New insights into the glycosylation of the surface layer protein SgsE from Geobacillus stearothermophilus NRS 2004/3a

Journal of Bacteriology

Volumn 188, Issue 22, 2006, Pages 7914-7921

  Steiner, Kerstin ^a   Pohlentz, Gottfried ^b   Dreisewerd, Klaus ^b   Berkenkamp, Stefan ^b,c   Messner, Paul ^a   Peter Katalinić, Jasna ^b   Schäffer, Christina ^a  

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

^b UNIVERSITY OF MÜNSTER   (Germany)

^c Sequenom GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARBOHYDRATE; GLYCAN; GLYCOPROTEIN; PROTEIN SGSE; PROTEIN SUBUNIT; RHAMNOSE; SERINE; THREONINE; TRISACCHARIDE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BIOTECHNOLOGY; GEOBACILLUS STEAROTHERMOPHILUS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR WEIGHT; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; SOLUBILITY; TIME OF FLIGHT MASS SPECTROMETRY;

BACILLACEAE; BACTERIAL PROTEINS; CATALYTIC DOMAIN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GLYCOPROTEINS; GLYCOSYLATION; MEMBRANE PROTEINS; MOLECULAR WEIGHT; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

GEOBACILLUS STEAROTHERMOPHILUS;

EID: 33751074462     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00802-06     Document Type: Article

References (45)

1. Allmaier, G., C. Schäffer, P. Messner, U. Rapp, and F. J. Mayer-Posner. 1995. Accurate determination of the molecular weight of the major surface layer protein isolated from Clostridium thermosaccharolyticum by time-of-flight mass spectrometry. J. Bacteriol. 177:1402-1404.
2. Berkenkamp, S., C. Menzel, M. Karas, and F. Hillenkamp. 1997. Performance of infrared matrix-assisted laser desorption/ionization mass spectrometry with lasers emitting in the 3 μm wavelength range. Rapid Commun. Mass Spectrom. 11:1399-1406.
3. Bock, K., J. Schuster-Kolbe, E. Altman, G. Allmaier, B. Stahl, R. Christian, U. B. Sleytr, and P. Messner. 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. 269:7137-7144.
4. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
5. 2+ ions for their detection during peptide microsequencing. Biochem. J. 280:261-265.
6. Christian, R., G. Schulz, J. Schuster-Kolbe, G. Allmaier, E. R. Schmid, U. B. Sleytr, and P. Messner. 1993. Complete structure of the tyrosine-linked saccharide moiety from the surface layer glycoprotein of Closiridium thermohydrosulfuricum S102-70. J. Bacteriol. 175:1250-1256.
7. Christian, R., G. Schulz, F. M. Unger, P. Messner, Z. Küpcü, and U. B. Sleytr. 1986. Structure of a rhamnan from the surface-layer glycoprotein of Bacillus stearothermophilus strain NRS 2004/3a. Carbohydr. Res. 150:265-272.
8. Cristoni, S., and L. R. Bernardi. 2003. Development of new methodologies for the mass spectrometry study of bioorganic macromolecules. Mass Spectrom. Rev. 22:369-406.
9. Dreisewerd, K., J. Müthing, A. Rohlfing, I. Meisen, Z. Vukelić, J. Peter-Katalinić, F. Hillenkamp, and S. Berkenkamp. 2005. Analysis of gangliosides directly from thin-layer chromatography plates by infrared matrix-assisted laser desorption/ionization orthogonal time-of-flight mass spectrometry with a glycerol matrix. Anal. Chem. 77:4098-4107.
10. Hanisch, F. G., M. Jovanovic, and J. Peter-Katalinić. 2001. Glycoprotein identification and localization of O-glycosylation sites by mass spectrometric analysis of deglycosylated/alkylaminylated peptide fragments. Anal. Biochem. 290:47-59.
11. Hart, C., B. Schulenberg, T. H. Steinberg, W. Y. Leung, and W. F. Patton. 2003. Detection of glycoproteins in polyacrylamide gels and on electroblots using Pro-Q Emerald 488 dye, a fluorescent periodate Schiff-base stain. Electrophoresis 24:588-598.
12. Harvey, D. J. 2005. Proteomic analysis of glycosylation: structural determination of N- and O-linked glycans by mass spectrometry. Expert Rev. Proteomics 2:87-101.
13. Huang, Y., T. Konse, Y. Mechref, and M. V. Novotny. 2002. Matrix-assisted laser desorption/ionization mass spectrometry compatible beta-elimination of O-linked oligosaccharides. Rapid Commun. Mass Spectrom. 16:1199-1204.
14. Küpcü, Z., L. März, P. Messner, and U. B. Sleytr. 1984. Evidence for the glycoprotein nature of the crystalline cell wall surface layer of Bacillus stearothermophilus strain NRS2004/3a. FEBS Lett. 173:185-190.
15. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
16. Lechner, J., and M. Sumper. 1987. The primary structure of a procaryotic glycoprotein. Cloning and sequencing of the cell surface glycoprotein gene of halobacteria. J. Biol. Chem. 262:9724-9729.
17. Mattila, K., J. Siltainsuu, L. Balaspiri, M. Ora, and H. Lonnberg. 2005. Derivatization of phosphopeptides with mercapto- and amino-functionalized conjugate groups by phosphate elimination and subsequent Michael addition. Org. Biomol. Chem. 3:3039-3044.
18. Mauri, P. L., P. G. Pietta, A. Maggioni, M. Cerquetti, A. Sebastianelli, and P. Mastrantonio. 1999. Characterization of surface layer proteins from Clostridium difficile by liquid chromatography/electrospray ionization mass spectrometry. Rapid Commun. Mass Spectrom. 13:695-703.
19. Messner, P. 2004. Prokaryotic glycoproteins: unexplored but important. J. Bacteriol. 186:2517-2519.
20. Messner, P., D. Pum, and U. B. Sleytr. 1986. Characterization of the ultrastructure and the self-assembly of the surface layer of Bacillus stearothermophilus strain NRS 2004/3a. J. Ultrastruct. Mol. Struct. Res. 97:73-88.
21. Messner, P., R. Christian, C. Neuninger, and G. Schulz. 1995. Similarity of "core" structures in two different glycans of tyrosine-linked eubacterial S-layer glycoproteins. J. Bacteriol. 177:2188-2193.
22. Messner, P., F. Hollaus, and U. B. Sleytr. 1984. Paracrystalline cell wall surface layers of different Bacillus stearothermophilus strains. Int. J. Syst. Bacteriol. 34:202-210.
23. Messner, P., and C. Schäffen 2003. Prokaryotic glycoproteins. Fortschr. Chem. Org. Naturst. 85:51-124.
24. Messner, P., J. Schuster-Kolbe, C. Schäffer, U. B. Sleytr, and R. Christian. 1993. Glycoprotein nature of select bacterial S-layers, p. 95-107. In T. J. Beveridge and S. F. Koval (ed.), Advances in bacterial paracrystalline surface layers. Plenum Publishing Corp., New York, N.Y.
25. Messner, P., and U. B. Sleytr. 1988. Separation and purification of S-layers from gram-positive and gram-negative bacteria, p. 97-104. In I. Hancock and I. R. Poxton (ed.), Bacterial cell surface techniques. John Wiley & Sons, Chichester, United Kingdom.
26. Nazina, T. N., T. P. Tourova, A. B. Poltaraus, E. V. Novikova, A. A. Grigoryan, A. E. Ivanova, A. M. Lysenko, V. V. Petrunyaka, G. A. Osipov, S. S. Belyaev, and M. V. Ivanov. 2001. Taxonomic study of aerobic thermophilic bacilli: descriptions of Geobacillus subtetraneus gen. nov., sp. nov. and Geobacillus uzenensis sp. nov. from petroleum reservoirs and transfer of Bacillus stearothermophilus, Bacillus thermocatenulatus, Bacillus thermoleovorans. Bacillus kaustophilus, Bacillus thermodenitrificans to Geobacillus as the new combinations G. stearothermophilus, G. thermoleovorans, G. kaustophilus, G. thermoglucosidasius and G. thermodenitrificans. Int. J. Syst. Evol. Microbiol. 51:433-446.
27. Novotny, R., C. Schäffer, J. Strauss, and P. Messner. 2004. S-layer glycan-specific loci on the chromosome of Geobacillus stearothermophilus NRS 2004/3a and dTDP-L-rhamnose biosynthesis potential of G. stearothermophilus strains. Microbiology 150:953-965.
28. Overberg, A., M. Karas, U. Bahr, R. Kaufmann, and F. Hillenkamp. 1990. Matrix-assisted infrared-laser (2.94 μm) desorption ionization mass-spectrometry of large biomolecules. Rapid Commun. Mass Spectrom. 4:293-296.
29. Packer, N. H., M. A. Lawson, D. R. Jardine, and J. W. Redmond. 1998. A general approach to desalting oligosaccharides released from glycoproteins. Glycoconj. J. 15:737-747.
30. Peter-Katalinić, J. 2005. O-glycosylation of proteins. Methods Enzymol. 405:139-171.
31. Pulfer, M., and R. C. Murphy. 2003. Electrospray mass spectrometry of phospholipids. Mass Spectrom. Rev. 22:332-364.
32. Rademaker, G. J., S. A. Pergantis, L. Blok-Tip, J. I. Langridge, A. Kleen, and J. E. Thomas-Oates. 1998. Mass spectrometric determination of the sites of O-glycan attachment with low picomolar sensitivity. Anal. Biochem. 257:149-160.
33. Schäffer, C., and P. Messner. 2004. Surface-layer glycoproteins: an example for the diversity of bacterial glycosylation with promising impacts on nanobiotechnology. Glycobiology 14:31R-42R.
34. Schäffer, C., N. Müller, R. Christian, M. Graninger, T. Wugeditsch, A. Scheberl, and P. Messner. 1999. Complete glycan structure of the S-layer glycoprotein of Aneurinibacillus thermoaerophilus GS4-97. Glycobiology 9:407-414.
35. Schäffer, C., T. Wugeditsch, H. Kählig, A. Scheberl, S. Zayni, and P. Messner. 2002. The surface layer (S-layer) glycoprotein of Geobacillus stearothermophilus NRS 2004/3a. Analysis of its glycosylation. J. Biol. Chem. 277:6230-6239.
36. Schmidt, M. A., L. W. Riley, and I. Benz. 2003. Sweet new world: glycoproteins in bacterial pathogens. Trends Microbiol. 11:554-561.
37. Sleytr, U. B., and P. Messner. 2003. Crystalline bacterial cell surface layers (S layers), p. 286-293. In M. Schaechter (ed.), Desk encyclopedia of microbiology. Elsevier Science, Inc., San Diego, Calif.
38. Steiner, K. 2006. Unravelling details of the S-layer glycoprotein of Geobacillus stearothermophilus NRS 2004/3a. Ph.D. thesis. University of Natural Resources and Applied Life Sciences, Vienna, Austria.
39. Sumper, M., E. Berg, R. Mengele, and I. Strobel. 1990. Primary structure and glycosylation of the S-layer protein of Haloferax volcanii. J. Bacteriol. 172:7111-7118.
40. Szymanski, C. M., and B. W. Wren. 2005. Protein glycosylation in bacterial mucosal pathogens. Nat. Rev. Microbiol. 3:225-237.
41. Upreti, R. K., M. Kumar, and V. Shankar. 2003. Bacterial glycoproteins: functions, biosynthesis and applications. Proteomics 3:363-379.
42. Vaidyanathan, S., C. L. Winder, S. C. Wade, D. B. Kell, and R. Goodacre. 2002. Sample preparation in matrix-assisted laser desorption/ionization mass spectrometry of whole bacterial cells and the detection of high mass (>20 kDa) proteins. Rapid Commun. Mass Spectrom. 16:1276-1286.
43. Wacker, M., D. Linton, P. G. Hitchen, M. Nita-Lazar, S. M. Haslam, S. J. North, M. Panico, H. R. Morris, A. Dell, B. W. Wren, and M. Aebi. 2002. N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science 298:1790-1793.
44. Wugeditsch, T., N. E. Zachara, M. Puchberger, P. Kosma, A. A. Gooley, and P. Messner. 1999. Structural heterogeneity in the core oligosaccharide of the S-layer glycoprotein from Aneurinibacillus thermoaerophilus DSM 10155. Glycobiology 9:787-795.
45. Zaia, J. 2004. Mass spectrometry of oligosaccharides. Mass Spectrom. Rev. 23:161-227.