AMP-activated protein kinase inhibits transforming growth factor-β-mediated vascular smooth muscle cell growth: Implications for a smad-3-dependent mechanism

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 309, Issue 8, 2015, Pages H1251-H1259

  Stone, Joshua D ^a,b   Holt, Andrew W ^a   Vuncannon, Jackson R ^a   Brault, Jeffrey J ^a   Tulis, David A ^a  

^a EAST CAROLINA UNIVERSITY   (United States)

^b Carson Newman College   (United States)

Author keywords

Adenosine monophosphate activated protein kinase; Proliferation

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; CYCLIN D1; CYCLIN DEPENDENT KINASE 2; CYCLIN E; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; CELL CYCLE PROTEIN; ENZYME ACTIVATOR; MADH3 PROTEIN, RAT; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL COUNT; CELL PROLIFERATION; CONTROLLED STUDY; FLOW CYTOMETRY; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; GENE OVEREXPRESSION; GROWTH INHIBITION; GROWTH REGULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; CELL CULTURE; CELL CYCLE; DOSE RESPONSE; DRUG EFFECTS; ENZYME ACTIVATION; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; MALE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SMOOTH MUSCLE CELL; SPRAGUE DAWLEY RAT; THORACIC AORTA; TIME FACTOR; VASCULAR SMOOTH MUSCLE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; AORTA, THORACIC; CELL CYCLE; CELL CYCLE PROTEINS; CELL PROLIFERATION; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; ENZYME ACTIVATORS; MALE; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PHOSPHORYLATION; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SMAD3 PROTEIN; TIME FACTORS; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84944382352     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00846.2014     Document Type: Article

References (28)

1. Adderley SP, Joshi CN, Martin DN, Tulis DA. Phosphodiesterases regulate BAY 41-2272-induced VASP phosphorylation in vascular smooth muscle cells. Frontiers Pharmacol 3: 10, 2012.
2. Akhurst RJ, Hata A. Targeting the TGFbeta signalling pathway in disease. Nat Rev 11: 790–811, 2012.
3. Battegay EJ, Raines EW, Seifert RA, Bowen-Pope DF, Ross R. TGF-beta induces bimodal proliferation of connective tissue cells via complex control of an autocrine PDGF loop. Cell 63: 515–524, 1990.
4. Bollinger LM, Witczak CA, Houmard JA, Brault JJ. SMAD3 augments FoxO3-induced MuRF-1 promoter activity in a DNA-bindingdependent manner. Am J Physiol Cell Physiol 307: C278–C287, 2014.
5. Durante W, Schini VB, Catovsky S, Kroll MH, Vanhoutte PM, Schafer AI. Plasmin potentiates induction of nitric oxide synthesis by interleukin-1β in vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 264: H617–H624, 1993.
6. Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Borden WB, Bravata DM, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Magid D, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER, Moy CS, Mussolino ME, Nichol G, Paynter NP, Schreiner PJ, Sorlie PD, Stein J, Turan TN, Virani SS, Wong ND, Woo D, Turner MB. Heart disease and stroke statistics–2013 update: a report from the American Heart Association. Circulation 127: e6–e245, 2013.
7. Hardie DG. AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev 25: 1895–1908, 2011.
8. Hardie DG. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev 8: 774–785, 2007.
9. Hneino M, Bouazza L, Bricca G, Li JY, Langlois D. Density-dependent shift of transforming growth factor-beta-1 from inhibition to stimulation of vascular smooth muscle cell growth is based on unconventional regulation of proliferation, apoptosis and contact inhibition. J Vasc Res 46: 85–97, 2009.
10. Igata M, Motoshima H, Tsuruzoe K, Kojima K, Matsumura T, Kondo T, Taguchi T, Nakamaru K, Yano M, Kukidome D, Matsumoto K, Toyonaga T, Asano T, Nishikawa T, Araki E. Adenosine monophosphate-activated protein kinase suppresses vascular smooth muscle cell proliferation through the inhibition of cell cycle progression. Circ Res 97: 837–844, 2005.
11. Joshi CN, Martin DN, Fox JC, Mendelev NN, Brown TA, Tulis DA. The soluble guanylate cyclase stimulator BAY 41–2272 inhibits vascular smooth muscle growth through the cAMP-dependent protein kinase and cGMP-dependent protein kinase pathways. J Pharmacol Exp Ther 339: 394–402, 2011.
12. Nagata D, Takeda R, Sata M, Satonaka H, Suzuki E, Nagano T, Hirata Y. AMP-activated protein kinase inhibits angiotensin II-stimulated vascular smooth muscle cell proliferation. Circulation 110: 444–451, 2004.
13. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84: 767–801, 2004.
14. Polyak K, Kato JY, Solomon MJ, Sherr CJ, Massague J, Roberts JM, Koff A. p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest. Genes Dev 8: 9–22, 1994.
15. Reardon C, McKay DM. TGF-β suppresses IFN-gamma-STAT1-dependent gene transcription by enhancing STAT1-PIAS1 interactions in epithelia but not monocytes/macrophages. J Immunol 178: 4284–4295, 2007.
16. Rubin LJ, Magliola L, Feng X, Jones AW, Hale CC. Metabolic activation of AMP kinase in vascular smooth muscle. J Appl Physiol 98: 296–306, 2005.
17. Ruiz-Ortega M, Rodriguez-Vita J, Sanchez-Lopez E, Carvajal G, Egido J. TGF-beta signaling in vascular fibrosis. Cardiovasc Res 74: 196–206, 2007.
18. Samarakoon R, Higgins SP, Higgins CE, Higgins PJ. TGF-beta1-induced plasminogen activator inhibitor-1 expression in vascular smooth muscle cells requires pp60(c-src)/EGFR(Y845) and Rho/ROCK signaling. J Mol Cell Cardiol 44: 527–538, 2008.
19. Sanders MJ, Grondin PO, Hegarty BD, Snowden MA, Carling D. Investigating the mechanism for AMP activation of the AMP-activated protein kinase cascade. Biochem J 403: 139–148, 2007.
20. Santibanez JF, Quintanilla M, Bernabeu C. TGF-beta/TGF-beta receptor system and its role in physiological and pathological conditions. Clin Sci (Lond) 121: 233–251, 2011.
21. Shirwany NA, Zou MH. AMPK in cardiovascular health and disease. Acta Pharmacol 31: 1075–1084, 2010.
22. Stone JD, Narine A, Shaver PR, Fox JC, Vuncannon JR, Tulis DA. AMP-activated protein kinase inhibits vascular smooth muscle cell proliferation and migration and vascular remodeling following injury. Am J Physiol Heart Circ Physiol 304: H369–H381, 2013.
23. Stone JD, Narine A, Tulis DA. Inhibition of vascular smooth muscle growth via signaling crosstalk between AMP-activated protein kinase and cAMP-dependent protein kinase. Frontiers Physiol 3: 409, 2012.
24. Suwanabol PA, Seedial SM, Shi X, Zhang F, Yamanouchi D, Roenneburg D, Liu B, Kent KC. Transforming growth factor-beta increases vascular smooth muscle cell proliferation through the Smad3 and extracellular signal-regulated kinase mitogen-activated protein kinases pathways. J Vasc Surg 56: 446–454, 2012.
25. Suwanabol PA, Seedial SM, Zhang F, Shi X, Si Y, Liu B, Kent KC. TGF-β and Smad3 modulate PI3K/Akt signaling pathway in vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 302: H2211–H2219, 2012.
26. Tsai S, Hollenbeck ST, Ryer EJ, Edlin R, Yamanouchi D, Kundi R, Wang C, Liu B, Kent KC. TGF-β through Smad3 signaling stimulates vascular smooth muscle cell proliferation and neointimal formation. Am J Physiol Heart Circ Physiol 297: H540–H549, 2009.
27. Yokote K, Kobayashi K, Saito Y. The role of Smad3-dependent TGFbeta signal in vascular response to injury. Trends Cardiovasc Med 16: 240–245, 2006.
28. Zhao J, Miyamoto S, You YH, Sharma K. AMP-activated protein kinase (AMPK) activation inhibits nuclear translocation of Smad4 in mesangial cells and diabetic kidneys. Am J Physiol Renal Physiol 308: F1167–F1177, 2015.