Summary
The distribution of enkephalin, an endogenous opioid, in tissues and cells of the developing and adult rat was determined by immunocytochemistry with antibodies to met- and leu-enkephalin. Met- and leu-enkephalin were found in all developing cells investigated, with staining generally located throughout the cytoplasm; cell nuclei were not immunoreactive. In comparison to developing cells, immunoreactive analogues to met-enkephalin were usually difficult to detect in the adult. Some notable exceptions were reaction products in leukocytes in blood, lung, and cortex of thymus, fibroblasts in the skin, and seminiferous tubules. These results, in concert with earlier reports that opioid receptors are found largely in developing, but not adult, tissues, indicate that endogenous opioids are specifically involved in biological development, particularly cell proliferation and differentiation. Immunoreactivity in adult nonneural cells may be related to their development in some cases, but also could indicate other functions.
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References
Akil H, Watson WJ, Young E, Lewis ME, Khachaturian H., Walker JM (1984) Endogenous opioids: biology and function. Ann Rev Neurosci 7:223–255
Ausiello CN, Roda, LG (1984) Leu-enkephalin binding to cultured T lymphocytes. Cell Biol Int Rep 8:97–106
Bayon A, Shoemaker WJ, Bloom FE, Mauss A, Guillemin R (1979) Perinatal development of the endorphin- and enkephalin-containing systems in the rat brain. Brain Res 179:93–101
Beaumont A, Hughes J (1979) Biology of opioid peptides Ann Rev Pharmacol Toxicol 19:245–267
Clendeninn NJ, Petraitis M, Simon EJ (1976) Ontological development of opiate receptors in rodent brain. Brain Res 118:157–160
Coyle JT, Pert CB (1976) Ontogenetic development of opiate receptors in rodent brain. Brain Res 118:157–160
Csontos K, Rust M, Hollt V, Mahr W, Kromer W, Tcschemacher HJ (1979) Elevated plasma β-endorphin levels in pregnant women and their neonates. Life Sci 25:835–844
Cutz E, Chan W, Track NS (1981) Bombesin, calcitonin and leuenkephalin immunoreactivity in endocrine cells of human lung. Experientia 37:765–767
Gibson DA, Vernadakis A (1982) [3H]etorphine binding activity in early chick embryos: brain and body tissue. Dev Brain Res 4:23–29
Kent JL, Pert CB, Herkenham M (1982) Ontogeny of opiate receptors in rat forebrain; visualization by in vitro autoradiography. Dev Brain Res 2:487–504
Knodel EL, Richelson E (1980) Methionine-enkephalin immunoreactivity in fetal rat brain cells in aggregating culture and in mouse neuroblastoma cells. Brain Res 197:565–570
Krumins SA, Faden AI, Feuerstein G (1985) Opiate binding in rat hearts: modulation of binding after hemorrhagic shock. Biochem Biophys Res Comm 127:120–128
Lolait SJ, Lim ATW, Toh BH, Funder JW (1984) Immunoreactive β-endorphin in a subpopulation of mouse spleen macrophages. J Clin Invest 73:277–280
Lopker A, Abood LG, Hoss W, Lionetti FJ (1980) Stereoselective muscarinic acetylcholine and opiate receptors in human phagocytic leukocytes. Biochem Pharmacol 29:1361–1365
Marzullo G, Friedhoff AJ (1980) Opiate binding and cerebroside sulfates in brain and lung of developing chick. In: Way EL (ed) Endogenous and exogenous opiate agonists and antagonists. Pergamon, New York, pp 47–50
Maseda C, Aguado EG, Mena MA, De Yebenes JG (1983) Ontogenetic development of β-endorphin immunoreactivity in rat brain regions. Neurosci Lett [Suppl] 14:8237
McLaughlin PJ, Zagon IS (1984) Opioid regulation of neurotumor cell growth in vitro. Society for Neurosci 10:1111
Neale JH, Barker JL, Uhl GR, Snyder SH (1979) Enkephalincontaining neurons visualized in spinal cord cell cultures. Science 201:467–469
Neidle A, Manigault I, Wajda IJ (1979) Distribution of opiate-like substances in rat tissues. Neurochem Res 4:399–410
Shana C, Liotta AS, Krieger DT, Bardin CW (1984) The ontogeny of immunoreactive β-endorphin in fetal, neonatal, and pubertal testes from mouse and hamster. Endocrinology 114:1584–1591
Simon EJ (1971) Single cells. In: Clouet D (ed) Narcotic drugs; biochemical pharmacology. Plenum, New York, pp 310–341
Singer R, Bruchis S, Barnet M, Sagiv M, Kaufman H, Servadio C (1985) β-endorphin in normozoospermic and pathologic human semen. Experientia 41:64–65
Spain JW, Roth BL, Coscia CJ (1985) Differential ontogeny of multiple opioid receptors (μ, δ, and κ), J Neurosci 5:584–588
Tsang D, Ng SC, Ho KP, Ho WKK (1982) Ontogenesis of opiate binding sites and radioimmunoassayable β-endorphin and enkephalin in regions of rat brain. Dev Brain Res 5:257–261
Vertes Z, Melegh G, Vertes M, Kovacs S (1982) Effect of naloxone and D-met2-pro5-enkephalinamide treatment on DNA synthesis in the developing rat brain, Life Sci 31:119–126
Vethanany-Globus S, Globus M, Milton G (1984) β-endorphins (B-EP) in amphibians: higher B-EP levels during regenerating stages of anuran life cycle and immunocytochemical localization of B-EP in regeneration blastema. J Exp Zool 232:259–267
Winick M, Noble A (1965) Quantitative changes in DNA, RNA, and protein during prenatal and postnatal growth in the rat. Dev Biol 12:451–466
Wybran J, Appelboom T, Famaey JP, Govaerts A (1979) Suggestive evidence for receptors for morphine and methionine-enkephalin on normal human blood T lymphocytes. J Immunology 123:1068–1070
Zagon IS, McLaughlin PJ (1983a) Increased brain size and cellular content in infant rats treated with an opiate antagonist. Science 221:671–673
Zagon IS, McLaughlin PJ (1983a) Naltrexone modulates growth in infant rats. Life Sci 33:2449–2454
Zagon IS, McLaughlin PJ (1984a) Naltrexone modulates body and brain development in rats: a role for endogenous opioids in growth. Life Sci 35:2057–2064
Zagon, IS, McLaughlin PJ (1984b) Endogenous opioid systems and brain development. In: Caciaglia F, Giacobini E, Paoletti R (eds) Developmental neuroscience: physiological, pharmacological and clinical aspects. Elsevier, Amsterdam, pp 67–70
Zagon IS, McLaughlin PJ (1985a) Naltrexone's influence on neurobehavioral development. Pharmacol Biochem Behav 22:441–448
Zagon IS, McLaughlin PJ (1985b) Opioid antagonist-induced regulation of organ development. Physiol Behav 34:507–511
Zagon IS, McLaughlin PJ (1986a) Opioid antagonist (naltrexone) modulation of cerebellar development: histological and morphometric studies. J Neurosci 6:1424–1432
Zagon IS, McLaughlin PJ (1986b) Opioid antagonist-induced modulation of cerebral and hippocampal development: histological and morphometric studies. Dev Brain Res (in press)
Zagon IS, Rhodes RE, McLaughlin PJ (1985) Localization of enkephalin immunoreactivity in germinative cells of developing rat cerebellum. Science 227:1049–1051
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Zagon, I.S., Rhodes, R.E. & McLaughlin, P.J. Localization of enkephalin immunoreactivity in diverse tissues and cells of the developing and adult rat. Cell Tissue Res. 246, 561–565 (1986). https://doi.org/10.1007/BF00215197
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DOI: https://doi.org/10.1007/BF00215197