Intestinal inflammation alters the susceptibility to pentylenetetrazole- induced seizure in mice

Journal of Gastroenterology and Hepatology (Australia)

Volumn 19, Issue 3, 2004, Pages 270-277

  Riazi, Kiarash ^a   Honar, Hooman ^a   Homayoun, Houman ^a   Demehri, Shadpour ^a   Bahadori, Moslem ^a   Dehpour, Ahmad Reza ^a  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Clonic seizure threshold; Intestinal inflammation; Mice; Nitric oxide; Opioid receptors; Pentylenetetrazole

Indexed keywords

AMINOGUANIDINE; CROTON OIL; N(G) NITROARGININE METHYL ESTER; NALTREXONE; NITRIC OXIDE SYNTHASE INHIBITOR; OPIATE ANTAGONIST; PENTETRAZOLE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLONIC SEIZURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENTERITIS; EVALUATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEIZURE THRESHOLD; STATISTICAL SIGNIFICANCE;

EID: 1542616621     PISSN: 08159319     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1440-1746.2003.03284.x     Document Type: Article

References (66)

1. Ghezzi A, Zaffaroni M. Neurological manifestations of gastrointestinal disorders, with particular reference to the differential diagnosis of multiple sclerosis. Neurol. Sci. 2001; 22: S117-S122.
2. Epilepsy Foundation of America. Basic Statistics on the Epilepsies. Philadelphia: FA Davis, 1975.
3. Porter RJ. Recognizing and classifying epileptic seizures and epileptic syndromes. In: Porter RJ, Theodore WH, eds. Neurologic Clinics: Epilepsy, Vol. 4. Philadelphia: WB Saunders, 1986; 495-508.
4. Lossos A, River Y, Eliakim A, Steiner I. Neurological aspects of inflammatory bowel disease. Neurology 1995; 45: 416-21.
5. Elsehety A, Bertorini TE. Neurologic and neuropsychiatric complications of Crohn's Disease. South. Med. J. 1997; 90: 606-10.
6. Kidd BL, Urban LA. Mechanisms of inflammatory pain. Br. J. Anaesth. 2001; 87: 3-11.
7. Pol O, Ferrer I, Puig MM. Diarrhea associated with intestinal inflammation increases the potency of μ and δ opioids on the inhibition of gastrointestinal transit in mice. J. Pharmacol. Exp. Ther. 1994; 270: 386-91.
8. Puig MM, Pol M. Peripheral effects of opioids in a model of chronic intestinal inflammation in mice. J. Pharmacol. Exp. Ther. 1998; 287: 1068-75.
9. Foote F, Gale K. Proconvulsant effect of morphine on seizures induced by penthylenetetrazole in the rat. Eur. J. Pharmacol. 1994; 105: 179-84.
10. Lauretti GR, Ahmed I, Pleuvry BJ. The activity of opioid analgesics in seizure models utilizing N-methyl-D-aspartic acid, kainic acid, bicuculline, and penthylenetetrazole. Neuropharmacology 1994; 33: 155-60.
11. Homayoun H, Khavandgar S, Namiranian Kh, Gaskari SA, Dehpour AR. The role of nitric oxide in anticonvulsant and proconvulsant effects of morphine in mice. Epilepsy Res. 2002; 48: 33-41.
12. Nidhi G, Balakrishnan S, Pandhi P. Role of nitric oxide in electroshock and pentylenetetrazole seizure threshold in rats. Methods Find. Exp. Clin. Pharmacol. 1999; 21: 609-12.
13. Frenk H. Pro- and anticonvulsant actions of morphine and the endogenous opioids: involvement and interactions of multiple opiate and non-opiate systems. Brain Res. Rev. 1983; 6: 197-210.
14. Moncada S, Higgs A. The 1-arginine-nitric oxide pathway. N. Engl. J. Med. 1993; 329: 2002-12.
15. Przegalinski EB, Siwanowicz J. The role of nitric oxide in chemically- and electrically-induced seizures in mice. Neurosci. Lett. 1996; 217: 145-8.
16. Starr MS, Starr BS. Paradoxical facilitation of pilocarpine-induced seizures in the mouse by MK-801 and the nitric oxide synthesis inhibitor L-NAME. Pharmacol. Biochem. Behav. 1993; 45: 321-5.
17. Homayoun H, Khavandgar S, Dehpour AR. The involvement of endogenous opioids and nitricoxidergic pathway in the anticonvulsant effect of foot-shock stress in mice. Epilepsy Res. 2002; 49: 131-42.
18. Sengupta JN, Snider A, Su X, Gebhart GF. Effects of kappa opioids in the inflamed rat colon. Pain 1999; 79: 175-85.
19. Guslandi M. Nitric oxide and inflammatory bowel diseases. Eur. J. Clin. Invest. 1998; 28: 904-7.
20. Valle L, Pol O, Puig MM. Intestinal inflammation enhances the inhibitory effects of opioids on intestinal permeability in mice. J. Pharmacol. Exp. Ther. 2001; 296: 378-87.
21. Tran DD, Visser JJ, Pool MO et al. Enhanced systemic nitric oxide production in inflammatory bowel disease. Lancet 1993; 341: 1150.
22. Rachmilewitz D, Stamler JS, Bachwich D, Karmeli F, Ackerman Z, Podolsky DK. Enhanced colonic nitric oxide generation and nitric oxide synthase activity in ulcerative colitis and Crohn's disease. Gut 1995; 36: 718-23.
23. Hokari R, Kato S, Matsuzaki K et al. Reduced sensitivity of inducible nitric oxide synthase-deficient mice to chronic colitis. Free Radic. Biol. Med. 2001; 31: 153-63.
24. Gyires K. The role of endogenous nitric oxide in the gastroprotective action of morphine. Eur. J. Pharmacol. 1994; 255: 33-7.
25. Kolesnikov YA, Pick CG, Ciszewaska G, Pasternak GW. Blockade of tolerance to morphine but not to κ opioids by a nitric oxide synthase inhibitor. Proc. Natl Acad. Sci. USA 1993; 90: 5162-6.
26. Dehpour AR, Akbarloo N, Ghafourifar P. Endogenous nitric oxide modulates naloxone precipitated withdrawal signs in a mouse model with acute cholestasis. Behav. Pharmacol. 1998; 9: 77-80.
27. Stefano GB, Goumon Y, Bilfinger TV, Welters ID, Cadet P. Basal nitric oxide limits immune, nervous and cardiovascular excitation: human endothelia express a mu opiate receptor. Prog. Neurobiol. 2000; 60: 513-30.
28. Homayoun H, Sayyah M, Dehpour AH. The additive effect of opioids and nitric oxide in increasing pentylene-tetrazole-induced seizure threshold in cholestatic mice. J. Gastroenterol. Hepatol. 2002; 17: 96-101.
29. Pol O, Planas E, Puig MM. Peripheral effects of naloxone in mice with acute diarrhea associated with intestinal inflammation. J. Pharmacol. Exp. Ther. 1995; 272: 1271-6.
30. Pol O, Planas E, Puig MM. Effects of morphine and liposomal morphine in a model of intestinal inflammation in mice. Pharmacology 1996; 53: 180-9.
31. Pol O, Sanchez B, Puig MM. Peripheral effects of opioids in a model of intestinal inflammation in mice. Pharmacology 1996; 53: 340-50.
32. Pol O, Valle L, Sanchez-Blazquez P, Garzon J, Puig MM. Antibodies and antisense oligodeoxynucleotides to muopioid receptors, selectively block the effects of mu-opioid agonists on intestinal transit and permeability in mice. Br. J. Pharmacol. 1999; 127: 397-404.
33. Pol O, Puig MM. Reversal of tolerance to the antitransit effects of morphine during acute intestinal inflammation in mice. Br. J. Pharmacol 1997; 122: 1216-22.
34. Pol O, Valle L, Puig MM. Antisense oligodeoxynucleotides to μ- and δ-opioid receptor mRNA block the enhanced effects of opioids during intestinal inflammation. Eur. J. Pharmacol. 2001; 428: 127-36.
35. Oliverio A, Castellano C, Puglisi-Allegra S. Anticonvulsant effects of stress: role of endogenous opioids. Brain Res. 1983; 271: 193-5.
36. Shavit Y, Caldecott-Hazard S, Liebeskind JC. Activating endogenous opioid systems by electroconvulsive shock or footshock stress inhibits recurrent kindled seizures in rats. Brain Res. 1984; 305: 203-7.
37. Mayer EA, Gebhart GF. Basic and clinical aspects of visceral hyperalgesia. Gastroenterology 1994; 107: 271-93.
38. Rice AS, McMahon SB. Pre-emptive intrathecal administration of an NMDA receptor antagonist (AP-5) prevents hyper-reflexia in a model of persistent visceral pain. Pain 1994; 57: 335-40.
39. Coutinho VS, Urban MO, Gebhart GF. The role of CNS NMDA receptors and nitric oxide in visceral hyperalgesia. Eur. J. Pharmacol. 2001; 429: 319-25.
40. Riedel W, Neeck G. Nociception, pain, and antinociception: current concepts. Z. Rheumatol. 2001; 60: 404-15.
41. Sarkar S, Hobson AR, Furlong PL, Woolf CJ, Thompson DG, Aziz Q. Central neural mechanisms mediating human visceral hypersensitivity. Am. J. Physiol. Gastrointest. Liver Physiol. 2001; 281: G1196-G1202.
42. Coderre TJ, Katz J, Vaccarino AL, Melzack R. Contribution of central neuroplasticity to pathological pain: review of clinical and experimental evidence. Pain 1993; 52: 259-85.
43. Celerier E, Laulin J, Larcher A, Le Moal M, Simonnet G. Evidence for opiate-activated NMDA processes masking opiate analgesia in rats. Brain Res. 1999; 847: 18-25.
44. Friedrich AE, Gebhart GF. Effects of spinal cholecystokinin receptor antagonists on morphine antinociception in a model of visceral pain in the rat. J. Pharmacol. Exp. Ther. 2000; 292: 538-44.
45. Philippe D, Dubuquoy L, Groux H et al. Anti-inflammatory properties of the mu opioid receptor support its use in the treatment of colon inflammation. J. Clin. Invest. 2003; 111: 1329-38.
46. Pol O, Palacio JR, Puig MM. The expression of δ-and κ-opioid receptor is enhanced during intestinal inflammation in mice. J. Pharmacol. Exp. Ther. 2003; 306: 455-62.
47. Bergasa NV, Vergalla J, Swain MG, Jones EA. Hepatic concentrations of proenkephalin-derived opioids are increased in a rat model of cholestasis. Liver 1996; 16: 298-302.
48. Jones EA, Bergasa NV. The pruritus of cholestasis. Hepatology 1999; 29: 1003-6.
49. Dehpour AR, Rastegar H, Jorjani M, Roushanzamir F, Joharchi K, Ahmadiani A. Subsensitivity to opioids is receptor-specific in isolated guinea pig ileum and mouse vas deferens after obstructive cholestasis. J. Pharmacol. Exp. Ther. 2000; 293: 946-51.
50. Fiocchi C. The immune system in inflammatory bowel disease. Acta Gastroenterol. Belg. 1997; 60: 156-62.
51. MacDermott RP, Sanderson IR, Reinecker HC. The central role of chemokines (chemotactic cytokines) in the immunopathogenesis of ulcerative colitis and Crohn's disease. Inflamm. Bowel Dis. 1998; 4: 54-67.
52. Salzet M. Neuroimmunology of opioids from invertebrates to human. Neuroendocrinol. Lett. 2001; 22: 467-74.
53. Stefano GB, Scharrer B, Smith EM et al. Opioid and opiate immunoregulatory processes. Crit. Rev. Immunol. 1996; 16: 109-44.
54. Yuhas Y, Shulman L, Weizman A, Kaminsky E, Vanichkin A, Ashkenazi S. Involvement of tumor necrosis factor alpha and interleukin-1beta in enhancement of pentylene-tetrazole-induced seizures caused by Shigella dysenteriae. Infect. Immun. 1999; 67: 1455-60.
55. Binder DK, Croll SD, Gall CM, Scharfman HE. BDNF and epilepsy: too much of a good thing? Trends Neurosci. 2001; 24: 47-53.
56. Jankowsky JL, Patterson PH. The role of cytokines and growth factors in seizures and their sequelae. Prog. Neurobiol. 2001; 63: 125-49.
57. Peltola J, Palmio J, Korhonen L et al. Interleukin-6 and interleukin-1 receptor antagonist in cerebrospinal fluid from patients with recent tonic-clonic seizures. Epilepsy Res. 2000; 41: 205-11.
58. Go T, Nakamura K. Frequent seizures with elevated interleukin-6 at the eruptive stage of exanthema subitum. Eur. J. Paediatr. Neurol. 2002; 6: 221-3.
59. Masuyama T, Matsuo M, Ichimaru T, Ishii K, Tsuchiya K, Hamasaki Y. Possible contribution of interferon-alpha to febrile seizures in influenza. Pediatr. Neurol. 2002; 27: 289-92.
60. Fiorucci S, Distrutti E, Ajuebor MN et al. NO-mesalamine protects colonic epithelial cells against apoptotic damage induced by proinflammatory cytokines. Am. J. Physiol. Gastrointest. Liver Physiol 2001; 281: G654-65.
61. Fiorucci S, Antonelli E, Distrutti E et al. NCX-1015a nitric-oxide derivative of prednisolone, enhances regulatory T cells in the lamina propria and protects against 2,4,6-trinitrobenzene sulfonic acid-induced colitis in mice. Proc. Natl Acad. Sci. USA 2002; 99: 15770-5.
62. Di Lorenzo M, Krantis A. Altered nitric oxide production in the premature gut may increase susceptibility to intestinal damage in necrotizing enterocolitis. J. Pediatr. Surg. 2001; 36: 700-5.
63. Krieglstein CF, Cerwinka WH, Laroux FS et al. Regulation of murine intestinal inflammation by reactive metabolites of oxygen and nitrogen: divergent roles of superoxide and nitric oxide. J. Exp. Med. 2001; 194: 1207-18.
64. Tanaka A, Mizoguchi H, Kunikata T, Miyazawa T, Takeuchi K. Protection by constitutively formed nitric oxide of intestinal damage induced by indomethacin in rats. J. Physiol. Paris 2001; 95: 35-41.
65. Thomas S, Ramachandran A, Patra S, Vidyasagar S, Balasubramanian KA. Nitric oxide protects the intestine from the damage induced by laparotomy and gut manipulation. J. Surg. Res. 2001; 99: 25-32.
66. Khavandgar S, Homayoun H, Dehpour AR. The role of nitric oxide in the proconvulsant effect of delta-opioid agonist SNC80 in mice. Neurosci. Lett. 2002; 329: 237-9.