Primary cortical motor neurons undergo apoptosis after axotomizing spinal cord injury

Journal of Comparative Neurology

Volumn 462, Issue 3, 2003, Pages 328-341

  Hains, Bryan C ^a,b   Black, Joel A ^a,b   Waxman, Stephen G ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CT Vet Admin Healthcare System   (United States)

Author keywords

Cell death; Locomotor; Motor cortex; Neuronal survival; Neurotrauma; Paralysis

Indexed keywords

CASPASE 3; DNA; HOE 33342; PROTEIN BAX;

ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL SURVIVAL; HISTOLOGY; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MALE; MOTOR CORTEX; NERVE CELL NECROSIS; NEUROTRAUMATOLOGY; NICK END LABELING; NONHUMAN; PARALYSIS; PRIORITY JOURNAL; RAT; SPINAL CORD INJURY;

ANIMALS; APOPTOSIS; AXOTOMY; BCL-2-ASSOCIATED X PROTEIN; CASPASE 3; CASPASES; ELECTROPHORESIS, AGAR GEL; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; MALE; MOTOR CORTEX; MOTOR NEURONS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRAMIDAL TRACTS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD INJURIES;

EID: 0038649642     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10733     Document Type: Article

References (93)

1. Abe Y, Yamamoto T, Sugiyama Y, Watanabe T, Saito N, Kayama H, Kumagai T. 1999. Apoptotic cells associated with Wallerian degeneration after experimental spinal cord injury: a possible mechanism of oligodendroglial death. J Neurotrauma 16:945-952.
2. Abusaad I, MacKay D, Zhao J, Stanford P, Collier DA, Everall IP. 1999. Stereological estimation of the total number of neurons in the murine hippocampus using the optical disector. J Comp Neurol 408:560-566.
3. Aroniadou VA, Keller A. 1993. The patterns and synaptic properties of horizontal intracortical connections in the rat motor cortex. J Neurophysiol 70:1553-1569.
4. Baba N, Koji T, Itoh M, Mizuno A. 1999. Reciprocal changes in the expression of Bcl-2 and Bax in hypoglossal nucleus after axotomy in adult rats: possible involvement in the induction of neuronal cell death. Brain Res 827:122-129.
5. Barres BA, Raff MC. 1993. Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 361:258-260.
6. Barron KD, Dentinger MP, Popp AJ, Mankes R. 1988. Neurons of layer Vb of rat sensorimotor cortex atrophy but do not die after thoracic cord transection. J Neuropathol Exp Neurol 47:62-74.
7. Basso DM, Beattie MS, Bresnahan JC. 1996. Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Exp Neurol 139:244-256.
8. Blight AR. 1983. Cellular morphology of chronic spinal cord injury in the cat: analysis of myelinated axons by line-sampling. Neuroscience 10: 521-543.
9. Blits B, Dijkhuizen PA, Boer GJ, Verhaagen J. 2000. Intercostal nerve implants transduced with an adenoviral vector encoding neurotrophin-3 promote regrowth of injured rat corticospinal tract fibers and improve hindlimb function. Exp Neurol 164:25-37.
10. Bonatz H, Rohrig S, Mestres P, Meyer M, Giehl KM. 2000. An axotomy model for the induction of death of rat and mouse corticospinal neurons in vivo. J Neurosci Methods 100:105-115.
11. Bregman BS, Kunkel-Bagden E, Schnell L, Dai HN, Gao D, Schwab ME. 1995. Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature 378:498-501.
12. Bregman BS, McAtee M, Dai HN, Kuhn PL. 1997. Neurotrophic factors increase axonal growth after spinal cord injury and transplantation in the adult rat. Exp Neurol 148:475-494.
13. Brosamle C, Schwab ME. 1997. Cells of origin, course, and termination patterns of the ventral, uncrossed component of the mature rat corticospinal tract. J Comp Neurol 386:293-303.
14. Charriaut-Marlangue C, Ben-Ari Y. 1995. A cautionary note on the use of the TUNEL stain to determine apoptosis. Neuroreport 7:61-64.
15. Collins JA, Schandi CA, Young KK, Vesely J, Willingham MC. 1997. Major DNA fragmentation is a late event in apoptosis. J Histochem Cytochem 45:923-934.
16. Cowley KC, Schmidt BJ. 1997. Regional distribution of the locomotor pattern-generating network in the neonatal rat spinal cord. J Neurophysiol 77:247-259.
17. Crowe MJ, Bresnahan JC, Shuman SL, Masters JN, Beattie MS. 1997. Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat Med 3:73-76.
18. D'Amato CJ, Hicks SP. 1980. Development of the motor system: effects of radiation on developing corticospinal neurons and locomotor function. Exp Neurol 70:1-23.
19. de Bilbao F, Dubois-Dauphin M. 1996. Time course of axotomy-induced apoptotic cell death in facial motoneurons of neonatal wild type and bcl-2 transgenic mice. Neuroscience 71:1111-1119.
20. Dietz V, Wirz M, Curt A, Colombo G. 1998. Locomotor pattern in paraplegic patients: training effects and recovery of spinal cord function. Spinal Cord 36:380-390.
21. Eidelberg E, Yu J. 1981. Effects of corticospinal lesions upon treadmill locomotion by cats. Exp Brain Res 43:101-103.
22. Elliott EJ, Parks DA, Fishman PS. 1997. Effect of proximal axotomy on GAP-43 expression in cortical neurons in the mouse. Brain Res 755: 221-228.
23. Fehlings MG, Tator CH. 1995. The relationships among the severity of spinal cord injury, residual neurological function, axon counts, and counts of retrogradely labeled neurons after experimental spinal cord injury. Exp Neurol 132:220-228.
24. Ferguson IA, Xian C, Barati E, Rush RA. 2001. Comparison of wheat germ agglutinin-horseradish peroxidase and biotinylated dextran for anterograde tracing of corticospinal tract following spinal cord injury. J Neurosci Methods 109:81-89.
25. Feringa ER, Vahlsing HL. 1985. Labeled corticospinal neurons one year after spinal cord transection. Neurosci Lett 58:283-286.
26. Feringa ER, Gilbertie WJ, Vahlsing HL. 1984. Histologic evidence for death of cortical neurons after spinal cord transection. Neurology 34: 1002-1006.
27. Frost EE, Buttery PC, Milner R, ffrench-Constant C. 1999. Integrins mediate a neuronal survival signal for oligodendrocytes. Curr Biol 9:1251-1254.
28. 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.
29. Giehl KM, Tetzlaff W. 1996. BDNF and NT-3, but not NGF, prevent axotomy-induced death of rat corticospinal neurons in vivo. Eur J Neurosci 8:1167-1175.
30. Goshgarian HG, Koistinen JM, Schmidt ER. 1983. Cell death and changes in the retrograde transport of horseradish peroxidase in rubrospinal neurons following spinal cord hemisection in the adult rat. J Comp Neurol 214:251-257.
31. Grill R, Murai K, Blesch A, Gage FH, Tuszynski MH. 1997. Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J Neurosci 17: 5560-5572.
32. Grossman SD, Rosenberg LJ, Wrathall JR. 2001. Temporal-spatial pattern of acute neuronal and glial loss after spinal cord contusion. Exp Neurol 168:273-282.
33. Gundersen HJ, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B. 1988. The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96:857-881.
34. Hadi B, Zhang YP, Burke DA, Shields CB, Magnuson DS. 2000. Lasting paraplegia caused by loss of lumbar spinal cord interneurons in rats: no direct correlation with motor neuron loss. J Neurosurg 93:266-275.
35. Hicks SP, D'Amato CJ. 1975. Motor-sensory cortex-corticospinal system and developing locomotion and placing in rats. Am J Anat 143:1-42.
36. Hill CE, Beattie MS, Bresnahan JC. 2001. Degeneration and sprouting of identified descending supraspinal axons after contusive spinal cord injury in the rat. Exp Neurol 171:153-169.
37. Holmes G, May WP. 1909. On the exact origin of the pyramidal tracts in man and other mammals. Brain 33:1-43.
38. Houle JD, Ye JH. 1999. Survival of chronically-injured neurons can be prolonged by treatment with neurotrophic factors. Neuroscience 94: 929-936.
39. Houweling DA, Lankhorst AJ, Gispen WH, Bar PR, Joosten EA. 1998. Collagen containing neurotrophin-3 (NT-3) attracts regrowing injured corticospinal axons in the adult rat spinal cord and promotes partial functional recovery. Exp Neurol 153:49-59.
40. Isenmann S, Engel S, Gillardon F, Bahr M. 1999. Bax antisense oligonucleotides reduce axotomy-induced retinal ganglion cell death in vivo by reduction of Bax protein expression. Cell Death Differ 6:673-682.
41. Kaneko T, Cho R, Li Y, Nomura S, Mizuno N. 2000. Predominant information transfer from layer III pyramidal neurons to corticospinal neurons. J Comp Neurol 423:52-65.
42. Kanellopoulos GK, Kato H, Wu Y, Dougenis D, Mackey M, Hsu CY, Kouchoukos NT. 1997. Neuronal cell death in the ischemic spinal cord: the effect of methylprednisolone. Ann Thorac Surg 64:1279-1285.
43. Kato H, Kanellopoulos GK, Matsuo S, Wu YJ, Jacquin MF, Hsu CY, Kouchoukos NT, Choi DW. 1997. Neuronal apoptosis and necrosis following spinal cord ischemia in the rat. Exp Neurol 148:464-474.
44. Katoh K, Ikata T, Katoh S, Hamada Y, Nakauchi K, Sano T, Niwa M. 1996. Induction and its spread of apoptosis in rat spinal cord after mechanical trauma. Neurosci Lett 216:9-12.
45. Kermer P, Klocker N, Labes M, Thomsen S, Srinivasan A, Bahr M. 1999. Activation of caspase-3 in axotomized rat retinal ganglion cells in vivo. FEBS Lett 453:361-364.
46. Kitanaka C, Kuchino Y. 1999. Caspase-independent programmed cell death with necrotic morphology. Cell Death Differ 6:508-515.
47. Krishnan RV. 1980. Corticospinal tract interaction in locomotor development and motor units formation: an hypothesis. Int J Neurosci 10:89-93.
48. Kuang RZ, Kalil K. 1990. Branching patterns of corticospinal axon arbors in the rodent. J Comp Neurol 292:585-598.
49. Kwon BK, Liu J, Messerer C, Kobayashi NR, McGraw J, Oschipok L, Tetzlaff W. 2002a. Survival and regeneration of rubrospinal neurons 1 year after spinal cord injury. Proc Natl Acad Sci U S A 99:3246-3251.
50. Kwon BK, Liu J, Oschipok L, Tetzlaff W. 2002b. Reaxotomy of chronically injured rubrospinal neurons results in only modest cell loss. Exp Neurol 177:332-337.
51. Landry P, Wilson CJ, Kitai ST. 1984. Morphological and electrophysiological characteristics of pyramidal tract neurons in the rat. Exp Brain Res 57:177-190.
52. Lee YB, Yune TY, Baik SY, Shin YH, Du S, Rhim H, Lee EB, Kim YC, Shin ML, Markelonis GJ, Oh TH. 2000. Role of tumor necrosis factor-alpha in neuronal and glial apoptosis after spinal cord injury. Exp Neurol 166:190-195.
53. Li GL, Farooque M, Holtz A, Olsson Y. 1999. Apoptosis of oligodendrocytes occurs for long distances away from the primary injury after compression trauma to rat spinal cord. Acta Neuropathol 98:473-480.
54. Liang F, Rouiller EM, Wiesendanger M. 1993. Modulation of sustained electromyographic activity by single intracortical microstimuli: comparison of two forelimb motor cortical areas of the rat. Somatosens Mot Res 10:51-61.
55. Liu XZ, Xu XM, Hu R, Du C, Zhang SX, McDonald JW, Dong HX, Wu YJ, Fan GS, Jacquin MF, Hsu CY, Choi DW. 1997. Neuronal and glial apoptosis after traumatic spinal cord injury. J Neurosci 17:5395-5406.
56. Liu Y, Kim D, Himes BT, Chow SY, Schallert T, Murray M, Tessler A, Fischer I. 1999. Transplants of fibroblasts genetically modified to express BDNF promote regeneration of adult rat rubrospinal axons and recovery of forelimb function. J Neurosci 19:4370-4387.
57. Liu Y, Himes BT, Murray M, Tessler A, Fischer I. 2002. Grafts of BDNF-producing fibroblasts rescue axotomized rubrospinal neurons and prevent their atrophy. Exp Neurol 178:150-164.
58. Loy DN, Magnuson DS, Zhang YP, Onifer SM, Mills MD, Cao QL, Darnall JB, Fajardo LC, Burke DA, Whittemore SR. 2002. Functional redundancy of ventral spinal locomotor pathways. J Neurosci 22:315-323.
59. Lu P, Blesch A, Tuszynski MH. 2001. Neurotrophism without neurotropism: BDNF promotes survival but not growth of lesioned corticospinal neurons. J Comp Neurol 436:456-470.
60. McBride RL, Feringa ER, Garver MK, Williams JK. 1989. Prelabeled red nucleus and sensorimotor cortex neurons of the rat survive 10 and 20 weeks after spinal cord transection. J Neuropathol Exp Neurol 48:568-576.
61. McKay Hart A, Brannstrom T, Wiberg M, Terenghi G. 2002. Primary sensory neurons and satellite cells after peripheral axotomy in the adult rat: timecourse of cell death and elimination. Exp Brain Res 142:308-318.
62. Merry DE, Korsmeyer SJ. 1997. Bcl-2 gene family in the nervous system. Annu Rev Neurosci 20:245-267.
63. Migheli A, Attanasio A, Schiffer D. 1995. Ultrastructural detection of DNA strand breaks in apoptotic neural cells by in situ end-labeling techniques. J Pathol 176:27-35.
64. Mori F, Himes BT, Kowada M, Murray M, Tessler A. 1997. Fetal spinal cord transplants rescue some axotomized rubrospinal neurons from retrograde cell death in adult rats. Exp Neurol 143:45-60.
65. Muir GD, Whishaw IQ. 1999. Complete locomotor recovery following corticospinal tract lesions: measurement of ground reaction forces during overground locomotion in rats. Behav Brain Res 103:45-53.
66. Neafsey EJ, Bold EL, Haas G, Hurley-Gius KM, Quirk G, Sievert CF, Terreberry RR. 1986. The organization of the rat motor cortex: a microstimulation mapping study. Brain Res 396:77-96.
67. Neumann S, Woolf CJ. 1999. Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron 23: 83-91.
68. Pallini R, Fernandez E, Sbriccoli A. 1988. Retrograde degeneration of corticospinal axons following transection of the spinal cord in rats. J Neurosurg 68:163-172.
69. Pasikova NV, Marchenko VG, Kositsyn NS. 2001. Structural bases of intracortical processes underlying the synchronization of epileptic potentials in the sensorimotor areas of the neocortex in rats. Neurosci Behav Physiol 31:497-501.
70. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates. 4th ed. San Diego, CA: Academic Press.
71. Portera-Cailliau C, Hedreen JC, Price DL, Koliatsos VE. 1995. Evidence for apoptotic cell death in Huntington disease and excitotoxic animal models. J Neurosci 15:3775-3787.
72. Prendergast J, Stelzner DJ. 1976. Changes in the magnocellular portion of the red nucleus following thoracic hemisection in the neonatal and adult rat. J Comp Neurol 166:163-172.
73. Qiu J, Nesic O, Ye Z, Rea H, Westlund KN, Xu GY, McAdoo D, Hulsebosch CE, Perez-Polo JR. 2001. Bcl-xL expression after contusion to the rat spinal cord. J Neurotrauma 18:1267-1278.
74. Raff MC, Barres BA, Burne JF, Coles HS, Ishizaki Y, Jacobson MD. 1993. Programmed cell death and the control of cell survival: lessons from the nervous system. Science 262:695-700.
75. Sanner CA, Cunningham TJ, Goldberger ME. 1994. NMDA receptor blockade rescues Clarke's and red nucleus neurons after spinal hemisection. J Neurosci 14:6472-6480.
76. Schmued LC, Fallon JH. 1986. Fluoro-gold: a new fluorescent retrograde axonal tracer with numerous unique properties. Brain Res 377:147-154.
77. Schnell L, Schneider R, Kolbeck R, Barde YA, Schwab ME. 1994. Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 367:170-173.
78. Schreyer DJ, Jones EH. 1988. Topographic sequence of outgrowth of corticospinal axons in the rat: a study using retrograde axonal labeling with Fast blue. Brain Res 466:89-101.
79. Schutte A, Yan Q, Mestres P, Giehl KM. 2000. The endogenous survival promotion of axotomized rat corticospinal neurons by brain-derived neurotrophic factor is mediated via paracrine, rather than autocrine mechanisms. Neurosci Lett 290:185-188.
80. Shuman SL, Bresnahan JC, Beattie MS. 1997. Apoptosis of microglia and oligodendrocytes after spinal cord contusion in rats. J Neurosci Res 50:798-808.
81. Smolen AJ, Wright LL, Cunningham TJ. 1983. Neuron numbers in the superior cervical sympathetic ganglion of the rat: a critical comparison of methods for cell counting. J Neurocytol 12:739-750.
82. Springer JE, Azbill RD, Knapp PE. 1999. Activation of the caspase-3 apoptotic cascade in traumatic spinal cord injury. Nat Med 5:943-946.
83. Theriault E, Tator CH. 1994. Persistence of rubrospinal projections following spinal cord injury in the rat. J Comp Neurol 342:249-258.
84. Thornberry NA, Lazebnik Y. 1998. Caspases: enemies within. Science 281:1312-1316.
85. Tseng GF, Prince DA. 1993. Heterogeneity of rat corticospinal neurons. J Comp Neurol 335:92-108.
86. Vanderluit JL, McPhail LT, Fernandes KJ, McBride CB, Huguenot C, Roy S, Robertson GS, Nicholson DW, Tetzlaff W. 2000. Caspase-3 is activated following axotomy of neonatal facial motoneurons and caspase-3 gene deletion delays axotomy-induced cell death in rodents. Eur J Neurosci 12:3469-3480.
87. Von Meyenburg J, Brosamle C, Metz GA, Schwab ME. 1998. Regeneration and sprouting of chronically injured corticospinal tract fibers in adult rats promoted by NT-3 and the mAb IN-1, which neutralizes myelin-associated neurite growth inhibitors. Exp Neurol 154:583-594.
88. Warden P, Bamber NI, Li H, Esposito A, Ahmad KA, Hsu CY, Xu XM. 2001. Delayed glial cell death following wallerian degeneration in white matter tracts after spinal cord dorsal column cordotomy in adult rats. Exp Neurol 168:213-224.
89. Weidner N, Ner A, Salimi N, Tuszynski MH. 2001. Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. Proc Natl Acad Sci U S A 98:3513-3518.
90. Willingham MC. 1999. Cytochemical methods for the detection of apoptosis. J Histochem Cytochem 47:1101-1110.
91. Yong C, Arnold PM, Zoubine MN, Citron BA, Watanabe I, Berman NE, Festoff BW. 1998. Apoptosis in cellular compartments of rat spinal cord after severe contusion injury. J Neurotrauma 15:459-472.
92. Zhang C, Siman R, Xu Y, Mills A, Frederick J, Neumar R. 2002. Comparison of calpain and caspase activities in the adult rat brain after transient forebrain ischemia. Neurobiol Dis 10:289.
93. Zurita M, Vaquero J, Oya S, Morales C. 2002. Effects of dexamethasone on apoptosis-related cell death after spinal cord injury. J Neurosurg 96: 83-89.