1887

Abstract

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 -helices, integral outer-membrane proteins (OMPs) form -barrels. Similar -barrel proteins are found in the outer membranes of mitochondria and chloroplasts, probably reflecting the endosymbiont origin of these eukaryotic cell organelles. How these -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 -barrel proteins into the outer membrane as well. Although accessory components of the machineries are different between bacteria and mitochondria, a mitochondrial -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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2010-09-01
2019-11-19
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References

  1. Agterberg, M., Adriaanse, H., van Bruggen, A., Karperien, M. & Tommassen, J. ( 1990; ). Outer-membrane PhoE protein of Escherichia coli K-12 as an exposure vector: possibilities and limitations. Gene 88, 37–45.[CrossRef]
    [Google Scholar]
  2. Anwari, K., Poggio, S., Perry, A., Gatsos, X., Ramarathinam, S. H., Williamson, N. A., Noinaj, N., Buchanan, S., Gabriel, K. & other authors ( 2010; ). A modular BAM complex in the outer membrane of the α-proteobacterium Caulobacter crescentus. PLoS One 5, e8619 [CrossRef]
    [Google Scholar]
  3. Bayrhuber, M., Meins, T., Habeck, M., Becker, S., Giller, K., Villinger, S., Vonrhein, C., Griesinger, C., Zweckstetter, M. & Zeth, K. ( 2008; ). Structure of the human voltage-dependent anion channel. Proc Natl Acad Sci U S A 105, 15370–15375.[CrossRef]
    [Google Scholar]
  4. Behrens, S., Maier, R., de Cock, H., Schmid, F. X. & Gross, C. A. ( 2001; ). The SurA periplasmic PPIase lacking its parvulin domains functions in vivo and has chaperone activity. EMBO J 20, 285–294.[CrossRef]
    [Google Scholar]
  5. Bos, M. P., Tefsen, B., Geurtsen, J. & Tommassen, J. ( 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.[CrossRef]
    [Google Scholar]
  6. Bos, M. P., Robert, V. & Tommassen, J. ( 2007a; ). Biogenesis of the Gram-negative bacterial outer membrane. Annu Rev Microbiol 61, 191–214.[CrossRef]
    [Google Scholar]
  7. Bos, M. P., Robert, V. & Tommassen, J. ( 2007b; ). Functioning of outer membrane protein assembly factor Omp85 requires a single POTRA domain. EMBO Rep 8, 1149–1154.[CrossRef]
    [Google Scholar]
  8. Bosch, D., Voorhout, W. & Tommassen, J. ( 1988; ). Export and localization of N-terminally truncated derivatives of Escherichia coli K-12 outer membrane protein PhoE. J Biol Chem 263, 9952–9957.
    [Google Scholar]
  9. Chacinska, A., Koehler, C. A., Milenkovic, D., Lithgow, T. & Pfanner, N. ( 2009; ). Importing mitochondrial proteins: machineries and mechanisms. Cell 138, 628–644.[CrossRef]
    [Google Scholar]
  10. Chen, R. & Henning, U. ( 1996; ). A periplasmic protein (Skp) of Escherichia coli selectively binds a class of outer membrane proteins. Mol Microbiol 19, 1287–1294.[CrossRef]
    [Google Scholar]
  11. Costanzo, A. & Ades, S. E. ( 2006; ). Growth phase-dependent regulation of the extracytoplasmic stress factor, σ E, by guanosine 3′,5′-bipyrophosphate (ppGpp). J Bacteriol 188, 4627–4634.[CrossRef]
    [Google Scholar]
  12. de Cock, H., Struyvé, M., Kleerebezem, M., van der Krift, T. & Tommassen, J. ( 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.[CrossRef]
    [Google Scholar]
  13. de Cock, H., Schäfer, U., Potgeter, M., Demel, R., Müller, M. & Tommassen, J. ( 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.[CrossRef]
    [Google Scholar]
  14. Dekker, N., Merck, K., Tommassen, J. & Verheij, H. M. ( 1995; ). In vitro folding of Escherichia coli outer-membrane phospholipase A. Eur J Biochem 232, 214–219.[CrossRef]
    [Google Scholar]
  15. Driessen, A. J. M. & Nouwen, N. ( 2008; ). Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem 77, 643–667.[CrossRef]
    [Google Scholar]
  16. Fardini, Y., Trotereau, J., Bottreau, E., Souchard, C., Velge, P. & Virlogeux-Payant, I. ( 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.[CrossRef]
    [Google Scholar]
  17. Fussenegger, M., Facius, D., Meier, J. & Meyer, T. F. ( 1996; ). A novel peptidoglycan-linked lipoprotein (ComL) that functions in natural transformation competence of Neisseria gonorrhoeae. Mol Microbiol 19, 1095–1105.[CrossRef]
    [Google Scholar]
  18. Gatsos, X., Perry, A. J., Anwari, K., Dolezal, P., Wolynec, P. P., Likić, V. A., Purcell, A. W., Buchanan, S. K. & Lithgow, T. ( 2008; ). Protein secretion and outer membrane assembly in Alphaproteobacteria. FEMS Microbiol Rev 32, 995–1009.[CrossRef]
    [Google Scholar]
  19. Gatzeva-Topalova, P. Z., Walton, T. A. & Sousa, M. C. ( 2008; ). Crystal structure of YaeT: conformational flexibility and substrate recognition. Structure 16, 1873–1881.[CrossRef]
    [Google Scholar]
  20. Gentle, I., Gabriel, K., Beech, P., Waller, R. & Lithgow, T. ( 2004; ). The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J Cell Biol 164, 19–24.[CrossRef]
    [Google Scholar]
  21. Habib, S. J., Waizenegger, T., Niewienda, A., Paschen, S. A., Neupert, W. & Rapaport, D. ( 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.[CrossRef]
    [Google Scholar]
  22. Harms, N., Koningstein, G., Dontje, W., Müller, M., Oudega, B., Luirink, J. & de Cock, H. ( 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.[CrossRef]
    [Google Scholar]
  23. Hiller, S., Garces, R. G., Malia, T. J., Orekhov, V. Y., Colombini, M. & Wagner, G. ( 2008; ). Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 321, 1206–1210.[CrossRef]
    [Google Scholar]
  24. Hsu, S.-C. & Inoue, K. ( 2009; ). Two evolutionarily conserved essential β-barrel proteins in the chloroplast outer envelope membrane. Biosci Trends 3, 168–178.
    [Google Scholar]
  25. Ishikawa, D., Yamamoto, H., Tamura, Y., Moritoh, K. & Endo, T. ( 2004; ). Two novel proteins in the mitochondrial outer membrane mediate β-barrel protein assembly. J Cell Biol 166, 621–627.[CrossRef]
    [Google Scholar]
  26. Johansen, J., Rasmussen, A. A., Overgaard, M. & Valentin-Hansen, P. ( 2006; ). Conserved small non-coding RNAs that belong to the σ E regulon: role in down-regulation of outer membrane proteins. J Mol Biol 364, 1–8.[CrossRef]
    [Google Scholar]
  27. Kim, S., Malinverni, J. C., Sliz, P., Silhavy, T. J., Harrison, S. C. & Kahne, D. ( 2007; ). Structure and function of an essential component of the outer membrane protein assembly machine. Science 317, 961–964.[CrossRef]
    [Google Scholar]
  28. Knowles, T. J., Jeeves, M., Bobat, S., Dancea, F., McClelland, D., Palmer, T., Overduin, M. & Henderson, I. R. ( 2008; ). Fold and function of polypeptide transport-associated domains responsible for delivering unfolded proteins to membranes. Mol Microbiol 68, 1216–1227.[CrossRef]
    [Google Scholar]
  29. Koebnik, R., Locher, K. P. & Van Gelder, P. ( 2000; ). Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37, 239–253.[CrossRef]
    [Google Scholar]
  30. Korndörfer, I. P., Dommel, M. K. & Skerra, A. ( 2004; ). Structure of the periplasmic chaperone Skp suggests functional similarity with cytosolic chaperones despite differing architecture. Nat Struct Mol Biol 11, 1015–1020.[CrossRef]
    [Google Scholar]
  31. Kozjak, V., Wiedemann, N., Milenkovic, D., Lohaus, C., Meyer, H. E., Guiard, B., Meisinger, C. & Pfanner, N. ( 2003; ). An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. J Biol Chem 278, 48520–48523.[CrossRef]
    [Google Scholar]
  32. Krimmer, T., Rapaport, D., Ryan, M. T., Meisinger, C., Kassenbrock, C. K., Blachly-Dyson, E., Forte, M., Douglas, M. G., Neupert, W. & other authors ( 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, 289–300.[CrossRef]
    [Google Scholar]
  33. Krojer, T., Sawa, J., Schäfer, E., Saibil, H. R., Ehrmann, M. & Clausen, T. ( 2008; ). Structural basis for the regulated protease and chaperone function of DegP. Nature 453, 885–890.[CrossRef]
    [Google Scholar]
  34. Kutik, S., Stojanovski, D., Becker, L., Becker, T., Meinecke, M., Krüger, V., Prinz, C., Meisinger, C., Guiard, B. & other authors ( 2008; ). Dissecting membrane insertion of mitochondrial β-barrel proteins. Cell 132, 1011–1024.[CrossRef]
    [Google Scholar]
  35. Lazar, S. W. & Kolter, R. ( 1996; ). SurA assists the folding of Escherichia coli outer membrane proteins. J Bacteriol 178, 1770–1773.
    [Google Scholar]
  36. Malinverni, J. C., Werner, J., Kim, S., Sklar, J. G., Kahne, D., Misra, R. & Silhavy, T. J. ( 2006; ). YfiO stabilizes the YaeT complex and is essential for outer membrane protein assembly in Escherichia coli. Mol Microbiol 61, 151–164.[CrossRef]
    [Google Scholar]
  37. Manning, D. S., Reschke, D. K. & Judd, R. 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.[CrossRef]
    [Google Scholar]
  38. Milenkovic, D., Kozjak, V., Wiedemann, N., Lohaus, C., Meyer, H. E., Guiard, B., Pfanner, N. & Meisinger, C. ( 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.[CrossRef]
    [Google Scholar]
  39. Model, K., Meisinger, C., Prinz, T., Wiedemann, N., Truscott, K. N., Pfanner, N. & Ryan, M. T. ( 2001; ). Multistep assembly of the protein import channel of the mitochondrial outer membrane. Nat Struct Biol 8, 361–370.[CrossRef]
    [Google Scholar]
  40. Nakamura, K. & Mizushima, S. ( 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.
    [Google Scholar]
  41. Nikaido, H. ( 2003; ). Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67, 593–656.[CrossRef]
    [Google Scholar]
  42. Papenfort, K., Pfeiffer, V., Mika, F., Lucchini, S., Hinton, J. C. D. & Vogel, J. ( 2006; ). σ E-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Mol Microbiol 62, 1674–1688.[CrossRef]
    [Google Scholar]
  43. Paschen, S. A., Waizenegger, T., Stan, T., Preuss, M., Cyrklaff, M., Hell, K., Rapaport, D. & Neupert, W. ( 2003; ). Evolutionary conservation of biogenesis of β-barrel membrane proteins. Nature 426, 862–866.[CrossRef]
    [Google Scholar]
  44. Rapaport, D. & Neupert, W. ( 1999; ). Biogenesis of Tom40, core component of the TOM complex of mitochondria. J Cell Biol 146, 321–331.[CrossRef]
    [Google Scholar]
  45. Reumann, S., Davila-Aponte, J. & Keegstra, K. ( 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.[CrossRef]
    [Google Scholar]
  46. Rizzitello, A. E., Harper, J. R. & Silhavy, T. J. ( 2001; ). Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli. J Bacteriol 183, 6794–6800.[CrossRef]
    [Google Scholar]
  47. Robert, V., Volokhina, E. B., Senf, F., Bos, M. P., Van Gelder, P. & Tommassen, J. ( 2006; ). Assembly factor Omp85 recognizes its outer membrane protein substrates by a species-specific C-terminal motif. PLoS Biol 4, e377 [CrossRef]
    [Google Scholar]
  48. Rouvière, P. E. & Gross, C. A. ( 1996; ). SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Genes Dev 10, 3170–3187.[CrossRef]
    [Google Scholar]
  49. Ruiz, N. & Silhavy, T. J. ( 2005; ). Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr Opin Microbiol 8, 122–126.[CrossRef]
    [Google Scholar]
  50. Rutten, L., Mannie, J.-P. B. A., Stead, C. M., Raetz, C. R. H., Reynolds, C. M., Bonvin, A. M. J. J., Tommassen, J. P., Egmond, M. R., Trent, M. S. & Gros, P. ( 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.[CrossRef]
    [Google Scholar]
  51. Sánchez-Pulido, L., Devos, D., Genevrois, S., Vicente, M. & Valencia, A. ( 2003; ). POTRA: a conserved domain in the FtsQ family and a class of β-barrel outer membrane proteins. Trends Biochem Sci 28, 523–526.[CrossRef]
    [Google Scholar]
  52. Schäfer, U., Beck, K. & Müller, M. ( 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.[CrossRef]
    [Google Scholar]
  53. Sklar, J. G., Wu, T., Gronenberg, L. S., Malinverni, J. C., Kahne, D. & Silhavy, T. 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.[CrossRef]
    [Google Scholar]
  54. Sklar, J. G., Wu, T., Kahne, D. & Silhavy, T. J. ( 2007b; ). Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli. Genes Dev 21, 2473–2484.[CrossRef]
    [Google Scholar]
  55. Spiess, C., Beil, A. & Ehrmann, M. ( 1999; ). A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97, 339–347.[CrossRef]
    [Google Scholar]
  56. Steeghs, L., den Hartog, R., den Boer, A., Zomer, B., Roholl, P. & van der Ley, P. ( 1998; ). Meningitis bacterium is viable without endotoxin. Nature 392, 449–450.[CrossRef]
    [Google Scholar]
  57. Steeghs, L., de Cock, H., Evers, E., Zomer, B., Tommassen, J. & van der Ley, P. ( 2001; ). Outer membrane composition of a lipopolysaccharide-deficient Neisseria meningitidis mutant. EMBO J 20, 6937–6945.[CrossRef]
    [Google Scholar]
  58. Stegmeier, J. F. & Andersen, C. ( 2006; ). Characterization of pores formed by YaeT (Omp85) from Escherichia coli. J Biochem 140, 275–283.[CrossRef]
    [Google Scholar]
  59. Struyvé, M., Moons, M. & Tommassen, J. ( 1991; ). Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J Mol Biol 218, 141–148.[CrossRef]
    [Google Scholar]
  60. Tam, C. & Missiakas, D. ( 2005; ). Changes in lipopolysaccharide structure induce the σ E-dependent response of Escherichia coli. Mol Microbiol 55, 1403–1412.[CrossRef]
    [Google Scholar]
  61. Tefsen, B., Bos, M. P., Beckers, F., Tommassen, J. & de Cock, H. ( 2005; ). MsbA is not required for phospholipid transport in Neisseria meningitidis. J Biol Chem 280, 35961–35966.[CrossRef]
    [Google Scholar]
  62. Thomas, K. L., Leduc, I., Olsen, B., Thomas, C. E., Cameron, D. W. & Elkins, C. ( 2001; ). Cloning, overexpression, purification, and immunobiology of an 85-kilodalton outer membrane protein from Haemophilus ducreyi. Infect Immun 69, 4438–4446.[CrossRef]
    [Google Scholar]
  63. Tsukazaki, T., Mori, H., Fukai, S., Ishitani, R., Mori, T., Dohmae, N., Perederina, A., Sugita, Y., Vassylyev, D. G. & other authors ( 2008; ). Conformational transition of Sec machinery inferred from bacterial SecYE structures. Nature 455, 988–992.[CrossRef]
    [Google Scholar]
  64. Ujwal, R., Cascio, D., Colletier, J. P., Faham, S., Zhang, J., Toro, L., Ping, P. & Abramson, J. ( 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.[CrossRef]
    [Google Scholar]
  65. Vertommen, D., Ruiz, N., Leverrier, P., Silhavy, T. J. & Collet, J.-F. ( 2009; ). Characterization of the role of the Escherichia coli periplasmic chaperone SurA using differential proteomics. Proteomics 9, 2432–2443.[CrossRef]
    [Google Scholar]
  66. Volokhina, E. B., Beckers, F., Tommassen, J. & Bos, M. P. ( 2009; ). The β-barrel outer membrane protein assembly complex of Neisseria meningitidis. J Bacteriol 191, 7074–7085.[CrossRef]
    [Google Scholar]
  67. Voulhoux, R. & Tommassen, J. ( 2004; ). Omp85, an evolutionarily conserved bacterial protein involved in outer-membrane-protein assembly. Res Microbiol 155, 129–135.[CrossRef]
    [Google Scholar]
  68. Voulhoux, R., Bos, M. P., Geurtsen, J., Mols, M. & Tommassen, J. ( 2003; ). Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299, 262–265.[CrossRef]
    [Google Scholar]
  69. Waizenegger, T., Habib, S. J., Lech, M., Mokranjac, D., Paschen, S. A., Hell, K., Neupert, W. & Rapaport, D. ( 2004; ). Tob38, a novel essential component in the biogenesis of β-barrel proteins of mitochondria. EMBO Rep 5, 704–709.[CrossRef]
    [Google Scholar]
  70. Walther, D. M. & Rapaport, D. ( 2009; ). Biogenesis of mitochondrial outer membrane proteins. Biochim Biophys Acta 1793, 42–51.[CrossRef]
    [Google Scholar]
  71. Walther, D. M., Papic, D., Bos, M. P., Tommassen, J. & Rapaport, D. ( 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.[CrossRef]
    [Google Scholar]
  72. Walther, D. M., Rapaport, D. & Tommassen, J. ( 2009b; ). Biogenesis of β-barrel membrane proteins in bacteria and eukaryotes: evolutionary conservation and divergence. Cell Mol Life Sci 66, 2789–2804.[CrossRef]
    [Google Scholar]
  73. Walther, D. M., Bos, M. P., Rapaport, D. & Tommassen, J. ( 2010; ). The mitochondrial porin, VDAC, has retained the ability to be assembled in the bacterial outer membrane. Mol Biol Evol 27, 887–895.[CrossRef]
    [Google Scholar]
  74. Walton, T. A. & Sousa, M. C. ( 2004; ). Crystal structure of Skp, a prefoldin-like chaperone that protects soluble and membrane proteins from aggregation. Mol Cell 15, 367–374.[CrossRef]
    [Google Scholar]
  75. Walton, T. A., Sandoval, C. M., Fowler, C. A., Pardi, A. & Sousa, M. 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.[CrossRef]
    [Google Scholar]
  76. Wiedemann, N., Kozjak, V., Chacinska, A., Schönfish, B., Rospert, S., Ryan, M. T., Pfanner, N. & Meisinger, C. ( 2003; ). Machinery for protein sorting and assembly in the mitochondrial outer membrane. Nature 424, 565–571.[CrossRef]
    [Google Scholar]
  77. Wu, T., Malinverni, J., Ruiz, N., Kim, S., Silhavy, T. J. & Kahne, D. ( 2005; ). Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121, 235–245.[CrossRef]
    [Google Scholar]
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