MiR-135a targets IRS2 and regulates insulin signaling and glucose uptake in the diabetic gastrocnemius skeletal muscle

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 8, 2013, Pages 1294-1303

  Agarwal, Priyanka ^a,c   Srivastava, Rohit ^b   Srivastava, Arvind K ^b   Ali, Shakir ^c   Datta, Malabika ^a  

^a CSIR INSTITUTE OF GENOMICS AND INTEGRATIVE BIOLOGY   (India)

^b CENTRAL DRUG RESEARCH INSTITUTE   (India)

^c HAMDARD UNIVERSITY   (India)

Author keywords

Diabetes; Insulin; IRS2; Microarray; MiR 135a; Skeletal muscle

Indexed keywords

GLUCOSE; INSULIN; LUCIFERASE; MICRORNA; MICRORNA 135A; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE P85 ALPHA; PROTEIN KINASE B; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CELL DIFFERENTIATION; CONTROLLED STUDY; DIABETES MELLITUS; ENZYME ACTIVATION; GASTROCNEMIUS MUSCLE; GENE MUTATION; GENE SILENCING; GLUCOSE TOLERANCE; GLUCOSE TRANSPORT; HYPERGLYCEMIA; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REPORTER GENE; SIGNAL TRANSDUCTION; UPREGULATION;

3' UNTRANSLATED REGIONS; ANIMALS; BINDING SITES; CELL DIFFERENTIATION; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DOWN-REGULATION; GLUCOSE; GLUCOSE TOLERANCE TEST; HEK293 CELLS; HUMANS; HYPERGLYCEMIA; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICRORNAS; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RNA, MESSENGER; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84877345280     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.03.021     Document Type: Article

References (41)

1. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
2. Lee R.C., Feinbaum R.L., Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75:843-854.
3. Zhao C., Sun G., Li S., Lang M.F., Yang S., Li W., Shi Y. MicroRNA let-7b regulates neural stem cell proliferation and differentiation by targeting nuclear receptor TLX signaling. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:1876-1881.
4. Pandey A.K., Agarwal P., Kaur K., Datta M. MicroRNAs in diabetes: tiny players in big disease. Cell. Physiol. Biochem. 2009, 23:221-232.
5. DeFronzo R.A., Tripathy D. Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care 2009, 32(Suppl. 2):S157-S163.
6. Phielix E., Mensink M. Type 2 diabetes mellitus and skeletal muscle metabolic function. Physiol. Behav. 2008, 94:252-258.
7. Carey A.L., Steinberg G.R., Macaulay S.L., Thomas W.G., Holmes A.G., Ramm G., Prelovsek O., Hohnen-Behrens C., Watt M.J., James D.E., Kemp B.E., Pedersen B.K., Febbraio M.A. Interleukin-6 increases insulin-stimulated glucose disposal in humans and glucose uptake and fatty acid oxidation in vitro via AMP-activated protein kinase. Diabetes 2006, 55:2688-2697.
8. DeFronzo R.A., Tripathy D. Pathogenesis of type 2 diabetes mellitus. Diabetes Care 2009, 32(Suppl. 2):S157-S163.
9. Groop L., Forsblom C., Lehtovirta M., Tuomi T., Karanko S., Nissen M., Ehrnstrom B.O., Forsen B., Isomaa B., Snickars B., Taskinen M.R. Metabolic consequences of a family history of NIDDM (the Botnia study): evidence for sex-specific parental effects. Diabetes 1996, 45:1585-1593.
10. Perseghin G., Price T.B., Petersen K.F., Roden M., Cline G.W., Gerow K., Rothman D.L., Shulman G.I. Increased glucose transport-phosphorylation and muscle glycogen synthesis after exercise training in insulin-resistant subjects. N. Engl. J. Med. 1996, 335:1357-1362.
11. Weyer C., Bogardus C., Mott D.M., Pratley R.E. The natural history of insulin secretory dysfunction and insulin resistance in the pathogenesis of type 2 diabetes mellitus. J. Clin. Invest. 1999, 104:787-794.
12. Warram J.H., Martin B.C., Krolewski A.S., Soeldner J.S., Kahn C.R. Slow glucose removal rate and hyperinsulinemia precede the development of type II diabetes in the offspring of diabetic parents. Ann. Intern. Med. 1990, 113:909-915.
13. Petersen K.F., Dufour S., Savage D.B., Bilz S., Solomon G., Yonemitsu S., Cline G.W., Befroy D., Zemany L., Kahn B.B., Papademetris X., Rothman D.L., Shulman G.I. The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:12587-12594.
14. Bouzakri K., Koistinen H.A., Zierath J.R. Molecular mechanisms of skeletal muscle insulin resistance in type 2 diabetes. Curr. Diabetes Rev. 2005, 1:167-174.
15. Gallagher I.J., Scheele C., Keller P., Nielsen A.R., Remenyi J., Fischer C.P., Roder K., Babraj J., Wahlestedt C., Hutvagner G., Pedersen B.K., Timmons J.A. Integration of microRNA changes in vivo identifies novel molecular features of muscle insulin resistance in type 2 diabetes. Genome Med. 2010, 2:9.
16. Huang B., Qin W., Zhao B., Shi Y., Yao C., Li J., Xiao H., Jin Y. MicroRNA expression profiling in diabetic GK rat model. Acta Biochim. Biophys. Sin. (Shanghai) 2009, 41:472-477.
17. Karolina D.S., Armugam A., Tavintharan S., Wong M.T.K., Lim S.C., Sum C.F., Jayaseelan K. MicroRNA 144 impairs insulin signaling by inhibiting the expression of insulin receptor substrate 1 in type 2 diabetes mellitus. PLoS One 2011, 6:e22839.
18. Kaur K., Pandey A.K., Srivastava S., Srivastava A.K., Datta M. Comprehensive miRNome and in silico analyses identify the Wnt signaling pathway to be altered in the diabetic liver. Mol. Biosyst. 2011, 7:3234-3244.
19. McArthur K., Feng B., Wu Y., Chen S., Chakrabarti S. MicroRNA-200b regulates vascular endothelial growth factor-mediated alterations in diabetic retinopathy. Diabetes 2011, 60:1314-1323.
20. Senador D., Kanakamedala K., Irigoyen M.C., Morris M., Elased K.M. Cardiovascular and autonomic phenotype of db/db diabetic mice. Exp. Physiol. 2009, 94:648-658.
21. Cesana M., Cacchiarelli D., Legnini I., Santini T., Sthandier O., Chinappi M., Tramontano A., Bozzoni I. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 2011, 147:358-369.
22. Greco S., De Simone M., Colussi C., Zaccagnini G., Fasanaro P., Pescatori M., Cardani R., Perbellini R., Isaia E., Sale P., Meola G., Capogrossi M.C., Gaetano C., Martelli F. Common micro-RNA signature in skeletal muscle damage and regeneration induced by Duchenne muscular dystrophy and acute ischemia. FASEB J. 2009, 23:3335-3346.
23. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
24. Chen Y., Zhang J., Wang H., Zhao J., Xu C., Du Y., Luo X., Zheng F., Liu R., Zhang H., Ma D. miRNA-135a promotes breast cancer cell migration and invasion by targeting HOXA10. BMC Cancer 2012, 12:111.
25. Wang J., Song Y., Zhang Y., Xiao H., Sun Q., Hou N., Guo S., Wang Y., Fan K., Zhan D., Zha L., Cao Y., Li Z., Cheng X., Zhang Y., Yang X. Cardiomyocyte over-expression of miR-27b induces cardiac hypertrophy and dysfunction in mice. Cell Res. 2012, 22:516-527.
26. Bossel Ben-Moshe N., Avraham R., Kedmi M., Zeisel A., Yitzhaky A., Yarden Y., Domany E. Context-specific microRNA analysis: identification of functional microRNAs and their mRNA targets. Nucleic Acids Res. 2012, 40:10614-10627.
27. Witkos T.M., Koscianska E., Krzyzosiak W.J. Practical aspects of microRNA target prediction. Curr. Mol. Med. 2011, 11:93-109.
28. Lin Q., Schwarz J., Bucana C., Olson E.N. Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 1997, 276:1404-1407.
29. Withers D.J., Gutierrez J.S., Towery H., Burks D.J., Ren J.M., Previs S., Zhang Y., Bernal D., Pons S., Shulman G.I., Bonner-Weir S., White M.F. Disruption of IRS-2 causes type 2 diabetes in mice. Nature 1998, 391:900-904.
30. Brady M.J. IRS2 takes center stage in the development of type 2 diabetes. J. Clin. Invest. 2004, 114:886-888.
31. Sadowski C.L., Choi T.-S., Le M., Wheeler T.T., Wang Lu-Hai, Sadowski H.B. Insulin induction of SOCS-2 and SOCS-3 mRNA expression in C2C12 skeletal muscle cells is mediated by Stat5. J. Biol. Chem. 2001, 276:20703-20710.
32. Lilly B., Zhao B., Ranganayakulu G., Paterson B.M., Schulz R.A., Olson E.N. Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila. Science 1995, 267:688-693.
33. Potthoff M.J., Arnold M.A., McAnally J., Richardson J.A., Bassel-Duby R., Olson E.N. Regulation of skeletal muscle sarcomere integrity and postnatal muscle function by Mef2C. Mol. Cell. Biol. 2007, 27:8143-8151.
34. Li Z., Hassan M.Q., Volinia S., van Wijnen A.J., Stein J.L., Croce C.M., Lian J.B., Stein G.S. A microRNA signature for a BMP2-induced osteoblast lineage commitment program. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:13906-13911.
35. Navarro A., Diaz T., Martinez A., Gaya A., Pons A., Gel B., Codony C., Ferrer G., Martinez C., Montserrat E., Monzo M. Regulation of JAK2 by miR-135a: prognostic impact in classic Hodgkin lymphoma. Blood 2009, 114:2945-2951.
36. Tsuji Y., Kaburagi Y., Terauchi Y., Satoh S., Kubota N., Tamemoto H., Kraemer F.B., Sekihara H., Aizawa S., Akanuma Y., Tobe K., Kimura S., Kadowaki T. Subcellular localization of insulin receptor substrate family proteins associated with phosphatidylinositol 3-kinase activity and alterations in lipolysis in primary mouse adipocytes from IRS-1 null mice. Diabetes 2001, 50:1455-1463.
37. Sesti G., Federici M., Hribal M.L., Lauro D., Sbraccia P., Lauro R. Defects of the insulin receptor substrate (IRS) system in human metabolic disorders. FASEB J. 2001, 15:2099-2111.
38. Sawka-Verhelle D., Tartare-Deckert S., White M.F., Van O.E. Insulin receptor substrate-2 binds to the insulin receptor through its phosphotyrosine-binding domain and through a newly identified domain comprising amino acids 591-786. J. Biol. Chem. 1996, 271:5980-5983.
39. Previs S.F., Withers D.J., Ren J.-M., White M.F., Shulman G.I. Contrasting effects of IRS1 and IRS2 gene disruption on carbohydrate and lipid metabolism in vivo. J. Biol. Chem. 2000, 275:38990-38994.
40. del Aguila L.F., Claffey K.P., Kirwan J.P. TNF-alpha impairs insulin signaling and insulin stimulation of glucose uptake in C2C12 muscle cells. Am. J. Physiol. 1999, 276:E849-E855.
41. Vollenweider P., Menard B., Nicod P. Insulin resistance, defective insulin receptor substrate 2-associated phosphatidylinositol-3'-kinase activation and impaired atypical protein kinase C (ζ/λ) activation in myotubes from obese patients with impaired glucose tolerance. Diabetes 2002, 51:1052-1059.