Rab11 rescues synaptic dysfunction and behavioural deficits in a Drosophila model of Huntington's disease

Human Molecular Genetics

Volumn 21, Issue 13, 2012, Pages 2912-2922

  Steinert, Joern R ^a   Campesan, Susanna ^a   Richards, Paul ^a   Kyriacou, Charalambos P ^a   Forsythe, Ian D ^a   Giorgini, Flaviano ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HUNTINGTIN; MUTANT PROTEIN; RAB11 PROTEIN;

ARTICLE; BEHAVIOR DISORDER; CONTROLLED STUDY; DISEASE MODEL; DROSOPHILA MELANOGASTER; HUNTINGTON CHOREA; LARVA; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; TRANSGENICS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ELECTROPHYSIOLOGICAL PHENOMENA; HUNTINGTON DISEASE; LARVA; MICROTUBULE-ASSOCIATED PROTEINS; NERVE DEGENERATION; NEUROMUSCULAR JUNCTION; RAB GTP-BINDING PROTEINS; SYNAPSES; SYNAPTIC POTENTIALS; SYNAPTIC TRANSMISSION;

DROSOPHILA MELANOGASTER;

EID: 84863518971     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds117     Document Type: Article

References (56)

1. The Huntington's Disease Collaborative Research Group (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell, 72, 971-983.
2. Gutekunst, C.A., Norflus, F. and Hersch, S.M. (2002) In: Bates, G., Harper, P.S. and Jones, L. (eds), Huntington's Disease. Oxford University Press, Oxford, pp. 251-275.
3. Ross, C.A. and Tabrizi, S.J. (2011) Huntington's disease: from molecular pathogenesis to clinical treatment. Lancet Neurol., 10, 83-98.
4. Paulsen, J.S., Langbehn, D.R., Stout, J.C., Aylward, E., Ross, C.A., Nance, M., Guttman, M., Johnson, S., MacDonald, M., Beglinger, L.J. et al. (2008) Detection of Huntington's disease decades before diagnosis: the Predict-HD study. J. Neurol. Neurosurg. Psychiatry, 79, 874-880.
5. Orth, M., Schippling, S., Schneider, S.A., Bhatia, K.P., Talelli, P., Tabrizi, S.J. and Rothwell, J.C. (2010) Abnormal motor cortex plasticity in premanifest and very early manifest Huntington disease. J. Neurol. Neurosurg. Psychiatry, 81, 267-270.
6. Schippling, S., Schneider, S.A., Bhatia, K.P., Munchau, A., Rothwell, J.C., Tabrizi, S.J. and Orth, M. (2009) Abnormal motor cortex excitability in preclinical and very early Huntington's disease. Biol. Psychiatry, 65, 959-965.
7. Milnerwood, A.J. and Raymond, L.A. (2010) Early synaptic pathophysiology in neurodegeneration: insights from Huntington's disease. Trends Neurosci., 33, 513-523.
8. Moreno, J.A. and Mallucci, G.R. (2010) Dysfunction and recovery of synapses in prion disease: implications for neurodegeneration. Biochem. Soc. Trans., 38, 482-487.
9. Simons, K. and Zerial, M. (1993) Rab proteins and the road maps for intracellular transport. Neuron, 11, 789-799.
10. Ullrich, O., Reinsch, S., Urbe, S., Zerial, M. and Parton, R.G. (1996) Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol., 135, 913-924.
11. Hales, C.M., Vaerman, J.P. and Goldenring, J.R. (2002) Rab11 family interacting protein 2 associates with Myosin Vb and regulates plasma membrane recycling. J. Biol. Chem., 277, 50415-50421.
12. Li, X., Sapp, E., Chase, K., Comer-Tierney, L.A., Masso, N., Alexander, J., Reeves, P., Kegel, K.B., Valencia, A., Esteves, M. et al. (2009) Disruption of Rab11 activity in a knock-in mouse model of Huntington's disease. Neurobiol. Dis., 36, 374-383.
13. Li, X., Standley, C., Sapp, E., Valencia, A., Qin, Z.H., Kegel, K.B., Yoder, J., Comer-Tierney, L.A., Esteves, M., Chase, K. et al. (2009) Mutant huntingtin impairs vesicle formation from recycling endosomes by interfering with Rab11 activity. Mol. Cell Biol., 29, 6106-6116.
14. Li, X., Valencia, A., Sapp, E., Masso, N., Alexander, J., Reeves, P., Kegel, K.B., Aronin, N. and Difiglia, M. (2010) Aberrant Rab11-dependent trafficking of the neuronal glutamate transporter EAAC1 causes oxidative stress and cell death in Huntington's disease. J. Neurosci., 30, 4552-4561.
15. Richards, P., Didszun, C., Campesan, S., Simpson, A., Horley, B., Young, K.W., Glynn, P., Cain, K., Kyriacou, C.P., Giorgini, F. et al. (2011) Dendritic spine loss and neurodegeneration is rescued by Rab11 in models of Huntington's disease. Cell Death Differ., 18, 191-200.
16. Rohrbough, J. and Broadie, K. (2005) Lipid regulation of the synaptic vesicle cycle. Nat. Rev. Neurosci., 6, 139-150.
17. Marsh, J.L., Pallos, J. and Thompson, L.M. (2003) Fly models of Huntington's disease. Hum. Mol. Genet., 12 (Spec No 2), R187-R193.
18. Steffan, J.S., Bodai, L., Pallos, J., Poelman, M., McCampbell, A., Apostol, B.L., Kazantsev, A., Schmidt, E., Zhu, Y.Z., Greenwald, M. et al. (2001) Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature, 413, 739-743.
19. Romero, E., Cha, G.H., Verstreken, P., Ly, C.V., Hughes, R.E., Bellen, H.J. and Botas, J. (2008) Suppression of neurodegeneration and increased neurotransmission caused by expanded full-length huntingtin accumulating in the cytoplasm. Neuron, 57, 27-40.
20. Karunanithi, S., Marin, L., Wong, K. and Atwood, H.L. (2002) Quantal size and variation determined by vesicle size in normal and mutant Drosophila glutamatergic synapses. J. Neurosci., 22, 10267-10276.
21. Steinert, J.R., Kuromi, H., Hellwig, A., Knirr, M., Wyatt, A.W., Kidokoro, Y. and Schuster, C.M. (2006) Experience-dependent formation and recruitment of large vesicles from reserve pool. Neuron, 50, 723-733.
22. Atwood, H.L. and Karunanithi, S. (2002) Diversification of synaptic strength: presynaptic elements. Nat. Rev. Neurosci., 3, 497-516.
23. Katz, B. and Miledi, R. (1967) A study of synaptic transmission in the absence of nerve impulses. J. Physiol., 192, 407-436.
24. DiAntonio, A., Petersen, S.A., Heckmann, M. and Goodman, C.S. (1999) Glutamate receptor expression regulates quantal size and quantal content at the Drosophila neuromuscular junction. J. Neurosci., 19, 3023-3032.
25. Marrus, S.B., Portman, S.L., Allen, M.J., Moffat, K.G. and DiAntonio, A. (2004) Differential localization of glutamate receptor subunits at the Drosophila neuromuscular junction. J. Neurosci., 24, 1406-1415.
26. Petersen, S.A., Fetter, R.D., Noordermeer, J.N., Goodman, C.S. and DiAntonio, A. (1997) Genetic analysis of glutamate receptors in Drosophila reveals a retrograde signal regulating presynaptic transmitter release. Neuron, 19, 1237-1248.
27. Daniels, R.W., Collins, C.A., Gelfand, M.V., Dant, J., Brooks, E.S., Krantz, D.E. and DiAntonio, A. (2004) Increased expression of the Drosophila vesicular glutamate transporter leads to excess glutamate release and a compensatory decrease in quantal content. J. Neurosci., 24, 10466-10474.
28. Czaja, M.J. (2010) Autophagy in health and disease. 2. Regulation of lipid metabolism and storage by autophagy: pathophysiological implications. Am. J. Physiol. Cell Physiol., 298, C973-C978.
29. Renger, J.J., Ueda, A., Atwood, H.L., Govind, C.K. and Wu, C.F. (2000) Role of cAMP cascade in synaptic stability and plasticity: ultrastructural and physiological analyses of individual synaptic boutons in Drosophila memory mutants. J. Neurosci., 20, 3980-3992.
30. Davis, G.W., DiAntonio, A., Petersen, S.A. and Goodman, C.S. (1998) Postsynaptic PKA controls quantal size and reveals a retrograde signal that regulates presynaptic transmitter release in Drosophila. Neuron, 20, 305-315.
31. Wang, J.W., Sylwester, A.W., Reed, D., Wu, D.A., Soll, D.R. and Wu, C.F. (1997) Morphometric description of the wandering behavior in Drosophila larvae: aberrant locomotion in Na+ and K+ channel mutants revealed by computer-assisted motion analysis. J. Neurogenet., 11, 231- 254.
32. Wang, J.W., Soll, D.R. and Wu, C.F. (2002) Morphometric description of the wandering behavior in Drosophila larvae: a phenotypic analysis of K+ channel mutants. J. Neurogenet., 16, 45-63.
33. Cheng, L.E., Song, W., Looger, L.L., Jan, L.Y. and Jan, Y.N. (2010) The role of the TRP channel NompC in Drosophila larval and adult locomotion. Neuron, 67, 373-380.
34. Nishimura, Y., Yalgin, C., Akimoto, S., Doumanis, J., Sasajima, R., Nukina, N., Miyakawa, H., Moore, A.W. and Morimoto, T. (2010) Selection of behaviors and segmental coordination during larval locomotion is disrupted by nuclear polyglutamine inclusions in a new Drosophila Huntington's disease-like model. J. Neurogenet., 24, 194-206.
35. Lanson, N.A. Jr, Maltare, A., King, H., Smith, R., Kim, J.H., Taylor, J.P., Lloyd, T.E. and Pandey, U.B. (2011) A Drosophila model of FUS-related neurodegeneration reveals genetic interaction between FUS and TDP-43. Hum. Mol. Genet., 20, 2510-2523.
36. Pennetta, G., Hiesinger, P.R., Fabian-Fine, R., Meinertzhagen, I.A. and Bellen, H.J. (2002) Drosophila VAP-33A directs bouton formation at neuromuscular junctions in a dosage-dependent manner. Neuron, 35, 291-306.
37. Smith, R., Brundin, P. and Li, J.Y. (2005) Synaptic dysfunction in Huntington's disease: a new perspective. Cell Mol. Life Sci., 62, 1901-1912.
38. Parker, J.A., Metzler, M., Georgiou, J., Mage, M., Roder, J.C., Rose, A.M., Hayden, M.R. and Neri, C. (2007) Huntingtin-interacting protein 1 influences worm and mouse presynaptic function and protects Caenorhabditis elegans neurons against mutant polyglutamine toxicity. J. Neurosci., 27, 11056-11064.
39. Verstreken, P., Ohyama, T. and Bellen, H.J. (2008) FM 1-43 labeling of synaptic vesicle pools at the Drosophila neuromuscular junction. Methods Mol. Biol., 440, 349-369.
40. Li, X., Sapp, E., Valencia, A., Kegel, K.B., Qin, Z.H., Alexander, J., Masso, N., Reeves, P., Ritch, J.J., Zeitlin, S. et al. (2008) A function of huntingtin in guanine nucleotide exchange on Rab11. Neuroreport, 19, 1643-1647.
41. Rozas, J.L., Gomez-Sanchez, L., Tomas-Zapico, C., Lucas, J.J. and Fernandez-Chacon, R. (2011) Increased neurotransmitter release at the neuromuscular junction in a mouse model of polyglutamine disease. J. Neurosci., 31, 1106-1113.
42. Hodgson, J.G., Agopyan, N., Gutekunst, C.A., Leavitt, B.R., LePiane, F., Singaraja, R., Smith, D.J., Bissada, N., McCutcheon, K., Nasir, J. et al. (1999) A YAC mouse model for Huntington's disease with full-length mutant huntingtin, cytoplasmic toxicity, and selective striatal neurodegeneration. Neuron, 23, 181-192.
43. Sinadinos, C., Burbidge-King, T., Soh, D., Thompson, L.M., Marsh, J.L., Wyttenbach, A. and Mudher, A.K. (2009) Live axonal transport disruption by mutant huntingtin fragments in Drosophila motor neuron axons. Neurobiol. Dis., 34, 389-395.
44. Truant, R., Atwal, R.S., Desmond, C., Munsie, L. and Tran, T. (2008) Huntington's disease: revisiting the aggregation hypothesis in polyglutamine neurodegenerative diseases. FEBS J., 275, 4252-4262.
45. Olshina, M.A., Angley, L.M., Ramdzan, Y.M., Tang, J., Bailey, M.F., Hill, A.F. and Hatters, D.M. (2010) Tracking mutant huntingtin aggregation kinetics in cells reveals three major populations that include an invariant oligomer pool. J. Biol. Chem., 285, 21807-21816.
46. Legleiter, J., Mitchell, E., Lotz, G.P., Sapp, E., Ng, C., DiFiglia, M., Thompson, L.M. and Muchowski, P.J. (2010) Mutant huntingtin fragments form oligomers in a polyglutamine length-dependent manner in vitro and in vivo. J. Biol. Chem., 285, 14777-14790.
47. Gunawardena, S., Her, L.S., Brusch, R.G., Laymon, R.A., Niesman, I.R., Gordesky-Gold, B., Sintasath, L., Bonini, N.M. and Goldstein, L.S. (2003) Disruption of axonal transport by loss of huntingtin or expression of pathogenic polyQ proteins in Drosophila. Neuron, 40, 25-40.
48. Lee, W.C., Yoshihara, M. and 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, 3224-3229.
49. Liu, J., Zhang, J.P., Shi, M., Quinn, T., Bradner, J., Beyer, R., Chen, S. and Zhang, J. (2009) Rab11a and HSP90 regulate recycling of extracellular alpha-synuclein. J. Neurosci., 29, 1480-1485.
50. Dumanchin, C., Czech, C., Campion, D., Cuif, M.H., Poyot, T., Martin, C., Charbonnier, F., Goud, B., Pradier, L. and Frebourg, T. (1999) Presenilins interact with Rab11, a small GTPase involved in the regulation of vesicular transport. Hum. Mol. Genet., 8, 1263-1269.
51. Greenfield, J.P., Leung, L.W., Cai, D., Kaasik, K., Gross, R.S., Rodriguez-Boulan, E., Greengard, P. and Xu, H. (2002) Estrogen lowers Alzheimer beta-amyloid generation by stimulating trans-Golgi network vesicle biogenesis. J. Biol. Chem., 277, 12128-12136.
52. Agola, J., Jim, P., Ward, H., Basuray, S. and Wandinger-Ness, A. (2011) Rab GTPases as regulators of endocytosis, targets of disease and therapeutic opportunities. Clin. Genet., 80, 305-318.
53. Postlethwaite, M., Hennig, M.H., Steinert, J.R., Graham, B.P. and Forsythe, I.D. (2007) Acceleration of AMPA receptor kinetics underlies temperature-dependent changes in synaptic strength at the rat calyx of Held. J. Physiol., 579, 69-84.
54. Sigrist, S.J., Reiff, D.F., Thiel, P.R., Steinert, J.R. and Schuster, C.M. (2003) Experience-dependent strengthening of Drosophila neuromuscular junctions. J. Neurosci., 23, 6546-6556.
55. Andres, A.J. and Thummel, C.S. (1994) Methods for quantitative analysis of transcription in larvae and prepupae. Methods Cell Biol., 44, 565-573.
56. Maroni, G. and Laurie-Ahlberg, C.C. (1983) Genetic control of Adh expression in Drosophila melanogaster. Genetics, 105, 921-933.