GRK2 contribution to the regulation of energy expenditure and brown fat function

FASEB Journal

Volumn 26, Issue 8, 2012, Pages 3503-3514

  Vila Bedmar, Rocio ^a,b,c,d   Garcia Guerra, Lucia ^a,e   Nieto Vazquez, Iria ^a   Mayor, Federico ^b,c,d   Lorenzo, Margarita ^a   Murga, Cristina ^b,c,d   Fernández Veledo, Sonia ^a,f  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b CSIC   (Spain)

^c CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^d Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas   (Spain)

^e CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^f HOSPITAL UNIVERSITARI JOAN XXIII   (Spain)

Author keywords

Brown adipose tissue; Cold exposure; Obesity; Thermogenesis

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ADENYLATE KINASE; BETA ACTIN; CARNITINE PALMITOYLTRANSFERASE I; CCAAT ENHANCER BINDING PROTEIN ALPHA; FATTY ACID; FATTY ACID SYNTHASE; G PROTEIN COUPLED RECEPTOR KINASE 2; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PERILIPIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN COXIV; PROTEIN P2; PROTEIN PER A; PROTEIN PER B; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; CELL DIFFERENTIATION; CONTROLLED STUDY; CORE TEMPERATURE; DETERIORATION; DOWN REGULATION; ENERGY BALANCE; ENERGY EXPENDITURE; FATTY ACID OXIDATION; GENE EXPRESSION; HEMIZYGOSITY; LEAN BODY WEIGHT; LIPID METABOLISM; LIPOLYSIS; LUNG GAS EXCHANGE; MALE; METABOLIC REGULATION; MORPHOLOGY; MOUSE; NONHUMAN; OBESITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; THERMOGENESIS; WHITE ADIPOSE TISSUE; WILD TYPE;

MUS;

EID: 84864746050     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-202267     Document Type: Article

References (61)

1. Weiser, M., Frishman, W. H., Michaelson, M. D., and Abdeen, M. A. (1997) The pharmacologic approach to the treatment of obesity. J. Clin. Pharmacol. 37, 453-473 (Pubitemid 27265646)
2. Cannon, B., and Nedergaard, J. (2004) Brown adipose tissue: function and physiological significance. Physiol. Rev. 84, 277-359 (Pubitemid 38054374)
3. Lowell, B. B., and Spiegelman, B. M. (2000) Towards a molecular understanding of adaptive thermogenesis. Nature 404, 652-660 (Pubitemid 30205070)
4. 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 (Pubitemid 47205086)
5. 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
6. Virtanen, K. A., Lidell, M. E., Orava, J., Heglind, M., Westergren, R., Niemi, T., Taittonen, M., Laine, J., Savisto, N. J., Enerback, S., and Nuutila, P. (2009) Functional brown adipose tissue in healthy adults. N. Engl. J. Med. 360, 1518-1525
7. 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
8. Vila-Bedmar, R., and Fernandez-Veledo, S. (2011) A new era for brown adipose tissue: New insights into brown adipocyte function and differentiation. Arch. Physiol. Biochem. 117, 195-208
9. Cannon, B., and Nedergaard, J. (2010) Metabolic consequences of the presence or absence of the thermogenic capacity of brown adipose tissue in mice (and probably in humans). Int. J. Obes. (Lond.) 34(Suppl. 1), S7-S16
10. Nedergaard, J., and Cannon, B. (2010) The changed metabolic world with human brown adipose tissue: therapeutic visions. Cell. Metab. 11, 268-272
11. Sell, H., Deshaies, Y., and Richard, D. (2004) The brown adipocyte: update on its metabolic role. Int. J. Biochem. Cell Biol. 36, 2098-2104 (Pubitemid 39094431)
12. Ribas, C., Penela, P., Murga, C., Salcedo, A., Garcia-Hoz, C., Jurado-Pueyo, M., Aymerich, I., and Mayor, F., Jr. (2007) The G protein-coupled receptor kinase (GRK) interactome: role of GRKs in GPCR regulation and signaling. Biochim. Biophys. Acta 1768, 913-922 (Pubitemid 46452540)
13. Mayor, F., Jr., Lucas, E., Jurado-Pueyo, M., Garcia-Guerra, L., Nieto-Vazquez, I., Vila-Bedmar, R., Fernandez-Veledo, S., and Murga, C. (2011) G Protein-coupled receptor kinase 2 (GRK2): A novel modulator of insulin resistance. Arch. Physiol. Biochem. 117, 125-130
14. Usui, I., Imamura, T., Satoh, H., Huang, J., Babendure, J. L., Hupfeld, C. J., and Olefsky, J. M. (2004) GRK2 is an endogenous protein inhibitor of the insulin signaling pathway for glucose transport stimulation. EMBO J. 23, 2821-2829 (Pubitemid 39013554)
15. Shahid, G., and Hussain, T. (2007) GRK2 negatively regulates glycogen synthesis in mouse liver FL83B cells. J. Biol. Chem. 282, 20612-20620 (Pubitemid 47100045)
16. Cipolletta, E., Campanile, A., Santulli, G., Sanzari, E., Leosco, D., Campiglia, P., Trimarco, B., and Iaccarino, G. (2009) The G protein coupled receptor kinase 2 plays an essential role in beta-adrenergic receptor-induced insulin resistance. Cardiovasc. Res. 84, 407-415
17. Garcia-Guerra, L., Nieto-Vazquez, I., Vila-Bedmar, R., Jurado-Pueyo, M., Zalba, G., Diez, J., Murga, C., Fernandez-Veledo, S., Mayor, F., Jr., and Lorenzo, M. (2010) G protein-coupled receptor kinase 2 plays a relevant role in insulin resistance and obesity. Diabetes 59, 2407-2417
18. Anis, Y., Leshem, O., Reuveni, H., Wexler, I., Ben, S. R., Yahalom, B., Laster, M., Raz, I., Ben, S. S., Shafrir, E., and Ziv, E. (2004) Antidiabetic effect of novel modulating peptides of G-protein-coupled kinase in experimental models of diabetes. Diabetologia 47, 1232-1244 (Pubitemid 39093319)
19. Kopecky, J., Clarke, G., Enerback, S., Spiegelman, B., and Kozak, L. P. (1995) Expression of the mitochondrial uncoupling protein gene from the aP2 gene promoter prevents genetic obesity. J. Clin. Invest. 96, 2914-2923
20. Vila-Bedmar, R., Lorenzo, M., and Fernandez-Veledo, S. (2010) Adenosine 5′-monophosphate-activated protein kinase-mammalian target of rapamycin crosstalk regulates brown adipocyte differentiation. Endocrinology 151, 980-992
21. Barroso, E., Rodriguez-Calvo, R., Serrano-Marco, L., Astudillo, A. M., Balsinde, J., Palomer, X., and Vazquez-Carrera, M. (2011) The PPARβ/δ activator GW501516 prevents the down-regulation of AMPK caused by a high-fat diet in liver and amplifies the PGC-α-lipin 1-PPARα pathway leading to increased fatty acid oxidation. Endocrinology 152, 1848-1859
22. Kolditz, C. I., and Langin, D. (2010) Adipose tissue lipolysis. Curr. Opin. Clin. Nutr. Metab. Care. 13, 377-381
23. Ricquier, D. (2005) Respiration uncoupling and metabolism in the control of energy expenditure. Proc. Nutr. Soc. 64, 47-52
24. McDonald, R. B., and Horwitz, B. A. (1999) Brown adipose tissue thermogenesis during aging and senescence. J. Bioenerg. Biomembr. 31, 507-516 (Pubitemid 30053963)
25. Gray, S. L., Dalla, N. E., Backlund, E. C., Manieri, M., Virtue, S., Noland, R. C., O'Rahilly, S., Cortright, R. N., Cinti, S., Cannon, B., and Vidal-Puig, A. (2006) Decreased brown adipocyte recruitment and thermogenic capacity in mice with impaired peroxisome proliferator-activated receptor (P465L PPARgamma) function. Endocrinology 147, 5708-5714 (Pubitemid 44833487)
26. Golozoubova, V., Hohtola, E., Matthias, A., Jacobsson, A., Cannon, B., and Nedergaard, J. (2001) Only UCP1 can mediate adaptive nonshivering thermogenesis in the cold. FASEB J. 15, 2048-2050
27. Hutchinson, D. S., Chernogubova, E., Dallner, O. S., Cannon, B., and Bengtsson, T. (2005) Beta-adrenoceptors, but not alpha-adrenoceptors, stimulate AMP-activated protein kinase in brown adipocytes independently of uncoupling protein-1. Diabetologia 48, 2386-2395 (Pubitemid 41618931)
28. Mulligan, J. D., Gonzalez, A. A., Stewart, A. M., Carey, H. V., and Saupe, K. W. (2007) Up-regulation of AMPK during cold exposure occurs via distinct mechanisms in brown and white adipose tissue of the mouse. J. Physiol. 580, 677-684 (Pubitemid 46564191)
29. De Jesus, L. A., Carvalho, S. D., Ribeiro, M. O., Schneider, M., Kim, S. W., Harney, J. W., Larsen, P. R., and Bianco, A. C. (2001) The type 2 iodothyronine deiodinase is essential for adaptive thermogenesis in brown adipose tissue. J. Clin. Invest. 108, 1379-1385 (Pubitemid 33107766)
30. Hall, J. A., Ribich, S., Christoffolete, M. A., Simovic, G., Correa-Medina, M., Patti, M. E., and Bianco, A. C. (2010) Absence of thyroid hormone activation during development underlies a permanent defect in adaptive thermogenesis. Endocrinology 151, 4573-4582
31. Carvalho, S. D., Kimura, E. T., Bianco, A. C., and Silva, J. E. (1991) Central role of brown adipose tissue thyroxine 5′-deiodinase on thyroid hormone-dependent thermogenic response to cold. Endocrinology 128, 2149-2159
32. Bianco, A. C., Salvatore, D., Gereben, B., Berry, M. J., and Larsen, P. R. (2002) Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr. Rev. 23, 38-89 (Pubitemid 34185306)
33. Atgie, C., D'Allaire, F., and Bukowiecki, L. J. (1997) Role of beta1- and beta3-adrenoceptors in the regulation of lipolysis and thermogenesis in rat brown adipocytes. Am. J. Physiol. 273, C1136-C1142
34. St-Onge, M. P. (2005) Relationship between body composition changes and changes in physical function and metabolic risk factors in aging. Curr. Opin. Clin. Nutr. Metab. Care 8, 523-528
35. Collins, S., Cao, W., and Robidoux, J. (2004) Learning new tricks from old dogs: beta-adrenergic receptors teach new lessons on firing up adipose tissue metabolism. Mol. Endocrinol. 18, 2123-2131 (Pubitemid 39215245)
36. Tansey, J. T., Sztalryd, C., Gruia-Gray, J., Roush, D. L., Zee, J. V., Gavrilova, O., Reitman, M. L., Deng, C. X., Li, C., Kimmel, A. R., and Londos, C. (2001) Perilipin ablation results in a lean mouse with aberrant adipocyte lipolysis, enhanced leptin production, and resistance to diet-induced obesity. Proc. Natl. Acad. Sci. U. S. A. 98, 6494-6499 (Pubitemid 32488265)
37. Carpentier, A. C. (2008) Postprandial fatty acid metabolism in the development of lipotoxicity and type 2 diabetes. Diabetes Metab. 34, 97-107
38. Collins, S., Yehuda-Shnaidman, E., and Wang, H. (2010) Positive and negative control of Ucp1 gene transcription and the role of β-adrenergic signaling networks. Int. J. Obes. (Lond.) 34(Suppl. 1), S28-S33
39. Florez-Duquet, M., and McDonald, R. B. (1998) Cold-induced thermoregulation and biological aging. Physiol. Rev. 78, 339-358 (Pubitemid 28182897)
40. Valle, A., Guevara, R., Garcia-Palmer, F. J., Roca, P., and Oliver, J. (2008) Caloric restriction retards the age-related decline in mitochondrial function of brown adipose tissue. Rejuvenation Res. 11, 597-604 (Pubitemid 351931469)
41. Petrovic, N., Shabalina, I. G., Timmons, J. A., Cannon, B., and Nedergaard, J. (2008) Thermogenically competent nonadrenergic recruitment in brown preadipocytes by a PPARgamma agonist. Am. J. Physiol. Endocrinol. Metab. 295, E287-E296
42. Villena, J. A., Hock, M. B., Chang, W. Y., Barcas, J. E., Giguere, V., and Kralli, A. (2007) Orphan nuclear receptor estrogenrelated receptor alpha is essential for adaptive thermogenesis. Proc. Natl. Acad. Sci. U. S. A. 104, 1418-1423 (Pubitemid 46184019)
43. Christoffolete, M. A., Linardi, C. C., de Jesus, L., Ebina, K. N., Carvalho, S. D., Ribeiro, M. O., Rabelo, R., Curcio, C., Martins, L., Kimura, E. T., and Bianco, A. C. (2004) Mice with targeted disruption of the Dio2 gene have cold-induced overexpression of the uncoupling protein 1 gene but fail to increase brown adipose tissue lipogenesis and adaptive thermogenesis. Diabetes 53, 577-584 (Pubitemid 38270625)
44. Enerback, S., Jacobsson, A., Simpson, E. M., Guerra, C., Yamashita, H., Harper, M. E., and Kozak, L. P. (1997) Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 387, 90-94 (Pubitemid 27202655)
45. Tabbi-Anneni, I., Cooksey, R., Gunda, V., Liu, S., Mueller, A., Song, G., McClain, D. A., and Wang, L. (2010) Overexpression of nuclear receptor SHP in adipose tissues affects diet-induced obesity and adaptive thermogenesis. Am. J. Physiol. Endocrinol. Metab. 298, E961-E970
46. Qi, J., Gong, J., Zhao, T., Zhao, J., Lam, P., Ye, J., Li, J. Z., Wu, J., Zhou, H. M., and Li, P. (2008) Down-regulation of AMP-activated protein kinase by Cidea-mediated ubiquitination and degradation in brown adipose tissue. EMBO J. 27, 1537-1548 (Pubitemid 351794037)
47. Perwitz, N., Wenzel, J., Wagner, I., Buning, J., Drenckhan, M., Zarse, K., Ristow, M., Lilienthal, W., Lehnert, H., and Klein, J. (2010) Cannabinoid type 1 receptor blockade induces transdifferentiation toward a brown fat phenotype in white adipocytes. Diabetes Obes. Metab. 12, 158-166
48. Hernandez, A., and Obregon, M. J. (1996) Presence and mRNA expression of T3 receptors in differentiating rat brown adipocytes. Mol. Cell. Endocrinol. 121, 37-46 (Pubitemid 26268051)
49. Bianco, A. C., and Silva, J. E. (1987) Optimal response of key enzymes and uncoupling protein to cold in BAT depends on local T3 generation. Am. J. Physiol. 253, E255-E263
50. Silva, J. E., and Bianco, S. D. (2008) Thyroid-adrenergic interactions: physiological and clinical implications. Thyroid 18, 157-165 (Pubitemid 351271529)
51. Sabio, G., Cavanagh-Kyros, J., Barrett, T., Jung, D. Y., Ko, H. J., Ong, H., Morel, C., Mora, A., Reilly, J., Kim, J. K., and Davis, R. J. (2010) Role of the hypothalamic-pituitary-thyroid axis in metabolic regulation by JNK1. Genes Dev. 24, 256-264
52. Haemmerle, G., Lass, A., Zimmermann, R., Gorkiewicz, G., Meyer, C., Rozman, J., Heldmaier, G., Maier, R., Theussl, C., Eder, S., Kratky, D., Wagner, E. F., Klingenspor, M., Hoefler, G., and Zechner, R. (2006) Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science 312, 734-737
53. Lopez, M., Varela, L., Vazquez, M. J., Rodriguez-Cuenca, S., Gonzalez, C. R., Velagapudi, V. R., Morgan, D. A., Schoenmakers, E., Agassandian, K., Lage, R., Martinez de Morentin, P. B., Tovar, S., Nogueiras, R., Carling, D., Lelliott, C., Gallego, R., Oresic, M., Chatterjee, K., Saha, A. K., Rahmouni, K., Dieguez, C., and Vidal-Puig, A. (2010) Hypothalamic AMPK and fatty acid metabolism mediate thyroid regulation of energy balance. Nat. Med. 16, 1001-1008
54. Liggett, S. B., Freedman, N. J., Schwinn, D. A., and Lefkowitz, R. J. (1993) Structural basis for receptor subtype-specific regulation revealed by a chimeric beta 3/beta 2-adrenergic receptor. Proc. Natl. Acad. Sci. U. S. A. 90, 3665-3669 (Pubitemid 23111428)
55. Jimenez-Sainz, M. C., Murga, C., Kavelaars, A., Jurado-Pueyo, M., Krakstad, B. F., Heijnen, C. J., Mayor, F., Jr., and Aragay, A. M. (2006) G protein-coupled receptor kinase 2 negatively regulates chemokine signaling at a level downstream from G protein subunits. Mol. Biol. Cell 17, 25-31 (Pubitemid 43049458)
56. Puigserver, P., Rhee, J., Lin, J., Wu, Z., Yoon, J. C., Zhang, C. Y., Krauss, S., Mootha, V. K., Lowell, B. B., and Spiegelman, B. M. (2001) Cytokine stimulation of energy expenditure through p38 MAP kinase activation of PPARgamma coactivator-1. Mol. Cell 8, 971-982 (Pubitemid 34031800)
57. 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 mitogen-activated 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 (Pubitemid 38381292)
58. Robidoux, J., Cao, W., Quan, H., Daniel, K. W., Moukdar, F., Bai, X., Floering, L. M., and Collins, S. (2005) Selective activation of mitogen-activated protein (MAP) kinase kinase 3 and p38alpha MAP kinase is essential for cyclic AMP-dependent UCP1 expression in adipocytes. Mol. Cell. Biol. 25, 5466-5479 (Pubitemid 40853582)
59. Peregrin, S., Jurado-Pueyo, M., Campos, P. M., Sanz-Moreno, V., Ruiz-Gomez, A., Crespo, P., Mayor, F., Jr., and Murga, C. (2006) Phosphorylation of p38 by GRK2 at the docking groove unveils a novel mechanism for inactivating p38MAPK. Curr. Biol. 16, 2042-2047 (Pubitemid 44604449)
60. Brinks, H., Das, A., and Koch, W. J. (2011) A role for GRK2 in myocardial ischemic injury: indicators of a potential future therapy and diagnostic. Future Cardiol. 7, 547-556
61. Harvey, A. N., Nguyen, K., and Lymperopoulos, A. (2011) GRK2 and beta-arrestins in cardiovascular disease: established and emerging possibilities for therapeutic targeting. [E-pub ahead of print] Curr. Mol. Pharmacol. PMID: 21756224