Lipocalin 2 regulates brown fat activation via a nonadrenergic activation mechanism

Journal of Biological Chemistry

Volumn 289, Issue 32, 2014, Pages 22063-22077

  Zhang, Yuanyuan ^a   Guo, Hong ^a   Deis, Jessica A ^a   Mashek, Mara G ^a   Zhao, Ming ^a   Ariyakumar, Donsanjiv ^b   Armien, Anibal G ^b   Bernlohr, David A ^a   Mashek, Douglas G ^b   Chen, Xiaoli ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b Minnesota Veterinary Diagnostic Laboratory   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METABOLISM;

ACTIVATION MECHANISMS; ADIPOCYTES; LIPOCALIN 2; OXIDATIVE METABOLISM;

CHEMICAL ACTIVATION;

ACUTE PHASE PROTEIN; CATECHOLAMINE; ION CHANNEL; LCN2 PROTEIN, MOUSE; LIPOCALIN; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; ONCOPROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PPARGC1A PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL; BROWN ADIPOCYTE; BROWN ADIPOSE TISSUE; C57BL MOUSE; DEFICIENCY; GENE EXPRESSION; GENETICS; KNOCKOUT MOUSE; LIPID METABOLISM; METABOLISM; MITOCHONDRION; MOUSE; OXIDATION REDUCTION REACTION; PEROXISOME; PHOSPHORYLATION; PHYSIOLOGY; THERMOGENESIS;

ACUTE-PHASE PROTEINS; ADIPOCYTES, BROWN; ADIPOSE TISSUE, BROWN; ANIMALS; CATECHOLAMINES; GENE EXPRESSION; ION CHANNELS; LIPID METABOLISM; LIPOCALINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; ONCOGENE PROTEINS; OXIDATION-REDUCTION; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PEROXISOMES; PHOSPHORYLATION; PPAR GAMMA; THERMOGENESIS; TRANSCRIPTION FACTORS;

EID: 84905844118     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.559104     Document Type: Article

References (48)

1. Waki, H., and Tontonoz, P. (2007) Endocrine functions of adipose tissue. Annu. Rev. Pathol. 2, 31-56
2. Ouchi, N., Parker, J. L., Lugus, J. J., and Walsh, K. (2011) Adipokines in inflammation and metabolic disease. Nat. Rev. Immunol. 11, 85-97
3. Enerbäck, S. (2010) Human brown adipose tissue. Cell Metab. 11, 248-252
4. Lidell, M. E., Betz, M. J., Dahlqvist Leinhard, O., Heglind, M., Elander, L., Slawik, M., Mussack, T., Nilsson, D., Romu, T., Nuutila, P., Virtanen, K. A., Beuschlein, F., Persson, A., Borga, M., and Enerbäck, S. (2013) Evidence for two types of brown adipose tissue in humans. Nat. Med. 19, 631-634
5. Nedergaard, J., Bengtsson, T., and Cannon, B. (2007) Unexpected evidence for active brown adipose tissue in adult humans. Am. J. Physiol. Endocrinol. Metab. 293, E444-E452
6. Saito, M., Okamatsu-Ogura, Y., Matsushita, M., Watanabe, K., Yoneshiro, T., Nio-Kobayashi, J., Iwanaga, T., Miyagawa, M., Kameya, T., Nakada, K., Kawai, Y., and Tsujisaki, M. (2009) High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 58, 1526-1531
7. Orava, J., Nuutila, P., Lidell, M. E., Oikonen, V., Noponen, T., Viljanen, T., Scheinin, M., Taittonen, M., Niemi, T., Enerbäck, S., and Virtanen, K. A. (2011) Different metabolic responses of human brown adipose tissue to activation by cold and insulin. Cell Metab. 14, 272-279
8. van Marken Lichtenbelt, W. D., Vanhommerig, J. W., Smulders, N. M., Drossaerts, J. M., Kemerink, G. J., Bouvy, N. D., Schrauwen, P., and Teule, G. J. (2009) Cold-activated brown adipose tissue in healthy men. N. Engl. J. Med. 360, 1500-1508
9. Virtanen, K. A., Lidell, M. E., Orava, J., Heglind, M., Westergren, R., Niemi, T., Taittonen, M., Laine, J., Savisto, N. J., Enerbäck, S., and Nuutila, P. (2009) Functional brown adipose tissue in healthy adults. N. Engl. J. Med. 360, 1518-1525
10. Cypess, A. M., Lehman, S., Williams, G., Tal, I., Rodman, D., Goldfine, A. B., Kuo, F. C., Palmer, E. L., Tseng, Y. H., Doria, A., Kolodny, G. M., and Kahn, C. R. (2009) Identification and importance of brown adipose tissue in adult humans. N. Engl. J. Med. 360, 1509-1517
11. Zingaretti, M. C., Crosta, F., Vitali, A., Guerrieri, M., Frontini, A., Cannon, B., Nedergaard, J., and Cinti, S. (2009) The presence of UCP1 demonstrates that metabolically active adipose tissue in the neck of adult humans truly represents brown adipose tissue. FASEB J. 23, 3113-3120
12. Ouellet, V., Labbé, S. M., Blondin, D. P., Phoenix, S., Guérin, B., Haman, F., Turcotte, E. E., Richard, D., and Carpentier, A. C. (2012) Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. J. Clin. Invest. 122, 545-552
13. Bartelt, A., Bruns, O. T., Reimer, R., Hohenberg, H., Ittrich, H., Peldschus, K., Kaul, M. G., Tromsdorf, U. I., Weller, H., Waurisch, C., Eychmüller, A., Gordts, P. L., Rinninger, F., Bruegelmann, K., Freund, B., Nielsen, P., Merkel, M., and Heeren, J. (2011) Brown adipose tissue activity controls triglyceride clearance. Nat. Med. 17, 200-205
14. Villarroya, F., and Vidal-Puig, A. (2013) Beyond the sympathetic tone: the new brown fat activators. Cell Metab. 17, 638-643
15. Trayhurn, P. (1981) Fatty acid synthesis in mouse brown adipose tissue. The influence of environmental temperature on the proportion of wholebody fatty acid synthesis in brown adipose tissue and the liver. Biochim. Biophys. Acta 664, 549-560
16. Shimomura, I., Funahashi, T., Takahashi, M., Maeda, K., Kotani, K., Nakamura, T., Yamashita, S., Miura, M., Fukuda, Y., Takemura, K., Tokunaga, K., and Matsuzawa, Y. (1996) Enhanced expression of PAI-1 in visceral fat: possible contributor to vascular disease in obesity. Nat. Med. 2, 800-803
17. Timmons, J. A., Wennmalm, K., Larsson, O., Walden, T. B., Lassmann, T., Petrovic, N., Hamilton, D. L., Gimeno, R. E., Wahlestedt, C., Baar, K., Nedergaard, J., and Cannon, B. (2007) Myogenic gene expression signature establishes that brown and white adipocytes originate from distinct cell lineages. Proc. Natl. Acad. Sci. U.S.A. 104, 4401-4406
18. Cao, W., Daniel, K. W., Robidoux, J., Puigserver, P., Medvedev, A. V., Bai, X., Floering, L. M., Spiegelman, B. M., and Collins, S. (2004) p38 mitogenactivated protein kinase is the central regulator of cyclic AMP-dependent transcription of the brown fat uncoupling protein 1 gene. Mol. Cell. Biol. 24, 3057-3067
19. Cao, W., Medvedev, A. V., Daniel, K. W., and Collins, S. (2001)-Adrenergic activation of p38MAPkinase in adipocytes: cAMP induction of the uncoupling protein 1 (UCP1) gene requires p38MAPkinase. J. Biol. Chem. 276, 27077-27082
20. Bordicchia, M., Liu, D., Amri, E. Z., Ailhaud, G., Dessì-Fulgheri, P., Zhang, C., Takahashi, N., Sarzani, R., and Collins, S. (2012) Cardiac natriuretic peptides act via p38 MAPK to induce the brown fat thermogenic program in mouse and human adipocytes. J. Clin. Invest. 122, 1022-1036
21. Somwar, R., Perreault, M., Kapur, S., Taha, C., Sweeney, G., Ramlal, T., Kim, D. Y., Keen, J., Côte, C. H., Klip, A., and Marette, A. (2000) Activation of p38 mitogen-activated protein kinase α and α by insulin and contraction in rat skeletal muscle: potential role in the stimulation of glucose transport. Diabetes 49, 1794-1800
22. Fujishiro, M., Gotoh, Y., Katagiri, H., Sakoda, H., Ogihara, T., Anai, M., Onishi, Y., Ono, H., Funaki, M., Inukai, K., Fukushima, Y., Kikuchi, M., Oka, Y., and Asano, T. (2001) MKK6/3 and p38MAPKpathway activation is not necessary for insulin-induced glucose uptake but regulates glucose transporter expression. J. Biol. Chem. 276, 19800-19806
23. Geiger, P. C., Wright, D. C., Han, D. H., and Holloszy, J. O. (2005) Activation of p38 MAP kinase enhances sensitivity of muscle glucose transport to insulin. Am. J. Physiol. Endocrinol. Metab. 288, E782-E788
24. Raingeaud, J., Gupta, S., Rogers, J. S., Dickens, M., Han, J., Ulevitch, R. J., and Davis, R. J. (1995) Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J. Biol. Chem. 270, 7420-7426
25. Zhang, J., Wu, Y., Zhang, Y., Leroith, D., Bernlohr, D. A., and Chen, X. (2008) The role of lipocalin 2 in the regulation of inflammation in adipocytes and macrophages. Mol. Endocrinol. 22, 1416-1426
26. Yan, Q. W., Yang, Q., Mody, N., Graham, T. E., Hsu, C. H., Xu, Z., Houstis, N. E., Kahn, B. B., and Rosen, E. D. (2007) The adipokine lipocalin 2 is regulated by obesity and promotes insulin resistance. Diabetes 56, 2533-2540
27. LaLonde, J. M., Bernlohr, D. A., and Banaszak, L. J. (1994) The up-anddown-barrel proteins. FASEB J. 8, 1240-1247
28. Guo, H., Jin, D., Zhang, Y., Wright, W., Bazuine, M., Brockman, D. A., Bernlohr, D. A., and Chen, X. (2010) Lipocalin-2 deficiency impairs thermogenesis and potentiates diet-induced insulin resistance in mice. Diabetes 59, 1376-1385
29. Jin, D., Guo, H., Bu, S. Y., Zhang, Y., Hannaford, J., Mashek, D. G., and Chen, X. (2011) Lipocalin 2 is a selective modulator of peroxisome proliferator-activated receptor-activation and function in lipid homeostasis and energy expenditure. FASEB J. 25, 754-764
30. Guo, H., Zhang, Y., Brockman, D. A., Hahn, W., Bernlohr, D. A., and Chen, X. (2012) Lipocalin 2 deficiency alters estradiol production and estrogen receptor signaling in female mice. Endocrinology 153, 1183-1193
31. Guo, H., Bazuine, M., Jin, D., Huang, M. M., Cushman, S. W., and Chen, X. (2013) Evidence for the regulatory role of lipocalin 2 in high-fat dietinduced adipose tissue remodeling in male mice. Endocrinology 154, 3525-3538
32. Chen, X., Hausman, D. B., Dean, R. G., and Hausman, G. J. (1997) Differentiation-dependent expression of obese (ob) gene by preadipocytes and adipocytes in primary cultures of porcine stromal-vascular cells. Biochim. Biophys. Acta 1359, 136-142
33. Cannon, B., and Nedergaard, J. (2004) Brown adipose tissue: function and physiological significance. Physiol. Rev. 84, 277-359
34. Nguyen, K. D., Qiu, Y., Cui, X., Goh, Y. P., Mwangi, J., David, T., Mukundan, L., Brombacher, F., Locksley, R. M., and Chawla, A. (2011) Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis. Nature 480, 104-108
35. Warszawska, J. M., Gawish, R., Sharif, O., Sigel, S., Doninger, B., Lakovits, K., Mesteri, I., Nairz, M., Boon, L., Spiel, A., Fuhrmann, V., Strobl, B., Müller, M., Schenk, P., Weiss, G., and Knapp, S. (2013) Lipocalin 2 deactivates macrophages and worsens pneumococcal pneumonia outcomes. J. Clin. Invest. 123, 3363-3372
36. Uldry, M., Yang, W., St-Pierre, J., Lin, J., Seale, P., and Spiegelman, B. M. (2006) Complementary action of the PGC-1 coactivators in mitochondrial biogenesis and brown fat differentiation. Cell Metab. 3, 333-341
37. Collins, S., Yehuda-Shnaidman, E., and Wang, H. (2010) Positive and negative control of Ucp1 gene transcription and the role of-adrenergic signaling networks. Int. J. Obes. 34, S28-S33
38. Ohno, H., Shinoda, K., Spiegelman, B. M., and Kajimura, S. (2012) PPAR agonists induce a white-to-brown fat conversion through stabilization of PRDM16 protein. Cell Metab. 15, 395-404
39. Bogacka, I., Xie, H., Bray, G. A., and Smith, S. R. (2005) Pioglitazone induces mitochondrial biogenesis in human subcutaneous adipose tissue in vivo. Diabetes 54, 1392-1399
40. Wilson-Fritch, L., Nicoloro, S., Chouinard, M., Lazar, M. A., Chui, P. C., Leszyk, J., Straubhaar, J., Czech, M. P., and Corvera, S. (2004) Mitochon-drial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone. J. Clin. Invest. 114, 1281-1289
41. Kramar, R. (1986) The contribution of peroxisomes to lipid metabolism. J. Clin. Chem. Clin. Biochem. 24, 109-118
42. Wanders, R. J., and Waterham, H. R. (2006) Biochemistry of mammalian peroxisomes revisited. Annu. Rev. Biochem. 75, 295-332
43. Nedergaard, J., Alexson, S., and Cannon, B. (1980) Cold adaptation in the rat: increased brown fat peroxisomal-oxidation relative to maximal mitochondrial oxidative capacity. Am. J. Physiol. 239, C208-C216
44. Wanders, R. J., Visser, W. F., van Roermund, C. W., Kemp, S., and Waterham, H. R. (2007) The peroxisomal ABC transporter family. Pflugers Arch. 453, 719-734
45. Bagattin, A., Hugendubler, L., and Mueller, E. (2010) Transcriptional coactivator PGC-1alpha promotes peroxisomal remodeling and biogenesis. Proc. Natl. Acad. Sci. U.S.A. 107, 20376-20381
46. Paton, C. M., Rogowski, M. P., Kozimor, A. L., Stevenson, J. L., Chang, H., and Cooper, J. A. (2013) Lipocalin-2 increases fat oxidation in vitro and is correlated with energy expenditure in normal weight but not obese women. Obesity 21, E640-E648
47. Fernandez-Marcos, P. J., and Auwerx, J. (2011) Regulation of PGC-1alpha, a nodal regulator of mitochondrial biogenesis. Am. J. Clin. Nutr. 93, S884-S890
48. Zhang, Y., Foncea, R., Deis, J. A., Guo, H., Bernlohr, D. A., and Chen, X. (2014) Lipocalin 2 expression and secretion is highly regulated by metabolic stress, cytokines, and nutrients in adipocytes. PLoS One 9, e96997