High-fat diet-induced insulin resistance does not increase plasma anandamide levels or potentiate anandamide insulinotropic effect in isolated canine islets

Obesity has been associated with elevated plasma anandamide levels. In addition, anandamide has been shown to stimulate insulin secretion in vitro, suggesting that anandamide might be linked to hyperinsulinemia. To determine whether high-fat diet-induced insulin resistance increases anandamide level...

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Veröffentlicht in:PloS one 2015-04, Vol.10 (4), p.e0123558-e0123558
Hauptverfasser: Woolcott, Orison O, Richey, Joyce M, Kabir, Morvarid, Chow, Robert H, Iyer, Malini S, Kirkman, Erlinda L, Stefanovski, Darko, Lottati, Maya, Kim, Stella P, Harrison, L Nicole, Ionut, Viorica, Zheng, Dan, Hsu, Isabel R, Catalano, Karyn J, Chiu, Jenny D, Bradshaw, Heather, Wu, Qiang, Kolka, Cathryn M, Bergman, Richard N
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container_start_page e0123558
container_title PloS one
container_volume 10
creator Woolcott, Orison O
Richey, Joyce M
Kabir, Morvarid
Chow, Robert H
Iyer, Malini S
Kirkman, Erlinda L
Stefanovski, Darko
Lottati, Maya
Kim, Stella P
Harrison, L Nicole
Ionut, Viorica
Zheng, Dan
Hsu, Isabel R
Catalano, Karyn J
Chiu, Jenny D
Bradshaw, Heather
Wu, Qiang
Kolka, Cathryn M
Bergman, Richard N
description Obesity has been associated with elevated plasma anandamide levels. In addition, anandamide has been shown to stimulate insulin secretion in vitro, suggesting that anandamide might be linked to hyperinsulinemia. To determine whether high-fat diet-induced insulin resistance increases anandamide levels and potentiates the insulinotropic effect of anandamide in isolated pancreatic islets. Dogs were fed a high-fat diet (n = 9) for 22 weeks. Abdominal fat depot was quantified by MRI. Insulin sensitivity was assessed by the euglycemic-hyperinsulinemic clamp. Fasting plasma endocannabinoid levels were analyzed by liquid chromatography-mass spectrometry. All metabolic assessments were performed before and after fat diet regimen. At the end of the study, pancreatic islets were isolated prior to euthanasia to test the in vitro effect of anandamide on islet hormones. mRNA expression of cannabinoid receptors was determined in intact islets. The findings in vitro were compared with those from animals fed a control diet (n = 7). Prolonged fat feeding increased abdominal fat content by 81.3±21.6% (mean±S.E.M, P
doi_str_mv 10.1371/journal.pone.0123558
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In addition, anandamide has been shown to stimulate insulin secretion in vitro, suggesting that anandamide might be linked to hyperinsulinemia. To determine whether high-fat diet-induced insulin resistance increases anandamide levels and potentiates the insulinotropic effect of anandamide in isolated pancreatic islets. Dogs were fed a high-fat diet (n = 9) for 22 weeks. Abdominal fat depot was quantified by MRI. Insulin sensitivity was assessed by the euglycemic-hyperinsulinemic clamp. Fasting plasma endocannabinoid levels were analyzed by liquid chromatography-mass spectrometry. All metabolic assessments were performed before and after fat diet regimen. At the end of the study, pancreatic islets were isolated prior to euthanasia to test the in vitro effect of anandamide on islet hormones. mRNA expression of cannabinoid receptors was determined in intact islets. The findings in vitro were compared with those from animals fed a control diet (n = 7). Prolonged fat feeding increased abdominal fat content by 81.3±21.6% (mean±S.E.M, P&lt;0.01). In vivo insulin sensitivity decreased by 31.3±12.1% (P&lt;0.05), concomitant with a decrease in plasma 2-arachidonoyl glycerol (from 39.1±5.2 to 15.7±2.0 nmol/L) but not anandamide, oleoyl ethanolamide, linoleoyl ethanolamide, or palmitoyl ethanolamide. In control-diet animals (body weight: 28.8±1.0 kg), islets incubated with anandamide had a higher basal and glucose-stimulated insulin secretion as compared with no treatment. Islets from fat-fed animals (34.5±1.3 kg; P&lt;0.05 versus control) did not exhibit further potentiation of anandamide-induced insulin secretion as compared with control-diet animals. Glucagon but not somatostatin secretion in vitro was also increased in response to anandamide, but there was no difference between groups (P = 0.705). No differences in gene expression of CB1R or CB2R between groups were found. In canines, high-fat diet-induced insulin resistance does not alter plasma anandamide levels or further potentiate the insulinotropic effect of anandamide in vitro.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0123558</identifier><identifier>PMID: 25855974</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abdominal Fat - drug effects ; Abdominal Fat - metabolism ; Analysis ; Anandamide ; Animals ; Antimicrobial Cationic Peptides - biosynthesis ; Arachidonic Acids - blood ; Arachidonic Acids - genetics ; Blood Glucose ; Body Weight ; Cannabinoid CB1 receptors ; Cannabinoid CB2 receptors ; Chromatography ; Diet ; Diet, High-Fat - adverse effects ; Dogs ; Endocannabinoids - blood ; Endocannabinoids - genetics ; Euthanasia ; Gene expression ; Glucagon ; Glucose ; Glycerol ; High fat diet ; Hormones ; Humans ; Hyperinsulinemia ; In vitro methods and tests ; In vivo methods and tests ; Insulin ; Insulin - metabolism ; Insulin Resistance ; Insulin secretion ; Islets of Langerhans ; Islets of Langerhans - metabolism ; Islets of Langerhans - pathology ; Kinases ; Liquid chromatography ; Magnetic resonance imaging ; Mass spectrometry ; Mass spectroscopy ; Obesity ; Obesity - blood ; Obesity - pathology ; Pancreas ; Physicians ; Physiological aspects ; Polyunsaturated Alkamides - blood ; Potentiation ; Receptor, Cannabinoid, CB2 - biosynthesis ; Receptors ; Rodents ; Secretion ; Sensitivity ; Sensitivity analysis ; Somatostatin</subject><ispartof>PloS one, 2015-04, Vol.10 (4), p.e0123558-e0123558</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Woolcott et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2015 Woolcott et al 2015 Woolcott et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-6553208da24b1f3f46637f864621f6ecb44160fdd6b2500a5d6d630c303ccb6d3</citedby><cites>FETCH-LOGICAL-c692t-6553208da24b1f3f46637f864621f6ecb44160fdd6b2500a5d6d630c303ccb6d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4391925/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4391925/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,2097,2916,23848,27906,27907,53773,53775,79350,79351</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25855974$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Alquier, Thierry</contributor><creatorcontrib>Woolcott, Orison O</creatorcontrib><creatorcontrib>Richey, Joyce M</creatorcontrib><creatorcontrib>Kabir, Morvarid</creatorcontrib><creatorcontrib>Chow, Robert H</creatorcontrib><creatorcontrib>Iyer, Malini S</creatorcontrib><creatorcontrib>Kirkman, Erlinda L</creatorcontrib><creatorcontrib>Stefanovski, Darko</creatorcontrib><creatorcontrib>Lottati, Maya</creatorcontrib><creatorcontrib>Kim, Stella P</creatorcontrib><creatorcontrib>Harrison, L Nicole</creatorcontrib><creatorcontrib>Ionut, Viorica</creatorcontrib><creatorcontrib>Zheng, Dan</creatorcontrib><creatorcontrib>Hsu, Isabel R</creatorcontrib><creatorcontrib>Catalano, Karyn J</creatorcontrib><creatorcontrib>Chiu, Jenny D</creatorcontrib><creatorcontrib>Bradshaw, Heather</creatorcontrib><creatorcontrib>Wu, Qiang</creatorcontrib><creatorcontrib>Kolka, Cathryn M</creatorcontrib><creatorcontrib>Bergman, Richard N</creatorcontrib><title>High-fat diet-induced insulin resistance does not increase plasma anandamide levels or potentiate anandamide insulinotropic effect in isolated canine islets</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Obesity has been associated with elevated plasma anandamide levels. In addition, anandamide has been shown to stimulate insulin secretion in vitro, suggesting that anandamide might be linked to hyperinsulinemia. To determine whether high-fat diet-induced insulin resistance increases anandamide levels and potentiates the insulinotropic effect of anandamide in isolated pancreatic islets. Dogs were fed a high-fat diet (n = 9) for 22 weeks. Abdominal fat depot was quantified by MRI. Insulin sensitivity was assessed by the euglycemic-hyperinsulinemic clamp. Fasting plasma endocannabinoid levels were analyzed by liquid chromatography-mass spectrometry. All metabolic assessments were performed before and after fat diet regimen. At the end of the study, pancreatic islets were isolated prior to euthanasia to test the in vitro effect of anandamide on islet hormones. mRNA expression of cannabinoid receptors was determined in intact islets. The findings in vitro were compared with those from animals fed a control diet (n = 7). Prolonged fat feeding increased abdominal fat content by 81.3±21.6% (mean±S.E.M, P&lt;0.01). In vivo insulin sensitivity decreased by 31.3±12.1% (P&lt;0.05), concomitant with a decrease in plasma 2-arachidonoyl glycerol (from 39.1±5.2 to 15.7±2.0 nmol/L) but not anandamide, oleoyl ethanolamide, linoleoyl ethanolamide, or palmitoyl ethanolamide. In control-diet animals (body weight: 28.8±1.0 kg), islets incubated with anandamide had a higher basal and glucose-stimulated insulin secretion as compared with no treatment. Islets from fat-fed animals (34.5±1.3 kg; P&lt;0.05 versus control) did not exhibit further potentiation of anandamide-induced insulin secretion as compared with control-diet animals. Glucagon but not somatostatin secretion in vitro was also increased in response to anandamide, but there was no difference between groups (P = 0.705). No differences in gene expression of CB1R or CB2R between groups were found. In canines, high-fat diet-induced insulin resistance does not alter plasma anandamide levels or further potentiate the insulinotropic effect of anandamide in vitro.</description><subject>Abdominal Fat - drug effects</subject><subject>Abdominal Fat - metabolism</subject><subject>Analysis</subject><subject>Anandamide</subject><subject>Animals</subject><subject>Antimicrobial Cationic Peptides - biosynthesis</subject><subject>Arachidonic Acids - blood</subject><subject>Arachidonic Acids - genetics</subject><subject>Blood Glucose</subject><subject>Body Weight</subject><subject>Cannabinoid CB1 receptors</subject><subject>Cannabinoid CB2 receptors</subject><subject>Chromatography</subject><subject>Diet</subject><subject>Diet, High-Fat - adverse effects</subject><subject>Dogs</subject><subject>Endocannabinoids - blood</subject><subject>Endocannabinoids - genetics</subject><subject>Euthanasia</subject><subject>Gene expression</subject><subject>Glucagon</subject><subject>Glucose</subject><subject>Glycerol</subject><subject>High fat diet</subject><subject>Hormones</subject><subject>Humans</subject><subject>Hyperinsulinemia</subject><subject>In vitro methods and tests</subject><subject>In vivo methods and tests</subject><subject>Insulin</subject><subject>Insulin - metabolism</subject><subject>Insulin Resistance</subject><subject>Insulin secretion</subject><subject>Islets of Langerhans</subject><subject>Islets of Langerhans - metabolism</subject><subject>Islets of Langerhans - pathology</subject><subject>Kinases</subject><subject>Liquid chromatography</subject><subject>Magnetic resonance imaging</subject><subject>Mass spectrometry</subject><subject>Mass spectroscopy</subject><subject>Obesity</subject><subject>Obesity - blood</subject><subject>Obesity - pathology</subject><subject>Pancreas</subject><subject>Physicians</subject><subject>Physiological aspects</subject><subject>Polyunsaturated Alkamides - blood</subject><subject>Potentiation</subject><subject>Receptor, Cannabinoid, CB2 - biosynthesis</subject><subject>Receptors</subject><subject>Rodents</subject><subject>Secretion</subject><subject>Sensitivity</subject><subject>Sensitivity 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diet-induced insulin resistance does not increase plasma anandamide levels or potentiate anandamide insulinotropic effect in isolated canine islets</title><author>Woolcott, Orison O ; Richey, Joyce M ; Kabir, Morvarid ; Chow, Robert H ; Iyer, Malini S ; Kirkman, Erlinda L ; Stefanovski, Darko ; Lottati, Maya ; Kim, Stella P ; Harrison, L Nicole ; Ionut, Viorica ; Zheng, Dan ; Hsu, Isabel R ; Catalano, Karyn J ; Chiu, Jenny D ; Bradshaw, Heather ; Wu, Qiang ; Kolka, Cathryn M ; Bergman, Richard N</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-6553208da24b1f3f46637f864621f6ecb44160fdd6b2500a5d6d630c303ccb6d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Abdominal Fat - drug effects</topic><topic>Abdominal Fat - metabolism</topic><topic>Analysis</topic><topic>Anandamide</topic><topic>Animals</topic><topic>Antimicrobial Cationic Peptides - biosynthesis</topic><topic>Arachidonic Acids - blood</topic><topic>Arachidonic Acids - genetics</topic><topic>Blood Glucose</topic><topic>Body Weight</topic><topic>Cannabinoid CB1 receptors</topic><topic>Cannabinoid CB2 receptors</topic><topic>Chromatography</topic><topic>Diet</topic><topic>Diet, High-Fat - adverse effects</topic><topic>Dogs</topic><topic>Endocannabinoids - blood</topic><topic>Endocannabinoids - genetics</topic><topic>Euthanasia</topic><topic>Gene expression</topic><topic>Glucagon</topic><topic>Glucose</topic><topic>Glycerol</topic><topic>High fat diet</topic><topic>Hormones</topic><topic>Humans</topic><topic>Hyperinsulinemia</topic><topic>In vitro methods and tests</topic><topic>In vivo methods and tests</topic><topic>Insulin</topic><topic>Insulin - metabolism</topic><topic>Insulin Resistance</topic><topic>Insulin secretion</topic><topic>Islets of Langerhans</topic><topic>Islets of Langerhans - metabolism</topic><topic>Islets of Langerhans - 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Database</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing &amp; Allied Health Premium</collection><collection>Advanced Technologies &amp; Aerospace Database</collection><collection>ProQuest Advanced Technologies &amp; Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Woolcott, Orison O</au><au>Richey, Joyce M</au><au>Kabir, Morvarid</au><au>Chow, Robert H</au><au>Iyer, Malini S</au><au>Kirkman, Erlinda L</au><au>Stefanovski, Darko</au><au>Lottati, Maya</au><au>Kim, Stella P</au><au>Harrison, L Nicole</au><au>Ionut, Viorica</au><au>Zheng, Dan</au><au>Hsu, Isabel R</au><au>Catalano, Karyn J</au><au>Chiu, Jenny D</au><au>Bradshaw, Heather</au><au>Wu, Qiang</au><au>Kolka, Cathryn M</au><au>Bergman, Richard N</au><au>Alquier, Thierry</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>High-fat diet-induced insulin resistance does not increase plasma anandamide levels or potentiate anandamide insulinotropic effect in isolated canine islets</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-04-09</date><risdate>2015</risdate><volume>10</volume><issue>4</issue><spage>e0123558</spage><epage>e0123558</epage><pages>e0123558-e0123558</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Obesity has been associated with elevated plasma anandamide levels. In addition, anandamide has been shown to stimulate insulin secretion in vitro, suggesting that anandamide might be linked to hyperinsulinemia. To determine whether high-fat diet-induced insulin resistance increases anandamide levels and potentiates the insulinotropic effect of anandamide in isolated pancreatic islets. Dogs were fed a high-fat diet (n = 9) for 22 weeks. Abdominal fat depot was quantified by MRI. Insulin sensitivity was assessed by the euglycemic-hyperinsulinemic clamp. Fasting plasma endocannabinoid levels were analyzed by liquid chromatography-mass spectrometry. All metabolic assessments were performed before and after fat diet regimen. At the end of the study, pancreatic islets were isolated prior to euthanasia to test the in vitro effect of anandamide on islet hormones. mRNA expression of cannabinoid receptors was determined in intact islets. The findings in vitro were compared with those from animals fed a control diet (n = 7). Prolonged fat feeding increased abdominal fat content by 81.3±21.6% (mean±S.E.M, P&lt;0.01). In vivo insulin sensitivity decreased by 31.3±12.1% (P&lt;0.05), concomitant with a decrease in plasma 2-arachidonoyl glycerol (from 39.1±5.2 to 15.7±2.0 nmol/L) but not anandamide, oleoyl ethanolamide, linoleoyl ethanolamide, or palmitoyl ethanolamide. In control-diet animals (body weight: 28.8±1.0 kg), islets incubated with anandamide had a higher basal and glucose-stimulated insulin secretion as compared with no treatment. Islets from fat-fed animals (34.5±1.3 kg; P&lt;0.05 versus control) did not exhibit further potentiation of anandamide-induced insulin secretion as compared with control-diet animals. Glucagon but not somatostatin secretion in vitro was also increased in response to anandamide, but there was no difference between groups (P = 0.705). No differences in gene expression of CB1R or CB2R between groups were found. In canines, high-fat diet-induced insulin resistance does not alter plasma anandamide levels or further potentiate the insulinotropic effect of anandamide in vitro.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25855974</pmid><doi>10.1371/journal.pone.0123558</doi><oa>free_for_read</oa></addata></record>
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subjects Abdominal Fat - drug effects
Abdominal Fat - metabolism
Analysis
Anandamide
Animals
Antimicrobial Cationic Peptides - biosynthesis
Arachidonic Acids - blood
Arachidonic Acids - genetics
Blood Glucose
Body Weight
Cannabinoid CB1 receptors
Cannabinoid CB2 receptors
Chromatography
Diet
Diet, High-Fat - adverse effects
Dogs
Endocannabinoids - blood
Endocannabinoids - genetics
Euthanasia
Gene expression
Glucagon
Glucose
Glycerol
High fat diet
Hormones
Humans
Hyperinsulinemia
In vitro methods and tests
In vivo methods and tests
Insulin
Insulin - metabolism
Insulin Resistance
Insulin secretion
Islets of Langerhans
Islets of Langerhans - metabolism
Islets of Langerhans - pathology
Kinases
Liquid chromatography
Magnetic resonance imaging
Mass spectrometry
Mass spectroscopy
Obesity
Obesity - blood
Obesity - pathology
Pancreas
Physicians
Physiological aspects
Polyunsaturated Alkamides - blood
Potentiation
Receptor, Cannabinoid, CB2 - biosynthesis
Receptors
Rodents
Secretion
Sensitivity
Sensitivity analysis
Somatostatin
title High-fat diet-induced insulin resistance does not increase plasma anandamide levels or potentiate anandamide insulinotropic effect in isolated canine islets
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