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Effects of hibernation on somatostatin-like immunoreactivity in the brain of the ground squirrel (Spermophilus richardsonii) and European hedgehog (Erinaceus europaeus)

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Summary

The localization of the somatostatin system in the brains of Richardson's ground squirrels (Spermophilus richardsonii) and European hedgehogs (Erinaceus europaeus) was described by use of immunocytochemical methods. In addition, (i) chemically differing types of somatostatin and (ii) different activity phases of the somatostatin system during the hibernation cycle were investigated in the ground squirrel by means of high pressure liquid chromatography (HPLC) and radioimmunoassay (RIA).

In both species, the hypothalamic component of the somatostatin system (periventricular nuclei, fiber projections to the median eminence) is more prominent than the widespread extrahypothalamic representation of the system displaying mainly scattered perikarya and nerve fibers. The reactivity pattern of the somatostatin system varied among hibernating, aroused, and non-hibernating animals; moreover, the interspecific differences were pronounced. The activity of the hypothalamic somatostatin system in the hibernating ground squirrel appeared to be suppressed when compared to non-hibernating controls, whereas in the hibernating hedgehog this system showed signs of increased activity in comparison to non-hibernating controls. In contrast, in the present material the extrahypothalamic components of the somatostatin system did not exhibit significant changes in their activity.

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References

  • Arnold MA, Reppert SM, Rostad OP, Sayar SM, Keutmann HT, Perlow MJ, Martin JB (1982) Temporal patterns of somatostatin immunoreactivity in the cerebrospinal fluid of the Rhesus monkey: Effect of environmental lighting. J Neurosci 2:674–680

    Google Scholar 

  • Azzali G (1955) Aspetti istofisiologici dell'apparato neurosecretorio diencephalico nel riccio (Erinaceus europaeus) in condizioni normali e sperimentali. Z Zellforsch 41:391–406

    Google Scholar 

  • Benoit R, Ling N, Alford B, Guillemin R (1982) Seven peptides derived from pro-somatostatin in rat brain. Biochem Biophys Res Commun 107:944–950

    Google Scholar 

  • Blähser S, Fellmann D, Bugnon C (1978) Immunocytochemical demonstration of somatostatin-containing neurons in the hypothalamus of the domestic mallard. Cell Tissue Res 195:183–187

    Google Scholar 

  • Brownstein MJ, Arimura A, Fernandez-Durango R, Schally AV, Palkovits M, Kizer JS (1977) The effect of hypothalamic deafferentation on somatostatin-like activity in the rat brain. Endocirnology 100:246–249

    Google Scholar 

  • Bugnon C, Fellmann D, Block B (1977) Immunocytochemical study on the ontogenesis of the hypothalamic somatostatincontaining neurons in the human fetus. Cell Tissue Res 183:319–328

    Google Scholar 

  • Demeneix BA, Henderson NE (1978) Thyroid hormone metabolism over the annual cycle of Spermophilus richardsoni. J Therm Biol 3:89–90

    Google Scholar 

  • Doerr-Schott J, Dubois MP (1978) Immunohistochemical localization of different peptidergic substances in the brain of amphibians and reptiles. In: Gaillard PG, Boer HH (eds) Comparative endocrinology. Elsevier/North Holland Biomedical Press, Amsterdam, pp 367–370

    Google Scholar 

  • Dube D, Leclerc R, Pelletier G, Arimura A, Schally AV (1975) Immunocytochemical detection of growth-hormone release inhibiting hormone (somatostatin) in the guinea-pig brain. Cell Tissue Res 161:385–392

    Google Scholar 

  • Dubois MP (1976) Le système à somatostatine. Ann endocrinol (Paris) 37:277–278

    Google Scholar 

  • Dubois MP, Barry J, Leonardelli J (1974) Mise en évidence par immunofluorescence et répartition de la somatostatine (SRIF) dans l'éminence mediane des Vertébrés (Mammifères, Oiseaux, Amphibiens, Poissons). CR acad Sci Paris 279:1899–1902

    Google Scholar 

  • Dubois MP, Billard R, Breton B, Peter RE (1979) Comparative distribution of somatostatin, LH-RH, neurophysin, and endorphin in the rainbow trout: an immunocytological study. Gen Comp Endocrinol 37:220–232

    Google Scholar 

  • Eisentraut M (1934) Der Winterschlaf der Fledermäuse mit besonderer Berücksichtigung der Wärmeregulation. Z Morphol Ökol 29:231–267

    Google Scholar 

  • Eisentraut M (1956) Der Winterschlaf mit seinen ökologischen und physiologischen Begleiterscheinungen. Fischer, Jena

    Google Scholar 

  • Elde R, Hökfelt T (1978) Distribution of hypothalamic hormones and other peptides in the brain. In: Ganong WF, Martini L (eds) Frontiers in neuroendocrinology. Vol 5. Raven Press, New York, pp 1–33

    Google Scholar 

  • Elde R, Parsons JA (1975) Immunocytochemical localization of somatostatin in cell bodies of the rat hypothalamus. Am J Anat 144:541–548

    Google Scholar 

  • Elde R, Hökfelt T, Johansson O, Shultzberg M, Efendic S, Luft R (1978) Cellular localization of somatostatin. Metabolism 27:1151–1159

    Google Scholar 

  • Epelbaum J, Brazeau P, Tsang D, Brawer J, Martin JB (1977) Subcellular distribution of radioimmunoassayable somatostatin in rat brain. Brain Res 126:309–323

    Google Scholar 

  • Finlay JCW, Maderdrut JL, Petrusz P (1981) The immunocytochemical localization of enkephalin in the central nervous system of the rat. J Comp Neurol 198:541–565

    Google Scholar 

  • Gomes S, Morel A, Nicholas P, Cohen P (1983) Regional distribution of the Mr 15000 somatostatin precursor, somatostatin-28 and somatostatin-14 in the rat brain suggests a differential intracellular processing of the high molecular weight species. Biochem Biophys Res Commun 112:297–305

    Google Scholar 

  • Graybiel AM, Elde RP (1983) Somatostatin-like immunoreactivity characterizes neurons of the nucleus reticularis thalami in the cat and monkey. J Neurosci 3:1308–1321

    Google Scholar 

  • Hökfelt T, Efendic S, Hellström C, Johansson O, Luft R, Arimura A (1975) Cellular localization of somatostatin in endocrine like cells and neuorns of the rat with special reference to the a1 cells of the pancreatic islets and to the hypothalamus. Acta Endocrinol (Kbh) 80 [Suppl] 200:5–41

    Google Scholar 

  • Hökfelt T, Elde R, Fuxe K, Johansson O, Ljungdahl A, Goldstein M, Luft R, Efendic S, Nilsson G, Terenius L, Ganten D, Jeffcoate SL, Rehfeld J, Said S, Perez de la Mora M, Possani L, Tapia R, Teran L, Palacios R (1978) Aminergic and peptidergic pathways in the nervous system with special reference to the hypothalamus. In: Rechlin S, Baidessarini R, Martin JB (eds) The hypothalamus. Vol 56. Raven Press, New York, pp 69ff

    Google Scholar 

  • Hudson JW, Wang LCH (1969) Thyroid function in dessert ground squirrels. In: Hoff CC, Riedesel ML (eds) Physiological systems in semiarid environments. Univ of New Mexico Press, Albuquerque, pp 17–33

    Google Scholar 

  • Hudson JW, Wang LCH (1979) Hibernation: endocrine aspects. Ann Rev Physiol 41:287–303

    Google Scholar 

  • Kayser C (1961) The physiology of natural hibernation. Pergamon Press, Oxford

    Google Scholar 

  • Kobayashi RM, Brown M, Vale W (1977) Regional distribution of neurotensin and somatostatin in rat brain. Brain Res 126:584–588

    Google Scholar 

  • Krisch B (1977) Morphological equivalent of the bifunctional role of somatostatin. Cell Tissue Res 179:211–224

    Google Scholar 

  • Krisch B (1978) Hypothalamic and extrahypothalamic distribution of somatostatin-immunoreactive elements in the rat brain. Cell Tissue Res 195:499–513

    Google Scholar 

  • Lauber M, Camier M, Cohen P (1979) Immunocytochemical and biochemical characterisation of distinct high molecular weight forms of neurophysin and somatostatin in mouse hypothalamus extracts. FEBS Lett 97:343–347

    Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall R (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Lyman CP, Willis JS, Malan A, Wang LCH (1982) Hibernation and torpor in mammals and birds. Academic Press, New York

    Google Scholar 

  • Muchlinski AE, Ho FJ, Chew P, Yamada T (1983) The concentrations of four neuropeptides in various brain areas of summer active and hibernating Spermophilus lateralis. Comp Biochem Physiol 74C: 185–189

    Google Scholar 

  • Nozaki M, Gorbman A (1983) Immunocytochemical localization of somatostatin and vasotocin in the brain of the Pacific hagfish, Eptatretus stouti. Cell Tissue Res 229:541–550

    Google Scholar 

  • Oertel WH, Graybiel AM, Mugnaini E, Elde RP, Schmechel DE, Kopin IJ (1983) Coexistence of glutamic acid decarboxylase- and somatostatin like immunoreactivity in neurons of the feline nucleus reticularis thalami. J Neurosci 3:1322–1332

    Google Scholar 

  • Parsons JA, Erlandsen SL, Hegre OD, McEvoy RC, Elde RP (1976) Central and peripheral localization of somatostatin: Immunoenzyme immunocytochemical studies. J Histochem Cytochem 24:872–882

    Google Scholar 

  • Patel Y, Wheatley T, Ning C (1981) Multiple forms of immunoreactive somatostatin: comparison of distribution in neural and nonneural tissues and portal plasma of the rat. Endocrinology 108:1943–1949

    Google Scholar 

  • Pinatel MC, Duirand N, Girod C (1970) Etude des variations de l'iodénie et de l'iode thyroïdien au cours du cycle annuel chez le Hérisson, Erinaceus europaeus L.; comparaison avec l'histologie thyroidïenne. CR Seances Soc Biol Ses Fil 164:1719–1722

    Google Scholar 

  • Renaud LP, Martin JB, Brazeau P (1975) Depressant action of TRH, LH-RH and somatostatin on activity of central neurons. Nature 255:233–235

    Google Scholar 

  • Renaud LP, Martin JB, Brazeau P (1976) Hypothalamic releasing factors: Physiological evidence for a regulatory action on central neurons and pathways for their distribution in brain. Pharmacol Biochem Behav 5, Suppl 1:171 ff

  • Richoux JP Dubois MP (1980) Neuronal systems immunologically related to the somatostatin system in the garden dormouse. Cell Tissue Res 209:455–472

    Google Scholar 

  • Rorstad OP (1983) Effects of different radioligands on the antigen binding specificity of somatostatin antisera. J Immunoassay 4:49–63

    Google Scholar 

  • Rorstad OP, Epelbaum J, Brazeau P, Martin JB (1979) Chromatographic and biological properties of immunoreactive somatostatin in hypothalamic and extrahypothalamic brain regions of the rat. Endocrinology 105:1083–1092

    Google Scholar 

  • Rorstad OP, Martin JB, Terry LC (1980) Somatostatin and the nervous system. In: Barker JL, Smith TG (eds) The role of peptides in neuronal function. Marcel Dekker, New York, pp 573–614

    Google Scholar 

  • Spiess J, Vale W (1980) Multiple forms of somatostatin-like activity in rat hypothalamus. Biochemistry 19:2861–2866

    Google Scholar 

  • Sternberger LA (1979) Immunocytochemistry. J Wiley, New York

    Google Scholar 

  • Suomalainen P, Nyholm P (1956) Neurosecretion in the hibernating hedgehog. In: Wingstrand KG (ed) Bertil Hanström zoological papers. Göteborg, pp 269–277

  • Tähti H, Soivio A (1977) Respiratory and circulatory differences between induced and spontaneous arousals in hibernating hedgehogs (Erinaceus europaeus L.). Ann Zool Fenn 14:197–202

    Google Scholar 

  • Trent PF, Weir GC (1981) Heterogeneity of somatostatin-like peptides in rat brain, pancreas and gastrointestinal tract. Endocrinology 108:2033–2038

    Google Scholar 

  • Vale W, Rivier J, Ling N, Brown M (1978) Biologic and immunologic activities and applications of somatostatin analogs. Metabolism 27 [Suppl] 27:1391–1402

    Google Scholar 

  • Vandesande F, Dierickx K (1980) Immunocytochemical localization of somatostatin-containing neurons in the brain of Rana temporaria. Cell Tissue Res 205:43–53

    Google Scholar 

Download references

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Nürnberger, F., Lederis, K. & Rorstad, O.P. Effects of hibernation on somatostatin-like immunoreactivity in the brain of the ground squirrel (Spermophilus richardsonii) and European hedgehog (Erinaceus europaeus). Cell Tissue Res. 243, 263–271 (1986). https://doi.org/10.1007/BF00251040

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