LXRα fuels fatty acid-stimulated oxygen consumption in white adipocytes

Journal of Lipid Research

Volumn 55, Issue 2, 2014, Pages 247-257

  Dib, Lea ^a   Bugge, Anne ^a   Collins, Sheila ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

Adipose tissue; Lipolysis; Mitochondria; Oxidation

Indexed keywords

ADIPOSE TISSUE; LIPOLYSIS; MITOCHONDRIA; OXIDATION;

ADIPOCYTES, WHITE; ANIMALS; BODY WEIGHT; DIET, HIGH-FAT; FATTY ACIDS; GENE EXPRESSION REGULATION; GENE KNOCKOUT TECHNIQUES; HYDROCARBONS, FLUORINATED; LIPOLYSIS; MALE; MICE; MITOCHONDRIA; OBESITY; ORPHAN NUCLEAR RECEPTORS; OXIDATION-REDUCTION; OXYGEN CONSUMPTION; PHENOTYPE; RECEPTORS, ADRENERGIC, BETA; SULFONAMIDES;

EID: 84893372286     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M043422     Document Type: Article

References (73)

1. Yach, D., D. Stuckler, and K. D. Brownell.2006.Epidemiologic and economic consequences of the global epidemics of obesity and diabetes. Nat. Med. 12 : 62-66.
2. Shoelson, S. E., L. Herrero, and A. Naaz.2007.Obesity, inflammation, and insulin resistance. Gastroenterology.132 : 2169-2180.
3. Pi-Sunyer, F. X. 1993.Medical hazards of obesity. Ann. Intern. Med. 119 : 655-660.
4. Sethi, J. K., and A. J. Vidal-Puig.2007.Thematic review series: adipocyte biology. Adipose tissue function and plasticity orchestrate nutritional adaptation. J. Lipid Res. 48 : 1253-1262.
5. Strawford, A., F. Antelo, M. Christiansen, and M. K. Hellerstein.2004. Adipose tissue triglyceride turnover, de novo lipogenesis, and cell proliferation in humans measured with 2H2O. Am. J. Physiol. Endocrinol. Metab. 286 : E577-E588.
6. Langin, D., A. Dicker, G. Tavernier, J. Hoffstedt, A. Mairal, M. Ryden, E. Arner, A. Sicard, C. M. Jenkins, N. Viguerie, et al.2005.Adipocyte lipases and defect of lipolysis in human obesity. Diabetes.54 : 3190-3197.
7. Eckel, R. H., S. M. Grundy, and P. Z. Zimmet.2005.The metabolic syndrome. Lancet.365 : 1415-1428.
8. Bartness, T. J., Y. B. Shrestha, C. H. Vaughan, G. J. Schwartz, and C. K. Song.2010.Sensory and sympathetic nervous system control of white adipose tissue lipolysis. Mol. Cell. Endocrinol. 318 : 34-43.
9. Fliers, E., F. Kreier, P. J. Voshol, L. M. Havekes, H. P. Sauerwein, A. Kalsbeek, R. M. Buijs, and J. A. Romijn.2003.White adipose tissue: getting nervous. J. Neuroendocrinol. 15 : 1005-1010.
10. Cannon, B., and J. Nedergaard.2004.Brown adipose tissue: function and physiological significance. Physiol. Rev. 84 : 277-359.
11. Lafontan, M., C. Moro, M. Berlan, F. Crampes, C. Sengenes, and J. Galitzky.2008.Control of lipolysis by natriuretic peptides and cyclic GMP. Trends Endocrinol. Metab. 19 : 130-137.
12. Matthias, A., K. B. Ohlson, J. M. Fredriksson, A. Jacobsson, J. Nedergaard, and B. Cannon.2000.Thermogenic responses in brown fat cells are fully UCP1-dependent. UCP2 or UCP3 do not substitute for UCP1 in adrenergically or fatty scid-induced thermogenesis. J. Biol. Chem. 275 : 25073-25081.
13. Lidell, M. E., M. J. Betz, O. Dahlqvist Leinhard, M. Heglind, L. Elander, M. Slawik, T. Mussack, D. Nilsson, T. Romu, P. Nuutila, et al.2013.Evidence for two types of brown adipose tissue in humans. Nat. Med. 19 : 631-634
14. Cypess, A. M., S. Lehman, G. Williams, I. Tal, D. Rodman, A. B. Goldfine, F. C. Kuo, E. L. Palmer, Y. H. Tseng, A. Doria, et al.2009.Identification and importance of brown adipose tissue in adult humans. N. Engl. J. Med. 360 : 1509-1517.
15. Horowitz, J. F. 2003.Fatty acid mobilization from adipose tissue during exercise. Trends Endocrinol. Metab. 14 : 386-392.
16. Bartelt, A., O. T. Bruns, R. Reimer, H. Hohenberg, H. Ittrich, K. Peldschus, M. G. Kaul, U. I. Tromsdorf, H. Weller, C. Waurisch, et al.2011.Brown adipose tissue activity controls triglyceride clearance. Nat. Med. 17 : 200-205.
17. Wilson-Fritch, L., S. Nicoloro, M. Chouinard, M. A. Lazar, P. C. Chui, J. Leszyk, J. Straubhaar, M. P. Czech, and S. Corvera.2004.Mitochondrial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone. J. Clin. Invest. 114 : 1281-1289.
18. Maassen, J. A., J. A. Romijn, and R. J. Heine.2007.Fatty acid-induced mitochondrial uncoupling in adipocytes as a key protective factor against insulin resistance and beta cell dysfunction: a new concept in the pathogenesis of obesity-Associated type 2 diabetes mellitus. Diabetologia.50 : 2036-2041.
19. Kusminski, C. M., and P. E. Scherer.2012.Mitochondrial dysfunction in white adipose tissue. Trends Endocrinol. Metab. 23 : 435-443.
20. Wang, T., Y. Zang, W. Ling, B. E. Corkey, and W. Guo.2003.Metabolic partitioning of endogenous fatty acid in adipocytes. Obes. Res. 11 : 880-887.
21. Stenson, B. M., M. Ryden, K. R. Steffensen, K. Wahlen, A. T. Pettersson, J. W. Jocken, P. Arner, and J. Laurencikiene.2009.Activation of liver X receptor regulates substrate oxidation in white adipocytes. Endocrinology.150 : 4104-4113.
22. Yehuda-Shnaidman, E., B. Buehrer, J. Pi, N. Kumar, and S. Collins.2010.Acute stimulation of white adipocyte respiration by PKAinduced lipolysis. Diabetes.59 : 2474-2483.
23. Bottcher, H., and P. Furst.1997.Decreased white fat cell thermogenesis in obese individuals. Int. J. Obes. Relat. Metab. Disord. 21 : 439-444.
24. Beaven, S. W., and P. Tontonoz.2006.Nuclear receptors in lipid metabolism: targeting the heart of dyslipidemia. Annu. Rev. Med. 57 : 313-329.
25. Laurencikiene, J., and M. Ryden.2012.Liver X receptors and fat cell metabolism. Int. J. Obes. (Lond).36 : 1494-1502.
26. Calkin, A. C., and P. Tontonoz.2012.Transcriptional integration of metabolism by the nuclear sterol-Activated receptors LXR and FXR. Nat. Rev. Mol. Cell Biol. 13 : 213-224.
27. Jakobsson, T., E. Treuter, J. A. Gustafsson, and K. R. Steffensen.2012.Liver X receptor biology and pharmacology: new pathways, challenges and opportunities. Trends Pharmacol. Sci. 33 : 394-404.
28. Chen, W., G. Chen, D. L. Head, D. J. Mangelsdorf, and D. W. Russell.2007.Enzymatic reduction of oxysterols impairs LXR signaling in cultured cells and the livers of mice. Cell Metab. 5 : 73-79.
29. Repa, J. J., S. D. Turley, J. A. Lobaccaro, J. Medina, L. Li, K. Lustig, B. Shan, R. A. Heyman, J. M. Dietschy, and D. J. Mangelsdorf.2000.Regulation of absorption and ABC1-mediated efflux of cholesterol by RXR heterodimers. Science.289 : 1524-1529.
30. Yu, L., J. York, K. von Bergmann, D. Lutjohann, J. C. Cohen, and H. H. Hobbs.2003.Stimulation of cholesterol excretion by the liver X receptor agonist requires ATP-binding cassette transporters G5 and G8. J. Biol. Chem. 278 : 15565-15570.
31. Zelcer, N., C. Hong, R. Boyadjian, and P. Tontonoz.2009.LXR regulates cholesterol uptake through Idol-dependent ubiquitination of the LDL receptor. Science.325 : 100-104.
32. Griesel, B. A., J. Weems, R. A. Russell, E. D. Abel, K. Humphries, and A. L. Olson.2010.Acute inhibition of fatty acid import inhibits GLUT4 transcription in adipose tissue, but not skeletal or cardiac muscle tissue, partly through liver X receptor (LXR) signaling. Diabetes.59 : 800-807.
33. Laffitte, B. A., L. C. Chao, J. Li, R. Walczak, S. Hummasti, S. B. Joseph, A. Castrillo, D. C. Wilpitz, D. J. Mangelsdorf, J. L. Collins, et al.2003.Activation of liver X receptor improves glucose tolerance through coordinate regulation of glucose metabolism in liver and adipose tissue. Proc. Natl. Acad. Sci. USA.100 : 5419-5424.
34. Yoon, C. H., Y. J. Kwon, S. W. Lee, Y. B. Park, S. K. Lee, and M. C. Park.2013.Activation of liver X receptors suppresses inflammatory gene expressions and transcriptional corepressor clearance in rheumatoid arthritis fibroblast like synoviocytes. J. Clin. Immunol. 33 : 190-199.
35. Spann, N. J., L. X. Garmire, J. G. McDonald, D. S. Myers, S. B. Milne, N. Shibata, D. Reichart, J. N. Fox, I. Shaked, D. Heudobler, et al.2012.Regulated accumulation of desmosterol integrates macrophage lipid metabolism and inflammatory responses. Cell.151 : 138-152.
36. Bonamassa, B., and A. Moschetta.2013.Atherosclerosis: lessons from LXR and the intestine. Trends Endocrinol. Metab. 24 : 120-128.
37. Willy, P. J., K. Umesono, E. S. Ong, R. M. Evans, R. A. Heyman, and D. J. Mangelsdorf.1995.LXR, a nuclear receptor that defines a distinct retinoid response pathway. Genes Dev. 9 : 1033-1045.
38. Auboeuf, D., J. Rieusset, L. Fajas, P. Vallier, V. Frering, J. P. Riou, B. Staels, J. Auwerx, M. Laville, and H. Vidal.1997.Tissue distribution and quantification of the expression of mRNAs of peroxisome proliferator-Activated receptors and liver X receptor-Alpha in humans: no alteration in adipose tissue of obese and NIDDM patients. Diabetes.46 : 1319-1327.
39. Krause, B. R., and A. D. Hartman.1984.Adipose tissue and cholesterol metabolism. J. Lipid Res. 25 : 97-110.
40. Stenson, B. M., M. Ryden, N. Venteclef, I. Dahlman, A. M. Pettersson, A. Mairal, G. Astrom, L. Blomqvist, V. Wang, J. W. Jocken, et al.2011.Liver X receptor (LXR) regulates human adipocyte lipolysis. J. Biol. Chem. 286 : 370-379.
41. Ross, S. E., R. L. Erickson, I. Gerin, P. M. DeRose, L. Bajnok, K. A. Longo, D. E. Misek, R. Kuick, S. M. Hanash, K. B. Atkins, et al.2002.Microarray analyses during adipogenesis: understanding the effects of Wnt signaling on adipogenesis and the roles of liver X receptor alpha in adipocyte metabolism. Mol. Cell. Biol. 22 : 5989-5999.
42. Commerford, S. R., L. Vargas, S. E. Dorfman, N. Mitro, E. C. Rocheford, P. A. Mak, X. Li, P. Kennedy, T. L. Mullarkey, and E. Saez.2007.Dissection of the insulin-sensitizing effect of liver X receptor ligands. Mol. Endocrinol. 21 : 3002-3012.
43. Wang, H., Y. Zhang, E. Yehuda-Shnaidman, A. V. Medvedev, N. Kumar, K. W. Daniel, J. Robidoux, M. P. Czech, D. J. Mangelsdorf, and S. Collins.2008.Liver X receptor alpha is a transcriptional repressor of the uncoupling protein 1 gene and the brown fat phenotype. Mol. Cell. Biol. 28 : 2187-2200.
44. Zhang, Y., S. R. Breevoort, J. Angdisen, M. Fu, D. R. Schmidt, S. R. Holmstrom, S. A. Kliewer, D. J. Mangelsdorf, and I. G. Schulman. Liver LXRalpha expression is crucial for whole body cholesterol homeostasis and reverse cholesterol transport in mice. J. Clin. Invest. 122 : 1688-1699.
45. He, W., Y. Barak, A. Hevener, P. Olson, D. Liao, J. Le, M. Nelson, E. Ong, J. M. Olefsky, and R. M. Evans.2003.Adipose-specific peroxisome proliferator-Activated receptor gamma knockout causes insulin resistance in fat and liver but not in muscle. Proc. Natl. Acad. Sci. USA.100 : 15712-15717.
46. Kalaany, N. Y., K. C. Gauthier, A. M. Zavacki, P. P. Mammen, T. Kitazume, J. A. Peterson, J. D. Horton, D. J. Garry, A. C. Bianco, and D. J. Mangelsdorf.2005.LXRs regulate the balance between fat storage and oxidation. Cell Metab. 1 : 231-244.
47. Gao, M., and D. Liu.2013.The liver X receptor agonist T0901317 protects mice from high fat diet-induced obesity and insulin resistance. AAPS J. 15 : 258-266.
48. Schultz, J. R., H. Tu, A. Luk, J. J. Repa, J. C. Medina, L. Li, S. Schwendner, S. Wang, M. Thoolen, D. J. Mangelsdorf, et al.2000.Role of LXRs in control of lipogenesis. Genes Dev. 14 : 2831-2838.
49. Seo, J. B., H. M. Moon, W. S. Kim, Y. S. Lee, H. W. Jeong, E. J. Yoo, J. Ham, H. Kang, M. G. Park, K. R. Steffensen, et al.2004.Activated liver X receptors stimulate adipocyte differentiation through induction of peroxisome proliferator-Activated receptor gamma expression. Mol. Cell. Biol. 24 : 3430-3444.
50. Bugge, A., L. Dib, and S. Collins.2014.Measuring respiratory activity of adipocytes and adipose tissues in real time. In Methods in Enzymology: Methods of Adipose Tissue Biology. Part A, Vol. 527. O. A. McDougald, editor. Academic Press. In press.
51. Wu, M., A. Neilson, A. L. Swift, R. Moran, J. Tamagnine, D. Parslow, S. Armistead, K. Lemire, J. Orrell, J. Teich, et al.2007.Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am. J. Physiol. Cell Physiol. 292 : C125-C136.
52. Londos, C. 2004.Hormone-sensitive lipase, perilipins, and the control of lipolysis in adipocytes. In Diabetes Mellitus: A Fundamental and Clinical Text. D. LeRoith, I. Simeon, M. D. Taylor, and J. M. Olefsky, editors. Lippincott Williams & Wilkins. 365-371.
53. Miyoshi, H., J. W. Perfield 2nd, S. C. Souza, W. J. Shen, H. H. Zhang, Z. S. Stancheva, F. B. Kraemer, M. S. Obin, and A. S. Greenberg.2007.Control of adipose triglyceride lipase action by serine 517 of perilipin A globally regulates protein kinase A-stimulated lipolysis in adipocytes. J. Biol. Chem. 282 : 996-1002.
54. Nye, C. K., R. W. Hanson, and S. C. Kalhan.2008.Glyceroneogenesis is the dominant pathway for triglyceride glycerol synthesis in vivo in the rat. J. Biol. Chem. 283 : 27565-27574.
55. Janowski, B. A., M. J. Grogan, S. A. Jones, G. B. Wisely, S. A. Kliewer, E. J. Corey, and D. J. Mangelsdorf.1999.Structural requirements of ligands for the oxysterol liver X receptors LXRalpha and LXRbeta. Proc. Natl. Acad. Sci. USA.96 : 266-271.
56. Peet, D. J., B. A. Janowski, and D. J. Mangelsdorf.1998.The LXRs: a new class of oxysterol receptors. Curr. Opin. Genet. Dev. 8 : 571-575.
57. Korach-Andre, M., P. Parini, L. Larsson, A. Arner, K. R. Steffensen, and J. A. Gustafsson.2010.Separate and overlapping metabolic functions of LXRalpha and LXRbeta in C57Bl/6 female mice. Am. J. Physiol. Endocrinol. Metab. 298 : E167-E178.
58. Korach-Andre, M., A. Archer, R. P. Barros, P. Parini, and J. A. Gustafsson.2011.Both liver-X receptor (LXR) isoforms control energy expenditure by regulating brown adipose tissue activity. Proc. Natl. Acad. Sci. USA.108 : 403-408.
59. Yoshikawa, T., H. Shimano, M. Amemiya-Kudo, N. Yahagi, A. H. Hasty, T. Matsuzaka, H. Okazaki, Y. Tamura, Y. Iizuka, K. Ohashi, et al.2001. Identification of liver X receptor-retinoid X receptor as an activator of the sterol regulatory element-binding protein 1c gene promoter. Mol. Cell. Biol. 21 : 2991-3000.
60. Sekiya, M., N. Yahagi, T. Matsuzaka, Y. Takeuchi, Y. Nakagawa, H. Takahashi, H. Okazaki, Y. Iizuka, K. Ohashi, T. Gotoda, et al.2007.SREBP-1- independent regulation of lipogenic gene expression in adipocytes. J. Lipid Res. 48 : 1581-1591.
61. Duncan, R. E., M. Ahmadian, K. Jaworski, E. Sarkadi-Nagy, and H. S. Sul.2007.Regulation of lipolysis in adipocytes. Annu. Rev. Nutr. 27 : 79-101.
62. Orci, L., W. S. Cook, M. Ravazzola, M. Y. Wang, B. H. Park, R. Montesano, and R. H. Unger.2004.Rapid transformation of white adipocytes into fat-oxidizing machines. Proc. Natl. Acad. Sci. USA.01 : 2058-2063.
63. Vosselman, M. J., A. A. van der Lans, B. Brans, R. Wierts, M. A. van Baak, P. Schrauwen, and W. D. van Marken Lichtenbelt.2012.Systemic beta-Adrenergic stimulation of thermogenesis is not accompanied by brown adipose tissue activity in humans. Diabetes.61 : 3106-3113.
64. Lewis, G. F., A. Carpentier, K. Adeli, and A. Giacca.2002.Disordered fat storage and mobilization in the pathogenesis of insulin resistance and type 2 diabetes. Endocr. Rev. 23 : 201-229.
65. Collins, S., K. W. Daniel, and E. M. Rohlfs.1999.Depressed expression of adipocyte beta-Adrenergic receptors is a common feature of congenital and diet-induced obesity in rodents. Int. J. Obes. Relat. Metab. Disord. 23 : 669-677.
66. Carpene, C., M. Berlan, and M. Lafontan.1983.Influence of development and reduction of fat stores on the antilipolytic alpha 2-Adrenoceptor in hamster adipocytes: comparison with adenosine and beta-Adrenergic lipolytic responses. J. Lipid Res. 24 : 766-774.
67. Bischoff, E. D., C. L. Daige, M. Petrowski, H. Dedman, J. Pattison, J. Juliano, A. C. Li, and I. G. Schulman.2010.Non-redundant roles for LXRalpha and LXRbeta in atherosclerosis susceptibility in low density lipoprotein receptor knockout mice. J. Lipid Res. 51 : 900-906.
68. Beyer, T. P., R. J. Schmidt, P. Foxworthy, Y. Zhang, J. Dai, W. R. Bensch, R. F. Kauffman, H. Gao, T. P. Ryan, X. C. Jiang, et al.2004. Coadministration of a liver X receptor agonist and a peroxisome proliferator activator receptor-Alpha agonist in mice: effects of nuclear receptor interplay on high-density lipoprotein and triglyceride metabolism in vivo. J. Pharmacol. Exp. Ther. 309 : 861-868.
69. Hu, T., P. Foxworthy, A. Siesky, J. V. Ficorilli, H. Gao, S. Li, M. Christe, T. Ryan, G. Cao, P. Eacho, et al.2005.Hepatic peroxisomal fatty acid beta-oxidation is regulated by liver X receptor alpha. Endocrinology.146 : 5380-5387.
70. Kase, E. T., G. H. Thoresen, S. Westerlund, K. Hojlund, A. C. Rustan, and M. Gaster.2007.Liver X receptor antagonist reduces lipid formation and increases glucose metabolism in myotubes from lean, obese and type 2 diabetic individuals. Diabetologia.50 : 2171-2180.
71. Gao, M., L. Bu, Y. Ma, and D. Liu.2013.Concurrent activation of liver x receptor and peroxisome proliferator-Activated receptor alpha exacerbates hepatic steatosis in high fat diet-induced obese mice. PLoS ONE.8 : e65641.
72. Benz, V., M. Bloch, S. Wardat, C. Bohm, L. Maurer, S. Mahmoodzadeh, P. Wiedmer, J. Spranger, A. Foryst-Ludwig, and U. Kintscher.2012.Sexual dimorphic regulation of body weight dynamics and adipose tissue lipolysis. PLoS ONE.7 : e37794.
73. Cho, S. Y., P. J. Park, E. S. Shin, J. H. Lee, H. K. Chang, and T. R. Lee.2009.Proteomic analysis of mitochondrial proteins of basal and lipolytically (isoproterenol and TNF-Alpha)-stimulated adipocytes. J. Cell. Biochem. 106 : 257-266.