Training alters the distribution of perilipin proteins in muscle following acute free fatty acid exposure

S. O. Shepherd; J. A. Strauss; Q. Wang; J. J. Dube; B. Goodpaster; D. G. Mashek; L. S. Chow

doi:10.1113/JP274374

Training alters the distribution of perilipin proteins in muscle following acute free fatty acid exposure

S. O. Shepherd, J. A. Strauss, Q. Wang, J. J. Dube, B. Goodpaster, D. G. Mashek, L. S. Chow

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

16 Scopus citations

Abstract

Key points: The lipid droplet (LD)-associated perilipin (PLIN) proteins promote intramuscular triglyceride (IMTG) storage, although whether the abundance and association of the PLIN proteins with LDs is related to the diverse lipid storage in muscle between trained and sedentary individuals is unknown. We show that lipid infusion augments IMTG content in type I fibres of both trained and sedentary individuals. Most importantly, despite there being no change in PLIN protein content, lipid infusion did increase the number of LDs connected with PLIN proteins in trained individuals only. We conclude that trained individuals are able to redistribute the pre-existing pool of PLIN proteins to an expanded LD pool during lipid infusion and, via this adaptation, may support the storage of fatty acids in IMTG. Abstract: Because the lipid droplet (LD)-associated perilipin (PLIN) proteins promote intramuscular triglyceride (IMTG) storage, we investigated the hypothesis that differential protein content of PLINs and their distribution with LDs may be linked to the diverse lipid storage in muscle between trained and sedentary individuals. Trained (n = 11) and sedentary (n = 10) subjects, matched for age, sex and body mass index, received either a 6 h lipid or glycerol infusion in the setting of a concurrent hyperinsulinaemic–euglycaemic clamp. Sequential muscle biopsies (0, 2 and 6 h) were analysed using confocal immunofluorescence microscopy for fibre type-specific IMTG content and PLIN associations with LDs. In both groups, lipid infusion increased IMTG content in type I fibres (trained: +62%, sedentary: +79%; P < 0.05) but did not affect PLIN protein content. At baseline, PLIN2 (+65%), PLIN3 (+105%) and PLIN5 (+53%; all P < 0.05) protein content was higher in trained compared to sedentary individuals. In trained individuals, lipid infusion increased the number of LDs associated with PLIN2 (+27%), PLIN3 (+73%) and PLIN5 (+40%; all P < 0.05) in type I fibres. By contrast, in sedentary individuals, lipid infusion only increased the number of LDs not associated with PLIN proteins. Acute free fatty acid elevation therefore induces a redistribution of PLIN proteins to an expanded LD pool in trained individuals only and this may be part of the mechanism that enables fatty acids to be stored in IMTG.

Original language	English (US)
Pages (from-to)	5587-5601
Number of pages	15
Journal	Journal of Physiology
Volume	595
Issue number	16
DOIs	https://doi.org/10.1113/JP274374
State	Published - Aug 15 2017

Bibliographical note

Funding Information:
This work was supported by the National Institutes of Health [5K12-RR-023247-02, DK-50456, UL1 TR000135 (Mayo CTSA)], the Minnesota Medical Foundation, the Pennock Family Foundation, the University of Minnesota (CTSA: NIH UL1TR000114) and the Metabolic Studies Core of the Minnesota Obesity Center. The antibody against myosin (human slow twitch fibres, A4.840) used in the present study was developed by Dr H.?M.?Blau and obtained from the Developmental Studies Hybridoma Bank developed under the auspices of the NICHD and maintained by the Department of Biological Sciences at the University of Iowa (Iowa City, IA, USA). The authors would like to thank Professor Anton Wagenmakers (Liverpool John Moores University) for critically review and editing the manuscript submitted for publication.

Keywords

intramuscular triglyceride
perilipin 2
perilipin 3

Access

10.1113/JP274374

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5556155

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title = "Training alters the distribution of perilipin proteins in muscle following acute free fatty acid exposure",

abstract = "Key points: The lipid droplet (LD)-associated perilipin (PLIN) proteins promote intramuscular triglyceride (IMTG) storage, although whether the abundance and association of the PLIN proteins with LDs is related to the diverse lipid storage in muscle between trained and sedentary individuals is unknown. We show that lipid infusion augments IMTG content in type I fibres of both trained and sedentary individuals. Most importantly, despite there being no change in PLIN protein content, lipid infusion did increase the number of LDs connected with PLIN proteins in trained individuals only. We conclude that trained individuals are able to redistribute the pre-existing pool of PLIN proteins to an expanded LD pool during lipid infusion and, via this adaptation, may support the storage of fatty acids in IMTG. Abstract: Because the lipid droplet (LD)-associated perilipin (PLIN) proteins promote intramuscular triglyceride (IMTG) storage, we investigated the hypothesis that differential protein content of PLINs and their distribution with LDs may be linked to the diverse lipid storage in muscle between trained and sedentary individuals. Trained (n = 11) and sedentary (n = 10) subjects, matched for age, sex and body mass index, received either a 6 h lipid or glycerol infusion in the setting of a concurrent hyperinsulinaemic–euglycaemic clamp. Sequential muscle biopsies (0, 2 and 6 h) were analysed using confocal immunofluorescence microscopy for fibre type-specific IMTG content and PLIN associations with LDs. In both groups, lipid infusion increased IMTG content in type I fibres (trained: +62%, sedentary: +79%; P < 0.05) but did not affect PLIN protein content. At baseline, PLIN2 (+65%), PLIN3 (+105%) and PLIN5 (+53%; all P < 0.05) protein content was higher in trained compared to sedentary individuals. In trained individuals, lipid infusion increased the number of LDs associated with PLIN2 (+27%), PLIN3 (+73%) and PLIN5 (+40%; all P < 0.05) in type I fibres. By contrast, in sedentary individuals, lipid infusion only increased the number of LDs not associated with PLIN proteins. Acute free fatty acid elevation therefore induces a redistribution of PLIN proteins to an expanded LD pool in trained individuals only and this may be part of the mechanism that enables fatty acids to be stored in IMTG.",

keywords = "intramuscular triglyceride, perilipin 2, perilipin 3",

author = "Shepherd, {S. O.} and Strauss, {J. A.} and Q. Wang and Dube, {J. J.} and B. Goodpaster and Mashek, {D. G.} and Chow, {L. S.}",

note = "Funding Information: This work was supported by the National Institutes of Health [5K12-RR-023247-02, DK-50456, UL1 TR000135 (Mayo CTSA)], the Minnesota Medical Foundation, the Pennock Family Foundation, the University of Minnesota (CTSA: NIH UL1TR000114) and the Metabolic Studies Core of the Minnesota Obesity Center. The antibody against myosin (human slow twitch fibres, A4.840) used in the present study was developed by Dr H.?M.?Blau and obtained from the Developmental Studies Hybridoma Bank developed under the auspices of the NICHD and maintained by the Department of Biological Sciences at the University of Iowa (Iowa City, IA, USA). The authors would like to thank Professor Anton Wagenmakers (Liverpool John Moores University) for critically review and editing the manuscript submitted for publication.",

year = "2017",

month = aug,

day = "15",

doi = "10.1113/JP274374",

language = "English (US)",

volume = "595",

pages = "5587--5601",

journal = "Journal of Physiology",

issn = "0022-3751",

publisher = "Wiley-Blackwell",

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TY - JOUR

T1 - Training alters the distribution of perilipin proteins in muscle following acute free fatty acid exposure

AU - Shepherd, S. O.

AU - Strauss, J. A.

AU - Wang, Q.

AU - Dube, J. J.

AU - Goodpaster, B.

AU - Mashek, D. G.

AU - Chow, L. S.

N1 - Funding Information: This work was supported by the National Institutes of Health [5K12-RR-023247-02, DK-50456, UL1 TR000135 (Mayo CTSA)], the Minnesota Medical Foundation, the Pennock Family Foundation, the University of Minnesota (CTSA: NIH UL1TR000114) and the Metabolic Studies Core of the Minnesota Obesity Center. The antibody against myosin (human slow twitch fibres, A4.840) used in the present study was developed by Dr H.?M.?Blau and obtained from the Developmental Studies Hybridoma Bank developed under the auspices of the NICHD and maintained by the Department of Biological Sciences at the University of Iowa (Iowa City, IA, USA). The authors would like to thank Professor Anton Wagenmakers (Liverpool John Moores University) for critically review and editing the manuscript submitted for publication.

PY - 2017/8/15

Y1 - 2017/8/15

N2 - Key points: The lipid droplet (LD)-associated perilipin (PLIN) proteins promote intramuscular triglyceride (IMTG) storage, although whether the abundance and association of the PLIN proteins with LDs is related to the diverse lipid storage in muscle between trained and sedentary individuals is unknown. We show that lipid infusion augments IMTG content in type I fibres of both trained and sedentary individuals. Most importantly, despite there being no change in PLIN protein content, lipid infusion did increase the number of LDs connected with PLIN proteins in trained individuals only. We conclude that trained individuals are able to redistribute the pre-existing pool of PLIN proteins to an expanded LD pool during lipid infusion and, via this adaptation, may support the storage of fatty acids in IMTG. Abstract: Because the lipid droplet (LD)-associated perilipin (PLIN) proteins promote intramuscular triglyceride (IMTG) storage, we investigated the hypothesis that differential protein content of PLINs and their distribution with LDs may be linked to the diverse lipid storage in muscle between trained and sedentary individuals. Trained (n = 11) and sedentary (n = 10) subjects, matched for age, sex and body mass index, received either a 6 h lipid or glycerol infusion in the setting of a concurrent hyperinsulinaemic–euglycaemic clamp. Sequential muscle biopsies (0, 2 and 6 h) were analysed using confocal immunofluorescence microscopy for fibre type-specific IMTG content and PLIN associations with LDs. In both groups, lipid infusion increased IMTG content in type I fibres (trained: +62%, sedentary: +79%; P < 0.05) but did not affect PLIN protein content. At baseline, PLIN2 (+65%), PLIN3 (+105%) and PLIN5 (+53%; all P < 0.05) protein content was higher in trained compared to sedentary individuals. In trained individuals, lipid infusion increased the number of LDs associated with PLIN2 (+27%), PLIN3 (+73%) and PLIN5 (+40%; all P < 0.05) in type I fibres. By contrast, in sedentary individuals, lipid infusion only increased the number of LDs not associated with PLIN proteins. Acute free fatty acid elevation therefore induces a redistribution of PLIN proteins to an expanded LD pool in trained individuals only and this may be part of the mechanism that enables fatty acids to be stored in IMTG.

AB - Key points: The lipid droplet (LD)-associated perilipin (PLIN) proteins promote intramuscular triglyceride (IMTG) storage, although whether the abundance and association of the PLIN proteins with LDs is related to the diverse lipid storage in muscle between trained and sedentary individuals is unknown. We show that lipid infusion augments IMTG content in type I fibres of both trained and sedentary individuals. Most importantly, despite there being no change in PLIN protein content, lipid infusion did increase the number of LDs connected with PLIN proteins in trained individuals only. We conclude that trained individuals are able to redistribute the pre-existing pool of PLIN proteins to an expanded LD pool during lipid infusion and, via this adaptation, may support the storage of fatty acids in IMTG. Abstract: Because the lipid droplet (LD)-associated perilipin (PLIN) proteins promote intramuscular triglyceride (IMTG) storage, we investigated the hypothesis that differential protein content of PLINs and their distribution with LDs may be linked to the diverse lipid storage in muscle between trained and sedentary individuals. Trained (n = 11) and sedentary (n = 10) subjects, matched for age, sex and body mass index, received either a 6 h lipid or glycerol infusion in the setting of a concurrent hyperinsulinaemic–euglycaemic clamp. Sequential muscle biopsies (0, 2 and 6 h) were analysed using confocal immunofluorescence microscopy for fibre type-specific IMTG content and PLIN associations with LDs. In both groups, lipid infusion increased IMTG content in type I fibres (trained: +62%, sedentary: +79%; P < 0.05) but did not affect PLIN protein content. At baseline, PLIN2 (+65%), PLIN3 (+105%) and PLIN5 (+53%; all P < 0.05) protein content was higher in trained compared to sedentary individuals. In trained individuals, lipid infusion increased the number of LDs associated with PLIN2 (+27%), PLIN3 (+73%) and PLIN5 (+40%; all P < 0.05) in type I fibres. By contrast, in sedentary individuals, lipid infusion only increased the number of LDs not associated with PLIN proteins. Acute free fatty acid elevation therefore induces a redistribution of PLIN proteins to an expanded LD pool in trained individuals only and this may be part of the mechanism that enables fatty acids to be stored in IMTG.

KW - intramuscular triglyceride

KW - perilipin 2

KW - perilipin 3

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