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A thyroid hormone-vasopressin interaction promotes survival and maturation of hippocampal neurons dissociated postnatally

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Abstract

Hippocampal cells dissociated from 5-day-old rat pups were grown in a suitable chemically defined basal medium, supplemented or not with 3,3′,5-triiodo-l-thyronine (T3), [Arg8]-vasopressin (AVP), or both, at different concentrations. Four days after plating, neuron-like cells began to degenerate drastically in the basal medium. Although AVP alone had no effect, T3, and to a greater extent T3 and AVP together, prevented their death. Moreover, T3, and AVP also acted synergically in promoting the maturation of surviving cells, especially AchE-positive neurons, either directly or through glial cells.

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References

  1. Rami, A., Rabié, A., and Patel, A. J. 1986. Thyroid hormone and development of the rat hippocampus: cell acquisition in the dentate gyrus. Neuroscience 19:1207–1216.

    PubMed  Google Scholar 

  2. Rami, A., Patel, A. J., and Rabié, A. 1986. Thyroid hormone and development of the rat hippocampus: morphological alterations in the granule and pyramidal cells. Neuroscience 19:1212–1226.

    Google Scholar 

  3. Rami, A., Rabié, A., and Clos, J. 1989. The time course of hippocampal cholinergic innervation in developing hypothyroid rat. A combined histochemical and biochemical study of acetylcholinesterase activity. Int. J. Devl. Neurosc. 7:301–308.

    Google Scholar 

  4. Boer, G. J., and Patel, A. J. 1983. Disorders of cell acquisition in the brain of rats deficient in vasopressin (Brattleboro mutant). Neurochem. Int. 5:463–469.

    Google Scholar 

  5. Boer, G. J. 1986. Vasopressin and the developing rat brain. Peptides 1:203–209.

    Google Scholar 

  6. Kaplan, M. S., and Hinds, J. W. 1977. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197:1092–1099.

    PubMed  Google Scholar 

  7. Swaab, D. F. 1980. Neuropeptides and brain development. A working hypothesis, pages 181–96, in Di Benedetta, C., Balázs, R., Gombos, G., and Porcellatti, G. (eds), Multidisciplinary approach to brain development, Elsevier/North Holland Biomedical Press.

  8. Brinton, R. E., and Gruener, R. 1987. Vasopressin promotes neurite growth in cultured embryonic neurons. Synapse 1:329–334.

    PubMed  Google Scholar 

  9. Rami, A., Barberis, C., and Clos, J. 1989. Effects of hypothyroidism on high-affinity vasopressin binding sites in developing hippocampal synaptosomes. Synapse 3:200–204.

    PubMed  Google Scholar 

  10. Boss, B. D., Peterson, G. M., and Cowan, W. M. 1985. On the number of neurons in the dentate gyrus of the rat. Brain Res. 338:144–155.

    PubMed  Google Scholar 

  11. Rabié, A., Patel, A. J., Clavel, M. C., and Legrand, J. 1979. Effect of thyroid deficiency on the hippocampus in the rat. A combined biochemical and morphological study. Dev. Neurosc. 2:183–194.

    Google Scholar 

  12. Boss, B. D., Gozes, I., and Cowan, W. M. 1987. The survival of dentate gyrus neurons in dissociated culture. Dev. Brain Res. 36:199–228.

    Google Scholar 

  13. Bostwick, J. R., Appel, S. H., and Perez-Polo, J. R. 1987. Distinct influences of nerve growth factor and a central cholinergic trophic factor on medial septal explants. Brain Res. 422:92–98.

    PubMed  Google Scholar 

  14. Hayashi, M., and Patel, A. J., 1987. An interaction between thyroid hormone and nerve growth factor in the regulation of choline acetyltransferase activity in neuronal cultures, derived from the septal-diagonal band region of the embryonic rat brain. Dev. Brain Res. 36:109–120.

    Google Scholar 

  15. Hefti, F., Hartikka, J., Eckeinstein, F., Gnhan, H., Heumann, R., and Schwaab, M. 1985. Nerve growth factor increases choline acetyltransferase but not survival or fiber outgrowth of cultured fetal septal cholinergic neurons. Neuroscience 14:55–68.

    PubMed  Google Scholar 

  16. Puymirat, J., Barbet, A., Picart, R., Vigny, A., Loudes, C., Faivre-Bauman, A., and Tixier-Vidal, A., 1983. Triiodothyronine enhances the morphological maturation of dopaminergic neurons from fetal mouse hypothalamus cultured in serum-free medium. Neuroscience 10:801–810.

    PubMed  Google Scholar 

  17. Bottenstein, J. E., and Sato, G. H. 1970. Growth of the rat neuroblastoma cell line in serum free supplemented medium. Proc. Ntl. Acad. Sci. USA 76:514–517.

    Google Scholar 

  18. Faivre-Bauman, A., Puymirat, C., Loudes, C., and Tixier-Vidal, A. 1984. Differentiated mouse fetal hypothalamic cells in serumfree medium. Methods for Serum-Free Culture of Neuronal and Lymphoid Cells. Alan A. Riss, INC, New York.

    Google Scholar 

  19. Reggio, H., Webster, P., and Louvard, D. 1983. Use of immunocytochemical techniques in studying the biogenesis of cell surface in polarized opithelia. Meth. Enzym. 98:379–395.

    PubMed  Google Scholar 

  20. Gabe, M. 1968. Techniques histologiques, p. 621, Masson, Paris.

    Google Scholar 

  21. Ellman, G., Courtney, K. D., Andres, V. Jr., and Featherstone, R. A. 1961. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 7:88–95.

    PubMed  Google Scholar 

  22. Balázs, R., Kovács, S., Teichgrāber, P., Cocks, W. A., and Eayrs, J. T. 1971. Effect of thyroid hormone on the biochemical maturation of rat brain: postnatal cell formation. Brain Res. 25:555–570.

    PubMed  Google Scholar 

  23. Burton, K. 1956. A study of the conditions and mechanisms of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acids. Biochem. J. 62:315–323.

    PubMed  Google Scholar 

  24. Matthews, D. A., Nadler, J. V., Lynch, G. S., and Cotman, C. W. 1974. Development of cholinergic innervation in the hippocampal formation of the rat. I. Histochemical demonstration of acetylcholinesterase activity. Dev. Biol. 36:130–141.

    PubMed  Google Scholar 

  25. Matthews, D. A., Salvaterra, P. M., Crawford, G. D., Houser, C. R., and Vaughn, J. E. 1987. An immunocytochemical study of choline acetyltransferase-containing neurons and axon terminals in normal and partially deafferented hippocampal formation. Brain Res. 402:30–43.

    PubMed  Google Scholar 

  26. Andrä, J., Lachman, I., and Luppa, H. 1988. A comparison of the localization of acetylcholinesterase in the rat brain as demonstrated by enzyme histochemistry and immunocytochemistry. Histochemistry 88:595–601.

    PubMed  Google Scholar 

  27. Mellgren, S. I. 1973. Distribution of acetylcholinesterase in the hippocampal region of the rat during postnatal development. Z. Zellforsch 141:375–400.

    PubMed  Google Scholar 

  28. Schegg, K. M., Futamachi, K. J., and Peacock, J. H. 1986. Characterization of acetylcholinesterase isoforms in septal and hippocampal cultures and cocultures. Dev. Brain Res. 30:221–230.

    Google Scholar 

  29. Massoulié, J., and Bon, S. 1982. The molecular forms of cholinesterase and acetylcholinesterase in Vertebrates. Ann. Rev. Neurosc. 5:57–106.

    Google Scholar 

  30. Massoulié, J., Bon, S., Lazar, M., Grassi, J., Marsh, D., Meflah, K., Toutant, J. T., Valette, F., and Vigny, M. 1984. The polymorphisme of cholinesterases: classification of molecular forms; interactions and solubilization characteristics; metabolism relationship and regulation, Pages 289–303, in Brzin, M., Barnard, E. A., and Sketr, D. (eds), Cholinesterases. Fundamental and applied aspects, Walter de Gryter, Berlin, New York.

    Google Scholar 

  31. Walsh-Reitz, M., and Toback, G. 1983. Vasopressin stimulates growth of renal epithelial cells in culture. Ame. J. Physiol. 245:C365–370.

    Google Scholar 

  32. Rozengurt, E., Legg, A., and Pettican, P. 1979. Vasopressin stimulation of mouse 3T3 cell growth. Proc. Natl. Acad. Sci. USA. 76:1284–1287.

    PubMed  Google Scholar 

  33. Hatanaka, H., Tsukui, H., and Nihonmatsu, I. 1988. Developmental change in the nerve growth factor action from induction of choline acetyltransferase to promotion of cell survival in cultured basal forebrain cholinergic neurons from postnatal rats. Develop. Brain Res. 39:85–95.

    Google Scholar 

  34. Rami, A., Bréhier, A., Thomasset, M., and Rabié, A. 1987. Cholecalcin in the rat hippocampus. Development in normal animals and altered thyroid states. An immuno-cytochemical study. Develop. Biol. 124:228–238.

    PubMed  Google Scholar 

  35. Banker, G. A. 1980. Tropic interaction between astroglia cells and hippocampal neurons in culture. Sciences 209:809–810.

    Google Scholar 

  36. Hatanaka, H., and Tsukui, H. 1986. Differential effects of nerve growth factor and glioma-conditioned medium on neurons cultured from various regions of fetal rat central nervous system. Dev. Brain Res. 30:47–56.

    Google Scholar 

  37. Yusta, B., Besnard, F., Ortiz-Caro, J., Pascual, A., Aranda, A., and Sarlieve, L. 1988. Evidence for the presence of nuclear 3,5,3′-triiodothyronine receptors in secondary cultures of pure rat oligodendrocytes. Endocrinology 122:2278–2284.

    PubMed  Google Scholar 

  38. Oppenheimer, J. H. 1985. Thyroid hormone action at the nuclear level. Ann. Internal. Med. 102:374–384.

    Google Scholar 

  39. Thompson, C. C., Weinberger, C., and Evans, R. M. 1987. Identification of a novel thyroid hormone receptor expressed in the mammalian central nervous system. Science 237:1610–1614.

    PubMed  Google Scholar 

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Special issue dedicated to Dr. Paola S. Timiras

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Clos, J., Gabrion, J. A thyroid hormone-vasopressin interaction promotes survival and maturation of hippocampal neurons dissociated postnatally. Neurochem Res 14, 919–925 (1989). https://doi.org/10.1007/BF00965924

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