Persistent pulmonary hypertension results in reduced tetralinoleoyl-cardiolipin and mitochondrial complex II + III during the development of right ventricular hypertrophy in the neonatal pig heart

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 301, Issue 4, 2011, Pages

  Saini Chohan, Harjot K ^a   Dakshinamurti, Shyamala ^a   Taylor, William A ^a   Shen, Garry X ^b   Murphy, Robert ^b   Sparagna, Genevieve C ^c   Hatch, Grant M ^a,b,d  

^a MANITOBA INSTITUTE OF CHILD HEALTH   (Canada)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY OF COLORADO   (United States)

^d UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Cardiomyopathy; Heart failure; Lipid; Metabolism; Mitochondria

Indexed keywords

BRAIN NATRIURETIC PEPTIDE; CARBON 14; CARDIOLIPIN; LINOLEOYL COENZYME A DESATURASE; MITOCHONDRIAL COMPLEX II; OXIDOREDUCTASE; TETRALINOLEOYL; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; ENZYME ACTIVITY; EXPERIMENTAL PIG; HEART LEFT VENTRICLE; HEART RIGHT VENTRICLE FAILURE; HEART RIGHT VENTRICLE HYPERTROPHY; HEART VENTRICLE REMODELING; HEART WEIGHT; NEWBORN; NONHUMAN; PERSISTENT PULMONARY HYPERTENSION; PHOSPHOLIPID SYNTHESIS; PIGLET; PRECURSOR; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; CARDIOLIPINS; DISEASE MODELS, ANIMAL; ELECTRON TRANSPORT COMPLEX II; ELECTRON TRANSPORT COMPLEX III; HUMANS; HYPERTROPHY, RIGHT VENTRICULAR; INFANT, NEWBORN; LIPID METABOLISM; MUSCLE, SMOOTH, VASCULAR; PERSISTENT FETAL CIRCULATION SYNDROME; PULMONARY ARTERY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; RNA, MESSENGER; SUBCELLULAR FRACTIONS; SWINE;

EID: 80053266457     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00247.2011     Document Type: Article

References (60)

1. Cao J, Lockwood J, Burn P, Shi Y. A novel cardiolipin-remodeling pathway revealed by a gene encoding an endoplasmic reticulum-associated acyl-CoA:lysocardiolipin acyltransferase (ALCAT1) in mouse. J Biol Chem 279: 31727-31734, 2004.
2. Carraway MS, Suliman HB, Schuyler Jones W, Chen CW, Babiker A, Piantadosi CA. Erythropoietin activates mitochondrial biogenesis and couples red cell mass to mitochondrial mass in the heart. Circ Res 106: 1722-1730, 2010.
3. Cheng P, Hatch GM. Inhibition of cardiolipin biosynthesis in the hypoxic rat heart. Lipids 30: 513-519, 1995.
4. Chicco AJ, Sparagna GC. Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am J Physiol Cell Physiol 292: C33-C44, 2007.
5. Christie D, Lemke CD, Elias I, Chau LA, Kirchhof MG, Li B, Dunn SD, Ball EH, Hatch GM, Madrenas J. Stomatin-like protein 2 scaffolds prohibitins to cardiolipin and regulates mitochondrial biogenesis. Mol Cell Biol. doi:10.1128/MCB.05393-11, 2011.
6. Daicho T, Yagi T, Abe Y, Ohara M, Marunouchi T, Takeo S, Tanonaka K. Possible involvement of mitochondrial energy-producing ability in the development of right ventricular failure in monocrotalineinduced pulmonary hypertensive rats. J Pharmacol Sci 111: 33-43, 2009.
7. Dakshinamurti S. Pathophysiologic mechanisms of persistent pulmonary hypertension of the newborn. Pediatr Pulmonol 39: 492-503, 2005.
8. Dakshinamurti S, Mellow L, Stephens NL. Regulation of pulmonary arterial myosin phosphatase activity in neonatal circulatory transition and in hypoxic pulmonary hypertension: a role for CPI-17. Pediatr Pulmonol 40: 398-407, 2005.
9. Deng MY, Wang H, Ward GB, Beckham TR, McKenna TS. Comparison of six RNA extraction methods for the detection of classical swine fever virus by real-time and conventional reverse transcription-PCR. J Vet Diagn Invest 17: 574-578, 2005.
10. Deprez RHL, Fijnvandraat AC, Ruijter JM, Moorman AF. Sensitivity and accuracy of quantitative real-time polymerase chain reaction using SYBR green I depends on cDNA synthesis conditions. Anal Biochem 307: 63-69, 2002.
11. Gersony WM. Neonatal pulmonary hypertension: pathophysiology, classification, and etiology. Clin Perinatol 11: 517-524, 1984.
12. Hall SM, Hislop AA, Wu Z, Haworth SG. Remodelling of the pulmonary arteries during recovery from pulmonary hypertension induced by neonatal hypoxia. J Pathol 203: 575-583, 2004.
13. Hatch GM. Cardiolipin biosynthesis in the isolated heart. Biochem J 297: 201-208, 1994.
14. Hatch GM. Cardiolipin: biosynthesis, remodeling and trafficking in the heart and mammalian cells. Int J Mol Med 1: 33-41, 1998.
15. Hatch GM. Cell biology of cardiac mitochondrial phospholipids. Biochem Cell Biol 82: 99-112, 2004.
16. Hatch GM, Cao SG, Angel A. Decrease in cardiac phosphatidylglycerol in streptozotocin-induced diabetic rats does not affect cardiolipin biosynthesis: evidence for distinct pools of phosphatidylglycerol in the heart. Biochem J 306: 759-764, 1995.
17. Hatch GM, McClarty G. Regulation of cardiolipin biosynthesis in H9c2 cardiac myoblasts by cytidine 5'-triphosphate. J Biol Chem 271: 25810-25816, 1996.
18. Hauff KD, Choi SY, Frohman MA, Hatch GM. Cardiolipin synthesis is required to support human cholesterol biosynthesis from palmitate upon serum removal in Hela cells. Can J Physiol Pharmacol 87: 813-820, 2009.
19. Hauff K, Linda D, Hatch GM. Mechanism of the elevation in cardiolipin during HeLa cell entry into the S-phase of the human cell cycle. Biochem J 417: 573-582, 2009.
20. Hauff KD, Hatch GM. Cardiolipin metabolism and Barth Syndrome. Prog Lipid Res 45: 91-101, 2006.
21. Haworth SG, Hislop AA. Effect of hypoxia on adaptation of the pulmonary circulation to extra-uterine life in the pig. Cardiovasc Res 16: 293-303, 1982.
22. Heather LC, Carr CA, Stuckey DJ, Pope S, Morten KJ, Carter EE, Edwards LM, Clarke K. Critical role of complex III in the early metabolic changes following myocardial infarction. Cardiovasc Res 85: 127-136, 2010.
23. Hinton M, Gutsol A, Dakshinamurti S. Thromboxane hypersensitivity in hypoxic pulmonary artery myocytes: altered TP receptor localization and kinetics. Am J Physiol Lung Cell Mol Physiol 292: L654-L663, 2007.
24. Hinton M, Mellow L, Halayko AJ, Gutsol A, Dakshinamurti S. Hypoxia induces hypersensitivity and hyperreactivity to thromboxane receptor agonist in neonatal pulmonary arterial myocytes. Am J Physiol Lung Cell Mol Physiol 290: L375-L384, 2006.
25. Hostetler KY. Phosholipids. Amsterdam: Elsevier, 1992, p. 215-242.
26. Khan AR, Birbach M, Cohen MS, Ittenbach RF, Spray TL, Levy RJ, Gaynor JW. Chronic hypoxemia increases ventricular brain natriuretic peptide precursors in neonatal swine. Ann Thorac Surg 85: 618-623, 2008.
27. Kinsella JP, Abman SH. Recent developments in the pathophysiology and treatment of persistent pulmonary hypertension of the newborn. J Pediatr 126: 853-864, 1995.
28. Latini G, Del Vecchio A, De Felice C, Verrotti A, Bossone E. Persistent pulmonary hypertension of the newborn: therapeutical approach. Mini Rev Med Chem 8: 1507-1513, 2008.
29. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔCT) method. Methods 25: 402-408, 2001.
30. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275, 1959.
31. McHowat J, Tappia PS, Liu S, McCrory R, Panagia V. Redistribution and abnormal activity of phospholipase A2 isoenzymes in postinfarct congestive heart failure. Am J Physiol Cell Physiol 280: C573-C580, 2001.
32. McKenzie M, Lazarou M, Thorburn DR, Ryan MT. Mitochondrial respiratory chain supercomplexes are destabilized in Barth syndrome patients. J Mol Biol 361: 462-469, 2006.
33. Ma BJ, Taylor WA, Dolinsky VW, Hatch GM. Acylation of monolysocardiolipin in rat heart. J Lipid Res 40: 1837-1845, 1999.
34. Ma L, Vaz FM, Gu Z, Wanders RJ, Greenberg ML. The human TAZ gene complements mitochondrial dysfunction in the yeast taz1Delta mutant. Implications for Barth syndrome. J Biol Chem 279: 44394-44399, 2004.
35. Mancuso DJ, Sims HF, Han X, Jenkins CM, Guan SP, Yang K, Moon SH, Pietka T, Abumrad NA, Schlesinger PH, Gross RW. Cardiac ischemia activates calcium-independent phospholipase A2β, precipitating ventricular tachyarrhythmias in transgenic mice: rescue of the lethal electrophysiologic phenotype by mechanism-based inhibition. J Biol Chem 282: 34611-34622, 2007.
36. Ohtsuka T, Nishijima M, Susuki K, Akamatsu Y. Mitochondrial dysfunction of a cultured Chinese hamster ovary cell mutant deficient in cardiolipin. J Biol Chem 268: 22914-22919, 1993.
37. Ostrea EM, Villanueva-Uy ET, Natarajan G, Uy HG. Persistent pulmonary hypertension of the newborn: pathogenesis, etiology, and management. Paediatr Drugs 8: 179-188, 2006.
38. Peterson CJ, Whitman V, Watson PA, Schuler HG, Morgan HE. Mechanisms of differential growth of heart ventricles in newborn pigs. Circ Res 64: 360-369, 1989.
39. Pfeiffer K, Gohil V, Stuart RA, Hunte C, Brandt U, Greenberg ML, Schägger H. Cardiolipin stabilizes respiratory chain supercomplexes. J Biol Chem 278: 52873-52880, 2003.
40. Rosca M, Minkler P, Hoppel CL. Cardiac mitochondria in heart failure: normal cardiolipin profile and increased threonine phosphorylation of complex IV. Biochim Biophys Acta, doi: 10.1016/j.bbabio.2011.02.003.
41. Rouser G, Fkeischer S, Yamamoto A. Two dimensional thin layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids 5: 494-496, 1970.
42. Sabbah HN, Chandler MP, Mishima T, Suzuki G, Chaudhry P, Nass O, Biesiadecki BJ, Blackburn B, Wolff A, Stanley WC. Ranolazine, a partial fatty acid oxidation (pFOX) inhibitor, improves left ventricular function in dogs with chronic heart failure. J Card Fail 8: 416-422, 2002.
43. Saini-Chohan HK, Holmes MG, Chicco AJ, Taylor WA, Moore RL, McCune SA, Hickson-Bick DL, Hatch GM, Sparagna GC. Cardiolipin biosynthesis and remodeling enzymes are altered during development of heart failure. J Lipid Res 50: 1600-1608, 2009.
44. Sangle GV, Chowdhury SK, Xie X, Stelmack GL, Halayko AJ, Shen GX. Impairment of mitochondrial respiratory chain activity in aortic endothelial cells induced by glycated low-density lipoprotein. Free Radic Biol Med 48: 781-790, 2010.
45. Schlame M, Ren M. Barth syndrome, a human disorder of cardiolipin metabolism. FEBS Lett 580: 5450-5455, 2006.
46. Schlame M, Ren M, Xu Y, Greenberg ML, Haller I. Molecular symmetry in mitochondrial cardiolipins. Chem Phys Lipids 138: 38-49, 2005.
47. Schlame M, Rua D, Greenberg ML. The biosynthesis and functional role of cardiolipin. Prog Lipid Res 39: 257-288, 2000.
48. Shaikh NA, Downar E. Time course of changes in porcine myocardial phospholipid levels during ischemia. A reassessment of the lysolipid hypothesis. Circ Res 49: 316-325, 1981.
49. Sparagna GC, Chicco AJ, Murphy RC, Bristow MR, Johnson CA, Rees ML, Maxey M, McCune SA, Moore RL. Loss of cardiac tetralinoleoyl cardiolipin in human and experimental heart failure. J Lipid Res 48: 1559-1570, 2007.
50. Sparagna GC, Johnson CA, McCune SA, Moore RL, Murphy RC. Quantitation of cardiolipin molecular species in spontaneously hypertensive heart failure rats using electrospray ionization mass spectrometry. J Lipid Res 46: 1196-1204, 2005.
51. Stanley WC, Hoppel CL. Mitochondrial dysfunction in heart failure: potential for therapeutic interventions? Cardiovasc Res 45: 805-806, 2000.
52. Stenmark KR, Frid M, Nemenoff R, Dempsey EC, Das M. Hypoxia induces cell-specific changes in gene expression in vascular wall cells: implications for pulmonary hypertension. Adv Exp Med Biol 474: 231-258, 1999.
53. Taylor WA, Hatch GM. Purification and characterization of monolysocardiolipin acyltransferase from pig liver mitochondria. J Biol Chem 278: 12716-12721, 2003.
54. Taylor WA, Hatch GM. Identification of the human mitochondrial linoleoyl-coenzyme A monolysocardiolipin acyltransferase (MLCL AT-1). J Biol Chem 284: 30360-30371, 2009.
55. Therese P. Persistent pulmonary hypertension of the newborn. Paediatr Respir Rev 7: S175-S176, 2006.
56. Vosatka RJ. Persistent pulmonary hypertension of the newborn. N Engl J Med 346: 864, 2002.
57. Xu Y, Kelley RI, Blanck TJ, Schlame M. Remodeling of cardiolipin by phospholipid transacylation. J Biol Chem 278: 51380-51385, 2003.
58. Yamaoka S, Urade R, Kito M. Cardiolipin molecular species in rat heart mitochondria are sensitive to essential fatty acid-deficient dietary lipids. J Nutr 120: 415-421, 1990.
59. Yamaoka-Koseki S, Urade R, Kito M. Cardiolipins from rats fed different dietary lipids affect bovine heart cytochrome c oxidase activity. J Nutr 121: 956-958, 1991.
60. Zachman DK, Chicco AJ, McCune SA, Murphy RC, Moore RL, Sparagna GC. The role of calcium-independent phospholipase A2 in cardiolipin remodeling in the spontaneously hypertensive heart failure rat heart. J Lipid Res 51: 525-534, 2010.