UBA1: At the Crossroads of Ubiquitin Homeostasis and Neurodegeneration

Trends in Molecular Medicine

Volumn 21, Issue 10, 2015, Pages 622-632

  Groen, Ewout J N ^a   Gillingwater, Thomas H ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; E1 UBIQUITIN ACTIVATING ENZYME; UBIQUITIN; UBIQUITIN LIKE MODIFIER ACTIVATING ENZYME 1; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; UBE1 PROTEIN, HUMAN;

DEGENERATIVE DISEASE; HUNTINGTON CHOREA; NERVE DEGENERATION; NONHUMAN; PROTEIN HOMEOSTASIS; REGULATORY MECHANISM; REVIEW; SPINAL MUSCULAR ATROPHY; ANIMAL; HOMEOSTASIS; HUMAN; NEURODEGENERATIVE DISEASES; PHYSIOLOGY;

ANIMALS; HOMEOSTASIS; HUMANS; NEURODEGENERATIVE DISEASES; UBIQUITIN-ACTIVATING ENZYMES;

EID: 84942511422     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2015.08.003     Document Type: Review

References (82)

1. Bredesen D.E., et al. Cell death in the nervous system. Nature 2006, 443:796-802.
2. Schapira A.H., et al. Slowing of neurodegeneration in Parkinson's disease and Huntington's disease: future therapeutic perspectives. Lancet 2014, 384:545-555.
3. van den Berg L.H. Therapy of amyotrophic lateral sclerosis remains a challenge. Lancet Neurol. 2014, 13:1062-1063.
4. Mitsui J., Tsuji S. Genomic aspects of sporadic neurodegenerative diseases. Biochem. Biophys. Res. Commun. 2014, 452:221-225.
5. Rubinsztein D.C. The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 2006, 443:780-786.
6. Arrasate M., Finkbeiner S. Protein aggregates in Huntington's disease. Exp. Neurol. 2012, 238:1-11.
7. Blokhuis A.M., et al. Protein aggregation in amyotrophic lateral sclerosis. Acta Neuropathol. 2013, 125:777-794.
8. Ittner L.M., Gotz J. Amyloid-beta and tau - a toxic pas de deux in Alzheimer's disease. Nat. Rev. Neurosci. 2011, 12:65-72.
9. Lashuel H.A., et al. The many faces of alpha-synuclein: from structure and toxicity to therapeutic target. Nat. Rev. Neurosci. 2013, 14:38-48.
10. Ramser J., et al. Rare missense and synonymous variants in UBE1 are associated with X-linked infantile spinal muscular atrophy. Am. J. Hum. Genet. 2008, 82:188-193.
11. Wishart T.M., et al. Dysregulation of ubiquitin homeostasis and beta-catenin signaling promote spinal muscular atrophy. J. Clin. Invest. 2014, 124:1821-1834.
12. Komander D., Rape M. The ubiquitin code. Annu. Rev. Biochem. 2012, 81:203-229.
13. Schulman B.A., Harper J.W. Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways. Nat. Rev. Mol. Cell Biol. 2009, 10:319-331.
14. Shen H.M., Mizushima N. At the end of the autophagic road: an emerging understanding of lysosomal functions in autophagy. Trends Biochem. Sci. 2014, 39:61-71.
15. Nakatogawa H. Two ubiquitin-like conjugation systems that mediate membrane formation during autophagy. Essays Biochem. 2013, 55:39-50.
16. Leroy E., et al. The ubiquitin pathway in Parkinson's disease. Nature 1998, 395:451-452.
17. Ryan B.J., et al. Mitochondrial dysfunction and mitophagy in Parkinson's: from familial to sporadic disease. Trends Biochem. Sci. 2015, 40:200-210.
18. Deng H.X., et al. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature 2011, 477:211-215.
19. Fecto F., et al. SQSTM1 mutations in familial and sporadic amyotrophic lateral sclerosis. Arch. Neurol. 2011, 68:1440-1446.
20. Hara T., et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 2006, 441:885-889.
21. Komatsu M., et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 2006, 441:880-884.
22. Tashiro Y., et al. Motor neuron-specific disruption of proteasomes, but not autophagy, replicates amyotrophic lateral sclerosis. J. Biol. Chem. 2012, 287:42984-42994.
23. Ye Y., Rape M. Building ubiquitin chains: E2 enzymes at work. Nat. Rev. Mol. Cell Biol. 2009, 10:755-764.
24. Buckley D.L., Crews C.M. Small-molecule control of intracellular protein levels through modulation of the ubiquitin proteasome system. Angew. Chem. Int. Ed. Engl. 2014, 53:2312-2330.
25. Wade B.E., et al. Ubiquitin-activating enzyme activity contributes to differential accumulation of mutant huntingtin in brain and peripheral tissues. J. Neurosci. 2014, 34:8411-8422.
26. Kulkarni M., Smith H.E. E1 ubiquitin-activating enzyme UBA-1 plays multiple roles throughout C. elegans development. PLoS Genet. 2008, 4:e1000131.
27. McGrath J.P., et al. UBA 1: an essential yeast gene encoding ubiquitin-activating enzyme. EMBO J. 1991, 10:227-236.
28. Chiu Y.H., et al. E1-L2 activates both ubiquitin and FAT10. Mol. Cell 2007, 27:1014-1023.
29. Jin J., et al. Dual E1 activation systems for ubiquitin differentially regulate E2 enzyme charging. Nature 2007, 447:1135-1138.
30. Pelzer C., et al. UBE1L2, a novel E1 enzyme specific for ubiquitin. J. Biol. Chem. 2007, 282:23010-23014.
31. Leidecker O., et al. The ubiquitin E1 enzyme Ube1 mediates NEDD8 activation under diverse stress conditions. Cell Cycle 2012, 11:1142-1150.
32. Chang T.K., et al. Uba1 functions in Atg7- and Atg3-independent autophagy. Nat. Cell Biol. 2013, 15:1067-1078.
33. Lee P.C., et al. Altered social behavior and neuronal development in mice lacking the Uba6-Use1 ubiquitin transfer system. Mol. Cell 2013, 50:172-184.
34. Bialas J., et al. Conjugation of the ubiquitin activating enzyme UBE1 with the ubiquitin-like modifier FAT10 targets it for proteasomal degradation. PLoS ONE 2015, 10:e0120329.
35. Kitagaki J., et al. Nitric oxide prodrug JS-K inhibits ubiquitin E1 and kills tumor cells retaining wild-type p53. Oncogene 2009, 28:619-624.
36. Yang Y., et al. Inhibitors of ubiquitin-activating enzyme (E1), a new class of potential cancer therapeutics. Cancer Res. 2007, 67:9472-9481.
37. Joo H.Y., et al. Regulation of cell cycle progression and gene expression by H2A deubiquitination. Nature 2007, 449:1068-1072.
38. Ghaboosi N., Deshaies R.J. A conditional yeast E1 mutant blocks the ubiquitin-proteasome pathway and reveals a role for ubiquitin conjugates in targeting Rad23 to the proteasome. Mol. Biol. Cell 2007, 18:1953-1963.
39. Sugaya K., et al. Characterization of ubiquitin-activating enzyme Uba1 in the nucleus by its mammalian temperature-sensitive mutant. PLoS ONE 2014, 9:e96666.
40. Grenfell S.J., et al. Nuclear localization of the ubiquitin-activating enzyme, E1, is cell-cycle-dependent. Biochem. J. 1994, 300:701-708.
41. Cook J.C., Chock P.B. Phosphorylation of ubiquitin-activating enzyme in cultured cells. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:3454-3457.
42. Stephen A.G., et al. Identification of a region within the ubiquitin-activating enzyme required for nuclear targeting and phosphorylation. J. Biol. Chem. 1997, 272:10895-10903.
43. Nouspikel T., Hanawalt P.C. Impaired nucleotide excision repair upon macrophage differentiation is corrected by E1 ubiquitin-activating enzyme. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:16188-16193.
44. Moudry P., et al. Ubiquitin-activating enzyme UBA1 is required for cellular response to DNA damage. Cell Cycle 2012, 11:1573-1582.
45. Deglincerti A., et al. Coupled local translation and degradation regulate growth cone collapse. Nat. Commun. 2015, 6:6888.
46. Jiang X., et al. A role for the ubiquitin-proteasome system in activity-dependent presynaptic silencing. J. Neurosci. 2010, 30:1798-1809.
47. Rinetti G.V., Schweizer F.E. Ubiquitination acutely regulates presynaptic neurotransmitter release in mammalian neurons. J. Neurosci. 2010, 30:3157-3166.
48. Watts R.J., et al. Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron 2003, 38:871-885.
49. s) gene. Mol. Cell. Proteomics 2007, 6:1318-1330.
50. s). Genome Biol. 2008, 9:R101.
51. Lee T.V., et al. The E1 ubiquitin-activating enzyme Uba1 in Drosophila controls apoptosis autonomously and tissue growth non-autonomously. Development 2008, 135:43-52.
52. Pfleger C.M., et al. Mutation of the gene encoding the ubiquitin activating enzyme ubal causes tissue overgrowth in Drosophila. Fly (Austin) 2007, 1:95-105.
53. Liu H.Y., Pfleger C.M. Mutation in E1, the ubiquitin activating enzyme, reduces Drosophila lifespan and results in motor impairment. PLoS ONE 2013, 8:e32835.
54. Dlamini N., et al. Clinical and neuropathological features of X-linked spinal muscular atrophy (SMAX2) associated with a novel mutation in the UBA1 gene. Neuromuscul. Disord. 2013, 23:391-398.
55. Jedrzejowska M., et al. X-linked spinal muscular atrophy (SMAX2) caused by de novo c.1731C>T substitution in the UBA1 gene. Neuromuscul. Disord. 2015, 25:661-666.
56. Hamilton G., Gillingwater T.H. Spinal muscular atrophy: going beyond the motor neuron. Trends Mol. Med. 2013, 19:40-50.
57. Hunter G., et al. SMN-dependent intrinsic defects in Schwann cells in mouse models of spinal muscular atrophy. Hum. Mol. Genet. 2014, 23:2235-2250.
58. Aghamaleky Sarvestany A., et al. Label-free quantitative proteomic profiling identifies disruption of ubiquitin homeostasis as a key driver of Schwann cell defects in spinal muscular atrophy. J. Proteome Res. 2014, 13:4546-4557.
59. Nollen E.A., et al. Genome-wide RNA interference screen identifies previously undescribed regulators of polyglutamine aggregation. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:6403-6408.
60. Blard O., et al. Cytoskeleton proteins are modulators of mutant tau-induced neurodegeneration in Drosophila. Hum. Mol. Genet. 2007, 16:555-566.
61. Wang T., et al. Interaction of amyotrophic lateral sclerosis/frontotemporal lobar degeneration-associated fused-in-sarcoma with proteins involved in metabolic and protein degradation pathways. Neurobiol. Aging 2015, 36:527-535.
62. Chou A.P., et al. Ziram causes dopaminergic cell damage by inhibiting E1 ligase of the proteasome. J. Biol. Chem. 2008, 283:34696-34703.
63. Viquez O.M., et al. Electrophilic adduction of ubiquitin activating enzyme E1 by N,N-diethyldithiocarbamate inhibits ubiquitin activation and is accompanied by striatal injury in the rat. Chem. Res. Toxicol. 2012, 25:2310-2321.
64. Martin C.A., et al. Synergistic effects on dopamine cell death in a Drosophila model of chronic toxin exposure. Neurotoxicology 2014, 44:344-351.
65. Lopez Salon M., et al. Defective ubiquitination of cerebral proteins in Alzheimer's disease. J. Neurosci. Res. 2000, 62:302-310.
66. Sleigh J.N., et al. The contribution of mouse models to understanding the pathogenesis of spinal muscular atrophy. Dis. Model. Mech. 2011, 4:457-467.
67. McNaught K.S., et al. Aggresome-related biogenesis of Lewy bodies. Eur. J. Neurosci. 2002, 16:2136-2148.
68. Tydlacka S., et al. Differential activities of the ubiquitin-proteasome system in neurons versus glia may account for the preferential accumulation of misfolded proteins in neurons. J. Neurosci. 2008, 28:13285-13295.
69. Popovic D., et al. Ubiquitination in disease pathogenesis and treatment. Nat. Med. 2014, 20:1242-1253.
70. Dimopoulos M.A., et al. Current treatment landscape for relapsed and/or refractory multiple myeloma. Nat. Rev. Clin. Oncol. 2015, 12:42-54.
71. da Silva S.R., et al. Exploring a new frontier in cancer treatment: targeting the ubiquitin and ubiquitin-like activating enzymes. J. Med. Chem. 2013, 56:2165-2177.
72. Bedford L., et al. Ubiquitin-like protein conjugation and the ubiquitin-proteasome system as drug targets. Nat. Rev. Drug Discov. 2011, 10:29-46.
73. Yang X., et al. Absolute quantification of E1, ubiquitin-like proteins and Nedd8-MLN4924 adduct by mass spectrometry. Cell. Biochem. Biophys. 2013, 67:139-147.
74. Clague M.J., et al. The demographics of the ubiquitin system. Trends Cell Biol. 2015, 25:417-426.
75. Powis R.A., et al. Increased levels of UCHL1 are a compensatory response to disrupted ubiquitin homeostasis in spinal muscular atrophy and do not represent a viable therapeutic target. Neuropathol. Appl. Neurobiol. 2014, 40:873-887.
76. Yasvoina M.V., et al. eGFP expression under UCHL1 promoter genetically labels corticospinal motor neurons and a subpopulation of degeneration-resistant spinal motor neurons in an ALS mouse model. J. Neurosci. 2013, 33:7890-7904.
77. Salvat C., et al. Molecular characterization of the thermosensitive E1 ubiquitin-activating enzyme cell mutant A31N-ts20. Requirements upon different levels of E1 for the ubiquitination/degradation of the various protein substrates in vivo. Eur. J. Biochem. 2000, 267:3712-3722.
78. Lee I., Schindelin H. Structural insights into E1-catalyzed ubiquitin activation and transfer to conjugating enzymes. Cell 2008, 134:268-278.
79. Szczepanowski R.H., et al. Crystal structure of a fragment of mouse ubiquitin-activating enzyme. J. Biol. Chem. 2005, 280:22006-22011.
80. Haas A.L., et al. Ubiquitin-activating enzyme. Mechanism and role in protein-ubiquitin conjugation. J. Biol. Chem. 1982, 257:2543-2548.
81. Ambrozkiewicz M.C., Kawabe H. HECT-type E3 ubiquitin ligases in nerve cell development and synapse physiology. FEBS Lett. 2015, 589:1635-1643.
82. Ciechanover A. Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat. Rev. Mol. Cell Biol. 2005, 6:79-87.