Intrathecal interleukin-1β administration induces thermal hyperalgesia by activating inducible nitric oxide synthase expression in the rat spinal cord

Brain Research

Volumn 1015, Issue 1-2, 2004, Pages 145-153

  Sung, Chun Sung ^a,b   Wen, Zhi Hong ^c   Chang, Wen Kuei ^b   Ho, Shung Tai ^c   Tsai, Shen Kou ^b   Chang, Yi Chen ^c   Wong, Chih Shung ^c  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^c TRI SERVICE GENERAL HOSPITAL   (Taiwan)

Author keywords

Hyperalgesia; Interleukin 1; Nitric oxide; Nitric oxide synthase; Pain modulation: pharmacology; Pain: pathways; Sensory systems; Spinal cord

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; AMIDINE; BENZYLAMINE DERIVATIVE; ENZYME INHIBITOR; INTERLEUKIN 1; N (3 (AMINOMETHYL)BENZYL)ACETAMIDINE; N-(3-(AMINOMETHYL)BENZYL)ACETAMIDINE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NOS2 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CEREBROSPINAL FLUID; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INDUCTION; ENZYME LOCALIZATION; HYPERALGESIA; MALE; MICRODIALYSIS; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SPINAL CORD; STIMULUS RESPONSE; THERMAL STIMULATION; TISSUE DISTRIBUTION; WESTERN BLOTTING; ANIMAL; COMPARATIVE STUDY; CYTOLOGY; DRUG EFFECT; ENZYMOLOGY; HEAT; INTRASPINAL DRUG ADMINISTRATION; METABOLISM; NOCICEPTIVE RECEPTOR; PATHOPHYSIOLOGY; PERCEPTION; PHYSIOLOGY; REACTION TIME; STIMULATION; TIME; WISTAR RAT;

AMIDINES; ANIMALS; BENZYLAMINES; ENZYME INHIBITORS; HEAT; HYPERALGESIA; INJECTIONS, SPINAL; INTERLEUKIN-1; MALE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; NOCICEPTORS; PERCEPTION; RATS; RATS, WISTAR; REACTION TIME; SIGNAL TRANSDUCTION; SPINAL CORD; STIMULATION, CHEMICAL; TIME FACTORS;

EID: 3042561735     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2004.04.068     Document Type: Article

References (47)

1. Beauregard C., Brandt P.C., Chiou G.C. Induction of nitric oxide synthase and over-production of nitric oxide by interleukin-1β in cultured lacrimal gland acinar cells. Exp. Eye Res. 77:2003;109-114
2. Braman R.S., Hendrix S.A. Nanogram nitrite and nitrate determination in environmental and biological materials by vanadium (III) reduction with chemiluminescence detection. Anal. Chem. 61:1989;2715-2718
3. Bush P.A., Gonzalez N.E., Griscavage J.M., Ignarro L.J. Nitric oxide synthase from cerebellum catalyzes the formation of equimolar quantities of nitric oxide and citrulline from L-arginine. Biochem. Biophys. Res. Commun. 185:1992;960-966
4. Casamenti F., Prosperi C., Scali C., Giovannelli L., Colivicchi M.A., Faussone-Pellegrini M.S., Pepeu G. Interleukin-1β activates forebrain glial cells and increases nitric oxide production and cortical glutamate and GABA release in vivo: implications for Alzheimer's disease. Neuroscience. 91:1999;831-842
5. Coelho A., Fioramonti J., Bueno L. Brain interleukin-1β and tumor necrosis factor-alpha are involved in lipopolysaccharide-induced delayed rectal allodynia in awake rats. Brain Res. Bull. 52:2000;223-228
6. Coleman J.W. Nitric oxide in immunity and inflammation. Int. Immunopharmacol. 1:2001;1397-1406
7. da S Rocha J.C., Peixoto M.E., Jancar S., de Q Cunha F., de A Ribeiro R., da Rocha F.A. Dual effect of nitric oxide in articular inflammatory pain in zymosan-induced arthritis in rats. Br. J. Pharmacol. 136:2002;588-596
8. DeLeo J.A., Colburn R.W., Ricknia, n A.J. Cytokine and growth factor immunohistochemical spinal profiles in two animal models of mononeuropathy. Brain Res. 759:1997;50-57
9. Donnelly L.E., Barnes P.J. Expression and regulation of inducible nitric oxide synthase from human primary airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 26:2002;144-151
10. Falchi M., Ferrara F., Gharib C., Dib B. Hyperalgesic effect of intrathecally administered interleukin-1 in rats. Drugs Exp. Clin. Res. 27:2001;97-101
11. Ferreira S.H., Lorenzetti B.B., Bristow A.F., Poole S. Interleukin-1β as a potent hyperalgesic agent antagonized by a tripeptide analogue. Nature. 334:1988;698-700
12. Finder J.D., Petrus J.L., Hamilton A., Villavicencio R.T., Pitt B.R., Sebti S.M. Signal transduction pathways of IL-1β-mediated iNOS in pulmonary vascular smooth muscle cells. Am. J. Physiol., Lung Cell. Mol. Physiol. 281:2001;L816-L823
13. Heitmeier M.R., Arnush M., Scarim A.L., Corbet J.A. Pancreatic beta-cell damage mediated by beta-cell production of interleukin-1. A novel mechanism for virus-induced diabetes. J. Biol. Chem. 276:2001;11151-11158
14. Hildeman D., Muller D. Immunopathologic weight loss in intracranial LCMV infection initiated by the anorexigenic effects of IL-1β Viral Immunol. 13:2000;273-285
15. Igwe O.J., Marray J.N., Moolwaney A.S. Interleukin 1-induced cyclooxygenase and nitric oxide synthase gene expression in the rat dorsal root ganglia is modulated by antioxidants. Neuroscience. 105:2001;971-985
16. Ji G.C., Zhang Y.Q., Ma F., Wu G.C. Increase of nociceptive threshold induced by intrathecal injection of interleukin-1β in normal and carrageenan inflammatory rat. Cytokine. 19:2002;31-36
17. Licastro F., Pedrini S., Caputo L., Annoni G., Davis L.J., Ferri C., Casadei V., Grimaldi L.M. Increased plasma levels of interleukin-1, interleukin-6 and α-1-antichymotrypsin in patients with Alzheimer's disease: peripheral inflammation or signals from the brain? J. Neuroimmunol. 103:2000;97-102
18. Lin T.J., Garduno R., Boudreau R.T., Issekutz A.C. Pseudomonas aeruginosa activates human mast cells to induce neutrophil transendothelial migration via mast cell-derived IL-1α and β J. Immunol. 169:2002;4522-4530
19. Lowry D.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193:1951;265-275
20. Maihöfner C., Euchenhofer C., Tegeder I., Beck K.F., Pfeilschifter J., Geisslinger G. Regulation and immunohistochemical localization of nitric oxide synthases and soluble guanylyl cyclase in mouse spinal cord following nociceptive stimulation. Neurosci. Lett. 290:2000;71-75
21. Marsala M., Malmberg A.B., Yaksh T.L. The spinal loop dialysis catheter: characterization of use in the unanesthetized rat. J. Neurosci. Methods. 62:1995;43-53
22. Meller S.T., Dykstra C., Grzybycki D., Murphy S., Gebhart G.F. The possible role of glia in nociceptive processing and hyperalgesia in the spinal cord of the rat. Neuropharmacology. 33:1994;1471-1478
23. Nathan C., Xie Q.W. Regulation of biosynthesis of nitric oxide. J. Biol. Chem. 269:1994;13725-13728
24. Oka T., Aou S., Hori T. Intracerebroventricular injection of interleukin-1β induces hyperalgesia in rats. Brain Res. 624:1993;61-68
25. Oka T., Aou S., Hori T. Intracerebroventricular injection of interleukin-1β enhances nociceptive neuronal responses of the trigeminal nucleus caudalis in rats. Brain Res. 656:1994;236-244
26. Omote K., Hazama K., Kawamata T., Kawamata M., Nakayaka Y., Toriyabe M., Namiki A. Peripheral nitric oxide in carrageenan-induced inflammation. Brain Res. 912:2001;171-175
27. Osborne M.G., Coderre T.J. Effects of intrathecal administration of nitric oxide synthase inhibitors on carrageenan-induced thermal hyperalgesia. Br. J. Pharmacol. 126:1999;1840-1846
28. Quan N., Stern E.L., Whiteside M.B., Herkenham M. Induction of pro-inflammatory cytokine mRNAs in the brain after peripheral injection of subseptic doses of lipopolysaccharide in the rat. J. Neuroimmunol. 93:1999;72-80
29. Rady J.J., Fujimoto J.M. Confluence of antianalgesic action of diverse agents through brain interleukin-1β in mice. J. Pharmacol. Exp. Ther. 299:2001;659-665
30. Reeve A.J., Patel S., Fox A., Walker K., Urban L. Intrathecally administered endotoxin or cytokines produce allodynia, hyperalgesia and changes in spinal cord neuronal responses to nociceptive stimuli in the rat. Eur. J. Pain. 4:2000;247-257
31. Roche A.K., Cook M., Wilcox G.L., Kajander K.C. A nitric oxide synthesis inhibitor (L-NAME) reduces licking behavior and Fos-labeling in the spinal cord of rats during formalin-induced inflammation. Pain. 66:1996;331-341
32. Safieh-Garabedian B., Poole S., Allchorne A., Winter J., Woolf C.J. Contribution of interleukin-1β to the inflammation-induced increase in nerve growth factor levels and inflammatory hyperalgesia. Br. J. Pharmacol. 115:1995;1265-1275
33. Sakurada T., Suhiyama A., Sakurada C., Tan-No K., Yonezawa A., Sakurada S., Kisara K. Effect of spinal nitric oxide inhibition on capsaicin-induced nociceptive response. Life Sci. 59:1996;921-930
34. Samad T.A., Moore K.A., Sapirstein A., Billet S., Allchorne A., Poole S., Bonventre J.V., Woolf C.J. Interleukin-1β-mediated induction of COX-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature. 410:2001;471-475
35. Schafers M., Brinkhoff J., Neukirchen S., Marziniak M., Sommer C. Combined epineurial therapy with neutralizing antibodies to tumor necrosis factor-alpha and interleukin-1 receptor has an additive effect in reducing neuropathic pain in mice. Neurosci. Lett. 310:2001;113-116
36. Schultz M.J., Rijneveld A.W., Florquin S., Edwards C.K., Dinarello C.A., van der Poll T. Role of interleukin-1 in the pulmonary immune response during Pseudomonas aeruginosa pneumonia. Am. J. Physiol., Lung Cell. Mol. Physiol. 282:2002;L285-L290
37. Sommer C., Petrausch S., Lindenlaub T., Toyka K.V. Neutralizing antibodies to interleukin 1-receptor reduce pain associated behavior in mice with experimental neuropathy. Neurosci. Lett. 270:1999;25-28
38. Souter A.J., Garry M.G., Tanelian D.L. Spinal interleukin-1β reduces inflammatory pain. Pain. 86:2000;63-68
39. Sweitzer S.M., Colburn R.W., Rutkowski M., DeLeo J.A. Acute peripheral inflammation induces moderate glial activation and spinal IL-1β expression that correlates with pain behavior in the rat. Brain Res. 829:1999;209-221
40. Sweitzer S., Martin D., DeLeo J.A. Intrathecal interleukin-1 receptor antagonist in combination with soluble tumor necrosis factor receptor exhibits an anti-allodynic action in a rat model of neuropathic pain. Neuroscience. 103:2001;529-539
41. Tao Y.X., Johns R.A. Activation and up-regulation of spinal cord nitric oxide receptor, soluble guanylate cyclase, after formalin injection into the rat hind paw. Neuroscience. 112:2002;439-446
42. Tao F., Tao Y.X., Mao P., Zhao C., Li D., Liaw W.J., Raja S.N., Johns R.A. Intact carrageenan-induced thermal hyperalgesia in mice lacking inducible nitric oxide synthase. Neuroscience. 120:2003;847-854
43. Wang C.X., Olschowka J.A., Wrathall J.R. Increase of interleukin-1β mRNA and protein in the spinal cord following experimental traumatic injury in the rat. Brain Res. 759:1997;190-196
44. Watkins L.R., Wiertelak E.P., Goehler L.E., Smith K.P., Martin D., Maier S.F. Characterization of cytokine-induced hyperalgesia. Brain Res. 654:1994;15-26
45. Wen Z.H., Yang L.C., Wang J.J., Chang Y.C., Hsing C.H., Chen J.Y., Wong C.S. Intrathecal pertussis toxin induces thermal hyperalgesia: involvement of excitatory and inhibitory amino acids. Neuroscience. 116:2003;871-878
46. Wu J., Fang L., Lin Q., Willis W.D. Nitric oxide synthase in spinal cord central sensitization following intradermal injection of capsaicin. Pain. 94:2001;47-58
47. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain. 16:1983;109-110