SRA gene knockout protects against diet-induced obesity and improves glucose tolerance

Journal of Biological Chemistry

Volumn 289, Issue 19, 2014, Pages 13000-13009

  Liu, Shannon ^a   Sheng, Liang ^a,c   Miao, Hongzhi ^a   Saunders, Thomas L ^b   Macdougal, Ormond A ^a   Koenig, Ronald J ^a   Xu, Bin ^a,d  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c NANJING MEDICAL UNIVERSITY   (China)

^d Division of Molecular Medicine and Genetics Transgenic Animal Model Core University of Michigan Medical Center ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE EXPRESSION; GLUCOSE; INSULIN; MAMMALS; MEDICAL PROBLEMS; MOLECULAR WEIGHT; NUTRITION; RNA; TISSUE;

ADIPOCYTE DIFFERENTIATION; ADIPOSE TISSUE; DIET-INDUCED OBESITY; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE; NON-CODING RNAS; STEROID RECEPTORS; TRANSCRIPTIONAL CO-ACTIVATORS;

TISSUE HOMEOSTASIS;

GLUCOSE; INSULIN; TUMOR NECROSIS FACTOR ALPHA;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FAT MASS; FEMALE; GENE FUNCTION; GENE INACTIVATION; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE; IN VIVO STUDY; INSULIN SENSITIVITY; LIPID DIET; LIPOGENESIS; MALE; MARKER GENE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OBESITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SRA1 GENE;

ADIPOCYTE; GENE EXPRESSION; GENE KNOCKOUT; OBESITY; RNA;

ADIPOCYTES; ADIPOSE TISSUE; ANIMALS; BLOOD GLUCOSE; DIETARY FATS; HOMEOSTASIS; MICE; MICE, KNOCKOUT; OBESITY; RNA, LONG NONCODING; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84900430009     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.564658     Document Type: Article

References (53)

1. Gesta, S., Tseng, Y. H., and Kahn, C. R. (2007) Developmental origin of fat: tracking obesity to its source. Cell 131, 242-256
2. Doria, A., Patti, M. E., and Kahn, C. R. (2008) The emerging genetic architecture of type 2 diabetes. Cell Metab. 8, 186-200
3. Olefsky, J. M., and Glass, C. K. (2010) Macrophages, inflammation, and insulin resistance. Annu. Rev. Physiol. 72, 219-246
4. Barak, Y., Nelson, M. C., Ong, E. S., Jones, Y. Z., Ruiz-Lozano, P., Chien, K. R., Koder, A., and Evans, R. M. (1999) PPARγ is required for placental, cardiac, and adipose tissue development. Mol. Cell 4, 585-595
5. Farmer, S. R. (2006) Transcriptional control of adipocyte formation. Cell Metab. 4, 263-273
6. Linhart, H. G., Ishimura-Oka, K., De Mayo, F., Kibe, T., Repka, D., Poindexter, B., Bick, R. J., and Darlington, G. J. (2001) C/EBPα is required for differentiation of white, but not brown, adipose tissue. Proc. Natl. Acad. Sci. U. S. A. 98, 12532-12537
7. Siersbćk, R., Nielsen, R., John, S., Sung, M. H., Baek, S., Loft, A., Hager, G. L., and Mandrup, S. (2011) Extensive chromatin remodelling and establishment of transcription factor "hotspots" during early adipogenesis. EMBO J. 30, 1459-1472
8. Steger, D. J., Grant, G. R., Schupp, M., Tomaru, T., Lefterova, M. I., Schug, J., Manduchi, E., Stoeckert, C. J., Jr., and Lazar, M. A. (2010) Propagation of adipogenic signals through an epigenomic transition state. Genes Dev. 24, 1035-1044
9. Lowe, C. E., O'Rahilly, S., and Rochford, J. J. (2011) Adipogenesis at a glance. J. Cell Sci. 124, 2681-2686
10. Cristancho, A. G., and Lazar, M. A. (2011) Forming functional fat: a growing understanding of adipocyte differentiation. Nat. Rev. Mol. Cell Biol. 12, 722-734
11. Rosen, E. D., and MacDougald, O. A. (2006) Adipocyte differentiation from the inside out. Nat. Rev. Mol. Cell Biol. 7, 885-896
12. Rinn, J. L., and Chang, H. Y. (2012) Genome regulation by long noncoding RNAs. Annu. Rev. Biochem. 81, 145-166
13. Wang, X., Song, X., Glass, C. K., and Rosenfeld, M. G. (2011) The long arm of long noncoding RNAs: roles as sensors regulating gene transcriptional programs. Cold Spring Harbor Perspect. Biol. 3, a003756
14. Lanz, R. B., McKenna, N. J., Onate, S. A., Albrecht, U., Wong, J., Tsai, S. Y., Tsai, M. J., and O'Malley, B. W. (1999) A steroid receptor coactivator, SRA, functions as an RNA and is present in an SRC-1 complex. Cell 97, 17-27
15. Xu, B., and Koenig, R. J. (2004) An RNA-binding domain in the thyroid hormone receptor enhances transcriptional activation. J. Biol. Chem. 279, 33051-33056
16. Zhao, X., Patton, J. R., Davis, S. L., Florence, B., Ames, S. J., and Spanjaard, R. A. (2004) Regulation of nuclear receptor activity by a pseudouridine synthase through posttranscriptional modification of steroid receptor RNA activator. Mol. Cell 15, 549-558
17. Caretti, G., Schiltz, R. L., Dilworth, F. J., Di Padova, M., Zhao, P., Ogryzko, V., Fuller-Pace, F. V., Hoffman, E. P., Tapscott, S. J., and Sartorelli, V. (2006) The RNA helicases p68/p72 and the noncoding RNA SRA are coregulators of MyoD and skeletal muscle differentiation. Dev. Cell 11, 547-560
18. Emberley, E., Huang, G. J., Hamedani, M. K., Czosnek, A., Ali, D., Grolla, A., Lu, B., Watson, P. H., Murphy, L. C., and Leygue, E. (2003) Identification of new human coding steroid receptor RNA activator isoforms. Biochem. Biophys. Res. Commun. 301, 509-515
19. Kawashima, H., Takano, H., Sugita, S., Takahara, Y., Sugimura, K., and Nakatani, T. (2003) A novel steroid receptor co-Activator protein (SRAP) as an alternative form of steroid receptor RNA-Activator gene: expression in prostate cancer cells and enhancement of androgen receptor activity. Biochem. J. 369, 163-171
20. Hubé, F., Velasco, G., Rollin, J., Furling, D., and Francastel, C. (2011) Steroid receptor RNA activator protein binds to and counteracts SRA RNAmediated activation of MyoD and muscle differentiation. Nucleic Acids Res. 39, 513-525
21. Xu, B., Yang, W. H., Gerin, I., Hu, C. D., Hammer, G. D., and Koenig, R. J. (2009) Dax-1 and steroid receptor RNA activator (SRA) function as transcriptional coactivators for steroidogenic factor 1 in steroidogenesis. Mol. Cell. Biol. 29, 1719-1734
22. Lanz, R. B., Razani, B., Goldberg, A. D., and O'Malley, B. W. (2002) Distinct RNA motifs are important for coactivation of steroid hormone receptors by steroid receptor RNA activator (SRA). Proc. Natl. Acad. Sci. U. S. A. 99, 16081-16086
23. Leygue, E., Dotzlaw, H., Watson, P. H., and Murphy, L. C. (1999) Expression of the steroid receptor RNA activator in human breast tumors. Cancer Res. 59, 4190-4193
24. Murphy, L. C., Simon, S. L., Parkes, A., Leygue, E., Dotzlaw, H., Snell, L., Troup, S., Adeyinka, A., and Watson, P. H. (2000) Altered expression of estrogen receptor coregulators during human breast tumorigenesis. Cancer Res. 60, 6266-6271
25. Friedrichs, F., Zugck, C., Rauch, G. J., Ivandic, B., Weichenhan, D., Müller-Bardorff, M., Meder, B., El Mokhtari, N. E., Regitz-Zagrosek, V., Hetzer, R., Schäfer, A., Schreiber, S., Chen, J., Neuhaus, I., Ji, R., Siemers, N. O., Frey, N., Rottbauer, W., Katus, H. A., and Stoll, M. (2009) HBEGF, SRA1, and IK: three cosegregating genes as determinants of cardiomyopathy. Genome Res. 19, 395-403
26. Xu, B., Gerin, I., Miao, H., Vu-Phan, D., Johnson, C. N., Xu, R., Chen, X. W., Cawthorn, W. P., MacDougald, O. A., and Koenig, R. J. (2010) Multiple roles for the non-coding RNA SRA in regulation of adipogenesis and insulin sensitivity. PLoS One 5, e14199
27. Even, P. C., and Nadkarni, N. A. (2012) Indirect calorimetry in laboratory mice and rats: principles, practical considerations, interpretation and perspectives. Am. J. Physiol. Regul. Integr. Comp. Physiol. 303, R459-476
28. Du, B., Cawthorn, W. P., Su, A., Doucette, C. R., Yao, Y., Hemati, N., Kampert, S., McCoin, C., Broome, D. T., Rosen, C. J., Yang, G., and Mac-Dougald, O. A. (2013) The transcription factor paired-related homeobox 1 (Prrx1) inhibits adipogenesis by activating transforming growth factor-α (TGFα) signaling. J. Biol. Chem. 288, 3036-3047
29. Skarnes, W. C., Rosen, B., West, A. P., Koutsourakis, M., Bushell, W., Iyer, V., Mujica, A. O., Thomas, M., Harrow, J., Cox, T., Jackson, D., Severin, J., Biggs, P., Fu, J., Nefedov, M., De Jong, P. J., Stewart, A. F., and Bradley, A. (2011) A conditional knockout resource for the genome-wide study of mouse gene function. Nature 474, 337-342
30. Glass, C. K., and Olefsky, J. M. (2012) Inflammation and lipid signaling in the etiology of insulin resistance. Cell Metab. 15, 635-645
31. Coste, A., Louet, J. F., Lagouge, M., Lerin, C., Antal, M. C., Meziane, H., Schoonjans, K., Puigserver, P., O'Malley, B. W., and Auwerx, J. (2008) The genetic ablation of SRC-3 protects against obesity and improves insulin sensitivity by reducing the acetylation of PGC-1α. Proc. Natl. Acad. Sci. U. S. A. 105, 17187-17192
32. Picard, F., Géhin, 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
33. Guerra, C., Koza, R. A., Yamashita, H., Walsh, K., and Kozak, L. P. (1998) Emergence of brown adipocytes in white fat in mice is under genetic control. Effects on body weight and adiposity. J. Clin. Invest. 102, 412-420
34. Petrovic, N., Walden, T. B., Shabalina, I. G., Timmons, J. A., Cannon, B., and Nedergaard, J. (2010) Chronic peroxisome proliferator-Activated receptor γ (PPARγ) activation of epididymally derived white adipocyte cultures reveals a population of thermogenically competent, UCP1-containing adipocytes molecularly distinct from classic brown adipocytes. J. Biol. Chem. 285, 7153-7164
35. Schulz, T. J., Huang, T. L., Tran, T. T., Zhang, H., Townsend, K. L., Shadrach, J. L., Cerletti, M., McDougall, L. E., Giorgadze, N., Tchkonia, T., Schrier, D., Falb, D., Kirkland, J. L., Wagers, A. J., and Tseng, Y. H. (2011) Identification of inducible brown adipocyte progenitors residing in skeletal muscle and white fat. Proc. Natl. Acad. Sci. U. S. A. 108, 143-148
36. Wu, J., Boström, P., Sparks, L. M., Ye, L., Choi, J. H., Giang, A. H., Khandekar, M., Virtanen, K. A., Nuutila, P., Schaart, G., Huang, K., Tu, H., Van Marken Lichtenbelt, W. D., Hoeks, J., Enerbäck, S., Schrauwen, P., and Spiegelman, B. M. (2012) Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150, 366-376
37. Vitali, A., Murano, I., Zingaretti, M. C., Frontini, A., Ricquier, D., and Cinti, S. (2012) The adipose organ of obesity-prone C57BL/6J mice is composed of mixed white and brown adipocytes. J. Lipid Res. 53, 619-629
38. Harms, M., and Seale, P. (2013) Brown and beige fat: development, function and therapeutic potential. Nat. Med. 19, 1252-1263
39. Boström, P., Wu, J., Jedrychowski, M. P., Korde, A., Ye, L., Lo, J. C., Rasbach, K. A., Boström, E. A., Choi, J. H., Long, J. Z., Kajimura, S., Zingaretti, M. C., Vind, B. F., Tu, H., Cinti, S., Højlund, K., Gygi, S. P., and Spiegelman, B. M. (2012) A PGC1-α-dependent myokine that drives brown fat-like development of white fat and thermogenesis. Nature 481, 463-468
40. Whittle, A. J., Carobbio, S., Martins, L., Slawik, M., Hondares, E., Vázquez, M. J., Morgan, D., Csikasz, R. I., Gallego, R., Rodriguez-Cuenca, S., Dale, M., Virtue, S., Villarroya, F., Cannon, B., Rahmouni, K., López, M., and Vidal-Puig, A. (2012) BMP8B increases brown adipose tissue thermogenesis through both central and peripheral actions. Cell 149, 871-885
41. Gburcik, V., Cawthorn, W. P., Nedergaard, J., Timmons, J. A., and Cannon, B. (2012) An essential role for Tbx15 in the differentiation of brown and "brite" but not white adipocytes. Am. J. Physiol. Endocrinol. Metab. 303, E1053-1060
42. Hotamisligil, G. S., Shargill, N. S., and Spiegelman, B. M. (1993) Adipose expression of tumor necrosis factor-α: direct role in obesity-linked insulin resistance. Science 259, 87-91
43. Arner, P. (2005) Resistin: yet another adipokine tells us that men are not mice. Diabetologia 48, 2203-2205
44. Seppälä-Lindroos, A., Vehkavaara, S., Häkkinen, A. M., Goto, T., Westerbacka, J., Sovijärvi, A., Halavaara, J., and Yki-Järvinen, H. (2002) Fat accumulation in the liver is associated with defects in insulin suppression of glucose production and serum free fatty acids independent of obesity in normal men. J. Clin. Endocrinol. Metab. 87, 3023-3028
45. Schmitz, K. M., Mayer, C., Postepska, A., and Grummt, I. (2010) Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev. 24, 2264-2269
46. Martianov, I., Ramadass, A., Serra Barros, A., Chow, N., and Akoulitchev, A. (2007) Repression of the human dihydrofolate reductase gene by a non-coding interfering transcript. Nature 445, 666-670
47. Ishibashi, J., and Seale, P. (2010) Medicine: beige can be slimming. Science 328, 1113-1114
48. Seale, P., Conroe, H. M., Estall, J., Kajimura, S., Frontini, A., Ishibashi, J., Cohen, P., Cinti, S., and Spiegelman, B. M. (2011) Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J. Clin. Invest. 121, 96-105
49. Cypess, A. M., White, A. P., Vernochet, C., Schulz, T. J., Xue, R., Sass, C. A., Huang, T. L., Roberts-Toler, C., Weiner, L. S., Sze, C., Chacko, A. T., Deschamps, L. N., Herder, L. M., Truchan, N., Glasgow, A. L., Holman, A. R., Gavrila, A., Hasselgren, P. O., Mori, M. A., Molla, M., and Tseng, Y. H. (2013) Anatomical localization, gene expression profiling and functional characterization of adult human neck brown fat. Nat. Med. 19, 635-639
50. Lumeng, C. N., and Saltiel, A. R. (2011) Inflammatory links between obesity and metabolic disease. J. Clin. Invest. 121, 2111-2117
51. Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., and Gordon, J. I. (2006) An obesity-Associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027-1031
52. Vijay-Kumar, M., Aitken, J. D., Carvalho, F. A., Cullender, T. C., Mwangi, S., Srinivasan, S., Sitaraman, S. V., Knight, R., Ley, R. E., and Gewirtz, A. T. (2010) Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science 328, 228-231
53. Tschöp, M. H., Speakman, J. R., Arch, J. R., Auwerx, J., Brüning, J. C., Chan, L., Eckel, R. H., Farese, R. V., Jr., Galgani, J. E., Hambly, C., Herman, M. A., Horvath, T. L., Kahn, B. B., Kozma, S. C., Maratos-Flier, E., Müller, T. D., Münzberg, H., Pfluger, P. T., Plum, L., Reitman, M. L., Rahmouni, K., Shulman, G. I., Thomas, G., Kahn, C. R., and Ravussin, E. (2012) Aguide to analysis of mouse energy metabolism. Nat. Methods 9, 57-63