Simultaneous characterization of glyco- and phosphoproteomes of mouse brain membrane proteome with electrostatic repulsion hydrophilic interaction chromatography

Molecular and Cellular Proteomics

Volumn 9, Issue 4, 2010, Pages 635-647

  Zhang, Huoming ^a   Guo, Tiannan ^a   Li, Xin ^a   Datta, Arnab ^a   Park, Jung Eun ^a   Yang, Jie ^a   Lim, Sai Kiang ^b   Tam, James P ^a   Sze, Siu Kwan ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPEPTIDE; GLYCOPROTEIN; HYDRAZIDE; PHOSPHOPEPTIDE; PROTEOME;

ANIMAL TISSUE; ARTICLE; BRAIN MEMBRANE; CHROMATOGRAPHY; COMPLEX FORMATION; DATA BASE; ELECTRICITY; GLYCOSYLATION; HYDROPHILICITY; METHODOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; SWISS-PROT;

AMINO ACID SEQUENCE; ANIMALS; BRAIN; BRAIN CHEMISTRY; CELL MEMBRANE; CHROMATOGRAPHY; GLYCOPROTEINS; GLYCOSYLATION; HYDROPHOBICITY; MICE; MICE, INBRED C57BL; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; STATIC ELECTRICITY; TANDEM MASS SPECTROMETRY;

EID: 77950632171     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M900314-MCP200     Document Type: Article

References (69)

1. Apweiler, R., Hermjakob, H., and Sharon, N. (1999) On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim. Biophys. Acta 1473, 4-8
2. Cohen, P. (2000) The regulation of protein function by multisite phosphorylation-a 25 year update. Trends Biochem. Sci. 25, 596-601
3. Roth, J. (2002) Protein N-glycosylation along the secretory pathway: relationship to organelle topography and function, protein quality control, and cell interactions. Chem. Rev. 102, 285-303
4. Schmidt-Ullrich, R. K., Contessa, J. N., Lammering, G., Amorino, G., and Lin, P. S. (2003) ERBB receptor tyrosine kinases and cellular radiation responses. Oncogene 22, 5855-5865 (Pubitemid 37176706)
5. Dennis, J. W., Granovsky, M., and Warren, C. E. (1999) Protein glycosylation in development and disease. BioEssays 21, 412-421
6. Ballif, B. A., Villén, J., Beausoleil, S. A., Schwartz, D., and Gygi, S. P. (2004) Phosphoproteomic analysis of the developing mouse brain. Mol. Cell. Proteomics 3, 1093-1101 (Pubitemid 40012102)
7. Guevara, J., Espinosa, B., Zenteno, E., Vázguez, L., Luna, J., Perry, G., and Mena, R. (1998) Altered glycosylation pattern of proteins in Alzheimer disease. J. Neuropathol. Exp. Neurol. 57, 905-914 (Pubitemid 28478001)
8. Takahashi, M., Tsujioka, Y., Yamada, T., Tsuboi, Y., Okada, H., Yamamoto, T., and Liposits, Z. (1999) Glycosylation of microtubule-associated protein tau in Alzheimer's disease brain. Acta Neuropathol. 97, 635-641 (Pubitemid 29231682)
9. Mi, K., and Johnson, G. V. (2006) The role of tau phosphorylation in the pathogenesis of Alzheimer's disease. Curr. Alzheimer Res. 3, 449-463 (Pubitemid 46070114)
10. Castellani, R., Smith, M. A., Richey, P. L., and Perry, G. (1996) Glycoxidation and oxidative stress in Parkinson disease and diffuse Lewy body disease. Brain Res. 737, 195-200 (Pubitemid 26366614)
11. Muntané , G., Dalfó , E., Martinez, A., and Ferrer, I. (2008) Phosphorylation of tau and alpha-synuclein in synaptic-enriched fractions of the frontal cortex in Alzheimer's disease, and in Parkinson's disease and related alpha-synucleinopathies. Neuroscience 152, 913-923
12. Guerry, P. (1997) Nonlipopolysaccharide surface antigens of Campylobacter species. J. Infect. Dis. 176, Suppl. 2, S122-S124
13. Liu, J., Ball, S. L., Yang, Y., Mei, P., Zhang, L., Shi, H., Kaminski, H. J., Lemmon, V. P., and Hu, H. (2006) A genetic model for muscle-eye-brain disease in mice lacking protein O-mannose 1,2-N-acetylglucosaminyl-transferase (POMGnT1). Mech. Dev. 123, 228-240
14. Zhang, H., Loriaux, P., Eng, J., Campbell, D., Keller, A., Moss, P., Bonneau, R., Zhang, N., Zhou, Y., Wollscheid, B., Cooke, K., Yi, E. C., Lee, H., Peskind, E. R., Zhang, J., Smith, R. D., and Aebersold, R. (2006) Uni-Pep - a database for human N-linked glycosites: a resource for biomarker discovery. Genome Biol. 7, R73 (Pubitemid 44468851)
15. Chalmers, M. J., Kolch, W., Emmett, M. R., Marshall, A. G., and Mischak, H. (2004) Identification and analysis of phosphopeptides. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 803, 111-120
16. Mintz, G., and Glaser, L. (1979) Glycoprotein purification on a high-capacity wheat germ lectin affinity column. Anal. Biochem. 97, 423-427 (Pubitemid 10240175)
17. Mechref, Y., Madera, M., and Novotny, M. V. (2008) Glycoprotein enrichment through lectin affinity techniques. Methods Mol. Biol. 424, 373-396
18. Drake, R. R., Schwegler, E. E., Malik, G., Diaz, J., Block, T., Mehta, A., and Semmes, O. J. (2006) Lectin capture strategies combined with mass spectrometry for the discovery of serum glycoprotein biomarkers. Mol. Cell. Proteomics 5, 1957-1967 (Pubitemid 44688203)
19. Hourani, B. T., Chace, N. M., and Pincus, J. H. (1973) Plasma membrane glycoproteins from nucleated cells. I. Preparative techniques for isolation and partial characterization of a membrane glycoprotein extract from L1210 cells with lectin receptor activity. Biochim. Biophys. Acta 328, 520-532
20. Debray, H., Decout, D., Strecker, G., Spik, G., and Montreuil, J. (1981) Specificity of twelve lectins towards oligosaccharides and glycopeptides related to N-glycosylproteins. Eur. J. Biochem. 117, 41-55
21. Ghosh, D., Krokhin, O., Antonovici, M., Ens, W., Standing, K. G., Beavis, R. C., and Wilkins, J. A. (2004) Lectin affinity as an approach to the proteomic analysis of membrane glycoproteins. J. Proteome Res. 3, 841-850 (Pubitemid 39166246)
22. Lee, A., Kolarich, D., Haynes, P. A., Jensen, P. H., Baker, M. S., and Packer, N. H. (2009) Rat liver membrane glycoproteome: enrichment by phase partitioning and glycoprotein capture. J. Proteome Res. 8, 770-781
23. Wada, Y., Tajiri, M., and Yoshida, S. (2004) Hydrophilic affinity isolation and MALDI multiple-stage tandem mass spectrometry of glycopeptides for glycoproteomics. Anal. Chem. 76, 6560-6565 (Pubitemid 39507245)
24. Tajiri, M., Yoshida, S., and Wada, Y. (2005) Differential analysis of site-specific glycans on plasma and cellular fibronectins: application of a hydrophilic affinity method for glycopeptide enrichment. Glycobiology 15, 1332-1340 (Pubitemid 41724337)
25. Ding, W., Nothaft, H., Szymanski, C. M., and Kelly, J. (2009) Identification and quantification of glycoproteins using ion-pairing normal-phase liquid chromatography and mass spectrometry. Mol. Cell. Proteomics 8, 2170-2185
26. Zhang, H., Li, X. J., Martin, D. B., and Aebersold, R. (2003) Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry. Nat. Biotechnol. 21, 660-666 (Pubitemid 36638093)
27. Sun, B., Ranish, J. A., Utleg, A. G., White, J. T., Yan, X., Lin, B., and Hood, L. (2007) Shotgun glycopeptide capture approach coupled with mass spectrometry for comprehensive glycoproteomics. Mol. Cell. Proteomics 6, 141-149 (Pubitemid 46152699)
28. Zhang, H., Yi, E. C., Li, X. J., Mallick, P., Kelly-Spratt, K. S., Masselon, C. D., Camp, D. G., 2nd, Smith, R. D., Kemp, C. J., and Aebersold, R. (2005) High throughput quantitative analysis of serum proteins using glycopeptide capture and liquid chromatography mass spectrometry. Mol. Cell. Proteomics 4, 144-155
29. Ramachandran, P., Boontheung, P., Xie, Y., Sondej, M., Wong, D. T., and Loo, J. A. (2006) Identification of N-linked glycoproteins in human saliva by glycoprotein capture and mass spectrometry. J. Proteome Res. 5, 1493-1503 (Pubitemid 43865819)
30. Lewandrowski, U., Moebius, J., Walter, U., and Sickmann, A. (2006) Elucidation of N-glycosylation sites on human platelet proteins: a glycoproteomic approach. Mol. Cell. Proteomics 5, 226-233 (Pubitemid 43329301)
31. Chen, R., Jiang, X., Sun, D., Han, G., Wang, F., Ye, M., Wang, L., and Zou, H. (2009) Glycoproteomics analysis of human liver tissue by combination of multiple enzyme digestion and hydrazide chemistry. J. Proteome Res. 8, 651-661
32. Zhang, H., Liu, A. Y., Loriaux, P., Wollscheid, B., Zhou, Y., Watts, J. D., and Aebersold, R. (2007) Mass spectrometric detection of tissue proteins in plasma. Mol. Cell. Proteomics 6, 64-71 (Pubitemid 46152692)
33. Cao, J., Shen, C., Wang, H., Shen, H., Chen, Y., Nie, A., Yan, G., Lu, H., Liu, Y., and Yang, P. (2009) Identification of N-glycosylation sites on secreted proteins of human hepatocellular carcinoma cells with a complementary proteomics approach. J. Proteome Res. 8, 662-672
34. Tao, W. A., Wollscheid, B., O'Brien, R., Eng, J. K., Li, X. J., Bodenmiller, B., Watts, J. D., Hood, L., and Aebersold, R. (2005) Quantitative phosphoproteome analysis using a dendrimer conjugation chemistry and tandem mass spectrometry. Nat. Methods 2, 591-598 (Pubitemid 41086850)
35. Rush, J., Moritz, A., Lee, K. A., Guo, A., Goss, V. L., Spek, E. J., Zhang, H., Zha, X. M., Polakiewicz, R. D., and Comb, M. J. (2005) Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat. Biotechnol. 23, 94-101 (Pubitemid 41724631)
36. Ficarro, S. B., McCleland, M. L., Stukenberg, P. T., Burke, D. J., Ross, M. M., Shabanowitz, J., Hunt, D. F., and White, F. M. (2002) Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat. Biotechnol. 20, 301-305 (Pubitemid 34205425)
37. Beausoleil, S. A., Jedrychowski, M., Schwartz, D., Elias, J. E., Villén, J., Li, J., Cohn, M. A., Cantley, L. C., and Gygi, S. P. (2004) Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc. Natl. Acad. Sci. U.S.A. 101, 12130-12135 (Pubitemid 39145408)
38. Larsen, M. R., Thingholm, T. E., Jensen, O. N., Roepstorff, P., and Jørgensen, T. J. (2005) Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol. Cell. Proteomics 4, 873-886 (Pubitemid 41309146)
39. Villén, J., Beausoleil, S. A., Gerber, S. A., and Gygi, S. P. (2007) Large-scale phosphorylation analysis of mouse liver. Proc. Natl. Acad. Sci. U.S.A. 104, 1488-1493 (Pubitemid 46214617)
40. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P., and Mann, M. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648 (Pubitemid 44647421)
41. Bodenmiller, B., Mueller, L. N., Mueller, M., Domon, B., and Aebersold, R. (2007) Reproducible isolation of distinct, overlapping segments of the phosphoproteome. Nat. Methods 4, 231-237 (Pubitemid 46358873)
42. Alpert, A. J. (2008) Electrostatic repulsion hydrophilic interaction chromatography for isocratic separation of charged solutes and selective isolation of phosphopeptides. Anal. Chem. 80, 62-76
43. Gan, C. S., Guo, T., Zhang, H., Lim, S. K., and Sze, S. K. (2008) A comparative study of electrostatic repulsion-hydrophilic interaction chromatography (ERLIC) versus SCX-IMAC-based methods for phosphopeptide isolation/enrichment. J. Proteome Res. 7, 4869-4877
44. Lewandrowski, U., Lohrig, K., Zahedi, R., Walter, D., and Sickmann, A. (2008) Glycosylation site analysis of human platelets by electrostatic repulsion hydrophilic interaction chromatography. Clin. Proteomics 4, 25-36
45. Kersey, P. J., Duarte, J., Williams, A., Karavidopoulou, Y., Birney, E., and Apweiler, R. (2004) The International Protein Index: an integrated database for proteomics experiments. Proteomics 4, 1985-1988 (Pubitemid 38880363)
46. Guo, T., Gan, C. S., Zhang, H., Zhu, Y., Kon, O. L., and Sze, S. K. (2008) Hybridization of pulsed-Q dissociation and collision-activated dissociation in linear ion trap mass spectrometer for iTRAQ quantitation. J. Proteome Res. 7, 4831-4840
47. Elias, J. E., and Gygi, S. P. (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 4, 207-214
48. Bendtsen, J. D., Nielsen, H., von Heijne, G., and Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340, 783-795 (Pubitemid 38829638)
49. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E. L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567-580 (Pubitemid 33032862)
50. Mi, H., Lazareva-Ulitsky, B., Loo, R., Kejariwal, A., Vandergriff, J., Rabkin, S., Guo, N., Muruganujan, A., Doremieux, O., Campbell, M. J., Kitano, H., and Thomas, P. D. (2005) The PANTHER database of protein families, subfamilies, functions and pathways. Nucleic Acids Res. 33, D284-D288 (Pubitemid 40207879)
51. Zhang, H., Lin, Q., Ponnusamy, S., Kothandaraman, N., Lim, T. K., Zhao, C., Kit, H. S., Arijit, B., Rauff, M., Hew, C. L., Chung, M. C., Joshi, S. B., and Choolani, M. (2007) Differential recovery of membrane proteins after extraction by aqueous methanol and trifluoroethanol. Proteomics 7, 1654-1663 (Pubitemid 46841826)
52. Danziger, R. S. (2008) Aminopeptidase N in arterial hypertension. Heart Fail. Rev. 13, 293-298
53. Elias, J. E., Haas, W., Faherty, B. K., and Gygi, S. P. (2005) Comparative evaluation of mass spectrometry platforms used in large-scale proteomics investigations. Nat. Methods 2, 667-675 (Pubitemid 41223093)
54. Thingholm, T. E., Larsen, M. R., Ingrell, C. R., Kassem, M., and Jensen, O. N. (2008) TiO(2)-based phosphoproteomic analysis of the plasma membrane and the effects of phosphatase inhibitor treatment. J. Proteome Res. 7, 3304-3313
55. Kenwrick, S., Watkins, A., and De Angelis, E. (2000) Neural cell recognition molecule L1: relating biological complexity to human disease mutations. Hum. Mol. Genet. 9, 879-886 (Pubitemid 30216098)
56. Kleene, R., and Schachner, M. (2004) Glycans and neural cell interactions. Nat. Rev. Neurosci. 5, 195-208
57. Albach, C., Klein, R. A., and Schmitz, B. (2001) Do rodent and human brains have different N-glycosylation patterns? Biol. Chem. 382, 187-194 (Pubitemid 32243927)
58. Owen, F., Poulter, M., Lofthouse, R., Collinge, J., Crow, T. J., Risby, D., Baker, H. F., Ridley, R. M., Hsiao, K., and Prusiner, S. B. (1989) Insertion in prion protein gene in familial Creutzfeldt-Jakob disease. Lancet 1, 51-52 (Pubitemid 19035247)
59. Goh, A. X., Li, C., Sy, M. S., and Wong, B. S. (2007) Altered prion protein glycosylation in the aging mouse brain. J. Neurochem. 100, 841-854 (Pubitemid 46095632)
60. Mole, S. E. (2006) Neuronal ceroid lipofuscinoses (NCL). Eur. J. Paediatr. Neurol. 10, 255-257
61. Tsiakas, K., Steinfeld, R., Storch, S., Ezaki, J., Lukacs, Z., Kominami, E., Kohlschütter, A., Ullrich, K., and Braulke, T. (2004) Mutation of the glycosylated asparagine residue 286 in human CLN2 protein results in loss of enzymatic activity. Glycobiology 14, 1C-5C (Pubitemid 38628107)
62. Sennvik, K., Fastbom, J., Blomberg, M., Wahlund, L. O., Winblad, B., and Benedikz, E. (2000) Levels of alpha- and beta-secretase cleaved amyloid precursor protein in the cerebrospinal fluid of Alzheimer's disease patients. Neurosci. Lett. 278, 169-172 (Pubitemid 30009484)
63. Akasaka-Manya, K., Manya, H., Sakurai, Y., Wojczyk, B. S., Spitalnik, S. L., and Endo, T. (2008) Increased bisecting and core-fucosylated N-glycans on mutant human amyloid precursor proteins. Glycoconj. J. 25, 775-786
64. Helisalmi, S., Hiltunen, M., Vepsäläinen, S., Iivonen, S., Mannermaa, A., Lehtovirta, M., Koivisto, A. M., Alafuzoff, I., and Soininen, H. (2004) Polymorphisms in neprilysin gene affect the risk of Alzheimer's disease in Finnish patients. J. Neurol. Neurosurg. Psychiatry 75, 1746-1748 (Pubitemid 39611478)
65. Tian, Q., and Wang, J. (2002) Role of serine/threonine protein phosphatase in Alzheimer's disease. Neurosignals 11, 262-269 (Pubitemid 37494393)
66. Wan, Q., Xiong, Z. G., Man, H. Y., Ackerley, C. A., Braunton, J., Lu, W. Y., Becker, L. E., MacDonald, J. F., and Wang, Y. T. (1997) Recruitment of functional GABA(A) receptors to postsynaptic domains by insulin. Nature 388, 686-690 (Pubitemid 27366441)
67. Brüning, J. C., Gautam, D., Burks, D. J., Gillette, J., Schubert, M., Orban, P. C., Klein, R., Krone, W., Müller-Wieland, D., and Kahn, C. R. (2000) Role of brain insulin receptor in control of body weight and reproduction. Science 289, 2122-2125
68. Das, U. N. (2002) Is type 2 diabetes mellitus a disorder of the brain? Nutrition 18, 667-672 (Pubitemid 34687112)
69. World Health Organization (2002) Active Ageing: a Policy Framework, World Health Organization, Geneva