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.
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
Koebnik, R., Locher, K. P., and Van Gelder, P. (2000) Mol. Microbiol., 37, 239–253.
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.
Chandran, V., Fronzes, R., Duquerroy, S., Cronin, N., Navaza, J., and Waksman, G. (2009) Nature, 462, 1011–1015.
Randall, L. L., Topping, T. B., Suciu, D., and Hardy, S. J. (1998) Prot. Sci., 7, 1195–1200.
Randall, L. L., Topping, T. B., and Hardy, S. J. (1990) Science, 248, 860–863.
Xu, Z., Knafels, J. D., and Yoshino, K. (2000) Nat. Struct. Biol., 7, 1172–1177.
Dekker, C., de Kruijff, B., and Gros, P. (2003) J. Struct. Biol., 144, 313–319.
Crane, J. M., Suo, Y., Lilly, A. A., Mao, C., Hubbell, W. L., and Randall, L. L. (2006) J. Mol. Biol., 363, 63–74.
Tang, Y., Pan, X., Tai, P. C., and Sui, S.-F. (2010) Biochem. Biophys. Res. Commun., 393, 698–702.
Lilly, A. A., Crane, J. M., and Randall, L. L. (2009) Protein Sci., 18, 1860–1868.
Randall, L. L., and Hardy, S. J. S. (1995) Trends Biochem. Sci., 20, 65–69.
Hartl, F. U., Lecker, S., Schiebel, E., Hendrick, J. P., and Wickner, W. (1990) Cell, 63, 269–279.
Zhou, J., and Xu, Z. (2003) Nat. Struct. Biol., 10, 942–947.
Cabelli, R. J., Dolan, K. V., Qian, L. P., and Oliver, D. B. (1991) J. Biol. Chem., 6, 24420–24427.
Lill, R., Dowhan, W., and Wickner, W. (1990) Cell, 60, 271–280.
Woodbury, R. L., Hardy, S. J. S., and Randall, L. L. (2002) Prot. Sci., 11, 875–882.
Zimmer, J., Li, W., and Rapoport, T. A. (2006) J. Mol. Biol., 364, 259–265.
Hunt, J. F., Weinkauf, S., Henry, L., Fak, J. J., McNicholas, P., Oliver, D. B., and Deisenhofer, J. (2002) Science, 297, 2018–2026.
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.
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.
Papanikolau, Y., Papadovasilaki, M., Ravelli, R. B., McCarthy, A. A., Cusack, S., Economou, A., and Petratos, K. (2007) J. Mol. Biol., 366, 1545–1557.
Driessen, A. J. M. (1993) Biochemistry, 32, 13190–13197.
Or, E., Navon, A., and Rapoport, T. A. (2002) EMBO J., 21, 4470–4479.
Duong, F. (2003) EMBO J., 22, 4375–4384.
Or, E., Boyd, D., Gon, S., Beckwith, J., and Rapoport, T. A. (2004) J. Biol. Chem., 280, 9097–9105.
Alami, M., Dalal, K., Lelj-Garolla, B., Sligar, S. G., and Duong, F. (2007) EMBO J., 26, 1995–2004.
Jilaveanu, L. B., Zito, C. L., and Oliver, D. (2005) Proc. Natl. Acad. Sci. USA, 102, 7511–7516.
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.
Mitra, K., Frank, J., and Driessen, A. (2006) Nature Struct. Mol. Biol., 13, 957–964.
Osborne, A. R., Clemons, W. M., and Rapoport, T. A. (2004) Proc. Natl. Acad. Sci. USA, 101, 10937–10942.
Caruthers, J. M., and McKay, D. B. (2002) Curr. Opin. Struct. Biol., 12, 123–133.
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.
Vrontou, E., Karamanou, S., Baud, C., Sianidis, G., and Economou, A. (2004) J. Biol. Chem., 279, 22490–22497.
Erlandson, K. J., Miller, S. B. M., Nam, Y., Osborne, A. R., Zimmer, J., and Rapoport, T. A. (2008) Nature, 455, 984–988.
Zimmer, J., Nam, Y., and Rapoport, T. A. (2008) Nature, 455, 936–943.
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.
Sianidis, G., Karamanou, S., Vrontou, E., Boulias, K., Repanas, K., Kyrpides, N., Politou, A. S., and Economou, A. (2001) EMBO J., 20, 961–970.
Karamanou, S., Vrontou, E., Sianidis, G., Baud, K., Roos, T., Kuhn, A., Politou, A. S., and Economou, A. (1999) Mol. Microbiol., 34, 1133–1145.
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.
Kimura, E., Akita, M., Matsuyama, S., and Mizushima, S. (1991) J. Biol. Chem., 266, 6600–6606.
Kourtz, L., and Oliver, D. (2002) Mol. Microbiol., 37, 1342–1356.
Van Voorst, F., Vereyken, I. J., and de Kruijff, B. (2000) FEBS Lett., 486, 57–62.
Morshauser, R. C., Hu, W., Wang, H., Pang, Y., Flynn, G. C., and Zuiderweg, E. R. (1999) J. Mol. Biol., 289, 1387–1403.
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.
Auclair, S. M., Moses, J. P., Musial-Siwek, M., Kendall, D. A., Oliver, D. B., and Mukerji, I. (2010) Biochemistry, 49, 782–792.
Brundage, L., Hendric, J. P., Schiebel, E., Driessen, A. J. M., and Wickner, W. (1990) Cell, 62, 649–657.
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.
Breyton, C., Haase, W., Rapoport, T. A., Kuhlbrandt, W., and Collinson, I. (2002) Nature, 418, 662–665.
Driessen, A. J. M., and Nouwen, N. (2008) Annu. Rev. Biochem., 77, 643–667.
Kihara, A., Akiyama, Y., and Ito, K. (1995) Proc. Natl. Acad. Sci. USA, 92, 4532–4536.
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.
Tani, K., Tokuda, H., and Mizushima, S. (1990) J. Biol. Chem., 265, 17341–17347.
Kowarik, M., Kung, S., Martoglio, B., and Helenius, A. (2002) Mol. Cell., 10, 769–778.
Meyer, T., Menetret, J., Breitling, R., Miller, K., Akey, C. W., and Rapoport, T. A. (1999) J. Mol. Biol., 285, 1789–1800.
Manting, E., van der Does, C., Remigy, H., Engel, A., and Driessen, A. (2000) EMBO J., 19, 852–861.
Yahr, T. L., and Wickner, W. T. (2000) EMBO J., 19, 4393–4401.
Bessonneau, P., Besson, V., Collinson, I., and Duong, F. (2002) EMBO J., 21, 995–1003.
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.
Boy, D., and Koch, H.-G. (2009) Mol. Biol. Cell., 20, 1804–1815.
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.
Cannon, K., Or, E., Clemons, W. M., Shibata, Y., and Rapoport, T. J. (2005) J. Cell Biol., 169, 219–225.
Osborne, A. R., and Rapoport, T. A. (2007) Cell, 129, 97–110.
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.
Gold, V. A. M., Robson, A., Bao, H., Romantsov, T., Duong, F., and Collinson, I. (2010) Proc. Natl. Acad. Sci. USA, 107, 10044–10049.
Das, S., and Oliver, L. B. (2011) J. Biol. Chem., 286, 12371–12380.
Douville, K., Price, A., Eichler, J., Economou, A., and Wickner, W. (1995) J. Biol. Chem., 270, 20106–20111.
Chiba, K., Mori, H., and Ito, K. (2002) J. Bacteriol., 184, 2243–2250.
Mori, H., and Ito, K. (2001) Proc. Natl. Acad. Sci. USA, 98, 5128–5133.
Mori, H., and Ito, K. (2006) Proc. Natl. Acad. Sci. USA, 103, 5128–5133.
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.
Karamanou, S., Bariami, V., Papanikou, E., Kalodimos, C. G., and Economou, A. (2008) Mol. Microbiol., 70, 311–322.
Tam, P. C., Maillard, A. P., Chan, K. K., and Duong, F. (2005) EMBO J., 24, 3380–3388.
Pogliano, J. A., and Beckwith, J. (1994) EMBO J., 13, 554–561.
Pogliano, K. J., and Beckwith, J. (1994) J. Bacteriol., 176, 804–814.
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.
Rapoport, T. A. (2007) Nature, 450, 663–668.
Du Plessis, D. J. F., Nouwen, N., and Drissen, A. J. M. (2011) Biochim. Biophys. Acta, 1808, 851–865.
Musial-Siwek, M., Rusch, S. L., and Kendall, D. A. (2006) J. Mol. Biol., 365, 637–648.
Van Dalen, A., Killian, A., and de Kruijff, B. (1999) J. Biol. Chem., 274, 19913–19918.
Nouwen, N., Tommassen, J., and de Kruijff, B. (1994) J. Biol. Chem., 269, 16029–16033.
Schiebel, E., Driessen, A. J., Hartl, F. U., and Wickner, W. (1991) Cell, 64, 927–939.
Van der Wolk, J. P. W., de Wit, J. G., and Driessen, A. J. M. (1997) EMBO J., 16, 7297–7304.
Tomkiewicz, D., Nouwen, N., van Leeuwen, R., Tans, S., and Driessen, A. J. M. (2006) J. Biol. Chem., 281, 15709–15713.
Plath, K., Mothes, W., Wilkinson, B. M., Stirling, C. J., and Rapoport, T. A. (1998) Cell, 94, 795–807.
Du Plessis, D. J. F., Berrelkamp, G., Nouwen, N., and Driessen, A. J. M. (2009) J. Biol. Chem., 284, 15805–15814.
Economou, A., and Wickner, W. (1994) Cell, 78, 835–843.
Kim, Y. J., Rajapandi, T., and Oliver, D. (1994) Cell, 78, 845–853.
Erlandson, K. J., Or, E., Osborne, A. R., and Rapoport, T. A. (2008) J. Biol. Chem., 283, 15709–15715.
Martin, A., Baker, T. A., and Sauer, R. T. (2008) Mol. Cell., 29, 441–450.
Liang, F.-C., Bageshwar, U. K., and Musser, S. M. (2009) Mol. Biol. Cell., 20, 4256–4266.
Dalbey, R. E., and Wickner, W. (1985) J. Biol. Chem., 260, 15925–15931.
De Cock, Y., Schafer, U., Potgeter, M., Demel, R., Muller, M., and Tommassen, J. (1999) Eur. J. Biochem., 259, 96–103.
Harms, N., Koningstein, G., Dontje, W., Muller, M., Oudega, B., Luirink, J., and de Cock, H. (2001) J. Biol. Chem., 276, 18804–18811.
Schafer, U., Beck, K., and Muller, M. (1999) J. Biol. Chem., 274, 24567–24574.
Bulieris, P. V., Behrens, S., Holst, O., and Kleinschmidt, J. Y. (2003) J. Biol. Chem., 278, 9092–9099.
Walton, T. A., and Sousa, M. C. (2004) Mol. Cell., 15, 367–374.
Schlapschy, M., Dommel, M. K., Hadian, K., Fogarasi, M., Korndorfer, I. P., and Skerra, A. (2004) Biol. Chem., 385, 137–143.
Korndorfer, I. P., Dommel, M. K., and Skerra, A. (2004) Nat. Struct. Mol. Biol., 11, 1015–1020.
Walton, T. A., Sandoval, C. M., Fowler, C. A., Pardi, A., and Sousa, M. C. (2009) Proc. Natl. Acad. Sci. USA, 106, 1772–1777.
Tormo, A., Almiron, M., and Kolter, R. (1990) J. Bacteriol., 172, 4339–4347.
Bitto, E., and McKay, D. B. (2002) Structure, 10, 1489–1498.
Bitto, E., and McKay, D. B. (2003) J. Biol. Chem., 278, 49316–49322.
Hennecke, G., Nolte, J., Volkmer-Engert, R., Schneider-Mergener, J., and Behrens, S. (2005) J. Biol. Chem., 280, 23540–23548.
Xu, X., Wang, S., Hu, Y. X., and McKay, D. B. (2007) J. Mol. Biol., 373, 367–381.
Webb, H. M., Ruddock, L. W., Marchant, R. J., Jonas, K., and Klappa, P. (2001) J. Biol. Chem., 276, 45622–45627.
Rouviere, P. E., and Gross, C. A. (1996) Genes Dev., 10, 3170–3182.
Sklar, J. G., Wu, T., Kahne, D., and Silhavy, T. J. (2007) Genes Dev., 21, 2473–2484.
Fanning, A. S., and Anderson, J. M. (1999) J. Clin. Invest., 103, 767–772.
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.
Krojer, T., Sawa, J., Schafer, E., Saibil, H. R., Ehrman, M., and Clausen, T. (2008) Nature, 453, 885–890.
De Cock, H., Hendriks, R., de Vrije, T., and Tommassen, J. (1990) J. Biol. Chem., 265, 4646–4651.
Rizzitello, A. E., Harper, J. R., and Silhavy, T. J. (2001) J. Bacteriol., 183, 6794–6800.
Wu, S., Ge, X., Lu, Z., Zhi, Z., Chang, Z., and Zhao, X. S. (2011) Biochem. J., 438, 505–511.
Bos, M. P., Robert, V., and Tommassen, J. (2007) Annu. Rev. Microbiol., 61, 191–214.
Walther, D. M., Rapaport, D., and Tommassen, J. (2009) Cell Mol. Life Sci., 66, 2789–2804.
Voulhoux, R., Bos, M., Geurtsen, J., Mois, M., and Tommassen, J. (2003) Science, 299, 262–265.
Voulhoux, R., and Tommassen, J. (2004) Res. Microbiol., 155, 129–135.
Doerrier, W. T., and Raetz, C. R. H. (2005) J. Biol. Chem., 280, 27679–27687.
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.
Gentel, I. E., Burri, L., and Lithgow, T. (2005) Mol. Microbiol., 58, 1216–1225.
Wu, T., Malinverni, J., Ruiz, N., Kim, S., Silhavy, T. J., and Kahne, D. (2005) Cell, 121, 235–245.
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.
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.
Volokhina, E. B., Beckers, F., Tommassen, J., and Bos, M. P. (2009) J. Bacteriol., 191, 7074–7085.
Fardini, Y., Trotereau, J., Bottrearu, E., Souchard, C., Velge, P., and Virlogeux-Payant, I. (2009) Microbiology, 155, 1613–1622.
Hagan, C. L., Kim, S., and Kahne, D. (2010) Science, 328, 890–892.
Stegmeier, J. F., and Andersen, C. (2006) J. Biochem., 140, 275–283.
Robert, V., Volokhina, E. B., Senf, F., Bos, M. P., Van Gelder, P., and Tommassen, J. (2006) PLoS Biol., 4, 1984–1995.
Struyve, M., Moons, M., and Tommassen, J. (1991) J. Mol. Biol., 218, 141–148.
De Cock, H., Struyve, M., Kleerebezem, M., van der Krift, T., and Tommassen, J. (1997) J. Mol. Biol., 269, 473–478.
Sanchez-Pulido, L., Devos, D., Genevrois, S., Vicente, M., and Valencia, A. (2003) Trends Biochem. Sci., 28, 523–526.
Bos, V. P., Robert, V., and Tommassen, J. (2007) EMBO Rep., 8, 1149–1154.
Kim, S., Malinverni, J. C., Sliz, P., Silhavy, T. J., Harrison, S. C., and Kahne, D. (2007) Science, 317, 961–964.
Gatzeva-Topalova, P. Z., Walton, T. A., and Sousa, M. C. (2008) Structure, 16, 1873–1881.
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.
Jacob-Dubuisson, F., Villert, V., Clantin, B., Delattre, A. S., and Saint, N. (2009) Biol. Chem., 390, 675–684.
Hagan, C. L., Silhavy, T. J., and Kahne, D. (2011) Annu. Rev. Biochem., 80, 189–210.
Bos, M. P., and Tommassen, J. (2004) Curr. Opin. Microbiol., 7, 610–616.
Walther, D. M., Papic, D., Bos, M. P., Tommassen, J., and Rapaport, D. (2009) Proc. Natl. Acad. Sci. USA, 106, 2531–2536.
Walther, D. M., Bos, M. P., Rapaport, D., and Tommassen, J. (2010) Mol. Biol. Evol., 27, 887–895.
Hsu, S.-C., and Inoue, K. (2009) Biosci. Trends, 3, 168–178.
Author information
Authors and Affiliations
Corresponding author
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
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
Received:
Revised:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0006297912110016