Cited by 694Cannabis and Cannabinoid ResearchAdipokines, Inflammation, and Metabolic DiseasesRegulation of Appetite and Obesity

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Activation of the Peripheral Endocannabinoid System in Human Obesity

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Engeli, Stefan, Böhnke, Jana, Feldpausch, Mareike, Gorzelniak, Kerstin, Janke, Jürgen, Bátkai, Sándor, Pacher, Pál, Harvey-White, Judy, Luft, Friedrich C., Sharma, Arya M., Jordan, Jens·2005·Diabetes

DOI 10.2337/diabetes.54.10.2838PMC PMC2228268

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Abstract

Obesity is the main risk factor for the development of type 2 diabetes. Activation of the central endocannabinoid system increases food intake and promotes weight gain. Blockade of the cannabinoid type 1 (CB-1) receptor reduces body weight in animals by central and peripheral actions; the role of the peripheral endocannabinoid system in human obesity is now being extensively investigated. We measured circulating endocannabinoid concentrations and studied the expression of CB-1 and the main degrading enzyme, fatty acid amide hydrolase (FAAH), in adipose tissue of lean (n = 20) and obese (n = 20) women and after a 5% weight loss in a second group of women (n = 17). Circulating levels of anandamide and 1/2-arachidonoylglycerol were increased by 35 and 52% in obese compared with lean women (P < 0.05). Adipose tissue mRNA levels were reduced by -34% for CB-1 and -59% for FAAH in obese subjects (P < 0.05). A strong negative correlation was found between FAAH expression in adipose tissue and circulating endocannabinoids. Circulating endocannabinoids and CB-1 or FAAH expression were not affected by 5% weight loss. The expression of CB-1 and FAAH was increased in mature human adipocytes compared with in preadipocytes and was found in several human tissues. Our findings support the presence of a peripheral endocannabinoid system that is upregulated in human obesity.

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Background
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“…lung (Galiegue et al., 1995; Rice et al., 1997), adrenals (Galiegue et al., 1995), white adipose tissue (Bensaid et al., 2003; Cota et al., 2003; Engeli et al., 2005; Matias et al., 2006; Roche et al., 2006), liver (Osei-Hyiaman et al., 2005), gut (Buckley et al., 1998; Coutts and Izzo, 2004),…”
Background
Human adipose tissue binds and metabolizes the endocannabinoids anandamide and 2-arachidonoylglycerol
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Background
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Background
Effect of rimonabant on blood pressure in overweight/obese patients with/without co-morbidities: analysis of pooled RIO study results
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GPR55 deficiency is associated with increased adiposity and impaired insulin signaling in peripheral metabolic tissues
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Nutritional Properties of Dietary Omega-3-Enriched Phospholipids
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“This increase of 2-AG plasma levels was in agreement with previous findings in postmenopausal women [173].”
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“This is in line with previous work which observed higher levels of AEA among obese postmeno-Figure pausal women compared with normal-weight counter-parts [6].”
Influential
High Fat Diet Increases Circulating Endocannabinoids Accompanied by Increased Synthesis Enzymes in Adipose Tissue
Kuipers, E. N., Kantae, V., Maarse, B. C. E., van den Berg, S. M., van Eenige, R., Nahon, K. J., Reifel-Miller, A. E., Coşkun, T., de Winther, M. P. J., Lutgens, E., et al. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2018.01913 · Cited by 67
Deletion of G-protein-coupled receptor 55 promotes obesity by reducing physical activity
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“of key genes coding for CB1 and the fatty acid amide hydrolase, FAAH (Bl€uher et al. 2006; Coté et al. 2007; Engeli et al. 2005; Matias et al. 2006).”
Background
Cannabinoid Type 1 Receptor: Another Arrow in the Adipocytes’ Bow
Bellocchio, L., Cervino, C., Vicennati, V., Pasquali, R., & Pagotto, U. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01682.x · Cited by 68
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Rimonabant
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“In rodents and humans, it has been reported that the endocannabinoid system activation in peripheral tissue are associated with multiple cardiometabolic risk factors, including obesity and increased serum lipid production.(10,11) In this study, we also observed that the endocannabinoid system in macrophages was activa…”
Background
Cannabinoid Receptor Type 1 (CB1R) Signaling Regulates Hepatic Gluconeogenesis via Induction of Endoplasmic Reticulum-bound Transcription Factor cAMP-responsive Element-binding Protein H (CREBH) in Primary Hepatocytes
Chanda, D., Kim, D., Li, T., Kim, Y., Koo, S., Lee, C., Chiang, J. Y. L., & Choi, H. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.224352 · Cited by 63
The endovanilloid/endocannabinoid system: A new potential target for osteoporosis therapy
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Strategies for preventing type 2 diabetes: an update for clinicians
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“The endocannabinoid system is overexpressed in obese subjects [Engeli et al. 2005] and mechanistic studies in animals have shown alterations in food intake with administration of cannabinoid agonists/ antagonists [Ligresti et al.”
Background
Adipocyte OGT governs diet-induced hyperphagia and obesity
Li, M., Vera, N. B., Yang, Y., Zhang, B., Ni, W., Ziso-Qejvanaj, E., Ding, S., Zhang, K., Yin, R., Wang, S., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-07461-x · Cited by 64
The L‐α‐Lysophosphatidylinositol/G Protein–Coupled Receptor 55 System Induces the Development of Nonalcoholic Steatosis and Steatohepatitis
Fondevila, M. F., Fernandez, U., Gonzalez-Rellan, M. J., Lima, N. D. S., Buqué, X., González‐Rodríguez, Á., Alonso, C., Iruarrizaga‐Lejarreta, M., Delgado, T. C., Varela‐Rey, M., et al. (2020) · Hepatology · doi:10.1002/hep.31290 · Cited by 64
“Pathologic overactivation of the ECS is associated with the development of dyslipidemia, obesity, and type 2 diabetes.(4,28,29) These actions of the ECS have been mainly attributed to the activation of central and peripheral CB1 receptors.”
Background
The G1422A variant of the cannabinoid receptor gene (CNR1) is associated with abdominal adiposity in obese men
Peeters, A. V., Beckers, S., Mertens, I. L., Hul, W. V., & Gaal, L. V. (2007) · Endocrine · doi:10.1007/s12020-007-0022-y · Cited by 62
Endogenous ω-3 Polyunsaturated Fatty Acid Production Confers Resistance to Obesity, Dyslipidemia, and Diabetes in Mice
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Overactive endocannabinoid signaling impairs apolipoprotein E-mediated clearance of triglyceride-rich lipoproteins
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The endocannabinoid system: Role in glucose and energy metabolism
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Antidiabetic Effects of Hydroxytyrosol: In Vitro and In Vivo Evidence
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“A new proposed approach includes molecules that may potentially modulate endocannabinoid receptor gene expression [39].”
Background
Effect of the cannabinoid CB1receptor antagonist rimonabant on nociceptive responses and adjuvant‐induced arthritis in obese and lean rats
Croci, T., & Zarini, E. (2007) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0707138 · Cited by 63
“…effects and it may exert several intrinsic actions possibly by blocking the activation of cannabinoid CB1 receptors by the endocannabinoid system, which is tonically activated under certain pathophysiological conditions (Di Marzo and Matias, 2005; Engeli et al., 2005; Matias et al., 2006).”
Background
Overweight and obesity: Key components of cardiometabolic risk
Aronne, L. J., & Isoldi, K. K. (2007) · Clinical cornerstone · doi:10.1016/s1098-3597(07)80026-3 · Cited by 60
The functional Pro129Thr variant of the FAAH gene is not associated with various fat accumulation phenotypes in a population-based cohort of 5,801 whites
Jensen, D. P., Andreasen, C. H., Andersen, M. K., Hansen, L., Eiberg, H., Borch‐Johnsen, K., Jørgensen, T., Hansen, T. F., & Pedersen, O. B. (2007) · Journal of Molecular Medicine · doi:10.1007/s00109-006-0139-0 · Cited by 64
“In animals, food intake and weight gain are influenced by endocannabinoids [4–6] acting upon endocannabinoid CB1 receptors in the brain [7], the gastrointestinal tract [8], adipose tissues [9, 10], hepatocytes [11], and in the soleus muscle of mice [12].”
Background
Insulin differentially modulates the peripheral endocannabinoid system in human subcutaneous abdominal adipose tissue from lean and obese individuals
Murdolo, G., Kempf, K., Hammarstedt, A., Herder, C., Smith, U., & Jansson, P. A. (2007) · Journal of Endocrinological Investigation · doi:10.1007/bf03347440 · Cited by 58
Anti‐obesity efficacy of LH‐21, a cannabinoid CB 1 receptor antagonist with poor brain penetration, in diet‐induced obese rats
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“In fact, increased concentrations of endocannabinoids might overstimulate CB1 receptors in a pathophysiological manner contributing to obesity (Engeli et al., 2005; Bluher et al., 2006; Di Marzo, 2008; Engeli, 2008; Matias et al., 2008; Starowicz et al., 2008).”
Background
Profiling plasma N-Acylethanolamine levels and their ratios as a biomarker of obesity and dysmetabolism
Fanelli, F., Mezzullo, M., Repaci, A., Belluomo, I., Gasparini, D. I., Dalmazi, G. D., Mastroroberto, M., Vicennati, V., Gambineri, A., Morselli‐Labate, A. M., et al. (2018) · Molecular Metabolism · doi:10.1016/j.molmet.2018.06.002 · Cited by 58
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Result
Endocannabinoids and cardiac contractile function: Pathophysiological implications
Bátkai, S., & Pacher, P. (2009) · Pharmacological Research · doi:10.1016/j.phrs.2009.04.003 · Cited by 57
“adipose tissue (7,8), liver (9,10), myocardium (11-14), and the vascular endothelium and smooth muscle cells (15-17).”
Background
Adipose tissue endocannabinoid system gene expression: depot differences and effects of diet and exercise
You, T., DiSanzo, B., Wang, X., Yang, R., & Gong, D. (2011) · Lipids in Health and Disease · doi:10.1186/1476-511x-10-194 · Cited by 56
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Influential
Determination of endocannabinoids and N-acylethanolamines in human hair with LC-MS/MS and their relation to symptoms of depression, burnout, and anxiety
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Endocannabinoid regulation of β ‐cell functions: implications for glycaemic control and diabetes
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Background
The endocannabinoid system in cardiovascular function: novel insights and clinical implications
Sierra, S., Luquin, N., & Navarro‐Otano, J. (2017) · Clinical Autonomic Research · doi:10.1007/s10286-017-0488-5 · Cited by 56
Endocannabinoids and the Gut-Brain Control of Food Intake and Obesity
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Circulating endocannabinoids in insulin sensitive vs. Insulin resistant obese postmenopausal women. A MONET group study
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“Repeated measures ANOVA were performed to determine the main effect of two groups (ISO vs. IRO) for: 1) baseline and last 30 min of HEC; 2) baseline and after 6 month weight loss on ECs.”
BackgroundInfluential
Vaccenic acid suppresses intestinal inflammation by increasing anandamide and related N-acylethanolamines in the JCR:LA-cp rat
Jácome-Sosa, M., Vacca, C., Mangat, R., Diané, A., Nelson, R. C., Reaney, M. J. T., Shen, J., Curtis, J. M., Vine, D. F., Field, C. J., et al. (2016) · Journal of Lipid Research · doi:10.1194/jlr.m066308 · Cited by 55
Cannabinoid CB1 Receptors Inhibit Gut-Brain Satiation Signaling in Diet-Induced Obesity
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Role of cannabinoid receptor 1 in human adipose tissue for lipolysis regulation and insulin resistance
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Vagus Nerve Stimulation Reduces Body Weight and Fat Mass in Rats
Banni, S., Carta, G., Murru, E., Cordeddu, L., Giordano, E., Marrosu, F., Puligheddu, M., Floris, G., Asuni, G. P., Cappai, A. L., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044813 · Cited by 53
“Indeed adipocytes are implicated in the control of endocannabinoid availability, affecting energy balance via central orexigenic drive and peripheral lipogenesis [21–23].”
Background
Pharmacological and non-pharmacological interventions to influence adipose tissue function
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“Interestingly enough, peripheral endocannabinoid levels are increased in human obesity, probably due to diminished insulin mediated down regulation of the endocannabinoid system in insulin resistant adipocytes [51,52].”
Background

Authors: Engeli, S., Böhnke, J., Feldpausch, M., Gorzelniak, K., Janke, J., Bátkai, S., Pacher, P., Harvey-White, J., Luft, F. C., Sharma, A. M., & Jordan, J.
Affiliations: Helios Hospital Berlin-Buch (DE)
Franz Volhard Clinical Research Center, Charité Campus Buch, and HELIOS Klinikum Berlin, Berlin, Germany
Laboratory of Physiologic Studies, National Institute on Alcohol Abuse & Alcoholism, National Institutes of Health, Bethesda, Maryland
National Institutes of Health (US)
McMaster University (CA)
ORCID: Engeli, Stefan
Luft, Friedrich C.
Sharma, Arya M.
Jordan, Jens
Venue: Diabetes
Publisher: American Diabetes Association
Published: 2005-10-01
Volume: 54
Issue: 10
Pages: 2838-2843
ISSN: 0012-1797 (ISSN-L)
1939-327X
DOI: 10.2337/diabetes.54.10.2838
PMC: PMC2228268
OpenAlex: W2162112945
Cited by: 686
References: 37
Citations by year: 2026: 11 · 2025: 14 · 2024: 20 · 2023: 19 · 2022: 20 · 2021: 30 · 2020: 29 · 2019: 24 · 2018: 30 · 2017: 30 · 2016: 15 · 2015: 31 · 2014: 29 · 2013: 29 · 2012: 33
FWCI: 38.06
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Diabetes (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (submittedVersion)
Funders: Sanofi
Bundesministerium für Bildung und Forschung
National Institutes of Health
National Institute on Alcohol Abuse and Alcoholism (Z01AA000375)
Topics: Health Sciences › Medicine › Pharmacology (medical) › Cannabis and Cannabinoid Research
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
Keywords: obesity, cannabinoid type 1 receptor, fatty acid amide hydrolase, anandamide, 2-arachidonoylglycerol, adipose tissue, weight loss, human adipocytes, type 2 diabetes risk
MeSH terms: Fatty Acid Amide Hydrolases, Adipose Tissue, Amidohydrolases, Arachidonic Acids, Body Composition, Female, Glycerides, Humans, Middle Aged, Obesity, RNA, Messenger, Weight Loss, Gene Expression, Body Mass Index, Linear Models, Postmenopause, Reverse Transcriptase Polymerase Chain Reaction, Receptor, Cannabinoid, CB1, Polyunsaturated Alkamides, Cannabinoid Receptor Modulators, Endocannabinoids

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Activation of the Peripheral Endocannabinoid System in Human Obesity

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