Glycoproteomic analysis of human fibrinogen reveals novel regions of O-glycosylation

Journal of Proteome Research

Volumn 11, Issue 12, 2012, Pages 5804-5814

  Zauner, Gerhild ^a   Hoffmann, Marcus ^b   Rapp, Erdmann ^b   Koeleman, Carolien A M ^a   Dragan, Irina ^a   Deelder, André M ^a   Wuhrer, Manfred ^a   Hensbergen, Paul J ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MAX PLANCK INSTITUTE FOR DYNAMICS OF COMPLEX TECHNICAL SYSTEMS   (Germany)

Author keywords

fibrinogen; glycopeptide; O glycosylation; proteinase K; trypsin

Indexed keywords

ANTIGEN; ASPARAGINE; FIBRINOGEN; GLUTAMINE; GLYCINE; PROTEINASE K; SERINE; THREONINE; TRYPSIN;

AMINO ACID SEQUENCE; ARTICLE; BETA CHAIN; BLOOD CLOTTING; CONTROLLED STUDY; DEAMINATION; GLYCOSYLATION; HUMAN; ION TRAP MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN MOTIF; PROTEOMICS; SIALYLATION; STOICHIOMETRY;

AMINO ACID SEQUENCE; BINDING SITES; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDOPEPTIDASE K; FIBRINOGEN; GLYCOPEPTIDES; GLYCOSYLATION; HUMANS; MOLECULAR SEQUENCE DATA; NANOTECHNOLOGY; OLIGOSACCHARIDES; POLYSACCHARIDES; PROTEOLYSIS; PROTEOME; PROTEOMICS; SEQUENCE ANALYSIS, PROTEIN; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TRYPSIN;

EID: 84870891070     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr3005937     Document Type: Article

References (37)

1. Weisel, J. W. Fibrinogen and fibrin Adv. Protein Chem. 2005, 70, 247-299
2. Hantgan, R. R. An investigation of fibrin-platelet adhesive interactions by microfluorimetry Biochim. Biophys. Acta 1987, 927 (1) 55-64
3. Lang, T.; Johanning, K.; Metzler, H.; Piepenbrock, S.; Solomon, C.; Rahe-Meyer, N.; Tanaka, K. A. The effects of fibrinogen levels on thromboelastometric variables in the presence of thrombocytopenia Anesth. Analg. 2009, 108 (3) 751-758
4. Fu, Y.; Zhang, J. Z.; Redman, C. M.; Grieninger, G. Formation of the human fibrinogen subclass fib420: disulfide bonds and glycosylation in its unique (alphaE chain) domains Blood 1998, 92 (9) 3302-3308
5. Marchi, R.; Meyer, M.; de, B. N.; Soria, J.; Arocha-Pinango, C. L.; Weisel, J. W. Biophysical characterization of fibrinogen Caracas I with an Aalpha-chain truncation at Aalpha-466 Ser: identification of the mutation and biophysical characterization of properties of clots from plasma and purified fibrinogen Blood Coagulation Fibrinolysis 2004, 15 (4) 285-293
6. Marchi, R.; Carvajal, Z.; Weisel, J. W. Comparison of the effect of different homocysteine concentrations on clot formation using human plasma and purified fibrinogen Thromb. Haemostasis 2008, 99 (2) 451-452
7. Marchi, R.; Rojas, H.; Castillo, O.; Kanzler, D. Structure of fibrin network of two abnormal fibrinogens with mutations in the alphaC domain on the human dermal microvascular endothelial cells 1 Blood Coagul Fibrinolysis 2011, 22 (8) 706-711
8. Mirshahi, M.; Soria, J.; Soria, C.; Bertrand, O.; Mirshahi, M.; Basdevant, A. Glycosylation of human fibrinogen and fibrin in vitro. Its consequences on the properties of fibrin(ogen) Thromb. Res. 1987, 48 (3) 279-289
9. Pieters, M.; van Zyl, D. G.; Rheeder, P.; Jerling, J. C.; Loots, d. T.; van der Westhuizen, F. H.; Gottsche, L. T.; Weisel, J. W. Glycation of fibrinogen in uncontrolled diabetic patients and the effects of glycaemic control on fibrinogen glycation Thromb. Res. 2007, 120 (3) 439-446
10. Pieters, M.; Covic, N.; van der Westhuizen, F. H.; Nagaswami, C.; Baras, Y.; Toit, L. D.; Jerling, J. C.; Elgar, D.; Edmondson, K. S.; van Zyl, D. G.; Rheeder, P.; Weisel, J. W. Glycaemic control improves fibrin network characteristics in type 2 diabetes-a purified fibrinogen model Thromb. Haemostasis 2008, 99 (4) 691-700
11. L'Hote, C.; Berger, S.; Karamanos, Y. O-glycosylation of fibrinogen from different mammalian species as revealed by the binding of Escherichia coli biotinylated lectins Thromb. Haemostasis 1996, 76 (5) 710-714
12. L'Hote, C.; Berger, S.; Bourgerie, S.; Duval-Iflah, Y.; Julien, R.; Karamanos, Y. Use of porcine fibrinogen as a model glycoprotein to study the binding specificity of the three variants of K88 lectin Infect. Immun. 1995, 63 (5) 1927-1932
13. Pacchiarotta, T.; Hensbergen, P. J.; Wuhrer, M.; van, N. C.; Nevedomskaya, E.; Derks, R. J.; Schoenmaker, B.; Koeleman, C. A.; van, D. J.; Deelder, A. M.; Mayboroda, O. A. Fibrinogen alpha chain O-glycopeptides as possible markers of urinary tract infection J Proteomics 2012, 75 (3) 1067-1073
14. Watt, K. W.; Cottrell, B. A.; Strong, D. D.; Doolittle, R. F. Amino acid sequence studies on the alpha chain of human fibrinogen. Overlapping sequences providing the complete sequence Biochemistry 1979, 18 (24) 5410-5416
15. Clowers, B. H.; Dodds, E. D.; Seipert, R. R.; Lebrilla, C. B. Site determination of protein glycosylation based on digestion with immobilized nonspecific proteases and Fourier transform ion cyclotron resonance mass spectrometry J. Proteome Res. 2007, 6 (10) 4032-4040
16. Dodds, E. D.; Seipert, R. R.; Clowers, B. H.; German, J. B.; Lebrilla, C. B. Analytical performance of immobilized Pronase for glycopeptide footprinting and implications for surpassing reductionist glycoproteomics J. Proteome Res. 2009, 8 (2) 502-512
17. Nwosu, C. C.; Seipert, R. R.; Strum, J. S.; Hua, S. S.; An, H. J.; Zivkovic, A. M.; German, B. J.; Lebrilla, C. B. Simultaneous and extensive site-specific N- and O-glycosylation analysis in protein mixtures J. Proteome Res. 2011, 10 (5) 2612-2624
18. Froehlich, J. W.; Barboza, M.; Chu, C.; Lerno, L. A., Jr.; Clowers, B. H.; Zivkovic, A. M.; German, J. B.; Lebrilla, C. B. Nano-LC-MS/MS of glycopeptides produced by nonspecific proteolysis enables rapid and extensive site-specific glycosylation determination Anal. Chem. 2011, 83 (14) 5541-5547
19. Songsrirote, K.; Li, Z.; Ashford, D.; Bateman, A.; Thomas-Oates, J. Development and application of mass spectrometric methods for the analysis of progranulin N-glycosylation J. Proteomics 2010, 73 (8) 1479-1490
20. Zauner, G.; Koeleman, C. A.; Deelder, A. M.; Wuhrer, M. Protein glycosylation analysis by HILIC-LC-MS of Proteinase K-generated N- and O-glycopeptides J. Sep. Sci. 2010, 33 (6-7) 903-910
21. Zauner, G.; Koeleman, C. A.; Deelder, A. M.; Wuhrer, M. Mass spectrometric O-glycan analysis after combined O-glycan release by beta-elimination and 1-phenyl-3-methyl-5-pyrazolone labeling Biochim. Biophys. Acta 2012, 1820, 1420-1428
22. Huddleston, M. J.; Bean, M. F.; Carr, S. A. Collisional fragmentation of glycopeptides by electrospray ionization LC/MS and LC/MS/MS: methods for selective detection of glycopeptides in protein digests Anal. Chem. 1993, 74 (7) 877-884
23. Kollman, J. M.; Pandi, L.; Sawaya, M. R.; Riley, M.; Doolittle, R. F. Crystal structure of human fibrinogen Biochemistry 2009, 48 (18) 3877-3886
24. Zhang, J. Z.; Redman, C. Fibrinogen assembly and secretion. Role of intrachain disulfide loops J. Biol. Chem. 1996, 271 (47) 30083-30088
25. Townsend, R. R.; Hilliker, E.; Li, Y. T.; Laine, R. A.; Bell, W. R.; Lee, Y. C. Carbohydrate structure of human fibrinogen. Use of 300-MHz 1H-NMR to characterize glycosidase-treated glycopeptides J. Biol. Chem. 1982, 257 (16) 9704-9710
26. Townsend, R. R.; Heller, D. N.; Fenselau, C. C.; Lee, Y. C. Determination of the sialylation pattern of human fibrinogen glycopeptides with fast atom bombardment Biochemistry 1984, 23 (26) 6389-6392
27. Wopereis, S.; Lefeber, D. J.; Morava, E.; Wevers, R. A. Mechanisms in protein O-glycan biosynthesis and clinical and molecular aspects of protein O-glycan biosynthesis defects: a review Clin Chem 2006, 52 (4) 574-600
28. Henschen-Edman, A. H. Fibrinogen non-inherited heterogeneity and its relationship to function in health and disease Ann. N. Y. Acad. Sci. 2001, 936, 580-593
29. Darula, Z.; Sherman, J.; Medzihradszky, K. F. How to dig deeper? Improved enrichment methods for mucin core-1 type glycopeptides Mol. Cell. Proteomics 2012, 11, O111.016774
30. Darula, Z.; Medzihradszky, K. F. Affinity enrichment and characterization of mucin core-1 type glycopeptides from bovine serum Mol. Cell. Proteomics 2009, 8 (11) 2515-2526
31. Harvey, D. J.; Mattu, T. S.; Wormald, M. R.; Royle, L.; Dwek, R. A.; Rudd, P. M. Internal residue loss: rearrangements occurring during the fragmentation of carbohydrates derivatized at the reducing terminus Anal. Chem. 2002, 74 (4) 734-740
32. Wuhrer, M.; Koeleman, C. A.; Deelder, A. M. Hexose rearrangements upon fragmentation of N-glycopeptides and reductively aminated N-glycans Anal. Chem. 2009, 81 (11) 4422-4432
33. Wuhrer, M.; Deelder, A. M.; van der Burgt, Y. E. Mass spectrometric glycan rearrangements Mass Spectrom. Rev. 2011, 30 (4) 664-680
34. Halim, A.; Nilsson, J.; Ruetschi, U.; Hesse, C.; Larson, G. Human urinary glycoproteomics; attachment site specific analysis of N- and O-linked glycosylations by CID and ECD Mol. Cell. Proteomics 2012, 11 (4) M111
35. Bach-Gansmo, E. T.; Halvorsen, S.; Godal, H. C.; Skjonsberg, O. H. Impaired coagulation of fibrinogen due to digestion of the C-terminal end of the A alpha-chain by human neutrophil elastase Thromb. Res. 1994, 73 (1) 61-68
36. Bach-Gansmo, E. T.; Halvorsen, S.; Godal, H. C.; Skjonsberg, O. H. Degradation of the alpha-chain of fibrin by human neutrophil elastase reduces the stimulating effect of fibrin on plasminogen activation Thromb. Res. 1994, 75 (3) 307-317
37. Prieto-Garcia, A.; Zheng, D.; Adachi, R.; Xing, W.; Lane, W. S.; Chung, K.; Anderson, P.; Hansbro, P. M.; Castells, M.; Stevens, R. L. Mast cell restricted mouse and human tryptase.heparin complexes hinder thrombin-induced coagulation of plasma and the generation of fibrin by proteolytically destroying fibrinogen J. Biol. Chem. 2012, 287 (11) 7834-7844