Assembly of outer-membrane proteins in bacteria and mitochondria

Microbiology (United Kingdom) - Tập 156 Số 9 - Trang 2587-2596 - 2010
Jan Tommassen1
1Department of Molecular Microbiology and Institute of Biomembranes, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands

Tóm tắt

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 hydrophobicα-helices, integral outer-membrane proteins (OMPs) formβ-barrels. Similarβ-barrel proteins are found in the outer membranes of mitochondria and chloroplasts, probably reflecting the endosymbiont origin of these eukaryotic cell organelles. How theseβ-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 ofβ-barrel proteins into the outer membrane as well. Although accessory components of the machineries are different between bacteria and mitochondria, a mitochondrialβ-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.

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Tài liệu tham khảo

Agterberg, 1990, Outer-membrane PhoE protein of Escherichia coli K-12 as an exposure vector: possibilities and limitations, Gene, 88, 37, 10.1016/0378-1119(90)90057-X

Anwari, 2010, A modular BAM complex in the outer membrane of the α-proteobacterium Caulobacter crescentus, PLoS One, 5, e8619, 10.1371/journal.pone.0008619

Bayrhuber, 2008, Structure of the human voltage-dependent anion channel, Proc Natl Acad Sci U S A, 105, 15370, 10.1073/pnas.0808115105

Behrens, 2001, The SurA periplasmic PPIase lacking its parvulin domains functions in vivo and has chaperone activity, EMBO J, 20, 285, 10.1093/emboj/20.1.285

Bos, 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, 10.1073/pnas.0402340101

Bos, 2007a, Biogenesis of the Gram-negative bacterial outer membrane, Annu Rev Microbiol, 61, 191, 10.1146/annurev.micro.61.080706.093245

Bos, 2007b, Functioning of outer membrane protein assembly factor Omp85 requires a single POTRA domain, EMBO Rep, 8, 1149, 10.1038/sj.embor.7401092

Bosch, 1988, Export and localization of N-terminally truncated derivatives of Escherichia coli K-12 outer membrane protein PhoE, J Biol Chem, 263, 9952, 10.1016/S0021-9258(19)81610-1

Chacinska, 2009, Importing mitochondrial proteins: machineries and mechanisms, Cell, 138, 628, 10.1016/j.cell.2009.08.005

Chen, 1996, A periplasmic protein (Skp) of Escherichia coli selectively binds a class of outer membrane proteins, Mol Microbiol, 19, 1287, 10.1111/j.1365-2958.1996.tb02473.x

Costanzo, 2006, Growth phase-dependent regulation of the extracytoplasmic stress factor, σE, by guanosine 3′,5′-bipyrophosphate (ppGpp, J Bacteriol, 188, 4627, 10.1128/JB.01981-05

de Cock, 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, 10.1006/jmbi.1997.1069

de Cock, 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, 10.1046/j.1432-1327.1999.00010.x

Dekker, 1995, In vitro folding of Escherichia coli outer-membrane phospholipase A, Eur J Biochem, 232, 214, 10.1111/j.1432-1033.1995.tb20801.x

Driessen, 2008, Protein translocation across the bacterial cytoplasmic membrane, Annu Rev Biochem, 77, 643, 10.1146/annurev.biochem.77.061606.160747

Fardini, 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, 10.1099/mic.0.025155-0

Fussenegger, 1996, A novel peptidoglycan-linked lipoprotein (ComL) that functions in natural transformation competence of Neisseria gonorrhoeae, Mol Microbiol, 19, 1095, 10.1046/j.1365-2958.1996.457984.x

Gatsos, 2008, Protein secretion and outer membrane assembly in Alphaproteobacteria, FEMS Microbiol Rev, 32, 995, 10.1111/j.1574-6976.2008.00130.x

Gatzeva-Topalova, 2008, Crystal structure of YaeT: conformational flexibility and substrate recognition, Structure, 16, 1873, 10.1016/j.str.2008.09.014

Gentle, 2004, The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria, J Cell Biol, 164, 19, 10.1083/jcb.200310092

Habib, 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, 10.1083/jcb.200602050

Harms, 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, 10.1074/jbc.M011194200

Hiller, 2008, Solution structure of the integral human membrane protein VDAC-1 in detergent micelles, Science, 321, 1206, 10.1126/science.1161302

Hsu, 2009, Two evolutionarily conserved essential β-barrel proteins in the chloroplast outer envelope membrane, Biosci Trends, 3, 168

Ishikawa, 2004, Two novel proteins in the mitochondrial outer membrane mediate β-barrel protein assembly, J Cell Biol, 166, 621, 10.1083/jcb.200405138

Johansen, 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, 10.1016/j.jmb.2006.09.004

Kim, 2007, Structure and function of an essential component of the outer membrane protein assembly machine, Science, 317, 961, 10.1126/science.1143993

Knowles, 2008, Fold and function of polypeptide transport-associated domains responsible for delivering unfolded proteins to membranes, Mol Microbiol, 68, 1216, 10.1111/j.1365-2958.2008.06225.x

Koebnik, 2000, Structure and function of bacterial outer membrane proteins: barrels in a nutshell, Mol Microbiol, 37, 239, 10.1046/j.1365-2958.2000.01983.x

Korndörfer, 2004, Structure of the periplasmic chaperone Skp suggests functional similarity with cytosolic chaperones despite differing architecture, Nat Struct Mol Biol, 11, 1015, 10.1038/nsmb828

Kozjak, 2003, An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane, J Biol Chem, 278, 48520, 10.1074/jbc.C300442200

Krimmer, 2001, 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, 10.1083/jcb.152.2.289

Krojer, 2008, Structural basis for the regulated protease and chaperone function of DegP, Nature, 453, 885, 10.1038/nature07004

Kutik, 2008, Dissecting membrane insertion of mitochondrial β-barrel proteins, Cell, 132, 1011, 10.1016/j.cell.2008.01.028

Lazar, 1996, SurA assists the folding of Escherichia coli outer membrane proteins, J Bacteriol, 178, 1770, 10.1128/JB.178.6.1770-1773.1996

Malinverni, 2006, YfiO stabilizes the YaeT complex and is essential for outer membrane protein assembly in Escherichia coli, Mol Microbiol, 61, 151, 10.1111/j.1365-2958.2006.05211.x

Manning, 1998, Omp85 of Neisseria gonorrhoeae and Neisseria meningitidis are similar to Haemophilus influenzae D-15-Ag and Pasteurella multocida Oma87, Microb Pathog, 25, 11, 10.1006/mpat.1998.0206

Milenkovic, 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, 10.1074/jbc.C400120200

Model, 2001, Multistep assembly of the protein import channel of the mitochondrial outer membrane, Nat Struct Biol, 8, 361, 10.1038/86253

Nakamura, 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, 10.1093/oxfordjournals.jbchem.a131414

Nikaido, 2003, Molecular basis of bacterial outer membrane permeability revisited, Microbiol Mol Biol Rev, 67, 593, 10.1128/MMBR.67.4.593-656.2003

Papenfort, 2006, σE-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay, Mol Microbiol, 62, 1674, 10.1111/j.1365-2958.2006.05524.x

Paschen, 2003, Evolutionary conservation of biogenesis of β-barrel membrane proteins, Nature, 426, 862, 10.1038/nature02208

Rapaport, 1999, Biogenesis of Tom40, core component of the TOM complex of mitochondria, J Cell Biol, 146, 321, 10.1083/jcb.146.2.321

Reumann, 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, 10.1073/pnas.96.2.784

Rizzitello, 2001, Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli, J Bacteriol, 183, 6794, 10.1128/JB.183.23.6794-6800.2001

Robert, 2006, Assembly factor Omp85 recognizes its outer membrane protein substrates by a species-specific C-terminal motif, PLoS Biol, 4, e377, 10.1371/journal.pbio.0040377

Rouvière, 1996, SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins, Genes Dev, 10, 3170, 10.1101/gad.10.24.3170

Ruiz, 2005, Sensing external stress: watchdogs of the Escherichia coli cell envelope, Curr Opin Microbiol, 8, 122, 10.1016/j.mib.2005.02.013

Rutten, 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, 10.1073/pnas.0813064106

Sánchez-Pulido, 2003, POTRA: a conserved domain in the FtsQ family and a class of β-barrel outer membrane proteins, Trends Biochem Sci, 28, 523, 10.1016/j.tibs.2003.08.003

Schäfer, 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, 10.1074/jbc.274.35.24567

Sklar, 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, 10.1073/pnas.0701579104

Sklar, 2007b, Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli, Genes Dev, 21, 2473, 10.1101/gad.1581007

Spiess, 1999, A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein, Cell, 97, 339, 10.1016/S0092-8674(00)80743-6

Steeghs, 1998, Meningitis bacterium is viable without endotoxin, Nature, 392, 449, 10.1038/33046

Steeghs, 2001, Outer membrane composition of a lipopolysaccharide-deficient Neisseria meningitidis mutant, EMBO J, 20, 6937, 10.1093/emboj/20.24.6937

Stegmeier, 2006, Characterization of pores formed by YaeT (Omp85) from Escherichia coli, J Biochem, 140, 275, 10.1093/jb/mvj147

Struyvé, 1991, Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein, J Mol Biol, 218, 141, 10.1016/0022-2836(91)90880-F

Tam, 2005, Changes in lipopolysaccharide structure induce the σE-dependent response of Escherichia coli, Mol Microbiol, 55, 1403, 10.1111/j.1365-2958.2005.04497.x

Tefsen, 2005, MsbA is not required for phospholipid transport in Neisseria meningitidis, J Biol Chem, 280, 35961, 10.1074/jbc.M509026200

Thomas, 2001, Cloning, overexpression, purification, and immunobiology of an 85-kilodalton outer membrane protein from Haemophilus ducreyi, Infect Immun, 69, 4438, 10.1128/IAI.69.7.4438-4446.2001

Tsukazaki, 2008, Conformational transition of Sec machinery inferred from bacterial SecYE structures, Nature, 455, 988, 10.1038/nature07421

Ujwal, 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, 10.1073/pnas.0809634105

Vertommen, 2009, Characterization of the role of the Escherichia coli periplasmic chaperone SurA using differential proteomics, Proteomics, 9, 2432, 10.1002/pmic.200800794

Volokhina, 2009, The β-barrel outer membrane protein assembly complex of Neisseria meningitidis, J Bacteriol, 191, 7074, 10.1128/JB.00737-09

Voulhoux, 2004, Omp85, an evolutionarily conserved bacterial protein involved in outer-membrane-protein assembly, Res Microbiol, 155, 129, 10.1016/j.resmic.2003.11.007

Voulhoux, 2003, Role of a highly conserved bacterial protein in outer membrane protein assembly, Science, 299, 262, 10.1126/science.1078973

Waizenegger, 2004, Tob38, a novel essential component in the biogenesis of β-barrel proteins of mitochondria, EMBO Rep, 5, 704, 10.1038/sj.embor.7400183

Walther, 2009, Biogenesis of mitochondrial outer membrane proteins, Biochim Biophys Acta, 1793, 42, 10.1016/j.bbamcr.2008.04.013

Walther, 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, 10.1073/pnas.0807830106

Walther, 2009b, Biogenesis of β-barrel membrane proteins in bacteria and eukaryotes: evolutionary conservation and divergence, Cell Mol Life Sci, 66, 2789, 10.1007/s00018-009-0029-z

Walther, 2010, The mitochondrial porin, VDAC, has retained the ability to be assembled in the bacterial outer membrane, Mol Biol Evol, 27, 887, 10.1093/molbev/msp294

Walton, 2004, Crystal structure of Skp, a prefoldin-like chaperone that protects soluble and membrane proteins from aggregation, Mol Cell, 15, 367, 10.1016/j.molcel.2004.07.023

Walton, 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, 10.1073/pnas.0809275106

Wiedemann, 2003, Machinery for protein sorting and assembly in the mitochondrial outer membrane, Nature, 424, 565, 10.1038/nature01753

Wu, 2005, Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli, Cell, 121, 235, 10.1016/j.cell.2005.02.015