Lifestyle and Metabolic Syndrome: Contribution of the Endocannabinoidome
Abstract
:1. Introduction
2. The Endocannabinoidome
3. Dietary Fats and the Endocannabinoidome
4. Dietary Fiber and Prebiotics: Improving Gut Barrier Function through the Endocannabinoidome
5. TRPV1: Linking the Endocannabinoidome to the Metabolic Benefits Attributed to Spicy Food
6. Sunlight Effects on the Endocannabinoidome: A Role for Vitamin D?
7. Effects of Exercise on the Endocannabinoidome
8. Cannabis Use and Metabolic Health
9. Conclusions
Author Contributions
Funding
Conflicts of Interest
Abbreviations
Mediators | |
2-AcGs | 2-acylglycerols |
2-AG | 2-arachidonoylglycerol |
2-LG | 2-linoleoyl glycerol |
2-OG | 2-oleoylglycerol |
AcNeuro | acyl neurotransmitters |
AEA | N-arachidonoylethanolamine |
DHEA | N-docosahexanoylethanolamine |
LEA | N-linoleoylethanolamine |
Lipo-AAs | lipoamino acids |
NAEs | N-acylethanolamines |
OA | oleoylamide |
OEA | N-oleoylethanolamine |
PA | fatty acid primary amides |
PEA | N-palmitoylethanolamine |
Receptors | |
Cav3 | T-type Ca2+ channel |
CB1 | cannabinoid receptor 1 |
CB2 | cannabinoid receptor 2 |
GPR110 | G protein-coupled receptor 110 |
GPR119 | G protein-coupled receptor 119 |
GPR18 | G protein-coupled receptor 18 |
GPR55 | G protein-coupled receptor 55 |
PPARA | peroxisome proliferator-activated receptor alpha |
PPARG | peroxisome proliferator-activated receptor gamma |
TRPV1 | transient receptor potential cation channel sub-family V member 1 |
TRPV4 | transient receptor potential cation channel subfamily V member 4 |
Anabolic enzymes | |
AANATL2 | arylalkylamine N-acyltransferase-like 2, isoform A |
ABHD4 | alpha/beta-hydrolase domain containing 4 |
DAGLA/B | diacylglycerol lipase alpha/beta |
GDE1 | glycerophosphodiester phosphodiesterase 1 |
GLYATL3 | glycine N-acyltransferase-like protein 3 |
LPA-Phos | lysophosphatidic acid phosphatase |
Lyso-PLC | lysophospholipase C Lyso-PLC, lysophospholipase D |
NAPEPLD | N-acyl phosphatidylethanolamine-hydrolyzing phospholipase D |
PA-phos. hyd. | phosphatidic acid phosphohydrolase |
PLA1A | phospholipase A1 member A |
PLC | phospholipase C |
PLCB | phospholipase C beta |
PTPN22 | tyrosine protein phosphatase non-receptor type 22 |
sPLA2 | soluble phospholipase A2. |
Catabolic enzymes | |
ABHD12 | alpha/beta-hydrolase domain containing 12 |
ABHD6 | alpha/beta hydrolase domain containing 6 |
COMT | catechol-O-methyltransferase |
COX2 | cyclooxygenase 2 |
CYP450 | cytochrome P450 |
FAAH | fatty acid amide hydrolase |
LOX12/15 | arachidonate lipoxygenase 12/15 |
MAGK | monoacylglycerol kinase |
MGLL | monoacylglycerol lipase |
NAAA | N-acylethanolamine-hydrolyzing acid amidase |
PAM | peptidyl-glycine α-amidating monooxygenase |
References
- Yamaoka, K.; Tango, T. Effects of lifestyle modification on metabolic syndrome: A systematic review and meta-analysis. BMC Med. 2012, 10, 138. [Google Scholar] [CrossRef]
- Reilly, J.J.; El-Hamdouchi, A.; Diouf, A.; Monyeki, A.; Somda, S.A. Determining the worldwide prevalence of obesity. Lancet 2018, 391, 1773–1774. [Google Scholar] [CrossRef]
- NCD Risk Factor Collaboration (NCD-RisC). Worldwide trends in diabetes since 1980: A pooled analysis of 751 population-based studies with 4·4 million participants. Lancet 2016, 387, 1513–1530. [Google Scholar] [CrossRef]
- Liu, H.-H.; Li, J.-J. Aging and dyslipidemia: A review of potential mechanisms. Ageing Res. Rev. 2015, 19, 43–52. [Google Scholar] [CrossRef] [PubMed]
- Blacher, J.; Levy, B.I.; Mourad, J.-J.; Safar, M.E.; Bakris, G. From epidemiological transition to modern cardiovascular epidemiology: Hypertension in the 21st century. Lancet 2016, 388, 530–532. [Google Scholar] [CrossRef]
- Halcox, J.P.; Banegas, J.R.; Roy, C.; Dallongeville, J.; De Backer, G.; Guallar, E.; Perk, J.; Hajage, D.; Henriksson, K.M.; Borghi, C. Prevalence and treatment of atherogenic dyslipidemia in the primary prevention of cardiovascular disease in Europe: EURIKA, a cross-sectional observational study. BMC Cardiovasc. Disord. 2017, 17, 160. [Google Scholar] [CrossRef] [PubMed]
- Barquera, S.; Pedroza-Tobías, A.; Medina, C.; Hernández-Barrera, L.; Bibbins-Domingo, K.; Lozano, R.; Moran, A.E. Global Overview of the Epidemiology of Atherosclerotic Cardiovascular Disease. Arch. Med. Res. 2015, 46, 328–338. [Google Scholar] [CrossRef] [PubMed]
- Saboya, P.P.; Bodanese, L.C.; Zimmermann, P.R.; da Silva Gustavo, A.; Macagnan, F.E.; Feoli, A.P.; da Silva Oliveira, M. Lifestyle Intervention on Metabolic Syndrome and its Impact on Quality of Life: A Randomized Controlled Trial. Arq. Bras. Cardiol. 2017, 108, 60–69. [Google Scholar] [CrossRef] [PubMed]
- VanWormer, J.J.; Boucher, J.L.; Sidebottom, A.C.; Sillah, A.; Knickelbine, T. Lifestyle changes and prevention of metabolic syndrome in the Heart of New Ulm Project. Prev. Med. Rep. 2017, 6, 242–245. [Google Scholar] [CrossRef]
- Silvestri, C.; Di Marzo, V. The Endocannabinoid System in Energy Homeostasis and the Etiopathology of Metabolic Disorders. Cell Metab. 2013, 17, 475–490. [Google Scholar] [CrossRef] [Green Version]
- Cristino, L.; Becker, T.; Di Marzo, V. Endocannabinoids and energy homeostasis: An update: Regolatory Role of Endocannabinoids in Obesity. BioFactors 2014, 40, 389–397. [Google Scholar] [CrossRef] [PubMed]
- Piscitelli, F.; Carta, G.; Bisogno, T.; Murru, E.; Cordeddu, L.; Berge, K.; Tandy, S.; Cohn, J.S.; Griinari, M.; Banni, S.; et al. Effect of dietary krill oil supplementation on the endocannabinoidome of metabolically relevant tissues from high-fat-fed mice. Nutr. Metab. (Lond.) 2011, 8, 51. [Google Scholar] [CrossRef] [PubMed]
- Osei-Hyiaman, D.; DePetrillo, M.; Pacher, P.; Liu, J.; Radaeva, S.; Bátkai, S.; Harvey-White, J.; Mackie, K.; Offertáler, L.; Wang, L.; et al. Endocannabinoid activation at hepatic CB1 receptors stimulates fatty acid synthesis and contributes to diet-induced obesity. J. Clin. Invest. 2005, 115, 1298–1305. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bäckhed, F.; Ding, H.; Wang, T.; Hooper, L.V.; Koh, G.Y.; Nagy, A.; Semenkovich, C.F.; Gordon, J.I. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. USA 2004, 101, 15718–15723. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Esteve, E.; Ricart, W.; Fernández-Real, J.-M. Gut microbiota interactions with obesity, insulin resistance and type 2 diabetes: Did gut microbiote co-evolve with insulin resistance? Curr. Opin. Clin. Nutr. Metab. Care 2011, 14, 483–490. [Google Scholar] [CrossRef]
- Ridaura, V.K.; Faith, J.J.; Rey, F.E.; Cheng, J.; Duncan, A.E.; Kau, A.L.; Griffin, N.W.; Lombard, V.; Henrissat, B.; Bain, J.R.; et al. Gut Microbiota from Twins Discordant for Obesity Modulate Metabolism in Mice. Science 2013, 341, 1241214. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cohen, L.J.; Esterhazy, D.; Kim, S.-H.; Lemetre, C.; Aguilar, R.R.; Gordon, E.A.; Pickard, A.J.; Cross, J.R.; Emiliano, A.B.; Han, S.M.; et al. Commensal bacteria make GPCR ligands that mimic human signalling molecules. Nature 2017, 549, 48–53. [Google Scholar] [CrossRef] [Green Version]
- Everard, A.; Plovier, H.; Rastelli, M.; Van Hul, M.; de Wouters d’Oplinter, A.; Geurts, L.; Druart, C.; Robine, S.; Delzenne, N.M.; Muccioli, G.G.; et al. Intestinal epithelial N-acylphosphatidylethanolamine phospholipase D links dietary fat to metabolic adaptations in obesity and steatosis. Nat. Commun. 2019, 10, 457. [Google Scholar] [CrossRef]
- Geurts, L.; Everard, A.; Van Hul, M.; Essaghir, A.; Duparc, T.; Matamoros, S.; Plovier, H.; Castel, J.; Denis, R.G.P.; Bergiers, M.; et al. Adipose tissue NAPE-PLD controls fat mass development by altering the browning process and gut microbiota. Nat. Commun. 2015, 6, 6495. [Google Scholar] [CrossRef] [Green Version]
- Song, J.-X.; Ren, H.; Gao, Y.-F.; Lee, C.-Y.; Li, S.-F.; Zhang, F.; Li, L.; Chen, H. Dietary Capsaicin Improves Glucose Homeostasis and Alters the Gut Microbiota in Obese Diabetic ob/ob Mice. Front. Physiol. 2017, 8, 602. [Google Scholar] [CrossRef] [Green Version]
- Mehrpouya-Bahrami, P.; Chitrala, K.N.; Ganewatta, M.S.; Tang, C.; Murphy, E.A.; Enos, R.T.; Velazquez, K.T.; McCellan, J.; Nagarkatti, M.; Nagarkatti, P. Blockade of CB1 cannabinoid receptor alters gut microbiota and attenuates inflammation and diet-induced obesity. Sci. Rep. 2017, 7, 15645. [Google Scholar] [CrossRef] [PubMed]
- Costantini, L.; Molinari, R.; Farinon, B.; Merendino, N. Impact of Omega-3 Fatty Acids on the Gut Microbiota. Int. J. Mol. Sci. 2017, 18, 2645. [Google Scholar] [CrossRef] [PubMed]
- Dahiya, D.K.; Renuka; Puniya, M.; Shandilya, U.K.; Dhewa, T.; Kumar, N.; Kumar, S.; Puniya, A.K.; Shukla, P. Gut Microbiota Modulation and Its Relationship with Obesity Using Prebiotic Fibers and Probiotics: A Review. Front. Microbiol. 2017, 8, 563. [Google Scholar] [CrossRef] [PubMed]
- Mailing, L.J.; Allen, J.M.; Buford, T.W.; Fields, C.J.; Woods, J.A. Exercise and the Gut Microbiome: A Review of the Evidence, Potential Mechanisms, and Implications for Human Health. Exerc. Sport Sci. Rev. 2019, 47, 75–85. [Google Scholar] [CrossRef] [PubMed]
- Pertwee, R.; Cascio, M.G. Chapter 6: Known Pharmacological Actions of Delta-9-Tetrahydrocannabinol and of Four Other Chemical Constituents of Cannabis that Activate Cannabinoid Receptors. In Handbook of Cannabis; Pertwee, R., Ed.; Oxford University Press: Oxford, UK, 2014; pp. 115–136. ISBN 978-0-19-178756-0. [Google Scholar]
- Devane, W.A.; Hanus, L.; Breuer, A.; Pertwee, R.G.; Stevenson, L.A.; Griffin, G.; Gibson, D.; Mandelbaum, A.; Etinger, A.; Mechoulam, R. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 1992, 258, 1946–1949. [Google Scholar] [CrossRef] [PubMed]
- Mechoulam, R.; Ben-Shabat, S.; Hanus, L.; Ligumsky, M.; Kaminski, N.E.; Schatz, A.R.; Gopher, A.; Almog, S.; Martin, B.R.; Compton, D.R. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem. Pharmacol. 1995, 50, 83–90. [Google Scholar] [CrossRef]
- Di Marzo, V.; De Petrocellis, L.; Bisogno, T. The biosynthesis, fate and pharmacological properties of endocannabinoids. Handb. Exp. Pharmacol. 2005, 147–185. [Google Scholar]
- Dinh, T.P.; Carpenter, D.; Leslie, F.M.; Freund, T.F.; Katona, I.; Sensi, S.L.; Kathuria, S.; Piomelli, D. Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc. Natl. Acad. Sci. USA 2002, 99, 10819–10824. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cravatt, B.F.; Giang, D.K.; Mayfield, S.P.; Boger, D.L.; Lerner, R.A.; Gilula, N.B. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 1996, 384, 83–87. [Google Scholar] [CrossRef]
- Bisogno, T.; Howell, F.; Williams, G.; Minassi, A.; Cascio, M.G.; Ligresti, A.; Matias, I.; Schiano-Moriello, A.; Paul, P.; Williams, E.-J.; et al. Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J. Cell Biol. 2003, 163, 463–468. [Google Scholar] [CrossRef]
- Okamoto, Y.; Morishita, J.; Tsuboi, K.; Tonai, T.; Ueda, N. Molecular Characterization of a Phospholipase D Generating Anandamide and Its Congeners. J. Biol. Chem. 2004, 279, 5298–5305. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Di Marzo, V. New approaches and challenges to targeting the endocannabinoid system. Nat. Rev. Drug Discov. 2018, 17, 623–639. [Google Scholar] [CrossRef] [PubMed]
- Simon, G.M.; Cravatt, B.F. Anandamide Biosynthesis Catalyzed by the Phosphodiesterase GDE1 and Detection of Glycerophospho-N-acyl Ethanolamine Precursors in Mouse Brain. J. Biol. Chem. 2008, 283, 9341–9349. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, J.; Wang, L.; Harvey-White, J.; Osei-Hyiaman, D.; Razdan, R.; Gong, Q.; Chan, A.C.; Zhou, Z.; Huang, B.X.; Kim, H.-Y.; et al. A biosynthetic pathway for anandamide. Proc. Natl. Acad. Sci. USA 2006, 103, 13345–13350. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Naughton, S.S.; Mathai, M.L.; Hryciw, D.H.; McAinch, A.J. Fatty Acid modulation of the endocannabinoid system and the effect on food intake and metabolism. Int. J. Endocrinol. 2013, 2013, 361895. [Google Scholar] [CrossRef] [PubMed]
- Bluher, M.; Engeli, S.; Kloting, N.; Berndt, J.; Fasshauer, M.; Batkai, S.; Pacher, P.; Schon, M.R.; Jordan, J.; Stumvoll, M. Dysregulation of the Peripheral and Adipose Tissue Endocannabinoid System in Human Abdominal Obesity. Diabetes 2006, 55, 3053–3060. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Côté, M.; Matias, I.; Lemieux, I.; Petrosino, S.; Alméras, N.; Després, J.-P.; Di Marzo, V. Circulating endocannabinoid levels, abdominal adiposity and related cardiometabolic risk factors in obese men. Int. J. Obes. 2007, 31, 692–699. [Google Scholar] [CrossRef] [Green Version]
- Engeli, S.; Böhnke, J.; Feldpausch, M.; Gorzelniak, K.; Janke, J.; Bátkai, S.; Pacher, P.; Harvey-White, J.; Luft, F.C.; Sharma, A.M.; et al. Activation of the Peripheral Endocannabinoid System in Human Obesity. Diabetes 2005, 54, 2838–2843. [Google Scholar] [CrossRef] [Green Version]
- Karvela, A.; Rojas-Gil, A.P.; Samkinidou, E.; Papadaki, H.; Pappa, A.; Georgiou, G.; Spiliotis, B.E. Endocannabinoid (EC) receptor, CB1, and EC enzymes’ expression in primary adipocyte cultures of lean and obese pre-pubertal children in relation to adiponectin and insulin. J. Pediatr. Endocrinol. Metab. 2010, 23, 1011–1024. [Google Scholar] [CrossRef]
- Pagano, C.; Pilon, C.; Calcagno, A.; Urbanet, R.; Rossato, M.; Milan, G.; Bianchi, K.; Rizzuto, R.; Bernante, P.; Federspil, G.; et al. The Endogenous Cannabinoid System Stimulates Glucose Uptake in Human Fat Cells via Phosphatidylinositol 3-Kinase and Calcium-Dependent Mechanisms. J. Clin. Endocrinol. Metab. 2007, 92, 4810–4819. [Google Scholar] [CrossRef] [Green Version]
- Diep, T.A.; Madsen, A.N.; Holst, B.; Kristiansen, M.M.; Wellner, N.; Hansen, S.H.; Hansen, H.S. Dietary fat decreases intestinal levels of the anorectic lipids through a fat sensor. FASEB J. 2011, 25, 765–774. [Google Scholar] [CrossRef] [PubMed]
- Aviello, G.; Matias, I.; Capasso, R.; Petrosino, S.; Borrelli, F.; Orlando, P.; Romano, B.; Capasso, F.; Di Marzo, V.; Izzo, A.A. Inhibitory effect of the anorexic compound oleoylethanolamide on gastric emptying in control and overweight mice. J. Mol. Med. 2008, 86, 413–422. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kuipers, E.N.; Kantae, V.; Maarse, B.C.E.; van den Berg, S.M.; van Eenige, R.; Nahon, K.J.; Reifel-Miller, A.; Coskun, T.; de Winther, M.P.J.; Lutgens, E.; et al. High Fat Diet Increases Circulating Endocannabinoids Accompanied by Increased Synthesis Enzymes in Adipose Tissue. Front. Physiol. 2019, 9, 1913. [Google Scholar] [CrossRef] [PubMed]
- Miranda, R.A.; De Almeida, M.M.; Rocha, C.P.D.D.; de Brito Fassarella, L.; De Souza, L.L.; Souza, A.F.P.D.; Andrade, C.B.V.D.; Fortunato, R.S.; Pazos-Moura, C.C.; Trevenzoli, I.H. Maternal high-fat diet consumption induces sex-dependent alterations of the endocannabinoid system and redox homeostasis in liver of adult rat offspring. Sci. Rep. 2018, 8, 14751. [Google Scholar] [CrossRef] [PubMed]
- Dias-Rocha, C.P.; Almeida, M.M.; Santana, E.M.; Costa, J.C.B.; Franco, J.G.; Pazos-Moura, C.C.; Trevenzoli, I.H. Maternal high-fat diet induces sex-specific endocannabinoid system changes in newborn rats and programs adiposity, energy expenditure and food preference in adulthood. J. Nutr. Biochem. 2018, 51, 56–68. [Google Scholar] [CrossRef] [PubMed]
- Kris-Etherton, P.M.; Taylor, D.S.; Yu-Poth, S.; Huth, P.; Moriarty, K.; Fishell, V.; Hargrove, R.L.; Zhao, G.; Etherton, T.D. Polyunsaturated fatty acids in the food chain in the United States. Am. J. Clin. Nutr. 2000, 71, 179S–188S. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alvheim, A.R.; Malde, M.K.; Osei-Hyiaman, D.; Lin, Y.H.; Pawlosky, R.J.; Madsen, L.; Kristiansen, K.; Frøyland, L.; Hibbeln, J.R. Dietary linoleic acid elevates endogenous 2-AG and anandamide and induces obesity. Obesity (Silver Spring) 2012, 20, 1984–1994. [Google Scholar] [CrossRef] [PubMed]
- Matias, I.; Petrosino, S.; Racioppi, A.; Capasso, R.; Izzo, A.A.; Di Marzo, V. Dysregulation of peripheral endocannabinoid levels in hyperglycemia and obesity: Effect of high fat diets. Mol. Cell. Endocrinol. 2008, 286, S66–S78. [Google Scholar] [CrossRef] [Green Version]
- Alvheim, A.R.; Torstensen, B.E.; Lin, Y.H.; Lillefosse, H.H.; Lock, E.-J.; Madsen, L.; Frøyland, L.; Hibbeln, J.R.; Malde, M.K. Dietary Linoleic Acid Elevates the Endocannabinoids 2-AG and Anandamide and Promotes Weight Gain in Mice Fed a Low Fat Diet. Lipids 2014, 49, 59–69. [Google Scholar] [CrossRef]
- Batetta, B.; Griinari, M.; Carta, G.; Murru, E.; Ligresti, A.; Cordeddu, L.; Giordano, E.; Sanna, F.; Bisogno, T.; Uda, S.; et al. Endocannabinoids may mediate the ability of (n-3) fatty acids to reduce ectopic fat and inflammatory mediators in obese Zucker rats. J. Nutr. 2009, 139, 1495–1501. [Google Scholar] [CrossRef]
- Rossmeisl, M.; Jilkova, Z.M.; Kuda, O.; Jelenik, T.; Medrikova, D.; Stankova, B.; Kristinsson, B.; Haraldsson, G.G.; Svensen, H.; Stoknes, I.; et al. Metabolic Effects of n-3 PUFA as Phospholipids Are Superior to Triglycerides in Mice Fed a High-Fat Diet: Possible Role of Endocannabinoids. PLoS ONE 2012, 7, e38834. [Google Scholar] [CrossRef] [PubMed]
- Berge, K.; Piscitelli, F.; Hoem, N.; Silvestri, C.; Meyer, I.; Banni, S.; Di Marzo, V. Chronic treatment with krill powder reduces plasma triglyceride and anandamide levels in mildly obese men. Lipids Health Dis. 2013, 12, 78. [Google Scholar] [CrossRef] [PubMed]
- Demizieux, L.; Piscitelli, F.; Troy-Fioramonti, S.; Iannotti, F.A.; Borrino, S.; Gresti, J.; Muller, T.; Bellenger, J.; Silvestri, C.; Di Marzo, V.; et al. Early Low-Fat Diet Enriched With Linolenic Acid Reduces Liver Endocannabinoid Tone and Improves Late Glycemic Control After a High-Fat Diet Challenge in Mice. Diabetes 2016, 65, 1824–1837. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pachikian, B.D.; Essaghir, A.; Demoulin, J.-B.; Neyrinck, A.M.; Catry, E.; De Backer, F.C.; Dejeans, N.; Dewulf, E.M.; Sohet, F.M.; Portois, L.; et al. Hepatic n-3 polyunsaturated fatty acid depletion promotes steatosis and insulin resistance in mice: Genomic analysis of cellular targets. PLoS ONE 2011, 6, e23365. [Google Scholar] [CrossRef] [PubMed]
- Berger, A.; Crozier, G.; Bisogno, T.; Cavaliere, P.; Innis, S.; Marzo, V.D. Anandamide and diet: Inclusion of dietary arachidonate and docosahexaenoate leads to increased brain levels of the corresponding N-acylethanolamines in piglets. Proc. Natl. Acad. Sci. USA 2001, 98, 6402–6406. [Google Scholar] [CrossRef] [PubMed]
- Artmann, A.; Petersen, G.; Hellgren, L.I.; Boberg, J.; Skonberg, C.; Nellemann, C.; Hansen, S.H.; Hansen, H.S. Influence of dietary fatty acids on endocannabinoid and N-acylethanolamine levels in rat brain, liver and small intestine. Biochimica et Biophysica Acta (BBA) Mol. Cell Biol. Lipids 2008, 1781, 200–212. [Google Scholar] [CrossRef] [PubMed]
- Ramsden, C.E.; Zamora, D.; Makriyannis, A.; Wood, J.T.; Mann, J.D.; Faurot, K.R.; MacIntosh, B.A.; Majchrzak-Hong, S.F.; Gross, J.R.; Courville, A.B.; et al. Diet-Induced Changes in n-3- and n-6-Derived Endocannabinoids and Reductions in Headache Pain and Psychological Distress. J. Pain 2015, 16, 707–716. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Verhoeckx, K.C.M.; Voortman, T.; Balvers, M.G.J.; Hendriks, H.F.J.; Wortelboer, H.M.; Witkamp, R.F. Presence, formation and putative biological activities of N-acyl serotonins, a novel class of fatty-acid derived mediators, in the intestinal tract. Biochimica et Biophysica Acta (BBA) Mol. Cell Biol. Lipids 2011, 1811, 578–586. [Google Scholar] [CrossRef] [PubMed]
- Arshad, A.; Chung, W.Y.; Steward, W.; Metcalfe, M.S.; Dennison, A.R. Reduction in circulating pro-angiogenic and pro-inflammatory factors is related to improved outcomes in patients with advanced pancreatic cancer treated with gemcitabine and intravenous omega-3 fish oil. HPB (Oxford) 2013, 15, 428–432. [Google Scholar] [CrossRef]
- Watson, J.E.; Kim, J.S.; Das, A. Emerging class of omega-3 fatty acid endocannabinoids & their derivatives. Prostaglandins Other Lipid Mediat. 2019, 143, 106337. [Google Scholar]
- Wainwright, C.L.; Michel, L. Endocannabinoid system as a potential mechanism for n-3 long-chain polyunsaturated fatty acid mediated cardiovascular protection. Proc. Nutr. Soc. 2013, 72, 460–469. [Google Scholar] [CrossRef] [PubMed]
- Meijerink, J.; Balvers, M.; Witkamp, R. N-Acyl amines of docosahexaenoic acid and other n-3 polyunsatured fatty acids—From fishy endocannabinoids to potential leads. Br. J. Pharmacol. 2013, 169, 772–783. [Google Scholar] [CrossRef] [PubMed]
- Rossmeisl, M.; Pavlisova, J.; Janovska, P.; Kuda, O.; Bardova, K.; Hansikova, J.; Svobodova, M.; Oseeva, M.; Veleba, J.; Kopecky, J.; et al. Differential modulation of white adipose tissue endocannabinoid levels by n-3 fatty acids in obese mice and type 2 diabetic patients. Biochimica et Biophysica Acta (BBA) Mol. Cell Biol. Lipids 2018, 1863, 712–725. [Google Scholar] [CrossRef] [PubMed]
- Moran, C.P.; Shanahan, F. Gut microbiota and obesity: Role in aetiology and potential therapeutic target. Best Pract. Res. Clin. Gastroenterol. 2014, 28, 585–597. [Google Scholar] [CrossRef] [PubMed]
- David, L.A.; Maurice, C.F.; Carmody, R.N.; Gootenberg, D.B.; Button, J.E.; Wolfe, B.E.; Ling, A.V.; Devlin, A.S.; Varma, Y.; Fischbach, M.A.; et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014, 505, 559–563. [Google Scholar] [CrossRef]
- Finucane, M.M.; Sharpton, T.J.; Laurent, T.J.; Pollard, K.S. A Taxonomic Signature of Obesity in the Microbiome? Getting to the Guts of the Matter. PLoS ONE 2014, 9, e84689. [Google Scholar] [CrossRef]
- Turnbaugh, P.J.; Hamady, M.; Yatsunenko, T.; Cantarel, B.L.; Duncan, A.; Ley, R.E.; Sogin, M.L.; Jones, W.J.; Roe, B.A.; Affourtit, J.P.; et al. A core gut microbiome in obese and lean twins. Nature 2009, 457, 480–484. [Google Scholar] [CrossRef]
- Kasselman, L.J.; Vernice, N.A.; DeLeon, J.; Reiss, A.B. The gut microbiome and elevated cardiovascular risk in obesity and autoimmunity. Atherosclerosis 2018, 271, 203–213. [Google Scholar] [CrossRef]
- Ascher, S.; Reinhardt, C. The gut microbiota: An emerging risk factor for cardiovascular and cerebrovascular disease. Eur. J. Immunol. 2018, 48, 564–575. [Google Scholar] [CrossRef] [PubMed]
- Ma, J.; Li, H. The Role of Gut Microbiota in Atherosclerosis and Hypertension. Front. Pharmacol. 2018, 9, 1082. [Google Scholar] [CrossRef]
- van den Munckhof, I.C.L.; Kurilshikov, A.; ter Horst, R.; Riksen, N.P.; Joosten, L.A.B.; Zhernakova, A.; Fu, J.; Keating, S.T.; Netea, M.G.; de Graaf, J.; et al. Role of gut microbiota in chronic low-grade inflammation as potential driver for atherosclerotic cardiovascular disease: A systematic review of human studies: Impact of gut microbiota on low-grade inflammation. Obes. Rev. 2018, 19, 1719–1734. [Google Scholar] [CrossRef] [PubMed]
- Zhou, W.; Sailani, M.R.; Contrepois, K.; Zhou, Y.; Ahadi, S.; Leopold, S.R.; Zhang, M.J.; Rao, V.; Avina, M.; Mishra, T.; et al. Longitudinal multi-omics of host–microbe dynamics in prediabetes. Nature 2019, 569, 663. [Google Scholar] [CrossRef] [PubMed]
- Rose, S.M.S.-F.; Contrepois, K.; Moneghetti, K.J.; Zhou, W.; Mishra, T.; Mataraso, S.; Dagan-Rosenfeld, O.; Ganz, A.B.; Dunn, J.; Hornburg, D.; et al. A longitudinal big data approach for precision health. Nat. Med. 2019, 25, 792. [Google Scholar]
- Cui, C.; Li, Y.; Gao, H.; Zhang, H.; Han, J.; Zhang, D.; Li, Y.; Zhou, J.; Lu, C.; Su, X. Modulation of the gut microbiota by the mixture of fish oil and krill oil in high-fat diet-induced obesity mice. PLoS ONE 2017, 12, e0186216. [Google Scholar] [CrossRef] [PubMed]
- Shen, W.; Gaskins, H.R.; McIntosh, M.K. Influence of dietary fat on intestinal microbes, inflammation, barrier function and metabolic outcomes. J. Nutr. Biochem. 2014, 25, 270–280. [Google Scholar] [CrossRef]
- Pu, S.; Khazanehei, H.; Jones, P.J.; Khafipour, E. Interactions between Obesity Status and Dietary Intake of Monounsaturated and Polyunsaturated Oils on Human Gut Microbiome Profiles in the Canola Oil Multicenter Intervention Trial (COMIT). Front. Microbiol. 2016, 7, 1612. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Everard, A.; Cani, P.D. Diabetes, obesity and gut microbiota. Best Pract. Res. Clin. Gastroenterol. 2013, 27, 73–83. [Google Scholar] [CrossRef] [Green Version]
- Muccioli, G.G.; Naslain, D.; Bäckhed, F.; Reigstad, C.S.; Lambert, D.M.; Delzenne, N.M.; Cani, P.D. The endocannabinoid system links gut microbiota to adipogenesis. Mol. Syst. Biol. 2010, 6, 392. [Google Scholar] [CrossRef]
- Cani, P.D.; Plovier, H.; Van Hul, M.; Geurts, L.; Delzenne, N.M.; Druart, C.; Everard, A. Endocannabinoids—At the crossroads between the gut microbiota and host metabolism. Nat. Rev. Endocrinol. 2016, 12, 133–143. [Google Scholar] [CrossRef]
- Veronese, N.; Solmi, M.; Caruso, M.G.; Giannelli, G.; Osella, A.R.; Evangelou, E.; Maggi, S.; Fontana, L.; Stubbs, B.; Tzoulaki, I. Dietary fiber and health outcomes: An umbrella review of systematic reviews and meta-analyses. Am. J. Clin. Nutr. 2018, 107, 436–444. [Google Scholar] [CrossRef]
- Ahmadi, S.; Mainali, R.; Nagpal, R.; Sheikh-Zeinoddin, M.; Soleimanian-Zad, S.; Wang, S.; Deep, G.; Kumar Mishra, S.; Yadav, H. Dietary Polysaccharides in the Amelioration of Gut Microbiome Dysbiosis and Metabolic Diseases. Obes. Control Ther. 2017, 4. [Google Scholar] [CrossRef]
- Bindels, L.B.; Delzenne, N.M.; Cani, P.D.; Walter, J. Towards a more comprehensive concept for prebiotics. Nat. Rev. Gastroenterol. Hepatol. 2015, 12, 303–310. [Google Scholar] [CrossRef] [PubMed]
- Cani, P.D.; Amar, J.; Iglesias, M.A.; Poggi, M.; Knauf, C.; Bastelica, D.; Neyrinck, A.M.; Fava, F.; Tuohy, K.M.; Chabo, C.; et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007, 56, 1761–1772. [Google Scholar] [CrossRef] [PubMed]
- Cani, P.D.; Bibiloni, R.; Knauf, C.; Waget, A.; Neyrinck, A.M.; Delzenne, N.M.; Burcelin, R. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 2008, 57, 1470–1481. [Google Scholar] [CrossRef] [PubMed]
- Cani, P.D.; Possemiers, S.; Van de Wiele, T.; Guiot, Y.; Everard, A.; Rottier, O.; Geurts, L.; Naslain, D.; Neyrinck, A.; Lambert, D.M.; et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 2009, 58, 1091–1103. [Google Scholar] [CrossRef] [Green Version]
- Everard, A.; Belzer, C.; Geurts, L.; Ouwerkerk, J.P.; Druart, C.; Bindels, L.B.; Guiot, Y.; Derrien, M.; Muccioli, G.G.; Delzenne, N.M.; et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. USA 2013, 110, 9066–9071. [Google Scholar] [CrossRef]
- Dehghan, P.; Pourghassem Gargari, B.; Asghari Jafar-abadi, M. Oligofructose-enriched inulin improves some inflammatory markers and metabolic endotoxemia in women with type 2 diabetes mellitus: A randomized controlled clinical trial. Nutrition 2014, 30, 418–423. [Google Scholar] [CrossRef]
- Depommier, C.; Everard, A.; Druart, C.; Plovier, H.; Hul, M.V.; Vieira-Silva, S.; Falony, G.; Raes, J.; Maiter, D.; Delzenne, N.M.; et al. Supplementation with Akkermansia muciniphila in overweight and obese human volunteers: A proof-of-concept exploratory study. Nat. Med. 2019, 25, 1096. [Google Scholar] [CrossRef]
- Jourdan, T.; Szanda, G.; Cinar, R.; Godlewski, G.; Holovac, D.J.; Park, J.K.; Nicoloro, S.; Shen, Y.; Liu, J.; Rosenberg, A.Z.; et al. Developmental Role of Macrophage Cannabinoid-1 Receptor Signaling in Type 2 Diabetes. Diabetes 2017, 66, 994–1007. [Google Scholar] [CrossRef] [Green Version]
- Jourdan, T.; Godlewski, G.; Cinar, R.; Bertola, A.; Szanda, G.; Liu, J.; Tarn, J.; Han, T.; Mukhopadhyay, B.; Skarulis, M.C.; et al. Activation of the Nlrp3 inflammasome in infiltrating macrophages by endocannabinoids mediates beta cell loss in type 2 diabetes. Nat. Med. 2013, 19, 1132–1140. [Google Scholar] [CrossRef] [Green Version]
- Lv, J.; Qi, L.; Yu, C.; Yang, L.; Guo, Y.; Chen, Y.; Bian, Z.; Sun, D.; Du, J.; Ge, P.; et al. Consumption of spicy foods and total and cause specific mortality: Population based cohort study. BMJ 2015, 351, h3942. [Google Scholar] [CrossRef] [PubMed]
- Yuan, L.-J.; Qin, Y.; Wang, L.; Zeng, Y.; Chang, H.; Wang, J.; Wang, B.; Wan, J.; Chen, S.-H.; Zhang, Q.-Y.; et al. Capsaicin-containing chili improved postprandial hyperglycemia, hyperinsulinemia, and fasting lipid disorders in women with gestational diabetes mellitus and lowered the incidence of large-for-gestational-age newborns. Clin. Nutr. 2016, 35, 388–393. [Google Scholar] [CrossRef] [PubMed]
- Kroff, J.; Hume, D.J.; Pienaar, P.; Tucker, R.; Lambert, E.V.; Rae, D.E. The metabolic effects of a commercially available chicken peri-peri (African bird’s eye chilli) meal in overweight individuals. Br. J. Nutr. 2017, 117, 635–644. [Google Scholar] [CrossRef] [PubMed]
- Dömötör, A.; Szolcsányi, J.; Mózsik, G. Capsaicin and glucose absorption and utilization in healthy human subjects. Eur. J. Pharmacol. 2006, 534, 280–283. [Google Scholar] [CrossRef] [PubMed]
- Ludy, M.-J.; Moore, G.E.; Mattes, R.D. The Effects of Capsaicin and Capsiate on Energy Balance: Critical Review and Meta-analyses of Studies in Humans. Chem. Senses 2012, 37, 103–121. [Google Scholar] [CrossRef] [PubMed]
- Kang, J.-H.; Tsuyoshi, G.; Han, I.-S.; Kawada, T.; Kim, Y.M.; Yu, R. Dietary Capsaicin Reduces Obesity-induced Insulin Resistance and Hepatic Steatosis in Obese Mice Fed a High-fat Diet. Obesity 2010, 18, 780–787. [Google Scholar] [CrossRef]
- Zhang, L.L.; Yan Liu, D.; Ma, L.Q.; Luo, Z.D.; Cao, T.B.; Zhong, J.; Yan, Z.C.; Wang, L.J.; Zhao, Z.G.; Zhu, S.J.; et al. Activation of Transient Receptor Potential Vanilloid Type-1 Channel Prevents Adipogenesis and Obesity. Circ. Res. 2007, 100, 1063–1070. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Motter, A.L.; Ahern, G.P. TRPV1-null mice are protected from diet-induced obesity. FEBS Lett. 2008, 582, 2257–2262. [Google Scholar] [CrossRef] [Green Version]
- Lee, E.; Jung, D.Y.; Kim, J.H.; Patel, P.R.; Hu, X.; Lee, Y.; Azuma, Y.; Wang, H.-F.; Tsitsilianos, N.; Shafiq, U.; et al. Transient receptor potential vanilloid type-1 channel regulates diet-induced obesity, insulin resistance, and leptin resistance. FASEB J. 2015, 29, 3182–3192. [Google Scholar] [CrossRef] [Green Version]
- Wanner, S.P.; Garami, A.; Romanovsky, A.A. Hyperactive when young, hypoactive and overweight when aged: Connecting the dots in the story about locomotor activity, body mass, and aging in Trpv1 knockout mice. Aging (Albany NY) 2011, 3, 450–454. [Google Scholar] [CrossRef] [Green Version]
- Baboota, R.K.; Murtaza, N.; Jagtap, S.; Singh, D.P.; Karmase, A.; Kaur, J.; Bhutani, K.K.; Boparai, R.K.; Premkumar, L.S.; Kondepudi, K.K.; et al. Capsaicin-induced transcriptional changes in hypothalamus and alterations in gut microbial count in high fat diet fed mice. J. Nutr. Biochem. 2014, 25, 893–902. [Google Scholar] [CrossRef] [PubMed]
- Shen, W.; Shen, M.; Zhao, X.; Zhu, H.; Yang, Y.; Lu, S.; Tan, Y.; Li, G.; Li, M.; Wang, J.; et al. Anti-obesity Effect of Capsaicin in Mice Fed with High-Fat Diet Is Associated with an Increase in Population of the Gut Bacterium Akkermansia muciniphila. Front. Microbiol. 2017, 8, 272. [Google Scholar] [CrossRef] [PubMed]
- Kang, C.; Wang, B.; Kaliannan, K.; Wang, X.; Lang, H.; Hui, S.; Huang, L.; Zhang, Y.; Zhou, M.; Chen, M.; et al. Gut Microbiota Mediates the Protective Effects of Dietary Capsaicin against Chronic Low-Grade Inflammation and Associated Obesity Induced by High-Fat Diet. mBio 2017, 8, e00470-17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Karwad, M.A.; Macpherson, T.; Wang, B.; Theophilidou, E.; Sarmad, S.; Barrett, D.A.; Larvin, M.; Wright, K.L.; Lund, J.N.; O’Sullivan, S.E. Oleoylethanolamine and palmitoylethanolamine modulate intestinal permeability in vitro via TRPV1 and PPARα. FASEB J. 2017, 31, 469–481. [Google Scholar] [CrossRef] [PubMed]
- Kang, C.; Zhang, Y.; Zhu, X.; Liu, K.; Wang, X.; Chen, M.; Wang, J.; Chen, H.; Hui, S.; Huang, L.; et al. Healthy Subjects Differentially Respond to Dietary Capsaicin Correlating with Specific Gut Enterotypes. J. Clin. Endocrinol. Metab. 2016, 101, 4681–4689. [Google Scholar] [CrossRef] [Green Version]
- Perez-Burgos, A.; Wang, L.; McVey Neufeld, K.-A.; Mao, Y.-K.; Ahmadzai, M.; Janssen, L.J.; Stanisz, A.M.; Bienenstock, J.; Kunze, W.A. The TRPV1 channel in rodents is a major target for antinociceptive effect of the probiotic Lactobacillus reuteri DSM 17938. J. Physiol. 2015, 593, 3943–3957. [Google Scholar] [CrossRef]
- Holick, M.F.; Chen, T.C. Vitamin D deficiency: A worldwide problem with health consequences. Am. J. Clin. Nutr. 2008, 87, 1080S–1086S. [Google Scholar] [CrossRef]
- Al-Dabhani, K.; Tsilidis, K.K.; Murphy, N.; Ward, H.A.; Elliott, P.; Riboli, E.; Gunter, M.; Tzoulaki, I. Prevalence of vitamin D deficiency and association with metabolic syndrome in a Qatari population. Nutr. Diabetes 2017, 7, e263. [Google Scholar] [CrossRef]
- Moon, R.J.; Curtis, E.M.; Cooper, C.; Davies, J.H.; Harvey, N.C. Vitamin D supplementation: Are multivitamins sufficient? Arch. Dis. Child. 2019. [Google Scholar] [CrossRef]
- Strange, R.C.; Shipman, K.E.; Ramachandran, S. Metabolic syndrome: A review of the role of vitamin D in mediating susceptibility and outcome. World J. Diabetes 2015, 6, 896–911. [Google Scholar] [CrossRef]
- Su, D.; Nie, Y.; Zhu, A.; Chen, Z.; Wu, P.; Zhang, L.; Luo, M.; Sun, Q.; Cai, L.; Lai, Y.; et al. Vitamin D Signaling through Induction of Paneth Cell Defensins Maintains Gut Microbiota and Improves Metabolic Disorders and Hepatic Steatosis in Animal Models. Front. Physiol. 2016, 7, 498. [Google Scholar] [CrossRef] [PubMed]
- Ooi, J.H.; Li, Y.; Rogers, C.J.; Cantorna, M.T. Vitamin D regulates the gut microbiome and protects mice from dextran sodium sulfate-induced colitis. J. Nutr. 2013, 143, 1679–1686. [Google Scholar] [CrossRef] [PubMed]
- Ghaly, S.; Kaakoush, N.O.; Lloyd, F.; Gordon, L.; Forest, C.; Lawrance, I.C.; Hart, P.H. Ultraviolet Irradiation of Skin Alters the Faecal Microbiome Independently of Vitamin D in Mice. Nutrients 2018, 10, 1069. [Google Scholar] [CrossRef] [PubMed]
- Bikle, D. Vitamin D: Production, Metabolism, and Mechanisms of Action. In Endotext; Feingold, K.R., Anawalt, B., Boyce, A., Chrousos, G., Dungan, K., Grossman, A., Hershman, J.M., Kaltsas, G., Koch, C., et al., Eds.; MDText.com, Inc.: South Dartmouth, MA, USA, 2000. [Google Scholar]
- Kendall, A.C.; Pilkington, S.M.; Massey, K.A.; Sassano, G.; Rhodes, L.E.; Nicolaou, A. Distribution of Bioactive Lipid Mediators in Human Skin. J. Invest. Dermatol. 2015, 135, 1510–1520. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Magina, S.; Esteves-Pinto, C.; Moura, E.; Serrão, M.P.; Moura, D.; Petrosino, S.; Di Marzo, V.; Vieira-Coelho, M.A. Inhibition of basal and ultraviolet B-induced melanogenesis by cannabinoid CB1 receptors: A keratinocyte-dependent effect. Arch. Dermatol. Res. 2011, 303, 201–210. [Google Scholar] [CrossRef] [PubMed]
- Felton, S.J.; Kendall, A.C.; Almaedani, A.F.M.; Urquhart, P.; Webb, A.R.; Kift, R.; Vail, A.; Nicolaou, A.; Rhodes, L.E. Serum endocannabinoids and N-acyl ethanolamines and the influence of simulated solar UVR exposure in humans in vivo. Photochem. Photobiol. Sci. 2017, 16, 564–574. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Magina, S.; Vieira-Coelho, M.A.; Moura, E.; Serrão, M.P.; Piscitelli, F.; Moura, D.; Di Marzo, V. Effect of narrowband ultraviolet B treatment on endocannabinoid plasma levels in patients with psoriasis. Br. J. Dermatol. 2014, 171, 198–201. [Google Scholar] [CrossRef] [PubMed]
- Guida, F.; Boccella, S.; Belardo, C.; Iannotta, M.; Piscitelli, F.; De Filippis, F.; Paino, S.; Ricciardi, F.; Siniscalco, D.; Marabese, I.; et al. Altered gut microbiota and endocannabinoid system tone in vitamin D deficiency-mediated chronic pain. Brain Behav. Immunity 2019. [Google Scholar] [CrossRef]
- Di Marzo, V.; Côté, M.; Matias, I.; Lemieux, I.; Arsenault, B.J.; Cartier, A.; Piscitelli, F.; Petrosino, S.; Alméras, N.; Després, J.-P. Changes in plasma endocannabinoid levels in viscerally obese men following a 1 year lifestyle modification programme and waist circumference reduction: Associations with changes in metabolic risk factors. Diabetologia 2009, 52, 213–217. [Google Scholar] [CrossRef]
- Gasperi, V.; Ceci, R.; Tantimonaco, M.; Talamonti, E.; Battista, N.; Parisi, A.; Florio, R.; Sabatini, S.; Rossi, A.; Maccarrone, M. The Fatty Acid Amide Hydrolase in Lymphocytes from Sedentary and Active Subjects. Med. Sci. Sports Exerc. 2014, 46, 24–32. [Google Scholar] [CrossRef]
- Fernández-Aranda, F.; Sauchelli, S.; Pastor, A.; Gonzalez, M.L.; de la Torre, R.; Granero, R.; Jiménez-Murcia, S.; Baños, R.; Botella, C.; Fernández-Real, J.M.; et al. Moderate-Vigorous Physical Activity across Body Mass Index in Females: Moderating Effect of Endocannabinoids and Temperament. PLoS ONE 2014, 9, e104534. [Google Scholar] [CrossRef] [PubMed]
- Raichlen, D.A.; Foster, A.D.; Seillier, A.; Giuffrida, A.; Gerdeman, G.L. Exercise-induced endocannabinoid signaling is modulated by intensity. Eur. J. Appl. Physiol. 2013, 113, 869–875. [Google Scholar] [CrossRef] [PubMed]
- Raichlen, D.A.; Foster, A.D.; Gerdeman, G.L.; Seillier, A.; Giuffrida, A. Wired to run: Exercise-induced endocannabinoid signaling in humans and cursorial mammals with implications for the “runner’s high”. J. Exp. Biol. 2012, 215, 1331–1336. [Google Scholar] [CrossRef] [PubMed]
- Heyman, E.; Gamelin, F.-X.; Goekint, M.; Piscitelli, F.; Roelands, B.; Leclair, E.; Di Marzo, V.; Meeusen, R. Intense exercise increases circulating endocannabinoid and BDNF levels in humans—Possible implications for reward and depression. Psychoneuroendocrinology 2012, 37, 844–851. [Google Scholar] [CrossRef] [PubMed]
- Heyman, E.; Gamelin, F.-X.; Aucouturier, J.; Marzo, V.D. The role of the endocannabinoid system in skeletal muscle and metabolic adaptations to exercise: Potential implications for the treatment of obesity. Obes. Rev. 2012, 13, 1110–1124. [Google Scholar] [CrossRef] [PubMed]
- Cedernaes, J.; Fanelli, F.; Fazzini, A.; Pagotto, U.; Broman, J.-E.; Vogel, H.; Dickson, S.L.; Schiöth, H.B.; Benedict, C. Sleep restriction alters plasma endocannabinoids concentrations before but not after exercise in humans. Psychoneuroendocrinology 2016, 74, 258–268. [Google Scholar] [CrossRef] [PubMed]
- Gamelin, F.-X.; Aucouturier, J.; Iannotti, F.A.; Piscitelli, F.; Mazzarella, E.; Aveta, T.; Leriche, M.; Dupont, E.; Cieniewski-Bernard, C.; Montel, V.; et al. Effects of chronic exercise on the endocannabinoid system in Wistar rats with high-fat diet-induced obesity. J. Physiol. Biochem. 2016, 72, 183–199. [Google Scholar] [CrossRef] [PubMed]
- Mikkelsen, K.; Stojanovska, L.; Polenakovic, M.; Bosevski, M.; Apostolopoulos, V. Exercise and mental health. Maturitas 2017, 106, 48–56. [Google Scholar] [CrossRef] [PubMed]
- Fuss, J.; Steinle, J.; Bindila, L.; Auer, M.K.; Kirchherr, H.; Lutz, B.; Gass, P. A runner’s high depends on cannabinoid receptors in mice. Proc. Natl. Acad. Sci. USA 2015, 112, 13105–13108. [Google Scholar] [CrossRef]
- Hill, M.N.; Titterness, A.K.; Morrish, A.C.; Carrier, E.J.; Lee, T.T.-Y.; Gil-Mohapel, J.; Gorzalka, B.B.; Hillard, C.J.; Christie, B.R. Endogenous cannabinoid signaling is required for voluntary exercise-induced enhancement of progenitor cell proliferation in the hippocampus. Hippocampus 2010, 20, 513–523. [Google Scholar] [CrossRef] [PubMed]
- De Chiara, V.; Errico, F.; Musella, A.; Rossi, S.; Mataluni, G.; Sacchetti, L.; Siracusano, A.; Castelli, M.; Cavasinni, F.; Bernardi, G.; et al. Voluntary exercise and sucrose consumption enhance cannabinoid CB1 receptor sensitivity in the striatum. Neuropsychopharmacology 2010, 35, 374–387. [Google Scholar] [CrossRef] [PubMed]
- Swenson, S.; Hamilton, J.; Robison, L.; Thanos, P.K. Chronic aerobic exercise: Lack of effect on brain CB1 receptor levels in adult rats. Life Sci. 2019, 230, 84–88. [Google Scholar] [CrossRef] [PubMed]
- Stone, N.L.; Millar, S.A.; Herrod, P.J.J.; Barrett, D.A.; Ortori, C.A.; Mellon, V.A.; O’Sullivan, S.E. An Analysis of Endocannabinoid Concentrations and Mood Following Singing and Exercise in Healthy Volunteers. Front. Behav. Neurosci. 2018, 12, 269. [Google Scholar] [CrossRef] [PubMed]
- Antunes, H.K.M.; Leite, G.S.F.; Lee, K.S.; Barreto, A.T.; dos Santos, R.V.T.; de Sá Souza, H.; Tufik, S.; de Mello, M.T. Exercise deprivation increases negative mood in exercise-addicted subjects and modifies their biochemical markers. Physiol. Behav. 2016, 156, 182–190. [Google Scholar] [CrossRef] [PubMed]
- Hsu, Y.J.; Chiu, C.C.; Li, Y.P.; Huang, W.C.; Huang, Y.T.; Huang, C.C.; Chuang, H.L. Effect of Intestinal Microbiota on Exercise Performance in Mice. J. Strength Cond. Res. 2015, 29, 552–558. [Google Scholar] [CrossRef] [PubMed]
- Petriz, B.A.; Castro, A.P.; Almeida, J.A.; Gomes, C.P.; Fernandes, G.R.; Kruger, R.H.; Pereira, R.W.; Franco, O.L. Exercise induction of gut microbiota modifications in obese, non-obese and hypertensive rats. BMC Genom. 2014, 15, 511. [Google Scholar] [CrossRef] [PubMed]
- Denou, E.; Marcinko, K.; Surette, M.G.; Steinberg, G.R.; Schertzer, J.D. High-intensity exercise training increases the diversity and metabolic capacity of the mouse distal gut microbiota during diet-induced obesity. Am. J. Physiol.-Endocrinol. Metab. 2016, 310, E982–E993. [Google Scholar] [CrossRef]
- Lai, Z.-L.; Tseng, C.-H.; Ho, H.J.; Cheung, C.K.Y.; Lin, J.-Y.; Chen, Y.-J.; Cheng, F.-C.; Hsu, Y.-C.; Lin, J.-T.; El-Omar, E.M.; et al. Fecal microbiota transplantation confers beneficial metabolic effects of diet and exercise on diet-induced obese mice. Sci. Rep. 2018, 8, 15625. [Google Scholar] [CrossRef]
- Maillard, F.; Vazeille, E.; Sauvanet, P.; Sirvent, P.; Combaret, L.; Sourdrille, A.; Chavanelle, V.; Bonnet, R.; Otero, Y.F.; Delcros, G.; et al. High intensity interval training promotes total and visceral fat mass loss in obese Zucker rats without modulating gut microbiota. PLoS ONE 2019, 14, e0214660. [Google Scholar] [CrossRef]
- Barton, W.; Penney, N.C.; Cronin, O.; Garcia-Perez, I.; Molloy, M.G.; Holmes, E.; Shanahan, F.; Cotter, P.D.; O’Sullivan, O. The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level. Gut 2017. [Google Scholar] [CrossRef]
- Clarke, S.F.; Murphy, E.F.; O’Sullivan, O.; Lucey, A.J.; Humphreys, M.; Hogan, A.; Hayes, P.; O’Reilly, M.; Jeffery, I.B.; Wood-Martin, R.; et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut 2014, 63, 1913–1920. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Estaki, M.; Pither, J.; Baumeister, P.; Little, J.P.; Gill, S.K.; Ghosh, S.; Ahmadi-Vand, Z.; Marsden, K.R.; Gibson, D.L. Cardiorespiratory fitness as a predictor of intestinal microbial diversity and distinct metagenomic functions. Microbiome 2016, 4, 42. [Google Scholar] [CrossRef] [PubMed]
- Munukka, E.; Ahtiainen, J.P.; Puigbó, P.; Jalkanen, S.; Pahkala, K.; Keskitalo, A.; Kujala, U.M.; Pietilä, S.; Hollmén, M.; Elo, L.; et al. Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women. Front. Microbiol. 2018, 9, 2323. [Google Scholar] [CrossRef] [PubMed]
- Cristiano, C.; Pirozzi, C.; Coretti, L.; Cavaliere, G.; Lama, A.; Russo, R.; Lembo, F.; Mollica, M.P.; Meli, R.; Calignano, A.; et al. Palmitoylethanolamide counteracts autistic-like behaviours in BTBR T+tf/J mice: Contribution of central and peripheral mechanisms. Brain Behav. Immunity 2018, 74, 166–175. [Google Scholar] [CrossRef] [PubMed]
- Vidot, D.C.; Prado, G.; Hlaing, W.M.; Florez, H.J.; Arheart, K.L.; Messiah, S.E. Metabolic Syndrome among Marijuana Users in the United States: An Analysis of National Health and Nutrition Examination Survey Data. Am. J. Med. 2016, 129, 173–179. [Google Scholar] [CrossRef] [PubMed]
- Le Strat, Y.; Le Foll, B. Obesity and Cannabis Use: Results from 2 Representative National Surveys. Am. J. Epidemiol. 2011, 174, 929–933. [Google Scholar] [CrossRef] [PubMed]
- Alshaarawy, O.; Anthony, J.C. Are cannabis users less likely to gain weight? Results from a national 3-year prospective study. Int. J. Epidemiol. 2019. [Google Scholar] [CrossRef] [PubMed]
- Penner, E.A.; Buettner, H.; Mittleman, M.A. The Impact of Marijuana Use on Glucose, Insulin, and Insulin Resistance among US Adults. Am. J. Med. 2013, 126, 583–589. [Google Scholar] [CrossRef]
- Alshaarawy, O.; Anthony, J.C. Cannabis Smoking and Diabetes Mellitus: Results from Meta-Analysis with Eight Independent Replication Samples. Epidemiology 2015, 26, 597–600. [Google Scholar] [CrossRef]
- Rajavashisth, T.B.; Shaheen, M.; Norris, K.C.; Pan, D.; Sinha, S.K.; Ortega, J.; Friedman, T.C. Decreased prevalence of diabetes in marijuana users: Cross-sectional data from the National Health and Nutrition Examination Survey (NHANES) III. BMJ Open 2012, 2, e000494. [Google Scholar] [CrossRef]
- Danielsson, A.K.; Lundin, A.; Yaregal, A.; Östenson, C.G.; Allebeck, P.; Agardh, E.E. Cannabis Use as Risk or Protection for Type 2 Diabetes: A Longitudinal Study of 18 000 Swedish Men and Women. J. Diabetes Res. 2016, 2016, 1–6. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ngueta, G.; Bélanger, R.E.; Laouan-Sidi, E.A.; Lucas, M. Cannabis use in relation to obesity and insulin resistance in the inuit population. Obesity 2015, 23, 290–295. [Google Scholar] [CrossRef] [PubMed]
- Adejumo, A.C.; Ajayi, T.O.; Adegbala, O.M.; Adejumo, K.L.; Alliu, S.; Akinjero, A.M.; Onyeakusi, N.E.; Ojelabi, O.; Bukong, T.N. Cannabis use is associated with reduced prevalence of progressive stages of alcoholic liver disease. Liver Int. 2018, 38, 1475–1486. [Google Scholar] [CrossRef] [PubMed]
- Adejumo, A.C.; Alliu, S.; Ajayi, T.O.; Adejumo, K.L.; Adegbala, O.M.; Onyeakusi, N.E.; Akinjero, A.M.; Durojaiye, M.; Bukong, T.N. Cannabis use is associated with reduced prevalence of non-alcoholic fatty liver disease: A cross-sectional study. PLoS ONE 2017, 12, e0176416. [Google Scholar] [CrossRef] [PubMed]
- Akturk, H.K.; Taylor, D.D.; Camsari, U.M.; Rewers, A.; Kinney, G.L.; Shah, V.N. Association Between Cannabis Use and Risk for Diabetic Ketoacidosis in Adults With Type 1 Diabetes. JAMA Intern. Med. 2019, 179, 115. [Google Scholar] [CrossRef] [PubMed]
- Auer, R.; Sidney, S.; Goff, D.; Vittinghoff, E.; Pletcher, M.J.; Allen, N.B.; Reis, J.P.; Lewis, C.E.; Carr, J.; Rana, J.S. Lifetime marijuana use and subclinical atherosclerosis: The Coronary Artery Risk Development in Young Adults (CARDIA) study. Addiction 2018, 113, 845–856. [Google Scholar] [CrossRef]
- DeFilippis, E.M.; Singh, A.; Divakaran, S.; Gupta, A.; Collins, B.L.; Biery, D.; Qamar, A.; Fatima, A.; Ramsis, M.; Pipilas, D.; et al. Cocaine and Marijuana Use Among Young Adults With Myocardial Infarction. J. Am. Coll. Cardiol. 2018, 71, 2540–2551. [Google Scholar] [CrossRef] [PubMed]
- Villares, J. Chronic use of marijuana decreases cannabinoid receptor binding and mRNA expression in the human brain. Neuroscience 2007, 145, 323–334. [Google Scholar] [CrossRef]
- Ceccarini, J.; Kuepper, R.; Kemels, D.; van Os, J.; Henquet, C.; Laere, K.V. [18F]MK-9470 PET measurement of cannabinoid CB1 receptor availability in chronic cannabis users. Addict. Biol. 2015, 20, 357–367. [Google Scholar] [CrossRef]
- Marzo, V.D.; Berrendero, F.; Bisogno, T.; González, S.; Cavaliere, P.; Romero, J.; Cebeira, M.; Ramos, J.A.; Fernández-Ruiz, J.J. Enhancement of Anandamide Formation in the Limbic Forebrain and Reduction of Endocannabinoid Contents in the Striatum of Δ9-Tetrahydrocannabinol-Tolerant Rats. J. Neurochem. 2000, 74, 1627–1635. [Google Scholar] [CrossRef]
- Morgan, C.J.A.; Page, E.; Schaefer, C.; Chatten, K.; Manocha, A.; Gulati, S.; Curran, H.V.; Brandner, B.; Leweke, F.M. Cerebrospinal fluid anandamide levels, cannabis use and psychotic-like symptoms. Br. J. Psychiatry 2013, 202, 381–382. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maia, J.; Midão, L.; Cunha, S.C.; Almada, M.; Fonseca, B.M.; Braga, J.; Gonçalves, D.; Teixeira, N.; Correia-da-Silva, G. Effects of cannabis tetrahydrocannabinol on endocannabinoid homeostasis in human placenta. Arch. Toxicol. 2019, 93, 649–658. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McIntosh, A.L.; Martin, G.G.; Huang, H.; Landrock, D.; Kier, A.B.; Schroeder, F. Δ9-Tetrahydrocannabinol induces endocannabinoid accumulation in mouse hepatocytes: Antagonism by Fabp1 gene ablation. J. Lipid Res. 2018, 59, 646–657. [Google Scholar] [CrossRef] [PubMed]
- De Petrocellis, L.; Ligresti, A.; Moriello, A.S.; Allarà, M.; Bisogno, T.; Petrosino, S.; Stott, C.G.; Di Marzo, V. Effects of cannabinoids and cannabinoid-enriched Cannabis extracts on TRP channels and endocannabinoid metabolic enzymes. Br. J. Pharmacol. 2011, 163, 1479–1494. [Google Scholar] [CrossRef] [PubMed]
- Cluny, N.L.; Keenan, C.M.; Reimer, R.A.; Le Foll, B.; Sharkey, K.A. Prevention of Diet-Induced Obesity Effects on Body Weight and Gut Microbiota in Mice Treated Chronically with Δ9-Tetrahydrocannabinol. PLoS ONE 2015, 10, e0144270. [Google Scholar] [CrossRef] [PubMed]
- Wargent, E.T.; Zaibi, M.S.; Silvestri, C.; Hislop, D.C.; Stocker, C.J.; Stott, C.G.; Guy, G.W.; Duncan, M.; Di Marzo, V.; Cawthorne, M.A. The cannabinoid Δ9-tetrahydrocannabivarin (THCV) ameliorates insulin sensitivity in two mouse models of obesity. Nutr. Diabetes 2013, 3, e68. [Google Scholar] [CrossRef] [PubMed]
- Weiss, L.; Zeira, M.; Reich, S.; Har-Noy, M.; Mechoulam, R.; Slavin, S.; Gallily, R. Cannabidiol lowers incidence of diabetes in non-obese diabetic mice. Autoimmunity 2006, 39, 143–151. [Google Scholar] [CrossRef] [Green Version]
- Jadoon, K.A.; Ratcliffe, S.H.; Barrett, D.A.; Thomas, E.L.; Stott, C.; Bell, J.D.; O’Sullivan, S.E.; Tan, G.D. Efficacy and Safety of Cannabidiol and Tetrahydrocannabivarin on Glycemic and Lipid Parameters in Patients With Type 2 Diabetes: A Randomized, Double-Blind, Placebo-Controlled, Parallel Group Pilot Study. Diabetes Care 2016, 39, 1777–1786. [Google Scholar] [CrossRef] [Green Version]
- Silvestri, C.; Paris, D.; Martella, A.; Melck, D.; Guadagnino, I.; Cawthorne, M.; Motta, A.; Di Marzo, V. Two non-psychoactive cannabinoids reduce intracellular lipid levels and inhibit hepatosteatosis. J. Hepatol. 2015, 62, 1382–1390. [Google Scholar] [CrossRef]
- Le Bastard, Q.; Al-Ghalith, G.A.; Grégoire, M.; Chapelet, G.; Javaudin, F.; Dailly, E.; Batard, E.; Knights, D.; Montassier, E. Systematic review: Human gut dysbiosis induced by non-antibiotic prescription medications. Aliment. Pharmacol. Ther. 2018, 47, 332–345. [Google Scholar] [CrossRef]
- Panee, J.; Gerschenson, M.; Chang, L. Associations between Microbiota, Mitochondrial Function, and Cognition in Chronic Marijuana Users. J. Neuroimmune Pharmacol. 2018, 13, 113–122. [Google Scholar] [CrossRef] [PubMed]
- Wu, G.D.; Chen, J.; Hoffmann, C.; Bittinger, K.; Chen, Y.-Y.; Keilbaugh, S.A.; Bewtra, M.; Knights, D.; Walters, W.A.; Knight, R.; et al. Linking Long-Term Dietary Patterns with Gut Microbial Enterotypes. Science 2011, 334, 105–108. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Smit, E.; Crespo, C.J. Dietary intake and nutritional status of US adult marijuana users: Results from the Third National Health and Nutrition Examination Survey. Public Health Nutr. 2001, 4, 781–786. [Google Scholar] [CrossRef] [PubMed]
- Fulcher, J.A.; Hussain, S.K.; Cook, R.; Li, F.; Tobin, N.H.; Ragsdale, A.; Shoptaw, S.; Gorbach, P.M.; Aldrovandi, G.M. Effects of Substance Use and Sex Practices on the Intestinal Microbiome During HIV-1 Infection. J. Infect. Dis. 2018, 218, 1560–1570. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yun, Y.; Kim, H.-N.; Kim, S.E.; Heo, S.G.; Chang, Y.; Ryu, S.; Shin, H.; Kim, H.-L. Comparative analysis of gut microbiota associated with body mass index in a large Korean cohort. BMC Microbiol. 2017, 17, 151. [Google Scholar] [CrossRef] [PubMed]
- Ottosson, F.; Brunkwall, L.; Ericson, U.; Nilsson, P.M.; Almgren, P.; Fernandez, C.; Melander, O.; Orho-Melander, M. Connection Between BMI-Related Plasma Metabolite Profile and Gut Microbiota. J. Clin. Endocrinol. Metab. 2018, 103, 1491–1501. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Precup, G.; Vodnar, D.-C. Gut Prevotella as a possible biomarker of diet and its eubiotic versus dysbiotic roles-A comprehensive literature review. Br. J. Nutr. 2019, 1–24. [Google Scholar] [CrossRef]
- Al-Ghezi, Z.Z.; Busbee, P.B.; Alghetaa, H.; Nagarkatti, P.S.; Nagarkatti, M. Combination of cannabinoids, delta-9-tetrahydrocannabinol (THC) and cannabidiol (CBD), mitigates experimental autoimmune encephalomyelitis (EAE) by altering the gut microbiome. Brain Behav. Immun. 2019. [Google Scholar] [CrossRef]
- Becker, W.J.; Nagarkatti, M.; Nagarkatti, P.S. Δ9-tetrahydrocannabinol (THC) activation of cannabinoid receptors induces unique changes in the murine gut microbiome and associated induction of myeloid-derived suppressor cells and Th17 cells. J. Immunol. 2017, 198, 218.11. [Google Scholar]
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Di Marzo, V.; Silvestri, C. Lifestyle and Metabolic Syndrome: Contribution of the Endocannabinoidome. Nutrients 2019, 11, 1956. https://doi.org/10.3390/nu11081956
Di Marzo V, Silvestri C. Lifestyle and Metabolic Syndrome: Contribution of the Endocannabinoidome. Nutrients. 2019; 11(8):1956. https://doi.org/10.3390/nu11081956
Chicago/Turabian StyleDi Marzo, Vincenzo, and Cristoforo Silvestri. 2019. "Lifestyle and Metabolic Syndrome: Contribution of the Endocannabinoidome" Nutrients 11, no. 8: 1956. https://doi.org/10.3390/nu11081956
APA StyleDi Marzo, V., & Silvestri, C. (2019). Lifestyle and Metabolic Syndrome: Contribution of the Endocannabinoidome. Nutrients, 11(8), 1956. https://doi.org/10.3390/nu11081956