A point mutation in the dynein heavy chain gene leads to striatal atrophy and compromises neurite outgrowth of striatal neurons

Human Molecular Genetics

Volumn 19, Issue 22, 2010, Pages 4385-4398

  Braunstein, Kerstin E ^a,g   Eschbach, Judith ^b,c   Ròna Vörös, Krisztina ^a   Soylu, Rana ^d   Mikrouli, Elli ^d   Larmet, Yves ^b,c   René, Frédérique ^b,c   de Aguilar, Jose Luis Gonzalez ^b,c   Loeffler, Jean Philippe ^b,c   Müller, Hans Peter ^a   Bucher, Selina ^e   Kaulisch, Thomas ^e   Niessen, Heiko G ^e   Tillmanns, Julia ^e   Fischer, Kristina ^f   Schwalenstöcker, Birgit ^a   Kassubek, Jan ^a   Pichler, Bernd ^f   Stiller, Detlef ^e   Petersen, Åsa ^d   Ludolph, Albert C ^a   Dupuis, Luc ^b,c   more..

^a UNIVERSITY OF ULM   (Germany)

^b INSERM   (France)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d LUND UNIVERSITY   (Sweden)

^e BOEHRINGER INGELHEIM PHARMA GMBH AND CO KG   (Germany)

^f UNIVERSITY OF TÜBINGEN   (Germany)

^g JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA TUBULIN; DOPAMINE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; DYNACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; GLIAL FIBRILLARY ACIDIC PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 2; MUTANT PROTEIN; PROENKEPHALIN; PROTEIN SUBUNIT; SUBSTANCE P;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; BASAL GANGLION; BRAIN ATROPHY; BRAIN VENTRICLE DILATATION; CELL LOSS; CELL STRUCTURE; CORPUS STRIATUM; DEGENERATIVE DISEASE; EMBRYO; HEAVY CHAIN; HINDLIMB; HUNTINGTON CHOREA; HYPERACTIVITY; IN VITRO STUDY; IN VIVO STUDY; MOTOR COORDINATION; MOUSE; MOUSE STRAIN; MUSCLE WEAKNESS; NERVE DEGENERATION; NERVE FIBER GROWTH; NERVE FIBER TRANSPORT; NEURITE; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARKINSONISM; PATHOGENESIS; PERRY SYNDROME; POINT MUTATION; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RECEPTOR BINDING; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA;

MUS;

EID: 77958479351     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq361     Document Type: Article

References (64)

1. Morfini, G.A., Burns, M., Binder, L.I., Kanaan, N.M., LaPointe, N., Bosco, D.A., Brown, R.H. Jr, Brown, H., Tiwari, A., Hayward, L. et al. (2009) Axonal transport defects in neurodegenerative diseases. J. Neurosci., 29, 12776-12786.
2. Chevalier-Larsen, E. and Holzbaur, E.L. (2006) Axonal transport and neurodegenerative disease. Biochim. Biophys. Acta, 1762, 1094-1108.
3. Levy, J.R. and Holzbaur, E.L. (2006) Cytoplasmic dynein/dynactin function and dysfunction in motor neurons. Int. J. Dev. Neurosci., 24, 103-111.
4. LaMonte, B.H., Wallace, K.E., Holloway, B.A., Shelly, S.S., Ascano, J., Tokito, M., Van Winkle, T., Howland, D.S. and Holzbaur, E.L. (2002) Disruption of dynein/dynactin inhibits axonal transport in motor neurons causing late-onset progressive degeneration. Neuron, 34, 715-727.
5. Teuling, E., van Dis, V., Wulf, P.S., Haasdijk, E.D., Akhmanova, A., Hoogenraad, C.C. and Jaarsma, D. (2008) A novel mouse model with impaired dynein/dynactin function develops amyotrophic lateral sclerosis (ALS)-like features in motor neurons and improves lifespan in SOD1-ALS mice. Hum. Mol. Genet., 17, 2849-2862.
6. 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. (2003) Mutant dynactin in motor neuron disease. Nat. Genet., 33, 455-456.
7. Munch, C., Sedlmeier, R., Meyer, T., Homberg, V., Sperfeld, A.D., Kurt, A., Prudlo, J., Peraus, G., Hanemann, C.O., Stumm, G. et al. (2004) Point mutations of the p150 subunit of dynactin (DCTN1) gene in ALS. Neurology, 63, 724-726.
8. Puls, I., Oh, S.J., Sumner, C.J., Wallace, K.E., Floeter, M.K., Mann, E.A., Kennedy, W.R., Wendelschafer-Crabb, G., Vortmeyer, A., Powers, R. et al. (2005) Distal spinal and bulbar muscular atrophy caused by dynactin mutation. Ann. Neurol., 57, 687-694.
9. Wider, C., Dachsel, J.C., Farrer, M.J., Dickson, D.W., Tsuboi, Y. and Wszolek, Z.K. Elucidating the genetics and pathology of Perry syndrome. J. Neurol. Sci., 289, 149-154.
10. Farrer, M.J., Hulihan, M.M., Kachergus, J.M., Dachsel, J.C., Stoessl, A.J., Grantier, L.L., Calne, S., Calne, D.B., Lechevalier, B., Chapon, F. et al. (2009) DCTN1 mutations in Perry syndrome. Nat. Genet., 41, 163-165.
11. Levy, J.R., Sumner, C.J., Caviston, J.P., Tokito, M.K., Ranganathan, S., Ligon, L.A., Wallace, K.E., LaMonte, B.H., Harmison, G.G., Puls, I. et al. (2006) A motor neuron disease-associated mutation in p150Glued perturbs dynactin function and induces protein aggregation. J. Cell Biol., 172, 733-745.
12. Laird, F.M., Farah, M.H., Ackerley, S., Hoke, A., Maragakis, N., Rothstein, J.D., Griffin, J., Price, D.L., Martin, L.J. and Wong, P.C. (2008) Motor neuron disease occurring in a mutant dynactin mouse model is characterized by defects in vesicular trafficking. J. Neurosci., 28, 1997-2005.
13. Chevalier-Larsen, E.S., Wallace, K.E., Pennise, C.R. and Holzbaur, E.L. (2008) Lysosomal proliferation and distal degeneration in motor neurons expressing the G59S mutation in the p150Glued subunit of dynactin. Hum. Mol. Genet., 17, 1946-1955.
14. Lai, C., Lin, X., Chandran, J., Shim, H., Yang, W.J. and Cai, H. (2007) The G59S mutation in p150(glued) causes dysfunction of dynactin in mice. J. Neurosci., 27, 13982-13990.
15. Berezuk, M.A. and Schroer, T.A. (2007) Dynactin enhances the processivity of kinesin-2. Traffic, 8, 124-129.
16. King, S.J. and Schroer, T.A. (2000) Dynactin increases the processivity of the cytoplasmic dynein motor. Nat. Cell Biol., 2, 20-24.
17. Lee, S.J., Chae, C. and Wang, M.M. (2009) p150/glued modifies nuclear estrogen receptor function. Mol. Endocrinol., 23, 620-629.
18. Shrum, C.K., Defrancisco, D. and Meffert, M.K. (2009) Stimulated nuclear translocation of NF-kappaB and shuttling differentially depend on dynein and the dynactin complex. Proc. Natl Acad. Sci. USA, 106, 2647-2652.
19. Li, S.H., Gutekunst, C.A., Hersch, S.M. and Li, X.J. (1998) Interaction of huntingtin-associated protein with dynactin P150Glued. J. Neurosci., 18, 1261-1269.
20. Li, X.J., Li, S.H., Sharp, A.H., Nucifora, F.C. Jr, Schilling, G., Lanahan, A., Worley, P., Snyder, S.H. and Ross, C.A. (1995) A huntingtin-associated protein enriched in brain with implications for pathology. Nature, 378, 398-402.
21. Caviston, J.P., Ross, J.L., Antony, S.M., Tokito, M. and Holzbaur, E.L. (2007) Huntingtin facilitates dynein/dynactin-mediated vesicle transport. Proc. Natl Acad. Sci. USA, 104, 10045-10050.
22. Gauthier, L.R., Charrin, B.C., Borrell-Pages, M., Dompierre, J.P., Rangone, H., Cordelieres, F.P., De Mey, J., MacDonald, M.E., Lessmann, V., Humbert, S. et al. (2004) Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell, 118, 127-138.
23. Morfini, G.A., You, Y.M., Pollema, S.L., Kaminska, A., Liu, K., Yoshioka, K., Bjorkblom, B., Coffey, E.T., Bagnato, C., Han, D. et al. (2009) Pathogenic huntingtin inhibits fast axonal transport by activating JNK3 and phosphorylating kinesin. Nat. Neurosci., 12, 864-871.
24. Hafezparast, M., Klocke, R., Ruhrberg, C., Marquardt, A., Ahmad-Annuar, A., Bowen, S., Lalli, G., Witherden, A.S., Hummerich, H., Nicholson, S. et al. (2003) Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science, 300, 808-812.
25. Perlson, E., Jeong, G.B., Ross, J.L., Dixit, R., Wallace, K.E., Kalb, R.G. and Holzbaur, E.L. (2009) A switch in retrograde signaling from survival to stress in rapid-onset neurodegeneration. J. Neurosci., 29, 9903-9917.
26. Ilieva, H.S., Yamanaka, K., Malkmus, S., Kakinohana, O., Yaksh, T., Marsala, M. and Cleveland, D.W. (2008) Mutant dynein (Loa) triggers proprioceptive axon loss that extends survival only in the SOD1 ALS model with highest motor neuron death. Proc. Natl Acad. Sci. USA, 105, 12599-12604.
27. Dupuis, L., Fergani, A., Braunstein, K.E., Eschbach, J., Holl, N., Rene, F., Gonzalez De Aguilar, J.L., Zoerner, B., Schwalenstocker, B., Ludolph, A.C. et al. (2009) Mice with a mutation in the dynein heavy chain 1 gene display sensory neuropathy but lack motor neuron disease. Exp. Neurol., 215, 146-152.
28. Chen, X.J., Levedakou, E.N., Millen, K.J., Wollmann, R.L., Soliven, B. and Popko, B. (2007) Proprioceptive sensory neuropathy in mice with a mutation in the cytoplasmic Dynein heavy chain 1 gene. J. Neurosci., 27, 14515-14524.
29. Luesse, H.G., Schiefer, J., Spruenken, A., Puls, C., Block, F. and Kosinski, C.M. (2001) Evaluation of R6/2 HD transgenic mice for therapeutic studies in Huntington's disease: Behavioral testing and impact of diabetes mellitus. Behav. Brain Res., 126, 185-195.
30. Schiefer, J., Landwehrmeyer, G.B., Luesse, H.G., Sprunken, A., Puls, C., Milkereit, A., Milkereit, E. and Kosinski, C.M. (2002) Riluzole prolongs survival time and alters nuclear inclusion formation in a transgenic mouse model of Huntington's disease. Mov. Disord., 17, 748-757.
31. Bolivar, V.J., Manley, K. and Messer, A. (2004) Early exploratory behavior abnormalities in R6/1 Huntington's disease transgenic mice. Brain Res., 1005, 29-35.
32. Gantois, I., Fang, K., Jiang, L., Babovic, D., Lawrence, A.J., Ferreri, V., Teper, Y., Jupp, B., Ziebell, J., Morganti-Kossmann, C.M. et al. (2007) Ablation of D1 dopamine receptor-expressing cells generates mice with seizures, dystonia, hyperactivity, and impaired oral behavior. Proc. Natl Acad. Sci. USA, 104, 4182-4187.
33. Siessmeier, T., Zhou, Y., Buchholz, H.G., Landvogt, C., Vernaleken, I., Piel, M., Schirrmacher, R., Rosch, F., Schreckenberger, M., Wong, D.F. et al. (2005) Parametric mapping of binding in human brain of D2 receptor ligands of different affinities. J. Nucl. Med., 46, 964-972.
34. Baquet, Z.C., Gorski, J.A. and Jones, K.R. (2004) Early striatal dendrite deficits followed by neuron loss with advanced age in the absence of anterograde cortical brain-derived neurotrophic factor. J. Neurosci., 24, 4250-4258.
35. Rauskolb, S., Zagrebelsky, M., Dreznjak, A., Deogracias, R., Matsumoto, T., Wiese, S., Erne, B., Sendtner, M., Schaeren-Wiemers, N., Korte, M. et al. (2010) Global deprivation of brain-derived neurotrophic factor in the CNS reveals an area-specific requirement for dendritic growth. J. Neurosci., 30, 1739-1749.
36. Santi, S., Cappello, S., Riccio, M., Bergami, M., Aicardi, G., Schenk, U., Matteoli, M. and Canossa, M. (2006) Hippocampal neurons recycle BDNF for activity-dependent secretion and LTP maintenance. EMBO J., 25, 4372-4380.
37. Zhou, P., Porcionatto, M., Pilapil, M., Chen, Y., Choi, Y., Tolias, K.F., Bikoff, J.B., Hong, E.J., Greenberg, M.E. and Segal, R.A. (2007) Polarized signaling endosomes coordinate BDNF-induced chemotaxis of cerebellar precursors. Neuron, 55, 53-68.
38. Bogush, A., Pedrini, S., Pelta-Heller, J., Chan, T., Yang, Q., Mao, Z., Sluzas, E., Gieringer, T. and Ehrlich, M.E. (2007) AKT and CDK5/p35 mediate brain-derived neurotrophic factor induction of DARPP-32 in medium size spiny neurons in vitro. J. Biol. Chem., 282, 7352-7359.
39. Gokce, O., Runne, H., Kuhn, A. and Luthi-Carter, R. (2009) Short-term striatal gene expression responses to brain-derived neurotrophic factor are dependent on MEK and ERK activation. PLoS ONE, 4, e5292.
40. Auer-Grumbach, M. (2008) Hereditary sensory neuropathy type I. Orphanet J. Rare Dis., 3,7.
41. Reddy, P.H., Williams, M., Charles, V., Garrett, L., Pike-Buchanan, L., Whetsell, W.O. Jr, Miller, G. and Tagle, D.A. (1998) Behavioural abnormalities and selective neuronal loss in HD transgenic mice expressing mutated full-length HD cDNA. Nat. Genet., 20, 198-202.
42. Lin, J., Wu, P.H., Tarr, P.T., Lindenberg, K.S., St-Pierre, J., Zhang, C.Y., Mootha, V.K., Jager, S., Vianna, C.R., Reznick, R.M. et al. (2004) Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell, 119, 121-135.
43. Laruelle, M. (2000) Imaging synaptic neurotransmission with in vivo binding competition techniques: A critical review. J. Cereb. Blood Flow Metab., 20, 423-451.
44. Xiao, M.F., Xu, J.C., Tereshchenko, Y., Novak, D., Schachner, M. and Kleene, R. (2009) Neural cell adhesion molecule modulates dopaminergic signaling and behavior by regulating dopamine D2 receptor internalization. J. Neurosci., 29, 14752-14763.
45. Namkung, Y., Dipace, C., Urizar, E., Javitch, J.A. and Sibley, D.R. (2009) G protein-coupled receptor kinase-2 constitutively regulates D2 dopamine receptor expression and signaling independently of receptor phosphorylation. J. Biol. Chem., 284, 34103-34115.
46. Tirotta, E., Fontaine, V., Picetti, R., Lombardi, M., Samad, T.A., Oulad-Abdelghani, M., Edwards, R. and Borrelli, E. (2008) Signaling by dopamine regulates D2 receptors trafficking at the membrane. Cell Cycle, 7, 2241-2248.
47. Kim, O.J., Ariano, M.A., Namkung, Y., Marinec, P., Kim, E., Han, J. and Sibley, D.R. (2008) D2 dopamine receptor expression and trafficking is regulated through direct interactions with ZIP. J. Neurochem., 106, 83-95.
48. Menalled, L.B., Sison, J.D., Wu, Y., Olivieri, M., Li, X.J., Li, H., Zeitlin, S. and Chesselet, M.F. (2002) Early motor dysfunction and striosomal distribution of huntingtin microaggregates in Huntington's disease knock-in mice. J. Neurosci., 22, 8266-8276.
49. Zheng, Y., Wildonger, J., Ye, B., Zhang, Y., Kita, A., Younger, S.H., Zimmerman, S., Jan, L.Y. and Jan, Y.N. (2008) Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons. Nat. Cell Biol., 10, 1172-1180.
50. Satoh, D., Sato, D., Tsuyama, T., Saito, M., Ohkura, H., Rolls, M.M., Ishikawa, F. and Uemura, T. (2008) Spatial control of branching within dendritic arbors by dynein-dependent transport of Rab5-endosomes. Nat. Cell Biol., 10, 1164-1171.
51. Fleck, M.W., Hirotsune, S., Gambello, M.J., Phillips-Tansey, E., Suares, G., Mervis, R.F., Wynshaw-Boris, A. and McBain, C.J. (2000) Hippocampal abnormalities and enhanced excitability in a murine model of human lissencephaly. J. Neurosci., 20, 2439-2450.
52. Liu, Z., Steward, R. and Luo, L. (2000) Drosophila Lis1 is required for neuroblast proliferation, dendritic elaboration and axonal transport. Nat. Cell Biol., 2, 776-783.
53. Murray, J.W. and Wolkoff, A.W. (2003) Roles of the cytoskeleton and motor proteins in endocytic sorting. Adv. Drug Deliv. Rev., 55, 1385-1403.
54. Aniento, F., Emans, N., Griffiths, G. and Gruenberg, J. (1993) Cytoplasmic dynein-dependent vesicular transport from early to late endosomes. J. Cell Biol., 123, 1373-1387.
55. Jan, Y.N. and Jan, L.Y. (2010) Branching out: Mechanisms of dendritic arborization. Nat. Rev. Neurosci., 11, 316-328.
56. Kieran, D., Hafezparast, M., Bohnert, S., Dick, J.R., Martin, J., Schiavo, G., Fisher, E.M. and Greensmith, L. (2005) A mutation in dynein rescues axonal transport defects and extends the life span of ALS mice. J. Cell Biol., 169, 561-567.
57. Gertler, T.S., Chan, C.S. and Surmeier, D.J. (2008) Dichotomous anatomical properties of adult striatal medium spiny neurons. J. Neurosci., 28, 10814-10824.
58. Ravikumar, B., Acevedo-Arozena, A., Imarisio, S., Berger, Z., Vacher, C., O'Kane, C.J., Brown, S.D. and Rubinsztein, D.C. (2005) Dynein mutations impair autophagic clearance of aggregate-prone proteins. Nat. Genet., 37, 771-776.
59. Weydt, P., Pineda, V.V., Torrence, A.E., Libby, R.T., Satterfield, T.F., Lazarowski, E.R., Gilbert, M.L., Morton, G.J., Bammler, T.K., Strand, A.D. et al. (2006) Thermoregulatory and metabolic defects in Huntington's disease transgenic mice implicate PGC-1alpha in Huntington's disease neurodegeneration. Cell Metab., 4, 349-362.
60. Teuchert, M., Fischer, D., Schwalenstoecker, B., Habisch, H.J., Bockers, T.M. and Ludolph, A.C. (2006) A dynein mutation attenuates motor neuron degeneration in SOD1(G93A) mice. Exp. Neurol., 198, 271-274.
61. Bode, F.J., Stephan, M., Suhling, H., Pabst, R., Straub, R.H., Raber, K.A., Bonin, M., Nguyen, H.P., Riess, O., Bauer, A. et al. (2008) Sex differences in a transgenic rat model of Huntington's disease: Decreased 17beta-estradiol levels correlate with reduced numbers of DARPP32+ neurons in males. Hum. Mol. Genet., 17, 2595-2609.
62. West, M.J., Slomianka, L. and Gundersen, H.J. (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec., 231, 482-497.
63. Lammertsma, A.A. and Hume, S.P. (1996) Simplified reference tissue model for PET receptor studies. Neuroimage, 4, 153-158.
64. Yakushev, I., Hammers, A., Fellgiebel, A., Schmidtmann, I., Scheurich, A., Buchholz, H.G., Peters, J., Bartenstein, P., Lieb, K. and Schreckenberger, M. (2009) SPM-based count normalization provides excellent discrimination of mild Alzheimer's disease and amnestic mild cognitive impairment from healthy aging. Neuroimage, 44, 43-50.