Neuropeptides
Volume 43, Issue 1 , Pages 31-39 , February 2009

Changes in the NPY immunoreactivity in gerbil hippocampus after hypoxic and ischemic preconditioning

  • Malgorzata Duszczyk

      Affiliations

    • Medical Research Centre, Polish Academy of Sciences, 5 Pawinskiego Street, Warsaw 02-106, Poland
  • ,
  • Apolonia Ziembowicz

      Affiliations

    • Medical Research Centre, Polish Academy of Sciences, 5 Pawinskiego Street, Warsaw 02-106, Poland
  • ,
  • Roman Gadamski

      Affiliations

    • Medical Research Centre, Polish Academy of Sciences, 5 Pawinskiego Street, Warsaw 02-106, Poland
  • ,
  • Joanna M. Wieronska

      Affiliations

    • Institute of Pharmacology, Polish Academy of Sciences, 12 Smetna Street, Cracow 31-343, Poland
  • ,
  • Maria Smialowska

      Affiliations

    • Institute of Pharmacology, Polish Academy of Sciences, 12 Smetna Street, Cracow 31-343, Poland
  • ,
  • Jerzy W. Lazarewicz

      Affiliations

    • Medical Research Centre, Polish Academy of Sciences, 5 Pawinskiego Street, Warsaw 02-106, Poland
    • Corresponding Author InformationCorresponding author. Tel.: +48 22 608 65 28; fax: +48 22 668 54 23.

Received 30 June 2008 ,Accepted 28 September 2008.

References 

  1. Bergeron M, Gidday JM, Yu AY, Semenza GL, Ferriero DM, Sharp FR. Role of hypoxia-inducible factor-1 in hypoxia-induced ischemic tolerance in neonatal rat brain. Annals of Neurology. 2000;48:285–296
  2. Bering R, Draguhn A, Diemer NH, Johansen FF. Ischemia changes the coexpression of somatostatin and neuropeptide Y in hippocampal interneurons. Experimental Brain Research. 1997;115:423–429
  3. Bernaudin M, Nedelec AS, Divoux D, MacKenzie ET, Petit E, Schumann-Bard P. Normobaric hypoxia induces tolerance to focal permanent cerebral ischemia in association with an increased expression of hypoxia-inducible factor-1 and its target genes, erythropoietin and VEGF, in the adult mouse brain. Journal of Cerebral Blood Flow and Metabolism. 2002;22:393–403
  4. Bond A, Lodge D, Hicks CA, Ward MA, O’Neill MJ. NMDA receptors antagonism, but not AMPA receptors antagonism attenuates induced ischemic tolerance in gerbil hippocampus. European Journal of Pharmacology. 1999;380:91–99
  5. Chen SH, Cheung RT. Peripheral and central administration of neuropeptide Y in a rat middle cerebral artery occlusion stroke model reduces cerebral blood flow and increases infarct volume. Brain Research. 2002;927:138–143
  6. Cheung RT, Cechetto DF. Neuropeptide Y–Y1 receptor antisense oligodeoxynucleotide increases the infarct volume after middle cerebral artery occlusion in rats. Neuroscience. 2000;98:771–777
  7. Chopp M, Chen H, Ho KL, Dereski MO, Brown E, Hetzel FW, et al. Transient hyperthermia protects against subsequent forebrain ischemic cell damage in the rat. Neurology. 1989;39:1396–1398
  8. Colmers WF. Modulation of synaptic transmission in hippocampus by neuropeptide Y: presynaptic actions. Annals of the New York Academy of Sciences. 1990;611:206–218
  9. Corbett D, Crooks P. Ischemic preconditioning: a long term survival study using behavioural and histological endpoints. Brain Research. 1997;760:29–36
  10. Domin H, Kajta M, Smialowska M. Neuroprotective effects of MTEP, a selective mGluR5 antagonists and neuropeptide Y on the kainate-induced toxicity in primary neuronal cultures. Pharmacological Reports. 2006;58:846–858
  11. Dowden J, Corbett D. Ischemic preconditioning in 18- to 20-month-old gerbils: long-term survival with functional outcome measures. Stroke. 1999;30:1240–1246
  12. Duszczyk M, Gadamski R, Ziembowicz A, Danysz W, Lazarewicz JW. NMDA receptor antagonism does not inhibit induction of ischemic tolerance in gerbil brain in vivo. Neurotoxicity Research. 2005;7:283–292
  13. Duszczyk M, Gadamski R, Ziembowicz A, Lazarewicz JW. Antagonists of group I metabotropic glutamate receptors do not inhibit induction of ischemic tolerance in gerbil hippocampus. Neurochemistry International. 2006;48:478–484
  14. El Bahh B, Auvergne R, Lere C, Brana C, Le Gal La Salle G, Rougier A. Decrease epileptic susceptibility correlates with neuropeptide Y overexpression in a model of tolerance to excitotoxicity. Brain Research. 2001;894:209–217
  15. Grabb MC, Choi DW. Ischemic tolerance in murine cortical cell culture, critical role for NMDA receptors. The Journal of Neuroscience. 1999;19:1657–1662
  16. Gruber B, Greber S, Rupp E, Sperk G. Differential NPY mRNA expression in granule cells and interneurons of the rat dentate gyrus after kainic acid injection. Hippocampus. 1994;4:474–482
  17. Kato H, Liu Y, Kogure K, Kato K. Induction of 27-kDa heat shock protein following cerebral ischemia in a rat model of ischemic tolerance. Brain Research. 1994;634:235–244
  18. Kelly ME, McIntyre DC. Hippocampal kindling protects several structures from the neuronal damage resulting from kainic acid-induced status epilepticus. Brain Research. 1994;634:245–256
  19. Kirino T. Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Research. 1982;239:57–69
  20. Kirino T. Ischemic tolerance. Journal of Cerebral Blood Flow and Metabolism. 2002;22:1283–1296
  21. Kirino T, Tsujita Y, Tamura A. Induced tolerance to ischemia in gerbil hippocampal neurons. Journal of Cerebral Blood Flow and Metabolism. 1991;11:299–307
  22. Kitagawa K, Matsumoto M, Tagaya M, Hata R, Ueda H, Niinobe M, et al. ‘Ischemic tolerance’ phenomenon found in the brain. Brain Research. 1990;528:21–24
  23. Kuroiwa T, Bonnekoh P, Hossmann KA. Prevention of postischemic hyperthermia prevents ischemic injury of CA1 neurons in gerbils. Journal of Cerebral Blood Flow and Metabolism. 1990;10:550–556
  24. Lazarewicz JW, Gadamski R, Parsons CG, Danysz W. Protection against post-ischaemic neuronal loss in gerbil hippocampal CA1 by glycineB and AMPA antagonists. Journal of Neural Transmission. 1997;104:1249–1254
  25. Lere C, El Bahh B, Le Gal le Salle G, Rougier A. A model of ‘‘epileptic tolerance” for investigating neuroprotection, epileptic susceptibility and gene expression-related plastic changes. Brain research. Brain Research Protocols. 2002;9:49–56
  26. Luo Y, Kaur C, Ling EA. Hypobaric hypoxia induces fos and neuronal nitric oxide synthase expression in the paraventricular and supraoptic nucleus in rats. Neuroscience Letters. 2000;296:145–148
  27. Lurton D, Coussemacq M, Barrow P, Sundstrom LE, Rougier A. Widespread ectopic neuropeptide-Y immunoreactivity in conyralateral mossy fibres after a unilateral intrahippocampal kainic acid injection in the rat. Neuroscience Letters. 1996;213:181–184
  28. Marini AM, Paul SM. N-methyl-d-aspartate receptor-mediated neuroprotection in cerebellar granule cells requires new RNA and protein synthesis. Proceedings of the National Academy of Sciences of the United States of America. 1992;89:6555–6559
  29. Mason N. The pathology of high altitude, an introduction to the disease states of high altitude. Current Anaesthesia and Critical Care. 2000;11:104–112
  30. Miller BA, Perez RS, Shah AR, Gonzales ER, Park TS, Gidday JM. Cerebral protection by hypoxic preconditioning in a murine model of focal ischemia-reperfusion. Neuroreport. 2001;12:1663–1669
  31. Morocz IA, Zientara GP, Gudbjartsson H, Muza S, Lyons T, Rock PB, et al. Volumetric quantification of brain swelling after hypobaric hypoxia exposure. Experimental Neurology. 2001;168:96–104
  32. Ohtsuki T, Ruetzler CA, Tasaki K, Hallenbeck JM. Interleukin-1 mediates induction of tolerance to global ischemia in gerbil hippocampal CA1 neurons. Journal of Cerebral Blood Flow and Metabolism. 1996;16:1137–1142
  33. Plamondon H, Blondeau N, Heurteaux C, Lazdunski M. Mutually protective actions of kainic acid epileptic preconditioning and sublethal global ischemia on hippocampal neuronal death, involvement of adenosine A1 receptors and K(ATP) channels. Journal of Cerebral Blood Flow and Metabolism. 1999;19:1296–1308
  34. Ruscher K, Freyer D, Karsch M, Isaev N, Megow D, Sawitzki B, et al. Erythropoietin is a paracrine mediator of ischemic tolerance in the brain, evidence from an in vitro model. The Journal of Neuroscience. 2002;22:10291–10301
  35. Sadowski M, Wisniewski HM, Jakubowska-Sadowska K, Tarnawski M, Lazarewicz JW, Mossakowski MJ. Pattern of neuronal loss in the rat hippocampus following experimental cardiac arrest-induced ischemia. Journal of the Neurological Sciences. 1999;168(1):13–20
  36. Semenov DG, Miller OL, Samoilov MO. Effect of in vivo hypoxic preconditioning on changes in intracellular calcium content induced by long-term anoxia in rat brain slices. Bulletin of Experimental Biology and Medicine. 2004;138:338–340
  37. Semenov DG, Samoilov MO, Lazarewicz JW. Preconditioning reduces hypoxia-evoked alterations in glutamatergic Ca2+ signaling in rat cortex. Acta Neurobiologiae Experimentalis. 2008;68(2):169–179
  38. Sharp FR, Ran R, Lu A, Tang Y, Strauss KI, Glass T, et al. Hypoxic preconditioning protects against ischemic brain injury. NeuroRx: The Journal of the American Society for Experimental NeuroTherapeutics. 2004;1:26–35
  39. Silva AP, Carvalho AP, Carvalho CM, Malva JO. Modulation of intracellular calcium changes and glutamate release by neuropeptide Y1 and Y2 receptors in the rat hippocampus, differential effects in CA1, CA3 and dentate gyrus. Journal of Neurochemistry. 2001;79:286–296
  40. Silva AP, Carvalho AP, Carvalho CM, Malva JO. Functional interaction between neuropeptide Y receptors and modulation of calcium channels in the rat hippocampus. Neuropharmacology. 2003;44:282–292
  41. Smialowska M, Wieronska JM, Szewczyk B. Neuroprotective effect of NPY on kainate neurotoxicity in the hippocampus. Polish Journal of Pharmacology. 2003;55:979–986
  42. Sommer C, Roth SU, Kuhn R, Kiessling M. Metabotropic glutamate receptor subtypes are differentially expressed after transient cerebral ischemia without, during and after tolerance induction in the gerbil hippocampus. Brain Research. 2000;872:172–180
  43. Stroev SA, Gluschenko TS, Tjulkova EI, Spyrou G, Rybnikova EA, Samoilov MO, et al. Preconditioning enhances the expression of mitochondrial antioxidant thioredoxin-2 in the forebrain of rats exposed to severe hypobaric hypoxia. Journal of Neuroscience Research. 2004;78:563–569
  44. Stroev SA, Tjulkova EI, Gluschenko TS, Rybnikova EA, Samoilov MO, Pelto-Huikko M. The augmentation of brain thioredoxin-1 expression after severe hypobaric hypoxia by the preconditioning in rats. Neuroscience Letters. 2004;370:224–229
  45. Tanaka H, Calderone A, Jover T, Grooms SY, Yokota H, Zukin RS, et al. Ischemic preconditioning acts upstream of GluR2 down-regulation to afford neuroprotection in the hippocampal CA1. Proceedings of the National Academy of Sciences of the United States of America. 2002;99:2362–2637
  46. Truettner J, Busto R, Zhao W, Ginsberg MD, Perez-Pinzon MA. Effect of ischemic preconditioning on the expression of putative neuroprotective genes in the rat brain. Brain research. Molecular Brain Research. 2002;103:106–115
  47. Vezzani A, Sperk G, Colmers WF. Neuropeptide Y, emerging evidence for a functional role in seizure modulation. Trends in Neurosciences. 1999;22:25–30
  48. Wada K, Miyazawa T, Katoh H, Nomura N, Yano A, Shima K, et al. Intraischemic hypothermia during pretreatment with sublethal ischemia reduces the induction of ischemic tolerance in the gerbil hippocampus. Brain Research. 1997;746:301–304
  49. Werner CG, Scartabelli T, Pancani T, Landucci E, Moroni F, Pellegrini-Giampietro DE. Differential role of mGlu1 and mGlu5 receptors in rat hippocampal slice models of ischemic tolerance. The European Journal of Neuroscience. 2007;25:3597–3604

PII: S0143-4179(08)00109-1

doi: 10.1016/j.npep.2008.09.008

Neuropeptides
Volume 43, Issue 1 , Pages 31-39 , February 2009