Ablation of the transcriptional regulator Id1 enhances energy expenditure, increases insulin sensitivity, and protects against age and diet induced insulin resistance, and hepatosteatosis

FASEB Journal

Volumn 26, Issue 1, 2012, Pages 309-323

  Satyanarayana, Ande ^a   Klarmann, Kimberly D ^a   Gavrilova, Oksana ^b   Keller, Jonathan R ^a  

^a SAIC FREDERICK INC   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Adipogenesis; Brown adipose tissue; PGC1a; Thermogenesis; UCP1

Indexed keywords

CHOLESTEROL; INHIBITOR OF DIFFERENTIATION 1; LEPTIN; TRIACYLGLYCEROL; UNCOUPLING PROTEIN 1;

ABLATION THERAPY; ADIPOCYTE; ADIPOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; CELL METABOLISM; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIET; ENERGY EXPENDITURE; FATTY ACID OXIDATION; FATTY LIVER; HOMEOSTASIS AND REGULATION; HORMONE BLOOD LEVEL; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPOLYSIS; LUNG GAS EXCHANGE; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; THERMOGENESIS; TRANSCRIPTION REGULATION; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION; WHITE ADIPOSE TISSUE;

ADIPOCYTES; ADIPOGENESIS; ADIPOSE TISSUE, BROWN; ADIPOSE TISSUE, WHITE; AGING; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; ENERGY METABOLISM; FATTY ACIDS; FATTY LIVER; FEMALE; FIBROBLASTS; INHIBITOR OF DIFFERENTIATION PROTEIN 1; INSULIN RESISTANCE; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; OXIDATION-REDUCTION; PREGNANCY; THERMOGENESIS;

ANIMALIA; MUS;

EID: 84855414794     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-190892     Document Type: Article

References (75)

1. Spiegelman, B. M., and Flier, J. S. (1996) Adipogenesis and obesity: rounding out the big picture. Cell 87, 377-389 (Pubitemid 26374313)
2. Klaus, S. (1997) Functional differentiation of white and brown adipocytes. Bioessays 19, 215-223
3. Galic, S., Oakhill, J. S., and Steinberg, G. R. (2010) Adipose tissue as an endocrine organ. Mol. Cell. Endocrinol. 316, 129-139
4. Kajimura, S., Seale, P., and Spiegelman, B. M. (2010) Transcriptional control of brown fat development. Cell. Metab. 11, 257-262
5. Ricquier, D. (2005) Respiration uncoupling and metabolism in the control of energy expenditure. Proc. Nutr. Soc. 64, 47-52
6. Argyropoulos, G., and Harper, M. E. (2002) Uncoupling proteins and thermoregulation. J. Appl. Physiol. 92, 2187-2198
7. De Ferranti, S., and Mozaffarian, D. (2008) The perfect storm: obesity, adipocyte dysfunction, and metabolic consequences. Clin. Chem. 54, 945-955 (Pubitemid 351793400)
8. Fajas, L., Fruchart, J. C., and Auwerx, J. (1998) Transcriptional control of adipogenesis. Curr. Opin. Cell Biol. 10, 165-173 (Pubitemid 28174758)
9. Kim, J. B., and Spiegelman, B. M. (1996) ADD1/SREBP1 promotes adipocyte differentiation and gene expression linked to fatty acid metabolism. Genes Dev. 10, 1096-1107 (Pubitemid 26152851)
10. Rosen, E. D., Sarraf, P., Troy, A. E., Bradwin, G., Moore, K., Milstone, D. S., Spiegelman, B. M., and Mortensen, R. M. (1999) PPAR gamma is required for the differentiation of adipose tissue in vivo and in vitro. Mol. Cell 4, 611-617 (Pubitemid 29531140)
11. Schroeder-Gloeckler, J. M., Rahman, S. M., Janssen, R. C., Qiao, L., Shao, J., Roper, M., Fischer, S. J., Lowe, E., Orlicky, D. J., McManaman, J. L., Palmer, C., Gitomer, W. L., Huang, W., O'Doherty, R. M., Becker, T. C., Klemm, D. J., Jensen, D. R., Pulawa, L. K., Eckel, R. H., and Friedman, J. E. (2007) CCAAT/enhancer-binding protein beta deletion reduces adiposity, hepatic steatosis, and diabetes in Lepr(db/db) mice. J. Biol. Chem. 282, 15717-15729 (Pubitemid 47093283)
12. Shimomura, I., Hammer, R. E., Richardson, J. A., Ikemoto, S., Bashmakov, Y., Goldstein, J. L., and Brown, M. S. (1998) Insulin resistance and diabetes mellitus in transgenic mice expressing nuclear SREBP-1c in adipose tissue: model for congenital generalized lipodystrophy. Genes Dev. 12, 3182-3194 (Pubitemid 28496263)
13. Wang, N. D., Finegold, M. J., Bradley, A., Ou, C. N., Abdelsayed, S. V., Wilde, M. D., Taylor, L. R., Wilson, D. R., and Darlington, G. J. (1995) Impaired energy homeostasis in C/EBP alpha knockout mice. Science 269, 1108-1112
14. Chiang, S. H., Bazuine, M., Lumeng, C. N., Geletka, L. M., Mowers, J., White, N. M., Ma, J. T., Zhou, J., Qi, N., Westcott, D., Delproposto, J. B., Blackwell, T. S., Yull, F. E., and Saltiel, A. R. (2009) The protein kinase IKKepsilon regulates energy balance in obese mice. Cell 138, 961-975
15. Feige, J. N., and Auwerx, J. (2007) Transcriptional coregulators in the control of energy homeostasis. Trends Cell Biol. 17, 292-301 (Pubitemid 46829846)
16. Lin, J., Wu, P. H., Tarr, P. T., Lindenberg, K. S., St-Pierre, J., Zhang, C. Y., Mootha, V. K., Jager, S., Vianna, C. R., Reznick, R. M., Cui, L., Manieri, M., Donovan, M. X., Wu, Z., Cooper, M. P., Fan, M. C., Rohas, L. M., Zavacki, A. M., Cinti, S., Shulman, G. I., Lowell, B. B., Krainc, D., and Spiegelman, B. M. (2004) Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell 119, 121-135 (Pubitemid 39349325)
17. Picard, F., Gehin, M., Annicotte, J., Rocchi, S., Champy, M. F., O'Malley, B. W., Chambon, P., and Auwerx, J. (2002) SRC-1 and TIF2 control energy balance between white and brown adipose tissues. Cell 111, 931-941 (Pubitemid 36044686)
18. Zhou, Z., Yon Toh, S., Chen, Z., Guo, K., Ng, C. P., Ponniah, S., Lin, S. C., Hong, W., and Li, P. (2003) Cidea-deficient mice have lean phenotype and are resistant to obesity. Nat. Genet. 35, 49-56 (Pubitemid 37048595)
19. Benezra, R., Rafii, S., and Lyden, D. (2001) The Id proteins and angiogenesis. Oncogene 20, 8334-8341 (Pubitemid 34121904)
20. Lasorella, A., Uo, T., and Iavarone, A. (2001) Id proteins at the cross-road of development and cancer. Oncogene 20, 8326-8333 (Pubitemid 34121903)
21. Chen, M., Wang, J., Dickerson, K. E., Kelleher, J., Xie, T., Gupta, D., Lai, E. W., Pacak, K., Gavrilova, O., and Weinstein, L. S. (2009) Central nervous system imprinting of the G protein G(s) alpha and its role in metabolic regulation. Cell Metab. 9, 548-555
22. Sordella, R., Jiang, W., Chen, G. C., Curto, M., and Settleman, J. (2003) Modulation of Rho GTPase signaling regulates a switch between adipogenesis and myogenesis. Cell 113, 147-158 (Pubitemid 36514967)
23. Suh, H. C., Leeanansaksiri, W., Ji, M., Klarmann, K. D., Renn, K., Gooya, J., Smith, D., McNiece, I., Lugthart, S., Valk, P. J., Delwel, R., and Keller, J. R. (2008) Id1 immortalizes hematopoietic progenitors in vitro and promotes a myeloproliferative disease in vivo. Oncogene 27, 5612-5623
24. Bligh, E. G., and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917
25. Chen, M., Chen, H., Nguyen, A., Gupta, D., Wang, J., Lai, E. W., Pacak, K., Gavrilova, O., Quon, M. J., and Weinstein, L. S. (2010) G(s) alpha deficiency in adipose tissue leads to a lean phenotype with divergent effects on cold tolerance and diet-induced thermogenesis. Cell Metab. 11, 320-330
26. Kajimura, S., Seale, P., Tomaru, T., Erdjument-Bromage, H., Cooper, M. P., Ruas, J. L., Chin, S., Tempst, P., Lazar, M. A., and Spiegelman, B. M. (2008) Regulation of the brown and white fat gene programs through a PRDM16/CtBP transcriptional complex. Genes Dev. 22, 1397-1409 (Pubitemid 351717529)
27. Zhong, L., D'Urso, A., Toiber, D., Sebastian, C., Henry, R. E., Vadysirisack, D. D., Guimaraes, A., Marinelli, B., Wikstrom, J. D., Nir, T., Clish, C. B., Vaitheesvaran, B., Iliopoulos, O., Kurland, I., Dor, Y., Weissleder, R., Shirihai, O. S., Ellisen, L. W., Espinosa, J. M., and Mostoslavsky, R. (2010) The histone deacetylase Sirt6 regulates glucose homeostasis via Hif1alpha. Cell 140, 280-293
28. Gautam, D., Gavrilova, O., Jeon, J., Pack, S., Jou, W., Cui, Y., Li, J. H., and Wess, J. (2006) Beneficial metabolic effects of M3 muscarinic acetylcholine receptor deficiency. Cell Metab. 4, 363-375 (Pubitemid 44645070)
29. Heron-Milhavet, L., Haluzik, M., Yakar, S., Gavrilova, O., Pack, S., Jou, W. C., Ibrahimi, A., Kim, H., Hunt, D., Yau, D., Asghar, Z., Joseph, J., Wheeler, M. B., Abumrad, N. A., and LeRoith, D. (2004) Muscle-specific overexpression of CD36 reverses the insulin resistance and diabetes of MKR mice. Endocrinology 145, 4667-4676 (Pubitemid 39281460)
30. Sun, L., Trausch-Azar, J. S., Muglia, L. J., and Schwartz, A. L. (2008) Glucocorticoids differentially regulate degradation of MyoD and Id1 by N-terminal ubiquitination to promote muscle protein catabolism. Proc. Natl. Acad. Sci. U. S. A. 105, 3339-3344 (Pubitemid 351723554)
31. Cederberg, A., Gronning, L. M., Ahren, B., Tasken, K., Carlsson, P., and Enerback, S. (2001) FOXC2 is a winged helix gene that counteracts obesity, hypertriglyceridemia, and diet-induced insulin resistance. Cell 106, 563-573 (Pubitemid 32879318)
32. Chiu, C. H., Lin, W. D., Huang, S. Y., and Lee, Y. H. (2004) Effect of a C/EBP gene replacement on mitochondrial biogenesis in fat cells. Genes Dev. 18, 1970-1975
33. Hansen, J. B., and Kristiansen, K. (2006) Regulatory circuits controlling white versus brown adipocyte differentiation. Biochem. J. 398, 153-168 (Pubitemid 44338472)
34. Scime, A., Grenier, G., Huh, M. S., Gillespie, M. A., Bevilacqua, L., Harper, M. E., and Rudnicki, M. A. (2005) Rb and p107 regulate preadipocyte differentiation into white versus brown fat through repression of PGC-1alpha. Cell. Metab. 2, 283-295
35. Florez-Duquet, M., and McDonald, R. B. (1998) Cold-induced thermoregulation and biological aging. Physiol. Rev. 78, 339-358 (Pubitemid 28182897)
36. Szekely, M., Petervari, E., and Balasko, M. (2010) Thermoregulation, energy balance, regulatory peptides: recent developments. Front. Biosci. 2, 1009-1046
37. Butler, A. A. (2006) The melanocortin system and energy balance. Peptides. 27, 281-290
38. Iwen, K. A., Senyaman, O., Schwartz, A., Drenckhan, M., Meier, B., Hadaschik, D., and Klein, J. (2008) Melanocortin crosstalk with adipose functions: ACTH directly induces insulin resistance, promotes a pro-inflammatory adipokine profile and stimulates UCP-1 in adipocytes. J. Endocrinol. 196, 465-472 (Pubitemid 351425502)
39. Verty, A. N., Allen, A. M., and Oldfield, B. J. (2010) The endogenous actions of hypothalamic peptides on brown adipose tissue thermogenesis in the rat. Endocrinology 151, 4236-4246
40. Hurov, J. B., Huang, M., White, L. S., Lennerz, J., Choi, C. S., Cho, Y. R., Kim, H. J., Prior, J. L., Piwnica-Worms, D., Cantley, L. C., Kim, J. K., Shulman, G. I., and Piwnica-Worms, H. (2007) Loss of the Par-1b/MARK2 polarity kinase leads to increased metabolic rate, decreased adiposity, and insulin hypersensitivity in vivo. Proc. Natl. Acad. Sci. U. S. A. 104, 5680-5685 (Pubitemid 47175740)
41. Lazar, M. A. (2005) How obesity causes diabetes: not a tall tale. Science 307, 373-375
42. Postic, C., and Girard, J. (2008) The role of the lipogenic pathway in the development of hepatic steatosis. Diabetes Metab. 34, 643-648
43. Murad, J. M., Place, C. S., Ran, C., Hekmatyar, S. K., Watson, N. P., Kauppinen, R. A., and Israel, M. A. (2010) Inhibitor of DNA binding 4 (ID4) regulation of adipocyte differentiation and adipose tissue formation in mice. J. Biol. Chem. 285, 24164-24173
44. Park, K. W., Waki, H., Villanueva, C. J., Monticelli, L. A., Hong, C., Kang, S., MacDougald, O. A., Goldrath, A. W., and Tontonoz, P. (2008) Inhibitor of DNA binding 2 is a small molecule-inducible modulator of peroxisome proliferator-activated receptor-gamma expression and adipocyte differentiation. Mol. Endocrinol. 22, 2038-2048
45. Puigserver, P., and Spiegelman, B. M. (2003) Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr. Rev. 24, 78-90 (Pubitemid 36223280)
46. Bluher, M., Michael, M. D., Peroni, O. D., Ueki, K., Carter, N., Kahn, B. B., and Kahn, C. R. (2002) Adipose tissue selective insulin receptor knockout protects against obesity and obesity-related glucose intolerance. Dev. Cell. 3, 25-38 (Pubitemid 34778393)
47. Foley, J. E., Laursen, A. L., Sonne, O., and Gliemann, J. (1980) Insulin binding and hexose transport in rat adipocytes. Relation to cell size. Diabetologia 19, 234-241 (Pubitemid 10003185)
48. Hulver, M. W., and Dohm, G. L. (2004) The molecular mechanism linking muscle fat accumulation to insulin resistance. Proc. Nutr. Soc. 63, 375-380 (Pubitemid 38787493)
49. Langin, D. (2006) Adipose tissue lipolysis as a metabolic pathway to define pharmacological strategies against obesity and the metabolic syndrome. Pharmacol. Res. 53, 482-491
50. Ordovas, J. M., and Schaefer, E. J. (1999) Genes, variation of cholesterol and fat intake and serum lipids. Curr. Opin. Lipidol. 10, 15-22 (Pubitemid 29084104)
51. Gantois, I., Fang, K., Jiang, L., Babovic, D., Lawrence, A. J., Ferreri, V., Teper, Y., Jupp, B., Ziebell, J., Morganti-Kossmann, C. M., O'Brien, T. J., Nally, R., Schutz, G., Waddington, J., Egan, G. F., and Drago, J. (2007) Ablation of D1 dopamine receptor-expressing cells generates mice with seizures, dystonia, hyperactivity, and impaired oral behavior. Proc. Natl. Acad. Sci. U. S. A. 104, 4182-4187 (Pubitemid 47181599)
52. Kim, A., and Park, T. (2010) Diet-induced obesity regulates the galanin-mediated signaling cascade in the adipose tissue of mice. Mol. Nutr. Food. Res. 54, 1361-1370
53. Conarello, S. L., Jiang, G., Mu, J., Li, Z., Woods, J., Zycband, E., Ronan, J., Liu, F., Roy, R. S., Zhu, L., Charron, M. J., and Zhang, B. B. (2007) Glucagon receptor knockout mice are resistant to diet-induced obesity and streptozotocin-mediated beta cell loss and hyperglycaemia. Diabetologia 50, 142-150 (Pubitemid 46035862)
54. List, E. O., Sackmann-Sala, L., Berryman, D. E., Funk, K., Kelder, B., Gosney, E. S., Okada, S., Ding, J., Cruz-Topete, D., and Kopchick, J. J. (2011) Endocrine parameters and phenotypes of the growth hormone receptor gene disrupted (GHR-/-) muse. Endocr. Rev. 32, 356-386
55. Baggio, L. L., and Drucker, D. J. (2002) Harnessing the therapeutic potential of glucagon-like peptide-1: a critical review. Treat. Endocrinol. 1, 117-125 (Pubitemid 36828431)
56. Ye, J. M., Lim-Fraser, M., Cooney, G. J., Cooper, G. J., Iglesias, M. A., Watson, D. G., Choong, B., and Kraegen, E. W. (2001) Evidence that amylin stimulates lipolysis in vivo: a possible mediator of induced insulin resistance. Am. J. Physiol. 280, E562-E569
57. Khan, A. H., and Pessin, J. E. (2002) Insulin regulation of glucose uptake: a complex interplay of intracellular signalling pathways. Diabetologia 45, 1475-1483
58. Kanzaki, M., and Pessin, J. E. (2001) Signal integration and the specificity of insulin action. Cell. Biochem. Biophys. 35, 191-209 (Pubitemid 33622687)
59. Su, P. Y., and Ko, M. C. (2011) The role of central GRP and NMB receptors in the modulation of scratching behavior in rats. J. Pharmacol. Exp. Ther. 337, 822-829
60. Wilding, J. P. (2002) Neuropeptides and appetite control. Diabet. Med. 19, 619-627
61. Evans, R. M., Barish, G. D., and Wang, Y. X. (2004) PPARs and the complex journey to obesity. Nat. Med. 10, 355-361 (Pubitemid 38508511)
62. Puigserver, P. (2005) Tissue-specific regulation of metabolic pathways through the transcriptional coactivator PGC1-alpha. Int. J. Obes. (2005) 29(Suppl. 1), S5-S9
63. Das, U. N. (2010) Obesity: genes, brain, gut, and environment. Nutrition 26, 459-473
64. Tomimoto, S., Ojika, T., Shintani, N., Hashimoto, H., Hamagami, K., Ikeda, K., Nakata, M., Yada, T., Sakurai, Y., Shimada, T., Morita, Y., Ishida, C., and Baba, A. (2008) Markedly reduced white adipose tissue and increased insulin sensitivity in adcyap1-deficient mice. J. Pharmacol. Sci. 107, 41-48 (Pubitemid 351760826)
65. D'Agostino, D., Cordle, R. A., Kullman, J., Erlanson-Albertsson, C., Muglia, L. J., and Lowe, M. E. (2002) Decreased postnatal survival and altered body weight regulation in procolipase-deficient mice. J. Biol. Chem. 277, 7170-7177 (Pubitemid 34953107)
66. Tedesco, L., Valerio, A., Dossena, M., Cardile, A., Ragni, M., Pagano, C., Pagotto, U., Carruba, M. O., Vettor, R., and Nisoli, E. (2010) Cannabinoid receptor stimulation impairs mitochondrial biogenesis in mouse white adipose tissue, muscle, and liver: the role of eNOS, p38 MAPK, and AMPK pathways. Diabetes 59, 2826-2836
67. Guesdon, B., Denis, R. G., and Richard, D. (2010) Additive effects of olanzapine and melanin-concentrating hormone agonism on energy balance. Behav. Brain. Res. 207, 14-20
68. Ohki-Hamazaki, H., Watase, K., Yamamoto, K., Ogura, H., Yamano, M., Yamada, K., Maeno, H., Imaki, J., Kikuyama, S., Wada, E., and Wada, K. (1997) Mice lacking bombesin receptor subtype-3 develop metabolic defects and obesity. Nature 390, 165-169 (Pubitemid 27507984)
69. Wielinga, P. Y., Lowenstein, C., Muff, S., Munz, M., Woods, S. C., and Lutz, T. A. (2010) Central amylin acts as an adiposity signal to control body weight and energy expenditure. Physiol. Behav. 101, 45-52
70. Budhiraja, S., and Chugh, A. (2009) Neuromedin U: physiology, pharmacology and therapeutic potential. Fundam. Clin. Pharmacol. 23, 149-157
71. Fan, W., Voss-Andreae, A., Cao, W. H., and Morrison, S. F. (2005) Regulation of thermogenesis by the central melanocortin system. Peptides 26, 1800-1813 (Pubitemid 41354538)
72. Atrens, D. M., and Menendez, J. A. (1993) Somatostatin and the paraventricular hypothalamus: modulation of energy balance. Brain Res. 630, 238-244 (Pubitemid 23342846)
73. Silva, J. E. (1995) Thyroid hormone control of thermogenesis and energy balance. Thyroid 5, 481-492
74. 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)
75. Jequier, E. (2002) Leptin signaling, adiposity, and energy balance. Ann. N. Y. Acad. Sci. 967, 379-388