Continuous cold exposure induces an anti-inflammatory response in mesenteric adipose tissue associated with catecholamine production and thermogenin expression in rats

Batra A, Heimesaat MM, Bereswill S, Fischer A, Glauben R, Kunkel D, Scheff old A, Erben U, Kuhl A, Loddenkemper C, Lehr HA, Schumann M, Schulzke JD, Zeitz M, Siegmund B. Mesenteric fat - control site for bacterial translocation in colitis? Mucosal Immunol 5, 580-591, 2012Bertin B, Desreumaux P, Dubuquoy L. Obesity, visceral fat and Crohn’s disease. Curr Opin Clin Nutr Metab Care 13, 574-580, 2010.10.1038/mi.2012.3322569302Search in Google Scholar

Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev 84, 277-359, 2004.10.1152/physrev.00015.200314715917Search in Google Scholar

Cohen P, Levy JD, Zhang Y, Frontini A, Kolodin DP, Svensson KJ. Ablation of PRDM16 and beige adipose causes metabolic dysfunction and a subcutaneous to visceral fat switch. Cell 156, 304-316, 2014.10.1016/j.cell.2013.12.021392240024439384Search in Google Scholar

Cousin B, Cinti S, Morroni M, Raimbault S, Ricquier D, Penicaud L, Casteilla L. Occurrence of brown adipocytes in rat white adipose tissue: molecular and morphological characterization. J Cell Sci 103 (Pt 4), 931-942, 1992.10.1242/jcs.103.4.9311362571Search in Google Scholar

Enerback S. Th e origins of brown adipose tissue. N Engl J Med 360, 2021-2023, 2009.10.1056/NEJMcibr080961019420373Search in Google Scholar

Harms M, Seale P. Brown and beige fat: development, function and therapeutic potential. Nat Med 19, 1252-1263, 2013.10.1038/nm.336124100998Search in Google Scholar

Kanhai DA, Kappelle LJ, van der Graaf Y, Uiterwaal CS, Visseren FL. SMART Study Group, The risk of general and abdominal adiposity in the occurrence of new vascular events and mortality in patients with various manifestations of vascular disease, Int J Obes 36, 695-702, 2012.10.1038/ijo.2011.11521712810Search in Google Scholar

Khazen W, M’Bika JP, Tomkiewicz C, Benelli C, Chany C, Achour A, Forest C. Expression of macrophage-selective markers in human and rodent adipocytes. FEBS Lett 579, 5631-5634, 2005.10.1016/j.febslet.2005.09.03216213494Search in Google Scholar

Kleiner S, Mepani RJ, Laznik D, Ye L, Jurczak MJ, Jornayvaz FR. Development of insulin resistance in mice lacking PGC-1alpha in adipose tissues. Proc Natl Acad Sci USA 109, 9635-9640, 2012.10.1073/pnas.1207287109338612322645355Search in Google Scholar

Kranendonk ME, van Herwaarden JA, Stupkova T, de Jager W, Vink A, Moll FL, Kalkhoven E, Visseren FL.Inflammatory characteristics of distinct abdominal adipose tissue depots relate differently to metabolic risk factors for cardiovascular disease: distinct fat depots and vascular risk factors. Atherosclerosis 239, 419-427, 2015.10.1016/j.atherosclerosis.2015.01.03525682042Search in Google Scholar

Kvetnansky R, Ukropec J, Laukova M, Manz B, Pacak K, Vargovic P. Stress stimulates production of catecholamines in rat adipocytes. Cell Mol Neurobiol 32, 801-813, 2012.10.1007/s10571-012-9822-6341900922402834Search in Google Scholar

Laukova M, Vargovic P, Krizanova O, Kvetnansky R. Repeated stress down-regulates β(2)- and α (2C)-adrenergic receptors and up-regulates gene expression of IL-6 in the rat spleen. Cell Mol Neurobiol 30, 1077-1087, 2010.10.1007/s10571-010-9540-x20607388Search in Google Scholar

Lee YH, Petkova Anelia P, Mottillo Emilio P, Granneman JG. In vivo identification of bipotential adipocyte progenitors recruited by beta 3-adrenoceptor activation and high-fat feeding. Cell Metab 15, 480-491, 2012.10.1016/j.cmet.2012.03.009332239022482730Search in Google Scholar

Lee YH, Petkova Anelia P, Granneman JG. Identification of an adipogenic niche for adipose tissue remodeling and restoration. Cell Metab 18, 355-367, 2013.10.1016/j.cmet.2013.08.003418530524011071Search in Google Scholar

Lee MW, Odegaard JI, Mukundan L, Qiu Y, Molofsky AB, Nussbaum JC, Yun K, Locksley RM, Chawla A. Activated type 2 innate lymphoid cells regulate beige fat biogenesis. Cell 160, 74-87, 2015.10.1016/j.cell.2014.12.011429751825543153Search in Google Scholar

Lin J, Wu PH, Tarr PT, Lindenberg KS, St-Pierre J, Zhang CY. Defects in adaptive energy metabolism with CNSlinked hyperactivity in PGC-1alpha null mice. Cell 119, 121-135, 2004.10.1016/j.cell.2004.09.01315454086Search in Google Scholar

Liu PS, Lin YW, Burton FH, Wei LN. M1-M2 balancing act in white adipose tissue browning - a new role for RIP140. Adipocyte 4, 146-148, 2015.10.4161/21623945.2014.981428449697426167418Search in Google Scholar

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402-408, 2001.10.1006/meth.2001.126211846609Search in Google Scholar

Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117, 175-184, 2007.10.1172/JCI29881171621017200717Search in Google Scholar

Lumeng CN, DelProposto JB, Westcott DJ, Saltiel AR. Phenotypic switching of adipose tissue macrophages with obesity is generated by spatiotemporal differences in macrophage subtypes. Diabetes 57, 3239-3246, 2008.10.2337/db08-0872258412918829989Search in Google Scholar

Miyazaki Y, Glass L, Triplitt C, Wajcberg E, Mandarino LJ, DeFronzo RA. Abdominal fat distribution and peripheral and hepatic insulin resistance in type 2 diabetes mellitus. Am J Physiol Endocrinol Metab 283, 1135-1143, 2002.10.1152/ajpendo.0327.200112424102Search in Google Scholar

Nicklas BJ, Penninx BW, Cesari M, Kritchevsky SB, Newman AB, Kanaya AM, Pahor M, Jingzhong D, Harris TB. Association of v isceral adipose tissue with incident myocardial infarction in older men and women: the health, aging and body composition study, Am J Epidemiol 160, 741-749, 2004.Search in Google Scholar

Nguyen KD, Qiu Y, Cui X, Goh YP, Mwangi J, David T, Mukundan L, Brombacher F, Locksley RM, Chawla A. Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis. Nature 480, 104-108, 2011.10.1038/nature10653337176122101429Search in Google Scholar

Olefsky JM, Glass CK. Macrophages, inflammation and insulin resistance. Annu Rev Physiol 72, 219-246, 2010.10.1146/annurev-physiol-021909-13584620148674Search in Google Scholar

Qiu Y, Nguyen KD, Odegaard JI, Cui X, Tian X, Locksley RM, Palmiter RD, Chawla A. Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat. Cell 157, 1292-1308, 2014.10.1016/j.cell.2014.03.066412951024906148Search in Google Scholar

Sam S, Haffner S, Davidson MH, D’Agostino RB Sr, Feinstein S, Kondos G, Perez A, Mazzone T. Relation of abdominal fat depots to systemic markers of inflammation in type 2 diabetes. Diabetes Care, 32, 932-937, 2009.10.2337/dc08-1856267113019228869Search in Google Scholar

Seale P, Bjork B, Yang W, Kajimura S, Chin S, Kuang S, Scime A, Devarakonda S, Conroe HM, Erdjument-Bromage H, Tempst P, Rudnicki MA, Beier DR, Spiegelman BM. PRDM16 controls a brown fat/skeletal muscle switch. Nature 454, 961-967, 2008. 10.1038/nature07182258332918719582Search in Google Scholar

Vargovic P, Ukropec J, Laukova M, Cleary S, Manz B, Pacak K, Kvetnansky R. Adipocytes as a new source of catecholamine production. FEBS Lett 585, 2279-2284, 2011.10.1016/j.febslet.2011.06.00121689652Search in Google Scholar

Vargovic P, Ukropec J, Laukova M, Kurdiova T, Balaz M, Manz B, Ukropcova B, Kvetnansky R. Repeated immobilization stress induces catecholamine production in rat mesenteric adipocytes. Stress 16, 340-352, 2013.10.3109/10253890.2012.73604623035889Search in Google Scholar

Vargovic P, Laukova M, Ukropec J, Manz G, Kvetnansky R. Lipopolysaccharide induces catecholamine production in mesenteric adipose tissue of rats previously exposed to immobilization stress. Stress 2016. [Epub ahead of print].10.1080/10253890.2016.120341427314578Search in Google Scholar

Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112, 1796-1808, 2003.10.1172/JCI200319246Search in Google Scholar

Wu J, Bostrom P, Sparks LM, Ye L, Choi JH, Giang AH, Khandekar M, Virtanen KA, Nuutila P, Schaart G, Huang K, Tu H, van Marken Lichtenbelt WD, Hoeks J, Enerback S, Schrauwen P, Spiegelman BM. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150, 366-376, 2012.10.1016/j.cell.2012.05.016Search in Google Scholar

Yang YK, Chen M, Clements RH, Abrams GA, Aprahamian CJ, Harmon CM. Human mesenteric adipose tissue plays unique role versus subcutaneous and omental fat in obesity related diabetes. Cell Physiol Biochem 22, 531-538, 2008.10.1159/000185527Search in Google Scholar

Young P, Wilson S, Arch JR. Prolonged beta-adrenoceptor stimulation increases the amount of GDP-binding protein in brown adipose tissue mitochondria. Life Sci 34, 1111-1117, 1984. 10.1016/0024-3205(84)90081-XSearch in Google Scholar