Journal Article

Adipose tissue and skeletal muscle insulin-mediated glucose uptake in insulin resistance: role of blood flow and diabetes

Ele Ferrannini, Patricia Iozzo, Kirsi A Virtanen, Miikka-Juhani Honka, Marco Bucci and Pirjo Nuutila

in The American Journal of Clinical Nutrition

Published on behalf of American Society for Nutrition

Volume 108, issue 4, pages 749-758
Published in print October 2018 | ISSN: 0002-9165
Published online September 2018 | e-ISSN: 1938-3207 | DOI: https://dx.doi.org/10.1093/ajcn/nqy162
Adipose tissue and skeletal muscle insulin-mediated glucose uptake in insulin resistance: role of blood flow and diabetes

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ABSTRACT

Background

Adipose tissue glucose uptake is impaired in insulin-resistant states, but ex vivo studies of human adipose tissue have yielded heterogeneous results. This discrepancy may be due to different regulation of blood supply.

Objective

The aim of this study was to test the flow dependency of in vivo insulin-mediated glucose uptake in fat tissues, and to contrast it with that of skeletal muscle.

Design

We reanalyzed data from 159 individuals in which adipose tissue depots—subcutaneous abdominal and femoral, and intraperitoneal—and femoral skeletal muscle were identified by MRI, and insulin-stimulated glucose uptake ([18F]-fluoro-2-deoxyglucose) and blood flow ([15O]-H2O) were measured simultaneously by positron emission tomography scanning.

Results

Individuals in the bottom tertile of whole-body glucose uptake [median (IQR) 36 (17) µmol. kg fat-free mass (kgFFM)−1 . min−1 .nM−1] displayed all features of insulin resistance compared with the rest of the group [median (IQR) 97 (71) µmol . kgFFM−1 .min−1 . nM−1]. Rates of glucose uptake were directly related to the degree of insulin resistance in all fat depots as well as in skeletal muscle. However, blood flow was inversely related to insulin sensitivity in each fat depot (all ≤ 0.03), whereas femoral muscle blood flow was not significantly different between insulin-resistant and insulin-sensitive subjects, and was not related to insulin sensitivity. Furthermore, in subjects performing one-leg exercise, blood flow increased 5- to 6-fold in femoral muscle but not in the overlying adipose tissue. The presence of diabetes was associated with a modest increase in fat and muscle glucose uptake independent of insulin resistance.

Conclusions

Reduced blood supply is an important factor for the impairment of in vivo insulin-mediated glucose uptake in both subcutaneous and visceral fat. In contrast, the insulin resistance of glucose uptake in resting skeletal muscle is predominantly a cellular defect. Diabetes provides a modest compensatory increase in fat and muscle glucose uptake that is independent of insulin resistance.

Keywords: fat glucose uptake; muscle glucose uptake; insulin resistance; tissue blood flow; one-leg exercise; adipose tissue physiology; whole-body integrated physiology

Journal Article.  7425 words.  Illustrated.

Subjects: Medicine and Health ; Dietetics and Nutrition ; Biochemistry ; Food Microbiology ; Gut Microbiology

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