BimEL as a possible molecular link between proteasome dysfunction and cell death induced by mutant huntingtin

European Journal of Neuroscience

Volumn 31, Issue 11, 2010, Pages 1915-1925

  Leon, Rebecca ^a   Bhagavatula, Nithya ^a   Ulukpo, Onome ^a   McCollum, Mark ^a   Wei, Jianning ^a  

^a FLORIDA ATLANTIC UNIVERSITY   (United States)

Author keywords

BimEL; Huntington's disease; Mice; Phosphorylation; Protein degradation; Ubiquitin proteasome system

Indexed keywords

BIM PROTEIN; HUNTINGTIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BAX; STRESS ACTIVATED PROTEIN KINASE; APOPTOSIS REGULATORY PROTEIN; BCL-2-LIKE PROTEIN 11; HUNTINGTON PROTEIN, MOUSE; MEMBRANE PROTEIN; NERVE PROTEIN; NUCLEAR PROTEIN; ONCOPROTEIN; PROTEASOME; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CONTROLLED STUDY; HUNTINGTON CHOREA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; ANIMAL; C57BL MOUSE; CBA MOUSE; CELL LINE; DISEASE MODEL; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; GENETICS; HUMAN; METABOLISM; MITOCHONDRION; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; CELL DEATH; CELL LINE; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; HUNTINGTON DISEASE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, TRANSGENIC; MITOCHONDRIA; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS; RNA, SMALL INTERFERING;

EID: 77953213749     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07215.x     Document Type: Article

References (47)

1. Apostol, B.L., Illes, K., Pallos, J., Bodai, L., Wu, J., Strand, A., Schweitzer, E.S., Olson, J.M., Kazantsev, A., Marsh, J.L. Thompson, L.M. (2006) Mutant huntingtin alters MAPK signaling pathways in PC12 and striatal cells: ERK1/2 protects against mutant huntingtin-associated toxicity. Hum. Mol. Genet., 15, 273 285.
2. Becker, E.B.E., Howell, J., Kodama, Y., Barker, P.A. Bonni, A. (2004) Characterization of the c-Jun N-terminal kinase-BimEL signaling pathway in neuronal apoptosis. J. Neurosci., 24, 8762 8770.
3. Bence, N.F., Sampat, R.M. Kopito, R.R. (2001) Impairment of the ubiquitin-proteasome system by protein aggregation. Sci. STKE, 292, 1552 1555.
4. Bennett, E., Bence, N., Jayakumar, R. Kopito, R. (2005) Global impairment of the ubiquitin-proteasome system by nuclear or cytoplasmic protein aggregates precedes inclusion body formation. Mol. Cell, 17, 351 365.
5. Bennett, E.J., Shaler, T.A., Woodman, B., Ryu, K.Y., Zaitseva, T.S., Becker, C.H., Bates, G.P., Schulman, H. Kopito, R.R. (2007) Global changes to the ubiquitin system in Huntington's disease. Nature, 448, 704 708.
6. Bett, J., Goellner, G., Woodman, B., Pratt, G., Rechsteiner, M. Bates, G. (2006) Proteasome impairment does not contribute to pathogenesis in R6/2 Huntington's disease mice: exclusion of proteasome activator REG as a therapeutic target. Hum. Mol. Genet., 15, 33 44.
7. Biagioli, M., Pifferi, S., Ragghianti, M., Bucci, S., Rizzuto, R. Pinton, P. (2008) Endoplasmic reticulum stress and alteration in calcium homeostasis are involved in cadmium-induced apoptosis. Cell Calcium, 43, 184 195.
8. Biswas, S.C., Shi, Y., Vonsattel, J.P.G., Leung, C.L., Troy, C.M. Greene, L.A. (2007) Bim is elevated in Alzheimer's disease neurons and is required for β-amyloid-induced neuronal apoptosis. J. Neurosci., 27, 893 900.
9. Cornett, J., Cao, F., Wang, C.-E., Ross, C.A., Bates, G.P., Li, S.-H. Li, X.-J. (2005) Polyglutamine expansion of huntingtin impairs its nuclear export. Nat. Genet., 37, 198 204.
10. Diaz-Hernandez, M., Hernandez, F., Martin-Aparicio, E., Gomez-Ramos, P., Moran, M., Castano, J., Ferrer, I., Avila, J. Lucas, J. (2003) Neuronal induction of the immunoproteasome in Huntington's disease. J. Neurosci., 23, 11653 11661.
11. DiFiglia, M., Sapp, E., Chase, K.O., Davies, S.W., Bates, G.P., Vonsattel, J.P. Aronin, N. (1997) Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science, 277, 1990 1993.
12. Garcia-Martinez, J.M., Perez-Navarro, E., Xifro, X., Canals, J.M., Diaz-Hernandez, M., Trioulier, Y., Brouillet, E., Lucas, J.J. Alberch, J. (2007) BH3-only proteins Bid and Bim (EL) are differentially involved in neuronal dysfunction in mouse models of Huntington's disease. J. Neurosci. Res., 85, 2756 2769.
13. Gilley, J., Coffer, P.J. Ham, J. (2003) FOXO transcription factors directly activate bim gene expression and promote apoptosis in sympathetic neurons. J. Cell Biol., 162, 613 622.
14. Hickey, M.A. Chesselet, M.F. (2003) Apoptosis in Huntington's disease. Prog. Neuropsychopharmacol. Biol. Psychiatry, 27, 255 265.
15. Huang, D. Strasser, A. (2000) BH3-only proteins-ssential initiators of apoptotic cell death. Cell, 103, 839 842.
16. Hubner, A., Barrett, T., Flavell, R.A. Davis, R.J. (2008) Multisite phosphorylation regulates Bim stability and apoptotic activity. Mol. Cell, 30, 415 425.
17. Iwata, A., Christianson, J.C., Bucci, M., Ellerby, L.M., Nukina, N., Forno, L.S. Kopito, R.R. (2005) Increased susceptibility of cytoplasmic over nuclear polyglutamine aggregates to autophagic degradation. Proc. Natl. Acad. Sci. USA, 102, 13135 13140.
18. Jana, N.R., Zemskov, E.A., Wang, G. Nukina, N. (2001) Altered proteasomal function due to the expression of polyglutamine-expanded truncated N-terminal huntingtin induces apoptosis by caspase activation through mitochondrial cytochrome c release. Hum. Mol. Genet., 10, 1049 1059.
19. King, M., Goemans, C., Hafiz, F., Prehn, J., Wyttenbach, A. Tolkovsky, A. (2008) Cytoplasmic inclusions of Htt Exon1 containing an expanded polyglutamine tract suppress execution of apoptosis in sympathetic neurons. J. Neurosci., 28, 14401 14415.
20. Kong, P.J., Kil, M.O., Lee, H., Kim, S.S., Johnson, G.V. Chun, W. (2009) Increased expression of Bim contributes to the potentiation of serum deprivation-induced apoptotic cell death in Huntington inverted exclamation mark s disease knock-in striatal cell line. Neurol. Res., 31, 77 83.
21. Krobitsch, S. Lindquist, S. (2000) Aggregation of huntingtin in yeast varies with the length of the polyglutamine expansion and the expression of chaperone proteins. Proc. Natl. Acad. Sci. USA, 97, 1589 1594.
22. Lam, Y.A., Pickart, C.M., Alban, A., Landon, M., Jamieson, C., Ramage, R., Mayer, R.J. Layfield, R. (2000) Inhibition of the ubiquitin-proteasome system in Alzheimer's disease. Proc Natl Acad Sci USA, 97, 9902 9906.
23. Lei, K. Davis, R.J. (2003) JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc. Natl. Acad. Sci. USA, 100, 2432 2437.
24. Ley, R., Ewings, K.E., Hadfield, K., Howes, E., Balmanno, K. Cook, S.J. (2004) Extracellular signal-regulated kinases 1/2 are serum-stimulated "Bim(EL) kinases" that bind to the BH3-only protein Bim(EL) causing its phosphorylation and turnover. J. Biol. Chem., 279, 8837 8847.
25. Ley, R., Ewings, K.E., Hadfield, K. Cook, S.J. (2005) Regulatory phosphorylation of Bim: sorting out the ERK from the JNK. Cell Death Differ., 12, 1008 1014.
26. Li, H., Zhu, H., Xu, C. Yuan, J. (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell, 94, 491 502.
27. Li, H., Li, S.H., Johnston, H., Shelbourne, P.F. Li, X.J. (2000a) Amino-terminal fragments of mutant huntingtin show selective accumulation in striatal neurons and synaptic toxicity. Nat. Genet., 25, 385 389.
28. Li, S.H., Lam, S., Cheng, A.L. Li, X.J. (2000b) Intranuclear huntingtin increases the expression of caspase-1 and induces apoptosis. Hum. Mol. Genet., 9, 2859 2867.
29. Luciano, F., Jacquel, A., Colosetti, P., Herrant, M., Cagnol, S., Pages, G. Auberger, P. (2003) Phosphorylation of Bim-EL by Erk1/2 on serine 69 promotes its degradation via the proteasome pathway and regulates its proapoptotic function. Oncogene, 22, 6785 6793.
30. Luo, X., Budihardjo, I., Zou, H., Slaughter, C. Wang, X. (1998) Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell, 94, 481 490.
31. McNaught, K.S.P., Olanow, C.W., Halliwell, B., Isacson, O. Jenner, P. (2001) Opinion: Failure of the ubiquitin-proteasome system in Parkinson's disease. Nat. Rev. Neurosci., 2, 589 594.
32. Mullen, P. (2004) PARP cleavage as a means of assessing apoptosis. Methods Mol. Med., 88, 171 182.
33. Nishitoh, H., Matsuzawa, A., Tobiume, K., Saegusa, K., Takeda, K., Inoue, K., Hori, S., Kakizuka, A. Ichijo, H. (2002) ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev., 16, 1345 1355.
34. Oliver, F.J., de la Rubia, G., Rolli, V., Ruiz-Ruiz, M.C., de Murcia, G. Murcia, J.M (1998) Importance of poly(ADP-ribose) polymerase and its cleavage in apoptosis. Lesson from an uncleavable mutant. J. Biol. Chem., 273, 33533 33539. (Pubitemid 29005737)
35. O'Reilly, L.A., Cullen, L., Visvader, J., Lindeman, G.J., Print, C., Bath, M.L., Huang, D.C.S. Strasser, A. (2000) The proapoptotic BH3-only protein Bim is expressed in hematopoietic, epithelial, neuronal, and germ cells. Am. J. Pathol., 157, 449 461.
36. Perier, C., Bove, J., Wu, D.-C., Dehay, B., Choi, D.-K., Jackson-Lewis, V., Rathke-Hartlieb, S., Bouillet, P., Strasser, A., Schulz, J.B., Przedborski, S. Vila, M. (2007) Two molecular pathways initiate mitochondria-dependent dopaminergic neurodegeneration in experimental Parkinson's disease. Proc. Natl. Acad. Sci. USA, 104, 8161 8166.
37. de Pril, R., Fischer, D.F., Maat-Schieman, M.L.C., Hobo, B., de Vos, R.A.I., Brunt, E.R., Hol, E.M., Roos, R.A.C. van Leeuwen, F.W. (2004) Accumulation of aberrant ubiquitin induces aggregate formation and cell death in polyglutamine diseases. Hum. Mol. Genet., 13, 1803 1813.
38. Putcha, G.V., Moulder, K.L., Golden, J.P., Bouillet, P., Adams, J.A., Strasser, A. Johnson, E.M. (2001) Induction of BIM, a proapoptotic BH3-Only BCL-2 family member, is critical for neuronal apoptosis. Neuron, 29, 615 628.
39. Putcha, G.V., Le, S., Frank, S., Besirli, C.G., Clark, K., Chu, B., Alix, S., Youle, R.J., LaMarche, A. Maroney, A.C. (2003) JNK-mediated BIM phosphorylation potentiates BAX-dependent apoptosis. Neuron, 38, 899 914.
40. Puthalakath, H., Huang, D.C.S., O'Reilly, L.A., King, S.M. Strasser, A. (1999) The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol. Cell, 3, 287 296.
41. Puthalakath, H., O'Reilly, L.A., Gunn, P., Lee, L., Kelly, P.N., Huntington, N.D., Hughes, P.D., Michalak, E.M., McKimm-Breschkin, J. Motoyama, N. (2007) ER stress triggers apoptosis by activating BH3-only protein Bim. Cell, 129, 1337 1349.
42. Senut, M.C., Suhr, S.T., Kaspar, B. Gage, F.H. (2000) Intraneuronal aggregate formation and cell death after viral expression of expanded polyglutamine tracts in the adult rat brain. J. Neurosci., 20, 219 229.
43. Turmaine, M., Raza, A., Mahal, A., Mangiarini, L., Bates, G.P. Davies, S.W. (2000) Nonapoptotic neurodegeneration in a transgenic mouse model of Huntington's disease. Proc. Natl Acad. Sci. USA, 97, 8093 8097.
44. Verhoef, L.G.G.C., Lindsten, K., Masucci, M.G. Dantuma, N.P. (2002) Aggregate formation inhibits proteasomal degradation of polyglutamine proteins. Hum. Mol. Genet., 11, 2689 2700.
45. Wang, J., Wang, C.-E., Orr, A., Tydlacka, S., Li, S.-H. Li, X.-J. (2008) Impaired ubiquitin-proteasome system activity in the synapses of Huntington's disease mice. J. Cell Biol., 180, 1177 1189.
46. Yin, X., Wang, K., Gross, A., Zhao, Y., Zinkel, S., Klocke, B., Roth, K. Korsmeyer, S. (1999) Bid-deficient mice are resistant to Fas-induced hepatocellular apoptosis. Nature, 400, 886 891.
47. Zhang, Y., Ona, V., Li, M., Drozda, M. Dubois-Dauphin, M. (2003) Sequential activation of individual caspases, and of alterations in Bcl-2 proapoptotic signals in a mouse model of Huntington's disease. J. Neurochem., 87, 1184 1192.