Transcellular spreading of huntingtin aggregates in the Drosophila brain

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 39, 2015, Pages E5427-E5433

  Babcock, Daniel T ^a   Ganetzky, Barry ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Disease model; Expanded triplet repeat; Huntington's disease; Neurodegeneration; Transmission

Indexed keywords

HUNTINGTIN; N ETHYLMALEIMIDE SENSITIVE FACTOR; N ETHYLMALEIMIDE SENSITIVE FUSION PROTEIN 1; POLYGLUTAMINE; PROTEIN AGGREGATE; UNCLASSIFIED DRUG; HUNTINGTIN PROTEIN, DROSOPHILA; MICROTUBULE ASSOCIATED PROTEIN; PEPTIDE;

ADULT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; DEGENERATIVE DISEASE; DISEASE COURSE; DROSOPHILA; ENDOCYTOSIS; HUNTINGTON CHOREA; INTERNALIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; ANIMAL; BRAIN; CONFOCAL MICROSCOPY; GENETICS; IMMUNOHISTOCHEMISTRY; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSCYTOSIS; TRINUCLEOTIDE REPEAT;

ANIMALS; BRAIN; DROSOPHILA; HUNTINGTIN PROTEIN; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; MICROTUBULE-ASSOCIATED PROTEINS; NEURODEGENERATIVE DISEASES; PEPTIDES; PROTEIN AGGREGATES; TRANSCYTOSIS; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 84942844599     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1516217112     Document Type: Article

References (48)

1. Braak H, Braak E. (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82(4):239-259.
2. Braak H, et al (2003) Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 24(2):197-211.
3. Braak H, Rüb U, Gai WP, Del Tredici K (2003) Idiopathic Parkinson's disease: Possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen. J Neural Transm 110(5):517-536.
4. Ravits J, Laurie P, Fan Y, Moore D.H. (2007) Implications of ALS focality: Rostral-caudal distribution of lower motor neuron loss postmortem. Neurology 68(19):1576-1582.
5. Ravits J, Paul P, Jorg C. (2007) Focality of upper and lower motor neuron degeneration at the clinical onset of ALS. Neurology 68(19):1571-1575.
6. Deng YP, et al (2004) Differential loss of striatal projection systems in Huntington's disease: A quantitative immunohistochemical study. J Chem Neuroanat 27(3):143-164.
7. Raj A, Kuceyeski A, Weiner M. (2012) A network diffusion model of disease progression in dementia. Neuron 73(6):1204-1215.
8. Zhou J, Gennatas ED, Kramer JH, Miller BL, Seeley W.W. (2012) Predicting regional neurodegeneration from the healthy brain functional connectome. Neuron 73(6): 1216-1227.
9. Guo JL, Lee V.M. (2014) Cell-to-cell transmission of pathogenic proteins in neurode-generative diseases. Nat Med 20(2):130-138.
10. Soto C (2012) Transmissible proteins: Expanding the prion heresy. Cell 149(5):968-977.
11. Pecho-Vrieseling E, et al (2014) Transneuronal propagation of mutant huntingtin contributes to non-cell autonomous pathology in neurons. Nat Neurosci 17(8):1064-1072.
12. Feany MB, Bender W.W. (2000) A Drosophila model of Parkinson's disease. Nature 404(6776):394-398.
13. Fernandez-Funez P, et al (2000) Identification of genes that modify ataxin-1-induced neurodegeneration. Nature 408(6808):101-106.
14. Warrick JM, et al (1998) Expanded polyglutamine protein forms nuclear inclusions and causes neural degeneration in Drosophila. Cell 93(6):939-949.
15. Gunawardena S, et al (2003) Disruption of axonal transport by loss of huntingtin or expression of pathogenic polyQ proteins in Drosophila. Neuron 40(1):25-40.
16. Jackson GR, et al (1998) Polyglutamine-expanded human huntingtin transgenes induce degeneration of Drosophila photoreceptor neurons. Neuron 21(3):633-642.
17. Lee WC, Yoshihara M, Littleton J.T. (2004) Cytoplasmic aggregates trap polyglutamine-containing proteins and block axonal transport in a Drosophila model of Huntington's disease. Proc Natl Acad Sci USA 101(9):3224-3229.
18. Steffan JS, et al (2001) Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature 413(6857):739-743.
19. Pearce MM, Spartz EJ, Hong W, Luo L, Kopito R.R. (2015) Prion-like transmission of neuronal huntingtin aggregates to phagocytic glia in the Drosophila brain. Nat Commun 6:6768.
20. Brand AH, Perrimon N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118(2):401-415.
21. Lai SL, Lee T. (2006) Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat Neurosci 9(5):703-709.
22. Weiss KR, Kimura Y, Lee WC, Littleton J.T. (2012) Huntingtin aggregation kinetics and their pathological role in a Drosophila Huntington's disease model. Genetics 190(2):581-600.
23. Graham RK, et al (2006) Cleavage at the caspase-6 site is required for neuronal dysfunction and degeneration due to mutant huntingtin. Cell 125(6):1179-1191.
24. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis R.L. (2003) Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302(5651):1765-1768.
25. Blanco Redondo B, et al (2013) Identification and structural characterization of interneurons of the Drosophila brain by monoclonal antibodies of the würzburg hybridoma library. PLoS One 8(9):e75420.
26. Hofbauer A, et al (2009) The Wuerzburg hybridoma library against Drosophila brain. J Neurogenet 23(1-2):78-91.
27. Hindle SJ, Elliott C.J. (2013) Spread of neuronal degeneration in a dopaminergic, Lrrk-G2019S model of Parkinson disease. Autophagy 9(6):936-938.
28. Jenett A, et al (2012) A GAL4-driver line resource for Drosophila neurobiology. Cell Reports 2(4):991-1001.
29. Pfeiffer BD, Truman JW, Rubin G.M. (2012) Using translational enhancers to increase transgene expression in Drosophila. Proc Natl Acad Sci USA 109(17):6626-6631.
30. Weiss LA, Dahanukar A, Kwon JY, Banerjee D, Carlson J.R. (2011) The molecular and cellular basis of bitter taste in Drosophila. Neuron 69(2):258-272.
31. Freeman M (1996) Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87(4):651-660.
32. Littleton JT, et al (2001) SNARE-complex disassembly by NSF follows synaptic-vesicle fusion. Proc Natl Acad Sci USA 98(21):12233-12238.
33. Sanyal S, Tolar LA, Pallanck L, Krishnan K.S. (2001) Genetic interaction between shibire and comatose mutations in Drosophila suggest a role for snap-receptor complex assembly and disassembly for maintenance of synaptic vesicle cycling. Neurosci Lett 311(1):21-24.
34. Tolar LA, Pallanck L. (1998) NSF function in neurotransmitter release involves rearrangement of the SNARE complex downstream of synaptic vesicle docking. J Neurosci 18(24):10250-10256.
35. Babcock DT, Shen W, Ganetzky B. (2015) A neuroprotective function of NSF1 sustains autophagy and lysosomal trafficking in Drosophila. Genetics 199(2):511-522.
36. Dietzl G, et al (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448(7150):151-156.
37. Harjes P, Wanker E.E. (2003) The hunt for huntingtin function: Interaction partners tell many different stories. Trends Biochem Sci 28(8):425-433.
38. Cowan CM, Raymond L.A. (2006) Selective neuronal degeneration in Huntington's disease. Curr Top Dev Biol 75:25-71.
39. Han I, You Y, Kordower JH, Brady ST, Morfini G.A. (2010) Differential vulnerability of neurons in Huntington's disease: The role of cell type-specific features. J Neurochem 113(5):1073-1091.
40. Kuemmerle S, et al (1999) Huntington aggregates may not predict neuronal death in Huntington's disease. Ann Neurol 46(6):842-849.
41. Jackson WS (2014) Selective vulnerability to neurodegenerative disease: the curious case of Prion Protein. Dis Model Mech 7(1):21-29.
42. Saxena S, Caroni P. (2011) Selective neuronal vulnerability in neurodegenerative diseases: From stressor thresholds to degeneration. Neuron 71(1):35-48.
43. Desplats P, et al (2009) Inclusion formation and neuronal cell death through neuron-to-neuron transmission of alpha-synuclein. Proc Natl Acad Sci USA 106(31):13010-13015.
44. Fraser KB, et al (2013) LRRK2 secretion in exosomes is regulated by 14-3-3. Hum Mol Genet 22(24):4988-5000.
45. Costanzo M, et al (2013) Transfer of polyglutamine aggregates in neuronal cells occurs in tunneling nanotubes. J Cell Sci 126(Pt 16):3678-3685.
46. Kreher SA, Kwon JY, Carlson J.R. (2005) The molecular basis of odor coding in the Drosophila larva. Neuron 46(3):445-456.
47. Zhang YQ, Rodesch CK, Broadie K. (2002) Living synaptic vesicle marker: Synaptotagmin-GFP. Genesis 34(1-2):142-145.
48. Pfeiffer BD, et al (2010) Refinement of tools for targeted gene expression in Drosophila. Genetics 186(2):735-755.