Systematic proteomic analysis identifies β-site amyloid precursor protein cleaving enzyme 2 and 1 (BACE2 and BACE1) substrates in pancreatic β-cells

Journal of Biological Chemistry

Volumn 288, Issue 15, 2013, Pages 10536-10547

  Stützer, Ina ^a   Selevsek, Nathalie ^a   Esterházy, Daria ^a   Schmidt, Alexander ^b   Aebersold, Ruedi ^a   Stoffel, Markus ^a,c  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEINS; BIO-MARKER DISCOVERY; MOLECULAR UNDERSTANDING; PHARMACOLOGICAL INHIBITION; PHYSIOLOGICAL PROCESS; QUANTITATIVE PROTEOMIC ANALYSIS; THERAPEUTIC INTERVENTION; THERAPEUTIC TARGETS;

CELL MEMBRANES; PHYSIOLOGY; PROTEINS; SUBSTRATES;

CYTOLOGY;

BETA SECRETASE 1; BETA SECRETASE 2; PROTEIN SEZ6L; PROTEIN SEZ6L2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME SUBSTRATE; HOMEOSTASIS; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN TARGETING; PROTEOMICS; REGULATORY MECHANISM;

AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ACID ENDOPEPTIDASES; INSULIN-SECRETING CELLS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; PROTEOMICS;

EID: 84876263985     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.444703     Document Type: Article

References (64)

1. Bouwens, L., and Rooman, I. (2005) Regulation of pancreatic beta-cell mass. Physiol. Rev. 85, 1255-1270
2. Kahn, S. E., Hull, R. L., and Utzschneider, K. M. (2006) Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 444, 840-846
3. Eberhard, D., and Lammert, E. (2009) The pancreatic beta-cell in the islet and organ community. Curr. Opin. Genet. Dev. 19, 469-475
4. Prentki, M., and Nolan, C. J. (2006) Islet beta cell failure in type 2 diabetes. J. Clin. Investig. 116, 1802-1812
5. Stützer, I., Esterházy, D., and Stoffel, M. (2012) The pancreatic beta cell surface proteome. Diabetologia 55, 1877-1889
6. Buteau, J., Foisy, S., Joly, E., and Prentki, M. (2003) Glucagon-like peptide 1 induces pancreatic beta-cell proliferation via transactivation of the epidermal growth factor receptor. Diabetes 52, 124-132
7. Trajkovski, M., Mziaut, H., Altkrüger, A., Ouwendijk, J., Knoch, K. P., Müller, S., and Solimena, M. (2004) Nuclear translocation of an ICA512 cytosolic fragment couples granule exocytosis and insulin expression in {beta}-cells. J. Cell Biol. 167, 1063-1074
8. Esterházy, D., Stützer, I., Wang, H., Rechsteiner, M. P., Beauchamp, J., Döbeli, H., Hilpert, H., Matile, H., Prummer, M., Schmidt, A., Lieske, N., Boehm, B., Marselli, L., Bosco, D., Kerr-Conte, J., Aebersold, R., Spinas, G. A., Moch, H., Migliorini, C., and Stoffel, M. (2011) Bace2 is a beta cell-enriched protease that regulates pancreatic beta cell function and mass. Cell Metabolism 14, 365-377
9. Danzer, C., Eckhardt, K., Schmidt, A., Fankhauser, N., Ribrioux, S., Wollscheid, B., Müller, L., Schiess, R., Züllig, R., Lehmann, R., Spinas, G., Aebersold, R., and Krek, W. (2012) Comprehensive description of the N-glycoproteome of mouse pancreatic beta-cells and human islets. J. Proteome Res. 11, 1598-1608
10. Arribas, J., and Merlos-Suárez, A. (2003) Shedding of plasma membrane proteins. Current Topics in Dev. Biol. 54, 125-144
11. Lichtenthaler, S. F., and Steiner, H. (2007) Sheddases and intramembranecleaving proteases: RIPpers of the membrane. Symposium on regulated intramembrane proteolysis. EMBO Rep. 8, 537-541
12. Hussain, I., Christie, G., Schneider, K., Moore, S., and Dingwall, C. (2001) Prodomain processing of Asp1 (BACE2) is autocatalytic. J. Biol. Chem. 276, 23322-23328
13. Figueroa, D. J., Shi, X. P., Gardell, S. J., and Austin, C. P. (2001) Abetapp secretases are co-expressed with Abetapp in the pancreatic islets. J. Alzheimer's Disease : JAD 3, 393-396
14. Makridakis, M., and Vlahou, A. (2010) Secretome proteomics for discovery of cancer biomarkers. J. Proteomics 73, 2291-2305
15. Akpinar, P., Kuwajima, S., Krützfeldt, J., and Stoffel, M. (2005) Tmem27: a cleaved and shed plasma membrane protein that stimulates pancreatic beta cell proliferation. Cell Metabolism 2, 385-397
16. Schmidt, A., Beck, M., Malmström, J., Lam, H., Claassen, M., Campbell, D., and Aebersold, R. (2011) Absolute quantification of microbial proteomes at different states by directed mass spectrometry. Mol. Systems Biol. 7, 510
17. Yates, J. R., 3rd, Eng, J. K., McCormack, A. L., and Schieltz, D. (1995) Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal. Chem. 67, 1426-1436
18. Keller, A., Nesvizhskii, A. I., Kolker, E., and Aebersold, R. (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383-5392
19. Nesvizhskii, A. I., Keller, A., Kolker, E., and Aebersold, R. (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658
20. Mueller, L. N., Rinner, O., Schmidt, A., Letarte, S., Bodenmiller, B., Brusniak, M. Y., Vitek, O., Aebersold, R., and Müller, M. (2007) SuperHirn - a novel tool for high resolution LC-MS-based peptide/protein profiling. Proteomics 7, 3470-3480
21. Picotti, P., Rinner, O., Stallmach, R., Dautel, F., Farrah, T., Domon, B., Wenschuh, H., and Aebersold, R. (2010) High-throughput generation of selected reaction-monitoring assays for proteins and proteomes. Nature Methods 7, 43-46
22. Käll, L., Krogh, A., and Sonnhammer, E. L. (2004) A combined transmembrane topology and signal peptide prediction method. J. Mol. Biol. 338, 1027-1036
23. Selevsek, N., Matondo, M., Sanchez Carbayo, M., Aebersold, R., and Domon, B. (2011) Systematic quantification of peptides/proteins in urine using selected reaction monitoring. Proteomics 11, 1135-1147
24. MacLean, B., Tomazela, D. M., Shulman, N., Chambers, M., Finney, G. L., Frewen, B., Kern, R., Tabb, D. L., Liebler, D. C., and MacCoss, M. J. (2010) Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26, 966-968
25. Chang, C. Y., Picotti, P., Huttenhain, R., Heinzelmann-Schwarz, V., Jovanovic, M., Aebersold, R., and Vitek, O. (2012) Protein significance analysis in selected reaction monitoring (SRM) measurements. Mol. Cell Proteomics 11, M111 014662
26. Schiess, R., Mueller, L. N., Schmidt, A., Mueller, M., Wollscheid, B., and Aebersold, R. (2009) Analysis of cell surface proteome changes via labelfree, quantitative mass spectrometry. Mol. Cell. Proteomics 8, 624-638
27. 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. Nature Biotechnol. 21, 660-666
28. Huang da, W., Sherman, B. T., and Lempicki, R. A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols 4, 44-57
29. Overall, C. M., and Blobel, C. P. (2007) In search of partners: linking extracellular proteases to substrates. Nat. Rev. Mol. Cell Biol. 8, 245-257
30. McDermott, M. F., Aksentijevich, I., Galon, J., McDermott, E. M., Ogunkolade, B. W., Centola, M., Mansfield, E., Gadina, M., Karenko, L., Pettersson, T., McCarthy, J., Frucht, D. M., Aringer, M., Torosyan, Y., Teppo, A. M., Wilson, M., Karaarslan, H. M., Wan, Y., Todd, I., Wood, G., Schlimgen, R., Kumarajeewa, T. R., Cooper, S. M., Vella, J. P., Amos, C. I., Mulley, J., Quane, K. A., Molloy, M. G., Ranki, A., Powell, R. J., Hitman, G. A., O'Shea, J. J., and Kastner, D. L. (1999) Germline mutations in the extracellular domains of the 55 kDa TNF receptor, TNFR1, define a family of dominantly inherited autoinflammatory syndromes. Cell 97, 133-144
31. Peiretti, F., Canault, M., Bernot, D., Bonardo, B., Deprez-Beauclair, P., Juhan-Vague, I., and Nalbone, G. (2005) Proteasome inhibition activates the transport and the ectodomain shedding of TNF-γ receptors in human endothelial cells. J. Cell Science 118, 1061-1070
32. Dowling, P., and Clynes, M. (2011) Conditioned media from cell lines: a complementary model to clinical specimens for the discovery of diseasespecific biomarkers. Proteomics 11, 794-804
33. Butler, G. S., and Overall, C. M. (2009) Proteomic identification of multitasking proteins in unexpected locations complicates drug targeting. Nat. Rev. Drug Discov. 8, 935-948
34. Silva, J. C., Gorenstein, M. V., Li, G. Z., Vissers, J. P., and Geromanos, S. J. (2006) Absolute quantification of proteins by LCMSE: a virtue of parallel MS acquisition. Mol. Cell Proteomics 5, 144-156
35. Dowling, P., Shields, W., Rani, S., Meleady, P., Henry, M., Jeppesen, P., O'Driscoll, L., and Clynes, M. (2008) Proteomic analysis of conditioned media from glucose responsive and glucose non-responsive phenotypes reveals a panel of secreted proteins associated with beta cell dysfunction. Electrophoresis 29, 4141-4149
36. Kahn, S. E., D'Alessio, D. A., Schwartz, M. W., Fujimoto, W. Y., Ensinck, J. W., Taborsky, G. J., Jr., and Porte, D., Jr. (1990) Evidence of cosecretion of islet amyloid polypeptide and insulin by beta-cells. Diabetes 39, 634-638
37. Whim, M. D. (2011) Pancreatic beta cells synthesize neuropeptide Y and can rapidly release peptide co-transmitters. PloS one 6, e19478
38. Blanton, D., Han, Z., Bierschenk, L., Linga-Reddy, M. V., Wang, H., Clare- Salzler, M., Haller, M., Schatz, D., Myhr, C., She, J. X., Wasserfall, C., and Atkinson, M. (2011) Reduced serum vitamin D-binding protein levels are associated with type 1 diabetes. Diabetes 60, 2566-2570
39. Thomas, P. D., Kejariwal, A., Campbell, M. J., Mi, H., Diemer, K., Guo, N., Ladunga, I., Ulitsky-Lazareva, B., Muruganujan, A., Rabkin, S., Vandergriff, J. A., and Doremieux, O. (2003) PANTHER: a browsable database of gene products organized by biological function, using curated protein family and subfamily classification. Nucleic Acids Res. 31, 334-341
40. Kuhn, P. H., Koroniak, K., Hogl, S., Colombo, A., Zeitschel, U., Willem, M., Volbracht, C., Schepers, U., Imhof, A., Hoffmeister, A., Haass, C., Rossner, S., Brase, S., and Lichtenthaler, S. F. (2012) Secretome protein enrichment identifies physiological BACE1 protease substrates in neurons. EMBO J 31, 3157-3168.
41. Zhou, L., Barão, S., Laga, M., Bockstael, K., Borgers, M., Gijsen, H., Annaert, W., Moechars, D., Mercken, M., Gevaert, K., and De Strooper, B. (2012) The neural cell adhesion molecules L1 and CHL1 are cleaved by BACE1 protease in vivo. J. Biol. Chem. 287, 25927-25940
42. Hemming, M. L., Elias, J. E., Gygi, S. P., and Selkoe, D. J. (2009) Identification of beta-secretase (BACE1) substrates using quantitative proteomics. PloS one 4, e8477
43. Butler, G. S., and Overall, C. M. (2007) Proteomic validation of protease drug targets: pharmacoproteomics of matrix metalloproteinase inhibitor drugs using isotope-coded affinity tag labelling and tandem mass spectrometry. Curr. Pharm. Des. 13, 263-270
44. Hald, J., Galbo, T., Rescan, C., Radzikowski, L., Sprinkel, A. E., Heimberg, H., Ahnfelt-Rønne, J., Jensen, J., Scharfmann, R., Gradwohl, G., Kaestner, K. H., Stoeckert, C., Jr., Jensen, J. N., and Madsen, O. D. (2012) Pancreatic islet and progenitor cell surface markers with cell sorting potential. Diabetologia 55, 154-165
45. Schroeter, E. H., Kisslinger, J. A., and Kopan, R. (1998) Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature 393, 382-386
46. Rawson, R. B., Zelenski, N. G., Nijhawan, D., Ye, J., Sakai, J., Hasan, M. T., Chang, T. Y., Brown, M. S., and Goldstein, J. L. (1997) Complementation cloning of S2P, a gene encoding a putative metalloprotease required for intramembrane cleavage of SREBPs. Mol. Cell 1, 47-57
47. Gunnersen, J. M., Kim, M. H., Fuller, S. J., De Silva, M., Britto, J. M., Hammond, V. E., Davies, P. J., Petrou, S., Faber, E. S., Sah, P., and Tan, S. S. (2007) Sez-6 proteins affect dendritic arborization patterns and excitability of cortical pyramidal neurons. Neuron 56, 621-639
48. Ghosh, P., Dahms, N. M., and Kornfeld, S. (2003) Mannose 6-phosphate receptors: new twists in the tale. Nature Reviews. Mol. Cell Biol. 4, 202-212
49. Brown, J., Jones, E. Y., and Forbes, B. E. (2009) Interactions of IGF-II with the IGF2R/cation-independent mannose-6-phosphate receptor mechanism and biological outcomes. Vitam. Horm. 80, 699-719
50. Hill, D. J., Petrik, J., and Arany, E. (1998) Growth factors and the regulation of fetal growth. Diabetes Care 21, Suppl. 2, B60-B69
51. Zhang, Q., Tally, M., Larsson, O., Kennedy, R. T., Huang, L., Hall, K., and Berggren, P. O. (1997) Insulin-like growth factor II signaling through the insulin-like growth factor II/mannose-6-phosphate receptor promotes exocytosis in insulin-secreting cells. Proc. Natl. Acad. Sci. U. S.A. 94, 6232-6237
52. Zaina, S., and Squire, S. (1998) The soluble type 2 insulin-like growth factor (IGF-II) receptor reduces organ size by IGF-II-mediated and IGFII- independent mechanisms. J. Biol. Chem. 273, 28610-28616
53. Willnow, T. E., Petersen, C. M., and Nykjaer, A. (2008) VPS10P-domain receptors-regulators of neuronal viability and function. Nature Reviews. Neuroscience 9, 899-909
54. Dolais-Kitabgi, J., Kitabgi, P., Brazeau, P., and Freychet, P. (1979) Effect of neurotensin on insulin, glucagon, and somatostatin release from isolated pancreatic islets. Endocrinology 105, 256-260
55. Beraud-Dufour, S., Abderrahmani, A., Noel, J., Brau, F., Waeber, G., Mazella, J., and Coppola, T. (2010) Neurotensin is a regulator of insulin secretion in pancreatic beta-cells. Int. J. Biochem. Cell Biol. 42, 1681-1688
56. Evans, S. F., Irmady, K., Ostrow, K., Kim, T., Nykjaer, A., Saftig, P., Blobel, C., and Hempstead, B. L. (2011) Neuronal brain-derived neurotrophic factor is synthesized in excess, with levels regulated by sortilin-mediated trafficking and lysosomal degradation. J. Biol. Chem. 286, 29556-29567
57. Casas, S., Casini, P., Piquer, S., Altirriba, J., Soty, M., Cadavez, L., Gomis, R., and Novials, A. (2010) BACE2 plays a role in the insulin receptor trafficking in pancreatic ss-cells. Amer. J. Physiol. Endocrinol. Metab. 299, E1087-E1095
58. In't Veld, P., and Marichal, M. (2010) Microscopic anatomy of the human islet of Langerhans. Adv. Exp. Med. Biol. 654, 1-19
59. Braun, M., Ramracheya, R., Bengtsson, M., Zhang, Q., Karanauskaite, J., Partridge, C., Johnson, P. R., and Rorsman, P. (2008) Voltage-gated ion channels in human pancreatic beta-cells: electrophysiological characterization and role in insulin secretion. Diabetes 57, 1618-1628
60. Mziaut, H., Trajkovski, M., Kersting, S., Ehninger, A., Altkrüger, A., Lemaitre, R. P., Schmidt, D., Saeger, H. D., Lee, M. S., Drechsel, D. N., Müller, S., and Solimena, M. (2006) Synergy of glucose and growth hormone signalling in islet cells through ICA512 and STAT5. Nature Cell Biol. 8, 435-445
61. Torii, S., Saito, N., Kawano, A., Hou, N., Ueki, K., Kulkarni, R. N., and Takeuchi, T. (2009) Gene silencing of phogrin unveils its essential role in glucose-responsive pancreatic beta-cell growth. Diabetes 58, 682-692
62. Fukumoto, H., Cheung, B. S., Hyman, B. T., and Irizarry, M. C. (2002) Beta-secretase protein and activity are increased in the neocortex in Alzheimer disease. Arch. Neurol. 59, 1381-1389
63. Holsinger, R. M., McLean, C. A., Beyreuther, K., Masters, C. L., and Evin, G. (2002) Increased expression of the amyloid precursor beta-secretase in Alzheimer's disease. Annals Neurol. 51, 783-786
64. Miyazaki, J., Araki, K., Yamato, E., Ikegami, H., Asano, T., Shibasaki, Y., Oka, Y., and Yamamura, K. (1990) Establishment of a pancreatic beta cell line that retains glucose-inducible insulin secretion: special reference to expression of glucose transporter isoforms. Endocrinology 127, 126-132