Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Structure of the outer membrane protein A transmembrane domain

Nature Structural Biology volume 5, pages 1013–1017 (1998)Cite this article

Abstract

The outer membrane protein A of Escherichia coli (OmpA) is an intensely studied example in the field of membrane protein folding. We have determined the structure of the OmpA transmembrane domain consisting of residues 1–171, by X-ray diffraction analysis, to a resolution of 2.5 Å. It consists of a regular, extended eight-stranded ß-barrel and appears to be constructed like an inverse micelle with large water-filled cavities, but does not form a pore. Surprisingly, the cavities seem to be highly conserved during evolution. The structure corroborates the concept that all outer membrane proteins consist of ß-barrels. The structure constitutes a ß-barrel membrane anchor that appears to be the outer membrane equivalent of the single-chain α-helix anchor of the inner membrane.

Access through your institution
Buy or subscribe

This is a preview of subscription content, access via your institution

Access options

Access through your institution

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Structure of the OmpA transmembrane domain.
Figure 2
Figure 3: Topology sketch of OmpA171 as viewed from the barrel exterior.
Figure 4: Stereoviews of the internal architecture of OmpA171.
Figure 5: Sequence alignment of the transmembrane domain of the outer membrane protein A of E. coli (OmpA171 numbering) with five homologues found with FASTA in the EMBL Data Bank.

Similar content being viewed by others

Accession codes

Accessions

Protein Data Bank

References

  1. Deisenhofer, J., Epp, O., Miki, K., Huber, R. & Michel, H. Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å. Nature 318, 618–624( 1985).

    Article  CAS  Google Scholar 

  2. Weiss, M.S., Wacker, T., Weckesser, J., Welte, W. & Schulz, G.E. The three dimensional structure of porin from Rhodobacter capsulatus at 3 Å resolution. FEBS Lett. 267, 268–272( 1990).

    Article  CAS  Google Scholar 

  3. Sonntag, I., Schwarz, H., Hirota, Y. & Henning, U. Cell envelope and shape of Escherichia coli :Multiple mutants missing the outer membrane lipoprotein and other major outer membrane proteins. J. Bacteriol. 136, 280–285( 1978).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Ried, G. & Henning, U. A unique amino acid substitution in the outer membrane protein OmpA causes conjugation deficiency in Escherichia coli K12. FEBS Lett. 223, 387– 390(1987).

    Article  CAS  Google Scholar 

  5. Morona, R., Krämer, C. & Henning, U. Bacteriophage receptor area of outer membrane protein OmpA of Escherichia coli K-12. J. Bacteriol. 164, 539–543(1985).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Foulds, J. & Barrett, C. Characterization of Escherichia coli mutants tolerant to bacteriocin JF246: Two new classes of tolerant mutants. J. Bacteriol. 116, 885– 892(1973).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Weiser, J.N. & Gotschlich, E.C. Outer membrane protein A (OmpA) contributes to serum resistance and pathogenicity of Escherichia coli K-1. Infect. Immun. 59, 2252– 2258(1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Prasadarao, N.V. et al. Outer membrane protein A of Escherichia coli contributes to invasion of brain microvascular endothelial cells. Infect. Immun. 64, 146–153( 1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Kleinschmidt, J.H. & Tamm, L.K. Folding intermediates of a ß-barrel membrane protein. Kinetic evidence for a multi-step membrane insertion mechanism. Biochemistry 35, 12993 –13000(1996).

    Article  CAS  Google Scholar 

  10. Freudl, R., Klose, M. & Henning, U. Export and sorting of the Escherichia coli outer membrane protein OmpA. J. Bioenerget. Biomemb. 22, 441–449(1990).

    Article  CAS  Google Scholar 

  11. Vogel, H. & Jähnig, F. Models for the structure of outer membrane proteins of Escherichia coli derived from Raman spectroscopy and prediction methods. J. Mol. Biol. 190, 191–199(1986).

    Article  CAS  Google Scholar 

  12. Klose, M., MacIntyre, S., Schwarz, H. & Henning, U. The influence of amino acid substitutions within the mature part of an Escherichia coli outer membrane protein (OmpA) on assembly of the polypeptide into its membrane. J. Biol. Chem. 263, 13297 –13302(1988).

    CAS  PubMed  Google Scholar 

  13. Rodionova, N.A., Tatulian, S.A., Surrey, T., Jähnig, F. & Tamm, L.K. Characterization of two membrane-bound forms of OmpA. Biochemistry 34, 1921– 1929(1995).

    Article  CAS  Google Scholar 

  14. Sugawara, E., Steiert, M., Rouhani, S. & Nikaido, H. Secondary structure of outer membrane proteins OmpA of Escherichia coli and OprF of Pseudomonas aeruginosa. J. Bacteriol. 178, 6067– 6069(1996).

    Article  CAS  Google Scholar 

  15. Ried, G., Koebnik, R., Hindennach, I., Mutschler, B. & Henning, U. Membrane topology and assembly of the outer membrane protein OmpA of Escherichia coli K12. Mol. Gen. Genet. 243, 127–135(1994).

    CAS  PubMed  Google Scholar 

  16. Koebnik, R. & Krämer, L. Membrane assembly of circularly permuted variants of the E. coli outer membrane protein OmpA. J. Mol. Biol. 250, 617–626(1995).

    Article  CAS  Google Scholar 

  17. Sugawara, E. & Nikaido, H. Pore forming activity of OmpA protein of Escherichia coli. J. Biol. Chem. 267, 2507–2511(1992).

    CAS  PubMed  Google Scholar 

  18. Saint, N., De, E., Julien, S., Orange, N. & Molle, G. Ionophore properties of OmpA of Escherichia coli. Biochim. Biophys. Acta 1145, 119–123 (1993).

    Article  CAS  Google Scholar 

  19. Sugawara, E. & Nikaido, H. OmpA protein of Escherichia coli outer membrane occurs in open and closed channel forms. J. Biol. Chem. 269, 17981–17987(1994).

    CAS  PubMed  Google Scholar 

  20. Stathopoulos, C. An alternative topological model for Escherichia coli OmpA. Protein Sci. 5, 170–173( 1996).

    Article  CAS  Google Scholar 

  21. Pautsch, A., Vogt, J., Model, K., Siebold, C. & Schulz, G.E. Strategy for membrane protein crystallization exemplied with OmpA and OmpX. Proteins: Struct. Funct. Genet., in the press.

  22. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283– 291(1993).

    Article  CAS  Google Scholar 

  23. Liu, W.-M. Shear numbers of protein ß-barrels: Definition, refinements and statistics. J. Mol. Biol. 275, 541– 545 (1998).

    Article  CAS  Google Scholar 

  24. Schulz, G.E. Porins: general to specific, native to engineered passive pores. Curr. Opin. Struct. Biol. 6, 485–490 (1996).

    Article  CAS  Google Scholar 

  25. Meyer, J.E.W., Hofnung, M. & Schulz, G.E. Structure of maltoporin from Salmonella typhimurium ligated with a nitrophenyl-maltotrioside. J. Mol. Biol. 226, 761–775 (1997).

    Article  Google Scholar 

  26. Benz, R. & Bauer, K. Permeation of hydrophilic molecules through the outer membrane of gram-negative bacteria. Eur. J. Biochem. 176, 1–19(1988 ).

    Article  CAS  Google Scholar 

  27. Koebnik, R. Proposal for a peptidoglycan associating alpha-helical motif in the C-terminal regions of some bacterial cell-surface proteins. Mol. Microbiol. 16, 1269–1270 ( 1995).

    Article  CAS  Google Scholar 

  28. Song, L., et al. Structure of staphylococcal α-hemolysin, a heptameric transmembrane pore. Science 274, 1859– 1866 (1996).

    Article  CAS  Google Scholar 

  29. Guo, X.W., et al. Molecular design of the voltage-dependent anion-selective channel in the mitochondrial outer membrane. J. Struct. Biol. 114, 41–49 (1995).

    Article  CAS  Google Scholar 

  30. Rost, B. Marrying structure and genomics. Structure 6, 259–263 (1998).

    Article  CAS  Google Scholar 

  31. Kabsch, W. Evaluation of single-crystal X-ray diffraction data from a position-sensitive detector. J. Appl. Crystallogr. 21, 916– 924 (1988).

    Article  CAS  Google Scholar 

  32. Collaborative Computational Project No.4, Acta Crystallogr. D 50, 760–763 (1994).

  33. De la Fortelle, E. & Bricogne, G. Maximum likelihood heavy atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Meth. Enz.. 276, 472–494 (1997).

    Article  CAS  Google Scholar 

  34. Abrahams, J.P. & Leslie, A.G.W. Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr. D 52, 30– 42 (1996).

    Article  CAS  Google Scholar 

  35. Brünger, A.T. X-PLOR version 3.1 a system for X-ray crystallography and NMR (Yale Univ. Press, New Haven, 1993).

    Google Scholar 

  36. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. Refinement of protein structures by the maximum likelihood method. Acta Crystallogr. D 53, 240– 255 (1997).

    Article  CAS  Google Scholar 

  37. Connolly, M.L. The molecular surface package. J. Mol. Graph. 11, 139–141 (1993).

    Article  CAS  Google Scholar 

  38. Kraulis, P.J. MOLSCRIPT - a program to produce both detailed and schematic plots of proteins structures. J. Appl. Crystallogr. 24, 946 –950 (1991).

    Article  Google Scholar 

  39. Merritt, E.A. & Bacon, D.J. Raster3D: Photorealistic molecular graphics. Meth. Enz. 277, 505– 524(1997).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank U. Henning for providing us with the gene of OmpA171 and K. Model and C. Siebold for essential contributions during crystal production. The project was supported by the Sonderforschungsbereich-428.

Author information

Authors and Affiliations

  1. Institut für Organische Chemie und Biochemie, Albert-Ludwigs-Universität, Albertstrasse 21, Freiburg im Breisgau, D-79104, Germany

    Alex Pautsch & Georg E. Schulz

Authors
  1. Alex Pautsch
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Georg E. Schulz
    View author publications

    You can also search for this author inPubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pautsch, A., Schulz, G. Structure of the outer membrane protein A transmembrane domain. Nat Struct Mol Biol 5, 1013–1017 (1998). https://doi.org/10.1038/2983

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/2983

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing