Cell type-specific modulation of lipid mediator's formation in murine adipose tissue by omega-3 fatty acids

Biochemical and Biophysical Research Communications

Volumn 469, Issue 3, 2016, Pages 731-736

  Kuda, Ondrej ^a   Rombaldova, Martina ^a,b   Janovska, Petra ^a   Flachs, Pavel ^a   Kopecky, Jan ^a  

^a INSTITUTE OF PHYSIOLOGY   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

Author keywords

Adipose tissue macrophages; Lipid mediators; Lipidomics; Omega 3 PUFA; Protectin D1

Indexed keywords

ANANDAMIDE; CD11B ANTIGEN; CD59 ANTIGEN; DOCOSAHEXAENOIC ACID; ENDOCANNABINOID; ICOSAPENTAENOIC ACID; LIPID; OMEGA 3 FATTY ACID; PROTECTIN D1; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; ANTIINFLAMMATORY AGENT; IMMUNOLOGIC FACTOR;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALORIC RESTRICTION; CONTROLLED STUDY; EPIDIDYMIS; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; INFLAMMATION; LIPID DEGRADATION; LIPID DIET; LIPID METABOLISM; LIPIDOMICS; MACROPHAGE; MACROPHAGE ACTIVATION; MALE; MONOCYTE; MOUSE; NONHUMAN; OBESITY; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; TISSUE LEVEL; WEIGHT GAIN; WHITE ADIPOSE TISSUE; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DIETARY SUPPLEMENT; DRUG EFFECTS; ENZYMOLOGY; IMMUNOLOGY; ORAL DRUG ADMINISTRATION; STROMA CELL;

ADIPOCYTES; ADIPOSE TISSUE, WHITE; ADMINISTRATION, ORAL; ANIMALS; ANTI-INFLAMMATORY AGENTS; CELLS, CULTURED; DIETARY SUPPLEMENTS; FATTY ACIDS, OMEGA-3; IMMUNOLOGIC FACTORS; LIPID METABOLISM; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; STROMAL CELLS;

EID: 84953635674     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2015.12.055     Document Type: Article

References (42)

1. M. Masoodi, O. Kuda, M. Rossmeisl, P. Flachs, and J. Kopecky Lipid signaling in adipose tissue: connecting inflammation & metabolism Biochim. Biophys. Acta 1851 2015 503 518
2. P. Flachs, M. Rossmeisl, O. Kuda, and J. Kopecky Stimulation of mitochondrial oxidative capacity in white fat independent of UCP1: a key to lean phenotype Biochim. Biophys. Acta 1831 2013 986 1003
3. A. Iyer, D.P. Fairlie, J.B. Prins, B.D. Hammock, and L. Brown Inflammatory lipid mediators in adipocyte function and obesity Nat. Rev. Endocrinol. 6 2010 71 82
4. W. Wahli, and L. Michalik PPARs at the crossroads of lipid signaling and inflammation Trends Endocrinol. Metab. 23 2012 351 363
5. G. Cildir, S.C. Akincilar, and V. Tergaonkar Chronic adipose tissue inflammation: all immune cells on the stage Trends Mol. Med. 19 2013 487 500
6. C.N. Lumeng, J.L. Bodzin, and A.R. Saltiel Obesity induces a phenotypic switch in adipose tissue macrophage polarization J. Clin. Investig. 117 2007 175 184
7. C.N. Lumeng, S.M. Deyoung, J.L. Bodzin, and A.R. Saltiel Increased inflammatory properties of adipose tissue macrophages recruited during diet-induced obesity Diabetes 56 2007 16 23
8. A. Chawla, K.D. Nguyen, and Y.P. Goh Macrophage-mediated inflammation in metabolic disease Nat. Rev. Immunol. 11 2011 738 749
9. A. Kosteli, E. Sugaru, G. Haemmerle, J.F. Martin, J. Lei, R. Zechner, and A.W. Ferrante Jr. Weight loss and lipolysis promote a dynamic immune response in murine adipose tissue J. Clin. Investig. 120 2010 3466 3479
10. S.P. Weisberg, D. McCann, M. Desai, M. Rosenbaum, R.L. Leibel, and A.W. Ferrante Obesity is associated with macrophage accumulation in adipose tissue J. Clin. Investig. 112 2003 1796 1808
11. H. Xu, G.T. Barnes, Q. Yang, G. Tan, D. Yang, C.J. Chou, J. Sole, A. Nichols, J.S. Ross, L.A. Tartaglia, and H. Chen Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance J. Clin. Investig. 112 2003 1821 1830
12. N. Kloting, M. Fasshauer, A. Dietrich, P. Kovacs, M.R. Schon, M. Kern, M. Stumvoll, and M. Bluher Insulin-sensitive obesity Am. J. Physiol. Endocrinol. Metab. 299 2010 E506 E515
13. C.N. Lumeng, J.B. Delproposto, D.J. Westcott, and A.R. Saltiel Phenotypic switching of adipose tissue macrophages with obesity is generated by spatiotemporal differences in macrophage subtypes Diabetes 57 2008 3239 3246
14. D.Y. Oh, S. Talukdar, E.J. Bae, T. Imamura, H. Morinaga, W.Q. Fan, P.P. Li, W.J. Lu, S.M. Watkins, and J.M. Olefsky GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects Cell 142 2010 687 698
15. M.E. Shaul, G. Bennett, K.J. Strissel, A.S. Greenberg, and M.S. Obin Dynamic, M2-like remodeling phenotypes of CD11c+ adipose tissue macrophages during high-fat diet-induced obesity in mice Diabetes 59 2010 1171 1181
16. X. Prieur, C.Y. Mok, V.R. Velagapudi, V. Nunez, L. Fuentes, D. Montaner, K. Ishikawa, A. Camacho, N. Barbarroja, S. O'Rahilly, J.K. Sethi, J. Dopazo, M. Oresic, M. Ricote, and A. Vidal-Puig Differential lipid partitioning between adipocytes and tissue macrophages modulates macrophage lipotoxicity and M2/M1 polarization in obese mice Diabetes 60 2011 797 809
17. M. Kratz, B.R. Coats, K.B. Hisert, D. Hagman, V. Mutskov, E. Peris, K.Q. Schoenfelt, J.N. Kuzma, I. Larson, P.S. Billing, R.W. Landerholm, M. Crouthamel, D. Gozal, S. Hwang, P.K. Singh, and L. Becker Metabolic dysfunction drives a mechanistically distinct proinflammatory phenotype in adipose tissue macrophages Cell Metab. 20 2014 614 625
18. M. Aouadi, P. Vangala, J.C. Yawe, M. Tencerova, S.M. Nicoloro, J.L. Cohen, Y. Shen, and M.P. Czech Lipid storage by adipose tissue macrophages regulates systemic glucose tolerance Am. J. Physiol. Endocrinol. Metab. 307 2014 E374 E383
19. S.K. Koliwad, R.S. Streeper, M. Monetti, I. Cornelissen, L. Chan, K. Terayama, S. Naylor, M. Rao, B. Hubbard, and R.V. Farese Jr. DGAT1-dependent triacylglycerol storage by macrophages protects mice from diet-induced insulin resistance and inflammation J. Clin. Investig. 120 2010 756 767
20. S. Cinti, G. Mitchell, G. Barbatelli, I. Murano, E. Ceresi, E. Faloia, S. Wang, M. Fortier, A.S. Greenberg, and M.S. Obin Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans J. Lipid Res. 46 2005 2347 2355
21. J. Hellmann, Y. Tang, M. Kosuri, A. Bhatnagar, and M. Spite Resolvin D1 decreases adipose tissue macrophage accumulation and improves insulin sensitivity in obese-diabetic mice FASEB J. 25 2011 2399 2407
22. E. Titos, B. Rius, A. Gonzalez-Periz, C. Lopez-Vicario, E. Moran-Salvador, M. Martinez-Clemente, V. Arroyo, and J. Claria Resolvin D1 and its precursor docosahexaenoic acid promote resolution of adipose tissue inflammation by eliciting macrophage polarization toward an M2-like phenotype J. Immunol. 187 2011 5408 5418
23. P. Flachs, R. Ruhl, M. Hensler, P. Janovska, P. Zouhar, V. Kus, J.Z. Macek, E. Papp, O. Kuda, M. Svobodova, M. Rossmeisl, G. Tsenov, V. Mohamed-Ali, and J. Kopecky Synergistic induction of lipid catabolism and anti-inflammatory lipids in white fat of dietary obese mice in response to calorie restriction and n-3 fatty acids Diabetologia 54 2011 2626 2638
24. A. Neuhofer, M. Zeyda, D. Mascher, B.K. Itariu, I. Murano, L. Leitner, E.E. Hochbrugger, P. Fraisl, S. Cinti, C.N. Serhan, and T.M. Stulnig Impaired local production of proresolving lipid mediators in obesity and 17-HDHA as a potential treatment for obesity-associated inflammation Diabetes 62 2013 1945 1956
25. M. Rossmeisl, J.Z. Macek, O. Kuda, T. Jelenik, D. Medrikova, B. Stankova, B. Kristinsson, G.G. Haraldsson, H. Svensen, I. Stoknes, P. Sjovall, Y. Magnusson, M.G. Balvers, K.C. Verhoeckx, E. Tvrzicka, M. Bryhn, and J. Kopecky 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 7 2012 e38834
26. O. Kuda, T. Jelenik, Z. Jilkova, P. Flachs, M. Rossmeisl, M. Hensler, L. Kazdova, N. Ogston, M. Baranowski, J. Gorski, P. Janovska, V. Kus, J. Polak, V. Mohamed-Ali, R. Burcelin, S. Cinti, M. Bryhn, and J. Kopecky n-3 Fatty acids and rosiglitazone improve insulin sensitivity through additive stimulatory effects on muscle glycogen synthesis in mice fed a high-fat diet Diabetologia 52 2009 941 951
27. M. Rodbell Metabolism of isolated fat cells. I. Effects of hormones on glucose metabolism and lipolysis J. Biol. Chem. 239 1964 375 380
28. O. Kuda, C.M. Jenkins, J.R. Skinner, S.H. Moon, X. Su, R.W. Gross, and N.A. Abumrad CD36 protein is involved in store-operated calcium flux, phospholipase A2 activation, and production of prostaglandin E2 J. Biol. Chem. 286 2011 17785 17795
29. D.S. Dumlao, M.W. Buczynski, P.C. Norris, R. Harkewicz, and E.A. Dennis High-throughput lipidomic analysis of fatty acid derived eicosanoids and N-acylethanolamines Biochim. Biophys. Acta 1811 2011 724 736
30. R. Yang, N. Chiang, S.F. Oh, C.N. Serhan, Metabolomics-lipidomics of eicosanoids and docosanoids generated by phagocytes, Current Protocols in Immunology/edited by John E. Coligan. [et al.], Chapter 14 (2011) Unit 14 26.
31. M. Lisa, M. Holcapek, and H. Sovova Comparison of various types of stationary phases in non-aqueous reversed-phase high-performance liquid chromatography-mass spectrometry of glycerolipids in blackcurrant oil and its enzymatic hydrolysis mixture J. Chromatogr. A 1216 2009 8371 8378
32. M. Yuan, S.B. Breitkopf, X. Yang, and J.M. Asara A positive/negative ion-switching, targeted mass spectrometry-based metabolomics platform for bodily fluids, cells, and fresh and fixed tissue Nat. Protoc. 7 2012 872 881
33. W.B. Dunn, D. Broadhurst, P. Begley, E. Zelena, S. Francis-McIntyre, N. Anderson, M. Brown, J.D. Knowles, A. Halsall, J.N. Haselden, A.W. Nicholls, I.D. Wilson, D.B. Kell, R. Goodacre, and C. Human Serum Metabolome Procedures for large-scale metabolic profiling of serum and plasma using gas chromatography and liquid chromatography coupled to mass spectrometry Nat. Protoc. 6 2011 1060 1083
34. K.W. Cho, D.L. Morris, and C.N. Lumeng Flow cytometry analyses of adipose tissue macrophages Methods Enzymol. 537 2014 297 314
35. J. Fitzgerald, R. Colas, M. Shinohara, J. Dalli, and C.N. Serhan Lipid Mediator Metabololipidomics LC-MS-MS Spectra Book 2014 2014 Harvard Medical School
36. J.W. Pollard Trophic macrophages in development and disease Nat. Rev. Immunol. 9 2009 259 270
37. Y.H. Lee, A.P. Petkova, and J.G. Granneman Identification of an adipogenic niche for adipose tissue remodeling and restoration Cell Metab. 18 2013 355 367
38. T. Yamada, Y. Tani, H. Nakanishi, R. Taguchi, M. Arita, and H. Arai Eosinophils promote resolution of acute peritonitis by producing proresolving mediators in mice FASEB J. 25 2011 561 568
39. M. Aursnes, J.E. Tungen, R.A. Colas, I. Vlasakov, J. Dalli, C.N. Serhan, T.V. Hansen, Synthesis of the 16S,17S-epoxyprotectin intermediate in the biosynthesis of protectins by human macrophages, J. Nat. Prod. 10.1021/acs.jnatprod.5b00574. Publication Date (Web): November 18, 2015.
40. A. Ariel, P.L. Li, W. Wang, W.X. Tang, G. Fredman, S. Hong, K.H. Gotlinger, and C.N. Serhan The docosatriene protectin D1 is produced by TH2 skewing and promotes human T cell apoptosis via lipid raft clustering J. Biol. Chem. 280 2005 43079 43086
41. Y. Huo, L. Zhao, M.C. Hyman, P. Shashkin, B.L. Harry, T. Burcin, S.B. Forlow, M.A. Stark, D.F. Smith, S. Clarke, S. Srinivasan, C.C. Hedrick, D. Pratico, J.L. Witztum, J.L. Nadler, C.D. Funk, and K. Ley Critical role of macrophage 12/15-lipoxygenase for atherosclerosis in apolipoprotein E-deficient mice Circulation 110 2004 2024 2031
42. B.K. Cole, D.C. Lieb, A.D. Dobrian, and J.L. Nadler 12- and 15-lipoxygenases in adipose tissue inflammation Prostaglandins Other Lipid Mediat. 104-105 2013 84 92