Biogenesis of Fatty Acids, Lipids and Membranes pp 553-574 | Cite as
Functional Roles of Individual Membrane Phospholipids in Escherichia coli and Saccharomyces cerevisiae
Abstract
The physical and chemical properties of membrane lipids containing both a hydrophobic and hydrophilic domain result in organization into the lipid bilayer that provides the barrier function and defines the limits of cells and organelles. The lipid bilayer provides the solvent for integral membrane proteins and the scaffold with which peripheral membrane proteins associate. The properties of the lipid bilayer are defined by the collective properties of the diverse mixture of resident lipids. The lipidome is composed of glycerol-based phospholipids and glycolipids found in bacteria and the additional steroids and sphingolipids found in eukaryotic cells. The diversity of the lipidome far exceeds that of the proteome when the composition of both the hydrophilic and hydrophilic domains is considered. Therefore, it is not surprising that the diverse physical, chemical, and collective properties of the membrane bilayer have a profound effect on the structure and function of membrane-associated proteins. Lipids affect membrane proteins through the collective properties of the lipid bilayer and through direct specific lipid-protein interactions. Given the vast complexity and diversity of the influence of lipids on membrane proteins throughout nature, this review will focus on selected roles of lipids in Escherichia coli and Saccharomyces cerevisiae. The lipid genetics of each organism will be reviewed in relation to the phenotypes resulting from mutations in lipid biosynthetic pathways. The combined use of genetic manipulation and biochemical characterization will be outlined as a means to establish an understanding at the molecular level of the importance of lipids in cellular processes.
References
- Baile MG, Sathappa M, Lu YW, Pryce E, Whited K, McCaffery JM, Han X, Alder NN, Claypool SM (2014) Unremodeled and remodeled cardiolipin are functionally indistinguishable in yeast. J Biol Chem 289:1768–1778PubMedCrossRefPubMedCentralGoogle Scholar
- Baker CD, Basu Ball W, Pryce EN, Gohil VM (2016) Specific requirements of nonbilayer phospholipids in mitochondrial respiratory chain function and formation. Mol Biol Cell 27:2161–2171PubMedPubMedCentralCrossRefGoogle Scholar
- 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 288:401–411PubMedCrossRefPubMedCentralGoogle Scholar
- Bogdanov M, Dowhan W (1995) Phosphatidylethanolamine is required for in vivo function of the membrane-associated lactose permease of Escherichia coli. J Biol Chem 270:732–739PubMedCrossRefPubMedCentralGoogle Scholar
- Bogdanov M, Dowhan W (2012) Lipid-dependent generation of dual topology for a membrane protein. J Biol Chem 287:37939–37948PubMedPubMedCentralCrossRefGoogle Scholar
- Bogdanov M, Xie J, Heacock P, Dowhan W (2008) To flip or not to flip: lipid-protein charge interactions are a determinant of final membrane protein topology. J Cell Biol 182:925–935PubMedPubMedCentralCrossRefGoogle Scholar
- Bogdanov M, Heacock P, Guan Z, Dowhan W (2010) Plasticity of lipid-protein interactions in the function and topogenesis of the membrane protein lactose permease from Escherichia coli. Proc Natl Acad Sci U S A 107:15057–15062PubMedPubMedCentralCrossRefGoogle Scholar
- Bogdanov M, Dowhan W, Vitrac H (2014) Lipids and topological rules governing membrane protein assembly. Biochim Biophys Acta 1843:1475–1488PubMedCrossRefGoogle Scholar
- Caforio A, Driessen AJ (2016) Archaeal phospholipids: Structural properties and biosynthesis. Biochim Biophys Acta. https://doi.org/10.1016/j.bbalip.2016.1012.1006CrossRefGoogle Scholar
- Chance B, Williams GR (1955) A method for the localization of sites for oxidative phosphorylation. Nature 176:250–254PubMedCrossRefPubMedCentralGoogle Scholar
- Chang SC, Heacock PN, Clancey CJ, Dowhan W (1998a) The PEL1 gene (renamed PGS1) encodes the phosphatidylglycerophosphate synthase of Saccharomyces cerevisiae. J Biol Chem 273:9829–9836PubMedCrossRefPubMedCentralGoogle Scholar
- Chang SC, Heacock PN, Mileykovskaya E, Voelker DR, Dowhan W (1998b) Isolation and characterization of the gene (CLS1) encoding cardiolipin synthase in Saccharomyces cerevisiae. J Biol Chem 273:14933–14941PubMedCrossRefPubMedCentralGoogle Scholar
- Chen CC, Wilson TH (1984) The phospholipid requirement for activity of the lactose carrier of Escherichia coli. J Biol Chem 259:10150–10158PubMedPubMedCentralGoogle Scholar
- Choi JY, Martin WE, Murphy RC, Voelker DR (2004) Phosphatidylcholine and N-methylated phospholipids are nonessential in Saccharomyces cerevisiae. J Biol Chem 279:42321–42330PubMedCrossRefPubMedCentralGoogle Scholar
- Christensen H, Garton NJ, Horobin RW, Minnikin DE, Barer MR (1999) Lipid domains of mycobacteria studied with fluorescent molecular probes. Mol Microbiol 31:1561–1572PubMedCrossRefPubMedCentralGoogle Scholar
- Clancey CJ, Chang SC, Dowhan W (1993) Cloning of a gene (PSD1) encoding phosphatidylserine decarboxylase from Saccharomyces cerevisiae by complementation of an Escherichia coli mutant. J Biol Chem 268:24580–24590PubMedPubMedCentralGoogle Scholar
- Claypool SM (2009) Cardiolipin, a critical determinant of mitochondrial carrier protein assembly and function. Biochim Biophys Acta 1788:2059–2068PubMedPubMedCentralCrossRefGoogle Scholar
- de Vrije T, de Swart RL, Dowhan W, Tommassen J, de Kruijff B (1988) Phosphatidylglycerol is involved in protein translocation across Escherichia coli inner membranes. Nature 334:173–175PubMedCrossRefPubMedCentralGoogle Scholar
- DeChavigny A, Heacock PN, Dowhan W (1991) Phosphatidylethanolamine may not be essential for the viability of Escherichia coli. J Biol Chem 266:5323–5332PubMedPubMedCentralGoogle Scholar
- Dowhan W (1997) Molecular basis for membrane phospholipid diversity: why are there so many lipids? Annu Rev Biochem 66:199–232PubMedCrossRefGoogle Scholar
- Dowhan W (2009) Molecular genetic approaches to defining lipid function. J Lipid Res 50(Suppl):S305–S310PubMedPubMedCentralCrossRefGoogle Scholar
- Dowhan W (2013) A retrospective: use of Escherichia coli as a vehicle to study phospholipid synthesis and function. Biochim Biophys Acta 1831:471–494PubMedCrossRefGoogle Scholar
- Dowhan W, Bogdanov M (2012) Molecular genetic and biochemical approaches for defining lipid-dependent membrane protein folding. Biochim Biophys Acta 1818:1097–1107PubMedCrossRefGoogle Scholar
- Dunlop J, Jones PC, Finbow ME (1995) Membrane insertion and assembly of ductin: a polytopic channel with dual orientations. EMBO J 14:3609–3616PubMedPubMedCentralCrossRefGoogle Scholar
- Emoto K, Kobayashi T, Yamaji A, Aizawa H, Yahara I, Inoue K, Umeda M (1996) Redistribution of phosphatidylethanolamine at the cleavage furrow of dividing cells during cytokinesis. Proc Natl Acad Sci U S A 93:12867–12872PubMedPubMedCentralCrossRefGoogle Scholar
- Gold VA, Robson A, Bao H, Romantsov T, Duong F, Collinson I (2010) The action of cardiolipin on the bacterial translocon. Proc Natl Acad Sci U S A 107:10044–10049PubMedPubMedCentralCrossRefGoogle Scholar
- von Heijne G (2006) Membrane-protein topology. Nat Rev Mol Cell Biol 7:909–918CrossRefGoogle Scholar
- Hendrick JP, Wickner W (1991) SecA protein needs both acidic phospholipids and SecY/E protein for functional high-affinity binding to the Escherichia coli plasma membrane. J Biol Chem 266:24596–24600PubMedGoogle Scholar
- Henry SA, Kohlwein SD, Carman GM (2012) Metabolism and regulation of glycerolipids in the yeast Saccharomyces cerevisiae. Genetics 190:317–349PubMedPubMedCentralCrossRefGoogle Scholar
- Herate C, Ramdani G, Grant NJ, Marion S, Gasman S, Niedergang F, Benichou S, Bouchet J (2016) Phospholipid Scramblase 1 Modulates FcR-Mediated Phagocytosis in Differentiated Macrophages. PLoS One 11:e0145617PubMedPubMedCentralCrossRefGoogle Scholar
- Horvath SE, Daum G (2013) Lipids of mitochondria. Prog Lipid Res 52:590–614PubMedCrossRefPubMedCentralGoogle Scholar
- Hunte C (2005) Specific protein-lipid interactions in membrane proteins. Biochem Soc Trans 33:938–942PubMedCrossRefGoogle Scholar
- Iwamoto K, Kobayashi S, Fukuda R, Umeda M, Kobayashi T, Ohta A (2004) Local exposure of phosphatidylethanolamine on the yeast plasma membrane is implicated in cell polarity. Genes Cells 9:891–903PubMedCrossRefPubMedCentralGoogle Scholar
- Jiang F, Rizavi HS, Greenberg ML (1997) Cardiolipin is not essential for the growth of Saccharomyces cerevisiae on fermentable or non-fermentable carbon sources. Mol Microbiol 26:481–491PubMedCrossRefPubMedCentralGoogle Scholar
- Jiang F, Ryan MT, Schlame M, Zhao M, Gu Z, Klingenberg M, Pfanner N, Greenberg ML (2000) Absence of cardiolipin in the crd1 null mutant results in decreased mitochondrial membrane potential and reduced mitochondrial function. J Biol Chem 275:22387–22394PubMedCrossRefPubMedCentralGoogle Scholar
- Kainulainen V, Korhonen TK (2014) Dancing to another tune-adhesive moonlighting proteins in bacteria. Biology (Basel) 3:178–204Google Scholar
- Kandasamy P, Numata M, Berry KZ, Fickes R, Leslie CC, Murphy RC, Voelker DR (2016) Structural analogs of pulmonary surfactant phosphatidylglycerol inhibit toll-like receptor 2 and 4 signaling. J Lipid Res 57:993–1005PubMedPubMedCentralCrossRefGoogle Scholar
- Kannan M, Riekhof WR, Voelker DR (2015) Transport of phosphatidylserine from the endoplasmic reticulum to the site of phosphatidylserine decarboxylase2 in yeast. Traffic 16:123–134PubMedCrossRefPubMedCentralGoogle Scholar
- Kawai F, Shoda M, Harashima R, Sadaie Y, Hara H, Matsumoto K (2004) Cardiolipin domains in Bacillus subtilis marburg membranes. J Bacteriol 186:1475–1483PubMedPubMedCentralCrossRefGoogle Scholar
- Killian JA, Fabrie CH, Baart W, Morein S, de Kruijff B (1992) Effects of temperature variation and phenethyl alcohol addition on acyl chain order and lipid organization in Escherichia coli derived membrane systems. A 2H- and 31P-NMR study. Biochim Biophys Acta 1105:253–262PubMedCrossRefPubMedCentralGoogle Scholar
- Killian JA, Koorengevel MC, Bouwstra JA, Gooris G, Dowhan W, de Kruijff B (1994) Effect of divalent cations on lipid organization of cardiolipin isolated from Escherichia coli strain AH930. Biochim Biophys Acta 1189:225–232PubMedCrossRefPubMedCentralGoogle Scholar
- Konovalova A, Mitchell AM, Silhavy TJ (2016) A lipoprotein/beta-barrel complex monitors lipopolysaccharide integrity transducing information across the outer membrane. Elife 5(e15276):1–17Google Scholar
- Koppelman CM, Den Blaauwen T, Duursma MC, Heeren RM, Nanninga N (2001) Escherichia coli minicell membranes are enriched in cardiolipin. J Bacteriol 183:6144–6147PubMedPubMedCentralCrossRefGoogle Scholar
- Levy D (1996) Membrane proteins which exhibit multiple topological orientations. Essays Biochem 31:49–60PubMedGoogle Scholar
- Li C, Tan BK, Zhao J, Guan Z (2016) In vivo and in vitro Synthesis of Phosphatidylglycerol by an Escherichia coli Cardiolipin Synthase. J Biol Chem 291:25144–25153PubMedPubMedCentralCrossRefGoogle Scholar
- Lill R, Dowhan W, Wickner W (1990) The ATPase activity of SecA is regulated by acidic phospholipids, SecY, and the leader and mature domains of precursor proteins. Cell 60:271–280PubMedCrossRefGoogle Scholar
- Matsumoto K, Hara H, Fishov I, Mileykovskaya E, Norris V (2015) The membrane: transertion as an organizing principle in membrane heterogeneity. Front Microbiol 6:572PubMedPubMedCentralCrossRefGoogle Scholar
- Megyeri M, Riezman H, Schuldiner M, Futerman AH (2016) Making Sense of the Yeast Sphingolipid Pathway. J Mol Biol 428:4765–4775PubMedCrossRefPubMedCentralGoogle Scholar
- Mileykovskaya E, Dowhan W (2009) Cardiolipin domains in prokaryotes and eukaryotes. Biochim Biophys Acta 1778:2084–2091CrossRefGoogle Scholar
- Mileykovskaya E, Dowhan W (2015) The role of cardiolipin in mitochondrial supercomplex assembly. In: Louro RO, Diaz-Moreno I (eds) Redox proteins in supercomplexes and signalosomes. Lumina Datamatics, Puducherry, pp 81–105CrossRefGoogle Scholar
- Mileykovskaya E, Sun Q, Margolin W, Dowhan W (1998) Localization and function of early cell division proteins in filamentous Escherichia coli cells lacking phosphatidylethanolamine. J Bacteriol 180:4252–4257PubMedPubMedCentralGoogle Scholar
- Mileykovskaya E, Fishov I, Fu X, Corbin BD, Margolin W, Dowhan W (2003) Effects of phospholipid composition on MinD-membrane interactions in vitro and in vivo. J Biol Chem 278:22193–22198PubMedCrossRefGoogle Scholar
- Mileykovskaya E, Ryan AC, Mo X, Lin CC, Khalaf KI, Dowhan W, Garrett TA (2009) Phosphatidic acid and N-acyl phosphatidylethanolamine form membrane domains in Escherichia coli mutant lacking cardiolipin and phosphatidylglycerol. J Biol Chem 284:2990–3000PubMedPubMedCentralCrossRefGoogle Scholar
- Mileykovskaya E, Penczek PA, Fang J, Mallampalli VK, Sparagna GC, Dowhan W (2012) Arrangement of the respiratory chain complexes in Saccharomyces cerevisiae supercomplex III2IV2 revealed by single particle cryo-electron microscopy. J Biol Chem 287:23095–23103PubMedPubMedCentralCrossRefGoogle Scholar
- Miller KJ, Kennedy EP (1987) Transfer of phosphoethanolamine residues from phosphatidylethanolamine to the membrane-derived oligosaccharides of Escherichia coli. J Bacteriol 169:682–686PubMedPubMedCentralCrossRefGoogle Scholar
- Moise AR, Grant JR, Lippe R, Gabathuler R, Jefferies WA (2004) The adenovirus E3-6.7K protein adopts diverse membrane topologies following posttranslational translocation. J Virol 78:454–463PubMedPubMedCentralCrossRefGoogle Scholar
- Moser M, Nagamori S, Huber M, Tokuda H, Nishiyama K (2013) Glycolipozyme MPIase is essential for topology inversion of SecG during preprotein translocation. Proc Natl Acad Sci U S A 110:9734–9739PubMedPubMedCentralCrossRefGoogle Scholar
- Nagahama H, Sakamoto Y, Matsumoto K, Hara H (2006) RcsA-dependent and -independent growth defects caused by the activated Rcs phosphorelay system in the Escherichia coli pgsA null mutant. J Gen Appl Microbiol 52:91–98PubMedCrossRefPubMedCentralGoogle Scholar
- Nikawa J, Kodaki T, Yamashita S (1987) Primary structure and disruption of the phosphatidylinositol synthase gene of Saccharomyces cerevisiae. J Biol Chem 262:4876–4881PubMedPubMedCentralGoogle Scholar
- Nishibori A, Kusaka J, Hara H, Umeda M, Matsumoto K (2005) Phosphatidylethanolamine domains and localization of phospholipid synthases in Bacillus subtilis membranes. J Bacteriol 187:2163–2174PubMedPubMedCentralCrossRefGoogle Scholar
- Ostrander DB, Zhang M, Mileykovskaya E, Rho M, Dowhan W (2001) Lack of mitochondrial anionic phospholipids causes an inhibition of translation of protein components of the electron transport chain. A yeast genetic model system for the study of anionic phospholipid function in mitochondria. J Biol Chem 276:25262–25272PubMedCrossRefGoogle Scholar
- Raetz CR, Carman GM, Dowhan W, Jiang RT, Waszkuc W, Loffredo W, Tsai MD (1987) Phospholipids chiral at phosphorus. Steric course of the reactions catalyzed by phosphatidylserine synthase from Escherichia coli and yeast. Biochemistry 26:4022–4027PubMedCrossRefGoogle Scholar
- Raja V, Joshi AS, Li G, Maddipati KR, Greenberg ML (2017) Loss of cardiolipin leads to perturbation of Acetyl-CoA synthesis. J Biol Chem 292:1092–1102PubMedCrossRefGoogle Scholar
- Reynolds CM, Kalb SR, Cotter RJ, Raetz CR (2005) A phosphoethanolamine transferase specific for the outer 3-deoxy-d-manno-octulosonic acid residue of Escherichia coli lipopolysaccharide. Identification of the eptB gene and Ca2+ hypersensitivity of an eptB deletion mutant. J Biol Chem 280:21202–21211PubMedCrossRefGoogle Scholar
- Rietveld AG, Killian JA, Dowhan W, de Kruijff B (1993) Polymorphic regulation of membrane phospholipid composition in Escherichia coli. J Biol Chem 268:12427–12433PubMedGoogle Scholar
- Rietveld AG, Chupin VV, Koorengevel MC, Wienk HL, Dowhan W, de Kruijff B (1994) Regulation of lipid polymorphism is essential for the viability of phosphatidylethanolamine-deficient Escherichia coli cells. J Biol Chem 269:28670–28675PubMedGoogle Scholar
- Rietveld AG, Koorengevel MC, de Kruijff B (1995) Non-bilayer lipids are required for efficient protein transport across the plasma membrane of Escherichia coli. EMBO J 14:5506–5513PubMedPubMedCentralCrossRefGoogle Scholar
- Romantsov T, Battle AR, Hendel JL, Martinac B, Wood JM (2010) Protein localization in Escherichia coli cells: comparison of the cytoplasmic membrane proteins ProP, LacY, ProW, AqpZ, MscS, and MscL. J Bacteriol 192:912–924PubMedCrossRefGoogle Scholar
- Schagger H, Pfeiffer K (2000) Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J 19:1777–1783PubMedPubMedCentralCrossRefGoogle Scholar
- Schlame M, Greenberg ML (2017) Biosynthesis, remodeling and turnover of mitochondrial cardiolipin. Biochim Biophys Acta 1862:3–7CrossRefGoogle Scholar
- Shen H, Dowhan W (1996) Reduction of CDP-diacylglycerol synthase activity results in the excretion of inositol by Saccharomyces cerevisiae. J Biol Chem 271:29043–29048PubMedCrossRefPubMedCentralGoogle Scholar
- Shen H, Heacock PN, Clancey CJ, Dowhan W (1996) The CDS1 gene encoding CDP-diacylglycerol synthase in Saccharomyces cerevisiae is essential for cell growth. J Biol Chem 271:789–795PubMedCrossRefGoogle Scholar
- Shiba Y, Yokoyama Y, Aono Y, Kiuchi T, Kusaka J, Matsumoto K, Hara H (2004) Activation of the Rcs signal transduction system is responsible for the thermosensitive growth defect of an Escherichia coli mutant lacking phosphatidylglycerol and cardiolipin. J Bacteriol 186:6526–6535PubMedPubMedCentralCrossRefGoogle Scholar
- 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, Yoshikawa S (2007) Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase. EMBO J 26:1713–1725PubMedPubMedCentralCrossRefGoogle Scholar
- 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 276:48539–48548PubMedCrossRefPubMedCentralGoogle Scholar
- Swameye I, Schaller H (1997) Dual topology of the large envelope protein of duck hepatitis B virus: determinants preventing pre-S translocation and glycosylation. J Virol 71:9434–9441PubMedPubMedCentralGoogle Scholar
- Tamura Y, Harada Y, Nishikawa S, Yamano K, Kamiya M, Shiota T, Kuroda T, Kuge O, Sesaki H, Imai K, Tomii K, Endo T (2013) Tam41 is a CDP-diacylglycerol synthase required for cardiolipin biosynthesis in mitochondria. Cell Metab 17:709–718PubMedPubMedCentralCrossRefGoogle Scholar
- Tan BK, Bogdanov M, Zhao J, Dowhan W, Raetz CR, Guan Z (2012) Discovery of a cardiolipin synthase utilizing phosphatidylethanolamine and phosphatidylglycerol as substrates. Proc Natl Acad Sci U S A 109:16504–16509PubMedPubMedCentralCrossRefGoogle Scholar
- Trotter PJ, Pedretti J, Voelker DR (1993) Phosphatidylserine decarboxylase from Saccharomyces cerevisiae. Isolation of mutants, cloning of the gene, and creation of a null allele. J Biol Chem 268:21416–21424PubMedGoogle Scholar
- Tsai M, Ohniwa RL, Kato Y, Takeshita SL, Ohta T, Saito S, Hayashi H, Morikawa K (2011) Staphylococcus aureus requires cardiolipin for survival under conditions of high salinity. BMC Microbiol 11:13PubMedPubMedCentralCrossRefGoogle Scholar
- Vanounou S, Parola AH, Fishov I (2003) Phosphatidylethanolamine and phosphatidylglycerol are segregated into different domains in bacterial membrane. A study with pyrene-labelled phospholipids. Mol Microbiol 49:1067–1079PubMedCrossRefGoogle Scholar
- Vitrac H, Bogdanov M, Heacock P, Dowhan W (2011) Lipids and topological rules of membrane protein assembly: balance between long- and short-range lipid-protein interactions. J Biol Chem 286:15182–15194PubMedPubMedCentralCrossRefGoogle Scholar
- Vitrac H, Bogdanov M, Dowhan W (2013a) In vitro reconstitution of lipid-dependent dual topology and postassembly topological switching of a membrane protein. Proc Natl Acad Sci U S A 110:9338–9343PubMedPubMedCentralCrossRefGoogle Scholar
- Vitrac H, Bogdanov M, Dowhan W (2013b) Proper fatty acid composition rather than an ionizable lipid amine is required for full transport function of lactose permease from Escherichia coli. J Biol Chem 288:5873–5885PubMedPubMedCentralCrossRefGoogle Scholar
- Vitrac H, MacLean DM, Jayaraman V, Bogdanov M, Dowhan W (2015) Dynamic membrane protein topological switching upon changes in phospholipid environment. Proc Natl Acad Sci U S A 112:13874–13879PubMedPubMedCentralCrossRefGoogle Scholar
- Vitrac H, MacLean DM, Karlstaedt A, Taegtmeyer H, Jayaraman V, Bogdanov M, Dowhan W (2017) Dynamic lipid-dependent modulation of protein topology by post-translational phosphorylation. J Biol Chem 292:1613–1624PubMedCrossRefGoogle Scholar
- Whitfield C, Trent MS (2014) Biosynthesis and export of bacterial lipopolysaccharides. Annu Rev Biochem 83:99–128PubMedCrossRefPubMedCentralGoogle Scholar
- Wikstrom M, Kelly AA, Georgiev A, Eriksson HM, Klement MR, Bogdanov M, Dowhan W, Wieslander A (2009) Lipid-engineered Escherichia coli membranes reveal critical lipid headgroup size for protein function. J Biol Chem 284:954–965PubMedPubMedCentralCrossRefGoogle Scholar
- Xia W, Dowhan W (1995a) In vivo evidence for the involvement of anionic phospholipids in initiation of DNA replication in Escherichia coli. Proc Natl Acad Sci U S A 92:783–787PubMedPubMedCentralCrossRefGoogle Scholar
- Xia W, Dowhan W (1995b) Phosphatidylinositol cannot substitute for phosphatidylglycerol in supporting cell growth of Escherichia coli. J Bacteriol 177:2926–2928PubMedPubMedCentralCrossRefGoogle Scholar
- Xie J, Bogdanov M, Heacock P, Dowhan W (2006) Phosphatidylethanolamine and monoglucosyldiacylglycerol are interchangeable in supporting topogenesis and function of the polytopic membrane protein lactose permease. J Biol Chem 281:19172–19178PubMedPubMedCentralCrossRefGoogle Scholar
- Ye C, Lou W, Li Y, Chatzispyrou IA, Huttemann M, Lee I, Houtkooper RH, Vaz FM, Chen S, Greenberg ML (2014) Deletion of the cardiolipin-specific phospholipase Cld1 rescues growth and life span defects in the tafazzin mutant: implications for Barth syndrome. J Biol Chem 289:3114–3125PubMedCrossRefGoogle Scholar
- Ye C, Shen Z, Greenberg ML (2016) Cardiolipin remodeling: a regulatory hub for modulating cardiolipin metabolism and function. J Bioenerg Biomembr 48:113–123PubMedCrossRefGoogle Scholar
- 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 277:43553–43556PubMedCrossRefGoogle Scholar
- Zhang M, Mileykovskaya E, Dowhan W (2005) Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria. J Biol Chem 280:29403–29408PubMedPubMedCentralCrossRefGoogle Scholar
- Zhao YJ, Zhu WJ, Wang XW, Zhang LH, Lee HC (2014) Determinants of the membrane orientation of a calcium signaling enzyme CD38. Biochim Biophys Acta 1853:2095–2103PubMedCrossRefGoogle Scholar
- Zhong Q, Gvozdenovic-Jeremic J, Webster P, Zhou J, Greenberg ML (2005) Loss of function of KRE5 suppresses temperature sensitivity of mutants lacking mitochondrial anionic lipids. Mol Biol Cell 16:665–675PubMedPubMedCentralCrossRefGoogle Scholar