Suppression of aggregate formation of mutant huntingtin potentiates CREB-binding protein sequestration and apoptotic cell death

Molecular and Cellular Neuroscience

Volumn 49, Issue 2, 2012, Pages 127-137

  Choi, Yong Joon ^a   Kim, Song In ^a   Lee, Jae Won ^a   Kwon, Yong Soo ^a   Lee, Hee Jae ^a   Kim, Sung Soo ^a   Chun, Wanjoo ^a  

^a Kangwon National University   (South Korea)

Author keywords

Aggregation; Apoptosis; CREB binding protein; Huntington's disease; Peroxisome proliferator activated receptor coactivator 1 ; Polyglutamine

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; HUNTINGTIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; YELLOW FLUORESCENT PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; EXON; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION;

APOPTOSIS; CELL LINE; CREB-BINDING PROTEIN; EXONS; GREEN FLUORESCENT PROTEINS; HEAT-SHOCK PROTEINS; HUMANS; HUNTINGTON DISEASE; MUTATION; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 83755228990     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2011.11.003     Document Type: Article

References (52)

1. Aiken C.T., Steffan J.S., Guerrero C.M., Khashwji H., Lukacsovich T., Simmons D., Purcell J.M., Menhaji K., Zhu Y.Z., Green K., Laferla F., Huang L., Thompson L.M., Marsh J.L. Phosphorylation of threonine 3: implications for Huntingtin aggregation and neurotoxicity. J. Biol. Chem. 2009, 284:29427-29436.
2. Alba M.M., Guigo R. Comparative analysis of amino acid repeats in rodents and humans. Genome Res. 2004, 14:549-554.
3. Arrasate M., Mitra S., Schweitzer E.S., Segal M.R., Finkbeiner S. Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 2004, 431:805-810.
4. Bae B.I., Xu H., Igarashi S., Fujimuro M., Agrawal N., Taya Y., Hayward S.D., Moran T.H., Montell C., Ross C.A., Snyder S.H., Sawa A. p53 mediates cellular dysfunction and behavioral abnormalities in Huntington's disease. Neuron 2005, 47:29-41.
5. Becher M.W., Kotzuk J.A., Sharp A.H., Davies S.W., Bates G.P., Price D.L., Ross C.A. Intranuclear neuronal inclusions in Huntington's disease and dentatorubral and pallidoluysian atrophy: correlation between the density of inclusions and IT15 CAG triplet repeat length. Neurobiol. Dis. 1998, 4:387-397.
6. Bossy-Wetzel E., Petrilli A., Knott A.B. Mutant huntingtin and mitochondrial dysfunction. Trends Neurosci. 2008, 31:609-616.
7. Buttler K., Kreysing A., von Kaisenberg C.S., Schweigerer L., Gale N., Papoutsi M., Wilting J. Mesenchymal cells with leukocyte and lymphendothelial characteristics in murine embryos. Dev. Dyn. 2006, 235:1554-1562.
8. Cha J.H. Transcriptional dysregulation in Huntington's disease. Trends Neurosci. 2000, 23:387-392.
9. Cha J.H. Transcriptional signatures in Huntington's disease. Prog. Neurobiol. 2007, 83:228-248.
10. Chen M., Ona V.O., Li M., Ferrante R.J., Fink K.B., Zhu S., Bian J., Guo L., Farrell L.A., Hersch S.M., Hobbs W., Vonsattel J.P., Cha J.H., Friedlander R.M. Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease. Nat. Med. 2000, 6:797-801.
11. Ciechanover A. The ubiquitin proteolytic system and pathogenesis of human diseases: a novel platform for mechanism-based drug targeting. Biochem. Soc. Trans. 2003, 31:474-481.
12. Ciechanover A., Brundin P. The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron 2003, 40:427-446.
13. Cong S.Y., Pepers B.A., Evert B.O., Rubinsztein D.C., Roos R.A., van Ommen G.J., Dorsman J.C. Mutant huntingtin represses CBP, but not p300, by binding and protein degradation. Mol. Cell. Neurosci. 2005, 30:560-571.
14. Cui L., Jeong H., Borovecki F., Parkhurst C.N., Tanese N., Krainc D. Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cell 2006, 127:59-69.
15. Cummings C.J., Orr H.T., Zoghbi H.Y. Progress in pathogenesis studies of spinocerebellar ataxia type 1. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1999, 354:1079-1081.
16. Davies S.W., Turmaine M., Cozens B.A., DiFiglia M., Sharp A.H., Ross C.A., Scherzinger E., Wanker E.E., Mangiarini L., Bates G.P. Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 1997, 90:537-548.
17. Dunah A.W., Jeong H., Griffin A., Kim Y.M., Standaert D.G., Hersch S.M., Mouradian M.M., Young A.B., Tanese N., Krainc D. Sp1 and TAFII130 transcriptional activity disrupted in early Huntington's disease. Science 2002, 296:2238-2243.
18. Gunawardena S., Goldstein L.S. Polyglutamine diseases and transport problems: deadly traffic jams on neuronal highways. Arch. Neurol. 2005, 62:46-51.
19. Gunawardena S., Her L.S., Brusch R.G., Laymon R.A., Niesman I.R., Gordesky-Gold B., Sintasath L., Bonini N.M., Goldstein L.S. Disruption of axonal transport by loss of huntingtin or expression of pathogenic polyQ proteins in Drosophila. Neuron 2003, 40:25-40.
20. Gutekunst C.A., Li S.H., Yi H., Mulroy J.S., Kuemmerle S., Jones R., Rye D., Ferrante R.J., Hersch S.M., Li X.J. Nuclear and neuropil aggregates in Huntington's disease: relationship to neuropathology. J. Neurosci. 1999, 19:2522-2534.
21. Hackam A.S., Yassa A.S., Singaraja R., Metzler M., Gutekunst C.A., Gan L., Warby S., Wellington C.L., Vaillancourt J., Chen N., Gervais F.G., Raymond L., Nicholson D.W., Hayden M.R. Huntingtin interacting protein 1 induces apoptosis via a novel caspase-dependent death effector domain. J. Biol. Chem. 2000, 275:41299-41308.
22. Jiang H., Poirier M.A., Liang Y., Pei Z., Weiskittel C.E., Smith W.W., DeFranco D.B., Ross C.A. Depletion of CBP is directly linked with cellular toxicity caused by mutant huntingtin. Neurobiol. Dis. 2006, 23:543-551.
23. Jin Y.N., Johnson G.V. The interrelationship between mitochondrial dysfunction and transcriptional dysregulation in Huntington disease. J. Bioenerg. Biomembr. 2010, 42:199-205.
24. Kim M., Lee H.S., LaForet G., McIntyre C., Martin E.J., Chang P., Kim T.W., Williams M., Reddy P.H., Tagle D., Boyce F.M., Won L., Heller A., Aronin N., DiFiglia M. Mutant huntingtin expression in clonal striatal cells: dissociation of inclusion formation and neuronal survival by caspase inhibition. J. Neurosci. 1999, 19:964-973.
25. Klement I.A., Skinner P.J., Kaytor M.D., Yi H., Hersch S.M., Clark H.B., Zoghbi H.Y., Orr H.T. Ataxin-1 nuclear localization and aggregation: role in polyglutamine-induced disease in SCA1 transgenic mice. Cell 1998, 95:41-53.
26. Kuemmerle S., Gutekunst C.A., Klein A.M., Li X.J., Li S.H., Beal M.F., Hersch S.M., Ferrante R.J. Huntington aggregates may not predict neuronal death in Huntington's disease. Ann. Neurol. 1999, 46:842-849.
27. Leavitt B.R., van Raamsdonk J.M., Shehadeh J., Fernandes H., Murphy Z., Graham R.K., Wellington C.L., Raymond L.A., Hayden M.R. Wild-type huntingtin protects neurons from excitotoxicity. J. Neurochem. 2006, 96:1121-1129.
28. Legleiter J., Mitchell E., Lotz G.P., Sapp E., Ng C., DiFiglia M., Thompson L.M., Muchowski P.J. Mutant huntingtin fragments form oligomers in a polyglutamine length-dependent manner in vitro and in vivo. J. Biol. Chem. 2010, 285:14777-14790.
29. Li S.H., Cheng A.L., Zhou H., Lam S., Rao M., Li H., Li X.J. Interaction of Huntington disease protein with transcriptional activator Sp1. Mol. Cell. Biol. 2002, 22:1277-1287.
30. McCampbell A., Taylor J.P., Taye A.A., Robitschek J., Li M., Walcott J., Merry D., Chai Y., Paulson H., Sobue G., Fischbeck K.H. CREB-binding protein sequestration by expanded polyglutamine. Hum. Mol. Genet. 2000, 9:2197-2202.
31. McGill J.K., Beal M.F. PGC-1alpha, a new therapeutic target in Huntington's disease?. Cell 2006, 127:465-468.
32. Muchowski P.J., Ning K., D'Souza-Schorey C., Fields S. Requirement of an intact microtubule cytoskeleton for aggregation and inclusion body formation by a mutant huntingtin fragment. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:727-732.
33. Nucifora F.C., Sasaki M., Peters M.F., Huang H., Cooper J.K., Yamada M., Takahashi H., Tsuji S., Troncoso J., Dawson V.L., Dawson T.M., Ross C.A. Interference by huntingtin and atrophin-1 with cbp-mediated transcription leading to cellular toxicity. Science 2001, 291:2423-2428.
34. Ona V.O., Li M., Vonsattel J.P., Andrews L.J., Khan S.Q., Chung W.M., Frey A.S., Menon A.S., Li X.J., Stieg P.E., Yuan J., Penney J.B., Young A.B., Cha J.H., Friedlander R.M. Inhibition of caspase-1 slows disease progression in a mouse model of Huntington's disease. Nature 1999, 399:263-267.
35. Palmer T.D., Markakis E.A., Willhoite A.R., Safar F., Gage F.H. Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J. Neurosci. 1999, 19:8487-8497.
36. Poirier M.A., Jiang H., Ross C.A. A structure-based analysis of huntingtin mutant polyglutamine aggregation and toxicity: evidence for a compact beta-sheet structure. Hum. Mol. Genet. 2005, 14:765-774.
37. Puigserver P., Spiegelman B.M. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr. Rev. 2003, 24:78-90.
38. Sadri-Vakili G., Menon A.S., Farrell L.A., Keller-McGandy C.E., Cantuti-Castelvetri I., Standaert D.G., Augood S.J., Yohrling G.J., Cha J.H. Huntingtin inclusions do not down-regulate specific genes in the R6/2 Huntington's disease mouse. Eur. J. Neurosci. 2006, 23:3171-3175.
39. Saudou F., Finkbeiner S., Devys D., Greenberg M.E. Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell 1998, 95:55-66.
40. Schaffar G., Breuer P., Boteva R., Behrends C., Tzvetkov N., Strippel N., Sakahira H., Siegers K., Hayer-Hartl M., Hartl F.U. Cellular toxicity of polyglutamine expansion proteins: mechanism of transcription factor deactivation. Mol. Cell 2004, 15:95-105.
41. Scherzinger E., Lurz R., Turmaine M., Mangiarini L., Hollenbach B., Hasenbank R., Bates G.P., Davies S.W., Lehrach H., Wanker E.E. Huntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo. Cell 1997, 90:549-558.
42. Scherzinger E., Sittler A., Schweiger K., Heiser V., Lurz R., Hasenbank R., Bates G.P., Lehrach H., Wanker E.E. Self-assembly of polyglutamine-containing huntingtin fragments into amyloid-like fibrils: implications for Huntington's disease pathology. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:4604-4609.
43. Shimohata T., Nakajima T., Yamada M., Uchida C., Onodera O., Naruse S., Kimura T., Koide R., Nozaki K., Sano Y., Ishiguro H., Sakoe K., Ooshima T., Sato A., Ikeuchi T., Oyake M., Sato T., Aoyagi Y., Hozumi I., Nagatsu T., Takiyama Y., Nishizawa M., Goto J., Kanazawa I., Davidson I., Tanese N., Takahashi H., Tsuji S. Expanded polyglutamine stretches interact with TAFII130, interfering with CREB-dependent transcription. Nat. Genet. 2000, 26:29-36.
44. Sieradzan K.A., Mechan A.O., Jones L., Wanker E.E., Nukina N., Mann D.M. Huntington's disease intranuclear inclusions contain truncated, ubiquitinated huntingtin protein. Exp. Neurol. 1999, 156:92-99.
45. Slow E.J., Graham R.K., Osmand A.P., Devon R.S., Lu G., Deng Y., Pearson J., Vaid K., Bissada N., Wetzel R., Leavitt B.R., Hayden M.R. Absence of behavioral abnormalities and neurodegeneration in vivo despite widespread neuronal huntingtin inclusions. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:11402-11407.
46. Steffan J.S., Kazantsev A., Spasic-Boskovic O., Greenwald M., Zhu Y.Z., Gohler H., Wanker E.E., Bates G.P., Housman D.E., Thompson L.M. The Huntington's disease protein interacts with p53 and CREB-binding protein and represses transcription. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:6763-6768.
47. Sugars K.L., Rubinsztein D.C. Transcriptional abnormalities in Huntington disease. Trends Genet. 2003, 19:233-238.
48. Thomas E.A. Striatal specificity of gene expression dysregulation in Huntington's disease. J. Neurosci. Res. 2006, 84:1151-1164.
49. Walton M.R., Dragunow I. Is CREB a key to neuronal survival?. Trends Neurosci. 2000, 23:48-53.
50. Wellington C.L., Ellerby L.M., Hackam A.S., Margolis R.L., Trifiro M.A., Singaraja R., McCutcheon K., Salvesen G.S., Propp S.S., Bromm M., Rowland K.J., Zhang T., Rasper D., Roy S., Thornberry N., Pinsky L., Kakizuka A., Ross C.A., Nicholson D.W., Bredesen D.E., Hayden M.R. Caspase cleavage of gene products associated with triplet expansion disorders generates truncated fragments containing the polyglutamine tract. J. Biol. Chem. 1998, 273:9158-9167.
51. Weydt P., Pineda V.V., Torrence A.E., Libby R.T., Satterfield T.F., Lazarowski E.R., Gilbert M.L., Morton G.J., Bammler T.K., Strand A.D., Cui L., Beyer R.P., Easley C.N., Smith A.C., Krainc D., Luquet S., Sweet I.R., Schwartz M.W., La Spada A.R. Thermoregulatory and metabolic defects in Huntington's disease transgenic mice implicate PGC-1alpha in Huntington's disease neurodegeneration. Cell Metab. 2006, 4:349-362.
52. Zuccato C., Ciammola A., Rigamonti D., Leavitt B.R., Goffredo D., Conti L., MacDonald M.E., Friedlander R.M., Silani V., Hayden M.R., Timmusk T., Sipione S., Cattaneo E. Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science 2001, 293:493-498.