Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-24T00:40:23.178Z Has data issue: false hasContentIssue false
  • English
  • Français

Somatostatin and prosomatostatin in the retina of the rat: An immunohistochemical, in-situ hybridization, and chromatographic study

Published online by Cambridge University Press:  02 June 2009

Jens Nicolai Brink Larsen ,
Maurizio Bersani ,
James Olcese ,
Jens Juul Holst  and
Morten Møller
Jens Nicolai Brink Larsen
Affiliation:
Institute of Medical Anatomy, Department B, University of Copenhagen, Denmark
Maurizio Bersani
Affiliation:
Institute of Medical Physiology, Department C, University of Copenhagen, Denmark
James Olcese
Affiliation:
Institute of Medical Anatomy, Department B, University of Copenhagen, Denmark
Jens Juul Holst
Affiliation:
Institute of Medical Physiology, Department C, University of Copenhagen, Denmark
Morten Møller
Affiliation:
Institute of Medical Anatomy, Department B, University of Copenhagen, Denmark
Get access Rights & Permissions [Opens in a new window]

Abstract

Specific antisera, raised in rabbits, against somatostatin 1-14, somatostatin 1-28, the fragment 1-12 of somatostatin 1-28, and prosomatostatin 20-36 were used for immunohistochemistry and gel filtration of the rat retina.

With all antisera, immunoreactive perikarya could be located in the inner nuclear and ganglion cell layers. In the inner nuclear layer, amacrine cells with processes extending predominantly into the first sublayer of the inner plexiform layer were observed. Some processes extended also to the ganglion cell layer. In addition, somatostatin-immunoreactive interplexiform cells were present in the inner nuclear layer.

In the ganglion cell layer, perikarya were found located in the midperiphery and in the far periphery of the retina. The neurons located in the midperiphery of the retina possessed a round perikaryon from which processes could be followed going into the inner plexiform layer, where they dichotomized in the third and first sublayers. The perikarya in the far periphery of the retina near the ora serrata exhibited an ovoid-shaped cell body from which processes extended horizontally in a bipolar manner in the layer itself.

By use of an [35S]-labeled antisense oligonucleotide probe, in situ hybridization of the rat retina showed the presence of perikarya in the inner nuclear layer and ganglion cell layer containing mRNA encoding for prosomatostatin.

Gel filtration of the retinal extracts followed by radioimmunoassay showed the presence of somatostatin 1-14, the fragment 1-12 of somatostatin 1-28, and prosomatostatin 1-64. However, somatostatin 1-28 was not detected.

The results obtained in this study verify the presence of somatostatin 1-14 in the rat retina located in perikarya and processes in the inner nuclear and ganglion cell layers. The positive in-situ hybridization signals show that the intraneuronal somatostatin immunoreactivity is due to synthesis of the peptide and not uptake in the neurons. The presence of the somatostatin propeptide and fragments of this propeptide, in both intraretinal perikarya and fibers, indicate a posttranslational modification of this neuropeptide in the perikarya and the processes as well.

Keywords

SomatostatinProsomatostatinRetinaRatImmunohistochemistryIn-situ hybridizationRIAGel filtration
Type
Research Article
Information
Visual Neuroscience , Volume 5 , Issue 5 , November 1990 , pp. 441 - 452
Copyright
Copyright © Cambridge University Press 1990

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Baldissera, F.G.A., Holst, J.J., Jensen, S.L., & Krarup, T. (1985). Distribution and molecular forms of peptide-containing somatostatin immunodeterminants in extracts from th entire gastrointestinal tract of man and pig. Biochimica et Biophysica Acta 838, 132–143.CrossRefGoogle Scholar
Benoit, R., Böhlen, P., Ling, N., Briski, A., Esch, F., Brazau, P., Ying, S.-Y. & Guillemin, R. (1982). Presence of somatostatin-28-(l-12) in hypothalamus and pancreas. Proceeings of the NationalAcademy of Sciences of the U.S.A. 79, 917–921.CrossRefGoogle Scholar
Bersani, M., Thim, L., Baldissera, F.G.A. & Holst, J.J. (1989). Prosomatostatin 1-64 is a major product of somatostatin gene expression in pancreas and gut. Journal of Biological Chemistry 264, 10633–10636.CrossRefGoogle Scholar
Brecha, N. (1983). Retinal neurotransmitters. Histochemical and biochemical studies. In Chemical Neuroanatomy, ed. Emson, P.C., pp. 85–129. New York: Raven Press.Google Scholar
Cowey, A. & Perry, V.H. (1979). The projection of the temporal retina in rats, studied by retrograde transport of horseradish peroxidase. Expermental Brain Research 35, 457–464.Google ScholarPubMed
Eayrs, J.T. (1952). Relationship between the ganglion cell layer of the retina and the optic nerve of the rat. British Journal of Ophthalmology 36, 453–459.CrossRefGoogle ScholarPubMed
Ehinger, B. & Dowling, J.E. (1987). Retinal neurocircuitry and transmission. In Handbook of Chemical Neuroanatomy, Vol. 5: Integrated Systems of the CNS, Part I, ed., Bjöklund, A., Hökfelt, T. & Swanson, L. W., pp. 389–446. Elsevier Science Publishers.Google Scholar
Eriksen, E.F. & Larsson, L.-I. (1981). Neuropeptides in the retina: evidence for differential topographical localization. Peptides, 2, 153–157.CrossRefGoogle ScholarPubMed
Eskay, R.L., Long, R.T. & Iuvone, P.M. (1980). Evidence that TRH, somatostatin, and substance P are present in neurosecretory elements of the vertebrate retina. Brain Research 196, 554–559.CrossRefGoogle ScholarPubMed
Ferriero, D.M. & Sagar, S.M. (1987). Development of somatostatinimmunoreactive neurons in the rat retina. Developmental Brain Research 34, 207–214.CrossRefGoogle Scholar
Goodman, R.H., Aron, D.C. & Roos, B.A. (1983). Rat pre-prosomatostatin: structure and processing by microsomal membranes. Journal of Biological Chemistry 258, 5570–5573.CrossRefGoogle ScholarPubMed
Hilsted, L. & Holst, J.J. (1982). On the accuracy of radioimmunological determination of somatostatin in plasma. Regulatory Peptides 4, 13–31.CrossRefGoogle ScholarPubMed
Holst, J.J. & Aasted, B. (1974). Production and evaluation of glucagon antibodies for radioimmunoassay. Acta Endocrinol (Copenhagen) 77, 715–726.Google ScholarPubMed
Holst, J.J., Baldiserra, F.G.A., Bersani, M., Skak-Nielsen, T., Seier-Poulsen, S. & Nielsen, O. V. (1988). Processing and secretion of prosomatostatin by the pig pancreas. Pancreas 3, 653–661.CrossRefGoogle ScholarPubMed
Johansson, O., Hökfelt, T. & Elde, R.P. (1984). Immunohistochemical distribution of somatostatin-like immunoreactivity in the central nervous system of the adult rat. Neuroscience 13, 265–339.CrossRefGoogle ScholarPubMed
Kossut, M., Yamada, T., Aldrich, L.B. & Pinto, L.H. (1989). Localization and characterization of somatostatin-binding sites in the mouse retina. Brain Research 476, 78–84.CrossRefGoogle ScholarPubMed
Krisch, B. & Leonhardt, H. (1979). Demonstration of somatostatinlike activity in retinal cells of the rat. Cell Tissue Research 204,127–140.CrossRefGoogle Scholar
Larsen, J.N.B., Bersani, M., Olcese, J., Holst, J.J. & Møller, M. (1989). Prosomatostatin and somatostatin in the retina of the rat. An immunocytochemical, chromatografic, and in-situ hybridization study (Abstract). European Journal of Neurosicence (Suppl.). 2, 20.8.Google Scholar
Larsen, J. N. B., Olcese, J., Bersani, M., Holst, J.J. & Møller, M. (in preparation). Prosomatostatin and somatostatin in the retina of the rat. An immunocytochemical, chromatografic, and in-situ hybridization study (Abstract).Google Scholar
Lin, C.T., Li, H.Z. & Wu, J.Y. (1983). Immunocytochemical localization of L-glutamate decarboxylase, gamma-aminobutyric acid transferase, cysteine sulfonic acid decarboxylase, aspartate aminotransferase, and somatostatin in rat retina. Brain Research 270, 273–283.CrossRefGoogle Scholar
Marshak, D. & Yamada, T. (1984). Characterization of somatostatinlike immunoreactivity in vertebrate retinas. Investigative Ophthalmology 25, 112–115.Google ScholarPubMed
Marshak, D., Reewe, J.R., Shively, J.E., Hawke, D., Takami, M.S. & Yamada, T. (1983). Structure of somatostatin isolated from bovine retina. Journal of Neurochemistry 41, 601–606.CrossRefGoogle ScholarPubMed
Mikkelsen, J.D., Larsen, J.N.B., Fahrenkrug, J. & Møller, M. (1987). Peptide histidine-isoleucine (PHI)-immunoreactive amacrine cells in the retina of the rat. Neuorscience Letters 79, 281–285.CrossRefGoogle ScholarPubMed
Negishi, K., Kato, S., Teranishi, T., Kiyama, H., Katayama, Y. & Tohyama, M. (1985). So-called interplexiform cells immunoreactive to tyrosine hydroxylase or somatostatin in rat retina. Brain Research 346, 136–140.CrossRefGoogle ScholarPubMed
Newgard, C. B. & Holst, J.J. (1981). Heterogeneity of somatostatinlike immunoreactivity in extracts of porcine, canine, and human pancreas. Acta Endocrinol (Copenhagen) 98, 564–572.Google Scholar
Nguyen-Legros, J. (1988). Morphology and distribution of catecholamine-neurons in mammalian retina. Progress in Retinal Research 7, 113–147.CrossRefGoogle Scholar
Perry, V.H. (1981). The ganglion cell layer of mammalian retina. Progress in Retinal Research 1, 53–80.CrossRefGoogle Scholar
Rorstad, O.P., Brownstein, M.J. & Martin, J.B. (1979). Immunoreactive and biological active somatostatin-like material in rat retina. Proceedings of the National Academy of Sciences of the U.S.A. 76, 3019–3023.CrossRefGoogle ScholarPubMed
Rorstad, O.P., Senterman, M.K., Hoyte, K.M. & Martin, J.B. (1980). Immunoreactive and biologically active somatostatin-like material in the human retina. Brain Research 199, 488–492.CrossRefGoogle ScholarPubMed
Sagar, S.M. & Marhsall, P.E. (1986). Somatostatin-like immunoreactivity in the human retina. Society for Neuroscience Abstracts 12, 642.Google Scholar
Sagar, S.M. & Marshall, P.E. (1989). Somatostatin-like immunoreactive material in associational ganglion cells of human retina. Neuroscience 27, 507–516.CrossRefGoogle Scholar
Sagar, S.M., Rorstad, O.P., Landis, D.M.D., Arnold, K.A. & Martin, J.B. (1982). Somatostatin-like immunoreactive material in the rabbit retina. Brain Research 224, 91–99.CrossRefGoogle Scholar
Sagar, S.M., Marshall, P.E. & Landix, D.M.D. (1985). Immunoreactive somatostatin in the rat retina: light-microscopic immunocytochemistry and chromatographic characterization. Brain Research 336, 235–242.CrossRefGoogle ScholarPubMed
Shapiro, B., Kronheim, S. & Pimstone, B. (1979). The presence of immunoreactive somatostatin in rat retina. Hormone Metabolic Research 11, 79–80.CrossRefGoogle ScholarPubMed
Shen, L.-P., Pictet, R.L. & Rutter, W.J. (1982). Human somatostatin, I: Sequence of the cDNA. Proceedings of the National Academy of Sciences of the U.S.A. 79, 4575–4579.CrossRefGoogle ScholarPubMed
Skak-Nielsen, T., Holst, J.J., Baldissera, F.G.A. & Poulsen, S.S. (1987). Localization in the gastrointestinal tract of immunoreactive prosomatostatin. Regulatory Peptides 19, 183–195.CrossRefGoogle ScholarPubMed
Smiley, J.F. & Basinger, S.F. (1988). Somatostatin-like immunoreactivity and glycine high-affinity uptake colocalize to an interplexiform cell of the Xenopus laevis retina. Journal of Comparative Neurology 274, 608–618.CrossRefGoogle Scholar
Smiley, J.F. & Basinger, S.F. (1989). Glycine high-affinity uptake labels a subpopulation of somatostatin-like immunoreactive cells in the Rana pipiens retina. Brain Research 495, 31–44.CrossRefGoogle ScholarPubMed
Tornqvist, K., Uddman, R., Sundler, F. & Ehinger, B. (1982). Somatostatin and VIP neurons in the retina of different species. Histochemistry 76, 137–152.CrossRefGoogle ScholarPubMed
Yamada, T. (1989). Biochemistry and localization of somatostatin in the retina. Progress in Retinal Research 8, 109–128.CrossRefGoogle Scholar
Yamada, T., Marshak, D., Basinger, S., Walsh, J., Morley, J. & Stell, W. (1980). Somatostatin-like immunoreactivity in the retina. Proceedings of the National Academy of Sciences of the U.S.A. 7 1691–1695.CrossRefGoogle Scholar