Specific requirements of nonbilayer phospholipids in mitochondrial respiratory chain function and formation

Molecular Biology of the Cell

Volumn 27, Issue 14, 2016, Pages 2161-2171

  Baker, Charli D ^a   Ball, Writoban Basu ^a   Pryce, Erin N ^b   Gohil, Vishal M ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; CARDIOLIPIN; PHOSPHOLIPID;

ANIMAL CELL; ARTICLE; BIOGENESIS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; LIPOGENESIS; MITOCHONDRIAL RESPIRATION; MITOCHONDRIAL RESPIRATORY CHAIN; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RESPIRATORY CHAIN; SIGNAL TRANSDUCTION; ELECTRON TRANSPORT; METABOLISM; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

CARDIOLIPINS; ELECTRON TRANSPORT; ENDOPLASMIC RETICULUM; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLETHANOLAMINES; PHOSPHOLIPIDS; SACCHAROMYCES CEREVISIAE;

EID: 84978640742     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E15-12-0865     Document Type: Article

References (53)

1. Acín-Pérez R, Fernández-Silva P, Peleato ML, Pérez-Martos A, Enriquez JA (2008). Respiratory active mitochondrial supercomplexes. Mol Cell 32, 529-539.
2. AhYoung AP, Jiang J, Zhang J, Khoi Dang X, Loo JA, Zhou ZH, Egea PF (2015). Conserved SMP domains of the ERMES complex bind phospholipids and mediate tether assembly. Proc Natl Acad Sci USA 112, 3179-3188.
3. Aktas M, Wessel M, Hacker S, Klusener S, Gleichenhagen J, Narberhaus F (2010). Phosphatidylcholine biosynthesis and its significance in bacteria interacting with eukaryotic cells. Eur J Cell Biol 89, 888-894.
4. Amberg DC, Burke DJ, Strathern JN (2005). Methods in Yeast Genetics. A Cold Spring Harbor Laboratory Course Manual, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
5. Bartlett GR (1959). Phosphorus assay in column chromatography. J Biol Chem 234, 466-468.
6. Bazán S, Mileykovskaya E, Mallampalli VK, Heacock P, Sparagna GC, Dowhan W (2013). Cardiolipin-dependent reconstitution of respiratory supercomplexes from purified Saccharomyces cerevisiae complexes III and IV. J Biol Chem 288, 401-411.
7. Birner R, Burgermeister M, Schneiter R, Daum G (2001). Roles of phosphatidylethanolamine and of its several biosynthetic pathways in Saccharomyces cerevisiae. Mol Biol Cell 12, 997-1007.
8. Bottinger L, Horvath SE, Kleinschroth T, Hunte C, Daum G, Pfanner N, Becker T (2012). Phosphatidylethanolamine and cardiolipin differentially affect the stability of mitochondrial respiratory chain supercomplexes. J Mol Biol 423, 677-686.
9. Boumann HA, Gubbens J, Koorengevel MC, Oh CS, Martin CE, Heck AJ, Patton-Vogt J, Henry SA, de Kruijff B, de Kroon AI (2006). Depletion of phosphatidylcholine in yeast induces shortening and increased saturation of the lipid acyl chains: evidence for regulation of intrinsic membrane curvature in a eukaryote. Mol Biol Cell 17, 1006-1017.
10. Börgermeister M, Birner-Grönberger R, Heyn M, Daum G (2004a). Contribution of different biosynthetic pathways to species selectivity of aminoglycerophospholipids assembled into mitochondrial membranes of the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1686, 148-160.
11. Börgermeister M, Birner-Grunberger R, Nebauer R, Daum G (2004b). Contribution of different pathways to the supply of phosphatidylethanolamine and phosphatidylcholine to mitochondrial membranes of the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1686, 161-168.
12. Carman GM, Han GS (2011). Regulation of phospholipid synthesis in the yeast Saccharomyces cerevisiae. Annu Rev Biochem 80, 859-883.
13. Chan EY, McQuibban GA (2012). Phosphatidylserine decarboxylase 1 (Psd1) promotes mitochondrial fusion by regulating the biophysical properties of the mitochondrial membrane and alternative topogenesis of mitochondrial genome maintenance protein 1 (Mgm1). J Biol Chem 287, 40131-40139.
14. Chicco AJ, Sparagna GC (2007). Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am J Physiol Cell Physiol 292, 33-44.
15. Choi JY, Martin WE, Murphy RC, Voelker DR (2004). Phosphatidylcholine and N-methylated phospholipids are nonessential in Saccharomyces cerevisiae. J Biol Chem 279, 42321-42330.
16. Cogliati S, Frezza C, Soriano ME, Varanita T, Quintana-Cabrera R, Corrado M, Cipolat S, Costa V, Casarin A, Gomes LC, et al. (2013). Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency. Cell 155, 160-171.
17. Daum G (1985). Lipids of mitochondria. Biochim Biophys Acta 822, 1-42.
18. Dudkina NV, Kudryashev M, Stahlberg H, Boekema EJ (2011). Interaction of complexes I, III, and IV within the bovine respirasome by single particle cryoelectron tomography. Proc Natl Acad Sci USA 108, 15196-15200.
19. Folch J, Lees M, Sloane Stanley GH (1957). A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226, 497-509.
20. Gohil VM, Greenberg ML (2009). Mitochondrial membrane biogenesis: phospholipids and proteins go hand in hand. J Cell Biol 184, 469-472.
21. Gohil VM, Thompson MN, Greenberg ML (2005). Synthetic lethal interaction of the mitochondrial phosphatidylethanolamine and cardiolipin biosynthetic pathways in Saccharomyces cerevisiae. J Biol Chem 280, 35410-35416.
22. Gulshan K, Shahi P, Moye-Rowley WS (2010). Compartment-specific synthesis of phosphatidylethanolamine is required for normal heavy metal resistance. Mol Biol Cell 21, 443-455.
23. Holthuis JC, Menon AK (2014). Lipid landscapes and pipelines in membrane homeostasis. Nature 510, 48-57.
24. Horvath SE, Wagner A, Steyrer E, Daum G (2011). Metabolic link between phosphatidylethanolamine and triacylglycerol metabolism in the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1811, 1030-1037.
25. Horvath SE, Daum G (2013). Lipids of mitochondria. Prog Lipid Res 52, 590-614.
26. Janke C, Magiera MM, Rathfelder N, Taxis C, Reber S, Maekawa H, Moreno-Borchart A, Doenges G, Schwob E, Schiebel E, Knop M (2004). A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21, 947-962.
27. Joshi AS, Zhou J, Gohil VM, Chen S, Greenberg ML (2009). Cellular functions of cardiolipin in yeast. Biochim Biophys Acta 1793, 212-218.
28. Koopman WJ, Willems PH, Smeitink JA (2012). Monogenic mitochondrial disorders. N Engl J Med 366, 1132-1141.
29. Kornmann B, Currie E, Collins SR, Schuldiner M, Nunnari J, Weissman JS, Walter P (2009). An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325, 477-481.
30. Lahiri S, Toulmay A, Prinz WA (2015). Membrane contact sites, gateways for lipid homeostasis. Curr Opin Cell Biol 33, 82-87.
31. Lu YW, Claypool SM (2015). Disorders of phospholipid metabolism: An emerging class of mitochondrial disease due to defects in nuclear genes. Front Genet 6, 1-27.
32. Meisinger C, Pfanner N, Truscott KN (2006). Isolation of yeast mitochondria. Methods Mol Biol 313, 33-39.
33. Mileykovskaya E, Dowhan W (2014). Cardiolipin-dependent formation of mitochondrial respiratory supercomplexes. Chem Phys Lipids 179, 42-48.
34. Nunnari J, Suomalainen A (2012). Mitochondria: in sickness and in health. Cell 148, 1145-1159.
35. Osman C, Voelker DR, Langer T (2011). Making heads or tails of phospholipids in mitochondria. J Cell Biol 192, 7-16.
36. Pfeiffer K, Gohil V, Stuart RA, Hunte C, Brandt U, Greenberg ML, Schagger H (2003). Cardiolipin stabilizes respiratory chain supercomplexes. J Biol Chem 278, 52873-52880.
37. Ren M, Phoon CK, Schlame M (2014). Metabolism and function of mitochondrial cardiolipin. Prog Lipid Res 55, 1-16.
38. Riekhof WR, Voelker DR (2006). Uptake and utilization of lyso-phosphatidylethanolamine by Saccharomyces cerevisiae. J Biol Chem 281, 36588-36596.
39. Schagger H, Pfeiffer K (2000). Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J 19, 1777-1783.
40. Schuler MH, Di Bartolomeo F, Bottinger L, Horvath SE, Wenz LS, Daum G, Becker T (2015). Phosphatidylcholine affects the role of the sorting and assembly machinery in the biogenesis of mitochondrial β-barrel proteins. J Biol Chem 290, 26523-26532.
41. Storey MK, Clay KL, Kutateladze T, Murphy RC, Overduin M, Voelker DR (2001). Phosphatidylethanolamine has an essential role in Saccharomyces cerevisiae that is independent of its ability to form hexagonal phase structures. J Biol Chem 276, 48539-48548.
42. Tasseva G, Bai HD, Davidescu M, Haromy A, Michelakis E, Vance JE (2013). Phosphatidylethanolamine deficiency in mammalian mitochondria impairs oxidative phosphorylation and alters mitochondrial morphology. J Biol Chem 288, 4158-4173.
43. Tuller G, Nemec T, Hrastnik C, Daum G (1999). Lipid composition of subcellular membranes of an FY1679-derived haploid yeast wild-Type strain grown on different carbon sources. Yeast 15, 1555-1564.
44. Vafai SB, Mootha VK (2012). Mitochondrial disorders as windows into an ancient organelle. Nature 491, 374-383.
45. van der Veen JN, Lingrell S, da Silva RP, Jacobs RL, Vance DE (2014). The concentration of phosphatidylethanolamine in mitochondria can modulate ATP production and glucose metabolism in mice. Diabetes 63, 2620-2630.
46. van Meer G, Voelker DR, Feigenson GW (2008). Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9, 112-124.
47. Walters AM, Porter GA Jr, Brookes PS (2012). Mitochondria as a drug target in ischemic heart disease and cardiomyopathy. Circ Res 111, 1222-1236.
48. Wang S, Zhang S, Liou LC, Ren Q, Zhang Z, Caldwell GA, Caldwell KA, Witt SN (2014). Phosphatidylethanolamine deficiency disrupts α-synuclein homeostasis in yeast and worm models of Parkinson disease. Proc Natl Acad Sci USA 111, 3976-E3985.
49. Weinberg SE, Chandel NS (2015). Targeting mitochondria metabolism for cancer therapy. Nat Chem Biol 11, 9-15.
50. Wenz T, Hielscher R, Hellwig P, Schägger H, Richers S, Hunte C (2009). Role of phospholipids in respiratory cytochrome bc(1) complex catalysis and supercomplex formation. Biochim Biophys Acta 1787, 609-616.
51. Wittig I, Braun HP, Schagger H (2006). Blue native PAGE. Nat Protoc 1, 418-428.
52. Wittig I, Karas M, Schagger H (2007). High resolution clear native electrophoresis for in-gel functional assays and fluorescence studies of membrane protein complexes. Mol Cell Proteomics 6, 1215-1225.
53. Zhang M, Mileykovskaya E, 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.