The contribution of hormone sensitive lipase to adipose tissue lipolysis and its regulation by insulin in periparturient dairy cows

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Abstract

Hormone sensitive lipase (HSL) activation is part of the metabolic adaptations to the negative energy balance common to the mammalian periparturient period. This study determined HSL contribution to adipose tissue (AT) lipolysis and how insulin regulates its activity in periparturient dairy cows. Subcutaneous AT (SCAT) samples were collected at 11 d prepartum (dry) and 11 (fresh) and 24 d (lactation) postpartum. Basal and stimulated lipolysis (ISO) responses were determined using explant cultures. HSL contribution to lipolysis was assessed using an HSL inhibitor (CAY). Basal lipolysis was higher in SCAT at dry compared with fresh. CAY inhibited basal lipolysis negligibly at dry, but at fresh and lactation it reduced basal lipolysis by 36.1 ± 4.51% and 43.1 ± 4.83%, respectively. Insulin inhibited lipolysis more pronouncedly in dry compared to fresh. Results demonstrate that HSL contribution to basal lipolysis is negligible prepartum. However, HSL is a major driver of SCAT lipolytic responses postpartum. Lower basal lipolysis postpartum suggests that reduced lipogenesis is an important contributor to fatty acid release from SCAT. Loss of adipocyte sensitivity to the antilipolytic action of insulin develops in the early lactation period and supports a state of insulin resistance in AT of cows during the first month postpartum.

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Carbohydrate and lipid metabolism in pregnancy: normal compared with gestational diabetes mellitus.

Faraz N. Butte (2000)

This article reviews maternal metabolic strategies for accommodating fetal nutrient requirements in normal pregnancy and in gestational diabetes mellitus (GDM). Pregnancy is characterized by a progressive increase in nutrient-stimulated insulin responses despite an only minor deterioration in glucose tolerance, consistent with progressive insulin resistance. The hyperinsulinemic-euglycemic glucose clamp technique and intravenous-glucose-tolerance test have indicated that insulin action in late normal pregnancy is 50-70% lower than in nonpregnant women. Metabolic adaptations do not fully compensate in GDM and glucose intolerance ensues. GDM may reflect a predisposition to type 2 diabetes or may be an extreme manifestation of metabolic alterations that normally occur in pregnancy. In normal pregnant women, basal endogenous hepatic glucose production (R(a)) was shown to increase by 16-30% to meet the increasing needs of the placenta and fetus. Total gluconeogenesis is increased in late gestation, although the fractional contribution of total gluconeogenesis to R(a), quantified from (2)H enrichment on carbon 5 of glucose (65-85%), does not differ in pregnant women after a 16-h fast. Endogenous hepatic glucose production was shown to remain sensitive to increased insulin concentration in normal pregnancy (96% suppression), but is less sensitive in GDM (80%). Commensurate with the increased rate of glucose appearance, an increased contribution of carbohydrate to oxidative metabolism has been observed in late pregnancy compared with pregravid states. The 24-h respiratory quotient is significantly higher in late pregnancy than postpartum. Recent advances in carbohydrate metabolism during pregnancy suggest that preventive measures should be aimed at improving insulin sensitivity in women predisposed to GDM. Further research is needed to elucidate the mechanisms and consequences of alterations in lipid metabolism during pregnancy.

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Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores.

Robert Zimmermann, Petra Kienesberger, Guenter Haemmerle … (2008)

Fatty acids (FAs) are essential components of all lipid classes and pivotal substrates for energy production in all vertebrates. Additionally, they act directly or indirectly as signaling molecules and, when bonded to amino acid side chains of peptides, anchor proteins in biological membranes. In vertebrates, FAs are predominantly stored in the form of triacylglycerol (TG) within lipid droplets of white adipose tissue. Lipid droplet-associated TGs are also found in most nonadipose tissues, including liver, cardiac muscle, and skeletal muscle. The mobilization of FAs from all fat depots depends on the activity of TG hydrolases. Currently, three enzymes are known to hydrolyze TG, the well-studied hormone-sensitive lipase (HSL) and monoglyceride lipase (MGL), discovered more than 40 years ago, as well as the relatively recently identified adipose triglyceride lipase (ATGL). The phenotype of HSL- and ATGL-deficient mice, as well as the disease pattern of patients with defective ATGL activity (due to mutation in ATGL or in the enzyme's activator, CGI-58), suggest that the consecutive action of ATGL, HSL, and MGL is responsible for the complete hydrolysis of a TG molecule. The complex regulation of these enzymes by numerous, partially uncharacterized effectors creates the "lipolysome," a complex metabolic network that contributes to the control of lipid and energy homeostasis. This review focuses on the structure, function, and regulation of lipolytic enzymes with a special emphasis on ATGL.

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Ruminant adaptation to negative energy balance. Influences on the etiology of ketosis and fatty liver.

T Herdt (2000)

Ketosis and fatty liver occur when physiologic mechanisms for the adaptation to negative energy balance fail. Failure of hepatic gluconeogenesis to supply adequate glucose for lactation and body needs may be one cause of ketosis; however, poor feedback control of nonesterified fatty acid release from adipose tissue is another likely cause of ketosis and fatty liver. The types of ketosis resulting from these two metabolic lesions may require different therapeutic and prophylactic approaches.

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Author and article information

Contributors

G. Andres Contreras:

ORCID: http://orcid.org/0000-0003-4969-2178

contre28@msu.edu

Journal

Journal ID (nlm-ta): Sci Rep

Journal ID (iso-abbrev): Sci Rep

Title: Scientific Reports

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2045-2322

Publication date (Electronic): 6 September 2018

Publication date PMC-release: 6 September 2018

Publication date Collection: 2018

Volume: 8

Electronic Location Identifier: 13378

Affiliations

[1 ]ISNI 0000 0001 2150 1785, GRID grid.17088.36, Department of Large Animal Clinical Sciences, , Michigan State University, ; East Lansing, Michigan USA

[2 ]ISNI 0000 0001 2150 1785, GRID grid.17088.36, Department of Animal Science, , Michigan State University, ; East Lansing, Michigan USA

Author information

G. Andres Contreras http://orcid.org/0000-0003-4969-2178

Article

Publisher ID: 31582

DOI: 10.1038/s41598-018-31582-4

PMC ID: 6127149

PubMed ID: 30190510

SO-VID: baccfaf6-dc85-40a0-91ac-30abe9329625

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Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 4 June 2018

Date accepted : 22 August 2018

Funding

Funded by: Global Agri-Trade Corporation, Rancho Dominguez, California, USA

Funded by: FundRef https://doi.org/10.13039/100005825, USDA | National Institute of Food and Agriculture (NIFA);

Award ID: 2015-67015-23207

Award Recipient : G. Andres Contreras

Funded by: Large Animal Clinical Sciences, Michigan State University, East Lansing, Michigan, USA Global Agri-Trade Corporation, Gardena, California, USA

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The contribution of hormone sensitive lipase to adipose tissue lipolysis and its regulation by insulin in periparturient dairy cows

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Most cited references 41

Carbohydrate and lipid metabolism in pregnancy: normal compared with gestational diabetes mellitus.

Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores.

Ruminant adaptation to negative energy balance. Influences on the etiology of ketosis and fatty liver.

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