Deletion of the Cardiolipin-specific Phospholipase Cld1 rescues growth and life span defects in the Tafazzin Mutant implications for Barth Syndrome

Journal of Biological Chemistry

Volumn 289, Issue 6, 2014, Pages 3114-3125

  Ye, Cunqi ^a   Lou, Wenjia ^a   Li, Yiran ^a   Chatzispyrou, Iliana A ^e   Hüttemann, Maik ^b,c   Lee, Icksoo ^d   Houtkooper, Riekelt H ^e   Vaz, Frédéric M ^e   Chen, Shuliang ^a,f   Greenberg, Miriam L ^a  

^a WAYNE STATE UNIVERSITY   (United States)

^b Center for Molecular Medicine and Genetics   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Dankook University   (South Korea)

^e ACADEMIC MEDICAL CENTER   (Netherlands)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BARTH SYNDROME; CARDIOLIPIN; MITOCHONDRIA; PHOSPHOLIPASE; PHOSPHOLIPID; RESPIRATION; TAFAZZIN;

1-ACYLGLYCEROPHOSPHOCHOLINE O-ACYLTRANSFERASE; BARTH SYNDROME; CARDIOLIPINS; DNA, FUNGAL; DNA, MITOCHONDRIAL; ENERGY METABOLISM; GENE DELETION; HUMANS; MITOCHONDRIA; OXYGEN CONSUMPTION; PHOSPHOLIPASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84893656180     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.529487     Document Type: Article

References (87)

1. Hostetler, K. Y., van den Bosch, H., and van Deenen, L. L. (1972) The mechanism of cardiolipin biosynthesis in liver mitochondria. Biochim. Biophys. Acta 260, 507-513
2. Joshi, A. S., Zhou, J., Gohil, V. M., Chen, S., and Greenberg, M. L. (2009) Cellular functions of cardiolipin in yeast. Biochim. Biophys. Acta 1793, 212-218
3. Pangborn, M. C. (1947) The composition of cardiolipin. J. Biol. Chem. 168, 351-361
4. Lecocq, J., and Ballou, C. E. (1964) On the structure of cardiolipin. Biochemistry 3, 976-980
5. Jakovcic, S., Getz, G. S., Rabinowitz, M., Jakob, H., and Swift, H. (1971) Cardiolipin content of wild type and mutant yeasts in relation to mitochondrial function and development. J. Cell Biol. 48, 490-502
6. Schlame, M., Rua, D., and Greenberg, M. L. (2000) The biosynthesis and functional role of cardiolipin. Prog. Lipid Res. 39, 257-288
7. Claypool, S. M. (2009) Cardiolipin, a critical determinant of mitochondrial carrier protein assembly and function. Biochim. Biophys. Acta 1788, 2059-2068
8. Schlame, M., and Ren, M. (2009) The role of cardiolipin in the structural organization of mitochondrial membranes. Biochim. Biophys. Acta 1788, 2080-2083
9. Klingenberg, M. (2009) Cardiolipin and mitochondrial carriers. Biochim. Biophys. Acta 1788, 2048-2058
10. Beyer, K., and Klingenberg, M. (1985) ADP/ATP carrier protein from beef heart mitochondria has high amounts of tightly bound cardiolipin, as revealed by 31P nuclear magnetic resonance. Biochemistry 24, 3821-3826
11. Claypool, S. M., Oktay, Y., Boontheung, P., Loo, J. A., and Koehler, C. M. (2008) Cardiolipin defines the interactome of the major ADP/ATP carrier protein of the mitochondrial inner membrane. J. Cell Biol. 182, 937-950
12. Lange, C., Nett, J. H., Trumpower, B. L., and Hunte, C. (2001) Specific roles of protein-phospholipid interactions in the yeast cytochrome bc1 complex structure. EMBO J. 20, 6591-6600
13. Palsdottir, H., Lojero, C. G., Trumpower, B. L., and Hunte, C. (2003) Structure of the yeast cytochrome bc1 complex with a hydroxyquinone anion Qo site inhibitor bound. J. Biol. Chem. 278, 31303-31311
14. Eble, K. S., Coleman, W. B., Hantgan, R. R., and Cunningham, C. C. (1990) Tightly associated cardiolipin in the bovine heart mitochondrial ATP synthase as analyzed by 31P nuclear magnetic resonance spectroscopy. J. Biol. Chem. 265, 19434-19440
15. Shinzawa-Itoh, K., Aoyama, H., Muramoto, K., Terada, H., Kurauchi, T., Tadehara, Y., Yamasaki, A., Sugimura, T., Kurono, S., Tsujimoto, K., Mizushima, T., Yamashita, E., Tsukihara, T., and Yoshikawa, S. (2007) Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase. EMBO J. 26, 1713-1725
16. Pfeiffer, K., Gohil, V., Stuart, R. A., Hunte, C., Brandt, U., Greenberg, M. L., and Schägger, H. (2003) Cardiolipin stabilizes respiratory chain supercomplexes. J. Biol. Chem. 278, 52873-52880
17. 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
18. Jiang, F., Ryan, M. T., Schlame, M., Zhao, M., Gu, Z., Klingenberg, M., Pfanner, N., and Greenberg, M. L. (2000) Absence of cardiolipin in the crd1 null mutant results in decreased mitochondrial membrane potential and reduced mitochondrial function. J. Biol. Chem. 275, 22387-22394
19. Gohil, V. M., Hayes, P., Matsuyama, S., Schägger, H., Schlame, M., and Greenberg, M. L. (2004) Cardiolipin biosynthesis and mitochondrial respiratory chain function are interdependent. J. Biol. Chem. 279, 42612-42618
20. DeVay, R. M., Dominguez-Ramirez, L., Lackner, L. L., Hoppins, S., Stahlberg, H., and Nunnari, J. (2009) Coassembly of Mgm1 isoforms requires cardiolipin and mediates mitochondrial inner membrane fusion. J. Cell Biol. 186, 793-803
21. Joshi, A. S., Thompson, M. N., Fei, N., Hüttemann, M., and Greenberg, M. L. (2012) Cardiolipin and mitochondrial phosphatidylethanolamine have overlapping functions in mitochondrial fusion in Saccharomyces cerevisiae. J. Biol. Chem. 287, 17589-17597
22. Gebert, N., Joshi, A. S., Kutik, S., Becker, T., McKenzie, M., Guan, X. L., Mooga, V. P., Stroud, D. A., Kulkarni, G., Wenk, M. R., Rehling, P., Meisinger, C., Ryan, M. T., Wiedemann, N., Greenberg, M. L., and Pfanner, N. (2009) Mitochondrial cardiolipin involved in outer-membrane protein biogenesis: implications for Barth syndrome. Curr. Biol. 19, 2133-2139
23. Zhong, Q., Gvozdenovic-Jeremic, J., Webster, P., Zhou, J., and Greenberg, M. L. (2005) Loss of function of KRE5 suppresses temperature sensitivity of mutants lacking mitochondrial anionic lipids. Mol. Biol. Cell 16, 665-675
24. Zhong, Q., Li, G., Gvozdenovic-Jeremic, J., and Greenberg, M. L. (2007) Up-regulation of the cell integrity pathway in Saccharomyces cerevisiae suppresses temperature sensitivity of the pgs1-mutant. J. Biol. Chem. 282, 15946-15953
25. Chen, S., Tarsio, M., Kane, P. M., and Greenberg, M. L. (2008) Cardiolipin mediates cross-talk between mitochondria and the vacuole. Mol. Biol. Cell 19, 5047-5058
26. Chen, S., Liu, D., Finley, R. L., Jr., and Greenberg, M. L. (2010) Loss of mitochondrialDNAin the yeast cardiolipin synthase crd1 mutant leads to up-regulation of the protein kinase Swe1p that regulates the G2/M transition. J. Biol. Chem. 285, 10397-10407
27. Zhou, J., Zhong, Q., Li, G., and Greenberg, M. L. (2009) Loss of cardiolipin leads to longevity defects that are alleviated by alterations in stress response signaling. J. Biol. Chem. 284, 18106-18114
28. Gonzalvez, F., and Gottlieb, E. (2007) Cardiolipin: setting the beat of apoptosis. Apoptosis 12, 877-885
29. Houtkooper, R. H., and Vaz, F. M. (2008) Cardiolipin, the heart of mitochondrial metabolism. Cell. Mol. Life Sci. 65, 2493-2506
30. Schug, Z. T., and Gottlieb, E. (2009) Cardiolipin acts as a mitochondrial signalling platform to launch apoptosis. Biochim. Biophys. Acta 1788, 2022-2031
31. Chang, S. C., Heacock, P. N., Clancey, C. J., and Dowhan, W. (1998) The PEL1 gene (renamed PGS1) encodes the phosphatidylglycero-phosphate synthase of Saccharomyces cerevisiae. J. Biol. Chem. 273, 9829-9836
32. Osman, C., Haag, M., Wieland, F. T., Brügger, B., and Langer, T. (2010) A mitochondrial phosphatase required for cardiolipin biosynthesis: the PGP phosphatase Gep4. EMBO J. 29, 1976-1987
33. Kelly, B. L., and Greenberg, M. L. (1990) Characterization and regulation of phosphatidylglycerol phosphate phosphatase in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1046, 144-150
34. Chang, S. C., Heacock, P. N., Mileykovskaya, E., Voelker, D. R., and Dowhan, W. (1998) Isolation and characterization of the gene (CLS1) encoding cardiolipin synthase in Saccharomyces cerevisiae. J. Biol. Chem. 273, 14933-14941
35. Tuller, G., Hrastnik, C., Achleitner, G., Schiefthaler, U., Klein, F., and Daum, G. (1998) YDL142c encodes cardiolipin synthase (Cls1p) and is non-essential for aerobic growth of Saccharomyces cerevisiae. FEBS Lett. 421, 15-18
36. Tamai, K. T., and Greenberg, M. L. (1990) Biochemical characterization and regulation of cardiolipin synthase in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1046, 214-222
37. Jiang, F., Rizavi, H. S., and Greenberg, M. L. (1997) Cardiolipin is not essential for the growth of Saccharomyces cerevisiae on fermentable or non-fermentable carbon sources. Mol. Microbiol. 26, 481-491
38. Beranek, A., Rechberger, G., Knauer, H., Wolinski, H., Kohlwein, S. D., and Leber, R. (2009) Identification of a cardiolipin-specific phospholipase encoded by the gene CLD1 (YGR110W) in yeast. J. Biol. Chem. 284, 11572-11578
39. Baile, M. G., Whited, K., and Claypool, S. M. (2013) Deacylation on the matrix side of the mitochondrial inner membrane regulates cardiolipin remodeling. Mol. Biol. Cell 24, 2008-2020
40. Testet, E., Laroche-Traineau, J., Noubhani, A., Coulon, D., Bunoust, O., Camougrand, N., Manon, S., Lessire, R., and Bessoule, J. J. (2005) Ypr140wp, 'the yeast tafazzin', displays a mitochondrial lysophosphatidylcholine (lyso-PC) acyltransferase activity related to triacylglycerol and mitochondrial lipid synthesis. Biochem. J. 387, 617-626
41. Gu, Z., Valianpour, F., Chen, S., Vaz, F. M., Hakkaart, G. A., Wanders, R. J., and Greenberg, M. L. (2004) Aberrant cardiolipin metabolism in the yeast taz1 mutant: a model for Barth syndrome. Mol. Microbiol. 51, 149-158
42. Brandner, K., Mick, D. U., Frazier, A. E., Taylor, R. D., Meisinger, C., and Rehling, P. (2005) Taz1, an outer mitochondrial membrane protein, affects stability and assembly of inner membrane protein complexes: implications for Barth syndrome. Mol. Biol. Cell 16, 5202-5214
43. Claypool, S. M., Boontheung, P., McCaffery, J. M., Loo, J. A., and Koehler, C. M. (2008) The cardiolipin transacylase, tafazzin, associates with two distinct respiratory components providing insight into Barth syndrome. Mol. Biol. Cell 19, 5143-5155
44. Vaz, F. M., Houtkooper, R. H., Valianpour, F., Barth, P. G., and Wanders, R. J. (2003) Only one splice variant of the human TAZ gene encodes a functional protein with a role in cardiolipin metabolism. J. Biol. Chem. 278, 43089-43094
45. Xu, Y., Kelley, R. I., Blanck, T. J., and Schlame, M. (2003) Remodeling of cardiolipin by phospholipid transacylation. J. Biol. Chem. 278, 51380-51385
46. Barth, P. G., Scholte, H. R., Berden, J. A., Van der Klei-Van Moorsel, J. M., Luyt-Houwen, I. E., Van 't Veer-Korthof, E. T., Van der Harten, J. J., and Sobotka-Plojhar, M. A. (1983) An X-linked mitochondrial disease affecting cardiac muscle, skeletal muscle and neutrophil leucocytes. J. Neurol. Sci. 62, 327-355
47. Barth, P. G., Wanders, R. J., Vreken, P., Janssen, E. A., Lam, J., and Baas, F. (1999) X-linked cardioskeletal myopathy and neutropenia (Barth syndrome) (MIM 302060). J. Inherit. Metab. Dis. 22, 555-567
48. Barth, P. G., Valianpour, F., Bowen, V. M., Lam, J., Duran, M., Vaz, F. M., and Wanders, R. J. (2004) X-linked cardioskeletal myopathy and neutropenia (Barth syndrome): an update. Am. J. Med. Genet. A 126, 349-354
49. Schlame, M., Kelley, R. I., Feigenbaum, A., Towbin, J. A., Heerdt, P. M., Schieble, T., Wanders, R. J., DiMauro, S., and Blanck, T. J. (2003) Phospholipid abnormalities in children with Barth syndrome. J. Am. Coll. Cardiol. 42, 1994-1999
50. Valianpour, F., Wanders, R. J., Barth, P. G., Overmars, H., and van Gennip, A. H. (2002) Quantitative and compositional study of cardiolipin in platelets by electrospray ionization mass spectrometry: application for the identification of Barth syndrome patients. Clin. Chem. 48, 1390-1397
51. Vreken, P., Valianpour, F., Nijtmans, L. G., Grivell, L. A., Plecko, B., Wanders, R. J., and Barth, P. G. (2000) Defective remodeling of cardiolipin and phosphatidylglycerol in Barth syndrome. Biochem. Biophys. Res. Commun. 279, 378-382
52. Xu, Y., Condell, M., Plesken, H., Edelman-Novemsky, I., Ma, J., Ren, M., and Schlame, M. (2006) A Drosophila model of Barth syndrome. Proc. Natl. Acad. Sci. U.S.A. 103, 11584-11588
53. Acehan, D., Vaz, F., Houtkooper, R. H., James, J., Moore, V., Tokunaga, C., Kulik, W., Wansapura, J., Toth, M. J., Strauss, A., and Khuchua, Z. (2011) Cardiac and skeletal muscle defects in a mouse model of human Barth syndrome. J. Biol. Chem. 286, 899-908
54. Houtkooper, R. H., Rodenburg, R. J., Thiels, C., van Lenthe, H., Stet, F., Poll-The, B. T., Stone, J. E., Steward, C. G., Wanders, R. J., Smeitink, J., Kulik, W., and Vaz, F. M. (2009) Cardiolipin and monolysocardiolipin analysis in fibroblasts, lymphocytes, and tissues using high-performance liquid chromatography-mass spectrometry as a diagnostic test for Barth syndrome. Anal. Biochem. 387, 230-237
55. Malhotra, A., Edelman-Novemsky, I., Xu, Y., Plesken, H., Ma, J., Schlame, M., and Ren, M. (2009) Role of calcium-independent phospholipase A2 in the pathogenesis of Barth syndrome. Proc. Natl. Acad. Sci. U.S.A. 106, 2337-2341
56. Hsu, Y. H., Dumlao, D. S., Cao, J., and Dennis, E. A. (2013) Assessing phospholipase A2 activity toward cardiolipin by mass spectrometry. PLoS One 8, e59267
57. Fabrizio, P., and Longo, V. D. (2003) The chronological life span of Saccharomyces cerevisiae. Aging Cell 2, 73-81
58. Hu, J., Wei, M., Mirisola, M. G., and Longo, V. D. (2013) Assessing chronological aging in Saccharomyces cerevisiae. Methods Mol. Biol. 965, 463-472
59. Köhrer, K., and Domdey, H. (1991) Preparation of high molecular weight RNA. Methods Enzymol. 194, 398-405
60. Lee, I., Pecinova, A., Pecina, P., Neel, B. G., Araki, T., Kucherlapati, R., Roberts, A. E., and Hüttemann, M. (2010) A suggested role for mitochondria in Noonan syndrome. Biochim. Biophys. Acta 1802, 275-283
61. Diekert, K., de Kroon, A. I., Kispal, G., and Lill, R. (2001) Isolation and subfractionation of mitochondria from the yeast Saccharomyces cerevisiae. Methods Cell Biol. 65, 37-51
62. Gardner, P. R. (2002) Aconitase: sensitive target and measure of superoxide. Methods Enzymol. 349, 9-23
63. 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
64. Ocampo, A., Liu, J., Schroeder, E. A., Shadel, G. S., and Barrientos, A. (2012) Mitochondrial respiratory thresholds regulate yeast chronological life span and its extension by caloric restriction. Cell Metab. 16, 55-67
65. Dimitrov, L. N., Brem, R. B., Kruglyak, L., and Gottschling, D. E. (2009) Polymorphisms in multiple genes contribute to the spontaneous mitochondrial genome instability of Saccharomyces cerevisiae S288C strains. Genetics 183, 365-383
66. Nehlin, J. O., and Ronne, H. (1990) Yeast MIG1 repressor is related to the mammalian early growth response and Wilms' tumour finger proteins. EMBO J. 9, 2891-2898
67. Pfeifer, K., Kim, K. S., Kogan, S., and Guarente, L. (1989) Functional dissection and sequence of yeast HAP1 activator. Cell 56, 291-301
68. Santangelo, G. M. (2006) Glucose signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 70, 253-282
69. Schüller, H. J. (2003) Transcriptional control of nonfermentative metabolism in the yeast Saccharomyces cerevisiae. Curr. Genet 43, 139-160
70. Bu, Y., and Schmidt, M. C. (1998) Identification of cis-Acting elements in the SUC2 promoter of Saccharomyces cerevisiae required for activation of transcription. Nucleic Acids Res. 26, 1002-1009
71. Wu, J., and Trumbly, R. J. (1998) Multiple regulatory proteins mediate repression and activation by interaction with the yeast Mig1 binding site. Yeast 14, 985-1000
72. Chen, X. J., Wang, X., Kaufman, B. A., and Butow, R. A. (2005) Aconitase couples metabolic regulation to mitochondrial DNA maintenance. Science 307, 714-717
73. 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
74. Schlame, M., and Ren, M. (2006) Barth syndrome, a human disorder of cardiolipin metabolism. FEBS Lett. 580, 5450-5455
75. Valianpour, F., Wanders, R. J., Overmars, H., Vaz, F. M., Barth, P. G., and van Gennip, A. H. (2003) Linoleic acid supplementation of Barth syndrome fibroblasts restores cardiolipin levels: implications for treatment. J. Lipid Res. 44, 560-566
76. Hüttemann, M., Lee, I., Grossman, L. I., Doan, J. W., and Sanderson, T. H. (2012) Phosphorylation of mammalian cytochrome c and cytochrome c oxidase in the regulation of cell destiny: respiration, apoptosis, and human disease. Adv. Exp. Med. Biol. 748, 237-264
77. Koshkin, V., and Greenberg, M. L. (2000) Oxidative phosphorylation in cardiolipin-lacking yeast mitochondria. Biochem. J. 347, 687-691
78. Kwast, K. E., Burke, P. V., Staahl, B. T., and Poyton, R. O. (1999) Oxygen sensing in yeast: evidence for the involvement of the respiratory chain in regulating the transcription of a subset of hypoxic genes. Proc. Natl. Acad. Sci. U.S.A. 96, 5446-5451
79. Fontanesi, F., Jin, C., Tzagoloff, A., and Barrientos, A. (2008) Transcriptional activators HAP/NF-Y rescue a cytochrome c oxidase defect in yeast and human cells. Hum. Mol. Genet. 17, 775-788
80. Su, X., and Dowhan, W. (2006) Translational regulation of nuclear gene COX4 expression by mitochondrial content of phosphatidylglycerol and cardiolipin in Saccharomyces cerevisiae. Mol. Cell. Biol. 26, 743-753
81. Paradies, G., Ruggiero, F. M., Petrosillo, G., and Quagliariello, E. (1998) Peroxidative damage to cardiac mitochondria: cytochrome oxidase and cardiolipin alterations. FEBS Lett. 424, 155-158
82. Paradies, G., Petrosillo, G., Pistolese, M., and Ruggiero, F. M. (2000) The effect of reactive oxygen species generated from the mitochondrial electron transport chain on the cytochrome c oxidase activity and on the cardiolipin content in bovine heart submitochondrial particles. FEBS Lett. 466, 323-326
83. Paradies, G., Petrosillo, G., Pistolese, M., and Ruggiero, F. M. (2001) Reactive oxygen species generated by the mitochondrial respiratory chain affect the complex III activity via cardiolipin peroxidation in beef-heart submitochondrial particles. Mitochondrion 1, 151-159
84. Petrosillo, G., Portincasa, P., Grattagliano, I., Casanova, G., Matera, M., Ruggiero, F. M., Ferri, D., and Paradies, G. (2007) Mitochondrial dysfunction in rat with nonalcoholic fatty liver Involvement of complex I, reactive oxygen species and cardiolipin. Biochim. Biophys. Acta 1767, 1260-1267
85. Kiebish, M. A., Yang, K., Liu, X., Mancuso, D. J., Guan, S., Zhao, Z., Sims, H. F., Cerqua, R., Cade, W. T., Han, X., and Gross, R. W. (2013) Dysfunctional cardiac mitochondrial bioenergetic, lipidomic, and signaling in a murine model of Barth syndrome. J. Lipid Res. 54, 1312-1325
86. Szijgyarto, Z., Garedew, A., Azevedo, C., and Saiardi, A. (2011) Influence of inositol pyrophosphates on cellular energy dynamics. Science 334, 802-805
87. 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