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The endocannabinoid system links gut microbiota to adipogenesis

Bibliographic reference Muccioli, Giulio ; Naslain, Damien ; Bäckhed, Fredrik ; Reigstad, Christopher S. ; Lambert, Didier ; et. al. The endocannabinoid system links gut microbiota to adipogenesis. In: Molecular Systems Biology, Vol. 6, p. 392 [1-15] (2010)
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  1. Backhed 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, 10.1073/pnas.0407076101
  2. Bäckhed Fredrik, Manchester Jill K., Semenkovich Clay F., Gordon Jeffrey I., Mechanisms underlying the resistance to diet-induced obesity in germ-free mice, 10.1073/pnas.0605374104
  3. Bennetzen M. F., Nielsen T. S., Paulsen S. K., Bendix J., Fisker S., Jessen N., Lund S., Richelsen B., Pedersen S. B., Reduced cannabinoid receptor 1 protein in subcutaneous adipose tissue of obese, 10.1111/j.1365-2362.2009.02231.x
  4. Bellocchio L., Cervino C., Vicennati V., Pasquali R., Pagotto U., Cannabinoid Type 1 Receptor: Another Arrow in the Adipocytes’ Bow, 10.1111/j.1365-2826.2008.01682.x
  5. 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, 10.2337/db06-0812
  6. Bouaboula Monsif, Hilairet Sandrine, Marchand Jean, Fajas Lluis, Fur Gerard Le, Casellas Pierre, Anandamide induced PPARγ transcriptional activation and 3T3-L1 preadipocyte differentiation, 10.1016/j.ejphar.2005.05.032
  7. Brun P., Castagliuolo I., Leo V. D., Buda A., Pinzani M., Palu G., Martines D., Increased intestinal permeability in obese mice: new evidence in the pathogenesis of nonalcoholic steatohepatitis, 10.1152/ajpgi.00024.2006
  8. Buettner Christoph, Muse Evan D, Cheng Andrew, Chen Linghong, Scherer Thomas, Pocai Alessandro, Su Kai, Cheng Bob, Li Xiasong, Harvey-White Judith, Schwartz Gary J, Kunos George, Rossetti Luciano, Buettner Christoph, Leptin controls adipose tissue lipogenesis via central, STAT3–independent mechanisms, 10.1038/nm1775
  9. Cani P. D., Amar J., Iglesias M. A., Poggi M., Knauf C., Bastelica D., Neyrinck A. M., Fava F., Tuohy K. M., Chabo C., Waget A., Delmee E., Cousin B., Sulpice T., Chamontin B., Ferrieres J., Tanti J.-F., Gibson G. R., Casteilla L., Delzenne N. M., Alessi M. C., Burcelin R., Metabolic Endotoxemia Initiates Obesity and Insulin Resistance, 10.2337/db06-1491
  10. 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, 10.2337/db07-1403
  11. Cani Patrice, Delzenne Nathalie, The Role of the Gut Microbiota in Energy Metabolism and Metabolic Disease, 10.2174/138161209788168164
  12. Cani P. D., Knauf C., Iglesias M. A., Drucker D. J., Delzenne N. M., Burcelin R., Improvement of Glucose Tolerance and Hepatic Insulin Sensitivity by Oligofructose Requires a Functional Glucagon-Like Peptide 1 Receptor, 10.2337/db05-1360
  13. Cani P. D., Neyrinck A. M., Fava F., Knauf C., Burcelin R. G., Tuohy K. M., Gibson G. R., Delzenne N. M., Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia, 10.1007/s00125-007-0791-0
  14. Cani P. D., Possemiers S., Van de Wiele T., Guiot Y., Everard A., Rottier O., Geurts L., Naslain D., Neyrinck A., Lambert D. M., Muccioli G. G., Delzenne N. M., Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability, 10.1136/gut.2008.165886
  15. Caraceni P., Pertosa A. M., Giannone F., Domenicali M., Grattagliano I., Principe A., Mastroleo C., Perrelli M. G., Cutrin J., Trevisani F., Croci T., Bernardi M., Antagonism of the cannabinoid CB-1 receptor protects rat liver against ischaemia-reperfusion injury complicated by endotoxaemia, 10.1136/gut.2007.147652
  16. Chung Soonkyu, LaPoint Kathleen, Martinez Kristina, Kennedy Arion, Boysen Sandberg Maria, McIntosh Michael K., Preadipocytes Mediate Lipopolysaccharide-Induced Inflammation and Insulin Resistance in Primary Cultures of Newly Differentiated Human Adipocytes, 10.1210/en.2006-0536
  17. Claus Sandrine P, Tsang Tsz M, Wang Yulan, Cloarec Olivier, Skordi Eleni, Martin François-Pierre, Rezzi Serge, Ross Alastair, Kochhar Sunil, Holmes Elaine, Nicholson Jeremy K, Systemic multicompartmental effects of the gut microbiome on mouse metabolic phenotypes, 10.1038/msb.2008.56
  18. Cota Daniela, Marsicano Giovanni, Tschöp Matthias, Grübler Yvonne, Flachskamm Cornelia, Schubert Mirjam, Auer Dorothee, Yassouridis Alexander, Thöne-Reineke Christa, Ortmann Sylvia, Tomassoni Federica, Cervino Cristina, Nisoli Enzo, Linthorst Astrid C.E., Pasquali Renato, Lutz Beat, Stalla Günter K., Pagotto Uberto, The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis, 10.1172/jci200317725
  19. Cote M, Int J Obes (Lond), 31, 692 (2007)
  20. Cravatt Benjamin F., Giang Dan K., Mayfield Stephen P., Boger Dale L., Lerner Richard A., Gilula Norton B., Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides, 10.1038/384083a0
  21. D'Eon T. M., Pierce K. A., Roix J. J., Tyler A., Chen H., Teixeira S. R., The Role of Adipocyte Insulin Resistance in the Pathogenesis of Obesity-Related Elevations in Endocannabinoids, 10.2337/db07-1186
  22. DeLeve Laurie D., Wang Xiangdong, Kanel Gary C., Atkinson Roscoe D., McCuskey Robert S., Prevention of Hepatic Fibrosis in a Murine Model of Metabolic Syndrome with Nonalcoholic Steatohepatitis, 10.2353/ajpath.2008.070720
  23. Devane W., Hanus L, Breuer A, Pertwee R., Stevenson L., Griffin G, Gibson D, Mandelbaum A, Etinger A, Mechoulam R, Isolation and structure of a brain constituent that binds to the cannabinoid receptor, 10.1126/science.1470919
  24. Di Marzo Vincenzo, Targeting the endocannabinoid system: to enhance or reduce?, 10.1038/nrd2553
  25. Di Marzo Vincenzo, Bisogno Tiziana, De Petrocellis Luciano, Melck Dominique, Orlando Pierangelo, Wagner Jens A., Kunos George, Biosynthesis and inactivation of the endocannabinoid 2-arachidonoylglycerol in circulating and tumoral macrophages, 10.1046/j.1432-1327.1999.00631.x
  26. 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, 10.1007/s00125-008-1178-6
  27. 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, 10.1073/pnas.152334899
  28. Dubois Severine G., Heilbronn Leonie K., Smith Steven R., Albu Jeanine B., Kelley David E., Ravussin Eric, Decreased Expression of Adipogenic Genes in Obese Subjects with Type 2 Diabetes*, 10.1038/oby.2006.178
  29. Engeli S., Bohnke J., Feldpausch M., Gorzelniak K., Janke J., Batkai S., Pacher P., Harvey-White J., Luft F. C., Sharma A. M., Jordan J., Activation of the Peripheral Endocannabinoid System in Human Obesity, 10.2337/diabetes.54.10.2838
  30. Gary-Bobo Magali, Elachouri Ghizlane, Gallas Jean François, Janiak Philip, Marini Pietro, Ravinet-Trillou Christine, Chabbert Michèle, Cruccioli Noël, Pfersdorff Christian, Roque Claude, Arnone Michèle, Croci Tiziano, Soubrié Philippe, Oury-Donat Florence, Maffrand Jean Pierre, Scatton Bernard, Lacheretz Frederic, Le Fur Gérard, Herbert Jean Marc, Bensaid Mohammed, Rimonabant reduces obesity-associated hepatic steatosis and features of metabolic syndrome in obese Zucker fa/fa rats, 10.1002/hep.21641
  31. Gary-Bobo M., The Cannabinoid CB1 Receptor Antagonist Rimonabant (SR141716) Inhibits Cell Proliferation and Increases Markers of Adipocyte Maturation in Cultured Mouse 3T3 F442A Preadipocytes, 10.1124/mol.105.015040
  32. Gustafson B., Gogg S., Hedjazifar S., Jenndahl L., Hammarstedt A., Smith U., Inflammation and impaired adipogenesis in hypertrophic obesity in man, 10.1152/ajpendo.00377.2009
  33. Hoareau Laurence, Buyse Marion, Festy Franck, Ravanan Palaniyandi, Gonthier Marie-Paule, Matias Isabel, Petrosino Stefania, Tallet Frank, D'Hellencourt Christian Lefebvre, Cesari Maya, Di Marzo Vincenzo, Roche Régis, Anti-inflammatory Effect of Palmitoylethanolamide on Human Adipocytes, 10.1038/oby.2008.591
  34. Hotamisligil Gökhan S., Erbay Ebru, Nutrient sensing and inflammation in metabolic diseases, 10.1038/nri2449
  35. Isakson P., Hammarstedt A., Gustafson B., Smith U., Impaired Preadipocyte Differentiation in Human Abdominal Obesity: Role of Wnt, Tumor Necrosis Factor- , and Inflammation, 10.2337/db08-1770
  36. Izzo Angelo A, Piscitelli Fabiana, Capasso Raffaele, Aviello Gabriella, Romano Barbara, Borrelli Francesca, Petrosino Stefania, Di Marzo Vincenzo, Peripheral endocannabinoid dysregulation in obesity: relation to intestinal motility and energy processing induced by food deprivation and re-feeding : Dysfunctional endocannabinoids in obese rodents, 10.1111/j.1476-5381.2009.00183.x
  37. Kathuria Satish, Gaetani Silvana, Fegley Darren, Valiño Fernando, Duranti Andrea, Tontini Andrea, Mor Marco, Tarzia Giorgio, Rana Giovanna La, Calignano Antonio, Giustino Arcangela, Tattoli Maria, Palmery Maura, Cuomo Vincenzo, Piomelli Daniele, Modulation of anxiety through blockade of anandamide hydrolysis, 10.1038/nm803
  38. Kimura Hiromichi, Sawada Norimasa, Tobioka Hirotoshi, Isomura Hiroshi, Kokai Yasuo, Hirata Koichi, Mori Michio, Bacterial lipopolysaccharide reduced intestinal barrier function and altered localization of 7H6 antigen in IEC-6 rat intestinal crypt cells, 10.1002/(sici)1097-4652(199706)171:3<284::aid-jcp6>;2-k
  39. Lambert Didier M, Muccioli Giulio G, Endocannabinoids and related N-acylethanolamines in the control of appetite and energy metabolism: emergence of new molecular players : , 10.1097/mco.0b013e3282f00061
  40. Ley R. E., Backhed F., Turnbaugh P., Lozupone C. A., Knight R. D., Gordon J. I., Obesity alters gut microbial ecology, 10.1073/pnas.0504978102
  41. Ley Ruth E., Turnbaugh Peter J., Klein Samuel, Gordon Jeffrey I., Microbial ecology: Human gut microbes associated with obesity, 10.1038/4441022a
  42. Liu Jie, Bátkai Sándor, Pacher Pál, Harvey-White Judith, Wagner Jens A., Cravatt Benjamin F., Gao Bin, Kunos George, Lipopolysaccharide Induces Anandamide Synthesis in Macrophages via CD14/MAPK/Phosphoinositide 3-Kinase/NF-κB Independently of Platelet-activating Factor, 10.1074/jbc.m306062200
  43. Maccarrone Mauro, De Petrocellis Luciano, Bari Monica, Fezza Filomena, Salvati Simona, Di Marzo Vincenzo, Finazzi-Agrò Alessandro, Lipopolysaccharide Downregulates Fatty Acid Amide Hydrolase Expression and Increases Anandamide Levels in Human Peripheral Lymphocytes, 10.1006/abbi.2001.2500
  44. Martin François-Pierre J, Dumas Marc-Emmanuel, Wang Yulan, Legido-Quigley Cristina, Yap Ivan K S, Tang Huiru, Zirah Séverine, Murphy Gerard M, Cloarec Olivier, Lindon John C, Sprenger Norbert, Fay Laurent B, Kochhar Sunil, van Bladeren Peter, Holmes Elaine, Nicholson Jeremy K, A top-down systems biology view of microbiome-mammalian metabolic interactions in a mouse model, 10.1038/msb4100153
  45. Martin FP, Mol Syst Biol, 4, 205 (2008)
  46. Matias Isabel, Gonthier Marie-Paule, Orlando Pierangelo, Martiadis Vassilis, De Petrocellis Luciano, Cervino Cristina, Petrosino Stefania, Hoareau Laurence, Festy Franck, Pasquali Renato, Roche Regis, Maj Mario, Pagotto Uberto, Monteleone Palmiero, Di Marzo Vincenzo, Regulation, Function, and Dysregulation of Endocannabinoids in Models of Adipose and β-Pancreatic Cells and in Obesity and Hyperglycemia, 10.1210/jc.2005-2679
  47. McLaughlin T., Deng A., Yee G., Lamendola C., Reaven G., Tsao P. S., Cushman S. W., Sherman A., Inflammation in subcutaneous adipose tissue: relationship to adipose cell size, 10.1007/s00125-009-1496-3
  48. Mechoulam Raphael, Ben-Shabat Shimon, Hanus Lumir, Ligumsky Moshe, Kaminski Norbert E., Schatz Anthony R., Gopher Asher, Almog Shlomo, Martin Billy R., Compton David R., Pertwee Roger G., Griffin Graeme, Bayewitch Michael, Barg Jacob, Vogel Zvi, Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors, 10.1016/0006-2952(95)00109-d
  49. Membrez M., Blancher F., Jaquet M., Bibiloni R., Cani P. D., Burcelin R. G., Corthesy I., Mace K., Chou C. J., Gut microbiota modulation with norfloxacin and ampicillin enhances glucose tolerance in mice, 10.1096/fj.07-102723
  50. Muccioli Giulio G., Endocannabinoid biosynthesis and inactivation, from simple to complex, 10.1016/j.drudis.2010.03.007
  51. Muccioli Giulio G., Stella Nephi, An optimized GC–MS method detects nanomolar amounts of anandamide in mouse brain, 10.1016/j.ab.2007.09.030
  52. Muccioli G. G., Xu C., Odah E., Cudaback E., Cisneros J. A., Lambert D. M., Lopez Rodriguez M. L., Bajjalieh S., Stella N., Identification of a Novel Endocannabinoid-Hydrolyzing Enzyme Expressed by Microglial Cells, 10.1523/jneurosci.4830-06.2007
  53. Osei-Hyiaman Douglas, DePetrillo Michael, Pacher Pál, Liu Jie, Radaeva Svetlana, Bátkai Sándor, Harvey-White Judith, Mackie Ken, Offertáler László, Wang Lei, Kunos George, Endocannabinoid activation at hepatic CB1 receptors stimulates fatty acid synthesis and contributes to diet-induced obesity, 10.1172/jci200523057
  54. Osei-Hyiaman Douglas, Liu Jie, Zhou Liang, Godlewski Grzegorz, Harvey-White Judith, Jeong Won-il, Bátkai Sándor, Marsicano Giovanni, Lutz Beat, Buettner Christoph, Kunos George, Hepatic CB1 receptor is required for development of diet-induced steatosis, dyslipidemia, and insulin and leptin resistance in mice, 10.1172/jci34827
  55. Pagano Claudio, Pilon Catia, Calcagno Alessandra, Urbanet Riccardo, Rossato Marco, Milan Gabriella, Bianchi Katiuscia, Rizzuto Rosario, Bernante Paolo, Federspil Giovanni, Vettor Roberto, The Endogenous Cannabinoid System Stimulates Glucose Uptake in Human Fat Cells via Phosphatidylinositol 3-Kinase and Calcium-Dependent Mechanisms, 10.1210/jc.2007-0768
  56. Pagano C., Rossato M., Vettor R., Endocannabinoids, Adipose Tissue and Lipid Metabolism, 10.1111/j.1365-2826.2008.01690.x
  57. Poulain-Godefroy Odile, Froguel Philippe, Preadipocyte response and impairment of differentiation in an inflammatory environment, 10.1016/j.bbrc.2007.03.053
  58. Poulain-Godefroy O., Lecoeur C., Pattou F., Fruhbeck G., Froguel P., Inflammation is associated with a decrease of lipogenic factors in omental fat in women, 10.1152/ajpregu.00926.2007
  59. Precourt Louis-Philippe, Seidman Ernest, Delvin Edgard, Amre Devendra, Deslandres Colette, Dominguez Michel, Sinnett Daniel, Levy Emile, Comparative expression analysis reveals differences in the regulation of intestinal paraoxonase family members, 10.1016/j.biocel.2009.02.013
  60. Rousseaux Christel, Thuru Xavier, Gelot Agathe, Barnich Nicolas, Neut Christel, Dubuquoy Laurent, Dubuquoy Caroline, Merour Emilie, Geboes Karen, Chamaillard Mathias, Ouwehand Arthur, Leyer Greg, Carcano Didier, Colombel Jean-Frédéric, Ardid Denis, Desreumaux Pierre, Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors, 10.1038/nm1521
  61. Sarzani Riccardo, Bordicchia Marica, Marcucci Pierfrancesco, Bedetta Samuele, Santini Silvia, Giovagnoli Andrea, Scappini Lorena, Minardi Daniele, Muzzonigro Giovanni, Dessì-Fulgheri Paolo, Rappelli Alessandro, Altered pattern of cannabinoid type 1 receptor expression in adipose tissue of dysmetabolic and overweight patients, 10.1016/j.metabol.2008.10.009
  62. Samuel B. S., Shaito A., Motoike T., Rey F. E., Backhed F., Manchester J. K., Hammer R. E., Williams S. C., Crowley J., Yanagisawa M., Gordon J. I., Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41, 10.1073/pnas.0808567105
  63. Scherer Thomas, Buettner Christoph, The dysregulation of the endocannabinoid system in diabesity—a tricky problem, 10.1007/s00109-009-0459-y
  64. Seki Ekihiro, De Minicis Samuele, Österreicher Christoph H, Kluwe Johannes, Osawa Yosuke, Brenner David A, Schwabe Robert F, TLR4 enhances TGF-β signaling and hepatic fibrosis, 10.1038/nm1663
  65. Sheth P., Delos Santos N., Seth A., LaRusso N. F., Rao R. K., Lipopolysaccharide disrupts tight junctions in cholangiocyte monolayers by a c-Src-, TLR4-, and LBP-dependent mechanism, 10.1152/ajpgi.00582.2006
  66. Shoelson Steven E, Goldfine Allison B, Getting away from glucose: fanning the flames of obesity-induced inflammation, 10.1038/nm0409-373
  67. Starowicz Katarzyna M., Cristino Luigia, Matias Isabel, Capasso Raffaele, Racioppi Alessandro, Izzo Angelo A., Di Marzo Vincenzo, Endocannabinoid Dysregulation in the Pancreas and Adipose Tissue of Mice Fed With a High-fat Diet, 10.1038/oby.2007.106
  68. Turnbaugh Peter J., Hamady Micah, Yatsunenko Tanya, Cantarel Brandi L., Duncan Alexis, Ley Ruth E., Sogin Mitchell L., Jones William J., Roe Bruce A., Affourtit Jason P., Egholm Michael, Henrissat Bernard, Heath Andrew C., Knight Rob, Gordon Jeffrey I., A core gut microbiome in obese and lean twins, 10.1038/nature07540
  69. Turnbaugh Peter J., Ley Ruth E., Mahowald Michael A., Magrini Vincent, Mardis Elaine R., Gordon Jeffrey I., An obesity-associated gut microbiome with increased capacity for energy harvest, 10.1038/nature05414
  70. Weisberg Stuart P., McCann Daniel, Desai Manisha, Rosenbaum Michael, Leibel Rudolph L., Ferrante Anthony W., Obesity is associated with macrophage accumulation in adipose tissue, 10.1172/jci200319246
  71. Yang Xiaolin, Jansson Per-Anders, Nagaev Ivan, Jack Maia M, Carvalho Eugenia, Sunnerhagen Katharina Stibrant, Cam Margaret C, Cushman Samuel W, Smith Ulf, Evidence of impaired adipogenesis in insulin resistance, 10.1016/j.bbrc.2004.03.152