SRA regulates adipogenesis by modulating p38/jnk phosphorylation and stimulating insulin receptor gene expression and downstream signaling

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Liu, Shannon ^a   Xu, Ruichuan ^a   Gerin, Isabelle ^a   Cawthorn, William P ^a   MacDougald, Ormond A ^a   Chen, Xiao Wei ^b   Saltiel, Alan R ^a,b   Koenig, Ronald J ^a   Xu, Bin ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEXAMETHASONE; INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR BETA; INSULIN RECEPTOR SUBSTRATE 1; ISOBUTYLMETHYLXANTHINE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE B; SOMATOMEDIN C; STEROID RECEPTOR; STEROID RECEPTOR RNA ACTIVATOR; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; LONG UNTRANSLATED RNA;

3T3 CELL LINE; ADIPOGENESIS; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL LINE; CELL MATURATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; SIGNAL TRANSDUCTION; ST2 CELL LINE; ANIMAL; GENETICS; IMMUNOBLOTTING; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

3T3 CELLS; ADIPOGENESIS; ANIMALS; CELL LINE; HUMANS; IMMUNOBLOTTING; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RECEPTOR, INSULIN; RNA, LONG NONCODING; SIGNAL TRANSDUCTION;

EID: 84899669364     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095416     Document Type: Article

References (49)

1. Rosen ED, Spiegelman BM (2006) Adipocytes as regulators of energy balance and glucose homeostasis. Nature 444: 847-853.
2. Arner P (2005) Resistin: yet another adipokine tells us that men are not mice. Diabetologia 48: 2203-2205.
3. Cristancho AG, Lazar MA (2011) Forming functional fat: a growing understanding of adipocyte differentiation. Nat Rev Mol Cell Biol 12: 722-734.
4. Farmer SR (2006) Transcriptional control of adipocyte formation. Cell Metab 4: 263-273.
5. Rosen ED, MacDougald OA (2006) Adipocyte differentiation from the inside out. Nat Rev Mol Cell Biol 7: 885-896.
6. Siersbaek R, Nielsen R, Mandrup S (2012) Transcriptional networks and chromatin remodeling controlling adipogenesis. Trends Endocrinol Metab 23: 56-64.
7. Birsoy K, Chen Z, Friedman J (2008) Transcriptional regulation of adipogenesis by KLF4. Cell Metab 7: 339-347.
8. Ross SE, Hemati N, Longo KA, Bennett CN, Lucas PC, et al. (2000) Inhibition of adipogenesis by Wnt signaling. Science 289: 950-953.
9. Fajas L, Landsberg RL, Huss-Garcia Y, Sardet C, Lees JA, et al. (2002) E2Fs regulate adipocyte differentiation. Dev Cell 3: 39-49.
10. Ding J, Nagai K, Woo JT (2003) Insulin-dependent adipogenesis in stromal ST2 cells derived from murine bone marrow. Biosci Biotechnol Biochem 67: 314-321.
11. Green H, Kehinde O (1975) An established preadipose cell line and its differentiation in culture. II. Factors affecting the adipose conversion. Cell 5: 19-27
12. Bost F, Aouadi M, Caron L, Binetruy B (2005) The role of MAPKs in adipocyte differentiation and obesity. Biochimie 87: 51-56.
13. Miki H, Yamauchi T, Suzuki R, Komeda K, Tsuchida A, et al. (2001) Essential role of insulin receptor substrate 1 (IRS-1) and IRS-2 in adipocyte differentiation. Mol Cell Biol 21: 2521-2532.
14. Tseng YH, Kriauciunas KM, Kokkotou E, Kahn CR (2004) Differential roles of insulin receptor substrates in brown adipocyte differentiation. Mol Cell Biol 24: 1918-1929.
15. Garofalo RS, Orena SJ, Rafidi K, Torchia AJ, Stock JL, et al. (2003) Severe diabetes, age-dependent loss of adipose tissue, and mild growth deficiency in mice lacking Akt2/PKB beta. J Clin Invest 112: 197-208.
16. Peng XD, Xu PZ, Chen ML, Hahn-Windgassen A, Skeen J, et al. (2003) Dwarfism, impaired skin development, skeletal muscle atrophy, delayed bone development, and impeded adipogenesis in mice lacking Akt1 and Akt2. Genes Dev 17: 1352-1365.
17. Zhang HH, Huang J, Duvel K, Boback B, Wu S, et al. (2009) Insulin stimulates adipogenesis through the Akt-TSC2-mTORC1 pathway. PLoS ONE 4: e6189.
18. Youngren JF (2007) Regulation of insulin receptor function. Cell Mol Life Sci 64: 873-891.
19. Saltiel AR, Kahn CR (2001) Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414: 799-806.
20. Taniguchi CM, Emanuelli B, Kahn CR (2006) Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol 7: 85-96.
21. Kahn CR (1980) Role of insulin receptors in insulin-resistant states. Metabolism 29: 455-466.
22. Harrison LC, Martin FI, Melick RA (1976) Correlation between insulin receptor binding in isolated fat cells and insulin sensitivity in obese human subjects. J Clin Invest 58: 1435-1441.
23. Crettaz M, Jeanrenaud B (1980) Postreceptor alterations in the states of insulin resistance. Metabolism 29: 467-473.
24. Lanz RB, McKenna NJ, Onate SA, Albrecht U, Wong J, et al. (1999) A steroid receptor coactivator, SRA, functions as an RNA and is present in an SRC-1 complex. Cell 97: 17-27.
25. Caretti G, Schiltz RL, Dilworth FJ, Di Padova M, Zhao P, et al. (2006) The RNA helicases p68/p72 and the noncoding RNA SRA are coregulators of MyoD and skeletal muscle differentiation. Dev Cell 11: 547-560.
26. Xu B, Koenig RJ (2004) An RNA-binding domain in the thyroid hormone receptor enhances transcriptional activation. J Biol Chem 279: 33051-33056.
27. Xu B, Yang WH, Gerin I, Hu CD, Hammer GD, et al. (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.
28. Zhao X, Patton JR, Davis SL, Florence B, Ames SJ, et al. (2004) Regulation of nuclear receptor activity by a pseudouridine synthase through posttranscriptional modification of steroid receptor RNA activator. Mol Cell 15: 549-558.
29. Xu B, Gerin I, Miao H, Vu-Phan D, Johnson CN, et al. (2010) Multiple Roles for the Non-Coding RNA SRA in Regulation of Adipogenesis and Insulin Sensitivity. PLoS ONE 5: e14199.
30. Emberley E, Huang GJ, Hamedani MK, Czosnek A, Ali D, et al. (2003) Identification of new human coding steroid receptor RNA activator isoforms. Biochem Biophys Res Commun 301: 509-515.
31. Kawashima H, Takano H, Sugita S, Takahara Y, Sugimura K, et al. (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.
32. Kang S, Bennett CN, Gerin I, Rapp LA, Hankenson KD, et al. (2007) Wnt signaling stimulates osteoblastogenesis of mesenchymal precursors by suppressing CCAAT/enhancer-binding protein alpha and peroxisome proliferatoractivated receptor gamma. J Biol Chem 282: 14515-14524.
33. Chooniedass-Kothari S, Emberley E, Hamedani MK, Troup S, Wang X, et al. (2004) The steroid receptor RNA activator is the first functional RNA encoding a protein. FEBS Lett 566: 43-47.
34. Lanz RB, Razani B, Goldberg AD, O'Malley BW (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.
35. Singh R, De Aguiar RB, Naik S, Mani S, Ostadsharif K, et al. (2013) LRP6 Enhances Glucose Metabolism by Promoting TCF7L2-Dependent Insulin Receptor Expression and IGF Receptor Stabilization in Humans. Cell Metab 17: 197-209.
36. Kletzien RF, Clarke SD, Ulrich RG (1992) Enhancement of adipocyte differentiation by an insulin-sensitizing agent. Mol Pharmacol 41: 393-398.
37. Li Y, Lazar MA (2002) Differential gene regulation by PPARgamma agonist and constitutively active PPARgamma2. Mol Endocrinol 16: 1040-1048.
38. Aouadi M, Laurent K, Prot M, Le Marchand-Brustel Y, Binetruy B, et al. (2006) Inhibition of p38MAPK increases adipogenesis from embryonic to adult stages. Diabetes 55: 281-289.
39. Benito M, Porras A, Nebreda AR, Santos E (1991) Differentiation of 3T3-L1 fibroblasts to adipocytes induced by transfection of ras oncogenes. Science 253: 565-568.
40. Hirosumi J, Tuncman G, Chang L, Gorgun CZ, Uysal KT, et al. (2002) A central role for JNK in obesity and insulin resistance. Nature 420: 333-336.
41. Sale EM, Atkinson PG, Sale GJ (1995) Requirement of MAP kinase for differentiation of fibroblasts to adipocytes, for insulin activation of p90 S6 kinase and for insulin or serum stimulation of DNA synthesis. Embo J 14: 674-684.
42. Gupta S, Barrett T, Whitmarsh AJ, Cavanagh J, Sluss HK, et al. (1996) Selective interaction of JNK protein kinase isoforms with transcription factors. Embo J 15: 2760-2770.
43. Wiltshire C, Matsushita M, Tsukada S, Gillespie DA, May GH (2002) A new c-Jun N-terminal kinase (JNK)-interacting protein, Sab (SH3BP5), associates with mitochondria. Biochem J 367: 577-585.
44. Choo MK, Kawasaki N, Singhirunnusorn P, Koizumi K, Sato S, et al. (2006) Blockade of transforming growth factor-beta-activated kinase 1 activity enhances TRAIL-induced apoptosis through activation of a caspase cascade. Mol Cancer Ther 5: 2970-2976.
45. Nguyen MT, Satoh H, Favelyukis S, Babendure JL, Imamura T, et al. (2005) JNK and tumor necrosis factor-alpha mediate free fatty acid-induced insulin resistance in 3T3-L1 adipocytes. J Biol Chem 280: 35361-35371.
46. Aguirre V, Uchida T, Yenush L, Davis R, White MF (2000) The c-Jun NH(2)-terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser(307). J Biol Chem 275: 9047-9054.
47. Hube F, Velasco G, Rollin J, Furling D, Francastel C (2011) Steroid receptor RNA activator protein binds to and counteracts SRA RNA-mediated activation of MyoD and muscle differentiation. Nucleic Acids Res 39: 513-525.
48. Lanz RB, Chua SS, Barron N, Soder BM, DeMayo F, et al. (2003) Steroid receptor RNA activator stimulates proliferation as well as apoptosis in vivo. Mol Cell Biol 23: 7163-7176.
49. Yan Y, Skliris GP, Penner C, Chooniedass-Kothari S, Cooper C, et al. (2009) Steroid Receptor RNA Activator Protein (SRAP): a potential new prognostic marker for estrogen receptor-positive/node-negative/younger breast cancer patients. Breast Cancer Res 11: R67.