Mitochondrial integrity in a neonatal bovine model of right ventricular dysfunction

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 308, Issue 2, 2015, Pages L158-L167

  Bruns, Danielle R ^a   Dale Brown, R ^b   Stenmark, Kurt R ^b   Buttrick, Peter M ^a   Walker, Lori A ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b University of Colorado Denver and Children s Hospital Colorado   (United States)

Author keywords

Cardiac; Mitochondria; Pulmonary hypertension; Right ventricle

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; VASCULOTROPIN A; 6 PHOSPHOFRUCTOKINASE; GLUCOSE TRANSPORTER 4; PROTEIN KINASE C; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; GLYCOLYSIS; HEART OUTPUT; HEART RIGHT ATRIUM PRESSURE; HEART RIGHT VENTRICLE FUNCTION; HEART STROKE VOLUME; IMMUNOBLOTTING; LUNG ARTERY PRESSURE; LUNG RESISTANCE; MALE; MITOCHONDRIAL DYNAMICS; MYOFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; RESPIRATORY CHAIN; UPREGULATION; ANIMAL; BIOSYNTHESIS; BOVINE; COPY NUMBER VARIATION; DISEASE MODEL; GENETICS; HEART FAILURE; HEART RIGHT VENTRICLE HYPERTROPHY; HEART VENTRICLE; METABOLISM; MITOCHONDRION; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; CATTLE; DISEASE MODELS, ANIMAL; DNA COPY NUMBER VARIATIONS; ELECTRON TRANSPORT COMPLEX I; GLUCOSE TRANSPORTER TYPE 4; HEART FAILURE; HEART VENTRICLES; HYPERTENSION, PULMONARY; HYPERTROPHY, RIGHT VENTRICULAR; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MITOCHONDRIA; PHOSPHOFRUCTOKINASE-1; PROTEIN KINASE C; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VENTRICULAR DYSFUNCTION, RIGHT; VENTRICULAR FUNCTION, RIGHT;

EID: 84921299251     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00270.2014     Document Type: Article

References (42)

1. Allard MF, Schonekess BO, Henning SL, English DR, Lopaschuk GD. Contribution of oxidative metabolism and glycolysis to ATP production in hypertrophied hearts. Am J Physiol Heart Circ Physiol 267: H742-H750, 1994.
2. Bakerman PR, Stenmark KR, Fisher JH. Skeletal actin mRNA increases in acute right ventricular hypertrophy. Am J Physiol Lung Cell Mol Physiol 258: L173-L178, 1990.
3. Beer M, Seyfarth T, Sandstede J, Landschutz W, Lipke C, Kostler H, von Kienlin M, Harre K, Hahn D, Neubauer S. Absolute concentrations of high-energy phosphate metabolites in normal, hypertrophied, and failing human myocardium measured noninvasively with (31)P-SLOOP magnetic resonance spectroscopy. J Am Coll Cardiol 40: 1267-1274, 2002.
4. Carley AN, Taegtmeyer H, Lewandowski ED. Matrix revisited: mechanisms linking energy substrate metabolism to the function of the heart. Circ Res 114: 717-729, 2014.
5. Chandel NS, Schumacker PT. Cellular oxygen sensing by mitochondria: old questions, new insight. J Appl Physiol 88: 1880-1889, 2000.
6. Chen L, Gong Q, Stice JP, Knowlton AA. Mitochondrial OPA1, apoptosis, and heart failure. Cardiovasc Res 84: 91-99, 2009.
7. Chen L Mitochondrial dynamics in heart failure. Congest Heart Fail 17: 257-261, 2011.
8. Christofk HR, Vander Heiden MG, Harris MH, Ramanathan A, Gerszten RE, Wei R, Fleming MD, Schreiber SL, Cantley LC. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452: 230-233, 2008.
9. Dagda RK, Cherra SJ, Kulich SM, Tandon A, Park D, Chu CT. Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J Biol Chem 284: 13843-13855, 2009.
10. Dagda RK, Zhu J, Kulich SM, Chu CT. Mitochondrially localized ERK2 regulates mitophagy and autophagic cell stress: implications for Parkinson’s disease. Autophagy 4: 770-782, 2008.
11. Drake JC, Peelor FF, Biela LM, Watkins MK, Miller RA, Hamilton KL, Miller BF. Assessment of mitochondrial biogenesis and mTORC1 signaling during chronic rapamycin feeding in male and female mice. J Gerontol 68: 1493-1501, 2013.
12. Frid MG, Li M, Gnanasekharan M, Burke DL, Fragoso M, Strassheim D, Sylman JL, Stenmark KR. Sustained hypoxia leads to the emergence of cells with enhanced growth, migratory, and promitogenic potentials within the distal pulmonary artery wall. Am J Physiol Lung Cell Mol Physiol 297: L1059-L1072, 2009.
13. Gao Z, Cooper TA. Reexpression of pyruvate kinase M2 in type 1 myofibers correlates with altered glucose metabolism in myotonic dystrophy. Proc Natl Acad Sci USA 110: 13570-13575, 2013.
14. Haddad F, Bodell PW, Baldwin KM. Pressure-induced regulation of myosin expression in rodent heart. J Appl Physiol 78: 1489-1495, 1995.
15. Ingwall JS. Energy metabolism in heart failure and remodelling. Cardiovasc Res 81: 412-419, 2009.
16. Inscore SC, Stenmark KR, Orton C, Irvin CG. Neonatal calves develop airflow limitation due to chronic hypobaric hypoxia. J Appl Physiol 70: 384-390, 1991.
17. Jung F, Weiland U, Johns RA, Ihling C, Dimmeler S. Chronic hypoxia induces apoptosis in cardiac myocytes: a possible role for Bcl-2-like proteins. Biochem Biophys Res Commun 286: 419-425, 2001.
18. Kagaya Y, Kanno Y, Takeyama D, Ishide N, Maruyama Y, Takahashi T, Ido T, Takishima T. Effects of long-term pressure overload on regional myocardial glucose and free fatty acid uptake in rats. A quantitative autoradiographic study. Circulation 81: 1353-1361, 1990.
19. Kodde IF, van der Stok J, Smolenski RT, de Jong JW. Metabolic and genetic regulation of cardiac energy substrate preference. Comp Biochem Physiol A Mol Integr Physiol 146: 26-39, 2007.
20. Kolwicz SC, Tian R. Glucose metabolism and cardiac hypertrophy. Cardiovasc Res 90: 194-201, 2011.
21. Kulisz A, Chen N, Chandel NS, Shao Z, Schumacker PT. Mitochondrial ROS initiate phosphorylation of p38 MAP kinase during hypoxia in cardiomyocytes. Am J Physiol Lung Cell Mol Physiol 282: L1324-L1329, 2002.
22. Lammers S, Scott D, Hunter K, Tan W, Shandas R, Stenmark KR. Mechanics and function of the pulmonary vasculature: implications for pulmonary vascular disease and right ventricular function. Comprehen Physiol 2: 295-319, 2012.
23. Lammers SR, Kao PH, Qi HJ, Hunter K, Lanning C, Albietz J, Hofmeister S, Mecham R, Stenmark KR, Shandas R. Changes in the structure-function relationship of elastin and its impact on the proximal pulmonary arterial mechanics of hypertensive calves. Am J Physiol Heart Circ Physiol 295: H1451-1459, 2008.
24. Lemler MS, Bies RD, Frid MG, Sastravaha A, Zisman LS, Bohlmeyer T, Gerdes AM, Reeves JT, Stenmark KR. Myocyte cytoskeletal disorganization and right heart failure in hypoxia-induced neonatal pulmonary hypertension. Am J Physiol Heart Circ Physiol 279: H1365-H1376, 2000.
25. Marin-Garcia J, Goldenthal MJ. Mitochondrial centrality in heart failure. Heart Fail Rev 13: 137-150, 2008.
26. Miller BF, Robinson MM, Bruss MD, Hellerstein M, Hamilton KL. A comprehensive assessment of mitochondrial protein synthesis and cellular proliferation with age and caloric restriction. Aging Cell 11: 150-161, 2012.
27. Morrell NW, Adnot S, Archer SL, Dupuis J, Jones PL, MacLean MR, McMurtry IF, Stenmark KR, Thistlethwaite PA, Weissmann N, Yuan JX, Weir EK. Cellular and molecular basis of pulmonary arterial hypertension. J Am Coll Cardiol 54: S20-S31, 2009.
28. Morrell NW, Danilov SM, Satyan KB, Morris KG, Stenmark KR. Right ventricular angiotensin converting enzyme activity and expression is increased during hypoxic pulmonary hypertension. Cardiovasc Res 34: 393-403, 1997.
29. Neubauer S. The failing heart-an engine out of fuel. N Engl J Med 356: 1140-1151, 2007.
30. Nouette-Gaulain K, Forestier F, Malgat M, Marthan R, Mazat JP, Sztark F. Effects of bupivacaine on mitochondrial energy metabolism in heart of rats following exposure to chronic hypoxia. Anesthesiology 97: 1507-1511, 2002.
31. Nouette-Gaulain K, Malgat M, Rocher C, Savineau JP, Marthan R, Mazat JP, Sztark F. Time course of differential mitochondrial energy metabolism adaptation to chronic hypoxia in right and left ventricles. Cardiovasc Res 66: 132-140, 2005.
32. Papanicolaou KN, Khairallah RJ, Ngoh GA, Chikando A, Luptak I, O’Shea KM, Riley DD, Lugus JJ, Colucci WS, Lederer WJ, Stanley WC, Walsh K. Mitofusin-2 maintains mitochondrial structure and contributes to stress-induced permeability transition in cardiac myocytes. Mol Cell Biol 31: 1309-1328, 2011.
33. Paulin R, Michelakis ED. The metabolic theory of pulmonary arterial hypertension. Circ Res 115: 148-164, 2014.
34. Rosca MG, Hoppel CL. Mitochondrial dysfunction in heart failure. Heart Fail Rev 18: 607-622, 2013.
35. Rumsey WL, Abbott B, Bertelsen D, Mallamaci M, Hagan K, Nelson D, Erecinska M. Adaptation to hypoxia alters energy metabolism in rat heart. Am J Physiol Heart Circ Physiol 276: H71-H80, 1999.
36. Ryan JJ, Archer SL. The right ventricle in pulmonary arterial hypertension: disorders of metabolism, angiogenesis and adrenergic signaling in right ventricular failure. Circ Res 115: 176-188, 2014.
37. Sabbah HN, Sharov V, Riddle JM, Kono T, Lesch M, Goldstein S. Mitochondrial abnormalities in myocardium of dogs with chronic heart failure. J Mol Cell Cardiol 24: 1333-1347, 1992.
38. Sharov VG, Todor AV, Silverman N, Goldstein S, Sabbah HN. Abnormal mitochondrial respiration in failed human myocardium. J Mol Cell Cardiol 32: 2361-2367, 2000.
39. Stenmark KR, Aldashev AA, Orton EC, Durmowicz AG, Badesch DB, Parks WC, Mecham RP, Voelkel NF, Reeves JT. Cellular adaptation during chronic neonatal hypoxic pulmonary hypertension. Am J Physiol 261: 97-104, 1991.
40. Taanman JW, Bodnar AG, Cooper JM, Morris AA, Clayton PT, Leonard JV, Schapira AH. Molecular mechanisms in mitochondrial DNA depletion syndrome. Hum Mol Genet 6: 935-942, 1997.
41. Takeyama D, Kagaya Y, Yamane Y, Shiba N, Chida M, Takahashi T, Ido T, Ishide N, Takishima T. Effects of chronic right ventricular pressure overload on myocardial glucose and free fatty acid metabolism in the conscious rat. Cardiovasc Res 29: 763-767, 1995.
42. Walker LA, Walker JS, Glazier A, Brown DR, Stenmark KR, Buttrick PM. Biochemical and myofilament responses of the right ventricle to severe pulmonary hypertension. Am J Physiol Heart Circ Physiol 301: H832-H840, 2011.