Human adipocytes induce inflammation and atrophy in muscle cells during obesity

Diabetes

Volumn 64, Issue 9, 2015, Pages 3121-3134

  Pellegrinelli, Vanessa ^a,b   Rouault, Christine ^a,b,c   Rodriguez Cuenca, Sergio ^d   Albert, Victorine ^a,b,c   Edom Vovard, Frédérique ^a,b,e,f   Vidal Puig, Antonio ^d   Clément, Karine ^a,b,c   Butler Browne, Gillian S ^a,b,e,f   Lacasa, Danièle ^a,b,c  

^a INSERM   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e CNRS   (France)

^f Institut de Myologie   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CONTRACTILE PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; SOMATOMEDIN B; SOMATOMEDIN BINDING PROTEIN 5; CYTOKINE; IGF2 PROTEIN, HUMAN; INTERLEUKIN 10; TUMOR NECROSIS FACTOR ALPHA;

ADIPOCYTE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; COCULTURE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; INFLAMMATION; INTRAABDOMINAL FAT; MALE; MOUSE; MUSCLE ATROPHY; MUSCLE CELL; MUSCLE CONTRACTILITY; MUSCLE DEVELOPMENT; MUSCLE HYPERTROPHY; MYOTUBE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SKELETAL MUSCLE; ADULT; ANIMAL; ATROPHY; CYTOLOGY; FEMALE; GENE EXPRESSION REGULATION; IMMUNOLOGY; METABOLISM; MORBID OBESITY; MOUSE MUTANT; PATHOLOGY; SUBCUTANEOUS FAT;

ADIPOCYTES; ADULT; ANIMALS; ATROPHY; COCULTURE TECHNIQUES; CONTRACTILE PROTEINS; CYTOKINES; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 5; INSULIN-LIKE GROWTH FACTOR II; INTERLEUKIN-10; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTRA-ABDOMINAL FAT; MALE; MICE; MICE, OBESE; MUSCLE FIBERS, SKELETAL; OBESITY, MORBID; SUBCUTANEOUS FAT; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84947330563     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-0796     Document Type: Article

References (48)

1. Cancello R, Tordjman J, Poitou C, et al. Increased infiltration of macro-phages in omental adipose tissue is associated with marked hepatic lesions in morbid human obesity. Diabetes 2006;55:1554-1561
2. Villaret A, Galitzky J, Decaunes P, et al. Adipose tissue endothelial cells from obese human subjects: differences among depots in angiogenic, metabolic, and inflammatory gene expression and cellular senescence. Diabetes 2010;59:2755-2763
3. Jensen MD. Role of body fat distribution and the metabolic complications of obesity. J Clin Endocrinol Metab 2008;93(Suppl. 1):S57-S63
4. Harwood HJ Jr. The adipocyte as an endocrine organ in the regulation of metabolic homeostasis. Neuropharmacology 2012;63:57-75
5. Rytka JM, Wueest S, Schoenle EJ, Konrad D. The portal theory supported by venous drainage-selective fat transplantation. Diabetes 2011;60:56-63
6. Fontana L, Eagon JC, Trujillo ME, Scherer PE, Klein S. Visceral fat adipokine secretion is associated with systemic inflammation in obese humans. Diabetes 2007;56:1010-1013
7. Kewalramani G, Bilan PJ, Klip A. Muscle insulin resistance: assault by lipids, cytokines and local macrophages. Curr Opin Clin Nutr Metab Care 2010;13:382-390
8. Akhmedov D, Berdeaux R. The effects of obesity on skeletal muscle regeneration. Front Physiol 2013;4:371
9. Masgrau A, Mishellany-Dutour A, Murakami H, et al. Time-course changes of muscle protein synthesis associated with obesity-induced lipotoxicity. J Physiol 2012;590:5199-5210
10. Boettcher M, Machann J, Stefan N, et al. Intermuscular adipose tissue (IMAT): association with other adipose tissue compartments and insulin sensitivity. J Magn Reson Imaging 2009;29:1340-1345
11. Thomas EL, Saeed N, Hajnal JV, et al. Magnetic resonance imaging of total body fat. J Appl Physiol (1985) 1998;85:1778-1785
12. Gallagher D, Kelley DE, Yim J-E, et al.; MRI Ancillary Study Group of the Look AHEAD Research Group. Adipose tissue distribution is different in type 2 diabetes. Am J Clin Nutr 2009;89:807-814
13. Goodpaster BH, Krishnaswami S, Harris TB, et al. Obesity, regional body fat distribution, and the metabolic syndrome in older men and women. Arch Intern Med 2005;165:777-783
14. Coen PM, Hames KC, Leachman EM, et al. Reduced skeletal muscle oxi-dative capacity and elevated ceramide but not diacylglycerol content in severe obesity. Obesity (Silver Spring) 2013;21:2362-2371
15. Kemp JG, Blazev R, Stephenson DG, Stephenson GMM. Morphological and biochemical alterations of skeletal muscles from the genetically obese (ob/ob) mouse. Int J Obes (Lond) 2009;33:831-841
16. Denies MS, Johnson J, Maliphol AB, et al. Diet-induced obesity alters skeletal muscle fiber types of male but not female mice. Physiol Rep 2014;2: e00204
17. Borst SE, Conover CF, Bagby GJ. Association of resistin with visceral fat and muscle insulin resistance. Cytokine 2005;32:39-44
18. Vu V, Kim W, Fang X, Liu Y-T, Xu A, Sweeney G. Coculture with primary visceral rat adipocytes from control but not streptozotocin-induced diabetic animals increases glucose uptake in rat skeletal muscle cells: role of adiponectin. Endocrinology 2007;148:4411-4419
19. Dietze D, Koenen M, Röhrig K, Horikoshi H, Hauner H, Eckel J. Impairment of insulin signaling in human skeletal muscle cells by co-culture with human adipocytes. Diabetes 2002;51:2369-2376
20. Kovalik J-P, Slentz D, Stevens RD, et al. Metabolic remodeling of human skeletal myocytes by cocultured adipocytes depends on the lipolytic state of the system. Diabetes 2011;60:1882-1893
21. Glass DJ. PI3 kinase regulation of skeletal muscle hypertrophy and atrophy. Curr Top Microbiol Immunol 2010;346:267-278
22. Pedersen BK, Febbraio MA. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol 2012;8:457-465
23. Whittle AJ, Carobbio S, Martins L, et al. BMP8B increases brown adipose tissue thermogenesis through both central and peripheral actions. Cell 2012;149: 871-885
24. Riehle C, Wende AR, Zaha VG, et al. PGC-1b deficiency accelerates the transition to heart failure in pressure overload hypertrophy. Circ Res 2011;109: 783-793
25. Briguet A, Courdier-Fruh I, Foster M, Meier T, Magyar JP. Histological parameters for the quantitative assessment of muscular dystrophy in the mdx-mouse. Neuromuscul Disord 2004;14:675-682
26. Pellegrinelli V, Rouault C, Veyrie N, Clément K, Lacasa D. Endothelial cells from visceral adipose tissue disrupt adipocyte functions in a three-dimensional setting: partial rescue by angiopoietin-1. Diabetes 2014;63:535-549
27. Pellegrinelli V, Heuvingh J, du Roure O, et al. Human adipocyte function is impacted by mechanical cues. J Pathol 2014;233:183-195
28. Decary S, Mouly V, Hamida CB, Sautet A, Barbet JP, Butler-Browne GS. Replicative potential and telomere length in human skeletal muscle: implications for satellite cell-mediated gene therapy. Hum Gene Ther 1997;8:1429-1438
29. Delaporte C, Dautreaux B, Fardeau M. Human myotube differentiation in vitro in different culture conditions. Biol Cell 1986;57:17-22
30. Rouault C, Pellegrinelli V, Schilch R, et al. Roles of chemokine ligand-2 (CXCL2) and neutrophils in influencing endothelial cell function and inflammation of human adipose tissue. Endocrinology 2013;154:1069-1079
31. Hilton TN, Tuttle LJ, Bohnert KL, Mueller MJ, Sinacore DR. Excessive adipose tissue infiltration in skeletal muscle in individuals with obesity, diabetes mellitus, and peripheral neuropathy: association with performance and function. Phys Ther 2008;88:1336-1344
32. Dalmas E, Rouault C, Abdennour M, et al. Variations in circulating inflammatory factors are related to changes in calorie and carbohydrate intakes early in the course of surgery-induced weight reduction. Am J Clin Nutr 2011;94: 450-458
33. Spranger J, Kroke A, Möhlig M, et al. Inflammatory cytokines and the risk to develop type 2 diabetes: results of the prospective population-based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. Diabetes 2003;52:812-817
34. Stapp JM, Sjoelund V, Lassiter HA, Feldhoff RC, Feldhoff PW. Recombi-nant rat IL-1beta and IL-6 synergistically enhance C3 mRNA levels and complement component C3 secretion by H-35 rat hepatoma cells. Cytokine 2005;30:78-85
35. Ren H, Yin P, Duan C. IGFBP-5 regulates muscle cell differentiation by binding to IGF-II and switching on the IGF-II auto-regulation loop. J Cell Biol 2008; 182:979-991
36. Glass DJ. Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell Biol 2005;37:1974-1984
37. Chau Y-Y, Bandiera R, Serrels A, et al. Visceral and subcutaneous fat have different origins and evidence supports a mesothelial source. Nat Cell Biol 2014; 16:367-375
38. Macotela Y, Emanuelli B, Mori MA, et al. Intrinsic differences in adipo-cyte precursor cells from different white fat depots. Diabetes 2012;61:1691-1699
39. Yu J, Shi L, Wang H, et al. Conditioned medium from hypoxia-treated adipocytes renders muscle cells insulin resistant. Eur J Cell Biol 2011;90: 1000-1015
40. Kern PA, Ranganathan S, Li C, Wood L, Ranganathan G. Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab 2001;280:E745-E751
41. Moschen AR, Molnar C, Enrich B, Geiger S, Ebenbichler CF, Tilg H. Adipose and liver expression of interleukin (IL)-1 family members in morbid obesity and effects of weight loss. Mol Med 2011;17:840-845
42. Buxboim A, Ivanovska IL, Discher DE. Matrix elasticity, cytoskeletal forces and physics of the nucleus: how deeply do cells 'feel' outside and in? J Cell Sci 2010;123:297-308
43. Berkes CA, Tapscott SJ. MyoD and the transcriptional control of myo-genesis. Semin Cell Dev Biol 2005;16:585-595
44. Le Grand F, Rudnicki MA. Skeletal muscle satellite cells and adult myo-genesis. Curr Opin Cell Biol 2007;19:628-633
45. Gautel M. Cytoskeletal protein kinases: titin and its relations in mechano-sensing. Pflugers Arch 2011;462:119-134
46. Cai D, Yuan M, Frantz DF, et al. Local and systemic insulin resistance resulting from hepatic activation of IKK-beta and NF-kappaB. Nat Med 2005;11: 183-190
47. Takegahara Y, Yamanouchi K, Nakamura K, Nakano S, Nishihara M. My-otube formation is affected by adipogenic lineage cells in a cell-to-cell contact-independent manner. Exp Cell Res 2014;324:105-114
48. Stephens FB, Chee C, Wall BT, et al. Lipid induced insulin resistance is associated with an impaired skeletal muscle protein synthetic response to amino acid ingestion in healthy young men. Diabetes. 18 December 2014 [Epub ahead of print]