Advertisement

Amino Acids

, Volume 26, Issue 1, pp 37–43 | Cite as

Nitric oxide is not involved in the control of vasopressin release during acute forced swimming in rats

  • Mario EngelmannEmail author
  • G. Wolf
  • J Putzke
  • F. E. Bloom
  • J. Raber
  • R. Landgraf
  • M. G. Spina
  • T. F. W. Horn
Article

Summary.

Neurons of the hypothalamo-neurohypophyseal system (HNS) are known to contain high amounts of neuronal nitric oxide (NO) synthase (nNOS). NO produced by those neurons is commonly supposed to be involved as modulator in the release of the two nonapeptides vasopressin (AVP) and oxytocin into the blood stream. Previous studies showed that forced swimming fails to increase the release of AVP into the blood stream while its secretion into the hypothalamus is triggered. We investigated here whether hypothalamically acting NO contributes to the control of the AVP release into blood under forced swimming conditions. Intracerebral microdialysis and in situ hybridization were employed to analyze the activity of the nitrergic system within the supraoptic nucleus (SON), the hypothalamic origin of the HNS. A 10-min forced swimming session failed to significantly alter the local NO release as indicated both by nitrite and, the main by-product of NO synthesis, citrulline levels in microdialysis samples collected from the SON. Microdialysis administration of NO directly into the SON increased the concentration of AVP in plasma samples collected during simultaneous forced swimming. In an additional experiment the effect of the defined stressor exposure on the concentration of mRNA coding for nNOS within the SON was investigated by in situ hybridization. Forced swimming increased the expression of nNOS mRNA at two and four hours after onset of the stressor compared to untreated controls. Taken together, our results imply that NO within the SON does not contribute to the regulation of the secretory activity of HNS neurons during acute forced swimming. Increased nNOS mRNA in the SON after forced swimming and the increase in AVP release in the presence of exogenous NO under forced swimming points to a possible role of NO in the regulation of the HNS under repeated stressor exposure.

Keywords

In situ hybridization Microdialysis Hypothalamoneurohypophyseal system Stress 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bredt DS, Hwang PM, Glatt CE, Lowenstein C, Reed RR, Snyder SH (1991) Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 351: 714–718PubMedCrossRefGoogle Scholar
  2. Bruhwyler J, Chleide E, Liegeois JF, Carreer F (1993) Nitric oxide: a new messenger in the brain. Neurosci Biobehav Rev 17: 373–384Google Scholar
  3. Calka J, Block CH (1993) Relationship of vasopressin with NADPHdiaphorase in the hypothalamo-neurohypophysial system. Brain Res Bull 32: 207–210Google Scholar
  4. Cao L, Sun X, Shen E (1996) Nitric oxide stimulates both the basal and reflex release of vasopressin in anesthetized rats. Neurosci Lett 221: 49–52PubMedCrossRefGoogle Scholar
  5. Carlberg M (1994) Assay of neuronal nitric oxide synthase by HPLC determination of citrulline. J Neurosci Meth 52: 165–167CrossRefGoogle Scholar
  6. Chenais B, Yapo A, Lepoivre M, Tenu JP (1991) High-performance liquid chromatographic analysis of the unusual pathway of oxidation of Larginine to citrulline and nitric oxide in mammalian cells. J Chromatogr 539: 433–441PubMedCrossRefGoogle Scholar
  7. Engelmann M, Ebner K, Landgraf R, Holsboer F, Wotjak CT (1999) Emotional stress triggers intrahypothalamic but not peripheral release of oxytocin in male rats. J Neuroendocrinol 11: 867–872PubMedCrossRefGoogle Scholar
  8. Engelmann M, Wolf G, Horn TFW (2002) Release patterns of excitatory and inhibitory amino acids within the hypothalamic supraoptic nucleus in response to direct nitric oxide administration during forced swimming in rats. Neurosci Lett 324/3: 252–254CrossRefGoogle Scholar
  9. Förstermann U, Kleinert H (1995) Nitric oxide synthase: expression and expressional control of the three isoforms. Naunyn-Schmiedebergs Arch Pharmacol 352: 351–364PubMedCrossRefGoogle Scholar
  10. Hemmens B, Mayer B (1998) Enzymology of nitric oxide synthase. In: Titheradge MA (ed) Methods in molecular biology, nitric oxide protocols. Humana, Totowa, pp 1–32Google Scholar
  11. Horn TFW, Engelmann M (2001) In vivo microdialysis for nonapeptides in rat brain - a practical guide. Methods 23: 41–53PubMedCrossRefGoogle Scholar
  12. Horn T, Smith PM, McLaughlin BE, Bauce L, Marks GS, Pittman QJ, Ferguson AV (1994) Nitric oxide actions in paraventricular nucleus: cardiovascular and neurochemical implications. Am J Physiol 266: R306–R313PubMedGoogle Scholar
  13. Garthwaite J, Garthwaite G, Palmer RM, Moncada S (1989) NMDA receptor activation induces nitric oxide synthesis from arginine in rat brain slices. Eur J Pharmacol 172: 413–416PubMedCrossRefGoogle Scholar
  14. Guevara-Guzman R, Barrera-Mera B, de la Riva C, Kendrick KM (2000) Release of classical transmitters and nitric oxide in the rat olfactory bulb, evoked by vaginocervical stimulation and potassium, varies with the oestrus cycle. Eur J Neurosci 12: 80–88PubMedCrossRefGoogle Scholar
  15. Ignarro LJ (1990) Nitric oxide. A novel signal transduction mechanism for transcellular communication. Hypertension 16: 477–483Google Scholar
  16. Jefferys D, Funder J (1996) Nitric oxide modulates retention of immobility in the forced swimming test in rats. Eur J Pharmacol 295: 131–135PubMedCrossRefGoogle Scholar
  17. Kadekaro M, Summy-Long JY (2000) Centrally produced nitric oxide and the regulation of body fluid and blood pressure homeostases. Clin Exp Pharmacol Physiol 27: 450–459PubMedCrossRefGoogle Scholar
  18. Keilhoff G, Reiser M, Stanarius A, Aoki E, Wolf G (2000) Citrulline immunohistochemistry for demonstration of NOS activity in vivo and in vitro. Nitric Oxide 4: 343–353PubMedCrossRefGoogle Scholar
  19. Kishimoto J, Tsuchiya T, Emson PC, Nakayama Y (1996) Immobilization- induced stress activates neuronal nitric oxide synthase (nNOS) mRNA and protein in hypothalamic-pituitary-adrenal axis in rats. Brain Res 720: 159–171PubMedCrossRefGoogle Scholar
  20. Krukoff TL, Khalili P (1997) Stress-induced activation of nitric oxideproducing neurons in the rat brain. J Comp Neurol 377: 509–519PubMedCrossRefGoogle Scholar
  21. Landgraf R, Kubota M, Holsboer F, Wotjak CT (1995) Release of vasopressin and oxytocin within the brain and into blood: microdialysis and antisense targeting. In: Saito T, Kurokawa K, Yoshida S (eds) Neurohypophysis: recent progress of vasopressin and oxytocin research. Elsevier, Amsterdam, pp 243–256Google Scholar
  22. Luckman SM, Huckett L, Bicknell RJ, Voisin DL, Herbison AE (1997) Upregulation of nitric oxide synthase messenger RNA in an integrated forebrain circuit involved in oxytocin secretion. Neuroscience 77: 37–48PubMedCrossRefGoogle Scholar
  23. Mayer B, John M, Böhme E (1990) Purification of a Ca2+/calmodulin-dependent nitric oxide synthase from porcine cerebellum. Cofactor-role of tetrahydrobiopterin. FEBS Lett 277: 215–219PubMedCrossRefGoogle Scholar
  24. Miyagawa A, Okamura H, Ibata Y (1994) Coexistence of oxytocin and NADPH-diaphorase in magnocellular neurons of the paraventricular and the supraoptic nuclei of the rat hypothalamus. Neurosci Lett 171: 13–16PubMedCrossRefGoogle Scholar
  25. Pasqualotto BA, Hope BT, Vincent SR (1991) Citrulline in the rat brain: immunohistochemistry and coexistence with NADPH-diaphorase. Neurosci Lett 128: 155–160PubMedCrossRefGoogle Scholar
  26. Raber J, Pich EM, Koob GF, Bloom FE (1994) IL-1 beta potentiates the acetylcholine-induced release of vasopressin from the hypothalamus in vitro, but not from the amygdala. Neuroendocrinology 59: 208–217PubMedCrossRefGoogle Scholar
  27. Roychowdhury S, Wolf G, Keilhoff G, Bagchi D, Horn T (2001) Protection of primary glial cells by grape seed proanthocyanidin extract against nitrosative/oxidative stress. Nitric Oxide 5: 137–149PubMedCrossRefGoogle Scholar
  28. Sanchez F, Moreno MN, Vacas P, Carretero J, Vazquez R (1999) Swim stress enhances the NADPH-diaphorase histochemical staining in the paraventricular nucleus of the hypothalamus. Brain Res 828: 159–162PubMedCrossRefGoogle Scholar
  29. Srisawat R, Ludwig M, Bull PM, Douglas AJ, Russell JA, Leng G (2000) Nitric oxide and the oxytocin system in pregnancy. J Neurosci 20: 6721–6727PubMedGoogle Scholar
  30. Stern JE, Ludwig M (2001) Nitric oxide inhibits supraoptic oxytocin and vasopressin neurones via activation of GABAergic synaptic inputs. Am J Physiol 280: R1815–R1822Google Scholar
  31. Summy-Long JY, Bui V, Mantz S, Koehler E, Weisz J, Kadekaro M (1993) Central inhibition of nitric oxide synthase preferentially augments release of oxytocin during dehydration. Neurosci Lett 152: 190–193PubMedCrossRefGoogle Scholar
  32. Thomsen LL, Ching LM, Baguley BC (1990) Evidence for the production of nitric oxide by activated macrophages treated with the antitumor agents flavone-8-acetic acid and xanthenone-4-acetic acid. Cancer Res 50: 6966–6970PubMedGoogle Scholar
  33. Villar MJ, Ceccatelli S, Ronnqvist M, Hökfelt T (1994) Nitric oxide synthase increases in hypothalamic magnocellular neurons after salt loading in the rat. An immunohistochemical and in situ hybridization study. Brain Res 644: 273–281PubMedCrossRefGoogle Scholar
  34. Woodside B, Amir S (1996) Reproductive state changes NADPH-diaphorase staining in the paraventricular and supraoptic nuclei of female rats. Brain Res 739: 339–342PubMedCrossRefGoogle Scholar
  35. Wotjak CT, Ganster J, Kohl G, Holsboer F, Landgraf R, Engelmann M (1998) Dissociated central and peripheral release of vasopressin, but not oxytocin, in response to repeated swim stress: new insights into the secretory capacities of peptidergic neurons. Neuroscience 85: 1209–1222PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag/Wien 2004

Authors and Affiliations

  • Mario Engelmann
    • 1
    Email author
  • G. Wolf
    • 1
  • J Putzke
    • 1
  • F. E. Bloom
    • 2
  • J. Raber
    • 2
  • R. Landgraf
    • 3
  • M. G. Spina
    • 1
  • T. F. W. Horn
    • 1
  1. 1.Otto-von-Guericke-Universität MagdeburgInstitut für Medizinische NeurobiologieMagdeburgGermany
  2. 2.Department of NeuropharmacologyScripps Clinics and Research InstituteLa JollaUSA
  3. 3.Max-Planck-Institut für PsychiatrieMünchenGermany

Personalised recommendations