The cell envelope of Gram-negative bacteria consists of two membranes separated by the periplasm. In contrast with most integral membrane proteins, which span the membrane in the form of hydrophobic α-helices, integral outer-membrane proteins (OMPs) form β-barrels. Similar β-barrel proteins are found in the outer membranes of mitochondria and chloroplasts, probably reflecting the endosymbiont origin of these eukaryotic cell organelles. How these β-barrel proteins are assembled into the outer membrane has remained enigmatic for a long time. In recent years, much progress has been reached in this field by the identification of the components of the OMP assembly machinery. The central component of this machinery, called Omp85 or BamA, is an essential and highly conserved bacterial protein that recognizes a signature sequence at the C terminus of its substrate OMPs. A homologue of this protein is also found in mitochondria, where it is required for the assembly of β-barrel proteins into the outer membrane as well. Although accessory components of the machineries are different between bacteria and mitochondria, a mitochondrial β-barrel OMP can be assembled into the bacterial outer membrane and, vice versa, bacterial OMPs expressed in yeast are assembled into the mitochondrial outer membrane. These observations indicate that the basic mechanism of OMP assembly is evolutionarily highly conserved.
AgterbergM.,
AdriaanseH.,
van BruggenA.,
KarperienM.,
TommassenJ.1990; Outer-membrane PhoE protein of Escherichia coli K-12 as an exposure vector: possibilities and limitations. Gene 88:37–45
AnwariK.,
PoggioS.,
PerryA.,
GatsosX.,
RamarathinamS. H.,
WilliamsonN. A.,
NoinajN.,
BuchananS.,
GabrielK.other authors2010; A modular BAM complex in the outer membrane of the α-proteobacterium Caulobacter crescentus. PLoS One 5:e8619
BayrhuberM.,
MeinsT.,
HabeckM.,
BeckerS.,
GillerK.,
VillingerS.,
VonrheinC.,
GriesingerC.,
ZweckstetterM.,
ZethK.2008; Structure of the human voltage-dependent anion channel. Proc Natl Acad Sci U S A 105:15370–15375
BehrensS.,
MaierR.,
de CockH.,
SchmidF. X.,
GrossC. A.2001; The SurA periplasmic PPIase lacking its parvulin domains functions in vivo and has chaperone activity. EMBO J 20:285–294
BosM. P.,
TefsenB.,
GeurtsenJ.,
TommassenJ.2004; Identification of an outer membrane protein required for lipopolysaccharide transport to the bacterial cell surface. Proc Natl Acad Sci U S A 101:9417–9422
ChenR.,
HenningU.1996; A periplasmic protein (Skp) of Escherichia coli selectively binds a class of outer membrane proteins. Mol Microbiol 19:1287–1294
de CockH.,
StruyvéM.,
KleerebezemM.,
van der KriftT.,
TommassenJ.1997; Role of the carboxy-terminal phenylalanine in the biogenesis of outer membrane protein PhoE of Escherichia coli K-12. J Mol Biol 269:473–478
de CockH.,
SchäferU.,
PotgeterM.,
DemelR.,
MüllerM.,
TommassenJ.1999; Affinity of the periplasmic chaperone Skp of Escherichia coli for phospholipids, lipopolysaccharides and non-native outer membrane proteins. Role of Skp in the biogenesis of outer membrane protein. Eur J Biochem 259:96–103
FardiniY.,
TrotereauJ.,
BottreauE.,
SouchardC.,
VelgeP.,
Virlogeux-PayantI.2009; Investigation of the role of the BAM complex and SurA chaperone in outer membrane protein biogenesis and T3SS expression in Salmonella. Microbiology 155:1613–1622
GatsosX.,
PerryA. J.,
AnwariK.,
DolezalP.,
WolynecP. P.,
LikićV. A.,
PurcellA. W.,
BuchananS. K.,
LithgowT.2008; Protein secretion and outer membrane assembly in Alphaproteobacteria. FEMS Microbiol Rev 32:995–1009
GentleI.,
GabrielK.,
BeechP.,
WallerR.,
LithgowT.2004; The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J Cell Biol 164:19–24
HabibS. J.,
WaizeneggerT.,
NiewiendaA.,
PaschenS. A.,
NeupertW.,
RapaportD.2007; The N-terminal domain of Tob55 has a receptor-like function in the biogenesis of mitochondrial β-barrel proteins. J Cell Biol 176:77–88
HarmsN.,
KoningsteinG.,
DontjeW.,
MüllerM.,
OudegaB.,
LuirinkJ.,
de CockH.2001; The early interaction of the outer membrane protein PhoE with the periplasmic chaperone Skp occurs at the cytoplasmic membrane. J Biol Chem 276:18804–18811
HillerS.,
GarcesR. G.,
MaliaT. J.,
OrekhovV. Y.,
ColombiniM.,
WagnerG.2008; Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 321:1206–1210
JohansenJ.,
RasmussenA. A.,
OvergaardM.,
Valentin-HansenP.2006; Conserved small non-coding RNAs that belong to the σE regulon: role in down-regulation of outer membrane proteins. J Mol Biol 364:1–8
KimS.,
MalinverniJ. C.,
SlizP.,
SilhavyT. J.,
HarrisonS. C.,
KahneD.2007; Structure and function of an essential component of the outer membrane protein assembly machine. Science 317:961–964
KozjakV.,
WiedemannN.,
MilenkovicD.,
LohausC.,
MeyerH. E.,
GuiardB.,
MeisingerC.,
PfannerN.2003; An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. J Biol Chem 278:48520–48523
KrimmerT.,
RapaportD.,
RyanM. T.,
MeisingerC.,
KassenbrockC. K.,
Blachly-DysonE.,
ForteM.,
DouglasM. G.,
NeupertW.other authors2001; Biogenesis of the major mitochondrial outer membrane protein porin involves a complex import pathway via receptors and the general import pore. J Cell Biol 152:289–300
KrojerT.,
SawaJ.,
SchäferE.,
SaibilH. R.,
EhrmannM.,
ClausenT.2008; Structural basis for the regulated protease and chaperone function of DegP. Nature 453:885–890
MalinverniJ. C.,
WernerJ.,
KimS.,
SklarJ. G.,
KahneD.,
MisraR.,
SilhavyT. J.2006; YfiO stabilizes the YaeT complex and is essential for outer membrane protein assembly in Escherichia coli. Mol Microbiol 61:151–164
ManningD. S.,
ReschkeD. K.,
JuddR. C.1998; Omp85 of Neisseria gonorrhoeae and Neisseria meningitidis are similar to Haemophilus influenzae D-15-Ag and Pasteurella multocida Oma87. Microb Pathog 25:11–21
MilenkovicD.,
KozjakV.,
WiedemannN.,
LohausC.,
MeyerH. E.,
GuiardB.,
PfannerN.,
MeisingerC.2004; Sam35 of the mitochondrial protein sorting and assembly machinery is a peripheral outer membrane protein essential for cell viability. J Biol Chem 279:22781–22785
ModelK.,
MeisingerC.,
PrinzT.,
WiedemannN.,
TruscottK. N.,
PfannerN.,
RyanM. T.2001; Multistep assembly of the protein import channel of the mitochondrial outer membrane. Nat Struct Biol 8:361–370
NakamuraK.,
MizushimaS.1976; Effects of heating in dodecyl sulfate solution on the conformation and electrophoretic mobility of isolated major outer membrane proteins from Escherichia coli K-12. J Biochem 80:1411–1422
PapenfortK.,
PfeifferV.,
MikaF.,
LucchiniS.,
HintonJ. C. D.,
VogelJ.2006; σE-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Mol Microbiol 62:1674–1688
ReumannS.,
Davila-AponteJ.,
KeegstraK.1999; The evolutionary origin of the protein-translocating channel of chloroplastic envelope membranes: Identification of a cyanobacterial homolog. Proc Natl Acad Sci U S A 96:784–789
RizzitelloA. E.,
HarperJ. R.,
SilhavyT. J.2001; Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli. J Bacteriol 183:6794–6800
RouvièreP. E.,
GrossC. A.1996; SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Genes Dev 10:3170–3187
RuttenL.,
MannieJ.-P. B. A.,
SteadC. M.,
RaetzC. R. H.,
ReynoldsC. M.,
BonvinA. M. J. J.,
TommassenJ. P.,
EgmondM. R.,
TrentM. S.,
GrosP.2009; Active-site architecture and catalytic mechanism of the lipid A deacylase LpxR of Salmonella typhimurium. Proc Natl Acad Sci U S A 106:1960–1964
Sánchez-PulidoL.,
DevosD.,
GenevroisS.,
VicenteM.,
ValenciaA.2003; POTRA: a conserved domain in the FtsQ family and a class of β-barrel outer membrane proteins. Trends Biochem Sci 28:523–526
SchäferU.,
BeckK.,
MüllerM.1999; Skp, a molecular chaperone of Gram-negative bacteria, is required for the formation of soluble periplasmic intermediates of outer membrane proteins. J Biol Chem 274:24567–24574
SklarJ. G.,
WuT.,
GronenbergL. S.,
MalinverniJ. C.,
KahneD.,
SilhavyT. J.2007a; Lipoprotein SmpA is a component of the YaeT complex that assembles outer membrane proteins in Escherichia coli. Proc Natl Acad Sci U S A 104:6400–6405
SklarJ. G.,
WuT.,
KahneD.,
SilhavyT. J.2007b; Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli. Genes Dev 21:2473–2484
SteeghsL.,
de CockH.,
EversE.,
ZomerB.,
TommassenJ.,
van der LeyP.2001; Outer membrane composition of a lipopolysaccharide-deficient Neisseria meningitidis mutant. EMBO J 20:6937–6945
StruyvéM.,
MoonsM.,
TommassenJ.1991; Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J Mol Biol 218:141–148
TefsenB.,
BosM. P.,
BeckersF.,
TommassenJ.,
de CockH.2005; MsbA is not required for phospholipid transport in Neisseria meningitidis. J Biol Chem 280:35961–35966
ThomasK. L.,
LeducI.,
OlsenB.,
ThomasC. E.,
CameronD. W.,
ElkinsC.2001; Cloning, overexpression, purification, and immunobiology of an 85-kilodalton outer membrane protein from Haemophilus ducreyi. Infect Immun 69:4438–4446
UjwalR.,
CascioD.,
ColletierJ. P.,
FahamS.,
ZhangJ.,
ToroL.,
PingP.,
AbramsonJ.2008; The crystal structure of mouse VDAC1 at 2.3 Å resolution reveals mechanistic insights into metabolite gating. Proc Natl Acad Sci U S A 105:17742–17747
VertommenD.,
RuizN.,
LeverrierP.,
SilhavyT. J.,
ColletJ.-F.2009; Characterization of the role of the Escherichia coli periplasmic chaperone SurA using differential proteomics. Proteomics 9:2432–2443
VoulhouxR.,
TommassenJ.2004; Omp85, an evolutionarily conserved bacterial protein involved in outer-membrane-protein assembly. Res Microbiol 155:129–135
VoulhouxR.,
BosM. P.,
GeurtsenJ.,
MolsM.,
TommassenJ.2003; Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299:262–265
WaizeneggerT.,
HabibS. J.,
LechM.,
MokranjacD.,
PaschenS. A.,
HellK.,
NeupertW.,
RapaportD.2004; Tob38, a novel essential component in the biogenesis of β-barrel proteins of mitochondria. EMBO Rep 5:704–709
WaltherD. M.,
PapicD.,
BosM. P.,
TommassenJ.,
RapaportD.2009a; Signals in bacterial β-barrel proteins are functional in eukaryotic cells for targeting to and assembly in mitochondria. Proc Natl Acad Sci U S A 106:2531–2536
WaltherD. M.,
RapaportD.,
TommassenJ.2009b; Biogenesis of β-barrel membrane proteins in bacteria and eukaryotes: evolutionary conservation and divergence. Cell Mol Life Sci 66:2789–2804
WaltherD. M.,
BosM. P.,
RapaportD.,
TommassenJ.2010; The mitochondrial porin, VDAC, has retained the ability to be assembled in the bacterial outer membrane. Mol Biol Evol 27:887–895
WaltonT. A.,
SousaM. C.2004; Crystal structure of Skp, a prefoldin-like chaperone that protects soluble and membrane proteins from aggregation. Mol Cell 15:367–374
WaltonT. A.,
SandovalC. M.,
FowlerC. A.,
PardiA.,
SousaM. C.2009; The cavity-chaperone Skp protects its substrate from aggregation but allows independent folding of substrate domains. Proc Natl Acad Sci U S A 106:1772–1777
WiedemannN.,
KozjakV.,
ChacinskaA.,
SchönfishB.,
RospertS.,
RyanM. T.,
PfannerN.,
MeisingerC.2003; Machinery for protein sorting and assembly in the mitochondrial outer membrane. Nature 424:565–571