Neuronal nitric oxide synthase mRNA upregulation in rat sensory neurons after spinal nerve ligation: Lack of a role in allodynia development

Journal of Neuroscience

Volumn 19, Issue 21, 1999, Pages 9201-9208

  Luo, Z David ^a   Chaplan, S R ^a   Scott, B P ^a   Cizkova, D ^a,b   Calcutt, N A ^a   Yaksh, T L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

Allodynia; Diabetic neuropathy; Dorsal root ganglia; mRNA regulation; Nerve injury; Neuronal nitric oxide synthase; Sensory neurons; Spinal cord

Indexed keywords

MESSENGER RNA; NITRIC OXIDE SYNTHASE;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EVOKED RESPONSE; HYPERALGESIA; MESSENGER RNA SYNTHESIS; NERVE CELL PLASTICITY; NERVE INJURY; NERVE LIGATION; NONHUMAN; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR UPREGULATION; SENSORY NERVE CELL; SPINAL GANGLION; SPINAL NERVE;

EID: 0033232917     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-21-09201.1999     Document Type: Article

References (53)

1. Akira T, Henry D, Baldwin RA, Wasterlain CG (1994) Nitric oxide participates in excitotoxic mechanisms induced by chemical hypoxia. Brain Res 645:285-290.
2. Ambron RT, Walters ET (1996) Priming events and retrograde injury signals. A new perspective on the cellular and molecular biology of nerve regeneration. Mol Neurobiol 13:61-79.
3. Ambron RT, Dulin MF, Zhang XP, Schmied R, Walters ET (1995) Axoplasm enriched in a protein mobilized by nerve injury induces memory-like alterations in Aplysia neurons. J Neurosci 15:3440-3446.
4. Ambron RT, Zhang XP, Gunstream JD, Povelones M, Walters ET (1996) Intrinsic injury signals enhance growth, survival, and excitability of Aplysia neurons. J Neurosci 16:7469-7477.
5. Anderson LC, von Bartheld CS, Byers MR (1998) NGF depletion reduces ipsilateral and contralateral trigeminal satellite cell reactions after inferior alveolar nerve injury in adult rats. Exp Neurol 150:312-320.
6. Babbedge RC, Bland-Ward PA, Hart SL, Moore PK (1993) Inhibition of rat cerebellar nitric oxide synthase by 7-nitro indazole and related substituted indazoles. Br J Pharmacol 110:225-228.
7. Barbin G, Manthorpe M, Varon S (1984) Purification of the chick eye ciliary neuronotrophic factor. J Neurochem 43:1468-1478.
8. Bogdanov MB, Wurtman RJ (1997) Possible involvement of nitric oxide in NMDA-induced glutamate release in the rat striatum: an in vivo microdialysis study. Neurosci Lett 221:197-201.
9. Calcutt NA, Chaplan SR (1997) Spinal pharmacology of tactile allodynia in diabetic rats. Br J Pharmacol 122:1478-1482.
10. Calcutt NA, Muir D, Powell HC, Mizisin AP (1992) Reduced ciliary neuronotrophic factor-like activity in nerves from diabetic or galactose-fed rats. Brain Res 575:320-324.
11. Calcutt NA, Jorge MC, Yaksh TL, Chaplan SR (1996) Tactile allodynia and formalin hyperalgesia in streptozotocin-diabetic rats: effects of insulin, aldose reductase inhibition and lidocaine. Pain 68:293-299.
12. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55-63.
13. Chaplan SR, Malmberg AB, Yaksh TL (1997) Efficacy of spinal NMDA receptor antagonism in formalin hyperalgesia and nerve injury evoked allodynia in the rat. J Pharmacol Exp Ther 280:829-838.
14. Choi Y, Raja SN, Moore LC, Tobin JR (1996) Neuropathic pain in rats is associated with altered nitric oxide synthase activity in neural tissue. J Neurol Sci 138:14-20.
15. Curtis R, Adryan KM, Zhu Y, Harkness PJ, Lindsay RM, DiStefano PS (1993) Retrograde axonal transport of ciliary neurotrophic factor is increased by peripheral nerve injury. Nature 365:253-255.
16. Dawson VL, Dawson TM (1996) Nitric oxide neurotoxicity. J Chem Neuroanat 10:179-190.
17. Dawson VL, Kizushi VM, Huang PL, Snyder SH, Dawson TM (1996) Resistance to neurotoxicity in cortical cultures from neuronal nitric oxide synthase-deficient mice. J Neurosci 16:2479-2487.
18. Dib-Hajj SD, Black JA, Cummins TR, Kenney AM, Kocsis JD, Waxman SG (1998) Rescue of alpha-SNS sodium channel expression in small dorsal root ganglion neurons after axotomy by nerve growth factor in vivo. J Neurophysiol 79:2668-2676.
19. Dixon WJ (1980) Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 20:441-462.
20. Dun NJ, Dun SL, Wu SY, Förstermann U, Schmidt HH, Tseng LF (1993) Nitric oxide synthase immunoreactivity in the rat, mouse, cat and squirrel monkey spinal cord. Neuroscience 54:845-857.
21. Fernyhough P, Diemel LT, Hardy J, Brewster WJ, Mohiuddin L, Tomlinson DR (1995) Human recombinant nerve growth factor replaces deficient neurotrophic support in the diabetic rat. Eur J Neurosci 7:1107-1110.
22. Fernyhough P, Diemel LT, Tomlinson DR (1998) Target tissue production and axonal transport of neurotrophin-3 are reduced in streptozotocin-diabetic rats. Diabetologia 41:300-306.
23. Goff JR, Burkey AR, Goff DJ, Jasmin L (1998) Reorganization of the spinal dorsal horn in models of chronic pain: correlation with behaviour. Neuroscience 82:559-574.
24. Grzybicki D, Gebhart GF, Murphy S (1996) Expression of nitric oxide synthase type II in the spinal cord under conditions producing thermal hyperalgesia. J Chem Neuroanat 10:221-229.
25. Gunstream JD, Castro GA, Walters ET (1995) Retrograde transport of plasticity signals in Aplysia sensory neurons following axonal injury. J Neurosci 15:439-448.
26. Hao JX, Xu XJ (1996) Treatment of a chronic allodynia-like response in spinally injured rats: effects of systemically administered nitric oxide synthase inhibitors. Pain 66:313-319.
27. Herdegen T, Rüdiger S, Mayer B, Bravo R, 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. Brain Res Mol Brain Res 22:245-258.
28. Ichinose F, Mi WD, Miyazaki M, Onouchi T, Goto T, Morita S (1998) Lack of correlation between the reduction of sevoflurane M AC and the cerebellar cyclic GMP concentrations in mice treated with 7-nitroindazole. Anesthesiology 89:143-148.
29. Ientile R, Picciurro V, Pedale S, Nucci C, Malecka B, Nisticò G, Macaione S (1996) Nitric oxide enhances amino acid release from immature chick embryo retina. Neurosci Lett 219:79-82.
30. Ip N Y, Nye SH, Boulton TG, Davis S, Taga T, Li Y, Birren SJ, Yasukawa K, Kishimoto T, Anderson DJ, et al. (1992) CNTF and LIF act on neuronal cells via shared signaling pathways that involve the IL-6 signal transducing receptor component gp130. Cell 69:1121-1132.
31. Kim SH, Chung JM (1992) An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50:355-363.
32. Kolesnikov YA, Pan YX, Babey AM, Jain S, Wilson R, Pasternak GW (1997) Functionally differentiating two neuronal nitric oxide synthase isoforms through antisense mapping: evidence for opposing NO actions on morphine analgesia and tolerance. Proc Natl Acad Sci USA 94:8220-8225.
33. Luo D, Vincent SR (1994) NMDA-dependent nitric oxide release in the hippocampus in vivo: interactions with noradrenaline. Neuropharmacology 33:1345-1350.
34. Luo Z, Fuentes ME, Taylor P (1994) Regulation of acetylcholinesterase mRNA stability by calcium during differentiation from myoblasts to myotubes. J Biol Chem 269:27216-27223.
35. Luo ZD, Pincon-Raymond M, Taylor P (1996) Acetylcholinesterase and nicotinic acetylcholine receptor expression diverge in muscular dysgenic mice lacking the L-type calcium channel. J Neurochem 67:111-118.
36. Meller ST, Dykstra C, Grzybycki D, Murphy S, Gebhart GF (1994) The possible role of glia in nociceptive processing and hyperalgesia in the spinal cord of the rat. Neuropharmacology 33:1471-1478.
37. Mollace V, Colasanti M, Rodino P, Lauro GM, Rotiroti D, Nistico G (1995) NMDA-dependent prostaglandin E2 release by human cultured astroglial cells is driven by nitric oxide. Biochem Biophys Res Commun 215:793-799.
38. Montague PR, Gancayco CD, Winn MJ, Marchase RB, Friedlander MJ (1994) Role of NO production in NMDA receptor-mediated neurotransmitter release in cerebral cortex. Science 263:973-977.
39. Nei K, Matsuyama S, Shuntoh H, Tanaka C (1996) NMDA receptor activation induces glutamate release through nitric oxide synthesis in guinea pig dentate gyrus. Brain Res 728:105-110.
40. Njå A, Purves D (1978) The effects of nerve growth factor and its antiserum on synapses in the superior cervical ganglion of the guinea-pig. J Physiol (Lond) 277:55-75.
41. Ohno M, Arai I, Watanabe S (1995) N-Methyl-D-aspartate stimulates dopamine release through nitric oxide formation in the nucleus accumbens of rats. Brain Res 699:332-335.
42. Sakai M, Minami T, Hara N, Nishihara I, Kitade H, Kamiyama Y, Okuda K, Takahashi H, Mori H, Ito S (1998) Stimulation of nitric oxide release from rat spinal cord by prostaglandin E2. Br J Pharmacol 123:890-894.
43. Sandor NT, Brassai A, Puskas A, Lendvai B (1995) Role of nitric oxide in modulating neurotransmitter release from rat striatum. Brain Res Bull 36:483-486.
44. Siegan JB, Hama AT, Sagen J (1997) Suppression of neuropathic pain by a naturally-derived peptide with NMDA antagonist activity. Brain Res 755:331-334.
45. Skaper SD, Varon S (1986) Age-dependent control of dorsal root ganglion neuron survival by macromolecular and low-molecular-weight trophic agents and substratum-bound laminins. Brain Res 389:39-46.
46. Snyder SH (1992) Nitric oxide: first in a new class of neurotransmitters. Science 257:494-496.
47. Steel JH, Terenghi G, Chung JM, Na HS, Carlton SM, Polak JM (1994) Increased nitric oxide synthase immunoreactivity in rat dorsal root ganglia in a neuropathic pain model. Neurosci Lett 169:81-84.
48. Thoenen H (1991) The changing scene of neurotrophic factors. Trends Neurosci 14:165-170.
49. Verge VM, Riopelle RJ, Richardson PM (1989) Nerve growth factor receptors on normal and injured sensory neurons. J Neurosci 9:914-922.
50. Verge VM, Tetzlaff W, Bisby MA, Richardson PM (1990) Influence of nerve growth factor on neurofilament gene expression in mature primary sensory neurons. J Neurosci 10:2018-2025.
51. Verge VM, Xu Z, Xu XJ, Wiesenfeld-Hallin Z, Hökfelt T (1992) Marked increase in nitric oxide synthase mRNA in rat dorsal root ganglia after peripheral axotomy: in situ hybridization and functional studies. Proc Natl Acad Sci USA 89:11617-11621.
52. Yamamoto T, Yaksh TL (1993) Effects of colchicine applied to the peripheral nerve on the thermal hyperalgesia evoked with chronic nerve constriction. Pain 55:227-233.
53. Yoon YW, Sung B, Chung JM (1998) Nitric oxide mediates behavioral signs of neuropathic pain in an experimental rat model. NeuroReport 9:367-372.