Advertisement

Neurochemical Journal

, Volume 6, Issue 3, pp 185–193 | Cite as

Localization of NADPH-diaphorase and neuronal NO-synthase in the digestive tract of the Masu salmon, Oncorhynchus masou (Osteichthyes: Salmonidae)

  • E. A. Pimenova
  • A. A. Varaksin
Experimental Articles
  • 55 Downloads

Abstract

The morphology, localization, and distribution of nitrergic neurons in the digestive tract of juvenile and adult Masu salmon, Oncorhynchus masou, were studied using histochemical and immunohistochemical methods. We revealed general and age-related peculiarities in the distribution and number of NO-ergic enteric neurons. These neurons were detected in juveniles only in the esophagus and the stomach, while in the adult fish, the neurons were present throughout the gastrointestinal tract. The total number of labeled cells was considerably lower in the proximal intestine than in the esophagus and the stomach, but was some-what greater in the distal intestine. Both in juveniles and adults, neurons and nerve fibers were located within the branches of the vagus nerve, in the myenteric nervous plexus and the circular muscle, and, more rarely, in the submucous nervous plexus and in the longitudinal muscle. Unipolar and bipolar neurons and a large number of undifferentiated and subdifferentiated cells were found, with the latter being more numerous in juveniles. Among multipolar cells, the neurons of Dogiel’s morphological types I and II occurred and they were more abundant in adult fish. Moreover, positive nerve fibers were present in the muscle wall of numerous blood vessels and the swim bladder ducts of juvenile and adult fish.

Keywords

NADPH-diaphorase neuronal NO-synthase digestive tract enteric nervous system Masu salmon Oncorhynchus masou Teleosts 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Bredt, D.S. and Snyder, S.H., Proc. Natl. Acad. Sci. USA, 1990, vol. 87, p. 682–685.PubMedCrossRefGoogle Scholar
  2. 2.
    Donald, J.A. and Broughton, B.R.S., Comp. Biochem. Physiol., 2005, vol. 142, p. 188–197.CrossRefGoogle Scholar
  3. 3.
    Hyndman, K.E., Choe, K.P., Havird, J.S., Rose, R.E., Piermarini, P.M., and Evans, D.H., Comp. Biochem. Physiol., 2006, vol. 144, p. 510–519.CrossRefGoogle Scholar
  4. 4.
    Dawson, T.M., Bredt, D.S., Fotuhi, M., Hwang, P.M., and Snyder, S.H., Proc. Natl. Acad. Sci. USA, 1991, vol. 88, p. 7797–7801.PubMedCrossRefGoogle Scholar
  5. 5.
    Matsumoto, T., Nakane, M., Pollock, J.S., Kuk, J.E., and Forstermann, U., Neurosci. Let, 1993, vol. 155, p. 61–64.CrossRefGoogle Scholar
  6. 6.
    Lamanna, C., Costagliola, A., Vittoria, A., Mayer, B., Assisi, L., Botte, V., and Cecio, A., Anat. Embryol, 1999, vol. 199, p. 397–405.PubMedCrossRefGoogle Scholar
  7. 7.
    Singru, P.S., Sakharkar, A.J., and Subhedar, N., Brain Res., 2003, vol. 977, p. 157–168.PubMedCrossRefGoogle Scholar
  8. 8.
    Shah, V., Lyford, G., Gores, G., and Farrugia, G., Gastroenterology, 2004, vol. 126, p. 903–913.PubMedCrossRefGoogle Scholar
  9. 9.
    Olson, K.R. and Donald, J.A., Acta Histochem, 2009, vol. 111, p. 244–256.PubMedCrossRefGoogle Scholar
  10. 10.
    Olsson, C. and Karila, P., Cell Tissue Res., 1995, vol. 280, p. 297–305.Google Scholar
  11. 11.
    Villani, L., Eur. J. Histochem, 1999, vol. 43, p. 301–310.PubMedGoogle Scholar
  12. 12.
    Chusovitina, S.V. and Varaksin, A.A., Morfologiya, 2003, vol. 123, no. 3, p. 50–53.Google Scholar
  13. 13.
    Chusovitina, S.V., Varaksina, G.S., and Varaksin, A.A., Zh. Evol. Biokhim. Fiziol., 2003, vol. 39, no. 3, p. 287–291.PubMedGoogle Scholar
  14. 14.
    Chusovitina, S.V., Biol. Morya, 2004, vol. 30, no. 3, p. 240–244.Google Scholar
  15. 15.
    Brüning, G., Hattwig, K., and Mayer, B., Cell Tissue Res., 1996, vol. 284, p. 87–98.PubMedCrossRefGoogle Scholar
  16. 16.
    Li, Z.S. and Furness, J.B., Arch. Histol. Cytol, 1993, vol. 56, p. 185–193.PubMedCrossRefGoogle Scholar
  17. 17.
    Domeneghini, C., Radaelli, G., Arrighi, S., Mascarello, F., and Veggeti, A., Eur. J. Histochem., 2000, vol. 44, p. 295–306.PubMedGoogle Scholar
  18. 18.
    Pederzoli, A., Conte, A., Tagliazucchi, D., Gambarelli, A., and Mola, L., Histol. Histopathol., 2007, vol. 22, p. 1057–1064.PubMedGoogle Scholar
  19. 19.
    Holmberg, A., Olsson, C., and Holmgren, S., J. Exp. Biol., 2006, vol. 209, p. 2472–2479.PubMedCrossRefGoogle Scholar
  20. 20.
    Olsson, C., Holmberg, A., and Holmgren, S., J. Comp. Neurol., 2008, vol. 10, p. 756–770.CrossRefGoogle Scholar
  21. 21.
    Uyttebroek, L., Shepherd, I.T., Harrisson, F., Hubens, G., Blust, R., Timmermans, J.P., and Van Nassauw, L., J. Comp. Neurol., 2010, vol. 518, pp. 4419–4438.PubMedCrossRefGoogle Scholar
  22. 22.
    Hope, B.T. and Vincent, S.R., J. Histochem. Cytochem., 1989, vol. 37, p. 653–661.PubMedCrossRefGoogle Scholar
  23. 23.
    Kapoor, B.G., Smit, H., and Verighina, I.A., in Advances in Marine Biology, Russell, F.S., Yonge, M, and Eds., London-New York-San Francisco: Acad. Press, 1975, p. 109–211.Google Scholar
  24. 24.
    Voronina, E.P., Vopr. Ikhtiol., 1997a, vol. 35, no. 5, p. 667–675.Google Scholar
  25. 25.
    Voronina, E.P., Vopr. Ikhtiol., 1997a, vol. 35, no. 5, p. 676–688.Google Scholar
  26. 26.
    Young, H.M., Furness, J.B., Shuttleworth, C.W.R., Bredt, D.S., and Snyder, S.H., Histochemistry, 1992, vol. 97, p. 375–378.PubMedCrossRefGoogle Scholar
  27. 27.
    Costa, M., Furness, J.B., Pompolo, S., Brookes, S.J.H., Bornstein, J.C., Bredt, D.S., and Snyder, S.H., Neurosci. Let., 1992, vol. 148, p. 121–125.CrossRefGoogle Scholar
  28. 28.
    Balaskas, C., Saffrey, M.J., and Burnstock, G., Anat. Rec, 1995, vol. 243, p. 10–18.PubMedCrossRefGoogle Scholar
  29. 29.
    Li, Z.S., Young, H.M., and Furness, J.B., J. Anat, 1994, vol. 184, p. 261–272.PubMedGoogle Scholar
  30. 30.
    Li, Z.S., Furness, J.B., Young, H.M., and Campbell, G., Arch. Histol. Cytol., 1992, vol. 55, p. 333–350.PubMedCrossRefGoogle Scholar
  31. 31.
    Lavrent’ev, B.I., Teoriya stroeniya vegetativnoi nervnoi sistemy (Theory of Structure of Vegetative Nervous System), Moscow: Meditsina, 1983.Google Scholar
  32. 32.
    Nozdrachev, A.D., Skopichev, V.G., and Balashov, I.V., Fiziol. Zh., 1992, vol. 78, no. 7, p. 43–50.Google Scholar
  33. 33.
    Garg, U. and Hassid, A., Biochem. Biophys. Res. Commun., 1990, vol. 171, p. 474–479.PubMedCrossRefGoogle Scholar
  34. 34.
    Cornwell, T.L., Arnold, E., Boerth, N.J., and Lincoln, T.M., Am. J. Physiol., 1994, vol. 267, p. 1405–1413.Google Scholar
  35. 35.
    Murillo-Carretero, M., Ruano, M.J., Matarredona, E.R., Villalobo, A., and Estrada, C., J. Neurochem., 2002, vol. 83, p. 119–131.PubMedCrossRefGoogle Scholar
  36. 36.
    Peunova, N., Scheinker, V., Cline, H., and Enikolopov, G., J. Neurosci., 2001, vol. 21, p. 8809–8818.PubMedGoogle Scholar
  37. 37.
    Santacana, V., Uttenthal, L.O., Bentura, M.L., Fernandez, A.P., and Serrano, J., Martinez De Velasco J., Alinso D., Martinez-Murillo R., Rodrigo J, Dev. Brain Res, 1998, vol. 111, p. 205–222.CrossRefGoogle Scholar
  38. 38.
    Matarredona, E.R., Murillo-Carretero, M., Moreno-Lopez, B., and Estrada, C., Brain Res., 2004, vol. 995, p. 274–284.PubMedCrossRefGoogle Scholar
  39. 39.
    Reutov, V.P., Sorokina, E.G., Okhotin, V.E., and Kositsin, N.S., Tsiklicheskie prevrashcheniya oksida azota v organizme mlekopitayushchikh (Cyclic Transformations of Nitric Oxide in Mammalian Body), Moscow: Nauka, 1997.Google Scholar
  40. 40.
    Brehmer, A., Adv. Anat. Embryol. Cell Biol, 2006, vol. 186, p. 1–91.PubMedCrossRefGoogle Scholar
  41. 41.
    Ramkumar, D. and Schulze, K.S., Curr. Opin. Gastroenterol, 2003, vol. 19, p. 540–545.PubMedCrossRefGoogle Scholar
  42. 42.
    Toda, N. and Okamura, T., Pharmacol. Rev., 2003, vol. 55, p. 271–324.PubMedCrossRefGoogle Scholar
  43. 43.
    Jennings, B.L., Broughton, B.R.S., and Donald, J.A., J. Exp. Biol, 2004, vol. 207, p. 1295–1303.PubMedCrossRefGoogle Scholar
  44. 44.
    Swenson, K.E., Eveland, R.L., Gladwin, M.T., and Swenson, E.R., J. Exp. Zool. A, 2005, vol. 302, p. 154–160.CrossRefGoogle Scholar
  45. 45.
    Nilsson, S., Acta Histochem, 2009, vol. 111, pp. 176–184.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2012

Authors and Affiliations

  1. 1.Zhirmunsky Institute of Marine Biology, Far East BranchRussian Academy of SciencesVladivostokRussia
  2. 2.VladivostokRussia

Personalised recommendations