Axonal Defects in Mouse Models of Motoneuron Disease

Journal of Neurobiology

Volumn 58, Issue 2, 2004, Pages 272-286

  Jablonka, Sibylle ^a   Wiese, Stefan ^a   Sendtner, Michael ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

actin mRNA transport; Axon elongation; Axonal motor proteins; Motoneuron disease; Tubulin specific chaperones

Indexed keywords

BETA ACTIN; CHAPERONE; DYNACTIN; ETHYLNITROSOUREA; GENE PRODUCT; PROTEIN; PROTEIN P 150; PROTEIN SUBUNIT; TUBULIN; UNCLASSIFIED DRUG;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CONTROLLED STUDY; DISEASE MODEL; EMBRYO; FAMILIAL DISEASE; GENE MUTATION; HEREDITARY SPINAL MUSCULAR ATROPHY; MOTOR NEURON DISEASE; MOUSE; MUSCLE ATROPHY; NERVE FIBER DEGENERATION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RESPIRATORY DISTRESS; REVIEW; RNA PROCESSING; SPINAL MUSCULAR ATROPHY WITH RESPIRATORY DISTRESS;

AGED; ALTERNATIVE SPLICING; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; AXONAL TRANSPORT; AXONS; CARRIER PROTEINS; CASPASE 2; CASPASES; CELL SURVIVAL; CELLS, CULTURED; CILIARY NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; EMBRYO; FUNGAL PROTEINS; GENES, RRNA; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; MIDDLE AGED; MOTOR NEURON DISEASE; MUTATION; NERVE GROWTH FACTOR; NERVE TISSUE PROTEINS; PRECIPITIN TESTS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS A-RAF; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-RAF; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA-BINDING PROTEINS; SCIATIC NERVE; SPINE; SUPEROXIDE DISMUTASE; TAU PROTEINS; TRANSCRIPTION FACTORS; TUBULIN;

EID: 0842290736     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10313     Document Type: Review

References (77)

1. Andersen PM, Nilsson P, Ala Hurula V, Keranen ML, Tarvainen I, Haltia T, Nilsson L, Binzer M, Forsgren L, Marklund SL. 1995. Amyotrophic lateral sclerosis associated with homozygosity for an Asp90Ala mutation in CuZn-superoxide dismutase. Nat Genet 10:61-66.
2. Antar LN, Bassell GJ. 2003. Sunrise at the synapse: the FMRP mRNP shaping the synaptic interface. Neuron 37:555-558.
3. Bassell GJ, Oleynikov Y, Singer RH. 1999. The travels of mRNAs through all cells large and small. FASEB J 13:447-454.
4. Batulan Z, Shinder GA, Minotti S, He BP, Doroudchi MM, Nalbantoglu J, Strong MJ, Durham HD. 2003. High threshold for induction of the stress response in motor neurons is associated with failure to activate HSF1. J Neurosci 23:5789-5798.
5. Beckman JS, Carson M, Smith CD, Koppenol WH. 1993. ALS, SOD and peroxynitrite. Nature 364:584.
6. Bommel H, Xie G, Rossoll W, Wiese S, Jablonka S, Boehm T, Sendtner M. 2002. Missense mutation in the tubulin-specific chaperone E (Tbce) gene in the mouse mutant progressive motor neuronopathy, a model of human motoneuron disease. J Cell Biol 159:563-569.
7. Bordet T, Schmalbruch H, Pettmann B, Hagege A, Castelnau-Ptakhine L, Kahn A, Haase G. 1999. Adenoviral cardiotrophin-1 gene transfer protects pmn mice from progressive motor neuronopathy. J Clin Invest 104:1077-1085.
8. Brown RH, Meininger V, Swash M. 2000. Amyotrophic Lateral Sclerosis. London: Martin Dunitz Ltd. 226 p.
9. Bruening W, Roy J, Giasson B, Figlewicz DA, Mushynski WE, Durham HD. 1999. Up-regulation of protein chaperones preserves viability of cells expressing toxic Cu/ Zn-superoxide dismutase mutants associated with amyotrophic lateral sclerosis. J Neurochem 72:693-699.
10. Bruijn LI, Houseweart MK, Kato S, Anderson KL, Anderson SD, Ohama E, Reaume AG, Scott RW, Cleveland DW. 1998. Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science 281:1851-1854.
11. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857-868.
12. Chou SM. 1992. Pathology-Light microscopy of Amyotrophic lateral sclerosis. Handbook of Amyotrophic Lateral sclerosis. New York: Marcel Dekker, Inc. p 133-182
13. Cifuentes-Diaz C, Nicole S, Velasco ME, Borra-Cebrian C, Panozzo C, Frugier T, Millet G, Roblot N, Joshi V, Melki J. 2002. Neurofilament accumulation at the motor end-plate and lack of axonal sprouting in a spinal muscular atrophy mouse model. Hum Mol Genet 11:1439-1447.
14. Cleveland DW, Rothstein JD. 2001. From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat Rev Neurosci 2:806-819.
15. Cox GA, Mahaffey CL, Frankel WN. 1998. Identification of the mouse neuromuscular degeneration gene and mapping of a second site suppressor allele. Neuron 21:1327-1337.
16. Crino PB, Eberwine J. 1996. Molecular characterization of the dendritic growth cone: regulated mRNA transport and local protein synthesis. Neuron 17:1173-1187.
17. Deng HX, Hentati A, Tainer JA, Iqbal Z, Cayabyab A, Hung WY, Getzoff ED, Hu P, Herzfeldt B, Roos RP. 1993. Amyotrophic lateral sclerosis and structural defects in Cu,Zn superoxide dismutase. Science 261:1047-1051.
18. Duchen LW, Strich SJ, (with an Appendix by D.S. Falconer). 1968. An hereditary motor neurone disease with progressive denervation of muscle in the mouse: the mutant "wobbler". J Neurol Neurosurg Psychiat 31:535-542.
19. Durham HD, Roy J, Dong L, Figlewicz DA. 1997. Aggregation of mutant Cu/ Zn superoxide dismutase proteins in a culture model of ALS. J Neuropathol Exp Neurol 56: 523-530.
20. Endrizzi M, Huang S, Scharf JM, Kelter AR, Wirth B, Kunkel LM, Miller W, Dietrich WF. 1999. Comparative sequence analysis of the mouse and human Lgn1/ SMA interval. Genomics 60:137-151.
21. Estevez AG, Crow JP, Sampson JB, Reiter C, Zhuang Y, Richardson GJ, Tarpey MM, Barbeito L, Beckman JS. 1999. Induction of nitric oxide-dependent apoptosis in motor neurons by zinc-deficient superoxide dismutase. Science 286:2498-2500.
22. Ferri A, Sanes JR, Coleman MP, Cunningham JM, Kato AC. 2003. Inhibiting axon degeneration and synapse loss attenuates apoptosis and disease progression in a mouse model of motoneuron disease. Curr Biol 13:669-673.
23. Frugier T, Tiziano FD, Cifuentes-Diaz C, Miniou P, Roblot N, Dierich A, Le Meur M, Melki J. 2000. Nuclear targeting defect of SMN lacking the C-terminus in a mouse model of spinal muscular atrophy. Hum Mol Genet 9:849-858.
24. Gassler CS, Wiederkehr T, Brehmer D, Bukau B, Mayer MP. 2001. Bag-1M accelerates nucleotide release for human Hsc70 and Hsp70 and can act concentration-dependent as positive and negative cofactor. J Biol Chem 276:32538-32544.
25. Giess R, Holtmann B, Braga M, Grimm T, Muller-Myhsok B, Toyka KV, Sendtner M. 2002. Early onset of severe familial amyotrophic lateral sclerosis with a SOD-1 mutation: potential impact of CNTF as a candidate modifier gene. Am J Hum Genet 70:1277-1286.
26. Grohmann K, Schuelke M, Diers A, Hoffmann K, Lucke B, Adams C, Bertini E, Leonhardt-Horti H, Muntoni F, Ouvrier R, et al. 2001. Mutations in the gene encoding immunoglobulin mu-binding protein 2 cause spinal muscular atrophy with respiratory distress type 1. Nat Genet 29:75-77.
27. Gu W, Pan F, Zhang HL, Bassell GJ, Singer RH. 2002. A predominantly nuclear protein affecting cytoplasmic localization of beta-actin mRNA in fibroblasts and neurons. J Cell Biol 156:41-51.
28. Haase G, Pettmann B, Vigne E, Castelnau-Ptakhine L, Schmalbruch H, Kahn A. 1998. Adenovirus-mediated transfer of the neurotrophin-3 gene into skeletal muscle of pmn mice: therapeutic effects and mechanisms of action. J Neurol Sci 1:97-105
29. Hadano S, Hand CK, Osuga H, Yanagisawa Y, Otomo A, Devon RS, Miyamoto N, Showguchi-Miyata J, Okada Y, Singaraja R, et al. 2001. A gene encoding a putative GTPase regulator is mutated in familial amyotrophic lateral sclerosis 2. Nat Genet 29:166-173.
30. Hafezparast M, Klocke R, Ruhrberg C, Marquardt A, Ahmad-Annuar A, Bowen S, Lalli G, Witherden AS, Hummerich H, Nicholson S, et al. 2003. Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science 300:808-812.
31. Holtmann B, Zielasek J, Toyka KV, Sendtner M. 1999. Comparative analysis of motoneuron loss and functional deficits in PMN mice: implications for human motoneuron disease. J Neurol Sci 169:140-147.
32. Hsieh-Li HM, Chang JG, Jong YJ, Wu MH, Wang NM, Tsai CH, Li H. 2000. A mouse model for spinal muscular atrophy. Nat Genet 24:66-70
33. Jaarsma D, Haasdijk ED, Grashorn JA, Hawkins R, van Duijn W, Verspaget HW, London J, Holstege JC. 2000. Human Cu/Zn superoxide dismutase (SOD1) overexpression in mice causes mitochondrial vacuolization, axonal degeneration, and premature motoneuron death and accelerates motoneuron disease in mice expressing a familial amyotrophic lateral sclerosis mutant SOD1. Neurobiol Dis 7:623-643.
34. Jablonka S, Schrank B, Kralewski M, Rossoll W, Sendtner M. 2000. Reduced survival motor neuron (Smn) gene dose in mice leads to motor neuron degeneration: an animal model for spinal muscular atrophy type III. Hum Mol Genet 9:341-346.
35. Kaspar BK, Llado J, Sherkat N, Rothstein JD, Gage FH. 2003. Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model. Science 301:839-842.
36. LaMonte BH, Wallace KE, Holloway BA, Shelly SS, Ascano J, Tokito M, Van Winkle T, Howland DS, Holzbaur EL. 2002. Disruption of dynein/dynactin inhibits axonal transport in motor neurons causing late-onset progressive degeneration. Neuron 34:715-727.
37. Lefebvre S, Burglen L, Reboullet S, Clermont O, Burlet P, Viollet L, Benichou B, Cruaud C, Millasseau P, Zeviani M. 1995. Identification and characterization of a spinal muscular atrophy-determining gene. Cell 80:155-165.
38. Lerner EA, Lerner MR, Janeway CA Jr, Steitz JA. 1981. Monoclonal antibodies to nucleic acid-containing cellular constituents: probes for molecular biology and autoimmune disease. Proc Natl Acad Sci USA 78:2737-2741.
39. Liu Q, Dreyfuss G. 1996. A novel nuclear structure containing the survival of motor neurons protein. EMBO J 15:3555-3565.
40. Liu Q, Fischer U, Wang F, Dreyfuss G. 1997. The spinal muscular atrophy disease gene product, SMN, and its associated protein SIP1 are in a complex with spliceosomal snRNP proteins. Cell 90:1013-1021.
41. Lorson CL, Hahnen E, Androphy EJ, Wirth B. 1999. A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy. Proc Natl Acad Sci USA 96:6307-6311.
42. Markus A, Zhong J, Snider WD. 2002. Raf and akt mediate distinct aspects of sensory axon growth. Neuron 35:65-76.
43. Martin N, Jaubert J, Gounon P, Salido E, Haase G, Szatanik M, Guenet JL. 2002. A missense mutation in Tbce causes progressive motor neuronopathy in mice. Nat Genet 32: 443-447.
44. Masu Y, Wolf E, Holtmann B, Sendtner M, Brem G, Thoenen H. 1993. Disruption of the CNTF gene results in motor neuron degeneration. Nature 365:27-32.
45. Meister G, Eggert C, Fischer U. 2002. SMN-mediated assembly of RNPs: a complex story. Trends Cell Biol 12:472-478.
46. Messer A, Plummer J, Maskin P, Coffin JM, Frankel WN. 1992. Mapping of the motor neuron degeneration (mnd) gene, a mouse model of amyotrophic lateral sclerosis (ALS). Genomics 18:797-802.
47. Mohr E, Richter D. 2000. Axonal mRNAs: functional significance in vertebrates and invertebrates. J Neurocytol 29:783-791.
48. Monani UR, Lorson CL, Parsons DW, Prior TW, Androphy EJ, Burghes AH, McPherson JD. 1999. A single nucleotide difference that alters splicing patterns distinguishes the SMA gene SMN1 from the copy gene SMN2. Hum Mol Genet 8:1177-1183.
49. Monani UR, Pastore MT, Gavrilina TO, Jablonka S, Le TT, Andreassi C, DiCocco JM, Lorson C, Androphy EJ, Sendtner M, et al. 2003. A transgene carrying an A2G missense mutation in the SMN gene modulates phenotypic severity in mice with severe (type I) spinal muscular atrophy. J Cell Biol 160:41-52.
50. Monani UR, Sendtner M, Coovert DD, Parsons DW, Andreassi C, Le TT, Jablonka S, Schrank B, Rossol W, Prior TW, et al. 2000. The human centromeric survival motor neuron gene (SMN2) rescues embryonic lethality in Smn(-/-) mice and results in a mouse with spinal muscular atrophy. Hum Mol Genet 9:333-339.
51. Mourelatos Z, Abel L, Yong J, Kataoka N, Dreyfuss G. 2001 SMN interacts with a novel family of hnRNP and spliceosomal proteins. EMBO J 20:5443-5452.
52. Oppenheim RW, Wiese S, Prevette D, Armanini M, Wang S, Houenou LJ, Holtmann B, Gotz R, Pennica D, Sendtner M. 2001. Cardiotrophin-1, a muscle-derived cytokine, is required for the survival of subpopulations of developing motoneurons. J Neurosci 21:1283-1291.
53. Pellizzoni L, Kataoka N, Charroux B, Dreyfuss G. 1998. A novel function for SMN, the spinal muscular atrophy disease gene product, in pre-mRNA splicing. Cell 95: 615-624.
54. Puls I, Jonnakuty C, LaMonte BH, Holzbaur EL, Tokito M, Mann E, Floeter MK, Bidus K, Drayna D, Oh SJ, et al. 2003. Mutant dynactin in motor neuron disease. Nat Genet 33:455-456.
55. Raoul C, Estevez AG, Nishimune H, Cleveland DW, deLa-peyriere O, Henderson CE, Haase G, Pettmann B. 2002. Motoneuron death triggered by a specific pathway downstream of Fas, potentiation by ALS-linked SOD1 mutations. Neuron 35:1067-1083.
56. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O'Regan JP, Deng H-X, et al. 1993. Mutation in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362:59-62.
57. Ross AF, Oleynikov Y, Kislauskis EH, Taneja KL, Singer RH. 1997. Characterization of a beta-actin mRNA zipcode-binding protein. Mol Cell Biol 17:2158-2165.
58. Rossoll W, Kroning AK, Ohndorf UM, Steegborn C, Jablonka S, Sendtner M. 2002. Specific interaction of Smn, the spinal muscular atrophy determining gene product, with hnRNP-R and gry-rbp/hnRNP-Q: a role for Smn in RNA processing in motor axons? Hum Mol Genet 11: 93-105.
59. Sagot Y, Dubois Dau: Increased accumulation of transferrin by motor neurons of the mouse mutant progressive motor neuronopathy (pmn/pmn), Moos T. 1995. Bcl-2 overexpression prevents motoneuron cell body loss but not axonal degeneration in a mouse model of a neurodegenerative disease. J Neurocytol 24:389-398.
60. Sagot Y, Dubois Dau: Increased accumulation of transferrin by motor neurons of the mouse mutant progressive motor neuronopathy (pmn/pmn), Moos T. 1995. Bcl-2 overexpression prevents motoneuron cell body loss but not axonal degeneration in a mouse model of a neurodegenerative disease. J Neurocytol 24:389-398.
61. Sagot Y, Rosse T, Vejsada R, Perrelet D, Kato AC. 1998. Differential effects of neurotrophic factors on motoneuron retrograde labeling in a murine model of motoneuron disease. J Neurosci 18:1132-1141.
62. Sagot Y, Tan SA, Hammang JP, Aebischer P, Kato AC. 1996. GDNF slows loss of motoneurons but not axonal degeneration or premature death of pmn/pmn mice. J Neurosci 16:2335-2341.
63. Schmalbruch H, Jensen HJS, Bjaerg M, Kamieniecka Z, Kurland L. 1991. A new mouse mutant with progressive motor neuronopathy. J Neuropathol Exp Neurol 50:192-204.
64. Schrank B, Gotz R, Gunnersen JM, Ure JM, Toyka KV, Smith AG, Sendtner M. 1997. Inactivation of the survival motor neuron gene, a candidate gene for human spinal muscular atrophy, leads to massive cell death in early mouse embryos. Proc Natl Acad Sci USA 94:9920-9925.
65. Schweizer U, Gunnersen J, Karch C, Wiese S, Holtmann B, Takeda K, Akira S, Sendtner M. 2002. Conditional gene ablation of Stat3 reveals differential signaling requirements for survival of motoneurons during development and after nerve injury in the adult. J Cell Biol 156:287-297.
66. Sendtner M, Götz R, Holtmann B, Escary J-L, Masu Y, Carroll P, Wolf E, Brehm G, Brulet P, Thoenen H. 1996. Cryptic physiological trophic support of motoneurons by LIF disclosed by double gene targeting of CNTF and LIF. Current Biol 6:686-694.
67. Sendtner M, Schmalbruch H, Stöckli KA, Carroll P, Kreutzberg GW, Thoenen H. 1992. Ciliary neurotrophic factor prevents degeneration of motor neurons in mouse mutant progressive motor neuronopathy. Nature 358:502-504.
68. Shinder GA, Lacourse MC, Minotti S, Durham HD. 2001. Mutant Cu/Zn-superoxide dismutase proteins have altered solubility and interact with heat shock/stress proteins in models of amyotrophic lateral sclerosis. J Biol Chem 276:12791-12796.
69. Snider WD, Zhou FQ, Zhong J, Markus A. 2002. Signaling the pathway to regeneration. Neuron 35:13-16.
70. Sobue G, Sahashi K, Takahashi A, Matsuoka Y, Muroga T, Sobue I. 1983. Degenerating compartment and functioning compartment of motor neurons in ALS: possible process of motor neuron loss. Neurology 33:654-657.
71. Sondermann H, Scheufler C, Schneider C, Hohfeld J, Hartl FU, Moarefi I. 2001. Structure of a Bag/Hsc70 complex: convergent functional evolution of Hsp70 nucleotide exchange factors. Science 291:1553-1557.
72. Song J, Takeda M, Morimoto RI. 2001. Bagl-Hsp70 mediates a physiological stress signaling pathway that regulates Raf-1/ERK and cell growth. Nat Cell Biol 3:276-282.
73. Takeuchi H, Kobayashi Y, Yoshihara T, Niwa J, Doyu M, Ohtsuka K, Sobue G. 2002. Hsp70 and Hsp40 improve neurite outgrowth and suppress intracytoplasmic aggregate formation in cultured neuronal cells expressing mutant SOD1. Brain Res 949:11-22.
74. Wiese S, Metzger F, Holtmann B, Sendtner M. 1999. The role of p75NTR in modulating neurotrophin survival effects in developing motoneurons. Eur J Neurosci 11: 1668-1676.
75. Wiese S, Pei G, Karch C, Troppmair J, Holtmann B, Rapp UR, Sendtner M. 2001. Specific function of B-Raf in mediating survival of embryonic motoneurons and sensory neurons. Nat Neurosci 4:137-142.
76. Yang Y, Hentati A, Deng HX, Dabbagh O, Sasaki T, Hirano M, Hung WY, Ouahchi K, Yan J, Azim AC, et al. 2001. The gene encoding alsin, a protein with three guanine-nucleotide exchange factor domains, is mutated in a form of recessive amyotrophic lateral sclerosis. Nat Genet 29: 160-165.
77. Zhang HL, Eom T, Oleynikov Y, Shenoy SM, Liebelt DA, Dictenberg JB, Singer RH, Bassell GJ. 2001. Neurotrophin-induced transport of a beta-actin mRNP complex increases beta-actin levels and stimulates growth cone motility. Neuron 31:261-275.