A Drosophila model of ALS: Human ALS-associated mutation in VAP33A suggests a dominant negative mechanism

PLoS ONE

Volumn 3, Issue 6, 2008, Pages

  Ratnaparkhi, Anuradha ^a   Lawless, George M ^a   Schweizer, Felix E ^a   Golshani, Peyman ^a   Jackson, George R ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; VAMP ASSOCIATED MEMBRANE PROTEIN B; VESICLE ASSOCIATED MEMBRANE PROTEIN 33A; DROSOPHILA PROTEIN; MEMBRANE PROTEIN; VAP33A PROTEIN, DROSOPHILA;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CONTROLLED STUDY; DROSOPHILA; GENETIC ANALYSIS; GENETIC SCREENING; MICROTUBULE ASSEMBLY; MORPHOLOGY; MOTOR NEURON DISEASE; MUTATIONAL ANALYSIS; NEUROMUSCULAR SYNAPSE; NONHUMAN; PATHOGENESIS; PHENOTYPIC VARIATION; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ULTRASTRUCTURE; WILD TYPE; ANIMAL; DISEASE MODEL; DOMINANT GENE; GENETICS; HUMAN; METABOLISM; MUTATION; TRANSGENE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BONE MORPHOGENETIC PROTEINS; DISEASE MODELS, ANIMAL; DROSOPHILA; DROSOPHILA PROTEINS; GENES, DOMINANT; HUMANS; MEMBRANE PROTEINS; MUTATION; SIGNAL TRANSDUCTION; TRANSGENES;

EID: 48449098142     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0002334     Document Type: Article

References (50)

1. Cleveland DW, Rothstein JD (2001) From Charcot to Lou Gehrig: deciphering selectwe motor neuron death in ALS. Nat Rev Neurosci 2: 806-819.
2. Nishimura AL, Mitne-Neto M, Silva HC, Richieri-Costa A, Middleton S, et al. (2004) A mutation in the vesicle-trafficking protein VAPB causes late-onset spinal muscular atrophy and amyotrophic lateral sclerosis. Am J Hum Genet 75: 822-831.
3. Marques VD, Barreira AA, Davis MB, Abou-Sleiman PM, Silva WA Jr, et al. (2006) Expanding the phenotypes of the Pro56Ser VAPB mutation: proximal SMA with dysautonomia. Muscle Nerve 34: 731-739.
4. Nishimura Y, Hayashi M, Inada H, Tanaka T (1999) Molecular cloning and characterization of mammalian homologues of vesicle-associated membrane protein-associated (VAMP-associated) proteins. Biochem Biophys Res Commun 254: 21-26.
5. Weir ML, Klip A, Trimble WS (1998) Identification of a human homologue of the vesicle-associated membrane protein (VAMP)-associated protein of 33 kDa (VAP-33): a broadly expressed protein that binds to VAMP. Biochem J 333 (Pt 2): 247-251.
6. Kaiser SE, Brickner JH, Reilein AR, Fenn TD, Walter P, et al. (2005) Structural basis of FFAT motif-mediated ER targeting. Structure 13: 1035-1045.
7. Italiano JE Jr, Stewart M, Roberts TM (2001) How the assembly dynamics of the nematode major sperm protein generate amoeboid cell motility. Int Rev Cytol 202: 1-34.
8. Amarilio R, Ramachandran S, Sabanay H, Lev S (2005) Differential regulation of endoplasmic reticulum structure through VAP-Nir protein interaction. J Biol Chem 280: 5934-5944.
9. Foster LJ, Weir ML, Lim DY, Liu Z, Trimble WS, et al. (2000) A functional role for VAP-33 in insulin-stimulated GLUT4 traffic. Traffic 1: 512-521.
10. Skehel PA, Martin KC, Kandel ER, Bartsch D (1995) A VAMP-binding protein from Aplysia required for neurotransmitter release. Science 269: 1580-1583.
11. Kagiwada S, Hosaka K, Murata M, Nikawa J, Takatsuki A (1998) The Saccharomyces cerevisiae SCS2 gene product, a homolog of a synaptobrevin-associated protein, is an integral membrane protein of the endoplasmic reticulum and is required for inositol metabolism. J Bacteriol 180: 1700-1708.
12. Pennetta G, Hiesinger PR, Fabian-Fine R, Meinertzhagen IA, Bellen HJ (2002) Drosophila VAP-33A directs bouton formation at neuromuscular junctions in a dosage-dependent manner. Neuron 35: 291-306.
13. Kanekura K, Nishimoto I, Aiso S, Matsuoka M (2006) Characterization of amyotrophic lateral sclerosis-linked P56S mutation of vesicle-associated membrane protein-associated protein B (VAPB/ALS8). J Biol Chem 281: 30223-30233.
14. Teuling E, Ahmed S, Haasdijk E, Demmers J, Steinmetz MO, et al. (2007) Motor neuron disease-associated mutant vesicle-associated membrane protein-associated protein (VAP) B recruits wild-type VAPs into endoplasmic reticulum-derived tubular aggregates. J Neurosci 27: 9801-9815.
15. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
16. Aberle H, Haghighi AP, Fetter RD, McCabe BD, Magalhaes TR, et al. (2002) wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 33: 545-558.
17. Tsuda H, Jafar-Nejad H, Patel AJ, Sun Y, Chen HK, et al. (2005) The AXH domain of Ataxin-1 mediates neurodegeneration through its interaction with Gfi-1/Senseless proteins. Cell 122: 633-644.
18. Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat Rev Mol Cell Biol 8: 101-112.
19. Bruijn LI, Housewcart MK, Kato S, Anderson KL, Anderson SD, et al. (1998) Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science 281: 1851-1854.
20. Forman MS, Trojanowski JQ, Lee VM (2004) Neurodegenerative diseases: a decade of discoveries paves the way for therapeutic breakthroughs. Nat Med 10: 1055-1063.
21. Soto C, Estrada L, Castilla J (2006) Amyloids, prions and the inherent infectious nature of misfolded protein aggregates. Trends Biochem Sci 31: 150-155.
22. Orr HT, Zoghbi HY (2007) Trinucleotide repeat disorders. Annu Rev Neurosci 30: 575-621.
23. Ciechanover A, Brundin P (2003) The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron 40: 427-446.
24. Ross CA, Pickart CM (2004) The ubiquitin-proteasome pathway in Parkinson's disease and other neurodegenerative diseases. Trends Cell Biol 14: 703-711.
25. Cairns NJ, Lee VM, Trojanowski JQ (2004) The cytoskeleton in neurodegenerative diseases. J Pathol 204: 438-449.
26. Collard JF, Cote F, Julien JP (1995) Defective axonal transport in a transgenic mouse model of amyotrophic lateral sclerosis. Nature 375: 61-64.
27. Sasaki S, Iwata M (1996) Impairment of fast axonal transport in the proximal axons of anterior horn neurons in amyotrophic lateral sclerosis. Neurology 47: 535-540.
28. Williamson TL, Cleveland DW (1999) Sloving of axonal transport is a very early event in the toxicity of ALS-linked SOD1 mutants to motor neurons. Nat Neurosci 2: 50-56.
29. Hummel T, Krukkert K, Roos J, Davis G, Klambt C (2000) Drosophila Futsch/ 22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 26: 357-370.
30. Roos J, Hummel T, Ng N, Klambt C, Davis GW (2000) Drosophila Futsch regulates synaptic microtubule organization and is necessary for synaptic growth. Neuron 26: 371-382.
31. Sherwood NT, Sun Q, Xue M, Zhang B, Zinn K (2004) Drosophila spastin regulates synaptic microtubule networks and is required for normal motor function. PLoS Biol 2: e429.
32. Packard M, Koo ES, Gorczyca M, Sharpe J, Cumberledge S, et al. (2002) The Drosophila Wnt, wingless, provides an essential signal for pre- and postsynaptic differentiation. Cell 111: 319-330.
33. Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, et al. (2006) Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49: 833-844.
34. Kittel RJ, Wichmann C, Rasse TM, Fouquet W, Schmidt M, et al. (2006) Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release. Science 312: 1051-1054.
35. Fischer LR, Culver DG, Tennant P, Davis AA, Wang M, et al. (2004) Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp Neurol 185: 232-240.
36. Frey D, Schneider C, Xu L, Borg J, Spooren W, et al. (2000) Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J Neurosci 20: 2534-2542.
37. Pun S, Santos AF, Saxena S, Xu L, Caroni P (2006) Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat Neurosci 9: 408-419.
38. Chai A, Withers J, Koh YH, Parry K, Bao H, et al. (2008) hVAPB, the causative gene of a heterogeneous group of motor neuron diseases in humans, is functionally interchangeable with its Drosophila homologue DVAP-33A at the neuromuscular junction. Hum Mol Genet 17: 266-280.
39. McCabe BD, Marques G, Haghighi AP, Fetter RD, Crotty ML, et al. (2003) The BMP homolog Gbb provides a retrograde signal that regulates synaptic growth at the Drosophila neuromuscular junction. Neuron 39: 241-254.
40. McCabe BD, Hom S, Aberle H, Fetter RD, Marques G, et al. (2004) Highwire regulates presynaptic BMP signaling essential for synaptic growth. Neuron 41: 891-905.
41. Marques G, Haerry TE, Crotty ML, Xue M, Zhang B, et al. (2003) Retrograde Gbb signaling through the Bmp type 2 receptor wishful thinking regulates systemic FMRFa expression in Drosophila. Development 130: 5457-5470.
42. Massague J (1996) TGFbeta signaling: receptors, transducers, and Mad proteins. Cell 85: 947-950.
43. Shimizu K, Gurdon JB (1999) A quantitative analysis of signal transduction from activin receptor to nucleus and its relevance to morphogen gradient interpretation. Proc Natl Acad Sci U S A 96: 6791-6796.
44. Tanimoto H, Itoh S, ten Dijke P, Tabata T (2000) Hedgehog creates a gradient of DPP activity in Drosophila wing imaginal discs. Mol Cell 5: 59-71.
45. Dudu V, Bittig T, Entchev E, Kicheva A, Julicher F, et al. (2006) Postsynaptic mad signaling at the Drosophila neuromuscular junction. Curr Biol 16: 625-635.
46. Tesseur I, Zou K, Esposito L, Bard F, Berber E, et al. (2006) Deficiency in neuronal TGF-beta signaling promotes neurodegeneration and Alzheimer's pathology. J Clin Invest 116: 3060-3069.
47. Haerry TE, Khalsa O, O'Connor MB, Wharton KA (1998) Synergistic signaling by two BMP ligands through the SAX and TKV receptors controls wing growth and patterning in Drosophila. Development 125: 3977-3987.
48. Hoang B, Chiba A (2001) Single-cell analysis of Drosophila larval neuromuscular synapses. Dev Biol 229: 55-70.
49. Persson U, Izumi H, Souchelnytskyi S, Itoh S, Grimsby S, et al. (1998) The L45 loop in type I receptors for TGF-beta family members is a critical determinant in specifying Smad isoforum activation. FEBS Lett 434: 83-87.
50. Sang TK, Chang HY, Lawless GM, Ratnaparkhi A, Mee L, et al. (2007) A Drosophila model of mutant human parkin-induced toxicity demonstrates selective loss of dopaminergic neurons and dependence on cellular dopamine. J Neurosci 27: 981-992.