Nitric oxide reversibly impairs axonal conduction in guinea pig spinal cord

Journal of Neurotrauma

Volumn 23, Issue 12, 2006, Pages 1779-1793

  Ashki, Negin ^a   Hayes, Keith C ^a,b   Shi, Riyi ^c  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^c PURDUE UNIVERSITY   (United States)

Author keywords

Axons; Conduction; Guinea pig; Nitric oxide; Spinal cord injury

Indexed keywords

NITRATE; NITRIC OXIDE; NITRIC OXIDE DONOR; NITRIC OXIDE SYNTHASE; NITRITE; SPERMINE;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CENTRAL NERVOUS SYSTEM; COMPOUND ACTION POTENTIAL; COMPOUND MEMBRANE POTENTIAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; ELECTRICAL POTENTIAL PARAMETERS; ELECTROPHYSIOLOGY; EXTRACELLULAR SPACE; FEMALE; GUINEA PIG; IMMUNE SYSTEM; NERVE CONDUCTION; NERVE CONDUCTION DISORDER; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; SPINAL CORD INJURY; SPINAL CORD NERVE CELL; WHITE MATTER;

ACTION POTENTIALS; ANIMALS; AXONS; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GUINEA PIGS; MEMBRANE POTENTIALS; NEURAL CONDUCTION; NITRIC OXIDE DONORS; SPERMINE; SPINAL CORD; TIME FACTORS; TISSUE CULTURE TECHNIQUES;

EID: 33845953193     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2006.23.1779     Document Type: Article

References (63)

1. AHN, M.J., SHERWOOD, E.R., PROUGH, D.S., LIN, C.Y., and DEWITT, D.S. (2004). The effects of traumatic brain injury on cerebral blood flow and brain tissue nitric oxide levels and cytokine expression. J. Neurotrauma 21, 1431-1442.
2. BAO, F., and LIU, D. (2002). Peroxynitrite generated in the rat spinal cord induces neuron death and neurological deficits. Neuroscience 115, 839-849.
3. BECKMAN, J.S., and CROW, J.P. (1993). Pathological implications of nitric oxide, superoxide and peroxynitrite formation. Biochem. Soc. Trans. 21, 330-334.
4. BROWN, G.C., and BAL-PRICE, A. (2003). Inflammatory neurodegeneration mediated by nitric oxide, glutamate, and mitochondria. Mol. Neurobiol. 27, 325-355.
5. CALABRESE, V., BATES, T.E., and STELLA, A.M. (2000). NO synthase and NO-dependent signal pathways in brain aging and neurodegenerative disorders: the role of oxidant/antioxidant balance. Neurochem. Res. 25, 1315-1341.
6. CAMPOS DE CARVALHO, A., RAMON, F., and SPRAY, C. (1986). Effects of protein reagents on electrotonic coupling in crayfish septate axon. Am. Physiol. Soc. C99-C103.
7. CHATZIPANTELI, K., GARCIA, R., MARCILLO, A.E., LOOR, K.E., KRAYDIEH, S., and DIETRICH, W.D. (2002). Temporal and segmental distribution of constitutive and inducible nitric oxide synthases after traumatic spinal cord injury: effect of aminoguanidine treatment. J. Neurotrauma 19, 639-651.
8. DAVIES, A., HAYES, K.C., and SHI, R. (2006). Recombinant human TNF-alpha induces concentration-dependent alterations in axonal conduction in mammalian spinal cord. J. Neurotrauma 23, 1261-1273.
9. DIAZ-RUIZ, A., VERGARA, P., PEREZ-SEVERIANO, F., et al. (2004). Cyclosporin-A inhibits inducible nitric oxide synthase activity and expression after spinal cord injury in rats. Neurosci. Lett. 357, 49-52.
10. DIETZ, V., and COLOMBO, G. (2004). Recovery from spinal cord injury-underlying mechanisms and efficacy of rehabilitation. Acta Neurochir. Suppl. 89, 95-100.
11. DITUNNO, J.F., LITTLE, J.W., TESSLER, A., and BURNS, A.S. (2004). Spinal shock revisited: a four-phase model. Spinal Cord 42, 383-395.
12. FISHER, C.G., NOONAN, V.K., SMITH, D.E., WING, P.C., DVORAK, M.F., and KWON, B. (2005). Motor recovery, functional status, and health-related quality of life in patients with complete spinal cord injuries. Spine 30, 2200-2207.
13. GARTHWAITE, G., GOODWIN, D.A., BATCHELOR, A.M., LEEMING, K., and GARTHWAITE, J. (2002). Nitric oxide toxicity in CNS white matter: an in vitro study using rat optic nerve. Neuroscience 109, 145-155.
14. GATTI, R.M., RADI, R., and AUGUSTO, O. (1994). Peroxynitrite-mediated oxidation of albumin to the protein-thiyl free radical. FEBS Lett. 348, 287-290.
15. HAKIM, T.S., SUGIMORI, K., CAMPORESI, E.M., and ANDERSON, G. (1996). Half-life of nitric oxide in aqueous solutions with and without haemoglobin. Physiol. Meas. 17, 267-277.
16. HAYES, K.C., HULL, T.C., DELANEY, G.A., et al. (2002). Elevated serum titers of proinflammatory cytokines and CNS autoantibodies in patients with chronic spinal cord injury. J. Neurotrauma 19, 753-761.
17. HAYES, K.C., and KAKULAS, B.A. (1997). Neuropathology of human spinal cord injury sustained in sports-related activities. J. Neurotrauma 14, 235-248.
18. HOGG, N., DARLEY-USMAR, V.M., WILSON, M.T., and MONCADA, S. (1992). Production of hydroxyl radicals from the simultaneous generation of superoxide and nitric oxide. Biochem. J. 281, 419-424.
19. IADECOLA, C. (1997). Bright and dark sides of nitric oxide in ischemic brain injury. Trends Neurosci. 20, 132-139.
20. ISAKSSON, J., FAROOQUE, M., and OLSSON, Y. (2005). Improved functional outcome after spinal cord injury in iNOS-deficient mice. Spinal Cord 43, 167-170.
21. KAPOOR, R., DAVIES, M., and SMITH, K.J. (1999). Temporary axonal conduction block and axonal loss in inflammatory neurological disease. A potential role for nitric oxide? Ann. N.Y. Acad. Sci. 893, 304-308.
22. KEEFER, L.K., NIMS, R.W., DAVIES, K.M., and WINK, D.A. (1996). "NONOates" (1-substituted diazen-1-ium-1,2-diolates) as nitric oxide donors: convenient nitric oxide dosage forms. Methods Enzymol. 268, 281-293.
23. KIRSHBLUM, S., MILLIS, S., MCKINLEY, W., and TULSKY, D. (2004). Late neurologic recovery after traumatic spinal cord injury. Arch. Phys. Med. Rehabil. 85, 1811-1817.
24. KÖLLER, H., SIEBLER, M., and HARTUNG, H.P. (1997). Immunologically induced electrophysiological dysfunction: implications for inflammatory diseases of the CNS and PNS. Prog. Neurobiol. 52, 1-26.
25. KRONCKE, K.D., FEHSEL, K., and KOLB-BACHOFEN, V. (1997). Nitric oxide: cytotoxicity versus cytoprotection-how, why, when, and where? Nitric Oxide 1, 107-120.
26. KWAK, E.K., KIM, J.W., KANG, K.S., et al. (2005). The role of inducible nitric oxide synthase following spinal cord injury in rat. J. Korean Med. Sci. 20, 663-669.
27. LANCASTER, J.R., JR. (1996). Diffusion of free nitric oxide. Methods Enzymol. 268, 31-50.
28. LAURENT, M., LEPOIVRE, M., and TENU, J.P. (1996). Kinetic modelling of the nitric oxide gradient generated in vitro by adherent cells expressing inducible nitric oxide synthase. Biochem. J. 314, 109-113.
29. LI, Z., CHAPLEAU, M.W., BATES, J.N., BIELEFELDT, K., LEE, H.C., and ABBOUD, P.M. (1998). Nitric oxide as an autocrine regulator of sodium currents in baroreceptor neurons. Neuron 20, 1039-1049.
30. LIU, X.Z., XU, X.M., HU, R., et al. (1997). Neuronal and glial apoptosis after traumatic spinal cord injury. J. Neurosci. 17, 5395-5406.
31. LU, J., MOOCHHALA, S., SHIRHAN, M., et al. (2003). Nitric oxide induces macrophage apoptosis following traumatic brain injury in rats. Neurosci. Lett. 339, 147-150.
32. MARAGOS, C.M., MORLEY, D., WINK, D.A., et al. (1991). Complexes of NO with nucleophiles as agents for the controlled biological release of nitric oxide. Vasorelaxant effects. J. Med. Chem. 34, 3242-3247.
33. MATSUYAMA, Y., SATO, K., KAMIYA, M., YANO, J., IWATA, H., and ISOBE, K. (1998). Nitric oxide: a possible etiologic factor in spinal cord cavitation. J. Spinal Disord. 11, 248-252.
34. MONCADA, S., and ERUSALIMSKY, J.D. (2002). Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat. Rev. Mol. Cell Biol. 3, 214-220.
35. NAKAHARA, S., YONE, K., SETOGUCHI, T., et al. (2002). Changes in nitric oxide and expression of nitric oxide synthase in spinal cord after acute traumatic injury in rats. J. Neurotrauma 19, 1467-1474.
36. RADI, R., BECKMAN, J.S., BUSH, K.M., and FREEMAN, B.A. (1991). Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch. Biochem. Biophys. 288, 481-487.
37. REDFORD, E.J., KAPOOR, R., and SMITH, K.J. (1997). Nitric oxide donors reversibly block axonal conduction: demyelinated axons are especially susceptible. Brain 120, 2149-2157.
38. REJDAK, K., EIKELENBOOM, M.J., PETZOLD, A., et al. (2004). CSF nitric oxide metabolites are associated with activity and progression of multiple sclerosis. Neurology 63, 1439-1445.
39. + channels in C-type DRG neurons by S-nitrosylation. J. Neurophysiol. 87, 761-775.
40. ROSE, M.R. (1998). Neurological channelopathies. BMJ 316, 1104-1105.
41. SATAKE, K., MATSUYAMA, Y., KAMIYA, M., et al. (2000). Nitric oxide via macrophage iNOS induces apoptosis following traumatic spinal cord injury. Brain Res. Mol. Brain Res. 85, 114-122.
42. +)-ATPase activity from porcine cerebral cortex by NO generating drugs. Brain Res. 704, 117-120.
43. SCHMIDT, K., DESCH, W., KLATT, P., KUKOVETZ, W.R., and MAYER, B. (1997). Release of nitric oxide from donors with known half-life: a mathematical model for calculating nitric oxide concentrations in aerobic solutions. Naunyn Schmiedebergs Arch. Pharmacol. 355, 457-462.
44. SHI, R., and BLIGHT, A.R. (1996). Compression injury of mammalian spinal cord in vitro and the dynamics of action potential conduction failure. J. Neurophysiol. 76, 1572-1580.
45. SHI, R., and PRYOR, J.D. (2000). Temperature dependence of membrane sealing following transection in mammalian spinal cord axons. Neuroscience 98, 157-166.
46. SHI, R., and PRYOR, J.D. (2002). Pathological changes of isolated spinal cord axons in response to mechanical stretch. Neuroscience 110, 765-777.
47. SHRAGER, P. (1977). Slow sodium inactivation in nerve after exposure to sulhydryl blocking reagents. J. Gen. Physiol 69, 183-202.
48. SHRAGER, P., CUSTER, A.W., KAZARINOVA, K., RASBAND, M.N., and MATTSON, D. (1998). Nerve conduction block by nitric oxide that is mediated by the axonal environment. J. Neurophysiol. 79, 529-536.
49. SIMMONS, M.L., and MURPHY, S. (1992). Induction of nitric oxide synthase in glial cells. J. Neurochem. 59, 897-905.
50. STARKUS, J.G., and SHRAGER, P. (1978). Modification of slow sodium inactivation in nerve after internal perfusion with trypsin. Am. J. Physiol. 235, C238-C244.
51. STEINER, L., KRONCKE, K., FEHSEL, K., and KOLBBACHOFEN, V. (1997). Endothelial cells as cytotoxic effector cells: cytokine-activated rat islet endothelial cells lyse syngeneic islet cells via nitric oxide. Diabetologia 40, 150-155.
52. STYS, P.K., and LOPACHIN, R.M. (1998). Mechanisms of calcium and sodium fluxes in anoxic myelinated central nervous system axons. Neuroscience 82, 21-32.
53. 2+ exchanger. J. Neurosci. 12, 430-439.
54. TAKEUCHI, A., ISOBE, K.I., MIYAISHI, O., et al. (1998). Microglial NO induces delayed neuronal death following acute injury in the striatum. Eur. J. Neurosci. 10, 1613-1620.
55. TRUDRUNG, P., WIRTH, U., and MENSE, S. (2000). Changes in the number of nitric oxide-synthesizing neurones on both sides of a chronic transection of the rat spinal cord. Neurosci. Lett. 287, 125-128.
56. WADA, K., CHATZIPANTELI, K., BUSTO, R., and DIETRICH, W.D. (1998). Role of nitric oxide in traumatic brain injury in the rat. J. Neurosurg. 89, 807-818.
57. WANG, X., and FEUERSTEIN, G.Z. (2000). Role of immune and inflammatory mediators in CNS injury. Drug News Perspect. 13, 133-140.
58. WAXMAN, S.G. (2001). Acquired channelopathies in nerve injury and MS. Neurology 56, 1621-1627.
59. 2 reaction. Chem. Res. Toxicol. 6, 23-27.
60. WOOD, J., and GARTHWAITE, J. (1994). Models of the diffusional spread of nitric oxide: implications for neural nitric oxide signalling and its pharmacological properties. Neuropharmacology 33, 1235-1244.
61. WU, W., LIUZZI, F.J., SCHINCO, F.P., et al. (1994). Neuronal nitric oxide synthase is induced in spinal neurons by traumatic injury. Neuroscience 61, 719-726.
62. YAMADA, K., and NABESHIMA, T. (1997). Simultaneous measurement of nitrite and nitrate levels as indices of nitric oxide release in the cerebellum of conscious rats. J. Neurochem. 68, 1234-1243.
63. ZIELASEK, J., TAUSCH, M., TOYKA, K.V., and HARTUNG, H.P. (1992). Production of nitrite by neonatal rat microglial cells/brain macrophages. Cell Immunol. 141, 111-120.