A functional deficiency of TERA/VCP/p97 contributes to impaired DNA repair in multiple polyglutamine diseases

Nature Communications

Volumn 4, Issue , 2013, Pages

  Fujita, Kyota ^a   Nakamura, Yoko ^a   Oka, Tsutomu ^a   Ito, Hikaru ^a   Tamura, Takuya ^a   Tagawa, Kazuhiko ^a   Sasabe, Toshikazu ^a   Katsuta, Asuka ^a,b   Motoki, Kazumi ^a   Shiwaku, Hiroki ^a   Sone, Masaki ^a,b   Yoshida, Chisato ^a   Katsuno, Masahisa ^c   Eishi, Yoshinobu ^d   Murata, Miho ^e   Paul Taylor, J ^f   Wanker, Erich E ^g   Kono, Kazuteru ^h   Tashiro, Satoshi ^h   Sobue, Gen ^c   La Spada, Albert R ⁱ   Okazawa, Hitoshi ^a   more..

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b TOHO UNIVERSITY   (Japan)

^c NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^e NATIONAL INSTITUTE OF MENTAL HEALTH   (Japan)

^f ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^g MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^h HIROSHIMA UNIVERSITY   (Japan)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; ATAXIN 1; ATAXIN 7; HUNTINGTIN; POLYGLUTAMINE; VALOSIN CONTAINING PROTEIN; ADENOSINE TRIPHOSPHATASE; ATAXIN-1; CDC48 PROTEIN; CELL CYCLE PROTEIN; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; HISTONE; MUTANT PROTEIN; NERVE PROTEIN; NUCLEAR PROTEIN; PEPTIDE; DOUBLE STRANDED DNA; PROTEIN P97; PROTEIN BINDING;

DISEASE PREVALENCE; DNA; ENZYME ACTIVITY; MUTATION; PATHOLOGY; PROTEIN; DISEASE INCIDENCE; FLY; GENE EXPRESSION; NEUROLOGY;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEGENERATIVE DISEASE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; FEMALE; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NERVE CELL; NONHUMAN; PROTEIN INTERACTION; ANIMAL; BRAIN CORTEX; CELL INCLUSION; CELL STRAIN HEK293; DROSOPHILA MELANOGASTER; ENDOPLASMIC RETICULUM; HELA CELL; IMMUNOPRECIPITATION; LONGEVITY; METABOLISM; MOTONEURON; PATHOLOGY; PHENOTYPE; PROTEIN BINDING; PROTEIN TRANSPORT; TRANSGENIC ANIMAL; ANIMAL EXPERIMENT; ANIMAL MODEL; DNA STRAND BREAKAGE; DROSOPHILA; ENZYME ACTIVITY; MULTIPLE POLYGLUTAMINE DISEASE; MUTANT; PROTEIN DEFECT; PROTEIN FUNCTION; DEFICIENCY; HEK293 CELL LINE; HELA CELL LINE;

ADENOSINE TRIPHOSPHATASES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL CYCLE PROTEINS; CEREBRAL CORTEX; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DROSOPHILA MELANOGASTER; ENDOPLASMIC RETICULUM; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HELA CELLS; HISTONES; HUMANS; IMMUNOPRECIPITATION; INCLUSION BODIES; LONGEVITY; MICE; MOTOR NEURONS; MUTANT PROTEINS; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PEPTIDES; PHENOTYPE; PROTEIN BINDING; PROTEIN TRANSPORT;

EID: 84878555942     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2828     Document Type: Article

References (58)

1. Watts, G. D. et al. Inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia is caused by mutant valosin-containing protein. Nat. Genet. 36, 377-381 (2004) (Pubitemid 38437260)
2. Johnson, J. O. et al. Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron 68, 857-864 (2010)
3. Imafuku, I. et al. Polar amino acid-rich sequences bind to polyglutamine tracts. Biochem. Biophys. Res. Commun. 253, 16-20 (1998) (Pubitemid 29015592)
4. Hirabayashi, M. et al. VCP/p97 in abnormal protein aggregates, cytoplasmic vacuoles, and cell death, phenotypes relevant to neurodegeneration. Cell Death Differ. 8, 977-984 (2001) (Pubitemid 32994648)
5. Woodman, P.G. p97, a protein coping with multiple identities. J. Cell Sci. 116, 4283-4290 (2003) (Pubitemid 37369586)
6. Zhang, L., Ashendel, C. L., Becker, G. W. & Morré, D. J. Isolation and characterization of the principal ATPase associated with transitional endoplasmic reticulum of rat liver. J. Cell Biol. 127, 1871-1883 (1994)
7. Rabouille, C., Levine, T. P., Peters, J. M. & Warren, G. An NSF-like ATPase, p97, and NSF mediate cisternal regrowth from mitotic Golgi fragments. Cell 82, 905-914 (1995)
8. Pleasure, I. T., Black, M. M. & Keen, J. H. Valosin-containing protein, VCP, is a ubiquitous clathrin-binding protein. Nature 365, 459-462 (1993) (Pubitemid 23311044)
9. Ye, Y., Shibata, Y., Yun, C., Ron, D. & Rapoport, T. A. A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature 429, 841-847 (2004) (Pubitemid 38843292)
10. Ye, Y., Meyer, H. H. & Rapoport, T. A. The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414, 652-656 (2001) (Pubitemid 33151262)
11. Zhong, X. et al. AAA ATPase p97/valosin-containing protein interacts with gp78, a ubiquitin ligase for endoplasmic reticulum-associated degradation. J. Biol. Chem. 279, 45676-45684 (2004) (Pubitemid 39491556)
12. Kittler, R. et al. An endoribonuclease-prepared siRNA screen in human cells identifies genes essential for cell division. Nature 432, 1036-1040 (2004) (Pubitemid 40052235)
13. Acs, K. et al. The AAA-ATPase VCP/p97 promotes 53BP1 recruitment by removing L3MBTL1 from DNA double-strand breaks. Nat. Struct. Mol. Biol. 18, 1345-1350 (2011)
14. Meerang, M. et al. The ubiquitin-selective segregase VCP/p97 orchestrates the response to DNA double-strand breaks. Nat. Cell. Biol. 13, 1376-1382 (2011)
15. Wo'jcik, C., Yano, M. & DeMartino, G.N. RNA interference of valosincontaining protein (VCP/p97) reveals multiple cellular roles linked to ubiquitin/proteasome-dependent proteolysis. J. Cell Sci. 117, 281-292 (2004) (Pubitemid 38128906)
16. Dalal, S., Rosser, M.F., Cyr, D.M. & Hanson, P.I. Distinct roles for the AAA ATPases NSF and p97 in the secretory pathway. Mol. Biol. Cell 15, 637-648 (2004) (Pubitemid 38146480)
17. Mimnaugh, E. G., Xu, W., Vos, M., Yuan, X. & Neckers, L. Endoplasmic reticulum vacuolization and valosin-containing protein relocalization result from simultaneous hsp90 inhibition by geldanamycin and proteasome inhibition by velcade. Mol. Cancer Res. 4, 667-681 (2006) (Pubitemid 44497219)
18. Ju, J.S. et al. Valosin-containing protein (VCP) is required for autophagy and is disrupted in VCP disease. J. Cell Biol. 187, 875-888 (2009)
19. Weihl, C.C., Miller, S.E., Hanson, P.I. & Pestronk, A. Transgenic expression of inclusion body myopathy associated mutant p97/VCP causes weakness and ubiquitinated protein inclusions in mice. Hum. Mol. Genet. 16, 919-928 (2007) (Pubitemid 47062736)
20. Custer, S.K., Neumann, M., Lu, H., Wright, A.C. & Taylor, J.P. Transgenic mice expressing mutant forms VCP/p97 recapitulate the full spectrum of IBMPFD including degeneration in muscle, brain and bone. Hum. Mol. Genet. 19, 1741-1755 (2010)
21. Badadani, M. et al. VCP associated inclusion body myopathy and paget disease of bone knock-in mouse model exhibits tissue pathology typical of human disease. PLoS One 5, e13183 (2010)
22. Halawani, D. et al. Hereditary inclusion body myopathy-linked p97/VCP mutations in the NH2 domain and the D1 ring modulate p97/VCP ATPase activity and D2 ring conformation. Mol. Cell Biol. 29, 4484-4494 (2009)
23. Manno, A., Noguchi, M., Fukushi, J., Motohashi, Y. & Kakizuka, A. Enhanced ATPase activities as a primary defect of mutant valosin-containing proteins that cause inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia. Genes Cells 15, 911-922 (2010)
24. Koike, M. et al. Valosin-containing protein (VCP) in novel feedback machinery between abnormal protein accumulation and transcriptional suppression. J. Biol. Chem. 285, 21736-21749 (2010)
25. Chai, Y., Shao, J., Miller, V. M., Williams, A. & Paulson, H. L. Live-cell imaging reveals divergent intracellular dynamics of polyglutamine disease proteins and supports a sequestration model of pathogenesis. Proc. Natl Acad. Sci. USA 99, 9310-9315 (2002) (Pubitemid 34764610)
26. Stenoien, D. L., Mielke, M. & Mancini, M. A. Intranuclear ataxin1 inclusions contain both fast- and slow-exchanging components. Nat. Cell Biol. 4, 806-810 (2002) (Pubitemid 35214775)
27. Kim, S., Nollen, E. A., Kitagawa, K., Bindokas, V. P. & Morimoto, R. I. Polyglutamine protein aggregates are dynamic. Nat. Cell Biol. 4, 826-831 (2002)
28. Wheeler, V. C. et al. Length-dependent gametic CAG repeat instability in the Huntington's disease knock-in mouse. Hum. Mol. Genet. 8, 115-122 (1999) (Pubitemid 29039056)
29. Watase, K. et al. A long CAG repeat in the mouse Sca1 locus replicates SCA1 features and reveals the impact of protein solubility on selective neurodegeneration. Neuron 34, 905-919 (2002) (Pubitemid 34722281)
30. Mangiarini, L. et al. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87, 493-506 (1996) (Pubitemid 26374323)
31. La Spada, A. R. et al. Polyglutamine-expanded ataxin-7 antagonizes CRX function and induces cone-rod dystrophy in a mouse model of SCA7. Neuron 31, 913-927 (2001) (Pubitemid 32925279)
32. Katsuno, M. et al. Testosterone reduction prevents phenotypic expression in a transgenic mouse model of spinal and bulbar muscular atrophy. Neuron 35, 843-854 (2002)
33. Fry, W.H., Simion, C., Sweeney, C. & Carraway, K. L. Quantity control of the ErbB3 receptor tyrosine kinase at the endoplasmic reticulum. Mol. Cell Biol. 31, 3009-3018 (2011)
34. Ju, J. S. & Weihl, C. C. Inclusion body myopathy, Paget's disease of the bone and fronto-temporal dementia: a disorder of autophagy. Hum. Mol. Genet. 19, R38-R45 (2010)
35. Tamura, T. et al. Ku70 alleviates neurodegeneration in Drosophila models of Huntington's disease. PLoS One 6, e27408 (2011)
36. Qi, M. L. et al. Proteome analysis of soluble nuclear proteins reveals that HMGB1/2 suppress genotoxic stress in polyglutamine diseases. Nat. Cell Biol. 9, 402-414 (2007)
37. Enokido, Y. et al. Mutant huntingtin impairs Ku70-mediated DNA repair. J. Cell Biol. 189, 425-443 (2010)
38. Hu, Y. et al. Transcriptional modulator H2A histone family, member Y (H2AFY) marks Huntington disease activity in man and mouse. Proc. Natl Acad. Sci. USA 108, 17141-17146 (2011)
39. Ehrlich, M. E. & Gandy, S. Chromatin plasticity and the pathogenesis of Huntington disease. Proc. Natl Acad. Sci. USA 108, 16867-16868 (2011)
40. Ramadan, K. et al. Cdc48/p97 promotes reformation of the nucleus by extracting the kinase Aurora B from chromatin. Nature 450, 1258-1262 (2007)
41. McShea, A., Harris, P.L., Webster, K.R., Wahl, A.F. & Smith, M.A. Abnormal expression of the cell cycle regulators P16 and CDK4 in Alzheimer's disease. Am. J. Pathol. 150, 1933-1939 (1997) (Pubitemid 27233067)
42. Busser, J., Geldmacher, D.S. & Herrup, K. Ectopic cell cycle proteins predict the sites of neuronal cell death in Alzheimer's disease brain. J. Neurosci. 18, 2801- 2807 (1998) (Pubitemid 28163210)
43. Kruman, I.I. et al. Cell cycle activation linked to neuronal cell death initiated by DNA damage. Neuron 41, 549-561 (2004) (Pubitemid 38253067)
44. Al-Ramahi, I. et al. dAtaxin-2 mediates expanded Ataxin-1-induced neurodegeneration in a Drosophila model of SCA1. PLoS Genet. 3, e234 (2007)
45. Stelzl, U. et al. A human protein-protein interaction network: a resource for annotating the proteome. Cell 122, 957-968 (2005) (Pubitemid 41345212)
46. Lim, J. et al. A protein-protein interaction network for human inherited ataxias and disorders of Purkinje cell degeneration. Cell 125, 801-814 (2006) (Pubitemid 43732348)
47. Kahle, J.J. et al. Comparison of an expanded ataxia interactome with patient medical records reveals a relationship between macular degeneration and ataxia. Hum. Mol. Genet. 20, 510-527 (2011)
48. Guinto, J.B., Ritson, G.P., Taylor, J.P. & Forman, M.S. Valosin-containing protein and the pathogenesis of frontotemporal dementia associated with inclusion body myopathy. Acta. Neuropathol. 114, 55-61 (2007) (Pubitemid 47029060)
49. 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 431, 805-810 (2004) (Pubitemid 39434070)
50. Tagawa, K. et al. Distinct aggregation and cell death patterns among different types of primary neurons induced by mutant huntingtin protein. J. Neurochem. 89, 974-987 (2004) (Pubitemid 38684744)
51. Ravikumar, B. et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat. Genet. 36, 585-595 (2004) (Pubitemid 38715985)
52. Rose, C. et al. Rilmenidine attenuates toxicity of polyglutamine expansions in a mouse model of Huntington's disease. Hum. Mol. Genet. 19, 2144-2153 (2010)
53. Tsvetkov, AS. et al. A small-molecule scaffold induces autophagy in primary neurons and protects against toxicity in a Huntington disease model. Proc Natl Acad. Sci. USA 107, 16982-16987 (2010)
54. Boland, B. et al. Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. J. Neurosci. 28, 6926-6937 (2008)
55. Crews, L. et al. Selective molecular alterations in the autophagy pathway in patients with Lewy body disease and in models of alpha-synucleinopathy. PLoS One 5, e9313 (2010)
56. Fox, JH. et al. The mTOR kinase inhibitor Everolimus decreases S6 kinase phosphorylation but fails to reduce mutant huntingtin levels in brain and is not neuroprotective in the R6/2 mouse model of Huntington's disease. Mol. Neurodegener. 5, 26 (2010)
57. Unno, T. et al. Development of Purkinje cell degeneration in a knockin mouse model reveals lysosomal involvement in the pathogenesis of SCA6. Proc Natl Acad. Sci. USA 109, 17693-17698 (2012)
58. Lukas, C, Falck, J, Bartkova, J, Bartek, J & Lukas, J. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat. Cell. Biol. 5, 255-260 (2003). (Pubitemid 36322254)