Cold-Induced browning dynamically alters the expression profiles of inflammatory adipokines with tissue specificity in mice

International Journal of Molecular Sciences

Volumn 17, Issue 5, 2016, Pages

  Luo, Xiao ^a,b   Jia, Ru ^a,b   Zhang, Qiangling ^a,b   Sun, Bo ^a,b   Yan, Jianqun ^a,b  

^a MEDICAL SCHOOL OF XI AN JIAOTONG UNIVERSITY   (China)

^b XI'AN JIAOTONG UNIVERSITY   (China)

Author keywords

Beige cells; Cold exposure; Depot specificity; Inflammatory adipokines; 3 adrenoceptor agonist

Indexed keywords

ADIPOCYTOKINE; ADIPONECTIN; LEPTIN; 1,3 DIOXOLANE DERIVATIVE; BETA 3 ADRENERGIC RECEPTOR STIMULATING AGENT; DISODIUM (R,R)-5-(2-((2-(3-CHLOROPHENYL)-2-HYDROXYETHYL)-AMINO)PROPYL)-1,3-BENZODIOXOLE-2,3-DICARBOXYLATE;

ADIPOCYTE; ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; COLD EXPOSURE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FAMILIAL COLD AUTOINFLAMMATORY SYNDROME; MALE; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION; RNA EXTRACTION; WESTERN BLOTTING; WHITE ADIPOSE TISSUE; ANIMAL; ANTIBODY SPECIFICITY; BROWN ADIPOCYTE; C57BL MOUSE; CELL CULTURE; COLD; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; WHITE ADIPOCYTE;

ADIPOCYTES, BROWN; ADIPOCYTES, WHITE; ADIPOKINES; ADIPOSE TISSUE, BROWN; ADRENERGIC BETA-3 RECEPTOR AGONISTS; ANIMALS; CELLS, CULTURED; COLD TEMPERATURE; DIOXOLES; GENE EXPRESSION REGULATION; MALE; MICE; MICE, INBRED C57BL; ORGAN SPECIFICITY; STRESS, PHYSIOLOGICAL;

EID: 84969592603     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17050795     Document Type: Article

References (51)

1. Cook, K.S.; Min, H.Y.; Johnson, D.; Chaplinsky, R.J.; Flier, J.S.; Hunt, C.R.; Spiegelman, B.M. Adipsin: A circulating serine protease homolog secreted by adipose tissue and sciatic nerve. Science 1987, 237, 402-405. [CrossRef] [PubMed]
2. Flier, J.S.; Cook, K.S.; Usher, P.; Spiegelman, B.M. Severely impaired adipsin expression in genetic and acquired obesity. Science 1987, 237, 405-408. [CrossRef] [PubMed]
3. Kershaw, E.E.; Flier, J.S. Adipose tissue as an endocrine organ. J. Clin. Endocrinol. Metab. 2004, 89, 2548-2556. [CrossRef] [PubMed]
4. Rodríguez, A.; Becerril, S.; Ezquerro, S.; Méndez-Giménez, L.; Frühbeck, G. Cross-talk between adipokines and myokines in fat browning. Acta Physiol. 2016. [CrossRef] [PubMed]
5. Wood, I.S.; de Heredia, F.P.; Wang, B.; Trayhurn, P. Cellular hypoxia and adipose tissue dysfunction in obesity. Proc. Nutr. Soc. 2009, 68, 370-377. [CrossRef] [PubMed]
6. Wellen, K.E.; Hotamisligil, G.S. Inflammation, stress, and diabetes. J. Clin. Investig. 2005, 115, 1111-1119. [CrossRef] [PubMed]
7. Cannon, B.; Nedergaard, J. Brown adipose tissue: Function and physiological significance. Physiol. Rev. 2004, 84, 277-359. [CrossRef] [PubMed]
8. Cinti, S. Adipocyte differentiation and transdifferentiation: Plasticity of the adipose organ. J. Endocrinol. Investig. 2002, 25, 823-835. [CrossRef] [PubMed]
9. Xue, B.; Coulter, A.; Rim, J.S.; Koza, R.A.; Kozak, L.P. Transcriptional synergy and the regulation of Ucp1 during brown adipocyte induction in white fat depots. Mol. Cell. Biol. 2005, 25, 8311-8322. [CrossRef] [PubMed]
10. Jespersen, N.Z.; Larsen, T.J.; Peijs, L.; Daugaard, S.; Homoe, P.; Loft, A.; de Jong, J.; Mathur, N.; Cannon, B.; Nedergaard, J. et al. A classical brown adipose tissue mRNA signature partly overlaps with brite in the supraclavicular region of adult humans. Cell Metab. 2013, 17, 798-805. [CrossRef] [PubMed]
11. Lidell, M.E.; Betz, M.J.; Dahlqvist Leinhard, O.; Heglind, M.; Elander, L.; Slawik, M.; Mussack, T.; Nilsson, D.; Romu, T.; Nuutila, P. et al. Evidence for two types of brown adipose tissue in humans. Nat. Med. 2013, 19, 631-634. [CrossRef] [PubMed]
12. Landsberg, L.; Young, J.B. The role of the sympathoadrenal system in modulating energy expenditure. Clin. Endocrinol. Metab. 1984, 13, 475-499. [CrossRef]
13. Scheja, L.; Heeren, J. Metabolic interplay between white, beige, brown adipocytes and the liver. J. Hepatol. 2016, 64, 1176-1186. [CrossRef] [PubMed]
14. Nakamura, K.; Fuster, J.J.; Walsh, K. Adipokines: A link between obesity and cardiovascular disease. J. Cardiol. 2014, 63, 250-259. [CrossRef] [PubMed]
15. Trujillo, M.E.; Scherer, P.E. Adipose tissue-derived factors: Impact on health and disease. Endocr. Rev. 2006, 27, 762-778. [CrossRef] [PubMed]
16. Zhang, Y.; Proenca, R.; Maffei, M.; Barone, M.; Leopold, L.; Friedman, J.M. Positional cloning of the mouse obese gene and its human homologue. Nature 1994, 372, 425-432. [CrossRef] [PubMed]
17. Campfield, L.A.; Smith, F.J.; Guisez, Y.; Devos, R.; Burn, P. Recombinant mouse OB protein: Evidence for a peripheral signal linking adiposity and central neural networks. Science 1995, 269, 546-549. [CrossRef] [PubMed]
18. Lord, G.M.; Matarese, G.; Howard, J.K.; Baker, R.J.; Bloom, S.R.; Lechler, R.I. Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature 1998, 394, 897-901. [PubMed]
19. Santos-Alvarez, J.; Goberna, R.; Sanchez-Margalet, V. Human leptin stimulates proliferation and activation of human circulating monocytes. Cell. Immunol. 1999, 194, 6-11. [CrossRef] [PubMed]
20. Kiguchi, N.; Maeda, T.; Kobayashi, Y.; Fukazawa, Y.; Kishioka, S. Leptin enhances CC-chemokine ligand expression in cultured murine macrophage. Biochem. Biophys. Res. Commun. 2009, 384, 311-315. [CrossRef] [PubMed]
21. Zarkesh-Esfahani, H.; Pockley, A.G.; Wu, Z.; Hellewell, P.G.; Weetman, A.P.; Ross, R.J. Leptin indirectly activates human neutrophils via induction of TNF-α. J. Immunol. 2004, 172, 1809-1814. [CrossRef] [PubMed]
22. Yamauchi, T.; Kamon, J.; Waki, H.; Terauchi, Y.; Kubota, N.; Hara, K.; Mori, Y.; Ide, T.; Murakami, K.; Tsuboyama-Kasaoka, N. et al. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat. Med. 2001, 7, 941-946. [CrossRef] [PubMed]
23. Maeda, N.; Shimomura, I.; Kishida, K.; Nishizawa, H.; Matsuda, M.; Nagaretani, H.; Furuyama, N.; Kondo, H.; Takahashi, M.; Arita, Y. et al. Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat. Med. 2002, 8, 731-737. [CrossRef] [PubMed]
24. Ohashi, K.; Parker, J.L.; Ouchi, N.; Higuchi, A.; Vita, J.A.; Gokce, N.; Pedersen, A.A.; Kalthoff, C.; Tullin, S.; Sams, A. et al. Adiponectin promotes macrophage polarization toward an anti-inflammatory phenotype. J. Biol. Chem. 2010, 285, 6153-6160. [CrossRef] [PubMed]
25. Jia, R.; Luo, X.; Lin, C.; Qiao, H.; Wang, N.; Yao, T.; Barclay, J.L.; Whitehead, J.P.; Luo, X.; Yan, J.-Q. Characterization of cold-induced remodeling reveals depot-specific differences across and within brown and white adipose tissues in mice. Acta Physiol. 2016. [CrossRef] [PubMed]
26. Wu, J.; Bostrom, P.; Sparks, L.M.; Ye, L.; Choi, J.H.; Giang, A.H.; Khandekar, M.; Virtanen, K.A.; Nuutila, P.; Schaart, G. et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 2012, 150, 366-376. [CrossRef] [PubMed]
27. Daikoku, T.; Shinohara, Y.; Shima, A.; Yamazaki, N.; Terada, H. Specific elevation of transcript levels of particular protein subtypes induced in brown adipose tissue by cold exposure. Biochim. Biophys. Acta 2000, 1457, 263-272. [CrossRef]
28. Luan, B.; Goodarzi, M.O.; Phillips, N.G.; Guo, X.; Chen, Y.D.; Yao, J.; Allison, M.; Rotter, J.I.; Shaw, R.; Montminy, M. Leptin-mediated increases in catecholamine signaling reduce adipose tissue inflammation via activation of macrophage HDAC4. Cell Metab. 2014, 19, 1058-1065. [CrossRef] [PubMed]
29. Ghigliotti, G.; Barisione, C.; Garibaldi, S.; Fabbi, P.; Brunelli, C.; Spallarossa, P.; Altieri, P.; Rosa, G.; Spinella, G.; Palombo, D. et al. Adipose tissue immune response: Novel triggers and consequences for chronic inflammatory conditions. Inflammation 2014, 37, 1337-1353. [CrossRef] [PubMed]
30. Waki, H.; Tontonoz, P. Endocrine functions of adipose tissue. Annu. Rev. Pathol. 2007, 2, 31-56. [CrossRef] [PubMed]
31. Fasshauer, M.; Bluher, M. Adipokines in health and disease. Trends Pharmacol. Sci. 2015, 36, 461-470. [CrossRef] [PubMed]
32. Friedman, J.M.; Halaas, J.L. Leptin and the regulation of body weight in mammals. Nature 1998, 395, 763-770. [CrossRef] [PubMed]
33. Trayhurn, P.; Duncan, J.S.; Rayner, D.V. Acute cold-induced suppression of ob (obese) gene expression in white adipose tissue of mice: Mediation by the sympathetic system. Biochem. J. 1995, 311, 729-733. [CrossRef] [PubMed]
34. Trayhurn, P.; Duncan, J.S.; Hoggard, N.; Rayner, D.V. Regulation of leptin production: A dominant role for the sympathetic nervous system? Proc. Nutr. Soc. 1998, 57, 413-419. [CrossRef] [PubMed]
35. Evans, B.A.; Agar, L.; Summers, R.J. The role of the sympathetic nervous system in the regulation of leptin synthesis in C57BL/6 mice. FEBS Lett. 1999, 444, 149-154. [CrossRef]
36. Hardie, L.J.; Rayner, D.V.; Holmes, S.; Trayhurn, P. Circulating leptin levels are modulated by fasting, cold exposure and insulin administration in lean but not Zucker (fa/fa) rats as measured by ELISA. Biochem. Biophys. Res. Commun. 1996, 223, 660-665. [CrossRef] [PubMed]
37. Puerta, M.; Abelenda, M.; Rocha, M.; Trayhurn, P. Effect of acute cold exposure on the expression of the adiponectin, resistin and leptin genes in rat white and brown adipose tissues. Horm. Metab. Res. 2002, 34, 629-634. [CrossRef] [PubMed]
38. Korhonen, T.; Saarela, S. Role of adiposity hormones in the mouse during fasting and winter-acclimatization. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2005, 140, 217-223. [CrossRef] [PubMed]
39. Hui, X.; Gu, P.; Zhang, J.; Nie, T.; Pan, Y.; Wu, D.; Feng, T.; Zhong, C.; Wang, Y.; Lam, K.S. et al. Adiponectin enhances cold-induced browning of subcutaneous adipose tissue via promoting M2 macrophage proliferation. Cell Metab. 2015, 22, 279-290. [CrossRef] [PubMed]
40. Wijers, S.L.; Saris, W.H.; van Marken Lichtenbelt, W.D. Individual thermogenic responses to mild cold and overfeeding are closely related. J. Clin. Endocrinol. Metab. 2007, 92, 4299-4305. [CrossRef] [PubMed]
41. Fasshauer, M.; Klein, J.; Neumann, S.; Eszlinger, M.; Paschke, R. Adiponectin gene expression is inhibited by β-adrenergic stimulation via protein kinase A in 3T3-L1 adipocytes. FEBS Lett. 2001, 507, 142-146. [CrossRef]
42. Walden, T.B.; Hansen, I.R.; Timmons, J.A.; Cannon, B.; Nedergaard, J. Recruited vs. nonrecruited molecular signatures of brown, “brite”, and white adipose tissues. Am. J. Physiol. Endocrinol. Metab. 2012, 302, E19-E31. [CrossRef] [PubMed]
43. Villaret, A.; Galitzky, J.; Decaunes, P.; Esteve, D.; Marques, M.A.; Sengenes, C.; Chiotasso, P.; Tchkonia, T.; Lafontan, M.; Kirkland, J.L. 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. [CrossRef] [PubMed]
44. Fontana, L.; Eagon, J.C.; Trujillo, M.E.; Scherer, P.E.; Klein, S. Visceral fat adipokine secretion is associated with systemic inflammation in obese humans. Diabetes 2007, 56, 1010-1013. [CrossRef] [PubMed]
45. Kannel, W.B.; Cupples, L.A.; Ramaswami, R.; Stokes, J., III; Kreger, B.E.; Higgins, M. Regional obesity and risk of cardiovascular disease; the Framingham study. J. Clin. Epidemiol. 1991, 44, 183-190. [CrossRef]
46. Miyazaki, Y.; Glass, L.; Triplitt, C.; Wajcberg, E.; Mandarino, L.J.; DeFronzo, R.A. Abdominal fat distribution and peripheral and hepatic insulin resistance in type 2 diabetes mellitus. Am. J. Physiol. Endocrinol. Metab. 2002, 283, E1135-E1143. [CrossRef] [PubMed]
47. Torres-Leal, F.L.; Fonseca-Alaniz, M.H.; Rogero, M.M.; Tirapegui, J. The role of inflamed adipose tissue in the insulin resistance. Cell Biochem. Funct. 2010, 28, 623-631. [CrossRef] [PubMed]
48. Yang, Y.K.; Chen, M.; Clements, R.H.; Abrams, G.A.; Aprahamian, C.J.; Harmon, C.M. Human mesenteric adipose tissue plays unique role versus subcutaneous and omental fat in obesity related diabetes. Cell. Physiol. Biochem. 2008, 22, 531-538. [CrossRef] [PubMed]
49. Dempersmier, J.; Sambeat, A.; Gulyaeva, O.; Paul, S.M.; Hudak, C.S.; Raposo, H.F.; Kwan, H.Y.; Kang, C.; Wong, R.H.; Sul, H.S. Cold-inducible Zfp516 activates UCP1 transcription to promote browning of white fat and development of brown fat. Mol. Cell 2015, 57, 235-246. [CrossRef] [PubMed]
50. Cinti, S. The adipose organ. Prostaglandins Leukot Essent. Fatty Acids 2005, 73, 9-15. [CrossRef] [PubMed]
51. Luo, X.; Hutley, L.J.; Webster, J.A.; Kim, Y.H.; Liu, D.F.; Newell, F.S.; Widberg, C.H.; Bachmann, A.; Turner, N.; Schmitz-Peiffer, C. et al. Identification of BMP and activin membrane-bound inhibitor (BAMBI) as a potent negative regulator of adipogenesis and modulator of autocrine/paracrine adipogenic factors. Diabetes 2012, 61, 124-136. [CrossRef] [PubMed]