The endosome-associated deubiquitinating enzyme USP8 regulates BACE1 enzyme ubiquitination and degradation

Journal of Biological Chemistry

Volumn 291, Issue 30, 2016, Pages 15753-15766

  Yeates, Eniola Funmilayo Aduke ^a   Tesco, Giuseppina ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINS; BIOLOGICAL MEMBRANES; CELL MEMBRANES; DISEASE CONTROL; ENZYME ACTIVITY; ENZYMES; GLYCOPROTEINS; NEURODEGENERATIVE DISEASES;

AMYLOID PRECURSOR PROTEINS; DEUBIQUITINATING ENZYMES; LYSOSOMAL DEGRADATION; NEUROGLIOMA CELLS; PLASMA MEMBRANE PROTEIN; RATE-LIMITING ENZYMES; RECYCLING ENDOSOMES; REVERSIBLE PROCESS;

PROTEINS;

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE 1; DEUBIQUITINASE; LYSINE; UNCLASSIFIED DRUG; USP8 PROTEIN; APP PROTEIN, HUMAN; ASPARTIC PROTEINASE; BACE1 PROTEIN, HUMAN; ESCRT PROTEIN; GGA ADAPTOR PROTEINS; PROTEINASE; SECRETASE; UBIQUITIN THIOLESTERASE; USP8 PROTEIN, HUMAN; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ARTICLE; BIOACCUMULATION; ENDOSOME; ENZYME DEGRADATION; GLIOMA CELL; HUMAN; HUMAN CELL; LYSOSOME; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEPLETION; PROTEIN EXPRESSION; RNA INTERFERENCE; UBIQUITINATION; ALZHEIMER DISEASE; GENETICS; METABOLISM; PROTEIN DEGRADATION; PROTEIN TRANSPORT; TUMOR CELL LINE;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ASPARTIC ACID ENDOPEPTIDASES; CELL LINE, TUMOR; ENDOPEPTIDASES; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; HUMANS; LYSOSOMES; PROTEIN TRANSPORT; PROTEOLYSIS; UBIQUITIN THIOLESTERASE; UBIQUITINATION;

EID: 84978985707     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.718023     Document Type: Article

References (71)

1. 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., et al. (1999) Purification and cloning of amyloid precursor protein β-secretase from human brain. Nature 402, 537-540
2. 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 β-secretase activity. Nature 402, 533-537
3. Hong, L., Koelsch, G., Lin, X., Wu, S., Terzyan, S., Ghosh, A. K., Zhang, X. C., and Tang, J. (2000) Structure of the protease domain of memapsin 2 (β-secretase) complexed with inhibitor. Science 290, 150-153
4. 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., et al. (1999) β-Secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286, 735-741
5. De Strooper, B. (2000) Alzheimer's disease. Closing in on γ-secretase. Nature 405, 627, 629
6. Buxbaum, J. D., Liu, K. N., Luo, Y., Slack, J. L., Stocking, K. L., Peschon, J. J., Johnson, R. S., Castner, B. J., Cerretti, D. P., and Black, R. A. (1998) Evidence that tumor necrosis factor α converting enzyme is involved in regulated α-secretase cleavage of the Alzheimer amyloid protein precursor. J. Biol. Chem. 273, 27765-27767
7. Lammich, S., Kojro, E., Postina, R., Gilbert, S., Pfeiffer, R., Jasionowski, M., Haass, C., and Fahrenholz, F. (1999) Constitutive and regulated α-secretase cleavage of Alzheimer's amyloid precursor protein by a disintegrin metalloprotease. Proc. Natl. Acad. Sci. U.S.A. 96, 3922-3927
8. Haass, C. (2004) Take five-BACE and the γ-secretase quartet conduct Alzheimer's amyloid β-peptide generation. EMBO J. 23, 483-488
9. Lichtenthaler, S. F., Haass, C., and Steiner, H. (2011) Regulated intramembrane proteolysis-lessons from amyloid precursor protein processing. J. Neurochem. 117, 779-796
10. Citron, M. (2004) β-Secretase inhibition for the treatment of Alzheimer's disease-promise and challenge. Trends Pharmacol. Sci. 25, 92-97
11. Haass, C., Kaether, C., Thinakaran, G., and Sisodia, S. (2012) Trafficking and proteolytic processing of APP. Cold Spring Harb. Perspect. Med. 2, a006270
12. Bonifacino, J. S., and Traub, L. M. (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72, 395-447
13. 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
14. 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., Simpkins, J. W., and Tanzi, R. E. (2007) Depletion of gga3 stabilizes BACE and enhances β-secretase activity. Neuron 54, 721-737
15. 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
16. 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
17. Kang, E. L., Biscaro, B., Piazza, F., and Tesco, G. (2012) BACE1 protein endocytosis and trafficking are differentially regulated by ubiquitination at lysine 501 and the di-leucine motif in the carboxyl terminus. J. Biol. Chem. 287, 42867-42880
18. Piper, R. C., and Luzio, J. P. (2007) Ubiquitin-dependent sorting of integral membrane proteins for degradation in lysosomes. Curr. Opin. Cell Biol. 19, 459-465
19. Davies, B. A., Lee, J. R., Oestreich, A. J., and Katzmann, D. J. (2009) Membrane protein targeting to the MVB/lysosome. Chem. Rev. 109, 1575-1586
20. Lauwers, E., Erpapazoglou, Z., Haguenauer-Tsapis, R., and André, B. (2010) The ubiquitin code of yeast permease trafficking. Trends Cell Biol. 20, 196-204
21. Clague, M. J., Coulson, J. M., and Urbé, S. (2012) Cellular functions of the dubs. J. Cell Sci. 125, 277-286
22. Bruzzone, F., Vallarino, M., Berruti, G., and Angelini, C. (2008) Expression of the deubiquitinating enzyme mubpy in the mouse brain. Brain Res. 1195, 56-66
23. Mizuno, E., Iura, T., Mukai, A., Yoshimori, T., Kitamura, N., and Komada, M. (2005) Regulation of epidermal growth factor receptor down-regulation by ubpy-mediated deubiquitination at endosomes. Mol. Biol. Cell 16, 5163-5174
24. Row, P. E., Prior, I. A., McCullough, J., Clague, M. J., and Urbé, S. (2006) The ubiquitin isopeptidase ubpy regulates endosomal ubiquitin dynamics and is essential for receptor down-regulation. J. Biol. Chem. 281, 12618-12624
25. Ceriani, M., Amigoni, L., D'Aloia, A., Berruti, G., and Martegani, E. (2015) The deubiquitinating enzyme ubpy/usp8 interacts with trka and inhibits neuronal differentiation in pc12 cells. Exp. Cell Res. 333, 49-59
26. Clague, M. J., and Urbé, S. (2006) Endocytosis: The dub version. Trends Cell Biol. 16, 551-559
27. Durcan, T. M., Tang, M. Y., Pérusse, J. R., Dashti, E. A., Aguileta, M. A., McLelland, G. L., Gros, P., Shaler, T. A., Faubert, D., Coulombe, B., and Fon, E. A. (2014) Usp8 regulates mitophagy by removing k6-linked ubiquitin conjugates from parkin. EMBO J. 33, 2473-2491
28. Alwan, H. A., and van Leeuwen, J. E. (2007) Ubpy-mediated epidermal growth factor receptor (egfr) de-ubiquitination promotes egfr degradation. J. Biol. Chem. 282, 1658-1669
29. Sirisaengtaksin, N., Gireud, M., Yan, Q., Kubota, Y., Meza, D., Waymire, J. C., Zage, P. E., and Bean, A. J. (2014) Ube4b protein couples ubiquitination and sorting machineries to enable epidermal growth factor receptor (egfr) degradation. J. Biol. Chem. 289, 3026-3039
30. Scudder, S. L., Goo, M. S., Cartier, A. E., Molteni, A., Schwarz, L. A., Wright, R., and Patrick, G. N. (2014) Synaptic strength is bidirectionally controlled by opposing activity-dependent regulation of nedd4-1 and usp8. J. Neurosci. 34, 16637-16649
31. Smith, G. A., Fearnley, G. W., Abdul-Zani, I., Wheatcroft, S. B., Tomlinson, D. C., Harrison, M. A., and Ponnambalam, S. (2016) Vegfr2 trafficking, signaling and proteolysis is regulated by the ubiquitin isopeptidase usp8. Traffic 17, 53-65
32. Oh, Y. M., Lee, S. B., Choi, J., Suh, H. Y., Shim, S., Song, Y. J., Kim, B., Lee, J. M., Oh, S. J., Jeong, Y., Cheong, K. H., Song, P. H., and Kim, K. A. (2014) Usp8 modulates ubiquitination of lrig1 for met degradation. Sci. Rep. 4, 4980
33. Balut, C. M., Loch, C. M., and Devor, D. C. (2011) Role of ubiquitylation and usp8-dependent deubiquitylation in the endocytosis and lysosomal targeting of plasma membrane kca3.1. FASEB J. 25, 3938-3948
34. Hasdemir, B., Murphy, J. E., Cottrell, G. S., and Bunnett, N. W. (2009) Endosomal deubiquitinating enzymes control ubiquitination and down-regulation of protease-activated receptor 2. J. Biol. Chem. 284, 28453-28466
35. Hislop, J. N., Henry, A. G., Marchese, A., and von Zastrow, M. (2009) Ubiquitination regulates proteolytic processing of g protein-coupled receptors after their sorting to lysosomes. J. Biol. Chem. 284, 19361-19370
36. Niendorf, S., Oksche, A., Kisser, A., Löhler, J., Prinz, M., Schorle, H., Feller, S., Lewitzky, M., Horak, I., and Knobeloch, K.-P. (2007) Essential role of ubiquitin-specific protease 8 for receptor tyrosine kinase stability and endocytic trafficking in vivo. Mol. Cell. Biol. 27, 5029-5039
37. Berlin, I., Schwartz, H., and Nash, P. (2010) Regulation of epidermal growth factor receptor ubiquitination and trafficking by the usp8: Stam complex. J. Biol. Chem. 285, 34909-34921
38. Kato, M., Miyazawa, K., and Kitamura, N. (2000) A deubiquitinating enzyme ubpy interacts with the src homology 3 domain of hrs-binding protein via a novel binding motif px(v/i)(d/n)rxxkp. J. Biol. Chem. 275, 37481-37487
39. Lichtenthaler, S. F., Ida, N., Multhaup, G., Masters, C. L., and Beyreuther, K. (1997) Mutations in the transmembrane domain of app altering γ-secretase specificity. Biochemistry 36, 15396-15403
40. Bache, K. G., Raiborg, C., Mehlum, A., and Stenmark, H. (2003) Stam and hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes. J. Biol. Chem. 278, 12513-12521
41. Mizuno, E., Kobayashi, K., Yamamoto, A., Kitamura, N., and Komada, M. (2006) A deubiquitinating enzyme ubpy regulates the level of protein ubiquitination on endosomes. Traffic 7, 1017-1031
42. Bowers, K., Piper, S. C., Edeling, M. A., Gray, S. R., Owen, D. J., Lehner, P. J., and Luzio, J. P. (2006) Degradation of endocytosed epidermal growth factor and virally ubiquitinated major histocompatibility complex class i is independent of mammalian escrtii. J. Biol. Chem. 281, 5094-5105
43. Morel, E., Chamoun, Z., Lasiecka, Z. M., Chan, R. B., Williamson, R. L., Vetanovetz, C., Dall'Armi, C., Simoes, S., Point Du Jour, K. S., McCabe, B. D., Small, S. A., and Di Paolo, G. (2013) Phosphatidylinositol-3-phosphate regulates sorting and processing of amyloid precursor protein through the endosomal system. Nat. Commun. 4, 2250
44. Edbauer, D., Winkler, E., Haass, C., and Steiner, H. (2002) Presenilin and nicastrin regulate each other and determine amyloid β-peptide production via complex formation. Proc. Natl. Acad. Sci. U.S.A. 99, 8666-8671
45. Kimberly, W. T., Zheng, J. B., Guénette, S. Y., and Selkoe, D. J. (2001) The intracellular domain of the β-amyloid precursor protein is stabilized by fe65 and translocates to the nucleus in a notch-like manner. J. Biol. Chem. 276, 40288-40292
46. Urbé, S., Liu, H., Hayes, S. D., Heride, C., Rigden, D. J., and Clague, M. J. (2012) Systematic survey of deubiquitinase localization identifies usp21 as a regulator of centrosome- and microtubule-associated functions. Mol. Biol. Cell 23, 1095-1103
47. Creemers, J. W., Ines Dominguez, D., Plets, E., Serneels, L., Taylor, N. A., Multhaup, G., Craessaerts, K., Annaert, W., and De Strooper, B. (2001) Processing of β-secretase by furin and other members of the proprotein convertase family. J. Biol. Chem. 276, 4211-4217
48. Wu, X., Yen, L., Irwin, L., Sweeney, C., and Carraway, K. L., 3rd. (2004) Stabilization of the e3 ubiquitin ligase nrdp1 by the deubiquitinating enzyme usp8. Mol. Cell. Biol. 24, 7748-7757
49. Avvakumov, G. V., Walker, J. R., Xue, S., Finerty, P. J., Jr., Mackenzie, F., Newman, E. M., and Dhe-Paganon, S. (2006) Amino-terminal dimerization, nrdp1-rhodanese interaction, and inhibited catalytic domain conformation of the ubiquitin-specific protease 8 (usp8). J. Biol. Chem. 281, 38061-38070
50. Soares, L., Seroogy, C., Skrenta, H., Anandasabapathy, N., Lovelace, P., Chung, C. D., Engleman, E., and Fathman, C. G. (2004) Two isoforms of otubain 1 regulate t cell anergy via grail. Nat. Immunol. 5, 45-54
51. Puertollano, R., and Bonifacino, J. S. (2004) Interactions of gga3 with the ubiquitin sorting machinery. Nat. Cell Biol. 6, 244-251
52. Bilodeau, P. S., Winistorfer, S. C., Allaman, M. M., Surendhran, K., Kearney, W. R., Robertson, A. D., and Piper, R. C. (2004) The gat domains of clathrin-associated gga proteins have two ubiquitin binding motifs. J. Biol. Chem. 279, 54808-54816
53. Prag, G., Lee, S., Mattera, R., Arighi, C. N., Beach, B. M., Bonifacino, J. S., and Hurley, J. H. (2005) Structural mechanism for ubiquitinated-cargo recognition by the golgi-localized, γ-ear-containing, adp-ribosylation-factor-binding proteins. Proc. Natl. Acad. Sci. U.S.A. 102, 2334-2339
54. Kawasaki, M., Shiba, T., Shiba, Y., Yamaguchi, Y., Matsugaki, N., Igarashi, N., Suzuki, M., Kato, R., Kato, K., Nakayama, K., and Wakatsuki, S. (2005) Molecular mechanism of ubiquitin recognition by gga3 gat domain. Genes Cells 10, 639-654
55. Das, U., Wang, L., Ganguly, A., Saikia, J. M., Wagner, S. L., Koo, E. H., and Roy, S. (2016) Visualizing app and bace-1 approximation in neurons yields insight into the amyloidogenic pathway. Nat. Neurosci. 19, 55-64
56. Das, U., Scott, D. A., Ganguly, A., Koo, E. H., Tang, Y., and Roy, S. (2013) Activity-induced convergence of app and bace-1 in acidic microdomains via an endocytosis-dependent pathway. Neuron 79, 447-460
57. Buggia-Prévot, V., Fernandez, C. G., Udayar, V., Vetrivel, K. S., Elie, A., Roseman, J., Sasse, V. A., Lefkow, M., Meckler, X., Bhattacharyya, S., George, M., Kar, S., Bindokas, V. P., Parent, A. T., Rajendran, L., et al. (2013) A function for ehd family proteins in unidirectional retrograde dendritic transport of bace1 and Alzheimer's disease Aβ production. Cell Rep. 5, 1552-1563
58. Bustamante, H. A., Rivera-Dictter, A., Cavieres, V. A., Muñoz, V. C., González, A., Lin, Y., Mardones, G. A., and Burgos, P. V. (2013) Turnover of c99 is controlled by a crosstalk between erad and ubiquitin-independent lysosomal degradation in human neuroglioma cells. PLoS ONE 8, e83096
59. Vingtdeux, V., Hamdane, M., Bégard, S., Loyens, A., Delacourte, A., Beauvillain, J. C., Buée, L., Marambaud, P., and Sergeant, N. (2007) Intracellular pH regulates amyloid precursor protein intracellular domain accumulation. Neurobiol. Dis. 25, 686-696
60. Vingtdeux, V., Hamdane, M., Loyens, A., Gelé, P., Drobeck, H., Bégard, S., Galas, M. C., Delacourte, A., Beauvillain, J. C., Buée, L., and Sergeant, N. (2007) Alkalizing drugs induce accumulation of amyloid precursor protein by-products in luminal vesicles of multivesicular bodies. J. Biol. Chem. 282, 18197-18205
61. Slomnicki, L. P., and Lesniak, W. (2008) A putative role of the amyloid precursor protein intracellular domain (aicd) in transcription. Acta Neurobiol. Exp. 68, 219-228
62. Lee, E. J., Hyun, S., Chun, J., Shin, S. H., and Kang, S. S. (2009) Ubiquitylation of fe65 adaptor protein by neuronal precursor cell expressed developmentally down regulated 4-2 (nedd4-2) via the ww domain interaction with fe65. Exp. Mol. Med. 41, 555-568
63. Matz, A., Lee, S. J., Schwedhelm-Domeyer, N., Zanini, D., Holubowska, A., Kannan, M., Farnworth, M., Jahn, O., Göpfert, M. C., and Stegmüller, J. (2015) Regulation of neuronal survival and morphology by the e3 ubiquitin ligase rnf157. Cell Death Differ. 22, 626-642
64. Zhang, M., Deng, Y., Luo, Y., Zhang, S., Zou, H., Cai, F., Wada, K., and Song, W. (2012) Control of bace1 degradation and app processing by ubiquitin carboxyl-terminal hydrolase l1. J. Neurochem. 120, 1129-1138
65. Guglielmotto, M., Monteleone, D., Boido, M., Piras, A., Giliberto, L., Borghi, R., Vercelli, A., Fornaro, M., Tabaton, M., and Tamagno, E. (2012) Aβ1-42-mediated down-regulation of uch-l1 is dependent on NF-κB activation and impaired bace1 lysosomal degradation. Aging Cell 11, 834-844
66. Liu, Y., Fallon, L., Lashuel, H. A., Liu, Z., and Lansbury, P. T., Jr. (2002) The uch-l1 gene encodes two opposing enzymatic activities that affect α-synuclein degradation and parkinson's disease susceptibility. Cell 111, 209-218
67. 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
68. Chauhan, D., Tian, Z., Nicholson, B., Kumar, K. G., Zhou, B., Carrasco, R., McDermott, J. L., Leach, C. A., Fulcinniti, M., Kodrasov, M. P., Weinstock, J., Kingsbury, W. D., Hideshima, T., Shah, P. K., Minvielle, S., et al. (2012) A small molecule inhibitor of ubiquitin-specific protease-7 induces apoptosis in multiple myeloma cells and overcomes bortezomib resistance. Cancer Cell 22, 345-358
69. Weinstock, J., Wu, J., Cao, P., Kingsbury, W. D., McDermott, J. L., Kodrasov, M. P., McKelvey, D. M., Suresh Kumar, K. G., Goldenberg, S. J., Mattern, M. R., and Nicholson, B. (2012) Selective dual inhibitors of the cancer-related deubiquitylating proteases usp7 and usp47. ACS Med. Chem. Lett. 3, 789-792
70. Arnst, J. L., Davies, C. W., Raja, S. M., Das, C., and Natarajan, A. (2013) High-throughput compatible fluorescence resonance energy transfer-based assay to identify small molecule inhibitors of amsh deubiquitinase activity. Anal. Biochem. 440, 71-77
71. Finan, G. M., Okada, H., and Kim, T. W. (2011) Bace1 retrograde trafficking is uniquely regulated by the cytoplasmic domain of sortilin. J. Biol. Chem. 286, 12602-12616