Downregulation of Homer1b/c in SOD1 G93A models of ALS: A novel mechanism of neuroprotective effect of lithium and valproic acid

International Journal of Molecular Sciences

Volumn 17, Issue 12, 2016, Pages

  Jiang, Hai Zhi ^a   Wang, Shu Yu ^a   Yin, Xiang ^a   Jiang, Hong Quan ^a   Wang, Xu Dong ^a   Wang, Jing ^a   Wang, Tian Hang ^a   Qi, Yan ^a   Yang, Yue Qing ^a   Wang, Ying ^a   Zhang, Chun Ting ^a   Feng, Hong Lin ^a  

^a THE FIRST AFFILIATED HOSPITAL OF HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

Amyotrophic lateral sclerosis; Homer1b c; Lithium; SOD1 G93A; Valproic acid (VPA)

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; LITHIUM; PROTEIN BAX; PROTEIN BCL 2; PROTEIN HOMER 1B; SMALL INTERFERING RNA; VALPROIC ACID; HOMER SCAFFOLDING PROTEIN; HOMER1 PROTEIN, MOUSE; SOD1 G93A PROTEIN; SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CULTURE; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION REGULATION; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MOUSE; MTT ASSAY; NEUROBLASTOMA; NEUROPROTECTION; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; TUNEL ASSAY; UPREGULATION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL LINE; GENETIC PREDISPOSITION; GENETICS; METABOLISM; PATHOLOGY; RNA INTERFERENCE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; APOPTOSIS; CELL LINE; GENETIC PREDISPOSITION TO DISEASE; HOMER SCAFFOLDING PROTEINS; HUMANS; LITHIUM; MICE; MICE, TRANSGENIC; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA INTERFERENCE; RNA, SMALL INTERFERING; SUPEROXIDE DISMUTASE; VALPROIC ACID;

EID: 85007107485     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17122129     Document Type: Article

References (34)

1. Belsh, J.M.; Schiffman, P.L. The amyotrophic lateral sclerosis (ALS) patient perspective on misdiagnosis and its repercussions. J. Neurol. Sci. 1996, 139, 110–116.
2. Chattopadhyay, M.; Valentine, J.S. Aggregation of copper-zinc superoxide dismutase in familial and sporadic ALS. Antioxid. Redox Signal. 2009, 11, 1603–1614.
3. Orrell, R.W. Understanding the causes of amyotrophic lateral sclerosis. N. Engl. J. Med. 2007, 357, 822–823.
4. Simonian, N.A.; Coyle, J.T. Oxidative stress in neurodegenerative diseases. Annu. Rev. Pharmacol. Toxicol. 1996, 36, 83–106.
5. Van Den Bosch, L.; van Damme, P.; Bogaert, E.; Robberecht, W. The role of excitotoxicity in the pathogenesis of amyotrophic lateral sclerosis. Biochim. Biophys. Acta 2006, 1762, 1068–1082.
6. Sathasivam, S.; Ince, P.G.; Shaw, P.J. Apoptosis in amyotrophic lateral sclerosis: A review of the evidence. Neuropathol. Appl. Neurobiol. 2001, 27, 257–274.
7. Mu, X.; He, J.; Anderson, D.W.; Trojanowski, J.Q.; Springer, J.E. Altered expression of Bcl-2 and Bax mRNA in amyotrophic lateral sclerosis spinal cord motor neurons. Ann. Neurol. 1996, 40, 379–386.
8. Vukosavic, S.; Dubois-Dauphin, M.; Romero, N.; Przedborski, S. Bax and Bcl-2 interaction in a transgenic mouse model of familial amyotrophic lateral sclerosis. J. Neurochem. 1999, 73, 2460–2468.
9. Li, M.; Ona, V.O.; Guegan, C.; Chen, M.; Jackson-Lewis, V.; Andrews, L.J.; Olszewski, A.J.; Stieg, P.E.; Lee, J.P.; Przedborski, S.; et al. Functional role of caspase-1 and caspase-3 in an ALS transgenic mouse model. Science 2000, 288, 335–339.
10. Kostic, V.; Jackson-Lewis, V.; de Bilbao, F.; Dubois-Dauphin, M.; Przedborski, S. Bcl-2: Prolonging life in a transgenic mouse model of familial amyotrophic lateral sclerosis. Science 1997, 277, 559–562.
11. Reyes, N.A.; Fisher, J.K.; Austgen, K.; VandenBerg, S.; Huang, E.J.; Oakes, S.A. Blocking the mitochondrial apoptotic pathway preserves motor neuron viability and function in a mouse model of amyotrophic lateral sclerosis. J. Clin. Investig. 2010, 120, 3673–3679.
12. Shaw, A.S.; Filbert, E.L. Scaffold proteins and immune-cell signalling. Nat. Rev. Immunol. 2009, 9, 47–56.
13. Shiraishi-Yamaguchi, Y.; Furuichi, T. The homer family proteins. Genome Biol. 2007, 8, 206.
14. Shiraishi, Y.; Mizutani, A.; Yuasa, S.; Mikoshiba, K.; Furuichi, T. Differential expression of homer family proteins in the developing mouse brain. J. Comp. Neurol. 2004, 473, 582–599.
15. Xiao, B.; Tu, J.C.; Petralia, R.S.; Yuan, J.P.; Doan, A.; Breder, C.D.; Ruggiero, A.; Lanahan, A.A.; Wenthold, R.J.; Worley, P.F. Homer regulates the association of group 1 metabotropic glutamate receptors with multivalent complexes of homer-related, synaptic proteins. Neuron 1998, 21, 707–716.
16. Tappe, A.; Klugmann, M.; Luo, C.; Hirlinger, D.; Agarwal, N.; Benrath, J.; Ehrengruber, M.U.; During, M.J.; Kuner, R. Synaptic scaffolding protein homer1a protects against chronic inflammatory pain. Nat. Med. 2006, 12, 677–681.
17. Cui, Z.; Zhou, L.; Liu, C.; Zhu, G.; Wu, X.; Yan, Y.; Xia, X.; Ben, Z.; Song, Y.; Zhou, Y.; et al. The role of homer1b/c in neuronal apoptosis following LPS-induced neuroinflammation. Neurochem. Res. 2015, 40, 204–215.
18. Sala, C.; Futai, K.; Yamamoto, K.; Worley, P.F.; Hayashi, Y.; Sheng, M. Inhibition of dendritic spine morphogenesis and synaptic transmission by activity-inducible protein homer1a. J. Neurosci. 2003, 23, 6327–6337.
19. Brakeman, P.R.; Lanahan, A.A.; O'Brien, R.; Roche, K.; Barnes, C.A.; Huganir, R.L.; Worley, P.F. Homer: A protein that selectively binds metabotropic glutamate receptors. Nature 1997, 386, 284–288.
20. 2+ entry. IUBMB Life 2013, 65, 497–504.
21. Mao, L.; Yang, L.; Tang, Q.; Samdani, S.; Zhang, G.; Wang, J.Q. The scaffold protein homer1b/c links metabotropic glutamate receptor 5 to extracellular signal-regulated protein kinase cascades in neurons. J. Neurosci. 2005, 25, 2741–2752.
22. Khasraw, M.; Ashley, D.; Wheeler, G.; Berk, M. Using lithium as a neuroprotective agent in patients with cancer. BMC Med. 2012, 10, 131.
23. Riadh, N.; Allagui, M.S.; Bourogaa, E.; Vincent, C.; Croute, F.; Elfeki, A. Neuroprotective and neurotrophic effects of long term lithium treatment in mouse brain. Biometals 2011, 24, 747–757.
24. De Bartolomeis, A.; Tomasetti, C.; Cicale, M.; Yuan, P.X.; Manji, H.K. Chronic treatment with lithium or valproate modulates the expression of homer1b/c and its related genes shank and inositol 1,4,5-trisphosphate receptor. Eur. Neuropsychopharmacol. 2012, 22, 527–535.
25. Yao, Y.X.; Jiang, Z.; Zhao, Z.Q. Knockdown of synaptic scaffolding protein homer 1b/c attenuates secondary hyperalgesia induced by complete freund’s adjuvant in rats. Anesth. Analg. 2011, 113, 1501–1508.
26. Yasuda, S.; Liang, M.H.; Marinova, Z.; Yahyavi, A.; Chuang, D.M. The mood stabilizers lithium and valproate selectively activate the promoter IV of brain-derived neurotrophic factor in neurons. Mol. Psychiatry 2009, 14, 51–59.
27. Chen, G.; Huang, L.D.; Jiang, Y.M.; Manji, H.K. The mood-stabilizing agent valproate inhibits the activity of glycogen synthase kinase-3. J. Neurochem. 1999, 72, 1327–1330.
28. Forlenza, O.V.; Aprahamian, I.; de Paula, V.J.; Hajek, T. Lithium, a therapy for ad: Current evidence from clinical trials of neurodegenerative disorders. Curr. Alzheimer Res. 2016, 13, 879–886.
29. Agam, G.; Israelson, A. Why lithium studies for ALS treatment should not be halted prematurely. Front. Neurosci. 2014, 8, 267.
30. Yanez, M.; Matias-Guiu, J.; Arranz-Tagarro, J.A.; Galan, L.; Vina, D.; Gomez-Pinedo, U.; Vela, A.; Guerrero, A.; Martinez-Vila, E.; Garcia, A.G. The neuroprotection exerted by memantine, minocycline and lithium, against neurotoxicity of CSF from patients with amyotrophic lateral sclerosis, is antagonized by riluzole. Neurodegener. Dis. 2014, 13, 171–179.
31. Naganska, E.; Matyja, E.; Taraszewska, A.; Rafalowska, J. Protective effect of valproic acid on cultured motor neurons under glutamate excitotoxic conditions—Ultrastructural study. Folia Neuropathol. 2015, 53, 309–316.
32. Feng, H.L.; Leng, Y.; Ma, C.H.; Zhang, J.; Ren, M.; Chuang, D.M. Combined lithium and valproate treatment delays disease onset, reduces neurological deficits and prolongs survival in an amyotrophic lateral sclerosis mouse model. Neuroscience 2008, 155, 567–572.
33. Boll, M.C.; Bayliss, L.; Vargas-Canas, S.; Burgos, J.; Montes, S.; Penaloza-Solano, G.; Rios, C.; Alcaraz-Zubeldia, M. Clinical and biological changes under treatment with lithium carbonate and valproic acid in sporadic amyotrophic lateral sclerosis. J. Neurol. Sci. 2014, 340, 103–108.
34. Wang, S.Y.; Ren, M.; Jiang, H.Z.; Wang, J.; Jiang, H.Q.; Yin, X.; Qi, Y.; Wang, X.D.; Dong, G.T.; Wang, T.H.; et al. Notch pathway is activated in cell culture and mouse models of mutant SOD1-related familial amyotrophic lateral sclerosis, with suppression of its activation as an additional mechanism of neuroprotection for lithium and valproate. Neuroscience 2015, 301, 276–288.