MicroRNAs overexpressed in growth-restricted rat skeletal muscles regulate the glucose transport in cell culture targeting central TGF-β factor SMAD4

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Raychaudhuri, Santanu ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; GLUCOSE TRANSPORTER 4; INSULIN; MICRORNA; MICRORNA 23A; MICRORNA 29A; NUCLEOLIN; PROTEIN DNAJ; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; GLUCOSE TRANSPORTER; HEAT SHOCK PROTEIN 40; MADH4 PROTEIN, RAT; MESSENGER RNA; PHOSPHOPROTEIN; RNA BINDING PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL SURVIVAL; CONTROLLED STUDY; EX VIVO STUDY; FEMALE; GENE OVEREXPRESSION; GLUCOSE TRANSPORT; GROWTH INHIBITION; IN VITRO STUDY; MALE; MICROARRAY ANALYSIS; MUSCLE CELL; MUSCLE TISSUE; MYOBLAST; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TARGETING; RAT; REPORTER GENE; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; STARVATION; UPREGULATION; ANIMAL; CULTURE TECHNIQUE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; SPRAGUE DAWLEY RAT; TRANSPORT AT THE CELLULAR LEVEL;

MAMMALIA; RATTUS;

ANIMALS; BIOLOGICAL TRANSPORT; CELL CULTURE TECHNIQUES; GLUCOSE; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; HSP40 HEAT-SHOCK PROTEINS; INSULIN; MALE; MICRORNAS; MUSCLE CELLS; MUSCLE, SKELETAL; MYOBLASTS, SKELETAL; PHOSPHOPROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UP-REGULATION;

EID: 84859565517     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034596     Document Type: Article

References (72)

1. Callis TE, Chen JF, Wang DZ, (2007) DNA Cell Biology DNA Cell Biology 26 (4): 219-25.
2. Williams AH, Liu N, van Rooij E, Olson EN, (2009) MicroRNA control of muscle development and disease. Curr Opin Cell Biol 21 (3): 461-9.
3. Townley-Tilson WH, Callis TE, Wang D, (2010) MicroRNAs 1, 133, and 206: critical factors of skeletal and cardiac muscle development, function, and disease. Int J Biochem Cell Biol 42 (8): 1252-5.
4. Hoffman NJ, Elmendorf JS, (2011) Signaling, cytoskeletal and membrane mechanisms regulating GLUT4 exocytosis. Trends Endocrinol Metab 22 (3): 110-6.
5. Leney SE, Tavaré JM, (2009) The molecular basis of insulin-stimulated glucose uptake: signaling, trafficking and potential drug targets. J Endocrinol 203 (1): 1-18.
6. Chen S, Wasserman DH, MacKintosh C, Sakamoto K, (2011) Peripheral but not hepatic insulin resistance in mice with one disrupted allele of the glucose transporter type 4 (GLUT4) gene. Cell Metab 13 (1): 68-79.
7. Rossetti L, Stenbit AE, Chen W, Hu M, Barzilai N, (1997) Peripheral but not hepatic insulin resistance in mice with one disrupted allele of the glucose transporter type 4 (GLUT4) gene. J Clin Invest 100 (7): 1831-9.
8. Zisman A, Peroni OD, Abel ED, Michael MD, Mauvais-Jarvis F, et al. (2000) Targeted disruption of the glucose transporter 4 selectively in muscle causes insulin resistance and glucose intolerance. Nat Med 6 (8): 924-8.
9. Wallberg-Henriksson H, Zierath JR, (2001) GLUT4: a key player regulating glucose homeostasis? Insights from transgenic and knockout mice. Mol Membr Biol 18 (3): 205-11.
10. Kim JK, Zisman A, Fillmore JJ, Peroni OD, Kotani K, et al. (2001) Adipose-specific overexpression of GLUT4 reverses insulin resistance and diabetes in mice lacking GLUT4 selectively in muscle. J Clin Invest 108 (1): 153-60.
11. Carvalho E, Kotani K, Peroni OD, Kahn BB, (2005) Adipose-specific overexpression of GLUT4 reverses insulin resistance and diabetes in mice lacking GLUT4 selectively in muscle. Am J Physiol Endocrinol Metab 289 (4): E551-61.
12. Karlsson HK, Ahlsén M, Zierath JR, Wallberg-Henriksson H, Koistinen HA, (2006) Insulin signaling and glucose transport in skeletal muscle from first-degree relatives of type 2 diabetic patients. Diabetes 55 (5): 1283-8.
13. Chen JF, Callis TE, Wang DZ, (2009) microRNAs and muscle disorders. J Cell Sci 122 (Pt 1): 13-20.
14. Williams AH, Liu N, van Rooij E, Olson EN, (2009) MicroRNA control of muscle development and disease. Curr Opin Cell Biol 21 (3): 461-9.
15. Wang H, Sun H, Guttridge DC, (2009) MicroRNAs: novel components in a muscle gene regulatory network. Cell Cycle 8 (12): 1833-7.
16. Townley-Tilson WH, Callis TE, Wang D, (2010) MicroRNAs 1, 133, and 206: critical factors of skeletal and cardiac muscle development, function, and disease. Int J Biochem Cell Biol 42 (8): 1252-5.
17. Gallagher IJ, Scheele C, Keller P, Nielsen AR, Remenyi J, et al. (2010) Integration of microRNA changes in vivo identifies novel molecular features of muscle insulin resistance in type 2 diabetes. Genome Med 2 (2): 9.
18. Juan AH, Kumar RM, Marx JG, Young RA, Sartorelli V, (2009) Mir-214-dependent regulation of the polycomb protein Ezh2 in skeletal muscle and embryonic stem cells. Mol Cell 36 (1): 61-74.
19. Cardinali B, Castellani L, Fasanaro P, Basso A, Alemà S, et al. (2009) Microrna-221 and microrna-222 modulate differentiation and maturation of skeletal muscle cells. PLoS One 4 (10): e7607.
20. Poy MN, Eliasson L, Krutzfeldt J, Kuwajima S, Ma X, et al. (2004) A pancreatic islet-specific microRNA regulates insulin secretion. Nature 432 (7014): 226-30.
21. Lynn FC, (2009) Meta-regulation: microRNA regulation of glucose and lipid metabolism. Trends Endocrinol Metab 20 (9): 452-9.
22. Tang X, Muniappan L, Tang G, Ozcan S, (2009) Identification of glucose-regulated miRNAs from pancreatic {beta} cells reveals a role for miR-30d in insulin transcription. RNA 15 (2): 287-93.
23. Michael LF, Wu Z, Cheatham RB, Puigserver P, Adelmant G, et al. (2001) Restoration of insulin-sensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC-1. Proc Natl Acad Sci U S A 98 (7): 3820-5.
24. Thai MV, Guruswamy S, Cao KT, Pessin JE, Olson AL, (1998) Myocyte enhancer factor 2 (MEF2)-binding site is required for GLUT4 gene expression in transgenic mice. Regulation of MEF2 DNA binding activity in insulin-deficient diabetes. J Biol Chem 273 (23): 14285-92.
25. Bogan JS, Kandror KV, (2010) Biogenesis and regulation of insulin-responsive vesicles containing GLUT4. Curr Opin Cell Biol 22 (4): 506-12.
26. Blot V, McGraw TE, (2008) Molecular mechanisms controlling GLUT4 intracellular retention. Mol Biol Cell 19 (8): 3477-87.
27. Varvarigou AA, (2010) Intrauterine growth restriction as a potential risk factor for disease onset in adulthood. J Pediatr Endocrinol Metab 23 (3): 215-24.
28. Gatford KL, Simmons RA, De Blasio MJ, Robinson JS, Owens JA, (2010) Placental programming of postnatal diabetes and impaired insulin action after IUGR Placenta 31: S60-5.
29. Garg M, Thamotharan M, Oak SA, Pan G, Maclaren DC, et al. (2009) Early exercise regimen improves insulin sensitivity in the intrauterine growth-restricted adult female rat offspring. Am J Physiol Endocrinol Metab 296 (2): E272-81.
30. Neitzke U, Harder T, Schellong K, Melchior K, Ziska T, et al. (2008) Intrauterine growth restriction in a rodent model and developmental programming of the metabolic syndrome: a critical appraisal of the experimental evidence. Placenta 29 (3): 246-54.
31. Thamotharan M, Garg M, Oak S, Rogers LM, Pan G, et al. (2007) Transgenerational inheritance of the insulin-resistant phenotype in embryo-transferred intrauterine growth-restricted adult female rat offspring. Am J Physiol Endocrinol Metab 292 (5): E1270-9.
32. Raychaudhuri N, Raychaudhuri S, Thamotharan M, Devaskar SU, (2008) Histone code modifications repress glucose transporter 4 expression in the intrauterine growth-restricted offspring. J Biol Chem 283 (20): 13611-26.
33. Tosh DN, Fu Q, Callaway CW, McKnight RA, McMillen IC, (2010) Epigenetics of programmed obesity: alteration in IUGR rat hepatic IGF1 mRNA expression and histone structure in rapid vs. delayed postnatal catch-up growth. Am J Physiol Gastrointest Liver Physiol 299 (5): G1023-9.
34. Mariman EC, (2008) Epigenetic manifestations in diet-related disorders. J Nutrigenet Nutrigenomics 1 (5): 232-9.
35. Horie T, Ono K, Nishi H, Iwanaga Y, Nagao K, et al. (2009) MicroRNA-133 regulates the expression of GLUT4 by targeting KLF15 and is involved in metabolic control in cardiac myocytes. Biochem Biophys Res Commun 389 (2): 315-20.
36. Lu H, Buchan RJ, Cook SA, (2010) MicroRNA-223 regulates Glut4 expression and cardiomyocyte glucose metabolism. Cardiovasc Res 86 (3): 410-20.
37. He A, Zhu L, Gupta N, Chang Y, Fang F, (2007) Overexpression of micro ribonucleic acid 29, highly up-regulated in diabetic rats, leads to insulin resistance in 3T3-L1 adipocytes. Mol Endocrinol 21 (11): 2785-94.
38. Oak SA, Tran C, Pan G, Thamotharan M, Devaskar SU, (2006) Perturbed skeletal muscle insulin signaling in the adult female intrauterine growth-restricted rat. Am J Physiol Endocrinol Metab 290 (6): E1321-30.
39. Dugani CB, Klip A, (2005) Glucose transporter 4: cycling, compartments and controversies. EMBO Rep 6 (12): 1137-42.
40. Ploug T, Ralston E, (2002) Exploring the whereabouts of GLUT4 in skeletal muscle. Mol Membr Biol 19 (1): 39-49.
41. Buchan JR, Parker R, (2009) Eukaryotic stress granules: the ins and outs of translation. Mol Cell 36 (6): 932-41.
42. Villeneuve LM, Kato M, Reddy MA, Wang M, Lanting L, et al. (2010) Enhanced levels of microRNA-125b in vascular smooth muscle cells of diabetic db/db mice lead to increased inflammatory gene expression by targeting the histone methyltransferase Suv39h1. Diabetes 59 (11): 2904-15.
43. Saccone V, Puri PL, (2010) Epigenetic regulation of skeletal myogenesis. Organogenesis 6 (1): 48-53.
44. Leeper NJ, Raiesdana A, Kojima Y, Chun HJ, Azuma J, et al. (2011) MicroRNA-26a is a novel regulator of vascular smooth muscle cell function. J Cell Physiol 226 (4): 1035-43.
45. Fazi F, Nervi C, (2008) MicroRNA: basic mechanisms and transcriptional regulatory networks for cell fate determination. Cardiovasc Res 79 (4): 553-61.
46. Rowland AF, Fazakerley DJ, James DE, (2011) Mapping Insulin/GLUT4 Circuitry. Traffic doi:10.1111/j.1600-0854.2011.01178.x.
47. Hou R, Liu L, Anees S, Hiroyasu S, Nicholas ES, et al. (2006) The Fat1 cadherin integrates vascular smooth muscle cell growth and migration signals. J Cell Biol 173 (3): 417-429.
48. Ida G, Lunde S, Anton L, Bruusgaard JC, Zaheer A, et al. (2011) Hypoxia inducible factor 1α links fast-patterned muscle activity and fast muscle phenotype in rats. J Physiol 589: 1443-1454.
49. Verleysdonk S, Hirschner W, Wellard J, Rapp M, de los Angeles Garcia M, et al. (2004) Regulation by insulin and insulin-like growth factor of 2-deoxyglucose uptake in primary ependymal cell cultures. Neurochem Res 29 (1): 127-34.
50. Doetsch F, Caillé I, Lim DA, García-Verdugo JM, Alvarez-Buylla A, (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97: 703-716.
51. Lund S, Flyvbjerg A, Holman GD, Larsen FS, Pedersen O, (1994) Comparative effects of IGF-I and insulin on the glucose transporter system in rat muscle. Am J Physiol 267 (3 Pt 1): E461-6.
52. Hardy RW, Gupta KB, McDonald JM, Williford J, Wells A, (1995) Epidermal growth factor (EGF) receptor carboxy-terminal domains are required for EGF-induced glucose transport in transgenic 3T3-L1 adipocytes. Endocrinology 136 (2): 431-9.
53. Salati LM, Adkins-Finke B, Clarke SD, (1988) Free fatty acid inhibition of the insulin induction of glucose-6-phosphate dehydrogenase in rat hepatocyte monolayers. Lipids 23: 36-41.
54. Standaert ML, Galloway L, Karnam P, Bandyopadhyay G, Moscat J, et al. (1997) Insulin Activates Protein Kinases C-ζ and C-λ by an Autophosphorylation-dependent Mechanism and Stimulates Their Translocation to GLUT4 Vesicles and Other Membrane Fractions in Rat Adipocytes J Biol Chem 272: 30075-30082.
55. Li-Zhong L, Hai-Lu Z, Zuo J, Stanley KS, Ho JCN, et al. (2006) Protein Kinase Cζ Mediates Insulin-induced Glucose Transport through Actin Remodeling in L6 Muscle Cells. Mol Biol Cell 17 (5): 2322-2330.
56. Braiman L, Alt A, Kuroki T, Ohba M, Bak A, Tennenbaum T, et al. (2001) Activation of protein kinase C zeta induces serine phosphorylation of VAMP2 in the GLUT4 compartment and increases glucose transport in skeletal muscle. Mol Cell Biol 21 (22): 7852-61.
57. Bornemann A, (1992) Desmin and vimentin in regenerating muscles. Muscle Nerve 15 (1): 14-20.
58. Yumi N, Sabur H, Eiichiro K, Maho Y, Hu M, et al. (2008) Reciprocal interaction with G-actin and tropomyosin is essential for aquaporin-2 trafficking. J Cell Biol 182 (3): 587-601.
59. Zhang J, Tsaprailis G, Bowden GT, (2008) Nucleolin stabilizes Bcl-X L messenger RNA in response to UVA irradiation. Cancer Res 68 (4): 1046-54.
60. Mahoney DJ, Safdar A, Parise G, Melov S, Fu M, et al. (2008) Gene expression profiling in human skeletal muscle during recovery from eccentric exercise. Am J Physiol Regul Integr Comp Physiol 294 (6): R1901-10.
61. Grobet L, Pirottin D, Farnir F, Poncelet D, Royo LJ, et al. (2003) Modulating Skeletal Muscle Mass by Postnatal, Muscle-Specific Inactivation of the Myostatin Gene. genesis 35: 227-238.
62. McPherron AC, Lee S-J, (1997) Double muscling in cattle due to mutations in the myostatin gene. Procedings of National Academy of Science 94 (23): 12457-12461.
63. Schaborta EJ, Merweb M, Loosa B, Moorea FP, Niesler CU, (2009) TGF-β's delay skeletal muscle progenitor cell differentiation in anisoform-independent manner. Experimental Cell Research 315: 373-384.
64. He A, Zhu L, Gupta N, Chang Y, Fang F, (2007) Overexpression of Micro Ribonucleic Acid 29, Highly Up-Regulated in Diabetic Rats, Leads to Insulin Resistance in 3T3-L1 Adipocytes. Molecular Endocrinology 21 (11): 2785-2794.
65. Black BL, Olson EN, (1998) Transcriptional control of muscle development by myocyte enhancer factor (Mef2) proteins. Annu Rev Cell Dev Biol 1998 14: 167-96.
66. Zhao Y, Samal E, Srivastava D, (2005) Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature 436 (7048): 214-20.
67. Huang S, He X, Ding X, Liang L, Zhao Y, (2008) Upregulation of miR-23a/27a/24 decreases transforming growth factor-beta-induced tumor-suppressive activities in human hepatocellular carcinoma cells. International Journal of Cancer 123 (4): 972-978.
68. Hata A, Davis BN, (2009) Control of microRNA biogenesis by TGFbeta signaling pathway-A novel role of Smads in the nucleus. Cytokine Growth Factor Rev 20 (5-6): 517-21.
69. Maurer B, Stanczyk J, Jüngel A, Akhmetshina A, Trenkmann M, et al. (2010) MicroRNA-29, a key regulator of collagen expression in systemic sclerosis. Arthritis Rheum 62 (6): 1733-43.
70. Moustakas A, Heldin C-H, (2005) Non-Smad TGF-β signals. J Cell Science 118: 3573-3584.
71. Mincione G, Esposito DL, Marcantonio MC, Piccirelli A, Cama A, et al. (2003) TGF-beta 1 modulation of IGF-I signaling pathway in rat thyroid epithelial cells. Exp Cell Res 287 (2): 411-23.
72. Song K, Cornelius SC, Reiss M, Danielpour D, (2003) Insulin-like growth factor-I inhibits transcriptional responses of transforming growth factor-beta by phosphatidylinositol 3-kinase/Akt-dependent suppression of the activation of Smad3 but not Smad2. J Biol Chem 278 (40): 38342-51.