Adipocyte-derived factors impair insulin signaling in differentiated human vascular smooth muscle cells via the upregulation of miR-143

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1842, Issue 2, 2014, Pages 275-283

  Blumensatt, Marcel ^a   Wronkowitz, Nina ^a   Wiza, Claudia ^a   Cramer, Andrea ^a   Mueller, Heidi ^a   Rabelink, Martijn J ^b   Hoeben, Rob C ^b   Eckel, Juergen ^a   Sell, Henrike ^a   Ouwens, D Margriet ^a,c  

^a LEIBNIZ CENTER FOR DIABETES RESEARCH AT HEINRICH HEINE UNIVERSITY DÜSSELDORF   (Germany)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c GHENT UNIVERSITY HOSPITAL   (Belgium)

Author keywords

Adipokines; Insulin signaling; MiRNA; P38; Vascular smooth muscle cells

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; 4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; ADIPOCYTOKINE; ALPHA SMOOTH MUSCLE ACTIN; BINDING PROTEIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INSULIN; MICRORNA 143; MICRORNA 145; MONOCYTE CHEMOTACTIC PROTEIN 1; OXYSTEROL BINDING PROTEIN RELATED PROTEIN 8; PROTEIN KINASE B; SMAD2 PROTEIN; SYNAPTOPHYSIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; UNCLASSIFIED DRUG;

ADIPOCYTE; ADULT; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HUMAN; HUMAN CELL; MIDDLE AGED; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; UPREGULATION; VASCULAR SMOOTH MUSCLE;

ADIPOKINES; INSULIN SIGNALING; MIRNA; P38; VASCULAR SMOOTH MUSCLE CELLS;

ADIPOCYTES; ADULT; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; FEMALE; HEK293 CELLS; HUMANS; INSULIN; MICRORNAS; MIDDLE AGED; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RECEPTORS, STEROID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; UP-REGULATION;

EID: 84890821838     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.12.001     Document Type: Article

References (37)

1. Blumensatt M., Greulich S., Herzfeld de Wiza D., Mueller H., Maxhera B., Rabelink M.J., Hoeben R.C., Akhyari P., Al-Hasani H., Ruige J.B., Ouwens D.M. Activin A impairs insulin action in cardiomyocytes via up-regulation of miR-143. Cardiovasc. Res. 2013, 100:201-210.
2. Boettger T., Beetz N., Kostin S., Schneider J., Kruger M., Hein L., Braun T. Acquisition of the contractile phenotype by murine arterial smooth muscle cells depends on the Mir143/145 gene cluster. J. Clin. Invest. 2009, 119:2634-2647.
3. Bornfeldt K.E., Tabas I. Insulin resistance, hyperglycemia, and atherosclerosis. Cell Metab. 2011, 14:575-585.
4. Carlotti F., Bazuine M., Kekarainen T., Seppen J., Pognonec P., Maassen J.A., Hoeben R.C. Lentiviral vectors efficiently transduce quiescent mature 3T3-L1 adipocytes. Mol. Ther. 2004, 9:209-217.
5. Cersosimo E., Xu X., Musi N. Potential role of insulin signaling on vascular smooth muscle cell migration, proliferation, and inflammation pathways. Am. J. Physiol. Cell Physiol. 2012, 302:C652-C657.
6. Cheng Y., Liu X., Yang J., Lin Y., Xu D.Z., Lu Q., Deitch E.A., Huo Y., Delphin E.S., Zhang C. MicroRNA-145, a novel smooth muscle cell phenotypic marker and modulator, controls vascular neointimal lesion formation. Circ. Res. 2009, 105:158-166.
7. Cipollone F., Felicioni L., Sarzani R., Ucchino S., Spigonardo F., Mandolini C., Malatesta S., Bucci M., Mammarella C., Santovito D., de L.F., Marchetti A., Mezzetti A., Buttitta F. A unique microRNA signature associated with plaque instability in humans. Stroke 2011, 42:2556-2563.
8. Cordes K.R., Sheehy N.T., White M.P., Berry E.C., Morton S.U., Muth A.N., Lee T.H., Miano J.M., Ivey K.N., Srivastava D. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 2009, 460:705-710.
9. Fulton D.J. Mechanisms of vascular insulin resistance: a substitute Akt?. Circ. Res. 2009, 104:1035-1037.
10. Garg U.C., Hassid A. Nitric oxide-generating vasodilators and 8-bromo-cyclic guanosine monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J. Clin. Invest. 1989, 83:1774-1777.
11. Greulich S., Maxhera B., Vandenplas G., de Wiza D.H., Smiris K., Mueller H., Heinrichs J., Blumensatt M., Cuvelier C., Akhyari P., Ruige J.B., Ouwens D.M., Eckel J. Secretory products from epicardial adipose tissue of patients with type 2 diabetes mellitus induce cardiomyocyte dysfunction. Circulation 2012, 126:2324-2334.
12. Grundy S.M. Obesity, metabolic syndrome, and cardiovascular disease. J. Clin. Endocrinol. Metab. 2004, 89:2595-2600.
13. Hansmann G., de Jesus Perez V.A., Alastalo T.P., Alvira C.M., Guignabert C., Bekker J.M., Schellong S., Urashima T., Wang L., Morrell N.W., Rabinovitch M. An antiproliferative BMP-2/PPARgamma/apoE axis in human and murine SMCs and its role in pulmonary hypertension. J. Clin. Invest. 2008, 118:1846-1857.
14. Hauner H., Petruschke T., Russ M., Rohrig K., Eckel J. Effects of tumour necrosis factor alpha (TNF alpha) on glucose transport and lipid metabolism of newly-differentiated human fat cells in cell culture. Diabetologia 1995, 38:764-771.
15. Izawa Y., Yoshizumi M., Fujita Y., Ali N., Kanematsu Y., Ishizawa K., Tsuchiya K., Obata T., Ebina Y., Tomita S., Tamaki T. ERK1/2 activation by angiotensin II inhibits insulin-induced glucose uptake in vascular smooth muscle cells. Exp. Cell Res. 2005, 308:291-299.
16. Jiang Z.Y., Lin Y.W., Clemont A., Feener E.P., Hein K.D., Igarashi M., Yamauchi T., White M.F., King G.L. Characterization of selective resistance to insulin signaling in the vasculature of obese Zucker (fa/fa) rats. J. Clin. Invest. 1999, 104:447-457.
17. Johansson G.S., Arnqvist H.J. Insulin and IGF-I action on insulin receptors, IGF-I receptors, and hybrid insulin/IGF-I receptors in vascular smooth muscle cells. Am. J. Physiol. Endocrinol. Metab. 2006, 291:E1124-E1130.
18. Jordan S.D., Kruger M., Willmes D.M., Redemann N., Wunderlich F.T., Bronneke H.S., Merkwirth C., Kashkar H., Olkkonen V.M., Bottger T., Braun T., Seibler J., Bruning J.C. Obesity-induced overexpression of miRNA-143 inhibits insulin-stimulated AKT activation and impairs glucose metabolism. Nat. Cell Biol. 2011, 13:434-446.
19. Kahn A.M., Husid A., Allen J.C., Seidel C.L., Song T. Insulin acutely inhibits cultured vascular smooth muscle cell contraction by a nitric oxide synthase-dependent pathway. Hypertension 1997, 30:928-933.
20. Lamers D., Schlich R., Greulich S., Sasson S., Sell H., Eckel J. Oleic acid and adipokines synergize in inducing proliferation and inflammatory signalling in human vascular smooth muscle cells. J. Cell. Mol. Med. 2011, 15:1177-1188.
21. Landmesser U., Hornig B., Drexler H. Endothelial function: a critical determinant in atherosclerosis?. Circulation 2004, 109:II27-II33.
22. Long X., Miano J.M. Transforming growth factor-beta1 (TGF-beta1) utilizes distinct pathways for the transcriptional activation of microRNA 143/145 in human coronary artery smooth muscle cells. J. Biol. Chem. 2011, 286:30119-30129.
23. Montero D., Walther G., Perez-Martin A., Vicente-Salar N., Roche E., Vinet A. Vascular smooth muscle function in type 2 diabetes mellitus: a systematic review and meta-analysis. Diabetologia 2013, 56:2122-2133.
24. Muniyappa R., Montagnani M., Koh K.K., Quon M.J. Cardiovascular actions of insulin. Endocr. Rev. 2007, 28:463-491.
25. Nakaki T., Nakayama M., Kato R. Inhibition by nitric oxide and nitric oxide-producing vasodilators of DNA synthesis in vascular smooth muscle cells. Eur. J. Pharmacol. 1990, 189:347-353.
26. Nunokawa Y., Tanaka S. Interferon-gamma inhibits proliferation of rat vascular smooth muscle cells by nitric oxide generation. Biochem. Biophys. Res. Commun. 1992, 188:409-415.
27. Owens G.K. Regulation of differentiation of vascular smooth muscle cells. Physiol. Rev. 1995, 75:487-517.
28. Santovito D., Mezzetti A., Cipollone F. MicroRNAs and atherosclerosis: new actors for an old movie. Nutr. Metab. Cardiovasc. Dis. 2012, 22:937-943.
29. Schlich R., Willems M., Greulich S., Ruppe F., Knoefel W.T., Ouwens D.M., Maxhera B., Lichtenberg A., Eckel J., Sell H. VEGF in the crosstalk between human adipocytes and smooth muscle cells: depot-specific release from visceral and perivascular adipose tissue. Mediat. Inflamm. 2013, 2013:982458.
30. Symons J.D., McMillin S.L., Riehle C., Tanner J., Palionyte M., Hillas E., Jones D., Cooksey R.C., Birnbaum M.J., McClain D.A., Zhang Q.J., Gale D., Wilson L.J., Abel E.D. Contribution of insulin and Akt1 signaling to endothelial nitric oxide synthase in the regulation of endothelial function and blood pressure. Circ. Res. 2009, 104:1085-1094.
31. Takanabe R., Ono K., Abe Y., Takaya T., Horie T., Wada H., Kita T., Satoh N., Shimatsu A., Hasegawa K. Up-regulated expression of microRNA-143 in association with obesity in adipose tissue of mice fed high-fat diet. Biochem. Biophys. Res. Commun. 2008, 376:728-732.
32. ten Dijke P., Arthur H.M. Extracellular control of TGFbeta signalling in vascular development and disease. Nat. Rev. Mol. Cell Biol. 2007, 8:857-869.
33. Trovati M., Massucco P., Mattiello L., Cavalot F., Mularoni E., Hahn A., Anfossi G. Insulin increases cyclic nucleotide content in human vascular smooth muscle cells: a mechanism potentially involved in insulin-induced modulation of vascular tone. Diabetologia 1995, 38:936-941.
34. Trovati M., Massucco P., Mattiello L., Costamagna C., Aldieri E., Cavalot F., Anfossi G., Bosia A., Ghigo D. Human vascular smooth muscle cells express a constitutive nitric oxide synthase that insulin rapidly activates, thus increasing guanosine 3':5'-cyclic monophosphate and adenosine 3':5'-cyclic monophosphate concentrations. Diabetologia 1999, 42:831-839.
35. Vandesompele J., De P.K., Pattyn F., Poppe B., Van R.N., De P.A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3. (p.RESEARCH0034).
36. Wichelhaus A., Russ M., Petersen S., Eckel J. G protein expression and adenylate cyclase regulation in ventricular cardiomyocytes from STZ-diabetic rats. Am. J. Physiol. 1994, 267:H548-H555.
37. Xin M., Small E.M., Sutherland L.B., Qi X., McAnally J., Plato C.F., Richardson J.A., Bassel-Duby R., Olson E.N. MicroRNAs miR-143 and miR-145 modulate cytoskeletal dynamics and responsiveness of smooth muscle cells to injury. Genes Dev. 2009, 23:2166-2178.