Phospholipid transport via mitochondria

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Volumn 15, Issue 9, 2014, Pages 933-945

  Tamura, Yasushi ^a   Sesaki, Hiromi ^b   Endo, Toshiya ^c  

^a NAGOYA UNIVERSITY   (Japan)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c KYOTO SANGYO UNIVERSITY   (Japan)

Author keywords

Cardiolipin; ERMES; Flippase; Membrane contact site; Mitochondria; Phospholipid; Scramblase; Ups protein

Indexed keywords

CYTIDINE DIPHOSPHATE DIGLYCERIDE; MEMBRANE PROTEIN; PHOSPHOLIPID; PROTEIN MDM35; PROTEIN UPS1; UNCLASSIFIED DRUG;

CELL MEMBRANE; COMPLEX FORMATION; ENDOPLASMIC RETICULUM; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; PHOSPHOLIPID SYNTHESIS; PHOSPHOLIPID TRANSFER; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; METABOLISM; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; ENDOPLASMIC RETICULUM; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; PHOSPHOLIPIDS;

EID: 84906318502     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12188     Document Type: Review

References (90)

1. Henry SA, Kohlwein SD, Carman GM. Metabolism and regulation of glycerolipids in the yeast Saccharomyces cerevisiae. Genetics 2012;190:317-349.
2. Horvath SE, Daum G. Lipids of mitochondria. Prog Lipid Res 2013;52:590-614.
3. Gibellini F, Smith TK. The Kennedy pathway - De novo synthesis of phosphatidylethanolamine and phosphatidylcholine. IUBMB Life 2010;62:414-428.
4. Osman C, Voelker DR, Langer T. Making heads or tails of phospholipids in mitochondria. J Cell Biol 2011;192:7-16.
5. Scharwey M, Tatsuta T, Langer T. Mitochondrial lipid transport at a glance. J Cell Sci 2013;126:5317-5323.
6. Tatsuta T, Scharwey M, Langer T. Mitochondrial lipid trafficking. Trends Cell Biol 2014;24:44-52.
7. Athenstaedt K, Daum G. Biosynthesis of phosphatidic acid in lipid particles and endoplasmic reticulum of Saccharomyces cerevisiae. J Bacteriol 1997;179:7611-7616.
8. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, O'Shea EK. Global analysis of protein localization in budding yeast. Nature 2003;425:686-691.
9. Jain S, Stanford N, Bhagwat N, Seiler B, Costanzo M, Boone C, Oelkers P. Identification of a novel lysophospholipid acyltransferase in Saccharomyces cerevisiae. J Biol Chem 2007;282:30562-30569.
10. Han GS, O'Hara L, Carman GM, Siniossoglou S. An unconventional diacylglycerol kinase that regulates phospholipid synthesis and nuclear membrane growth. J Biol Chem 2008;283:20433-20442.
11. Shen H, Heacock PN, Clancey CJ, Dowhan W. CDS1 gene encoding CDP-diacylglycerol synthase in Saccharomyces cerevisiae is essential for cell growth. J Biol Chem 1996;27:789-795.
12. Tamura Y, Harada Y, Nishikawa S, Yamano K, Kamiya M, Shiota T, Kuroda T, Kuge O, Sesaki H, Imai K, Tomii K, Endo T. Tam41 is a CDP-diacylglycerol synthase required for cardiolipin biosynthesis in mitochondria. Cell Metab 2013;17:709-718.
13. Letts VA, Klig LS, Bae-Lee M, Carman GM, Henry SA. Isolation of the yeast structural gene for the membrane-associated enzyme phosphatidylserine synthase. Proc Natl Acad Sci USA 1983;80:7279-7283.
14. Nikawa J, Kodaki T, Yamashita S. Primary structure and disruption of the phosphatidylinositol synthase gene of Saccharomyces cerevisiae. J Biol Chem 1987;262:4876-4881.
15. Gaigg B, Simbeni R, Hrastnik C, Paltauf F, Daum G. Characterization of a microsomal subfraction associated with mitochondria of the yeast, Saccharomyces cerevisiae. Involvement in synthesis and import of phospholipids into mitochondria. Biochim Biophys Acta 1995;1234:214-220.
16. Fischl AS, Carman GM. Phosphatidylinositol biosynthesis in Saccharomyces cerevisiae: purification and properties of microsome-associated phosphatidylinositol synthase. J Bacteriol 1983;154:304-311.
17. Horvath SE, Bottinger L, Vogtle FN, Wiedemann N, Meisinger C, Becker T, Daum G. Processing and topology of the yeast mitochondrial phosphatidylserine decarboxylase 1. J Biol Chem 2012;287:36744-36755.
18. Chang SC, Heacock PN, Clancey CJ, Dowhan W. The PEL1 gene (renamed PGS1) encodes the phosphatidylglycero-phosphate synthase of Saccharomyces cerevisiae. J Biol Chem 1998;273:9829-9836.
19. Osman C, Haag M, Wieland FT, Brugger B, Langer T. A mitochondrial phosphatase required for cardiolipin biosynthesis: the PGP phosphatase Gep4. EMBO J 2010;29:1976-1987.
20. Tuller G, Hrastnik C, Achleitner G, Schiefthaler U, Klein F, Daum G. YDL142c encodes cardiolipin synthase (Cls1p) and is non-essential for aerobic growth of Saccharomyces cerevisiae. FEBS Lett 1998;421:15-18.
21. Chang SC, Heacock PN, Mileykovskaya E, Voelker DR, Dowhan W. Isolation and characterization of the gene (CLS1) encoding cardiolipin synthase in Saccharomyces cerevisiae. J Biol Chem 1998;273:14933-14941.
22. Baile MG, Whited K, Claypool SM. Deacylation on the matrix side of the mitochondrial inner membrane regulates cardiolipin remodeling. Mol Biol Cell 2013;24:2008-2020.
23. Claypool SM, McCaffery JM, Koehler CM. Mitochondrial mislocalization and altered assembly of a cluster of Barth syndrome mutant tafazzins. J Cell Biol 2006;174:379-390.
24. Joshi AS, Zhou J, Gohil VM, Chen S, Greenberg ML. Cellular functions of cardiolipin in yeast. Biochim Biophys Acta 2009;1793:212-218.
25. Claypool SM, Koehler CM. The complexity of cardiolipin in health and disease. Trends Biochem Sci 2012;37:32-41.
26. Gebert N, Joshi AS, Kutik S, Becker T, McKenzie M, Guan XL, Mooga VP, Stroud DA, Kulkarni G, Wenk MR, Rehling P, Meisinger C, Ryan MT, Wiedemann N, Greenberg ML, et al. Mitochondrial cardiolipin involved in outer-membrane protein biogenesis: implications for Barth syndrome. Curr Biol 2009;19:2133-2139.
27. Chu CT, Ji J, Dagda RK, Jiang JF, Tyurina YY, Kapralov AA, Tyurin VA, Yanamala N, Shrivastava IH, Mohammadyani D, Qiang Wang KZ, Zhu J, Klein-Seetharaman J, Balasubramanian K, Amoscato AA, et al. Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells. Nat Cell Biol 2013;15:1197-1205.
28. Chu CT, Bayir H, Kagan VE. LC3 binds externalized cardiolipin on injured mitochondria to signal mitophagy in neurons: implications for Parkinson disease. Autophagy 2014;10:376-378.
29. Zinser E, Sperka-Gottlieb CD, Fasch EV, Kohlwein SD, Paltauf F, Daum G. Phospholipid synthesis and lipid composition of subcellular membranes in the unicellular eukaryote Saccharomyces cerevisiae. J Bacteriol 1991;173:2026-2034.
30. de Kroon AI, Dolis D, Mayer A, Lill R, de Kruijff B. Phospholipid composition of highly purified mitochondrial outer membranes of rat liver and Neurospora crassa. Is cardiolipin present in the mitochondrial outer membrane? Biochim Biophys Acta 1997;1325:108-116.
31. Palade G. Intracellular aspects of the process of protein synthesis. Science 1975;189:867.
32. Whyte JR, Munro S. Vesicle tethering complexes in membrane traffic. J Cell Sci 2002;115:2627-2637.
33. Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 2009;10:513-525.
34. Lev S. Non-vesicular lipid transport by lipid-transfer proteins and beyond. Nat Rev Mol Cell Biol 2010;11:739-750.
35. Toulmay A, Prinz WA. Lipid transfer and signaling at organelle contact sites: the tip of the iceberg. Curr Opin Cell Biol 2011;23:458-463.
36. Helle SC, Kanfer G, Kolar K, Lang A, Michel AH, Kornmann B. Organization and function of membrane contact sites. Biochim Biophys Acta 2013;1833:2526-2541.
37. Voelker DR. New perspectives on the regulation of intermembrane glycerophospholipid traffic. J Lipid Res 2003;44:441-449.
38. Hayashi T, Rizzuto R, Hajnoczky G, Su TP. MAM: more than just a housekeeper. Trends Cell Biol 2009;19:81-88.
39. Vance JE. MAM (mitochondria-associated membranes) in mammalian cells: lipids and beyond. Biochim Biophys Acta 2014;1841:595-609.
40. Kornmann B, Currie E, Collins SR, Schuldiner M, Nunnari J, Weissman JS, Walter P. An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 2009;325:477-481.
41. Stroud DA, Oeljeklaus S, Wiese S, Bohnert M, Lewandrowski U, Sickmann A, Guiard B, van der Laan M, Warscheid B, Wiedemann N. Composition and topology of the endoplasmic reticulum-mitochondria encounter structure. J Mol Biol 2011;413:743-750.
42. Burgess SM, Delannoy M, Jensen RE. MMM1 encodes a mitochondrial outer membrane protein essential for establishing and maintaining the structure of yeast mitochondria. J Cell Biol 1994;126:1375-1391.
43. Sogo LF, Yaffe MP. Regulation of mitochondrial morphology and inheritance by Mdm10p, a protein of the mitochondrial outer membrane. J Cell Biol 1994;126:1361-1373.
44. Berger KH, Sogo LF, Yaffe MP. Mdm12p, a component required for mitochondrial inheritance that is conserved between budding and fission yeast. J Cell Biol 1997;136:545-553.
45. Dimmer KS, Fritz S, Fuchs F, Messerschmitt M, Weinbach N, Neupert W, Westermann B. Genetic basis of mitochondrial function and morphology in Saccharomyces cerevisiae. Mol Biol Cell 2002;13:847-853.
46. Frederick RL, Okamoto K, Shaw JM. Multiple pathways influence mitochondrial inheritance in budding yeast. Genetics 2008;178:825-837.
47. Youngman MJ, Hobbs AE, Burgess SM, Srinivasan M, Jensen RE. Mmm2p, a mitochondrial outer membrane protein required for yeast mitochondrial shape and maintenance of mtDNA nucleoids. J Cell Biol 2004;164:677-688.
48. Hobbs AE, Srinivasan M, McCaffery JM, Jensen RE. Mmm1p, a mitochondrial outer membrane protein, is connected to mitochondrial DNA (mtDNA) nucleoids and required for mtDNA stability. J Cell Biol 2001;152:401-410.
49. Kornmann B, Osman C, Walter P. The conserved GTPase Gem1 regulates endoplasmic reticulum-mitochondria connections. Proc Natl Acad Sci USA 2011;108:14151-14156.
50. Yamano K, Tanaka-Yamano S, Endo T. Tom7 regulates Mdm10-mediated assembly of the mitochondrial import channel protein Tom40. J Biol Chem 2010;285:41222-41231.
51. Kopec KO, Alva V, Lupas AN. Homology of SMP domains to the TULIP superfamily of lipid-binding proteins provides a structural basis for lipid exchange between ER and mitochondria. Bioinformatics 2010;26:1927-1931.
52. Kopec KO, Alva V, Lupas AN. Bioinformatics of the TULIP domain superfamily. Biochem Soc Trans 2011;39:1033-1038.
53. Nguyen TT, Lewandowska A, Choi JY, Markgraf DF, Junker M, Bilgin M, Ejsing CS, Voelker DR, Rapoport TA, Shaw JM. Gem1 and ERMES do not directly affect phosphatidylserine transport from ER to mitochondria or mitochondrial inheritance. Traffic 2012;13:880-890.
54. Voss C, Lahiri S, Young BP, Loewen CJ, Prinz WA. ER-shaping proteins facilitate lipid exchange between the ER and mitochondria in S. cerevisiae. J Cell Sci 2012;125:4791-4799.
55. Connerth M, Tatsuta T, Haag M, Klecker T, Westermann B, Langer T. Intramitochondrial transport of phosphatidic acid in yeast by a lipid transfer protein. Science 2012;338:815-818.
56. Sesaki H, Dunn CD, Iijima M, Shepard KA, Yaffe MP, Machamer CE, Jensen RE. Ups1p, a conserved intermembrane space protein, regulates mitochondrial shape and alternative topogenesis of Mgm1p. J Cell Biol 2006;173:651-658.
57. Herlan M, Bornhovd C, Hell K, Neupert W, Reichert AS. Alternative topogenesis of Mgm1 and mitochondrial morphology depend on ATP and a functional import motor. J Cell Biol 2004;165:167-173.
58. Herlan M, Vogel F, Bornhovd C, Neupert W, Reichert AS. Processing of Mgm1 by the rhomboid-type protease Pcp1 is required for maintenance of mitochondrial morphology and of mitochondrial DNA. J Biol Chem 2003;278:27781-27788.
59. McQuibban GA, Saurya S, Freeman M. Mitochondrial membrane remodelling regulated by a conserved rhomboid protease. Nature 2003;423:537-541.
60. Sesaki H, Southard SM, Hobbs AE, Jensen RE. Cells lacking Pcp1p/Ugo2p, a rhomboid-like protease required for Mgm1p processing, lose mtDNA and mitochondrial structure in a Dnm1p-dependent manner, but remain competent for mitochondrial fusion. Biochem Biophys Res Commun 2003;308:276-283.
61. Tamura Y, Endo T, Iijima M, Sesaki H. Ups1p and Ups2p antagonistically regulate cardiolipin metabolism in mitochondria. J Cell Biol 2009;185:1029-1045.
62. Osman C, Haag M, Potting C, Rodenfels J, Dip PV, Wieland FT, Brugger B, Westermann B, Langer T. The genetic interactome of prohibitins: coordinated control of cardiolipin and phosphatidylethanolamine by conserved regulators in mitochondria. J Cell Biol 2009;184:583-596.
63. Tamura Y, Iijima M, Sesaki H. Mdm35p imports Ups proteins into the mitochondrial intermembrane space by functional complex formation. EMBO J 2010;29:2875-2887.
64. Potting C, Wilmes C, Engmann T, Osman C, Langer T. Regulation of mitochondrial phospholipids by Ups1/PRELI-like proteins depends on proteolysis and Mdm35. EMBO J 2010;29:2888-2898.
65. Kutik S, Rissler M, Guan XL, Guiard B, Shui G, Gebert N, Heacock PN, Rehling P, Dowhan W, Wenk MR, Pfanner N, Wiedemann N. The translocator maintenance protein Tam41 is required for mitochondrial cardiolipin biosynthesis. J Cell Biol 2008;183:1213-1221.
66. Kuroda T, Tani M, Moriguchi A, Tokunaga S, Higuchi T, Kitada S, Kuge O. FMP30 is required for the maintenance of a normal cardiolipin level and mitochondrial morphology in the absence of mitochondrial phosphatidylethanolamine synthesis. Mol Microbiol 2011;80:248-265.
67. Joshi AS, Thompson MN, Fei N, Huttemann M, Greenberg ML. Cardiolipin and mitochondrial phosphatidylethanolamine have overlapping functions in mitochondrial fusion in Saccharomyces cerevisiae. J Biol Chem 2012;287:17589-17597.
68. Tamura Y, Onguka O, Itoh K, Endo T, Iijima M, Claypool SM, Sesaki H. Phosphatidylethanolamine biosynthesis in mitochondria: phosphatidylserine (PS) trafficking is independent of a PS decarboxylase and intermembrane space proteins UPS1P and UPS2P. J Biol Chem 2012;287:43961-43971.
69. Tamura Y, Onguka O, Hobbs AE, Jensen RE, Iijima M, Claypool SM, Sesaki H. Role for two conserved intermembrane space proteins, Ups1p and Ups2p, in intra-mitochondrial phospholipid trafficking. J Biol Chem 2012;287:15205-15218.
70. Tamura Y, Harada Y, Shiota T, Yamano K, Watanabe K, Yokota M, Yamamoto H, Sesaki H, Endo T. Tim23-Tim50 pair coordinates functions of translocators and motor proteins in mitochondrial protein import. J Cell Biol 2009;184:129-141.
71. Shiota T, Mabuchi H, Tanaka-Yamano S, Yamano K, Endo T. In vivo protein-interaction mapping of a mitochondrial translocator protein Tom22 at work. Proc Natl Acad Sci USA 2011;108:15179-15183.
72. Wurm CA, Jakobs S. Differential protein distributions define two sub-compartments of the mitochondrial inner membrane in yeast. FEBS Lett 2006;580:5628-5634.
73. Wong ED, Wagner JA, Scott SV, Okreglak V, Holewinske TJ, Cassidy-Stone A, Nunnari J. The intramitochondrial dynamin-related GTPase, Mgm1p, is a component of a protein complex that mediates mitochondrial fusion. J Cell Biol 2003;160:303-311.
74. Sesaki H, Jensen RE. Ugo1p links the Fzo1p and Mgm1p GTPases for mitochondrial fusion. J Biol Chem 2004;279:28298-28303.
75. Sesaki H, Southard SM, Yaffe MP, Jensen RE. Mgm1p, a dynamin-related GTPase, is essential for fusion of the mitochondrial outer membrane. Mol Biol Cell 2003;14:2342-2356.
76. Harner M, Korner C, Walther D, Mokranjac D, Kaesmacher J, Welsch U, Griffith J, Mann M, Reggiori F, Neupert W. The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J 2011;30:4356-4370.
77. von der Malsburg K, Muller JM, Bohnert M, Oeljeklaus S, Kwiatkowska P, Becker T, Loniewska-Lwowska A, Wiese S, Rao S, Milenkovic D, Hutu DP, Zerbes RM, Schulze-Specking A, Meyer HE, Martinou JC, et al. Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis. Dev Cell 2011;21:694-707.
78. Hoppins S, Collins SR, Cassidy-Stone A, Hummel E, Devay RM, Lackner LL, Westermann B, Schuldiner M, Weissman JS, Nunnari J. A mitochondrial-focused genetic interaction map reveals a scaffold-like complex required for inner membrane organization in mitochondria. J Cell Biol 2011;195:323-340.
79. Pfanner N, van der Laan M, Amati P, Capaldi RA, Caudy AA, Chacinska A, Darshi M, Deckers M, Hoppins S, Icho T, Jakobs S, Ji J, Kozjak-Pavlovic V, Meisinger C, Odgren PR, et al. Uniform nomenclature for the mitochondrial contact site and cristae organizing system. J Cell Biol 2014;204:1083-1086.
80. Dimmer KS, Jakobs S, Vogel F, Altmann K, Westermann B. Mdm31 and Mdm32 are inner membrane proteins required for maintenance of mitochondrial shape and stability of mitochondrial DNA nucleoids in yeast. J Cell Biol 2005;168:103-115.
81. Tan T, Ozbalci C, Brugger B, Rapaport D, Dimmer KS. Mcp1 and Mcp2, two novel proteins involved in mitochondrial lipid homeostasis. J Cell Sci 2013;126:3563-3574.
82. Lackner LL, Ping H, Graef M, Murley A, Nunnari J. Endoplasmic reticulum-associated mitochondria-cortex tether functions in the distribution and inheritance of mitochondria. Proc Natl Acad Sci USA 2013;110:E458-E467.
83. Sebastian TT, Baldridge RD, Xu P, Graham TR. Phospholipid flippases: building asymmetric membranes and transport vesicles. Biochim Biophys Acta 2012;1821:1068-1077.
84. Liu J, Epand RF, Durrant D, Grossman D, Chi NW, Epand RM, Lee RM. Role of phospholipid scramblase 3 in the regulation of tumor necrosis factor-alpha-induced apoptosis. Biochemistry 2008;47:4518-4529.
85. Voelker DR. Reconstitution of phosphatidylserine import into rat liver mitochondria. J Biol Chem 1989;264:8019-8025.
86. Simbeni R, Tangemann K, Schmidt M, Ceolotto C, Paltauf F, Daum G. Import of phosphatidylserine into isolated yeast mitochondria. Biochim Biophys Acta 1993;1145:1-7.
87. Achleitner G, Zweytick D, Trotter PJ, Voelker DR, Daum G. Synthesis and intracellular transport of aminoglycerophospholipids in permeabilized cells of the yeast, Saccharomyces cerevisiae. J Biol Chem 1995;270:29836-29842.
88. Shiao YJ, Balcerzak B, Vance JE. A mitochondrial membrane protein is required for translocation of phosphatidylserine from mitochondria-associated membranes to mitochondria. Biochem J 1998;331:217-223.
89. Wu WI, Voelker DR. Characterization of phosphatidylserine transport to the locus of phosphatidylserine decarboxylase 2 in permeabilized yeast. J Biol Chem 2001;276:7114-7121.
90. Wu WI, Voelker DR. Reconstitution of phosphatidylserine transport from chemically defined donor membranes to phosphatidylserine decarboxylase 2 implicates specific lipid domains in the process. J Biol Chem 2004;279:6635-6642.