Skip to main content
Top
Published in: Journal of Translational Medicine 1/2016

Open Access 01-12-2016 | Research

Effects of acute hypoxia on human adipose tissue lipoprotein lipase activity and lipolysis

Authors: Bimit Mahat, Étienne Chassé, Jean-François Mauger, Pascal Imbeault

Published in: Journal of Translational Medicine | Issue 1/2016

Login to get access

Abstract

Background

Adipose tissue regulates postprandial lipid metabolism by storing dietary fat through lipoprotein lipase-mediated hydrolysis of exogenous triglycerides, and by inhibiting delivery of endogenous non-esterified fatty acid to nonadipose tissues. Animal studies show that acute hypoxia, a model of obstructive sleep apnea, reduces adipose tissue lipoprotein lipase activity and increases non-esterified fatty acid release, adversely affecting postprandial lipemia. These observations remain to be tested in humans.

Methods

We used differentiated human preadipocytes exposed to acute hypoxia as well as adipose tissue biopsies obtained from 10 healthy men exposed for 6 h to either normoxia or intermittent hypoxia following an isocaloric high-fat meal.

Results

In differentiated preadipocytes, acute hypoxia induced a 6-fold reduction in lipoprotein lipase activity. In humans, the rise in postprandial triglyceride levels did not differ between normoxia and intermittent hypoxia. Non-esterified fatty acid levels were higher during intermittent hypoxia session. Intermittent hypoxia did not affect subcutaneous abdominal adipose tissue lipoprotein lipase activity. No differences were observed in lipolytic responses of isolated subcutaneous abdominal adipocytes between normoxia and intermittent hypoxia sessions.

Conclusions

Acute hypoxia strongly inhibits lipoprotein lipase activity in differentiated human preadipocytes. Acute intermittent hypoxia increases circulating plasma non-esterified fatty acid in young healthy men, but does not seem to affect postprandial triglyceride levels, nor subcutaneous abdominal adipose tissue lipoprotein lipase activity and adipocyte lipolysis.
Literature
1.
go back to reference Young T, Peppard PE, Gottlieb DJ. Epidemiology of obstructive sleep apnea: a population health perspective. Am J Respir Crit Care Med. 2002;165:1217–39.CrossRef Young T, Peppard PE, Gottlieb DJ. Epidemiology of obstructive sleep apnea: a population health perspective. Am J Respir Crit Care Med. 2002;165:1217–39.CrossRef
3.
go back to reference Newman AB, Nieto FJ, Guidry U, Lind BK, Redline S, Pickering TG, et al. Relation of sleep-disordered breathing to cardiovascular disease risk factors: the sleep heart health study. Am J Epidemiol. 2001;154:50–9.CrossRef Newman AB, Nieto FJ, Guidry U, Lind BK, Redline S, Pickering TG, et al. Relation of sleep-disordered breathing to cardiovascular disease risk factors: the sleep heart health study. Am J Epidemiol. 2001;154:50–9.CrossRef
4.
go back to reference Samra JS. Sir David Cuthbertson Medal Lecture. Regulation of lipid metabolism in adipose tissue. Proc Nutr Soc. 2000;59:441–6.CrossRef Samra JS. Sir David Cuthbertson Medal Lecture. Regulation of lipid metabolism in adipose tissue. Proc Nutr Soc. 2000;59:441–6.CrossRef
5.
go back to reference Coppack SW, Fisher RM, Gibbons GF, Humphreys SM, McDonough MJ, Potts JL, et al. Postprandial substrate deposition in human forearm and adipose tissues in vivo. Clin Sci Lond Engl. 1979;1990(79):339–48. Coppack SW, Fisher RM, Gibbons GF, Humphreys SM, McDonough MJ, Potts JL, et al. Postprandial substrate deposition in human forearm and adipose tissues in vivo. Clin Sci Lond Engl. 1979;1990(79):339–48.
7.
go back to reference McGarry JD. What if Minkowski had been ageusic? An alternative angle on diabetes. Science. 1992;258:766–70.CrossRef McGarry JD. What if Minkowski had been ageusic? An alternative angle on diabetes. Science. 1992;258:766–70.CrossRef
9.
go back to reference Drager LF, Li J, Shin M-K, Reinke C, Aggarwal NR, Jun JC, et al. Intermittent hypoxia inhibits clearance of triglyceride-rich lipoproteins and inactivates adipose lipoprotein lipase in a mouse model of sleep apnoea. Eur Heart J. 2012;33:783–90. doi:10.1093/eurheartj/ehr097.CrossRefPubMed Drager LF, Li J, Shin M-K, Reinke C, Aggarwal NR, Jun JC, et al. Intermittent hypoxia inhibits clearance of triglyceride-rich lipoproteins and inactivates adipose lipoprotein lipase in a mouse model of sleep apnoea. Eur Heart J. 2012;33:783–90. doi:10.​1093/​eurheartj/​ehr097.CrossRefPubMed
12.
go back to reference Wang B, Wood IS, Trayhurn P. Dysregulation of the expression and secretion of inflammation-related adipokines by hypoxia in human adipocytes. Pflüg Arch Eur J Physiol. 2007;455:479–92. doi:10.1007/s00424-007-0301-8.CrossRef Wang B, Wood IS, Trayhurn P. Dysregulation of the expression and secretion of inflammation-related adipokines by hypoxia in human adipocytes. Pflüg Arch Eur J Physiol. 2007;455:479–92. doi:10.​1007/​s00424-007-0301-8.CrossRef
13.
go back to reference Taskinen MR, Nikkilä EA, Huttunen JK, Hilden H. A micromethod for assay of lipoprotein lipase activity in needle biopsy samples of human adipose tissue and skeletal muscle. Clin Chim Acta Int J Clin Chem. 1980;104:107–17.CrossRef Taskinen MR, Nikkilä EA, Huttunen JK, Hilden H. A micromethod for assay of lipoprotein lipase activity in needle biopsy samples of human adipose tissue and skeletal muscle. Clin Chim Acta Int J Clin Chem. 1980;104:107–17.CrossRef
14.
go back to reference Imbeault P, Alméras N, Richard D, Després JP, Tremblay A, Mauriège P. Effect of a moderate weight loss on adipose tissue lipoprotein lipase activity and expression: existence of sexual variation and regional differences. Int J Obes Relat Metab Disord J Int Assoc Study Obes. 1999;23:957–65.CrossRef Imbeault P, Alméras N, Richard D, Després JP, Tremblay A, Mauriège P. Effect of a moderate weight loss on adipose tissue lipoprotein lipase activity and expression: existence of sexual variation and regional differences. Int J Obes Relat Metab Disord J Int Assoc Study Obes. 1999;23:957–65.CrossRef
15.
go back to reference Harris JA, Benedict FG. A biometric study of human basal metabolism. Proc Natl Acad Sci USA. 1918;4:370–3.CrossRef Harris JA, Benedict FG. A biometric study of human basal metabolism. Proc Natl Acad Sci USA. 1918;4:370–3.CrossRef
18.
go back to reference Mauriège P, Imbeault P, Langin D, Lacaille M, Alméras N, Tremblay A, et al. Regional and gender variations in adipose tissue lipolysis in response to weight loss. J Lipid Res. 1999;40:1559–71.CrossRef Mauriège P, Imbeault P, Langin D, Lacaille M, Alméras N, Tremblay A, et al. Regional and gender variations in adipose tissue lipolysis in response to weight loss. J Lipid Res. 1999;40:1559–71.CrossRef
19.
go back to reference Buysse DJ, Reynolds CF, Monk TH, Berman SR, Kupfer DJ. The Pittsburgh sleep quality index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989;28:193–213.CrossRef Buysse DJ, Reynolds CF, Monk TH, Berman SR, Kupfer DJ. The Pittsburgh sleep quality index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989;28:193–213.CrossRef
20.
go back to reference Makoveichuk E, Vorrsjö E, Olivecrona T, Olivecrona G. Inactivation of lipoprotein lipase in 3T3-L1 adipocytes by angiopoietin-like protein 4 requires that both proteins have reached the cell surface. Biochem Biophys Res Commun. 2013;441:941–6. doi:10.1016/j.bbrc.2013.11.013.CrossRefPubMed Makoveichuk E, Vorrsjö E, Olivecrona T, Olivecrona G. Inactivation of lipoprotein lipase in 3T3-L1 adipocytes by angiopoietin-like protein 4 requires that both proteins have reached the cell surface. Biochem Biophys Res Commun. 2013;441:941–6. doi:10.​1016/​j.​bbrc.​2013.​11.​013.CrossRefPubMed
21.
go back to reference Wood IS, Stezhka T, Trayhurn P. Modulation of adipokine production, glucose uptake and lactate release in human adipocytes by small changes in oxygen tension. Pflüg Arch Eur J Physiol. 2011;462:469–77. doi:10.1007/s00424-011-0985-7.CrossRef Wood IS, Stezhka T, Trayhurn P. Modulation of adipokine production, glucose uptake and lactate release in human adipocytes by small changes in oxygen tension. Pflüg Arch Eur J Physiol. 2011;462:469–77. doi:10.​1007/​s00424-011-0985-7.CrossRef
22.
23.
go back to reference Trzepizur W, Le Vaillant M, Meslier N, Pigeanne T, Masson P, Humeau MP, et al. Independent association between nocturnal intermittent hypoxemia and metabolic dyslipidemia. Chest. 2013;143:1584–9. doi:10.1378/chest.12-1652.CrossRefPubMed Trzepizur W, Le Vaillant M, Meslier N, Pigeanne T, Masson P, Humeau MP, et al. Independent association between nocturnal intermittent hypoxemia and metabolic dyslipidemia. Chest. 2013;143:1584–9. doi:10.​1378/​chest.​12-1652.CrossRefPubMed
24.
go back to reference Carlsson M, Wessman Y, Almgren P, Groop L. High levels of nonesterified fatty acids are associated with increased familial risk of cardiovascular disease. Arterioscler Thromb Vasc Biol. 2000;20:1588–94.CrossRef Carlsson M, Wessman Y, Almgren P, Groop L. High levels of nonesterified fatty acids are associated with increased familial risk of cardiovascular disease. Arterioscler Thromb Vasc Biol. 2000;20:1588–94.CrossRef
27.
go back to reference McQuaid SE, Hodson L, Neville MJ, Dennis AL, Cheeseman J, Humphreys SM, et al. Downregulation of adipose tissue fatty acid trafficking in obesity: a driver for ectopic fat deposition? Diabetes. 2011;60:47–55.CrossRef McQuaid SE, Hodson L, Neville MJ, Dennis AL, Cheeseman J, Humphreys SM, et al. Downregulation of adipose tissue fatty acid trafficking in obesity: a driver for ectopic fat deposition? Diabetes. 2011;60:47–55.CrossRef
28.
Metadata
Title
Effects of acute hypoxia on human adipose tissue lipoprotein lipase activity and lipolysis
Authors
Bimit Mahat
Étienne Chassé
Jean-François Mauger
Pascal Imbeault
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2016
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-016-0965-y

Other articles of this Issue 1/2016

Journal of Translational Medicine 1/2016 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.