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Int J Sports Med 2017; 38(1): 27-34
DOI: 10.1055/s-0042-115567
Physiology & Biochemistry
© Georg Thieme Verlag KG Stuttgart · New York

Effects of pericardiectomy on training- and myocardial infarction-induced left ventricular hypertrophy, chamber dimensions and gene expression

A. M. Wolff   *
1   Division of Kinesiology & Health
2   Department of Molecular Biology, University of Wyoming, Laramie, Wyoming 82071, USA
,
T. P. Rasmussen   *
1   Division of Kinesiology & Health
,
C. R. Wichern
1   Division of Kinesiology & Health
,
M. R. Peterson
1   Division of Kinesiology & Health
,
M. M. Stayton
2   Department of Molecular Biology, University of Wyoming, Laramie, Wyoming 82071, USA
,
D. P. Thomas
1   Division of Kinesiology & Health
› Author Affiliations
Further Information

Publication History



accepted after revision 08 September 2016

Publication Date:
13 October 2016 (online)

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Abstract

The primary purpose of the study was to evaluate whether a pericardiectomy (PERI) alters training- or myocardial infarction (MI)-induced left ventricular hypertrophy (LVH), chamber geometry, gene expression and/or running performance. Mice were randomized into 6 groups: naïve control (CONT)-sedentary (Sed), CONT-trained (Tr), PERI-Sed, PERI-Tr, MI-Sed and MI-Tr. MI mice also received a pericardiectomy as part of the MI surgical procedure. 10 weeks of treadmill running resulted in enhanced running performance-to-exhaustion in all 3 trained groups (CONT-Tr, PERI-Tr, MI-Tr) compared to sedentary cohorts (P<0.001). Training also resulted in similar increases in normalized LVH (LV/BW) in CONT-Tr and PERI-Tr mice. 2D-echocardiographic evaluation of LV internal chamber dimensions revealed that stroke diameter (SD) was larger in PERI compared to MI (P<0.01) but not CONT mice. Ventricular B-type natriuretic peptide mRNA (BNP) was elevated only in the 2 MI groups. Left ventricle β1-adrenergic receptor (β1-AR) and melusin transcripts both demonstrated an overall increase in trained compared to sedentary mice (both P<0.05). Additionally long-term pericardiectomy did not further enhance running performance or increase LV/BW in either sedentary or trained mice.

Key words

infarction - left ventricular dilation - melusin - pericardiectomy - training

* Both authors contributed equally to the study


 

  • References

  • 1 Arbab-Zadeh A, Perhonen M, Howden E, Peshock RM, Zhang R, Adams-Huet B, Haykowsky MJ, Levine BD. Cardiac remodeling in response to 1 year of intensive endurance training. Circulation 2014; 130: 2152-2161
    CrossrefPubMedGoogle Scholar
  • 2 Aro J, Tokola H, Ronkainen V-P, Koivisto E, Tenhunen O, Ilves M, Szokodi I, Ruskoaho H, Rysä J. Regulation of cardiac melusin gene expression by hypertrophic stimuli in the rat. Acta Physiol 2013; 207: 470-484
    CrossrefPubMedGoogle Scholar
  • 3 Bayat H, Swaney JS, Ander AN, Dalton N, Kennedy BP, Hammond HK, Roth DM. Progressive heart failure after myocardial infarction in mice. Basic Res Cardiol 2002; 97: 206-213
    CrossrefPubMedGoogle Scholar
  • 4 De Acetis M. Cardiac Overexpression of melusin protects from dilated cardiomyopathy due to long-standing pressure overload. Circ Res 2005; 96: 1087-1094
    CrossrefPubMedGoogle Scholar
  • 5 De Waard MC, van der Velden J, Bito V, Ozdemir S, Biesmans L, Boontje NM, Dekkers DHW, Schoonderwoerd K, Schuurbiers HCH, Crom Rd, Stienen GJM, Sipido KR, Lamers JMJ, Duncker DJ. Early exercise training normalizes myofilament function and attenuates left ventricular pump dysfunction in mice with a large myocardial infarction. Circ Res 2007; 100: 1079-1088
    CrossrefPubMedGoogle Scholar
  • 6 Evangelista FS, Krieger JE. Small gene effect and exercise training-induced cardiac hypertrophy in mice: an Ace gene dosage study. Physiol Genomics 2006; 27: 231-236
    CrossrefPubMedGoogle Scholar
  • 7 Everaert BR, Boulet GA, Timmermans J-P, Vrints CJ. Importance of suitable reference gene selection for quantitative real-time PCR: Special reference to mouse myocardial infarction studies. PLoS ONE 2011; 6: e23793
    CrossrefPubMedGoogle Scholar
  • 8 Fernandes T, Hashimoto NY, Magalhães FC, Fernandes FB, Casarini DE, Carmona AK, Krieger JE, Phillips MI, Oliveira EM. Aerobic exercise training–induced left ventricular hypertrophy involves regulatory micrornas, decreased angiotensin-converting enzyme-angiotensin ii, and synergistic regulation of angiotensin-converting enzyme 2-angiotensin (1–7). Hypertension 2011; 58: 182-189
    CrossrefPubMedGoogle Scholar
  • 9 Finsen AV. Echocardiographic parameters discriminating myocardial infarction with pulmonary congestion from myocardial infarction without congestion in the mouse. J Appl Physiol 2004; 98: 680-689
    CrossrefPubMedGoogle Scholar
  • 10 Fishbein MC, Maclean D, Maroko PR. Experimental myocardial infarction in the rat: qualitative and quantitative changes during pathologic evolution. Am J Pathol 1978; 90: 57-70
    PubMedGoogle Scholar
  • 11 Fujii N, Shibata T, Homma S, Ikegami H, Murakami K, Miyazaki H. Exercise-induced changes in β-adrenergic-receptor mRNA level measured by competitive RT-PCR. J Appl Physiol 1997; 82: 1926-1931
    CrossrefPubMedGoogle Scholar
  • 12 Goetze JP, Christoffersen C, Perko M, Arendrup H, Rehfeld JF, Kastrup J, Nielsen LB. Increased cardiac BNP expression associated with myocardial ischemia. FASEB J 2003; 17: 1105-1107
    PubMedGoogle Scholar
  • 13 Hammond HK, White FC, Bhargava V, Shabetai R. Heart size and maximal cardiac output are limited by the pericardium. Am J Physiol 1992; 263: H1675-H1681
    PubMedGoogle Scholar
  • 14 Harpster MH, Bandyopadhyay S, Thomas DP, Ivanov PS, Keele JA, Pineguina N, Gao B, Amarendran V, Gomelsky M, McCormick RJ, Stayton MM. Earliest changes in the left ventricular transcriptome post-myocardial infarction. Mamm Genome 2006; 17: 701-715
    CrossrefPubMedGoogle Scholar
  • 15 Harriss DJ, Atkinson G. Ethical standards in sport and exercise science research: 2016 update. Int J Sports Med 2015; 36: 1121-1124
    Google Scholar
  • 16 Houser SR, Margulies KB, Murphy AM, Spinale FG, Francis GS, Prabhu SD, Rockman HA, Kass DA, Molkentin JD, Sussman MA, Koch WJ. Animal models of heart failure: A scientific statement from the american heart association. Circ Res 2012; 111: 131-150
    CrossrefPubMedGoogle Scholar
  • 17 Høydal MA, Wisløff U, Kemi OJ, Ellingsen Ø. Running speed and maximal oxygen uptake in rats and mice: practical implications for exercise training. Eur J Cardiovasc Prev Rehabil 2007; 14: 753-760
    CrossrefPubMedGoogle Scholar
  • 18 Iemitsu M, Miyauchi T, Maeda S, Sakai S, Kobayashi T, Fujii N, Miyazaki H, Matsuda M, Yamaguchi I. Physiological and pathological cardiac hypertrophy induce different molecular phenotypes in the rat. Am J Physiol 2001; 281: R2029-R2036
    CrossrefPubMedGoogle Scholar
  • 19 Kemi OJ, Loennechen JP, Wisløff U, Ellingsen Ø. Intensity-controlled treadmill running in mice: cardiac and skeletal muscle hypertrophy. J Appl Physiol 2002; 93: 1301-1309
    CrossrefPubMedGoogle Scholar
  • 20 Leosco D, Rengo G, Iaccarino G, Golino L, Marchese M, Fortunato F, Zincarelli C, Sanzari E, Ciccarelli M, Galasso G, Altobelli GG, Conti V, Matrone G, Cimini V, Ferrara N, Filippelli A, Koch WJ, Rengo F. Exercise promotes angiogenesis and improves beta-adrenergic receptor signalling in the post-ischaemic failing rat heart. Cardiovasc Res 2008; 78: 385-394
    CrossrefPubMedGoogle Scholar
  • 21 Mair J, Wagner I, Jakob G, Lechleitner P, Dienstl F, Puschendorf B, Michel G. Different time courses of cardiac contractile proteins after acute myocardial infarction. Clin Chim Acta 1994; 231: 47-60
    CrossrefPubMedGoogle Scholar
  • 22 McCormick RJ, Musch TI, Bergman BC, Thomas DP. Regional differences in LV collagen accumulation and mature cross-linking after myocardial infarction in rats. Am J Physiol 1994; 266: H354-H359
    PubMedGoogle Scholar
  • 23 Mercadier J-J, Lompré A-M, Wisnewsky C, Samuel J-L, Bercovici J, Swynghedauw B, Schwartz K. Myosin isoenzyme changes in several models of rat cardiac hypertrophy. Circ Res 1981; 49: 525-532
    CrossrefPubMedGoogle Scholar
  • 24 Moreira JBN, Bechara LRG, Bozi LHM, Jannig PR, Monteiro AWA, Dourado PM, Wisløff U, Brum PC. High- versus moderate-intensity aerobic exercise training effects on skeletal muscle of infarcted rats. J Appl Physiol Bethesda Md 1985 2013; 114: 1029-1041
    PubMedGoogle Scholar
  • 25 Naimark WA, Lee JM, Limeback H, Cheung DT. Correlation of structure and viscoelastic properties in the pericardia of four mammalian species. Am J Physiol 1992; 263: H1095-H1106
    PubMedGoogle Scholar
  • 26 Omura T, Yoshiyama M, Takeuchi K, Hanatani A, Kim S, Yoshida K, Izumi Y, Iwao H, Yoshikawa J. Differences in time course of myocardial mRNA expression in non-infarcted myocardium after myocardial infarction. Basic Res Cardiol 2000; 95: 316-323
    CrossrefPubMedGoogle Scholar
  • 27 Orenstein TL, Parker TG, Butany JW, Goodman JM, Dawood F, Wen W-H, Wee L, Martino T, McLaughlin PR, Liu PP. Favorable left ventricular remodeling following large myocardial infarction by exercise training. Effect on ventricular morphology and gene expression. J Clin Invest 1995; 96: 858-866
    CrossrefPubMedGoogle Scholar
  • 28 Ren J, Duan J, Thomas DP, Yang X, Sreejayan N, Sowers JR, Leri A, Kajstura J, Gao F, Anversa P. IGF-I alleviates diabetes-induced RhoA activation, eNOS uncoupling, and myocardial dysfunction. Am J Physiol 2008; 294: R793-R802
    PubMedGoogle Scholar
  • 29 Siu PM, Donley DA, Bryner RW, Alway SE. Citrate synthase expression and enzyme activity after endurance training in cardiac and skeletal muscles. J Appl Physiol 2003; 94: 555-560
    CrossrefPubMedGoogle Scholar
  • 30 Soci UPR, Fernandes T, Hashimoto NY, Mota GF, Amadeu MA, Rosa KT, Irigoyen MC, Phillips MI, Oliveira EM. MicroRNAs 29 are involved in the improvement of ventricular compliance promoted by aerobic exercise training in rats. Physiol Genomics 2011; 43: 665-673
    CrossrefPubMedGoogle Scholar
  • 31 Spina RJ, Chi MM, Hopkins MG, Nemeth PM, Lowry OH, Holloszy JO. Mitochondrial enzymes increase in muscle in response to 7–10 days of cycle exercise. J Appl Physiol 1996; 80: 2250-2254
    PubMedGoogle Scholar
  • 32 Srere P. 1Citrate synthase. [EC 4.1.3.7. Citrate oxaloacetate-lyase (CoA-acetylating). Methods Enzymol 1969; 13: 3-11
    PubMedGoogle Scholar
  • 33 Stray-Gundersen J, Musch TI, Haidet GC, Swain DP, Ordway GA, Mitchell JH. The effect of pericardiectomy on maximal oxygen consumption and maximal cardiac output in untrained dogs. Circ Res 1986; 58: 523-530
    CrossrefPubMedGoogle Scholar
  • 34 Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002; 3: research0034
    PubMedGoogle Scholar
  • 35 White DC, Hata JA, Shah AS, Glower DD, Lefkowitz RJ, Koch WJ. Preservation of myocardial β-adrenergic receptor signaling delays the development of heart failure after myocardial infarction. Proc Natl Acad Sci 2000; 97: 5428-5433
    CrossrefPubMedGoogle Scholar
  • 36 Yengo CM, Zimmerman SD, McCormick RJ, Thomas DP. Exercise training Post-MI favorably modifies heart extracellular matrix in the rat. Med Sci Sports Exerc 2012; 44: 1005-1012
    CrossrefPubMedGoogle Scholar
  • 37 Zolotareva AG, Kogan ME. Production of experimental occlusive myocardial infarction in mice. Cor Vasa 1978; 20: 308-314
    PubMedGoogle Scholar