Bisecting GlcNAc modification stabilizes BACE1 protein under oxidative stress conditions

Biochemical Journal

Volumn 473, Issue 1, 2016, Pages 21-30

  Kizuka, Yasuhiko ^a   Nakano, Miyako ^b   Kitazume, Shinobu ^a   Saito, Takashi ^c   Saido, Takaomi C ^c   Taniguchi, Naoyuki ^a  

^a RIKEN   (Japan)

^b HIROSHIMA UNIVERSITY   (Japan)

^c RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Alzheimer's disease; BACE1; Bisecting GlcNAc; Glycobiology; GnT III; Oxidative stress.

Indexed keywords

AMYLOID BETA PROTEIN; BETA SECRETASE 1; N ACETYLGLUCOSAMINE; ASPARTIC PROTEINASE; BACE1 PROTEIN, HUMAN; SECRETASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN INJURY; CONTROLLED STUDY; ELECTROSPRAY; EMBRYO; FIBROBLAST; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; MOUSE; NONHUMAN; OXIDATIVE STRESS; POINT MUTATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN STABILITY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION; STEADY STATE; TANDEM MASS SPECTROMETRY; UPREGULATION; ANIMAL; BIOSYNTHESIS; BRAIN; C57BL MOUSE; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; TRANSFORMED CELL LINE; TUMOR CELL LINE;

ACETYLGLUCOSAMINE; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ACID ENDOPEPTIDASES; BRAIN; BRAIN INJURIES; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OXIDATIVE STRESS;

EID: 84955477662     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20150607     Document Type: Article

References (43)

1. Selkoe, D.J. (2011) Resolving controversies on the path to Alzheimer's therapeutics. Nat. Med. 17, 1060-1065
2. Abbott, A. (2011) Dementia: A problem for our age. Nature 475, S2-S4
3. O'Brien, R.J. and Wong, P.C. (2011) Amyloid precursor protein processing and Alzheimer's disease. Annu. Rev. Neurosci. 34, 185-204
4. Karran, E., Mercken, M. and De Strooper, B. (2011) The amyloid cascade hypothesis for Alzheimer's disease: An appraisal for the development of therapeutics. Nat. Rev. Drug Discov. 10, 698-712
5. 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
6. Yang, L.B., Lindholm, K., Yan, R., Citron, M., Xia, W., Yang, X.L., Beach, T., Sue, L., Wong, P., Price, D. et al. (2003) Elevated beta-secretase expression and enzymatic activity detected in sporadic Alzheimer disease. Nat. Med. 9, 3-4
7. Loane, D.J., Pocivavsek, A., Moussa, C.E., Thompson, R., Matsuoka, Y., Faden, A.I., Rebeck, G.W. and Burns, M.P. (2009) Amyloid precursor protein secretases as therapeutic targets for traumatic brain injury. Nat. Med. 15, 377-379
8. Kandalepas, P.C., Sadleir, K.R., Eimer, W.A., Zhao, J., Nicholson, D.A. and Vassar, R. (2013) The Alzheimer's beta-secretase BACE1 localizes to normal presynaptic terminals and to dystrophic presynaptic terminals surrounding amyloid plaques. Acta Neuropathol. 126, 329-352
9. Kao, S.C., Krichevsky, A.M., Kosik, K.S. and Tsai, L. H. (2004) BACE1 suppression by RNA interference in primary cortical neurons. J. Biol. Chem. 279, 1942-1949
10. Lu, T., Pan, Y., Kao, S.Y., Li, C., Kohane, I., Chan, J. and Yankner, B.A. (2004) Gene regulation and DNA damage in the ageing human brain. Nature 429, 883-891
11. Mohmmad Abdul, H., Sultana, R., Keller, J.N., St Clair, D.K., Markesbery, W.R. and Butterfield, D.A. (2006) Mutations in amyloid precursor protein and presenilin-1 genes increase the basal oxidative stress in murine neuronal cells and lead to increased sensitivity to oxidative stress mediated by amyloid beta-peptide (1-42), HO and kainic acid: implications for Alzheimer's disease. J. Neurochem. 96, 1322-1335
12. Bains, M. and Hall, E.D. (2012) Antioxidant therapies in traumatic brain and spinal cord injury. Biochim. Biophys. Acta 1822, 675-684
13. Guglielmotto, M., Aragno, M., Autelli, R., Giliberto, L., Novo, E., Colombatto, S., Danni, O., Parola, M., Smith, M.A., Perry, G. et al. (2009) The up-regulation of BACE1 mediated by hypoxia and ischemic injury: role of oxidative stress and HIF1alpha. J. Neurochem. 108, 1045-1056
14. Tan, J.L., Li, Q.X., Ciccotosto, G.D., Crouch, P.J., Culvenor, J.G., White, A.R. and Evin, G. (2013) Mild oxidative stress induces redistribution of BACE1 in non-Apoptotic conditions and promotes the amyloidogenic processing of Alzheimer's disease amyloid precursor protein. PLoS One 8, e61246
15. Sadleir, K.R. and Vassar, R. (2012) Cdk5 protein inhibition and Abeta42 increase BACE1 protein level in primary neurons by a post-Transcriptional mechanism: implications of CDK5 as a therapeutic target for Alzheimer disease. J. Biol. Chem. 287, 7224-7235
16. Kizuka, Y., Kitazume, S., Fujinawa, R., Saito, T., Iwata, N., Saido, T.C., Nakano, M., Yamaguchi, Y., Hashimoto, Y., Staufenbiel, M. et al. (2015) An aberrant sugar modification of BACE1 blocks its lysosomal targeting in Alzheimer's disease. EMBO Mol. Med. 7, 175-189
17. Taniguchi, N., Miyoshi, E., Gu, J., Honke, K. and Matsumoto, A. (2006) Decoding sugar functions by identifying target glycoproteins. Curr. Opin. Struct. Biol. 16, 561-566
18. Miyoshi, E., Uozumi, N., Noda, K., Hayashi, N., Hori, M. and Taniguchi, N. (1997) Expression of alpha1-6 fucosyltransferase in rat tissues and human cancer cell lines. Int. J. Cancer 72, 1117-1121
19. Akasaka-Manya, K., Manya, H., Sakurai, Y., Wojczyk, B.S., Kozutsumi, Y., Saito, Y., Taniguchi, N., Murayama, S., Spitalnik, S.L. and Endo, T. (2010) Protective effect of N-glycan bisecting GlcNAc residues on beta-Amyloid production in Alzheimer's disease. Glycobiology 20, 99-106
20. Kurimoto, A., Kitazume, S., Kizuka, Y., Nakajima, K., Oka, R., Fujinawa, R., Korekane, H., Yamaguchi, Y., Wada, Y. and Taniguchi, N. (2014) The absence of core fucose up-regulates GnT-III and Wnt target genes: A possible mechanism for an adaptive response in terms of glycan function. J. Biol. Chem. 289, 11704-11714
21. Priatel, J.J., Sarkar, M., Schachter, H. and Marth, J.D. (1997) Isolation, characterization and inactivation of the mouse Mgat3 gene: The bisecting N-Acetylglucosamine in asparagine-linked oligosaccharides appears dispensable for viability and reproduction. Glycobiology 7, 45-56
22. Saito, T., Matsuba, Y., Mihira, N., Takano, J., Nilsson, P., Itohara, S., Iwata, N. and Saido, T.C. (2014) Single App knock-in mouse models of Alzheimer's disease. Nat. Neurosci. 17, 661-663
23. Kitazume, S., Tachida, Y., Oka, R., Shirotani, K., Saido, T.C. and Hashimoto, Y. (2001) Alzheimer's beta-secretase, beta-site amyloid precursor protein-cleaving enzyme, is responsible for cleavage secretion of a Golgi-resident sialyltransferase. Proc. Natl. Acad. Sci. U.S.A. 98, 13554-13559
24. Nakano, M., Nakagawa, T., Ito, T., Kitada, T., Hijioka, T., Kasahara, A., Tajiri, M., Wada, Y., Taniguchi, N. and Miyoshi, E. (2008) Site-specific analysis of N-glycans on haptoglobin in sera of patients with pancreatic cancer: A novel approach for the development of tumor markers. Int. J. Cancer. 122, 2301-2309
25. Nakano, M., Saldanha, R., Gobel, A., Kavallaris, M. and Packer, N.H. (2011) Identification of glycan structure alterations on cell membrane proteins in desoxyepothilone B resistant leukemia cells. Mol. Cell Proteomics 10, M111.009001
26. Mouton-Liger, F., Paquet, C., Dumurgier, J., Bouras, C., Pradier, L., Gray, F. and Hugon, J. (2012) Oxidative stress increases BACE1 protein levels through activation of the PKR-eIF2alpha pathway. Biochim. Biophys. Acta 1822, 885-896
27. Zhang, X.M., Cai, Y., Xiong, K., Cai, H., Luo, X.G., Feng, J.C., Clough, R.W., Struble, R.G., Patrylo, P.R. and Yan, X.X. (2009) Beta-secretase-1 elevation in transgenic mouse models of Alzheimer's disease is associated with synaptic/axonal pathology and amyloidogenesis: implications for neuritic plaque development. Eur. J. Neurosci. 30, 2271-2283
28. Cummings, R.D. and Kornfeld, S. (1982) Characterization of the structural determinants required for the high affinity interaction of asparagine-linked oligosaccharides with immobilized Phaseolus vulgaris leukoagglutinating and erythroagglutinating lectins. J. Biol. Chem. 257, 11230-11234
29. Parrinello, S., Samper, E., Krtolica, A., Goldstein, J., Melov, S. and Campisi, J. (2003) Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat. Cell Biol. 5, 741-747
30. Koh, Y.H., von Arnim, C.A., Hyman, B.T., Tanzi, R.E. and Tesco, G. (2005) BACE is degraded via the lysosomal pathway. J. Biol. Chem. 280, 32499-32504
31. Walker, K.R., Kang, E.L., Whalen, M.J., Shen, Y. and Tesco, G. (2012) Depletion of GGA1 and GGA3 mediates postinjury elevation of BACE1. J. Neurosci. 32, 10423-10437
32. Tesco, G., Koh, Y.H., Kang, E.L., Cameron, A.N., Das, S., Sena-Esteves, M., Hiltunen, M., Yang, S.H., Zhong, Z., Shen, Y. et al. (2007) Depletion of GGA3 stabilizes BACE and enhances beta-secretase activity. Neuron 54, 721-737
33. Mustafa, A.G., Singh, I.N., Wang, J., Carrico, K.M. and Hall, E.D. (2010) Mitochondrial protection after traumatic brain injury by scavenging lipid peroxyl radicals. J. Neurochem. 114, 271-280
34. Tamagno, E., Guglielmotto, M., Aragno, M., Borghi, R., Autelli, R., Giliberto, L., Muraca, G., Danni, O., Zhu, X., Smith, M.A. et al. (2008) Oxidative stress activates a positive feedback between the gamma-And beta-secretase cleavages of the beta-Amyloid precursor protein. J. Neurochem. 104, 683-695
35. von Bernhardi, R. and Eugenin, J. (2012) Alzheimer's disease: redox dysregulation as a common denominator for diverse pathogenic mechanisms. Antioxid. Redox Signal. 16, 974-1031
36. Sivanandam, T.M. and Thakur, M.K. (2012) Traumatic brain injury: A risk factor for Alzheimer's disease. Neurosci. Biobehav. Rev. 36, 1376-1381
37. Kang, E.L., Cameron, A.N., Piazza, F., Walker, K.R. and Tesco, G. (2010) Ubiquitin regulates GGA3-mediated degradation of BACE1. J. Biol. Chem. 285, 24108-24119
38. Zhao, Y., Sato, Y., Isaji, T., Fukuda, T., Matsumoto, A., Miyoshi, E., Gu, J. and Taniguchi, N. (2008) Branched N-glycans regulate the biological functions of integrins and cadherins. FEBS J. 275, 1939-1948
39. Taniguchi, N. and Korekane, H. (2011) Branched N-glycans and their implications for cell adhesion, signaling and clinical applications for cancer biomarkers and in therapeutics. BMB Rep. 44, 772-781
40. Nishima, W., Miyashita, N., Yamaguchi, Y., Sugita, Y. and Re, S. (2012) Effect of bisecting GlcNAc and core fucosylation on conformational properties of biantennary complex-Type N-glycans in solution. J. Phys. Chem. B 116, 8504-8512
41. Re, S., Miyashita, N., Yamaguchi, Y. and Sugita, Y. (2011) Structural diversity and changes in conformational equilibria of biantennary complex-Type N-glycans in water revealed by replica-exchange molecular dynamics simulation. Biophys. J. 101, L44-46
42. Schieber, M. and Chandel, N.S. (2014) ROS function in redox signaling and oxidative stress. Curr. Biol. 24, R453-462
43. Fiala, M., Liu, P.T., Espinosa-Jeffrey, A., Rosenthal, M. J., Bernard, G., Ringman, J.M., Sayre, J., Zhang, L., Zaghi, J., Dejbakhsh, S. et al. (2007) Innate immunity and transcription of MGAT-III and Toll-like receptors in Alzheimer's disease patients are improved by bisdemethoxycurcumin. Proc. Natl. Acad. Sci. U.S.A. 104, 12849-12854