Human omental and subcutaneous adipose tissue exhibit specific lipidomic signatures

FASEB Journal

Volumn 28, Issue 3, 2014, Pages 1071-1081

  Jové, Mariona ^a   Moreno Navarrete, José María ^b   Pamplona, Reinald ^a   Ricart, Wifredo ^b   Portero Otín, Manuel ^a   Fernández Real, José Manuel ^b  

^a UNIVERSITY OF LLEIDA   (Spain)

^b GIRONA BIOMEDICAL RESEARCH INSTITUTE IDIBGI   (Spain)

Author keywords

Insulin resistance; Metabolism; Systems biology

Indexed keywords

C REACTIVE PROTEIN; CHOLESTEROL; EPOXIDE; FAT DROPLET; FATTY ACID; GLYCEROLIPID; GLYCEROPHOSPHOLIPID; LIPIDOME; SPHINGOLIPID; TRIACYLGLYCEROL; CHOLESTEROL ALPHA OXIDE; CHOLESTEROL ALPHA-OXIDE; DRUG DERIVATIVE; PRIMER DNA; TRANSCRIPTOME;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE; ARTICLE; BODY MASS; CELL DIFFERENTIATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IN VITRO STUDY; INSULIN SENSITIVITY; INTRAABDOMINAL FAT; LIPID METABOLISM; LIPID PEROXIDATION; LIPIDOMICS; LIPOGENESIS; LIQUID CHROMATOGRAPHY; MAJOR CLINICAL STUDY; MALE; MASS SPECTROMETRY; MORBID OBESITY; OMENTAL ADIPOSE TISSUE; PRIORITY JOURNAL; SUBCUTANEOUS FAT; TRANSCRIPTOMICS; CYTOLOGY; DRUG EFFECT; INSULIN RESISTANCE; METABOLISM; NUCLEOTIDE SEQUENCE; OMENTUM; OXIDATION REDUCTION REACTION; REAL TIME POLYMERASE CHAIN REACTION; SYSTEMS BIOLOGY;

INSULIN RESISTANCE; METABOLISM; SYSTEMS BIOLOGY;

ADIPOCYTES; BASE SEQUENCE; CELL DIFFERENTIATION; CHOLESTEROL; DNA PRIMERS; FEMALE; GENE EXPRESSION; HUMANS; LIPID METABOLISM; MALE; OMENTUM; OXIDATION-REDUCTION; REAL-TIME POLYMERASE CHAIN REACTION; SUBCUTANEOUS FAT; TRANSCRIPTOME;

EID: 84899539937     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-234419     Document Type: Article

References (46)

1. Fox, C. S., Massaro, J. M., Hoffmann, U., Pou, K. M., Maurovich-Horvat, P., Liu, C. Y., Vasan, R. S., Murabito, J. M., Meigs, J. B., Cupples, L. A., D'Agostino, R. B., Sr., and O'Donnell, C. J. (2007) Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham heart study. Circulation 116, 39-48
2. Gomez-Ambrosi, J., Catalan, V., Diez-Caballero, A., Martinez-Cruz, L. A., Gil, M. J., Garcia-Foncillas, J., Cienfuegos, J. A., Salvador, J., Mato, J. M., and Fruhbeck, G. (2004) Gene expression profile of omental adipose tissue in human obesity. FASEB J. 18, 215-217
3. Arner, P. (2002) Insulin resistance in type 2 diabetes: role of fatty acids. Diabetes Metab. Res. Rev. 18 (Suppl. 2), S5-S9
4. Virtanen, K. A., Lonnroth, P., Parkkola, R., Peltoniemi, P., Asola, M., Viljanen, T., Tolvanen, T., Knuuti, J., Ronnemaa, T., Huupponen, R., and Nuutila, P. (2002) Glucose uptake and perfusion in subcutaneous and visceral adipose tissue during insulin stimulation in nonobese and obese humans. J. Clin. Endocrinol. Metab. 87, 3902-3910
5. Gesta, S., Bluher, M., Yamamoto, Y., Norris, A. W., Berndt, J., Kralisch, S., Boucher, J., Lewis, C., and Kahn, C. R. (2006) Evidence for a role of developmental genes in the origin of obesity and body fat distribution. Proc. Natl. Acad. Sci. U. S. A. 103, 6676-6681
6. MacLaren, R., Cui, W., Simard, S., and Cianflone, K. (2008) Influence of obesity and insulin sensitivity on insulin signaling genes in human omental and subcutaneous adipose tissue. J. Lipid Res. 49, 308-323
7. Perrini, S., Laviola, L., Cignarelli, A., Melchiorre, M., De Stefano, F., Caccioppoli, C., Natalicchio, A., Orlando, M. R., Garruti, G., De Fazio, M., Catalano, G., Memeo, V., Giorgino, R., and Giorgino, F. (2008) Fat depot-related differences in gene expression, adiponectin secretion, and insulin action and signalling in human adipocytes differentiated in vitro from precursor stromal cells. Diabetologia 51, 155-164
8. Perez-Perez, R., Ortega-Delgado, F. J., Garcia-Santos, E., Lopez, J. A., Camafeita, E., Ricart, W., Fernandez-Real, J. M., and Peral, B. (2009) Differential proteomics of omental and subcutaneous adipose tissue reflects their unalike biochemical and metabolic properties. J. Proteome Res. 8, 1682-1693
9. Perrini, S., Ficarella, R., Picardi, E., Cignarelli, A., Barbaro, M., Nigro, P., Peschechera, A., Palumbo, O., Carella, M., De Fazio, M., Natalicchio, A., Laviola, L., Pesole, G., and Giorgino, F. (2013) Differences in gene expression and cytokine release profiles highlight the heterogeneity of distinct subsets of adipose tissue-derived stem cells in the subcutaneous and visceral adipose tissue in humans. PloS One 8, e57892
10. Quehenberger, O., and Dennis, E. A. (2011) The human plasma lipidome. N. Engl. J. Med. 365, 1812-1823
11. Ortiz, A., and Sanchez-Nino, M. D. (2012) The human plasma lipidome. N. Engl. J. Med. 366, 668; author reply 668-669
12. Patti, G. J., Yanes, O., and Siuzdak, G. (2012) Innovation: metabolomics: the apogee of the omics trilogy. Nat. Rev. Mol. Cell Biol. 13, 263-269
13. Jung, H. R., Sylvanne, T., Koistinen, K. M., Tarasov, K., Kauhanen, D., and Ekroos, K. (2011) High throughput quantitative molecular lipidomics. Biochim. Biophys. Acta 1811, 925-934
14. Kolak, M., Westerbacka, J., Velagapudi, V. R., Wagsater, D., Yetukuri, L., Makkonen, J., Rissanen, A., Hakkinen, A. M., Lindell, M., Bergholm, R., Hamsten, A., Eriksson, P., Fisher, R. M., Oresic, M., and Yki-Jarvinen, H. (2007) Adipose tissue inflammation and increased ceramide content characterize subjects with high liver fat content independent of obesity. Diabetes 56, 1960-1968
15. Kim, J. K. (2009) Hyperinsulinemic-euglycemic clamp to assess insulin sensitivity in vivo. Methods Mol. Biol. 560, 221-238
16. Laaksonen, R., Katajamaa, M., Paiva, H., Sysi-Aho, M., Saarinen, L., Junni, P., Lutjohann, D., Smet, J., Van Coster, R., Seppanen-Laakso, T., Lehtimaki, T., Soini, J., and Oresic, M. (2006) A systems biology strategy reveals biological pathways and plasma biomarker candidates for potentially toxic statin-induced changes in muscle. PloS One 1, e97
17. Sandra, K., Pereira Ados, S., Vanhoenacker, G., David, F., and Sandra, P. (2010) Comprehensive blood plasma lipidomics by liquid chromatography/ quadrupole time-of-flight mass spectrometry. J. Chromatogr. A 1217, 4087-4099
18. Moreno-Navarrete, J. M., Ortega, F. J., Rodriguez-Hermosa, J. I., Sabater, M., Pardo, G., Ricart, W., and Fernandez-Real, J. M. (2011) OCT1 expression in adipocytes could contribute to increased metformin action in obese subjects. Diabetes 60, 168-176
19. Davies, J. D., Carpenter, K. L., Challis, I. R., Figg, N. L., McNair, R., Proudfoot, D., Weissberg, P. L., and Shanahan, C. M. (2005) Adipocytic differentiation and liver X receptor pathways regulate the accumulation of triacylglycerols in human vascular smooth muscle cells. J. Biol. Chem. 280, 3911-3919
20. Kha, H. T., Basseri, B., Shouhed, D., Richardson, J., Tetradis, S., Hahn, T. J., and Parhami, F. (2004) Oxysterols regulate differentiation of mesenchymal stem cells: pro-bone and anti-fat. J. Bone Miner. Res. 19, 830-840
21. Kim, W. K., Meliton, V., Amantea, C. M., Hahn, T. J., and Parhami, F. (2007) 20(S)-hydroxycholesterol inhibits PPARα expression and adipogenic differentiation of bone marrow stromal cells through a hedgehog-dependent mechanism. J. Bone Miner. Res. 22, 1711-1719
22. Johnson, J. S., Meliton, V., Kim, W. K., Lee, K. B., Wang, J. C., Nguyen, K., Yoo, D., Jung, M. E., Atti, E., Tetradis, S., Pereira, R. C., Magyar, C., Nargizyan, T., Hahn, T. J., Farouz, F., Thies, S., and Parhami, F. (2011) Novel oxysterols have pro-osteogenic and anti-Adipogenic effects in vitro and induce spinal fusion in vivo. J. Cell. Biochem. 112, 1673-1684
23. National Institute of General Medical Sciences. (2010) Lipid Metabolites and Pathways Strategy (Lipid MAPS) lipidomics gateway. Retrieved August 5, 2013 from http://www.lipidmaps. org/
24. Xia, J., Psychogios, N., Young, N., and Wishart, D. S. (2009) MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucl. Acids Res. 37, W652-W660
25. Otani, H. (2011) Oxidative stress as pathogenesis of cardiovascular risk associated with metabolic syndrome. Antioxid. Redox Signal. 15, 1911-1926
26. Wahle, K. W., McIntosh, G., Duncan, W. R., and James, W. P. (1991) Concentrations of linoleic acid in adipose tissue differ with age in women but not men. Eur. J. Clin. Nutr. 45, 195-202
27. Meex, R. C., Schrauwen, P., and Hesselink, M. K. (2009) Modulation of myocellular fat stores: lipid droplet dynamics in health and disease. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R913-R924
28. Horl, G., Wagner, A., Cole, L. K., Malli, R., Reicher, H., Kotzbeck, P., Kofeler, H., Hofler, G., Frank, S., Bogner-Strauss, J. G., Sattler, W., Vance, D. E., and Steyrer, E. (2011) Sequential synthesis and methylation of phosphatidylethanolamine pro-mote lipid droplet biosynthesis and stability in tissue culture and in vivo. J. Biol. Chem. 286, 17338-17350
29. Hodson, L., Skeaff, C. M., and Fielding, B. A. (2008) Fatty acid composition of adipose tissue and blood in humans and its use as a biomarker of dietary intake. Progr. Lipid Res. 47, 348-380
30. Bas, P., Gallouin, F., and Morand-Fehr, P. (1992) Changes in lipid content, fatty acid composition and lipoprotein lipase activity in dry goat omental adipose tissue according to tissue site. Lipids 27, 470-473
31. Garcia-Serrano, S., Moreno-Santos, I., Garrido-Sanchez, L., Gutierrez-Repiso, C., Garcia-Almeida, J. M., Garcia-Arnes, J., Rivas-Marin, J., Gallego-Perales, J. L., Garcia-Escobar, E., Rojo-Martinez, G., Tinahones, F., Soriguer, F., Macias-Gonzalez, M., and Garcia-Fuentes, E. (2011) Stearoyl-CoA desaturase-1 is associated with insulin resistance in morbidly obese subjects. Mol. Med. 17, 273-280
32. Machann, J., Stefan, N., Schabel, C., Schleicher, E., Fritsche, A., Wurslin, C., Haring, H. U., Claussen, C. D., and Schick, F. (2013) Fraction of unsaturated fatty acids in visceral adipose tissue (VAT) is lower in subjects with high total VAT volume -A combined 1 H MRS and volumetric MRI study in male subjects. NMR Biomed. 26, 232-236
33. Sato, D., Nakamura, T., Tsutsumi, K., Shinzawa, G., Karimata, T., Okawa, T., Feng, Z., and Kusunoki, M. (2012) Site dependency of fatty acid composition in adipose triacylglycerol in rats and its absence as a result of high-fat feeding. Metab. Clin. Exp. 61, 92-98
34. Ortega, F. J., Vazquez-Martin, A., Moreno-Navarrete, J. M., Bassols, J., Rodriguez-Hermosa, J., Girones, J., Ricart, W., Peral, B., Tinahones, F. J., Fruhbeck, G., Menendez, J. A., and Fernandez-Real, J. M. (2010) Thyroid hormone responsive spot 14 increases during differentiation of human adipocytes and its expression is down-regulated in obese subjects. Int. J. Obes. (Lond.) 34, 487-499
35. Zheng, W., Kollmeyer, J., Symolon, H., Momin, A., Munter, E., Wang, E., Kelly, S., Allegood, J. C., Liu, Y., Peng, Q., Ramaraju, H., Sullards, M. C., Cabot, M., and Merrill, A. H., Jr. (2006) Ceramides and other bioactive sphingolipid backbones in health and disease: lipidomic analysis, metabolism and roles in membrane structure, dynamics, signaling and autophagy. Biochim. Biophys. Acta1758, 1864-1884
36. Samad, F., Badeanlou, L., Shah, C., and Yang, G. (2011) Adipose tissue and ceramide biosynthesis in the pathogenesis of obesity. Adv. Exp. Med. Biol. 721, 67-86
37. Samad, F., Hester, K. D., Yang, G., Hannun, Y. A., and Bielawski, J. (2006) Altered adipose and plasma sphingolipid metabolism in obesity: A potential mechanism for cardiovascular and metabolic risk. Diabetes 55, 2579-2587
38. Kobayashi, A., Takanezawa, Y., Hirata, T., Shimizu, Y., Misasa, K., Kioka, N., Arai, H., Ueda, K., and Matsuo, M. (2006) Efflux of sphingomyelin, cholesterol, and phosphatidylcholine by ABCG1. J. Lipid Res. 47, 1791-1802
39. Guo, L., Zhou, D., Pryse, K. M., Okunade, A. L., and Su, X. (2010) Fatty acid 2-hydroxylase mediates diffusional mobility of raft-Associated lipids, GLUT4 level, and lipogenesis in 3T3-L1 adipocytes. J. Biol. Chem. 285, 25438-25447
40. Roberts, L. D., Virtue, S., Vidal-Puig, A., Nicholls, A. W., and Griffin, J. L. (2009) Metabolic phenotyping of a model of adipocyte differentiation. Physiol. Genomics 39, 109-119
41. Lau, W. F., and Das, N. P. (1995) In vitro modulation of rat adipocyte ghost membrane fluidity by cholesterol oxysterols. Experientia 51, 731-737
42. Laffitte, B. A., Repa, J. J., Joseph, S. B., Wilpitz, D. C., Kast, H. R., Mangelsdorf, D. J., and Tontonoz, P. (2001) LXRs control lipid-inducible expression of the apolipoprotein E gene in macrophages and adipocytes. Proc. Natl. Acad. Sci. U. S. A. 98, 507-512
43. Ulven, S. M., Dalen, K. T., Gustafsson, J. A., and Nebb, H. I. (2005) LXR is crucial in lipid metabolism. Prostaglandins Leukot. Essent. Fatty Acids 73, 59-63
44. Dwyer, J. R., Sever, N., Carlson, M., Nelson, S. F., Beachy, P. A., and Parhami, F. (2007) Oxysterols are novel activators of the hedgehog signaling pathway in pluripotent mesenchymal cells. J. Biol. Chem. 282, 8959-8968
45. Marwarha, G., Dasari, B., and Ghribi, O. (2012) Endoplasmic reticulum stress-induced CHOP activation mediates the downregulation of leptin in human neuroblastoma SH-SY5Y cells treated with the oxysterol 27-hydroxycholesterol. Cell. Signal. 24, 484-492
46. Leem, J., and Koh, E. H. (2012) Interaction between mitochondria and the endoplasmic reticulum: Implications for the pathogenesis of type 2 diabetes mellitus. Exp. Diabetes Res. 2012, 242984