Adipose tissue NAPE-PLD controls fat mass development by altering the browning process and gut microbiota

Nature Communications

Volumn 6, Issue , 2015, Pages

  Geurts, Lucie ^a   Everard, Amandine ^a   Van Hul, Matthias ^a   Essaghir, Ahmed ^b   Duparc, Thibaut ^a   Matamoros, Sébastien ^a   Plovier, Hubert ^a   Castel, Julien ^c   Denis, Raphael G P ^c   Bergiers, Marie ^a   Druart, Céline ^a   Alhouayek, Mireille ^a   Delzenne, Nathalie M ^a   Muccioli, Giulio G ^a   Demoulin, Jean Baptiste ^b   Luquet, Serge ^c   Cani, Patrice D ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b DE DUVE INSTITUTE   (Belgium)

^c UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOCANNABINOID; LIPID; N ACYLPHOSPHATIDYLETHANOLAMINE PHOSPHOLIPASE D; PHOSPHOLIPASE; UNCLASSIFIED DRUG; N-ACYLPHOSPHATIDYLETHANOLAMINE PHOSPHOLIPASE D, MOUSE; PHOSPHOLIPASE D;

BIOACTIVITY; BIOENERGETICS; ENZYME ACTIVITY; FAT; HOMEOSTASIS; LIPID; METABOLISM; MICROBIOLOGY; OBESITY; PHENOTYPE; PHYSIOLOGICAL RESPONSE; RODENT;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENERGY BALANCE; FAT MASS; GERMFREE MOUSE; GLUCOSE INTOLERANCE; GLYCATION; INFLAMMATION; INTESTINE FLORA; LIPID METABOLISM; METABOLIC REGULATION; MOUSE; NONHUMAN; OBESITY; PANDEMIC; PHENOTYPE; ANIMAL; BODY FAT DISTRIBUTION; BROWN ADIPOSE TISSUE; COLD; DEFICIENCY; ENERGY METABOLISM; GENE EXPRESSION; GENETICS; KNOCKOUT MOUSE; MALE; METABOLISM; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY; WHITE ADIPOSE TISSUE;

MUS;

ADIPOSE TISSUE, BROWN; ADIPOSE TISSUE, WHITE; ANIMALS; BODY FAT DISTRIBUTION; COLD TEMPERATURE; ENDOCANNABINOIDS; ENERGY METABOLISM; GASTROINTESTINAL MICROBIOME; GENE EXPRESSION; GLUCOSE INTOLERANCE; INFLAMMATION; MALE; MICE; MICE, KNOCKOUT; OBESITY; PHOSPHOLIPASE D;

EID: 84924667080     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7495     Document Type: Article

References (64)

1. Muccioli, G. G. Endocannabinoid biosynthesis and inactivation, from simple to complex. Drug Discov. Today 15, 474-483 (2010).
2. Jamshidi, N. & Taylor, D. A. Anandamide administration into the ventromedial hypothalamus stimulates appetite in rats. Br. J. Pharmacol. 134, 1151-1154 (2001).
3. Hansen, H. S. & Diep, T. A. N-acylethanolamines anandamide and food intake. Biochem. Pharmacol. 78, 553-560 (2009).
4. Leung, D., Saghatelian, A., Simon, G. M. & Cravatt, B. F. Inactivation of N-acyl phosphatidylethanolamine phospholipase D reveals multiple mechanisms for the biosynthesis of endocannabinoids. Biochemistry 45, 4720-4726 (2006).
5. Di Marzo, V. Endocannabinoids: synthesis and degradation. Rev. Physiol. Biochem. Pharmacol. 160, 1-24 (2008).
6. Ryberg, E. et al. The orphan receptor GPR55 is a novel cannabinoid receptor. Br. J. Pharmacol. 152, 1092-1101 (2007).
7. Lo Verme, J. et al. The nuclear receptor peroxisome proliferator-activated receptor-alpha mediates the anti-inflammatory actions of palmitoylethanolamide. Mol. Pharmacol. 67, 15-19 (2005).
8. Syed, S. K. et al. Regulation of GPR119 receptor activity with endocannabinoidlike lipids. Am. J. Physiol. Endocrinol. Metab. 303, E1469-E1478 (2012).
9. Hoareau, L. et al. Anti-inflammatory effect of palmitoylethanolamide on human adipocytes. Obesity(SilverSpring) 17, 431-438 (2009).
10. Esposito, G. et al. Palmitoylethanolamide improves colon inflammation through an enteric glia/toll like receptor 4-dependent PPAR-alpha activation. Gut 63, 1300-1312 (2014).
11. Simon, G. M. & Cravatt, B. F. Characterization of mice lacking candidate N-acyl ethanolamine biosynthetic enzymes provides evidence for multiple pathways that contribute to endocannabinoid production in vivo. Mol. Biosyst. 6, 1411-1418 (2010).
12. Galic, S., Oakhill, J. S. & Steinberg, G. R. Adipose tissue as an endocrine organ. Mol. Cell Endocrinol. 316, 129-139 (2010).
13. Lafontan, M. Adipose tissue and adipocyte dysregulation. Diabetes Metab. 40, 16-28 (2014).
14. Muccioli, G. G. et al. The endocannabinoid system links gut microbiota to adipogenesis. Mol. Syst. Biol. 6, 392 (2010).
15. Geurts, L. et al. Altered gut microbiota and endocannabinoid system tone in obese and diabetic leptin-resistant mice: impact on apelin regulation in adipose tissue. Front. Microbiol. 2, 149 (2011).
16. D'Eon, T. M. et al. The role of adipocyte insulin resistance in the pathogenesis of obesity-related elevations in endocannabinoids. Diabetes 57, 1262-1268 (2008).
17. Silvestri, C. et al. Anandamide-derived prostamide F2alpha negatively regulates adipogenesis. J. Biol. Chem. 288, 23307-23321 (2013).
18. Mori, M. A. et al. Altered miRNA processing disrupts brown/white adipocyte determination and associates with lipodystrophy. J. Clin. Invest. 124, 3339-3351 (2014).
19. Lee, K. Y. et al. Lessons on conditional gene targeting in mouse adipose tissue. Diabetes 62, 864-874 (2013).
20. Mullican, S. E. et al. A novel adipose-specific gene deletion model demonstrates potential pitfalls of existing methods. Mol. Endocrinol. 27, 127-134 (2013).
21. Tsuboi, K. et al. Enzymatic formation of N-acylethanolamines from N-acylethanolamine plasmalogen through N-acylphosphatidylethanolamine-hydrolyzing phospholipase D-dependent and -independent pathways. Biochim. Biophys. Acta 1811, 565-577 2011.
22. Funk, C. D. Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294, 1871-1875 (2001).
23. Moreno-Navarrete, J. M. et al. A role for adipocyte-derived lipopolysaccharide-binding protein in inflammation- and obesity-associated adipose tissue dysfunction. Diabetologia 56, 2524-2537 (2013).
24. Everard, A. et al. Microbiome of prebiotic-treated mice reveals novel targets involved in host response during obesity. ISME J. 8, 2116-2130 (2014).
25. Cani, P. D. et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56, 1761-1772 (2007).
26. Rosen, E. D. & Spiegelman, B. M. What we talk about when we talk about fat. Cell 156, 20-44 (2014).
27. Nedergaard, J. & Cannon, B. The browning of white adipose tissue: some burning issues. Cell Metab. 20, 396-407 (2014).
28. Turnbaugh, P. J., Backhed, F., Fulton, L. & Gordon, J. I. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3, 213-223 (2008).
29. Alhouayek, M. et al. N-Acylethanolamine-hydrolyzing acid amidase inhibition increases colon N-palmitoylethanolamine levels and counteracts murine colitis. FASEB J. 29, 650-661 (2015).
30. Buckley, C. D., Gilroy, D. W. & Serhan, C. N. Proresolving lipid mediators and mechanisms in the resolution of acute inflammation. Immunity 40, 315-327 (2014).
31. Zhu, C. et al. Proinflammatory stimuli control N-acylphosphatidylethanolamine-specific phospholipase D expression in macrophages. Mol. Pharmacol. 79, 786-792 (2011).
32. Geurts, L., Muccioli, G. G., Delzenne, N. M. & Cani, P. D. Chronic endocannabinoid system stimulation induces muscle macrophage and lipid accumulation in type 2 diabetic mice independently of metabolic endotoxaemia. PLoS ONE 8, e55963 (2013).
33. Li, Z., Schmidt, S. F. & Friedman, J. M. Developmental role for endocannabinoid signaling in regulating glucose metabolism and growth. Diabetes 62, 2359-2367 (2013).
34. Cani, P. D., Geurts, L., Matamoros, S., Plovier, H. & Duparc, T. Glucose metabolism: Focus on gut microbiota, the endocannabinoid system and beyond. Diabetes Metab. 40, 246-257 (2014).
35. Wellen, K. E. & Hotamisligil, G. S. Inflammation, stress, and diabetes. J. Clin. Invest. 115, 1111-1119 (2005).
36. Sell, H., Habich, C. & Eckel, J. Adaptive immunity in obesity and insulin resistance. Nat. Rev. Endocrinol. 8, 709-716 (2012).
37. Ussher, J. R. et al. Inhibition of de novo ceramide synthesis reverses dietinduced insulin resistance and enhances whole-body oxygen consumption. Diabetes 59, 2453-2464 (2010).
38. Cinar, R. et al. Hepatic cannabinoid-1 receptors mediate diet-induced insulin resistance by increasing de novo synthesis of long-chain ceramides. Hepatology 59, 143-153 (2014).
39. Alhouayek, M. & Muccioli, G. G. COX-2-derived endocannabinoid metabolites as novel inflammatory mediators. Trends Pharmacol. Sci. 35, 284-292 (2014).
40. Alhouayek, M., Masquelier, J., Cani, P. D., Lambert, D. M. & Muccioli, G. G. Implication of the anti-inflammatory bioactive lipid prostaglandin D2-glycerol ester in the control of macrophage activation and inflammation by ABHD6. Proc. Natl Acad. Sci. USA 110, 17558-17563 (2013).
41. Brown, K. L., Davidson, J. & Rotondo, D. Characterisation of the prostaglandin E2-ethanolamide suppression of tumour necrosis factor-alpha production in human monocytic cells. Biochim. Biophys. Acta 1831, 1098-1107 2013.
42. Gillum, M. P. et al. N-acylphosphatidylethanolamine, a gut- derived circulating factor induced by fat ingestion, inhibits food intake. Cell 135, 813-824 (2008).
43. Wu, J. et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150, 366-376 (2012).
44. Ye, L. et al. Fat cells directly sense temperature to activate thermogenesis. Proc. Natl Acad. Sci. USA 110, 12480-12485 (2013).
45. Cohen, P. et al. Ablation of PRDM16 and beige adipose causes metabolic dysfunction and a subcutaneous to visceral fat switch. Cell 156, 304-316 (2014).
46. Nakamura, Y., Sato, T., Shiimura, Y., Miura, Y. & Kojima, M. FABP3 and brown adipocyte-characteristic mitochondrial fatty acid oxidation enzymes are induced in beige cells in a different pathway from UCP1. Biochem. Biophys. Res. Commun. 441, 42-46 (2013).
47. Bajzer, M. et al. Cannabinoid receptor 1 (CB1) antagonism enhances glucose utilisation and activates brown adipose tissue in diet-induced obese mice. Diabetologia 54, 3121-3131 (2011).
48. Boon, M. R. et al. Peripheral cannabinoid 1 receptor blockade activates brown adipose tissue and diminishes dyslipidemia and obesity. FASEB J. 28, 5361-5375 (2014).
49. Suarez, J. et al. Oleoylethanolamide enhances beta-adrenergic-mediated thermogenesis and white-to-brown adipocyte phenotype in epididymal white adipose tissue in rat. Dis. Model. Mech. 7, 129-141 (2014).
50. Garcia-Alonso, V. et al. Coordinate functional regulation between microsomal prostaglandin E synthase-1 (mPGES-1) and peroxisome proliferator-activated receptor gamma (PPARgamma) in the conversion of white-to-brown adipocytes. J. Biol. Chem. 288, 28230-28242 (2013).
51. Zhang, X. et al. Structural changes of gut microbiota during berberine-mediated prevention of obesity and insulin resistance in high-fat diet-fed rats. PLoS ONE 7, e42529 (2012).
52. Geurts, L., Neyrinck, A. M., Delzenne, N. M., Knauf, C. & Cani, P. D. Gut microbiota controls adipose tissue expansion, gut barrier and glucose metabolism: novel insights into molecular targets and interventions using prebiotics. Benef. Microbes 5, 3-17 (2014).
53. Cani, P. D. & Van Hul, M. Novel opportunities for next-generation probiotics targeting metabolic syndrome. Curr. Opin. Biotechnol. 32, 21-27 (2015).
54. Cani, P. D. et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58, 1091-1103 (2009).
55. Liu, J. et al. Multiple pathways involved in the biosynthesis of anandamide. Neuropharmacology 54, 1-7 (2008).
56. Everard, A. et al. Intestinal epithelial MyD88 is a sensor switching host metabolism towards obesity according to nutritional status. Nat. Commun. 5, 5648 (2014).
57. Essaghir, A., Dif, N., Marbehant, C. Y., Coffer, P. J. & Demoulin, J. B. The transcription of FOXO genes is stimulated by FOXO3 and repressed by growth factors. J. Biol. Chem. 284, 10334-10342 (2009).
58. Huang da, W., Sherman, B. T. & Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).
59. Wu, G. D. et al. Sampling and pyrosequencing methods for characterizing bacterial communities in the human gut using 16S sequence tags. BMC Microbiol. 10, 206 (2010).
60. Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336 (2010).
61. Pachikian, B. D. et al. Hepatic n-3 polyunsaturated fatty acid depletion promotes steatosis and insulin resistance in mice: genomic analysis of cellular targets. PLoS ONE 6, e23365 (2011).
62. Zhang, X., Goncalves, R. & Mosser, D. M. The isolation and characterization of murine macrophages. Curr. Protoc. Immunol. Chapter 14, Unit 14 11 (2008).
63. Rajas, F., Bruni, N., Montano, S., Zitoun, C. & Mithieux, G. The glucose-6 phosphatase gene is expressed in human and rat small intestine: regulation of expression in fasted and diabetic rats. Gastroenterology 117, 132-139 (1999).
64. Everard, A. et al. Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes 60, 2775-2786 (2011).