Journal of Molecular and Cellular Cardiology
Volume 48, Issue 3 , Pages 512-517 , March 2010

Ventricular remodeling and function: Insights using murine echocardiography

  • Marielle Scherrer-Crosbie

      Affiliations

    • Corresponding Author InformationCorresponding author. Cardiac Ultrasound Laboratory, Massachusetts General Hospital, 55 Fruit Street, Boston, MA 02114, USA. Tel.: +1 617 726 7686; fax: +1 617 726 8383.
  • ,
  • Baptiste Kurtz

Received 26 April 2009 ,Revised 19 June 2009 ,Accepted 7 July 2009.

References 

  1. Diez J, Querejeta R, Lopez B, Gonzalez A, Larman M, Martinez Ubago JL. Losartan-dependent regression of myocardial fibrosis is associated with reduction of left ventricular chamber stiffness in hypertensive patients. Circulation. 2002 May;28(105):2512–2517
  2. Berk BC, Fujiwara K, Lehoux S. ECM remodeling in hypertensive heart disease. J. Clin. Invest. 2007 Mar;117:568–575
  3. Thomas CV, Coker ML, Zellner JL, Handy JR, Crumbley AJ, Spinale FG. Increased matrix metalloproteinase activity and selective upregulation in LV myocardium from patients with end-stage dilated cardiomyopathy. Circulation. 1998 May;5(97):1708–1715
  4. Spinale FG. Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol. Rev. 2007 Oct;87:1285–1342
  5. Ducharme A, Frantz S, Aikawa M, Rabkin E, Lindsey M, Rodhe L, et al. Targeted deletion of MMP-9 attenuates left ventricular enlargement and collagen accumulation after experimental myocardial infarction. J. Clin. Invest. 2000;106:55–62
  6. Heymans S, Lupu F, Terclavers S, Vanwetswinkel B, Herbert JM, Baker A, et al. Loss or inhibition of uPA or MMP-9 attenuates LV remodeling and dysfunction after acute pressure overload in mice. Am. J. Pathol. 2005 Jan;166:15–25
  7. Matsumura S, Iwanaga S, Mochizuki S, Okamoto H, Ogawa S, Okada Y. Targeted deletion or pharmacological inhibition of MMP-2 prevents cardiac rupture after myocardial infarction in mice. J. Clin. Invest. 2005 Mar;115:599–609
  8. Ikonomidis JS, Hendrick JW, Parkhurst AM, Herron AR, Escobar PG, Dowdy KB, et al. Accelerated LV remodeling after myocardial infarction in TIMP-1-deficient mice: effects of exogenous MMP inhibition. Am. J. Physiol., Heart Circ. Physiol. 2005 Jan;288:H149–H158
  9. Fedak PW, Smookler DS, Kassiri Z, Ohno N, Leco KJ, Verma S, et al. TIMP-3 deficiency leads to dilated cardiomyopathy. Circulation. 2004 Oct;19(110):2401–2409
  10. Roth DM, Swaney JS, Dalton ND, Gilpin EA, Ross J. Impact of anesthesia on cardiac function during echocardiography in mice. Am. J. Physiol., Heart Circ. Physiol. 2002;282:H2134–H2140
  11. Yang XP, Liu YH, Rhaleb NE, Kurihara N, Kim HE, Carretero OA. Echocardiographic assessment of cardiac function in conscious and anesthetized mice. Am. J. Physiol. 1999;277:H1967–H1974
  12. Scherrer-Crosbie M, Steudel W, Ullrich R, Hunziker PR, Liel-Cohen N, Newell J, et al. Echocardiographic determination of risk area size in a murine model of myocardial ischemia. Am. J. Physiol. 1999;277:H986–H992
  13. Tarin D, Sturdee A. Surgical anaesthesia of mice: evaluation of tribromo-ethanol, ether, halothane and methoxyflurane and development of a reliable technique. Lab. Anim. 1972;6:79–84
  14. Wyatt HL, Heng MK, Meerbaum S, Gueret P, Hestenes J, Dula E, et al. Cross-sectional echocardiography: II. Analysis of mathematic models for quantifying volume of the formalin-fixed left ventricle. Circulation. 1980 Jun;61:1119–1125
  15. Hataishi R, Rodrigues AC, Neilan TG, Morgan JG, Buys E, Shiva S, et al. Inhaled nitric oxide decreases infarction size and improves left ventricular function in a murine model of myocardial ischemia–reperfusion injury. Am. J. Physiol., Heart Circ. Physiol. 2006 Jul;291:H379–H384
  16. Scherrer-Crosbie M, Ullrich R, Bloch KD, Nakajima H, Aretz HT, Lindsey ML, et al. Nitric oxide synthase 3 limits left ventricular remodeling after myocardial infarction in mice. Circulation. 2001;104:1286–1291
  17. Collins KA, Korcarz CE, Shroff SG, Bednarz JE, Fentzke RC, Lin H, et al. Accuracy of echocardiographic estimates of left ventricular mass in mice. Am. J. Physiol., Heart Circ. Physiol. 2001;280:H1954–H1962
  18. Scherrer-Crosbie M, Steudel W, Hunziker PR, Liel-Cohen N, Ullrich R, Zapol WM, et al. Three-dimensional echocardiographic assessment of left ventricular wall motion abnormalities in mouse myocardial infarction. J. Am. Soc. Echocardiogr. 1999;12:834–840
  19. Dawson D, Lygate CA, Saunders J, Schneider JE, Ye X, Hulbert K, et al. Quantitative 3-dimensional echocardiography for accurate and rapid cardiac phenotype characterization in mice. Circulation. 2004;110:1632–1637
  20. Williams RV, Lorenz JN, Witt SA, Hellard DT, Khoury PR, Kimball TR. End-systolic stress-velocity and pressure–dimension relationships by transthoracic echocardiography in mice. Am. J. Physiol. 1998;274:H1828–H1835
  21. Ullrich R, Scherrer-Crosbie M, Bloch KD, Ichinose F, Nakajima H, Picard MH, et al. Congenital deficiency of nitric oxide synthase 2 protects against endotoxin-induced myocardial dysfunction in mice. Circulation. 2000 Sep;19(102):1440–1446
  22. Sebag IA, Handschumacher MD, Ichinose F, Morgan JG, Hataishi R, Rodrigues AC, et al. Quantitative assessment of regional myocardial function in mice by tissue Doppler imaging: comparison with hemodynamics and sonomicrometry. Circulation. 2005 May;24(111):2611–2616
  23. Derumeaux G, Ichinose F, Raher MJ, Morgan JG, Coman T, Lee C, et al. Myocardial alterations in senescent mice and effect of exercise training: a strain rate imaging study. Circ. Cardiovasc. Imag. 2008;1:227–234
  24. Neilan TN, Jassal DS, Perez-Sanz TM, Raher MJ, Pradhan AD, Buys ES, et al. Tissue Doppler imaging predicts left ventricular dysfunction and mortality in a murine model of cardiac injury. Eur. Heart J. 2006;27:1868–1875
  25. Thibault H, Gomez L, Donal E, Augeul L, Scherrer-Crosbie M, Ovize M, et al. Regional myocardial function after myocardial infarction in mice: a follow-up study by strain rate imaging. J. Am. Soc. Echocardiogr. 2009 Feb;22:198–205
  26. Li Y, Garson CD, Xu Y, Beyers RJ, Epstein FH, French BA, et al. Quantification and MRI validation of regional contractile dysfunction in mice post myocardial infarction using high resolution ultrasound. Ultrasound Med. Biol. 2007 Jun;33:894–904
  27. Ichihara S, Senbonmatsu T, Price E, Ichiki T, Gaffney FA, Inagami T. Angiotensin II type 2 receptor is essential for left ventricular hypertrophy and cardiac fibrosis in chronic angiotensin II-induced hypertension. See comment. Circulation. 2001;104:346–351
  28. Schaefer A, Meyer GP, Hilfiker-Kleiner D, Brand B, Drexler H, Klein G. Evaluation of tissue Doppler tei index for global left ventricular function in mice after myocardial infarction: comparison with pulsed Doppler tei index. Eur. J. Echocardiogr. 2005 Oct;6:367–375
  29. Prunier F, Gaertner R, Louedec L, Michel JB, Mercadier JJ, Escoubet B. Doppler echocardiographic estimation of left ventricular end-diastolic pressure after MI in rats. Am. J. Physiol., Heart Circ. Physiol. 2002 Jul;283:H346–H352
  30. Parlakian A, Charvet C, Escoubet B, Mericskay M, Molkentin JD, Gary-Bobo G, et al. Temporally controlled onset of dilated cardiomyopathy through disruption of the SRF gene in adult heart. Circulation. 2005 Nov;8(112):2930–2939
  31. Du J, Liu J, Feng HZ, Hossain MM, Gobara N, Zhang C, et al. Impaired relaxation is the main manifestation in transgenic mice expressing a restrictive cardiomyopathy mutation, R193H, in cardiac TnI. Am. J. Physiol., Heart Circ. Physiol. 2008 Jun;294:H2604–H2613
  32. Duncker DJ, de Beer VJ, Merkus D. Alterations in vasomotor control of coronary resistance vessels in remodelled myocardium of swine with a recent myocardial infarction. Med. Biol. Eng. Comput. 2008 May;46:485–497
  33. Cai W, Vosschulte R, Afsah-Hedjri A, Koltai S, Kocsis E, Scholz D, et al. Altered balance between extracellular proteolysis and antiproteolysis is associated with adaptive coronary arteriogenesis. J. Mol. Cell. Cardiol. 2000 Jun;32:997–1011
  34. Krishnan L, Hoying JB, Nguyen H, Song H, Weiss JA. Interaction of angiogenic microvessels with the extracellular matrix. Am. J. Physiol., Heart Circ. Physiol. 2007 Dec;293:H3650–H3658
  35. Wikstrom J, Gronros J, Bergstrom G, Gan LM. Functional and morphologic imaging of coronary atherosclerosis in living mice using high-resolution color Doppler echocardiography and ultrasound biomicroscopy. J. Am. Coll. Cardiol. 2005 Aug;16(46):720–727
  36. Hartley CJ, Reddy AK, Madala S, Michael LH, Entman ML, Taffet GE. Doppler estimation of reduced coronary flow reserve in mice with pressure overload cardiac hypertrophy. Ultrasound Med. Biol. 2008 Jun;34:892–901
  37. Wei K, Ragosta M, Thorpe J, Coggins M, Moos S, Kaul S. Noninvasive quantification of coronary blood flow reserve in humans using myocardial contrast echocardiography. Circulation. 2001;103:2560–2565
  38. Raher MJ, Thibault H, Poh KK, Liu R, Halpern EF, Derumeaux G, et al. In vivo characterization of murine myocardial perfusion using myocardial contrast echocardiography: validation and application in nitric oxide synthase 3-deficient mice. Circulation. 2007;116:1250–1257
  39. Raher MJ, Thibault HB, Buys ES, Kuruppu D, Shimizu N, Brownell AL, et al. A short duration of high-fat diet induces insulin resistance and predisposes to adverse left ventricular remodeling after pressure overload. Am. J. Physiol., Heart Circ. Physiol. 2008 Dec;295:H2495–H2502
  40. Kerut EK, Given M, Giles TD. Review of methods for texture analysis of myocardium from echocardiographic images: a means of tissue characterization. Echocardiography. 2003 Nov;20:727–736
  41. Maceira AM, Barba J, Varo N, Beloqui O, Diez J. Ultrasonic backscatter and serum marker of cardiac fibrosis in hypertensives. Hypertension. 2002 Apr;39:923–928
  42. Kovacs A, Courtois MR, Weinheimer CJ, Posdamer SH, Wallace KD, Holland MR, et al. Ultrasonic tissue characterization of the mouse myocardium: successful in vivo cyclic variation measurements. J. Am. Soc. Echocardiogr. 2004 Aug;17:883–892
  43. Chinali M, Romano C, Rocco A, Galderisi M, Betocchi S, De Simone G. Depth variation bias and interaction with gain setting in ultrasonic tissue characterization by integrated backscatter analysis. J. Am. Soc. Echocardiogr. 2003 Jan;16:54–60
  44. Wickline SA, Thomas LJ, Miller JG, Sobel BE, Perez JE. A relationship between ultrasonic integrated backscatter and myocardial contractile function. J. Clin. Invest. 1985 Dec;76:2151–2160
  45. Yang M, Krueger TM, Miller JG, Holland MR. Characterization of anisotropic myocardial backscatter using spectral slope, intercept and midband fit parameters. Ultrason. Imag. 2007 Apr;29:122–134
  46. St. John Sutton M, Sharpe N. Left ventricular remodeling after myocardial infarction: pathophysiology and therapy. Circulation. 2000;(101):2981–2989
  47. White HD, Norris RM, Brown MA, Brandt PW, Whitlock RM, Wild CJ. Left ventricular end-systolic volume as the major determinant of survival after recovery from myocardial infarction. Circulation. 1987;76:44–51
  48. Koren MJ, Devereux RB, Casale PN, Savage DD, Laragh JH. Relation of left ventricular mass and geometry to morbidity and mortality in uncomplicated essential hypertension. Ann. Inter. Med. 1991;114:345–352
  49. Patten RD, Aronovitz MJ, Deras-Mejia L, Pandian NG, Hanak GG, Smith JJ, et al. Ventricular remodeling in a mouse model of myocardial infarction. Am. J. Physiol. 1998;274:H1812–H1820
  50. Gao XM, Dart AM, Dewar E, Jennings G, Du XJ. Serial echocardiographic assessment of left ventricular dimensions and function after myocardial infarction in mice. Cardiovasc. Res. 2000;45:330–338
  51. Kanno S, Lerner DL, Schuessler RB, Betsuyaku T, Yamada KA, Saffitz JE, et al. Echocardiographic evaluation of ventricular remodeling in a mouse model of myocardial infarction. J. Am. Soc. Echocardiogr. 2002;15:601–609
  52. Rothermel BA, Berenji K, Tannous P, Kutschke W, Dey A, Nolan B, et al. Differential activation of stress–response signaling in load-induced cardiac hypertrophy and failure. Physiol. Genomics. 2005;23:18–27
  53. Peterson JT, Li H, Dillon L, Bryant JW. Evolution of matrix metalloprotease and tissue inhibitor expression during heart failure progression in the infarcted rat. Cardiovasc. Res. 2000 May;46:307–315
  54. Lin J, Davis HB, Dai Q, Chou YM, Craig T, Hinojosa-Laborde C, et al. Effects of early and late chronic pressure overload on extracellular matrix remodeling. Hypertens. Res. 2008 Jun;31:1225–1231
  55. Hayashidani S, Tsutsui H, Ikeuchi M, Shiomi T, Matsusaka H, Kubota T, et al. Targeted deletion of MMP-2 attenuates early LV rupture and late remodeling after experimental myocardial infarction. Am. J. Physiol., Heart Circ. Physiol. 2003 Sep;285:H1229–H1235
  56. Creemers EE, Davis JN, Parkhurst AM, Leenders P, Dowdy KB, Hapke E, et al. Deficiency of TIMP-1 exacerbates LV remodeling after myocardial infarction in mice. Am. J. Physiol., Heart Circ. Physiol. 2003 Jan;284:H364–H371
  57. Tian H, Cimini M, Fedak PW, Altamentova S, Fazel S, Huang ML, et al. TIMP-3 deficiency accelerates cardiac remodeling after myocardial infarction. J. Mol. Cell. Cardiol. 2007 Dec;43:733–743
  58. Matsusaka H, Ide T, Matsushima S, Ikeuchi M, Kubota T, Sunagawa K, et al. Targeted deletion of matrix metalloproteinase 2 ameliorates myocardial remodeling in mice with chronic pressure overload. Hypertension. 2006 Apr;47:711–717
  59. Kim HE, Dalal SS, Young E, Legato MJ, Weisfeldt ML, D'Armiento J. Disruption of the myocardial extracellular matrix leads to cardiac dysfunction. J. Clin. Invest. 2000 Oct;106:857–866
  60. Foronjy RF, Sun J, Lemaitre V, D'Armiento JM. Transgenic expression of matrix metalloproteinase-1 inhibits myocardial fibrosis and prevents the transition to heart failure in a pressure overload mouse model. Hypertens. Res. 2008 Apr;31:725–735
  61. Murohara T, Asahara T, Silver M, Bauters C, Masuda H, Kalka C, et al. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J. Clin. Invest. 1998;101:2567–2578
  62. Ritchie RH, Schiebinger RJ, LaPointe MC, Marsh JD. Angiotensin II-induced hypertrophy of adult rat cardiomyocytes is blocked by nitric oxide. Am. J. Physiol. 1998;275:H1370–H1374
  63. Kim NN, Villegas S, Summerour SR, Villarreal FJ. Regulation of cardiac fibroblast extracellular matrix production by bradykinin and nitric oxide. J. Mol. Cell. Cardiol. 1999;31:457–466
  64. Palmer RM, Ashton DS, Moncada S. Vascular endothelial cells synthesize nitric oxide from l-arginine. Nature. 1988 Jun;16(333):664–666
  65. Janssens S, Pokreisz P, Schoonjans L, Pellens M, Vermeersch P, Tjwa M, et al. Cardiomyocyte-specific overexpression of nitric oxide synthase 3 improves left ventricular performance and reduces compensatory hypertrophy after myocardial infarction. Circ. Res. 2004;94:1256–1262
  66. Jones SP, Greer JJ, van Haperen R, Duncker DJ, de Crom R, Lefer DJ. Endothelial nitric oxide synthase overexpression attenuates congestive heart failure in mice. Proc. Natl. Acad. Sci. U. S. A. 2003 Apr;15(100):4891–4896
  67. Ichinose F, Bloch KD, Wu JC, Hataishi R, Aretz HT, Picard MH, et al. Pressure overload-induced LV hypertrophy and dysfunction in mice are exacerbated by congenital NOS3 deficiency. Am. J. Physiol., Heart Circ. Physiol. 2004;286:H1070–H1075
  68. Buys E, Raher MJ, Blake SL, Neilan TG, Graveline AR, Passeri J, et al. Cardiomyocyte-restricted restoration of nitric oxide synthase 3 attenuates left ventricular remodeling after chronic pressure overload. Am. J. Physiol., Heart Circ. Physiol. 2007;293:H620–H627
  69. Hataishi R, Rodrigues AC, Morgan JG, Ichinose F, Derumeaux G, Bloch KD, et al. Nitric oxide synthase 2 and pressure-overload-induced left ventricular remodelling in mice. Exp. Physiol. 2006 May;91:633–639
  70. Salloum FN, Abbate A, Das A, Houser JE, Mudrick CA, Qureshi IZ, et al. Sildenafil (Viagra) attenuates ischemic cardiomyopathy and improves left ventricular function in mice. Am. J. Physiol., Heart Circ. Physiol. 2008 Mar;294:H1398–H1406
  71. Zhang P, Xu X, Hu X, van Deel ED, Zhu G, Chen Y. Inducible nitric oxide synthase deficiency protects the heart from systolic overload-induced ventricular hypertrophy and congestive heart failure. Circ. Res. 2007 Apr;13(100):1089–1098

PII: S0022-2828(09)00278-8

doi: 10.1016/j.yjmcc.2009.07.004

Journal of Molecular and Cellular Cardiology
Volume 48, Issue 3 , Pages 512-517 , March 2010