Characterization of spinal motoneuron degeneration following different types of peripheral nerve injury in neonatal and adult mice

Journal of Comparative Neurology

Volumn 396, Issue 2, 1998, Pages 158-168

  Li, Linxi ^a,c   Houenou, Lucien J ^a   Wu, Wutian ^b   Lei, Ming ^a   Prevette, David M ^a   Oppenheim, Ronald W ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Apoptosis; Avulsion; Axotomy; Injury; Motoneuron death; Necrosis

Indexed keywords

DNA FRAGMENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AVULSION INJURY; CONTROLLED STUDY; MOUSE; NERVE CELL DEGENERATION; NERVE CELL NECROSIS; NERVE FIBER TRANSECTION; NEWBORN; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; SPINAL CORD MOTONEURON;

EID: 0032578036     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(sici)1096-9861(19980629)396:2<158::aid-cne2>3.0.co;2-%23     Document Type: Article

References (54)

1. Arends, M.J., R.G. Morris, and A.H. Wyllie (1990) Apoptosis. The role of the endonucleases. Am. J. Pathol. 136:593-608.
2. Barres, B.A., I.K. Hart, H. Coles, J.F. Burne, J.T. Boyvodic, W.D. Richardson, and M.C. Raff (1992) Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70:31-46.
3. Berkelaar, M., D.B. Clarke, Y.-C. Wang, G.M. Bray, and A.J. Aguayo (1994) Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J. Neurosci. 14:4368-4374.
4. Bonfoco, E., D. Krainc, M. Ankarcrona, P. Nicotera, and S.A. Lipton (1995) Apoptosis and necrosis: Two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/ superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. USA 92:7162-7166.
5. Brown, R.H., Jr. (1995) Amyotrophic lateral sclerosis: Recent insights from genetics and transgenic mice. Cell 80:687-692.
6. Calderò, J., D. Ciutat, J. Liado, E. Castan, R.W. Oppenheim, and J.E. Esquerda (1997) Effects of excitatory amino acids on neuromuscular development in the chick embryo. J. Comp. Neurol. 387:73-95.
7. Charriaut-Marlangue, C., D. Aggoun-Zouaoui, A. Represa, and Y. Ben-Ari (1996) Apoptotic features of selective neuronal death in ischemia, epilepsy and gp 120 toxicity. Trends Neurosci. 19:109-114.
8. Choi, D.W. (1996) Ischemia-induced neuronal apoptosis. Curr. Opin. Neurobiol. 6:667-672.
9. Chu-Wang, I.-W. and R.W. Oppenheim (1978) Cell death of motoneurons in the chick embryo spinal cord. I. A light and electron microscopic study of naturally occurring and induced cell loss during development. J. Comp. Neurol. 177:33-58.
10. Clarke, P.G.H (1990) Developmental cell death: Morphological diversity and multiple mechanisms. Anat. Embryol. 181:195-213.
11. Clarke, P.G.H (1998) Apoptosis versus necrosis, how valid a dichotomy for neurons. In V. Koliatosis and R. Ratan (eds): Cell Death in Diseases of the Nervous System. Totowa, NJ: Humana Press, pp. 3-28.
12. Clarke, P.G.H. and R.W. Oppenheim (1995) Neuron death in vertebrate development: In vivo methods. Methods Cell Biol. 46:277-321.
13. Cohen, J.J. and C. Duke (1992) Apoptosis and programmed cell death in immunity. Annu. Rev. Immunol. 10:267-293.
14. Cuitat, D., J. Calderò, R.W. Oppenheim, and J.E. Esquerda (1996) Schwann cell apoptosis during normal development and after axonal degeneration induced by neurotoxins in the chick embryo. J. Neurosci. 16:3979-3990.
15. Dal Canto, M.C. and M.E. Gurney (1994) Development of central nervous system pathology in a murine transgenic model of human amyotrophic lateral sclerosis. Am. J. Pathol. 145:1271-1279.
16. Duvall, E. and A.H. Wyllie (1986) Death and the cell. Immunol. Today 7:115-119.
17. Ellis, R.E., J. Yuan, and R. Horvitz (1991) Mechanisms and functions of cell death. Annu. Rev. Cell Biol. 7:663-698.
18. Garcia-Valenzuela, E., W. Gorczyca, Z. Darzynkiewicz, and S.C. Sharma (1994) Apoptosis in adult retinal ganglion cells after axotomy. J. Neurobiol. 25:431-438.
19. Gavrieli, Y., Y. Sherman, and S.A. Ben-Sasson (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:493-501.
20. Kashihara, Y., M. Kuno, and Y. Miyata (1987) Cell death of axotomized motoneurons in neonatal rats, and its prevention by peripheral reinnervation. J. Physiol. (London) 386:135-148.
21. Kerr, J.F.R., A.H. Wyllie, and A.R. Currie (1972) Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26:239-257.
22. Kishino, A., Y. Ishige, T. Tatsuno, C. Nakayama, and H. Naguchi (1997) BDNF prevents and reverses adult rat motor neuron degeneration and induces axonal outgrowth. Exp. Neurol. 144:273-286.
23. Koliatsos, V.E., W.L. Price, C.A. Pardo, and D.L. Price (1994) Ventral root avulsion: An experimental model of death of adult motor neurons. J. Comp. Neurol. 342:35-44.
24. Li, L., R.W. Oppenheim, M. Lei, and L.J. Houenou (1994) Neurotrophic agents prevent motoneuron death following sciatic nerve section in the neonatal mouse. J. Neurobiol. 25:759-766.
25. Li, L., W. Wu, L.F.H. Lin, M. Lei, R.W. Oppenheim, and L.J. Houenou (1995) Rescue of adult mouse motoneurons from injury-induced cell death by glial cell line-derived neurotrophic factor. Proc. Natl. Acad. Sci. USA 92:9771-9775.
26. Lipton, J.W., E.D. Potter, D.E. Ewwse-Mayer, and P.M. Carvey (1996) Cocaine kills dopamine neurons in vitro by either apoptosis and/or necrosis: A possible uterine position phenomenon in fetal rats. Soc. Neurosci. Abstr. 22:1884.
27. Munson, J.B., D.L. Shelton, and S.B. McMahon (1997) Adult mammalian sensory and motor neurons: Roles of endogenous neurotrophins and rescue by exogenous neurotrophins after axotomy. J. Neurosci. 17:470-476.
28. Noven, S.V., N. Wallace, D. Muccio, A. Turtz, and M.J. Pinter (1993) Adult spinal motoneurons remain viable despite prolonged absence of functional synaptic contact with muscle. Exp. Neurol. 123:147-156.
29. Novikov, L., L. Novikova, and J. Kellerth (1997) Brain-derived neurotrophic factor promotes axonal regeneration and long-term survival of adult rat spinal motoneurons in vivo. Neuroscience 79:765-774.
30. Oppenheim, R.W. (1986) The absence of significant postnatal motoneuron death in the brachial and lumbar spinal cord of the rat. J. Comp. Neurol. 246:281-286.
31. Oppenheim, R.W., Houenou, L., Pincon-Raymond, M., Powell, J.A., Rieger, F. and Standish, L.J. (1986) The development of motoneurons in the embryonic spinal cord of the mouse mutant, muscular dysgenesis (mdg/mdg): Survival, morphology and biochemical differentiation. Dev. Biol. 114:426-436.
32. Oppenheim, R.W. (1991) Cell death during development of the nervous system. Annu. Rev. Neurosci. 14:453-501.
33. Oppenheim, R.W., I.-W. Chu-Wang, and J.L. Maderdrut (1978) Cell death of motoneurons in the chick embryo spinal cord. III. The differentiation of motoneurons prior to their induced degeneration following limb-bud removal. J. Comp. Neurol. 177:87-112.
34. Plaitakis, A. and P. Shashidharan (1995) Amyotrophic lateral sclerosis, glutamate, and oxidative stress. In F.E. Bloom and D.J. Kupfer (eds): Psychopharmacology: The Fourth Generation of Progress. New York: Raven Press, pp. 1531-1543.
35. Pollin, M.M., S. McHanwell, and C.R. Slater (1991) The effect of age on motor neuron death following axotomy in the mouse. Development 112:83-89.
36. Portera-Cailliau, C., D.L. Price, and L.J. Martin (1997a) Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J. Comp. Neurol. 378:70-87.
37. Portera-Cailliau, C., D.L. Price, and L.J. Martin (1997b) Non-NMDA and NMDA receptor-mediated excitotoxic neuronal deaths in adult brain are morphologically distinct: Further evidence for an apoptosis-necrosis continuum. J. Comp. Neurol. 378:88-104.
38. Rabacchi, S.A., L. Bonfanti, X.-H. Liu, and L. Maffei (1994) Apoptotic cell death induced by optic nerve lesion in the neonatal rat. J. Neurosci. 14:5292-5301.
39. Raff, M.C. (1992) Social controls on cell survival and cell death. Nature 356:397-400.
40. Rossiter, J.P., R.J. Riopelle, and M.A. Bisby (1996) Axotomy-induced apoptotic cell death of neonatal rat facial motoneurons: Time course analysis and relation to NADPH-diaphorase activity. Exp. Neurol. 138:33-44.
41. Rothstein, J.D., L. Jin, M. Dikes-Horberg, and R.W. Kuncl (1993) Chronic inhibition of glutamate uptake produces a model of slow neurotoxicity. Proc. Natl. Acad. Sci. USA 90:6591-6595.
42. Schmalbruch, H. (1988) The effect of peripheral nerve injury on immature motor and sensory neurons and on muscle fibers. Possible relation to the histogenesis of Werdnig-Hoffmann disease. Rev.Neurol. 144:721-9.
43. Schwartz, L.M., S.W. Smith, M.E. Jones, and B.A. Osborne (1993) Do all programmed cell deaths occur via apoptosis? Proc. Natl. Acad. Sci. USA 90:980-984.
44. Searle, J., J.F. Kerr, and C.J. Bishop (1982) Necrosis and apoptosis: Distinct modes of cell death with fundamentally different significance. Pathol. Annu. 2:229-259.
45. Snider, W.D., J.L. Elliott, and Q. Yan (1992) Axotomy-induced neuronal death during development. J. Neurobiol. 23:1231-1246.
46. Thompson, C.B. (1995) Apoptosis in the pathogenesis and treatment of disease. Science 267:1456-1462.
47. Vejsada, R., Y. Sagot, and A.C. Kato (1994) BDNF-mediated rescue of axotomized motoneurons decreases with increasing dose. Neuroreport 5:1889-92.
48. Vejsada, R., Y. Sagot, and A.C. Kato (1995) Quantitative comparison of the transient rescue effects of neurotrophic factors on axotomized motoneurons in vivo. Eur. J. Neurosci. 7:108-115.
49. Wong, P.C., C.A. Pardo, D.R. Borchelt, M.K. Lee, N.G. Copeland, N.A. Jenkins, S.S. Sisodia, D.W. Cleveland, and D.L. Price (1995) An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 14:1105-1116.
50. Wu, W. (1993) Expression of nitric oxide synthase (NOS) in injured CNS neurons as shown by NADPH diaphorase histochemistry. Exp. Neurol. 120:153-159.
51. Wu, W., L. Li, J.O. Penix, Y. Gu, H. Liu, D.M. Prevette, L.J. Houenou, and R.W. Oppenheim (1995) GDNF and BDNF inhibit the induction of NOS and prevent the death of adult rat spinal motoneurons following root avulsion. Soc. Neurosci. Abstr. 21:279.
52. Wyllie, A.H. (1987) Cell death. Int. Rev. Cytol. 17:755-785.
53. Wyllie, A.H., J.F.R. Kerr, and A.R. Currie (1980) Cell death: The significance of apoptosis. Int. Rev. Cytol. 68:251-300.
54. Zeman, S., B. Lioyd, B. Meldrum, and P.N. Leigh (1994) Excitatory amino acids, free radicals and the pathogenesis of motor neuron disease. Neuropathol. Appl. Neurobiol. 20:219-231.