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

Human Molecular Genetics

Volumn 17, Issue 18, 2008, Pages 2849-2862

  Teuling, Eva ^a   van Dis, Vera ^a   Wulf, Phebe S ^a   Haasdijk, Elize D ^a   Akhmanova, Anna ^a   Hoogenraad, Casper C ^a   Jaarsma, Dick ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; ADAPTOR PROTEIN; AMINO TERMINAL BICAUDAL D2 PROTEIN; COPPER ZINC SUPEROXIDE DISMUTASE; DYNACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL SWELLING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA FRAGMENTATION; GENE EXPRESSION; GENETIC CORRELATION; GOLGI COMPLEX; LIFESPAN; MALE; MOTOR NEURON DISEASE; MOTOR PERFORMANCE; MOUSE; NERVE TRANSECTION; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TRANSGENIC MOUSE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DYNEIN ATPASE; FEMALE; GENE EXPRESSION; GOLGI APPARATUS; HUMANS; LIFE EXPECTANCY; MALE; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; MOTOR NEURONS; RATS; SUPEROXIDE DISMUTASE; SURVIVAL;

MUS; MUS MUSCULUS;

EID: 50849110466     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddn182     Document Type: Article

References (63)

1. Boillee, S., Vande Velde, C. and Cleveland, D.W. (2006) ALS: A disease of motor neurons and their nonneuronal neighbors. Neuron, 52 39-59.
2. Pasinelli, P. and Brown, R.H. (2006) Molecular biology of amyotrophic lateral sclerosis: Insights from genetics. Nat. Rev. Neurosci., 7, 710-723.
3. Kwong, L.K., Neumann, M., Sampathu, D.M., Lee, V.M. and Trojanowski, J.Q. (2007) TDP-43 proteinopathy: The neuropathology underlying major forms of sporadic and familial frontotemporal lobar degeneration and motor neuron disease. Acta Neuropathol., 114, 63-70.
4. Jaarsma, D., Teuling, E., Haasdijk, E.D., De Zeeuw, C. I. and Hoogenraad, C.C. (2008) Neuron-specific expression of mutant superoxide dismutase is sufficient to induce amyotrophic lateral sclerosis in transgenic mice. J Neurosci., 28, 2075-2088.
5. Van Deerlin, V.M., Leverenz, J.B., Bekris, L.M., Bird, T.D., Yuan, W., Elman, L.B., Clay, D., Wood, E.M., Chen-Plotkin, A.S., Martinez-Lage, M. et al. (2008) TARDBP mutations in amyotrophic lateral sclerosis with TDP-43 neuropathology: A genetic and histopathological analysis. Lancet Neurol., 7, 409-416.
6. Sreedharan, J., Blair, I.P., Tripathi, V.B., Hu, X., Vance, C., Rogelj, B., Ackerley, S., Durnall, J.C., Williams, K.L., Buratti, E. et al. (2008) TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science, 319, 1668-1672.
7. Kabashi, E., Valdmanis, P.N., Dion, P., Spiegelman, D., McConkey, B.J., Vande Velde, C., Bouchard, J.P., Lacomblez, L., Pochigaeva, K., Salachas, F. et al. (2008) TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat. Genet, 40, 572-574.
8. 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.
9. 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.
10. 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.
11. 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.
12. 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.
13. Schroer, T.A. (2004) Dynactin. Annu. Rev. Cell Dev. Biol., 20 759-779.
14. Vallee, R.B., Williams, J.C., Varma, D. and Barnhart, L.E. (2004) Dynein: An ancient motor protein involved in multiple modes of transport. J. Neurobiol., 58, 189-200.
15. 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.
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. (2003) Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science, 300, 808-812.
17. Banks, G.T. and Fisher, E.M. (2008) Cytoplasmic dynein could be key to understanding neurodegeneration. Genome Biol., 9, 214.
18. Strom, A.L., Gal, J., Shi, P., Kasarskis, E.J., Hayward, L.J. and Zhu, H. (2008) Retrograde axonal transport and motor neuron disease. J. Neurochem, published online doi 10.1111/j.1471-4159.2008.05393.x.
19. J. Levy, J.R. and Holzbaur, E.L. (2006) Cytoplasmic dynein/dynactin function and dysfunction in motor neurons. Int. J. Dev. Neurosci., 24, 103-111.
20. Ibanez, C.F. (2007) Message in a bottle: Long-range retrograde signaling in the nervous system. Trends Cell Biol., 17, 519-528.
21. Roy, S., Zhang, B., Lee, V.M. and Trojanowski, J.Q. (2005) Axonal transport defects: A common theme in neurodegenerative diseases. Acta Neuropathol., 109, 5-13.
22. Johnston, J.A., Illing, M.E. and Kopito, R.R. (2002) Cytoplasmic dynein/ dynactin mediates the assembly of aggresomes. Cell Motil. Cytoskeleton, 53, 26-38.
23. 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.
24. Rao, M.V. and Nixon, R.A. (2003) Defective neurofilament transport in mouse models of amyotrophic lateral sclerosis: A review. Neurochem. Res., 28, 1041-1047.
25. Hanz, S. and Fainzilber, M. (2006) Retrograde signaling in injured nerve - the axon reaction revisited. J. Neurochem., 99, 13-19.
26. Hirano, A., Donnenfeld, H., Sasaki, S. and Nakano, I. (1984) Fine structural observations of neurofilamentous changes in amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol., 43, 461-470.
27. Delisle, M.B. and Carpenter, S. (1984) Neurofibrillary axonal swellings and amyotrophic lateral sclerosis. J. Neurol. Sci., 63, 241-250.
28. Motil, J., Dubey, M., Chan, W.K. and Shea, T.B. (2007) Inhibition of dynein but not kinesin induces aberrant focal accumulation of neurofilaments within axonal neurites. Brain Res., 1164, 125-131.
29. Burkhardt, J.K., Echeverri, C.J., Nilsson, T. and Vallee, R.B. (1997) Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J. Cell Biol., 139, 469-484.
30. Gonatas, N.K., Stieber, A. and Gonatas, J.O. (2006) Fragmentation of the Golgi apparatus in neurodegenerative diseases and cell death. J. Neurol. Sci., 246, 21-30.
31. Fujita, Y., Mizuno, Y., Takatama, M. and Okamoto, K. (2008) Anterior horn cells with abnormal TDP-43 immunoreactivities show fragmentation of the Golgi apparatus in ALS. J. Neurol. Sci., 269, 30-34.
32. Hoogenraad, C.C., Akhmanova, A., Howell, S.A., Dortland, B.R., De Zeeuw, C.I., Willemsen, R., Visser, P., Grosveld, F. and Galjart, N. (2001) Mammalian Golgi-associated Bicaudal-D2 functions in the dynein-dynactin pathway by interacting with these complexes. EMBO J., 20, 4041-4054.
33. Hoogenraad, C.C., Wulf, P., Schiefermeier, N., Stepanova, T., Galjart, N., Small, J.V., Grosveld, F., de Zeeuw, C.I. and Akhmanova, A. (2003) Bicaudal D induces selective dynein-mediated microtubule minus end-directed transport. EMBO J., 22, 6004-6015.
34. Matanis, T., Akhmanova, A., Wulf, P., Del Nery, E., Weide, T., Stepanova, T., Galjart, N., Grosveld, F., Goud, B., De Zeeuw, C.I. et al. (2002) Bicaudal-D regulates COPI-independent Golgi-ER transport by recruiting the dynein-dynactin motor complex. Nat. Cell Biol., 4, 986-992.
35. Grigoriev, I., Splinter, D., Keijzer, N., Wulf, P.S., Demmers, J., Ohtsuka, T., Modesti, M., Maly, I.V., Grosveld, F., Hoogenraad, C.C. et al. (2007) Rab6 regulates transport and targeting of exocytotic carriers. Dev. Cell, 13, 305-314.
36. Bullock, S.L. and Ish-Horowicz, D. (2001) Conserved signals and machinery for RNA transport in Drosophila oogenesis and embryogenesis. Nature, 414, 611-616.
37. Caroni, P. (1997) Overexpression of growth-associated proteins in the neurons of adult transgenic mice. J. Neurosci. Methods, 71, 3-9.
38. Feng, G., Mellor, R.H., Bernstein, M., Keller-Peck, C., Nguyen, Q.T., Wallace, M., Nerbonne, J.M., Lichtman, J.W. and Sanes, J.R. (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron, 28, 41-51.
39. Maier, K.C., Godfrey, J.E., Echeverri, C.J., Cheong, F.K. and Schroer, T.A. (2008) Dynamitin mutagenesis reveals protein-protein interactions important for dynactin structure. Traffic, 9, 481-491.
40. Dehmelt, L., Nalbant, P., Steffen, W. and Halpain, S. (2006) A microtubule-based, dynein-dependent force induces local cell protrusions: Implications for neurite initiation. Brain Cell Biol. 35, 39-56.
41. Harada, A., Takei, Y., Kanai, Y., Tanaka, Y., Nonaka, S. and Hirokawa, N. (1998) Golgi vesiculation and lysosome dispersion in cells lacking cytoplasmic dynein. J. Cell Biol., 141, 51-59.
42. Nakamura, N., Rabouille, C., Watson, R., Nilsson, T., Hui, N., Slusarewicz, P., Kreis, T.E. and Warren, G. (1995) Characterization of a cis-Golgi matrix protein, GM130. J. Cell Biol., 131, 1715-1726.
43. Caldero, J., Casanovas, A., Sorribas, A. and Esquerda, J.E. (1992) Calcitonin gene-related peptide in rat spinal cord motoneurons: subcellular distribution and changes induced by axotomy. Neuroscience 48, 449-461.
44. Tsujino, H., Kondo, E., Fukuoka, T., Dai, Y., Tokunaga, A., Miki, K., Yonenobu, K., Ochi, T. and Noguchi, K. (2000) Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: A novel neuronal marker of nerve injury. Mol. Cell. Neurosci., 15, 170-182.
45. Williamson, T.L. and Cleveland, D.W. (1999) Slowing of axonal transport is a very early event in the toxicity of ALS-linked SOD1 mutants to motor neurons. Nat. Neurosci., 2, 50-56.
46. De Vos, K.J., Chapman, A.L., Tennant, M.E., Manser, C., Tudor, E.L., Lau, K.F., Brownlees, J., Ackerley, S., Shaw, P.J., McLoughlin, D.M. et al. (2007) Familial amyotrophic lateral sclerosis-linked SOD1 mutants perturb fast axonal transport to reduce axonal mitochondria content. Hum. Mol. Genet., 16, 2720-2728.
47. Ligon, L.A., LaMonte, B.H., Wallace, K.E., Weber, N., Kalb, R.G. and Holzbaur, E.L. (2005) Mutant superoxide dismutase disrupts cytoplasmic dynein in motor neurons. Neuroreport, 16, 533-536.
48. Zhang, F., Strom, A.L., Fukada, K., Lee, S., Hayward, L.J. and Zhu, H. (2007) Interaction between familial amyotrophic lateral sclerosis (ALS)-linked SOD1 mutants and the dynein complex. J. Biol. Chem., 282, 16691-16699.
49. Gurney, M.E., Pu, H., Chiu, A.Y., Dal Canto, M.C., Polchow, C.Y., Alexander, D.D., Caliendo, J., Hentati, A., Kwon, Y.W., Deng, H.X. et al. (1994) Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science, 264, 1772-1775.
50. Vlug, A.S., Teuling, E., Haasdijk, E.D., French, P., Hoogenraad, C.C. and Jaarsma, D. (2005) ATF3 expression precedes death of spinal motoneurons in amyotrophic lateral sclerosis-SOD1 transgenic mice and correlates with c-Jun phosphorylation, CHOP expression, somato-dendritic ubiquitination and Golgi fragmentation. Eur. J. Neurosci., 22 1881-1894.
51. Allan, V.J., Thompson, H.M. and McNiven, M.A. (2002) Motoring around the Golgi. Nat. Cell Biol., 4, E236-E242.
52. 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.
53. 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.
54. 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.
55. 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.
56. 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.
57. Chevalier-Larsen, E. and Holzbaur, E.L. (2006) Axonal transport and neurodegenerative disease. Biochim. Biophys. Acta, 1762, 1094-1108.
58. Carson, C., Saleh, M., Fung, F.W., Nicholson, D.W. and Roskams, A.J. (2005) Axonal dynactin p150Glued transports caspase-8 to drive retrograde olfactory receptor neuron apoptosis. J. Neurosci., 25, 6092-6104.
59. Cavalli, V., Kujala, P., Klumperman, J. and Goldstein, L.S. (2005) Sunday Driver links axonal transport to damage signaling. J. Cell Biol., 168, 775-787.
60. Lobsiger, C.S., Boillee, S. and Cleveland, D.W. (2007) Toxicity from different SOD1 mutants dysregulates the complement system and the neuronal regenerative response in ALS motor neurons. Proc. Natl Acad. Sci. USA, 104, 7319-7326.
61. Jaarsma, D., Rognoni, F., Van Duijn, W., Verspaget, H., Haasdijk, E.D. and Holstege, J.C. (2001) CuZn superoxide dismutase (SOD1) accumulate in vacuolated mitochondria in transgenic mice expressing amyotrophic lateral sclerosis (ALS)-linked SOD1 mutations. Acta Neuropathol., 102, 293-305.
62. Hoogenraad, C.C., Milstein, A.D., Ethell, I.M., Henkemeyer, M. and Sheng, M. (2005) GRIP1 controls dendrite morphogenesis by regulating EphB receptor trafficking. Nat. Neurosci., 8, 906-915.
63. Hossaini, M., French, P.J. and Holstege, J.C. (2007) Distribution of glycinergic neuronal somata in the rat spinal cord. Brain Res., 1142, 61-69.