Neuropeptides
Volume 46, Issue 1 , Pages 11-17 , February 2012

The effect of pituitary adenylate cyclase-activating polypeptide on elevated plus maze behavior and hypothermia induced by morphine withdrawal

  • Nándor Lipták

      Affiliations

    • Department of Pathophysiology, Faculty of Medicine, University of Szeged, Szeged, Hungary
  • ,
  • Roberta Dochnal

      Affiliations

    • Department of Child and Adolescent Psychiatry, Faculty of Medicine, University of Szeged, Szeged, Hungary
  • ,
  • Anikó Babits

      Affiliations

    • Department of Pathophysiology, Faculty of Medicine, University of Szeged, Szeged, Hungary
  • ,
  • Krisztina Csabafi

      Affiliations

    • Department of Pathophysiology, Faculty of Medicine, University of Szeged, Szeged, Hungary
  • ,
  • Júlia Szakács

      Affiliations

    • Department of Pathophysiology, Faculty of Medicine, University of Szeged, Szeged, Hungary
  • ,
  • Gábor Tóth

      Affiliations

    • Department of Medical Chemistry, Faculty of Medicine, University of Szeged, Szeged, Hungary
  • ,
  • Gyula Szabó

      Affiliations

    • Department of Pathophysiology, Faculty of Medicine, University of Szeged, Szeged, Hungary
    • Corresponding Author InformationCorresponding author. Address: Department of Pathophysiology, Faculty of Medicine, University of Szeged, Semmelweis u. 1, Pf. 427, H-6701 Szeged, Hungary. Tel.: +36 62 545 994; fax: +36 62 545 710.

Received 28 April 2011 ,Accepted 12 December 2011.

References 

  1. Absood A, Chen D, Hakanson R. Neuropeptides of the vasoactive intestinal peptide/helodermin/pituitary adenylate cyclase activating peptide family elevate plasma cAMP in mice: comparison with a range of other regulatory peptides. Regulatory Peptides. 1992;40:311–322
  2. Adamik A, Telegdy G. Involvement of different receptors in pituitary adenylate cyclase activating polypeptide induced open field activity in rats. Neuropeptides. 2004;38:16–20
  3. Arimura A. Pituitary adenylate cyclase activating polypeptide (PACAP): discovery and current status of research. Regulatory Peptides. 1992;37:287–303
  4. Avila MA, Ruggiero RN, Cabral A, Brandao ML, Nobre MJ, Castilho VM. Involvement of the midbrain tectum in the unconditioned fear promoted by morphine withdrawal. European Journal of Pharmacology. 2008;590:217–223
  5. Azarov AV, Szabó G, Telegdy G. Effects of atrial natriuretic peptide on acute and chronic effects of morphine. Pharmacology Biochemistry and Behavior. 1992;43:193–197
  6. Babarczy E, Szabó G, Telegdy G. Effects of secretin on acute and chronic effects of morphine. Pharmacology Biochemistry and Behavior. 1995;51:469–472
  7. Babarczy E, Vizi Z, Tóth G, Telegdy G. C-type natriuretic peptide can modify the acute and chronic effects of morphine. Neuropeptides. 1995;29:145–149
  8. Babarczy E, Vizi Z, Szabó G, Telegdy G. Effects of brain natriuretic peptide on effects of morphine in mice. Neuropeptides. 1996;30:438–442
  9. Beitner DB, Duman RS, Nestler EJ. A novel action of morphine in the rat locus coeruleus: persistent decrease in adenylate cyclase. Molecular Pharmacology. 1989;35:559–564
  10. Bie B, Peng Y, Zhang Y, Pan ZZ. CAMP-mediated mechanisms for pain sensitization during opioid withdrawal. Journal of Neuroscience. 2005;25:3824–3832
  11. Buckman SG, Hodgson SR, Hofford RS, Eitan S. Increased elevated plus maze open-arm time in mice during spontaneous morphine withdrawal. Behavioral Brain Research. 2009;197:454–456
  12. Budziszewska B, Jaworska-Feil L, Lason W. Neurosteroids and the naloxone-precipitated withdrawal syndrome in morphine-dependent mice. European Neuropsychopharmacology. 1996;6:135–140
  13. Cauvin A, Buscail L, Gourlet P, De NP, Gossen D, Arimura A, et al. The novel VIP-like hypothalamic polypeptide PACAP interacts with high affinity receptors in the human neuroblastoma cell line NB-OK. Peptides. 1990;11:773–777
  14. Christophe J. Type I receptors for PACAP (a neuropeptide even more important than VIP?). Biochimica et Biophysica Acta. 1993;1154:183–199
  15. Contet C, Filliol D, Matifas A, Kieffer BL. Morphine-induced analgesic tolerance, locomotor sensitization and physical dependence do not require modification of mu opioid receptor, cdk5 and adenylate cyclase activity. Neuropharmacology. 2008;54:475–486
  16. De RJ, Avila MA, Ruggiero RN, Nobre MJ, Brandao ML, Castilho VM. The unconditioned fear produced by morphine withdrawal is regulated by mu- and kappa-opioid receptors in the midbrain tectum. Behavioral Brain Research. 2009;204:140–146
  17. Dietl MM, Hof PR, Martin JL, Magistretti PJ, Palacios JM. Autoradiographic analysis of the distribution of vasoactive intestinal peptide binding sites in the vertebrate central nervous system: a phylogenetic study. Brain Research. 1990;520:14–26
  18. Gourlet P, Vandermeers A, Vandermeers-Piret MC, De NP, Waelbroeck M, Robberecht P. Effect of introduction of an arginine16 in VIP, PACAP and secretin on ligand affinity for the receptors. Biochimica et Biophysica Acta. 1996;1314:267–273
  19. Gourlet P, Vandermeers A, Van RJ, De NP, Cnudde J, Waelbroeck M, et al. Analogues of VIP, helodermin, and PACAP discriminate between rat and human VIP1 and VIP2 receptors. Annals of the New York Academy of Sciences. 1998;865:247–252
  20. Hammack SE, Cheung J, Rhodes KM, Schutz KC, Falls WA, Braas KM, et al. Chronic stress increases pituitary adenylate cyclase-activating peptide (PACAP) and brain-derived neurotrophic factor (BDNF) mRNA expression in the bed nucleus of the stria terminalis (BNST): roles for PACAP in anxiety-like behavior. Psychoneuroendocrinology. 2009;34:833–843
  21. Higgins GA, Sellers EM. Antagonist-precipitated opioid withdrawal in rats: evidence for dissociations between physical and motivational signs. Pharmacology Biochemistry and Behavior. 1994;48:1–8
  22. Hodgson SR, Hofford RS, Norris CJ, Eitan S. Increased elevated plus maze open-arm time in mice during naloxone-precipitated morphine withdrawal. Behavioural Pharmacology. 2008;19:805–811
  23. Joo KM, Chung YH, Kim MK, Nam RH, Lee BL, Lee KH, et al. Distribution of vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide receptors (VPAC1, VPAC2, and PAC1 receptor) in the rat brain. Journal of Comparative Neurology. 2004;476:388–413
  24. Kishioka S, Nishida S, Fukunaga Y, Yamamoto H. Quantitative properties of plasma corticosterone elevation induced by naloxone-precipitated withdrawal in morphine-dependent rats. Japanese Journal of Pharmacology. 1994;66:257–263
  25. Kuriyama K, Nakagawa K, Naito K, Muramatsu M. Morphine-induced changes in cyclic AMP metabolism and protein kinase activity in the brain. Japanese Journal of Pharmacology. 1978;28:73–84
  26. Lister RG. The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology (Berl). 1987;92:180–185
  27. Mácsai M, Pataki I, Tóth G, Szabó G. The effects of pituitary adenylate cyclase-activating polypeptide on acute and chronic morphine actions in mice. Regulatory Peptides. 2002;109:57–62
  28. Marquez P, Bebawy D, Lelievre V, Coute AC, Evans CJ, Waschek JA, et al. The role of endogenous PACAP in motor stimulation and conditioned place preference induced by morphine in mice. Psychopharmacology (Berl). 2009;204:457–463
  29. Miller JM, Poulsen-Burke J, Cochin J. Latency to first naloxone-induced jump as a measure of precipitated abstinence intensity in morphine-dependent mice and the interaction of set on this test. Life Sciences. 1983;32:2205–2213
  30. Miyata A, Jiang L, Dahl RD, Kitada C, Kubo K, Fujino M, et al. Isolation of a neuropeptide corresponding to the N-terminal 27 residues of the pituitary adenylate cyclase activating polypeptide with 38 residues (PACAP38). Biochemical and Biophysical Research Communications. 1990;170:643–648
  31. Pataki I, Adamik A, Jászberényi M, Mácsai M, Telegdy G. Pituitary adenylate cyclase-activating polypeptide induces hyperthermia in the rat. Neuropharmacology. 2000;39:1303–1308
  32. Pataki I, Adamik A, Jászberényi M, Mácsai M, Telegdy G. Involvement of transmitters in pituitary adenylate cyclase-activating polypeptide-induced hyperthermia. Regulatory Peptides. 2003;115:187–193
  33. Rabbani M, Hajhashemi V, Mesripour A. Increase in brain corticosterone concentration and recognition memory impairment following morphine withdrawal in mice. Stress. 2009;12:451–456
  34. Rezayof A, Hosseini SS, Zarrindast MR. Effects of morphine on rat behaviour in the elevated plus maze: the role of central amygdala dopamine receptors. Behavioral Brain Research. 2009;202:171–178
  35. Ribeiro SJ, De Lima TC. Naloxone-induced changes in tachykinin NK3 receptor modulation of experimental anxiety in mice. Neuroscience Letters. 1998;258:155–158
  36. Sándor K, Kormos V, Botz B, Imreh A, Bölcskei K, Gaszner B, et al. Impaired nocifensive behaviours and mechanical hyperalgesia, but enhanced thermal allodynia in pituitary adenylate cyclase-activating polypeptide deficient mice. Neuropeptides. 2010;44:363–371
  37. Schulteis G, Markou A, Gold LH, Stinus L, Koob GF. Relative sensitivity to naloxone of multiple indices of opiate withdrawal: a quantitative dose-response analysis. Journal of Pharmacology and Experimental Therapeutics. 1994;271:1391–1398
  38. Schulteis G, Yackey M, Risbrough V, Koob GF. Anxiogenic-like effects of spontaneous and naloxone-precipitated opiate withdrawal in the elevated plus-maze. Pharmacology Biochemistry and Behavior. 1998;60:727–731
  39. Szakács J, Mácsai M, Dochnal R, Babits A, Pál A, Szabó G. The effect of the neuropeptide PACAP on morphine-induced locomotor activity. Acta Physiologica Hungarica. 2010;97:475
  40. Wang YQ, Guo J, Wang SB, Fang Q, He F, Wang R. Neuropeptide FF receptors antagonist, RF9, attenuates opioid-evoked hypothermia in mice. Peptides. 2008;29:1183–1190
  41. Xiao D, Chu MS, Lee KY, Wong AO, Lin HR. Effects of pituitary adenylate cyclase activating polypeptide (PACAP) on intracellular cAMP and Ca(2+) levels in common carp (Cyprinus carpio) pituitary cells in vitro. Sheng Wu Hua Xue.Yu Sheng Wu Wu Li Xue.Bao. (Shanghai). 2002;34:790–795
  42. Zhang Z, Schulteis G. Withdrawal from acute morphine dependence is accompanied by increased anxiety-like behavior in the elevated plus maze. Pharmacology Biochemistry and Behavior. 2008;89:392–403
  43. Zhou CJ, Yada T, Kohno D, Kikuyama S, Suzuki R, Mizushima H, et al. PACAP activates PKA, PKC and Ca(2+) signaling cascades in rat neuroepithelial cells. Peptides. 2001;22:1111–1117

PII: S0143-4179(11)00104-1

doi: 10.1016/j.npep.2011.12.001

Neuropeptides
Volume 46, Issue 1 , Pages 11-17 , February 2012