Expression of inflammation-related genes is associated with adipose tissue location in horses.
Abstract: In humans, adipose tissue (AT) originating from different depots shows varying gene expression profiles. In horses, the risk of certain metabolic disorders may also be influenced by the impact of specific AT depots. Macrophage infiltration in human and rat AT is considered to be a source of inflammatory changes. In horses, this relationship has not been extensively studied yet. Reverse transcription quantitative real-time polymerase chain reaction (RT-qPCR), a useful method to evaluate differences in mRNA expression across different tissues, can be used to evaluate differences between equine AT depots. For a correct interpretation of the RT-qPCR results, expression data have to be normalized by the use of validated reference genes. The main objectives of this study were to compare mRNA expression of inflammation-related genes, as well as adipocyte morphology and number between different equine AT depots; and in addition, to investigate the presence of antigen presenting cells in equine AT and any potential relationship with adipokine mRNA expression. Results: In this study, the mRNA expression of inflammation-related genes (leptin, chemokine ligand 5, interleukin 1β, interleukin 6, interleukin 10, adiponectin, matrix metalloproteinase 2, and superoxide dismutase 2) and candidate reference gene stability was investigated in 8 different AT depots collected from the nuchal, abdominal (mesenteric, retroperitoneal, and peri-renal) and subcutaneous (tail head and loin) AT region. By using GeNorm analysis, HPRT1, RPL32, and GAPDH were found to be the most stable genes in equine AT. The mRNA expression of leptin, chemokine ligand 5, interleukin 10, interleukin 1β, adiponectin, and matrix metalloproteinase 2 significantly differed across AT depots (P 0.05). Adipocyte area and number of antigen presenting cells per adipocyte significantly differed between AT depots (P < 0.05). Conclusions: Adipose tissue location was associated with differences in mRNA expression of inflammation-related genes. This depot-specific difference in mRNA expression suggests that the overall inflammatory status of horses could be partially determined by the relative proportion of the different AT depots.
Publication Date: 2013-12-02 PubMed ID: 24295090PubMed Central: PMC4220830DOI: 10.1186/1746-6148-9-240Google Scholar: Lookup
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- Journal Article
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Summary
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The research examines the variation in the expression of inflammation-related genes linked to adipose (fat) tissue location in horses. The study provides insights into how different fat deposits contribute to overall inflammatory status and potentially influence the risk of metabolic disorders in horses.
Objective of the Research
- The aim of the study was to compare the mRNA expression of inflammation-related genes, as well as examine the morphology and number of adipocytes (fat cells) across different adipose tissue depots in horses.
- The research also sought to investigate the presence of antigen presenting cells in horse fat deposits, and any correlation with adipokine mRNA expression.
Methodology and Materials
- Eight different adipose tissue depots including nuchal, abdominal (mesenteric, retroperitoneal, peri-renal), and subcutaneous (tail head and loin) were studied.
- Reverse transcription quantitative real-time polymerase chain reaction (RT-qPCR) was used to evaluate the differences in mRNA expression of inflammation-related genes across these tissues.
- To ensure accurate interpretation of the RT-qPCR results, the expression data was normalized using validated reference genes. Through GeNorm analysis, HPRT1, RPL32, and GAPDH were identified as the most stable genes in equine adipose tissue.
Results of the Study
- The mRNA expression of inflammation-related genes including leptin, chemokine ligand 5, interleukin 1β, interleukin 6, interleukin 10, adiponectin, matrix metalloproteinase 2, and superoxide dismutase 2 was investigated.
- Significant variance was found in the expression of leptin, chemokine ligand 5, interleukin 10, interleukin 1β, adiponectin, and matrix metalloproteinase 2 across the different adipose tissue depots. However, no significant variances were found for interleukin 6 and superoxide dismutase 2.
- The study also found significant differences in adipocyte area and number of antigen presenting cells per adipocyte across the different adipose tissue depots.
Conclusions of the Study
- The location of adipose tissue was associated with differences in mRNA expression of inflammation-related genes in horses. These depots-specific differences suggest that the overall inflammatory status of horses could be partially determined by the relative proportion of the different fat depots.
Cite This Article
APA
Bruynsteen L, Erkens T, Peelman LJ, Ducatelle R, Janssens GP, Harris PA, Hesta M.
(2013).
Expression of inflammation-related genes is associated with adipose tissue location in horses.
BMC Vet Res, 9, 240.
https://doi.org/10.1186/1746-6148-9-240 Publication
Researcher Affiliations
- Department of Nutrition, Genetics and Ethology, Faculty of Veterinary Medicine, Ghent University, Heidestraat 19, Merelbeke 9820, Belgium. lien.bruynsteen@ugent.be.
MeSH Terms
- Adipocytes / metabolism
- Adipose Tissue / metabolism
- Animals
- Gene Expression Regulation
- Horse Diseases / genetics
- Horse Diseases / metabolism
- Horses / genetics
- Horses / metabolism
- Inflammation / genetics
- Inflammation / metabolism
- Inflammation / veterinary
- Male
- Reverse Transcriptase Polymerase Chain Reaction / veterinary
- Transcriptome / genetics
References
This article includes 68 references
- Hahn P, Novak M. Development of brown and white adipose tissue.. J Lipid Res 1975 Mar;16(2):79-91.
- Fantuzzi G. Adipose tissue, adipokines, and inflammation.. J Allergy Clin Immunol 2005 May;115(5):911-9; quiz 920.
- Kershaw EE, Flier JS. Adipose tissue as an endocrine organ.. J Clin Endocrinol Metab 2004 Jun;89(6):2548-56.
- Maury E, Brichard SM. Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome.. Mol Cell Endocrinol 2010 Jan 15;314(1):1-16.
- Radin MJ, Sharkey LC, Holycross BJ. Adipokines: a review of biological and analytical principles and an update in dogs, cats, and horses.. Vet Clin Pathol 2009 Jun;38(2):136-56.
- Antuna-Puente B, Feve B, Fellahi S, Bastard JP. Adipokines: the missing link between insulin resistance and obesity.. Diabetes Metab 2008 Feb;34(1):2-11.
- Juge-Aubry CE, Henrichot E, Meier CA. Adipose tissue: a regulator of inflammation.. Best Pract Res Clin Endocrinol Metab 2005 Dec;19(4):547-66.
- Demeulemeester D, Collen D, Lijnen HR. Effect of matrix metalloproteinase inhibition on adipose tissue development.. Biochem Biophys Res Commun 2005 Apr 1;329(1):105-10.
- Halberg N, Wernstedt-Asterholm I, Scherer PE. The adipocyte as an endocrine cell.. Endocrinol Metab Clin North Am 2008 Sep;37(3):753-68, x-xi.
- Lijnen HR, Maquoi E, Hansen LB, Van Hoef B, Frederix L, Collen D. Matrix metalloproteinase inhibition impairs adipose tissue development in mice.. Arterioscler Thromb Vasc Biol 2002 Mar 1;22(3):374-9.
- Chavey C, Mari B, Monthouel MN, Bonnafous S, Anglard P, Van Obberghen E, Tartare-Deckert S. Matrix metalloproteinases are differentially expressed in adipose tissue during obesity and modulate adipocyte differentiation.. J Biol Chem 2003 Apr 4;278(14):11888-96.
- Fain JN, Madan AK, Hiler ML, Cheema P, Bahouth SW. Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans.. Endocrinology 2004 May;145(5):2273-82.
- Cinti S, Mitchell G, Barbatelli G, Murano I, Ceresi E, Faloia E, Wang S, Fortier M, Greenberg AS, Obin MS. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans.. J Lipid Res 2005 Nov;46(11):2347-55.
- Vick MM, Adams AA, Murphy BA, Sessions DR, Horohov DW, Cook RF, Shelton BJ, Fitzgerald BP. Relationships among inflammatory cytokines, obesity, and insulin sensitivity in the horse.. J Anim Sci 2007 May;85(5):1144-55.
- Vick MM, Murphy BA, Sessions DR, Reedy SE, Kennedy EL, Horohov DW, Cook RF, Fitzgerald BP. Effects of systemic inflammation on insulin sensitivity in horses and inflammatory cytokine expression in adipose tissue.. Am J Vet Res 2008 Jan;69(1):130-9.
- Adams AA, Katepalli MP, Kohler K, Reedy SE, Stilz JP, Vick MM, Fitzgerald BP, Lawrence LM, Horohov DW. Effect of body condition, body weight and adiposity on inflammatory cytokine responses in old horses.. Vet Immunol Immunopathol 2009 Feb 15;127(3-4):286-94.
- Murano I, Barbatelli G, Parisani V, Latini C, Muzzonigro G, Castellucci M, Cinti S. Dead adipocytes, detected as crown-like structures, are prevalent in visceral fat depots of genetically obese mice.. J Lipid Res 2008 Jul;49(7):1562-8.
- Van Harmelen V, Reynisdottir S, Eriksson P, Thörne A, Hoffstedt J, Lönnqvist F, Arner P. Leptin secretion from subcutaneous and visceral adipose tissue in women.. Diabetes 1998 Jun;47(6):913-7.
- Yang SH, Matsui T, Kawachi H, Yamada T, Nakanishi N, Yano H. Fat depot-specific differences in leptin mRNA expression and its relation to adicyte size in steers.. Anim Sci J 2008;74:17–21.
- Després JP, Lemieux I. Abdominal obesity and metabolic syndrome.. Nature 2006 Dec 14;444(7121):881-7.
- Waller AP, Kohler K, Burns TA, Mudge MC, Belknap JK, Lacombe VA. Naturally occurring compensated insulin resistance selectively alters glucose transporters in visceral and subcutaneous adipose tissues without change in AS160 activation.. Biochim Biophys Acta 2011 Sep;1812(9):1098-103.
- Carter RA, Treiber KH, Geor RJ, Douglass L, Harris PA. Prediction of incipient pasture-associated laminitis from hyperinsulinaemia, hyperleptinaemia and generalised and localised obesity in a cohort of ponies.. Equine Vet J 2009 Feb;41(2):171-8.
- Frank N, Geor RJ, Bailey SR, Durham AE, Johnson PJ. Equine metabolic syndrome.. J Vet Intern Med 2010 May-Jun;24(3):467-75.
- Burns TA, Geor RJ, Mudge MC, McCutcheon LJ, Hinchcliff KW, Belknap JK. Proinflammatory cytokine and chemokine gene expression profiles in subcutaneous and visceral adipose tissue depots of insulin-resistant and insulin-sensitive light breed horses.. J Vet Intern Med 2010 Jul-Aug;24(4):932-9.
- Bustin SA, Benes V, Nolan T, Pfaffl MW. Quantitative real-time RT-PCR--a perspective.. J Mol Endocrinol 2005 Jun;34(3):597-601.
- Gorzelniak K, Janke J, Engeli S, Sharma AM. Validation of endogenous controls for gene expression studies in human adipocytes and preadipocytes.. Horm Metab Res 2001 Oct;33(10):625-7.
- Bustin SA. Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): trends and problems.. J Mol Endocrinol 2002 Aug;29(1):23-39.
- Fleige S, Pfaffl MW. RNA integrity and the effect on the real-time qRT-PCR performance.. Mol Aspects Med 2006 Apr-Jun;27(2-3):126-39.
- Thellin O, Zorzi W, Lakaye B, De Borman B, Coumans B, Hennen G, Grisar T, Igout A, Heinen E. Housekeeping genes as internal standards: use and limits.. J Biotechnol 1999 Oct 8;75(2-3):291-5.
- Mehta R, Birerdinc A, Hossain N, Afendy A, Chandhoke V, Younossi Z, Baranova A. Validation of endogenous reference genes for qRT-PCR analysis of human visceral adipose samples.. BMC Mol Biol 2010 May 21;11:39.
- Erkens T, Van Poucke M, Vandesompele J, Goossens K, Van Zeveren A, Peelman LJ. Development of a new set of reference genes for normalization of real-time RT-PCR data of porcine backfat and longissimus dorsi muscle, and evaluation with PPARGC1A.. BMC Biotechnol 2006 Oct 9;6:41.
- Van Weyenberg S, Hesta M, Buyse J, Janssens GP. The effect of weight loss by energy restriction on metabolic profile and glucose tolerance in ponies.. J Anim Physiol Anim Nutr (Berl) 2008 Oct;92(5):538-45.
- Liburt NR, Fugaro MN, Wunderlich EK, Zambito JL, Horhov DW, Betancourt A, Boston RC, McKeever KH, Geor RJ. The effect of exercise training on insulin sensitivity and fat and muscle tissue cytokine profiles of old and young Standardbred mares [abstract]. J Equine Vet Sci 2011;31:237–238.
- Fried SK, Bunkin DA, Greenberg AS. Omental and subcutaneous adipose tissues of obese subjects release interleukin-6: depot difference and regulation by glucocorticoid.. J Clin Endocrinol Metab 1998 Mar;83(3):847-50.
- Park HS, Park JY, Yu R. Relationship of obesity and visceral adiposity with serum concentrations of CRP, TNF-alpha and IL-6.. Diabetes Res Clin Pract 2005 Jul;69(1):29-35.
- Tilg H, Moschen AR. Role of adiponectin and PBEF/visfatin as regulators of inflammation: involvement in obesity-associated diseases.. Clin Sci (Lond) 2008 Feb;114(4):275-88.
- Bruun JM, Lihn AS, Verdich C, Pedersen SB, Toubro S, Astrup A, Richelsen B. Regulation of adiponectin by adipose tissue-derived cytokines: in vivo and in vitro investigations in humans.. Am J Physiol Endocrinol Metab 2003 Sep;285(3):E527-33.
- Thalmann S, Meier CA. Local adipose tissue depots as cardiovascular risk factors.. Cardiovasc Res 2007 Sep 1;75(4):690-701.
- Overbergh L, Giulietti A, Valckx D, Decallonne R, Bouillon R, Mathieu C. The use of real-time reverse transcriptase PCR for the quantification of cytokine gene expression.. J Biomol Tech 2003 Mar;14(1):33-43.
- Maquoi E, Munaut C, Colige A, Collen D, Lijnen HR. Modulation of adipose tissue expression of murine matrix metalloproteinases and their tissue inhibitors with obesity.. Diabetes 2002 Apr;51(4):1093-101.
- Croissandeau G, Chrétien M, Mbikay M. Involvement of matrix metalloproteinases in the adipose conversion of 3T3-L1 preadipocytes.. Biochem J 2002 Jun 15;364(Pt 3):739-46.
- O'Connell J, Lynch L, Cawood TJ, Kwasnik A, Nolan N, Geoghegan J, McCormick A, O'Farrelly C, O'Shea D. The relationship of omental and subcutaneous adipocyte size to metabolic disease in severe obesity.. PLoS One 2010 Apr 1;5(4):e9997.
- Kabir M, Stefanovski D, Hsu IR, Iyer M, Woolcott OO, Zheng D, Catalano KJ, Chiu JD, Kim SP, Harrison LN, Ionut V, Lottati M, Bergman RN, Richey JM. Large size cells in the visceral adipose depot predict insulin resistance in the canine model.. Obesity (Silver Spring) 2011 Nov;19(11):2121-9.
- Van de Velde H, Janssens GP, de Rooster H, Polis I, Peters I, Ducatelle R, Nguyen P, Buyse J, Rochus K, Xu J, Verbrugghe A, Hesta M. The cat as a model for human obesity: insights into depot-specific inflammation associated with feline obesity.. Br J Nutr 2013 Oct;110(7):1326-35.
- Skurk T, Alberti-Huber C, Herder C, Hauner H. Relationship between adipocyte size and adipokine expression and secretion.. J Clin Endocrinol Metab 2007 Mar;92(3):1023-33.
- Huber J, Kiefer FW, Zeyda M, Ludvik B, Silberhumer GR, Prager G, Zlabinger GJ, Stulnig TM. CC chemokine and CC chemokine receptor profiles in visceral and subcutaneous adipose tissue are altered in human obesity.. J Clin Endocrinol Metab 2008 Aug;93(8):3215-21.
- Drolet R, Bélanger C, Fortier M, Huot C, Mailloux J, Légaré D, Tchernof A. Fat depot-specific impact of visceral obesity on adipocyte adiponectin release in women.. Obesity (Silver Spring) 2009 Mar;17(3):424-30.
- Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue.. J Clin Invest 2003 Dec;112(12):1796-808.
- Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, Sole J, Nichols A, Ross JS, Tartaglia LA, Chen H. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance.. J Clin Invest 2003 Dec;112(12):1821-30.
- Ting JP, Trowsdale J. Genetic control of MHC class II expression.. Cell 2002 Apr;109 Suppl:S21-33.
- Al-Daccak R, Mooney N, Charron D. MHC class II signaling in antigen-presenting cells.. Curr Opin Immunol 2004 Feb;16(1):108-13.
- Roth SM, Ferrell RE, Peters DG, Metter EJ, Hurley BF, Rogers MA. Influence of age, sex, and strength training on human muscle gene expression determined by microarray.. Physiol Genomics 2002 Sep 3;10(3):181-90.
- Moreaux S, Nichols J, Bowman J, Hatfield P. Psyllium lowers blood glucose and insulin concentrations in horses.. J Equine Vet Sci 2011;31:160–165.
- McManus CJ, Fitzgerald BP. Effects of a single day of feed restriction on changes in serum leptin, gonadotropins, prolactin, and metabolites in aged and young mares.. Domest Anim Endocrinol 2000 Jul;19(1):1-13.
- Gabrielsson BG, Olofsson LE, Sjögren A, Jernås M, Elander A, Lönn M, Rudemo M, Carlsson LM. Evaluation of reference genes for studies of gene expression in human adipose tissue.. Obes Res 2005 Apr;13(4):649-52.
- Hurtado del Pozo C, Calvo RM, Vesperinas-García G, Gómez-Ambrosi J, Frühbeck G, Corripio-Sánchez R, Rubio MA, Obregon MJ. IPO8 and FBXL10: new reference genes for gene expression studies in human adipose tissue.. Obesity (Silver Spring) 2010 May;18(5):897-903.
- Ferguson BS, Nam H, Hopkins RG, Morrison RF. Impact of reference gene selection for target gene normalization on experimental outcome using real-time qRT-PCR in adipocytes.. PLoS One 2010 Dec 13;5(12):e15208.
- Hosseini A, Sauerwein H, Mielenz M. Putative reference genes for gene expression studies in propionate and β-hydroxybutyrate treated bovine adipose tissue explants.. J Anim Physiol Anim Nutr (Berl) 2010 Oct;94(5):e178-84.
- Bogaert L, Van Poucke M, De Baere C, Peelman L, Gasthuys F, Martens A. Selection of a set of reliable reference genes for quantitative real-time PCR in normal equine skin and in equine sarcoids.. BMC Biotechnol 2006 Apr 27;6:24.
- Smits K, Goossens K, Van Soom A, Govaere J, Hoogewijs M, Vanhaesebrouck E, Galli C, Colleoni S, Vandesompele J, Peelman L. Selection of reference genes for quantitative real-time PCR in equine in vivo and fresh and frozen-thawed in vitro blastocysts.. BMC Res Notes 2009 Dec 11;2:246.
- Cappelli K, Felicetti M, Capomaccio S, Spinsanti G, Silvestrelli M, Supplizi AV. Exercise induced stress in horses: selection of the most stable reference genes for quantitative RT-PCR normalization.. BMC Mol Biol 2008 May 19;9:49.
- Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.. Genome Biol 2002 Jun 18;3(7):RESEARCH0034.
- Figueiredo MD, Salter CE, Andrietti AL, Vandenplas ML, Hurley DJ, Moore JN. Validation of a reliable set of primer pairs for measuring gene expression by real-time quantitative RT-PCR in equine leukocytes.. Vet Immunol Immunopathol 2009 Sep 15;131(1-2):65-72.
- Loftus JP, Belknap JK, Black SJ. Matrix metalloproteinase-9 in laminae of black walnut extract treated horses correlates with neutrophil abundance.. Vet Immunol Immunopathol 2006 Oct 15;113(3-4):267-76.
- Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers.. Methods Mol Biol 2000;132:365-86.
- Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool.. J Mol Biol 1990 Oct 5;215(3):403-10.
- Zuker M. Mfold web server for nucleic acid folding and hybridization prediction.. Nucleic Acids Res 2003 Jul 1;31(13):3406-15.
- Aloisi F. Immune function of microglia.. Glia 2001 Nov;36(2):165-79.
Citations
This article has been cited 8 times.- Stefaniuk-Szmukier M, Piórkowska K, Ropka-Molik K. Equine Metabolic Syndrome: A Complex Disease Influenced by Multifactorial Genetic Factors.. Genes (Basel) 2023 Jul 27;14(8).
- Blaue D, Schedlbauer C, Starzonek J, Gittel C, Brehm W, Blüher M, Pfeffer M, Vervuert I. The influence of equine body weight gain on inflammatory cytokine expressions of adipose tissue in response to endotoxin challenge.. Acta Vet Scand 2020 Apr 22;62(1):17.
- Adolph S, Schedlbauer C, Blaue D, Schöniger A, Gittel C, Brehm W, Fuhrmann H, Vervuert I. Lipid classes in adipose tissues and liver differ between Shetland ponies and Warmblood horses.. PLoS One 2019;14(3):e0207568.
- Durham AE, Frank N, McGowan CM, Menzies-Gow NJ, Roelfsema E, Vervuert I, Feige K, Fey K. ECEIM consensus statement on equine metabolic syndrome.. J Vet Intern Med 2019 Mar;33(2):335-349.
- Morrison PK, Harris PA, Maltin CA, Grove-White D, Argo CM. EQUIFAT: A novel scoring system for the semi-quantitative evaluation of regional adipose tissues in Equidae.. PLoS One 2017;12(3):e0173753.
- Selim S, Elo K, Jaakkola S, Karikoski N, Boston R, Reilas T, Särkijärvi S, Saastamoinen M, Kokkonen T. Relationships among Body Condition, Insulin Resistance and Subcutaneous Adipose Tissue Gene Expression during the Grazing Season in Mares.. PLoS One 2015;10(5):e0125968.
- Giles SL, Nicol CJ, Rands SA, Harris PA. Assessing the seasonal prevalence and risk factors for nuchal crest adiposity in domestic horses and ponies using the Cresty Neck Score.. BMC Vet Res 2015 Jan 31;11:13.
- Morrison PK, Bing C, Harris PA, Maltin CA, Grove-White D, Argo CM. Preliminary investigation into a potential role for myostatin and its receptor (ActRIIB) in lean and obese horses and ponies.. PLoS One 2014;9(11):e112621.
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