. M. F. D., Ramos, C. D., Chacon-Mikahil, M. P. T., Velloso, L. A., & Cavaglieri, C. R. (2022). Combined training increases thermogenic fat activity in patients with overweight and type 2 diabetes. International Journal of Obesity, 46, 1145-1154. https://doi.org/10.1038/s41366-022-01086-3

Bonfante, ILP, Monfort-Pires, M, Duft, RG, Mateus, KCDS, Júnior, JCDL, Trombeta, JCDS, Finardi, EAR, Brunelli, DT, Morari, J, Lima, JABD, Bellotto, ML, Araújo, TMFD, Ramos, CD, Chacon-Mikahil, MPT, Velloso, LA & Cavaglieri, CR 2022, 'Combined training increases thermogenic fat activity in patients with overweight and type 2 diabetes', International Journal of Obesity, vol. 46, pp. 1145-1154. https://doi.org/10.1038/s41366-022-01086-3

@article{2811bf1979b742d49bf6a451d0e4db3a,

title = "Combined training increases thermogenic fat activity in patients with overweight and type 2 diabetes",

abstract = "BackgroundExercise is an important strategy in the management of diabetes. Experimental studies have shown that exercise acts, at least in part, by inducing the production of myokines that improve metabolic control and activate brown/beige adipose tissue depots. Combined training (CT) is recommended by the major diabetes guidelines due to its metabolic and cardiovascular benefits, however, its impact on brown/beige adipose tissue activities has never been tested in humans with overweight and type 2 diabetes (T2D). Here, we evaluated the effects of 16-week combined training (CT) program on brown adipose tissue activity; browning and autophagy markers, and serum pro-thermogenic/inflammatory inducers in patients with overweight and T2D.MethodsThirty-four patients with overweight and T2D were assigned to either a control group (CG) or a combined training group (CTG) in a randomized and controlled study. Functional/fitness parameters, anthropometry/body composition parameters, blood hormone/biochemical parameters, thermogenic/autophagic gene expression in subcutaneous adipose tissue were evaluated before and at the end of the intervention. In addition, cold-induced 18-Fluoroxyglucose Positron Emission Computed Tomography (18F-FDG PET/CT) was performed in the training group before and after the end of the intervention.ResultsCT increased cervical/supraclavicular brown adipose tissue (BAT) thermogenic activity (p = 0.03) as well as in perirenal adipose tissue (p = 0.02). In addition, CT increased the expression of genes related to thermogenic profile (TMEM26: + 95%, p = 0.04; and EPSTI1: + 26%, p = 0.03) and decreased autophagic genes (ULK1: −15%, p = 0.04; LC3: −5%, p = 0.02; and ATG4: −22%, p < 0.001) in subcutaneous adipose tissue. There were positive correlations between Δ% BAT activity with Δ% of post training energy expenditure cold exposure, HDL-c, IL4, adiponectin, irisin, meteorin-like, and TMEM26 and ZIC1 genes, besides negative correlations with LDL-c, total cholesterol and C-reactive protein.ConclusionThis is the first evidence of the beneficial actions of CT on adipose tissue thermogenic activity in humans, and it adds important support for the recommendation of CT as a strategy in the management of diabetes.",

author = "Bonfante, {Ivan Luiz Padilha} and Milena Monfort-Pires and Duft, {Renata Garbellini} and Mateus, {Keryma Chaves da Silva} and J{\'u}nior, {Jos{\'e} Carlos de Lima} and Trombeta, {Joice Cristina dos Santos} and Finardi, {Enrico Antonio Rautenberg} and Brunelli, {Diego Trevisan} and Joseane Morari and Lima, {J{\'e}ssica Aparecida Barbosa de} and Bellotto, {Maria Luisa} and Ara{\'u}jo, {Thiago Matos Ferreira de} and Ramos, {Celso Dar{\'i}o} and Chacon-Mikahil, {Mara Patricia Traina} and Velloso, {Licio Augusto} and Cavaglieri, {Cl{\'a}udia Regina}",

note = "ILPB thank Luiz Carlos Bonfante (In memoriam). The authors thank the participants; Obesity and Comorbidities Research Center—University of Campinas; Clinics Hospital—University of Campinas; Faculty of Physical Education—University of Campinas; Nuclear Medicine and collaborators team of Clinics Hospital—University of Campinas; Integrated Teaching, Research and Extension Laboratory—School of Physical Education—University of Campinas; B{\'a}rbara J. Amorim, Sergio Brunetto, Edna Brunetto, Nat{\'a}lia Tobar, Antonio Calixto and Marcela Reymond Sim{\~o}es for your contribution in technical support. ",

year = "2022",

month = jun,

doi = "10.1038/s41366-022-01086-3",

language = "English",

volume = "46",

pages = "1145--1154",

journal = "International Journal of Obesity",

issn = "0307-0565",

publisher = "Nature Publishing Group",

}

TY - JOUR

T1 - Combined training increases thermogenic fat activity in patients with overweight and type 2 diabetes

AU - Bonfante, Ivan Luiz Padilha

AU - Monfort-Pires, Milena

AU - Duft, Renata Garbellini

AU - Mateus, Keryma Chaves da Silva

AU - Júnior, José Carlos de Lima

AU - Trombeta, Joice Cristina dos Santos

AU - Finardi, Enrico Antonio Rautenberg

AU - Brunelli, Diego Trevisan

AU - Morari, Joseane

AU - Lima, Jéssica Aparecida Barbosa de

AU - Bellotto, Maria Luisa

AU - Araújo, Thiago Matos Ferreira de

AU - Ramos, Celso Darío

AU - Chacon-Mikahil, Mara Patricia Traina

AU - Velloso, Licio Augusto

AU - Cavaglieri, Cláudia Regina

N1 - ILPB thank Luiz Carlos Bonfante (In memoriam). The authors thank the participants; Obesity and Comorbidities Research Center—University of Campinas; Clinics Hospital—University of Campinas; Faculty of Physical Education—University of Campinas; Nuclear Medicine and collaborators team of Clinics Hospital—University of Campinas; Integrated Teaching, Research and Extension Laboratory—School of Physical Education—University of Campinas; Bárbara J. Amorim, Sergio Brunetto, Edna Brunetto, Natália Tobar, Antonio Calixto and Marcela Reymond Simões for your contribution in technical support.

PY - 2022/6

Y1 - 2022/6

N2 - BackgroundExercise is an important strategy in the management of diabetes. Experimental studies have shown that exercise acts, at least in part, by inducing the production of myokines that improve metabolic control and activate brown/beige adipose tissue depots. Combined training (CT) is recommended by the major diabetes guidelines due to its metabolic and cardiovascular benefits, however, its impact on brown/beige adipose tissue activities has never been tested in humans with overweight and type 2 diabetes (T2D). Here, we evaluated the effects of 16-week combined training (CT) program on brown adipose tissue activity; browning and autophagy markers, and serum pro-thermogenic/inflammatory inducers in patients with overweight and T2D.MethodsThirty-four patients with overweight and T2D were assigned to either a control group (CG) or a combined training group (CTG) in a randomized and controlled study. Functional/fitness parameters, anthropometry/body composition parameters, blood hormone/biochemical parameters, thermogenic/autophagic gene expression in subcutaneous adipose tissue were evaluated before and at the end of the intervention. In addition, cold-induced 18-Fluoroxyglucose Positron Emission Computed Tomography (18F-FDG PET/CT) was performed in the training group before and after the end of the intervention.ResultsCT increased cervical/supraclavicular brown adipose tissue (BAT) thermogenic activity (p = 0.03) as well as in perirenal adipose tissue (p = 0.02). In addition, CT increased the expression of genes related to thermogenic profile (TMEM26: + 95%, p = 0.04; and EPSTI1: + 26%, p = 0.03) and decreased autophagic genes (ULK1: −15%, p = 0.04; LC3: −5%, p = 0.02; and ATG4: −22%, p < 0.001) in subcutaneous adipose tissue. There were positive correlations between Δ% BAT activity with Δ% of post training energy expenditure cold exposure, HDL-c, IL4, adiponectin, irisin, meteorin-like, and TMEM26 and ZIC1 genes, besides negative correlations with LDL-c, total cholesterol and C-reactive protein.ConclusionThis is the first evidence of the beneficial actions of CT on adipose tissue thermogenic activity in humans, and it adds important support for the recommendation of CT as a strategy in the management of diabetes.

AB - BackgroundExercise is an important strategy in the management of diabetes. Experimental studies have shown that exercise acts, at least in part, by inducing the production of myokines that improve metabolic control and activate brown/beige adipose tissue depots. Combined training (CT) is recommended by the major diabetes guidelines due to its metabolic and cardiovascular benefits, however, its impact on brown/beige adipose tissue activities has never been tested in humans with overweight and type 2 diabetes (T2D). Here, we evaluated the effects of 16-week combined training (CT) program on brown adipose tissue activity; browning and autophagy markers, and serum pro-thermogenic/inflammatory inducers in patients with overweight and T2D.MethodsThirty-four patients with overweight and T2D were assigned to either a control group (CG) or a combined training group (CTG) in a randomized and controlled study. Functional/fitness parameters, anthropometry/body composition parameters, blood hormone/biochemical parameters, thermogenic/autophagic gene expression in subcutaneous adipose tissue were evaluated before and at the end of the intervention. In addition, cold-induced 18-Fluoroxyglucose Positron Emission Computed Tomography (18F-FDG PET/CT) was performed in the training group before and after the end of the intervention.ResultsCT increased cervical/supraclavicular brown adipose tissue (BAT) thermogenic activity (p = 0.03) as well as in perirenal adipose tissue (p = 0.02). In addition, CT increased the expression of genes related to thermogenic profile (TMEM26: + 95%, p = 0.04; and EPSTI1: + 26%, p = 0.03) and decreased autophagic genes (ULK1: −15%, p = 0.04; LC3: −5%, p = 0.02; and ATG4: −22%, p < 0.001) in subcutaneous adipose tissue. There were positive correlations between Δ% BAT activity with Δ% of post training energy expenditure cold exposure, HDL-c, IL4, adiponectin, irisin, meteorin-like, and TMEM26 and ZIC1 genes, besides negative correlations with LDL-c, total cholesterol and C-reactive protein.ConclusionThis is the first evidence of the beneficial actions of CT on adipose tissue thermogenic activity in humans, and it adds important support for the recommendation of CT as a strategy in the management of diabetes.

U2 - 10.1038/s41366-022-01086-3

DO - 10.1038/s41366-022-01086-3

M3 - Article

SN - 0307-0565

VL - 46

SP - 1145

EP - 1154

JO - International Journal of Obesity

JF - International Journal of Obesity

ER -

Combined training increases thermogenic fat activity in patients with overweight and type 2 diabetes

Abstract

Bibliographical note

Data Availability Statement

UN SDGs

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