Comprehensive description of the N-Glycoproteome of mouse pancreatic β-cells and human islets

Journal of Proteome Research

Volumn 11, Issue 3, 2012, Pages 1598-1608

  Danzer, Carsten ^a,c   Eckhardt, Katrin ^a,c   Schmidt, Alexander ^a,c   Fankhauser, Niklaus ^a,c   Ribrioux, Sebastien ^a,c   Wollscheid, Bernd ^a   Müller, Lukas ^a,c   Schiess, Ralph ^a,c   Züllig, Richard ^b   Lehmann, Roger ^b   Spinas, Giatgen ^b,c   Aebersold, Rudolf ^a,c   Krek, Wilhelm ^a,c  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c Competence Center for Systems Physiology and Metabolic Diseases ^*  (Switzerland)

Author keywords

cells; diabetes; islets; proteomics; surface N glycoproteins

Indexed keywords

G PROTEIN COUPLED RECEPTOR; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; GLYCOPROTEIN; INSULIN; N GLYCOPROTEIN DERIVATIVE; PHOSPHATASE; PROTEIN KINASE; PROTEINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; CONFERENCE PAPER; HUMAN; HUMAN CELL; INSULIN RELEASE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION;

ADULT; AGED; ANIMALS; CELLS, CULTURED; GENE EXPRESSION; GENE EXPRESSION REGULATION; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE; HUMANS; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MEMBRANE GLYCOPROTEINS; MICE; PROTEIN TYROSINE PHOSPHATASES; PROTEOME; RECEPTOR PROTEIN-TYROSINE KINASES; TANDEM MASS SPECTROMETRY;

EID: 84857862630     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr2007895     Document Type: Conference Paper

References (74)

1. Smyth, S.; Heron, A. Diabetes and obesity: the twin epidemics Nat. Med. 2006, 12 (1) 75-80
2. Chang-Chen, K. J.; Mullur, R.; Bernal-Mizrachi, E. Beta-cell failure as a complication of diabetes Rev. Endocr. Metab. Disord. 2008, 9 (4) 329-43
3. Eberhard, D.; Lammert, E. The pancreatic beta-cell in the islet and organ community Curr. Opin. Genet. Dev. 2009, 19 (5) 469-75
4. Zhang, H.; Li, X. J.; Martin, D. B.; Aebersold, R. Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry Nat. Biotechnol. 2003, 21 (6) 660-6
5. Lilla, V.; Webb, G.; Rickenbach, K.; Maturana, A.; Steiner, D. F.; Halban, P. A.; Irminger, J. C. Differential gene expression in well-regulated and dysregulated pancreatic beta-cell (MIN6) sublines Endocrinology 2003, 144 (4) 1368-79
6. Bucher, P.; Mathe, Z.; Morel, P.; Bosco, D.; Andres, A.; Kurfuest, M.; Friedrich, O.; Raemsch-Guenther, N.; Buhler, L. H.; Berney, T. Assessment of a novel two-component enzyme preparation for human islet isolation and transplantation Transplantation 2005, 79 (1) 91-7
7. Tian, Y.; Zhou, Y.; Elliott, S.; Aebersold, R.; Zhang, H. Solid-phase extraction of N-linked glycopeptides Nat. Protoc. 2007, 2 (2) 334-9
8. Wollscheid, B.; Bausch-Fluck, D.; Henderson, C.; OBrien, R.; Bibel, M.; Schiess, R.; Aebersold, R.; Watts, J. D. Mass-spectrometric identification and relative quantification of N-linked cell surface glycoproteins Nat. Biotechnol. 2009, 27 (4) 378-86
9. Schmidt, A.; Gehlenborg, N.; Bodenmiller, B.; Mueller, L. N.; Campbell, D.; Mueller, M.; Aebersold, R.; Domon, B. An integrated, directed mass spectrometric approach for in-depth characterization of complex peptide mixtures Mol. Cell. Proteomics 2008, 7 (11) 2138-50
10. Keller, A.; Eng, J.; Zhang, N.; Li, X. J.; Aebersold, R. A uniform proteomics MS/MS analysis platform utilizing open XML file formats Mol. Syst. Biol. 2005, 1 (2005) 0017
11. Keller, A.; Nesvizhskii, A. I.; Kolker, E.; Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search Anal. Chem. 2002, 74 (20) 5383-92
12. Nesvizhskii, A. I.; Keller, A.; Kolker, E.; Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry Anal. Chem. 2003, 75 (17) 4646-58
13. Bause, E. Structural requirements of N-glycosylation of proteins. Studies with proline peptides as conformational probes Biochem. J. 1983, 209 (2) 331-6
14. Mueller, L. N.; Rinner, O.; Schmidt, A.; Letarte, S.; Bodenmiller, B.; Brusniak, M. Y.; Vitek, O.; Aebersold, R.; Muller, M. SuperHirn-a novel tool for high resolution LC-MS-based peptide/protein profiling Proteomics 2007, 7 (19) 3470-80
15. Kuster, B.; Schirle, M.; Mallick, P.; Aebersold, R. Scoring proteomes with proteotypic peptide probes Nat. Rev. Mol. Cell. Biol. 2005, 6 (7) 577-83
16. Schmidt, A.; Beck, M.; Malmstrom, J.; Lam, H.; Claassen, M.; Campbell, D.; Aebersold, R. Absolute quantification of microbial proteomes at different states by directed mass spectrometry Mol. Syst. Biol. 2011, 7, 510
17. Fankhauser, N.; Maser, P. Identification of GPI anchor attachment signals by a Kohonen self-organizing map Bioinformatics 2005, 21 (9) 1846-52
18. Schiess, R.; Mueller, L. N.; Schmidt, A.; Mueller, M.; Wollscheid, B.; Aebersold, R. Analysis of cell surface proteome changes via label-free, quantitative mass spectrometry Mol. Cell. Proteomics 2009, 624-38
19. Hirokawa, T.; Boon-Chieng, S.; Mitaku, S. SOSUI: classification and secondary structure prediction system for membrane proteins Bioinformatics 1998, 14 (4) 378-9
20. Emanuelsson, O.; Brunak, S.; von Heijne, G.; Nielsen, H. Locating proteins in the cell using TargetP, SignalP and related tools Nat. Protoc. 2007, 2 (4) 953-71
21. Ashburner, M.; Ball, C. A.; Blake, J. A.; Botstein, D.; Butler, H.; Cherry, J. M.; Davis, A. P.; Dolinski, K.; Dwight, S. S.; Eppig, J. T.; Harris, M. A.; Hill, D. P.; Issel-Tarver, L.; Kasarskis, A.; Lewis, S.; Matese, J. C.; Richardson, J. E.; Ringwald, M.; Rubin, G. M.; Sherlock, G. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium Nat. Genet. 2000, 25 (1) 25-9
22. Manning, G.; Whyte, D. B.; Martinez, R.; Hunter, T.; Sudarsanam, S. The protein kinase complement of the human genome Science 2002, 298 (5600) 1912-34
23. Caenepeel, S.; Charydczak, G.; Sudarsanam, S.; Hunter, T.; Manning, G. The mouse kinome: discovery and comparative genomics of all mouse protein kinases Proc. Natl. Acad. Sci. U.S.A. 2004, 101 (32) 11707-12
24. Wolstencroft, K. J.; Stevens, R.; Tabernero, L.; Brass, A. PhosphaBase: an ontology-driven database resource for protein phosphatases Proteins 2005, 58 (2) 290-4
25. Harmar, A. J.; Hills, R. A.; Rosser, E. M.; Jones, M.; Buneman, O. P.; Dunbar, D. R.; Greenhill, S. D.; Hale, V. A.; Sharman, J. L.; Bonner, T. I.; Catterall, W. A.; Davenport, A. P.; Delagrange, P.; Dollery, C. T.; Foord, S. M.; Gutman, G. A.; Laudet, V.; Neubig, R. R.; Ohlstein, E. H.; Olsen, R. W.; Peters, J.; Pin, J. P.; Ruffolo, R. R.; Searls, D. B.; Wright, M. W.; Spedding, M. IUPHAR-DB: the IUPHAR database of G protein-coupled receptors and ion channels Nucleic Acids Res. 2009, 37 (database) D680-5
26. Okuno, Y.; Tamon, A.; Yabuuchi, H.; Niijima, S.; Minowa, Y.; Tonomura, K.; Kunimoto, R.; Feng, C. GLIDA: GPCR - ligand database for chemical genomics drug discovery - database and tools update Nucleic Acids Res. 2008, 36 (database) D907-12
27. Theodoropoulou, M. C.; Bagos, P. G.; Spyropoulos, I. C.; Hamodrakas, S. J. gpDB: a database of GPCRs, G-proteins, effectors and their interactions Bioinformatics 2008, 24 (12) 1471-2
28. Fuller-Bicer, G. A.; Varadi, G.; Koch, S. E.; Ishii, M.; Bodi, I.; Kadeer, N.; Muth, J. N.; Mikala, G.; Petrashevskaya, N. N.; Jordan, M. A.; Zhang, S. P.; Qin, N.; Flores, C. M.; Isaacsohn, I.; Varadi, M.; Mori, Y.; Jones, W. K.; Schwartz, A. Targeted disruption of the voltage-dependent calcium channel alpha2/delta-1-subunit Am. J. Physiol. Heart Circ. Physiol. 2009, 297 (1) H117-24
29. Liu, B.; Dai, J.; Zheng, H.; Stoilova, D.; Sun, S.; Li, Z. Cell surface expression of an endoplasmic reticulum resident heat shock protein gp96 triggers MyD88-dependent systemic autoimmune diseases Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (26) 15824-9
30. Vo, Y. P.; Hutton, J. C.; Angleson, J. K. Recycling of the dense-core vesicle membrane protein phogrin in Min6 beta-cells Biochem. Biophys. Res. Commun. 2004, 324 (3) 1004-10
31. Kagami, T.; Chen, S.; Memar, P.; Choi, M.; Foster, L. J.; Numata, M. Identification and biochemical characterization of the SLC9A7 interactome Mol. Membr. Biol. 2008, 25 (5) 436-47
32. Di Cristina, M.; Minenkova, O.; Pavoni, E.; Beghetto, E.; Spadoni, A.; Felici, F.; Gargano, N. A novel approach for identification of tumor-associated antigens expressed on the surface of tumor cells Int. J. Cancer 2007, 120 (6) 1293-303
33. Dong, M.; Yeh, F.; Tepp, W. H.; Dean, C.; Johnson, E. A.; Janz, R.; Chapman, E. R. SV2 is the protein receptor for botulinum neurotoxin A Science 2006, 312 (5773) 592-6
34. Singec, I.; Knoth, R.; Ditter, M.; Hagemeyer, C. E.; Rosenbrock, H.; Frotscher, M.; Volk, B. Synaptic vesicle protein synaptoporin is differently expressed by subpopulations of mouse hippocampal neurons J. Comp. Neurol. 2002, 452 (2) 139-53
35. Valtorta, F.; Pennuto, M.; Bonanomi, D.; Benfenati, F. Synaptophysin: leading actor or walk-on role in synaptic vesicle exocytosis? Bioessays 2004, 26 (4) 445-53
36. Haass, N. K.; Kartenbeck, M. A.; Leube, R. E. Pantophysin is a ubiquitously expressed synaptophysin homologue and defines constitutive transport vesicles J. Cell Biol. 1996, 134 (3) 731-46
37. White, M. F. IRS proteins and the common path to diabetes Am. J. Physiol. Endocrinol. Metab. 2002, 283 (3) E413-22
38. Ahmad, F.; Goldstein, B. J. Functional association between the insulin receptor and the transmembrane protein-tyrosine phosphatase LAR in intact cells J. Biol. Chem. 1997, 272 (1) 448-57
39. Ahmad, F.; Considine, R. V.; Goldstein, B. J. Increased abundance of the receptor-type protein-tyrosine phosphatase LAR accounts for the elevated insulin receptor dephosphorylating activity in adipose tissue of obese human subjects J. Clin. Invest. 1995, 95 (6) 2806-12
40. Mooney, R. A.; Kulas, D. T.; Bleyle, L. A.; Novak, J. S. The protein tyrosine phosphatase LAR has a major impact on insulin receptor dephosphorylation Biochem. Biophys. Res. Commun. 1997, 235 (3) 709-12
41. Weng, L. P.; Yuan, J.; Yu, Q. Overexpression of the transmembrane tyrosine phosphatase LAR activates the caspase pathway and induces apoptosis Curr. Biol. 1998, 8 (5) 247-56
42. Burgoyne, A. M.; Palomo, J. M.; Phillips-Mason, P. J.; Burden-Gulley, S. M.; Major, D. L.; Zaremba, A.; Robinson, S.; Sloan, A. E.; Vogelbaum, M. A.; Miller, R. H.; Brady-Kalnay, S. M. PTPmu suppresses glioma cell migration and dispersal Neuro. Oncol. 2009, 11 (6) 767-78
43. Burgoyne, A. M.; Phillips-Mason, P. J.; Burden-Gulley, S. M.; Robinson, S.; Sloan, A. E.; Miller, R. H.; Brady-Kalnay, S. M. Proteolytic cleavage of protein tyrosine phosphatase mu regulates glioblastoma cell migration Cancer Res. 2009, 69 (17) 6960-8
44. Zondag, G. C.; Reynolds, A. B.; Moolenaar, W. H. Receptor protein-tyrosine phosphatase RPTPmu binds to and dephosphorylates the catenin p120(ctn) J. Biol. Chem. 2000, 275 (15) 11264-9
45. Dang, C. V. The interplay between MYC and HIF in the Warburg effect Ernst Schering Found. Symp. Proc. 2007, 4, 35-53
46. Siu, R.; Fladd, C.; Rotin, D. N-cadherin is an in vivo substrate for protein tyrosine phosphatase sigma (PTPsigma) and participates in PTPsigma-mediated inhibition of axon growth Mol. Cell. Biol. 2007, 27 (1) 208-19
47. Muise, A.; Rotin, D. Apical junction complex proteins and ulcerative colitis: a focus on the PTPRS gene Expert Rev. Mol. Diagn. 2008, 8 (4) 465-77
48. Widmann, C.; Dolci, W.; Thorens, B. Internalization and homologous desensitization of the GLP-1 receptor depend on phosphorylation of the receptor carboxyl tail at the same three sites Mol. Endocrinol. 1997, 11 (8) 1094-102
49. Bodenmiller, B.; Aebersold, R. Quantitative analysis of protein phosphorylation on a system-wide scale by mass spectrometry-based proteomics Methods Enzymol. 2010, 470, 317-34
50. Zhou, H.; Ranish, J. A.; Watts, J. D.; Aebersold, R. Quantitative proteome analysis by solid-phase isotope tagging and mass spectrometry Nat. Biotechnol. 2002, 20 (5) 512-5
51. Waanders, L. F.; Chwalek, K.; Monetti, M.; Kumar, C.; Lammert, E.; Mann, M. Quantitative proteomic analysis of single pancreatic islets Proc. Natl. Acad. Sci. U.S.A. 2009, 106 (45) 18902-7
52. Bauer, C. S.; Tran-Van-Minh, A.; Kadurin, I.; Dolphin, A. C. A new look at calcium channel alpha2delta subunits Curr. Opin. Neurobiol. 2010, 20 (5) 563-71
53. Shieh, J. J.; Pan, C. J.; Mansfield, B. C.; Chou, J. Y. The islet-specific glucose-6-phosphatase-related protein, implicated in diabetes, is a glycoprotein embedded in the endoplasmic reticulum membrane FEBS Lett. 2004, 562 (1-3) 160-4
54. Ahren, B. Islet G protein-coupled receptors as potential targets for treatment of type 2 diabetes Nat. Rev. Drug Discovery 2009, 8 (5) 369-85
55. Nelson, G.; Hoon, M. A.; Chandrashekar, J.; Zhang, Y.; Ryba, N. J.; Zuker, C. S. Mammalian sweet taste receptors Cell 2001, 106 (3) 381-90
56. Ren, X.; Zhou, L.; Terwilliger, R.; Newton, S. S.; de Araujo, I. E. Sweet taste signaling functions as a hypothalamic glucose sensor Front. Integr. Neurosci. 2009, 3, 12
57. Jang, H. J.; Kokrashvili, Z.; Theodorakis, M. J.; Carlson, O. D.; Kim, B. J.; Zhou, J.; Kim, H. H.; Xu, X.; Chan, S. L.; Juhaszova, M.; Bernier, M.; Mosinger, B.; Margolskee, R. F.; Egan, J. M. Gut-expressed gustducin and taste receptors regulate secretion of glucagon-like peptide-1 Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (38) 15069-74
58. Nakagawa, Y.; Nagasawa, M.; Yamada, S.; Hara, A.; Mogami, H.; Nikolaev, V. O.; Lohse, M. J.; Shigemura, N.; Ninomiya, Y.; Kojima, I. Sweet taste receptor expressed in pancreatic beta-cells activates the calcium and cyclic AMP signaling systems and stimulates insulin secretion PLoS One 2009, 4 (4) e5106
59. Bersell, K.; Arab, S.; Haring, B.; Kuhn, B. Neuregulin1/ErbB4 signaling induces cardiomyocyte proliferation and repair of heart injury Cell 2009, 138 (2) 257-70
60. Fujikawa, A.; Chow, J. P.; Shimizu, H.; Fukada, M.; Suzuki, R.; Noda, M. Tyrosine phosphorylation of ErbB4 is enhanced by PSD95 and repressed by protein tyrosine phosphatase receptor type Z J.Biochem. 2007, 142 (3) 343-50
61. den Hertog, J.; Ostman, A.; Bohmer, F. D. Protein tyrosine phosphatases: regulatory mechanisms FEBS J. 2008, 275 (5) 831-47
62. Ostman, A.; Hellberg, C.; Bohmer, F. D. Protein-tyrosine phosphatases and cancer Nat. Rev. Cancer 2006, 6 (4) 307-20
63. Chow, J. P.; Fujikawa, A.; Shimizu, H.; Suzuki, R.; Noda, M. Metalloproteinase- and gamma-secretase-mediated cleavage of protein-tyrosine phosphatase receptor type Z J. Biol. Chem. 2008, 283 (45) 30879-89
64. Ruhe, J. E.; Streit, S.; Hart, S.; Ullrich, A. EGFR signaling leads to downregulation of PTP-LAR via TACE-mediated proteolytic processing Cell. Signalling 2006, 18 (9) 1515-27
65. Anders, L.; Mertins, P.; Lammich, S.; Murgia, M.; Hartmann, D.; Saftig, P.; Haass, C.; Ullrich, A. Furin-, ADAM 10-, and gamma-secretase-mediated cleavage of a receptor tyrosine phosphatase and regulation of beta-catenins transcriptional activity Mol. Cell. Biol. 2006, 26 (10) 3917-34
66. Magistrelli, G.; Toma, S.; Isacchi, A. Substitution of two variant residues in the protein tyrosine phosphatase-like PTP35/IA-2 sequence reconstitutes catalytic activity Biochem. Biophys. Res. Commun. 1996, 227 (2) 581-8
67. Doi, A.; Shono, T.; Nishi, M.; Furuta, H.; Sasaki, H.; Nanjo, K. IA-2beta, but not IA-2, is induced by ghrelin and inhibits glucose-stimulated insulin secretion Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (4) 885-90
68. Maddux, B. A.; Goldfine, I. D. Membrane glycoprotein PC-1 inhibition of insulin receptor function occurs via direct interaction with the receptor alpha-subunit Diabetes 2000, 49 (1) 13-9
69. Keller, S. R. Role of the insulin-regulated aminopeptidase IRAP in insulin action and diabetes Biol. Pharm. Bull. 2004, 27 (6) 761-4
70. Taylor, K. M.; Morgan, H. E.; Johnson, A.; Nicholson, R. I. Structure-function analysis of a novel member of the LIV-1 subfamily of zinc transporters, ZIP14 FEBS Lett. 2005, 579 (2) 427-32
71. Fagerholm, V.; Scheinin, M.; Haaparanta, M. alpha2A-adrenoceptor antagonism increases insulin secretion and synergistically augments the insulinotropic effect of glibenclamide in mice Br. J. Pharmacol. 2008, 154 (6) 1287-96
72. Skouloudaki, K.; Puetz, M.; Simons, M.; Courbard, J. R.; Boehlke, C.; Hartleben, B.; Engel, C.; Moeller, M. J.; Englert, C.; Bollig, F.; Schafer, T.; Ramachandran, H.; Mlodzik, M.; Huber, T. B.; Kuehn, E. W.; Kim, E.; Kramer-Zucker, A.; Walz, G. Scribble participates in Hippo signaling and is required for normal zebrafish pronephros development Proc. Natl. Acad. Sci. U.S.A. 2009, 106 (21) 8579-84
73. Badouel, C.; Garg, A.; McNeill, H. Herding Hippos: regulating growth in flies and man Curr. Opin. Cell. Biol. 2009, 21 (6) 837-43
74. Zhang, J. V.; Ren, P. G.; Avsian-Kretchmer, O.; Luo, C. W.; Rauch, R.; Klein, C.; Hsueh, A. J. Obestatin, a peptide encoded by the ghrelin gene, opposes ghrelins effects on food intake Science 2005, 310 (5750) 996-9