Skip to main content
SpringerLink
Log in

Cells expressing preproenkephalin mRNA in the rat pineal gland are not serotonin-producing pinealocytes: Evidence usingin Situ hybridization combined with immunocytochemistry for serotonin

  • Published:
Cellular and Molecular Neurobiology Aims and scope Submit manuscript

Summary

1. Preproenkephalin (PPEnk) mRNA expressing cells have been identified in rat pineal gland using radioactivein situ hybridization histochemistry.

2. Approximately 7% of the cells in the pineal gland (7.5±0.86, mean ± 95% CI) express PPEnk mRNA. These cells are distributed throughout the pineal as either scattered single cells or small groups of cells with large round or oval nuclei.

3. Usingin situ hybridization combined with ABC immunocytochemistry for serotonin (5-HT) in the same pineal sections, the PPEnk mRNA labeling cells are found not to be serotonin-immunoreactive cells. These data indicate that the PPEnk mRNA is expressed in a certain discrete subpopulation of cells in the rat pineal gland and these cells are not serotonin-producing pinealocytes.

4. The physiologic role of PPEnk-derived peptides in the pineal remains unknown. It is possible that these peptides either are synthesized and secreted as hormones or act as pineal paracrine signals.

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

Similar content being viewed by others

References

  • Aloyo, V. J. (1991). Preproenkephalin A gene expression in rat pineal.Neuroendocrinology 54594–598.

    PubMed  CAS  Google Scholar 

  • Aloyo, V. J. (1992). Identification and characterization of delta opioid binding sites in the bovine pineal.J. Pharmacol. Exp. Ther. 262292–297.

    PubMed  CAS  Google Scholar 

  • Axelrod, J. (1974). The pineal gland: A neurochemical transducer.Science 1841341–1348.

    Article  PubMed  CAS  Google Scholar 

  • Buijs, R. M., and Pévet, P. (1980). Vasopressin- and oxytocin-containing fibers in the pineal gland and subcommissural organ of the rat.Cell Tissue Res. 20511–17.

    Article  PubMed  CAS  Google Scholar 

  • Ebadi, M., Hexum, T. D., Pfeiffer, R. F., and Govitrapong, P. (1989). Pineal and retinal peptides and their receptors. In Reiter, R. J. (Ed.),Pineal Research Reviews, Vol. 7, Alan R. Liss, New York, pp. 1–156.

    Google Scholar 

  • García-Mauriño, J. E., Boya, J., López-Muñoz, F., and Calvo, J. L. (1992). Immunohistochemical localization of nerve growth factor in the rat pineal gland.Brain Res. 585255–259.

    Article  PubMed  Google Scholar 

  • Korf, H.-W., and Moller, M. (1984). The innervation of the mammalian pineal gland with special reference to central pinealopetal projections. In Reiter, R. J. (Ed.),Pineal Research Reviews, Vol. 2, Alan R. Liss, New York, pp. 41–86.

    Google Scholar 

  • Luo, Z. R., Schultz, R. L., Whitter, E. F., and Vollrath, L. (1984). Ultrastructural characterization of glial cells in the rat pineal gland with special reference to the pineal stalk.Anat. Rec. 210663–674.

    Article  PubMed  CAS  Google Scholar 

  • Marín, F., Boya, J., Calvo, J. L., López-Muñoz, F., and García-Mauriño, J. E. (1994). Immunocytochemical localization of basic fibroblast growth factor in the rat pineal gland.J. Pineal Res. 1644–49.

    Article  PubMed  Google Scholar 

  • Martin, J., Prystowsky, M. B., and Angeletti, R. H. (1987). Preproenkephalin mRNA in T-cells, macrophages, and mast cells.J. Neurosci. Res. 1882–87.

    Article  PubMed  CAS  Google Scholar 

  • McNulty, J. A., Fox, L. M., and Silberman, S. (1993). Immunocytochemical demonstration of nerve growth factor (NGF) receptor in the pineal gland: effect of NGF on pinealocyte neurite formation.Brain Res. 610108–114.

    Article  PubMed  CAS  Google Scholar 

  • Mennenga, K., Ueck, M., and Reiter, R. J. (1991). Immunohistological localization of melatonin in the pineal gland and retina of the rat.J. Pineal Res. 10159–164.

    Article  PubMed  CAS  Google Scholar 

  • Mikkelsen, J. D., Moller, M., Larsen, P. J., and Fahrenkrug, J. (1994). The presence of nerve fibers immunoreactive for vasoactive intestinal peptide (VIP), peptide histidine isoleucine (PHI), and prepro VIP(111–122) in the mouse pineal gland.J. Pineal Res. 1650–56.

    Article  PubMed  CAS  Google Scholar 

  • Moller, M., Mikkelsen, J. D., Fahrenkrug, J., and Korf, H.-W. (1985). The presence of vasoactive intestinal polypeptide (VIP)-like-immunoreactive nerve fibres and VIP-receptors in the pineal gland of the Mongolian gerbil (Meriones unguiculatus): An immunohistochemical and receptor-autoradiographic study.Cell Tissue Res. 241333–340.

    Article  PubMed  CAS  Google Scholar 

  • Moore, R. Y., and Sibony, P. (1988). Enkephalin-like immunoreactivity in neurons in the human pineal gland.Brain Res. 457395–398.

    Article  PubMed  CAS  Google Scholar 

  • Pederson, E. B., Fox, L. M., Castro, A. J., and McNulty, J. A. (1993). Immunocytochemical and electron-microscopic characterization of macrophage/microglial cells and expression of class II major histocompatibility complex in the pineal gland of the rat.Cell Tissue Res. 272257–265.

    Article  Google Scholar 

  • Pévet, P. (1983). Anatomy of the pineal gland of mammals. In Relkin, R. (Ed.),The Pineal Gland, Elsevier Biomedical, New York, pp. 1–75.

    Google Scholar 

  • Pévet, P. (1986). The different classes of pineal peptides: Origin and probable physiological role during development. In Gupta, D., and Reiter, R. J. (Eds.),The Pineal Gland During Development: From Fetus to Adult, Croom Helm, London, pp. 234–247.

    Google Scholar 

  • Quay, W. B. (1963). Differential extractions for the spectrophotofluorometric measurement of diverse 5-hydroxy- and 5-methoxyindoles.Anal. Biochem. 551–59.

    Article  PubMed  CAS  Google Scholar 

  • Redding, T. W., and Schally, A. V. (1973). The distribution, half-life, and excretion of tritiated luteinizing hormone-releasing hormone (LH-RH) in rats.Life Sci. Part I 1223–32.

    Article  CAS  Google Scholar 

  • Reiter, R. J. (1991). Pineal melatonin: Cell biology of its synthesis and of its physiological interactions.Endocr. Rev. 12151–180.

    Article  PubMed  CAS  Google Scholar 

  • Reiter, R. J., Richardson, B. A., and King, T. S. (1983). The pineal gland and its indole products: Their importance in the control of reproduction in mammals. In Reiter, R. J. (Ed.),The Pineal Gland, Elsevier Biomedical, New York, pp. 151–199.

    Google Scholar 

  • Ronnekleiv, O. K., and Kelly, M. J. (1984). Distribution of substance P neurons in the epithelamus of the rat: An immunohistochemical investigation.J. Pineal Res. 1355–370.

    Article  PubMed  CAS  Google Scholar 

  • Rosen, H., Douglass, J., and Herbert, E. (1984). Isolation and characterization of the rat proenkephalin gene.J. Biol. Chem. 25914309–14313.

    PubMed  CAS  Google Scholar 

  • Rosenstein, R. E., Chuluyan, H. E., Kanterewicz, B. I., and Cardinali, D. P. (1991). Paracrine relationships among transmitters and modulators in mammalian pineal gland. In Foldes, A., and Reiter, R. J. (Eds),Advances in Pineal Research, Vol.6, John Libbey, pp. 47–55.

    CAS  Google Scholar 

  • Rossier, J., Vargo, T. M., Minick, S., Ling, N., Bloom, F. E., and Guillemin, R. (1977). Regional dissociation of B-endorphin and enkephalin contents in rat brain and pituitary.Proc. Natl. Acad. Sci. USA 745162–5165.

    Article  PubMed  CAS  Google Scholar 

  • Schröder, H., Weihe, E., Nohr, D., and Vollrath, L. (1988). Immunohistochemical evidence for the presence of peptides derived from proenkephalin, prodynorphin and proopiomelanocortin in the guinea pig pineal gland.Histochemistry 88333–341.

    PubMed  Google Scholar 

  • Shiotani, Y., Yamano, M., Shiosaka, S., Emson, P. C., Hillyard, C. J., Girgis, S., and MacIntyre, I. (1986). Distribution and origins of substance P (SP)-, calcitonin gene-related peptide (CGRP)-, vasoactive intestinal polypeptide (VIP)-and neuropeptide Y (NPY)-containing nerve fibers in the pineal gland of gerbils.Neurosci. Lett. 70187–192.

    Article  PubMed  CAS  Google Scholar 

  • Shivers, B. D., Harlan, R. E., Romano, G. J., Howells, R. D., and Pfaff, D. W. (1986). Cellular localization of proenkephalin mRNA in rat brain: Gene expression in the caudate-putamen and cerebellar cortex.Proc. Natl. Acad. Sci. USA 836221–6225.

    Article  PubMed  CAS  Google Scholar 

  • Siegel, R. E. (1987).In situ hybridization histochemistry. In Martin, J., Brownstein, M., and Krieger, D. (Eds.),Brain Peptides Update—Vol. 1, John Wiley and Sons, New York, pp. 81–100.

    Google Scholar 

  • Vaughan, M. K. (1984). Pineal peptides: An overview. In Reiter, R. J. (Ed.),The Pineal Gland, Raven Press, New York, pp. 39–81.

    Google Scholar 

  • Vivien-Roels, B., Pévet, P., Dubois, M. P., Arendt, J., and Brown, G. M. (1981). Immunohistochemical evidence for the presence of melatonin in the pineal gland, the retina and the Harderian gland.Cell Tissue Res. 217105–115.

    Article  PubMed  CAS  Google Scholar 

  • Wilcox, B. J., and Unnerstall, J. R. (1991). Expression of acidic fibroblast growth factor mRNA in the developing and adult rat brain.Neuron 6397–409.

    Article  PubMed  CAS  Google Scholar 

  • Yu, H.-S., Tsin, A. T. C., and Reiter, R. J. (1993). Melatonin: History, biosynthesis, and assay methodology. In Yu, H.-S., and Reiter, R. J. (Eds.),Melatonin: Biosynthesis, Physiological Effects, and Clinical Applications, CRC Press, Boca Raton, FL, pp. 1–16.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy and Cell Biology (M/C512), University of Illinois at Chicago College of Medicine, 808 South Wood Street, 60612, Chicago, Illinois

    Xi-Tao Wang, George D. Pappas, Jacqueline Sagen & James R. Unnerstall

Authors
  1. Xi-Tao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. George D. Pappas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jacqueline Sagen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. James R. Unnerstall
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, XT., Pappas, G.D., Sagen, J. et al. Cells expressing preproenkephalin mRNA in the rat pineal gland are not serotonin-producing pinealocytes: Evidence usingin Situ hybridization combined with immunocytochemistry for serotonin. Cell Mol Neurobiol 16, 73–84 (1996). https://doi.org/10.1007/BF02578388

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02578388

Key words

Search

Navigation