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Mini-Review |
Division of Molecular Biosciences, Faculty of Natural Sciences, Imperial College London, South Kensington Campus, London SW7 2AZ, UK
Correspondence
Paul G. Hitchen
p.hitchen{at}imperial.ac.uk
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ABSTRACT |
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 TOP ABSTRACT REFERENCES |
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Introduction
The proteome, in analogy to the genome, is used to describe the entire set of proteins expressed by an organism under a defined set of conditions. Whilst the genome is considered static, the proteome is dynamic and much more complex, constantly altering in response to changes in the environment. A further level of complexity is introduced by the addition of protein post-translational modifications. Glycosylation, the post-translational modification of proteins by carbohydrates, has long been recognized as a fundamental strategy used by eukaryotes to influence and modulate protein structure and function (Taylor & Drickamer, 2002
). It is increasingly evident that protein glycosylation is also abundant in prokaryotes, with an ever-growing number of glycoproteins being identified. The information derived from the genome has made it possible to relate the proteome to the genome. In this review, we introduce the emerging field of glycoproteomics, which is exploiting genomic and proteomic methodologies to facilitate the detection and analysis of bacterial glycoproteins. Traditionally, the analysis of the sugar molecules found on glycoproteins has been performed on the released glycans but new technologies are now permitting the analysis of the sugar in situ (Dell & Morris, 2001). Whilst our current understanding of the genetics, biosynthesis and function of bacterial glycoproteins is still in its infancy, we are beginning to correlate genetic and structural data in the functional analysis of bacterial glycosylation pathways.
Protein glycosylation
There are two main types of protein glycosylation: N-glycosylation, in which the oligosaccharide is attached to an asparagine residue, and O-glycosylation, in which the oligosaccharide can be attached to a serine, threonine or tyrosine residue. The glycans found on prokaryotic glycoproteins are far more diverse in terms of sugar composition and structure than those found in eukaryotic organisms. The earliest examples of protein glycosylation in prokaryotes were found in the archaea, which express glycosylated surface layer (S-layer) proteins (Mescher & Strominger, 1976). A number of S-layer glycoproteins have now been reported and a considerable amount is known about their structure and biosynthesis (reviewed by Schaffer & Messner, 2004). More recently, non-S-layer glycoproteins have been discovered in bacteria, particularly in the medically relevant pathogens. Our current knowledge of prokaryotic protein glycosylation has been discussed in detail in a number of excellent reviews (Benz & Schmidt, 2002; Szymanski & Wren, 2005; Upreti et al., 2003). Over the last decade, the prevalence of reported glycoproteins has been best demonstrated in the cell-surface appendages of bacteria, such as pili and flagella. The pilin proteins of the pathogenic bacteria Neisseria meningitidis, Neisseria gonorrhoeae and Pseudomonas aeruginosa have all been demonstrated to be O-glycosylated (Castric et al., 2001; Hegge et al., 2004; Stimson et al., 1995). The pilin glycans from Neisseria species share a common structure, in particular with respect to the unusual O-linked sugar residue 2,4-diacetamido-2,4,6-trideoxyhexose (DATDH) (Hegge et al., 2004). Like that of the neisseriae, the Pseudomonas pilin O-glycan is a short-chain oligosaccharide, although the sugar components differ. The flagella of the bacteria Campylobacter jejuni, Helicobacter pylori, P. aeruginosa and Listeria monocytogenes have also been shown to be O-glycosylated (Schirm et al., 2003, 2004a, b; Thibault et al., 2001). The flagella of Campylobacter and Helicobacter species are modified with derivatives of pseudaminic acid, a nine-carbon sugar that resembles sialic acid, commonly found coating mammalian cells. Glycosylated flagella have also been found in archaea, where the flagellin glycan of Methanococcus voltae was demonstrated to be N-glycosylated (Voisin et al., 2005). N-linked glycosylation was reported in bacteria for the first time with the characterization of an N-linked glycan, attached via the eukaryotic Asn-X-Ser/Thr consensus sequence, on multiple proteins in C. jejuni (Young et al., 2002).
The determination of increasing numbers of bacterial genomes has allowed the identification of genes involved in the glycosylation process. The genome sequences of Campylobacter coli and C. jejuni identified putative glycosylation loci (Fry et al., 1998; Guerry et al., 1996), with subsequent work establishing the presence of both N-linked and O-linked protein glycosylation pathways (Szymanski & Wren, 2005). Sequencing and microarray studies have demonstrated that homologues of the N-linked glycosylation pathway are highly conserved and clustered across Campylobacter species (Szymanski & Wren, 2005). Orthologues of the genes in both pathways are found in other bacteria, particularly the mucosal-associated pathogens. For example, both Campylobacter and Neisseria species possess protein glycosylation loci (pgl) and comparison indicates that they share genes involved in the synthesis and transfer of DATDH or bacillosamine (2,4-diacetamido-2,4,6-trideoxyglucose), a component of their respective glycans (Power & Jennings, 2003).
Mass spectrometry
Mass spectrometry (MS) has been used for many years to define carbohydrate structures found on bacterial proteins (Bock et al., 1994; Dobos et al., 1996). More recently, knowledge of genome sequences has led to the development of new strategies for the analysis of glycoproteins that exploit genomic information. These advances have been born from the success of proteomics and by developments in MS instrumentation. The capacity of MS to handle large numbers of proteins and analyse complex mixtures of peptides at high sensitivity and accuracy, coupled to their rapid identification from the information available from genome sequencing projects, has made proteomics an invaluable high-throughput technique for functional genomics. These developments in MS instrumentation and proteomic strategies are now being successfully applied to the analysis of prokaryotic glycoproteins.
MS is an analytical technique that detects samples that can be successfully converted to gas-phase ions. The resulting ions are accelerated out of the ionization source into a mass analyser, where they are separated according to their mass to charge ratio (m/z) and detected to produce a mass spectrum. The techniques of electrospray ionization (ES) and matrix-assisted laser desorption ionization (MALDI) MS have become the routine methods of choice for protein identification, and an in-depth description of the instrumentation, methods and applications is available in a number of reviews (Andersen & Mann, 2000; Mann et al., 2001; Yates, 2004). The key to both techniques is the ability to analyse large biological molecules without degradation. MALDI-MS is the pre-eminent technique for screening molecular ions (mass mapping), especially when high throughput and high sensitivity is required. Mass mapping alone is not always sufficient for identification of a protein, and sequence information may be required. ES-MS can be adapted to fragment intact molecular ions that provide complementary sequence information. ES instruments usually have tandem mass analysers in order to perform tandem MS or MS/MS experiments where fragments are produced by collisional activation [collision-activation-dissociation (CAD)] of a selected ion. The ion is selected for fragmentation by the first mass analyser for collision with an inert gas. The resulting fragment ions are then separated in the second analyser and detected. The most commonly used technology for ES-MS/MS is the quadrupole orthogonal acceleration time of flight (Q-TOF) mass spectrometer. An additional advantage of this type of instrument is the ability to perform MS/MS experiments online, for example on peaks eluting from a liquid chromatography (LC) system, in real time. Sample fractions for other experiments can be collected by stream splitting. Recent developments have seen the introduction of novel configuration mass spectrometers, such as MALDI-Q-TOF- and MALDI-TOF-TOF-type instruments, which combine the advantages of MALDI mass mapping with the ability to sequence (Medzihradszky et al., 2000; Shevchenko et al., 2000). Another instrument with great potential for glycoprotein analysis is the Fourier transform ion cyclotron resonance mass spectrometer (FT-ICR-MS), which offers high resolution and mass accuracy. FT-ICR-MS is currently being exploited with the recently developed electron capture dissociation (ECD) soft fragmentation technique, which mainly induces fragmentation of the peptide backbone, retaining the more labile modifications such as glycosylation and thus defining site attachment (Hakansson et al., 2001).
Identification of glycoproteins
The first indication that a protein may be glycosylated is often through aberrant migration on a gel. Further evidence may be obtained using glycan detection kits based on the oxidation of glycans with periodic acid. A lectin blot may also be performed, which may give some insight into the type of sugar residues likely to be present in the glycan moiety. For a more detailed study of the glycosylation of a protein, chromatographic purifications or antibody precipitations are often used to isolate sufficient material for analysis. Whilst MS analysis can tolerate some protein impurities, a final preparation step using SDS-PAGE is usually performed prior to MS analysis. Although modern MS instrumentation routinely works at the subpicomole level, the chances of detecting and characterizing protein glycosylation are increased with at least Coomassie-stainable amounts of material. In this regard, Coomassie is also the stain of choice, since other stains may interfere with the subsequent glycan analysis.
In a typical glycoproteomic experiment, the purified protein band will be cut from a gel, enzymically digested into peptides, cleaned up and analysed by MS. The general strategy is shown in Fig. 1. If the sequence is known, the peptide masses obtained experimentally are matched against the list of peptide masses expected from a theoretical enzyme digest. The remaining non-matching masses observed in the mass spectrum can be selected for MS/MS experiments in order to gain sequence information from which it may be possible to identify any peptides that are glycosylated within a sample. Non-matching masses observed in a MS spectrum commonly result from contaminating proteins and missed or unpredicted enzymic cleavages. Ideally, interpretation of the MS/MS fragmentation pattern provides information on the nature and location of any attached glycan as well as the peptide sequence to be determined. The glycosidic bonds are generally weaker than peptide bonds and thus fragment more easily, providing glycan sequence information. Peptide fragmentation also takes place, and in favourable circumstances crucial signals in the MS/MS spectrum, derived from cleavages on either side of the amino acid carrying the sugar, will provide information on the attachment site.
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Whilst the MS and MS/MS glycoproteomic techniques described can provide details on the nature of the glycan and the site of attachment, there is rarely sufficient information to define carbohydrate structures rigorously. After the initial evidence of protein glycosylation has been acquired, a detailed structural characterization of a novel prokaryotic glycan structure is often required and this presents a considerable challenge, especially when limited sample amounts are available for analysis. Also, in contrast to eukaryotic carbohydrate structure determination, the more unusual nature of bacterial sugars, together with the lack of a common, defined glycosylation biosynthetic pathway, significantly complicates carbohydrate structure determination in prokaryotes. A number of complementary techniques are usually required to fully characterize the structure of a novel glycan. MS techniques complementary to those described above have also proved useful in glycan characterization. Accurate intact mass measurements can provide elemental compositions, which can eliminate possible substituents of similar mass, whilst secondary MS/MS fragmentation, where sugar fragment ions are created for further fragmentation, can provide preliminary structural information (Thibault et al., 2001; Voisin et al., 2005). Data from chemical degradations are usually required to supplement molecular and fragment ion information to characterize structural features such as sugar type and branching. Another technique that has proved invaluable in carbohydrate structural determination is nuclear magnetic resonance (NMR), and this is often essential in the determination of novel or unusual sugars that are a common feature of bacterial glycoproteins (Castric et al., 2001; Thibault et al., 2001). The increased sample amounts required for NMR analysis can prove problematic but the introduction of cryoprobe technology for increased sensitivity in NMR analysis has shown the potential for detailed structural information from limited amounts of material (Voisin et al., 2005).
Examples of glycoproteomic analysis
The application of glycoproteomics in the study of bacterial glycosylation pathways is highlighted by the elucidation of the N-linked glycosylation pathway in C. jejuni. The sequencing of the C. jejuni NCTC 11168 genome revealed a capacity for the organism to produce a variety of cell-surface carbohydrates. Thus clusters of genes were sequenced for lipooligosaccharide (LOS) biosynthesis, capsule biosynthesis and flagellar modification (Parkhill et al., 2000). A cluster of genes originally thought to be involved in LOS biosynthesis was subsequently shown to play a role in protein glycosylation (Szymanski et al., 1999). Mutation of genes from this locus in C. jejuni did not result in changes to LOS or capsule but altered reactivity of multiple proteins with both rabbit and human sera (Szymanski et al., 1999). Chemical deglycosylation of protein fractions also resulted in altered antigenicity, suggesting that products of the gene locus are involved in glycoprotein biosynthesis. The genes from this locus were named pgl, for protein glycosylation. Subsequent work identified two glycoproteins, PEB3 and CgpA, which bound to the GalNAc-specific lectin soybean agglutinin (Linton et al., 2002). The structure of the PEB3 N-linked glycan was determined by MS and NMR and shown to be a heptasaccharide with the structure GalNAc
1-4GalNAc1-4[Glc
1-3]GalNAc1-4GalNAc1-4GalNAc1-3Bac, where Bac is the unusual sugar bacillosamine (Young et al., 2002). The authors demonstrated that the glycan was N-linked to Asn in the eukaryotic like sequence motif Asn-Xaa-Ser/Thr. Genetic and structural analyses have demonstrated that both the pgl gene locus and heptasaccharide glycan structure are highly conserved among strains of C. jejuni and C. coli (Szymanski et al., 1999, 2003).
One gene in the pgl locus, termed pglB, encodes a protein with significant homology to the STT3 protein, a component of the eukaryotic oligosaccharyltransferase that transfers the glycan moiety to the nascent protein (Dempski & Imperiali, 2002). A knockout mutation to pglB resulted in the loss of N-linked glycosylation, indicating its essential role in this process (Szymanski et al., 1999). The putative functions of the other members of the pgl gene cluster were predicted based on homology to functionally characterized proteins. In a recent study, MS was utilized in the functional analysis of the individual proteins involved in the N-linked glycosylation pathway. The ability to insert a functional glycosylation system together with the C. jejuni PEB3 target glycoprotein into Escherichia coli was exploited to study knockout mutations to 11 genes in the pgl locus. The subsequent effect on glycosylation of the target protein was characterized by MS after separation by SDS-PAGE. ES-MS/MS analysis of the variant glycan structure identified the specific role of a number of glycosyltransferases involved in the biosynthesis of the heptasaccharide (Linton et al., 2005) (Fig. 2). Furthermore, MS experiments provided evidence for the essential role of pgl gene products in the N-linked glycosylation pathway and that E. coli-encoded proteins interact with the C. jejuni-derived glycosylation process (Linton et al., 2005). The ability to transfer the C. jejuni glycosylation system into E. coli has recently been exploited to engineer novel glycoproteins expressing O-antigens and opens up the potential for further development of the system for glycoengineering (Feldman et al., 2005).
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). Both the C. jejuni N-linked glycan and the O-linked glycan of N. meningitidis and N. gonorrhoeae pilin contain the sugar residue DATDH (Hegge et al., 2004; Stimson et al., 1995; Wacker et al., 2002). MS/MS experiments on the C. jejuni variant N-linked glycan structures were supportive of the involvement of PglE and PglF in DATDH biosynthesis (Linton et al., 2005), with these enzymes subsequently determined as an aminotransferase and dehydratase involved in the bacillosamine biosynthetic pathway (Schoenhofen et al., 2006). In N. gonorrhoeae, knockout mutations to the gene homologues pglC, pglD and pglF were shown by MS/MS experiments to result in complete abolition of pilin glycosylation (Hegge et al., 2004), indicating their importance in DATDH biosynthesis.
Characterization of C. jejuni flagellin using a combination of MS and NMR techniques has demonstrated that flagellin is modified with the sugar pseudaminic acid (Pse) at 19 Ser/Thr residues. These techniques also revealed heterogeneity in the Pse residues, conferred by substitution of the acetamido groups with acetamidino and hydroxypropionyl groups (Thibault et al., 2001). Annotation of the C. jejuni flagellar glycosylation locus suggests that many of the genes encode proteins involved in the glycosylation process. One particular gene, CJ1293, was demonstrated to be involved in flagellin glycosylation, and a knockout mutation to this gene resulted in C. jejuni that was non-motile (Goon et al., 2003). MS experiments confirmed that the flagellin protein was non-glycosylated. MS strategies have also been employed in the structural determination of the O-linked glycans found on the flagellin of the bacteria H. pylori, P. aeruginosa and L. monocytogenes and the N-linked flagellin glycan of the archaeon M. voltae (Schirm et al., 2003, 2004a, b; Voisin et al., 2005). Novel MS strategies have recently been developed to screen flagellin glycosylation status. The flagellins of C. jejuni, H. pylori, Aeromonas caviae and L. monocytogenes were analysed in a ‘top-down’ approach that revealed both the extent of glycosylation and the nature of the attached carbohydrate (Schirm et al., 2005).
Summary and the future
Bacterial structural glycobiology is undergoing rapid expansion owing to developments in MS instrumentation and associated techniques, which are providing detailed information on the sequences and sites of attachment of glycans in glycosylated proteins. MS is also playing a major role in the study of entire bacterial glycomes, with an impressive amount of information being assembled on, for example, the cell walls of mycobacteria. As the design and use of novel algorithms, databases and software has become fundamental to the successful exploitation of genomic and proteomic data, bioinformatic tools will need to be developed for analysing the information gathered from our expanding knowledge of the bacterial glycome. The precise roles of glycosylation in bacteria have yet to be resolved, but because glycosylation is a costly investment, these modifications are likely to be crucial. The function and influence of bacterial glycosylation on the host immune response are some of the important questions still to be addressed. The new approach of ‘systems biology’ is likely to become central to our development of an understanding of the influence of the bacterial glycome in the biological complexity of host–pathogen interactions. The collaboration of multidisciplinary research teams who combine ‘omics' experimentation with mathematical and computer modelling can only increase our knowledge and understanding of the function of the prokaryotic glycome. Thus, MS strategies for glycomics and glycoproteomics will continue to provide some of the vital structural underpinning of research aimed at understanding host–pathogen interactions.
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ACKNOWLEDGEMENTS |
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