Cardiolipin synthesis for the assembly of bacterial and mitochondrial membranes

Journal of Lipid Research

Volumn 49, Issue 8, 2008, Pages 1607-1620

  Schlame, Michael ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Mitochondrial biogenesis; Molecular species; Phospholipids; Tafazzin

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; CARDIOLIPIN; CARDIOLIPIN SYNTHASE; GENE PRODUCT; MEMBRANE PROTEIN; PHOSPHOLIPASE A; PHOSPHOLIPASE D; TAFAZZIN; UNCLASSIFIED DRUG; PHOSPHOTRANSFERASE; TAZ PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

APOPTOSIS; BACTERIAL MEMBRANE; BARTH SYNDROME; CRYSTAL STRUCTURE; ENZYME DEGRADATION; EUKARYOTE; GENE MUTATION; HUMAN; LIPID ANALYSIS; LIPID DEGRADATION; LIPID OXIDATION; LIPOGENESIS; MEMBRANE TRANSPORT; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; REVIEW; STEREOCHEMISTRY; AMINO ACID SEQUENCE; ANIMAL; BACTERIUM; BIOSYNTHESIS; CELL MEMBRANE; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; SEQUENCE ALIGNMENT; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; BACTERIA; CARDIOLIPINS; CELL MEMBRANE; HUMANS; MEMBRANE PROTEINS; MITOCHONDRIAL MEMBRANES; MOLECULAR SEQUENCE DATA; PHOSPHOLIPASE D; PHOSPHOLIPASES A; SEQUENCE ALIGNMENT; TRANSCRIPTION FACTORS; TRANSFERASES (OTHER SUBSTITUTED PHOSPHATE GROUPS);

EID: 51449112852     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.R700018-JLR200     Document Type: Review

References (141)

1. LeCocq, J., and C. E. Ballou. 1964. On the structure of cardiolipin. Biochemistry. 3: 976-980.
2. Powell, G. L., and J. Jacobus. 1974. The nonequivalence of the phosphorus atoms in cardiolipin. Biochemistry. 13: 4024-4026.
3. Schlame, M., M. Ren, Y. Xu, M. L. Greenberg, and I. Haller. 2005. Molecular symmetry in mitochondrial cardiolipins. Chem. Phys. Lipids. 138: 38-49.
4. Kates, M., J-Y. Syz, D. Gosser, and T. H. Haines. 1993. pH-dissociation characteristics of cardiolipin and its 2'-deoxy analogue. Lipids. 28: 877-882.
5. Dahlberg, M. 2007. Polymorphic phase behavior of cardiolipin derivatives studied by coarse-grained molecular dynamics. J. Phys. Chem. 111: 7194-7200.
6. Schlame, M., D. Rua, and M. L. Greenberg. 2000. The biosynthesis and functional role of cardiolipin. Prog. Lipid Res. 39: 257-288.
7. Powell, G. L., and D. Marsh. 1985. Polymorphic phase behavior of cardiolipin derivatives studied by 31P NMR and X-ray diffraction. Biochemistry. 24: 2902-2908.
8. Allegrini, P. R., G. Pluschke, and J. Seelig. 1984. Cardiolipin conformation and dynamics in bilayer membranes as seen by deuterium magnetic resonance. Biochemistry. 23: 6452-6458.
9. Dowhan, W. 1997. Molecular basis for membrane phospholipid diversity: why are there so many lipids? Annu. Rev. Biochem. 66: 199-232.
10. Daum, G. 1985. Lipids of mitochondria. Biochim. Biophys. Acta. 822: 1-42.
11. De Andrade Rosa, I., M. Einicker-Lamas, R. R. Bernardo, L. M. Previatto, R. Mohana-Borges, J. A. Morgado-Diaz, and M. Benchimol. 2006. Cardiolipin in hydrogenosomes: evidence of symbiotic origin. Eukaryot. Cell. 5: 784-787.
12. Martin, W., M. Hoffmeister, C. Rotte, and K. Henze. 2001. An overview of endosymbiotic models for the origins of eukaryotes, their ATP-producing organelles (mitochondria and hydrogenosomes), and their heterotrophic lifestyle. Biol. Chem. 382: 1521-1539.
13. Corcelli, A., M. Colella, G. Mascolo, F. P. Fanizzi, and M. Kates. 2000. A novel glycolipid and phospholipid in the purple membrane. Biochemistry. 39: 3318-3326.
14. Lattanzio, V. M. T., A. Corcelli, G. Mascolo, and A. Oren. 2002. Presence of two novel cardiolipins in the halophilic archeal community in the crystallizer brines from the salterns of Margherita di Savoia (Italy) and Eliat (Israel). Extremophiles. 6: 437-444.
15. Fischer, W. 1977. The polar lipids of group B streptococci. I. Glucosylated diphosphatidylglycerol, a novel glycophospholipid. Biochim. Biophys. Acta. 487: 74-88.
16. Fischer, W., and D. Arneth-Seifert. 1998. D-Alanylcardiolipin, a major component of the unique lipid pattern of Vagococcus fluvialis. J. Bacteriol. 180: 2093-2101.
17. Peter-Katalinic, J., and W. Fischer. 1998. a-D-Glucopyranosyl-, D-alanyland L-lysylcardiolipin from Gram-positive bacteria: analysis by fast atom bombardment mass spectrometry. J. Lipid Res. 39: 2286-2292.
18. Shibuya, I. 1992. Metabolic regulations and biological functions of phospholipids in Escherichia coli. Prog. Lipid Res. 31: 245-299.
19. Short, S. A., and D. C. White. 1971. Metabolism of phosphatidylglycerol, lysophosphatidyl-glycerol and cardiolipin of Staphylococcus aureus. J. Bacteriol. 108: 219-226.
20. Koch, H. U., R. Haas, and W. Fischer. 1984. The role of lipoteichoic acid biosynthesis in membrane lipid metabolism of growing Staphylococcus aureus. Eur. J. Biochem. 138: 357-363.
21. Kanemasa, Y., T. Yioshioka, and H. Hayashi. 1972. Alteration of the phospholipid composition of Staphylococcus aureus cultures in medium containing NaCl. Biochim. Biophys. Acta. 280: 444-450.
22. Catucci, L., N. Depalo, V. M. T. Lattanzio, A. Agostiano, and A. Corcelli. 2004. Neosynthesis of cardiolipin in Rhodobacter sphaeroides under osmotic stress. Biochemistry. 43: 15066-15072.
23. Heber, S., and B. E. Tropp. 1991. Genetic regulation of cardiolipin synthase in Escherichia coli. Biochim. Biophys. Acta. 1129: 1-12.
24. Hiraoka, S., H. Matsuzaki, and I. Shibuya. 1993. Active increase in cardiolipin synthesis in the stationary phase and its physiological significance in Escherichia coli. FEBS Lett. 336: 221-224.
25. De Siervo, A. J., and M. R. J. Salton. 1971. Biosynthesis of cardiolipin in the membranes of Micrococcus lysodeikticus. Biochim. Biophys. Acta. 239: 280-292.
26. Hirschberg, C. B., and E. P. Kennedy. 1972. Mechanism of enzymatic synthesis of cardiolipin in Escherichia coli. Proc. Natl. Acad. Sci. USA. 69: 648-651.
27. Pluschke, G., Y. Hirota, and P. Overath. 1978. Function of phospholipids in Escherichia coli. Characterization of a mutant deficient in cardiolipin synthesis. J. Biol. Chem. 253: 5048-5055.
28. Ohta, A., T. Obara, Y. Asami, and I. Shibuya. 1985. Molecular cloning of the cls gene responsible for cardiolipin synthesis in Escherichia coli and phenotypic consequences of its amplification. J. Bacteriol. 163: 506-514.
29. Shibuya, I., and S. Hiraoka. 1992. Cardiolipin synthase from Escherichia coli. Methods Enzymol. 209: 321-330.
30. Ragolia, L., and B. E. Tropp. 1994. The effects of phosphoglycerides on Escherichia coli cardiolipin synthase. Biochim. Biophys. Acta. 1214: 323-332.
31. Tropp, B. E. 1997. Cardiolipin synthase from Escherichia coli. Biochim. Biophys. Acta. 1348: 192-200.
32. Waite, M. 1999. The PLD superfamily: insight into catalysis. Biochim. Biophys. Acta. 1439: 187-197.
33. Shibuya, I., S. Yamagoe, C. Miyazaki, H. Matsuzaki, and A. Ohta. 1985. Biosynthesis of novel acidic phospholipid analogs in Escherichia coli. J. Bacteriol. 161: 473-477.
34. Hiraoka, S., K. Nukui, N. Uetake, A. Ohta, and I. Shibuya. 1991. Amplification and substantial purification of cardiolipin synthase of Escherichia coli. J. Biochem. 110: 443-449.
35. Hostetler, K. Y., H. van den Bosch, and L. L. M. van Deenen. 1971. Biosynthesis of cardiolipin in liver mitochondria. Biochim. Biophys. Acta. 239: 113-119.
36. Hostetler, K. Y., H. van den Bosch, and L. L. M. van Deenen. 1972. The mechanism of cardiolipin biosynthesis in liver mitochondria. Biochim. Biophys. Acta. 260: 507-513.
37. Tamai, K. T., and M. L. Greenberg. 1990. Biochemical characterization and regulation of cardiolipin synthase in Saccharomyces cerevisiae. Biochim. Biophys. Acta. 1046: 214-222.
38. Schlame, M., S. Brody, and K. Y. Hostetler. 1993. Mitochondrial cardiolipin in diverse eukaryotes. Comparison of biosynthetic reactions and molecular species. Eur. J. Biochem. 212: 727-735.
39. Jiang, F., H. S. Rizavi, and M. L. Greenberg. 1997. Cardiolipin is not essential for the growth of Saccharomyces cerevisiae on fermentable or non-fermentable carbon sources. Mol. Microbiol. 26: 481-491.
40. Tuller, G., C. Hrastnik, G. Achleitner, U. Schiefthaler, F. Klein, and G. Daum. 1998. YDL142c encodes cardiolipin synthase (Cls1p) and is non-essential for aerobic growth of Saccharomyces cerevisiae. FEBS Lett. 421: 15-18.
41. Chang, S. C., P. N. Heacock, E. Mileykovskaya, D. R. Voelker, and W. Dowhan. 1998. Isolation and characterization of the gene (CLS1) encoding cardiolipin synthase in Saccharomyces cerevisiae. J. Biol. Chem. 273: 14933-14941.
42. Katayama, K., I. Sakurai, and H. Wada. 2004. Identification of an Arabidopsis thaliana gene for cardiolipin synthase located in mitochondria. FEBS Lett. 577: 193-198.
43. Nowicki, M., F. Müller, and M. Frentzen. 2005. Cardiolipin synthase of Arabidopsis thaliana. FEBS Lett. 579: 2161-2165.
44. Houtkooper, R. H., H. Akbari, H. van Lenthe, W. Kulik, R. J. A. Wanders, M. Frentzen, and F. M. Vaz. 2006. Identification and characterization of human cardiolipin synthase. FEBS Lett. 580: 3059-3064.
45. Lu, B., F. Y. Xu, Y. J. Jiang, P. C. Choy, G. M. Hatch, C. Grunfeld, and K. R. Feingold. 2006. Cloning and characterization of a cDNA encoding human cardiolipin synthase (hCLS1). J. Lipid Res. 47: 1140-1145.
46. Chen, D., X-Y. Zhang, and Y. Shi. 2006. Identification and functional characterization of hCLS1, a human cardiolipin synthase localized in mitochondria. Biochem. J. 398: 169-176.
47. Schlame, M., and K. Y. Hostetler. 1991. Solubilization, purification, and characterization of cardiolipin synthase from rat liver mitochondria. Demonstration of its phospholipid requirement. J. Biol. Chem. 266: 22398-22403.
48. Schlame, M., M. Zhao, D. Rua, D. Haldar, and M. L. Greenberg. 1995. Kinetic analysis of cardiolipin synthase: a membrane enzyme with two glycerophospholipid substrates. Lipids. 30: 633-640.
49. Poorthuis, B. J. H. M., and K. Y. Hostetler. 1976. Studies on nucleotide diphosphate diacylglycerol specificity of acidic phospholipid biosynthesis in rat liver subcellular fractions. Biochim. Biophys. Acta. 431: 408-415.
50. Hostetler, K. Y., J. M. Galesloot, P. Boer, and H. van den Bosch. 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.
51. McMurray, W. C., and E. C. Jarvis. 1980. Partial purification of diphosphatidylglycerol synthase from rat liver mitochondrial membranes. Can. J. Biochem. 58: 771-776.
52. Hostetler, K. Y., and H. van den Bosch. 1972. Subcellular and submitochondrial localization of the biosynthesis of cardiolipin and related phospholipids in rat liver. Biochim. Biophys. Acta. 260: 380-386.
53. Schlame, M., and D. Haldar. 1993. Cardiolipin is synthesized on the matrix side of the inner membrane in rat liver mitochondria. J. Biol. Chem. 268: 74-79.
54. Zhao, M., M. Schlame, D. Rua, and M. L. Greenberg. 1998. Cardiolipin synthase is associated with a large complex in yeast mitochondria. J. Biol. Chem. 273: 2402-2408.
55. Paradies, G., and F. M. Ruggiero. 1988. Effect of hyperthyroidism on the transport of pyruvate in rat heart. Biochim. Biophys. Acta. 935: 79-86.
56. Cao, S. G., P. Cheng, A. Angel, and G. M. Hatch. 1995. Thyroxine stimulates phosphatidylglycerolphosphate synthase activity in rat heart mitochondria. Biochim. Biophys. Acta. 1256: 241-244.
57. Paradies, G., and F. M. Ruggiero. 1990. Stimulation of phosphate transport in rat liver mitochondria by thyroid hormones. Biochim. Biophys. Acta. 1019: 133-136.
58. Nakashima-Kamimura, N., S. Asoh, Y. Ishibashi, Y. Mukai, Y. Shidara, H. Oda, K. Munakata, Y. Goto, and S. Ohta. 2005. MIDAS/GPP34, a nuclear gene product, regulates total mitochondrial mass in response to mitochondrial dysfunction. J. Cell Sci. 118: 5357-5367.
59. Gohil, V. M., P. Hayes, S. Matsuyama, H. Schagger, M. Schlame, and M. L. Greenberg. 2004. Cardiolipin biosynthesis and mito-chondrial respiratory chain function are interdependent. J. Biol. Chem. 279: 42612-42618.
60. Li, G., S. Chen, M. N. Thompson, and M. L. Greenberg. 2007. New insights into the regulation of cardiolipin biosynthesis in yeast: implications for Barth syndrome. Biochim. Biophys. Acta. 1771: 432-441.
61. Schlame, M., and B. Rustow. 1990. Lysocardiolipin formation and reacylation in isolated rat liver mitochondria. Biochem. J. 272: 589-595.
62. Rustow, B., M. Schlame, H. Rabe, G. Reichmann, and D. Kunze. 1989. Species pattern of phosphatidic acid, diacylglycerol, CDPdiacylglycerol and phosphatidylglycerol synthesized de novo in rat liver mitochondria. Biochim. Biophys. Acta. 1002: 261-263.
63. Schlame, M., J. A. Towbin, P. M. Heerdt, R. Jehle, S. DiMauro, and T. J. J. Blanck. 2002. Deficiency of tetralinoleoyl-cardiolipin in Barth syndrome. Ann. Neurol. 51: 634-637.
64. Han, X., J. Yang, K. Yang, Z. Zhao, D. R. Abendschein, and R. W. Gross. 2007. Alterations in myocardial cardiolipin content and composition occur at the very earliest stages of diabetes: a shotgun lipidomics study. Biochemistry. 46: 6417-6428.
65. Sparagna, G. C., A. J. Chicco, R. C. Murphy, M. R. Bristow, C. A. Johnson, M. L. Rees, M. L. Maxey, S. A. McCune, and R. L. Moore. 2007. Loss of cardiac tetralinoleoyl cardiolipin in human and experimental heart failure. J. Lipid Res. 48: 1559-1570.
66. Ellis, C. E., E. J. Murphy, D. C. Mitchell, M. Y. Golovko, F. Scaglia, G. C. Barcelo-Coblijn, and R. L. Nussbaum. 2005. Mitochondrial lipid abnormality and electron transport chain impairment in mice lacking a-synuclein. Mol. Cell. Biol. 25: 10190-10201.
67. Schlame, M., and M. Ren. 2006. Barth syndrome, a human disorder of cardiolipin metabolism. FEBS Lett. 580: 5450-5455.
68. Schlame, M., K. Beyer, M. Hayer-Hartl, and M. Klingenberg. 1991. Molecular species of cardiolipin in relation to other mitochondrial phospholipids. Is there an acyl specificity of the interaction between cardiolipin and the ADP/ATP carrier? Eur. J. Biochem. 199: 459-466.
69. Mita, M., and N. Ueta. 1989. Fatty chain composition of phospholipids in sea urchin spermatozoa. Comp. Biochem. Physiol. 92B: 319-322.
70. Wang, H-Y. J., S. N. Jackson, and A. S. Woods. 2007. Direct MALDIMS analysis of cardiolipin from rat organ sections. J. Am. Soc. Mass Spectrom. 18: 567-577.
71. Xu, Y., A. Malhotra, M. Ren, and M. Schlame. 2006. The enzymatic function of tafazzin. J. Biol. Chem. 281: 39217-39224.
72. Kraffe, E., P. Soudant, Y. Marty, and N. Kervarec. 2005. Docosahexaenoic acid- and eicosapentaenoic acid-enriched cardiolipin in the Manila clam Ruditapes philippinarum. Lipids. 40: 619-625.
73. Kraffe, E., P. Soudant, Y. Marty, N. Kervarec, and P. Jehan. 2002. Evidence of a tetradocosahexaenoic cardiolipin in some marine bivalves. Lipids. 37: 507-514.
74. Ma, B. J., W. A. Taylor, V. W. Dolinsky, and G. M. Hatch. 1999. Acylation of monolysocardiolipin in rat heart. J. Lipid Res. 40: 1837-1845.
75. Taylor, W. A., and G. M. Hatch. 2003. Purification and characterization of monolysocardiolipin acyltransferase from pig liver mitochondria. J. Biol. Chem. 278: 12716-12721.
76. Cao, J., Y. Liu, J. Lockwood, P. Burn, and Y. Shi. 2004. 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.
77. Eichberg, J. 1974. The reacylation of deacylated derivatives of diphosphatidylglycerol by microsomes and mitochondria from rat liver. J. Biol. Chem. 249: 3423-3429.
78. Riekhof, W. R., J. Wu, J. L. Jones, and D. R. Voelker. 2007. Identification and characterization of the major lysophosphatidylethanolamine acyltransferase in Saccharomyces cerevisiae. J. Biol. Chem. 282: 28344-28352.
79. Xu, Y., R. I. Kelley, T. J. J. Blanck, and M. Schlame. 2003. Remodeling of cardiolipin by phospholipid transacylation. J. Biol. Chem. 278: 51380-51385.
80. Schlame, M., R. I. Kelley, A. Feigenbaum, J. A. Towbin, P. M. Heerdt, T. Schieble, R. J. A. Wanders, S. DiMauro, and T. J. J. Blanck. 2003. Phospholipid abnormalities in children with Barth syndrome. J. Am. Coll. Cardiol. 42: 1994-1999.
81. Valianpour, F., R. J. A. Wanders, H. Overmars, P. Vreken, A. H. van Gennip, F. Baas, B. Plecko, R. Santer, K. Becker, and P. G. Barth. 2002. Cardiolipin deficiency in X-linked cardioskeletal myopathy and neutropenia (Barth syndrome, MIM 302060): a study in cultured skin fibroblasts. J. Pediatr. 141: 729-733.
82. Kuijpers, T. W., N. A. Maianski, A. T. J. Tool, K. Becker, B. Plecko, F. Valianpour, R. J. A. Wanders, R. Pereira, J. van Hove, A. J. Verhoeven, et al. 2004. Neutrophils in Barth syndrome (BTHS) avidly bind annexin-V in the absence of apoptosis. Blood. 103: 3915-3923.
83. Vaz, F. M., R. H. Houtkooper, F. Valianpour, P. G. Barth, and R. J. A. Wanders. 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.
84. Gu, Z., F. Valianpour, S. Chen, F. M. Vaz, G. A. Hakkaart, R. J. A. Wanders, and M. L. Greenberg. 2004. Aberrant cardiolipin metabolism in the yeast taz1 mutant: a model for Barth syndrome. Mol. Microbiol. 51: 149-158.
85. Xu, Y., M. Condell, H. Plesken, I. Edelman-Novemsky, J. Ma, M. Ren, and M. Schlame. 2006. A Drosophila model of Barth syndrome. Proc. Natl. Acad. Sci. USA. 103: 11584-11588.
86. Bione, S., P. D'Adamo, E. Maestrini, A. K. Gedeon, P. A. Bolhuis, and D. Toniolo. 1996. A novel X-linked gene, G4.5. is responsible for Barth syndrome. Nat. Genet. 12: 385-389.
87. Vreken, P., F. Valianpour, L. G. Nijtmans, L. A. Grivell, B. Plecko, R. J. A. Wanders, and P. G. Barth. 2000. Defective remodeling of cardiolipin and phosphatidylglycerol in Barth syndrome. Biochem. Biophys. Res. Commun. 279: 378-382.
88. Neuwald, A. F. 1997. Barth syndrome may be due to an acyltransferase deficiency. Curr. Biol. 7: R465-R466.
89. Lewin, T. M., P. Wang, and R. A. Coleman. 1999. Analysis of amino acid motifs diagnostic for the sn-glycerol-3-phosphate acyltransferase reaction. Biochemistry. 38: 5764-5771.
90. Heath, R. J., and C. O. Rock. 1998. A conserved histidine is essential for glycerolipid acyltransferase catalysis. J. Bacteriol. 180: 1425-1430.
91. Brandner, K., D. U. Mick, A. E. Frazier, R. D. Taylor, C. Meisinger, and P. Rehling. 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.
92. Nichols-Smith, S., S-Y. Teh, and T. L. Kuhl. 2004. Thermodynamic and mechanical properties of model mitochondrial membranes. Biochim. Biophys. Acta. 1663: 82-88.
93. Mileykovskaya, E., W. Dowhan, R. L. Birke, D. Zheng, L. Lutterodt, and T. H. Haines. 2001. Cardiolipin binds nonyl acridine orange by aggregating the dye at exposed hydrophobic domains on bilayer surfaces. FEBS Lett. 507: 187-190.
94. Gohil, V. M., M. N. Thompson, and M. L. Greenberg. 2005. Synthetic lethal interaction of the mitochondrial phosphatidylethanolamine and cardiolipin biosynthetic pathways in Saccharomyces cerevisiae. J. Biol. Chem. 280: 35410-35416.
95. Lewis, R. N. A. H., D. Zweytick, G. Pabst, K. Lohner, and R. N. McElhaney. 2007. Calorimetric, X-ray diffraction, and spectroscopic studies of the thermotropic phase behavior and organization of tetramyristoyl cardiolipin membranes. Biophys. J. 92: 3166-3177.
96. Lopez, C. S., A. F. Alice, H. Heras, E. A. Rivas, and C. Sanchez-Rivas. 2006. Role of anionic phospholipids in the adaptation of Bacillus subtilis to high salinity. Microbiology. 152: 605-616.
97. Bernal, P., J. Munoz-Rojas, A. Hurtado, J. L. Ramos, and A. Segura. 2007. A Pseudomonas putida cardiolipin synthesis mutant exhibits increased sensitivity to drugs related to transport functionality. Environ. Microbiol. 9: 1135-1145.
98. Mileykovskaya, E., and W. Dowhan. 2000. Visualization of phospholipid domains in Escherichia coli by using the cardiolipin-specific fluorescent dye 10-N-nonyl acridine orange. J. Bacteriol. 182: 1172-1175.
99. Kawai, F., M. Shoda, R. Harashima, Y. Sadaie, H. Hara, and K. Matsumoto. 2004. Cardiolipin domains in Bacillus subtilis Marburg membranes. J. Bacteriol. 186: 1475-1483.
100. Romantsov, T., S. Helbig, D. E. Culham, C. Gill, L. Stalker, and J. M. Wood. 2007. Cardiolipin promotes polar localization of osmosensory transporter ProP in Escherichia coli. Mol. Microbiol. 64: 1455-1465.
101. Huang, K. C., R. Mukhopadhyay, and N. S. Wingreen. A curvaturemediated mechanism for localization of lipids to bacterial poles. PLOS Comput. Biol. 2: e151. Epub ahead of print. October 4, 2006; doi: 10.1371/journal.pcbi.0020151.
102. Claypool, S. M., J. M. McCaffery, and C. M. Koehler. 2006. Mitochondrial mislocalization and altered assembly of a cluster of Barth syndrome mutant tafazzins. J. Cell Biol. 174: 379-390.
103. Liu, J., J. Chen, Q. Dai, and R. M. Lee. 2003. Phospholipid scramblase 3 is the mitochondrial target of protein kinase C δ-induced apoptosis. Cancer Res. 63: 1153-1156.
104. Liu, J., Q. Dai, J. Chen, D. Durrant, A. Freeman, T. Liu, D. Grossman, and R. M. Lee. 2003. Phospholipid scramblase 3 controls mitochondrial structure, function, and apoptotic response. Mol. Cancer Res. 1: 892-902.
105. Epand, R. F., U. Schlattner, T. Wallimann, M-L. Lacombe, and R. M. Epand. 2007. Novel lipid transfer property of two mitochondrial proteins that bridge the inner and outer membranes. Biophys. J. 92: 126-137.
106. Epand, R. F., M. Tokarska-Schlattner, U. Schlattner, T. Walliman, and R. M. Epand. 2007. Cardiolipin clusters and membrane domain formation induced by mitochondrial proteins. J. Mol. Biol. 365: 968-980.
107. Adams, V., W. Bosch, J. Schlegel, T. Walliman, and D. Brdiczka. 1989. Further characterization of contact sites from mitochondria of different tissues: topology of peripheral kinases. Biochim. Biophys. Acta. 981: 213-225.
108. Schlame, M., L. Horvath, and L. Vigh. 1990. Relationship between lipid saturation and lipid-protein interaction in liver mitochondria modified by catalytic hydrogenation with reference to cardiolipin molecular species. Biochem. J. 265: 79-85.
109. 31P nuclear magnetic resonance. Biochemistry. 24: 3821-3826.
110. Beyer, K., and B. Nuscher. 1996. Specific cardiolipin binding interferes with labeling of sulfhydryl residues in the adenosine diphosphate/ adenosine triphosphate carrier protein from beef heart mitochondria. Biochemistry. 35: 15784-15790.
111. Bogdanov, M., and W. Dowhan. 1999. Lipid-assisted protein folding. J. Biol. Chem. 274: 36827-36830.
112. Zardeneta, G., and P. M. Horowitz. 1993. Physical characterization of a reactivatable liposome-bound rhodanese folding intermediate. Biochemistry. 32: 13941-13948.
113. Lange, C., J. H. Nett, B. L. Trumpower, and C. Hunte. 2001. Specific roles of protein-phospholipid interactions in the yeast cytochrome bc1 complex structure. EMBO J. 20: 6591-6600.
114. Shinzawa-Itoh, K., H. Aoyama, K. Muramoto, H. Terada, T. Kurauchi, Y. Tadehara, A. Yamasaki, T. Sugimura, S. Kurono, K. Tsujimoto, et al. 2007. Structure and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase. EMBO J. 26: 1713-1725.
115. Pebay-Peyroula, E., G. Dahout, R. Kahn, V. Trezeguet, G. J. Lauquin, and G. Brandolin. 2003. Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature. 426: 39-44.
116. McAuley, K. E., P. K. Fyfe, J. P. Ridge, N. W. Isaacs, R. J. Cogdell, and M. R. Jones. 1999. Structural details of an interaction between cardiolipin and an integral membrane protein. Proc. Natl. Acad. Sci. USA. 96: 14706-14711.
117. Jormakka, M., S. Tornroth, B. Byrne, and S. Iwata. 2002. Molecular basis of proton motive force generation: structure of formate dehydrogenase N. Science. 295: 1863-1868.
118. Yankovskaya, V., R. Horsefield, S. Tornroth, C. Luna-Chavez, H. Miyoshi, C. Leger, B. Byrne, G. Cecchini, and S. Iwata. 2003. Architecture of succinate dehydrogenase and reactive oxygen species generation. Science. 299: 700-704.
119. Zhang, M., E. Mileykovskaya, and W. Dowhan. 2002. Gluing the respiratory chain together. Cardiolipin is required for supercomplex formation in the inner mitochondrial membrane. J. Biol. Chem. 277: 43553-43556.
120. Pfeiffer, K., V. Gohil, R. A. Stuart, C. Hunte, U. Brandt, M. L. Greenberg, and H. Schägger. 2003. Cardiolipin stabilizes respiratory chain supercomplexes. J. Biol. Chem. 278: 52873-52880.
121. Zhang, M., E. Mileykovskaya, and W. Dowhan. 2005. Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria. J. Biol. Chem. 280: 29403-29408.
122. McKenzie, M., M. Lazarou, D. R. Thorburn, and M. T. Ryan. 2006. Mitochondrial respiratory chain supercomplexes are destabilized in Barth syndrome patients. J. Mol. Biol. 361: 462-469.
123. Ma, L., F. M. Vaz, Z. Gu, R. J. A. Wanders, and M. L. Greenberg. 2004. The human TAZ gene complements mitochondrial dysfunction in yeast taz1Δ mutant. Implications for Barth syndrome. J. Biol. Chem. 279: 44394-44399.
124. Xu, Y., J. J. Sutachan, H. Plesken, R. I. Kelley, and M. Schlame. 2005. Characterization of lymphoblast mitochondria from patients with Barth syndrome. Lab. Invest. 85: 823-830.
125. Kagan, V. E., V. A. Tyurin, I. Jiang, Y. Y. Tyurina, V. B. Ritov, A. A. Amoscato, A. N. Osipov, N. A. Belikova, A. A. Kapralov, V. Kini, et al. 2005. Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat. Chem. Biol. 1: 223-232.
126. Lesnefsky, E. J., T. J. Slabe, M. S. K. Stoll, P. E. Minkler, and C. L. Hoppel. 2001. Myocardial ischemia selectively depletes cardiolipin in rabbit heart subsarcolemmal mitochondria. Am. J. Physiol. 280: H2770-H2778.
127. Paradies, G., G. Petrosillo, M. Pistolese, N. Di Venosa, A. Federici, and F. M. Ruggiero. 2004. Decrease in mitochondrial complex I activity in ischemic/reperfused rat heart: involvement of reactive oxygen species and cardiolipin. Circ. Res. 94: 53-59.
128. Ostrander, D. B., G. C. Sparagna, A. A. Amoscato, J. B. McMillin, and W. Dowhan. 2001. Decreased cardiolipin synthesis corresponds with cytochrome c release in palmitate-induced cardiomyocyte apoptosis. J. Biol. Chem. 276: 38061-38067.
129. Choi, S-Y., F. Gonzalvez, G. M. Jenkins, C. Slomianny, D. Chretien, D. Arnoult, P. X. Petit, and M. A. Frohman. 2006. Cardiolipin deficiency releases cytochrome c from the inner mitochondrial membrane and accelerates stimuli-elicited apoptosis. Cell Death Differ. 14: 597-606.
130. Petrosillo, G., F. M. Ruggiero, and G. Paradies. 2003. Role of reactive oxygen species and cardiolipin in the release of cytochrome c from mitochondria. FASEB J. 17: 2202-2208.
131. Nomura, K., H. Imai, T. Koumura, T. Kobayashi, and Y. Nakagawa. 2000. Mitochondrial phospholipid hydroperoxide glutathione peroxidase inhibits the release of cytochrome c from mitochondria by suppressing the peroxidation of cardiolipin in hypoglycaemiainduced apoptosis. Biochem. J. 351: 183-193.
132. Heath-Engel, H. M., and G. C. Shore. 2006. Mitochondrial membrane dynamics, cristae remodeling and apoptosis. Biochim. Biophys. Acta. 1763: 549-560.
133. Ott, M., B. Zhivotovsky, and S. Orrenius. 2007. Role of cardiolipin in cytochrome c release from mitochondria. Cell Death Differ. 14: 1243-1247.
134. Schlame, M., I. Haller, L. R. Sammaritano, and T. J. J. Blanck. 2001. Effect of cardiolipin oxidation on solid-phase immunoassay for antiphospholipid antibodies. Thromb. Haemost. 86: 1475-1482.
135. Williams, S. D., and R. A. Gottlieb. 2002. Inhibition of mitochondrial calcium-independent phospholipase A2 (iPLA2) attenuates mitochondrial phospholipid loss and is cardioprotective. Biochem. J. 362: 23-32.
136. 2χ. J. Biol. Chem. 282: 9216-9227.
137. 2β3 is a novel variant localized to mitochondria and early endosomes. J. Biol. Chem. 281: 16615-16624.
138. Valianpour, F., V. Mitsakos, D. Schlemmer, J. A. Towbin, J. M. Taylor, P. G. Ekert, D. R. Thorburn, A. Munnich, R. J. A. Wanders, P. G. Barth, et al. 2005. Monolysocardiolipins accumulate in Barth syndrome but do not lead to enhanced apoptosis. J. Lipid Res. 46: 1182-1195.
139. Esposti, M. D., I. M. Cristea, S. J. Gaskell, Y. Nakao, and C. Dive. 2003. Proapoptotic Bid binds to monolysocardiolipin, a new molecular connection between mitochondrial membranes and cell death. Cell Death Differ. 10: 1300-1309.
140. Tyurin, V. A., Y. Y. Tyurina, A. N. Osipov, N. A. Belikova, L. V. Basova, A. A. Kapralov, H. Bayir, and V. E. Kagan. 2007. Interactions of cardiolipin and lyso-cardiolipins with cytochrome c and tBid: conflict or assistance in apoptosis. Cell Death Differ. 14: 872-875.
141. Choi, S-Y., P. Huang, G. M. Jenkins, D. C. Chan, J. Schiller, and M. A. Frohman. 2006. A common lipid links Mfn-mediated mitochondrial fusion and SNARE-regulated exocytosis. Nat. Cell Biol. 8: 1255-1262.