Autonomic and Motor Neuron Death Is Progressive and Parallel in a Lumbosacral Ventral Root Avulsion Model of Cauda Equina Injury

Journal of Comparative Neurology

Volumn 467, Issue 4, 2003, Pages 477-486

  Hoang, Thao X ^a   Nieto, Jaime H ^a   Tillakaratne, Niranjala J K ^b   Havton, Leif A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis; Caspase; Choline acetyltransferase; Parasympathetic; Rat

Indexed keywords

CASPASE 3;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTONOMIC NERVOUS SYSTEM; AVULSION INJURY; CAUDA EQUINA SYNDROME; CHROMATIN CONDENSATION; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; LUMBOSACRAL PLEXUS; MALE; MOTONEURON; NERVE CELL DEGENERATION; NERVE FIBER TRANSECTION; NEUROPROTECTION; NONHUMAN; PARASYMPATHETIC NERVE CELL; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; VENTRAL ROOT;

ANIMALS; AUTONOMIC PATHWAYS; BISBENZIMIDE; CASPASE 3; CASPASES; CELL COUNT; CELL DEATH; CELL NUCLEUS; CELL SIZE; CHOLINE O-ACETYLTRANSFERASE; DISEASE MODELS, ANIMAL; FLUORESCENT DYES; IMMUNOHISTOCHEMISTRY; LAMINECTOMY; LUMBOSACRAL REGION; MALE; MOTOR NEURONS; POLYRADICULOPATHY; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; STILBAMIDINES; TIME FACTORS;

EID: 0345017009     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10928     Document Type: Article

References (71)

1. Ambalavanar R, Morris R. 1989. Fluoro-gold injected either subcutaneously or intravascularly results in extensive retrograde labelling of CNS neurons having axons terminating outside the blood-brain barrier. Brain Res 505:171-175.
2. Anderson CR. 1992. NADPH diaphorase-positive neurons in the rat spinal cord include a sub-population of autonomic preganglionic neurons. Neurosci Lett 139:280-284.
3. Anneser JMH, Berhele A, Borasio GD, Castro-Lopes JM, Zieglgä nsberger W, Tölle TR. 2000. Axotomy of the sciatic nerve differentially affects expression of metabotropic glutamate receptor mRNA in adult motoneurons. Brain Res 868:215-221.
4. Armstrong DM, Brady R, Hersh LB, Hayes RC, Wiley RG. 1991. Expression of choline acetyltransferase and nerve growth factor receptor within hypoglossal motoneurons following nerve injury. J Comp Neurol 304:596-607.
5. Barber RP, Phelps PE, Houser CR, Crawford GD, Salvaterra PM, Vaughn JE. 1984. The morphology and distribution of neurons containing choline acetyltransferase in the adult rat spinal cord: an immunocytochemical study. J Comp Neurol 229:329-346.
6. Beattie MS, Farooqui AA, Bresnahan JC. 2000. Review of current evidence for apoptosis after spinal cord injury. J Neurotrauma 17:915-925.
7. Beric A, Light JK. 1992. Function of the conus medullaris and cauda equina in the early period following spinal cord injury and the relationship to recovery of detrusor function. J Urol 148:1845-1848.
8. Brännström T, Havton L, Kellerth J-O. 1992. Changes in size and dendritic arborization patterns of adult cat spinal alpha-motoneurons following permanent axotomy. J Comp Neurol 318:439-451.
9. Brook GA, Schmitt AB, Nacimiento W, Weis J, Schrøder JM, Noth J. 1998. Distribution of B-50 (GAP-43) mRNA and protein in the normal adult human spinal cord. Acta Neuropathol (Berl) 95:378-386.
10. Bussmann KA, Sofroniew MV. 1999. Re-expression of p75NTR by adult motor neurons after axotomy is triggered by retrograde transport of a positive signal from axons regrowing through damaged or denervated peripheral nerve tissue. Neuroscience 91:273-281.
11. Carlson J, Lais AC, Dyck PJ. 1979. Axonal atrophy from permanent peripheral axotomy in adult cat. J Neuropathol Exp Neurol 38:579-585.
12. Carlstedt T, Lindå H, Cullheim S, Risling M. 1986. Reinnervation of hindlimb muscles after ventral root avulsion and implantation in the lumbar spinal cord of the adult rat. Acta Physiol Scand 128:645-646.
13. Chan YM, Wu W, Yip HK, So KF, Oppenheim RW. 2001. Caspase inhibitors promote the survival of avulsed spinal motoneurons in neonatal rats. Neuroreport 12:541-545.
14. Chin CH, Chew KC. 1997. Lumbosacral nerve root avulsion. Injury 28:674-678.
15. Citron BA, Arnold PM, Sebastian C, Qin F, Malladi S, Ameenuddin S, Landis ME, Festoff BW. 2000. Rapid upregulation of caspase-3 in rat spinal cord after injury: mRNA, protein, and cellular localization correlates with apoptotic cell death. Exp Neurol 166:213-226.
16. Coggeshall RE, Lekan HA. 1996. Methods for determining numbers of cells and synapses: a case for more uniform standards of review. J Comp Neurol 364:6-15.
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. Cryns V, Yuan J. 1998. Proteases to die for. Genes Dev 12:1551-1570.
19. Delgado-Garcia JM, Del Pozo F, Spencer RF, Baker RV. 1988. Behavior of neurons in the abducens nucleus of the alert cat. III. Axotomized motoneurons. Neuroscience 24:143-160.
20. Emery E, Aldana P, Bunge MB, Puckett W, Srinivasan A, Keane RW, Bethea J, Levi AD. 1998. Apoptosis after traumatic human spinal cord injury. J Neurosurg 89:911-920.
21. Johnson IP, Sears TA. 1989. Organelle changes in cat thoracic alpha- and gamma-motoneurons following axotomy. Brain Res 489:400-405.
22. Johnson I, Pullen A, Sears T. 1985. Target dependence of Nissl body ultrastructure in cat thoracic motoneurones. Neurosci Lett 61:201-205.
23. Johnson IP, Sears TA, Hunter AS. 1991. Retrograde response to axotomy of motoneurons in the thoracic spinal cord of the aging cat. Neurobiol Aging 12:151-160.
24. Kishino A, Ishige Y, Tatsuno T, Nakayama C, Noguchi H. 1997. BDNF prevents and reverses adult rat motor neuron degeneration and induces axonal outgrowth. Exp Neurol 144:273-286.
25. Koliatsos VE, Price WL, Pardo CA, Price DL. 1994a. Ventral root avulsion: an experimental model of death of adult motor neurons. J Comp Neurol 342:35-44.
26. Koliatsos VE, Price DL, Clatterbuck RE. 1994b. Motor neurons in Onuf's nucleus and its rat homologues express the p75 nerve growth factor receptor: sexual dimorphism and regulation by axotomy. J Comp Neurol 345:510-527.
27. Kou SY, Chiu AY, Patterson PH. 1995. Differential regulation of motor neuron survival and choline acetyltransferase expression following axotomy. J Neurobiol 27:561-572.
28. Lams BE, Isacson O, Sofroniew MV. 1988. Loss of transmitter-associated enzyme staining following axotomy does not indicate death of brainstem cholinergic neurons. Brain Res 475:401-406.
29. Leong SK, Ling EA. 1990. Labeling neurons with fluorescent dyes administered via intravenous, subcutaneous or intraperitoneal route. J Neurosci Methods 32:15-24.
30. 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.
31. Liu Z, Martin LJ. 2001. Motor neurons rapidly accumulate DNA single-strand breaks after in vitro exposure to nitric oxide and peroxynitrite and in vivo axotomy. J Comp Neurol 432:35-60.
32. Lowrie MB, Vrbova G. 1992. Dependence of postnatal motoneurones on their targets: review and hypothesis. TINS 15:80-84.
33. Ma J, Novikov LN, Wiberg M, Kellerth J-O. 2001. Delayed loss of spinal motoneurons after peripheral nerve injury in adult rats: a quantitative morphological study. Exp Brain Res 139:216-223.
34. Mannen T, Iwata M, Toyokura Y, Nagashima K. 1977. Preservation of a certain motoneurone group of the sacral cord in amyotrophic lateral sclerosis: its clinical significance. J Neurol Neurosurg Psychiatry 40:464-469.
35. Mannen T, Iwata M, Toyokura Y, Nagashima K. 1982. The Onuf's nucleus and the external anal sphincter muscles in amyotrophic lateral sclerosis and Shy-Drager syndrome. Acta Neuropathol (Berl) 58:255-260.
36. Marks N, Berg MJ. 1999. Recent advances on neuronal caspases in development and neurodegeneration. Neurochem Int 35:195-220.
37. Martin LJ, Liu Z. 2002. Injury-induced spinal motor neuron apoptosis is preceded by DNA single-strand breaks and is p53- and Bax-dependent. J Neurobiol 50:181-197.
38. Martin LJ, Kaiser A, Price AC. 1999. Motor neuron degeneration after sciatic nerve avulsion in adult rat evolves with oxidative stress and is apoptosis. J Neurobiol 40:185-201.
39. Michael GJ, Kaya E, Averill S, Rattray M, Clary DO, Priestley JV. 1997. TrkA immunoreactive neurones in the rat spinal cord. J Comp Neurol 385:441-455.
40. Molander C, Grant G. 1995. Spinal cord cytoarchitecture. In: Paxinos G, editor. The rat nervous system. San Diego: Academic Press.
41. Molander C, Xu Q, Grant G. 1984. The cytoarchitectonic organization of the spinal cord in the rat. I. The lower thoracic and lumbosacral cord. J Comp Neurol 230:133-141.
42. Moossy JJ, Nashold BSJ, Osborne D, Friedman AH. 1987. Conus medullaris nerve root avulsions. J Neurosurg 66:835-841.
43. Moschilla G, Song S, Chakera T. 2001. Post-traumatic lumbar nerve root avulsion. Austral Radiol 45:281-284.
44. Nacimiento W, Topper R, Fischer A, Mobius E, Oestreicher AB, Gispen WH, Nacimiento AC, Noth J, Kreutzberg GW. 1993. B-50 (GAP-43) in Onuf's nucleus of the adult cat. Brain Res 613:80-87.
45. Nicolopoulos-Stournaras S, Iles JF. 1983. Motor neuron columns in the lumbar spinal cord of the rat. J Comp Neurol 217:75-85.
46. 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.
47. Novikova L, Novikov L, Kellerth J-O. 1997. Persistent neuronal labeling by retrograde fluorescent tracers: a comparison between Fast Blue, Fluoro-Gold and various dextran conjugates. J Neurosci Methods 74:9-15.
48. Novikov LN, Novikova LN, Holmberg P, Kellerth J-O. 2000. Exogenous brain-derived neurotrophic factor regulates the synaptic composition of axonally lesioned and normal adult rat motoneurons. Neuroscience 100:171-181.
49. Pavlakis AJ, Siroky MB, Goldstein I. 1983. Neurologic findings in conus medullaris and cauda equina injury. Arch Neurol 40:570-573.
50. Piehl F, Tabar G, Cullheim S. 1995. Expression of NMDA receptor mRNAs in rat motoneurons is down-regulated after axotomy. Eur J Neurosci 7:2101-2110.
51. Pikov V, Wrathall JR. 2001. Coordination of the bladder detrusor and the external urethral sphincter in a rat model of spinal cord injury: effect of injury severity. J Neurosci 21:559-569.
52. Price DL, Porter KR. 1972. The response of ventral horn neurons to axonal transection. J Cell Biol 53:24-37.
53. Puigdellivol-Sánchez A, Valero-Cabre A, Prats-Galino A, Navarro X, Molander C. 2002. On the use of fast blue, fluoro-gold and diamidino yellow for retrograde tracing after peripheral nerve injury: uptake, fading, dye interactions, and toxicity. J Neurosci Methods 115:115-127.
54. Rende M, Giambanco I, Buratta M, Tonali P. 1995. Axotomy induces a different modulation of both low-affinity nerve growth factor receptor and choline acetyltransferase between adult rat spinal and brainstem motoneurons. J Comp Neurol 363:249-263.
55. Rexed B. 1954. A cytoarchitectonic analysis of the spinal cord in the cat. J Comp Neurol 100:297-380.
56. Romanes GJ. 1951. The motor cell columns of the lumbo-sacral spinal cord of the cat. J Comp Neurol 94:313-363.
57. Sampson JH, Cashman RE, Nashold BSJ, Friedman AH. 1995. Dorsal root entry zone lesions for intractable pain after trauma to the conus medullaris and cauda equina. J Neurosurg 82:28-34.
58. Schmalbruch H. 1984. Motoneuron death after sciatic nerve lesion in newborn rats. J Comp Neurol 224:252-258.
59. Schrøder HD. 1980. Organization of the motoneurons innervating the pelvic muscles of the male rat. J Comp Neurol 192:567-587.
60. Sherrington CS. 1892. Notes on the arrangement of some motor fibers in the lumbo-sacral plexus. J Physiol (Lond) 13:621-772.
61. Sindou M, Mertens P, Wael M. 2001. Microsurgical DREZotomy for pain due to spinal cord and/or cauda equina injuries: long-term results in a series of 44 patients. Pain 92:159-171.
62. Springer JE, Azbill RD, Knapp PE. 1999. Activation of the caspase-3 apoptotic cascade in traumatic spinal cord injury. Nat Med 5:943-946.
63. Taylor TK, Coolican MJ. 1988. Injuries of the conus medullaris. Paraplegia 26:393-400.
64. Ulfhake B, Kellerth J-O. 1984. Electrophysiological and morphological measurements in cat gastrocnemius and soleus alpha-motoneurones. Brain Res 307:167-179.
65. Vanden Noven S, Wallace N, Muccio D, Turtz A, Pinter MJ. 1993. Adult spinal motoneurons remain viable despite prolonged absence of functional synaptic contact with muscle. Exp Neurol 123:147-156.
66. Vanderhorst VG, Holstege G. 1997. Organization of lumbosacral motoneuronal cell groups innervating hindlimb, pelvic floor, and axial muscles in the cat. J Comp Neurol 382:46-76.
67. Vizzard MA, Erdman SL, de Groat WC. 1993. The effect of rhizotomy on NADPH diaphorase staining in the lumbar spinal cord of the rat. Brain Res 607:349-353.
68. Vizzard MA, Erdman SL, de Groat WC. 1995. Increased expression of neuronal nitric oxide synthase (NOS) in visceral neurons after nerve injury. J Neurosci 15:4033-4045.
69. West MJ. 1999. Stereological methods for estimating the total number of neurons and synapses: issues of precision and bias. TINS 22:51-61.
70. Wu W. 1993. Expression of nitric-oxide synthase (NOS) in injured CNS neurons as shown by NADPH diaphorase histochemistry. Exp Neurol 120:153-159.
71. Wu CW, Kaas JH. 2000. Spinal cord atrophy and reorganization of motoneuron connections following long-standing limb loss in primates. Neuron 28:967-978.