Association between skeletal muscle mass and serum concentrations of lipoprotein lipase, GPIHBP1, and hepatic triglyceride lipase in young Japanese men

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Abstract

Background

Two important regulators for circulating lipid metabolisms are lipoprotein lipase (LPL) and hepatic triglyceride lipase (HTGL). In relation to this, glycosylphosphatidylinositol anchored high-density lipoprotein binding protein 1 (GPIHBP1) has been shown to have a vital role in LPL lipolytic processing. However, the relationships between skeletal muscle mass and lipid metabolism, including LPL, GPIHBP1, and HTGL, remain to be elucidated. Demonstration of these relationships may lead to clarification of the metabolic dysfunctions caused by sarcopenia. In this study, these relationships were investigated in young Japanese men who had no age-related factors; participants included wrestling athletes with abundant skeletal muscle.

Methods

A total of 111 young Japanese men who were not taking medications were enrolled; 70 wrestling athletes and 41 control students were included. The participants’ body compositions, serum concentrations of lipoprotein, LPL, GPIHBP1 and HTGL and thyroid function test results were determined under conditions of no extreme dietary restrictions and exercises.

Results

Compared with the control participants, wrestling athletes had significantly higher skeletal muscle index (SMI) ( p < 0.001), higher serum concentrations of LPL ( p < 0.001) and GPIHBP1 ( p < 0.001), and lower fat mass index ( p = 0.024). Kruskal–Wallis tests with Bonferroni multiple comparison tests showed that serum LPL and GPIHBP1 concentrations were significantly higher in the participants with higher SMI. Spearman’s correlation analyses showed that SMI was positively correlated with LPL (ρ = 0.341, p < 0.001) and GPIHBP1 (ρ = 0.309, p = 0.001) concentration. The serum concentrations of LPL and GPIHBP1 were also inversely correlated with serum concentrations of triglyceride (LPL, ρ = − 0.198, p = 0.037; GPIHBP1, ρ = − 0.249, p = 0.008). Serum HTGL concentration was positively correlated with serum concentrations of total cholesterol (ρ = 0.308, p = 0.001), low-density lipoprotein-cholesterol (ρ = 0.336, p < 0.001), and free 3,5,3′-triiodothyronine (ρ = 0.260, p = 0.006), but not with SMI.

Conclusions

The results suggest that increased skeletal muscle mass leads to improvements in energy metabolism by promoting triglyceride-rich lipoprotein hydrolysis through the increase in circulating LPL and GPIHBP1.

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Most cited references 46

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Thyroid disease and lipids.

Leonidas H. Duntas (2002)

The composition and the transport of lipoproteins are seriously disturbed in thyroid diseases. Overt hypothyroidism is characterized by hypercholesterolaemia and a marked increase in low-density lipoproteins (LDL) and apolipoprotein B (apo A) because of a decreased fractional clearance of LDL by a reduced number of LDL receptors in the liver. The high-density lipoprotein (HDL) levels are normal or even elevated in severe hypothyroidism because of decreased activity of cholesteryl-ester transfer protein (CETP) and hepatic lipase (HL), which are enzymes regulated by thyroid hormones. The low activity of CETP, and more specifically of HL, results in reduced transport of cholesteryl esters from HDL(2) to very low-density lipoproteins (VLDL) and intermediate low-density lipoprotein (IDL), and reduced transport of HDL(2) to HDL(3). Moreover, hypothyroidism increases the oxidation of plasma cholesterol mainly because of an altered pattern of binding and to the increased levels of cholesterol, which presents a substrate for the oxidative stress. Cardiac oxygen consumption is reduced in hypothyroidism. This reduction is associated with increased peripheral resistance and reduced contractility. Hypothyroidism is often accompanied by diastolic hypertension that, in conjunction with the dyslipidemia, may promote atherosclerosis. However, thyroxine therapy, in a thyrotropin (TSH)-suppressive dose, usually leads to a considerable improvement of the lipid profile. The changes in lipoproteins are correlated with changes in free thyroxine (FT(4)) levels. Hyperthyroidism exhibits an enhanced excretion of cholesterol and an increased turnover of LDL resulting in a decrease of total and LDL cholesterol, whereas HDL are decreased or not affected. The action of thyroid hormone on Lp(a) lipoprotein is still debated, because both decrease or no changes have been reported. The discrepancies are mostly because of genetic polymorphism of apo(a) and to the differences between the various study groups. Subclinical hypothyroidism (SH) is associated with lipid disorders that are characterized by normal or slightly elevated total cholesterol levels, increased LDL, and lower HDL. Moreover, SH has been associated with endothelium dysfunction, aortic atherosclerosis, and myocardial infarction. Lipid disorders exhibit great individual variability. Nevertheless, they might be a link, although it has not been proved, between SH and atherosclerosis.

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Regional distribution of body fat, plasma lipoproteins, and cardiovascular disease

A. Tremblay, P J Lupien, A. Nadeau … (1990)

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The implications of sarcopenia and sarcopenic obesity on cardiometabolic disease.

Tae Kim, Kyung Mook Choi (2015)

The important changes in body composition associated with aging are a decline in skeletal muscle mass and an increase in body fat. Body fat distribution also changes with age; subcutaneous fat decreases and visceral abdominal fat increase, which contributes to numerous cardiometabolic diseases (CMDs) such as type 2 diabetes, dyslipidemia, and cardiovascular disease (CVD). Sarcopenia often accompanied by an increase in body fat and vice versa, a scenario termed sarcopenic obesity (SO), which might lead to the cumulative risk of both sarcopenia and obesity. However, there is still no consensus regarding the definition and consequences of SO. The lack of a unified definition for SO might contribute to inconsistent findings about the association of SO with CMD. Complex etiologies are associated with development of SO. A vicious cycle between the loss of muscle and the accumulation of ectopic fat might be associated with CMD via an intricate interplay of factors including proinflammatory cytokines, oxidative stress, mitochondrial dysfunction, insulin resistance, dietary energy, physical activity, mitochondrial dysfunction, and other factors that have yet to be identified. Moreover, recent epidemiological studies suggest that SO is related to CVD and mortality. This review focuses on the current literature with regard to the association between sarcopenia, dynapenia, and obesity, as well as their implications for CMD. The ultimate goal of this Prospects is to encourage conduct of well-designed future studies that elucidate the relationship among sarcopenia, SO, and CMD.

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Author and article information

Contributors

Katsuhiko Tsunekawa:

ORCID: http://orcid.org/0000-0002-6119-4158

ktsune@gunma-u.ac.jp

Journal

Journal ID (nlm-ta): Lipids Health Dis

Journal ID (iso-abbrev): Lipids Health Dis

Title: Lipids in Health and Disease

Publisher: BioMed Central (London )

ISSN (Electronic): 1476-511X

Publication date (Electronic): 4 April 2019

Publication date PMC-release: 4 April 2019

Publication date Collection: 2019

Volume: 18

Electronic Location Identifier: 84

Affiliations

[1 ]ISNI 0000 0000 9269 4097, GRID grid.256642.1, Department of Clinical Laboratory Medicine, , Gunma University Graduate School of Medicine, ; Maebashi, 371-8511 Japan

[2 ]Faculty of Education, Ikuei University, Takasaki, 370-0011 Japan

[3 ]School of Medical Technology, Faculty of Health Science, Gunma Paz University, Takasaki, 370-0006 Japan

[4 ]ISNI 0000 0001 2228 003X, GRID grid.412200.5, Graduate School of Health and Sport Science, , Nippon Sport Science University, ; Yokohama, 227-0033 Japan

Author information

Katsuhiko Tsunekawa http://orcid.org/0000-0002-6119-4158

Article

Publisher ID: 1014

DOI: 10.1186/s12944-019-1014-7

PMC ID: 6449999

PubMed ID: 30947712

SO-VID: 73dc9031-afbf-4385-810e-70985c8603f2

License:

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 8 February 2019

Date accepted : 8 March 2019

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ScienceOpen disciplines: Biochemistry

Keywords: skeletal muscle mass,lipoprotein lipase (lpl),glycosylphosphatidylinositol anchored high-density lipoprotein binding protein 1 (gpihbp1),hepatic triglyceride lipase (htgl),thyroid hormone

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ScienceOpen disciplines: Biochemistry

Keywords: skeletal muscle mass, lipoprotein lipase (lpl), glycosylphosphatidylinositol anchored high-density lipoprotein binding protein 1 (gpihbp1), hepatic triglyceride lipase (htgl), thyroid hormone

Association between skeletal muscle mass and serum concentrations of lipoprotein lipase, GPIHBP1, and hepatic triglyceride lipase in young Japanese men

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GLUT4 biology

Most cited references 46

Thyroid disease and lipids.

Regional distribution of body fat, plasma lipoproteins, and cardiovascular disease

The implications of sarcopenia and sarcopenic obesity on cardiometabolic disease.

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