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The Scientific World Journal
Volume 2012, Article ID 416936, 7 pages
http://dx.doi.org/10.1100/2012/416936
Research Article

Impact of Environmental Thermal Stimulation on Activation of Hypothalamic Neuronal Nitric Oxide Synthase during the Prenatal Ontogenesis in Muscovy Ducks

1Institute of Biology, Humboldt-University of Berlin, Philippstraße 13, 10115 Berlin, Germany
2Department of Human Ecology, Belorussian State University, prospect Nezavisimosti 4, 220050, Minsk, Belarus

Received 30 October 2011; Accepted 11 December 2011

Academic Editor: Richard A. Morrisett

Copyright © 2012 Valery Dunai and Barbara Tzschentke. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. B. Tzschentke and A. Plagemann, “Imprinting and critical periods in early development,” World's Poultry Science Journal, vol. 62, no. 4, pp. 626–726, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Szyf, P. McGowan, and M. J. Meaney, “The social environment and the epigenome,” Environmental and Molecular Mutagenesis, vol. 49, no. 1, pp. 46–60, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Nott and A. Riccio, “Nitric oxide-mediated epigenetic mechanisms in developing neurons,” Cell Cycle, vol. 8, no. 5, pp. 725–730, 2009. View at Google Scholar · View at Scopus
  4. J. Garthwaite and C. L. Boulton, “Nitric oxide signaling in the central nervous system,” Annual Review of Physiology, vol. 57, pp. 683–706, 1995. View at Google Scholar · View at Scopus
  5. J. Garthwaite, “Concepts of neural nitric oxide-mediated transmission,” European Journal of Neuroscience, vol. 27, no. 11, pp. 2783–2802, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. C. L. M. Bon and J. Garthwaite, “On the role of nitric oxide in hippocampal long-term potentiation,” Journal of Neuroscience, vol. 23, no. 5, pp. 1941–1948, 2003. View at Google Scholar · View at Scopus
  7. S. Liu, M. Fa, I. Ninan, F. Trinchese, W. Dauer, and O. Arancio, “α-Synuclein involvement in hippocampal synaptic plasticity: role of NO, cGMP, cGK and CaMKII,” European Journal of Neuroscience, vol. 25, no. 12, pp. 3583–3596, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. N. Majlessi, S. Choopani, T. Bozorgmehr, and Z. Azizi, “Involvement of hippocampal nitric oxide in spatial learning in the rat,” Neurobiology of Learning and Memory, vol. 90, no. 2, pp. 413–419, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. E. Fino, V. Paille, J. M. Deniau, and L. Venance, “Asymmetric spike-timing dependent plasticity of striatal nitric oxide-synthase interneurons,” Neuroscience, vol. 160, no. 4, pp. 744–754, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Zhang and S. H. Snyder, “Nitric oxide in the nervous system,” Annual Review of Pharmacology and Toxicology, vol. 35, pp. 213–233, 1995. View at Google Scholar · View at Scopus
  11. H. C. Pape and R. Mager, “Nitric oxide controls oscillatory activity in thalamocortical neurons,” Neuron, vol. 9, no. 3, pp. 441–448, 1992. View at Publisher · View at Google Scholar · View at Scopus
  12. W. F. Taylor and V. S. Bishop, “A role for nitric oxide in active thermoregulatory vasodilation,” American Journal of Physiology, vol. 264, no. 5, pp. H1355–H1359, 1993. View at Google Scholar · View at Scopus
  13. V. I. Dunai and A. V. Gourine, “Effect of the NO synthase inhibitor, L-NAME, on body temperature in birds in different periods of postnatal ontogenesis,” in Recent Advances in Thermal Biology, V. N. Guorine, Ed., pp. 18–19, Minsk, 1999. View at Google Scholar
  14. S. S. Malik and J. E. Fewell, “Thermoregulation in rats during early postnatal maturation: importance of nitric oxide,” American Journal of Physiology, vol. 285, no. 6, pp. R1366–R1372, 2003. View at Google Scholar · View at Scopus
  15. D. H. S. Pereira, L. G. S. Branco, E. C. Cárnio, and R. C. H. Barros, “nNOS is involved in behavioral thermoregulation of newborn rats during hypoxia,” Physiology and Behavior, vol. 89, no. 5, pp. 681–686, 2006. View at Publisher · View at Google Scholar
  16. A. C. Coleone, K. A. A. Torres, E. C. Carnio et al., “Role of brain nitric oxide in the thermoregulation of broiler chicks,” Comparative Biochemistry and Physiology, vol. 154, no. 2, pp. 204–210, 2009. View at Publisher · View at Google Scholar
  17. T. Hübschle, I. Küchenmeister, and R. Gerstberger, “Central action of nitric oxide in the saltwater-acclimated duck: modulation of extrarenal sodium excretion and vasotocin release,” Brain Research, vol. 825, no. 1-2, pp. 22–35, 1999. View at Publisher · View at Google Scholar · View at Scopus
  18. H. Schwimmer, R. Gerstberger, and M. Horowitz, “Heat acclimation affects the neuromodulatory role of AngII and nitric oxide during combined heat and hypohydration stress,” Molecular Brain Research, vol. 130, no. 1-2, pp. 95–108, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Amir, E. De Blasio, and A. M. English, “N(G)-Monomethyl-L-arginine co-injection attenuates the thermogenic and hyperthermic effects of E2 prostaglandin microinjection into the anterior hypothalamic preoptic area in rats,” Brain Research, vol. 556, no. 1, pp. 157–160, 1991. View at Publisher · View at Google Scholar · View at Scopus
  20. A. V. Gourine, “Role of nitric oxide in lipopolysaccharide-induced fever in conscious rabbits,” The Journal of Physiology, vol. 475, p. 28, 1994. View at Google Scholar
  21. Y. H. Choi, M. Furuse, J. I. Okumura, and D. M. Denbow, “Nitric oxide controls feeding behavior in the chicken,” Brain Research, vol. 654, no. 1, pp. 163–166, 1994. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Vozzo, G. A. Wittert, I. M. Chapman et al., “Evidence that nitric oxide stimulates feeding in the marsupial Sminthopsis crassicaudata,” Comparative Biochemistry and Physiology, vol. 123, no. 2, pp. 145–151, 1999. View at Publisher · View at Google Scholar
  23. S. J. Yang and D. M. Denbow, “Interaction of leptin and nitric oxide on food intake in broilers and Leghorns,” Physiology and Behavior, vol. 92, no. 4, pp. 651–657, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. M. S. I. Khan, T. Tachibana, Y. Hasebe, N. Masuda, and H. Ueda, “Peripheral or central administration of nitric oxide synthase inhibitor affects feeding behavior in chicks,” Comparative Biochemistry and Physiology, vol. 148, no. 2, pp. 458–462, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. M. S. I. Khan, Y. Nakano, T. Tachibana, and H. Ueda, “Nitric oxide synthase inhibitor attenuates the anorexigenic effect of corticotropin-releasing hormone in neonatal chicks,” Comparative Biochemistry and Physiology, vol. 149, no. 3, pp. 325–329, 2008. View at Publisher · View at Google Scholar
  26. C. J. Sadler and J. P. H. Wilding, “Reduced ventromedial hypothalamic neuronal nitric oxide synthase and increased sensitivity to NOS inhibition in dietary obese rats: further evidence of a role for nitric oxide in the regulation of energy balance,” Brain Research, vol. 1016, no. 2, pp. 222–228, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. T. Horn, P. M. Smith, B. E. McLaughlin et al., “Nitric oxide actions in paraventricular nucleus: cardiovascular and neurochemical implications,” American Journal of Physiology, vol. 266, no. 1, pp. R306–R313, 1994. View at Google Scholar · View at Scopus
  28. B. C. W. Groenendijk, B. P. Hierck, A. C. Gittenberger-De Groot, and R. E. Poelmann, “Development-related changes in the expression of shear stress responsive genes KLF-2, ET-1, and NOS-3 in the developing cardiovascular system of chicken embryos,” Developmental Dynamics, vol. 230, no. 1, pp. 57–68, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Pyner, “Neurochemistry of the paraventricular nucleus of the hypothalamus: implications for cardiovascular regulation,” Journal of Chemical Neuroanatomy, vol. 38, no. 3, pp. 197–208, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. S. Eriksson, H. Hjelmqvist, R. Keil, and R. Gerstberger, “Central application of a nitric oxide donor activates heat defense in the rabbit,” Brain Research, vol. 774, no. 1-2, pp. 269–273, 1997. View at Publisher · View at Google Scholar · View at Scopus
  31. G. Bruning, “Localization of NADPH-diaphorase in the brain of the chicken,” Journal of Comparative Neurology, vol. 334, no. 2, pp. 192–208, 1993. View at Google Scholar · View at Scopus
  32. C. M. Montagnese and A. Csillag, “Comparative distribution of NADPH-diaphorase activity and tyrosine hydroxylase immunoreactivity in the diencephalon and mesencephalon of the domestic chicken (Gallus domesticus),” Anatomy and Embryology, vol. 193, no. 5, pp. 427–439, 1996. View at Google Scholar · View at Scopus
  33. M. Nichelmann and B. Tzschentke, “Ontogeny of thermoregulation in precocial birds,” Comparative Biochemistry and Physiology, vol. 131, no. 4, pp. 751–763, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. B. Tzschentke and D. Basta, “Development of hypothalamic neuronal thermosensitivity in birds during the perinatal period,” Journal of Thermal Biology, vol. 25, no. 1-2, pp. 119–123, 2000. View at Publisher · View at Google Scholar · View at Scopus
  35. B. Tzschentke and D. Basta, “Early development of neuronal hypothalamic thermosensitivity in birds: influence of epigenetic temperature adaptation,” Comparative Biochemistry and Physiology, vol. 131, no. 4, pp. 825–832, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. B. Tzschentke, “Attainment of thermoregulation as affected by environmental factors,” Poultry Science, vol. 86, no. 5, pp. 1025–1036, 2007. View at Google Scholar · View at Scopus
  37. B. Tzschentke and M. Rumpf, “Embryonic development of endothermy,” Respiratory Physiology and Neurobiology, vol. 178, no. 1, pp. 97–107, 2011. View at Publisher · View at Google Scholar
  38. B. Tzschentke, D. Basta, O. Janke, and I. Maier, “Characteristics of early development of body functions and epigenetic adaptation to the environment in poultry: focused on development of central nervous mechanisms,” Avian and Poultry Biology Reviews, vol. 15, no. 3-4, pp. 107–118, 2004. View at Google Scholar · View at Scopus
  39. O. Janke and B. Tzschentke, “Long-lasting effect of changes in incubation temperature on heat stress induced neuronal hypothalamic c-Fos expression in chickens. Special Issue: early development and epigenetic programming of body functions in birds (Ed. Tzschentke, B.),” The Open Ornithology Journal, vol. 3, pp. 150–155, 2010. View at Google Scholar
  40. G. C. Whittow and H. Tazawa, “The early development of thermoregulation in birds,” Physiological Zoology, vol. 64, no. 6, pp. 1371–1390, 1991. View at Google Scholar · View at Scopus
  41. H. Tazawa and G. C. Whittow, “Incubation physiology,” in Sturkey’s Avian Physiology, pp. 617–634, Academic Press, New York, NY, USA, 5th edition, 2000. View at Google Scholar
  42. U. Scherer Singler, S. R. Vincent, H. Kimura, and E. G. McGeer, “Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry,” Journal of Neuroscience Methods, vol. 9, no. 3, pp. 229–234, 1983. View at Publisher · View at Google Scholar · View at Scopus
  43. B. T. Hope and S. R. Vincent, “Histochemical characterization of neuronal NADPH-diaphorase,” Journal of Histochemistry and Cytochemistry, vol. 37, no. 5, pp. 653–661, 1989. View at Google Scholar · View at Scopus
  44. T. Matsumoto, M. Nakane, J. S. Pollock, J. E. Kuk, and U. Forstermann, “A correlation between soluble brain nitric oxide synthase and NADPH-diaphorase activity is only seen after exposure of the tissue to fixative,” Neuroscience Letters, vol. 155, no. 1, pp. 61–64, 1993. View at Publisher · View at Google Scholar · View at Scopus
  45. W. J. Kuenzel and A. van Tienhoven, “Nomenclature and location of avian hypothalamic nuclei and associated circumventricular organs,” Journal of Comparative Neurology, vol. 206, no. 3, pp. 293–313, 1982. View at Google Scholar · View at Scopus
  46. W. J. Kuenzel and M. Masson, A Stereotaxic Atlas of the Brain of the Chick (Gallus domesticus), The John Hopkins University Press, Baltimore, Md, USA, 1998.
  47. B. Tzschentke, “Monitoring the development of thermoregulation in poultry embryos and its influence by incubation temperature,” Computers and Electronics in Agriculture, vol. 64, no. 1, pp. 61–71, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Nichelmann and B. Tzschentke, “Thermoregulation in precocial avian embryos,” Ornis Fennica, vol. 76, no. 4, pp. 177–187, 1999. View at Google Scholar · View at Scopus
  49. O. Janke, B. Tzschentke, J. Höchel, and M. Nichelmann, “Metabolic responses of chicken and muscovy duck embryos to high incubation temperatures,” Comparative Biochemistry and Physiology, vol. 131, no. 4, pp. 741–750, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Nichelmann, A. Burmeister, O. Janke, J. Höchel, and B. Tzschentke, “Avian embryonic thermoregulation: role of Q10 in interpretation of endothermic reactions,” Journal of Thermal Biology, vol. 23, no. 6, pp. 369–376, 1998. View at Publisher · View at Google Scholar · View at Scopus
  51. B. Loh, I. Maier, A. Winar, O. Janke, and B. Tzschentke, “Prenatal development of epigenetic adaptation processes in poultry: changes in metabolic and neuronal thermoregulatory mechanisms,” Avian and Poultry Biology Reviews, vol. 15, no. 3-4, pp. 119–128, 2004. View at Google Scholar · View at Scopus
  52. T. Nakashima, F. K. Pierau, E. Simon, and T. Hori, “Comparison between hypothalamic thermoresponsive neurons from duck and rat slices,” Pflugers Archiv European Journal of Physiology, vol. 409, no. 3, pp. 236–243, 1987. View at Google Scholar · View at Scopus
  53. H. A. Schmid, L. Jansky, and F. -K. Pierau, “Temperature sensitivity of neurons in slices of the rat PO/AH area: effect of bombesin and substance P,” American Journal of Physiology, vol. 264, no. 2, pp. R449–R455, 1993. View at Google Scholar
  54. B. Tzschentke and I. Halle, “Influence of temperature stimulation during the last 4 days of incubation on secondary sex ratio and later performance in male and female broiler chicks,” British Poultry Science, vol. 50, no. 5, pp. 634–640, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. B. Tzschentke and M. Nichelmann, “Development of avian thermoregulatory system during the early postnatal period: development of the thermoregulatory set-point,” Ornis Fennica, vol. 76, no. 4, pp. 189–198, 1999. View at Google Scholar · View at Scopus
  56. T. M. Gilbert and C. M. Blatteis, “Hypothalamic thermoregulatory pathways in the rat,” Journal of Applied Physiology Respiratory Environmental and Exercise Physiology, vol. 43, no. 5, pp. 770–777, 1977. View at Google Scholar · View at Scopus
  57. K. Kanosue, M. Yanase-Fujiwara, and T. Hosono, “Hypothalamic network for thermoregulatory vasomotor control,” American Journal of Physiology, vol. 267, no. 1, pp. R283–R288, 1994. View at Google Scholar
  58. K. Kanosue, Zhang Yi Hong, M. Yanase-Fujiwara, and T. Hosono, “Hypothalamic network for thermoregulatory shivering,” American Journal of Physiology, vol. 267, no. 1, pp. R275–R282, 1994. View at Google Scholar · View at Scopus
  59. B. J. Oldfield, M. E. Giles, A. Watson, C. Anderson, L. M. Colvill, and M. J. McKinley, “The neurochemical characterisation of hypothalamic pathways projecting polysynaptically to brown adipose tissue in the rat,” Neuroscience, vol. 110, no. 3, pp. 515–526, 2002. View at Publisher · View at Google Scholar · View at Scopus
  60. P. R. Kamerman, H. P. Laburn, and D. Mitchell, “Inhibitors of nitric oxide synthesis block cold-induced thermogenesis in rats,” Canadian Journal of Physiology and Pharmacology, vol. 81, no. 8, pp. 834–838, 2003. View at Google Scholar · View at Scopus
  61. A. C. R. Lacerda, U. Marubayashi, and C. C. Coimbra, “Nitric oxide pathway is an important modulator of heat loss in rats during exercise,” Brain Research Bulletin, vol. 67, no. 1-2, pp. 110–116, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. A. A. Steiner, J. Antunes-Rodrigues, S. M. McCann, and L. G. S. Branco, “Antipyretic role of the NO-cGMP pathway in the anteroventral preoptic region of the rat brain,” American Journal of Physiology, vol. 282, no. 2, pp. R584–R593, 2002. View at Google Scholar
  63. A. Ar, O. Ifergan, A. Feldman, L. Zelik, and A. Reizis, “Possible role of nitric oxide emission from bird embryos,” Avian and Poultry Biology Reviews, vol. 15, no. 3-4, pp. 105–106, 2004. View at Google Scholar · View at Scopus