Motor neuron degeneration after sciatic nerve avulsion in adult rat evolves with oxidative stress and is apoptosis

Journal of Neurobiology

Volumn 40, Issue 2, 1999, Pages 185-201

  Martin, Lee J ^a   Kaiser, Adeel ^a   Price, Ann C ^a  

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

Author keywords

Amyotrophic lateral sclerosis; Axotomy; Mitochondria; Neuronal cell death; Target deprivation

Indexed keywords

ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AVULSION INJURY; DNA DAMAGE; DNA DETERMINATION; MALE; NERVE CELL DEGENERATION; NERVE INJURY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SCIATIC NERVE; SPINAL CORD MOTONEURON;

EID: 0032864716     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(sici)1097-4695(199908)40:2<185::aid-neu5>3.0.co;2-%23     Document Type: Article

References (62)

1. Al-Abdulla NA, Portera-Cailliau C, Martin LJ. 1998. Occipital cortex ablation in adult rat causes retrograde neuronal death in the lateral geniculate nucleus that resembles apoptosis. Neuroscience 86:191-209.
2. Al-Abdulla NA, Martin LJ. 1998. Apoptosis of retrogradely degenerating neurons occurs in association with the accumulation of perikaryal mitochondria and oxidative damage to the nucleus. Am J Pathol 153:447-456.
3. Blümcke S, Neidorf HR, Rode J. 1966. Axoplasmic alterations in the proximal and distal stumps of transsected nerves. Acta Neuropathol 7:44-61.
4. Boveris A, Cadenas E. 1997. Cellular sources and steady-state levels of reactive oxygen species. In: Biadasz Clerch L, Massaro DJ, editors. Oxygen, gene expression, and cellular function. New York: Marcel Dekker. p 1-25.
5. Chu-Wang I-W, Oppenheim RW. 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.
6. Clarke PGH. 1990. Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol 181:195-213.
7. Conradi S. 1969. Ultrastructure of dorsal root boutons on lumbosacral motoneurons of the adult cat as revealed by dorsal root section. Acta Physiol Scand 332(Suppl):85-115.
8. Cork LC, Troncoso JC, Klavano GG, Johnsen ES, Sternberger LA, Sternberger NH, Price DL. 1988. Neurofilamentous abnormalities in motor neurons in spontaneously occurring animal disorders. J Neuropathol Exp Neurol 47:420-431.
9. Dal Canto MC, Gurney ME. 1994. Development of central nervous system pathology in a murine transgenic model of human amyotrophic lateral sclerosis. Am J Pathol 145:1271-1280.
10. Deshmukh M, Vasilakos J, Deckwerth TL, Lampe PA, Shivers BD, Johnson EM. 1996. Genetic and metabolic status of NGF-deprived sympathetic neurons saved by an inhibitor of ICE family proteases. J Cell Biol 135:1341-1354.
11. Devasagayam TPA, Steenken S, Obendorf MSW, Schultz WA, Sies H. 1991. Formation of 8-hydroxy(deoxy)-guartosine and generation of strand breaks at guanine residues in DNA by singlet oxygen. Biochemistry 30: 6283-6289.
12. Estévez AG, Spear N, Manuel SM, Radi R, Henderson CE, Barbeito L, Beckman JS. 1998. Nitric oxide and superoxide contribute to motor neuron apoptosis induced by trophic factor deprivation. J Neurosci 18:923-931.
13. Fraga CG, Shigenaga MK, Park J-W, Degan P, Ames BN. 1990. Oxidative damage to DNA during aging: 8-hydroxy-2′-deoxyguanosine in rat organ DNA and urine. Proc Natl Acad Sci USA 87:4533-4537.
14. Friedlander RM, Brown RH, Gagliardini V, Wang J, Juan, J. 1997. Inhibition of ICE slows ALS in mice. Nature 388:31.
15. Fry FJ, Cowan WM. 1972. A study of retrograde cell degeneration in the lateral mammillary nucleus of the cat, with special reference to the role of axonal branching in the preservation of the cell. J Comp Neurol 144:1-24.
16. Gavrieli Y, Sherman Y, Ben-Sasson SA. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493-501.
17. Gerschenson LE, Rotello RJ. 1992. Apoptosis: a different type of cell death. FASEB J 6:2450-2455.
18. Ginsberg SD, Martin LJ. 1998. Ultrastructural analysis of the progression of neurodegeneration in the septum following fimbria-fornix transection. Neuroscience 86:1259-1272.
19. Ginsberg SD, Portera-Cailliau C, Martin LJ. 1999. Fimbria-fornix transection and excitotoxicity produce similar neurodegeneration in the septum. Neuroscience 88:1059-1071.
20. Hamburger V. 1975. Cell death in the development of the lateral motor column of the chick embryo. J Comp Neurol 160:535-546.
21. Hartmann JF. 1954. Electron microscopy of motor nerve cells following section of axones. Anat Rec 118:19-33.
22. Hockenbery DM, Oltavi ZN, Yin X-M, Milliman CL, Korsmeyer SL. 1993. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75:241-252.
23. Ikonomidou C, Qin YQ, Labruyere J, Olney, JW. 1996. Motor neuron degeneration induced by excitotoxin agonists has features in common with those seen in the SOD-1 transgenic mouse model of amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 55:211-224.
24. Inoue S, Kawanishi S. 1995. Oxidative DNA damage induced by simultaneous generation of nitric oxide and superoxide. FEBS Lett 371:86-88.
25. Kasai H, Nishimura S. 1984. Hydroxylation of deoxyguanosine at the C-8 position by ascorbic acid and other reducing agents. Nucleic Acids Res 12:2137-2145.
26. Kerr JFR, Harmon BV. 1991. Definition and incidence of apoptosis: an historical perspective. In: Tomei LD, Cope FO, editors. Apoptosis: the molecular basis of cell death. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. p 5-29.
27. Koliatsos VE, Price WL, Pardo CA, Price DL. 1994. Ventral root avulsion: an experimental model of death of adult motor neurons. J Comp Neurol 342:35-44.
28. Kostic V, Jackson-Lewis V, de Bilbao F, Dubois-Dauphin M, Przedborski S. 1997. Bcl-2: prolonging life in a transgenic mouse model of familial amyotrophic lateral sclerosis. Science 277:559-562.
29. Kroemer G, Petit P, Zamzami N, Vayssière J-L, Mignotte B. 1995. The biochemistry of programmed cell death. FASEB J 9:1277-1287.
30. Kuchino Y, Mori F, Kasai H, Inoue H, Iwai S, Miura K, Ohtsuka E, Nishimura S. 1987. Misreading of DNA templates containing 8-hydroxydeoxyguanosine at the modified base and at adjacent residues. Nature 327:77-79.
31. Li L, Wu W, Lin LF, Oppenheim RW, Houenou LJ. 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.
32. Li L, Houenou LJ, Wu W, Lei M, Prevette DM, Oppenheim RW. 1998. Characterization of spinal motoneuron degeneration following different types of peripheral nerve injury in neonatal and adult mice. J Comp Neurol 396:158-168.
33. Lieberman AR. 1971. The axon reaction: a review of the principal features of perikaryal responses to axon injury. Int Rev Neurobiol 14:49-124.
34. Liu D, Yang R, Yan X, McAdoo DJ. 1994. Hydroxyl radicals generated in vivo kill neurons in the rat spinal cord: electrophysiological, histological, and neurochemical results. J Neurochem 62:37-44.
35. Lowrie MB, Vrbová; G. 1992. Dependence of postnatal motoneurones on their targets: review and hypothesis. Trends Neurosci 15:80-84.
36. Manetto V, Sternberger NH, Perry G, Sternberger LA, Gambetti P. 1988. Phosphorylation of neurofilaments is altered in amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 47:642-653.
37. Martin LJ. 1999. Neuronal death in amyotrophic lateral sclerosis is apoptosis: possible contribution of a programmed cell death mechanism. J Neuropathol Exp Neurol 58:459-471.
38. Martin LJ, Portera-Cailliau C, Ginsberg SD, Al-Abdulla NA. 1998a. Animal models and degenerative disorders of the human brain. Lab Animal 27:18-25.
39. Martin LJ, Al-Abdulla NA, Brambrink AM, Kirsch JR, Sieber FE, Portera-Cailliau C. 1998b. Neurodegeneration in excitotoxicity, global cerebral ischemia, and target deprivation: a perspective on the contributions of apoptosis and necrosis. Brain Res Bull 46:281-309.
40. McLaughlin B. 1972. Dorsal root projections to the motor nuclei in the cat spinal cord. J Comp Neurol 144:429-460.
41. Milligan CE, Prevette D, Yaginuma H, Homma S, Cardwell C, Fritz LC, Tomaselli KJ, Oppenheim RW, Schwartz LM. 1995. Peptide inhibitors of the ICE protease family arrest programmed cell death of motoneurons in vivo and in vitro. Neuron 15:385-393.
42. Munoz DG, Greene C, Perl DP, Selkoe DJ. 1988. Accumulation of phosphorylated neurofilaments in anterior horn motor neurons of amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 47:9-18.
43. Nicolopoulos-Stournaras S, Iles JF. 1983. Motor neuron columns in the lumbar spinal cord of the rat. J Comp Neurol 217:75-85.
44. Novikov L, Novikova L, Kellerth J-O. 1995. Brain-derived neurotrophic factor promotes survival and blocks nitric oxide synthase expression in adult rat spinal motoneurons after ventral root avulsion. Neurosci Lett 200:45-48.
45. Novikov L, Novikova L, Kellerth J-O. 1997. Brain-derived neurotrophic factor promotes axonal regeneration and long-term survival of adult rat spinal motoneurons in vivo. Neuroscience 79:765-774.
46. Pittman RN, Wang S, DiBenedetto AJ, Mills JC. 1993. A system for characterizing cellular and molecular events in programmed neuronal cell death. J Neurosci 13:3669-3680.
47. Portera-Cailliau C, Price DL, Martin LJ. 1997a. 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.
48. Portera-Cailliau C, Price DL, Martin LJ. 1997b. Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J Comp Neurol 378: 70-87.
49. Price DL, Martin LJ, Clatterbuck RE, Koliatsos VE, Sisodia SS, Walker LC, Cork LC. 1992. Neuronal degeneration in human diseases and animal models. J Neurobiol 23: 1277-1294.
50. Price DL, Porter KR. 1972. The response of ventral horn neurons to axonal transection. J Cell Biol 53:24-37.
51. Ramón y Cajal S. 1928. Degeneration and regeneration of the nervous system. NewYork: Oxford University Press 769 p.
52. Ratan RR, Murphy TH, Baraban JM. 1994. Oxidative stress induces apoptosis in embryonic cortical neurons. J Neurochem 62:376-379.
53. Romanes GJ. 1946. Motor localization and the effects of nerve injury on the ventral horn cells of the spinal cord. J Anat 80:117-131.
54. Sen S. 1992. Programmed cell death: concept, mechanism and control. Biol Rev 67:287-319.
55. Torvik A. 1976. Central chromatolysis and the axon reaction: a reappraisal. Neuropathol Appl Neurobiol 2:423-432.
56. Torvik A, Heding A. 1969. Effect of actinomycin D on retrograde nerve cell reaction: further observations. Acta Neuropathol 14:62-71.
57. Weiss P, Pillai A. 1965. Convection and fate of mitochondria in nerve fibers: axonal flow as vehicle. Proc Natl Acad Sci USA 54:48-56.
58. Wong-Riley MTT. 1979. Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res 171: 11-28.
59. Wood KA, Youle RJ. 1995. The role of free radicals and p53 in neuron apoptosis in vivo. J Neurosci 15:5851-5857.
60. Wu W. 1993. Expression of nitric oxide synthase (NOS) in injured CNS neurons as shown by NADPH diaphorase histochemistry. Exp Neurol 120:153-159.
61. Wu W, Li L. 1993. Inhibition of nitric oxide synthase reduces motoneuron death due to spinal root avulsion. Neurosci Lett 153:121-124.
62. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng T-I, Jones DP, Wang X. 1997. Prevention of apoptosis by bcl-2: release of cytochrome c from mitochondria blocked. Science 275, 1129-1132.