AMP-activated protein kinase inhibits vascular smooth muscle cell proliferation and migration and vascular remodeling following injury

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 304, Issue 3, 2013, Pages

  Stone, Joshua D ^a   Narine, Avinash ^a   Shaver, Patti R ^a   Fox, Jonathan C ^a   Vuncannon, Jackson R ^a   Tulis, David A ^a  

^a EAST CAROLINA UNIVERSITY   (United States)

Author keywords

Actin cy toskeleton; Adenosine monophosphate activated protein kinase; Cell cycle; Focal adhesion kinase; Matrix metalloproteinases; Migration; Proliferation; Protein phosphatase 2a; Vascular smooth muscle cell; Vasodilator activated serum phosphoprotein

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE DERIVATIVE; CYCLIN B; F ACTIN; FOCAL ADHESION KINASE; G ACTIN; GELATINASE B; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PAXILLIN; PHOSPHOPROTEIN PHOSPHATASE 2A; PLATELET DERIVED GROWTH FACTOR; VASODILATOR STIMULATED PHOSPHOPROTEIN;

ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; CARDIOVASCULAR FUNCTION; CAROTID ARTERY; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; EXTRACELLULAR MATRIX; IN VIVO STUDY; MALE; MITOSIS; NEOINTIMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; RAT; SMOOTH MUSCLE FIBER; STRESS FIBER; VASCULAR REMODELING; VASCULAR SMOOTH MUSCLE;

ACTINS; AMINOIMIDAZOLE CARBOXAMIDE; ANIMALS; AORTA, THORACIC; BLOOD VESSELS; CAROTID ARTERY INJURIES; CELL ADHESION; CELL CYCLE; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOSKELETON; FLUORESCENT ANTIBODY TECHNIQUE; HYPOGLYCEMIC AGENTS; IMMUNOHISTOCHEMISTRY; MALE; MATRIX METALLOPROTEINASES; MYOCYTES, SMOOTH MUSCLE; NEOINTIMA; RATS; RATS, SPRAGUE-DAWLEY; RIBONUCLEOTIDES;

EID: 84873285214     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00446.2012     Document Type: Article

References (64)

1. Adderley SP, Joshi CN, Martin DN, Tulis DA. Phosphodiesterases regulate BAY 41-2272-induced VASP phosphorylation in vascular smooth muscle cells. Front Pharmacol 3: 10, 2012.
2. Barzik M, Kotova TI, Higgs HN, Hazelwood L, Hanein D, Gertler FB, Schafer DA. Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins. J Biol Chem 280: 28653-28662, 2005.
3. Bear JE, Svitkina TM, Krause M, Schafer DA, Loureiro JJ, Strasser GA, Maly IV, Chaga OY, Cooper JA, Borisy GG, Gertler FB. Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109: 509-521, 2002.
4. Benz PM, Blume C, Seifert S, Wilhelm S, Waschke J, Schuh K, Gertler F, Munzel T, Renne T. Differential VASP phosphorylation controls remodeling of the actin cytoskeleton. J Cell Sci 122: 3954-3965, 2009.
5. Blume C, Benz PM, Walter U, Ha J, Kemp BE, Renne T. AMP-activated protein kinase impairs endothelial actin cytoskeleton assembly by phosphorylating vasodilator-stimulated phosphoprotein. J Biol Chem 282: 4601-4612, 2007.
6. Briones AM, Arribas SM, Salaices M. Role of extracellular matrix in vascular remodeling of hypertension. Curr Opin Nephrol Hypertens 19: 187-194, 2010.
7. Browner NC, Dey NB, Bloch KD, Lincoln TM. Regulation of cGMP-dependent protein kinase expression by soluble guanylyl cy-clase in vascular smooth muscle cells. J Biol Chem 279: 46631-46636, 2004.
8. Chang MY, Ho FM, Wang JS, Kang HC, Chang Y, Ye ZX, Lin WW. AICAR induces cyclooxygenase-2 expression through AMP-activated protein kinase-transforming growth factor-beta-activated kinase 1-p38 mitogen-activated protein kinase signaling pathway. Biochem Pharmacol 80: 1210-1220, 2010.
9. Chen L, Daum G, Chitaley K, Coats SA, Bowen-Pope DF, Eigenthaler M, Thumati NR, Walter U, Clowes AW. Vasodilator-stimulated phos-phoprotein regulates proliferation and growth inhibition by nitric oxide in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 24: 1403-1408, 2004.
10. Crute BE, Seefeld K, Gamble J, Kemp BE, Witters LA. Functional domains of the alpha1 catalytic subunit of the AMP-activated protein kinase. J Biol Chem 273: 35347-35354, 1998.
11. Durante W, Schini VB, Catovsky S, Kroll MH, Vanhoutte PM, Schafer AI. Plasmin potentiates induction of nitric oxide synthesis by interleukin-1 beta in vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 264: H617-H624, 1993.
12. Ewart MA, Kennedy S. AMPK and vasculoprotection. Pharmacol Ther 131: 242-253, 2011.
13. Ford RJ, Teschke SR, Reid EB, Durham KK, Kroetsch JT, Rush JW. AMP-activated protein kinase activator AICAR acutely lowers blood pressure and relaxes isolated resistance arteries of hypertensive rats. J Hypertens 30: 725-733, 2012.
14. Goirand F, Solar M, Athea Y, Viollet B, Mateo P, Fortin D, Leclerc J, Hoerter J, Ventura-Clapier R, Garnier A. Activation of AMP kinase alpha1 subunit induces aortic vasorelaxation in mice. J Physiol 581: 1163-1171, 2007.
15. Goransson O, McBride A, Hawley SA, Ross FA, Shpiro N, Foretz M, Viollet B, Hardie DG, Sakamoto K. Mechanism of action of A-769662, a valuable tool for activation of AMP-activated protein kinase. J Biol Chem 282: 32549-32560, 2007.
16. Handa N, Takagi T, Saijo S, Kishishita S, Takaya D, Toyama M, Terada T, Shirouzu M, Suzuki A, Lee S, Yamauchi T, Okada-Iwabu M, Iwabu M, Kadowaki T, Minokoshi Y, Yokoyama S. Structural basis for compound C inhibition of the human AMP-activated protein kinase alpha2 subunit kinase domain. Acta Crystallogr D Biol Crystallogr 67: 480-487, 2011.
17. Hao H, Gabbiani G, Bochaton-Piallat ML. Arterial smooth muscle cell heterogeneity: implications for atherosclerosis and restenosis development. Arterioscler Thromb Vasc Biol 23: 1510-1520, 2003.
18. Hardie DG. AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev 25: 1895-1908, 2011.
19. Hardie DG. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8: 774-785, 2007.
20. Hawley SA, Ross FA, Chevtzoff C, Green KA, Evans A, Fogarty S, Towler MC, Brown LJ, Ogunbayo OA, Evans AM, Hardie DG. Use of cells expressing gamma subunit variants to identify diverse mechanisms of AMPK activation. Cell Metab 11: 554-565, 2010.
21. Hervy M, Hoffman L, Beckerle MC. From the membrane to the nucleus and back again: bifunctional focal adhesion proteins. Curr Opin Cell Biol 18: 524-532, 2006.
22. 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 monophos-phate-activated protein kinase suppresses vascular smooth muscle cell proliferation through the inhibition of cell cycle progression. Circ Res 97: 837-844, 2005.
23. Insull W Jr. The pathology of atherosclerosis: plaque development and plaque responses to medical treatment. Am J Med 122: S3-S14, 2009.
24. Janssens V, Goris J. Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 353: 417-439, 2001.
25. Johnson C, Galis ZS. Matrix metalloproteinase-2 and -9 differentially regulate smooth muscle cell migration and cell-mediated collagen organization. Arterioscler Thromb Vasc Biol 24: 54-60, 2004.
26. 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.
27. Joshi CN, Martin DN, Shaver P, Madamanchi C, Muller-Borer BJ, Tulis DA. Control of vascular smooth muscle cell growth by connexin 43. Front Physiol 3: 220, 2012.
28. Kawaguchi T, Takenoshita M, Kabashima T, Uyeda K. Glucose and cAMP regulate the L-type pyruvate kinase gene by phosphorylation/ dephosphorylation of the carbohydrate response element binding protein. Proc Natl Acad Sci USA 98: 13710-13715, 2001.
29. Koshman YE, Kim T, Chu M, Engman SJ, Iyengar R, Robia SL, Samarel AM. FRNK inhibition of focal adhesion kinase-dependent signaling and migration in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 30: 2226-2233, 2010.
30. Lee EJ, Kim WJ, Moon SK. Cordycepin suppresses TNF-alpha-induced invasion, migration and matrix metalloproteinase-9 expression in human bladder cancer cells. Phytother Res 24: 1755-1761, 2010.
31. Luo Z, Zang M, Guo W. AMPK as a metabolic tumor suppressor: control of metabolism and cell growth. Future Oncol 6: 457-470, 2010.
32. Majesky MW. Neointima formation after acute vascular injury. Role of counteradhesive extracellular matrix proteins. Tex Heart Inst J 21: 78-85, 1994.
33. Mendelev NN, Williams VS, Tulis DA. Antigrowth properties of BAY 41-2272 in vascular smooth muscle cells. J Cardiovasc Pharmacol 53: 121-131, 2009.
34. Mihaylova MM, Shaw RJ. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol 13: 1016-1023, 2011.
35. Miranda L, Carpentier S, Platek A, Hussain N, Gueuning MA, Vertommen D, Ozkan Y, Sid B, Hue L, Courtoy PJ, Rider MH, Horman S. AMP-activated protein kinase induces actin cytoskeleton reorganization in epithelial cells. Biochem Biophys Res Commun 396: 656-661, 2010.
36. Momcilovic M, Hong SP, Carlson M. Mammalian TAK1 activates Snf1 protein kinase in yeast and phosphorylates AMP-activated protein kinase in vitro. J Biol Chem 281: 25336-25343, 2006.
37. 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.
38. Newby AC. Matrix metalloproteinases regulate migration, proliferation, and death of vascular smooth muscle cells by degrading matrix and non-matrix substrates. Cardiovasc Res 69: 614-624, 2006.
39. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84: 767-801, 2004.
40. Pastula C, Johnson I, Beechem JM, Patton WF. Development of fluorescence-based selective assays for serine/threonine and tyrosine phos-phatases. Comb Chem High Throughput Screen 6: 341-346, 2003.
41. Peyton KJ, Liu XM, Yu Y, Yates B, Durante W. Activation of AMP-activated protein kinase inhibits the proliferation of human endo-thelial cells. J Pharmacol Exp Ther 342: 827-834, 2012.
42. Peyton KJ, Yu Y, Yates B, Shebib AR, Liu XM, Wang H, Durante W. Compound C inhibits vascular smooth muscle cell proliferation and migration in an AMP-activated protein kinase-independent fashion. J Pharmacol Exp Ther 338: 476-484, 2011.
43. Raines EW, Ross R. Smooth muscle cells and the pathogenesis of the lesions of atherosclerosis. Br Heart J 69: S30-S37, 1993.
44. Rensen SS, Doevendans PA, van Eys GJ. Regulation and characteristics of vascular smooth muscle cell phenotypic diversity. Neth Heart J 15: 100-108, 2007.
45. Rossoni LV, Wareing M, Wenceslau CF, Al-Abri M, Cobb C, Austin C. Acute simvastatin increases endothelial nitric oxide synthase phosphor-ylation via AMP-activated protein kinase and reduces contractility of isolated rat mesenteric resistance arteries. Clin Sci (Lond) 121: 449-458, 2011.
46. 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.
47. 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.
48. Schaller MD. Cellular functions of FAK kinases: insight into molecular mechanisms and novel functions. J Cell Sci 123: 1007-1013, 2010.
49. Schirenbeck A, Arasada R, Bretschneider T, Stradal TE, Schleicher M, Faix J. The bundling activity of vasodilator-stimulated phosphoprotein is required for filopodium formation. Proc Natl Acad Sci USA 103: 7694-7699, 2006.
50. Scott JW, van Denderen BJ, Jorgensen SB, Honeyman JE, Steinberg GR, Oakhill JS, Iseli TJ, Koay A, Gooley PR, Stapleton D, Kemp BE. Thienopyridone drugs are selective activators of AMP-activated protein kinase beta1-containing complexes. Chem Biol 15: 1220-1230, 2008.
51. Song P, Wang S, He C, Liang B, Viollet B, Zou MH. AMPKalpha2 deletion exacerbates neointima formation by upregulating Skp2 in vascu lar smooth muscle cells. Circ Res 109: 1230-1239, 2011.
52. 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. Front Physiol 3: 409, 2012.
53. Sung JY, Choi HC. Aspirin-induced AMP-activated protein kinase activation regulates the proliferation of vascular smooth muscle cells from spontaneously hypertensive rats. Biochem Biophys Res Commun 408: 312-317, 2011.
54. Tomar A, Schlaepfer DD. Focal adhesion kinase: switching between GAPs and GEFs in the regulation of cell motility. Curr Opin Cell Biol 21: 676-683, 2009.
55. Tulis DA. Histological and morphometric analyses for rat carotid balloon injury model. Methods Mol Med 139: 31-66, 2007.
56. Tulis DA. Rat carotid artery balloon injury model. Methods Mol Med 139: 1-30, 2007.
57. Tulis DA, Bohl Masters KS, Lipke EA, Schiesser RL, Evans AJ, Peyton KJ, Durante W, West JL, Schafer AI. YC-1-mediated vascular protection through inhibition of smooth muscle cell proliferation and platelet function. Biochem Biophys Res Commun 291: 1014-1021, 2002.
58. Tulis DA, Durante W, Peyton KJ, Chapman GB, Evans AJ, Schafer AI. YC-1, a benzyl indazole derivative, stimulates vascular cGMP and inhibits neointima formation. Biochem Biophys Res Commun 279: 646-652, 2000.
59. Tulis DA, Durante W, Peyton KJ, Evans AJ, Schafer AI. Heme oxygenase-1 attenuates vascular remodeling following balloon injury in rat carotid arteries. Atherosclerosis 155: 113-122, 2001.
60. Tulis DA, Keswani AN, Peyton KJ, Wang H, Schafer AI, Durante W. Local administration of carbon monoxide inhibits neointima formation in balloon injured rat carotid arteries. Cell Mol Biol (Noisy-le-grand) 51: 441-446, 2005.
61. Tulis DA, Mnjoyan ZH, Schiesser RL, Shelat HS, Evans AJ, Zoldhelyi P, Fujise K. Adenoviral gene transfer of fortilin attenuates neointima formation through suppression of vascular smooth muscle cell proliferation and migration. Circulation 107: 98-105, 2003.
62. Woods A, Vertommen D, Neumann D, Turk R, Bayliss J, Schlattner U, Wallimann T, Carling D, Rider MH. Identification of phosphoryla-tion 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, 2003.
63. Woods AJ, Kantidakis T, Sabe H, Critchley DR, Norman JC. Interaction of paxillin with poly(A)-binding protein 1 and its role in focal adhesion turnover and cell migration. Mol Cell Biol 25: 3763-3773, 2005.
64. Yang XP, Thomas DP, Zhang XC, Culver BW, Alexander BM, Murdoch WJ, Rao MN, Tulis DA, Ren J, Sreejayan N. Curcumin inhibits platelet-derived growth factor-stimulated vascular smooth muscle cell function and injury-induced neointima formation. Arterioscler Thromb Vasc Biol 26: 85-90, 2006.