The Effect of Cauda Equina Constriction on Nitric Oxide Synthase Activity

Neurochemical Research

Volumn 29, Issue 2, 2004, Pages 429-439

  Lukáčová, Nadežda ^a   Kafka, Jozef ^b   Čížková, Dáša ^a   Maršala, Martin ^c   Maršala, Jozef ^a  

^a INSTITUTE OF CHEMISTRY   (Slovakia)

^b Med Faculty of Safarik University   (Slovakia)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dog; Multiple cauda equina constrictions; Nitric oxide synthase; Spinal cord regions

Indexed keywords

NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAUDA EQUINA SYNDROME; CONTROLLED STUDY; DOG; ENZYME ACTIVITY; GRAY MATTER; IMMUNOREACTIVITY; LUMBAR SPINE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SACRUM; SPINAL CORD DORSAL HORN; SPINAL CORD LESION; SPINAL CORD VENTRAL HORN; SPINAL GANGLION; THORACIC SPINE; WHITE MATTER;

ANIMALS; CAUDA EQUINA; CONSTRICTION; DOGS; FEMALE; LUMBAR VERTEBRAE; MALE; NITRIC OXIDE SYNTHASE; SACRUM; SPINAL CORD; THORACIC VERTEBRAE; TISSUE DISTRIBUTION;

ANIMALIA; CANIS FAMILIARIS;

EID: 10744225695     PISSN: 03643190     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:NERE.0000013748.93150.21     Document Type: Article

References (85)

1. Aho, A. J., Auranen, A., and Personen, K. 1969. Analysis of cauda equina symptoms in patients with lumbar disc prolapse. Acta Chir. Scand. 135:413-420.
2. Floman, Y., Wiesel, S. W., and Rothman, R. H. 1980. Cauda equina syndrome presenting as a lumbar disk. Clin. Orthop. Rel. Res. 147:234-237.
3. Rhein, F., Audic, B., Bor, Y., and Perrigot, M. 1985. Étude clinique de la récuperation des syndromes de la queue de cheval par hernie discale: Ápropos de 65 cas. Ann. Readapt. Med. Phys. 28:153-168.
4. Kostuik, J. P., Harrington, I., Alexander, D., Rand, W., and Evans, D. 1986. Cauda equina syndrome and lumbar disc herniation. J. Bone Joint Surg. 68A:386-391.
5. Humphrey, P. R. D. 1990. Degenerative and inflammatory diseases of the spine: Neurological consequences. Curr. Opin. Neurol. Neurosurg. 3:576-580.
6. Byrne, T. N. 1993. Disorders of the spinal cord and cauda equina [Editorial overview]. Curr. Opin. Neurol. Neurosurg. 6:545-548.
7. Jaradeh, S. 1993. Cauda equina syndrome: A neurologist's perspective. Region. Anesth. 18:473-480.
8. Shapiro, S. 1993. Cauda equina syndrome secondary to lumbar disc herniation. Neurosurgery 32:743-747.
9. Leroi, A. M., Berkelmans, I., Rabehenoina, C., Creissard, P., and Weber, J. 1994. Résultats de la prise en charge thérapeutique des troubles vésico-sphinctériens et ano-rectaux de 20 patients ayant un syndrome de la queue de cheval. Neurochirurgie (Paris) 40:301-306.
10. Drábek, P. 1995. Topografie caudae equinae: Diagnostické hledisko. Čes. a Slov. Neurol. Neurochir. 58:263-265.
11. Orendáčová, J., Čížková, D., Kafka, J., Lukáčová, N., Maršala, M., Šulla, I., Maršala, J., and Katsube, N. 2001. Cauda equina syndrome. Prog. Neurobiol. 64:613-637.
12. Kawakami, M. and Tamaki, T. 1992. Morphologic and quantitative changes in neurotransmitters in the lumbar spinal cord after acute or chronic mechanical compression of the cauda equina. Spine 17:13-17.
13. Iwamoto, H., Kuwahara, H., Matsuda, H., Noriage, A., and Yamano, Y. 1995. Production of chronic compression of the cauda equina in rats for use in studies of lumbar spinal canal stenosis. Spine 20:2750-2757.
14. Sayegh, F. E., Kapetanos, G. A., Symeonides, P. P., Anogiannakis, G., and Madentzidis, M. 1997. Functional outcome after experimental cauda equina compression. J. Bone Joint Surg. 79:670-674.
15. Yamamoto, K., Ishikawa, T., Takenobu, Y., Katsube, N., and Marsala, M. 1997. OP-1206 a prostaglandin E1 derivate ameliorates motor/sensory dysfunction and improve local spinal cord blood flow in rat spinal canal stenosis model. Soc. Neurosci. 23:923-3.
16. Yamaguchi, K., Murakami, M., Takahashi, K., Moriya, H., Tatsuoka, H., and Chiba, T. 1999. Behavioral and morphologic studies of the chronically compressed cauda equina: Experimental model of lumbar spinal stenosis in the rat. Spine 24:845-851.
17. Delamarter, R. B., Bohlman, H. H., Bodner, D., and Biro, C. 1990. Neurologic function after experimental cauda equina compression: Cystometrograms versus cortical-evoked potentials. Spine 15:864-870.
18. Konno, S., Yabuki, S., Sato, K., Olmarker, K., and Kikuchi, S. 1995. A model for acute, chronic and delayed graded compression of the dog cauda equina: Presentation of the gross, microscopic and vascular anatomy of the dog cauda equina and accuracy in pressure transmission of the compression model. Spine 20:2758-2764.
19. Mao, G. P., Konno, S., Arai, I., Olmarker, K., and Kukuchi, S. 1998. Chronic double-level cauda equina compression: An experimental study on the dog cauda equina with analyses of nerve conduction velocity. Spine 23:1641-1644.
20. Sato, K., Konno, S., Yabuki, S., Mao, G. P., Olmarker, K., and Kikuchi, S. 1995. A model for acute, chronic, and delayed graded compression of the dog cauda equina: Neurophysiologic and histologic changes induced by acute, graded compression. Spine 22:2386-2391.
21. Yoshizawa, H., Kobayashi, S., and Morita, T. 1995. Chronic nerve root compression: Pathophysiologic mechanism of nerve root dysfunction. Spine 20:397-407.
22. Sato, K. and Kikuchi, S. 1997. Clinical analysis of two-level compression of the cauda equina and the nerve roots in lumbar spinal canal stenosis. Spine 22:1898-1904.
23. Olmarker, K., Rydevik, B., and Holm, S. 1989. Edema formation in spinal nerve roots induced by experimental, graded compression: An experimental study on the pig cauda equina with special reference to differences in effects between rapid and slow onset of compression. Spine 14:569-573.
24. Olmarker, K., Rydevik, B., Holm, S., and Bagge, U. 1989. Effects of experimental graded compression on blood flow in spinal nerve roots: A vital microscopic study on the porcine cauda equina. J. Orthop. Res. 7:817-823.
25. Pedowitz, R. A., Rydevik, B. L., Swenson, M. R., Hargens, A. R., Massie, J. B., Myers, R. R., and Garfin, S. R. 1989. Differential recovery of motor and sensory nerve root conduction following 2 or 4 hours of graded compression of the pig cauda equina, Read at the Annual Meeting of the International Society for the Study of the Lumbar Spine, Kyoto, Japan, May 17.
26. Olmarker, K., Holm, S., and Rydevik, B. 1990. More pronounced effects of double level compression than single level compression on impulse propagation in the porcine cauda equina, Presented to the International Society for the Study of the Lumbar Spine, Boston.
27. Olmarker, K., Rydevik, B., Hansson, T., and Holm, S. 1990. Compression-induced changes of the nutritional supply to the porcine cauda equina. J. Spinal Disord. 3:25-29.
28. Garfin, S. R., Cohen, M. S., Massie, J. B., Abitbol, J. J., Swenson, M. R., Myers, R. R., and Rydevik, B. L. 1990. Nerve-roots of the cauda equina: The effect of hypotension and acute graded compression on function. J. Bone Joint Surg. 72:1185-1192.
29. Olmarker, K., Takahashi, K., and Rydevik, B. 1992. Anatomy and compression: Pathophysiology of the nerve roots of the lumbar spine. Pages 77-90, in Anderson, G. B. J. and MacNeill, T. (eds.), Spinal Stenosis, Mosby, St. Louis.
30. Rydevik, B. 1993. Neurophysiology of cauda equina compression. Acta Orthop. Scand. (Suppl. 251) 64:52-55.
31. Cornefjord, M., Olmarker, K., Rydevik, B., and Nordborg. C. 1996. Mechanical and biochemical injury of spinal nerve roots: A morphological and neurophysiological study. Eur. Spine J. 5:187-192.
32. Cornefjord, M., Sato, K., Olmarker, K., Rydevik, B., and Nordborg, C. 1997. A model for chronic nerve root compression studies: Presentation of a porcine model for controlled, slow-onset compression with analyses of anatomic aspects, compression onset rate, and morphologic and neurophysiologic effects. Spine 22:946-957.
33. Maršala, J., Šulla, I., Jalč, P., and Orendáčová, J. 1995. Multiple protracted cauda equina constrictions cause deep derangement in the lumbosacral spinal cord circuitry in the dog. Neurosci. Lett. 193:97-100.
34. Huang, E. P. 1997. Synaptic plasticity: A role for nitric oxide in LTP. Curr. Biol. 7:R141-R143.
35. Callsen-Cencic, P., Hoheisel, U., Kaske, A., Mense, S., and Tenschert, S. 1999. The controversy about spinal neuronal nitric oxide synthase: Under which conditions is it up- or downregulated? Cell Tissue Res. 295:183-194.
36. Keilhoff, G., Fansa, H., and Wolf, G. 2002. Neuronal nitric oxide synthase is the dominant nitric oxide supplier for the survival of dorsal root ganglia after peripheral nerve axotomy. J. Chem. Neuroanat. 24:181-187.
37. Norris, P. J., Faull, R. L., and Emson, P. C. 1996. Neuronal nitric oxide synthase (nNOS) mRNA expression and NADPH-diaphorase staining in the frontal cortex, visual cortex and hippocampus of control and Alzheimer's disease brains. Brain Res. Mol. Brain Res. 41:36-49.
38. Vodovotz, Y., Lucia, M. S., Flanders, K. C., Chesler, L., Xie, Q. W., Smith, T. W., Weidner, J., Mumford, R., Webber, R., Nathan, C., Roberts, A. B., Lippa, C. F., and Sporn, M. B. 1996. Inducible nitric oxide synthase in tangle-bearing neurons of patients with Alzheimer's disease. J. Exp. Med. 184:1425-1433.
39. Barger, S. W. and Harmon, A. D. 1997. Microglial activation by Alzheimer amyloid precursor protein and modulation by apolipoprotein E. Nature 388:878-881.
40. Meller, S. T., Pechman, P. S., Gebhart, G. F., and Maves, T. J. 1992. Nitric oxide mediates the thermal hyperalgesia produced in a model of neuropathic pain in the rat. Neuroscience 50:7-10.
41. Meller, S. T., Cummings, C. P., Traub, R. J., and Gebhart, G. F. 1994. The role of nitric oxide in the development and maintenance of the hyperalgesia produced by intraplantar injection of carrageenan in the rat. Neuroscience 60:367-374.
42. Wiertelak, E. P., Furness, L. E., Watkins, L. R., and Maier, S. F. 1994. Illness-induced hyperalgesia is mediated by a spinal NMDA-nitric oxide cascade. Brain Res. 664:9-16.
43. Salter, M., Strijbos, P. J., Neale, S., Duffy, C., Follenfant, R. L., and Garthwaite, J. 1996. The nitric oxide-cyclic GMP pathway is required for nociceptive signalling at specific loci within the somatosensory pathway. Neuroscience 73:649-655.
44. Maršala, J., Vanický, I., Maršala, M., Jalč, P., Orendáčová, J., and Taira, Y. 1998. Reduced nicotinamide adenine dinucleotide phosphate diaphorase in the spinal cord of dogs. Neuroscience 85:847-862.
45. Maršala, J., Maršala, M., Vanický, I., and Taira, Y. 1999. Localization of NADPHd exhibiting neurons in the spinal cord of the rabbit. J. Comp. Neurol. 406:263-284.
46. Orendáčová, J., Maršala, M., Šulla, I., Kafka, J., Jalč, P., Čížková, D., Taira, Y., and Maršala, J. 2000. Incipient cauda equina syndrome as a model of somatovisceral pain in dogs: Spinal cord structures involved as revealed by the expression of c-fos and NADPH diaphorase activity. Neuroscience 95:543-557.
47. Orendáčová, J., Maršala, M., Čížková, D., Kafka, J., Račeková, E., šulla, I., Vanický, I., and Mařala, J. 2001. Fos protein expression in sacral spinal cord in relation to early phase of cauda equina syndrome in dogs. Cell. Mol. Neurobiol. 21:413-419.
48. Lukàčová, N., Čížková, D., Maršala, M., Lukáč, I., and Maršala, J. 2002. The regional distribution of nitric oxide synthase activity in the spinal cord of the dog. Brain Res. Bull. 58:173-178.
49. Hoheisel, U., Kaske, A., Reinert, A., and Mense, S. 1997. Frequency-dependent expression of diaphorase staining and nNOS-immunoreactivity in rat dorsal horn neurones following C-fibre stimulation. Neurosci. Lett. 227:181-184.
50. Kaske, A., Klimaschewski L., Mense S. 1998. Stimulation of C-fibres but not A-fibres induces an increase in the expression of nNOS-mRNA, in rat dorsal horn neurons. Eur. J. Physiol. (Pflügers Archiv.) 435(Suppl):R:156.
51. Onozawa, T., Atsuta, Y., Sato, M., Ikawa, M., Tsunekawa, H., and Feng, X. 2003. Nitric oxide induced ectopic firing in a lumbar nerve root with cauda equina compression. Clin. Orthop. 408:167-173.
52. Bredt, D. S. and Snyder, S. H. 1990. Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc. Natl. Acad. Sci. USA 87:682-685.
53. Strosznajder, J. and Chalimoniuk, M. 1996. Biphasic enhancement of nitric oxide synthase activity and cGMP level following brain ischemia in gerbils. Acta Neurobiol. Exp. (Warsz.) 56:71-81.
54. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
55. Bredt, D. S., Hwang, P. M., and Snyder, S. H. 1990. Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347:768-770.
56. Herbison, A. E., Simonian, S. X., Norris, P. J., and Emson, P. C. 1996. Relationship of neuronal nitric oxide immunoreactivity to GnRH neurons in the ovariectomized and intact female rat. J. Neuroendocrinol. 8:73-82.
57. Coderre, T. J. and Yashpal, K. 1994. Intracellular messengers contributing to persistent nociception and hyperalgesia induced by L-glutamate and substance P in the rat formalin pain model. Eur. J. Neurosci. 6:1328-1334.
58. Herdegen, T., Rudiger, S., Mayer, B., Bravo, R., and Zimmermann, M. 1994. Expression of nitric oxide synthase and colocalisation with Jun, Fos and Krox transcription factors in spinal cord neurons following noxious stimulation of the rat hindpaw. Mol. Brain Res. 22:245-258.
59. Kawabata, A., Manabe, S., Manabe, Y., and Takagi, H. 1994. Effect of topical administration of L-arginine on formalin-induced nociception in the mouse: A dual role of peripherally formed NO in pain modulation. Br. J. Pharmacol. 112:547-550.
60. Abbott, F. V., Franklin, K. B., and Westbrook, R. F. 1995. The formalin test: Scoring properties of the first and second phases of the pain response in rats. Pain 60:91-102.
61. Puig, S., and Sorkin, L. S. 1996. Formalin-evoked activity in identified primary afferent fibers: Systemic lidocaine suppresses phase-2 activity. Pain 64:345-355.
62. Lam, H. H., Hanley, D. F., Trapp, B. D., Saito, S., Raja, S., Dawson, T. M., and Yamaguchi, H. 1996. Induction of spinal cord neuronal nitric oxide synthase (NOS) after formalin injection in the rat hind paw. Neurosci. Lett. 210:201-204.
63. Roche, A. K., Cook, M., Wilcox, G. L., and Kajander, K. C. 1996. A nitric oxide synthesis inhibitor (L-NAME) reduces licking behavior and Fos-labeling in the spinal cord of rats during formalin-induced inflammation. Pain 66:331-341.
64. Kocher, L., Anton, F., Reeh, P. W., and Handwerker, H. O. 1987. The effect of carrageenan-induced inflammation on the sensitivity of unmyelinated skin nociceptors in the rat. Pain 29:363-373.
65. Diehl, B., Hoheisel, U., and Mense, S. 1993. The influence of mechanical stimuli and of acetylsalicylic acid on the discharges of slowly conducting afferent units from normal and inflamed muscle in the rat. Exp. Brain Res. 92:431-440.
66. Traub, R. J., Solodkin, A., and Gebhart, G. F. 1994. NADPH-diaphorase histochemistry provides evidence for a bilateral, somatotopically inappropriate response to unilateral hindpaw inflammation in the rat. Brain Res. 647:113-123.
67. Traub, R. J., Solodkin, A., Meller, S. T., and Gebhart, G. F. 1994. Spinal cord NADPH-diaphorase histochemical staining but not nitric oxide synthase immunoreactivity increases following carrageenan-produced hindpaw inflammation in the rat. Brain Res. 668:204-210.
68. Hoheisel, U., Reinert, A., and Mense, S. 1995. Changes in NADPH-diaphorase activity in the rat dorsal horn following an acute experimental myositis. Histochem. Cell. Biol. 103:459-462.
69. Mense, S., Hoheisel, U., and Reinert, A. 1996. Spinal neurons showing NADPH-diaphorase activity react in a different way to peripheral lessions. Ann. Anat. 178(Suppl):11-12.
70. Goff, J. R., Burkey, A. R., Goff, D. J., and Jasmin, L. 1998. Reorganization of the spinal dorsal horn in models of chronic pain: Correlation with behaviour. Neuroscience 82:559-574.
71. Häbler, H. J., Janig, W., and Koltzenburg, M. 1990. Activation of unmyelinated afferent fibres by mechanical stimuli and inflammation of the urinary bladder in the cat. J. Physiol. 425:545-562.
72. Häbler, H. J., Janig, W., and Koltzenburg, M. 1993. Receptive properties of myelinated primary afferents innervating the inflamed urinary bladder of the cat. J. Neurophysiol. 69:395-405.
73. Callsen-Cencic, P. and Mense, S. 1997. Altered expression of neuronal nitric oxide synthase following inflamation of the rat urinary blader. Ann. Anat. 179(Suppl):2.
74. Steel, J. H., Terenghi, G., Chung, J. M., Na, H. S., Carlton, S. M., and Polak, J. M. 1994. Increased nitric oxide synthase immunoreactivity in rat dorsal root ganglia in a neuropathic pain model. Neurosci. Lett. 169:81-84.
75. Choi, Y., Raja, S. N., Moore, L. C., and Tobin, J. R. 1996. Neuropathic pain in rats is associated with altered nitric oxide synthase activity in neural tissue. J. Neurol. Sci. 138:14-20.
76. Maršala, J., Maršala, M., Lukáčová, N., Ishikawa, T., and Čížková, N. 2003. Localization and distribution patterns of nicotinamide adenine dinucleotide phosphate diaphorase exhibiting axons in the white matter of the spinal cord of the rabbit. Cell. Mol. Neurobiol. 23:57-93.
77. Matsushita, M. and Ueyama, T. 1973. Ventral motor nucleus of the cervical enlargement in some mammals: Its specific afferents from the lower cord levels and cytoarchitecture. J. Comp. Neurol. 150:33-52.
78. Brown, A. G. and Fyffe, R. E. 1978. The morphology of group Ia afferent fibre collaterals in the spinal cord of the cat. J. Physiol. 274:111-127.
79. Brown A. G. 1981. Organization in the Spinal Cord: The Anatomy and Physiology of Identified Neurons, Springer-Verlag, Berlin.
80. Fyffe, R. E. 1979. The morphology of group II muscle afferent fibre collaterals. J. Physiol. 296:39-40.
81. Brown, A. G. and Fyffe, R. E. 1979. The morphology of group Ib afferent fibre collaterals in the spinal cord of the cat. J. Physiol. 296:215-226.
82. Grozdanovic, Z. and Baumgarten, H. G. 1999. Nitric oxide synthase in skeletal muscle fibers: A signaling component of the dystrophin-glycoprotein complex. Histol. Histopathol. 14:243-256.
83. He, X. H., Tay, S. S., and Ling, E. A. 1997. Expression of NADPH-diaphorase and nitric oxide synthase in lumbosacral motoneurons after knee joint immobilisation in the guinea pig. J. Anal. 191:603-610.
84. Schmid, H. A. and Pehl, U. 1996. Regional specific effects of nitric oxide donors and cGMP on the electrical activity of neurons in the rat spinal cord. J. Chem. Neuroanat. 10:197-201.
85. Pehl, U. and Schmid, H. A. 1997. Electrophysiological responses of neurons in the rat spinal cord to nitric oxide. Neuroscience 77:563-573.