Skip to main content
Log in

Biogenesis of β-barrel integral proteins of bacterial outer membrane

  • Review
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

Gram-negative bacteria are enveloped by two membranes, the inner (cytoplasmic) (CM) and the outer (OM). The majority of integral outer membrane proteins are arranged in β-barrels of cylindrical shape composed of amphipathic antiparallel β-strands. In bacteria, β-barrel proteins function as water-filled pores, active transporters, enzymes, receptors, and structural proteins. Proteins of bacterial OM are synthesized in the cytoplasm as unfolded polypeptides with an N-terminal sequence that marks them for transport across the CM. Precursors of membrane proteins move through the aqueous medium of the cytosol and periplasm under the protection of chaperones (SecB, Skp, SurA, and DegP), then cross the CM via the Sec system composed of a polypeptide-conducting channel (SecYEG) and ATPase (SecA), the latter providing the energy for the translocation of the pre-protein. Pre-protein folding and incorporation in the OM require the participation of the Bam-complex, probably without the use of energy. This review summarizes current data on the biogenesis of the β-barrel proteins of bacterial OM. Data on the structure of the proteins included in the multicomponent system for delivery of the OM proteins to their destination in the cell and on their complexes with partners, including pre-proteins, are pre-sented. Molecular models constructed on the basis of structural, genetic, and biochemical studies that describe the mechanisms of β-barrel protein assembly by this molecular transport machinery are also considered.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

ATPase:

adenosine triphosphatase

CM:

cytoplasmic membrane

LPS:

lipopolysaccharide

OM:

outer membrane

PG:

peptidoglycan

PPI domain:

peptidyl-prolylisomerase domain

TM:

transmembrane

References

  1. Koebnik, R., Locher, K. P., and Van Gelder, P. (2000) Mol. Microbiol., 37, 239–253.

    Article  PubMed  CAS  Google Scholar 

  2. Dong, C. J., Beis, K., Nesper, J., Brunkan-Lamontagne, A. L., Clarke, B. R., Whitfield, C., and Naismith, J. H. (2006) Nature, 444, 226–229.

    Article  PubMed  CAS  Google Scholar 

  3. Chandran, V., Fronzes, R., Duquerroy, S., Cronin, N., Navaza, J., and Waksman, G. (2009) Nature, 462, 1011–1015.

    Article  PubMed  CAS  Google Scholar 

  4. Randall, L. L., Topping, T. B., Suciu, D., and Hardy, S. J. (1998) Prot. Sci., 7, 1195–1200.

    Article  CAS  Google Scholar 

  5. Randall, L. L., Topping, T. B., and Hardy, S. J. (1990) Science, 248, 860–863.

    Article  PubMed  CAS  Google Scholar 

  6. Xu, Z., Knafels, J. D., and Yoshino, K. (2000) Nat. Struct. Biol., 7, 1172–1177.

    Article  PubMed  CAS  Google Scholar 

  7. Dekker, C., de Kruijff, B., and Gros, P. (2003) J. Struct. Biol., 144, 313–319.

    Article  PubMed  CAS  Google Scholar 

  8. Crane, J. M., Suo, Y., Lilly, A. A., Mao, C., Hubbell, W. L., and Randall, L. L. (2006) J. Mol. Biol., 363, 63–74.

    Article  PubMed  CAS  Google Scholar 

  9. Tang, Y., Pan, X., Tai, P. C., and Sui, S.-F. (2010) Biochem. Biophys. Res. Commun., 393, 698–702.

    Article  PubMed  CAS  Google Scholar 

  10. Lilly, A. A., Crane, J. M., and Randall, L. L. (2009) Protein Sci., 18, 1860–1868.

    Article  PubMed  CAS  Google Scholar 

  11. Randall, L. L., and Hardy, S. J. S. (1995) Trends Biochem. Sci., 20, 65–69.

    Article  PubMed  CAS  Google Scholar 

  12. Hartl, F. U., Lecker, S., Schiebel, E., Hendrick, J. P., and Wickner, W. (1990) Cell, 63, 269–279.

    Article  PubMed  CAS  Google Scholar 

  13. Zhou, J., and Xu, Z. (2003) Nat. Struct. Biol., 10, 942–947.

    Article  PubMed  CAS  Google Scholar 

  14. Cabelli, R. J., Dolan, K. V., Qian, L. P., and Oliver, D. B. (1991) J. Biol. Chem., 6, 24420–24427.

    Google Scholar 

  15. Lill, R., Dowhan, W., and Wickner, W. (1990) Cell, 60, 271–280.

    Article  PubMed  CAS  Google Scholar 

  16. Woodbury, R. L., Hardy, S. J. S., and Randall, L. L. (2002) Prot. Sci., 11, 875–882.

    Article  CAS  Google Scholar 

  17. Zimmer, J., Li, W., and Rapoport, T. A. (2006) J. Mol. Biol., 364, 259–265.

    Article  PubMed  CAS  Google Scholar 

  18. Hunt, J. F., Weinkauf, S., Henry, L., Fak, J. J., McNicholas, P., Oliver, D. B., and Deisenhofer, J. (2002) Science, 297, 2018–2026.

    Article  PubMed  CAS  Google Scholar 

  19. Sharma, V., Arockiasamy, A., Ronning, D. R., Savva, C. G., Holzenburg, A., Braunstein, M., Jacobs, W. R., Jr., and Sacchettini, J. C. (2003) Proc. Natl. Acad. Sci. USA, 100, 2243–2248.

    Article  PubMed  CAS  Google Scholar 

  20. Vassylyev, D. G., Mori, H., Vassylyeva, M. N., Tsukaraki, T., Kimura, Y., Tahirov, T. H., and Ito, K. (2006) J. Mol. Biol., 364, 248–258.

    Article  PubMed  CAS  Google Scholar 

  21. Papanikolau, Y., Papadovasilaki, M., Ravelli, R. B., McCarthy, A. A., Cusack, S., Economou, A., and Petratos, K. (2007) J. Mol. Biol., 366, 1545–1557.

    Article  PubMed  CAS  Google Scholar 

  22. Driessen, A. J. M. (1993) Biochemistry, 32, 13190–13197.

    Article  PubMed  CAS  Google Scholar 

  23. Or, E., Navon, A., and Rapoport, T. A. (2002) EMBO J., 21, 4470–4479.

    Article  PubMed  CAS  Google Scholar 

  24. Duong, F. (2003) EMBO J., 22, 4375–4384.

    Article  PubMed  CAS  Google Scholar 

  25. Or, E., Boyd, D., Gon, S., Beckwith, J., and Rapoport, T. A. (2004) J. Biol. Chem., 280, 9097–9105.

    Article  PubMed  CAS  Google Scholar 

  26. Alami, M., Dalal, K., Lelj-Garolla, B., Sligar, S. G., and Duong, F. (2007) EMBO J., 26, 1995–2004.

    Article  PubMed  CAS  Google Scholar 

  27. Jilaveanu, L. B., Zito, C. L., and Oliver, D. (2005) Proc. Natl. Acad. Sci. USA, 102, 7511–7516.

    Article  PubMed  CAS  Google Scholar 

  28. De Keyzer, J., van der Sluis, E. O., Spelbrink, R. E. J., Nijstad, N., de Kruijff, B., Nouwen, N., van der Does, C., and Driessen, A. J. M. (2005) J. Biol. Chem., 280, 35255–35260.

    Article  PubMed  CAS  Google Scholar 

  29. Mitra, K., Frank, J., and Driessen, A. (2006) Nature Struct. Mol. Biol., 13, 957–964.

    Article  CAS  Google Scholar 

  30. Osborne, A. R., Clemons, W. M., and Rapoport, T. A. (2004) Proc. Natl. Acad. Sci. USA, 101, 10937–10942.

    Article  PubMed  CAS  Google Scholar 

  31. Caruthers, J. M., and McKay, D. B. (2002) Curr. Opin. Struct. Biol., 12, 123–133.

    Article  PubMed  CAS  Google Scholar 

  32. Papanikou, E., Karamanou, S., Baud, C., Frank, M., Sianidis, G., Keramisanou, D., Kaladimos, C. G., Kuhn, A., and Economou, A. (2005) J. Biol. Chem., 280, 43209–43217.

    Article  PubMed  CAS  Google Scholar 

  33. Vrontou, E., Karamanou, S., Baud, C., Sianidis, G., and Economou, A. (2004) J. Biol. Chem., 279, 22490–22497.

    Article  PubMed  CAS  Google Scholar 

  34. Erlandson, K. J., Miller, S. B. M., Nam, Y., Osborne, A. R., Zimmer, J., and Rapoport, T. A. (2008) Nature, 455, 984–988.

    Article  PubMed  CAS  Google Scholar 

  35. Zimmer, J., Nam, Y., and Rapoport, T. A. (2008) Nature, 455, 936–943.

    Article  PubMed  CAS  Google Scholar 

  36. Karamanou, S., Gouridis, G., Papanikou, E., Sianidis, G., Gelis, I., Keramisanou, D., Vrontou, E., Kalodimos, C. G., and Economou, A. (2007) EMBO J., 26, 2904–2914.

    Article  PubMed  CAS  Google Scholar 

  37. Sianidis, G., Karamanou, S., Vrontou, E., Boulias, K., Repanas, K., Kyrpides, N., Politou, A. S., and Economou, A. (2001) EMBO J., 20, 961–970.

    Article  PubMed  CAS  Google Scholar 

  38. Karamanou, S., Vrontou, E., Sianidis, G., Baud, K., Roos, T., Kuhn, A., Politou, A. S., and Economou, A. (1999) Mol. Microbiol., 34, 1133–1145.

    Article  PubMed  CAS  Google Scholar 

  39. Fak, J. J., Itkin, A., Ciobanu, D. D., Lin, E. C., Song, X. J., Chou, Y. T., Gierasch, L. M., and Hunt, J. F. (2004) Biochemistry, 43, 7307–7327.

    Article  PubMed  CAS  Google Scholar 

  40. Kimura, E., Akita, M., Matsuyama, S., and Mizushima, S. (1991) J. Biol. Chem., 266, 6600–6606.

    PubMed  CAS  Google Scholar 

  41. Kourtz, L., and Oliver, D. (2002) Mol. Microbiol., 37, 1342–1356.

    Article  Google Scholar 

  42. Van Voorst, F., Vereyken, I. J., and de Kruijff, B. (2000) FEBS Lett., 486, 57–62.

    Article  PubMed  Google Scholar 

  43. Morshauser, R. C., Hu, W., Wang, H., Pang, Y., Flynn, G. C., and Zuiderweg, E. R. (1999) J. Mol. Biol., 289, 1387–1403.

    Article  PubMed  CAS  Google Scholar 

  44. Cooper, D. B., Smith, V. F., Crane, J. M., Roth, H. C., Lilly, A. A., and Randall, L. L. (2008) J. Mol. Biol., 382, 74–87.

    Article  PubMed  CAS  Google Scholar 

  45. Auclair, S. M., Moses, J. P., Musial-Siwek, M., Kendall, D. A., Oliver, D. B., and Mukerji, I. (2010) Biochemistry, 49, 782–792.

    Article  PubMed  CAS  Google Scholar 

  46. Brundage, L., Hendric, J. P., Schiebel, E., Driessen, A. J. M., and Wickner, W. (1990) Cell, 62, 649–657.

    Article  PubMed  CAS  Google Scholar 

  47. Van den Berg, B., Clemons, W. M., Collinson, I., Modis, Y., Hartmann, E., Harrison, S. C., and Rapoport, T. A. (2004) Nature, 427, 36–44.

    Article  PubMed  CAS  Google Scholar 

  48. Breyton, C., Haase, W., Rapoport, T. A., Kuhlbrandt, W., and Collinson, I. (2002) Nature, 418, 662–665.

    Article  PubMed  CAS  Google Scholar 

  49. Driessen, A. J. M., and Nouwen, N. (2008) Annu. Rev. Biochem., 77, 643–667.

    Article  PubMed  CAS  Google Scholar 

  50. Kihara, A., Akiyama, Y., and Ito, K. (1995) Proc. Natl. Acad. Sci. USA, 92, 4532–4536.

    Article  PubMed  CAS  Google Scholar 

  51. Bonardi, F., Halza, E., Walko, M., Plessis, F. D., Nouwen, N., Feringa, B. L., and Driessen, A. J. M. (2011) Proc. Natl. Acad. Sci. USA, 108, 7775–7780.

    Article  PubMed  Google Scholar 

  52. Tani, K., Tokuda, H., and Mizushima, S. (1990) J. Biol. Chem., 265, 17341–17347.

    PubMed  CAS  Google Scholar 

  53. Kowarik, M., Kung, S., Martoglio, B., and Helenius, A. (2002) Mol. Cell., 10, 769–778.

    Article  PubMed  CAS  Google Scholar 

  54. Meyer, T., Menetret, J., Breitling, R., Miller, K., Akey, C. W., and Rapoport, T. A. (1999) J. Mol. Biol., 285, 1789–1800.

    Article  PubMed  CAS  Google Scholar 

  55. Manting, E., van der Does, C., Remigy, H., Engel, A., and Driessen, A. (2000) EMBO J., 19, 852–861.

    Article  PubMed  CAS  Google Scholar 

  56. Yahr, T. L., and Wickner, W. T. (2000) EMBO J., 19, 4393–4401.

    Article  PubMed  CAS  Google Scholar 

  57. Bessonneau, P., Besson, V., Collinson, I., and Duong, F. (2002) EMBO J., 21, 995–1003.

    Article  PubMed  CAS  Google Scholar 

  58. Mori, H., Tsukazaki, T., Masui, R., Kuramitsu, S., Yokoyama, S., Johnson, A., Kimura, Y., Akiyama, Y., and Ito, K. (2003) J. Biol. Chem., 278, 14257–14264.

    Article  PubMed  CAS  Google Scholar 

  59. Boy, D., and Koch, H.-G. (2009) Mol. Biol. Cell., 20, 1804–1815.

    Article  PubMed  CAS  Google Scholar 

  60. Tsukazaki, T., Mori, H., Fukai, S., Ishitani, R., Mori, T., Dohmae, N., Perederina, A., Sugiya, Y., Vassylyev, D. G., Ito, K., and Nureki, O. (2008) Nature, 455, 988–991.

    Article  PubMed  CAS  Google Scholar 

  61. Cannon, K., Or, E., Clemons, W. M., Shibata, Y., and Rapoport, T. J. (2005) J. Cell Biol., 169, 219–225.

    Article  PubMed  CAS  Google Scholar 

  62. Osborne, A. R., and Rapoport, T. A. (2007) Cell, 129, 97–110.

    Article  PubMed  CAS  Google Scholar 

  63. Deville, K., Gold, V. A. M., Robson, A., Whitehouse, S., Sessions, R. B., Baldwin S. A., Radford, S. E., and Collinson, I. (2011) J. Biol. Chem., 286, 4659–4669.

    Article  PubMed  CAS  Google Scholar 

  64. Gold, V. A. M., Robson, A., Bao, H., Romantsov, T., Duong, F., and Collinson, I. (2010) Proc. Natl. Acad. Sci. USA, 107, 10044–10049.

    Article  PubMed  CAS  Google Scholar 

  65. Das, S., and Oliver, L. B. (2011) J. Biol. Chem., 286, 12371–12380.

    Article  PubMed  CAS  Google Scholar 

  66. Douville, K., Price, A., Eichler, J., Economou, A., and Wickner, W. (1995) J. Biol. Chem., 270, 20106–20111.

    Article  PubMed  CAS  Google Scholar 

  67. Chiba, K., Mori, H., and Ito, K. (2002) J. Bacteriol., 184, 2243–2250.

    Article  PubMed  CAS  Google Scholar 

  68. Mori, H., and Ito, K. (2001) Proc. Natl. Acad. Sci. USA, 98, 5128–5133.

    Article  PubMed  CAS  Google Scholar 

  69. Mori, H., and Ito, K. (2006) Proc. Natl. Acad. Sci. USA, 103, 5128–5133.

    Article  CAS  Google Scholar 

  70. Van der Sluis, E. O., Nouwen, N., Koch, J., de Keyzer, J., van der Does, C., Tampe, R., and Driessen, A. J. M. (2006) J. Mol. Biol., 361, 839–849.

    Article  PubMed  CAS  Google Scholar 

  71. Karamanou, S., Bariami, V., Papanikou, E., Kalodimos, C. G., and Economou, A. (2008) Mol. Microbiol., 70, 311–322.

    Article  PubMed  CAS  Google Scholar 

  72. Tam, P. C., Maillard, A. P., Chan, K. K., and Duong, F. (2005) EMBO J., 24, 3380–3388.

    Article  PubMed  CAS  Google Scholar 

  73. Pogliano, J. A., and Beckwith, J. (1994) EMBO J., 13, 554–561.

    PubMed  CAS  Google Scholar 

  74. Pogliano, K. J., and Beckwith, J. (1994) J. Bacteriol., 176, 804–814.

    PubMed  CAS  Google Scholar 

  75. Tsukazaki, T., Mori, H., Echizen, Y., Ishitani, R., Fukai, S., Tanaka, T., Perederina, A., Vassylyev, D. G., Kohno, T., Maturana, A. D., Ito, K., and Nureki, O. (2011) Nature, 474, 235–238.

    Article  PubMed  CAS  Google Scholar 

  76. Rapoport, T. A. (2007) Nature, 450, 663–668.

    Article  PubMed  CAS  Google Scholar 

  77. Du Plessis, D. J. F., Nouwen, N., and Drissen, A. J. M. (2011) Biochim. Biophys. Acta, 1808, 851–865.

    Article  PubMed  CAS  Google Scholar 

  78. Musial-Siwek, M., Rusch, S. L., and Kendall, D. A. (2006) J. Mol. Biol., 365, 637–648.

    Article  PubMed  CAS  Google Scholar 

  79. Van Dalen, A., Killian, A., and de Kruijff, B. (1999) J. Biol. Chem., 274, 19913–19918.

    Article  PubMed  Google Scholar 

  80. Nouwen, N., Tommassen, J., and de Kruijff, B. (1994) J. Biol. Chem., 269, 16029–16033.

    PubMed  CAS  Google Scholar 

  81. Schiebel, E., Driessen, A. J., Hartl, F. U., and Wickner, W. (1991) Cell, 64, 927–939.

    Article  PubMed  CAS  Google Scholar 

  82. Van der Wolk, J. P. W., de Wit, J. G., and Driessen, A. J. M. (1997) EMBO J., 16, 7297–7304.

    Article  PubMed  Google Scholar 

  83. Tomkiewicz, D., Nouwen, N., van Leeuwen, R., Tans, S., and Driessen, A. J. M. (2006) J. Biol. Chem., 281, 15709–15713.

    Article  PubMed  CAS  Google Scholar 

  84. Plath, K., Mothes, W., Wilkinson, B. M., Stirling, C. J., and Rapoport, T. A. (1998) Cell, 94, 795–807.

    Article  PubMed  CAS  Google Scholar 

  85. Du Plessis, D. J. F., Berrelkamp, G., Nouwen, N., and Driessen, A. J. M. (2009) J. Biol. Chem., 284, 15805–15814.

    Article  PubMed  CAS  Google Scholar 

  86. Economou, A., and Wickner, W. (1994) Cell, 78, 835–843.

    Article  PubMed  CAS  Google Scholar 

  87. Kim, Y. J., Rajapandi, T., and Oliver, D. (1994) Cell, 78, 845–853.

    Article  PubMed  CAS  Google Scholar 

  88. Erlandson, K. J., Or, E., Osborne, A. R., and Rapoport, T. A. (2008) J. Biol. Chem., 283, 15709–15715.

    Article  PubMed  CAS  Google Scholar 

  89. Martin, A., Baker, T. A., and Sauer, R. T. (2008) Mol. Cell., 29, 441–450.

    Article  PubMed  CAS  Google Scholar 

  90. Liang, F.-C., Bageshwar, U. K., and Musser, S. M. (2009) Mol. Biol. Cell., 20, 4256–4266.

    Article  PubMed  CAS  Google Scholar 

  91. Dalbey, R. E., and Wickner, W. (1985) J. Biol. Chem., 260, 15925–15931.

    PubMed  CAS  Google Scholar 

  92. De Cock, Y., Schafer, U., Potgeter, M., Demel, R., Muller, M., and Tommassen, J. (1999) Eur. J. Biochem., 259, 96–103.

    Article  PubMed  Google Scholar 

  93. Harms, N., Koningstein, G., Dontje, W., Muller, M., Oudega, B., Luirink, J., and de Cock, H. (2001) J. Biol. Chem., 276, 18804–18811.

    Article  PubMed  CAS  Google Scholar 

  94. Schafer, U., Beck, K., and Muller, M. (1999) J. Biol. Chem., 274, 24567–24574.

    Article  PubMed  CAS  Google Scholar 

  95. Bulieris, P. V., Behrens, S., Holst, O., and Kleinschmidt, J. Y. (2003) J. Biol. Chem., 278, 9092–9099.

    Article  PubMed  CAS  Google Scholar 

  96. Walton, T. A., and Sousa, M. C. (2004) Mol. Cell., 15, 367–374.

    Article  PubMed  CAS  Google Scholar 

  97. Schlapschy, M., Dommel, M. K., Hadian, K., Fogarasi, M., Korndorfer, I. P., and Skerra, A. (2004) Biol. Chem., 385, 137–143.

    Article  PubMed  CAS  Google Scholar 

  98. Korndorfer, I. P., Dommel, M. K., and Skerra, A. (2004) Nat. Struct. Mol. Biol., 11, 1015–1020.

    Article  PubMed  CAS  Google Scholar 

  99. Walton, T. A., Sandoval, C. M., Fowler, C. A., Pardi, A., and Sousa, M. C. (2009) Proc. Natl. Acad. Sci. USA, 106, 1772–1777.

    Article  PubMed  CAS  Google Scholar 

  100. Tormo, A., Almiron, M., and Kolter, R. (1990) J. Bacteriol., 172, 4339–4347.

    PubMed  CAS  Google Scholar 

  101. Bitto, E., and McKay, D. B. (2002) Structure, 10, 1489–1498.

    Article  PubMed  CAS  Google Scholar 

  102. Bitto, E., and McKay, D. B. (2003) J. Biol. Chem., 278, 49316–49322.

    Article  PubMed  CAS  Google Scholar 

  103. Hennecke, G., Nolte, J., Volkmer-Engert, R., Schneider-Mergener, J., and Behrens, S. (2005) J. Biol. Chem., 280, 23540–23548.

    Article  PubMed  CAS  Google Scholar 

  104. Xu, X., Wang, S., Hu, Y. X., and McKay, D. B. (2007) J. Mol. Biol., 373, 367–381.

    Article  PubMed  CAS  Google Scholar 

  105. Webb, H. M., Ruddock, L. W., Marchant, R. J., Jonas, K., and Klappa, P. (2001) J. Biol. Chem., 276, 45622–45627.

    Article  PubMed  CAS  Google Scholar 

  106. Rouviere, P. E., and Gross, C. A. (1996) Genes Dev., 10, 3170–3182.

    Article  PubMed  CAS  Google Scholar 

  107. Sklar, J. G., Wu, T., Kahne, D., and Silhavy, T. J. (2007) Genes Dev., 21, 2473–2484.

    Article  PubMed  CAS  Google Scholar 

  108. Fanning, A. S., and Anderson, J. M. (1999) J. Clin. Invest., 103, 767–772.

    Article  PubMed  CAS  Google Scholar 

  109. Jiang, J., Zhang, X., Chen, Y., Wu, Y., Zhou, H., Chang, Z., and Sui, S.-F. (2008) Proc. Natl. Acad. Sci. USA, 105, 11939–11944.

    Article  PubMed  CAS  Google Scholar 

  110. Krojer, T., Sawa, J., Schafer, E., Saibil, H. R., Ehrman, M., and Clausen, T. (2008) Nature, 453, 885–890.

    Article  PubMed  CAS  Google Scholar 

  111. De Cock, H., Hendriks, R., de Vrije, T., and Tommassen, J. (1990) J. Biol. Chem., 265, 4646–4651.

    PubMed  Google Scholar 

  112. Rizzitello, A. E., Harper, J. R., and Silhavy, T. J. (2001) J. Bacteriol., 183, 6794–6800.

    Article  PubMed  CAS  Google Scholar 

  113. Wu, S., Ge, X., Lu, Z., Zhi, Z., Chang, Z., and Zhao, X. S. (2011) Biochem. J., 438, 505–511.

    PubMed  CAS  Google Scholar 

  114. Bos, M. P., Robert, V., and Tommassen, J. (2007) Annu. Rev. Microbiol., 61, 191–214.

    Article  PubMed  CAS  Google Scholar 

  115. Walther, D. M., Rapaport, D., and Tommassen, J. (2009) Cell Mol. Life Sci., 66, 2789–2804.

    Article  PubMed  CAS  Google Scholar 

  116. Voulhoux, R., Bos, M., Geurtsen, J., Mois, M., and Tommassen, J. (2003) Science, 299, 262–265.

    Article  PubMed  CAS  Google Scholar 

  117. Voulhoux, R., and Tommassen, J. (2004) Res. Microbiol., 155, 129–135.

    Article  PubMed  CAS  Google Scholar 

  118. Doerrier, W. T., and Raetz, C. R. H. (2005) J. Biol. Chem., 280, 27679–27687.

    Article  CAS  Google Scholar 

  119. Tashiro, Y., Nomura, N., Nakao, R., Senpuku, H., Kariyama, R., Kumon, H., Kosono, S., Watanabe, H., Nakajima, T., and Uchiyama, H. (2008) J. Bacteriol., 190, 3969–3978.

    Article  PubMed  CAS  Google Scholar 

  120. Gentel, I. E., Burri, L., and Lithgow, T. (2005) Mol. Microbiol., 58, 1216–1225.

    Article  CAS  Google Scholar 

  121. Wu, T., Malinverni, J., Ruiz, N., Kim, S., Silhavy, T. J., and Kahne, D. (2005) Cell, 121, 235–245.

    Article  PubMed  CAS  Google Scholar 

  122. Sklar, J. G., Wu, T., Gronenberg, L. S., Malinverni, J. C., Kahne, D., and Silhavy, T. J. (2007) Proc. Natl. Acad. Sci. USA, 104, 6400–6404.

    Article  PubMed  CAS  Google Scholar 

  123. Gatsos, X., Perry, A. J., Anwari, K., Dolezal, P., Wolynec, P. P., Likic, V. F., Purcell, A. W., Buchanan, S. K., and Lithgow, T. (2008) FEMS Microbiol. Rev., 32, 995–1009.

    Article  PubMed  CAS  Google Scholar 

  124. Volokhina, E. B., Beckers, F., Tommassen, J., and Bos, M. P. (2009) J. Bacteriol., 191, 7074–7085.

    Article  PubMed  CAS  Google Scholar 

  125. Fardini, Y., Trotereau, J., Bottrearu, E., Souchard, C., Velge, P., and Virlogeux-Payant, I. (2009) Microbiology, 155, 1613–1622.

    Article  PubMed  CAS  Google Scholar 

  126. Hagan, C. L., Kim, S., and Kahne, D. (2010) Science, 328, 890–892.

    Article  PubMed  CAS  Google Scholar 

  127. Stegmeier, J. F., and Andersen, C. (2006) J. Biochem., 140, 275–283.

    Article  PubMed  CAS  Google Scholar 

  128. Robert, V., Volokhina, E. B., Senf, F., Bos, M. P., Van Gelder, P., and Tommassen, J. (2006) PLoS Biol., 4, 1984–1995.

    Article  CAS  Google Scholar 

  129. Struyve, M., Moons, M., and Tommassen, J. (1991) J. Mol. Biol., 218, 141–148.

    Article  PubMed  CAS  Google Scholar 

  130. De Cock, H., Struyve, M., Kleerebezem, M., van der Krift, T., and Tommassen, J. (1997) J. Mol. Biol., 269, 473–478.

    Article  PubMed  Google Scholar 

  131. Sanchez-Pulido, L., Devos, D., Genevrois, S., Vicente, M., and Valencia, A. (2003) Trends Biochem. Sci., 28, 523–526.

    Article  PubMed  CAS  Google Scholar 

  132. Bos, V. P., Robert, V., and Tommassen, J. (2007) EMBO Rep., 8, 1149–1154.

    Article  PubMed  CAS  Google Scholar 

  133. Kim, S., Malinverni, J. C., Sliz, P., Silhavy, T. J., Harrison, S. C., and Kahne, D. (2007) Science, 317, 961–964.

    Article  PubMed  CAS  Google Scholar 

  134. Gatzeva-Topalova, P. Z., Walton, T. A., and Sousa, M. C. (2008) Structure, 16, 1873–1881.

    Article  PubMed  CAS  Google Scholar 

  135. Knowles, T. J., Jeeves, M., Bobat, S., Dancea, F., McClelland, D., Palmer, T., Overduin, M., and Henderson, I. R. (2008) Mol. Microbiol., 68, 1216–1227.

    Article  PubMed  CAS  Google Scholar 

  136. Jacob-Dubuisson, F., Villert, V., Clantin, B., Delattre, A. S., and Saint, N. (2009) Biol. Chem., 390, 675–684.

    Article  PubMed  CAS  Google Scholar 

  137. Hagan, C. L., Silhavy, T. J., and Kahne, D. (2011) Annu. Rev. Biochem., 80, 189–210.

    Article  PubMed  CAS  Google Scholar 

  138. Bos, M. P., and Tommassen, J. (2004) Curr. Opin. Microbiol., 7, 610–616.

    Article  PubMed  CAS  Google Scholar 

  139. Walther, D. M., Papic, D., Bos, M. P., Tommassen, J., and Rapaport, D. (2009) Proc. Natl. Acad. Sci. USA, 106, 2531–2536.

    Article  PubMed  CAS  Google Scholar 

  140. Walther, D. M., Bos, M. P., Rapaport, D., and Tommassen, J. (2010) Mol. Biol. Evol., 27, 887–895.

    Article  PubMed  CAS  Google Scholar 

  141. Hsu, S.-C., and Inoue, K. (2009) Biosci. Trends, 3, 168–178.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. F. Solov’eva.

Additional information

Original Russian Text © T. F. Solov’eva, O. D. Novikova, O. Yu. Portnyagina, 2012, published in Biokhimiya, 2012, Vol. 77, No. 11, pp. 1459–1477.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Solov’eva, T.F., Novikova, O.D. & Portnyagina, O.Y. Biogenesis of β-barrel integral proteins of bacterial outer membrane. Biochemistry Moscow 77, 1221–1236 (2012). https://doi.org/10.1134/S0006297912110016

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297912110016

Key words

Navigation