Inhibition of BACE2 counteracts hIAPP-induced insulin secretory defects in pancreatic β-cells

FASEB Journal

Volumn 29, Issue 1, 2015, Pages 95-104

  Alcarraz Vizán, Gema ^a   Casini, Paola ^a   Cadavez, Lisa ^a   Visa, Montse ^a   Montane, Joel ^a   Servitja, Joan Marc ^a   Novials, Anna ^a  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

Author keywords

Amylin; BACE activity; Secretase; Type 2 diabetes

Indexed keywords

AMYLIN; BETA SITE AMYLOID POLYPEPTIDE CLEAVING ENZYME 2; GLUCOSE; INSULIN; PROTEINASE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; ASPARTIC PROTEINASE; BACE2 PROTEIN, RAT; MESSENGER RNA; RECOMBINANT PROTEIN; SECRETASE; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME INHIBITION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; INSULIN RELEASE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STABLE TRANSFECTION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; DRUG EFFECTS; GENETIC TRANSFECTION; GENETICS; HUMAN; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOPHYSIOLOGY; SECRETION (PROCESS);

RATTUS;

AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ACID ENDOPEPTIDASES; CELL LINE; DIABETES MELLITUS, TYPE 2; GENE EXPRESSION PROFILING; GLUCOSE; HUMANS; INSULIN; INSULIN-SECRETING CELLS; ISLET AMYLOID POLYPEPTIDE; RATS; RECOMBINANT PROTEINS; RNA, MESSENGER; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 84928702501     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-255489     Document Type: Article

References (48)

1. Prentki, M., and Nolan, C. J. (2006) Islet beta cell failure in type 2 diabetes. J. Clin. Invest. 116, 1802-1812
2. Hull, R. L., Westermark, G. T., Westermark, P., and Kahn, S. E. (2004) Islet amyloid: a critical entity in the pathogenesis of type 2 diabetes. J. Clin. Endocrinol. Metab. 89, 3629-3643
3. Clark, A., Charge, S. B., Badman, M. K., MacArthur, D. A., and de Koning, E. J. (1996) Islet amyloid polypeptide: actions and role in the pathogenesis of diabetes. Biochem. Soc. Trans. 24, 594-599
4. Westermark, P., Andersson, A., and Westermark, G. T. (2011) Islet amyloid polypeptide, islet amyloid, and diabetes mellitus. Physiol. Rev. 91, 795-826
5. Butler, A. E., Janson, J., Bonner-Weir, S., Ritzel, R., Rizza, R. A., and Butler, P. C. (2003) Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52, 102-110
6. 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
7. Novials, A., Sarri, Y., Casamitjana, R., Rivera, F., and Gomis, R. (1993) Regulation of islet amyloid polypeptide in human pancreatic islets. Diabetes 42, 1514-1519
8. Westermark, P., Andersson, A., and Westermark, G. T. (2005) Is aggregated IAPP a cause of beta-cell failure in transplanted human pancreatic islets? Curr. Diab. Rep. 5, 184-188
9. Yankner, B. A., and Lu, T. (2009) Amyloid beta-protein toxicity and the pathogenesis of Alzheimer disease. J. Biol. Chem. 284, 4755-4759
10. Lu, J. X., Qiang, W., Yau, W. M., Schwieters, C. D., Meredith, S. C., and Tycko, R. (2013) Molecular structure of β-amyloid fibrils in Alzheimer's disease brain tissue. Cell 154, 1257-1268
11. Haataja, L., Gurlo, T., Huang, C. J., and Butler, P. C. (2008) Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis. Endocr. Rev. 29, 303-316
12. Casas, S., Gomis, R., Gribble, F. M., Altirriba, J., Knuutila, S., and Novials, A. (2007) Impairment of the ubiquitin-proteasome pathway is a downstream endoplasmic reticulum stress response induced by extracellular human islet amyloid polypeptide and contributes to pancreatic beta-cell apoptosis. Diabetes 56, 2284-2294
13. Casas, S., Novials, A., Reimann, F., Gomis, R., and Gribble, F. M. (2008) Calcium elevation in mouse pancreatic beta cells evoked by extracellular human islet amyloid polypeptide involves activation of the mechanosensitive ion channel TRPV4. Diabetologia 51, 2252-2262
14. Saunders, A. J., Kim, T.-W., Tanzi, R. E. (1999) BACE maps to chromosome 11 and a BACE homolog, BACE2, reside in the obligate Down syndrome region of chromosome 21. Science 286, 1255
15. Sun, X., Wang, Y., Qing, H., Christensen, M. A., Liu, Y., Zhou, W., Tong, Y., Xiao, C., Huang, Y., Zhang, S., Liu, X., and Song, W. (2005) Distinct transcriptional regulation and function of the human BACE2 and BACE1 genes. FASEB J. 19, 739-749
16. Lahiri, D. K., Maloney, B., and Ge, Y. W. (2006) Functional domains of the BACE1 and BACE2 promoters and mechanisms of transcriptional suppression of the BACE2 promoter in normal neuronal cells. J. Mol. Neurosci. 29, 65-80
17. Yan, R., Bienkowski, M. J., Shuck, M. E., Miao, H., Tory, M. C., Pauley, A. M., Brashier, J. R., Stratman, N. C., Mathews, W. R., Buhl, A. E., Carter, D. B., Tomasselli, A. G., Parodi, L. A., Heinrikson, R. L., and Gurney, M. E. (1999) Membrane-anchored aspartyl protease with Alzheimer's disease betasecretase activity. Nature 402, 533-537
18. Sinha, S., Anderson, J. P., Barbour, R., Basi, G. S., Caccavello, R., Davis, D., Doan, M., Dovey, H. F., Frigon, N., Hong, J., Jacobson-Croak, K., Jewett, N., Keim, P., Knops, J., Lieberburg, I., Power, M., Tan, H., Tatsuno, G., Tung, J., Schenk, D., Seubert, P., Suomensaari, S. M., Wang, S., Walker, D., Zhao, J., McConlogue, L., and John, V. (1999) Purification and cloning of amyloid precursor protein beta-secretase from human brain. Nature 402, 537-540
19. Bennett, B. D., Babu-Khan, S., Loeloff, R., Louis, J. C., Curran, E., Citron, M., and Vassar, R. (2000) Expression analysis of BACE2 in brain and peripheral tissues. J. Biol. Chem. 275, 20647-20651
20. Vassar, R., Bennett, B. D., Babu-Khan, S., Kahn, S., Mendiaz, E. A., Denis, P., Teplow, D. B., Ross, S., Amarante, P., Loeloff, R., Luo, Y., Fisher, S., Fuller, J., Edenson, S., Lile, J., Jarosinski, M. A., Biere, A. L., Curran, E., Burgess, T., Louis, J. C., Collins, F., Treanor, J., Rogers, G., and Citron, M. (1999) Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286, 735-741
21. Farzan, M., Schnitzler, C. E., Vasilieva, N., Leung, D., and Choe, H. (2000) BACE2, a beta -secretase homolog, cleaves at the beta site and within the amyloid-beta region of the amyloid-beta precursor protein. Proc. Natl. Acad. Sci. USA 97, 9712-9717
22. 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 β cell-enriched protease that regulates pancreatic β cell function and mass. Cell Metab. 14, 365-377
23. 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 β-cells. Am. J. Physiol. Endocrinol. Metab. 299, E1087-E1095
24. Soty, M., Visa, M., Soriano, S., Carmona, Mdel. C., Nadal, Á., and Novials, A. (2011) Involvement of ATP-sensitive potassium (K(ATP)) channels in the loss of beta-cell function induced by human islet amyloid polypeptide. J. Biol. Chem. 286, 40857-40866
25. Servitja, J. M., Pignatelli, M., Maestro, M. A., Cardalda, C., Boj, S. F., Lozano, J., Blanco, E., Lafuente, A., McCarthy, M. I., Sumoy, L., Guigó, R., and Ferrer, J. (2009) Hnf1alpha (MODY3) controls tissue-specific transcriptional programs and exerts opposed effects on cell growth in pancreatic islets and liver. Mol. Cell. Biol. 29, 2945-2959
26. Lu, A., Tebar, F., Alvarez-Moya, B., López-Alcalá, C., Calvo, M., Enrich, C., Agell, N., Nakamura, T., Matsuda, M., and Bachs, O. (2009) A clathrin-dependent pathway leads to KRas signaling on late endosomes en route to lysosomes. J. Cell Biol. 184, 863-879
27. Moreno-Asso, A., Castaño, C., Grilli, A., Novials, A., and Servitja, J. M. (2013) Glucose regulation of a cell cycle gene module is selectively lost in mouse pancreatic islets during ageing. Diabetologia 56, 1761-1772
28. Vassar, R., Kuhn, P. H., Haass, C., Kennedy, M. E., Rajendran, L., Wong, P. C., and Lichtenthaler, S. F. (2014) Function, therapeutic potential and cell biology of BACE proteases: current status and future prospects. J. Neurochem. 130, 4-28
29. Sun, X., Bromley-Brits, K., and Song, W. (2012) Regulation of β-site APP-cleaving enzyme 1 gene expression and its role in Alzheimer's disease. J. Neurochem. 120(Suppl 1), 62-70
30. Yang, Y., and Song, W. (2013) Molecular links between Alzheimer's disease and diabetes mellitus. Neuroscience 250, 140-150
31. Holler, C. J., Webb, R. L., Laux, A. L., Beckett, T. L., Niedowicz, D. M., Ahmed, R. R., Liu, Y., Simmons, C. R., Dowling, A. L., Spinelli, A., Khurgel, M., Estus, S., Head, E., Hersh, L. B., and Murphy, M. P. (2012) BACE2 expression increases in human neurodegenerative disease. Am. J. Pathol. 180, 337-350
32. Sun, X., He, G., and Song, W. (2006) BACE2, as a novel APP theta-secretase, is not responsible for the pathogenesis of Alzheimer's disease in Down syndrome. FASEB J. 20, 1369-1376
33. Abdul-Hay, S. O., Sahara, T., McBride, M., Kang, D., and Leissring, M. A. (2012) Identification of BACE2 as an avid β-amyloid-degrading protease. Mol. Neurodegener. 7, 46
34. Stützer, I., Esterházy, D., and Stoffel, M. (2012) The pancreatic beta cell surface proteome. Diabetologia 55, 1877-1889
35. Stützer, I., Selevsek, N., Esterházy, D., Schmidt, A., Aebersold, R., and Stoffel, M. (2013) Systematic proteomic analysis identifies β-site amyloid precursor protein cleaving enzyme 2 and 1 (BACE2 and BACE1) substrates in pancreatic β-cells. J. Biol. Chem. 288, 10536-10547
36. Altirriba, J., Gasa, R., Casas, S., Ramírez-Bajo, M. J., Ros, S., Gutierrez-Dalmau, A., Ruiz de Villa, M. C., Barbera, A., and Gomis, R. (2010) The role of transmembrane protein 27 (TMEM27) in islet physiology and its potential use as a beta cell mass biomarker. Diabetologia 53, 1406-1414
37. 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 Metab. 2, 385-397
38. Yamagata, K., Senokuchi, T., Lu, M., Takemoto, M., Fazlul Karim, M., Go, C., Sato, Y., Hatta, M., Yoshizawa, T., Araki, E., Miyazaki, J., and Song, W. J. (2011) Voltage-gated K+ channel KCNQ1 regulates insulin secretion in MIN6 β-cell line. Biochem. Biophys. Res. Commun. 407, 620-625
39. Jonsson, A., Isomaa, B., Tuomi, T., Taneera, J., Salehi, A., Nilsson, P., Groop, L., and Lyssenko, V. (2009) A variant in the KCNQ1 gene predicts future type 2 diabetes and mediates impaired insulin secretion. Diabetes 58, 2409-2413
40. Cho, Y. S., Chen, C. H., Hu, C., Long, J., Ong, R. T., Sim, X., Takeuchi, F., Wu, Y., Go, M. J., Yamauchi, T., Chang, Y. C., Kwak, S. H., Ma, R. C., Yamamoto, K., Adair, L. S., Aung, T., Cai, Q., Chang, L. C., Chen, Y. T., Gao, Y., Hu, F. B., Kim, H. L., Kim, S., Kim, Y. J., Lee, J. J., Lee, N. R., Li, Y., Liu, J. J., Lu, W., Nakamura, J., Nakashima, E., Ng, D. P., Tay, W. T., Tsai, F. J., Wong, T. Y., Yokota, M., Zheng, W., Zhang, R., Wang, C., So, W. Y., Ohnaka, K., Ikegami, H., Hara, K., Cho, Y. M., Cho, N. H., Chang, T. J., Bao, Y., Hedman, Å. K., Morris, A. P., McCarthy, M. I., DIAGRAM Consortium, MuTHER Consortium, Takayanagi, R., Park, K. S., Jia, W., Chuang, L. M., Chan, J. C., Maeda, S., Kadowaki, T., Lee, J. Y., Wu, J. Y., Teo, Y. Y., Tai, E. S., Shu, X. O., Mohlke, K. L., Kato, N., Han, B. G., and Seielstad, M. (2011) Meta-analysis of genome-wide association studies identifies eight new loci for type 2 diabetes in east Asians. Nat. Genet. 44, 67-72
41. Gurlo, T., Ryazantsev, S., Huang, C. J., Yeh, M. W., Reber, H. A., Hines, O. J., O'Brien, T. D., Glabe, C. G., and Butler, P. C. (2010) Evidence for proteotoxicity in beta cells in type 2 diabetes: toxic islet amyloid polypeptide oligomers form intracellularly in the secretory pathway. Am. J. Pathol. 176, 861-869
42. Meier, J. J., Kayed, R., Lin, C. Y., Gurlo, T., Haataja, L., Jayasinghe, S., Langen, R., Glabe, C. G., and Butler, P. C. (2006) Inhibition of human IAPP fibril formation does not prevent beta-cell death: evidence for distinct actions of oligomers and fibrils of human IAPP. Am. J. Physiol. Endocrinol. Metab. 291, E1317-E1324
43. Hull, R. L., Zraika, S., Udayasankar, J., Aston-Mourney, K., Subramanian, S. L., and Kahn, S. E. (2009) Amyloid formation in human IAPP transgenic mouse islets and pancreas, and human pancreas, is not associated with endoplasmic reticulum stress. Diabetologia 52, 1102-1111
44. Liu, X., Wang, Z., Wu, Y., Wang, J., and Song, W. (2013) BACE2 degradation mediated by the macroautophagy-lysosome pathway. Eur. J. Neurosci. 37, 1970-1977
45. Rivera, J. F., Gurlo, T., Daval, M., Huang, C. J., Matveyenko, A. V., Butler, P. C., and Costes, S. (2011) Human-IAPP disrupts the autophagy/lysosomal pathway in pancreatic β-cells: protective role of p62-positive cytoplasmic inclusions. Cell Death Differ. 18, 415-426
46. Southan, C. (2013) BACE2 as a new diabetes target: a patent review (2010-2012). Expert Opin. Ther. Pat. 23, 649-663
47. Southan, C., and Hancock, J. M. (2013) A tale of two drug targets: the evolutionary history of BACE1 and BACE2. Front. Genet. 4, 293
48. Gilbert, E. J. (2013) 1,3-Oxazines as BACE1 and/or BACE2 inhibitors: a patent evaluation (WO2012156284). Expert Opin. Ther. Pat. 23, 1069-1073