Excitotoxic stimulation downregulates the ubiquitin-proteasome system through activation of NMDA receptors in cultured hippocampal neurons

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 1, 2013, Pages 263-274

  Caldeira, Margarida V ^a,c   Curcio, Michele ^a,d   Leal, Graciano ^a   Salazar, Ivan L ^a   Mele, Miranda ^a   Santos, Ana Rita A ^a   Melo, Carlos V ^a   Pereira, Paulo ^b   Canzoniero, Lorella M T ^d   Duarte, Carlos B ^a,c  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b Center of Ophthalmology of Coimbra   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d UNIVERSITY OF SANNIO   (Italy)

Author keywords

Excitotoxicity; Glutamate; NMDA receptors; OGD; Proteasome; UPS

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMPA RECEPTOR; CALCIUM PHOSPHATE; CATHEPSIN L; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEASOME; UBIQUITIN; UBIQUITINATED PROTEIN;

ANIMAL CELL; ARTICLE; BIOLOGICAL ACTIVITY; BRAIN ISCHEMIA; BRAIN NERVE CELL; CALCIUM TRANSPORT; CONTROLLED STUDY; DEPOLARIZATION; DOWN REGULATION; EMBRYO; EXCITOTOXICITY; HALF LIFE TIME; HIPPOCAMPUS; INHIBITION KINETICS; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT; REAL TIME POLYMERASE CHAIN REACTION; UBIQUITINATION; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATE; ANIMALS; BRAIN ISCHEMIA; CELLS, CULTURED; DOWN-REGULATION; FEMALE; GLUTAMIC ACID; HIPPOCAMPUS; HUMANS; MALE; NEURONS; PROTEASOME ENDOPEPTIDASE COMPLEX; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; UBIQUITIN;

RATTUS;

EID: 84868560715     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2012.10.009     Document Type: Article

References (51)

1. Hershko A., Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 1998, 67:425-479.
2. Ravid T., Hochstrasser M. Diversity of degradation signals in the ubiquitin-proteasome system. Nat. Rev. Mol. Cell Biol. 2008, 9:679-690.
3. Kim H.M., Yu Y., Cheng Y. Structure characterization of the 26S proteasome. Biochim. Biophys. Acta 2011, 1809:67-79.
4. Glickman M.H., Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 2002, 82:373-428.
5. Orlowski M., Wilk S. Catalytic activities of the 20 S proteasome, a multicatalytic proteinase complex. Arch. Biochem. Biophys. 2000, 383:1-16.
6. Verma R., Oania R., Graumann J., Deshaies R.J. Multiubiquitin chain receptors define a layer of substrate selectivity in the ubiquitin-proteasome system. Cell 2004, 118:99-110.
7. Lander G.C., Estrin E., Matyskiela M.E., Bashore C., Nogales E., Martin A. Complete subunit architecture of the proteasome regulatory particle. Nature 2012, 482:186-191.
8. Wojcik C., Di Napoli M. Ubiquitin-proteasome system and proteasome inhibition: new strategies in stroke therapy. Stroke 2004, 35:1506-1518.
9. Hu B.R., Janelidze S., Ginsberg M.D., Busto R., Perez-Pinzon M., Sick T.J., Siesjo B.K., Liu C.L. Protein aggregation after focal brain ischemia and reperfusion. J. Cereb. Blood Flow Metab. 2001, 21:865-875.
10. Hu B.R., Martone M.E., Jones Y.Z., Liu C.L. Protein aggregation after transient cerebral ischemia. J. Neurosci. 2000, 20:3191-3199.
11. Liu C.L., Martone M.E., Hu B.R. Protein ubiquitination in postsynaptic densities after transient cerebral ischemia. J. Cereb. Blood Flow Metab. 2004, 24:1219-1225.
12. Ge P., Luo Y., Liu C.L., Hu B. Protein aggregation and proteasome dysfunction after brain ischemia. Stroke 2007, 38:3230-3236.
13. Asai A., Tanahashi N., Qiu J.H., Saito N., Chi S., Kawahara N., Tanaka K., Kirino T. Selective proteasomal dysfunction in the hippocampal CA1 region after transient forebrain ischemia. J. Cereb. Blood Flow Metab. 2002, 22:705-710.
14. Stephenson D., Yin T., Smalstig E.B., Hsu M.A., Panetta J., Little S., Clemens J. Transcription factor nuclear factor-kappa B is activated in neurons after focal cerebral ischemia. J. Cereb. Blood Flow Metab. 2000, 20:592-603.
15. Choi D.W. Calcium-mediated neurotoxicity: relationship to specific channel types and role in ischemic damage. Trends Neurosci. 1988, 11:465-469.
16. Takano J., Tomioka M., Tsubuki S., Higuchi M., Iwata N., Itohara S., Maki M., Saido T.C. Calpain mediates excitotoxic DNA fragmentation via mitochondrial pathways in adult brains: evidence from calpastatin mutant mice. J. Biol. Chem. 2005, 280:16175-16184.
17. Hardingham G.E., Fukunaga Y., Bading H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat. Neurosci. 2002, 5:405-414.
18. Bengtson C.P., Dick O., Bading H. A quantitative method to assess extrasynaptic NMDA receptor function in the protective effect of synaptic activity against neurotoxicity. BMC Neurosci. 2008, 9:11.
19. Dantuma N.P., Lindsten K., Glas R., Jellne M., Masucci M.G. Short-lived green fluorescent proteins for quantifying ubiquitin/proteasome-dependent proteolysis in living cells. Nat. Biotechnol. 2000, 18:538-543.
20. Gomes J.R., Lobo A.C., Melo C.V., Inacio A.R., Takano J., Iwata N., Saido T.C., de Almeida L.P., Wieloch T., Duarte C.B. Cleavage of the vesicular GABA transporter under excitotoxic conditions is followed by accumulation of the truncated transporter in nonsynaptic sites. J. Neurosci. 2011, 31:4622-4635.
21. Stocchi V., Cucchiarini L., Magnani M., Chiarantini L., Palma P., Crescentini G. Simultaneous extraction and reverse-phase high-performance liquid chromatographic determination of adenine and pyridine nucleotides in human red blood cells. Anal. Biochem. 1985, 146:118-124.
22. Almeida R.D., Manadas B.J., Melo C.V., Gomes J.R., Mendes C.S., Graos M.M., Carvalho R.F., Carvalho A.P., Duarte C.B. Neuroprotection by BDNF against glutamate-induced apoptotic cell death is mediated by ERK and PI3-kinase pathways. Cell Death Differ. 2005, 12:1329-1343.
23. Adori C., Low P., Moszkovkin G., Bagdy G., Laszlo L., Kovacs G.G. Subcellular distribution of components of the ubiquitin-proteasome system in non-diseased human and rat brain. J. Histochem. Cytochem. 2006, 54:263-267.
24. Hardingham G.E. Coupling of the NMDA receptor to neuroprotective and neurodestructive events. Biochem. Soc. Trans. 2009, 37:1147-1160.
25. Hardingham G.E., Bading H. Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat. Rev. Neurosci. 2010, 11:682-696.
26. Ferreira I.L., Duarte C.B., Carvalho A.P. Kainate-induced retina amacrine-like cell damage is mediated by AMPA receptors. Neuroreport 1998, 9:3471-3475.
27. Bading H., Ginty D.D., Greenberg M.E. Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 1993, 260:181-186.
28. 2+ ionic dysregulation. J. Neurochem. 2010, 112:173-182.
29. Bevers M.B., Neumar R.W. Mechanistic role of calpains in postischemic neurodegeneration. J. Cereb. Blood Flow Metab. 2008, 28:655-673.
30. Bevers M.B., Lawrence E., Maronski M., Starr N., Amesquita M., Neumar R.W. Knockdown of m-calpain increases survival of primary hippocampal neurons following NMDA excitotoxicity. J. Neurochem. 2009, 108:1237-1250.
31. Seyfried D.M., Veyna R., Han Y., Li K., Tang N., Betts R.L., Weinsheimer S., Chopp M., Anagli J. A selective cysteine protease inhibitor is non-toxic and cerebroprotective in rats undergoing transient middle cerebral artery ischemia. Brain Res. 2001, 901:94-101.
32. Meller R. The role of the ubiquitin proteasome system in ischemia and ischemic tolerance. Neuroscientist 2009, 15:243-260.
33. Ciechanover A., Brundin P. The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron 2003, 40:427-446.
34. Ankarcrona M., Dypbukt J.M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S.A., Nicotera P. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 1995, 15:961-973.
35. Ward M.W., Huber H.J., Weisova P., Dussmann H., Nicholls D.G., Prehn J.H. Mitochondrial and plasma membrane potential of cultured cerebellar neurons during glutamate-induced necrosis, apoptosis, and tolerance. J. Neurosci. 2007, 27:8238-8249.
36. Leggett D.S., Hanna J., Borodovsky A., Crosas B., Schmidt M., Baker R.T., Walz T., Ploegh H., Finley D. Multiple associated proteins regulate proteasome structure and function. Mol. Cell 2002, 10:495-507.
37. Siesjo B.K., Elmer E., Janelidze S., Keep M., Kristian T., Ouyang Y.B., Uchino H. Role and mechanisms of secondary mitochondrial failure. Acta Neurochir. Suppl. 1999, 73:7-13.
38. Tai H.C., Besche H., Goldberg A.L., Schuman E.M. Characterization of the brain 26S proteasome and its interacting proteins. Front. Mol. Neurosci. 2010, 3:12.
39. 2+ influx through glutamate receptor-associated channels in retina cells correlates with neuronal cell death. Eur. J. Pharmacol. 1996, 302:153-162.
40. Hardingham G.E., Bading H. The Yin and Yang of NMDA receptor signalling. Trends Neurosci. 2003, 26:81-89.
41. Djakovic S.N., Schwarz L.A., Barylko B., DeMartino G.N., Patrick G.N. Regulation of the proteasome by neuronal activity and calcium/calmodulin-dependent protein kinase II. J. Biol. Chem. 2009, 284:26655-26665.
42. Cuervo A.M., Palmer A., Rivett A.J., Knecht E. Degradation of proteasomes by lysosomes in rat liver. Eur. J. Biochem. 1995, 227:792-800.
43. Higuchi M., Tomioka M., Takano J., Shirotani K., Iwata N., Masumoto H., Maki M., Itohara S., Saido T.C. Distinct mechanistic roles of calpain and caspase activation in neurodegeneration as revealed in mice overexpressing their specific inhibitors. J. Biol. Chem. 2005, 280:15229-15237.
44. Satoh K., Sasajima H., Nyoumura K.I., Yokosawa H., Sawada H. Assembly of the 26S proteasome is regulated by phosphorylation of the p45/Rpt6 ATPase subunit. Biochemistry 2001, 40:314-319.
45. Ferrell K., Wilkinson C.R., Dubiel W., Gordon C. Regulatory subunit interactions of the 26S proteasome, a complex problem. Trends Biochem. Sci. 2000, 25:83-88.
46. Bingol B., Schuman E.M. Activity-dependent dynamics and sequestration of proteasomes in dendritic spines. Nature 2006, 441:1144-1148.
47. 2+-induced cortical neuronal death. Neuropharmacology 2003, 45:420-428.
48. Chen M., Chen Q., Cheng X.W., Lu T.J., Liu H.X., Jia J.M., Zhang C., Xu L., Xiong Z.Q. Zn2+ mediates ischemia-induced impairment of the ubiquitin-proteasome system in the rat hippocampus. J. Neurochem. 2009, 111:1094-1103.
49. Nakamura T., Lipton S.A. Cell death: protein misfolding and neurodegenerative diseases. Apoptosis 2009, 14:455-468.
50. Reyes-Turcu F.E., Ventii K.H., Wilkinson K.D. Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu. Rev. Biochem. 2009, 78:363-397.
51. Cartier A.E., Djakovic S.N., Salehi A., Wilson S.M., Masliah E., Patrick G.N. Regulation of synaptic structure by ubiquitin C-terminal hydrolase L1. J. Neurosci. 2009, 29:7857-7868.