Quantifying carbohydrate-protein interactions by electrospray ionization mass spectrometry analysis

Biochemistry

Volumn 51, Issue 21, 2012, Pages 4244-4253

  El Hawiet, Amr ^a   Kitova, Elena N ^a   Klassen, John S ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE AREA; ANALYTICAL METHOD; BINDING EQUILIBRIA; BIOLOGICAL PROCESS; CARBOHYDRATE-PROTEIN INTERACTIONS; COMMON SOURCE; ELECTROSPRAY IONIZATION MASS SPECTROMETRY; IN-VITRO; LIBRARY SCREENING; LIGAND BINDING; LOW LEVEL; SAMPLE CONSUMPTION;

BIOCHEMISTRY; MASS SPECTROMETRY; STOICHIOMETRY;

CARBOHYDRATES;

ANALYTICAL ERROR; ARTICLE; BINDING AFFINITY; ELECTROSPRAY MASS SPECTROMETRY; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CARBOHYDRATE INTERACTION; STOICHIOMETRY;

CARBOHYDRATE METABOLISM; CARBOHYDRATES; KINETICS; LIGANDS; MODELS, CHEMICAL; PROTEIN BINDING; PROTEINS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

EID: 84861581271     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300436x     Document Type: Article

References (80)

1. Ghazarian, H., Idoni, B., and Oppenheimer, S. B. (2011) A glycobiology review: Carbohydrates, lectins and implications in cancer therapeutics Acta Histochem. 113, 236-247
2. Lis, H. and Sharon, N. (1998) Lectins: Carbohydrate-specific proteins that mediate cellular recognition Chem. Rev. 98, 637-674
3. Sharon, N. and Lis, H. (1993) Carbohydrates in cell recognition Sci. Am. 268, 82-89
4. Quiocho, F. A. (1986) Carbohydrate-binding proteins: Tertiary structures and protein-sugar interactions Annu. Rev. Biochem. 55, 287-315
5. Holgersson, J., Gustafsson, A., and Breimer, M. E. (2005) Characteristics of protein-carbohydrate interactions as a basis for developing novel carbohydrate-based antirejection therapies Immunol. Cell Biol. 83, 694-708
6. Weis, W. I. and Drickamer, K. (1996) Structural basis of lectin-carbohydrate recognition Annu. Rev. Biochem. 65, 441-473
7. Sacchettini, J. C., Baum, L. G., and Brewer, C. F. (2001) Multivalent protein-carbohydrate interactions. A new paradigm for supermolecular assembly and signal transduction Biochemistry 40, 3009-3015
8. Utsuno, K. and Uludag, H. (2010) Thermodynamics of polyethylenimine-DNA binding and DNA condensation Biophys. J. 99, 201-207
9. Schuck, P. (1997) Use of surface plasmon resonance to probe the equilibrium and dynamic aspects of interactions between biological macromolecules Annu. Rev. Biophys. Biomol. Struct. 26, 541-566
10. Homola, J. (2003) Present and future of surface plasmon resonance biosensors: Analytical and bioanalytical chemistry Anal. Bioanal. Chem. 377, 528-539
11. Herberg, F. W. and Zimmermann, B. (1999) Analysis of protein kinase interactions using biomolecular interaction analysis. In Protein Phosphorylation: A Practical Approach (Hardie, D. G., Ed.) pp 335-371, Oxford University Press, Oxford, U.K.
12. Moll, D., Schweinsberg, S., Hammann, C., Friedrich, W., and Herberg, F. W. (2007) Comparative thermodynamic analysis of cyclic nucleotide binding to protein kinase A Biol. Chem. 388, 163-172
13. Ng, E. S. M., Chan, N. W. C., Lewis, D. F., Hindsgaul, O., and Schriemer, D. C. (2007) Frontal affinity chromatography-mass spectrometry Nat. Protoc. 2, 1907-1917
14. Larsen, K., Thygesen, M. B., Guillaumie, F., William, G. T., Willats, W. G. T., and Jensen, K. J. (2006) Solid-phase chemical tools for glycobiology Carbohydr. Res. 341, 1209-1234
15. Horlacher, T. and Seeberger, P. H. (2008) Carbohydrate arrays as tools for research and diagnostics Chem. Soc. Rev. 37, 1414-1422
16. Laurent, N., Voglmeir, J., and Flitsch, S. L. (2008) Glycoarrays: Tools for determining protein-carbohydrate interactions and glycoenzyme specificity Chem. Commun. 37, 4400-4412
17. Liu, Y., Palma, A. S., and Feizi, T. (2009) Carbohydrate microarrays: Key developments in glycobiology Biol. Chem. 390, 647-656
18. Disney, M. D. and Seeberger, P. H. (2004) Carbohydrate arrays as tools for the glycomics revolution Drug Discovery Today: Targets 3, 151-158
19. Ganem, B., Li, Y. T., and Henion, J. D. (1991) Observation of noncovalent enzyme-substrate and substrate-product complexes by ion spray MS J. Am. Chem. Soc. 113, 7818-7819
20. Kitova, E. N., Kitov, P. I., Bundle, D. R., and Klassen, J. S. (2001) The observation of multivalent complexes of Shiga-like toxin with globotriaoside and the determination of their stoichiometry by nanoelectrospray Fourier-transform ion cyclotron resonance mass spectrometry Glycobiology 11, 605-611
21. St.Hilaire, P. M., Boyd, M. K., and Toone, E. J. (1994) Interaction of the Shiga-like toxin type-1 B-subunit with its carbohydrate receptor Biochemistry 33, 14452-14463
22. Jorgensen, T. J. D., Roepstorff, P., and Heck, A. J. R. (1998) Direct determination of solution binding constants for noncovalent complexes between bacterial cell wall peptide analogues and vancomycin group antibiotics by electrospray ionization mass spectrometry Anal. Chem. 70, 4427-4432
23. Jecklin, M. C., Touboul, D., Bovet, C., Wortmann, A., and Zenobi, R. (2008) Which electrospray-based ionization method best reflects protein-ligand interactions found in solution? A comparison of ESI, NanoESI, and ESSI for the determination of dissociation constants with mass spectrometry J. Am. Soc. Mass Spectrom. 19, 332-343
24. Yu, Y. H., Kirkup, C. E., Pi, N., and Leary, J. A. (2004) Characterization of noncovalent protein-ligand complexes and associated enzyme intermediates of GlcNAc-6-O-sulfotransferase by electrospray ionization FT-ICR mass spectrometry J. Am. Soc. Mass Spectrom. 15, 1400-1407
25. Hofstadler, S. A. and Sannes-Lowery, K. A. (2006) Applications of ESI-MS in drug discovery: Interrogation of noncovalent complexes Nat. Rev. Drug Discovery 5, 585-595
26. Liu, L., Kitova, E. N., and Klassen, J. S. (2011) Quantifying protein-fatty acid interactions using electrospray ionization mass spectrometry J. Am. Soc. Mass Spectrom. 22, 310-318
27. Van Dongen, W. D. and Heck, A. J. R. (2000) Binding of selected carbohydrates to apo-concanavalin A studied by electrospray ionization mass spectrometry Analyst 125, 583-589
28. Sandbhor, M. S., Soya, N., Albohy, A., Zheng, R. B., Cartmell, J., Bundle, D. R., Klassen, J. S., and Cairo, C. W. (2011) Substrate recognition of the membrane-associated sialidase Neu3 requires a hydrophobic aglycone Biochemistry 50, 6753-6762
29. El-Hawiet, A., Kitova, E. N., Kitov, P., Eugenio, L., Ng, K. K. S., Mulvey, G. L., Dingle, T. C., Szpacenko, A., Armstrong, G. D., and Klassen, J. S. (2011) Binding of Clostridium difficile toxins to human milk oligosaccharides Glycobiology 21, 1217-1227
30. Soya, N., Fang, Y., Palcic, M. M., and Klassen, J. S. (2011) Trapping and characterization of covalent intermediates of mutant retaining glycosyltransferases Glycobiology 21, 547-552
31. El-Hawiet, A., Kitova, E. N., Liu, L., and Klassen, J. S. (2010) Quantifying labile protein-ligand interactions using electrospray ionization mass spectrometry J. Am. Soc. Mass Spectrom. 21, 1893-1899
32. Soya, N., Shoemaker, G. K., Palcic, M. M., and Klassen, J. S. (2009) Comparative study of substrate and product binding to the human ABO(H) blood group glycosyltransferases Glycobiology 19, 1224-1234
33. Humphries, R. M., Donnenbberg, M. S., Strecher, J., Kitova, E. N., Klassen, J. S., Cui, L., Griener, T. P., Mulvey, G. L., and Armstrong, G. D. (2009) From α to β: Identification of amino acids required for the N-acetyllactosamine specific lectin-like activity of bundlin Mol. Microbiol. 72, 859-868
34. Shoemaker, G. K., Soya, N., Palcic, M. M., and Klassen, J. S. (2008) Temperature-dependent cooperativity in donor-acceptor substrate binding to the human blood group glycosltransferases Glycobiology 18, 587-592
35. Dingle, T., Wee, S., Mulvey, G. L., Greco, A., Kitova, E. N., Sun, J., Lin, S., Klassen, J. S., Palcic, M. M., Ng, K. K., and Armstrong, G. D. (2008) Functional properties of the carboxy-terminal host cell-binding domains of the two toxins, TcdA and TcdB, expressed by Clostridium difficile Glycobiology 18, 698-706
36. Kitov, P. I., Lipinski, T., Paszkiewicz, E., Solomon, D., Sadowska, J. M., Grant, G. A., Mulvey, G. L., Kitova, E. N., Klassen, J. S., Armstrong, G. D., and Bundle, D. R. (2008) An entropically efficient supramolecular inhibition strategy for Shiga toxins Angew. Chem., Int. Ed. 47, 672-676
37. Kitova, E. N., Kitov, P. I., Paszkiewicz, E., Kim, J., Mulvey, G. L., Armstrong, G. D., Bundle, D. R., and Klassen, J. S. (2007) Affinities of Shiga toxins 1 and 2 for univalent and oligovalent Pk trisaccharide analogs measured by electrospray ionization mass spectrometry Glycobiology 17, 1127-1137
38. Rademacher, C., Shoemaker, G. K., Kim, H.-S., Zheng, R. B., Taha, H., Liu, C., Nacario, R. C., Schriemer, D. C., Klassen, J. S., Peters, T., and Lowary, T. L. (2007) Ligand specificity of CS-35, a monoclonal antibody that recognizes mycobacterial lipoarabinomannan. A model system for oligofuranoside-protein recognition J. Am. Chem. Soc. 129, 10489-10502
39. Wang, W., Kitova, E. N., and Klassen, J. S. (2003) Influence of solution and gas phase processes on protein-carbohydrate binding affinities determined by nanoelectrospray fourier-transform ion cyclotron resonance mass spectrometry Anal. Chem. 75, 4945-4955
40. Abzalimov, R. R., Dubin, P. L., and Kaltsahov, I. A. (2007) Glycosaminoglycans as naturally occuring combinatorial libraries: Spectrometry-based strategy for characterization of anti-thrombin interaction strategy with low molecular weight heparin and heparin oligomers Anal. Chem. 79, 6055-6063
41. El-Hawiet, A., Shoemaker, G. K., Daneshfar, R., Kitova, E. N., and Klassen, J. S. (2012) Applications of a catch and release electrospray ionization mass spectrometry assay for carbohydrate library screening Anal. Chem. 84, 50-58
42. Cederkvist, F. H., Zamfir, A. D., Bahrke, S., Eijsink, V. G. H., Sørlie, M., Peter-Katalinić, J., and Peter, M. G. (2006) Identification of a high-affinity-binding oligosaccharide by (+) nanoelectrospray quadrupole time-of-flight tandem mass spectrometry of a noncovalent enzyme-ligand complex Angew. Chem., Int. Ed. 45, 2429-2434
43. El-Hawiet, A., Kitova, E. N., Arutyunov, D., Szymanski, C. M., and Klassen, J. S. (2012) Quantifying ligand binding to large protein complexes using electrospray ionization mass spectrometry Anal. Chem. 84, 3867-3870
44. Kitova, E. N., El-Hawiet, A., Schnier, P. D., and Klassen, J. S. (2012) Reliable Determinations of Protein-Ligand Interactions by Direct ESI-MS Measurements. Are We There Yet? J. Am. Soc. Mass Spectrom. 23, 431-441
45. Zdanov, A., Bundle, D. R., Deng, S. J., MacKenzie, C. R., Narang, S. A., Young, M. N., and Cygler, M. (1994) Structure of a single-chain antibody variable domain (fv) fragment complexed with a carbohydrate antigen at 1.7-angstrom resolution Proc. Natl. Acad. Sci. U.S.A. 91, 6423-6427
46. Bundle, D. R. Private communication.
47. Sigurskjold, B. W., Altman, E., and Bundle, D. R. (1991) Sensitive titration microcalorimetric study of the binding of Salmonella O-antigenic oligosaccharides by a monoclonal antibody Eur. J. Biochem. 197, 239-246
48. Steinbacher, S., Baxa, U., Miller, S., Weintraub, A., Seckler, R., and Huber, R. (1996) Crystal structure of phage P22 tailspike protein complexed with Salmonella sp. O-antigen receptors Proc. Natl. Acad. Sci. U.S.A. 93, 10584-10588
49. Baxa, U., Steinbacher, S., Miller, S., Weintraub, A., Huber, R., and Seckler, R. (1996) Interactions of phage P22 tails with their cellular receptor, Salmonella O-antigen polysaccharide Biophys. J. 71, 2040-2048
50. Daneshfar, R., Kitova, E. N., and Klassen, J. S. (2004) Determination of protein-ligand association thermochemistry using variable-temperature nanoelectrospray mass spectrometry J. Am. Chem. Soc. 126, 4786-4787
51. Frahm, J. L., Muddiman, D. C., and Burke, M. J. (2005) Leveling response factors in the electrospray ionization process using a heated capillary interface J. Am. Soc. Mass Spectrom. 16, 772-778
52. Benesch, J. L. P., Sobott, F., and Robinson, C. V. (2003) Thermal dissociation of multimeric protein complexes by using nanoelectrospray mass spectrometry Anal. Chem. 75, 2208-2214
53. Wang, G., Abzalimov, R. R., and Kaltashov, I. A. (2011) Direct monitoring of heat-stressed biopolymers with temperature-controlled electrospray ionization mass spectrometry Anal. Chem. 83, 2870-2876
54. Cheng, X., Chen, R., Bruce, J. E., Schwartz, B., Landerson, G. A., Hofstadler, S. A., Gale, D. C., and Smith, R. D. (1995) Using electrospray-ionization FTICR mass-spectrometry to study competitive-binding of inhibitors to carbonic-anhydrase J. Am. Chem. Soc. 117, 8859-8860
55. Gao, J., Cheng, X., Chen, R., Sigal, G. B., Bruce, J. E., Schwartz, B. L., Hofstadler, S. A., Anderson, G. A., Smith, R. D., and Whitesides, G. M. (1996) Screening derivatized peptide libraries for tight binding inhibitors to carbonic anhydrase II by electrospray ionization mass spectrometry J. Med. Chem. 39, 1949-1955
56. Wigger, M., Eyler, J. R., Benner, S. A., Li, W., and Marshall, A. G. (2002) Fourier transform-ion cyclotron resonance mass spectrometric resolution, identification, and screening of non-covalent complexes of Hck Src homology 2 domain receptor and ligands from a 324-member peptide combinatorial library J. Am. Soc. Mass Spectrom. 13, 1162-1169
57. Maple, H. J., Garlish, R. A., Rigau-Roca, L., Porter, J., Whitcombe, I., Prosser, C. E., Kennedy, J., Henry, A. J., Taylor, R. J., Crump, M. P., and Crosby, J. (2012) Automated protein-ligand interaction screening by mass spectrometry J. Med. Chem. 55, 837-851
58. Dole, M., Mack, L. L., Hines, R. L., Mobley, R. C., Ferguson, L. D., and Alice, M. B. (1968) Molecular beams of macroions J. Chem. Phys. 49, 2240-2249
59. Wang, W., Kitova, E. N., and Klassen, J. S. (2005) Nonspecific protein-carbohydrate complexes produced by nanoelectrospray ionization. Factors influencing their formation and stability Anal. Chem. 77, 3060-3071
60. Dybvik, A. I., Norberg, A. L., Schute, V., Soltwisch, J., Peter-Katalinic, J., Varum, K. M., Eijsink, V. G. H., Dreisewerd, K., Mormann, M., and Sørlie, M. (2011) Analysis of noncovalent Chitinase-chito- oligosaccharide complexes by infrared-matrix assisted laser desorption ionization and nanoelectrospray ionization mass spectrometry Anal. Chem. 83, 4030-4036
61. Wang, W., Kitova, E. N., and Klassen, J. S. (2003) Bioactive recognition sites may not be energetically preferred in protein-carbohydrate complexes in the gas phase J. Am. Chem. Soc. 125, 13630-13631
62. Sun, J., Kitova, E. N., Wang, W., and Klassen, J. S. (2006) Method for distinguishing specific from nonspecific protein-ligand complexes in nanoelectrospray ionization mass spectrometry Anal. Chem. 78, 3010-3018
63. Sun, N., Soya, N., Kitova, E. N., and Klassen, J. S. (2010) Nonspecific interactions between proteins and charged biomolecules in electrospray ionization mass spectrometry J. Am. Soc. Mass Spectrom. 21, 472-481
64. Sun, J., Kitova, E. N., Sun, N., and Klassen, J. S. (2007) Method for identifying nonspecific protein-protein interactions in nanoelectrospray ionization mass spectrometry Anal. Chem. 79, 8301-8311
65. Deng, L., Sun, N., Kitova, E. N., and Klassen, J. S. (2010) Direct quantification of protein-metal ion affinities by electrospray ionization mass spectrometry Anal. Chem. 82, 2170-2174
66. Van Dongen, W. D. and Heck, A. J. R. (2000) Binding of selected carbohydrates to apo-concanavalin A studied by electrospray ionization mass spectrometry Analyst 125, 583-589
67. Clark, S. M. and Konermann, L. (2004) Determination of ligand-protein dissociation constants by electrospray mass spectrometry-based diffusion measurements Anal. Chem. 76, 7077-7083
68. Robinson, C. V., Chung, E. W., Kragelund, B. B., Knudsen, J., Aplin, R. T., Poulsen, F. M., and Dobson, C. M. (1996) Probing the nature of noncovalent interactions by mass spectrometry. A study of protein-CoA ligand binding and assembly J. Am. Chem. Soc. 118, 8646-8653
69. Bagal, D., Kitova, E. N., Liu, L., El-Hawiet, A., Schnier, P. D., and Klassen, J. S. (2009) Gas phase stabilization of noncovalent protein complexes formed by electrospray ionization Anal. Chem. 81, 7801-7806
70. Sun, J., Kitova, E. N., and Klassen, J. S. (2007) Method for stabilizing protein-ligand complexes in nanoelectrospray ionization mass spectrometry Anal. Chem. 79, 417-425
71. Kitova, E. N., Seo, M., Roy, P. N., and Klassen, J. S. (2008) Elucidating the intermolecular interactions within a desolvated protein-ligand complex. An experimental and computational study J. Am. Chem. Soc. 130, 1214-1216
72. Van Berkel, G. J., Asano, K. G., and Schnier, P. D. (2001) Electrochemical processes in a wire-in-a-capillary bulk-loaded, nano-electrospray emitter J. Am. Soc. Mass Spectrom. 12, 853-862
73. Hernandez, H. and Robinson, C. V. (2007) Determining the stoichiometry and interactions of macromolecular assemblies from mass spectrometry Nat. Protoc. 2, 715-726
74. Iavarone, A. T., Udekwu, O. A., and Williams, E. R. (2004) Buffer loading for counteracting metal salt-induced signal suppression in electrospray ionization Anal. Chem. 76, 3944-3950
75. Yang, P., Cooks, R. G., Ouyang, Z., Hawkridge, A. M., and Muddiman, D. C. (2005) Gentle protein ionization assisted by high-velocity gas flow Anal. Chem. 77, 6174-6183
76. Ferguson, C. N., Benchaar, S. A., Miao, Z., Loo, J. A., and Chen, H. (2011) Direct ionization of large proteins and protein complexes by desorption electrospray ionization-mass spectrometry Anal. Chem. 83, 6468-6473
77. Bundle, D. R., Eichler, E., Gidney, M. A. J., Meldal, M., Ragauskas, A., Sigurskjold, B. W., Sinnott, B., Watson, D. C., Yaguchi, M., and Young, N. M. (1994) Molecular recognition of a Salmonella trisaccharide epitope by monoclonal-antibody Se155-4 Biochemistry 33, 5172-5182
78. Yu, Y., Sweeney, M. D., Saad, O. M., Crown, S. E., Hsu, A. R., Handel, T. M., and Leary, J. A. (2005) Chemokine-glycosaminoglycan binding: Specificity for CCR2 ligand binding to highly sulfated oligosaccharides using FTICR mass spectrometry J. Biol. Chem. 280, 32200-32208
79. Wortmann, A., Jecklin, M. C., Touboul, D., Badertscher, M., and Zenobi, R. (2008) Binding constant determination of high-affinity protein-ligand complexes by electrospray ionization mass spectrometry and ligand competition J. Mass Spectrom. 43, 600-608
80. 50 measurements Anal. Chem. 81, 408-419