Analyzing protein micro-heterogeneity in chicken ovalbumin by high-resolution native mass spectrometry exposes qualitatively and semi-quantitatively 59 proteoforms

Analytical Chemistry

Volumn 85, Issue 24, 2013, Pages 12037-12045

  Yang, Yang ^a,b   Barendregt, Arjan ^a,b   Kamerling, Johannis P ^a   Heck, Albert J R ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b NETHERLANDS PROTEOMICS CENTRE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTROSPRAY IONIZATION MASS SPECTROMETRY; EUKARYOTIC PROTEINS; GLYCAN STRUCTURES; GLYCOSYLATION SITES; MICROHETEROGENEITY; NATIVE MASS SPECTROMETRIES; PHOSPHORYLATION SITES; SAMPLE PREPARATION;

ANIMALS; MASS SPECTROMETRY;

PROTEINS;

OVALBUMIN;

ANIMAL; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CHICKEN; ELECTROSPRAY MASS SPECTROMETRY; GLYCOSYLATION; METABOLISM; METHODOLOGY; PHOSPHORYLATION; PROTEIN CONFORMATION;

ANIMALS; CHICKENS; GLYCOSYLATION; MODELS, MOLECULAR; OVALBUMIN; PHOSPHORYLATION; PROTEIN CONFORMATION; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

EID: 84890453080     PISSN: 00032700     EISSN: 15206882     Source Type: Journal    
DOI: 10.1021/ac403057y     Document Type: Article

References (69)

1. Nisbet, A. D.; Saundry, R. H.; Moir, A. J. G.; Fothergill, L. A.; Fothergill, J. E. Eur. J. Biochem. 1981, 115 (2) 335-345
2. Huntington, J. A.; Stein, P. E. J. Chromatogr., B 2001, 756 (1-2) 189-198
3. Bushey, M. M.; Jorgenson, J. W. Anal. Chem. 1990, 62 (10) 978-984
4. Wagner, K.; Racaityte, K.; Unger, K. K.; Miliotis, T.; Edholm, L. E.; Bischoff, R.; Marko-Varga, G. J. Chromatogr., A 2000, 893 (2) 293-305
5. Landers, J. P.; Oda, R. P.; Madden, B. J.; Spelsberg, T. C. Anal. Biochem. 1992, 205 (1) 115-124
6. Dickerson, J. A.; Ramsay, L. M.; Dada, O. O.; Cermak, N.; Dovichi, N. J. Electrophoresis 2010, 31 (15) 2650-2654
7. Di Palma, S.; Hennrich, M. L.; Heck, A. J. R.; Mohammed, S. J. Proteomics 2012, 75 (13) 3791-3813
8. Danzo, B. J.; Bell, B. W. J. Biol. Chem. 1988, 263 (5) 2402-2408
9. Rose, R. J.; Damoc, E.; Denisov, E.; Makarov, A.; Heck, A. J. R. Nat. Methods 2012, 9 (11) 1084-1086
10. Ceroni, A.; Maass, K.; Geyer, H.; Geyer, R.; Dell, A.; Haslam, S. M. J. Proteome Res. 2008, 7 (4) 1650-1659
11. Stein, P. E.; Leslie, A. G. W.; Finch, J. T.; Carrell, R. W. J. Mol. Biol. 1991, 221 (3) 941-959
12. Tarentino, A. L.; Gomez, C. M.; Plummer, T. H. Biochemistry 1985, 24 (17) 4665-4671
13. Trimble, R. B.; Tarentino, A. L. J. Biol. Chem. 1991, 266 (3) 1646-1651
14. Tarentino, A. L.; Plummer, T. H., Jr. Methods Enzymol. 1994, 230, 44-57
15. Plummer, T. H., Jr.; Tarentino, A. L. Glycobiology 1991, 1 (3) 257-263
16. Woo, S. L. C.; Beattie, W. G.; Catterall, J. F.; Dugaiczyk, A.; Staden, R.; Brownlee, G. G.; O'Malley, B. W. Biochemistry 1981, 20 (22) 6437-46
17. Palmiter, R. D.; Gagnon, J.; Walsh, K. A. Proc. Natl. Acad. Sci. U.S.A. 1978, 75 (1) 94-98
18. Kinoshita-Kikuta, E.; Kinoshita, E.; Koike, T. Electrophoresis 2012, 33 (5) 849-855
19. Wei, J.; Yang, L.; Harrata, A. K.; Lee, C. S. Electrophoresis 1998, 19 (13) 2356-2360
20. Takahashi, N.; Khoo, K.-H.; Suzuki, N.; Johnson, J. R.; Lee, Y. C. J. Biol. Chem. 2001, 276 (26) 23230-23239
21. Cunningham, L.; Ford, J. D.; Rainey, J. M. Biochim. Biophys. Acta 1965, 101 (2) 233-235
22. Huang, C.-C.; Mayer, H. E., Jr; Montgomery, R. Carbohydr. Res. 1970, 13 (1) 127-137
23. Tarentino, A. L.; Plummer, T. H., Jr.; Maley, F. J. Biol. Chem. 1972, 247 (8) 2629-2631
24. Tai, T.; Yamashita, K.; Ogata-Arakawa, M.; Koide, N.; Muramatsu, T.; Iwashita, S.; Inoue, Y.; Kobata, A. J. Biol. Chem. 1975, 250 (21) 8569-8575
25. Tai, T.; Yamashita, K.; Ito, S.; Kobata, A. J. Biol. Chem. 1977, 252 (19) 6687-6694
26. Tai, T.; Yamashita, K.; Kobata, A. Biochem. Biophys. Res. Commun. 1977, 78 (1) 434-441
27. Yamashita, K.; Tachibana, Y.; Kobata, A. J. Biol. Chem. 1978, 253 (11) 3862-3869
28. Conchie, J.; Strachan, I. Carbohydr. Res. 1978, 63, 193-213
29. Narasimhan, S.; Harpaz, N.; Longmore, G.; Carver, J. P.; Grey, A. A.; Schachter, H. J. Biol. Chem. 1980, 255 (10) 4876-4884
30. Atkinson, P. H.; Grey, A.; Carver, J. P.; Hakimi, J.; Ceccarini, C. Biochemistry 1981, 20 (14) 3979-3986
31. Carver, J. P.; Grey, A. A.; Winnik, F. M.; Hakimi, J.; Ceccarini, C.; Atkinson, P. H. Biochemistry 1981, 20 (23) 6600-6606
32. Longmore, G. D.; Schachter, H. Carbohydr. Res. 1982, 100, 365-392
33. Yamashita, K.; Ueda, I.; Kobata, A. J. Biol. Chem. 1983, 258 (23) 14144-14147
34. Ceccarini, C.; Lorenzoni, P.; Atkinson, P. H. Biochim. Biophys. Acta 1983, 759 (3) 214-221
35. Nomoto, H.; Inoue, Y. Eur. J. Biochem. 1983, 135 (2) 243-250
36. Yamashita, K.; Tachibana, Y.; Hitoi, A.; Kobata, A. Carbohydr. Res. 1984, 130, 271-288
37. Tomiya, N.; Awaya, J.; Kurono, M.; Endo, S.; Arata, Y.; Takahashi, N. Anal. Biochem. 1988, 171 (1) 73-90
38. Chen, L. M.; Yet, M. G.; Shao, M. C. FASEB J. 1988, 2 (12) 2819-2824
39. Nomoto, H.; Yasukawa, K.; Inoue, Y. Biosci. Biotechnol. Biochem. 1992, 56 (7) 1090-1095
40. Rago, R. P.; Ramirez-Soto, D.; Poretz, R. D. Carbohydr. Res. 1992, 236, 1-8
41. Duffin, K. L.; Welply, J. K.; Huang, E.; Henion, J. D. Anal. Chem. 1992, 64 (13) 1440-1448
42. Corradi Da Silva, M. L.; Stubbs, H. J.; Tamura, T.; Rice, K. G. Arch. Biochem. Biophys. 1995, 318 (2) 465-475
43. North, S.; Okafo, G.; Birrell, H.; Haskins, N.; Camilleri, P. Rapid Commun. Mass Spectrom. 1997, 11 (15) 1635-1642
44. North, S.; Birrell, H.; Camilleri, P. Rapid Commun. Mass Spectrom. 1998, 12 (7) 349-356
45. Anumula, K. R.; Dhume, S. T. Glycobiology 1998, 8 (7) 685-694
46. Mechref, Y.; Novotny, M. V. Anal. Chem. 1998, 70 (3) 455-463
47. Harvey, D. J.; Wing, D. R.; Küster, B.; Wilson, I. B. H. J. Am. Soc. Mass Spectrom. 2000, 11 (6) 564-571
48. Charlwood, J.; Birrell, H.; Bouvier, E. S. P.; Langridge, J.; Camilleri, P. Anal. Chem. 2000, 72 (7) 1469-1474
49. Saba, J. A.; Shen, X.; Jamieson, J. C.; Perreault, H. J. Mass Spectrom. 2001, 36 (5) 563-574
50. An, H. J.; Peavy, T. R.; Hedrick, J. L.; Lebrilla, C. B. Anal. Chem. 2003, 75 (20) 5628-5637
51. Lattova, E.; Perreault, H. J. Chromatogr., A 2003, 1016 (1) 71-87
52. Lattova, E.; Perreault, H.; Krokhin, O. J. Am. Soc. Mass Spectrom. 2004, 15 (5) 725-735
53. Lattová, E.; Snovida, S.; Perreault, H.; Krokhin, O. J. Am. Soc. Mass Spectrom. 2005, 16 (5) 683-696
54. Plasencia, M. D.; Isailovic, D.; Merenbloom, S. I.; Mechref, Y.; Clemmer, D. E. J. Am. Soc. Mass Spectrom. 2008, 19 (11) 1706-1715
55. Gil, G.-C.; Kim, Y.-G.; Kim, B.-G. Anal. Biochem. 2008, 379 (1) 45-59
56. Qin, H.; Zhao, L.; Li, R.; Wu, R.; Zou, H. Anal. Chem. 2011, 83 (20) 7721-7728
57. Jeong, H.-J.; Kim, Y.-G.; Yang, Y.-H.; Kim, B.-G. Anal. Chem. 2012, 84 (7) 3453-3460
58. Yamashita, K.; Kamerling, J. P.; Kobata, A. J. Biol. Chem. 1982, 257 (21) 12809-12814
59. Paz-Parente, J.; Wieruszeski, J. M.; Strecker, G.; Montreuil, J.; Fournet, B.; van Halbeek, H.; Dorland, L.; Vliegenthart, J. F. G. J. Biol. Chem. 1982, 257 (22) 13173-13176
60. Yamashita, K.; Kamerling, J. P.; Kobata, A. J. Biol. Chem. 1983, 258 (5) 3099-3106
61. Paz-Parente, J.; Strecker, G.; Leroy, Y.; Montreuil, J.; Fournet, B.; van Halbeek, H.; Dorland, L.; Vliegenthart, J. F. G. FEBS Lett. 1983, 152 (2) 145-152
62. Egge, H.; Peter-Katalinić, J.; Paz-Parente, J.; Strecker, G.; Montreuil, J.; Fournet, B. FEBS Lett. 1983, 156 (2) 357-362
63. Dorland, L.; Haverkamp, J.; Vliegenthart, J. F. G.; Spik, G.; Fournet, B.; Montreuil, J. Eur. J. Biochem. 1979, 100 (2) 569-574
64. Piskarev, V. E.; Sepetov, N. F.; Likhosherstov, L. M.; Galenko, E. L.; Derevitskaia, V. A.; Kochetkov, N. K. Russ. J. Bioorg. Chem. 1989, 15 (11) 1546-1554
65. Likhosherstov, L. M.; Piskarev, V. E.; Sepetov, N. F.; Derevitskaia, V. A.; Kochetkov, N. K. Russ. J. Bioorg. Chem. 1991, 17 (2) 246-251
66. Suzuki, N.; Laskowski, M., Jr; Lee, Y. C. Proc. Natl. Acad. Sci. U.S.A. 2004, 101 (24) 9023-9028
67. Schweigert, F. J. Briefings Funct. Genomics Proteomics 2005, 4 (1) 7-15
68. Fekete, S.; Gassner, A.-L.; Rudaz, S.; Schappler, J.; Guillarme, D. Trends. Anal. Chem. 2013, 42, 74-83
69. Chen, G.; Warrack, B. M.; Goodenough, A. K.; Wei, H.; Wang-Iverson, D. B.; Tymiak, A. A. Drug Discovery Today 2011, 16 (1-2) 58-64