Effect of μ and κ opioids on injury-induced microglial accumulation in leech CNS: Involvement of the nitric oxide pathway

Neuroscience

Volumn 144, Issue 3, 2007, Pages 1075-1086

  Yahyavi Firouz Abadi, N ^a,b   Tahsili Fahadan, P ^a,b   Ostad, S N ^a  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

cell accumulation; Hirudo medicinalis; microglia; nerve injury; nitric oxide; opioids

Indexed keywords

4 [5 (4 METHYL 1 PIPERAZINYL)[2,5' BI 1H BENZIMIDAZOL] 2' YL]PHENOL; ALKALOID; ENDOTHELIAL NITRIC OXIDE SYNTHASE; KAPPA OPIATE RECEPTOR; KAPPA OPIATE RECEPTOR AGONIST; KAPPA OPIATE RECEPTOR ANTAGONIST; MONOCLONAL ANTIBODY; MORPHINE; MU OPIATE RECEPTOR; N(G) NITROARGININE METHYL ESTER; NALOXONE; NITRIC OXIDE; NORBINALTORPHIMINE; OPIATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CULTURE MEDIUM; DISSECTION; DRUG EFFECT; DRUG INHIBITION; FORCEPS; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; LEECH; MICROGLIA; NERVE CORD; NONHUMAN; PRIORITY JOURNAL; STAINING;

ANALGESICS, OPIOID; ANIMALS; ENZYME INHIBITORS; GLIOSIS; HIRUDO MEDICINALIS; MICROGLIA; NARCOTIC ANTAGONISTS; NERVOUS SYSTEM; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OPIOID PEPTIDES; RECEPTORS, OPIOID, KAPPA; RECEPTORS, OPIOID, MU; SIGNAL TRANSDUCTION; TRAUMA, NERVOUS SYSTEM;

EID: 33845733579     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2006.10.036     Document Type: Article

References (58)

1. Angelov D.N., Walther M., Streppel M., Guntinas-Lichius O., Neiss W.F., Probstmeier R., and Pesheva P. Tenascin-R is antiadhesive for activated microglia that induce downregulation of the protein after peripheral nerve injury: a new role in neuronal protection. J Neurosci 18 (1998) 6218-6229
2. Banati R.B., Gehrmann J., Schubert P., and Kreutzberg G.W. Cytotoxicity of microglia. Glia 7 (1993) 111-118
3. Barron K.D. The microglial cell. A historical review. J Neurol Sci 134 (1995) 57-68
4. Baskin D.S., Widmayer M.A., Browning J.L., Heizer M.L., and Schmidt W.K. Evaluation of delayed treatment of focal cerebral ischemia with three selective kappa-opioid agonists in cats. Stroke 25 (1994) 2047-2053
5. Blottner D., Grozdanovic Z., and Gossrau R. Histochemistry of nitric oxide synthase in the nervous system. Histochem J 27 (1995) 785-811
6. Brecknell J.E., and Fawcett J.W. Axonal regeneration. Biol Rev Camb Philos Soc 71 (1996) 227-255
7. Caroleo M.C., Arbitrio M., Melchiorri D., and Nistico G. A reappraisal of the role of the various opioid receptor subtypes in cell-mediated immunity. Neuroimmunomodulation 1 (1994) 141-147
8. Carr D.J., DeCosta B.R., Kim C.H., Jacobson A.E., Guarcello V., Rice K.C., and Blalock J.E. Opioid receptors on cells of the immune system: evidence for delta- and kappa-classes. J Endocrinol 122 (1989) 161-168
9. Chang R.C., Rota C., Glover R.E., Mason R.P., and Hong J.S. A novel effect of an opioid receptor antagonist, naloxone, on the production of reactive oxygen species by microglia: a study by electron paramagnetic resonance spectroscopy. Brain Res 854 (2000) 224-229
10. Chao C.C., Gekker G., Hu S., Sheng W.S., Shark K.B., Bu D.F., Archer S., Bidlack J.M., and Peterson P.K. Kappa opioid receptors in human microglia downregulate human immunodeficiency virus-1 expression. Proc Natl Acad Sci U S A 93 (1996) 8051-8056
11. Chao C.C., Hu S., Shark K.B., Sheng W.S., Gekker G., and Peterson P.K. Activation of mu opioid receptors inhibits microglial cell chemotaxis. J Pharmacol Exp Ther 281 (1997) 998-1004
12. Chao C.C., Hu S., Gekker G., Lokensgard J.R., Heyes M.P., and Peterson P.K. U50,488 protection against HIV-1-related neurotoxicity: involvement of quinolinic acid suppression. Neuropharmacology 39 (2000) 150-160
13. Chen A., Kumar S.M., Sahley C.L., and Muller K.J. Nitric oxide influences injury-induced microglial migration and accumulation in the leech CNS. J Neurosci 20 (2000) 1036-1043
14. Chen C.H., Toung T.J., Hurn P.D., Koehler R.C., and Bhardwaj A. Ischemic neuroprotection with selective kappa-opioid receptor agonist is gender specific. Stroke 36 (2005) 1557-1561
15. Duan Y., Haugabook S.J., Sahley C.L., and Muller K.J. Methylene blue blocks cGMP production and disrupts directed migration of microglia to nerve lesions in the leech CNS. J Neurobiol 57 (2003) 183-192
16. Elkabes S., DiCicco-Bloom E.M., and Black I.B. Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function. J Neurosci 16 (1996) 2508-2521
17. Gekker G., Hu S., Wentland M.P., Bidlack J.M., Lokensgard J.R., and Peterson P.K. Kappa-opioid receptor ligands inhibit cocaine-induced HIV-1 expression in microglial cells. J Pharmacol Exp Ther 309 (2004) 600-606
18. Goyagi T., Toung T.J., Kirsch J.R., Traystman R.J., Koehler R.C., Hurn P.D., and Bhardwaj A. Neuroprotective kappa-opioid receptor agonist BRL 52537 attenuates ischemia-evoked nitric oxide production in vivo in rats. Stroke 34 (2003) 1533-1538
19. Hu S., Peterson P.K., and Chao C.C. Kappa-opioid modulation of human microglial cell superoxide anion generation. Biochem Pharmacol 56 (1998) 285-288
20. Hu S., Chao C.C., Hegg C.C., Thayer S., and Peterson P.K. Morphine inhibits human microglial cell production of, and migration towards, RANTES. J Psychopharmacol 14 (2000) 238-243
21. Hu S., Sheng W.S., Lokensgard J.R., and Peterson P.K. Morphine induces apoptosis of human microglia and neurons. Neuropharmacology 42 (2002) 829-836
22. Itoh J., Ukai M., and Kameyama T. U-50,488H, a κ-opioid receptor agonist, markedly prevents memory dysfunctions induced by transient cerebral ischemia in mice. Brain Res 619 (1993) 223-228
23. Kuffler S.W., and Potter D.D. Glia in the leech central nervous system: physiological properties and neuron-glia relationship. J Neurophysiol 27 (1964) 290-320
24. Kumar S.M., Porterfield D.M., Muller K.J., Smith P.J., and Sahley C.L. Nerve injury induces a rapid efflux of nitric oxide (NO) detected with a novel NO microsensor. J Neurosci 21 (2001) 215-220
25. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19 (1996) 312-318
26. Laurent V., Salzet B., Verger-Bocquet M., Bernet F., and Salzet M. Morphine-like substance in leech ganglia, evidence and immune modulation. Eur J Biochem 267 (2000) 2354-2361
27. Liu B., Du L., and Hong J.S. Naloxone protects rat dopaminergic neurons against inflammatory damage through inhibition of microglia activation and superoxide generation. J Pharmacol Exp Ther 293 (2000) 607-617
28. Liu B., Du L., Kong L.Y., Hudson P.M., Wilson B.C., Chang R.C., Abel H.H., and Hong J.S. Reduction by naloxone of lipopolysaccharide-induced neurotoxicity in mouse cortical neuron-glia co-cultures. Neuroscience 97 (2000) 749-756
29. Liu Y., Shenouda D., Bilfinger T.V., Stefano M.L., Magazine H.I., and Stefano G.B. Morphine stimulates nitric oxide release from invertebrate microglia. Brain Res 722 (1996) 125-131
30. Lu X., Bing G., and Hagg T. Naloxone prevents microglia-induced degeneration of dopaminergic substantia nigra neurons in adult rats. Neuroscience 97 (2000) 285-291
31. Magazine H.I., Liu Y., Bilfinger T.V., Fricchione G.L., and Stefano G.B. Morphine-induced conformational changes in human monocytes, granulocytes, and endothelial cells and in invertebrate immunocytes and microglia are mediated by nitric oxide. J Immunol 156 (1996) 4845-4850
32. McGlade-McCulloh E., Morrissey A.M., Norona F., and Muller K.J. Individual microglia move rapidly and directly to nerve lesions in the leech central nervous system. Proc Natl Acad Sci U S A 86 (1989) 1093-1097
33. Modney B.K., Sahley C.L., and Muller K.J. Regeneration of a central synapse restores non-associative learning. J Neurosci 17 (1997) 6478-6482
34. Morgese V.J., Elliott E.J., and Muller K.J. Microglial movement to sites of nerve lesion in the leech CNS. Brain Res 272 (1983) 166-170
35. Nicholls J.G., and Baylor D.A. Specific modalities and receptive fields of sensory neurons in the CNS of the leech. J Neurophysiol 31 (1968) 740-756
36. Paakkari I., and Lindsberg P. Nitric oxide in the central nervous system. Ann Med 27 (1995) 369-377
37. Park S.W., Li J., Loh H.H., and Wei L.N. A novel signaling pathway of nitric oxide on transcriptional regulation of mouse kappa opioid receptor gene. J Neurosci 22 (2002) 7941-7947
38. Perry G.W., and Keane R.W. Modulation of microglial form and immune function by factors released from goldfish optic nerves. Int J Neurosci 91 (1997) 133-146
39. Pogozheva I.D., Przydzial M.J., and Mosberg H.I. Homology modelling of opioid receptor-ligand complexes using experimental constraints. AAPS J 7 (2005) E434-E448
40. Radulovic J., Miljevic C., Djergovic D., Vujic V., Antic J., von Horsten S., and Jankovic B.D. Opioid receptor-mediated suppression of humoral immune response in vivo and in vitro: involvement of kappa opioid receptors. J Neuroimmunol 57 (1995) 55-62
41. Ready D.F., and Nicholls J. Identified neurones isolated from leech CNS make selective connections in culture. Nature 281 (1979) 67-69
42. Shafer O.T., Chen A., Kumar S.M., Muller K.J., and Sahley C.L. Injury-induced expression of endothelial nitric oxide synthase by glial and microglial cells in the leech central nervous system within minutes after injury. Proc R Soc Lond B Biol Sci 265 (1998) 2171-2175
43. Sheng W.S., Hu S., Gekker G., Zhu S., Peterson P.K., and Chao C.C. Immunomodulatory role of opioids in the central nervous system. Arch Immunol Ther Exp (Warsz) 45 (1997) 359-366
44. Sonetti D., Ottaviani E., Bianchi F., Rodriguez M., Stefano M.L., Scharrer B., and Stefano G.B. Microglia in invertebrate ganglia. Proc Natl Acad Sci U S A 91 (1994) 9180-9184
45. Sonetti D., Ottaviani E., and Stefano G.B. Opiate signaling regulates microglia activities in the invertebrate nervous system. Gen Pharmacol 29 (1997) 39-47
46. Stefano G.B. Autoimmunovascular regulation: morphine and anandamide and ancondamide stimulated nitric oxide release. J Neuroimmunol 83 (1998) 70-76
47. Stefano G.B., Digenis A., Spector S., Leung M.K., Bilfinger T.V., Makman M.H., Scharrer B., and Abumrad N.N. Opiate-like substances in an invertebrate, a novel opiate receptor on invertebrate and human immunocytes, and a role in immunosuppression. Proc Natl Acad Sci U S A 90 (1993) 11099-11103
48. Stefano G.B., and Scharrer B. The presence of the m3 opiate receptor in invertebrate neural tissues. Comp Biochem Physiol 113 (1996) 369-373
49. Taub D.D., Eisenstein T.K., Geller E.B., Adler M.W., and Rogers T.J. Immunomodulatory activity of mu- and kappa-selective opioid agonists. Proc Natl Acad Sci U S A 88 (1991) 360-364
50. Takayama N., and Ueda H. Morphine-induced chemotaxis and brain-derived neurotrophic factor expression in microglia. J Neurosci 12 (2005) 430-435
51. Thanos S., Mey J., and Wild M. Treatment of the adult retina with microglia-suppressing factors retards axotomy-induced neuronal degradation and enhances axonal regeneration in vivo and in vitro. J Neurosci 13 (1993) 455-466
52. Tortella F.C., and DeCoster M.A. Kappa opioids: therapeutic considerations in epilepsy and CNS injury. Clin Neuropharmacol 17 (1994) 403-416
53. Verge V.M., Xu Z., Xu X.J., Wiesenfeld-Hallin Z., and Hokfelt T. 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 U S A 89 (1992) 11617-11621
54. Vizzard M.A., Erdman S.L., and de Groat W.C. Increased expression of neuronal nitric oxide synthase (NOS) in visceral neurons after nerve injury. J Neurosci 15 (1995) 4033-4045
55. von Bernhardi R., and Muller K.J. Repair of the central nervous system: lessons from lesions in leeches. J Neurobiol 27 (1995) 353-366
56. Widmayer M.A., Turner T.D., Browning J.L., and Baskin D.S. U50,488 reduces the severity of tissue damage in a rabbit model of focal cerebral ischemia. Mol Chem Neuropathol 22 (1994) 211-223
57. Zeynalov E., Nemoto M., Hurn P.D., Koehler R.C., and Bhardwaj A. Neuroprotective effect of selective kappa opioid receptor agonist is gender specific and linked to reduced neuronal nitric oxide. J Cereb Blood Flow Metab 26 (2006) 414-420
58. Zochodne D.W., Misra M., Cheng C., and Sun H. Inhibition of nitric oxide synthase enhances peripheral nerve regeneration in mice. Neurosci Lett 228 (1997) 71-74