Identifying Assembly-Inhibiting and Assembly-Tolerant Sites in the SbsB S-Layer Protein from Geobacillus stearothermophilus

Journal of Molecular Biology

Volumn 395, Issue 4, 2010, Pages 742-753

  Kinns, Helen ^a   Badelt Lichtblau, Helga ^b   Egelseer, Eva Maria ^b   Sleytr, Uwe B ^b   Howorka, Stefan ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

bacterial exoprotein; electron microscopy; insertion mutagenesis; S layer; supramolecular assemblies

Indexed keywords

BACTERIAL PROTEIN; CYSTEINE; EPITOPE; HEMAGGLUTININ; MONOMER; SBSB PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPY; FLUORESCENCE; GEL PERMEATION CHROMATOGRAPHY; GEOBACILLUS STEAROTHERMOPHILUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SITE DIRECTED MUTAGENESIS; STRUCTURE ANALYSIS;

BACTERIA (MICROORGANISMS); GEOBACILLUS STEAROTHERMOPHILUS;

EID: 73649103420     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.10.012     Document Type: Article

References (66)

1. Yeates T.O., Kerfeld C.A., Heinhorst S., Cannon G.C., and Shively J.M. Protein-based organelles in bacteria: carboxysomes and related microcompartments. Nat. Rev. Microbiol. 6 (2008) 681-691
2. Sára M., and Sleytr U.B. S-layer proteins. J. Bacteriol. 182 (2000) 859-868
3. Baumeister W., and Engelhardt H. Three-dimensional structure of bacterial surface layers. In: Harris J.R., and Horne R.W. (Eds). Electron Microscopy of Proteins, Vol. 6, Membranous Structures (1987), Academic Press, London, UK 109-154
4. Sleytr U.B., Sára M., Pum D., Schuster B., Messner P., and Schäffer C. Self-assembling protein systems: microbial S-layers. In: Steinbüchel A., and Fahnestock S.R. (Eds). Biopolymers 7 (2002), Wiley-VCH, Weinheim, Germany 285-338
5. Calabi E., Ward S., Wren B., Paxton T., Panico M., Morris H., et al. Molecular characterization of the surface layer proteins from Clostridium difficile. Mol. Microbiol. 40 (2001) 1187-1199
6. Steiner K., Novotny R., Patel K., Vinogradov E., Whitfield C., Valvano M.A., et al. Functional characterization of the initiation enzyme of S-layer glycoprotein glycan biosynthesis in Geobacillus stearothermophilus NRS 2004/3a. J. Bacteriol. 189 (2007) 2590-2598
7. Voisin S., Houliston R.S., Kelly J., Brisson J.R., Watson D., Bardy S.L., et al. Identification and characterization of the unique N-linked glycan common to the flagellins and S-layer glycoprotein of Methanococcus voltae. J. Biol. Chem. 280 (2005) 16586-16593
8. Sleytr U.B., Messner P., Pum D., and Sára M. Crystalline bacterial cell surface layers (S layers): from supramolecular cell structure to biomimetics and nanotechnology. Angew. Chem., Int. Ed. 38 (1999) 1035-1054
9. Sleytr U.B., and Beveridge T.J. Bacterial S-layers. Trends Microbiol. 7 (1999) 253-260
10. Scheuring S., Stahlberg H., Chami M., Houssin C., Rigaud J.L., and Engel A. Charting and unzipping the surface layer of Corynebacterium glutamicum with the atomic force microscope. Mol. Microbiol. 44 (2002) 675-684
11. Ebner A., Kienberger F., Huber C., Kamruzzahan A.S.M., Pastushenko V.P., Tang J., et al. Atomic force microscopy imaging and molecular recognition force microscopy of recrystallized heterotetramers comprising an S-layer-streptavidin fusion protein. ChemBioChem 7 (2006) 588-591
12. Györvary E.S., Stein O., Pum D., and Sleytr U.B. Self-assembly and recrystallization of bacterial S-layer proteins at silicon supports imaged in real time by atomic force microscopy. J. Microsc. 212 (2003) 300-306
13. Engelhardt H., Saxton W.O., and Baumeister W. Three-dimensional structure of the tetragonal surface layer of Sporosarcina ureae. J. Bacteriol. 168 (1986) 309-317
14. Hovmöller S. Crystallographic image processing applications for S-layers. In: Beveridge T.J., and Kovel S.F. (Eds). Advances in Bacterial Paracrystalline Surface Layers (1993), Plenum Press, New York, NY 13-21
15. Engelhardt H., and Peters J. Structural research on surface layers: a focus on stability, surface layer homology domains, and surface layer-cell wall interactions. J. Struct. Biol. 124 (1998) 276-302
16. Pum D., Messner P., and Sleytr U.B. Role of the S layer in morphogenesis and cell division of the archaebacterium Methanocorpusculum sinense. J. Bacteriol. 173 (1991) 6865-6873
17. Sára M., and Sleytr U.B. Molecular sieving through S layers of Bacillus stearothermophilus strains. J. Bacteriol. 169 (1987) 4092-4098
18. Egelseer E., Schocher I., Sára M., and Sleytr U.B. The S-layer from Bacillus stearothermophilus DSM 2358 functions as an adhesion site for a high-molecular-weight amylase. J. Bacteriol. 177 (1995) 1444-1451
19. Ford M.J., Nomellini J.F., and Smit J. S-layer anchoring and localization of an S-layer-associated protease in Caulobacter crescentus. J. Bacteriol. 189 (2007) 2226-2237
20. Ferner-Ortner-Bleckmann J., Huber-Gries C., Pavkov T., Keller W., Mader C., Ilk N., et al. The high-molecular-mass amylase (HMMA) of Geobacillus stearothermophilus ATCC 12980 interacts with the cell wall components by virtue of three specific binding regions. Mol. Microbiol. 72 (2009) 1448-1461
21. Calabi E., Calabi F., Phillips A.D., and Fairweather N. Binding of Clostridium difficile surface layer proteins to gastrointestinal tissues. Infect. Immun. 70 (2002) 5770-5778
22. Noonan B., and Trust T.J. The synthesis, secretion and role in virulence of the paracrystalline surface protein layers of Aeromonas salmonicida and A. hydrophila. FEMS Microbiol. Lett. 154 (1997) 1-7
23. Konstantinov S.R., Smidt H., de Vos W.M., Bruijns S.C.M., Singh S.K., Valence F., et al. S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proc. Natl Acad. Sci. USA 105 (2008) 19474-19479
24. Blaser M.J., Wang E., Tummuru M.K., Washburn R., Fujimoto S., and Labigne A. High-frequency S-layer protein variation in Campylobacter fetus revealed by sapA mutagenesis. Mol. Microbiol. 14 (1994) 453-462
25. Sleytr U.B., Egelseer E., Pum D., and Schuster B. S-layers. In: Niemeyer C.M., and Mirkin C.A. (Eds). Nanobiotechnology (2004), Wiley-VCH, Weinheim, Germany 77-92
26. Sleytr U.B., Huber C., Ilk N., Pum D., Schuster B., and Egelseer E.M. S-layers as a tool kit for nanobiotechnological applications. FEMS Microbiol. Lett. 267 (2007) 131-144
27. Liu J., Mao Y., Lan E., Banatao D.R., Forse G.J., Blom H.O., et al. Generation of oxide nanopatterns by combining self-assembly of S-layer proteins and area-selective atomic layer deposition. J. Am. Chem. Soc. 130 (2008) 16908-16913
28. Papapostolou D., and Howorka S. Engineering and exploiting protein assemblies in synthetic biology. Mol. BioSyst. 5 (2009) 723-732
29. Howorka S. Creating regular arrays of nanoparticles with self-assembling protein building blocks. J. Mater. Chem. 17 (2007) 2049-2053
30. Rünzler D., Huber C., Moll D., Köhler G., and Sára M. Biophysical characterization of the entire bacterial surface layer protein SbsB and its two distinct functional domains. J. Biol. Chem. 279 (2004) 5207-5215
31. Thomas S., Austin J.W., McCubbin W.D., Kay C.M., and Trust T.J. Roles of structural domains in the morphology and surface anchoring of the tetragonal paracrystalline array of Aeromonas hydrophila. Biochemical characterization of the major structural domain. J. Mol. Biol. 228 (1992) 652-661
32. Lupas A., Engelhardt H., Peters J., Santarius U., Volker S., and Baumeister W. Domain structure of the Acetogenium kivui surface layer revealed by electron crystallography and sequence analysis. J. Bacteriol. 176 (1994) 1224-1233
33. Huber C., Ilk N., Rünzler D., Egelseer E.M., Weigert S., Sleytr U.B., and Sára M. The three S-layer-like homology motifs of the S-layer protein SbpA of Bacillus sphaericus CCM 2177 are not sufficient for binding to the pyruvylated secondary cell wall polymer. Mol. Microbiol. 55 (2005) 197-205
34. Smit E., Jager D., Martinez B., Tielen F.J., and Pouwels P.H. Structural and functional analysis of the S-layer protein crystallisation domain of Lactobacillus acidophilus ATCC 4356: evidence for protein-protein interaction of two subdomains. J. Mol. Biol. 324 (2002) 953-964
35. Bingle W.H., Nomellini J.F., and Smit J. Cell-surface display of a Pseudomonas aeruginosa strain K pilin peptide within the paracrystalline S-layer of Caulobacter crescentus. Mol. Microbiol. 26 (1997) 277-288
36. Pavkov T., Egelseer E.M., Tesarz M., Svergun D.I., Sleytr U.B., and Keller W. The structure and binding behavior of the bacterial cell surface layer protein SbsC. Structure 16 (2008) 1226-1237
37. Stetefeld J., Jenny M., Schulthess T., Landwehr R., Engel J., and Kammerer R.A. Crystal structure of a naturally occurring parallel right-handed coiled coil tetramer. Nat. Struct. Biol. 7 (2000) 772-776
38. Norville J.E., Kelly D.F., Knight T.F.J., Belcher A.M., and Walz T. 7A projection map of the S-layer protein sbpA obtained with trehalose-embedded monolayer crystals. J. Struct. Biol. 160 (2007) 313-323
39. Fagan R.P., Qazi O., Svergun D.I., Brown K.A., and Fairweather N. Structural insights into the molecular organization of the S-layer from Clostridium difficile. Mol. Microbiol. 71 (2009) 1308-1322
40. Rosenbaum D.M., Cherezov V., Hanson M.A., Rasmussen S.G.F., Thian F.S., Kobilka T.S., et al. GPCR engineering yields high-resolution structural insights into beta2-adrenergic receptor function. Science 318 (2007) 1266-1273
41. Lisal J., Lam T.T., Kainov D.E., Emmett M.R., Marshall A.G., and Tuma R. Functional visualization of viral molecular motor by hydrogen-deuterium exchange reveals transient states. Nat. Struct. Mol. Biol. 12 (2005) 460-466
42. Lanman J., and Prevelige Jr. P.E. High-sensitivity mass spectrometry for imaging subunit interactions: hydrogen/deuterium exchange. Curr. Opin. Struct. Biol. 14 (2004) 181-188
43. Sára M., Pum D., Küpcü S., Messner P., and Sleytr U.B. Isolation of two physiologically induced variant strains of Bacillus stearothermophilus NRS 2004/3a and characterization of their S-layer lattices. J. Bacteriol. 176 (1994) 848-860
44. Sára M., Kuen B., Mayer H.F., Mandl F., Schuster K.C., and Sleytr U.B. Dynamics in oxygen-induced changes in S-layer protein synthesis from Bacillus stearothermophilus PV72 and the S-layer-deficient variant T5 in continuous culture and studies of the cell wall composition. J. Bacteriol. 178 (1996) 2108-2117
45. Kuen B., Koch A., Asenbauer E., Sára M., and Lubitz W. Molecular characterization of the Bacillus stearothermophilus PV72 S-layer gene sbsB induced by oxidative stress. J. Bacteriol. 179 (1997) 1664-1670
46. Moll D., Huber C., Schlegel B., Pum D., Sleytr U.B., and Sára M. S-layer-streptavidin fusion proteins as template for nanopatterned molecular arrays. Proc. Natl Acad. Sci. USA 99 (2002) 14646-14651
47. Sára M., Egelseer E.M., Dekitsch C., and Sleytr U.B. Identification of two binding domains, one for peptidoglycan and another for a secondary cell wall polymer on the N-terminal part of the S-layer protein SbsB from Bacillus stearothermophilus PV72/p2. J. Bacteriol. 180 (1998) 6780-6783
48. Mader C., Huber C., Moll D., Sleytr U.B., and Sara M. Interaction of the crystalline bacterial cell surface layer protein SbsB and the secondary cell wall polymer of Geobacillus stearothermophilus PV72 assessed by real-time surface plasmon resonance biosensor technology. J. Bacteriol. 186 (2004) 1758-1768
49. Howorka S., Sára M., Wang Y., Kuen B., Sleytr U.B., Lubitz W., and Bayley H. Surface accessible residues in the monomeric and assembled form of a bacterial surface layer protein. J. Biol. Chem. 275 (2000) 37876-37886
50. Kinns H., and Howorka S. The surface location of individual residues in a bacterial S-layer protein. J. Mol. Biol. 377 (2008) 589-604
51. Tasdemir A., Khan F., Jowitt T.A., Iuzzolino L., Lohmer S., Corazza S., and Schmidt T.J. Engineering of a monomeric fluorescent protein AsGFP(499) and its applications in a dual translocation and transcription assay. Protein Eng. Des. Sel. 21 (2008) 613-622
52. Pajunen M., Turakainen H., Poussu E., Peranen J., Vihinen M., and Savilahti H. High-precision mapping of protein-protein interfaces: an integrated genetic strategy combining en masse mutagenesis and DNA-level parallel analysis on a yeast two-hybrid platform. Nucleic Acids Res. e103 (2007) 35
53. Carreira A., Menendez M., Reguera J., Almendral J.M., and Mateu M.G. In vitro disassembly of a parvovirus capsid and effect on capsid stability of heterologous peptide insertions in surface loops. J. Biol. Chem. 279 (2004) 6517-6525
54. Jala V.R., Rao N.A., and Savithri H.S. Identification of amino acid residues, essential for maintaining the tetrameric structure of sheep liver cytosolic serine hydroxymethyltransferase, by targeted mutagenesis. Biochem. J. 369 (2003) 469-476
55. Taylor D.J., and Johnson J.E. Folding and particle assembly are disrupted by single-point mutations near the autocatalytic cleavage site of Nudaurelia capensis omega virus capsid protein. Protein Sci. 14 (2005) 401-408
56. Gerstmayr M., Ilk N., Schabussova I., Jahn-Schmid B., Egelseer E.M., Sleytr U.B., et al. A novel approach to specific allergy treatment: the recombinant allergen-S-layer fusion protein rSbsC-Bet v 1 matures dendritic cells that prime Th0/Th1 and IL-10-producing regulatory T cells. J. Immunol. 179 (2007) 7270-7275
57. Tang J., Ebner A., Ilk N., Lichtblau H., Huber C., Zhu R., et al. High-affinity tags fused to S-layer proteins probed by atomic force microscopy. Langmuir 24 (2008) 1324-1329
58. Banerjee A., and Swaan P.W. Membrane topology of human ASBT (SLC10A2) determined by dual label epitope insertion scanning mutagenesis. New evidence for seven transmembrane domains. Biochemistry 45 (2006) 943-953
59. Canfield V.A., Norbeck L., and Levenson R. Localization of cytoplasmatic and extracellular domains of Na,K-ATPase by epitope tag insertion. Biochemistry 35 (1996) 14165-14172
60. Kast C., and Gros P. Epitope insertion favors a six transmembrane domain model for the carboxy-terminal portion of the multidrug resistance-associated protein. Biochemistry 37 (1998) 2305-2313
61. Andrade M.A., Chacon P., Merelo J.J., and Moran F. Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network. Protein Eng. 6 (1993) 383-390
62. Waldo G.S., Standish B.M., Berendzen J., and Terwilliger T.C. Rapid protein-folding assay using green fluorescent protein. Nat. Biotechnol. 17 (1999) 691-695
63. Howorka S., and Bayley H. High-throughput scanning mutagenesis by recombination PCR. In: Braman J. (Ed). In Vitro Mutagenesis Protocols (Methods in Molecular Biology) (2002), Humana Press, Totowa, NJ 139-147
64. Howorka S., and Bayley H. Improved protocol for high-throughput cysteine scanning mutagenesis. BioTechniques 25 (1998) 764-772
65. Hanahan D., Jessee J., and Bloom F.R. Plasmid transformation of Escherichia coli and other bacteria. Methods Enzymol. 204 (1991) 63-113
66. Pum D., Sára M., and Sleytr U.B. Structure, surface charge, and self-assembly of the S-layer lattice from Bacillus coagulans E38-66. J. Bacteriol. 171 (1989) 5296-5303