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Lipid-Assisted Membrane Protein Folding and Topogenesis

  • William DowhanEmail author
  • Heidi Vitrac
  • Mikhail BogdanovEmail author
Article
  • 77 Downloads

Abstract

Due to the heterogenous lipid environment in which integral membrane proteins are embedded, they should follow a set of assembly rules, which govern transmembrane protein folding and topogenesis accordingly to a given lipid profile. Recombinant strains of bacteria have been engineered to have different membrane phospholipid compositions by molecular genetic manipulation of endogenous and foreign genes encoding lipid biosynthetic enzymes. Such strains provide a means to investigate the in vivo role of lipids in many different aspects of membrane function, folding and biogenesis. In vitro and in vivo studies established a function of lipids as molecular chaperones and topological determinants specifically assisting folding and topogenesis of membrane proteins. These results led to the extension of the Positive Inside Rule to Charge Balance Rule, which incorporates a role for lipid-protein interactions in determining membrane protein topological organization at the time of initial membrane insertion and dynamically after initial assembly. Membrane protein topogenesis appears to be a thermodynamically driven process in which lipid-protein interactions affect the potency of charged amino acid residues as topological signals. Dual topology for a membrane protein can be established during initial assembly where folding intermediates in multiple topological conformations are in rapid equilibrium (thus separated by a low activation energy), which is determined by the lipid environment. Post-assembly changes in lipid composition or post-translational modifications can trigger a reorganization of protein topology by inducing destabilization and refolding of a membrane protein. The lipid-dependent dynamic nature of membrane protein organization provides a novel means of regulating protein function.

Keywords

Membrane protein Phospholipid Topogenesis Charge Balance Rule Protein folding 

Abbreviations

TMD

Transmembrane domain

EMD

Extramembrane domain

PE

Phosphatidylethanolamine

PG

Phosphatidylglycerol

CL

Cardiolipin

PS

Phosphatidylserine

PC

Phosphatidylcholine

LacY

Lactose permease

PheP

Phenylalanine permease

GabP

γ-Aminobutyric acid permease

MelB

Melibiose permease

CscB

Sucrose permease

mAb4B1

Monoclonal antibody 4B1

SCAMTM

Substituted cysteine accessibility method applied to TMD orientation

ßMCD

ß-Methyl cyclodextrin

MLV

Multilamellar vesicle

FRET

Förster resonance energy transfer

Notes

Acknowledgements

This work was supported in whole or in part by National Institutes of Health Grant GM R01 121493 and the John Dunn Research Foundation both to W. D. and the European Union Marie Skłodowska-Curie Grant H2020-MSCA-RISE-2015-690853, NATO Science for Peace and Security Programme-SPS 985291 and Program of Competitive Growth of Kazan Federal University to M. B.

Compliance with Ethical Standards

Conflict of interest

Authors declare no conflicts of interest.

Human and Animal Rights

No human subjects or animals were used by the authors.

References

  1. 1.
    Blobel G (1980) Intracellular protein topogenesis. Proc Natl Acad Sci USA 77:1496–1500CrossRefPubMedGoogle Scholar
  2. 2.
    Kuhn A, Koch HG, Dalbey RE (2017) Targeting and insertion of membrane proteins. EcoSal Plus.  https://doi.org/10.1128/ecosalplus.esp-0012-2016 CrossRefPubMedGoogle Scholar
  3. 3.
    Rapoport TA (2007) Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450:663–669CrossRefPubMedGoogle Scholar
  4. 4.
    Cymer F, von Heijne G, White SH (2015) Mechanisms of integral membrane protein insertion and folding. J Mol Biol 427:999–1022CrossRefPubMedGoogle Scholar
  5. 5.
    Dowhan W (1997) Molecular basis for membrane phospholipid diversity: why are there so many lipids? Annu Rev Biochem 66:199–232CrossRefPubMedGoogle Scholar
  6. 6.
    Ulmschneider MB, Ulmschneider JP, Schiller N, Wallace BA, von Heijne G, White SH (2014) Spontaneous transmembrane helix insertion thermodynamically mimics translocon-guided insertion. Nat Commun 5:4863CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    von Heijne G (2006) Membrane-protein topology. Nat Rev Mol Cell Biol 7:909–918CrossRefGoogle Scholar
  8. 8.
    Andersson H, von Heijne G (1993) Position-specific Asp-Lys pairing can affect signal sequence function and membrane protein topology. J Biol Chem 268:21389–21393PubMedGoogle Scholar
  9. 9.
    Andersson H, von Heijne G (1994) Membrane protein topology: effects of ∆µ H+ on the translocation of charged residues explain the ‘positive inside’ rule. EMBO J 13:2267–2272CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Delgado-Partin VM, Dalbey RE (1998) The proton motive force, acting on acidic residues, promotes translocation of amino-terminal domains of membrane proteins when the hydrophobicity of the translocation signal is low. J Biol Chem 273:9927–9934CrossRefPubMedGoogle Scholar
  11. 11.
    van de Vossenberg JL, Albers SV, van der Does C, Driessen AJ, van Klompenburg W (1998) The positive inside rule is not determined by the polarity of the delta psi (transmembrane electrical potential). Mol Microbiol 29:1125–1127CrossRefPubMedGoogle Scholar
  12. 12.
    van Klompenburg W, Nilsson I, von Heijne G, de Kruijff B (1997) Anionic phospholipids are determinants of membrane protein topology. EMBO J 16:4261–4266CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Dowhan W (2013) A retrospective: use of Escherichia coli as a vehicle to study phospholipid synthesis and function. Biochim Biophys Acta 1831:471–494CrossRefPubMedGoogle Scholar
  14. 14.
    Bogdanov M, Dowhan W, Vitrac H (2014) Lipids and topological rules governing membrane protein assembly. Biochim Biophys Acta 1843:1475–1488CrossRefPubMedGoogle Scholar
  15. 15.
    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 182:925–935CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Manni MM, Tiberti ML, Pagnotta S, Barelli H, Gautier R, Antonny B (2018) Acyl chain asymmetry and polyunsaturation of brain phospholipids facilitate membrane vesiculation without leakage. Elife 7:e34394CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Dowhan W (2009) Molecular genetic approaches to defining lipid function. J Lipid Res 50:S305–S310CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Bogdanov M, Heacock PN, Dowhan W (2002) A polytopic membrane protein displays a reversible topology dependent on membrane lipid composition. EMBO J 21:2107–2116CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Bogdanov M, Dowhan W (1998) Phospholipid-assisted protein folding: phosphatidylethanolamine is required at a late step of the conformational maturation of the polytopic membrane protein lactose permease. EMBO J 17:5255–5264CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Wang X, Bogdanov M, Dowhan W (2002) Topology of polytopic membrane protein subdomains is dictated by membrane phospholipid composition. EMBO J 21:5673–5681CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    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 USA 107:15057–15062CrossRefPubMedGoogle Scholar
  22. 22.
    Conover GM, Martinez-Morales F, Heidtman MI, Luo ZQ, Tang M, Chen C, Geiger O, Isberg RR (2008) Phosphatidylcholine synthesis is required for optimal function of Legionella pneumophila virulence determinants. Cell Microbiol 10:514–528PubMedGoogle Scholar
  23. 23.
    Xia W, Dowhan W (1995) Phosphatidylinositol cannot substitute for phosphatidylglycerol in supporting cell growth of Escherichia coli. J Bacteriol 177:2926–2928CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    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 281:19172–19178CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Wikström M, Kelly AA, Georgiev A, Eriksson HM, Klement MR, Bogdanov M, Dowhan W, Wieslander Ä (2009) Lipid-engineered Escherichia coli membranes reveal critical lipid headgroup size for protein function. J Biol Chem 284:954–965CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Oku Y, Kurokawa K, Ichihashi N, Sekimizu K (2004) Characterization of the Staphylococcus aureus mprF gene, involved in lysinylation of phosphatidylglycerol. Microbiology 150:45–51CrossRefPubMedGoogle Scholar
  27. 27.
    Dowhan W, Bogdanov M, Mileykovskaya E, Vitrac H (2017) Functional roles of individual membrane phospholipids in Escherichia coli and Saccharomyces cerevisiae. In: Geiger O (ed) Biogenesis of Fatty acids, lipids and membranes handbook of hydrocarbon and lipid microbiology. Springer, ChamGoogle Scholar
  28. 28.
    DeChavigny A, Heacock PN, Dowhan W (1991) Phosphatidylethanolamine may not be essential for the viability of Escherichia coli. J Biol Chem 266:5323–5332PubMedGoogle Scholar
  29. 29.
    Wikstrom M, Xie J, Bogdanov M, Mileykovskaya E, Heacock P, Wieslander A, Dowhan W (2004) Monoglucosyldiacylglycerol, a foreign lipid, can substitute for phosphatidylethanolamine in essential membrane-associated functions in Escherichia coli. J Biol Chem 279:10484–10493CrossRefPubMedGoogle Scholar
  30. 30.
    Chen CC, Wilson TH (1984) The phospholipid requirement for activity of the lactose carrier of Escherichia coli. J Biol Chem 259:10150–10158PubMedGoogle Scholar
  31. 31.
    Seto-Young D, Chen CC, Wilson TH (1985) Effect of different phospholipids on the reconstitution of two functions of the lactose carrier of Escherichia coli. J Membr Biol 84:259–267CrossRefPubMedGoogle Scholar
  32. 32.
    Zhang W, Bogdanov M, Pi J, Pittard AJ, Dowhan W (2003) Reversible topological organization within a polytopic membrane protein is governed by a change in membrane phospholipid composition. J Biol Chem 278:50128–50135CrossRefPubMedGoogle Scholar
  33. 33.
    Zhang W, Campbell HA, King SC, Dowhan W (2005) Phospholipids as determinants of membrane protein topology. Phosphatidylethanolamine is required for the proper topological organization of the gamma-aminobutyric acid permease (GabP) of Escherichia coli. J Biol Chem 280:26032–26038CrossRefPubMedGoogle Scholar
  34. 34.
    Hariharan P, Tikhonova E, Medeiros-Silva J, Jeucken A, Bogdanov MV, Dowhan W, Brouwers JF, Weingarth M, Guan L (2018) Structural and functional characterization of protein-lipid interactions of the Salmonella typhimurium melibiose transporter MelB. BMC Biol 16:85CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    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 286:15182–15194CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Vitrac H, Dowhan W, Bogdanov M (2017) Effects of mixed proximal and distal topogenic signals on the topological sensitivity of a membrane protein to the lipid environment. Biochim Biophys Acta Biomembr 1859:1291–1300CrossRefPubMedGoogle Scholar
  37. 37.
    Bogdanov M, Dowhan W (1995) Phosphatidylethanolamine is required for in vivo function of the membrane-associated lactose permease of Escherichia coli. J Biol Chem 270:732–739CrossRefPubMedGoogle Scholar
  38. 38.
    Mileykovskaya EI, Dowhan W (1993) Alterations in the electron transfer chain in mutant strains of Escherichia coli lacking phosphatidylethanolamine. J Biol Chem 268:24824–24831PubMedGoogle Scholar
  39. 39.
    Rowlett VW, Mallampalli V, Karlstaedt A, Dowhan W, Taegtmeyer H, Margolin W, Vitrac H (2017) Impact of membrane phospholipid alterations in Escherichia coli on cellular function and bacterial stress adaptation. J Bacteriol 199:e00849CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Vitrac H, Bogdanov M, Dowhan W (2013) 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 288:5873–5885CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Bogdanov M, Sun J, Kaback HR, Dowhan W (1996) A phospholipid acts as a chaperone in assembly of a membrane transport protein. J Biol Chem 271:11615–11618CrossRefPubMedGoogle Scholar
  42. 42.
    Bogdanov M, Umeda M, Dowhan W (1999) Phospholipid-assisted refolding of an integral membrane protein. Minimum structural features for phosphatidylethanolamine to act as a molecular chaperone. J Biol Chem 274:12339–12345CrossRefPubMedGoogle Scholar
  43. 43.
    Frillingos S, Kaback HR (1996) Monoclonal antibody 4B1 alters the pKa of a carboxylic acid at position 325 (helix X) of the lactose permease of Escherichia coli. Biochemistry 35:10166–10171CrossRefPubMedGoogle Scholar
  44. 44.
    Frillingos S, Wu J, Venkatesan P, Kaback HR (1997) Binding of ligand or monoclonal antibody 4B1 induces discrete structural changes in the lactose permease of Escherichia coli. Biochemistry 36:6408–6414CrossRefPubMedGoogle Scholar
  45. 45.
    Dowhan W, Bogdanov M (2012) Molecular genetic and biochemical approaches for defining lipid-dependent membrane protein folding. Biochim Biophys Acta 1818:1097–1107CrossRefPubMedGoogle Scholar
  46. 46.
    Kaback HR, Sahin-Toth M, Weinglass AB (2001) The kamikaze approach to membrane transport. Nat Rev Mol Cell Biol 2:610–620CrossRefPubMedGoogle Scholar
  47. 47.
    Abramson J, Smirnova I, Kasho V, Verner G, Kaback HR, Iwata S (2003) Structure and mechanism of the lactose permease of Escherichia coli. Science 301:610–615CrossRefPubMedGoogle Scholar
  48. 48.
    Guan L, Mirza O, Verner G, Iwata S, Kaback HR (2007) Structural determination of wild-type lactose permease. Proc Natl Acad Sci USA 104:15294–15298CrossRefPubMedGoogle Scholar
  49. 49.
    Bogdanov M (2017) Mapping of membrane protein topology by substituted cysteine accessibility method (SCAM). Methods Mol Biol 1615:105–128CrossRefPubMedGoogle Scholar
  50. 50.
    Bogdanov M, Dowhan W (2012) Lipid-dependent generation of dual topology for a membrane protein. J Biol Chem 287:37939–37948CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Bogdanov M, Heacock PN, Dowhan W (2010) Study of polytopic membrane protein topological organization as a function of membrane lipid composition. Methods Mol Biol 619:79–101CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Bogdanov M, Xie J, Dowhan W (2009) Lipid-protein interactions drive membrane protein topogenesis in accordance with the positive inside rule. J Biol Chem 284:9637–9641CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Dowhan W, Bogdanov M (2009) Lipid-dependent membrane protein topogenesis. Annu Rev Biochem 78:515–540CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Bogdanov M, Vitrac H, Dowhan W (2018) Flip-flopping membrane proteins: how the charge balance rule governs dynamic membrane protein topology. Biogenesis of Fatty acids, lipids and membranes handbook of hydrocarbon and lipid microbiology. Springer, ChamGoogle Scholar
  55. 55.
    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 USA 110:9734–9739CrossRefPubMedGoogle Scholar
  56. 56.
    Nishiyama K, Suzuki T, Tokuda H (1996) Inversion of the membrane topology of SecG coupled with SecA-dependent preprotein translocation. Cell 85:71–81CrossRefPubMedGoogle Scholar
  57. 57.
    Yao XL, Hong M (2006) Effects of anionic lipid and ion concentrations on the topology and segmental mobility of colicin Ia channel domain from solid-state NMR. Biochemistry 45:289–295CrossRefPubMedGoogle Scholar
  58. 58.
    Tunuguntla R, Bangar M, Kim K, Stroeve P, Ajo-Franklin CM, Noy A (2013) Lipid bilayer composition can influence the orientation of proteorhodopsin in artificial membranes. Biophys J 105:1388–1396CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Zhang Y, Ren Y, Li S, Hayes JD (2014) Transcription factor Nrf1 is topologically repartitioned across membranes to enable target gene transactivation through its acidic glucose-responsive domains. PLoS ONE 9:e93458CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    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:e0145617CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Baker JA, Wong WC, Eisenhaber B, Warwicker J, Eisenhaber F (2017) Charged residues next to transmembrane regions revisited: “positive-inside rule” is complemented by the “negative inside depletion/outside enrichment rule”. BMC Biol 15:66CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Nilsson J, Persson B, von Heijne G (2005) Comparative analysis of amino acid distributions in integral membrane proteins from 107 genomes. Proteins 60:606–616CrossRefPubMedGoogle Scholar
  63. 63.
    Wallin E, von Heijne G (1998) Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci 7:1029–1038CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Bay DC, Turner RJ (2013) Membrane composition influences the topology bias of bacterial integral membrane proteins. Biochim Biophys Acta 1828:260–270CrossRefPubMedGoogle Scholar
  65. 65.
    Newport TD, Sansom MSP, Stansfeld PJ (2018) The MemProtMD database: a resource for membrane-embedded protein structures and their lipid interactions. Nucleic Acids Res 47:D390–D397CrossRefPubMedCentralGoogle Scholar
  66. 66.
    von Heijne G (1989) Control of topology and mode of assembly of a polytopic membrane protein by positively charged residues. Nature 341:456–458CrossRefGoogle Scholar
  67. 67.
    Kolbusz MA, ter Horst R, Slotboom DJ, Lolkema JS (2010) Orientation of small multidrug resistance transporter subunits in the membrane: correlation with the positive-inside rule. J Mol Biol 402:127–138CrossRefPubMedGoogle Scholar
  68. 68.
    Rapp M, Granseth E, Seppälä S, von Heijne G (2006) Identification and evolution of dual-topology membrane proteins. Nat Struct Mol Biol 13:112–116CrossRefPubMedGoogle Scholar
  69. 69.
    Seppälä S, Slusky JS, Lloris-Garcera P, Rapp M, von Heijne G (2010) Control of membrane protein topology by a single C-terminal residue. Science 328:1698–1700CrossRefPubMedGoogle Scholar
  70. 70.
    Woodall NB, Hadley S, Yin Y, Bowie JU (2017) Complete topology inversion can be part of normal membrane protein biogenesis. Protein Sci 26:824–833CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Fujita H, Yamagishi M, Kida Y, Sakaguchi M (2011) Positive charges on the translocating polypeptide chain arrest movement through the translocon. J Cell Sci 124:4184–4193CrossRefPubMedGoogle Scholar
  72. 72.
    Harley CA, Holt JA, Turner R, Tipper DJ (1998) Transmembrane protein insertion orientation in yeast depends on the charge difference across transmembrane segments, their total hydrophobicity, and its distribution. J Biol Chem 273:24963–24971CrossRefPubMedGoogle Scholar
  73. 73.
    Kim H, Paul S, Gennity J, Jennity J, Inouye M (1994) Reversible topology of a bifunctional transmembrane protein depends upon the charge balance around its transmembrane domain. Mol Microbiol 11:819–831CrossRefPubMedGoogle Scholar
  74. 74.
    Sato M, Hresko R, Mueckler M (1998) Testing the charge difference hypothesis for the assembly of a eucaryotic multispanning membrane protein. J Biol Chem 273:25203–25208CrossRefPubMedGoogle Scholar
  75. 75.
    Yamagishi M, Onishi Y, Yoshimura S, Fujita H, Imai K, Kida Y, Sakaguchi M (2014) A few positively charged residues slow movement of a polypeptide chain across the endoplasmic reticulum membrane. Biochemistry 53:5375–5383CrossRefPubMedGoogle Scholar
  76. 76.
    Andrews DW, Young JC, Mirels LF, Czarnota GJ (1992) The role of the N region in signal sequence and signal-anchor function. J Biol Chem 267:7761–7769PubMedGoogle Scholar
  77. 77.
    Beltzer JP, Fiedler K, Fuhrer C, Geffen I, Handschin C, Wessels HP, Spiess M (1991) Charged residues are major determinants of the transmembrane orientation of a signal-anchor sequence. J Biol Chem 266:973–978PubMedGoogle Scholar
  78. 78.
    Goder V, Bieri C, Spiess M (1999) Glycosylation can influence topogenesis of membrane proteins and reveals dynamic reorientation of nascent polypeptides within the translocon. J Cell Biol 147:257–266CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Goder V, Junne T, Spiess M (2004) Sec61p contributes to signal sequence orientation according to the positive-inside rule. Mol Biol Cell 15:1470–1478CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Sommer N, Junne T, Kalies KU, Spiess M, Hartmann E (2013) TRAP assists membrane protein topogenesis at the mammalian ER membrane. Biochim Biophys Acta 1833:3104–3111CrossRefPubMedGoogle Scholar
  81. 81.
    Enquist K, Fransson M, Boekel C, Bengtsson I, Geiger K, Lang L, Pettersson A, Johansson S, von Heijne G, Nilsson I (2009) Membrane-integration characteristics of two ABC transporters, CFTR and P-glycoprotein. J Mol Biol 387:1153–1164CrossRefPubMedGoogle Scholar
  82. 82.
    Zhang JT, Lee CH, Duthie M, Ling V (1995) Topological determinants of internal transmembrane segments in P-glycoprotein sequences. J Biol Chem 270:1742–1746CrossRefPubMedGoogle Scholar
  83. 83.
    Zhang JT, Ling V (1993) Membrane orientation of transmembrane segments 11 and 12 of MDR- and non-MDR-associated P-glycoproteins. Biochim Biophys Acta 1153:191–202CrossRefPubMedGoogle Scholar
  84. 84.
    May T, Soll J (1998) Positive charges determine the topology and functionality of the transmembrane domain in the chloroplastic outer envelope protein Toc34. J Cell Biol 141:895–904CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Andersson H, Bakker E, von Heijne G (1992) Different positively charged amino acids have similar effects on the topology of a polytopic transmembrane protein in Escherichia coli. J Biol Chem 267:1491–1495PubMedGoogle Scholar
  86. 86.
    Vitrac H, Bogdanov M, Dowhan W (2013) In vitro reconstitution of lipid-dependent dual topology and postassembly topological switching of a membrane protein. Proc Natl Acad Sci USA 110:9338–9343CrossRefPubMedGoogle Scholar
  87. 87.
    Schleiff E, Tien R, Salomon M, Soll J (2001) Lipid composition of outer leaflet of chloroplast outer envelope determines topology of OEP7. Mol Biol Cell 12:4090–4102CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Qbadou S, Tien R, Soll J, Schleiff E (2003) Membrane insertion of the chloroplast outer envelope protein, Toc34: constrains for insertion and topology. J Cell Sci 116:837–846CrossRefPubMedGoogle Scholar
  89. 89.
    McIlwain BC, Vandenberg RJ, Ryan RM (2015) Transport rates of a glutamate transporter homologue are influenced by the lipid bilayer. J Biol Chem 290:9780–9788CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Hickey KD, Buhr MM (2011) Lipid bilayer composition affects transmembrane protein orientation and function. J Lipids 2011:208457–208466CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Dowhan W, Vitrac H, Bogdanov M (2015) May the force be with you: unfolding lipid-protein interactions by single-molecule force spectroscopy. Structure 23:612–614CrossRefPubMedGoogle Scholar
  92. 92.
    Serdiuk T, Sugihara J, Mari SA, Kaback HR, Müller DJ (2015) Observing a lipid-dependent alteration in single lactose permeases. Structure 23:754–761CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    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 292:1613–1624CrossRefPubMedGoogle Scholar
  94. 94.
    Ikeda M, Arai M, Okuno T, Shimizu T (2003) TMPDB: a database of experimentally-characterized transmembrane topologies. Nucleic Acids Res 31:406–409CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Patel SJ, Van Lehn RC (2018) Characterizing the molecular mechanisms for flipping charged peptide flanking loops across a lipid bilayer. J Phys Chem B 122:10337–10348CrossRefPubMedGoogle Scholar
  96. 96.
    Van Lehn RC, Alexander-Katz A (2017) Grafting charged species to membrane-embedded scaffolds dramatically increases the rate of bilayer flipping. ACS Cent Sci 3:186–195CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Cheng HT, Megha London E (2009) Preparation and properties of asymmetric vesicles that mimic cell membranes: effect upon lipid raft formation and transmembrane helix orientation. J Biol Chem 284:6079–6092CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    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 USA 112:13874–13879CrossRefPubMedGoogle Scholar
  99. 99.
    Zhao YJ, Lam CM, Lee HC (2012) The membrane-bound enzyme CD38 exists in two opposing orientations. Sci Signal 5:67CrossRefGoogle Scholar
  100. 100.
    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 1853:2095–2103CrossRefPubMedGoogle Scholar
  101. 101.
    Dorobantu C, Macovei A, Lazar C, Dwek RA, Zitzmann N, Branza-Nichita N (2011) Cholesterol depletion of hepatoma cells impairs hepatitis B virus envelopment by altering the topology of the large envelope protein. J Virol 85:13373–13383CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Awe K, Lambert C, Prange R (2008) Mammalian BiP controls posttranslational ER translocation of the hepatitis B virus large envelope protein. FEBS Lett 582:3179–3184CrossRefPubMedGoogle Scholar
  103. 103.
    Lambert C, Prange R (2003) Chaperone action in the posttranslational topological reorientation of the hepatitis B virus large envelope protein: implications for translocational regulation. Proc Natl Acad Sci USA 100:5199–5204CrossRefPubMedGoogle Scholar
  104. 104.
    Lundin M, Monne M, Widell A, Von Heijne G, Persson MA (2003) Topology of the membrane-associated hepatitis C virus protein NS4B. J Virol 77:5428–5438CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Lu Y, Turnbull IR, Bragin A, Carveth K, Verkman AS, Skach WR (2000) Reorientation of aquaporin-1 topology during maturation in the endoplasmic reticulum. Mol Biol Cell 11:2973–2985CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Virkki MT, Agrawal N, Edsbacker E, Cristobal S, Elofsson A, Kauko A (2014) Folding of aquaporin 1: multiple evidence that helix 3 can shift out of the membrane core. Protein Sci 23:981–992CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Kanki T, Young MT, Sakaguchi M, Hamasaki N, Tanner MJ (2003) The N-terminal region of the transmembrane domain of human erythrocyte band 3. Residues critical for membrane insertion and transport activity. J Biol Chem 278:5564–5573CrossRefPubMedGoogle Scholar
  108. 108.
    Ota K, Sakaguchi M, Hamasaki N, Mihara K (1998) Assessment of topogenic functions of anticipated transmembrane segments of human band 3. J Biol Chem 273:28286–28291CrossRefPubMedGoogle Scholar
  109. 109.
    Jakes KS, Kienker PK, Slatin SL, Finkelstein A (1998) Translocation of inserted foreign epitopes by a channel-forming protein. Proc Natl Acad Sci USA 95:4321–4326CrossRefPubMedGoogle Scholar
  110. 110.
    Kienker PK, Qiu X, Slatin SL, Finkelstein A, Jakes KS (1997) Transmembrane insertion of the colicin Ia hydrophobic hairpin. J Membr Biol 157:27–37CrossRefPubMedGoogle Scholar
  111. 111.
    Slatin SL, Duche D, Kienker PK, Baty D (2004) Gating movements of colicin A and colicin Ia are different. J Membr Biol 202:73–83CrossRefPubMedGoogle Scholar
  112. 112.
    Nagamori S, Nishiyama K, Tokuda H (2002) Membrane topology inversion of SecG detected by labeling with a membrane-impermeable sulfhydryl reagent that causes a close association of SecG with SecA. J Biochem 132:629–634CrossRefPubMedGoogle Scholar
  113. 113.
    Fluman N, Tobiasson V, von Heijne G (2017) Stable membrane orientations of small dual-topology membrane proteins. Proc Natl Acad Sci USA 114:7987–7992CrossRefPubMedGoogle Scholar
  114. 114.
    Schlebach JP, Sanders CR (2015) Influence of Pathogenic mutations on the energetics of translocon-mediated bilayer integration of transmembrane helices. J Membr Biol 248:371–381CrossRefPubMedGoogle Scholar
  115. 115.
    Roushar FJ, Gruenhagen TC, Penn WD, Li B, Meiler J, Jastrzebska B, Schlebach JP (2018) Contribution of cotranslational folding defects to membrane protein homeostasis. J Am Chem Soc 141:204–215CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biochemistry and Molecular Biology, McGovern Medical SchoolUniversity of Texas Health Science CenterHoustonUSA

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