Dopamine exacerbates mutant Huntingtin toxicity via oxidative-mediated inhibition of autophagy in SH-SY5Y neuroblastoma cells: Beneficial effects of anti-oxidant therapeutics

Neurochemistry International

Volumn 101, Issue , 2016, Pages 132-143

  Vidoni, Chiara ^a   Castiglioni, Andrea ^a   Seca, Christian ^a   Secomandi, Eleonora ^a   Melone, Mariarosa A B ^b   Isidoro, Ciro ^a,b  

^a UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^b SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

Anti oxidant; Autophagy; Dopaminergic neurons; Huntington; Neurodegeneration; Parkinson

Indexed keywords

DOPAMINE; HUNTINGTIN; ANTIOXIDANT; NERVE PROTEIN; OXIDIZING AGENT;

APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL GROWTH; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DOPAMINERGIC NERVE CELL; ECTOPIC EXPRESSION; HUMAN; HUMAN CELL; NEUROBLASTOMA CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; CELL SURVIVAL; DRUG EFFECTS; GENETICS; HUNTINGTON CHOREA; METABOLISM; NERVE CELL; NEUROBLASTOMA; PHYSIOLOGY; TUMOR CELL LINE;

ANTIOXIDANTS; AUTOPHAGY; CELL LINE, TUMOR; CELL SURVIVAL; DOPAMINE; HUMANS; HUNTINGTON DISEASE; NERVE TISSUE PROTEINS; NEUROBLASTOMA; NEURONS; OXIDANTS; OXIDATIVE STRESS;

EID: 84996484033     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2016.11.003     Document Type: Article

References (59)

1. Bäckman, L., Farde, L., Dopamine and cognitive functioning: brain imaging findings in Huntington's disease and normal aging. Scand. J. Psychol. 42:3 (2001), 287–296 (Review).
2. Bjørkøy, G., Lamark, T., Brech, A., Outzen, H., Perander, M., Overvatn, A., Stenmark, H., Johansen, T., p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 171:4 (2005), 603–614.
3. Cagnin, M., Ozzano, M., Bellio, N., Fiorentino, I., Follo, C., Isidoro, C., Dopamine induces apoptosis in APPswe-expressing Neuro2A cells following Pepstatin-sensitive proteolysis of APP in acid compartments. Brain Res. 1471 (2012), 102–117, 10.1016/j.brainres.2012.06.025.
4. Castino, R., Davies, J., Beaucourt, S., Isidoro, C., Murphy, D., Autophagy is a prosurvival mechanism in cells expressing an autosomal dominant familial neurohypophyseal diabetes insipidus mutant vasopressin transgene. FASEB J. 19:8 (2005), 1021–1023.
5. Castino, R., Isidoro, C., Murphy, D., Autophagy-dependent cell survival and cell death in an autosomal dominant familial neurohypophyseal diabetes insipidus in vitro model. FASEB J. 19:8 (2005), 1024–1026.
6. Castino, R., Bellio, N., Nicotra, G., Follo, C., Trincheri, N.F., Isidoro, C., Cathepsin D-Bax death pathway in oxidative stressed neuroblastoma cells. Free Radic. Biol. Med. 42:9 (2007), 1305–1316.
7. Castino, R., Lazzeri, G., Lenzi, P., Bellio, N., Follo, C., Ferrucci, M., Fornai, F., Isidoro, C., Suppression of autophagy precipitates neuronal cell death following low doses of methamphetamine. J. Neurochem. 106:3 (2008), 1426–1439, 10.1111/j.1471-4159.2008.05488.
8. Castino, R., Thepparit, C., Bellio, N., Murphy, D., Isidoro, C., Akt induces apoptosis in neuroblastoma cells expressing a C98X vasopressin mutant following autophagy suppression. J. Neuroendocrinol. 20:10 (2008), 1165–1175, 10.1111/j.1365-2826.2008.01769.
9. Castino, R., Bellio, N., Follo, C., Murphy, D., Isidoro, C., Inhibition of PI3k class III-dependent autophagy prevents apoptosis and necrosis by oxidative stress in dopaminergic neuroblastoma cells. Toxicol. Sci. 117:1 (2010), 152–162, 10.1093/toxsci/kfq170.
10. Castino, R., Fiorentino, I., Cagnin, M., Giovia, A., Isidoro, C., Chelation of lysosomal iron protects dopaminergic SH-SY5Y neuroblastoma cells from hydrogen peroxide toxicity by precluding autophagy and Akt dephosphorylation. Toxicol. Sci. 123:2 (2011), 523–541, 10.1093/toxsci/kfr179.
11. Cepeda, C., Murphy, K.P., Parent, M., Levine, M.S., The role of dopamine in Huntington's disease. Prog. Brain Res. 211 (2014), 235–254, 10.1016/B978-0-444-63425-2.00010-6 (Review).
12. Chen, J.Y., Wang, E.A., Cepeda, C., Levine, M.S., Dopamine imbalance in Huntington's disease: a mechanism for the lack of behavioral flexibility. Front. Neurosci., 7, 2013, 114, 10.3389/fnins.2013.00114.
13. Cherra, S.J. 3rd, Dagda, R.K., Chu, C.T., Review: autophagy and neurodegeneration: survival at a cost?. Neuropathol. Appl. Neurobiol. 36:2 (2010), 125–132, 10.1111/j.1365-2990.2010.01062 (Review).
14. DiFiglia, M., Sapp, E., Chase, K.O., Davies, S.W., Bates, G.P., Vonsattel, J.P., Aronin, N., Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277:5334 (1997), 1990–1993.
15. Ekkapongpisit, M., Giovia, A., Nicotra, G., Ozzano, M., Caputo, G., Isidoro, C., Labeling and exocytosis of secretory compartments in RBL mastocytes by polystyrene and mesoporous silica nanoparticles. Int. J. Nanomedicine. 7 (2012), 1829–1840, 10.2147/IJN.S29034.
16. Erdmann, S., Ricken, A., Merkwitz, C., Struman, I., Castino, R., Hummitzsch, K., Gaunitz, F., Isidoro, C., Martial, J., Spanel-Borowski, K., The expression of prolactin and its cathepsin D-mediated cleavage in the bovine corpus luteum vary with the estrous cycle. Am. J. Physiol. Endocrinol. Metab. 293:5 (2007), E1365–E1377.
17. Follo, C., Ozzano, M., Mugoni, V., Castino, R., Santoro, M., Isidoro, C., Knock-down of cathepsin D affects the retinal pigment epithelium, impairs swim-bladder ontogenesis and causes premature death in zebrafish. PLoS One., 6(7), 2011, e21908, 10.1371/journal.pone.0021908.
18. Fusco, F.R., Anzilotti, S., Giampà, C., Dato, C., Laurenti, D., Leuti, A., Colucci D'Amato, L., Perrone, L., Bernardi, G., Melone, M.A., Changes in the expression of extracellular regulated kinase (ERK 1/2) in the R6/2 mouse model of Huntington's disease after phosphodiesterase IV inhibition. Neurobiol. Dis. 46:1 (2012), 225–233, 10.1016/j.nbd.2012.01.011.
19. Garrett, M.C., Soares-da-Silva, P., Increased cerebrospinal fluid dopamine and 3,4-dihydroxyphenylacetic acid levels in Huntington's disease: evidence for an overactive dopaminergic brain transmission. J. Neurochem. 58:1 (1992), 101–106.
20. Haleagrahara, N., Siew, C.J., Ponnusamy, K., Effect of quercetin and desferrioxamine on 6-hydroxydopamine (6-OHDA) induced neurotoxicity in striatum of rats. J. Toxicol. Sci. 38:1 (2013), 25–33.
21. Halloran, M., Parakh, S., Atkin, J.D., The role of s-nitrosylation and s-glutathionylation of protein disulphide isomerase in protein misfolding and neurodegeneration. Int. J. Cell Biol., 2013, 2013, 797914, 10.1155/2013/797914 (Review).
22. Heiseke, A., Aguib, Y., Riemer, C., Baier, M., Schätzl, H.M., Lithium induces clearance of protease resistant prion protein in prion-infected cells by induction of autophagy. J. Neurochem. 109:1 (2009), 25–34, 10.1111/j.1471-4159.2009.05906.
23. Heng, M.Y., Duong, D.K., Albin, R.L., Tallaksen-Greene, S.J., Hunter, J.M., Lesort, M.J., Osmand, A., Paulson, H.L., Detloff, P.J., Early autophagic response in a novel knock-in model of Huntington disease. Hum. Mol. Genet. 19:19 (2010), 3702–3720, 10.1093/hmg/ddq285.
24. Higgins, G.C., Devenish, R.J., Beart, P.M., Nagley, P., Autophagic activity in cortical neurons under acute oxidative stress directly contributes to cell death. Cell Mol. Life Sci. 68:22 (2011), 3725–3740, 10.1007/s00018-011-0667-9.
25. Isidoro, C., Biagioni, F., Giorgi, F.S., Fulceri, F., Paparelli, A., Fornai, F., The role of autophagy on the survival of dopamine neurons. Curr. Top. Med. Chem. 9:10 (2009), 869–879 (Review).
26. Jakel, R.J., Maragos, W.F., Neuronal cell death in Huntington's disease: a potential role for dopamine. Trends Neurosci. 23:6 (2000), 239–245 (Review).
27. Janda, E., Isidoro, C., Carresi, C., Mollace, V., Defective autophagy in Parkinson's disease: role of oxidative stress. Mol. Neurobiol. 46:3 (2012), 639–661, 10.1007/s12035-012-8318-1 (Review).
28. Janda, E., Lascala, A., Carresi, C., Parafati, M., Aprigliano, S., Russo, V., Savoia, C., Ziviani, E., Musolino, V., Morani, F., Isidoro, C., Mollace, V., Parkinsonian toxin-induced oxidative stress inhibits basal autophagy in astrocytes via NQO2/quinone oxidoreductase 2: implications for neuroprotection. Autophagy 11:7 (2015), 1063–1080, 10.1080/15548627.2015.1058683.
29. Jiao, Y., Ma, S., Wang, Y., Li, J., Shan, L., Liu, Q., Liu, Y., Song, Q., Yu, F., Yu, H., Liu, H., Huang, L., Chen, J., N-acetyl cysteine depletes reactive oxygen species and prevents dental monomer-induced intrinsic mitochondrial apoptosis in vitro in human dental pulp cells. PLoS One, 11(1), 2016, e0147858, 10.1371/journal.pone.0147858.
30. Kish, S.J., Shannak, K., Hornykiewicz, O., Elevated serotonin and reduced dopamine in subregionally divided Huntington's disease striatum. Ann. Neurol. 22:3 (1987), 386–389.
31. Klionsky, D.J., Abdelmohsen, K., Abe, A., et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 12:1 (2016), 1–222, 10.1080/15548627.2015.1100356.
32. Martinez-Vicente, M., Talloczy, Z., Wong, E., Tang, G., Koga, H., Kaushik, S., de Vries, R., Arias, E., Harris, S., Sulzer, D., Cuervo, A.M., Cargo recognition failure is responsible for inefficient autophagy in Huntington's disease. Nat. Neurosci. 13:5 (2010), 567–576, 10.1038/nn.2528.
33. Melone, M.A., Jori, F.P., Peluso, G., Huntington's disease: new frontiers for molecular and cell therapy. Curr. Drug Targets. 6:1 (2005), 43–56 (Review).
34. Nakamura, T., Cho, D.H., Lipton, S.A., Redox regulation of protein misfolding, mitochondrial dysfunction, synaptic damage, and cell death in neurodegenerative diseases. Exp. Neurol. 238:1 (2012), 12–21, 10.1016/j.expneurol.2012.06.032 Epub 2012 Jul 5. Review.
35. Oh, J.M., Choi, E.K., Carp, R.I., Kim, Y.S., Oxidative stress impairs autophagic flux in prion protein-deficient hippocampal cells. Autophagy 8:10 (2012), 1448–1461, 10.4161/auto.21164.
36. Papa, L., Rockwell, P., Persistent mitochondrial dysfunction and oxidative stress hinder neuronal cell recovery from reversible proteasome inhibition. Apoptosis 13:4 (2008), 588–599, 10.1007/s10495-008-0182-0.
37. Persichetti, F., Trettel, F., Huang, C.C., Fraefel, C., Timmers, H.T., Gusella, J.F., MacDonald, M.E., Mutant huntingtin forms in vivo complexes with distinct context-dependent conformations of the polyglutamine segment. Neurobiol. Dis. 6:5 (1999), 364–375.
38. Petersén, A., Hansson, O., Puschban, Z., Sapp, E., Romero, N., Castilho, R.F., Sulzer, D., Rice, M., DiFiglia, M., Przedborski, S., Brundin, P., Mice transgenic for exon 1 of the Huntington's disease gene display reduced striatal sensitivity to neurotoxicity induced by dopamine and 6-hydroxydopamine. Eur. J. Neurosci. 14:9 (2001), 1425–1435.
39. Petersén, A., Larsen, K.E., Behr, G.G., Romero, N., Przedborski, S., Brundin, P., Sulzer, D., Expanded CAG repeats in exon 1 of the Huntington's disease gene stimulate dopamine-mediated striatal neuron autophagy and degeneration. Hum. Mol. Genet. 10:12 (2001), 1243–1254.
40. Qin, Z.H., Wang, Y., Kegel, K.B., Kazantsev, A., Apostol, B.L., Thompson, L.M., Yoder, J., Aronin, N., DiFiglia, M., Autophagy regulates the processing of amino terminal huntingtin fragments. Hum. Mol. Genet. 12:24 (2003), 3231–3244.
41. Ratovitski, T., Nakamura, M., D'Ambola, J., Chighladze, E., Liang, Y., Wang, W., Graham, R., Hayden, M.R., Borchelt, D.R., Hirschhorn, R.R., Ross, C.A., N-terminal proteolysis of full-length mutant huntingtin in an inducible PC12 cell model of Huntington's disease. Cell Cycle 6:23 (2007), 2970–2981.
42. Ratovitski, T., Gucek, M., Jiang, H., Chighladze, E., Waldron, E., D'Ambola, J., Hou, Z., Liang, Y., Poirier, M.A., Hirschhorn, R.R., Graham, R., Hayden, M.R., Cole, R.N., Ross, C.A., Mutant huntingtin N-terminal fragments of specific size mediate aggregation and toxicity in neuronal cells. J. Biol. Chem. 284:16 (2009), 10855–10867, 10.1074/jbc.M804813200.
43. Ravikumar, B., Vacher, C., Berger, Z., Davies, J.E., Luo, S., Oroz, L.G., Scaravilli, F., Easton, D.F., Duden, R., O'Kane, C.J., Rubinsztein, D.C., Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat. Genet. 36:6 (2004), 585–595.
44. Roscic, A., Baldo, B., Crochemore, C., Marcellin, D., Paganetti, P., Induction of autophagy with catalytic mTOR inhibitors reduces huntingtin aggregates in a neuronal cell model. J. Neurochem. 119:2 (2011), 398–407, 10.1111/j.1471-4159.2011.07435.
45. Rossetti, G., Magistrato, A., Pastore, A., Persichetti, F., Carloni, P., Structural properties of polyglutamine aggregates investigated via molecular dynamics simulations. J. Phys. Chem. B 112:51 (2008), 16843–16850, 10.1021/jp806548p.
46. Rubinsztein, D.C., Lessons from animal models of Huntington's disease. Trends Genet. 18:4 (2002), 202–209 (Review).
47. Rubinsztein, D.C., The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 443:7113 (2006), 780–786 (Review).
48. Rui, Y.N., Xu, Z., Patel, B., Chen, Z., Chen, D., Tito, A., David, G., Sun, Y., Stimming, E.F., Bellen, H.J., Cuervo, A.M., Zhang, S., Huntingtin functions as a scaffold for selective macroautophagy. Nat. Cell Biol. 17:3 (2015), 262–275, 10.1038/ncb3101.
49. Sandhir, R., Sood, A., Mehrotra, A., Kamboj, S.S., N-Acetylcysteine reverses mitochondrial dysfunctions and behavioral abnormalities in 3-nitropropionic acid-induced Huntington's disease. Neurodegener. Dis. 9:3 (2012), 145–157, 10.1159/000334273.
50. Sarkar, S., Perlstein, E.O., Imarisio, S., Pineau, S., Cordenier, A., Maglathlin, R.L., Webster, J.A., Lewis, T.A., O'Kane, C.J., Schreiber, S.L., Rubinsztein, D.C., Small molecules enhance autophagy and reduce toxicity in Huntington's disease models. Nat. Chem. Biol. 3:6 (2007), 331–338.
51. Sarkar, S., Krishna, G., Imarisio, S., Saiki, S., O'Kane, C.J., Rubinsztein, D.C., A rational mechanism for combination treatment of Huntington's disease using lithium and rapamycin. Hum. Mol. Genet. 17:2 (2008), 170–178.
52. Sarkar, S., Rubinsztein, D.C., Huntington's disease: degradation of mutant huntingtin by autophagy. FEBS J. 275:17 (2008), 4263–4270, 10.1111/j.1742-4658.2008.06562 (Review).
53. Scherz-Shouval, R., Shvets, E., Elazar, Z., Oxidation as a post-translational modification that regulates autophagy. Autophagy 3:4 (2007), 371–373.
54. Soto, C., Unfolding the role of protein misfolding in neurodegenerative diseases. Nat. Rev. Neurosci. 4:1 (2003), 49–60 (Review).
55. Valencia, A., Sapp, E., Kimm, J.S., McClory, H., Reeves, P.B., Alexander, J., Ansong, K.A., Masso, N., Frosch, M.P., Kegel, K.B., Li, X., DiFiglia, M., Elevated NADPH oxidase activity contributes to oxidative stress and cell death in Huntington's disease. Hum. Mol. Genet. 22:6 (2013), 1112–1131, 10.1093/hmg/dds516.
56. Vidoni, C., Follo, C., Savino, M., Melone, M.A., Isidoro, C., The role of cathepsin D in the pathogenesis of human neurodegenerative disorders. Med. Res. Rev. 36:5 (2016), 845–870, 10.1002/med.21394 (Review).
57. Vonsattel, J.P., Myers, R.H., Stevens, T.J., Ferrante, R.J., Bird, E.D., Richardson, E.P. Jr., Neuropathological classification of Huntington's disease. J. Neuropathol. Exp. Neurol. 44:6 (1985), 559–577.
58. Wright, D.J., Renoir, T., Smith, Z.M., Frazier, A.E., Francis, P.S., Thorburn, D.R., McGee, S.L., Hannan, A.J., Gray, L.J., N-Acetylcysteine improves mitochondrial function and ameliorates behavioral deficits in the R6/1 mouse model of Huntington's disease. Transl. Psychiatry, 5, 2015, e492, 10.1038/tp.2014.131.
59. Zhang, S., Wang, J., Song, N., Xie, J., Jiang, H., Up-regulation of divalent metal transporter 1 is involved in 1-methyl-4-phenylpyridinium (MPP(+))-induced apoptosis in MES23.5 cells. Neurobiol. Aging. 30:9 (2009), 1466–1476, 10.1016/j.neurobiolaging.2007.11.025.