Reduced scar maturation and contractility lead to exaggerated left ventricular dilation after myocardial infarction in mice lacking AMPKα1

Journal of Molecular and Cellular Cardiology

Volumn 74, Issue , 2014, Pages 32-43

  Noppe, Gauthier ^a   Dufeys, Cécile ^a   Buchlin, Patricia ^a   Marquet, Nicolas ^a   Castanares Zapatero, Diego ^a   Balteau, Magali ^a   Hermida, Nerea ^a   Bouzin, Caroline ^a   Esfahani, Hrag ^a   Viollet, Benoit ^b,c,d   Bertrand, Luc ^a   Balligand, Jean Luc ^a   Vanoverschelde, Jean Louis ^a,c   Beauloye, Christophe ^a,e   Horman, Sandrine ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b INSTITUT COCHIN   (France)

^c CNRS   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e CLINIQUES UNIVERSITAIRES SAINT LUC   (Belgium)

Author keywords

AMPK; Cardiac fibroblast; Myocardial infarction; Myodifferentiation; Scar maturation

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; AMP ACTIVATED PROTEIN KINASE ALPHA1; COLLAGEN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE 14; PROTEIN LYSINE 6 OXIDASE; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; ACTIN; ALPHA-SMOOTH MUSCLE ACTIN, MOUSE; AMPK ALPHA1 SUBUNIT, MOUSE; AMPK ALPHA2 SUBUNIT, MOUSE; LOX PROTEIN, MOUSE; MITOGEN ACTIVATED PROTEIN KINASE P38; SCLEROPROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HEART INFARCTION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE CONTRACTILITY; HEART LEFT VENTRICLE ENDDIASTOLIC VOLUME; HEART LEFT VENTRICLE HYPERTROPHY; HEART MUSCLE CONTRACTILITY; HEART MUSCLE FIBROSIS; HEART VENTRICLE REMODELING; HUMAN; HUMAN CELL; MOLECULAR PATHOLOGY; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; SCAR FORMATION; WILD TYPE; ANIMAL; DEFICIENCY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HEART CONTRACTION; HEART MUSCLE; HEART MUSCLE CELL; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; SCAR; SIGNAL TRANSDUCTION;

ACTINS; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CELL PROLIFERATION; CICATRIX; EXTRACELLULAR MATRIX PROTEINS; FEMALE; GENE EXPRESSION REGULATION; MICE; MICE, KNOCKOUT; MYOCARDIAL CONTRACTION; MYOCARDIAL INFARCTION; MYOCARDIUM; MYOCYTES, CARDIAC; MYOFIBROBLASTS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN-LYSINE 6-OXIDASE; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA1; VENTRICULAR REMODELING;

EID: 84904758023     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.04.018     Document Type: Article

References (67)

1. Sun Y., Weber K.T. Angiotensin converting enzyme and myofibroblasts during tissue repair in the rat heart. J Mol Cell Cardiol 1996, 28:851-858.
2. Cleutjens J.P., Verluyten M.J., Smiths J.F., Daemen M.J. Collagen remodeling after myocardial infarction in the rat heart. Am J Pathol 1995, 147:325-338.
3. Weber K.T., Sun Y., Bhattacharya S.K., Ahokas R.A., Gerling I.C. Myofibroblast-mediated mechanisms of pathological remodelling of the heart. Nat Rev Cardiol 2013, 10:15-26.
4. Daskalopoulos E.P., Janssen B.J., Blankesteijn W.M. Myofibroblasts in the infarct area: concepts and challenges. Microsc Microanal 2012, 18:35-49.
5. Konstam M.A., Kramer D.G., Patel A.R., Maron M.S., Udelson J.E. Left ventricular remodeling in heart failure: current concepts in clinical significance and assessment. JACC Cardiovasc Imaging 2011, 4:98-108.
6. Porter K.E., Turner N.A. Cardiac fibroblasts: at the heart of myocardial remodeling. Pharmacol Ther 2009, 123:255-278.
7. Chen W., Frangogiannis N.G. Fibroblasts in post-infarction inflammation and cardiac repair. Biochim Biophys Acta 1833, 2013:945-953.
8. Zamilpa R., Lindsey M.L. Extracellular matrix turnover and signaling during cardiac remodeling following MI: causes and consequences. J Mol Cell Cardiol 2010, 48:558-563.
9. Peterson J.T., Li H., Dillon L., Bryant J.W. Evolution of matrix metalloprotease and tissue inhibitor expression during heart failure progression in the infarcted rat. Cardiovasc Res 2000, 46:307-315.
10. Dobaczewski M., Chen W., Frangogiannis N.G. Transforming growth factor (TGF)-beta signaling in cardiac remodeling. J Mol Cell Cardiol 2011, 51:600-606.
11. Deten A., Holzl A., Leicht M., Barth W., Zimmer H.G. Changes in extracellular matrix and in transforming growth factor beta isoforms after coronary artery ligation in rats. J Mol Cell Cardiol 2001, 33:1191-1207.
12. 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.
13. Iwata M., Cowling R.T., Yeo S.J., Greenberg B. Targeting the ACE2-Ang-(1-7) pathway in cardiac fibroblasts to treat cardiac remodeling and heart failure. J Mol Cell Cardiol 2011, 51:542-547.
14. Bujak M., Frangogiannis N.G. The role of TGF-beta signaling in myocardial infarction and cardiac remodeling. Cardiovasc Res 2007, 74:184-195.
15. Massague J., Wotton D. Transcriptional control by the TGF-beta/Smad signaling system. EMBO J 2000, 19:1745-1754.
16. Stratton R., Rajkumar V., Ponticos M., Nichols B., Shiwen X., Black C.M., et al. Prostacyclin derivatives prevent the fibrotic response to TGF-beta by inhibiting the Ras/MEK/ERK pathway. FASEB J 2002, 16:1949-1951.
17. Liu S., Xu S.W., Kennedy L., Pala D., Chen Y., Eastwood M., et al. FAK is required for TGFbeta-induced JNK phosphorylation in fibroblasts: implications for acquisition of a matrix-remodeling phenotype. Mol Biol Cell 2007, 18:2169-2178.
18. Vepachedu R., Gorska M.M., Singhania N., Cosgrove G.P., Brown K.K., Alam R. Unc119 regulates myofibroblast differentiation through the activation of Fyn and the p38 MAPK pathway. J Immunol 2007, 179:682-690.
19. Carling D., Mayer F.V., Sanders M.J., Gamblin S.J. AMP-activated protein kinase: nature's energy sensor. Nat Chem Biol 2011, 7:512-518.
20. Hardie D.G., Ross F.A., Hawley S.A. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 2012, 13:251-262.
21. Hawley S.A., Boudeau J., Reid J.L., Mustard K.J., Udd L., Makela T.P., et al. 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 2003, 2:28.
22. Hawley S.A., Pan D.A., Mustard K.J., Ross L., Bain J., Edelman A.M., et al. Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab 2005, 2:9-19.
23. Woods A., Dickerson K., Heath R., Hong S.P., Momcilovic M., Johnstone S.R., et al. Ca2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab 2005, 2:21-33.
24. Stapleton D., Mitchelhill K.I., Gao G., Widmer J., Michell B.J., Teh T., et al. Mammalian AMP-activated protein kinase subfamily. J Biol Chem 1996, 271:611-614.
25. Xing Y., Musi N., Fujii N., Zou L., Luptak I., Hirshman M.F., et al. Glucose metabolism and energy homeostasis in mouse hearts overexpressing dominant negative alpha2 subunit of AMP-activated protein kinase. J Biol Chem 2003, 278:28372-28377.
26. 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.
27. 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.
28. Gundewar S., Calvert J.W., Jha S., Toedt-Pingel I., Ji S.Y., Nunez D., et al. Activation of AMP-activated protein kinase by metformin improves left ventricular function and survival in heart failure. Circ Res 2009, 104:403-411.
29. Kim A.S., Miller E.J., Wright T.M., Li J., Qi D., Atsina K., et al. A small molecule AMPK activator protects the heart against ischemia-reperfusion injury. J Mol Cell Cardiol 2011, 51:24-32.
30. Castanares-Zapatero D., Bouleti C., Sommereyns C., Gerber B., Lecut C., Mathivet T., et al. Connection between cardiac vascular permeability, myocardial edema, and inflammation during sepsis: role of the alpha1AMP-activated protein kinase isoform. Crit Care Med 2013, 41:e411-e422.
31. Horman S., Morel N., Vertommen D., Hussain N., Neumann D., Beauloye C., et al. AMP-activated protein kinase phosphorylates and desensitizes smooth muscle myosin light chain kinase. J Biol Chem 2008, 283:18505-18512.
32. de Meester C., Timmermans A.D., Balteau M., Ginion A., Roelants V., Noppe G., et al. Role of AMP-activated protein kinase in regulating hypoxic survival and proliferation of mesenchymal stem cells. Cardiovasc Res 2013, 101:20-29.
33. Wang S., Song P., Zou M.H. Inhibition of AMP-activated protein kinase alpha (AMPKalpha) by doxorubicin accentuates genotoxic stress and cell death in mouse embryonic fibroblasts and cardiomyocytes: role of p53 and SIRT1. J Biol Chem 2012, 287:8001-8012.
34. Du J., Guan T., Zhang H., Xia Y., Liu F., Zhang Y. Inhibitory crosstalk between ERK and AMPK in the growth and proliferation of cardiac fibroblasts. Biochem Biophys Res Commun 2008, 368:402-407.
35. Igata M., Motoshima H., Tsuruzoe K., Kojima K., Matsumura T., Kondo T., et al. Adenosine monophosphate-activated protein kinase suppresses vascular smooth muscle cell proliferation through the inhibition of cell cycle progression. Circ Res 2005, 97:837-844.
36. Mishra R., Cool B.L., Laderoute K.R., Foretz M., Viollet B., Simonson M.S. AMP-activated protein kinase inhibits transforming growth factor-beta-induced Smad3-dependent transcription and myofibroblast transdifferentiation. J Biol Chem 2008, 283:10461-10469.
37. Hermida N., Markl A., Hamelet J., Van Assche T., Vanderper A., Herijgers P., et al. HMGCoA reductase inhibition reverses myocardial fibrosis and diastolic dysfunction through AMP-activated protein kinase activation in a mouse model of metabolic syndrome. Cardiovasc Res 2013, 99:44-54.
38. Nagata D., Mogi M., Walsh K. AMP-activated protein kinase (AMPK) signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress. J Biol Chem 2003, 278:31000-31006.
39. 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.
40. Ahluwalia A., Tarnawski A.S. Activation of the metabolic sensor-AMP activated protein kinase reverses impairment of angiogenesis in aging myocardial microvascular endothelial cells. Implications for the aging heart. J Physiol Pharmacol 2011, 62:583-587.
41. Ricour C., Delhaye S., Hato S.V., Olenyik T.D., Michel B., van Kuppeveld F.J., et al. Inhibition of mRNA export and dimerization of interferon regulatory factor 3 by Theiler's virus leader protein. J Gen Virol 2009, 90:177-186.
42. Junqueira L.C., Bignolas G., Brentani R.R. Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J 1979, 11:447-455.
43. Cerqueira M.D., Weissman N.J., Dilsizian V., Jacobs A.K., Kaul S., Laskey W.K., et al. Standardized myocardial segmentation and nomenclature for tomographic imaging of the heart. A statement for healthcare professionals from the Cardiac Imaging Committee of the Council on Clinical Cardiology of the American Heart Association. Circulation 2002, 105:539-542.
44. Hao J., Ju H., Zhao S., Junaid A., Scammell-La Fleur T., Dixon I.M. Elevation of expression of Smads 2, 3, and 4, decorin and TGF-beta in the chronic phase of myocardial infarct scar healing. J Mol Cell Cardiol 1999, 31:667-678.
45. Cieslik K.A., Taffet G.E., Crawford J.R., Trial J., Mejia Osuna P., Entman M.L. AICAR-dependent AMPK activation improves scar formation in the aged heart in a murine model of reperfused myocardial infarction. J Mol Cell Cardiol 2013, 63:26-36.
46. Zile M.R., Baicu C.F., Stroud R.E., Van Laer A., Arroyo J., Mukherjee R., et al. Pressure overload-dependent membrane type 1-matrix metalloproteinase induction: relationship to LV remodeling and fibrosis. Am J Physiol Heart Circ Physiol 2012, 302:H1429-H1437.
47. Beauloye C., Bertrand L., Horman S., Hue L. AMPK activation, a preventive therapeutic target in the transition from cardiac injury to heart failure. Cardiovasc Res 2011, 90:224-233.
48. Horman S., Beauloye C., Vanoverschelde J.L., Bertrand L. AMP-activated protein kinase in the control of cardiac metabolism and remodeling. Curr Heart Fail Rep 2012, 9:164-173.
49. Marsin A.S., Bertrand L., Rider M.H., Deprez J., Beauloye C., Vincent M.F., et al. Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr Biol 2000, 10:1247-1255.
50. Chen S., Zhu P., Guo H.M., Solis R.S., Wang Y., Ma Y., et al. Alpha1 catalytic subunit of AMPK modulates contractile function of cardiomyocytes through phosphorylation of troponin I. Life Sci 2014, 98:75-82.
51. Fredj S., Bescond J., Louault C., Potreau D. Interactions between cardiac cells enhance cardiomyocyte hypertrophy and increase fibroblast proliferation. J Cell Physiol 2005, 202:891-899.
52. Viereck J., Bang C., Foinquinos A., Thum T. Regulatory RNAs and paracrine networks in the heart. Cardiovasc Res 2014, 102:290-301.
53. Dolmatova E., Spagnol G., Boassa D., Baum J.R., Keith K., Ambrosi C., et al. Cardiomyocyte ATP release through pannexin 1 aids in early fibroblast activation. Am J Physiol Heart Circ Physiol 2012, 303:H1208-H1218.
54. Sun C.X., Zhong H., Mohsenin A., Morschl E., Chunn J.L., Molina J.G., et al. Role of A2B adenosine receptor signaling in adenosine-dependent pulmonary inflammation and injury. J Clin Invest 2006, 116:2173-2182.
55. Eckhouse S.R., Spinale F.G. Changes in the myocardial interstitium and contribution to the progression of heart failure. Heart Fail Clin 2012, 8:7-20.
56. Takeda N., Manabe I., Uchino Y., Eguchi K., Matsumoto S., Nishimura S., et al. Cardiac fibroblasts are essential for the adaptive response of the murine heart to pressure overload. J Clin Invest 2010, 120:254-265.
57. Balligand J.L., Feron O., Dessy C. eNOS activation by physical forces: from short-term regulation of contraction to chronic remodeling of cardiovascular tissues. Physiol Rev 2009, 89:481-534.
58. Zippel N., Malik R.A., Fromel T., Popp R., Bess E., Strilic B., et al. Transforming growth factor-beta-activated kinase 1 regulates angiogenesis via AMP-activated protein kinase-alpha1 and redox balance in endothelial cells. Arterioscler Thromb Vasc Biol 2013, 33:2792-2799.
59. 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.
60. Green A.S., Chapuis N., Maciel T.T., Willems L., Lambert M., Arnoult C., et al. The LKB1/AMPK signaling pathway has tumor suppressor activity in acute myeloid leukemia through the repression of mTOR-dependent oncogenic mRNA translation. Blood 2010, 116:4262-4273.
61. Gwinn D.M., Shackelford D.B., Egan D.F., Mihaylova M.M., Mery A., Vasquez D.S., et al. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 2008, 30:214-226.
62. Banko M.R., Allen J.J., Schaffer B.E., Wilker E.W., Tsou P., White J.L., et al. Chemical genetic screen for AMPKalpha2 substrates uncovers a network of proteins involved in mitosis. Mol Cell 2011, 44:878-892.
63. van den Borne S.W., van de Schans V.A., Strzelecka A.E., Vervoort-Peters H.T., Lijnen P.M., Cleutjens J.P., et al. Mouse strain determines the outcome of wound healing after myocardial infarction. Cardiovasc Res 2009, 84:273-282.
64. Tenhunen O., Soini Y., Ilves M., Rysa J., Tuukkanen J., Serpi R., et al. p38 Kinase rescues failing myocardium after myocardial infarction: evidence for angiogenic and anti-apoptotic mechanisms. FASEB J 2006, 20:1907-1909.
65. Momcilovic M., Hong S.P., Carlson M. Mammalian TAK1 activates Snf1 protein kinase in yeast and phosphorylates AMP-activated protein kinase in vitro. J Biol Chem 2006, 281:25336-25343.
66. Whittaker P., Kloner R.A., Boughner D.R., Pickering J.G. Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light. Basic Res Cardiol 1994, 89:397-410.
67. Poobalarahi F., Baicu C.F., Bradshaw A.D. Cardiac myofibroblasts differentiated in 3D culture exhibit distinct changes in collagen I production, processing, and matrix deposition. Am J Physiol Heart Circ Physiol 2006, 291:H2924-H2932.