Roles of the ubiquitin proteasome system in the effects of drugs of abuse

Frontiers in Molecular Neuroscience

Volumn 7, Issue JAN, 2015, Pages

  Massaly, Nicolas ^a,b,c   Francès, Bernard ^a,c   Moulédous, Lionel ^b,c  

^a CNRS   (France)

^b INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^c UNIVERSITÉ PAUL SABATIER   (France)

Author keywords

Addiction; Drug abuse; Nicotine; Opioid; Plasticity; Proteasome; Stimulants; Ubiquitin

Indexed keywords

ALCOHOL; COCAINE; ENKEPHALIN [2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; ENKEPHALIN [2 DEXTRO ALANINE 5 DEXTRO LEUCINE]; METHAMPHETAMINE; MORPHINE; NICOTINE; PROTEASOME; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; DRUG ABUSE; DRUG DEPENDENCE; HUMAN; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MEMORY; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN EXPRESSION; UBIQUITINATION;

EID: 84920601374     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2014.00099     Document Type: Article

References (72)

1. Alberini, C. M., and Ledoux, J. E. (2013). Memory reconsolidation. Curr. Biol. 23, R746-R750. doi: 10.1016/j.cub.2013.06.046
2. Alexander-Kaufman, K., James, G., Sheedy, D., Harper, C., and Matsumoto, I. (2006). Differential protein expression in the prefrontal white matter of human alcoholics: a proteomics study. Mol. Psychiatry 11, 56-65. doi: 10.1038/sj.mp.4001741
3. Artinian, J., McGauran, A. M., De Jaeger, X., Mouledous, L., Frances, B., and Roullet, P. (2008). Protein degradation, as with protein synthesis, is required during not only long-term spatial memory consolidation but also reconsolidation. Eur. J. Neurosci. 27, 3009-3019. doi: 10.1111/j.1460-9568.2008.06262.x
4. Bailey, C. P., and Connor, M. (2005). Opioids: cellular mechanisms of tolerance and physical dependence. Curr. Opin. Pharmacol. 5, 60-68. doi: 10.1016/j.coph.2004.08.012
5. Bindukumar, B., Mahajan, S. D., Reynolds, J. L., Hu, Z., Sykes, D. E., Aalinkeel, R., et al. (2008). Genomic and proteomic analysis of the effects of cannabinoids on normal human astrocytes. Brain Res. 1191, 1-11. doi: 10.1016/j.brainres.2007.10.062
6. Bingol, B., and Sheng, M. (2011). Deconstruction for reconstruction: the role of proteolysis in neural plasticity and disease. Neuron 69, 22-32. doi: 10.1016/j.neuron.2010.11.006
7. Bu, Q., Yang, Y., Yan, G., Hu, Z., Hu, C., Duan, J., et al. (2012). Proteomic analysis of the nucleus accumbens in rhesus monkeys of morphine dependence and withdrawal intervention. J. Proteomics 75, 1330-1342. doi: 10.1016/j.jprot.2011.11.008
8. Carle, T. L., Ohnishi, Y. N., Ohnishi, Y. H., Alibhai, I. N., Wilkinson, M. B., Kumar, A., et al. (2007). Proteasome-dependent and -independent mechanisms for FosB destabilization: identification of FosB degron domains and implications for DeltaFosB stability. Eur. J. Neurosci. 25, 3009-3019. doi: 10.1111/j.1460-9568.2007.05575.x
9. Chaturvedi, K., Bandari, P., Chinen, N., and Howells, R. D. (2001). Proteasome involvement in agonist-induced down-regulation ofmu and delta opioid receptors. J. Biol. Chem. 276, 12345-12355. doi: 10.1074/jbc.M008054200
10. Christianson, J. C., and Ye, Y. (2014). Cleaning up in the endoplasmic reticulum: ubiquitin in charge. Nat. Struct. Mol. Biol. 21, 325-335. doi: 10.1038/nsmb.2793
11. Christie, M. J. (2008). Cellular neuroadaptations to chronic opioids: tolerance, withdrawal and addiction. Br. J. Pharmacol. 154, 384-396. doi: 10.1038/bjp.2008.100
12. Ciechanover, A. (2005). Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat. Rev. Mol. Cell Biol. 6, 79-87. doi: 10.1038/nrm1552
13. Citri, A., Soler-Llavina, G., Bhattacharyya, S., and Malenka, R. C. (2009). N-methyl-D-aspartate receptor- and metabotropic glutamate receptor-dependent long-term depression are differentially regulated by the ubiquitin-proteasome system. Eur. J. Neurosci. 30, 1443-1450. doi: 10.1111/j.1460-9568.2009.06950.x
14. Colledge, M., Snyder, E. M., Crozier, R. A., Soderling, J. A., Jin, Y., Langeberg, L. K., et al. (2003). Ubiquitination regulates PSD-95 degradation and AMPA receptor surface expression. Neuron 40, 595-607. doi: 10.1016/S0896-6273(03)00687-1
15. Dietrich, J. B., Mangeol, A., Revel, M. O., Burgun, C., Aunis, D., and Zwiller, J. (2005). Acute or repeated cocaine administration generates reactive oxygen species and induces antioxidant enzyme activity in dopaminergic rat brain structures. Neuropharmacology 48, 965-974. doi: 10.1016/j.neuropharm.2005.01.018
16. Dong, C., Upadhya, S. C., Ding, L., Smith, T. K., and Hegde, A. N. (2008). Proteasome inhibition enhances the induction and impairs the maintenance of late-phase long-term potentiation. Learn. Mem. 15, 335-347. doi: 10.1101/lm.984508
17. Ehlers, M. D. (2003). Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat. Neurosci. 6, 231-242. doi: 10.1038/nn1013
18. Faure, J. J., Hattingh, S. M., Stein, D. J., and Daniels, W. M. (2009). Proteomic analysis reveals differentially expressed proteins in the rat frontal cortex after methamphetamine treatment. Metab. Brain Dis. 24, 685-700. doi: 10.1007/s11011-009-9167-0
19. Fonseca, R., Vabulas, R. M., Hartl, F. U., Bonhoeffer, T., and Nagerl, U. V. (2006). A balance of protein synthesis and proteasome-dependent degradation determines the maintenance of LTP. Neuron 52, 239-245. doi: 10.1016/j.neuron.2006.08.015
20. Govind, A. P., Walsh, H., and Green, W. N. (2012). Nicotine-induced upregulation of native neuronal nicotinic receptors is caused by multiple mechanisms. J. Neurosci. 32, 2227-2238. doi: 10.1523/JNEUROSCI.5438-11.2012
21. Guan, X., and Guan, Y. (2013). Proteomic profile of differentially expressed proteins in the medial prefrontal cortex after repeated cocaine exposure. Neuroscience 236, 262-270. doi: 10.1016/j.neuroscience.2013.01.039
22. Gutala, R., Wang, J., Kadapakkam, S., Hwang, Y., Ticku, M., and Li, M. D. (2004). Microarray analysis of ethanol-treated cortical neurons reveals disruption of genes related to the ubiquitin-proteasome pathway and protein synthesis. Alcohol Clin. Exp. Res. 28, 1779-1788. doi: 10.1097/01.ALC.0000148117.17707.B4
23. Hegde, A. N., Goldberg, A. L., and Schwartz, J. H. (1993). Regulatory subunits of cAMP-dependent protein kinases are degraded after conjugation to ubiqui-tin: a molecular mechanism underlying long-term synaptic plasticity. Proc. Natl. Acad. Sci. U.S.A. 90, 7436-7440. doi: 10.1073/pnas.90.16.7436
24. Hegde, A. N. (2010). The ubiquitin-proteasome pathway and synaptic plasticity. Learn. Mem. 17, 314-327. doi: 10.1101/lm.1504010
25. Henley, B. M., Williams, B. A., Srinivasan, R., Cohen, B. N., Xiao, C., Mackey, E. D., et al. (2013). Transcriptional regulation by nicotine in dopaminergic neurons. Biochem. Pharmacol. 86, 1074-1083. doi: 10.1016/j.bcp.2013.07.031
26. Hislop, J. N., Henry, A. G., and Von Zastrow, M. (2011). Ubiquitination in the first cytoplasmic loop of mu-opioid receptors reveals a hierarchical mechanism of lysosomal down-regulation. J. Biol. Chem. 286, 40193-40204. doi: 10.1074/jbc.M111.288555
27. Hyman, S. E., Malenka, R. C., and Nestler, E. J. (2006). Neural mechanisms of addiction: the role ofreward-related learningand memory. Annu. Rev. Neurosci. 29, 565-598. doi: 10.1146/annurev.neuro.29.051605.113009
28. Iwazaki, T., McGregor, I. S., and Matsumoto, I. (2006). Protein expression profile in the striatum of acute methamphetamine-treated rats. Brain Res. 1097, 19-25. doi: 10.1016/j.brainres.2006.04.052
29. Jarome, T. J., and Helmstetter, F. J. (2014). Protein degradation and protein synthesis in long-term memory formation. Front. Mol. Neurosci. 7:61. doi: 10.3389/fnmol.2014.00061
30. Jarome, T. J., Werner, C. T., Kwapis, J. L., and Helmstetter, F. J. (2011). Activity dependent protein degradation is critical for the formation and stability of fear memory in the amygdala. PLoS ONE 6:e24349. doi: 10.1371/journal.pone.0024349
31. Jordan, J. D., He, J. C., Eungdamrong, N. J., Gomes, I., Ali, W., Nguyen, T., et al. (2005). Cannabinoid receptor-induced neurite outgrowth is mediated by Rap1 activation through G(alpha)o/i-triggered proteasomal degradation of Rap1GAPII. J. Biol. Chem. 280, 11413-11421. doi: 10.1074/jbc.M4115 21200
32. Kane, J. K., Konu, O., Ma, J. Z., and Li, M. D. (2004). Nicotine coregulates multiple pathways involved in protein modification/degradation in rat brain. Brain Res. Mol. Brain Res. 132, 181-191. doi: 10.1016/j.molbrainres.2004.09.010
33. Kashem, M. A., James, G., Harper, C., Wilce, P., and Matsumoto, I. (2007). Differential protein expression in the corpus callosum (splenium) of human alcoholics: a proteomics study. Neurochem. Int. 50, 450-459. doi: 10.1016/j.neuint.2006.10.009
34. Kauer, J. A., and Malenka, R. C. (2007). Synaptic plasticityand addiction. Nat. Rev. Neurosci. 8, 844-858. doi: 10.1038/nrn2234
35. Kim, S. Y., Chudapongse, N., Lee, S. M., Levin, M. C., Oh, J. T., Park, H. J., et al. (2005). Proteomic analysis of phosphotyrosyl proteins in morphine-dependent rat brains. Brain Res. Mol. Brain Res. 133, 58-70. doi: 10.1016/j.molbrainres.2004.09.018
36. Kobeissy, F. H., Zhang, Z., Sadasivan, S., Gold, M. S., and Wang, K. K. (2009). Methods in drug abuse neuroproteomics: methamphetamine psychoproteome. Methods Mol. Biol. 566, 217-228. doi: 10.1007/978-1-59745-562-6_15
37. Le Merrer, J., Becker, J. A., Befort, K., and Kieffer, B. L. (2009). Reward processing by the opioid system in the brain. Physiol. Rev. 89, 1379-1412. doi: 10.1152/physrev.00005.2009
38. Lee, S. H., Choi, J. H., Lee, N., Lee, H. R., Kim, J. I., Yu, N. K., et al. (2008). Synaptic protein degradation underlies destabilization of retrieved fear memory. Science 319, 1253-1256. doi: 10.1126/science.1150541
39. Li, K. W., Jimenez, C. R., van Der Schors, R. C., Hornshaw, M. P., Schoffelmeer, A. N., and Smit, A. B. (2006). Intermittent administration of morphine alters protein expression in rat nucleus accumbens. Proteomics 6, 2003-2008. doi: 10.1002/pmic.200500045
40. Li, Q., Zhao, X., Zhong, L. J., Yang, H. Y., Wang, Q., and Pu, X. P. (2009). Effects of chronic morphine treatment on protein expression in rat dorsal root ganglia. Eur. J. Pharmacol. 612, 21-28. doi: 10.1016/j.ejphar.2009.03.049
41. Lin, M., Chandramani-Shivalingappa, P., Jin, H., Ghosh, A., Anantharam, V., Ali, S., et al. (2012). Methamphetamine-induced neurotoxicity linked to ubiquitin-proteasome system dysfunction and autophagy-related changes that can be modulated by protein kinase C delta in dopaminergic neuronal cells. Neuroscience 210, 308-332. doi: 10.1016/j.neuroscience.2012.03.004
42. Lin, X., Wang, Q., Cheng, Y., Ji, J., and Yu, L. C. (2011). Changes of protein expression profiles in the amygdala during the process of morphine-induced conditioned place preference in rats. Behav. Brain Res. 221, 197-206. doi: 10.1016/j.bbr.2011.03.002
43. Liu, S., and Chen, Z. J. (2011). Expanding role of ubiquitination in NF-kappaB signaling. Cell Res. 21, 6-21. doi: 10.1038/cr.2010.170
44. Lopez-Salon, M., Alonso, M., Vianna, M. R., Viola, H., Mello ESouza, T., Izquierdo, I., et al. (2001). The ubiquitin-proteasome cascade is required for mammalian long-term memory formation. Eur. J. Neurosci. 14, 1820-1826. doi: 10.1046/j.0953-816x.2001.01806.x
45. Mabb, A. M., and Ehlers, M. D. (2010). Ubiquitination in postsynaptic function and plasticity. Annu.Rev.CellDev.Biol. 26, 179-210. doi: 10.1146/annurev-cellbio-100109-104129
46. Macgurn, J. A., Hsu, P. C., and Emr, S. D. (2012). Ubiquitin and membrane pro-teinturnover:fromcradletograve. Annu. Rev. Biochem. 81, 231-259. doi: 10.1146/annurev-biochem-060210-093619
47. Mao, L.M., Wang, W., Chu, X.P., Zhang, G.C., Liu, X.Y., Yang, (2009). Stability of surface NMDA receptors controls synaptic and behavioral adaptations to amphetamine. Nat. Neurosci. 12, 602-610. doi: 10.1038/nn.2300
48. Massaly, N., Dahan, L., Baudonnat, M., Hovnanian, C., Rekik, K., Solinas, M., et al. (2013). Involvement of protein degradation by the ubiquitin proteasome system in opiate addictive behaviors. Neuropsychopharmacology 38, 596-604. doi: 10.1038/npp.2012.217
49. Mazzo, F., Pistillo, F., Grazioso, G., Clementi, F., Borgese, N., Gotti, C., et al. (2013). Nicotine-modulated subunit stoichiometry affects stability and traf-ricking of alpha3beta4 nicotinic receptor. J. Neurosci. 33, 12316-12328. doi: 10.1523/JNEUROSCI.2393-13.2013
50. Milton, A. L., and Everitt, B. J. (2012). The persistence of maladaptive memory: addiction, drug memories and anti-relapse treatments. Neurosci. Biobehav. Rev. 36, 1119-1139. doi: 10.1016/j.neubiorev.2012.01.002
51. Mimnaugh, E. G., Chen, H. Y., Davie, J. R., Celis, J. E., and Neckers, L. (1997). Rapid deubiquitination of nucleosomal histones in human tumor cells caused by proteasome inhibitors and stress response inducers: effects on replication, transcription, translation, and the cellular stress response. Biochemistry 36, 14418-14429. doi: 10.1021/bi970998j
52. Mouledous, L., Neasta, J., Uttenweiler-Joseph, S., Stella, A., Matondo, M., Corbani, M., et al. (2005). Long-term morphine treatment enhances proteasome-dependent degradation of G beta in human neuroblastoma SH-SY5Y cells: correlation with onset of adenylate cyclase sensitization. Mol. Pharmacol. 68, 467-476. doi: 10.1124/mol.105.013391
53. Neasta, J., Uttenweiler-Joseph, S., Chaoui, K., Monsarrat, B., Meunier, J. C., and Mouledous, L. (2006). Effect of long-term exposure of SH-SY5Y cells to morphine: a whole cell proteomic analysis. Proteome Sci. 4:23. doi: 10.1186/14775956-4-23
54. Patrick, G. N. (2006). Synapse formation and plasticity: recent insights from the perspective of the ubiquitin proteasome system. Curr. Opin. Neurobiol. 16, 90-94. doi: 10.1016/j.conb.2006.01.007
55. Pla, A., Pascual, M., Renau-Piqueras, J., and Guerri, C. (2014). TLR4 mediates the impairment of ubiquitin-proteasome and autophagy-lysosome pathways induced by ethanol treatment in brain. Cell Death Dis. 5:e1066. doi: 10.1038/cddis.2014.46
56. Qin, W. J., Wang, Y. T., Zhang, M., Wen, R. T., Liu, Q., Li, Y. L., et al. (2013). Molecular chaperone heat shock protein 70 participates in the labile phase of the development of behavioural sensitization induced by a single morphine exposure in mice. Int. J. Neuropsychopharmacol. 16, 647-659. doi: 10.1017/S1461145712000557
57. Rambhia, S., Mantione, K. J., Stefano, G. B., and Cadet, P. (2005). Morphine modulation ofthe ubiquitin-proteasome complexis neuroprotective. Med. Sci. Monit. 11, 386-396
58. Reis, D. S., Jarome, T. J., and Helmstetter, F. J. (2013). Memory formation for trace fear conditioning requires ubiquitin-proteasome mediated protein degradation in the prefrontal cortex. Front. Behav. Neurosci. 7:150. doi: 10.3389/fnbeh.2013.00150
59. Ren, Z. Y., Liu, M. M., Xue, Y. X., Ding, Z. B., Xue, L. F., Zhai, S. D., et al. (2013). A critical role for protein degradation in the nucleus accumbens core in cocaine reward memory. Neuropsychopharmacology 38, 778-790. doi: 10.1038/npp.2012.243
60. Rezvani, K., Teng, Y., Shim, D., and De Biasi, M. (2007). Nicotine regulates multiple synaptic proteins by inhibiting proteasomal activity. J. Neurosci. 27, 10508-10519. doi: 10.1523/JNEUROSCI.3353-07.2007
61. Robinson, T. E., and Kolb, B. (2004). Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 47(Suppl. 1), 33-46. doi: 10.1016/j.neuropharm.2004.06.025
62. Rodriguez-Ortiz, C. J., Balderas, I., Saucedo-Alquicira, F., Cruz-Castaneda, P., and Bermudez-Rattoni, F. (2011). Long-term aversive taste memoryrequires insular and amygdala protein degradation. Neurobiol. Learn. Mem. 95, 311-315. doi: 10.1016/j.nlm.2010.12.010
63. Russo, S. J., Dietz, D. M., Dumitriu, D., Morrison, J. H., Malenka, R. C., and Nestler, E. J. (2010). The addicted synapse: mechanisms of synaptic and structural plasticity in nucleus accumbens. Trends Neurosci. 33, 267-276. doi: 10.1016/j.tins.2010.02.002
64. Shen, H., Korutla, L., Champtiaux, N., Toda, S., Lalumiere, R., Vallone, J., etal. (2007). NAC1 regulates the recruitment of the proteasome complex into dendritic spines. J. Neurosci. 27, 8903-8913. doi: 10.1523/JNEUROSCI.1571-07.2007
65. Song, K.Y., Choi, H.S., Hwang, C.K., Kim, C.S., Law, P.Y., Wei, L.N.,etal. (2009). Differential use of an in-frame translation initiation codon regulates human mu opioid receptor (OPRM1). Cell.Mol.LifeSci.66, 2933-2942. doi: 10.1007/s00018-009-0082-7
66. Sun, X., and Wolf, M. E. (2009). Nucleus accumbens neurons exhibit synaptic scaling that is occluded by repeated dopamine pre-exposure. Eur. J. Neurosci. 30, 539-550. doi: 10.1111/j.1460-9568.2009.06852.x
67. Valjent, E., Corvol, J. C., Trzaskos, J. M., Girault, J. A., and Herve, D. (2006). Role of the ERK pathway in psychostimulant-induced locomotor sensitization. BMC Neurosci. 7:20. doi: 10.1186/1471-2202-7-20
68. Wang, Q., and Traynor, J. R. (2011). Opioid-induced Down-Regulation of RGS4: role of ubiquitination and implications for receptor cross-talk. J. Biol. Chem. 286, 7854-7864. doi: 10.1074/jbc.M110.160911
69. Woo, C. H., Le, N. T., Shishido, T., Chang, E., Lee, H., Heo, K. S., et al. (2010). Novel role of C terminus of Hsc70-interacting protein (CHIP) ubiquitin lig-ase on inhng cardiac apoptosis and dysfunction via regulating ERK5-mediated degradation of inducible cAMP early repressor. Faseb J. 24, 4917-4928. doi: 10.1096/fj.10-162636
70. Yang, H. Y., Pu, X. P., and Liu, Y. (2014). Chronic morphine treatment induces over-expression of HSP70 in mice striatum related with abnormal ubiquitin-proteasome degradation. Drug Alcohol Depend. 139, 53-59. doi: 10.1016/j.drugalcdep.2014.03.005
71. Yang, L., Wang, S., Lim, G., Sung, B., Zeng, Q., and Mao, J. (2008a). Inhibition of the ubiquitin-proteasome activity prevents glutamate transporter degradation and morphine tolerance. Pain 140, 472-478. doi: 10.1016/j.pain.2008.09.028
72. Yang, L., Wang, S., Sung, B., Lim, G., and Mao, J. (2008b). Morphine induces ubiquitin-proteasome activity and glutamate transporter degradation. J. Biol. Chem. 283, 21703-21713. doi: 10.1074/jbc.M8008 09200