Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules

Cell

Volumn 118, Issue 1, 2004, Pages 127-138

  Gauthier, Laurent R ^a,d   Charrin, Bénédicte C ^a   Borrell Pagès, Maria ^a   Dompierre, Jim P ^a   Rangone, Hélène ^a   Cordelières, Fabrice P ^a   De Mey, Jan ^a,e   MacDonald, Marcy E ^b   Leßmann, Volkmar ^c   Humbert, Sandrine ^a   Saudou, Frédéric ^a  

^a INSTITUT D'OPTIQUE GRADUATE SCHOOL   (France)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

^d INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^e CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; DYNACTIN; HUNTINGTIN;

APOPTOSIS; ARTICLE; CELL SURVIVAL; CORRELATION ANALYSIS; CYTOTOXICITY; HUMAN; HUMAN CELL; HUNTINGTON CHOREA; MICROTUBULE; NERVE CELL; PATHOGENESIS; PRIORITY JOURNAL; TRANSPORT VESICLE; WILD TYPE;

EID: 3142636768     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2004.06.018     Document Type: Article

References (45)

1. Altar C.A., Cai N., Bliven T., Juhasz M., Conner J.M., Acheson A.L., Lindsay R.M., Wiegand S.J. Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature. 389:1997;856-860
2. Baas P.W., Deitch J.S., Black M.M., Banker G.A. Polarity orientation of microtubules in hippocampal neurons. uniformity in the axon and nonuniformity in the dendrite Proc. Natl. Acad. Sci. USA. 85:1988;8335-8339
3. Baquet Z.C., Gorski J.A., Jones K.R. Early striatal dendrite deficits followed by neuron loss with advanced age in the absence of anterograde cortical brain-derived neurotrophic factor. J. Neurosci. 24:2004;4250-4258
4. Bertaux F., Sharp A.H., Ross C.A., Lehrach H., Bates G.P., Wanker E. HAP1-huntingtin interactions do not contribute to the molecular pathology in Huntington's disease transgenic mice. FEBS Lett. 426:1998;229-232
5. Block-Galarza J., Chase K.O., Sapp E., Vaughn K.T., Vallee R.B., DiFiglia M., Aronin N. Fast transport and retrograde movement of huntingtin and HAP 1 in axons. Neuroreport. 8:1997;2247-2251
6. Burkhardt J.K., Echeverri C.J., Nilsson T., Vallee R.B. Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J. Cell Biol. 139:1997;469-484
7. Cattaneo E., Rigamonti D., Goffredo D., Zuccato C., Squitieri F., Sipione S. Loss of normal huntingtin function. new developments in Huntington's disease research Trends Neurosci. 24:2001;182-188
8. Cordonnier M., Dauzonne D., Louvard D., Coudrier E. Actin filament and myosin I alpha cooperate with microtubules for the movement of lysosomes. Mol. Biol. Cell. 12:2001;4013-4029
9. Deacon S.W., Serpinskaya A.S., Vaughan P.S., Fanarraga M.L., Vernos I., Vaughan K.T., Gelfand V.I. Dynactin is required for bidirectional organelle transport. J Cell Biol. 160:2003;297-300
10. DiFiglia M. Huntingtin fragments that aggregate go their separate ways. Mol. Cell. 10:2002;224-225
11. Dragatsis I., Levine M.S., Zeitlin S. Inactivation of hdh in the brain and testis results in progressive neurodegeneration and sterility in mice. Nat. Genet. 26:2000;300-306
12. Engelender S., Sharp A.H., Colomer V., Tokito M.K., Lanahan A., Worley P., Holzbaur E.L., Ross C.A. Huntingtin-associated protein 1 (HAP1) interacts with the p150Glued subunit of dynactin. Hum. Mol. Genet. 6:1997;2205-2212
13. Ferrer I., Goutan E., Marin C., Rey M.J., Ribalta T. Brain-derived neurotrophic factor in Huntington disease. Brain Res. 866:2000;257-261
14. Gunawardena S., Her L.S., Brusch R.G., Laymon R.A., Niesman I.R., Gordesky-Gold B., Sintasath L., Bonini N.M., Goldstein L.S. Disruption of axonal transport by loss of huntingtin or expression of pathogenic polyQ proteins in Drosophila. Neuron. 40:2003;25-40
15. Gutekunst C.A., Li S.H., Yi H., Ferrante R.J., Li X.J., Hersch S.M. The cellular and subcellular localization of huntingtin-associated protein 1 (HAP1). comparison with huntingtin in rat and human J. Neurosci. 18:1998;7674-7686
16. Hafezparast M., Klocke R., Ruhrberg C., Marquardt A., Ahmad-Annuar A., Bowen S., Lalli G., Witherden A.S., Hummerich H., Nicholson S., et al. Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science. 300:2003;808-812
17. Harjes P., Wanker E.E. The hunt for huntingtin function. interaction partners tell many different stories Trends Biochem. Sci. 28:2003;425-433
18. Hartmann M., Heumann R., Lessmann V. Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses. EMBO J. 20:2001;5887-5897
19. Hoffner G., Kahlem P., Djian P. Perinuclear localization of huntingtin as a consequence of its binding to microtubules through an interaction with beta-tubulin. relevance to Huntington's disease J. Cell Sci. 115:2002;941-948
20. Humbert S., Bryson E.A., Cordelieres F.P., Connors N.C., Datta S.R., Finkbeiner S., Greenberg M.E., Saudou F. The IGF-1/Akt pathway is neuroprotective in Huntington's disease and involves Huntingtin phosphorylation by Akt. Dev. Cell. 2:2002;831-837
21. Kanai Y., Okada Y., Tanaka Y., Harada A., Terada S., Hirokawa N. KIF5C, a novel neuronal kinesin enriched in motor neurons. J. Neurosci. 20:2000;6374-6384
22. King S.J., Schroer T.A. Dynactin increases the processivity of the cytoplasmic dynein motor. Nat. Cell Biol. 2:2000;20-24
23. Kohara K., Kitamura A., Morishima M., Tsumoto T. Activity-dependent transfer of brain-derived neurotrophic factor to postsynaptic neurons. Science. 291:2001;2419-2423
24. LaMonte B.H., Wallace K.E., Holloway B.A., Shelly S.S., Ascano J., Tokito M., Van Winkle T., Howland D.S., Holzbaur E.L. Disruption of dynein/dynactin inhibits axonal transport in motor neurons causing late-onset progressive degeneration. Neuron. 34:2002;715-727
25. Leavitt B.R., Guttman J.A., Hodgson J.G., Kimel G.H., Singaraja R., Vogl A.W., Hayden M.R. Wild-type huntingtin reduces the cellular toxicity of mutant huntingtin in vivo. Am. J. Hum. Genet. 68:2001;313-324
26. Lee W.C., Yoshihara M., Littleton J.T. Cytoplasmic aggregates trap polyglutamine-containing proteins and block axonal transport in a Drosophila model of Huntington's disease. Proc. Natl. Acad. Sci. USA. 101:2004;3224-3229
27. Li X.J., Li S.H., Sharp A.H., Nucifora F.C. Jr., Schilling G., Lanahan A., Worley P., Snyder S.H., Ross C.A. A huntingtin-associated protein enriched in brain with implications for pathology. Nature. 378:1995;398-402
28. Li S.H., Gutekunst C.A., Hersch S.M., Li X.J. Interaction of huntingtin-associated protein with dynactin P150Glued. J. Neurosci. 18:1998;1261-1269
29. Lione L.A., Carter R.J., Hunt M.J., Bates G.P., Morton A.J., Dunnett S.B. Selective discrimination learning impairments in mice expressing the human Huntington's disease mutation. J. Neurosci. 19:1999;10428-10437
30. Piccioni F., Pinton P., Simeoni S., Pozzi P., Fascio U., Vismara G., Martini L., Rizzuto R., Poletti A. Androgen receptor with elongated polyglutamine tract forms aggregates that alter axonal trafficking and mitochondrial distribution in motor neuronal processes. FASEB J. 16:2002;1418-1420
31. Puls I., Jonnakuty C., LaMonte B.H., Holzbaur E.L., Tokito M., Mann E., Floeter M.K., Bidus K., Drayna D., Oh S.J., et al. Mutant dynactin in motor neuron disease. Nat. Genet. 33:2003;455-456. Published online March 10, 2003. doi:10.1038/ng1123
32. Ross C.A. Polyglutamine pathogenesis. emergence of unifying mechanisms for Huntington's disease and related disorders Neuron. 35:2002;819-822
33. Saudou F., Finkbeiner S., Devys D., Greenberg M.E. Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell. 95:1998;55-66
34. Savino T.M., Gébrane-Younès J., de Mey J., Sibarita J., Hernandez-Verdun D. Nucleolar assembly of the rRNA processing machinery in living cells. J. Cell Biol. 153:2001;1097-1110
35. Schroer T. Structure and function of dynactin. Semin. Cell Dev. Biol. 7:1996;321-328
36. Smith M.A., Brandt J., Shadmehr R. Motor disorder in Huntington's disease begins as a dysfunction in error feedback control. Nature. 403:2000;544-549
37. Stepanova T., Slemmer J., Hoogenraad C.C., Lansbergen G., Dortland B., De Zeeuw C.I., Grosveld F., van Cappellen G., Akhmanova A., Galjart N. Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J. Neurosci. 23:2003;2655-2664
38. Stowers R.S., Megeath L.J., Gorska-Andrzejak J., Meinertzhagen I.A., Schwarz T.L. Axonal transport of mitochondria to synapses depends on Milton, a novel Drosophila protein. Neuron. 36:2002;1063-1077
39. Szebenyi G., Morfini G.A., Babcock A., Gould M., Selkoe K., Stenoien D.L., Young M., Faber P.W., MacDonald M.E., McPhaul M.J., Brady S.T. Neuropathogenic forms of huntingtin and androgen receptor inhibit fast axonal transport. Neuron. 40:2003;41-52
40. Trettel F., Rigamonti D., Hilditch-Maguire P., Wheeler V.C., Sharp A.H., Persichetti F., Cattaneo E., MacDonald M.E. Dominant phenotypes produced by the HD mutation in STHdh(Q111) striatal cells. Hum. Mol. Genet. 9:2000;2799-2809
41. Tukamoto T., Nukina N., Ide K., Kanazawa I. Huntington's disease gene product, huntingtin, associates with microtubules in vitro. Brain Res. Mol. Brain Res. 51:1997;8-14
42. Vale R.D. The molecular motor toolbox for intracellular transport. Cell. 112:2003;467-480
43. White J.K., Auerbach W., Duyao M.P., Vonsattel J.P., Gusella J.F., Joyner A.L., MacDonald M.E. Huntingtin is required for neurogenesis and is not impaired by the Huntington's disease CAG expansion. Nat. Genet. 17:1997;404-410
44. Zeitlin S., Liu J.P., Chapman D.L., Papaioannou V.E., Efstratiadis A. Increased apoptosis and early embryonic lethality in mice nullizygous for the Huntington's disease gene homologue. Nat. Genet. 11:1995;155-163
45. Zuccato C., Ciammola A., Rigamonti D., Leavitt B.R., Goffredo D., Conti L., MacDonald M.E., Friedlander R.M., Silani V., Hayden M.R., et al. Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science. 293:2001;493-498