VCP associated inclusion body myopathy and paget disease of bone knock-in mouse model exhibits tissue pathology typical of human disease

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Badadani, Mallikarjun ^a   Nalbandian, Angèle ^a   Watts, Giles D ^b,d   Vesa, Jouni ^a   Kitazawa, Masashi ^a   Su, Hailing ^a   Tanaja, Jasmin ^a   Dec, Eric ^a   Wallace, Douglas C ^a,c   Mukherjee, Jogeshwar ^a   Caiozzo, Vincent ^c   Warman, Matthew ^b   Kimonis, Virginia E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; TAR DNA BINDING PROTEIN; UBIQUITIN; VALOSIN CONTAINING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BONE MARROW; BRAIN TISSUE; CELL INCLUSION; CELL NUCLEUS; CELL VACUOLE; CONTROLLED STUDY; CYTOPLASM; CYTOPLASM VESICLE; ENZYME ACTIVITY; FEMUR; GENE; GENE MUTATION; GENE TARGETING; HISTOPATHOLOGY; INCLUSION BODY MYOPATHY; MACROPHAGE; MICRO-COMPUTED TOMOGRAPHY; MOUSE; MUSCLE FIBRIL; MUSCLE WEAKNESS; MYOPATHY; NEUROPATHOLOGY; NICK END LABELING; NONHUMAN; OSTEOCLASTOGENESIS; PAGET BONE DISEASE; PATHOGENESIS; PROTEIN AGGREGATION; QUADRICEPS FEMORIS MUSCLE; TIBIA; VALOSIN CONTAINING PROTEIN GENE;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CELL CYCLE PROTEINS; IN SITU NICK-END LABELING; MICE; MICE, TRANSGENIC; MYOSITIS, INCLUSION BODY; OSTEITIS DEFORMANS;

MUS;

EID: 78049244477     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013183     Document Type: Article

References (64)

1. Kimonis VE, Kovach MJ, Waggoner B, Leal S, Salam A, et al. (2000) Clinical and molecular studies in a unique family with autosomal dominant limb-girdle muscular dystrophy and Paget disease of bone. Genet Med 2: 232-241.
2. Kimonis VE, Mehta SG, Fulchiero EC, Thomasova D, Pasquali M, et al. (2008) Clinical studies in familial VCP myopathy associated with Paget disease of bone and frontotemporal dementia. Am J Med Genet A 146: 745-757.
3. Kovach MJ, Waggoner B, Leal SM, Gelber D, Khardori R, et al. (2001) Clinical delineation and localization to chromosome 9p13.3-p12 of a unique dominant disorder in four families: hereditary inclusion body myopathy, Paget disease of bone, and frontotemporal dementia. Mol Genet Metab 74: 458-475.
4. Watts GD, Thorne M, Kovach MJ, Pestronk A, Kimonis VE (2003) Clinical and genetic heterogeneity in chromosome 9p associated hereditary inclusion body myopathy: exclusion of GNE and three other candidate genes. Neuromuscul Disord 13: 559-567.
5. Kimonis V, Watts G (2007) Inclusion Body Myopathy Associated with Paget Disease of Bone and/or Frontotemporal Dementia Gene GeneTests (wwwgenetestsorg) and University of Washington, Seattle.
6. 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.
7. Watts GD, Wymer J, Kovach MJ, Mehta SG, Mumm S, 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.
8. Weihl CC, Temiz P, Miller SE, Watts G, Smith C, et al. (2008) TDP-43 accumulation in inclusion body myopathy muscle suggests a common pathogenic mechanism with frontotemporal dementia. J Neurol Neurosurg Psychiatry 79: 1186-1189.
9. Vesa J, Su H, Watts GD, Krause S, Walter MC, et al. (2009) Valosin containing protein associated inclusion body myopathy: abnormal vacuolization, autophagy and cell fusion in myoblasts. Neuromuscul Disord 19: 766-772.
10. 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.
11. Arnold SE, Han LY, Clark CM, Grossman M, Trojanowski JQ (2000) Quantitative neurohistological features of frontotemporal degeneration. Neurobiol Aging 21: 913-919.
12. Turner RS, Kenyon LC, Trojanowski JQ, Gonatas N, Grossman M (1996) Clinical, neuroimaging, and pathologic features of progressive nonfluent aphasia. Ann Neurol 39: 166-173.
13. Zhukareva V, Vogelsberg-Ragaglia V, Van Deerlin VM, Bruce J, Shuck T, et al. (2001) Loss of brain tau defines novel sporadic and familial tauopathies with frontotemporal dementia. Ann Neurol 49: 165-175.
14. Ju JS, Weihl CC. Inclusion body myopathy, Paget's disease of the bone and fronto-temporal dementia: a disorder of autophagy. Hum Mol Genet.
15. Confalonieri F, Duguet M (1995) A 200-amino acid ATPase module in search of a basic function. Bioessays 17: 639-650.
16. Ogura T, Wilkinson AJ (2001) AAA+ superfamily ATPases: common structure-diverse function. Genes Cells 6: 575-597.
17. Patel S, Latterich M (1998) The AAA team: related ATPases with diverse functions. Trends Cell Biol 8: 65-71.
18. Wang Q, Song C, Li CC (2004) Molecular perspectives on p97-VCP: progress in understanding its structure and diverse biological functions. J Struct Biol 146: 44-57.
19. Zwickl P, Baumeister W (1999) AAA-ATPases at the crossroads of protein life and death. Nat Cell Biol 1: E97-98.
20. Hetzer M, Meyer HH, Walther TC, Bilbao-Cortes D, Warren G, et al. (2001) Distinct AAA-ATPase p97 complexes function in discrete steps of nuclear assembly. Nat Cell Biol 3: 1086-1091.
21. Jarosch E, Geiss-Friedlander R, Meusser B, Walter J, Sommer T (2002) Protein dislocation from the endoplasmic reticulum-pulling out the suspect. Traffic 3: 530-536.
22. Rabinovich E, Kerem A, Frohlich KU, Diamant N, Bar-Nun S (2002) AAAATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation. Mol Cell Biol 22: 626-634.
23. Rabouille C, Kondo H, Newman R, Hui N, Freemont P, et al. (1998) Syntaxin 5 is a common component of the NSF- and p97-mediated reassembly pathways of Golgi cisternae from mitotic Golgi fragments in vitro. Cell 92: 603-610.
24. Dai RM, Li CC (2001) Valosin-containing protein is a multi-ubiquitin chaintargeting factor required in ubiquitin-proteasome degradation. Nat Cell Biol 3: 740-744.
25. Rape M, Hoppe T, Gorr I, Kalocay M, Richly H, et al. (2001) Mobilization of processed, membrane-tethered SPT23 transcription factor by CDC48(UFD1/NPL4), a ubiquitin-selective chaperone. Cell 107: 667-677.
26. Watts GD, Thomasova D, Ramdeen SK, Fulchiero EC, Mehta SG, et al. (2007) Novel VCP mutations in inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia. Clin Genet 72: 420-426.
27. Kondo H, Rabouille C, Newman R, Levine TP, Pappin D, et al. (1997) P47 is a cofactor for p97-mediated membrane fusion. Nature 388: 75-78.
28. Meyer HH, Shorter JG, Seemann J, Pappin D, Warren G (2000) A complex of mammalian ufd1 and npl4 links the AAA-ATPase, p97, to ubiquitin and nuclear transport pathways. Embo J 19: 2181-2192.
29. Muller JM, Meyer HH, Ruhrberg C, Stamp GW, Warren G, et al. (1999) The mouse p97 (CDC48) gene. Genomic structure, definition of transcriptional regulatory sequences, gene expression, and characterization of a pseudogene. J Biol Chem 274: 10154-10162.
30. Muller JM, Deinhardt K, Rosewell I, Warren G, Shima DT (2007) Targeted deletion of p97 (VCP/CDC48) in mouse results in early embryonic lethality. Biochem Biophys Res Commun 354: 459-465.
31. 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.
32. 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.
33. Tresse E, Salomons FA, Vesa J, Bott LC, Kimonis V, 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: 1-11.
34. Hirabayashi M, Inoue K, Tanaka K, Nakadate K, Ohsawa 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.
35. 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.
36. Shirogane T, Fukada T, Muller JM, Shima DT, Hibi M, et al. (1999) Synergistic roles for Pim-1 and c-Myc in STAT3-mediated cell cycle progression and antiapoptosis. Immunity 11: 709-719.
37. Bays NW, Hampton RY (2002) Cdc48-Ufd1-Npl4: stuck in the middle with Ub. Curr Biol 12: R366-371.
38. Fu X, Ng C, Feng D, Liang C (2003) Cdc48p is required for the cell cycle commitment point at Start via degradation of the G1-CDK inhibitor Far1p. J Cell Biol 163: 21-26.
39. Richly H, Rape M, Braun S, Rumpf S, Hoege C, et al. (2005) A series of ubiquitin binding factors connects CDC48/p97 to substrate multiubiquitylation and proteasomal targeting. Cell 120: 73-84.
40. Ye Y, Meyer HH, Rapoport TA (2001) The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414: 652-656.
41. Frohlich KU, Fries HW, Rudiger M, Erdmann R, Botstein D, et al. (1991) Yeast cell cycle protein CDC48p shows full-length homology to the mammalian protein VCP and is a member of a protein family involved in secretion, peroxisome formation, and gene expression. J Cell Biol 114: 443-453.
42. Lamb JR, Fu V, Wirtz E, Bangs JD (2001) Functional analysis of the trypanosomal AAA protein TbVCP with trans-dominant ATP hydrolysis mutants. J Biol Chem 276: 21512-21520.
43. Leon A, McKearin D (1999) Identification of TER94, an AAA ATPase protein, as a Bam-dependent component of the Drosophila fusome. Mol Biol Cell 10: 3825-3834.
44. Wojcik C, Yano M, DeMartino GN (2004) RNA interference of valosincontaining protein (VCP/p97) reveals multiple cellular roles linked to ubiquitin/ proteasome-dependent proteolysis. J Cell Sci 117: 281-292.
45. Kimonis VE, Watts GD (2005) Autosomal dominant inclusion body myopathy, Paget disease of bone, and frontotemporal dementia. Alzheimer Dis Assoc Disord 19(Suppl 1): S44-47.
46. Bernardi P (1999) Mitochondria in muscle cell death. Ital J Neurol Sci 20: 395-400.
47. Boya P, Cohen I, Zamzami N, Vieira HL, Kroemer G (2002) Endoplasmic reticulum stress-induced cell death requires mitochondrial membrane permeabilization. Cell Death Differ 9: 465-467.
48. Farber JL (1994) Mechanisms of cell injury by activated oxygen species. Environ Health Perspect 102(Suppl 10): 17-24.
49. Braun RJ, Zischka H, Madeo F, Eisenberg T, Wissing S, et al. (2006) Crucial mitochondrial impairment upon CDC48 mutation in apoptotic yeast. J Biol Chem 281: 25757-25767.
50. Bergamini E, Cavallini G, Donati A, Gori Z (2007) The role of autophagy in aging: its essential part in the anti-aging mechanism of caloric restriction. Ann N Y Acad Sci 1114: 69-78.
51. Eskelinen EL (2005) Maturation of autophagic vacuoles in Mammalian cells. Autophagy 1: 1-10.
52. Galluzzi L, Vicencio JM, Kepp O, Tasdemir E, Maiuri MC, et al. (2008) To die or not to die: that is the autophagic question. Curr Mol Med 8: 78-91.
53. Scarlatti F, Granata R, Meijer AJ, Codogno P (2009) Does autophagy have a license to kill mammalian cells? Cell Death Differ 16: 12-20.
54. Nishino I (2003) Autophagic vacuolar myopathies. Curr Neurol Neurosci Rep 3: 64-69.
55. Tanaka Y, Guhde G, Suter A, Eskelinen EL, Hartmann D, et al. (2000) Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature 406: 902-906.
56. Stypmann J, Janssen PM, Prestle J, Engelen MA, Kogler H, et al. (2006) LAMP- 2 deficient mice show depressed cardiac contractile function without significant changes in calcium handling. Basic Res Cardiol 101: 281-291.
57. Neumann M, Mackenzie IR, Cairns NJ, Boyer PJ, Markesbery WR, et al. (2007) TDP-43 in the ubiquitin pathology of frontotemporal dementia with VCP gene mutations. J Neuropathol Exp Neurol 66: 152-157.
58. Okere CO, Kaba H (2000) Heterogenous immunohistochemical expression of microglia-specific ionized calcium binding adaptor protein (Iba1) in the mouse olfactory bulb. Brain Res 877: 85-90.
59. Goldshmit Y, Galea MP, Wise G, Bartlett PF, Turnley AM (2004) Axonal regeneration and lack of astrocytic gliosis in EphA4-deficient mice. J Neurosci 24: 10064-10073.
60. Schroder R, Watts GD, Mehta SG, Evert BO, Broich P, et al. (2005) Mutant valosin-containing protein causes a novel type of frontotemporal dementia. Ann Neurol 57: 457-461.
61. van Swieten JC, Rosso SM, Heutink P (2007) Frontotemporal Dementia with Parkinsonism-17. GeneReviews.
62. Mumby DG, Glenn MJ, Nesbitt C, Kyriazis DA (2002) Dissociation in retrograde memory for object discriminations and object recognition in rats with perirhinal cortex damage. Behav Brain Res 132: 215-226.
63. Abe S, Watanabe H, Hirayama A, Shibuya E, Hashimoto M, et al. (2000) Morphological study of the femur in osteopetrotic (op/op) mice using microcomputed tomography. Br J Radiol 73: 1078-1082.
64. Schneider R (1979) Coxarthrosis. c 12-15 year results with intertrochanteric osteotomies in patients with coxarthrosis. Orthopade 8: 79-82.