AICAR-dependent AMPK activation improves scar formation in the aged heart in a murine model of reperfused myocardial infarction

Journal of Molecular and Cellular Cardiology

Volumn 63, Issue , 2013, Pages 26-36

  Cieslik, Katarzyna A ^a   Taffet, George E ^a   Crawford, Jeffrey R ^a   Trial, JoAnn ^a   Mejia Osuna, Patricia ^a   Entman, Mark L ^a  

^a HOUSTON METHODIST HOSPITAL   (United States)

Author keywords

Aging; AMPK; Fibroblast; MSC; Myocardial infarction; Scar formation

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; CD45 ANTIGEN; COLLAGEN; HERMES ANTIGEN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APICAL END DIASTOLIC DIMENSION; ARTICLE; CARDIOVASCULAR PARAMETERS; CELL DIFFERENTIATION; COLLAGEN METABOLISM; CONTROLLED STUDY; DISEASE DURATION; DISEASE MODEL; DRUG EFFECT; ENZYME ACTIVATION; FIBROBLAST; HEART EJECTION FRACTION; HEART INFARCTION; HEART MUSCLE ISCHEMIA; HEART OUTPUT; LEFT ANTERIOR DESCENDING CORONARY ARTERY; MALE; MESENCHYMAL STEM CELL; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; SCAR FORMATION; SIGNAL TRANSDUCTION; STEM CELL MOBILIZATION;

MURINAE; MUS;

AGING; AMPK; FIBROBLAST; MSC; MYOCARDIAL INFARCTION; SCAR FORMATION;

AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CICATRIX; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; FIBROBLASTS; MALE; MICE; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; MYOFIBROBLASTS; PHOSPHORYLATION; RIBONUCLEOTIDES; VENTRICULAR REMODELING; WOUND HEALING;

EID: 84881523187     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.07.005     Document Type: Article

References (61)

1. Roger V.L., Go A.S., Lloyd-Jones D.M., Benjamin E.J., Berry J.D., Borden W.B., et al. Heart disease and stroke statistics-2012 update: a report from the American Heart Association. Circulation 2012, 125:e2-e220.
2. Gould K.E., Taffet G.E., Michael L.H., Christie R.M., Konkol D.L., Pocius J.S., et al. Heart failure and greater infarct expansion in middle-aged mice: a relevant model for postinfarction failure. Am J Physiol Heart Circ Physiol 2002, 282:H615-H621.
3. Bujak M., Kweon H.J., Chatila K., Li N., Taffet G., Frangogiannis N.G. Aging-related defects are associated with adverse cardiac remodeling in a mouse model of reperfused myocardial infarction. J Am Coll Cardiol 2008, 51:1384-1392.
4. Carlson S., Trial J., Soeller C., Entman M.L. Cardiac mesenchymal stem cells contribute to scar formation after myocardial infarction. Cardiovasc Res 2011, 91:99-107.
5. Chen S.J., Yuan W., Mori Y., Levenson A., Trojanowska M., Varga J. Stimulation of type I collagen transcription in human skin fibroblasts by TGF-beta: involvement of Smad 3. J Invest Dermatol 1999, 112:49-57.
6. Desmouliere A., Geinoz A., Gabbiani F., Gabbiani G. Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol 1993, 122:103-111.
7. Cleutjens J.P., Blankesteijn W.M., Daemen M.J., Smits J.F. The infarcted myocardium: simply dead tissue, or a lively target for therapeutic interventions. Cardiovasc Res 1999, 44:232-241.
8. Crawford J.R., Haudek S.B., Cieslik K.A., Trial J., Entman M.L. Origin of developmental precursors dictates the pathophysiologic role of cardiac fibroblasts. J Cardiovasc Transl Res 2012, 5:749-759.
9. Cieslik K.A., Trial J., Entman M.L. Defective myofibroblast formation from mesenchymal stem cells in the aging murine heart rescue by activation of the AMPK pathway. Am J Pathol 2011, 179:1792-1806.
10. Russell R.R., Li J., Coven D.L., Pypaert M., Zechner C., Palmeri M., et al. AMP-activated protein kinase mediates ischemic glucose uptake and prevents postischemic cardiac dysfunction, apoptosis, and injury. J Clin Invest 2004, 114:495-503.
11. Kudo N., Gillespie J.G., Kung L., Witters L.A., Schulz R., Clanachan A.S., et al. Characterization of 5'AMP-activated protein kinase activity in the heart and its role in inhibiting acetyl-CoA carboxylase during reperfusion following ischemia. Biochim Biophys Acta 1996, 1301:67-75.
12. Carvajal K., Zarrinpashneh E., Szarszoi O., Joubert F., Athea Y., Mateo P., et al. Dual cardiac contractile effects of the alpha2-AMPK deletion in low-flow ischemia and reperfusion. Am J Physiol Heart Circ Physiol 2007, 292:H3136-H3147.
13. Zarrinpashneh E., Carjaval K., Beauloye C., Ginion A., Mateo P., Pouleur A.C., et al. Role of the alpha2-isoform of AMP-activated protein kinase in the metabolic response of the heart to no-flow ischemia. Am J Physiol Heart Circ Physiol 2006, 291:H2875-H2883.
14. Russell R.R., Bergeron R., Shulman G.I., Young L.H. Translocation of myocardial GLUT-4 and increased glucose uptake through activation of AMPK by AICAR. Am J Physiol 1999, 277:H643-H649.
15. Dzeja P.P., Chung S., Faustino R.S., Behfar A., Terzic A. Developmental enhancement of adenylate kinase-AMPK metabolic signaling axis supports stem cell cardiac differentiation. PLoS One 2011, 6:e19300.
16. Padmasekar M., Sharifpanah F., Finkensieper A., Wartenberg M., Sauer H. Stimulation of cardiomyogenesis of embryonic stem cells by nitric oxide downstream of AMP-activated protein kinase and mTOR signaling pathways. Stem Cells Dev 2011, 20:2163-2175.
17. Kim E.K., Lim S., Park J.M., Seo J.K., Kim J.H., Kim K.T., et al. Human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by AMP-activated protein kinase. J Cell Physiol 2012, 227:1680-1687.
18. Li X., Han Y., Pang W., Li C., Xie X., Shyy J.Y., et al. AMP-activated protein kinase promotes the differentiation of endothelial progenitor cells. Arterioscler Thromb Vasc Biol 2008, 28:1789-1795.
19. Nossuli T.O., Lakshminarayanan V., Baumgarten G., Taffet G.E., Ballantyne C.M., Michael L.H., et al. A chronic mouse model of myocardial ischemia-reperfusion: essential in cytokine studies. Am J Physiol Heart Circ Physiol 2000, 278:H1049-H1055.
20. Cieslik K.A., Taffet G.E., Carlson S., Hermosillo J., Trial J., Entman M.L. Immune-inflammatory dysregulation modulates the incidence of progressive fibrosis and diastolic stiffness in the aging heart. J Mol Cell Cardiol 2011, 50:248-256.
21. Quinones M.A., Waggoner A.D., Reduto L.A., Nelson J.G., Young J.B., Winters W.L., et al. A new, simplified and accurate method for determining ejection fraction with two-dimensional echocardiography. Circulation 1981, 64:744-753.
22. Beckstead J.H. A simple technique for preservation of fixation-sensitive antigens in paraffin-embedded tissues. J Histochem Cytochem 1994, 42:1127-1134.
23. Constantine V.S., Mowry R.W. Selective staining of human dermal collagen. II. The use of picrosirius red F3BA with polarization microscopy. J Invest Dermatol 1968, 50:419-423.
24. Junqueira L.C., Cossermelli W., Brentani R. Differential staining of collagens type I, II and III by sirius red and polarization microscopy. Arch Histol Jpn 1978, 41:267-274.
25. Briaud S.A., Ding Z.M., Michael L.H., Entman M.L., Daniel S., Ballantyne C.M. Leukocyte trafficking and myocardial reperfusion injury in ICAM-1/P-selectin-knockout mice. Am J Physiol Heart Circ Physiol 2001, 280:H60-H67.
26. Hawley S.A., Davison M., Woods A., Davies S.P., Beri R.K., Carling D., et al. Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. J Biol Chem 1996, 271:27879-27887.
27. Baskin K.K., Taegtmeyer H. AMP-activated protein kinase regulates E3 ligases in rodent heart. Circ Res 2011, 109:1153-1161.
28. Dewald O., Zymek P., Winkelmann K., Koerting A., Ren G., Abou-Khamis T., et al. CCL2/monocyte chemoattractant protein-1 regulates inflammatory responses critical to healing myocardial infarcts. Circ Res 2005, 96:881-889.
29. Yano T., Miura T., Ikeda Y., Matsuda E., Saito K., Miki T., et al. Intracardiac fibroblasts, but not bone marrow derived cells, are the origin of myofibroblasts in myocardial infarct repair. Cardiovasc Pathol 2005, 14:241-246.
30. Martinelli R., Gegg M., Longbottom R., Adamson P., Turowski P., Greenwood J. ICAM-1-mediated endothelial nitric oxide synthase activation via calcium and AMP-activated protein kinase is required for transendothelial lymphocyte migration. Mol Biol Cell 2009, 20:995-1005.
31. Zhang Y., Qiu J., Wang X., Xia M. AMP-activated protein kinase suppresses endothelial cell inflammation through phosphorylation of transcriptional coactivator p300. Arterioscler Thromb Vasc Biol 2011, 31:2897-2908.
32. van Wijk B., Gunst Q.D., Moorman A.F., van den Hoff M.J. Cardiac regeneration from activated epicardium. PLoS One 2012, 7:e44692.
33. Sridurongrit S., Larsson J., Schwartz R., Ruiz-Lozano P., Kaartinen V. Signaling via the Tgf-beta type I receptor Alk5 in heart development. Dev Biol 2008, 322:208-218.
34. Rich L., Whitteker P. Collagen and picrosirius red staining: a polarized light assessment of fibrillar hue and spatial distribution. Braz J Morphol Sci 2005, 22:97-104.
35. MacKenna D.A., Omens J.H., McCulloch A.D., Covell J.W. Contribution of collagen matrix to passive left ventricular mechanics in isolated rat hearts. Am J Physiol 1994, 266:H1007-H1018.
36. Jelani A., Jugdutt B.I. STEMI and heart failure in the elderly: role of adverse remodeling. Heart Fail Rev 2010, 15:513-521.
37. Sos M.L., Fischer S., Ullrich R., Peifer M., Heuckmann J.M., Koker M., et al. Identifying genotype-dependent efficacy of single and combined PI3K- and MAPK-pathway inhibition in cancer. Proc Natl Acad Sci U S A 2009, 106:18351-18356.
38. Zaha V.G., Young L.H. AMP-activated protein kinase regulation and biological actions in the heart. Circ Res 2012, 111:800-814.
39. Chan A.Y., Soltys C.L., Young M.E., Proud C.G., Dyck J.R. Activation of AMP-activated protein kinase inhibits protein synthesis associated with hypertrophy in the cardiac myocyte. J Biol Chem 2004, 279:32771-32779.
40. Paiva M.A., Goncalves L.M., Providencia L.A., Davidson S.M., Yellon D.M., Mocanu M.M. Transitory activation of AMPK at reperfusion protects the ischaemic-reperfused rat myocardium against infarction. Cardiovasc Drugs Ther 2010, 24:25-32.
41. Kingma J.G., Simard D., Rouleau J.R. Timely administration of AICA riboside reduces reperfusion injury in rabbits. Cardiovasc Res 1994, 28:1003-1007.
42. Kristiansen S.B., Solskov L., Jessen N., Lofgren B., Schmitz O., Nielsen-Kudsk J.E., et al. 5-Aminoimidazole-4-carboxamide-1-beta-d-ribofuranoside increases myocardial glucose uptake during reperfusion and induces late pre-conditioning: potential role of AMP-activated protein kinase. Basic Clin Pharmacol Toxicol 2009, 105:10-16.
43. Bujak M., Frangogiannis N.G. The role of TGF-beta signaling in myocardial infarction and cardiac remodeling. Cardiovasc Res 2007, 74:184-195.
44. Dewald O., Ren G., Duerr G.D., Zoerlein M., Klemm C., Gersch C., et al. Of mice and dogs: species-specific differences in the inflammatory response following myocardial infarction. Am J Pathol 2004, 164:665-677.
45. Gabbiani G. The myofibroblast in wound healing and fibrocontractive diseases. J Pathol 2003, 200:500-503.
46. Serini G., Gabbiani G. Mechanisms of myofibroblast activity and phenotypic modulation. Exp Cell Res 1999, 250:273-283.
47. Hinz B., Celetta G., Tomasek J.J., Gabbiani G., Chaponnier C. Alpha-smooth muscle actin expression upregulates fibroblast contractile activity. Mol Biol Cell 2001, 12:2730-2741.
48. Hu B., Wu Z., Phan S.H. Smad3 mediates transforming growth factor-beta-induced alpha-smooth muscle actin expression. Am J Respir Cell Mol Biol 2003, 29:397-404.
49. Shanley C.J., Gharaee-Kermani M., Sarkar R., Welling T.H., Kriegel A., Ford J.W., et al. Transforming growth factor-beta 1 increases lysyl oxidase enzyme activity and mRNA in rat aortic smooth muscle cells. J Vasc Surg 1997, 25:446-452.
50. Li J., Miller E.J., Ninomiya-Tsuji J., Russell R.R., Young L.H. AMP-activated protein kinase activates p38 mitogen-activated protein kinase by increasing recruitment of p38 MAPK to TAB1 in the ischemic heart. Circ Res 2005, 97:872-879.
51. Stone J.D., Narine A., Shaver P.R., Fox J.C., Vuncannon J.R., Tulis D.A. AMP-activated protein kinase inhibits vascular smooth muscle cell proliferation and migration and vascular remodeling following injury. Am J Physiol Heart Circ Physiol 2013, 304:H369-H381.
52. Moopanar T.R., Xiao X.H., Jiang L., Chen Z.P., Kemp B.E., Allen D.G. AICAR inhibits the Na+/H+ exchanger in rat hearts-possible contribution to cardioprotection. Pflugers Arch 2006, 453:147-156.
53. Jin J., Mullen T.D., Hou Q., Bielawski J., Bielawska A., Zhang X., et al. AMPK inhibitor Compound C stimulates ceramide production and promotes Bax redistribution and apoptosis in MCF7 breast carcinoma cells. J Lipid Res 2009, 50:2389-2397.
54. Yang Z., Wang X., He Y., Qi L., Yu L., Xue B., et al. The full capacity of AICAR to reduce obesity-induced inflammation and insulin resistance requires myeloid SIRT1. PLoS One 2012, 7:e49935.
55. Gaidhu M.P., Fediuc S., Anthony N.M., So M., Mirpourian M., Perry R.L., et al. Prolonged AICAR-induced AMP-kinase activation promotes energy dissipation in white adipocytes: novel mechanisms integrating HSL and ATGL. J Lipid Res 2009, 50:704-715.
56. Treebak J.T., Birk J.B., Hansen B.F., Olsen G.S., Wojtaszewski J.F. A-769662 activates AMPK beta1-containing complexes but induces glucose uptake through a PI3-kinase-dependent pathway in mouse skeletal muscle. Am J Physiol Cell Physiol 2009, 297:C1041-C1052.
57. Ouyang J., Parakhia R.A., Ochs R.S. Metformin activates AMP kinase through inhibition of AMP deaminase. J Biol Chem 2011, 286:1-11.
58. Gaskin F.S., Kamada K., Yusof M., Korthuis R.J. 5'-AMP-activated protein kinase activation prevents postischemic leukocyte-endothelial cell adhesive interactions. Am J Physiol Heart Circ Physiol 2007, 292:H326-H332.
59. Miller E.J., Li J., Leng L., McDonald C., Atsumi T., Bucala R., et al. Macrophage migration inhibitory factor stimulates AMP-activated protein kinase in the ischaemic heart. Nature 2008, 451:578-582.
60. Ma H., Wang J., Thomas D.P., Tong C., Leng L., Wang W., et al. Impaired macrophage migration inhibitory factor-AMP-activated protein kinase activation and ischemic recovery in the senescent heart. Circulation 2010, 122:282-292.
61. Newman M.F., Ferguson T.B., White J.A., Ambrosio G., Koglin J., Nussmeier N.A., et al. Effect of adenosine-regulating agent acadesine on morbidity and mortality associated with coronary artery bypass grafting: the RED-CABG randomized controlled trial. JAMA 2012, 308:157-164.