Center for NanoBiotechnology, University of Applied Life Sciences and Natural Resources, Gregor-Mendel-Strasse 33, A-1180 Wien, Austria
Received on November 20, 2003; revised on January 28, 2004; accepted on February 16, 2004
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Abstract |
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Key words: bacterial glycosylation / genomic glycosylation loci / glycan diversity / glycoengineering / S-layer nanoglycobiology
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What are S-layer glycoproteins? |
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Accounting for the intrinsic, nanometer-scale cell surface display feature of bacterial S-layer glycoproteins, we have coined the neologism S-layer nanoglycobiology, which encompasses structural, functional, and biosynthetic aspects of S-layers. Structural investigations use novel, straightforward analytical techniques (for a comprehensive survey of methods applied for S-layer glycoprotein research, the reader is referred to a recent review article by Schäffer et al., 2001); functional and biosynthetic studies, however, are lagging behind due to the lack of suitable molecular tools. The awareness of the promising application potential of S-layer glycoproteins as a unique matrix with inherent self-assembly properties for nanobiotechnology applications (for review see Sleytr et al., 1999
, 2002
), let us recently focus our efforts on the biosynthesis of S-layer glycoproteins at the molecular level, which represents the key to the successful modification of S-layer glycosylation and, consequently, the generation of artificial S-layer neoglycoconjugates with rationally designed glycosylation motifs by glycoengineering techniques.
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Diversity of S-layer protein glycosylation: summary of facts |
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Composition
Presently, about 40 different S-layer glycoprotein glycan structures are fully or at least partially elucidated (a summary of S-layer glycan structures is given in Table I). The observed structures and glycosidic linkage types already exceed the display found in eukaryotes. Bacterial S-layer glycan chains are linear or branched homo- or heterosaccharides, which comprise 2050 identical repeating units, whereas in archaea, short oligosaccharides without repeats prevail. The monosaccharide constituents of the S-layer glycan chains include a wide range of neutral hexoses, 6-deoxyhexoses, and amino sugars. Among bacteria, this spectrum is further extended by rare sugars, which are otherwise typical constituents of lipopolysaccharide (LPS) O-antigens of Gram-negative bacteria (respective glycoses are marked by an asterisk in Table II). O-glycosidic linkage regions observed on S-layer glycoproteins occur to tyrosine, serine, and threonine; N-glycans have been found only in archaea. Interestingly, no antennary structures comparable to the N-glycans present in eukaryotes have so far been identified among S-layer glycoproteins. For those S-layer glycoproteins whose protein portion has been sequenced, the properties of the corresponding S-layer protein structural gene are given in Table III.
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Another important question concerned the relationship between the translation and translocation event of the archaeal S-layer protein components. Using a hybrid protein approach with the signal peptideencoding region of the S-layer glycoprotein gene of H. volcanii fused to either to the cellulose-binding domain of the Clostridium thermocellum cellulosome or a reductase of H. volcanii, it was demonstrated that the signal peptide-cleaved mature versions of both hybrid proteins were secreted into the growth medium, whereas the signal peptidebearing forms remained in the cytoplasm (Irihimovitch and Eichler, 2003). The results of these experiments provide evidence that in archaea at least some of the secreted proteins are first synthesized inside the cell and only then translocated across the plasma membrane. It is assumed that the investigated archaeal preproteins rely on the Sec machinery for their secretion (Mori and Ito, 2001
).
Concerning bacteria, the number of new glycan structures is growing steadily (compare with Table I). Detailed structural analyses have been performed with S-layer glycoproteins of thermophilic bacilli, such as Geobacillus stearothermophilus NRS 2004/3a (Schäffer et al., 2002). For that organism, the S-layer protein portion SgsE has been fully sequenced, which allowed, for the first time on a bacterial glycoprotein, the exact determination of the positions of the glycosylation sites; comparable analyses have only been performed with the thermophilic archaea H. halobium (Lechner and Sumper, 1987
) and H. volcanii (Sumper et al., 1990
). In the case of the G. stearothermophilus NRS 2004/3a S-layer glycoprotein, the attached poly-L-rhamnan S-layer glycan chains consist, in average, of 1318 trisaccharide repeats that are O-glycosidically linked to the amino acids Thr 620 and/or Ser 794 of the precursor protein via a ß-D-Gal residue (Schäffer et al., 2002
). The C-terminal localization of the glycosylation sites on SgsE may indicate that the C-terminus of the S-layer protein is surface-exposed, which would sterically allow the attached glycan chains to protrude into the exterior environment. Furthermore, this would be in accordance with the proposed involvement of the N-terminus in anchoring the S-layer protein to the peptidoglycan network (Sára, 2001
). A detailed structure of the entire S-layer glycoprotein of G. stearothermophilus NRS 2004/3a is given in Table I. This table also shows a novel D-fucose-containing S-layer glycan, whose complete structure is currently under investigation (Schäffer and Messner, unpublished data).
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How is S-layer glycoprotein diversity created? First insights |
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The interesting question arises as to how S-layer glycoprotein diversity is created by nature. Approaches for unravelling the details about the S-layer protein glycosylation machinery benefit form the molecular information available on the biosynthesis of LPS O-antigens, because due to structural similarities it may be speculated that both cell surface glycoconjugates are assembled via similar biosynthetic routes, involving comparable enzyme activities.
First information on bacterial S-layer glycosylation loci
Following the requirement of activated sugars for S-layer glycan biosynthesis, A. thermoaerophilus DSM 10155 (Graninger et al., 2002) and G. stearothermophilus NRS 2004/3a (Novotny et al., 2004
) have been probed with rml-specific probes from the Salmonella enterica dTDP-ß-L-Rhap biosynthesis pathway, which allowed the chromosomal localization of the biosynthesis enzymes of that nucleotide sugar. Currently, the genes encoding several other sugar processing enzymes involved in the biosynthesis of bacterial S-layer glycans are known (Table IV); these lead to the formation of GDP-
-D-Rhap (Kneidinger et al., 2001a
), GDP-D-glycero-D-manno-Hepp (Kneidinger et al., 2001b
), dTDP-
-D-Fucp3NAc (Pfoestl et al., 2003
), and dTDP-
-D-Quip3NAc (Pfoestl et al., unpublished data). Sequencing of upstream and downstream regions of the respective DNA regions of G. stearothermophilus NRS 2004/3a, A. thermoaerophilus strains DSM 10155 and L420-91T revealed the presence of S-layer glycan biosynthesis (slg) gene clusters (GenBank accession numbers AF328862, AF324836, and AY442352, respectively). Based on database sequence similarities, putative biological functions to most of the genes of the slg clusters could be assigned (Novotny et al., 2004
). Briefly, the clusters contain components for S-layer glycan assembly, lipid activation, and export. Furthermore, there is evidence for interplay of products of glycan-specific genes and housekeeping genes as is also well known from LPS biosynthesis (Whitfield, 1995
).
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Concerning the chromosomal location of the S-layer target protein in relation to the slg cluster, no general scheme is present in the investigated organisms. In G. stearothermophilus NRS 2004/3a, the S-layer structural gene sgsE is located immediately upstream of the slg gene cluster (Novotny et al., 2004), whereas the genes encoding the proteins SatA and SatB of A. thermoaerophilus L420-91T and DSM 10155, respectively, are located elsewhere on the chromosome (Novotny et al., forthcoming).
In the course of investigating the glycan-based diversification potential of S-layer proteins, another interesting observation was made concerning the occurrence of specific sugar-processing enzymes in organisms whose S-layers are nonglycosylated (for a selection of organisms, see Messner et al., 1984). Probing, for instance, the chromosomal DNA of G. stearothermophilus L32-65 with an rmlA-specific probe, coding for the glucose 1-phosphat thymidylyltransferase RmlA of the L-rhamnose pathway (Giraud and Naismith, 2000
), indicated that in this organism the rml genes are present and, surprisingly, the enzyme proteins are also fully active (Novotny et al., 2004
). Because the presence of other rhamnosylated glycoconjugates in that organism could be ruled out, it is conceivable to assume that the S-layer glycosylation process must have been switched off by a yet unknown regulatory event. This finding may implicate that this particular organism and probably many others, too, have been naturally endowed with the potential to synthesize rhamnose-containing S-layer glycoproteins. It may be concluded that S-layer protein glycosylation is more widespread among bacteria than initially assumed (compare with Table I), but obviously, due to the absence of a selective pressure when grown under laboratory conditions, this ability may be subject to change or even loss.
Protein-based variations
Another reason for S-layer glycoprotein diversity was found in Clostridium difficile, the causative agent of antibiotic-associated diarrhea. This Gram-positive organism is unusual in expressing two S-layer proteins with molecular masses in the range of 45 kDa and
36 kDa, respectively (Cerquetti et al., 2000
; Poxton et al., 1999
). Both S-layer proteins have been shown to derive by processing of a larger precursor molecule, including the removal of a signal sequence and internal cleavage (Calabi et al., 2001
). Proteolytic cleavage takes place approximately in the middle of the precursor protein at a site that is highly conserved among different C. difficile strains, releasing the N-terminal portion with the signal peptide that, later on, is removed to yield the lower molecular weight S-layer protein. The C-terminal portion represents the higher-molecular-weight S-layer protein; it exhibits peptidoglycan hydrolase activity and acts as an adhesin to bind to human gut tissues (Calabi et al., 2002
). An unusual feature of the S-layer of C. difficile is that the sizes of the two mature S-layer proteins vary widely between strains. Sequence analyses of six strains of C. difficile showed that this variation is due to insertions and deletions of stretches of DNA within the slpA gene, rather than to the expression of alternate structural genes (Calabi and Fairweather, 2002
). Early reports indicated that the S-layer proteins from C. difficile strain 253 were glycosylated (Mauri et al., 1999
). Recent studies on other strains showed that in these organisms only the 45-kDa protein was significantly O-glycosylated, whereas the 36-kDa protein is either nonglycosylated or only glycosylated to a minor extent (Calabi et al., 2001
). Besides the already known substantial differences in the primary amino acid sequences of the S-layer proteins of different C. difficile strains, analyses of their specific glycosylation patterns should show whether distinct genes are present specifying the glycosylation reactions.
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Outlook: S-layer glycoproteins in applied research |
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Recent molecular investigations of the S-layer glycoprotein biosynthesis have revealed several novelties about nucleotide-sugar synthesis. The heptose genes of A. thermoaerophilus DSM 10155 led to the first elucidation of the overall pathway for the biosynthesis of a nucleotide-activated D-glycero--D-manno-heptose from D-seduheptulose 7-phosphate (Kneidinger et al., 2001a
). Furthermore, these data allowed the assignment of the steps involved in the biosynthesis of the ADP-L-glycero-ß-D-manno-heptose precursor of the inner core lipopolysaccharide of prominent laboratory organisms like Escherichia coli or Salmonella enterica (Kneidinger et al., 2002
). During analysis of the S-layer glycosylation of A. thermoaerophilus L420-91T, Gmd was identified to be a novel bifunctional enzyme displaying both dehydratase and reductase activities, which is required for GDP-D-rhamnose biosynthesis (Kneidinger et al., 2001b
). In the course of the functional characterization of the biosynthesis of dTDP-D-Fucp3NAc from the same organism, a novel type of isomerase capable of synthesizing dTDP-6-deoxy-D-xylo-hex-3-ulose from dTDP- 6-deoxy-D-xylo-hex-4-ulose was described (Pfoestl et al., 2003
). Recombinant enzymes from that pathway may be relevant for the synthesis of several antibiotics that contain C-3-aminated deoxy-sugars, such as erythromycin or tylosin. Furthermore, recombinant RmlABCD enzymes from the thermophile A. thermoaerophilus DSM 10155 may be beneficial for dTDP-L-rhamnose-targeted antibacterial therapy, because the instability of enzymes from mesophilic organisms limits productivity. Most Rml enzymes from the thermophilic source exhibit significantly higher stability at 37°C than the enzymes from S. enterica (Graninger et al., 2002
).
The knowledge of the enzyme apparatus involved in S-layer glycoprotein glycan biosynthesis and the understanding of the underlying mechanisms, should eventually allow the alteration or the rational design of S-layer protein glycosylation patterns to obtain bioactive S-layer neoglycoproteins. The common trend of glycoengineering is reflected by many recent review articles on that topic (Endo and Koizumi, 2000; Mendez and Sala, 2001
; Saxon and Bertozzi, 2001
). The potency of glycoengineering as a strategy for increasing the in vivo activity and duration of action of therapeutic proteins has recently been shown by Elliott et al. (2003)
, using glycosylated analogs of recombinant human erythropoietin or leptin. The presentation of glycoengineered motifs on the cell surface of bacteria is a newly unfolding area of research. An impressing example was stated by Paton et al. (2000)
, who demonstrated that a recombinant E. coli that displayed a Shiga toxin receptor mimic on its cell surface was capable of adsorbing and neutralizing Shiga toxins with very high efficiency. In general, the display of heterologous (glyco)proteins on the surface of bacteria, enabled by means of recombinant DNA technology, has become an increasingly used strategy in various applications in microbiology, nanobiotechnology, and vaccinology (Samuelson et al., 2002
). Besides outer membrane proteins, lipoproteins, autotransporters, or subunits of surface appendages that are being evaluated for that kind of applications, the use of the S-layer (glyco)protein cell surface anchor is a very attractive and promising alternative. It offers the unique advantage of providing a crystalline, regular "immobilization matrix" that should eventually allow the controlled and periodic surface display of "intelligent" glycosylation motifs. Nanobiotechnology applications of such tailored S-layer neoglycoproteins may include the fields of receptor mimics, vaccine design, or drug delivery using carbohydrate recognition. The possibility to incorporate additional functional domains into the S-layer protein portion may allow additional tuning of structural and functional features of these S-layer neoglycoproteins.
As glycosylation engineering of S-layer (glyco)proteins represents a rather new area of research, the benefits of S-layer neoglycoproteins for potential nanobiotechnology applications may currently be only deduced form the successful cell surface display of foreign peptide epitopes. For instance, a tetanus toxin fragment C that is cell surfaceexposed via the S-layer protein system and is produced by recombinant Bacillus anthracis protects against tetanus toxin (Mesnage et al., 1999). Also the S-layers of various lactic acid bacteria have been successfully exploited for the surface display of different bioactive epitopes (Åvall-Jääskeläinen et al., 2003
; Smit et al., 2001
, 2002
). Even though not yet cell surface-displayed in vivo, the high potential of chimeric S-layer proteins for nanobiotechnology applications could be unambiguously demonstrated by several other recent studies. For instance, the fusion of the major birch pollen allergen Bet v 1 to the C-terminal domain of the S-layer protein SbsC of B. stearothermophilus ATCC 12980 (Breitwieser et al., 2002
) and Bacillus sphaericus CCM 2177, respectively (Ilk et al., 2002
) yielded stable hybrid proteins that retained the ability to self-assemble into monomolecular lattices while presenting the allergen in its functional form. Other S-layer hybrid proteins contain the variable domain of a camel heavy chain antibody (Pleschberger et al., 2003
). Due to the selected fusion sites, the functional epitope remains located on the outer S-layer surface, which ensures its accessibility for binding of target molecules in newly developed diagnostic devices. Other potential nanobiotechnology applications may utilize a chimeric streptavidin S-layer as a self-assembling nanopatterned molecular affinity matrix to arrange biotinylated compounds on a surface (Moll et al., 2002
).
Consequently, the S-layer (glyco)protein-inherent biomolecular self-assembly properties, in combination with tailored glycosylation, is recognized as a powerful tool for future nanoscale engineering.
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Acknowledgements |
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Footnotes |
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Abbreviations |
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References |
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Altman, E., Brisson, J.-R., Messner, P., and Sleytr, U.B. (1991) Chemical characterization of the regularly arranged surface layer glycoprotein of Bacillus alvei CCM 2051. Biochem. Cell Biol., 69, 7278.[ISI][Medline]
Altman, E., Brisson, J.-R., Gagné, S.M., Kolbe, J., Messner, P., and Sleytr, U.B. (1992) Structure of the glycan chain from the surface layer glycoprotein of Clostridium thermohydrosulfuricum L77-66. Biochim. Biophys. Acta, 1117, 7177.[ISI][Medline]
Altman, E., Schäffer, C., Brisson, J.-R., and Messner, P. (1995) Characterization of the glycan structure of a major glycopeptide from the surface layer glycoprotein of Clostridium thermosaccharolyticum E20771. Eur. J. Biochem., 229, 308315.[Abstract]
Åvall-Jääskeläinen, S., Lindholm, A., and Palva, A. (2003) Surface display of the receptor-binding region of the Lactobacillus brevis S-layer protein in Lactococcus lactis provides nonadhesive lactococci with the ability to adhere to intestinal epithelial cells. Appl. Environ. Microbiol., 69, 22302236.
Benz, I. and Schmidt, M.A. (2002) Never say never again: protein glycosylation in pathogenic bacteria. Mol. Microbiol., 45, 267276.[CrossRef][ISI][Medline]
Bock, K., Schuster-Kolbe, J., Altman, E., Allmaier, G., Stahl, B., Christian, R., Sleytr, U.B., and Messner, P. (1994) Primary structure of the O-glycosidically linked glycan chain of the crystalline surface layer glycoprotein of Thermoanaerobacter thermohydrosulfuricus L111-69. Galactosyl tyrosine as a novel linkage unit. J. Biol. Chem., 269, 71377144.
Breitwieser, A., Egelseer, E.M., Moll, D., Ilk, N., Hotzy, C., Bohle, B., Ebner, C., Sleytr, U.B., and Sára, M. (2002) A recombinant bacterial cell surface (S-layer)-major birch pollen allergen-fusion protein (rSbsC/Bet v 1) maintains the ability to self-assemble into regularly structured monomolecular lattices and the functionality of the allergen. Protein Eng., 15, 243249.[CrossRef][ISI][Medline]
Bröckl, G., Behr, M., Fabry, S., Hensel, R., Kaudewitz, H., Biendl, E., and König, H. (1991) Analysis and nucleotide sequence of the genes encoding the surface-layer glycoproteins of the hyperthermophilic methanogens Methanothermus fervidus and Methanothermus sociabilis. Eur. J. Biochem., 199, 147152.[Abstract]
Calabi, E. and Fairweather, N. (2002) Patterns of sequence conservation in the S-layer proteins and related sequences in Clostridium difficile. J. Bacteriol., 184, 38863897.
Calabi, E., Ward, S., Wren, B., Paxton, T., Panico, M., Morris, H., Dell, A., Dougan, G., and Fairweather, N. (2001) Molecular characterization of the surface layer proteins from Clostridium difficile. Mol. Microbiol., 40, 11871199.[CrossRef][ISI][Medline]
Calabi, E., Calabi, F., Phillips, A.D., and Fairweather, N.F. (2002) Binding of Clostridium difficile surface layer proteins to gastrointestinal tissues. Infect. Immun., 70, 57705778.
Cerquetti, M., Molinari, A., Sebastianelli, A., Diociaiuti, M., Petruzzelli, R., Capo, C., and Mastrantonio, P. (2000) Characterization of surface layer proteins from different Clostridium difficile clinical isolates. Microb. Pathol., 28, 363372.[CrossRef]
Christian, R., Messner, P., Weiner, C., Sleytr, U.B., and Schulz, G. (1988) Structure of a glycan from the surface-layer glycoprotein of Clostridium thermohydrosulfuricum L111-69. Carbohydr. Res., 176, 160163.[CrossRef][ISI][Medline]
Christian, R., Schulz, G., Schuster-Kolbe, J., Allmaier, G., Schmid, E.R., Sleytr, U.B., and Messner, P. (1993) Complete structure of the tyrosine-linked saccharide moiety from the surface layer glycoprotein of Clostridium thermohydrosulfuricum S102-70. J. Bacteriol., 175, 12501256.[Abstract]
Claus, H., Akça, E., Debaerdemaeker, T., Evrard, C., Declercq, J.-P., and König, H. (2002) Primary structure of selected archaeal mesophilic and extremely thermophilic outer surface layer proteins. System. Appl. Microbiol., 25, 312.[ISI]
Eichler, J. (2000) Novel glycoproteins of the halophilic archaeon Haloferax volcanii. Arch. Microbiol., 173, 445448.[CrossRef][ISI][Medline]
Eichler, J. (2001) Post-translational modification of the S-layer glycoprotein occurs following translocation across the plasma membrane of the haloarchaeon Haloferax volcanii. Eur. J. Biochem., 268, 43664373.
Eichler, J. and Irihimovitch, V. (2003) Move it on over: getting proteins across biological membranes. Bioessays, 25, 11541157.[CrossRef][ISI][Medline]
Elliott, S., Lorenzini, T., Asher, S., Aoki, K., Brankow, D., Buck, L., Busse, L., Chang, D., Fuller, J., Grant, J., and others. (2003) Enhancement of therapeutic protein in vivo activities through glycoengineering. Nat. Biotechnol., 21, 414421.[CrossRef][ISI][Medline]
Endo, T. and Koizumi, S. (2000) Large-scale production of oligosaccharides using engineered bacteria. Curr. Opin. Struct. Biol., 5, 536541.[CrossRef]
Eshinimaev, B.T., Khmelenina, V.N., Sakharovskii, V.G., Suzina, N.E., and Trotsenko, Y.A. (2002) Physiological, biochemical, and cytological characteristics of a haloalkalitolerant methanotroph grown on methanol. Microbiology (Moscow), 71, 512518.
Evrard, C., Declercq, J.-P., Debaerdemaeker, T., and König, H. (1999) The first successful crystallization of a prokaryotic extremely thermophilic outer surface layer glycoprotein. Z. Kristallogr., 214, 427429.
Giraud, M.-F. and Naismith, J.H. (2000) The rhamnose pathway. Curr. Opin. Struct. Biol., 10, 687696.[CrossRef][ISI][Medline]
Graninger, M., Kneidinger, B., Bruno, K., Scheberl, A., and Messner, P. (2002) Homologs of the Rml enzymes from Salmonella enterica are responsible for dTDP-ß-L-rhamnose biosynthesis in the Gram-positive thermophile Aneurinibacillus thermoaerophilus DSM 10155. Appl. Environ. Microbiol., 68, 37083715.
Ilk, N., Völlenkle, C., Egelseer, E.M., Breitwieser, A., Sleytr, U.B., and Sára, M. (2002) Molecular characterization of the S-layer gene, sbpA, of Bacillus sphaericus CCM 2177 and production of a functional S-layer fusion protein with the ability to recrystallize in a defined orientation while presenting the fused allergen. Appl. Environ. Microbiol., 68, 32513260.
Irihimovitch, V. and Eichler, J. (2003) Post-translational secretion of fusion proteins in the halophilic archaea Haloferax volcanii. J. Biol. Chem., 278, 1288112887.
Kaluzhnaya, M., Khmelenina, V., Eshinimaev, B., Suzina, N., Nikitin, D., Solonin, A., Lin, J.-L., McDonald, I., Murrell, C., and Trotsenko, Y. (2001) Taxonomic characterization of new alkaliphilic and alkalitolerant methanotrophs from soda lakes of the southeastern Transbaikal region and description of Methylomicrobium buryatense sp. nov. System. Appl. Microbiol., 24, 166176.[ISI]
Kandler, O. (1993) Archaea (Archaebacteria). Progr. Botany, 54, 124.
Kärcher, U., Schröder, H., Haslinger, E., Allmaier, G., Schreiner, R., Wieland, F., Haselbeck, A., and König, H. (1993) Primary structure of the heterosaccharide of the surface glycoprotein of Methanothermus fervidus. J. Biol. Chem., 268, 2682126826.
Keenleyside, W.J and Whitfield C. (1999) Genetics and biosynthesis of lipopolysaccharide O-antigens. In Brade, H., Opal, S.M., Vogel, S.N., and Morrison, D.C. (Eds.), Endotoxins in health and disease. Marcel Dekker, New York, pp. 331358.
Kikuchi, A., Sagami, H., and Ogura, K. (1999) Evidence for covalent attachment of diphytanylglycerol phosphate to the cell-surface glycoprotein of Halobacterium halobium. J. Biol. Chem., 274, 1801118016.
Kneidinger, B., Graninger, M., Adam, G., Puchberger, M., Kosma, P., Zayni, S., and Messner, P. (2001a) Identification of two GDP-6-deoxy-D-lyxo-4-hexulose reductases synthesizing GDP-D-rhamnose in Aneurinibacillus thermoaerophilus L420-91T. J. Biol. Chem., 276, 55775583.
Kneidinger, B., Graninger, M., Puchberger, M., Kosma, P., and Messner, P. (2001b) Biosynthesis of nucleotide-activated D-glycero-D-manno-heptose. J. Biol. Chem., 276, 2093520944.
Kneidinger, B., Marolda, C., Graninger, M., Zamyatina, A., McArthur, F., Kosma, P., Valvano, M.A., and Messner, P. (2002) Biosynthesis pathway of ADP-L-glycero-ß-D-manno-heptose in Escherichia coli. J. Bacteriol., 184, 363369.
Konrad, Z. and Eichler, J. (2002) Lipid modification of proteins in Archaea: attachment of a mevalonic acid-based lipid moiety to the surface-layer glycoprotein of Haloferax volcanii follows protein translocation. Biochem. J., 366, 959964.[ISI][Medline]
Kosma, P., Neuninger, C., Christian, R., Schulz, G., and Messner, P. (1995a) Glycan structure of the S-layer glycoprotein of Bacillus sp. L420-91. Glycoconj. J., 12, 99107.[ISI][Medline]
Kosma, P., Wugeditsch, T., Christian, R., Zayni, S., and Messner, P. (1995b) Glycan structure of a heptose-containing S-layer glycoprotein of Bacillus thermoaerophilus. Glycobiology, 5, 791796; Erratum (1996) Glycobiology, 6, 5.[Abstract]
Kuen, B. and Lubitz, W. (1996) Analysis of S-layer proteins and genes. In Sleytr, U.B., Messner, P., Pum, D. and Sára, M. (Eds.), Crystalline bacterial cell surface proteins. R.G. Landes Comp. and Academic Press, Austin, TX, pp. 77102.
Lawrence, J.G. and Hendrickson, H. (2003) Lateral gene transfer: when will adolescence end? Mol. Microbiol., 50, 739749.[CrossRef][ISI][Medline]
Lechner, J. and Sumper, M. (1987) The primary structure of a procaryotic glycoprotein. Cloning and sequencing of the cell surface glycoprotein gene of halobacteria. J. Biol. Chem., 262, 97249729.
Lechner, J. and Wieland, F. (1989) Structure and biosynthesis of prokaryotic glycoproteins. Annu. Rev. Biochem., 58, 173194.[CrossRef][ISI][Medline]
Mauri, P.L., Pietta, P.G., Maggioni, A., Cerquetti, M., Sebastianelli, A., and Mastrantonio, P. (1999) Characterization of surface layer proteins from Clostridium difficile by liquid chromatography/electrospray ionization mass spectrometry. Rapid Commun. Mass Spectrom., 13, 695703.[CrossRef][ISI][Medline]
Meier-Stauffer, K., Busse, H.-J., Rainey, F.A., Burghardt, J., Scheberl, A., Hollaus, F., Kuen, B., Makristathis, A., Sleytr, U.B., and Messner, P. (1996) Description of Bacillus thermoaerophilus sp. nov., to include sugar beet isolates and Bacillus brevis ATCC 12990. Int. J. Syst. Bacteriol., 46, 532541.
Mendez, C. and Salas, J.A. (2001) Altering the glycosylation pattern of bioactive compounds. Trends Biotechnol., 11, 449456.[CrossRef]
Mescher, M.F. and Strominger, J.L. (1976) Purification and characterization of a prokaryotic glycoprotein from the cell envelope of Halobacterium salinarium. J. Biol. Chem., 251, 20052014.[Abstract]
Mesnage, S., Weber-Levy, M., Haustant, M., Mock, M., and Fouet, A. (1999) Cell surface-exposed tetanus toxin fragment C produced by recombinant Bacillus anthracis protects against tetanus toxin. Infect. Immun., 67, 48474850.
Messner, P. (2004) Prokaryotic glycoproteins: unexplored but important. J. Bacteriol. 186, 25172519.
Messner, P. and Schäffer, C. (2000) Surface layer glycoproteins of bacteria and archaea. In Doyle, R.J. (Ed.), Glycomicrobiology. Kluwer Academic/Plenum, New York, pp. 93125.
Messner, P. and Schäffer, C. (2003) Prokaryotic glycoproteins. In Herz, W., Falk, H., and Kirby, G.W. (Eds.), Progress in the chemistry of organic natural products, vol. 85. Springer-Verlag, Wien, pp. 51124.
Messner, P., Hollaus, F., and Sleytr, U.B. (1984) Paracrystalline cell wall surface layers of different Bacillus stearothermophilus strains. Int. J. Syst. Bacteriol., 34, 202210.
Messner, P., Christian, R., Kolbe, J., Schulz, G., and Sleytr, U.B. (1992) Analysis of a novel linkage unit of O-linked carbohydrates from the crystalline surface layer glycoprotein of Clostridium thermohydrosulfuricum S102-70. J. Bacteriol., 174, 22362240.[Abstract]
Messner, P., Schuster-Kolbe, J., Schäffer, C., Sleytr, U.B., and Christian, R. (1993) Glycoprotein nature of select bacterial S-layers. In Beveridge, T.J. and Koval, S.F. (Eds.), Advances in bacterial paracrystalline surface layers. Plenum, New York, pp. 95107.
Messner, P., Christian, R., Neuninger, C., and Schulz, G. (1995) Similarity of "core" structures in two different glycans of tyrosine-linked eubacterial S-layer glycoproteins. J. Bacteriol., 177, 21882193.[Abstract]
Moens, S. (2000) Non-S-layer glycoproteins: a review. In Doyle, R.J. (Ed.), Glycomicrobiology. Kluwer Academic/Plenum, New York, pp. 130.
Moll, D., Huber, C., Schlegel, B., Pum, D., Sleytr, U.B., and Sára, M. (2002) S-layer-streptavidin fusion proteins as template for nanopatterned molecular arrays. Proc. Natl. Acad. Sci. USA, 99, 1464614651.
Mori, H. and Ito K. (2001) The Sec protein-translocation pathway. Trends Microbiol., 10, 494500.[CrossRef]
Möschl, A., Schäffer, C., Sleytr, U.B., Messner, P., Christian, R., and Schulz, G. (1993) Characterization of the S-layer glycoproteins of two lactobacilli. In Beveridge, T.J. and Koval, S.F. (Eds.), Advances in bacterial paracrystalline surface layers. Plenum, New York, pp. 281284.
Novotny, R., Schäffer, C., Strauss, J., and Messner, P. (2004) S-Layer glycan-specific loci on the chromosome of Geobacillus stearothermophilus NRS 2004/3a and dTDP-L-rhamnose biosynthesis potential of Geobacillus stearothermophilus strains. Microbiology 150, 953965.
Novotny, P., Pfoestl, A., Messner, P., and Schäffer, C. (Forthcoming) Genetic organization of chromosomal S-layer glycan biosynthesis loci of Bacillaceae: a minireview. Glycoconjugate J.
Ochman, H., Lawrence, J.G., and Groisman, E.A. (2000) Lateral gene transfer and the nature of bacterial innovation. Nature, 405, 299304.[CrossRef][ISI][Medline]
Paton, A.W., Morona, R., and Paton, J.C. (2000) A new biological agent for treatment of Shiga toxigenic Escherichia coli infections and dysentery in humans. Nat. Med., 6, 265270.[CrossRef][ISI][Medline]
Paul, G., Lottspeich, F., and Wieland, F. (1986) Asparaginyl-N-acetylgalactosamine. Linkage unit of halobacterial glycosaminoglycan. J. Biol. Chem., 261, 10201024.
Pellerin, P., Fournet, B., and Debeire, P. (1990) Evidence for the glycoprotein nature of the cell sheath of Methanosaeta-like cells in the culture of Methanothrix soehngenii strain FE. Can. J. Microbiol., 36, 631636.[ISI]
Pfoestl, A (2003) Biosynthesis of nucleotide-activated 3-acetamido-3,6-dideoxy hexoses. PhD diss., Universität für Bodenkultur Wien, 93 pp.
Pfoestl, A., Hofinger, A., Kosma, P., and Messner, P. (2003) Biosynthesis of dTDP-3-acetamido-3,6-dideoxy--D-galactose in Aneurinibacillus thermoaerophilus L420-91T. J. Biol. Chem., 278, 2641026417.
Pleschberger, M., Neubauer, A., Egelseer, E.M., Weigert, S., Lindner, B., Sleytr, U.B., Muyldermans, S., and Sára, M. (2003) Generation of a functional monomolecular protein lattice consisting of an S-layer fusion protein comprising the variable domain of a camel heavy chain antibody. Bioconj. Chem., 14, 440448.[CrossRef][ISI][Medline]
Pouwels, P., Kolen, C.P.A.M., and Boot, H.J. (1997) S-layer protein genes in Lactobacillus. FEMS Microbiol. Rev., 20, 7882.
Power, P.M. and Jennings, M.P. (2003) The genetics of glycosylation in Gram-negative bacteria. FEMS Microbiol. Lett., 218, 211222.[CrossRef][ISI][Medline]
Poxton, I.R., Higgins, P.G., Currie, C.G., and McCoubrey, J. (1999) Variation in the cell surface proteins of Clostridium difficile. Anaerobe, 5, 213215.[CrossRef][ISI]
Raetz, C.R.H. and Whitfield, C. (2002) Lipopolysaccharide endotoxins. Annu. Rev. Biochem., 71, 635700.[CrossRef][ISI][Medline]
Samuelson, P., Gunneriusson, E., Nygren, P.A., and Stahl, S. (2002) Display of proteins on bacteria. J. Biotechnol., 96, 129154.[CrossRef][ISI][Medline]
Sandercock, L.E., MacLeod, A.M., Ong, E., and Warren, R.A.J. (1994) Non-S-layer glycoproteins in eubacteria. FEMS Microbiol. Lett., 118, 17.[CrossRef][ISI][Medline]
Sára, M. (2001) Conserved anchoring mechanisms between crystalline cell surface S-layer proteins and secondary cell wall polymers in Gram-positive bacteria? Trends Microbiol., 2, 4749.
Saxon, E. and Bertozzi, C.R. (2001) Chemical and biological strategies for engineering cell surface glycosylation. Annu. Rev. Cell Dev. Biol., 17, 123.[CrossRef][ISI][Medline]
Schäffer, C. and Messner, P. (2001) Glycobiology of surface layer proteins. Biochimie, 83, 591599.[CrossRef][ISI][Medline]
Schäffer, C., Müller, N., Christian, R., Graninger, M., Wugeditsch, T., Scheberl, A., and Messner, P. (1999) Complete glycan structure of the S-layer glycoprotein of Aneurinibacillus thermoaerophilus GS4-97. Glycobiology, 9, 407414.
Schäffer, C., Dietrich, K., Unger, B., Scheberl, A., Rainey, F.A., Kählig, H., and Messner, P. (2000) A novel type of carbohydrate-protein linkage region in the tyrosine-bound S-layer glycan of Thermoanaerobacterium thermosaccharolyticum D120-70. Eur. J. Biochem., 267, 54825492.
Schäffer, C., Graninger, M., and Messner, P. (2001) Prokaryotic glycosylation. Proteomics, 1, 248261.[CrossRef][ISI][Medline]
Schäffer, C., Wugeditsch, T., Kählig, H., Scheberl, A., Zayni, S., and Messner, P. (2002) The surface layer (S-layer) glycoprotein of Geobacillus stearothermophilus NRS 2004/3a. Analysis of its glycosylation. J. Biol. Chem., 277, 62306239.
Schmidt, M.A., Riley, L.W., and Benz, I. (2003) Sweet new world: glycoproteins in bacterial pathogens. Trends Microbiol., 11, 554561.[CrossRef][ISI][Medline]
Sleytr, U.B. and Messner, P. (2003) Crystalline bacterial cell surface layers. In Schaechter, M. (Ed.), Desk encyclopedia of microbiology. Academic Press/Elsevier Science (USA), San Diego, pp. 286293.
Sleytr, U.B., Messner, P., Pum, D., and Sára, M. (1999) Crystalline bacterial cell surface layers (5-layers): from supramolecular cell structure to biomimetics and nanotechnology. Angew. Chem. Int. Ed. 38, 10341054.[CrossRef]
Sleytr, U.B. and Thorne, K.J.I. (1976) Chemical characterization of the regularly arrayed surface layers of Clostridium thermosaccharolyticum and Clostridium thermohydrosulfuricum. J. Bacteriol., 126, 377383.[ISI][Medline]
Sleytr, U.B., Sára, M., Pum, D., Schuster, B., Messner, P., and Schäffer, C. (2002) Self-assembly protein systems: microbial S-layers. In Steinbüchel, A. and Fahnestock, S.R. (Eds.), Biopolymers, vol. 7, Polyamides and complex proteinaceous matrices I. Wiley-VCH, Weinheim, pp. 285338.
Smit, E., Oling, F., Demel, R., Martinez, B., and Pouwels, P.H. (2001) The S-layer protein of Lactobacillus acidophilus ATCC 4356: identification and characterisation of domains responsible for S-protein assembly and cell wall binding. J. Mol. Biol., 305, 245257.[CrossRef][ISI][Medline]
Smit, E., Oling, F., Demel, R., Martinez, B., and Pouwels, P.H. (2002) Structural and functional analysis of the S-layer protein crystallisation domain of Lactobacillus acidophilus ATCC 4356: evidence for proteinprotein interaction of two subdomains. J Mol. Biol., 13, 953964.[CrossRef]
Spiro, R.G. (2002) Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology, 12, 43R56R.
Sumper, M. and Wieland F.T. (1995) Bacterial glycoproteins. In Montreuil, J., Vliegenthart, J.F.G., and Schachter, H. (Eds.), Glycoproteins. Elsevier, Amsterdam, pp. 455473.
Sumper, M., Berg, E., Mengele, R., and Strobel, I. (1990) Primary structure and glycosylation of the S-layer protein of Haloferax volcanii. J. Bacteriol., 172, 71117118.[ISI][Medline]
Szymanski, C.M., Logan, S.M., Linton, D., and Wren, B.W. (2003) Campylobactera tale of two protein glycosylation systems. Trends Microbiol., 11, 233238.[ISI][Medline]
Upreti, R.K., Kumar, M., and Shankar, V. (2003) Bacterial glycoproteins: functions, biosynthesis and applications. Proteomics, 3, 363379.[CrossRef][ISI][Medline]
Valvano, M.A. (2003) Export of O-specific lipopolysaccharides. Front. Biosci., 8, S452S471.[ISI][Medline]
Wacker, M., Linton, D., Hitchen, P.G., Nita-Lazar, M., Haslam, S.M., North, S.J., Panico, M., Morris, H.R., Dell, A., Wren, B.W., and Aebi, M. (2002) N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science, 298, 17901793.
Whitfield, C. (1995) Biosynthesis of lipopolysaccharide O antigens. Trends Microbiol., 3, 178185.[CrossRef][ISI][Medline]
Wieland, F., Heitzer, R., and Schaefer, W. (1983) Asparaginyl-glucose: novel type of carbohydrate linkage. Proc. Natl Acad. Sci. USA, 80, 54705474.[Abstract]
Woese, C.R., Kandler, O., and Wheelis, M.L. (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl Acad. Sci. USA, 87, 45764579.[Abstract]
Wugeditsch, T., Zachara, N.E., Puchberger, M., Kosma, P., Gooley, A.A., and Messner, P. (1999) Structural heterogeneity in the core oligosaccharide of the S-layer glycoprotein from Aneurinibacillus thermoaerophilus DSM 10155. Glycobiology, 9, 787795.
Zeitler, R., Hochmuth, E., Deutzmann, R., and Sumper, M. (1998) Exchange of Ser-4 for Val, Leu or Asn in the sequon Asn-Ala-Ser does not prevent N-glycosylation of the cell surface glycoprotein from Halobacterium halobium. Glycobiology, 8, 11571164.