Valosin-containing protein gene mutations: Cellular phenotypes relevant to neurodegeneration

Journal of Molecular Neuroscience

Volumn 44, Issue 2, 2011, Pages 91-102

  Poksay, Karen S ^a   Madden, David T ^a,c   Peter, Anna K ^a,d   Niazi, Kayvan ^a,e   Banwait, Surita ^a   Crippen, Danielle ^a   Bredesen, Dale E ^a,b   Rao, Rammohan V ^a  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c TOURO UNIVERSITY CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e Abraxis Bioscience   (United States)

Author keywords

Endoplasmic reticulum; ER stress; Programmed cell death; Valosin containing protein

Indexed keywords

ADENOSINE TRIPHOSPHATE; HUNTINGTIN; PROTEASOME; VALOSIN CONTAINING PROTEIN;

APOPTOSIS; ARTICLE; CELL INCLUSION; CELL VACUOLE; CONTROLLED STUDY; CYTOPLASM VESICLE; EMBRYO; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; FRONTOTEMPORAL DEMENTIA; GENE MUTATION; HUMAN; HUMAN CELL; MYOPATHY; NERVE DEGENERATION; PAGET BONE DISEASE; PHENOTYPE; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN;

ADENOSINE TRIPHOSPHATASES; CELL CYCLE PROTEINS; CELL DEATH; ENDOPLASMIC RETICULUM; ENZYME INHIBITORS; HEK293 CELLS; HUMANS; MUTATION; NERVE DEGENERATION; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PHENOTYPE; PROTEASOME ENDOPEPTIDASE COMPLEX; THAPSIGARGIN; UBIQUITIN;

EID: 79955918990     PISSN: 08958696     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12031-010-9489-8     Document Type: Article

References (59)

1. Bence NF, Sampat RM, Kopito RR (2001) Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292:1552-1555 (Pubitemid 32493425)
2. Bence NF, Bennett EJ, Kopito RR (2005) Application and analysis of the GFPu family of ubiquitin-proteasome system reporters. Methods Enzymol 399:481-490 (Pubitemid 41772749)
3. Boeddrich A, Gaumer S, Haacke A, Tzvetkov N, Albrecht M, Evert BO et al (2006) An arginine/lysine-rich motif is crucial for VCP/ p97-mediated modulation of ataxin-3 fibrillogenesis. Embo J 25:1547-1558
4. Bredesen DE, Rao RV, Mehlen P (2006) Cell death in the nervous system. Nature 443:796-802 (Pubitemid 44622684)
5. Chen L, Gao X (2002) Neuronal apoptosis induced by endoplasmic reticulum stress. Neurochem Res 27:891-898
6. Custer SK, Neumann M, Lu H, Wright AC, Taylor JP (2010) 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
7. Dai RM, Li CC (2001) Valosin-containing protein is a multi-ubiquitin chain-targeting factor required in ubiquitin-proteasome degradation. Nat Cell Biol 3:740-744 (Pubitemid 32734252)
8. Dai RM, Chen E, Longo DL, Gorbea CM, Li CC (1998) Involvement of valosin-containing protein, an ATPase co-purified with IkappaBalpha and 26 S proteasome, in ubiquitin-proteasome-mediated degradation of IkappaBalpha. J Biol Chem 273:3562-3573 (Pubitemid 28109780)
9. Doss-Pepe EW, Stenroos ES, Johnson WG, Madura K (2003) Ataxin-3 interactions with rad23 and valosin-containing protein and its associations with ubiquitin chains and the proteasome are consistent with a role in ubiquitin-mediated proteolysis. Mol Cell Biol 23:6469-6483 (Pubitemid 37075759)
10. Egerton M, Ashe OR, Chen D, Druker BJ, Burgess WH, Samelson LE (1992) VCP, the mammalian homolog of cdc48, is tyrosine phosphorylated in response to T cell antigen receptor activation. Embo J 11:3533-3540
11. Egger L, Madden DT, Rheme C, Rao RV, Bredesen DE (2007) Endoplasmic reticulum stress-induced cell death mediated by the proteasome. Cell Death Differ 14:1172-1180 (Pubitemid 46785108)
12. Forman MS, Lee VM, Trojanowski JQ (2003) 'Unfolding' pathways in neurodegenerative disease. Trends Neurosci 26:407-410
13. Forman MS, Mackenzie IR, Cairns NJ, Swanson E, Boyer PJ, Drachman DA et al (2006) Novel ubiquitin neuropathology in frontotemporal dementia with valosin-containing protein gene mutations. J Neuropathol Exp Neurol 65:571-581 (Pubitemid 44288941)
14. Gitcho MA, Strider J, Carter D, Taylor-Reinwald L, Forman MS, Goate AM et al (2009) VCP mutations causing frontotemporal lobar degeneration disrupt localization of TDP-43 and induce cell death. J Biol Chem 284:12384-12398
15. Guyant-Marechal L, Laquerriere A, Duyckaerts C, Dumanchin C, Bou J, Dugny F et al (2006) Valosin-containing protein gene mutations: clinical and neuropathologic features. Neurology 67:644-651
16. Halawani D, LeBlanc AC, Rouiller I, Michnick SW, Servant MJ, Latterich M (2009) 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
17. Hashimoto M, Rockenstein E, Crews L, Masliah E (2003) Role of protein aggregation in mitochondrial dysfunction and neurodegeneration in Alzheimer's and Parkinson's diseases. Neuromolecular Med 4:21-36
18. Higashiyama H, Hirose F, Yamaguchi M, Inoue YH, Fujikake N, Matsukage A et al (2002) Identification of ter94, Drosophila VCP, as a modulator of polyglutamine-induced neurodegeneration. Cell Death Differ 9:264-273 (Pubitemid 34223870)
19. Hirabayashi M, Inoue K, Tanaka K, Nakadate K, Ohsawa Y, Kamei Y et al (2001) VCP/p97 in abnormal protein aggregates, cytoplasmic vacuoles, and cell death, phenotypes relevant to neurodegeneration. Cell Death Differ 8:977-984 (Pubitemid 32994648)
20. Hubbers CU, Clemen CS, Kesper K, Boddrich A, Hofmann A, Kamarainen O et al (2007) Pathological consequences of VCP mutations on human striated muscle. Brain 130:381-393 (Pubitemid 46181092)
21. Igarashi S, Morita H, Bennett KM, Tanaka Y, Engelender S, Peters MF et al (2003) Inducible PC12 cell model of Huntington's disease shows toxicity and decreased histone acetylation. Neuroreport 14:565-568 (Pubitemid 36528991)
22. Ju JS, Miller SE, Hanson PI, Weihl CC (2008) Impaired protein aggregate handling and clearance underlie the pathogenesis of p97/VCP-associated disease. J Biol Chem 283:30289-30299
23. Ju JS, Fuentealba RA, Miller SE, Jackson E, Piwnica-Worms D, Baloh RH et al (2009) Valosin-containing protein (VCP) is required for autophagy and is disrupted in VCP disease. J Cell Biol 187:875-888
24. Katayama T, Imaizumi K, Manabe T, Hitomi J, Kudo T, Tohyama M (2004) Induction of neuronal death by ER stress in Alzheimer's disease. J Chem Neuroanat 28:67-78 (Pubitemid 39198955)
25. Kimonis VE, Fulchiero E, Vesa J, Watts G (2008) VCP disease associated with myopathy, Paget disease of bone and frontotemporal dementia: review of a unique disorder. Biochim Biophys Acta 1782:744-748
26. Kobayashi T, Tanaka K, Inoue K, Kakizuka A (2002) Functional ATPase activity of p97/valosin-containing protein (VCP) is required for the quality control of endoplasmic reticulum in neuronally differentiated mammalian PC12 cells. J Biol Chem 277:47358-47365 (Pubitemid 36159250)
27. Kopito RR (2000) Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 10:524-530
28. Lindholm D, Wootz H, Korhonen L (2006) ER stress and neurodegenerative diseases. Cell Death Differ 13:385-392
29. Manno A, Noguchi M, Fukushi J, Motohashi Y, Kakizuka A (2010) 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
30. Mimnaugh EG, Xu W, Vos M, Yuan X, Neckers L (2006) 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 (Pubitemid 44497219)
31. Mishra M, Paunesku T, Woloschak GE, Siddique T, Zhu LJ, Lin S et al (2007) Gene expression analysis of frontotemporal lobar degeneration of the motor neuron disease type with ubiquitinated inclusions. Acta Neuropathol 114:81-94 (Pubitemid 47029063)
32. Pleasure IT, Black MM, Keen JH (1993) Valosin-containing protein, VCP, is a ubiquitous clathrin-binding protein. Nature 365:459-462 (Pubitemid 23311044)
33. Rao RV, Bredesen DE (2004) Misfolded proteins, endoplasmic reticulum stress and neurodegeneration. Curr Opin Cell Biol 16:653-662 (Pubitemid 39463116)
34. Rao RV, Hermel E, Castro-Obregon S, del Rio G, Ellerby LM, Ellerby HM et al (2001) Coupling endoplasmic reticulum stress to the cell death program. Mechanism of caspase activation. J Biol Chem 276:33869-33874
35. Rao RV, Peel A, Logvinova A, del Rio G, Hermel E, Yokota T et al (2002) Coupling endoplasmic reticulum stress to the cell death program: role of the ER chaperoneGRP78. FEBS Lett 514:122-128
36. Rao RV, Ellerby HM, Bredesen DE (2004a) Coupling endoplasmic reticulum stress to the cell death program. Cell Death Differ 11:372-380 (Pubitemid 38489415)
37. Rao RV, PoksayKS, Castro-Obregon S, Schilling B, RowRH, Del Rio G et al (2004b) Molecular components of a cell death pathway activated by endoplasmic reticulum stress. J Biol Chem 279:177-187
38. Rao RV, Niazi K, Mollahan P, Mao X, Crippen D, Poksay KS et al (2006) Coupling endoplasmic reticulum stress to the cell-death program: a novel HSP90-independent role for the small chaperone protein p23. Cell Death Differ 13:415-425
39. Schilling B, Gafni J, Torcassi C, Cong X, Row RH, LaFevre-Bernt MA et al (2006) Huntingtin phosphorylation sites mapped by mass spectrometry. Modulation of cleavage and toxicity. J Biol Chem 281:23686-23697 (Pubitemid 44274144)
40. Schroder R, Watts GD, Mehta SG, Evert BO, Broich P, Fliessbach K et al (2005) Mutant valosin-containing protein causes a novel type of frontotemporal dementia. Ann Neurol 57:457-461 (Pubitemid 40343972)
41. Seki T, Takahashi H, Adachi N, Abe N, Shimahara T, Saito N et al (2007) Aggregate formation of mutant protein kinase C gamma found in spinocerebellar ataxia type 14 impairs ubiquitin-proteasome system and induces endoplasmic reticulum stress. Eur J Neurosci 26:3126-3140 (Pubitemid 350135178)
42. Song C, Wang Q, Li CC (2003) ATPase activity of p97-valosin-containing protein (VCP). D2 mediates the major enzyme activity, and D1 contributes to the heat-induced activity. J Biol Chem 278:3648-3655 (Pubitemid 36801088)
43. Tresse E, Salomons FA, Vesa J, Bott LC, Kimonis V, Yao TP et al (2010) VCP/p97 is essential for maturation of ubiquitin-containing autophagosomes and this function is impaired by mutations that cause IBMPFD. Autophagy 6
44. Vale RD (2000) AAA proteins. Lords of the ring J Cell Biol 150:F13-F19
45. Vandermoere F, El Yazidi-Belkoura I, Slomianny C, Demont Y, Bidaux G, Adriaenssens E et al (2006) The valosin-containing protein (VCP) is a target of Akt signaling required for cell survival. J Biol Chem 281:14307-14313
46. Vesa J, Su H, Watts GD, Krause S, Walter MC, Martin B et al (2009) Valosin containing protein associated inclusion body myopathy: abnormal vacuolization, autophagy and cell fusion in myoblasts. Neuromuscul Disord 19:766-772
47. Vij N (2008) AAA ATPase p97/VCP: cellular functions, disease and therapeutic potential. J Cell Mol Med 12:2511-2518
48. Wang Q, Song C, Yang X, Li CC (2003) D1 ring is stable and nucleotide-independent, whereas D2 ring undergoes major conformational changes during the ATPase cycle of p97-VCP. J Biol Chem 278:32784-32793 (Pubitemid 37055719)
49. Watts GD, Wymer J, Kovach MJ, Mehta SG, Mumm S, Darvish D et al (2004) Inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia is caused by mutant valosin-containing protein. Nat Genet 36:377-381 (Pubitemid 38437260)
50. Weihl CC, Dalal S, Pestronk A, Hanson PI (2006) Inclusion body myopathy-associated mutations in p97/VCP impair endoplasmic reticulum-associated degradation. Hum Mol Genet 15:189-199 (Pubitemid 43125974)
51. Weihl CC, Miller SE, Hanson PI, Pestronk A (2007) Transgenic expression of inclusion body myopathy associated mutant p97/VCP causes weakness and ubiquitinated protein inclusions in mice. Hum Mol Genet 16:919-928 (Pubitemid 47062736)
52. Weihl CC, Pestronk A, Kimonis VE (2009) Valosin-containing protein disease: inclusion body myopathy with Paget's disease of the bone and fronto-temporal dementia. Neuromuscul Disord 19:308-315
53. Whiteheart SW, Rossnagel K, Buhrow SA, Brunner M, Jaenicke R, Rothman JE (1994) N-ethylmaleimide-sensitive fusion protein: a trimeric ATPase whose hydrolysis of ATP is required for membrane fusion. J Cell Biol 126:945-954 (Pubitemid 24252141)
54. Wojcik C (2002) VCP - the missing link in protein degradation? Trends Cell Biol 12:212
55. Xu C, Bailly-Maitre B, Reed JC (2005) Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 115:2656-2664 (Pubitemid 41434389)
56. Yang H, Liu C, Zhong Y, Luo S, Monteiro MJ, Fang S (2010) Huntingtin interacts with the cue domain of gp78 and inhibits gp78 binding to ubiquitin and p97/VCP. PLoS One 5:e8905
57. Yoshida H (2007) ER stress and diseases. FEBS J 274:630-658
58. Zhang K, Kaufman RJ (2006) The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 66: S102-S109 (Pubitemid 43739994)
59. Zhong X, Pittman RN (2006) Ataxin-3 binds VCP/p97 and regulates retrotranslocation of ERAD substrates. Hum Mol Genet 15:2409-2420 (Pubitemid 44288695)