Naturally occurring structural isomers in serum IgA1 O -glycosylation

Journal of Proteome Research

Volumn 11, Issue 2, 2012, Pages 692-702

  Takahashi, Kazuo ^a,b   Smith, Archer D ^a   Poulsen, Knud ^d   Kilian, Mogens ^d   Julian, Bruce A ^b,c   Mestecky, Jiri ^b,c   Novak, Jan ^b   Renfrow, Matthew B ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c University of Alabama at Birmingham   (United States)

^d AARHUS UNIVERSITY   (Denmark)

Author keywords

ECD; electron capture dissociation; FT ICR MS; glycopeptide isomers; IgA1 immunoglobulin; O glycosylation

Indexed keywords

GLYCAN; GLYCOPEPTIDE; IMMUNOGLOBULIN A1; N ACETYLGALACTOSAMINYLTRANSFERASE; N ACETYLNEURAMINIC ACID; O GLYCOPEPTIDE; PARAPROTEIN; SERINE; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GLYCOSYLATION; HINGE REGION; HUMAN; HUMAN TISSUE; IMMUNOGLOBULIN BLOOD LEVEL; ISOMER; PRIORITY JOURNAL; PROTEIN ANALYSIS;

AMINO ACID SEQUENCE; GLYCOPEPTIDES; GLYCOSYLATION; HUMANS; IMMUNOGLOBULIN A; ISOMERISM; MASS SPECTROMETRY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIPLE MYELOMA; MYELOMA PROTEINS;

EID: 84863031236     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr200608q     Document Type: Article

References (69)

1. Mestecky, J.; Moro, I.; Kerr, M. A.; Woof, J. M. Mucosal immunoglobulins. In Mucosal Immunology, 3 rd ed.; Mestecky, J., Bienenstock, J., Lamm, M. E., Mayer, L., McGhee, J. R., Strober, W., Eds.; Elsevier Academic Press: Amsterdam, 2005; pp 153-181.
2. Macpherson, A. J.; McCoy, K. D.; Johansen, F. E.; Brandtzaeg, P. The immune geography of IgA induction and function Mucosal Immunol. 2008, 1 (1) 11-22
3. Mestecky, J.; Russell, M. W. IgA subclasses Monogr. Allergy 1986, 19, 277-301
4. Baenziger, J.; Kornfeld, S. Structure of the carbohydrate units of IgA1 immunoglobulin. II. Structure of the O -glycosidically linked oligosaccharide units J. Biol. Chem. 1974, 249 (22) 7270-81
5. Mattu, T. S.; Pleass, R. J.; Willis, A. C.; Kilian, M.; Wormald, M. R.; Lellouch, A. C.; Rudd, P. M.; Woof, J. M.; Dwek, R. A. The glycosylation and structure of human serum IgA1, Fab, and Fc regions and the role of N -glycosylation on Fc α receptor interactions J. Biol. Chem. 1998, 273 (4) 2260-72
6. Iwase, H.; Ishii-Karakasa, I.; Fujii, E.; Hotta, K.; Hiki, Y.; Kobayashi, Y. Analysis of glycoform of O -glycan from human myeloma immunoglobulin A1 by gas-phase hydrazinolysis following pyridylamination of oligosaccharides Anal. Biochem. 1992, 206 (1) 202-5
7. Iwase, H.; Tanaka, A.; Hiki, Y.; Kokubo, T.; Ishii-Karakasa, I.; Kobayashi, Y.; Hotta, K. Estimation of the number of O -linked oligosaccharides per heavy chain of human serum IgA1 by matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOFMS) analysis of the hinge glycopeptide J. Biochem. 1996, 120 (2) 393-7
8. Novak, J.; Tomana, M.; Kilian, M.; Coward, L.; Kulhavy, R.; Barnes, S.; Mestecky, J. Heterogeneity of O -glycosylation in the hinge region of human IgA1 Mol. Immunol. 2000, 37 (17) 1047-56
9. Renfrow, M. B.; Cooper, H. J.; Tomana, M.; Kulhavy, R.; Hiki, Y.; Toma, K.; Emmett, M. R.; Mestecky, J.; Marshall, A. G.; Novak, J. Determination of aberrant O -glycosylation in the IgA1 hinge region by electron capture dissociation fourier transform-ion cyclotron resonance mass spectrometry J. Biol. Chem. 2005, 280 (19) 19136-45
10. Renfrow, M. B.; Mackay, C. L.; Chalmers, M. J.; Julian, B. A.; Mestecky, J.; Kilian, M.; Poulsen, K.; Emmett, M. R.; Marshall, A. G.; Novak, J. Analysis of O -glycan heterogeneity in IgA1 myeloma proteins by Fourier transform ion cyclotron resonance mass spectrometry: implications for IgA nephropathy Anal. Bioanal. Chem. 2007, 389 (5) 1397-407
11. Wada, Y.; Dell, A.; Haslam, S. M.; Tissot, B.; Canis, K.; Azadi, P.; Backstrom, M.; Costello, C. E.; Hansson, G. C.; Hiki, Y.; Ishihara, M.; Ito, H.; Kakehi, K.; Karlsson, N.; Hayes, C. E.; Kato, K.; Kawasaki, N.; Khoo, K. H.; Kobayashi, K.; Kolarich, D.; Kondo, A.; Lebrilla, C.; Nakano, M.; Narimatsu, H.; Novak, J.; Novotny, M. V.; Ohno, E.; Packer, N. H.; Palaima, E.; Renfrow, M. B.; Tajiri, M.; Thomsson, K. A.; Yagi, H.; Yu, S. Y.; Taniguchi, N. Comparison of methods for profiling O -glycosylation: Human Proteome Organisation Human Disease Glycomics/Proteome Initiative multi-institutional study of IgA1 Mol. Cell. Proteomics 2010, 9 (4) 719-27
12. Takahashi, K.; Wall, S. B.; Suzuki, H.; Smith, A. D.; Hall, S.; Paulsen, K.; Kilian, M.; Mobley, J. A.; Julian, B. A.; Mestecky, J.; Novak, J.; Renfrow, M. B. Clustered O -glycans of IgA1: Defining macro- and micro-heterogeneity by use of electron capture/transfer dissociation Mol. Cell. Proteomics 2010, 9 (11) 2545-57
13. Iwase, H.; Tanaka, A.; Hiki, Y.; Kokubo, T.; Ishii-Karakasa, I.; Nishikido, J.; Kobayashi, Y.; Hotta, K. Application of matrix-assisted laser desorption ionization time-of-flight mass spectrometry to the analysis of glycopeptide-containing multiple O -linked oligosaccharides J. Chromatogr., B: Biomed. Sci. Appl. 1998, 709 (1) 145-9
14. Hiki, Y.; Tanaka, A.; Kokubo, T.; Iwase, H.; Nishikido, J.; Hotta, K.; Kobayashi, Y. Analyses of IgA1 hinge glycopeptides in IgA nephropathy by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry J. Am. Soc. Nephrol. 1998, 9 (4) 577-82
15. Iwase, H.; Tanaka, A.; Hiki, Y.; Kokubo, T.; Sano, T.; Ishii-Karakasa, I.; Hisatani, K.; Kobayashi, Y.; Hotta, K. Analysis of the microheterogeneity of the IgA1 hinge glycopeptide having multiple O -linked oligosaccharides by capillary electrophoresis Anal. Biochem. 2001, 288 (1) 22-7
16. Tarelli, E.; Smith, A. C.; Hendry, B. M.; Challacombe, S. J.; Pouria, S. Human serum IgA1 is substituted with up to six O -glycans as shown by matrix assisted laser desorption ionisation time-of-flight mass spectrometry Carbohydr. Res. 2004, 339 (13) 2329-35
17. Wada, Y.; Tajiri, M.; Ohshima, S. Quantitation of saccharide compositions of O -glycans by mass spectrometry of glycopeptides and its application to rheumatoid arthritis J. Proteome Res. 2010, 9 (3) 1367-73
18. Odani, H.; Hiki, Y.; Takahashi, M.; Nishimoto, A.; Yasuda, Y.; Iwase, H.; Shinzato, T.; Maeda, K. Direct evidence for decreased sialylation and galactosylation of human serum IgA1 Fc O -glycosylated hinge peptides in IgA nephropathy by mass spectrometry Biochem. Biophys. Res. Commun. 2000, 271 (1) 268-74
19. Hiki, Y.; Odani, H.; Takahashi, M.; Yasuda, Y.; Nishimoto, A.; Iwase, H.; Shinzato, T.; Kobayashi, Y.; Maeda, K. Mass spectrometry proves under- O -glycosylation of glomerular IgA1 in IgA nephropathy Kidney Int. 2001, 59 (3) 1077-85
20. Shimozato, S.; Hiki, Y.; Odani, H.; Takahashi, K.; Yamamoto, K.; Sugiyama, S. Serum under-galactosylated IgA1 is increased in Japanese patients with IgA nephropathy Nephrol. Dial. Transplant 2008, 23 (6) 1931-9
21. Iwasaki, H.; Zhang, Y.; Tachibana, K.; Gotoh, M.; Kikuchi, N.; Kwon, Y. D.; Togayachi, A.; Kudo, T.; Kubota, T.; Narimatsu, H. Initiation of O -glycan synthesis in IgA1 hinge region is determined by a single enzyme, UDP- N -acetyl-α-D-galactosamine:polypeptide N -acetylgalactosaminyltransferase 2 J. Biol. Chem. 2003, 278 (8) 5613-21
22. Wandall, H. H.; Irazoqui, F.; Tarp, M. A.; Bennett, E. P.; Mandel, U.; Takeuchi, H.; Kato, K.; Irimura, T.; Suryanarayanan, G.; Hollingsworth, M. A.; Clausen, H. The lectin domains of polypeptide GalNAc-transferases exhibit carbohydrate-binding specificity for GalNAc: lectin binding to GalNAc-glycopeptide substrates is required for high density GalNAc- O -glycosylation Glycobiology 2007, 17 (4) 374-87
23. Tarp, M. A.; Clausen, H. Mucin-type O -glycosylation and its potential use in drug and vaccine development Biochim. Biophys. Acta 2008, 1780 (3) 546-63
24. Suzuki, H.; Kiryluk, K.; Novak, J.; Moldoveanu, Z.; Herr, A. B.; Renfrow, M. B.; Wyatt, R. J.; Scolari, F.; Mestecky, J.; Gharavi, A. G.; Julian, B. A. The pathophysiology of IgA nephropathy J. Am. Soc. Nephrol. 2011, 22 (10) 1795-803
25. Suzuki, H.; Moldoveanu, Z.; Hall, S.; Brown, R.; Vu, H. L.; Novak, L.; Julian, B. A.; Tomana, M.; Wyatt, R. J.; Edberg, J. C.; Alarcon, G. S.; Kimberly, R. P.; Tomino, Y.; Mestecky, J.; Novak, J. IgA1-secreting cell lines from patients with IgA nephropathy produce aberrantly glycosylated IgA1 J. Clin. Invest. 2008, 118 (2) 629-39
26. Novak, J.; Julian, B. A.; Tomana, M.; Mestecky, J. IgA glycosylation and IgA immune complexes in the pathogenesis of IgA nephropathy Semin. Nephrol. 2008, 28 (1) 78-87
27. Tomana, M.; Matousovic, K.; Julian, B. A.; Radl, J.; Konecny, K.; Mestecky, J. Galactose-deficient IgA1 in sera of IgA nephropathy patients is present in complexes with IgG Kidney Int. 1997, 52 (2) 509-16
28. Tomana, M.; Novak, J.; Julian, B. A.; Matousovic, K.; Konecny, K.; Mestecky, J. Circulating immune complexes in IgA nephropathy consist of IgA1 with galactose-deficient hinge region and antiglycan antibodies J. Clin. Invest. 1999, 104 (1) 73-81
29. Moldoveanu, Z.; Wyatt, R. J.; Lee, J. Y.; Tomana, M.; Julian, B. A.; Mestecky, J.; Huang, W. Q.; Anreddy, S. R.; Hall, S.; Hastings, M. C.; Lau, K. K.; Cook, W. J.; Novak, J. Patients with IgA nephropathy have increased serum galactose-deficient IgA1 levels Kidney Int. 2007, 71 (11) 1148-54
30. Allen, A. C.; Bailey, E. M.; Brenchley, P. E.; Buck, K. S.; Barratt, J.; Feehally, J. Mesangial IgA1 in IgA nephropathy exhibits aberrant O -glycosylation: observations in three patients Kidney Int. 2001, 60 (3) 969-73
31. Andre, P. M.; Le Pogamp, P.; Chevet, D. Impairment of jacalin binding to serum IgA in IgA nephropathy J. Clin. Lab. Anal. 1990, 4 (2) 115-9
32. Mestecky, J.; Tomana, M.; Crowley-Nowick, P. A.; Moldoveanu, Z.; Julian, B. A.; Jackson, S. Defective galactosylation and clearance of IgA1 molecules as a possible etiopathogenic factor in IgA nephropathy Contrib. Nephrol. 1993, 104, 172-82
33. Allen, A. C. Abnormal glycosylation of IgA: is it related to the pathogenesis of IgA nephropathy? Nephrol. Dial. Transplant 1995, 10 (7) 1121-4
34. Smith, A. C.; Molyneux, K.; Feehally, J.; Barratt, J. O -glycosylation of serum IgA1 antibodies against mucosal and systemic antigens in IgA nephropathy J. Am. Soc. Nephrol. 2006, 17 (12) 3520-8
35. Lindfors, K.; Suzuki, H.; Novak, J.; Collin, P.; Saavalainen, P.; Koskinen, L. L.; Maki, M.; Kaukinen, K. Galactosylation of serum IgA1 O -glycans in celiac disease J. Clin. Immunol. 2011, 31 (1) 74-9
36. Dechant, M.; Beyer, T.; Schneider-Merck, T.; Weisner, W.; Peipp, M.; van de Winkel, J. G.; Valerius, T. Effector mechanisms of recombinant IgA antibodies against epidermal growth factor receptor J. Immunol. 2007, 179 (5) 2936-43
37. Dechant, M.; Vidarsson, G.; Stockmeyer, B.; Repp, R.; Glennie, M. J.; Gramatzki, M.; van De Winkel, J. G.; Valerius, T. Chimeric IgA antibodies against HLA class II effectively trigger lymphoma cell killing Blood 2002, 100 (13) 4574-80
38. Ashline, D. J.; Lapadula, A. J.; Liu, Y. H.; Lin, M.; Grace, M.; Pramanik, B.; Reinhold, V. N. Carbohydrate structural isomers analyzed by sequential mass spectrometry Anal. Chem. 2007, 79 (10) 3830-42
39. Aoki, K.; Porterfield, M.; Lee, S. S.; Dong, B.; Nguyen, K.; McGlamry, K. H.; Tiemeyer, M. The diversity of O -linked glycans expressed during Drosophila melanogaster development reflects stage- and tissue-specific requirements for cell signaling J. Biol. Chem. 2008, 283 (44) 30385-400
40. Prien, J. M.; Huysentruyt, L. C.; Ashline, D. J.; Lapadula, A. J.; Seyfried, T. N.; Reinhold, V. N. Differentiating N -linked glycan structural isomers in metastatic and nonmetastatic tumor cells using sequential mass spectrometry Glycobiology 2008, 18 (5) 353-66
41. Mestecky, J.; Kilian, M. Immunoglobulin A (IgA) Methods Enzymol. 1985, 116, 37-75
42. Moore, J. S.; Kulhavy, R.; Tomana, M.; Moldoveanu, Z.; Suzuki, H.; Brown, R.; Hall, S.; Kilian, M.; Poulsen, K.; Mestecky, J.; Julian, B. A.; Novak, J. Reactivities of N -acetylgalactosamine-specific lectins with human IgA1 proteins Mol. Immunol. 2007, 44 (10) 2598-604
43. Sullivan, B.; Addona, T. A.; Carr, S. A. Selective detection of glycopeptides on ion trap mass spectrometers Anal. Chem. 2004, 76 (11) 3112-8
44. Rebecchi, K. R.; Wenke, J. L.; Go, E. P.; Desaire, H. Label-free quantitation: a new glycoproteomics approach J. Am. Soc. Mass Spectrom. 2009, 20 (6) 1048-59
45. Perdivara, I.; Petrovich, R.; Allinquant, B.; Deterding, L. J.; Tomer, K. B.; Przybylski, M. Elucidation of O -glycosylation structures of the β-amyloid precursor protein by liquid chromatography-mass spectrometry using electron transfer dissociation and collision induced dissociation J. Proteome Res. 2009, 8 (2) 631-42
46. Hakansson, K.; Cooper, H. J.; Emmett, M. R.; Costello, C. E.; Marshall, A. G.; Nilsson, C. L. Electron capture dissociation and infrared multiphoton dissociation MS/MS of an N -glycosylated tryptic peptic to yield complementary sequence information Anal. Chem. 2001, 73 (18) 4530-6
47. Hakansson, K.; Chalmers, M. J.; Quinn, J. P.; McFarland, M. A.; Hendrickson, C. L.; Marshall, A. G. Combined electron capture and infrared multiphoton dissociation for multistage MS/MS in a Fourier transform ion cyclotron resonance mass spectrometer Anal. Chem. 2003, 75 (13) 3256-62
48. Darula, Z.; Medzihradszky, K. F. Affinity enrichment and characterization of mucin core-1 type glycopeptides from bovine serum Mol. Cell. Proteomics 2009, 8 (11) 2515-26
49. Good, D. M.; Wirtala, M.; McAlister, G. C.; Coon, J. J. Performance characteristics of electron transfer dissociation mass spectrometry Mol. Cell. Proteomics 2007, 6 (11) 1942-51
50. Suzuki, H.; Fan, R.; Zhang, Z.; Brown, R.; Hall, S.; Julian, B. A.; Chatham, W. W.; Suzuki, Y.; Wyatt, R. J.; Moldoveanu, Z.; Lee, J. Y.; Robinson, J.; Tomana, M.; Tomino, Y.; Mestecky, J.; Novak, J. Aberrantly glycosylated IgA1 in IgA nephropathy patients is recognized by IgG antibodies with restricted heterogeneity J. Clin. Invest. 2009, 119 (6) 1668-77
51. Sames, D.; Chen, X. T.; Danishefsky, S. J. Convergent total synthesis of a tumour-associated mucin motif Nature 1997, 389 (6651) 587-91
52. Dall'Olio, F.; Chiricolo, M. Sialyltransferases in cancer Glycoconj. J. 2001, 18 (11-12) 841-50
53. Marcos, N. T.; Pinho, S.; Grandela, C.; Cruz, A.; Samyn-Petit, B.; Harduin-Lepers, A.; Almeida, R.; Silva, F.; Morais, V.; Costa, J.; Kihlberg, J.; Clausen, H.; Reis, C. A. Role of the human ST6GalNAc-I and ST6GalNAc-II in the synthesis of the cancer-associated sialyl-Tn antigen Cancer Res. 2004, 64 (19) 7050-7
54. van Schooten, C. J.; Denis, C. V.; Lisman, T.; Eikenboom, J. C.; Leebeek, F. W.; Goudemand, J.; Fressinaud, E.; van den Berg, H. M.; de Groot, P. G.; Lenting, P. J. Variations in glycosylation of von Willebrand factor with O -linked sialylated T antigen are associated with its plasma levels Blood 2007, 109 (6) 2430-7
55. Ohyabu, N.; Hinou, H.; Matsushita, T.; Izumi, R.; Shimizu, H.; Kawamoto, K.; Numata, Y.; Togame, H.; Takemoto, H.; Kondo, H.; Nishimura, S. An essential epitope of anti-MUC1 monoclonal antibody KL-6 revealed by focused glycopeptide library J. Am. Chem. Soc. 2009, 131 (47) 17102-9
56. Medzihradszky, K. F.; Gillece-Castro, B. L.; Settineri, C. A.; Townsend, R. R.; Masiarz, F. R.; Burlingame, A. L. Structure determination of O -linked glycopeptides by tandem mass spectrometry Biomed. Environ. Mass Spectrom. 1990, 19 (12) 777-81
57. Medzihradszky, K. F.; Gillece-Castro, B. L.; Townsend, R. R.; Burlingame, A. L.; Hardy, M. R. Structural elucidation of O -linked glycopeptides by high energy collision-induced dissociation J. Am. Soc. Mass. Spectrom. 1996, 7 (4) 319-28
58. Zaia, J. Mass spectrometry of oligosaccharides Mass Spectrom. Rev. 2004, 23 (3) 161-227
59. Sagi, D.; Peter-Katalinic, J.; Conradt, H. S.; Nimtz, M. Sequencing of tri- and tetraantennary N -glycans containing sialic acid by negative mode ESI QTOF tandem MS J. Am. Soc. Mass Spectrom. 2002, 13 (9) 1138-48
60. Arnold, J. N.; Wormald, M. R.; Sim, R. B.; Rudd, P. M.; Dwek, R. A. The impact of glycosylation on the biological function and structure of human immunoglobulins Annu. Rev. Immunol. 2007, 25, 21-50
61. Malhotra, R.; Wormald, M. R.; Rudd, P. M.; Fischer, P. B.; Dwek, R. A.; Sim, R. B. Glycosylation changes of IgG associated with rheumatoid arthritis can activate complement via the mannose-binding protein Nat. Med. 1995, 1 (3) 237-43
62. Moore, J. S.; Wu, X.; Kulhavy, R.; Tomana, M.; Novak, J.; Moldoveanu, Z.; Brown, R.; Goepfert, P. A.; Mestecky, J. Increased levels of galactose-deficient IgG in sera of HIV-1-infected individuals AIDS 2005, 19 (4) 381-9
63. Novak, J.; Tomana, M.; Shah, G. R.; Brown, R.; Mestecky, J. Heterogeneity of IgG glycosylation in adult periodontal disease J. Dent. Res. 2005, 84 (10) 897-901
64. Rademacher, T. W.; Parekh, R. B.; Dwek, R. A.; Isenberg, D.; Rook, G.; Axford, J. S.; Roitt, I. The role of IgG glycoforms in the pathogenesis of rheumatoid arthritis Springer Semin. Immunopathol. 1988, 10 (2-3) 231-49
65. Tomana, M.; Schrohenloher, R. E.; Reveille, J. D.; Arnett, F. C.; Koopman, W. J. Abnormal galactosylation of serum IgG in patients with systemic lupus erythematosus and members of families with high frequency of autoimmune diseases Rheumatol. Int. 1992, 12 (5) 191-4
66. Troelsen, L. N.; Garred, P.; Madsen, H. O.; Jacobsen, S. Genetically determined high serum levels of mannose-binding lectin and agalactosyl IgG are associated with ischemic heart disease in rheumatoid arthritis Arthritis Rheum. 2007, 56 (1) 21-9
67. Youings, A.; Chang, S. C.; Dwek, R. A.; Scragg, I. G. Site-specific glycosylation of human immunoglobulin G is altered in four rheumatoid arthritis patients Biochem. J. 1996, 314 (Pt 2) 621-30
68. Durham, M.; Regnier, F. E. Targeted glycoproteomics: serial lectin affinity chromatography in the selection of O -glycosylation sites on proteins from the human blood proteome J. Chromatogr., A 2006, 1132 (1-2) 165-73
69. Schwientek, T.; Mandel, U.; Roth, U.; Muller, S.; Hanisch, F. G. A serial lectin approach to the mucin-type O -glycoproteome of Drosophila melanogaster S2 cells Proteomics 2007, 7 (18) 3264-77