Neuronal gene repression in Niemann-Pick type C models is mediated by the c-Abl/HDAC2 signaling pathway

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1859, Issue 2, 2016, Pages 269-279

  Contreras, Pablo S ^a,b   Gonzalez Zuñiga, Marcelo ^a   González Hódar, Lila ^b   Yáñez, María José ^a,b   Dulcey, Andrés ^c   Marugan, Juan ^c   Seto, Edward ^d   Alvarez, Alejandra R ^a   Zanlungo, Silvana ^b,e  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^e FONDAP Center for Genome Regulation (CGR)   (Chile)

Author keywords

GNF2; Histone deacetylase 2; Imatinib; Neuronal genes; Niemann Pick type C disease; Tyrosine kinase c Abl

Indexed keywords

ABELSON KINASE; ALPHA TOCOPHEROL; HISTONE DEACETYLASE 2; IMATINIB; METHYL BETA CYCLODEXTRIN; RNA; CHOLESTEROL; CYCLODEXTRIN; HDAC2 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE REPRESSION; IN VIVO STUDY; MOUSE; NIEMANN PICK DISEASE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SYNAPSE; ANIMAL; BIOSYNTHESIS; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LYSOSOME; METABOLISM; NERVE CELL; NIEMANN-PICK DISEASE, TYPE C; PATHOLOGY;

ANIMALS; CHOLESTEROL; CYCLODEXTRINS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HISTONE DEACETYLASE 2; HUMANS; LYSOSOMES; MICE; NEURONS; NIEMANN-PICK DISEASE, TYPE C; PROTO-ONCOGENE PROTEINS C-ABL; SIGNAL TRANSDUCTION; VITAMIN E;

EID: 84949661599     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2015.11.006     Document Type: Article

References (55)

1. Penney J., Tsai L.H. Histone deacetylases in memory and cognition. Sci. Signal. 2014, 7(355):re12.
2. Fischer A., Sananbenesi F., Wang X., Dobbin M., Tsai L.H. Recovery of learning and memory is associated with chromatin remodelling. Nature 2007, 447(7141):178-182.
3. Graff J., Rei D., Guan J.S., Wang W.Y., Seo J., Hennig K.M., et al. An epigenetic blockade of cognitive functions in the neurodegenerating brain. Nature 2012, 483(7388):222-226.
4. Guan J.S., Haggarty S.J., Giacometti E., Dannenberg J.H., Joseph N., Gao J., et al. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 2009, 459(7243):55-60.
5. Yang X.J., Seto E. Collaborative spirit of histone deacetylases in regulating chromatin structure and gene expression. Curr. Opin. Genet. Dev. 2003, 13(2):143-153.
6. Yang X.J., Seto E. Lysine acetylation: codified crosstalk with other posttranslational modifications. Mol. Cell 2008, 31(4):449-461.
7. Haberland M., Montgomery R.L., Olson E.N. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet. 2009, 10(1):32-42.
8. Brunmeir R., Lagger S., Seiser C. Histone deacetylase HDAC1/HDAC2-controlled embryonic development and cell differentiation. Int. J. Dev. Biol. 2009, 53(2-3):275-289.
9. Montgomery R.L., Hsieh J., Barbosa A.C., Richardson J.A., Olson E.N. Histone deacetylases 1 and 2 control the progression of neural precursors to neurons during brain development. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(19):7876-7881.
10. Gonzalez-Zuniga M., Contreras P.S., Estrada L.D., Chamorro D., Villagra A., Zanlungo S., et al. c-Abl stabilizes HDAC2 levels by tyrosine phosphorylation repressing neuronal gene expression in Alzheimer's disease. Mol. Cell 2014, 56(1):163-173.
11. Jawerka M., Colak D., Dimou L., Spiller C., Lagger S., Montgomery R.L., et al. The specific role of histone deacetylase 2 in adult neurogenesis. Neuron Glia Biol. 2010, 6(2):93-107.
12. MacDonald J.L., Roskams A.J. Histone deacetylases 1 and 2 are expressed at distinct stages of neuro-glial development. Dev. Dyn. 2008, 237(8):2256-2267.
13. Carstea E.D., Morris J.A., Coleman K.G., Loftus S.K., Zhang D., Cummings C., et al. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 1997, 277(5323):228-231.
14. Naureckiene S., Sleat D.E., Lackland H., Fensom A., Vanier M.T., Wattiaux R., et al. Identification of HE1 as the second gene of Niemann-Pick C disease. Science 2000, 290(5500):2298-2301.
15. Kwon H.J., Abi-Mosleh L., Wang M.L., Deisenhofer J., Goldstein J.L., Brown M.S., et al. Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol. Cell 2009, 137(7):1213-1224.
16. Lloyd-Evans E., Morgan A.J., He X., Smith D.A., Elliot-Smith E., Sillence D.J., et al. Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat. Med. 2008, 14(11):1247-1255.
17. Pentchev P.G., Boothe A.D., Kruth H.S., Weintroub H., Stivers J., Brady R.O. A genetic storage disorder in BALB/C mice with a metabolic block in esterification of exogenous cholesterol. J. Biol. Chem. 1984, 259(9):5784-5791.
18. Sturley S.L., Patterson M.C., Balch W., Liscum L. The pathophysiology and mechanisms of NP-C disease. Biochim. Biophys. Acta 2004, 1685(1-3):83-87.
19. Patterson M.C., Hendriksz C.J., Walterfang M., Sedel F., Vanier M.T., Wijburg F., et al. Recommendations for the diagnosis and management of Niemann-Pick disease type C: an update. Mol. Genet. Metab. 2012, 106(3):330-344.
20. Klein A.D., Alvarez A., Zanlungo S. The unique case of the Niemann-Pick type C cholesterol storage disorder. Pediatr. Endocrinol. Rev. 2014, 12(Suppl. 1):166-175.
21. Kim S.J., Lee B.H., Lee Y.S., Kang K.S. Defective cholesterol traffic and neuronal differentiation in neural stem cells of Niemann-Pick type C disease improved by valproic acid, a histone deacetylase inhibitor. Biochem. Biophys. Res. Commun. 2007, 360(3):593-599.
22. Pipalia N.H., Cosner C.C., Huang A., Chatterjee A., Bourbon P., Farley N., et al. Histone deacetylase inhibitor treatment dramatically reduces cholesterol accumulation in Niemann-Pick type C1 mutant human fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 2011, 108(14):5620-5625.
23. Helquist P., Maxfield F.R., Wiech N.L., Wiest O. Treatment of Niemann-Pick type C disease by histone deacetylase inhibitors. Neurotherapeutics 2013, 10(4):688-697.
24. Maceyka M., Milstien S., Spiegel S. The potential of histone deacetylase inhibitors in Niemann-Pick type C disease. FEBS J. 2013, 280(24):6367-6372.
25. Morris M.J., Mahgoub M., Na E.S., Pranav H., Monteggia L.M. Loss of histone deacetylase 2 improves working memory and accelerates extinction learning. J. Neurosci. 2013, 33(15):6401-6411.
26. Bie B., Wu J., Yang H., Xu J.J., Brown D.L., Naguib M. Epigenetic suppression of neuroligin 1 underlies amyloid-induced memory deficiency. Nat. Neurosci. 2014, 17(2):223-231.
27. Aoyama K., Yamaguchi N., Yuki R., Morii M., Kubota S., Hirata K., et al. c-Abl induces stabilization of histone deacetylase 1 (HDAC1) in a kinase activity-dependent manner. Cell Biol. Int. 2015, 39(4):446-456.
28. Malnar M., Hecimovic S., Mattsson N., Zetterberg H. Bidirectional links between Alzheimer's disease and Niemann-Pick type C disease. Neurobiol. Dis. 2014, 72(Pt A):37-47.
29. Nixon R.A. Niemann-Pick type C disease and Alzheimer's disease: the APP-endosome connection fattens up. Am. J. Pathol. 2004, 164(3):757-761.
30. Fu R., Yanjanin N.M., Elrick M.J., Ware C., Lieberman A.P., Porter F.D. Apolipoprotein E genotype and neurological disease onset in Niemann-Pick disease, type C1. Am. J. Med. Genet. A 2012, 158A(11):2775-2780.
31. Genin E., Hannequin D., Wallon D., Sleegers K., Hiltunen M., Combarros O., et al. APOE and Alzheimer disease: a major gene with semi-dominant inheritance. Mol. Psychiatry 2011, 16(9):903-907.
32. Poirier J. Apolipoprotein E and cholesterol metabolism in the pathogenesis and treatment of Alzheimer's disease. Trends Mol. Med. 2003, 9(3):94-101.
33. Yao J., Ho D., Calingasan N.Y., Pipalia N.H., Lin M.T., Beal M.F. Neuroprotection by cyclodextrin in cell and mouse models of Alzheimer disease. J. Exp. Med. 2012, 209(13):2501-2513.
34. Klein A., Maldonado C., Vargas L.M., Gonzalez M., Robledo F. Perez de arce K, et al. Oxidative stress activates the c-Abl/p73 proapoptotic pathway in Niemann-Pick type C neurons. Neurobiol. Dis. 2011, 41(1):209-218.
35. Alvarez A.R., Klein A., Castro J., Cancino G.I., Amigo J., Mosqueira M., et al. Imatinib therapy blocks cerebellar apoptosis and improves neurological symptoms in a mouse model of Niemann-Pick type C disease. FASEB J. 2008, 22(10):3617-3627.
36. Alvarez A.R., Sandoval P.C., Leal N.R., Castro P.U., Kosik K.S. Activation of the neuronal c-Abl tyrosine kinase by amyloid-beta-peptide and reactive oxygen species. Neurobiol. Dis. 2004, 17(2):326-336.
37. Cancino G.I., Toledo E.M., Leal N.R., Hernandez D.E., Yevenes L.F., Inestrosa N.C., et al. STI571 prevents apoptosis, tau phosphorylation and behavioural impairments induced by Alzheimer's beta-amyloid deposits. Brain 2008, 131(Pt 9):2425-2442.
38. Ko H.S., Lee Y., Shin J.H., Karuppagounder S.S., Gadad B.S., Koleske A.J., et al. Phosphorylation by the c-Abl protein tyrosine kinase inhibits parkin's ubiquitination and protective function. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(38):16691-16696.
39. Katsumata R., Ishigaki S., Katsuno M., Kawai K., Sone J., Huang Z., et al. c-Abl inhibition delays motor neuron degeneration in the G93A mouse, an animal model of amyotrophic lateral sclerosis. PLoS One 2012, 7(9).
40. Schlatterer S.D., Tremblay M.A., Acker C.M., Davies P. Neuronal c-Abl overexpression leads to neuronal loss and neuroinflammation in the mouse forebrain. J. Alzheimers Dis. 2011, 25(1):119-133.
41. Tsai S.C., Seto E. Regulation of histone deacetylase 2 by protein kinase CK2. J. Biol. Chem. 2002, 277(35):31826-31833.
42. Marin T., Contreras P., Castro J.F., Chamorro D., Balboa E., Bosch-Morato M., et al. Vitamin E dietary supplementation improves neurological symptoms and decreases c-Abl/p73 activation in Niemann-Pick C mice. Nutrients 2014, 6(8):3000-3017.
43. Yevenes L.F., Klein A., Castro J.F., Marin T., Leal N., Leighton F., et al. Lysosomal vitamin E accumulation in Niemann-Pick type C disease. Biochim. Biophys. Acta 2012, 1822(2):150-160.
44. Francis Y.I., Fa M., Ashraf H., Zhang H., Staniszewski A., Latchman D.S., et al. Dysregulation of histone acetylation in the APP/PS1 mouse model of Alzheimer's disease. J. Alzheimers Dis. 2009, 18(1):131-139.
45. Govindarajan N., Agis-Balboa R.C., Walter J., Sananbenesi F., Fischer A. Sodium butyrate improves memory function in an Alzheimer's disease mouse model when administered at an advanced stage of disease progression. J. Alzheimers Dis. 2011, 26(1):187-197.
46. Kilgore M., Miller C.A., Fass D.M., Hennig K.M., Haggarty S.J., Sweatt J.D., et al. Inhibitors of class 1 histone deacetylases reverse contextual memory deficits in a mouse model of Alzheimer's disease. Neuropsychopharmacology 2010, 35(4):870-880.
47. Ricobaraza A., Cuadrado-Tejedor M., Perez-Mediavilla A., Frechilla D., Del Rio J., Garcia-Osta A. Phenylbutyrate ameliorates cognitive deficit and reduces tau pathology in an Alzheimer's disease mouse model. Neuropsychopharmacology 2009, 34(7):1721-1732.
48. Nunes M.J., Moutinho M., Gama M.J., Rodrigues C.M., Rodrigues E. Histone deacetylase inhibition decreases cholesterol levels in neuronal cells by modulating key genes in cholesterol synthesis, uptake and efflux. PLoS One 2013, 8(1).
49. Graff J., Tsai L.H. The potential of HDAC inhibitors as cognitive enhancers. Annu. Rev. Pharmacol. Toxicol. 2013, 53:311-330.
50. Yang X.J., Seto E. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat. Rev. Mol. Cell Biol. 2008, 9(3):206-218.
51. Brigman J.L., Feyder M., Saksida L.M., Bussey T.J., Mishina M., Holmes A. Impaired discrimination learning in mice lacking the NMDA receptor NR2A subunit. Learn. Mem. 2008, 15(2):50-54.
52. Zhou R., Holmes A., Du J., Malkesman O., Yuan P., Wang Y., et al. Genome-wide gene expression profiling in GluR1 knockout mice: key role of the calcium signaling pathway in glutamatergically mediated hippocampal transmission. Eur. J. Neurosci. 2009, 30(12):2318-2326.
53. Vazquez M.C., del Pozo T., Robledo F.A., Carrasco G., Pavez L., Olivares F., et al. Alteration of gene expression profile in Niemann-Pick type C mice correlates with tissue damage and oxidative stress. PLoS One 2011, 6(12).
54. Kaech S., Banker G. Culturing hippocampal neurons. Nat. Protoc. 2006, 1(5):2406-2415.
55. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29(9).