A conditioning lesion provides selective protection in a rat model of amyotrophic lateral sclerosis

PLoS ONE

Volumn 4, Issue 10, 2009, Pages

  Franz, Colin K ^a,b   Quach, Eric T ^a   Krudy, Christina A ^a   Federici, Thais ^a   Kliem, Michele A ^a   Snyder, Brooke R ^a   Raore, Bethwel ^a   Boulis, Nicholas M ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; INNERVATION; MOTONEURON; MOTOR PERFORMANCE; NERVE FIBER; NEUROMUSCULAR SYNAPSE; NONHUMAN; RAT; SOMATIC CELL; ANIMAL; CRYOPRESERVATION; DISEASE MODEL; GENETICS; METABOLISM; MUSCLE STRENGTH; NERVOUS SYSTEM INJURY; PATHOLOGY; SPINAL CORD INJURY; TRANSGENIC RAT;

RATTUS;

SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; AXONS; CELL SURVIVAL; CRYOPRESERVATION; DISEASE MODELS, ANIMAL; MOTOR NEURONS; MUSCLE STRENGTH; NEUROMUSCULAR JUNCTION; RATS; RATS, TRANSGENIC; SPINAL CORD INJURIES; SUPEROXIDE DISMUTASE; TRAUMA, NERVOUS SYSTEM;

EID: 70350180220     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007357     Document Type: Article

References (57)

1. Mulder DW, Kurland LT, Offord KP, Beard CM (1986) Familial adult motor neuron disease: amyotrophic lateral sclerosis. Neurology 36: 511-517.
2. Gould TW, Oppenheim RW (2007) Synaptic dysfunction in disease and following injury in the developing and adult nervous system: caveats in the choice of therapeutic intervention. Neurosci Biobehav Rev 31: 1073-1087.
3. Forman DS, McQuarrie IG, Labore FW, Wood DK, Stone LS, et al. (1980) Time course of the conditioning lesion effect on axonal regeneration. Brain Res 182: 180-185.
4. McQuarrie IG, Grafstein B (1973) Axon outgrowth enhanced by a previous nerve injury. Arch Neurol 29: 53-55.
5. Jenq CB, Jenq LL, Bear HM, Coggeshall RE (1988) Conditioning lesions of peripheral nerves change regenerated axon numbers. Brain Res 457: 63-69.
6. McQuarrie IG (1985) Effect of conditioning lesion on axonal sprout formation at nodes of Ranvier. J Comp Neurol 231: 239-249.
7. Chong MS, Woolf CJ, Turmaine M, Emson PC, Anderson PN (1996) Intrinsic versus extrinsic factors in determining the regeneration of the central processes of rat dorsal root ganglion neurons: the influence of a peripheral nerve graft. J Comp Neurol 370: 97-104.
8. Oudega M, Varon S, Hagg T (1994) Regeneration of adult rat sensory axons into intraspinal nerve grafts: promoting effects of conditioning lesion and graft predegeneration. Exp Neurol 129: 194-206.
9. Richardson PM, Issa VM (1984) Peripheral injury enhances central regeneration of primary sensory neurones. Nature 309: 791-793.
10. Nieto-Sampedro M, Kesslak JP, Gibbs R, Cotman CW (1987) Effects of conditioning lesions on transplant survival, connectivity, and function. Role of neurotrophic factors. Ann N Y Acad Sci 495: 108-119.
11. Matsumoto A, Okada Y, Nakamichi M, Nakamura M, Toyama Y, et al. (2006) Disease progression of human SOD1 (G93A) transgenic ALS model rats. J Neurosci Res 83: 119-133.
12. Sharp PS, Dick JR, Greensmith L (2005) The effect of peripheral nerve injury on disease progression in the SOD1(G93A) mouse model of amyotrophic lateral sclerosis. Neuroscience 130: 897-910.
13. Mariotti R, Cristino L, Bressan C, Boscolo S, Bentivoglio M (2002) Altered reaction of facial motoneurons to axonal damage in the presymptomatic phase of a murine model of familial amyotrophic lateral sclerosis. Neuroscience 115: 331-335.
14. Ikeda K, Aoki M, Kawazoe Y, Sakamoto T, Hayashi Y, et al. (2005) Motoneuron degeneration after facial nerve avulsion is exacerbated in presymptomatic transgenic rats expressing human mutant Cu/Zn superoxide dismutase. J Neurosci Res 82: 63-70.
15. Kong J, Xu Z (1999) Peripheral axotomy slows motoneuron degeneration in a transgenic mouse line expressing mutant SOD1 G93A. J Comp Neurol 412: 373-380.
16. Kiernan JA, Hudson AJ (1991) Changes in sizes of cortical and lower motor neurons in amyotrophic lateral sclerosis. Brain 114 (Pt 2): 843-853.
17. Kong J, Xu Z (1998) Massive mitochondrial degeneration in motor neurons triggers the onset of amyotrophic lateral sclerosis in mice expressing a mutant SOD1. J Neurosci 18: 3241-3250.
18. Fischer LR, Culver DG, Tennant P, Davis AA, Wang M, et al. (2004) Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp Neurol 185: 232-240.
19. Frey D, Schneider C, Xu L, Borg J, Spooren W, et al. (2000) Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J Neurosci 20: 2534-2542.
20. Atkin JD, Scott RL, West JM, Lopes E, Quah AK, et al. (2005) Properties of slow- and fast-twitch muscle fibres in a mouse model of amyotrophic lateral sclerosis. Neuromuscul Disord 15: 377-388.
21. Pun S, Santos AF, Saxena S, Xu L, Caroni P (2006) Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat Neurosci 9: 408-419.
22. Snider WD, Elliott JL, Yan Q (1992) Axotomy-induced neuronal death during development. J Neurobiol 23: 1231-1246.
23. Kernell D (2006) The motoneurone and its muscle fibres. New York: Oxford.
24. Lambrechts D, Robberecht W, Carmeliet P (2007) Heterogeneity in motoneuron disease. Trends Neurosci 30: 536-544.
25. Dengler R, Konstanzer A, Kuther G, Hesse S, Wolf W, et al. (1990) Amyotrophic lateral sclerosis: macro-EMG and twitch forces of single motor units. Muscle Nerve 13: 545-550.
26. Hegedus J, Putman CT, Gordon T (2007) Time course of preferential motor unit loss in the SOD1 G93A mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 28: 154-164.
27. Hegedus J, Putman CT, Tyreman N, Gordon T (2008) Preferential motor unit loss in the SOD1 G93A transgenic mouse model of amyotrophic lateral sclerosis. J Physiol 586: 3337-3351.
28. Henneman E, Mendell LM (1981) Functional organization of the motoneurone pool and its inputs. In: Brooks VB, ed. Handbook of Physiology. Washington, DC: American Physiology Society. pp 345-442.
29. Nguyen MD, Lariviere RC, Julien JP (2000) Reduction of axonal caliber does not alleviate motor neuron disease caused by mutant superoxide dismutase 1. Proc Natl Acad Sci U S A 97: 12306-12311.
30. Ulfhake B, Kellerth JO (1982) Does alpha-motoneurone size correlate with motor unit type in cat triceps surae? Brain Res 251: 201-209.
31. Gordon T (2009) The role of neurotrophic factors in nerve regeneration. Neurosurg Focus 26: E3.
32. Federici T, Boulis NM (2006) Gene-based treatment of motor neuron diseases. Muscle Nerve 33: 302-323.
33. Gould TW, Enomoto H (2009) Neurotrophic modulation of motor neuron development. Neuroscientist 15: 105-116.
34. Simon M, Terenghi G, Green CJ, Coulton GR (2000) Differential effects of NT-3 on reinnervation of the fast extensor digitorum longus (EDL) and the slow soleus muscle of rat. Eur J Neurosci 12: 863-871.
35. Sterne GD, Coulton GR, Brown RA, Green CJ, Terenghi G (1997) Neurotrophin-3-enhanced nerve regeneration selectively improves recovery of muscle fibers expressing myosin heavy chains 2b. J Cell Biol 139: 709-715.
36. Simon M, Mann D, Coulton G, Terenghi G (2002) Differential tyrosine kinase C mRNA distribution in extensor digitorum longus and soleus motoneurons in adult rats: effect of axotomy and neurotrophin-3 treatment. Neurosci Lett 320: 9-12.
37. Simon M, Porter R, Brown R, Coulton GR, Terenghi G (2003) Effect of NT-4 and BDNF delivery to damaged sciatic nerves on phenotypic recovery of fast and slow muscles fibres. Eur J Neurosci 18: 2460-2466.
38. Sakuma K, Watanabe K, Sano M, Uramoto I, Nakano H, et al. (2001) A possible role for BDNF, NT-4 and TrkB in the spinal cord and muscle of rat subjected to mechanical overload, bupivacaine injection and axotomy. Brain Res 907: 1-19.
39. Beck M, Karch C, Wiese S, Sendtner M (2001) Motoneuron cell death and neurotrophic factors: basic models for development of new therapeutic strategies in ALS. Amyotroph Lateral Scler Other Motor Neuron Disord 2 Suppl 1: S55-68.
40. Edstrom L, Grimby L (1986) Effect of exercise on the motor unit. Muscle Nerve 9: 104-126.
41. Pette D, Vrbova G (1992) Adaptation of mammalian skeletal muscle fibers to chronic electrical stimulation. Rev Physiol Biochem Pharmacol 120: 115-202.
42. Kirkinezos IG, Hernandez D, Bradley WG, Moraes CT (2003) Regular exercise is beneficial to a mouse model of amyotrophic lateral sclerosis. Ann Neurol 53: 804-807.
43. Veldink JH, Bar PR, Joosten EA, Otten M, Wokke JH, et al. (2003) Sexual differences in onset of disease and response to exercise in a transgenic model of ALS. Neuromuscul Disord 13: 737-743.
44. Kaspar BK, Frost LM, Christian L, Umapathi P, Gage FH (2005) Synergy of insulin-like growth factor-1 and exercise in amyotrophic lateral sclerosis. Ann Neurol 57: 649-655.
45. Bello-Haas VD, Florence JM, Kloos AD, Scheirbecker J, Lopate G, et al. (2007) A randomized controlled trial of resistance exercise in individuals with ALS. Neurology 68: 2003-2007.
46. Drory VE, Goltsman E, Reznik JG, Mosek A, Korczyn AD (2001) The value of muscle exercise in patients with amyotrophic lateral sclerosis. J Neurol Sci 191: 133-137.
47. Pinto AC, Alves M, Nogueira A, Evangelista T, Carvalho J, et al. (1999) Can amyotrophic lateral sclerosis patients with respiratory insufficiency exercise? J Neurol Sci 169: 69-75.
48. Veldink JH, Kalmijn S, Groeneveld GJ, Titulaer MJ, Wokke JH, et al. (2005) Physical activity and the association with sporadic ALS. Neurology 64: 241-245.
49. Chio A, Benzi G, Dossena M, Mutani R, Mora G (2005) Severely increased risk of amyotrophic lateral sclerosis among Italian professional football players. Brain 128: 472-476.
50. Scarmeas N, Shih T, Stern Y, Ottman R, Rowland LP (2002) Premorbid weight, body mass, and varsity athletics in ALS. Neurology 59: 773-775.
51. Strickland D, Smith SA, Dolliff G, Goldman L, Roelofs RI (1996) Physical activity, trauma, and ALS: a case-control study. Acta Neurol Scand 94: 45-50.
52. Armon C (2007) Sports and trauma in amyotrophic lateral sclerosis revisited. J Neurol Sci 262: 45-53.
53. Qureshi MM, Hayden D, Urbinelli L, Ferrante K, Newhall K, et al. (2006) Analysis of factors that modify susceptibility and rate of progression in amyotrophic lateral sclerosis (ALS). Amyotroph Lateral Scler 7: 173-182.
54. Longstreth WT, McGuire V, Koepsell TD, Wang Y, van Belle G (1998) Risk of amyotrophic lateral sclerosis and history of physical activity: a population-based case-control study. Arch Neurol 55: 201-206.
55. Howland DS, Liu J, She Y, Goad B, Maragakis NJ, et al. (2002) Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS). Proc Natl Acad Sci U S A 99: 1604-1609.
56. Franz CK, Federici T, Yang J, Backus C, Oh SS, et al. (2009) Intraspinal cord delivery of IGF-I mediated by adeno-associated virus 2 is neuroprotective in a rat model of familial ALS. Neurobiol Dis 33: 473-481.
57. Basso DM, Beattie MS, Bresnahan JC (1995) A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12: 1-21.