Proteasome Inhibition Arrests Neurite Outgrowth and Causes "Dying-Back" Degeneration in Primary Culture

Journal of Neuroscience Research

Volumn 74, Issue 6, 2003, Pages 906-916

  Laser, Heike ^a   Mack, Till G A ^a,b   Wagner, Diana ^a   Coleman, Michael P ^a,c  

^a UNIVERSITY OF COLOGNE   (Germany)

^b KeyNeurotek Pharmaceuticals AG   (Germany)

^c BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

Axon; Lactacystin; Retrograde degeneration; Ubiquitin proteasome pathway

Indexed keywords

LACTACYSTIN; NERVE GROWTH FACTOR; PROTEASOME; PROTEINASE INHIBITOR; UBIQUITIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL STRAIN; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DEGENERATIVE DISEASE; DENDRITE; EMBRYO; MOUSE; NERVE CELL CULTURE; NERVE CELL DEGENERATION; NERVE CELL DIFFERENTIATION; NERVE FIBER; NERVE FIBER DEGENERATION; NERVE FIBER GROWTH; NEURITE; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; SYMPATHETIC NERVE;

ACETYLCYSTEINE; ANIMALS; CELL DIVISION; CELL SURVIVAL; CELLS, CULTURED; CYSTEINE ENDOPEPTIDASES; GROWTH INHIBITORS; MICE; MICE, INBRED C57BL; MULTIENZYME COMPLEXES; NERVE DEGENERATION; NEURAL INHIBITION; NEURITES; PC12 CELLS; PROTEASOME ENDOPEPTIDASE COMPLEX; RATS;

EID: 0344118165     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.10806     Document Type: Article

References (42)

1. Adams J. 2002. Proteasome inhibition: a novel approach to cancer therapy. Trends Mol Med 8(Suppl):49-54.
2. Bence NF, Sampat RM, Kopito RR. 2001. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292:1552-1555.
3. Campbell DS, Holt CE. 2001. Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32:1013-1026.
4. Coleman MP, Perry VH. 2002. Axon pathology in neurological disease: a neglected therapeutic target. Trends Neurosci 25:532-537.
5. Conforti L, Tarlton A, Mack TG, Mi W, Buckmaster EA, Wagner D, Perry VH, Coleman MP. 2000. A Ufd2/D4Cole1e chimeric protein and over-expression of Rbp7 in the slow Wallerian degeneration (WldS) mouse. Proc Nad Acad Sci USA 97:11377-11382.
6. DiAntonio A, Haghighi AP, Portman SL, Lee JD, Amaranto AM, Goodman CS. 2001. Ubiquitination-dependent mechanisms regulate synaptic growth and function. Nature 412:449-452.
7. Dickson DW, Wertkin A, Mattiace LA, Fier E, Kress Y, Davies P, Yen SH. 1990. Ubiquitin immunoelectron microscopy of dystrophic neurites in cerebellar senile plaques of Alzheimer's disease. Acta Neuropathol 79:486-493.
8. DiFiglia M, Sapp E, Chase KO, Davies SW, Bates GP, Vonsattel JP, Aronin N. 1997. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277:1990-1993.
9. Fenteany G, Standaert RF, Reichard GA, Corey EJ, Schreiber SL. 1994. A beta-lactone related to lactacystin induces neurite outgrowth in a neuroblastoma cell line and inhibits cell cycle progression in an osteosarcoma cell line. Proc Natl Acad Sci USA 91:3358-3362.
10. Fergusson J, Landon M, Lowe J, Ward L, van Leeuwen FW, Mayer RJ. 2000. Neurofibrillary tangles in progressive supranuclear palsy brains exhibit immunoreactivity to frameshift mutant ubiquitin-B protein. Neurosci Lett 279:69-72.
11. Ferri A, Sanes JR, Coleman MP, Cunningham JM, Kato AC. 2003. Inhibiting axon degeneration and synapse loss attenuates apoptosis and disease progression in a mouse model of motoneuron disease. Curr Biol 13:669-673.
12. Gai WP, Blessing WW, Blumbergs PC. 1995. Ubiquitin-positive degenerating neurites in the brainstem in Parkinson's disease. Brain 118:1447-1459.
13. Greene LA, Tischler AS. 1976. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci USA 73:2424-2428.
14. Ivins KJ, Bui ET, Cotman CW. 1998. Beta-amyloid induces local neurite degeneration in cultured hippocampal neurons: evidence for neuritic apoptosis. Neurobiol Dis 5:365-378.
15. Kisselev AF, Goldberg AL. 2001. Proteasome inhibitors: from research tools to drug candidates. Chem Biol 8:739-758.
16. Lam YA, Pickart CM, Alban A, Landon M, Jamieson C, Ramage R, Mayer RJ, Layfield R. 2000. Inhibition of the ubiquitin-proteasome system in Alzheimer's disease. Proc Natl Acad Sci USA 97:9902-9906.
17. Leroy E, Boyer R, Auburger G, Leube B, Ulm G, Mezey E, Harta G, Brownstein MJ, Jonnalagada S, Chernova T, Dehejia A, Lavedan C, Gasser T, Steinbach PJ, Wilkinson KD, Polymeropoulos MH. 1998. The ubiquitin pathway in Parkinson's disease. Nature 395:451-452.
18. Levi-Montalcini R, Meyer H, Hamburger V. 1954. In vitro experiments on the effects of mouse sarcomas 180 and 37 on the spinal and sympathetic ganglia of the chick embryo. Cancer Res 14:49-57.
19. Li H, Li SH, Yu ZX, Shelbourne P, Li XJ. 2001. Huntingtin aggregate-associated axonal degeneration is an early pathological event in Huntington's disease mice. J Neurosci 21:8473-8481.
20. Lunn ER, Perry VH, Brown MC, Rosen H, Gordon S. 1989. Absence of Wallerian degeneration does not hinder regeneration in peripheral nerve. Eur J Neurosci 1:27-33.
21. Mack TG, Reiner M, Beirowski B, Mi W, Emanuelli M, Wagner D, Thomson D, Gillingwater T, Court F, Conforti L, Fernando FS, Tarlton A, Andressen C, Addicks K, Magni G, Ribchester RR, Perry VH, Coleman MP. 2001. Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nat Neurosci 12:1199-1206.
22. Martin-Aparicio E, Yamamoto A, Hernandez F, Hen R, Avila J, Lucas JJ. 2001. Proteasomal-dependent aggregate reversal and absence of cell death in a conditional mouse model of Huntington's disease. J Neurosci 21:8772-8781.
23. Miura H, Oda K, Endo C, Yamazaki K, Shibasaki H, Kikuchi T. 1993. Progressive degeneration of motor nerve terminals in GAD mutant mouse with hereditary sensory axonopathy. Neuropathol Appl Neurobiol 19:41-51.
24. Obin M, Mesco E, Gong X, Haas AL, Joseph J, Taylor A. 1999. Neurite outgrowth in PC12 cells. Distinguishing the roles of ubiquitylation and ubiquitin-dependent proteolysis. J Biol Chem 274:11789-11795.
25. Oda K, Yamazaki K, Miura H, Shibasaki H, Kikuchi T. 1992. Dying back type axonal degeneration of sensory nerve terminals in muscle spindles of the gracile axonal dystrophy (GAD) mutant mouse. Neuropathol Appl Neurobiol 18:265-281.
26. Ohtani-Kaneko R, Takada K, Ligo M, Hara M, Yokosawa H, Kawashima S, Ohkawa K, Hirata K. 1998. Proteasome inhibitors which induce neurite outgrowth from PC12 cells cause different subcellular accumulations of multi-ubiquitin chains. Neurochem Res 23:1435-1443.
27. Omura S, Fujimoto T, Otoguro K, Matsuzaki K, Moriguchi R, Tanaka H, Sasaki Y. 1991. Lactacystin, a novel microbial metabolite, induces neuritogenesis of neuroblastoma cells. J Antibiot (Tokyo) 44:113-116.
28. Osaka H, Wang YL, Takada K, Takizawa S, Setsuie R, Li H, Sato Y, Nishikawa K, Sun YJ, Sakurai M, Harada T, Hara Y, Kimura I, Chiba S, Namikawa K, Kiyama H, Noda M, Aoki S, Wada K. 2003. Ubiquitin carboxy-terminal hydrolase L1 binds to and stabilizes monoubiquitin in neurons. Hum Mol Genet 12:1945-1958.
29. Osaka H, Wang YL, Takizawa S, Aoki S, Sakurai M, Li H, Hara Y, Takada K, Noda M, Wada K. 2001. Ubiquitin C-terminal hydrolase as a regulator of ubiquitin level. Soc Neurosci Program 195.16.
30. Phillips JB, Williams AJ, Adams J, Elliott PJ, Tortella FC. 2000. Proteasome inhibitor PS519 reduces infarction and attenuates leukocyte infiltration in a rat model of focal cerebral ischemia. Stroke 31:1686-1693.
31. Plum LA, Parada LF, Tsoulfas P, Clagett-Dame M. 2001. Retinoic acid combined with neurotrophin-3 enhances the survival and neurite out-growth of embryonic sympathetic neurons. Exp Biol Med (Maywood) 226:766-775.
32. Sadoul R, Fernandez PA, Quiquerez AL, Martinou I, Maki M, Schroter M, Becherer JD, Irmler M, Tschopp J, Martinou JC. 1996. Involvement of the proteasome in the programmed cell death of NGF-deprived sympathetic neurons. EMBO J 15:3845-3852.
33. Saigoh K, Wang YL, Suh JG, Yamanishi T, Sakai Y, Kiyosawa H, Harada T, Ichihara N, Wakana S, Kikuchi T, Wada K. 1999. Intragenic deletion in the gene encoding ubiquitin carboxy-terminal hydrolase in gad mice. Nat Genet 23:47-51.
34. Samsam M, Mi W, Wessig C, Zielasek J, Toyka KV, Coleman MP, Martini R. 2003. The WldS mutation delays robust loss of motor and sensory axons in a generic model for myelin-related axonopathy. J Neurosci 23:2833-2839.
35. Satoh J, Kuroda Y. 2001. A polymorphic variation of serine to tyrosine at codon 18 in the ubiquitin C-terminal hydrolase-L1 gene is associated with a reduced risk of sporadic Parkinson's disease in a Japanese population. J Neurol Sci 189:113-117.
36. Shimura H, Schlossmacher MG, Hattori N, Frosch MP, Trockenbacher A, Schneider R, Mizuno Y, Kosik KS, Selkoe DJ. 2001. Ubiquitination of a new form of alpha-synuclein by parkin from human brain: implications for Parkinson's disease. Science 293:263-269.
37. Sidell N, Altman A, Haussler MR, Seeger RC. 1983. Effects of retinoic acid (RA) on the growth and phenotypic expression of several human neuroblastoma cell lines. Exp Cell Res 148:21-30.
38. Sievers C, Platt N, Perry VH, Coleman MP, Conforti L. 2003. Neurites undergoing Wallerian degeneration show an apoptotic-like process with Annexin V positive staining and loss of mitochondrial membrane potential. Neurosci Res 46:161-169.
39. van Leeuwen FW, de Kleijn DP, van den Hurk HH, Neubauer A, Sonnemans MA, Sluijs JA, Koycu S, Ramdjielal RDJ, Salehi A, Martens GJM, Grosveld FG, Peter J, Burbach H, Hol EM. 1998. Frameshift mutants of beta amyloid precursor protein and ubiquitin-B in Alzheimer's and Down patients. Science 279:242-247.
40. Wang MS, Davis AA, Culver DG, Glass JD. 2002. WldS mice are resistant to paclitaxel (taxol) neuropathy. Ann Neurol 52:442-447.
41. Yamazaki K, Wakasugi N, Tomita T, Kikuchi T, Mukoyama M, Ando K. 1988. Gracile axonal dystrophy (GAD), a new neurological mutant in the mouse. Proc Soc Exp Biol Med 187:209-215.
42. Zhai Q, Wang J, Kim A, Liu Q, Watts R, Hoopfer E, Mitchison T, Luo L, He Z. 2003. Involvement of the ubiquitin-proteasome system in the early stages of Wallerian degeneration. Neuron 39:217-225.