Transcriptional repression induces a slowly progressive atypical neuronal death associated with changes of YAP isoforms and p73

Journal of Cell Biology

Volumn 172, Issue 4, 2006, Pages 589-604

  Hoshino, Masataka ^a   Qi, Mei Ling ^a   Yoshimura, Natsue ^a   Miyashita, Tomoyuki ^b   Tagawa, Kazuhiko ^a   Wada, Yo Ichi ^a   Enokido, Yasushi ^a   Marubuchi, Shigeki ^a   Harjes, Phoebe ^c   Arai, Nobutaka ^b   Oyanagi, Kiyomitsu ^b   Blandino, Giovanni ^d   Sudol, Marius ^e   Rich, Tina ^f   Kanazawa, Ichiro ^g   Wanker, Erich E ^c   Saitoe, Minoru ^b   Okazawa, Hitoshi ^a,b,h  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^d REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^e WEIS CENTER FOR RESEARCH   (United States)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^g NATIONAL INSTITUTE OF MENTAL HEALTH   (Japan)

^h JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HUNTINGTIN; ISOPROTEIN; PROTEIN; PROTEIN P73; UNCLASSIFIED DRUG; YES ASSOCIATED PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATTENUATION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EMBRYO; GENE EXPRESSION PROFILING; HUMAN; HUMAN TISSUE; HUNTINGTON CHOREA; MOUSE; NERVE CELL NECROSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; STRIATE CORTEX; TRANSCRIPTION REGULATION; TRANSGENIC MOUSE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMANITINS; AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS REGULATORY PROTEINS; CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; DOWN-REGULATION; DROSOPHILA MELANOGASTER; EMBRYO RESEARCH; GENES, TUMOR SUPPRESSOR; HUMANS; HUNTINGTON DISEASE; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; NEURONS; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PROTEIN ISOFORMS; RATS; RNA, SMALL INTERFERING; TIME FACTORS; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

ANIMALIA; DROSOPHILA MELANOGASTER; MUS MUSCULUS;

EID: 32644436068     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200509132     Document Type: Article

References (48)

1. Bae, B.-I.I., H. Xu, S. Igarashi, M. Fujimoto, N. Agrawal, Y. Taya, S.D. Hayward, T.H. Morgan, C. Montell, C.A. Ross, et al. 2005. p53 mediates cellular dysfunction and behavioral abnormalities in Huntington's disease. Neuron. 47:29-41.
2. Basu, S., N.F. Totty, M.S. Irwin, M. Sudol, and J. Downward. 2003. Akt phosphorylates the Yes-associated protein, YAP, to induce interaction with 14-3-3 and attenuation of p73-mediated apoptosis. Mol. Cell. 11:11-23.
3. Bates, G. 2003. Huntingtin aggregation and toxicity in Huntington's disease. Lancet. 361:1642-1644.
4. Bushnell, D.A., P. Cramer, and R.D. Kornberg. 2002. Structural basis of transcription: alpha-amanitin-RNA polymerase II cocrystal at 2.8 A resolution. Proc. Natl. Acad. Sci. USA. 99:1218-1222.
5. Clarke, P.G. 1990. Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. (Berl.). 181:195-213.
6. Cramer, P., D.A. Bushnell, and R.D. Kornberg. 2001. Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution. Science. 292:1863-1876.
7. Cornillon, S., C. Foa, J. Davoust, N. Buonavista, J.D. Gross, and P. Goldstein. 1994. Programmed cell death in Dictyostelium. J. Cell Sci. 107:2691-2704.
8. Degterev, A., Z. Huang, M. Boyce, Y. Li, P. Jagtap, N. Mizushima, G.D. Cuny, T.J. Mitchison, M.A. Moskowitz, and J. Yuan. 2005. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 1:112-119.
9. Dura, J.M., T. Preat, and T. Tully. 1993. Identification of linotte, a new gene affecting learning and memory in Drosophila melanogaster. J. Neurogenet. 9:1-14.
10. Gusella, J.F., and M.E. MacDonald. 2000. Molecular genetics: unmasking polyglutamine triggers in neurodegenerative disease. Nat. Rev. Neurosci. 1:109-115.
11. Hirabayashi, M., K. Inoue, K. Tanaka, K. Nakadate, Y. Ohsawa, Y. Kamei, A.H. Popiel, A. Sinohara, A. Iwamatsu, Y. Kimura, et al. 2001. VCP/p97 in abnormal protein aggregates, cytoplasmic vacuoles, and cell death, phenotypes relevant to neurodegeneration. Cell Death Differ. 8:977-984.
12. Hoshino, M., K. Tagawa, T. Okuda, and H. Okazawa. 2004. General transcriptional repression by polyglutamine disease proteins is not directly linked to the presence of inclusion bodies. Biochem. Biophys. Res. Commun. 313:110-116.
13. Irwin, M.S., and F.D. Miller. 2004. p73: regulator in cancer and neural development. Cell Death Differ. 11:S17-S22.
14. Iwata, A., J.C. Christianson, M. Bucci, L.M. Ellerby, N. Nukina, L.S. Forno, and R.R. Kopito. 2005. Increased susceptibility of cytoplasmic over nuclear polyglutamine aggregates to autophagic degradation. Proc. Natl. Acad. Sci. USA. 102:13135-13140.
15. Jackson, G.R., I. Salecker, X. Dong, X. Yao, N. Arnheim, P.W. Faber, M.E. MacDonald, and S.L. Zipursky. 1998. Polyglutamine-expanded human huntingtin transgenes induce degeneration of Drosophila photoreceptor neurons. Neuron. 21:633-642.
16. Jones, G.H. 1976. RNA synthesis in Streptomyces antibiotics: in vitro effects of actinomycin and transcriptional inhibitors from 48-h cells. Biochemistry. 15:3331-3341.
17. Kabeya, Y., N. Mizushima, T. Ueno, A. Yamamoto, T. Kirisako, T. Noda, E. Kominami, Y. Ohsumi, and T. Yoshimori. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19:5720-5728.
18. Katsuno, M., H. Adachi, M. Doyu, M. Minamiyama, C. Sang, Y. Kobayashi, A. Inukai, and G. Sobue. 2003. Leuprorelin rescues polyglutamine-dependent phenotypes in a transgenic mouse model of spinal and bulbar muscular atrophy. Nat. Med. 9:768-773.
19. Kegel, K.B., M. Kim, E. Sapp, C. McIntyre, J.G. Castano, N. Aronin, and M. Difiglia. 2000. Huntingtin expression stimulates endosomal-lysosomal activity, endosome tubulation, and autophagy. J. Neurosci. 20:7268-7278.
20. Kimura, H., K. Sugaya, and P.R. Cook. 2002. The transcription cycle of RNA polymerase II in living cells. J. Cell Biol. 159:777-782.
21. Klement, I.A., P.J. Skinner, M.D. Kaytor, H. Yi, S.M. Hersch, H.B. Clark, H.Y. Zoghbi, and H.T. Orr. 1998. Ataxin-1 nuclear localization and aggregation: role in polyglutamine-induced disease in SCA1 transgenic mice. Cell. 95:41-53.
22. Klionsky, D.J., and S.D. Emr. 2000. Autophagy as a regulated pathway of cellular degradation. Science. 290:1717-1721.
23. Kouroku, Y., E. Fujita, A. Jimbo, T. Kikuchi, T. Yamagata, M.Y. Momoi, E. Kominami, K. Kuida, K. Sakamaki, S. Yonehara, et al. 2002. Polyglutamine aggregates stimulate ER stress signals and caspase-12 activation. Hum. Mol. Genet. 11:1505-1515.
24. Melino, G., F. Bernassola, M. Ranalli, K. Yee, W.X. Zong, M. Corazzari, R.A. Knight, D.R. Green, C. Thompson, and K.H. Vousden. 2004. p73 Induces apoptosis via PUMA transactivation and Bax mitochondrial translocation. J. Biol. Chem. 279:8076-8083.
25. Mihara, M., S. Erster, A. Zaika, O. Petrenko, T. Chittenden, P. Pancoska, and U.M. Moll. 2003. p53 has a direct apoptogenic roleat the mitochondria. Mol. Cell. 11:577-590.
26. Nagata, E., A. Sawa, C.A. Ross, and S.H. Snyder. 2004. Autophagosome-like vacuole formation in Huntington's disease lymphoblasts. Neuroreport. 15:1325-1328.
27. Ni, Z., B.E. Schwartz, J. Werner, J.R. Suarez, and J.T. Lis. 2004. Coordination of transcription, RNA processing, and surveillance by P-TEFb kinase on heat shock genes. Mol. Cell. 13:55-65.
28. Nishitoh, H., A. Matsuzawa, K. Tobiume, K. Saegusa, K. Takeda, K. Inoue, S. Hori, A. Kakizuka, and H. Ichijo. 2002. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev. 16:1345-1355.
29. Okazawa, H. 2003. Polyglutamine diseases: a transcription disorder? Cell. Mol. Life Sci. 60:1427-1439.
30. Okazawa, H., J. Shimizu, M. Kamei, I. Imafuku, H. Hamada, and I. Kanazawa. 1996. Bcl-2 inhibits retinoic acid-induced apoptosis during the neural differentiation of embryonal stem cells. J. Cell Biol. 132:955-968.
31. Okazawa, H., T. Rich, A. Chang, X. Lin, M. Waragai, M. Kajikawa, Y. Enokido, A. Komuro, S. Kato, M. Shibata, et al. 2002. Interaction between mutant ataxin-1 and PQBP-1 affects transcription and cell death. Neuron. 34:701-713.
32. Ravikumar, B., C. Vacher, Z. Berger, J.E. Davies, S. Luo, L.G. Oroz, F. Scaravilli, D.F. Easton, R. Duden, C.J. O'Kane, and D.C. Rubinsztein. 2004. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington's disease. Nat. Genet. 36:585-595.
33. Ross, C.A. 2002. Polyglutamine pathogenesis: emergence of unifying mechanisms for Huntington's disease and related disorders. Neuron. 35:819-822.
34. Rubin, G.M., and A.C. Spradling. 1982. Genetic transformation of Drosophila with transposable element vectors. Science. 218:348-353.
35. Sapp, E., C. Schwarz, K. Chase, P.G. Bhide, A.B. Young, J. Penny, J.P. Vonsattel, N. Aronin, and M. Difiglia. 1997. Huntingtin localization in brains of normal and Huntington's disease patients. Ann. Neurol. 42:604-612.
36. Saudou, F., S. Finkbeiner, D. Devys, and M.E. Greenberg. 1998. Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell. 95:55-66.
37. Schweichel, J.U., and H.J. Merker. 1973. The morphology of various types of cell death in prenatal tissues. Teratology. 7:253-266.
38. Sperandio, S., I. de Belle, and D.E. Bredesen. 2000. An alternative nonapoptotic form of programmed cell death. Proc. Natl. Acad. Sci. USA. 97:14376-14381.
39. Steffan, J.S., A. Kazantsev, O. Spasic-Boskovic, M. Greenwald, Y.Z. Zhu, H. Gohler, E.E. Wanker, G.P. Bates, D.E. Houseman, and L.M. Thompson. 2000. The Huntington's disease protein interacts with p53 and CREB-binding protein and represses transcription. Proc. Natl. Acad. Sci. USA. 97:6763-6768.
40. Strano, S., G. Fontemaggi, A. Costanzo, M.G. Rizzo, O. Monti, A. Baccarini, G. DelSal, M. Levrero, A. Sacchi, M. Oren, and G. Blandino. 2002. Physical interaction with human tumor-derived p53 mutants inhibits p63 activities. J. Biol. Chem. 277:18817-18826.
41. Sudol, M., H.I. Chen, C. Bougeret, A. Einbond, and P. Bork. 1995. Characterization of a novel protein-binding module - the WW domain. FEBS Lett. 369:67-71.
42. Sugars, K.L., and D.C. Rubinsztein. 2003. Transcriptional abnormalities in Huntington disease. Trends Genet. 19:233-238.
43. Tagawa, K., M. Hoshino, T. Okuda, H. Ueda, H. Hayashi, S. Engemann, H. Okado, M. Ichikawa, E.E. Wanker, and H. Okazawa. 2004. Distinct aggregation and cell death patterns among different types of primary neurons induced by mutant huntingtin protein. J. Neurochem. 89:974-987.
44. Taylor, J.P., J. Hardy, and K.H. Fischbeck. 2002. Toxic proteins in neurodegenerative disease. Science. 296:1991-1995.
45. Terrinoni, A., M. Ranalli, B. Cadot, A. Leta, G. Bagetta, K.H. Vousden, and G. Melino. 2004. p73-alpha is capable of inducing scotin and ER stress. Oncogene. 23:3721-3725.
46. Wyllie, A.H., and P. Goldstein. 2001. More than one way to go. Proc. Natl. Acad. Sci. USA. 98:11-13.
47. Yagi, R., L.-F. Chen, K. Shigesada, Y. Murakami, and Y. Ito. 1999. A WW domain-containing Yes-associated protein (YAP) is a novel transcription co-activator. EMBO J. 18:2551-2562.
48. Zoghbi, H.Y., and H.T. Orr. 2000. Glutamine repeats and neurodegeneration. Annu. Rev. Neurosci. 23:217-247.