Differential reduction in cardiac and liver monolysocardiolipin acyltransferase-1 and reduction in cardiac and liver tetralinoleoyl-cardiolipin in the α-subunit of trifunctional protein heterozygous knockout mice

Biochemical Journal

Volumn 471, Issue 1, 2015, Pages 123-129

  Mejia, Edgard M ^a   Ibdah, Jamal A ^b   Sparagna, Genevieve C ^c   Hatch, Grant M ^a,d  

^a UNIVERSITY OF MANITOBA   (Canada)

^b University of Missouri   (United States)

^c UNIVERSITY OF COLORADO   (United States)

^d CHILDREN S HOSPITAL RESEARCH INSTITUTE OF MANITOBA   (Canada)

Author keywords

Acyltransferase; Alpha subunit; Cardiolipin; Heart; Liver; Lysocardiolipin; Monolysocardiolipin; Trifunctional protein

Indexed keywords

ACYLTRANSFERASE; CARDIOLIPIN; MITOCHONDRIAL TRIFUNCTIONAL PROTEIN ALPHA SUBUNIT; MONOLYSOCARDIOLIPIN ACYLTRANSFERASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; UNCLASSIFIED DRUG; MONOLYSOCARDIOLIPIN ACYLTRANSFERASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TETRALINOLEOYLCARDIOLIPIN;

ACYLATION; ANIMAL CELL; ARTICLE; ENZYME ACTIVITY; HEART MITOCHONDRION; IN VITRO STUDY; LIVER MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; GENETICS; HEART MUSCLE; KNOCKOUT MOUSE; LIVER; METABOLISM;

ACYLTRANSFERASES; ANIMALS; CARDIOLIPINS; ELECTRON TRANSPORT COMPLEX I; LIVER; MICE; MICE, KNOCKOUT; MITOCHONDRIAL TRIFUNCTIONAL PROTEIN, ALPHA SUBUNIT; MYOCARDIUM;

EID: 84942346119     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20150648     Document Type: Article

References (40)

1. Mejia, E.M., Nguyen, H. and Hatch, G.M. (2014) Mammalian cardiolipin biosynthesis. Chem. Phys. Lipids 179, 11-16
2. Gonzalvez, F., Schug, Z.T., Houtkooper, R.H., MacKenzie, E.D., Brooks, D.G., Wanders, R.J., Petit, P.X., Vaz, F.M. and Gottlieb, E. (2008) Cardiolipin provides an essential activating platform for caspase-8 on mitochondria. J. Cell Biol. 183, 681-696
3. Korytowski, W., Basova, L.V., Pilat, A., Kernstock, R.M. and Girotti, A.W. (2011) Permeabilization of the mitochondrial outer membrane by Bax/truncated Bid (tBid) proteins as sensitized by cardiolipin hydroperoxide translocation: mechanistic implications for the intrinsic pathway of oxidative apoptosis. J. Biol. Chem. 286, 26334-26343
4. Gonzalvez, F., D'Aurelio, M., Boutant, M., Moustapha, A., Puech, J.P., Landes, T., Arnaune-Pelloquin, L., Vial, G., Taleux, N., Slomianny, C. et al. (2013) Barth syndrome: cellular compensation of mitochondrial dysfunction and apoptosis inhibition due to changes in cardiolipin remodeling linked to tafazzin (TAZ) gene mutation. Biochim. Biophys. Acta 1832, 1194-1206
5. Schlame, M., Ren, M., Xu, Y., Greenberg, M.L. and Haller, I. (2005) Molecular symmetry in mitochondrial cardiolipins. Chem. Phys. Lipids 138, 38-49
6. Sparagna, G.C., Chicco, A.J., Murphy, R.C., Bristow, M.R., Johnson, C.A., Rees, M.L., Maxey, M.L., McCune, S.A. and Moore, R.L. (2007) Loss of cardiac tetralinoleoyl cardiolipin in human and experimental heart failure. J. Lipid Res. 48, 1559-1570
7. Hatch, G.M. (1998) Cardiolipin: biosynthesis, remodeling and trafficking in the heart and mammalian cells. Int. J. Mol. Med. 1, 33-41
8. Ma, B.J., Taylor, W.A., Dolinsky, V.W. and Hatch, G.M. (1999) Acylation of monolysocardiolipin in rat heart. J. Lipid Res. 40, 1837-1845
9. Xu, Y., Kelley, R.I., Blanck, T.J. and Schlame, M. (2003) Remodeling of cardiolipin by phospholipid transacylation. J. Biol. Chem. 278, 51380-51385
10. Hostetler, K.Y., Galesloot, J.M., Boer, P. and Van Den Bosch, H. (1975) Further studies on the formation of cardiolipin and phosphatidylglycerol in rat liver mitochondria. Effect of divalent cations and the fatty acid composition of CDP-diglyceride. Biochim. Biophys. Acta 380, 382-389
11. Houtkooper, R.H., Akbari, H., van Lenthe, H., Kulik, W., Wanders, R.J., Frentzen, M. and Vaz, F.M. (2006) Identification and characterization of human cardiolipin synthase. FEBS Lett. 580, 3059-3064
12. Zhang, M., Mileykovskaya, E. and Dowhan, W. (2002) Gluing the respiratory chain together. Cardiolipin is required for supercomplex formation in the inner mitochondrial membrane. J. Biol. Chem. 277, 43553-43556
13. McKenzie, M., Lazarou, M., Thorburn, D.R. and Ryan, M.T. (2006) Mitochondrial respiratory chain supercomplexes are destabilized in Barth Syndrome patients. J. Mol. Biol. 361, 462-469
14. van Gestel, R.A., Rijken, P.J., Surinova, S., O'Flaherty, M., Heck, A.J., Killian, J.A., de Kroon, A.I. and Slijper, M. (2010) The influence of the acyl chain composition of cardiolipin on the stability of mitochondrial complexes; an unexpected effect of cardiolipin in alpha-ketoglutarate dehydrogenase and prohibitin complexes. J. Proteomics 73, 806-814
15. Mejia, E.M., Cole, L. and Hatch, G.M. (2014) Cardiolipin metabolism and the role it plays in heart failure and mitochondrial supercomplex formation. Cardiovasc. Hematol. Disord. Drug Targets 14, 98-106
16. Schlame, M., Towbin, J.A., Heerdt, P.M., Jehle, R., DiMauro, S. and Blanck, T.J. (2002) Deficiency of tetralinoleoyl-cardiolipin in Barth syndrome. Ann. Neurol. 51, 634-637
17. Lu, B., Kelher, M.R., Lee, D.P., Lewin, T.M., Coleman, R.A., Choy, P.C. and Hatch, G.M. (2004) Complex expression pattern of the Barth syndrome gene product tafazzin in human cell lines and murine tissues. Biochem. Cell Biol. 82, 569-576
18. Maranzana, E., Barbero, G., Falasca, A.I., Lenaz, G. and Genova, M.L. (2013) Mitochondrial respiratory supercomplex association limits production of reactive oxygen species from complex I. Antioxid. Redox Signal. 19, 1469-1480
19. Taylor, W.A., Mejia, E.M., Mitchell, R.W., Choy, P.C., Sparagna, G.C. and Hatch, G.M. (2012) Human trifunctional protein alpha links cardiolipin remodeling to beta-oxidation. PLoS One 7, e48628
20. Taylor, W.A. and Hatch, G.M. (2009) Identification of the human mitochondrial linoleoyl-coenzyme A monolysocardiolipin acyltransferase (MLCL AT-1). J. Biol. Chem. 284, 30360-30371
21. Sparagna, G.C., Johnson, C.A., McCune, S.A., Moore, R.L. and Murphy, R.C. (2005) Quantitation of cardiolipin molecular species in spontaneously hypertensive heart failure rats using electrospray ionization mass spectrometry. J. Lipid Res. 46, 1196-1204
22. Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275
23. Minkler, P.E. and Hoppel, C.L. (2010) Separation and characterization of cardiolipin molecular species by reverse-phase ion pair high-performance liquid chromatography-mass spectrometry. J. Lipid Res. 51, 856-865
24. Kiebish, M.A., Yang, K., Sims, H.F., Jenkins, C.M., Liu, X., Mancuso, D.J., Zhao, Z., Guan, S., Abendschein, D.R., Han, X. and Gross, R.W. (2012) Myocardial regulation of lipidomic flux by cardiolipin synthase: setting the beat for bioenergetic efficiency. J. Biol. Chem. 287, 25086-25097
25. Han, X., Yang, J., Yang, K., Zhao, Z., Abendschein, D.R. and Gross, R.W. (2007) Alterations in myocardial cardiolipin content and composition occur at the very earliest stages of diabetes: a shotgun lipidomics study. Biochemistry 46, 6417-6428
26. Widlansky, M.E., Wang, J., Shenouda, S.M., Hagen, T.M., Smith, A.R., Kizhakekuttu, T.J., Kluge, M.A., Weihrauch, D., Gutterman, D.D. and Vita, J.A. (2010) Altered mitochondrial membrane potential, mass, and morphology in the mononuclear cells of humans with type 2 diabetes. Transl. Res. 156, 15-25
27. Ibdah, J.A., Perlegas, P., Zhao, Y., Angdisen, J., Borgerink, H., Shadoan, M.K., Wagner, J.D., Matern, D., Rinaldo, P. and Cline, J.M. (2005) Mice heterozygous for a defect in mitochondrial trifunctional protein develop hepatic steatosis and insulin resistance. Gastroenterology 128, 1381-1390
28. Rector, R.S., Morris, E.M., Ridenhour, S., Meers, G.M., Hsu, F.F., Turk, J. and Ibdah, J.A. (2013) Selective hepatic insulin resistance in a murine model heterozygous for a mitochondrial trifunctional protein defect. Hepatology 57, 2213-2223
29. Richter-Dennerlein, R., Korwitz, A., Haag, M., Tatsuta, T., Dargazanli, S., Baker, M., Decker, T., Lamkemeyer, T., Rugarli, E.I. and Langer, T. (2014) DNAJC19, a mitochondrial cochaperone associated with cardiomyopathy, forms a complex with prohibitins to regulate cardiolipin remodeling. Cell Metab. 20, 158-171
30. Schlame, M., Blais, S., Edelman-Novemsky, I., Xu, Y., Montecillo, F., Phoon, C.K., Ren, M. and Neubert, T.A. (2012) Comparison of cardiolipins from Drosophila strains with mutations in putative remodeling enzymes. Chem. Phys. Lipids 165, 512-519
31. Wang, E.T., Sandberg, R., Luo, S., Khrebtukova, I., Zhang, L., Mayr, C., Kingsmore, S.F., Schroth, G.P. and Burge, C.B. (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456, 470-476
32. Gasparre, G., Porcelli, A.M., Lenaz, G. and Romeo, G. (2013) Relevance of mitochondrial genetics and metabolism in cancer development. Cold Spring Harb. Perspect. Biol. 5, a011411
33. Gomez, L.A. and Hagen, T.M. (2012) Age-related decline in mitochondrial bioenergetics: does supercomplex destabilization determine lower oxidative capacity and higher superoxide production? Semin. Cell Dev. Biol. 23, 758-767
34. Paradies, G., Petrosillo, G., Paradies, V. and Ruggiero, F.M. (2011) Mitochondrial dysfunction in brain aging: role of oxidative stress and cardiolipin. Neurochem. Int. 58, 447-457
35. Rosca, M.G., Vazquez, E.J., Kerner, J., Parland, W., Chandler, M.P., Stanley, W., Sabbah, H.N. and Hoppel, C.L. (2008) Cardiac mitochondria in heart failure: decrease in respirasomes and oxidative phosphorylation. Cardiovasc. Res. 80, 30-39
36. Pfeiffer, K., Gohil, V., Stuart, R.A., Hunte, C., Brandt, U., Greenberg, M.L. and Schagger, H. (2003) Cardiolipin stabilizes respiratory chain supercomplexes. J. Biol. Chem. 278, 52873-52880
37. Zhang, M., Mileykovskaya, E. and Dowhan, W. (2005) Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria. J. Biol. Chem. 280, 29403-29408
38. Dudek, J., Cheng, I.F., Balleininger, M., Vaz, F.M., Streckfuss-Bomeke, K., Hubscher, D., Vukotic, M., Wanders, R.J., Rehling, P. and Guan, K. (2013) Cardiolipin deficiency affects respiratory chain function and organization in an induced pluripotent stem cell model of Barth syndrome. Stem Cell Res. 11, 806-819
39. Baile, M.G., Sathappa, M., Lu, Y.W., Pryce, E., Whited, K., McCaffery, J.M., Han, X., Alder, N.N. and Claypool, S.M. (2014) Unremodeled and remodeled cardiolipin are functionally indistinguishable in yeast. J. Biol. Chem. 289, 1768-1778
40. Han, X., Yang, K., Yang, J., Cheng, H. and Gross, R.W. (2006) Shotgun lipidomics of cardiolipin molecular species in lipid extracts of biological samples. J. Lipid Res. 47, 864-879