Germ-free mice exhibit profound gut microbiota-dependent alterations of intestinal endocannabinoidome signaling
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The gut microbiota is a unique ecosystem of microorganisms interacting with the host through several biochemical mechanisms. The endocannabinoidome (eCBome), a complex signaling system including the endocannabinoid system, approximately 50 receptors and metabolic enzymes, and more than 20 lipid mediators with important physiopathologic functions, modulates gastrointestinal tract function and may mediate host cell-microbe communications there. Germ-free (GF) mice, which lack an intestinal microbiome and so differ drastically from conventionally raised (CR) mice, offer a unique opportunity to explore the eCBome in a microbe-free model and in the presence of a reintroduced functional gut microbiome through fecal microbiota transplant (FMT). We aimed to gain direct evidence for a link between the microbiome and eCBome systems by investigating eCBome alterations in the gut in GF mice before and after FMT. Basal eCBome gene expression and lipid profiles were measured in various segments of the intestine of GF and CR mice at juvenile and adult ages using targeted quantitative PCR transcriptomics and LC-MS/MS lipidomics. GF mice exhibited age-dependent modifications in intestinal eCBome gene expression and lipid mediator levels. FMT from CR donor mice to age-matched GF male mice reversed several of these alterations, particularly in the ileum and jejunum, after only 1 week, demonstrating that the gut microbiome directly impacts the host eCBome and providing a cause-effect relationship between the presence or absence of intestinal microbes and eCBome signaling. These results open the way to new studies investigating the mechanisms through which intestinal microorganisms exploit eCBome signaling to exert some of their physiopathologic functions.
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Germ-free animals have significant changes in CB1, CB2, and eCB synthetic and degradative enzymes throughout the gut.
“Germ-free animals demonstrate significant changes in the expression of CB1 and CB2, and synthetic and degradative enzymes throughout the gut (251).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [251]
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A RAPID METHOD OF TOTAL LIPID EXTRACTION AND PURIFICATION
Bligh, E. G., & Dyer, W. J. (1959) · Canadian Journal of Biochemistry and Physiology · doi:10.1139/o59-099 · Cited by 54,751 · see citing works
DADA2: High–resolution sample inference from Illumina amplicon data
Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., & Holmes, S. P. (2016) · Nature Methods · doi:10.1038/nmeth.3869 · Cited by 35,698 · see citing works
A RAPID METHOD OF TOTAL LIPID EXTRACTION AND PURIFICATION
Bligh, E. G., & Dyer, W. J. (1959) · Canadian Journal of Biochemistry and Physiology · doi:10.1139/y59-099 · Cited by 23,189 · see citing works
FactoMineR : An R Package for Multivariate Analysis
Lê, S., Josse, J., & Husson, F. (2008) · Journal of Statistical Software · doi:10.18637/jss.v025.i01 · Cited by 12,103 · see citing works
Metabolic Endotoxemia Initiates Obesity and Insulin Resistance
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. (2007) · Diabetes · doi:10.2337/db06-1491 · Cited by 6,638 · see citing works
Self-citationThe gut microbiota as an environmental factor that regulates fat storage
Bäckhed, F., Ding, H., Wang, T., Hooper, L. V., Koh, G. Y., Nagy, A., Semenkovich, C. F., & Gordon, J. I. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407076101 · Cited by 6,245 · see citing works
The gut microbiota shapes intestinal immune responses during health and disease
Round, J. L., & Mazmanian, S. K. (2009) · Nature Reviews Immunology · doi:10.1038/nri2515 · Cited by 5,029 · see citing works
Host-gut microbiota metabolic interactions
Nicholson, J. K., Holmes, E., Kinross, J., Burcelin, R., Gibson, G., Jia, W., & Pettersson, S. (2012) · Science · doi:10.1126/science.1223813 · Cited by 4,760 · see citing works
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. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219451110 · Cited by 4,511 · see citing works
Self-citationThe impact of the gut microbiota on human health: an integrative view
Clemente, J. C., Ursell, L. K., Parfrey, L. W., & Knight, R. (2012) · Cell · doi:10.1016/j.cell.2012.01.035 · Cited by 3,710 · see citing works
Human Genetics Shape the Gut Microbiome
Goodrich, J. K., Waters, J. L., Poole, A. C., Sutter, J. L., Koren, O., Blekhman, R., Beaumont, M., Van Treuren, W., Knight, R., Bell, J. T., et al. (2014) · Cell · doi:10.1016/j.cell.2014.09.053 · Cited by 3,164 · see citing works
Role of the normal gut microbiota
Jandhyala, S. M. (2015) · World Journal of Gastroenterology · doi:10.3748/wjg.v21.i29.8787 · Cited by 3,001 · see citing works
Mechanisms underlying the resistance to diet-induced obesity in germ-free mice
Bäckhed, F., Manchester, J. K., Semenkovich, C. F., & Gordon, J. I. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605374104 · Cited by 2,615 · see citing works
2-Arachidonoylgylcerol: A Possible Endogenous Cannabinoid Receptor Ligand in Brain
Sugiura, T., Kondo, S., Sukagawa, A., Nakane, S., Shinoda, A., Itoh, K., Yamashita, A., & Waku, K. (1995) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1995.2437 · Cited by 2,196 · see citing works
Permutational Multivariate Analysis of Variance ( PERMANOVA )
Anderson, M. J. (2017) · Wiley StatsRef: Statistics Reference Online · doi:10.1002/9781118445112.stat07841 · Cited by 1,867 · see citing works
Interactions between commensal intestinal bacteria and the immune system
Macpherson, A. J., & Harris, N. L. (2004) · Nature reviews. Immunology · doi:10.1038/nri1373 · Cited by 1,607 · see citing works
Pawlak, M., Lefebvre, P., & Staels, B. (2015) · Journal of Hepatology · doi:10.1016/j.jhep.2014.10.039 · Cited by 1,578 · see citing works
Recognition of pathogen-associated molecular patterns by TLR family
Akira, S., & Hemmi, H. (2003) · Immunology Letters · doi:10.1016/s0165-2478(02)00228-6 · Cited by 1,139 · see citing works
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. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200305129 · Cited by 1,039 · see citing works
Self-citationReddy, J. K., & Hashimoto, T. (2001) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.21.1.193 · Cited by 955 · see citing works
The endocannabinoid system links gut microbiota to adipogenesis
Muccioli, G. G., Naslain, D., Bäckhed, F., Reigstad, C. S., Lambert, D. M., Delzenne, N. M., & Cani, P. D. (2010) · Molecular Systems Biology · doi:10.1038/msb.2010.46 · Cited by 691 · see citing works
Self-citationThe gut microbiota modulates host energy and lipid metabolism in mice
Velagapudi, V. R., Hezaveh, R., Reigstad, C. S., Gopalacharyulu, P., Yetukuri, L., Islam, S., Felin, J., Perkins, R., Borén, J., Orešič, M., et al. (2010) · Journal of Lipid Research · doi:10.1194/jlr.m002774 · Cited by 589 · see citing works
Hopkins, M. J., Sharp, R., & Macfarlane, G. T. (2001) · Gut · doi:10.1136/gut.48.2.198 · Cited by 577 · see citing works
Martínez, I., Stegen, J. C., Maldonado-Gómez, M. X., Eren, A. M., Siba, P. M., Greenhill, A. R., & Walter, J. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.03.049 · Cited by 576 · see citing works
New approaches and challenges to targeting the endocannabinoid system
Marzo, V. D. (2018) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2018.115 · Cited by 480 · see citing works
A biosynthetic pathway for anandamide
Liu, J., Wang, L., Harvey-White, J. D., Osei‐Hyiaman, D., Razdan, R. J., Gong, Q., Chan, A. C., Zhou, Z., Huang, B. X., Kim, H., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601832103 · Cited by 468 · see citing works
The serine hydrolase ABHD6 controls the accumulation and efficacy of 2-AG at cannabinoid receptors
Marrs, W., Blankman, J. L., Horne, E. A., Thomazeau, A., Lin, Y. H., Coy, J. W., Bodor, Á. L., Muccioli, G. G., Hu, S. S., Woodruff, G., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2601 · Cited by 442 · see citing works
Self-citationLauffer, L. M., Iakoubov, R., & Brubaker, P. L. (2009) · Diabetes · doi:10.2337/db08-1237 · Cited by 400 · see citing works
Microbial Modulation of Energy Availability in the Colon Regulates Intestinal Transit
Wichmann, A., Allahyar, A., Greiner, T. U., Plovier, H., Östergren‐Lundén, G., Larsson, T. P., Drucker, D. J., Delzenne, N. M., Cani, P. D., & Bäckhed, F. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.09.012 · Cited by 382 · see citing works
Self-citationThe Lipid Messenger OEA Links Dietary Fat Intake to Satiety
Schwartz, G. J., Fu, J., Astarita, G., Li, X., Gaetani, S., Campolongo, P., Cuomo, V., & Piomelli, D. (2008) · Cell Metabolism · doi:10.1016/j.cmet.2008.08.005 · Cited by 370 · see citing works
Sugiura, T., Kondo, S., Kishimoto, S., Miyashita, T., Nakane, S., Kodaka, T., Suhara, Y., Takayama, H., & Waku, K. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.1.605 · Cited by 370 · see citing works
Guida, F., Turco, F., Iannotta, M., De Gregorio, D., Palumbo, I., Sarnelli, G., Furiano, A., Napolitano, F., Boccella, S., Luongo, L., et al. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.09.001 · Cited by 367 · see citing works
Husebye, E., Hellström, P. M., Sundler, F., Chen, J., & Midtvedt, T. (2001) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.2001.280.3.g368 · Cited by 319 · see citing works
Evidence That the Cannabinoid CB1 Receptor Is a 2-Arachidonoylglycerol Receptor
Sugiura, T., Kodaka, T., Nakane, S., Miyashita, T., Kondo, S., Suhara, Y., Takayama, H., Waku, K., Seki, C., Baba, N., et al. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.5.2794 · Cited by 311 · see citing works
Endocannabinoids: synthesis and degradation
Marzo, V. D. (2006) · Reviews of physiology, biochemistry and pharmacology · doi:10.1007/112_0505 · Cited by 308 · see citing works
Role of Gut Microbiota in the Aetiology of Obesity: Proposed Mechanisms and Review of the Literature
Khan, M. J., Gerasimidis, K., Edwards, C. A., & Shaikh, M. G. (2016) · Journal of Obesity · doi:10.1155/2016/7353642 · Cited by 301 · see citing works
Anandamide induced PPARγ transcriptional activation and 3T3-L1 preadipocyte differentiation
Bouaboula, M., Hilairet, S., Marchand, J., Fajas, L., Fur, G. L., & Casellas, P. (2005) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2005.05.032 · Cited by 298 · see citing works
Why do cannabinoid receptors have more than one endogenous ligand?
Di Marzo, V., & De Petrocellis, L. (2012) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2011.0382 · Cited by 290 · see citing works
Self-citationGerm-free and antibiotic-treated mice are highly susceptible to epithelial injury in DSS colitis
Hernández-Chirlaque, C., Aranda, C. J., Ocón, B., Capitán-Cañadas, F., Ortega-González, M., Carrero, J. J., Suárez, M. D., Zarzuelo, A., Sánchez de Medina, F., & Martínez-Augustin, O. (2016) · Journal of Crohn's and Colitis · doi:10.1093/ecco-jcc/jjw096 · Cited by 262 · see citing works
Izzo, A. A., Fezza, F., Capasso, R., Bisogno, T., Pinto, L., Iuvone, T., Esposito, G., Mascolo, N., Marzo, V. D., & Capasso, F. (2001) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0704293 · Cited by 255 · see citing works
Intestinal Microbiota Regulate Xenobiotic Metabolism in the Liver
Björkholm, B., Bok, C. M., Lundin, A., Rafter, J., Hibberd, M. L., & Pettersson, S. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006958 · Cited by 249 · see citing works
Use of Germ-Free Animal Models in Microbiota-Related Research
Al‐Asmakh, M., & Zadjali, F. (2015) · Journal of Microbiology and Biotechnology · doi:10.4014/jmb.1501.01039 · Cited by 243 · see citing works
Everard, A., Geurts, L., Caesar, R., Hul, M. V., Matamoros, S., Duparc, T., Denis, R., Cochez, P. M., Pierard, F., Castel, J., et al. (2014) · Nature Communications · doi:10.1038/ncomms6648 · Cited by 237 · see citing works
Self-citationDietary intake, energy metabolism, and excretory losses of adult male germfree Wistar rats.
Wöstmann, B. S. J., Larkin, C. J., Moriarty, A., & Bruckner-Kardoss, E. (1983) · PubMed · Cited by 228 · see citing works
A Crypt-Specific Core Microbiota Resides in the Mouse Colon
Pédron, T., Mulet, C., Dauga, C., Frangeul, L., Chervaux, C., Grompone, G., & Sansonetti, P. J. (2012) · mBio · doi:10.1128/mbio.00116-12 · Cited by 219 · see citing works
Ringel, Y., Maharshak, N., Ringel‐Kulka, T., Wolber, E. A., Sartor, R. B., & Carroll, I. M. (2015) · Gut Microbes · doi:10.1080/19490976.2015.1044711 · Cited by 204 · see citing works
Gut microbiome and metabolic syndrome
Mazidi, M., Rezaie, P., Kengne, A. P., Ghayour‐Mobarhan, M., & Ferns, G. A. (2016) · Diabetes & Metabolic Syndrome Clinical Research & Reviews · doi:10.1016/j.dsx.2016.01.024 · Cited by 194 · see citing works
Endocannabinoid signal in the gut controls dietary fat intake
DiPatrizio, N. V., Astarita, G., Schwartz, G. J., Li, X., & Piomelli, D. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104675108 · Cited by 192 · see citing works
Hansen, H. S., ROSENKILDE, M. M., Holst, J. J., & Schwartz, T. W. (2012) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2012.03.014 · Cited by 186 · see citing works
Endocannabinoids as physiological regulators of colonic propulsion in mice
Pinto, L., Izzo, A. A., Mascolo, N., Capasso, F., Cascio, M. G., Bisogno, T., Marzo, V. D., Hospodar–Scott, K., & Brown, D. R. (2002) · Gastroenterology · doi:10.1053/gast.2002.34242 · Cited by 180 · see citing works
Navia‐Paldanius, D., Savinainen, J. R., & Laitinen, J. T. (2012) · Journal of Lipid Research · doi:10.1194/jlr.m030411 · Cited by 175 · see citing works
Geurts, L., Everard, A., Hul, M. V., Essaghir, A., Duparc, T., Matamoros, S., Plovier, H., Castel, J., Denis, R., Bergiers, M., et al. (2015) · Nature Communications · doi:10.1038/ncomms7495 · Cited by 171 · see citing works
Self-citationEverard, A., Plovier, H., Rastelli, M., Hul, M. V., d’Oplinter, A. D. W., Geurts, L., Druart, C., Robine, S., Delzenne, N. M., Muccioli, G. G., et al. (2019) · Nature Communications · doi:10.1038/s41467-018-08051-7 · Cited by 156 · see citing works
Self-citationLee, 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. (2015) · The FASEB Journal · doi:10.1096/fj.14-268300 · Cited by 147 · see citing works
Balvers, M. G. J., Verhoeckx, K. C. M., Plastina, P., Wortelboer, H. M., Meijerink, J., & Witkamp, R. F. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2010.06.006 · Cited by 145 · see citing works
Duncan, M., Mouihate, A., Mackie, K., Keenan, C. M., Buckley, N. E., Davison, J. S., Patel, K. D., Pittman, Q. J., & Sharkey, K. A. (2008) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.90285.2008 · Cited by 145 · see citing works
Ambrosino, P., Soldovieri, M. V., Russo, C., & Taglialatela, M. (2012) · British Journal of Pharmacology · doi:10.1111/bph.12029 · Cited by 143 · see citing works
Cannabinoids mediate opposing effects on inflammation‐induced intestinal permeability
Alhamoruni, A., Wright, K. L., Larvin, M., & O’Sullivan, S. E. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01589.x · Cited by 138 · see citing works
An endogenous cannabinoid tone attenuates cholera toxin-induced fluid accumulation in mice
Izzo, A. A., Capasso, F., Costagliola, A., Bisogno, T., Marsicano, G., Ligresti, A., Matias, I., Capasso, R., Pinto, L., Borrelli, F., et al. (2003) · Gastroenterology · doi:10.1016/s0016-5085(03)00892-8 · Cited by 132 · see citing works
Prostaglandin Ethanolamides (Prostamides): In Vitro Pharmacology and Metabolism
Matias, I., Chen, J., PETROCELLIS, L. D., Bisogno, T., Ligresti, A., Fezza, F., Krauss, A. H. ‐., Shi, L., Protzman, C. E., Li, C., et al. (2004) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.103.061705 · Cited by 132 · see citing works
Involvement of TRPV1 Channels in Energy Homeostasis
Christie, S., Wittert, G., Li, H., & Page, A. J. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00420 · Cited by 130 · see citing works
Rovito, D., Giordano, C., Vizza, D., Plastina, P., Barone, I., Casaburi, I., Lanzino, M., Amicis, F. D., Sisci, D., Mauro, L., et al. (2012) · Journal of Cellular Physiology · doi:10.1002/jcp.24288 · Cited by 128 · see citing works
Regulation of GPR119 receptor activity with endocannabinoid-like lipids
Syed, S. K., Bui, H. H., Beavers, L. S., Farb, T. B., FICORILLI, J. V., Chesterfield, A. K., Kuo, M., Bokvist, K. B., Barrett, D. G., & Efanov, A. M. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00269.2012 · Cited by 122 · see citing works
Astudillo, A. M., Balboa, M. A., & Balsinde, J. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2018.07.002 · Cited by 120 · see citing works
Gut microbial communities modulating brain development and function
Al‐Asmakh, M., Anuar, F., Zadjali, F., Rafter, J. J., & Pettersson, S. (2012) · Gut Microbes · doi:10.4161/gmic.21287 · Cited by 117 · see citing works
Raboune, S., Stuart, J. M., Leishman, E., Takacs, S. M., Rhodes, B. P., Basnet, A., Jameyfield, E., McHugh, D., Widlanski, T. S., & Bradshaw, H. B. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00195 · Cited by 117 · see citing works
Bassaganya-Riera, J., Misyak, S. A., Guri, A. J., & Hontecillas, R. (2009) · Cellular Immunology · doi:10.1016/j.cellimm.2009.04.003 · Cited by 100 · see citing works
The GPR 55 antagonist CID 16020046 protects against intestinal inflammation
Stančić, A., Jandl, K., Hasenoehrl, C., Reichmann, F., Marsche, G., Schuligoi, R., Heinemann, Á., Storr, M., & Schicho, R. (2015) · Neurogastroenterology & Motility · doi:10.1111/nmo.12639 · Cited by 99 · see citing works
A novel CB receptor GPR55 and its ligands are involved in regulation of gut movement in rodents
Lin, X. ‐., Yuece, B., Li, Y. ‐., Feng, Y., Feng, J. ‐., Yu, L. ‐., Li, K., Li, Y.-X., & Storr, M. (2011) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2011.01742.x · Cited by 94 · see citing works
CB1 Cannabinoid Receptor Ligands
Thakur, G. A., Nikas, S. P., & Makriyannis, A. (2005) · Mini-Reviews in Medicinal Chemistry · doi:10.2174/1389557054368772 · Cited by 90 · see citing works
Lan, H., Lin, H. V., Cf, W., Wright, M. J., Xu, S. S., Kang, L., Juhl, K., Hedrick, J., & Kowalski, T. J. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01754.x · Cited by 88 · see citing works
Sagar, D. R., Kendall, D. A., & Chapman, V. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.335 · Cited by 88 · see citing works
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. (2016) · The FASEB Journal · doi:10.1096/fj.201500132 · Cited by 87 · see citing works
GPR18 is required for a normal CD8αα intestinal intraepithelial lymphocyte compartment
Wang, X., Sumida, H., & Cyster, J. G. (2014) · The Journal of Experimental Medicine · doi:10.1084/jem.20140646 · Cited by 86 · see citing works
Actions and Regulation of Ionotropic Cannabinoid Receptors
PETROCELLIS, L. D., Nabissi, M., Santoni, G., & Ligresti, A. (2017) · Advances in pharmacology · doi:10.1016/bs.apha.2017.04.001 · Cited by 81 · see citing works
“Redundancy” of Endocannabinoid Inactivation: New Challenges and Opportunities for Pain Control
Piscitelli, F., & Marzo, V. D. (2012) · ACS Chemical Neuroscience · doi:10.1021/cn300015x · Cited by 74 · see citing works
A potential role for GPR55 in gastrointestinal functions
Schicho, R., & Storr, M. (2012) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2012.09.009 · Cited by 65 · see citing works
Cluny, N. L., Keenan, C. M., Duncan, M., Fox, A., Lutz, B., & Sharkey, K. A. (2010) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.110.169946 · Cited by 60 · see citing works
The role of CB 1 in intestinal permeability and inflammation
Karwad, M. A., Couch, D. G., Theophilidou, E., et al. (2017) · The FASEB Journal · doi:10.1096/fj.201601346r · Cited by 59 · see citing works
Endocannabinoids and the gastrointestinal tract.
Massa, F., & Monory, K. (2006) · PubMed · Cited by 58 · see citing works
PPARγ Modulates Long Chain Fatty Acid Processing in the Intestinal Epithelium
Duszka, K., Orešič, M., May, C. L., König, J. S., & Wahli, W. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18122559 · Cited by 54 · see citing works
Regner, E. H., Ohri, N., Stahly, A., Gerich, M. E., Fennimore, B. P., Ir, D., Jubair, W. K., Görg, C., Siebert, J., Robertson, C. E., et al. (2018) · Arthritis Research & Therapy · doi:10.1186/s13075-018-1639-3 · Cited by 50 · see citing works
Kramar, C. P., Loureiro, M., Renard, J., & Laviolette, S. R. (2017) · Cannabis and Cannabinoid Research · doi:10.1089/can.2016.0030 · Cited by 49 · see citing works
Wang, R., Borazjani, A., Matthews, A. T., Mangum, L. C., Edelmann, M. J., & Ross, M. K. (2013) · Biochemistry · doi:10.1021/bi401138s · Cited by 48 · see citing works
Parlar, A., Arslan, S. O., Doğan, M. F., Çam, S. A., Yal�in, A., Elibol, E., �zer, M., ��kardeş, F., & Kara, H. (2018) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2018.6753 · Cited by 43 · see citing works
Protein Tyrosine Phosphatases: Regulators of CD4 T Cells in Inflammatory Bowel Disease
Pike, K. A., & Tremblay, M. L. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02504 · Cited by 41 · see citing works
The endocannabinoidome : the world of endocannabinoids and related mediators
Marzo, V. D., & Wang, J. Y. (2015) · Cited by 38 · see citing works
Grunewald, Z. I., Lee, S., Kirkland, R. A., Ross, M. K., & Serre, C. B. D. L. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.11.035 · Cited by 21 · see citing works
Silveira, L. S., Pimentel, G. D., de Souza, C. O., Biondo, L. A., Teixeira, A. A. D. S., de Lima, E. A., Batatinha, H., Neto, J. C. R., & Lira, F. S. (2017) · Cell Biochemistry and Function · doi:10.1002/cbf.3308 · Cited by 17 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Piscitelli, F., and V. Di Marzo. 2015. The ever-expanding world of the endocannabinoids: a concise introduction. In Cannabinoids in Neurologic and Mental Disease. Accessed June 26, 2019, at http:// www.sciencedirect.com/science/article/pii/B9780124170414000242.
Cited by
Sorted by citations
Gut microbiome and health: mechanistic insights
de Vos, W. M., Tilg, H., Van Hul, M., & Cani, P. D. (2022) · Gut · doi:10.1136/gutjnl-2021-326789 · Cited by 2,388 · see citing works
Self-citationSignalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis
Rusch, J. A., Layden, B. T., & Dugas, L. R. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1130689 · Cited by 415 · see citing works
Goods and Bads of the Endocannabinoid System as a Therapeutic Target: Lessons Learned after 30 Years
Maccarrone, M., Di Marzo, V., Gertsch, J., Grether, U., Howlett, A. C., Hua, T., Makriyannis, A., Piomelli, D., Ueda, N., & van der Stelt, M. (2023) · Pharmacological Reviews · doi:10.1124/pharmrev.122.000600 · Cited by 183 · see citing works
Role of the endocannabinoid system in the regulation of intestinal homeostasis
Cuddihey, H., MacNaughton, W. K., & Sharkey, K. A. (2022) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2022.05.015 · Cited by 79 · see citing works
The microbiome and gut endocannabinoid system in the regulation of stress responses and metabolism
Srivastava, R. K., Lutz, B., & Ruiz de Azua, I. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.867267 · Cited by 56 · see citing works
The endocannabinoid system: a bridge between alzheimer’s disease and gut microbiota
Bisogno, T., Lauritano, A., & Piscitelli, F. (2021) · Life · doi:10.3390/life11090934 · Cited by 16 · see citing works
- Authors
- Manca, C., Boubertakh, B., Leblanc, N., Deschênes, T., Lacroix, S., Martin, C., Houde, A., Veilleux, A., Flamand, N., Muccioli, G. G., Raymond, F., Cani, P. D., Di Marzo, V., & Silvestri, C.
- Affiliations
- Institut universitaire de cardiologie et de pneumologie de Québec (CA)
- Université Laval (CA)
- Institut sur la nutrition et les aliments fonctionnels (INAF) (CA)
- UCLouvain (BE)
- Walloon Excellence in Lifesciences and Biotechnology (BE)
- Corresponding author
- Silvestri, Cristoforo
- ORCID
- Venue
- Journal of Lipid Research
- Publisher
- Elsevier BV
- Published
- 2020-01
- Volume
- 61
- Issue
- 1
- Pages
- 70-85
- ISSN
- 0022-2275 (ISSN-L)
- PMC
- PMC6939599
- OpenAlex
- W2985018913
- Cited by
- 152
- References
- 89
- Citations by year
- 2026: 21 · 2025: 33 · 2024: 22 · 2023: 27 · 2022: 20 · 2021: 18 · 2020: 11
- FWCI
- 7.59
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Lipid Research (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Digital Access to Libraries (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- UNICA IRIS Institutional Research Information System (University of Cagliari) (submittedVersion, other-oa)
- Funders
- Fonds Baillet Latour
- Fonds de la Recherche Scientifique - FNRS (WELBIO-CR-2019C-02R)
- European Research Council (336452-ENIGMO)
- Topics
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- gut microbiota, endocannabinoidome, germ-free mice, fecal microbiota transplantation, host-microbe interactions
- MeSH terms
- Gastrointestinal Microbiome, Animals, Intestines, Male, Mice, Inbred C57BL, Signal Transduction, Mice, Endocannabinoids
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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