Ubiquitin carboxyl-terminal hydrolase L1 is required for maintaining the structure and function of the neuromuscular junction

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 4, 2010, Pages 1636-1641

  Chen, Fujun ^a   Sugiura, Yoshie ^a   Myers, Kalisa Galina ^a   Liu, Yun ^a   Lin, Weichun ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Electrophysiology; Knockout mice; Neurodegeneration; Synaptic transmission

Indexed keywords

UBIQUITIN THIOLESTERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ANALYSIS; KNOCKOUT MOUSE; MOUSE; MUSCLE DENERVATION; NERVE DEGENERATION; NERVE STIMULATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ANIMALS; DISEASE PROGRESSION; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; MUTATION; NEUROMUSCULAR JUNCTION; PARALYSIS; SYNAPTIC TRANSMISSION; UBIQUITIN THIOLESTERASE;

MAMMALIA; MUS;

EID: 76549084350     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0911516107     Document Type: Article

References (52)

1. Doran JF, Jackson P, Kynoch PA, Thompson RJ (1983) Isolation of PGP 9.5, a new human neurone-specific protein detected by high-resolution two-dimensional electrophoresis. J Neurochem 40:1542-1547.
2. Wilkinson KD, et al. (1989) The neuron-specific protein PGP 9.5 is a ubiquitin carboxylterminal hydrolase. Science 246:670-673.
3. Ventii KH, Wilkinson KD (2008) Protein partners of deubiquitinating enzymes. Biochem J 414:161-175.
4. Liu Y, Fallon L, Lashuel HA, Liu Z, Lansbury PT Jr (2002) The UCH-L1 gene encodes two opposing enzymatic activities that affect alpha-synuclein degradation and Parkinson's disease susceptibility. Cell 111:209-218.
5. Osaka H, et al. (2003) Ubiquitin carboxy-terminal hydrolase L1 binds to and stabilizes monoubiquitin in neuron. Hum Mol Genet 12:1945-1958.
6. Setsuie R, Wada K (2007) The functions of UCH-L1 and its relation to neurodegenerative diseases. Neurochem Int 51:105-111.
7. Mukoyama M, Yamazaki K, Kikuchi T, Tomita T (1989) Neuropathology of gracile axonal dystrophy (GAD) mouse. An animal model of central distal axonopathy in primary sensory neurons. Acta Neuropathol 79:294-299.
8. Yamazaki K, et al. (1988) Gracile axonal dystrophy (GAD), a new neurological mutant in the mouse. Proc Soc Exp Biol Med 187:209-215.
9. Saigoh K, et al. (1999) Intragenic deletion in the gene encoding ubiquitin carboxyterminal hydrolase in gad mice. Nat Genet 23:47-51.
10. Lowe J, McDermott H, Landon M, Mayer RJ, Wilkinson KD (1990) Ubiquitin carboxylterminal hydrolase (PGP 9.5) is selectively present in ubiquitinated inclusion bodies characteristic of human neurodegenerative diseases. J Pathol 161:153-160.
11. Castegna A, et al. (2002) Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part I: Creatine kinase BB, glutamine synthase, and ubiquitin carboxy-terminal hydrolase L-1. Free Radic Biol Med 33:562-571.
12. Choi J, et al. (2004) Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson's and Alzheimer's diseases. J Biol Chem 279:13256-13264.
13. Ann ES, Mizoguchi A, Okajima S, Ide C (1994) Motor axon terminal regeneration as studied by protein gene product 9.5 immunohistochemistry in the rat. Arch Histol Cytol 57:317-330.
14. Hirata K, Zhou C, Nakamura K, KawabuchiM (1997) Postnatal development of Schwann cells at neuromuscular junctions, with special reference to synapse elimination. J Neurocytol 26:799-809.
15. Lin WM, Hsieh ST, Huang IT, Griffin JW, Chen WP (1997) Ultrastructural localization and regulation of protein gene product 9.5. Neuroreport 8:2999-3004.
16. Miura H, et al. (1993) Progressive degeneration of motor nerve terminals in GAD mutant mouse with hereditary sensory axonopathy. Neuropathol Appl Neurobiol 19: 41-51.
17. Mi W, et al. (2005) The slow Wallerian degeneration gene, WldS, inhibits axonal spheroid pathology in gracile axonal dystrophy mice. Brain 128:405-416.
18. Sakurai M, et al. (2008) Reduction in memory in passive avoidance learning, exploratory behaviour and synaptic plasticity in mice with a spontaneous deletion in the ubiquitin C-terminal hydrolase L1 gene. Eur J Neurosci 27:691-701.
19. Walters BJ, et al. (2008) Differential effects of Usp14 and Uch-L1 on the ubiquitin proteasome system and synaptic activity. Mol Cell Neurosci 39:539-548.
20. McArdle JJ, Sansone FM (1977) Re-innervation of fast and slow twitch muscle following nerve crush at birth. J Physiol 271:567-586.
21. Harris JB, Ribchester RR (1979) The relationship between end-plate size and transmitter release in normal and dystrophic muscles of the mouse. J Physiol 296: 245-265.
22. Balice-Gordon RJ, Thompson WJ (1988) The organization and development of compartmentalized innervation in rat extensor digitorum longus muscle. J Physiol 398:211-231.
23. Stålberg E, Trontelj JV (1997) The study of normal and abnormal neuromuscular transmission with single fibre electromyography. J Neurosci Methods 74:145-154.
24. Hennig R, Lømo T (1985) Firing patterns of motor units in normal rats. Nature 314: 164-166.
25. McArdle JJ, et al. (1981) Advantages of the triangularis sterni muscle of the mouse for investigations of synaptic phenomena. J Neurosci Methods 4:109-115.
26. Hall ZW, Sanes JR (1993) Synaptic structure and development: The neuromuscular junction. Cell 72 (Suppl):99-121.
27. Slater CR (2003) Structural determinants of the reliability of synaptic transmission at the vertebrate neuromuscular junction. J Neurocytol 32:505-522.
28. Dobrunz LE, Huang EP, Stevens CF (1997) Very short-term plasticity in hippocampal synapses. Proc Natl Acad Sci USA 94:14843-14847.
29. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405.
30. Katz B, Miledi R (1968) The role of calcium in neuromuscular facilitation. J Physiol 195: 481-492.
31. Rozov A, Burnashev N, Sakmann B, Neher E (2001) Transmitter release modulation by intracellular Ca2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics. J Physiol 531:807-826.
32. Elmqvist D, Quastel DM (1965) A quantitative study of end-plate potentials in isolated human muscle. J Physiol 178:505-529.
33. Betz WJ (1970) Depression of transmitter release at the neuromuscular junction of the frog. J Physiol 206:629-644.
34. Hegde AN, et al. (1997) Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia. Cell 89:115-126.
35. Chain DG, et al. (1999) Mechanisms for generating the autonomous cAMP-dependent protein kinase required for long-term facilitation in Aplysia. Neuron 22:147-156.
36. Fioravante D, Liu RY, Byrne JH (2008) The ubiquitin-proteasome system is necessary for long-term synaptic depression in Aplysia. J Neurosci 28:10245-10256.
37. Gong B, et al. (2006) Ubiquitin hydrolase Uch-L1 rescues beta-amyloid-induced decreases in synaptic function and contextual memory. Cell 126:775-788.
38. Heuser JE, Reese TS (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 57:315-344.
39. Koenig JH, Ikeda K (1989) Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J Neurosci 9:3844-3860.
40. Ferguson SM, et al. (2007) A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 316:570-574.
41. Hayashi M, et al. (2008) Cell- and stimulus-dependent heterogeneity of synaptic vesicle endocytic recycling mechanisms revealed by studies of dynamin 1-null neurons. Proc Natl Acad Sci USA 105:2175-2180.
42. Xu YF, Autio D, Rheuben MB, Atchison WD (2002) Impairment of synaptic vesicle exocytosis and recycling during neuromuscular weakness produced in mice by 2,4-dithiobiuret. J Neurophysiol 88:3243-3258.
43. Delgado R, Maureira C, Oliva C, Kidokoro Y, Labarca P (2000) Size of vesicle pools, rates of mobilization, and recycling at neuromuscular synapses of a Drosophila mutant, shibire. Neuron 28:941-953.
44. Cartier AE, et al. (2009) Regulation of synaptic structure by ubiquitin C-terminal hydrolase L1. J Neurosci 29:7857-7868.
45. Mukhopadhyay D, Riezman H (2007) Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315:201-205.
46. Liley AW (1956) An investigation of spontaneous activity at the neuromuscular junction of the rat. J Physiol 132:650-666.
47. McLachlan EM, Martin AR (1981) Non-linear summation of end-plate potentials in the frog and mouse. J Physiol 311:307-324.
48. Boyd IA, Martin AR (1956) The end-plate potential in mammalian muscle. J Physiol 132:74-91.
49. Pang ZP, et al. (2006) Synaptotagmin-2 is essential for survival and contributes to Ca2+ triggering of neurotransmitter release in central and neuromuscular synapses. J Neurosci 26:13493-13504.
50. Liu Y, et al. (2008) Essential roles of the acetylcholine receptor gamma-subunit in neuromuscular synaptic patterning. Development 135:1957-1967.
51. Kelly AM, Zacks SI (1969) The fine structure of motor endplate morphogenesis. J Cell Biol 42:154-169.
52. Reinecke M, Walther C (1981) Ultrastructural changes with high activity and subsequent recovery at locust motor nerve terminals. A stereological analysis. Neuroscience 6: 489-503.