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Methyl-β-cyclodextrin alters adipokine gene expression and glucose metabolism in swine adipose tissue*

Published online by Cambridge University Press:  19 July 2013

T. G. Ramsay ,
L. Blomberg  and
T. J. Caperna
T. G. Ramsay*
Affiliation:
Animal Biosciences and Biotechnology Laboratory, Animal and Natural Resources Institute, USDA/ARS, Beltsville Agricultural Research Center, USDA, Beltsville MD 20705, USA
L. Blomberg
Affiliation:
Animal Biosciences and Biotechnology Laboratory, Animal and Natural Resources Institute, USDA/ARS, Beltsville Agricultural Research Center, USDA, Beltsville MD 20705, USA
T. J. Caperna
Affiliation:
Animal Biosciences and Biotechnology Laboratory, Animal and Natural Resources Institute, USDA/ARS, Beltsville Agricultural Research Center, USDA, Beltsville MD 20705, USA
*
†E-mail: [email protected]
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Abstract

This study was designed to determine whether methyl-β-cyclodextrin (MCD) can substitute for albumin in incubation medium for neonatal swine adipose tissue explants, or whether MCD affects metabolism and cytokine expression. Subcutaneous adipose tissue explants (100 ± 10 mg) were prepared from 21-day-old pigs. Explants were incubated in medium 199 supplemented with 25 mM HEPES, 1.0 nM insulin at 37°C. The medium also contained bovine serum albumin (BSA) or MCD at 0%, 0.05%, 0.1%, 0.2% or 0.3%. Tissue explants were treated with these media for 1 h and then switched to the same basal incubation medium containing 0.05% BSA. Explants were removed from basal medium at 2 or 8 h of incubation, and real-time PCR was performed to assess expression of tumor necrosis α (TNF) and interleukin 6 (IL6), acetyl CoA carboxylase (ACAC) and fatty acid synthase (FASN). Alternatively, rates of 14C-glucose oxidation and lipogenesis were monitored ± insulin (100 nM), following MCD treatment. Incubation with BSA had minimal effects on gene expression or adipose tissue metabolism, only producing a doubling in TNF mRNA abundance (P < 0.01). Treatment with MCD increased TNF mRNA abundance by eightfold (P < 0.009), whereas IL6 gene expression increased a 100-fold (P < 0.001) with a suppression in ACAC and FASN expression (P < 0.01). This was paralleled by MCD inhibition of insulin-stimulated glucose oxidation and lipogenesis (P < 0.001). Addition of a TNF antibody to the incubation medium alleviated this inhibition of insulin-stimulated glucose metabolism by ∼30% (P < 0.05).

Keywords

adipose tissuecyclodextrintumor necrosis factorlipogenesis
Type
Physiology and functional biology of systems
Information
animal , Volume 7 , Issue 10 , October 2013 , pp. 1690 - 1696
Copyright
Copyright © The Animal Consortium. This is a work of the U.S. Government and is not subject to copyright protection in the United States. 2013 

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Footnotes

*

Mention of trade name, proprietary product or vendor does not constitute a guarantee or warranty of the product by the U.S. Department of Agriculture or imply its approval to the exclusion of other products or vendors that also may be suitable.

References

Ajuwon, KM, Spurlock, ME 2005. Adiponectin inhibits LPS-induced NF-kappaB activation and IL-6 production and increases PPARgamma2 expression in adipocytes. American Journal of Physiology 288, R1220–R1225.Google Scholar
Azain, MJ, Martin, RJ 1983. Effect of genetic obesity on the regulation of hepatic fatty acid metabolism. American Journal of Physiology 244, R400–R406.Google ScholarPubMed
Breen, MR, Camps, M, Carvalho-Simoes, F, Zorzano, A, Pilch, PF 2012. Cholesterol depletion in adipocytes causes caveolae collapse concomitant with proteosomal degradation of cavin-2 in a switch-like fashion. PLoS One 7, e34516.Google Scholar
Cawthorn, WP, Sethi, JK 2008. TNF-alpha and adipocyte biology. FEBS Letters 582, 117–131.Google Scholar
DeCingolani, CE 1972. Glucose metabolism by isolated fat cells from diabetic rats. Archives Internationale de Physiologie et de Biochimie 80, 269–274.Google Scholar
Doerrler, W, Feingold, KR, Grunfeld, C 1994. Cytokines induce catabolic effects in cultured adipocytes by multiple mechanisms. Cytokine 6, 478–484.CrossRefGoogle ScholarPubMed
Fasshauer, M, Klein, J, Lossner, U, Paschke, R 2003. Interleukin (IL)-6 mRNA expression is stimulated by insulin, isoproterenol, tumour necrosis factor alpha, growth hormone, and IL-6 in 3T3-L1 adipocytes. Hormone and Metabolic Research 35, 147–152.Google Scholar
Hausman, GJ, Poulos, SP, Richardson, RL, Barb, CR, Andacht, T, Kirk, HC, Mynatt, RL 2006. Secreted proteins and genes in fetal and neonatal pig adipose tissue and stromal-vascular cells. Journal of Animal Science 84, 1666–1681.Google Scholar
Jacobi, SK, Ajuwon, KM, Weber, TE, Kuske, JL, Dyer, CJ, Spurlock, ME 2004. Cloning and expression of porcine adiponectin, and its relationship to adiposity, lipogenesis and the acute phase response. Journal of Endocrinology 182, 133–144.Google Scholar
Karlsson, M, Thorn, H, Danielsson, A, Stenkula, KG, Ost, A, Gustavsson, J, Nystrom, FH, Strålfors, P 2004. Colocalization of insulin receptor and insulin receptor substrate-1 to caveolae in primary human adipocytes. Cholesterol depletion blocks insulin signalling for metabolic and mitogenic control. European Journal of Biochemistry 271, 2471–2479.Google Scholar
Kato, L, Szejtli, J, Szente, L 1993. Water soluble complex of palmitic acid in media for cultivation of leprosy-derived psychrophilic mycobacteria from Mycobacterium leprae infected tissues. Acta Microbiolica Hungarica 40, 47–58.Google ScholarPubMed
Kato, L, Szejtli, J, Szente, L 1994. Water soluble complexes of C14 and C16 fatty acids and alcohols in media for cultivation of leprosy-derived psychrophilic mycobacteria. International Journal of Leprosy and Other Mycobacterial Diseases 62, 75–88.Google Scholar
Lagathu, C, Bastard, JP, Auclair, M, Maachi, M, Capeau, J, Caron, M 2003. Chronic interleukin-6 (IL-6) treatment increased IL-6 secretion and induced insulin resistance in adipocyte: prevention by rosiglitazone. Biochemical and Biophysical Research Communications 311, 372–379.Google Scholar
Le Lay, S, Krief, S, Farnier, C, Lefrère, I, Le Liepvre, X, Bazin, R, Ferré, P, Dugail, I 2001. Cholesterol, a cell size-dependent signal that regulates glucose metabolism and gene expression in adipocytes. Journal of Biological Chemistry 276, 16904–16910.Google Scholar
Lenhard, JM 2011. Lipogenic enzymes as therapeutic targets for obesity and diabetes. Current Pharmaceutical Design 17, 325–331.Google Scholar
Livak, KJ, Schmittgen, TD 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–408.CrossRefGoogle ScholarPubMed
Pape, ME, Kim, KH 1988. Effect of tumor necrosis factor on acetyl-coenzyme A carboxylase gene expression and preadipocyte differentiation. Molecular Endocrinology 2, 395–403.Google Scholar
Parpal, S, Karlsson, M, Thorn, H, Strålfors, P 2001. Cholesterol depletion disrupts caveolae and insulin receptor signaling for metabolic control via insulin receptor substrate-1, but not for mitogen-activated protein kinase control. Journal of Biological Chemistry 276, 9670–9678.CrossRefGoogle Scholar
Ramsay, TG 2003. Porcine leptin inhibits lipogenesis in porcine adipocytes. Journal of Animal Science 81, 3008–3017.Google Scholar
Ramsay, TG, Richards, MP 2004. Hormonal regulation of leptin and leptin receptor expression in porcine subcutaneous adipose tissue. Journal of Animal Science 82, 3486–3492.Google Scholar
Ramsay, TG, Azain, MJ 2007. Comparison of gene expression in lean contemporary and crossbred obese swine. Adipocytes 2, 133–142.Google Scholar
Ramsay, TG, Caperna, TJ 2009. Ontogeny of adipokine expression in neonatal pig adipose tissue. Comparative Biochemistry and Physiology Part B 152, 72–78.Google Scholar
Ramsay, TG, Stoll, MJ, Caperna, TJ 2010. Adipokine gene transcription level in adipose tissue of runt piglets. Comparative Biochemistry and Physiology Part B 155, 97–105.Google Scholar
Rasouli, N, Kern, PA 2008. Adipocytokines and the metabolic complications of obesity. Journal of Clinical Endocrinology and Metabolism 93 (suppl. 1), S64–S73.CrossRefGoogle ScholarPubMed
Ruan, H, Zarnowski, MJ, Cushman, SW, Lodish, HF 2003. Standard isolation of primary adipose cells from mouse epididymal fat pads induces inflammatory mediators and down-regulates adipocyte genes. Journal of Biological Chemistry 278, 47585–47593.Google Scholar
Schlesinger, JB, van Harmelen, V, Alberti-Huber, CE, Hauner, H 2006. Albumin inhibits adipogenesis and stimulates cytokine release from human adipocytes. American Journal of Physiology 291, C27–C33.Google Scholar
Starkie, R, Ostrowski, SR, Jauffred, S, Febbraio, M, Pedersen, BK 2003. Exercise and IL-6 infusion inhibit endotoxin-induced TNF-alpha production in humans. FASEB Journal 17, 884–886.Google Scholar
Thorn, H, Stenkula, KG, Karlsson, M, Ortegren, U, Nystrom, FH, Gustavsson, J, Stralfors, P 2003. Cell surface orifices of caveolae and localization of caveolin to the necks of caveolae in adipocytes. Molecular Biology of the Cell 14, 3967–3976.CrossRefGoogle Scholar
Winer, J, Jung, CK, Shackel, I, Williams, PM 1999. Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Analytical Biochemistry 270, 41–49.Google Scholar
Wray-Cahen, D, Caperna, TJ, Steele, NC 2001. Methyl-β-cyclodextrin: an alternative carrier for intravenous infusion of palmitate during tracer studies in swine (Sus scrofa domestica). Comparative Biochemistry and Physiology Part A 130, 55–65.Google Scholar