Skip to main content
SpringerLink
Log in

Immunohistochemical demonstration of salmon olfactory glutathione S-transferase class pi (N24) in the olfactory system of lacustrine sockeye salmon during ontogenesis and cell proliferation

  • Original Article
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

In mammals, glutathione S-transferase (GST) in the olfactory epithelium is involved in assistance of the olfactory reception by the xenobiotic metabolism. We previously reported the protein and gene expressions of salmon olfactory GST class pi (soGST) in the olfactory receptor cells (ORCs) of the salmonid fish. However, the chronological appearances of soGST in ORCs during ontogeny and cell proliferation are still unknown in this species. In this study, we performed immunohistochemistry of soGST using an antibody specific to soGST in the olfactory system (olfactory placode, olfactory pit, olfactory epithelium, olfactory nerve and olfactory bulb) of lacustrine sockeye salmon (Oncorhynchus nerka) embryos and 5-bromo-2′-deoxyuridine (BrdU) experimental fish. The projection of olfactory nerve bundles from the olfactory pit to the presumptive olfactory bulb was identified at embryonic day 28 after fertilization. The olfactory cilia were first detected on the apical surface of ORCs at day 43. soGST-immunoreactivity was first detected within the olfactory pit cells at day 55. At 58 day, the number of soGST-immunoreactive cells increased markedly in the olfactory epithelia, and soGST-immunoreactive fibers were observed in the olfactory nerves and olfactory bulbs. By in vivo uptake of BrdU in 1-year-old fish, we observed for the first time at day 7 after labeling that the olfactory epithelia showed ORCs in which both soGST-immunoreactivity and BrdU coexisted. These results indicate that soGST is synthesized in the mature ORCs of lacustrine sockeye salmon after cell formation and differentiation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1A–E
Fig. 2A–D
Fig. 3
Fig. 4A–C
Fig. 5A, B

Similar content being viewed by others

References

  • Banger KK, Foster JR, Lock EA, Reed CJ (1994) Immunohistochemical localization of six glutathione S-transferases within the nasal cavity of the rat. Arch Toxicol 69:91–98

    Article  CAS  PubMed  Google Scholar 

  • Banger KK, Lock EA, Reed CJ (1993) The characterization of glutathione S-transferases from rat olfactory epithelium. Biochem J 290:199–204

    CAS  PubMed  Google Scholar 

  • Ben-Arie N, Khen M, Lancet D (1993) Glutathione S-transferase in rat olfactory epithelium: purification, molecular properties and odorant biotransformation. Biochem J 292:379–384

    CAS  PubMed  Google Scholar 

  • Dittman AH, Quinn TP (1996) Homing in pacific salmon: mechanisms and ecological basis. J Exp Biol 199:83–91

    PubMed  Google Scholar 

  • Farbman AI, Margolis FL (1980) Olfactory marker protein during ontogeny: immunohistochemical localization. Dev Biol 74:205–215

    CAS  PubMed  Google Scholar 

  • Graziadei PPC, Metcalf JF (1971) Autoradiographic and ultrastructural observations on the frog’s olfactory mucosa. Z Zellforsch Mikrosk Anat 116:305–318

    CAS  PubMed  Google Scholar 

  • Graziadei PPC, Monti-Graziadei GA (1979) Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J Neurocytol 8:1–18

    CAS  PubMed  Google Scholar 

  • Jakoby WB (1978) The glutathione S-transferase: a group of multifunctional detoxification proteins. Adv Enzymol Relat Areas Mol Biol 46:383–414

    CAS  PubMed  Google Scholar 

  • Krishna NS, Getchell TV, Getchell ML (1994) Differential expression of alpha, mu, and pi classes of glutathione S-transferases in chemosensory mucosae of rats during development. Cell Tissue Res 275:435–450

    Google Scholar 

  • Kudo H, Doi Y, Nishino T, Nara S, Hamasaki K, Fujimoto S (2000) Dietary zinc deficiency decreases glutathione S-transferase expression in the rat olfactory epithelium. J Nutr 130:38–44

    CAS  PubMed  Google Scholar 

  • Kudo H, Ueda H, Mochida K, Adachi S, Hara A, Nagasawa H, Doi Y, Fujimoto S, Yamauchi K (1999) Salmonid olfactory system-specific protein (N24) exhibits glutathione S-transferase class pi-like structure. J Neurochem 72:1344–1352

    Article  CAS  PubMed  Google Scholar 

  • Kudo H, Ueda H, Yamauchi K (1996) Immunocytochemical investigation of a salmonid olfactory system-specific protein in the olfactory system of kokanee salmon (Oncorhynchus nerka). Zool Sci 13:647–653

    CAS  Google Scholar 

  • Mannervik B, Danielson UH (1988) Glutathione transferases, structure and catalytic activity. Crit Rev Biochem 23:283–337

    CAS  Google Scholar 

  • Meyer DJ, Coles B, Pemble SE, Gilmore KS, Fraser GM, Ketterer B (1991) Theta, a new class of glutathione transferases purified from rat and man. Biochem J 274:409–414

    CAS  PubMed  Google Scholar 

  • Monti-Graziadei GA, Stanley RS, Graziadei PPC (1980) The olfactory marker protein in the olfactory system of the mouse during development. Neuroscience 5:1239–1252

    Article  PubMed  Google Scholar 

  • Nakamura H (1991) Immunohistochemical observations of dividing cells in olfactory epithelium using anti-BrdU antibody. Eur Arch Otorhinolaryngol 248:298–301

    CAS  PubMed  Google Scholar 

  • Riddle DR, Oakley B (1992) Immunocytochemical identification of primary olfactory afferents in rainbow trout. J Comp Neurol 324:575–589

    CAS  PubMed  Google Scholar 

  • Salinas AE, Wong MG (1999) Glutathione S-transferases: a review. Curr Med Chem 6:279–309

    CAS  PubMed  Google Scholar 

  • Shimizu M, Kudo H, Ueda H, Hara A, Shimazaki K, Yamauchi K (1993) Identification and immunological properties of an olfactory system-specific protein in kokanee salmon (Oncorhynchus nerka). Zool Sci 10:287–294

    CAS  Google Scholar 

  • Stabell OB (1992) Olfactory control of homing behaviour in salmonids: In: Hara TJ (ed) Fish Chemoreception. Chapman, London, pp 249–270

  • Starcevic SL, Muruganandam A, Mutus B, Zielinski BS (1993) Glutathione in the olfactory mucosa of rainbow trout (Oncorhynchus mykiss). Chem Senses 18:57–65

    CAS  Google Scholar 

  • Starcevic SL, Zielinski BS (1995) Immunohistochemical localization of glutathione S-transferase pi in rainbow trout olfactory receptor neurons. Neurosci Lett 183:175–178

    Article  CAS  PubMed  Google Scholar 

  • Suzuki Y, Takeda M (1993) Basal cells in the mouse olfactory epithelium during development: immunohistochemical and electron-microscopic studies. Brain Res Dev Brain Res 73:107–113

    Article  CAS  PubMed  Google Scholar 

  • Wang MM, Tsai RY, Schrader KA, Reed RR (1993) Genes encoding components of the olfactory signal transduction cascade contain a DNA binding site that may direct neuronal expression. Mol Cell Biol 13:5805–5813

    CAS  PubMed  Google Scholar 

  • Zielinski B, Hara TJ (1988) Morphological and physiological development of olfactory receptor cells in rainbow trout (Salmo gairdneri) embryos. J Comp Neurol 271:300–311

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Dr. Jill B.K. Leonard, Northern Michigan University for critical reading of the manuscript and Mr. Hiroyuki Haruna, Toya Lake Station for Environmental Biology, for his technical assistance in this study. This study was supported in part by Grants-in-Aids from the Fisheries Agency of Japan and from the Ministry of Education, Science, Sports and Culture, Japan.

Author information

Authors and Affiliations

  1. Division of Marine Biosciences, Graduate School of Fisheries Sciences, Hokkaido University, 041-8611, Hakodate, Japan

    S. Yanagi & K. Yamauchi

  2. Department of Anatomy, University of Occupational and Environmental Health, School of Medicine, 807-8555, Kitakyushu, Japan

    H. Kudo & Y. Doi

  3. Field Science Center for Northern Biosphere, Hokkaido University, 060-0809, Sapporo, Japan

    H. Ueda

Authors
  1. S. Yanagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H. Kudo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Y. Doi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. Yamauchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. H. Ueda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to H. Kudo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yanagi, S., Kudo, H., Doi, Y. et al. Immunohistochemical demonstration of salmon olfactory glutathione S-transferase class pi (N24) in the olfactory system of lacustrine sockeye salmon during ontogenesis and cell proliferation. Anat Embryol 208, 231–238 (2004). https://doi.org/10.1007/s00429-004-0392-3

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-004-0392-3

Keywords

Search

Navigation