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Gastric Plication Improves Glycemia Partly by Restoring the Altered Expression of Aquaglyceroporins in Adipose Tissue and the Liver in Obese Rats

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Abstract

Background

Gastric plication is a minimally invasive bariatric surgical procedure, where the greater curvature is plicated inside the gastric lumen. Our aims were to analyze the effectiveness of gastric plication on the resolution of obesity, impaired glucose tolerance, and fatty liver in an experimental model of diet-induced obesity (DIO) and to evaluate changes in glycerol metabolism, a key substrate for adiposity and gluconeogenesis, in adipose tissue and the liver.

Methods

Male Wistar DIO rats (n = 58) were subjected to surgical (sham operation and gastric plication) or dietary interventions [fed a normal diet (ND) or high-fat diet (HFD) or pair-fed to the amount of food eaten by gastric-plicated animals]. The expression of aquaglyceroporins (AQPs) in epididymal (EWAT) and subcutaneous (SCWAT) fat and the liver was analyzed by real-time PCR and Western blot.

Results

Gastric plication did not result in a significant weight loss in DIO rats, showing a modest reduction in whole-body adiposity and hepatic steatosis. However, gastric-plicated animals exhibited an improvement in basal glycemia and glucose clearance, without changes in hepatic gluconeogenic genes. DIO was associated with an increase in glycerol, higher AQP3 and AQP7 in EWAT and SCWAT, and a decrease in hepatic AQP9. Gastric plication downregulated AQP3 in both fat depots without changes in adipose AQP7 and hepatic AQP9.

Conclusion

Gastric plication results in a modest reduction in adiposity and hepatosteatosis but restores glycemia by downregulating AQP3, which entails lower efflux of glycerol from fat, lower plasma glycerol availability, and a reduced use of glycerol as a substrate for hepatic gluconeogenesis.

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Abbreviations

Adipo-IR:

Adipocyte insulin resistance index

AQP:

Aquaporin

CSA:

Cell surface area

DIO:

Diet-induced obesity

EWAT:

Epididymal white adipose tissue

EWL:

Excess weight loss

FFA:

Free fatty acids

GK:

Glycerol kinase

HFD:

High-fat diet

HOMA:

Homeostasis model assessment

NAFLD:

Non-alcoholic fatty liver disease

ND:

Normal diet

PCK1:

Phosphoenolpyruvate carboxykinase 1

PPARγ:

Peroxisome proliferator activator receptor γ

PRWAT:

Perirenal white adipose tissue

QUICKI:

Quantitative insulin sensitivity check index

SCWAT:

Subcutaneous white adipose tissue

SREBF1:

Sterol regulatory element-binding factor 1

TG:

Triacylglycerol

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Acknowledgements

We gratefully acknowledge the valuable collaboration of all the staff of the breeding house of the University of Navarra.

Author information

Authors and Affiliations

  1. Metabolic Research Laboratory, Clínica Universidad de Navarra, IdiSNA, Irunlarrea 1, 31008, Pamplona, Spain

    Leire Méndez-Giménez, Sara Becerril, Beatriz Ramírez, Victoria Catalán, Javier Gómez-Ambrosi, Amaia Rodríguez & Gema Frühbeck

  2. CIBER Fisiopatología de la Obesidad y Nutrición (CIBEROBN), Instituto de Salud Carlos III, Madrid, Spain

    Leire Méndez-Giménez, Sara Becerril, Rafael Moncada, Víctor Valentí, Secundino Fernández, Beatriz Ramírez, Victoria Catalán, Javier Gómez-Ambrosi, María M. Malagón, Carlos Diéguez, Amaia Rodríguez & Gema Frühbeck

  3. Department of Anesthesia, Clínica Universidad de Navarra, IdiSNA, Pamplona, Spain

    Rafael Moncada

  4. Department of Surgery, Clínica Universidad de Navarra, IdiSNA, Pamplona, Spain

    Víctor Valentí

  5. Department of Otorhinolaryngology, Clínica Universidad de Navarra, IdiSNA, Pamplona, Spain

    Secundino Fernández

  6. Research Institute for Medicines (iMed.ULisboa), Faculty of Pharmacy, Universidade de Lisboa, Lisbon, Portugal

    Graça Soveral

  7. Department of Cell Biology, Physiology, and Immunology, Instituto Maimónides de Investigación Biomédica (IMIBIC)/Reina Sofia University Hospital/University of Córdoba, Córdoba, Spain

    María M. Malagón

  8. Department of Physiology, CIMUS, University of Santiago de Compostela-Instituto de Investigación Sanitaria, Santiago de Compostela, Spain

    Carlos Diéguez

  9. Department of Endocrinology and Nutrition, Clínica Universidad de Navarra, IdiSNA, Pamplona, Spain

    Gema Frühbeck

Authors
  1. Leire Méndez-Giménez
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  2. Sara Becerril
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  3. Rafael Moncada
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  4. Víctor Valentí
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  6. Beatriz Ramírez
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  7. Victoria Catalán
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  11. Carlos Diéguez
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  13. Gema Frühbeck
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Corresponding author

Correspondence to Amaia Rodríguez.

Ethics declarations

This article does not contain any studies with human participants.

All applicable institutional and national guidelines for the care and use of animals were followed. All experimental procedures conformed to the European guidelines for the care and use of laboratory animals (directive 2010/63/EU) and were approved by the Ethical Committee for Animal Experimentation of the University of Navarra (049/10).

Conflict of Interest

The authors declare that they have no conflict of interest.

Funding

This work was supported by Fondo de Investigación Sanitaria-FEDER (FIS PI13/01430 and PI16/01217) from the Instituto de Salud Carlos III, by the Department of Health of the Gobierno de Navarra (61/2014), and by the Plan de Investigación de la Universidad de Navarra (project PIUNA 2011-14). CIBEROBN is an initiative of the Instituto de Salud Carlos III, Spain.

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Méndez-Giménez, L., Becerril, S., Moncada, R. et al. Gastric Plication Improves Glycemia Partly by Restoring the Altered Expression of Aquaglyceroporins in Adipose Tissue and the Liver in Obese Rats. OBES SURG 27, 1763–1774 (2017). https://doi.org/10.1007/s11695-016-2532-2

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