Spinal nerve ligation reduces nitric oxide synthase activity and expression: Effect of resveratrol

Pharmacology Biochemistry and Behavior

Volumn 90, Issue 4, 2008, Pages 742-747

  Pérez Severiano, Francisca ^a   Bermúdez Ocaña, Deysi Y ^b   López Sánchez, Pedro ^c   Ríos, Camilo ^a   Granados Soto, Vinicio ^b  

^a SECRETARÍA DE SALUD   (Mexico)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

^c INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

Author keywords

Neuropathic pain; nNOS expression; NOS activity; Resveratrol; Tactile allodynia

Indexed keywords

DRUG VEHICLE; NITRIC OXIDE SYNTHASE; RESVERATROL;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CATALYSIS; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; NERVE LIGATION; NEUROPATHIC PAIN; NONHUMAN; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD DORSAL HORN; SPINAL NERVE; TOUCH;

ACTINS; ANIMALS; ANTIOXIDANTS; FEMALE; INJECTIONS, SPINAL; LIGATION; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; PAIN MEASUREMENT; PHYSICAL STIMULATION; RATS; RATS, WISTAR; SPINAL CORD; SPINAL NERVES; STILBENES;

ANIMALIA; RATTUS;

EID: 48749111330     PISSN: 00913057     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbb.2008.05.024     Document Type: Article

References (48)

1. Akira T., Henry D., and Wasterlain C.G. Nitric oxide mediates the sustained opening of NMDA receptor-gated ionic channels which follows transient excitotoxic exposure in hippocampal slices. Brain Res 652 (1994) 190-194
2. Ates O., Cayli S.R., Yucel N., Altinoz E., Kocak A., Durak M.A., et al. Central nervous system protection by resveratrol in streptozotocin-induced diabetic rats. J Clin Neurosci 14 (2007) 256-260.
3. + channel pathway in the antiallodynic action of resveratrol. Pharmacol Biochem Behav 84 (2006) 535-542
4. Bogdanov M.B., and Wurtman R.J. Possible involvement of nitric oxide in NMDA-induced glutamate release in the rat striatum: an in vivo microdialysis study. Neurosci Lett 221 (1997) 197-201
5. Bredt D.S., and Snyder S.H. Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. PNAS 87 (1990) 682-685 1990
6. Caram-Salas N.L., Reyes-García G., Bartoszyk G.D., Araiza-Saldaña C.I., Ambriz-Tututi M., Rocha-González H.I., et al. Subcutaneous, intrathecal and periaqueductal grey administration of asimadoline and ICI-204448 reduces tactile allodynia in the rat. Eur J Pharmacol 573 (2007) 75-83
7. Chaplan S.R., Bach R.W., Pogrel J.W., Chung J.M., and Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53 (1994) 55-63
8. Chaplan S.R., Malmberg A.B., and Yaksh T.L. Efficacy of spinal NMDA receptor antagonism in formalin hyperalgesia and nerve injury evoked allodynia in the rat. J Pharmacol Exp Ther 280 (1997) 829-838
9. Chen S.R., Eisenach J.C., and Pan H.L. Intrathecal S-nitroso-N-acetylpenicillamine and l-cysteine attenuate nerve injury-induced allodynia through noradrenergic activation in rats. Neuroscience 101 (2000) 759-765
10. Chen S.R., Khan G.M., and Pan H.L. Antiallodynic effect of intrathecal neostigmine is mediated by spinal nitric oxide in a rat model of diabetic neuropathic pain. Anesthesiology 95 (2001) 1007-1012
11. Chen S.R., and Pan H.L. Spinal nitric oxide contributes to the analgesic effect of intrathecal [d-pen2,d-pen5]-enkephalin in normal and diabetic rats. Anesthesiology 98 (2003) 217-222
12. Choi Y., Raja S.N., Moore L.C., and Tobin J.R. Neuropathic pain in rats is associated with altered nitric oxide synthase activity in neural tissue. J Neurol Sci 138 (1996) 14-20
13. Cizkova D., Lukacova N., Marsala M., and Marsala J. Neuropathic pain is associated with alterations of nitric oxide synthase immunoreactivity and catalytic activity in dorsal root ganglia and spinal dorsal horn. Brain Res Bull 58 (2002) 161-171
14. Diaz-Barriga F., Hernández J.M., Carrizales L., Domínguez M.C., Yañez L., Palmer E., et al. Interactions of cadmiun with actin microfilaments. Toxicol In vitro 3 (1989) 277-284
15. Dixon W.J. Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 20 (1980) 441-462
16. Fiallos-Estrada C.E., Kummer W., Mayer B., Bravo R., Zimmermann M., and Herdegen T. Long-lasting increase of nitric oxide synthase immunoreactivity, NADPH-diaphorase reaction and c-JUN co-expression in rat dorsal root ganglion neurons following sciatic nerve transection. Neurosci Lett 150 (1993) 169-173
17. González-Hernández T., and Rustioni A. Nitric oxide synthase and growth-associated protein are co-expressed in primary sensory neurons after peripheral injury. J Comp Neurol 404 (1999) 64-74
18. Imamura G., Bertelli A.A., Bertelli A., Otani H., Maulik N., and Das DK. Pharmacological preconditioning with resveratrol: an insight with iNOS knockout mice. Am J Physiol Heart Circ Physiol 282 (2002) H1996-H2003
19. Inoue T., Mashimo T., Shibata M., Shibuta S., and Yoshiya I. Rapid development of nitric oxide-induced hyperalgesia depends on an alternate to the cGMP-mediated pathway in the rat neuropathic pain model. Brain Res 792 (1998) 263-270
20. Kim S.H., and Chung J.M. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50 (1992) 355-363
21. Koltzenburg M., Torebjork H.E., and Wahren L.K. Nociceptor modulated central sensitization causes mechanical hyperalgesia in acute chemogenic and chronic neuropathic pain. Brain 117 (1994) 579-591
22. Kumar A., Kaundal R.K., Iyer S., and Sharma S.S. Effects of resveratrol on nerve functions, oxidative stress and DNA fragmentation in experimental diabetic neuropathy. Life Sci 80 (2007) 1236-1244
23. Lee D.H., Singh J.P., and Lodge D. Experiments with nitric oxide synthase inhibitors in spinal nerve ligated rats provide no evidence of a role for nitric oxide in neuropathic mechanical allodynia. Neurosci Lett 385 (2005) 179-183
24. Leikert J.F., Rathel T.R., Wohlfart P., Cheynier V., Vollmar A.M., and Dirsch V.M. Red wine polyphenols enhance endothelial nitric oxide synthase expression and subsequent nitric oxide release from endothelial cells. Circulation 106 (2002) 1614-1617
25. Lowry O.H., Rosenbrough N.J., Farr L., and Randall L.J. Protein measurement with the folin phenol reagent. J Biol Chem 193 (1951) 265-275
26. Lukacova N., Cizkova D., Krizanova O., Pavel J., Marsala M., and Marsala J. Peripheral axotomy affects nicotinamide adenine dinucleotide phosphate diaphorase and nitric oxide synthases in the spinal cord of the rabbit. J Neurosci Res 71 (2003) 300-313
27. Luo Z.D., Chaplan S.R., Scott B.P., Cizkova D., Calcutt N.A., and Yaksh T.L. Neuronal nitric oxide synthase mRNA upregulation in rat sensory neurons after spinal nerve ligation: lack of a role in allodynia development. J Neurosci 19 (1999) 9201-9208
28. Meller S.T., Pechman P.S., Gebhart G.F., and Maves T.J. Nitric oxide mediates the thermal hyperalgesia produced in a model of neuropathic pain in the rat. Neuroscience 50 (1992) 7-10
29. + channel pathway participates in the antiallodynic effect of spinal gabapentin. Eur J Pharmacol 531 (2006) 87-95
30. Montague P.R., Gancayco C.D., Winn M.J., Marchase R.B., and Friedlander M.J. Role of NO production in NMDA receptor-mediated neurotransmitter release in cerebral cortex. Science 263 (1994) 973-977
31. Naik A.K., Tandan S.K., Kumar D., and Dudhgaonkar S.P. Nitric oxide and its modulators in chronic constriction injury-induced neuropathic pain in rats. Eur J Pharmacol 530 (2006) 59-69
32. Notas G., Nifli A.P., Kampa M., Vercauteren J., Kouroumalis E., and Castanas E. Resveratrol exerts its antiproliferative effect on HepG2 hepatocellular carcinoma cells, by inducing cell cycle arrest, and NOS activation. Biochim Biophys Acta 1760 (2006) 1657-1666
33. Pan H.L., Chen S.R., and Eisenach J.C. Role of spinal NO in antiallodynic effect of intrathecal clonidine in neuropathic rats. Anesthesiology 89 (1998) 1518-1523
34. Pérez-Severiano F., Escalante B., Vergara P., Ríos C., and Segovia J. Age-dependent changes in nitric oxide synthase activity and protein expression in striata of mice transgenic for the Huntington's disease mutation. Brain Res 951 (2002) 34-42
35. 2. Br J Pharmacol 123 (1998) 890-894
36. Segovia J., and Pérez-Severiano F. Oxidative damage in Huntington's disease. Methods Mol Biol 277 (2004) 321-334
37. Segovia J., Vergara P., and Brenner M. Differentiation-dependent expression of transgenes in engineered astrocyte cell lines. Neurosci Lett 242 (1998) 172-176
38. Sharma S., Kulkarni S.K., and Chopra K. Effect of resveratrol, a polyphenolic phytoalexin, on thermal hyperalgesia in a mouse model of diabetic neuropathic pain. Fundam Clin Pharmacol 21 (2007) 89-94
39. Siegan J.B., Hama A.T., and Sagen J. Suppression of neuropathic pain by a naturally-derived peptide with NMDA antagonist activity. Brain Res 755 (1997) 331-334
40. Snyder S.H. Nitric oxide: first in a new class of neurotransmitters. Science 257 (1992) 494-496
41. Steel J.H., Terenghi G., Chung J.M., Na H.S., Carlton S.M., and Polak J.M. Increased nitric oxide synthase immunoreactivity in rat dorsal root ganglia in a neuropathic pain model. Neurosci Lett 169 (1994) 81-84
42. Wallerath T., Deckert G., Ternes T., Anderson H., Li H., Witte K., et al. Resveratrol, a polyphenolic phytoalexin present in red wine, enhances expression and activity of endothelial nitric oxide synthase. Circulation 106 (2002) 1652-1658
43. Wallerath T., Li H., Gödtel-Ambrust U., Schwarz P.M., and Förstermann U. A blend of polyphenolic compounds explains the stimulatory effect of red wine on human endothelial NO synthase. Nitric Oxide 12 (2005) 97-104
44. Wallerath T., Poleo D., Li H., and Forstermann U. Red wine increases the expression of human endothelial nitric oxide synthase: a mechanism that may contribute to its beneficial cardiovascular effects. J Am Coll Cardiol 41 3 (2003) 471-478
45. Yaksh T.L., and Rudy T.A. Chronic catheterization of the spinal subarachnoid space. Physiol Behav 17 (1976) 1031-1036
46. Yamamoto T., and Shimoyama N. Role of nitric oxide in the development of thermal hyperesthesia induced by sciatic nerve constriction injury in the rat. Anesthesiology 82 (1995) 1266-1273
47. Zhang X., Verge V., Wiesenfeld-Hallin Z., Ju G., Bredt D., Synder S.H., et al. Nitric oxide synthase-like immunoreactivity in lumbar dorsal root ganglia and spinal cord of rat and monkey and effect of peripheral axotomy. J Comp Neurol 335 (1993) 563-575
48. Zimmermann M. Ethical guidelines for investigations on experimental pain in conscious animals. Pain 16 (1983) 109-110