Stretch-Sensitive Down-Regulation of the miR-144/451 Cluster in Vascular Smooth Muscle and Its Role in AMP-Activated Protein Kinase Signaling

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Turczyńska, Karolina M ^a   Bhattachariya, Anirban ^a   Säll, Johanna ^a   Göransson, Olga ^a   Swärd, Karl ^a   Hellstrand, Per ^a   Albinsson, Sebastian ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; ACETYL COENZYME A CARBOXYLASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MICRORNA; MICRORNA 144; MICRORNA 451; PROTEIN MO25ALPHA; SCAFFOLD PROTEIN; THREONINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME PHOSPHORYLATION; GENE CLUSTER; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; INTRACELLULAR SIGNALING; MALE; MICROARRAY ANALYSIS; MOUSE; MUSCLE STRETCHING; NONHUMAN; PORTAL VEIN; PROTEIN EXPRESSION; PROTEIN TARGETING; SMOOTH MUSCLE CONTRACTION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; AORTA; BASE SEQUENCE; CAROTID ARTERIES; DOWN-REGULATION; ENZYME ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MICRORNAS; MOLECULAR SEQUENCE DATA; MUSCLE CONTRACTION; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PHOSPHORYLATION; PORTAL VEIN; PRESSURE; RIBONUCLEOTIDES; SIGNAL TRANSDUCTION; STRESS, MECHANICAL; TRANSFECTION;

EID: 84877966077     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065135     Document Type: Article

References (41)

1. Owens GK, Kumar MS, Wamhoff BR, (2004) Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84: 767-801.
2. Komatsu R, Ueda M, Naruko T, Kojima A, Becker AE, (1998) Neointimal tissue response at sites of coronary stenting in humans: macroscopic, histological, and immunohistochemical analyses. Circulation 98: 224-233.
3. Zeidan A, Nordström I, Albinsson S, Malmqvist U, Swärd K, et al. (2003) Stretch-induced contractile differentiation of vascular smooth muscle: sensitivity to actin polymerization inhibitors. Am J Physiol Cell Physiol 284: C1387-1396.
4. Albinsson S, Nordström I, Hellstrand P, (2004) Stretch of the vascular wall induces smooth muscle differentiation by promoting actin polymerization. J Biol Chem 279: 34849-34855.
5. Hellstrand P, Albinsson S, (2005) Stretch-dependent growth and differentiation in vascular smooth muscle: role of the actin cytoskeleton. Can J Physiol Pharmacol 83: 869-875.
6. Albinsson S, Hellstrand P, (2007) Integration of signal pathways for stretch-dependent growth and differentiation in vascular smooth muscle. Am J Physiol Cell Physiol 293: C772-782.
7. Albinsson S, Nordström I, Swärd K, Hellstrand P, (2008) Differential dependence of stretch and shear stress signaling on caveolin-1 in the vascular wall. Am J Physiol Cell Physiol 294: C271-279.
8. Xu Q, Liu Y, Gorospe M, Udelsman R, Holbrook NJ, (1996) Acute hypertension activates mitogen-activated protein kinases in arterial wall. J Clin Invest 97: 508-514.
9. Wesselman JP, Dobrian AD, Schriver SD, Prewitt RL, (2001) Src tyrosine kinases and extracellular signal-regulated kinase 1/2 mitogen-activated protein kinases mediate pressure-induced c-fos expression in cannulated rat mesenteric small arteries. Hypertension 37: 955-960.
10. Kim J, Lee YR, Lee CH, Choi WH, Lee CK, et al. (2005) Mitogen-activated protein kinase contributes to elevated basal tone in aortic smooth muscle from hypertensive rats. Eur J Pharmacol 514: 209-215.
11. Carnevale D, Vecchione C, Mascio G, Esposito G, Cifelli G, et al. (2012) PI3Kgamma inhibition reduces blood pressure by a vasorelaxant Akt/L-type calcium channel mechanism. Cardiovasc Res 93: 200-209.
12. Kawahara S, Umemoto S, Tanaka M, Umeji K, Matsuda S, et al. (2005) Up-regulation of Akt and eNOS induces vascular smooth muscle cell differentiation in hypertension in vivo. J Cardiovasc Pharmacol 45: 367-374.
13. Seasholtz TM, Zhang T, Morissette MR, Howes AL, Yang AH, et al. (2001) Increased Expression and Activity of RhoA Are Associated With Increased DNA Synthesis and Reduced p27Kip1 Expression in the Vasculature of Hypertensive Rats. Circ Res 89: 488-495.
14. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, et al. (1997) Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389: 990-994.
15. Zeidan A, Broman J, Hellstrand P, Swärd K, (2003) Cholesterol Dependence of Vascular ERK1/2 Activation and Growth in Response to Stretch: Role of Endothelin-1. Arterioscler Thromb Vasc Biol 23: 1528-1534.
16. Ren J, Albinsson S, Hellstrand P, (2010) Distinct effects of voltage- and store-dependent calcium influx on stretch-induced differentiation and growth in vascular smooth muscle. J Biol Chem 285: 31829-31839.
17. Turczynska KM, Sadegh MK, Hellstrand P, Swärd K, Albinsson S, (2012) MicroRNAs are essential for stretch-induced vascular smooth muscle contractile differentiation via microRNA (miR)-145-dependent expression of L-type calcium channels. J Biol Chem 287: 19199-19206.
18. Bartel DP, (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
19. Albinsson S, Suarez Y, Skoura A, Offermanns S, Miano JM, et al. (2010) MicroRNAs are necessary for vascular smooth muscle growth, differentiation, and function. Arterioscler Thromb Vasc Biol 30: 1118-1126.
20. Albinsson S, Skoura A, Yu J, Dilorenzo A, Fernandez-Hernando C, et al. (2011) Smooth Muscle miRNAs Are Critical for Post-Natal Regulation of Blood Pressure and Vascular Function. PLoS One 6: e18869.
21. Sadegh MK, Ekman M, Rippe C, Uvelius B, Swärd K, et al. (2012) Deletion of dicer in smooth muscle affects voiding pattern and reduces detrusor contractility and neuroeffector transmission. PLoS One 7: e35882.
22. Albinsson S, Shakirova Y, Rippe A, Baumgarten M, Rosengren BI, et al. (2007) Arterial remodeling and plasma volume expansion in caveolin-1-deficient mice. Am J Physiol Regul Integr Comp Physiol 293: R1222-1231.
23. Long X, Tharp DL, Georger MA, Slivano OJ, Lee MY, et al. (2009) The smooth muscle cell-restricted KCNMB1 ion channel subunit is a direct transcriptional target of serum response factor and myocardin. J Biol Chem 284: 33671-33682.
24. Gormand A, Henriksson E, Strom K, Jensen TE, Sakamoto K, et al. (2011) Regulation of AMP-activated protein kinase by LKB1 and CaMKK in adipocytes. J Cell Biochem 112: 1364-1375.
25. Nagata D, Takeda R, Sata M, Satonaka H, Suzuki E, et al. (2004) AMP-activated protein kinase inhibits angiotensin II-stimulated vascular smooth muscle cell proliferation. Circulation 110: 444-451.
26. Song P, Wang S, He C, Liang B, Viollet B, et al. (2011) AMPKalpha2 deletion exacerbates neointima formation by upregulating Skp2 in vascular smooth muscle cells. Circ Res 109: 1230-1239.
27. Stone JD, Narine A, Shaver PR, Fox JC, Vuncannon JR, et al. (2012) AMP-Activated Protein Kinase Inhibits Vascular Smooth Muscle Cell Proliferation and Migration and Vascular Remodeling Following Injury. Am J Physiol Heart Circ Physiol.
28. Godlewski J, Nowicki MO, Bronisz A, Nuovo G, Palatini J, et al. (2010) MicroRNA-451 regulates LKB1/AMPK signaling and allows adaptation to metabolic stress in glioma cells. Mol Cell 37: 620-632.
29. Chen H, Untiveros GM, McKee LA, Perez J, Li J, et al. (2012) Micro-RNA-195 and-451 regulate the LKB1/AMPK signaling axis by targeting MO25. PLoS One 7: e41574.
30. Ding M, Xie Y, Wagner RJ, Jin Y, Carrao AC, et al. (2011) Adiponectin induces vascular smooth muscle cell differentiation via repression of mammalian target of rapamycin complex 1 and FoxO4. Arterioscler Thromb Vasc Biol 31: 1403-1410.
31. Birukov KG, Bardy N, Lehoux S, Merval R, Shirinsky VP, et al. (1998) Intraluminal pressure is essential for the maintenance of smooth muscle caldesmon and filamin content in aortic organ culture. Arterioscler Thromb Vasc Biol 18: 922-927.
32. Song J, Hu B, Qu H, Bi C, Huang X, et al. (2012) Mechanical stretch modulates microRNA 21 expression, participating in proliferation and apoptosis in cultured human aortic smooth muscle cells. PLoS One 7: e47657.
33. Song L, Duan P, Guo P, Li D, Li S, et al. (2012) Downregulation of miR-223 and miR-153 mediates mechanical stretch-stimulated proliferation of venous smooth muscle cells via activation of the insulin-like growth factor-1 receptor. Arch Biochem Biophys 528: 204-211.
34. Mohamed JS, Lopez MA, Boriek AM, (2010) Mechanical stretch up-regulates microRNA-26a and induces human airway smooth muscle hypertrophy by suppressing glycogen synthase kinase-3beta. J Biol Chem 285: 29336-29347.
35. Dore LC, Amigo JD, Dos Santos CO, Zhang Z, Gai X, et al. (2008) A GATA-1-regulated microRNA locus essential for erythropoiesis. Proc Natl Acad Sci U S A 105: 3333-3338.
36. Rasmussen KD, Simmini S, Abreu-Goodger C, Bartonicek N, Di Giacomo M, et al. (2010) The miR-144/451 locus is required for erythroid homeostasis. J Exp Med 207: 1351-1358.
37. Zhang X, Wang X, Zhu H, Zhu C, Wang Y, et al. (2010) Synergistic effects of the GATA-4-mediated miR-144/451 cluster in protection against simulated ischemia/reperfusion-induced cardiomyocyte death. J Mol Cell Cardiol 49: 841-850.
38. Wang X, Zhu H, Zhang X, Liu Y, Chen J, et al. (2012) Loss of the miR-144/451 cluster impairs ischaemic preconditioning-mediated cardioprotection by targeting Rac-1. Cardiovasc Res 94: 379-390.
39. Caruso P, MacLean MR, Khanin R, McClure J, Soon E, et al. (2010) Dynamic changes in lung microRNA profiles during the development of pulmonary hypertension due to chronic hypoxia and monocrotaline. Arterioscler Thromb Vasc Biol 30: 716-723.
40. Hawley SA, Boudeau J, Reid JL, Mustard KJ, Udd L, et al. (2003) Complexes between the LKB1 tumor suppressor, STRAD alpha/beta and MO25 alpha/beta are upstream kinases in the AMP-activated protein kinase cascade. J Biol 2: 28.
41. Woods A, Vertommen D, Neumann D, Turk R, Bayliss J, et al. (2003) Identification of phosphorylation sites in AMP-activated protein kinase (AMPK) for upstream AMPK kinases and study of their roles by site-directed mutagenesis. J Biol Chem 278: 28434-28442.