Opioid receptor and peptide mRNA expression in proliferative zones of fetal rat central nervous system

Canadian Journal of Physiology and Pharmacology

Volumn 76, Issue 3, 1998, Pages 284-293

  Leslie, Frances M ^a   Chen, Yiling ^a   Winzer Serhan, Ursula H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dynorphin; Enkephalin; Neurogenesis; Ontogeny

Indexed keywords

DYNORPHIN; KAPPA OPIATE RECEPTOR; MESSENGER RNA; OPIATE RECEPTOR; PRODYNORPHIN; PROENKEPHALIN;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL PROLIFERATION; CHOROID PLEXUS; CONTROLLED STUDY; FETUS; FOREBRAIN; IN SITU HYBRIDIZATION; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD;

EID: 0031819494     PISSN: 00084212     EISSN: None     Source Type: Journal    
DOI: 10.1139/y98-028     Document Type: Article

References (64)

1. Altman, J., and Bayer, S.A. 1984. The development of the rat spinal cord. Adv. Anat. Embryol. Cell Biol. 85: 1-164.
2. Altman, J., and Bayer, S.A. 1995. Atlas of prenatal rat brain development. CRC Press, Boca Raton, Fla.
3. Barg, J., Belcheva, M.M., and Coscia, C.J. 1992. Evidence for the implication of phosphoinositol signal transduction in mu-opioid inhibition of DNA synthesis. J. Neurochem. 59: 1145-1152.
4. Barg, J., Belcheva, M., McHale, R., Levy, R., Vogel, Z., and Coscia, C.J. 1993a. Beta-endorphin is a potent inhibitor of thymidine incorporation into DNA via mu- and kappa-opioid receptors in fetal rat brain cell aggregates in culture. J. Neurochem. 60: 765-767.
5. 3H]thymidine incorporation into DNA: evidence for the involvement of pertussis toxin-sensitive G protein-coupled phosphoinositide turnover. J. Neurochem. 60: 1505-1511.
6. Barg, J., Nah, S.Y., Levy, R., Saya, D., and Vogel, Z. 1993c. Modulation of thymidine incorporation by kappa-opioid ligands in rat spinal cord - dorsal root ganglion co-cultures. Brain Res. 629: 109-114.
7. Batter, D.K., Vilijn, M.H., and Kessler, J. 1991. Cultured astrocytes release proenkephalin. Brain Res. 563: 28-32.
8. Bayer, S.A., and Altman, J. 1995a. Neurogenesis and neuronal migration. In The rat nervous system. Edited by G.W. Paxinos. Academic Press, San Diego, Calif. pp. 1041-1078.
9. Bayer, S.A., and Altman, J. 1995b. Principles of neurogenesis, neuronal migration, and neural circuit formation. In The rat nervous system. Edited by G.W. Paxinos. Academic Press, San Diego, Calif. pp. 1079-1098.
10. 125I-β-endorphin cross-linked products in subcellular fractions from NG108-15 cells. Biochemistry, 35: 14818-14824.
11. Böttger, A., and Spruce, B.A. 1995. Proenkephalin is a nuclear protein responsive to growth arrest and differentiation signals. J. Cell Biol. 130: 1251-1262.
12. Brooks, P.J., Funabashi, T., Kleopoulos, S.P., Mobbs, C.V., and Pfaff, D.W. 1993. Cell-specific expression of preproenkephalin intronic heteronuclear RNA in the rat forebrain. Brain Res. Mol. Brain Res. 19: 22-30.
13. Chao, C.C., Hu, S., Shark, K.B., Sheng, W.S., Gekker, G., and Peterson, P.K. 1997. Activation of mu opioid receptors inhibits microglial cell chemotaxis. J. Pharmacol. Exp. Ther. 281: 998-1004.
14. Cox, K.H., DeLeon, D.V., Angerer, L.M., and Angerer, R.C. 1984. Detection of mRNAs in sea urchin embryos by in situ hybridization using asymmetric RNA probes. Dev. Biol. 101: 485-502.
15. Elkabes, S., Loh, Y.P., Nieburgs, A., and Wray, P. 1989. Prenatal ontogenesis of proopiomelanocortin in the mouse central nervous system and pituitary gland: an in situ hybridization and immunocytochemical study. Brain Res. Dev. Brain Res. 46: 85-95.
16. Gorodinsky, A., Barg, J., Belcheva, M.M., Levy, R., McHale, R.J., Vogel, Z., and Coscia, C.J. 1995. Dynorphins modulate DNA synthesis in fetal brain cell aggregates. J. Neurochem. 65: 1481-1486.
17. 2+ mobilization, development, and the antiproliferative effect of opioids. Brain Res. 737: 175-187.
18. Hammer, R.P., Jr. 1993. Effects of opioids on the developing brain. In The neurobiology of opiates. Edited by R.P. Hammer, Jr. CRC Press, Boca Raton, Fla. pp. 1-21.
19. Harlan, R.E., and Song, D.D. 1994. Prenatal morphine treatment and the development of striatum. Regul. Pept. 54: 117-118.
20. Hauser, K.F., and Stiene-Martin, A. 1993. Opiates and the regulation of nervous system development. In The neurobiology of opiates. Edited by R.P. Hammer, Jr. CRC Press, Boca Raton, Fla. pp. 23-61.
21. Hauser, K.F., Osborne, J.G., Stiene-Martin, A., and Melner, M.H. 1990. Cellular localization of proenkephalin mRNA and enkephalin peptide products in cultured astrocytes. Brain Res. 522: 347-353.
22. 2+-dependent mechanism. Brain Res. 720: 191-203.
23. Höllt, V. 1986. Opioid peptide processing and receptor selectivity. Annu. Rev. Pharmacol. Toxicol. 26: 59-77.
24. Hughes, J., Smith, T.W., Kosterlitz, H.W., Fothergill, L.A., Morgan, B.A., and Morris, H.R. 1975. Identification of two related pentapeptides from the brain with potent opiate agonist activity. Nature (London), 258: 577-580.
25. Hurlbut, D.E., Evans, C.J., Barchas, J.D., and Leslie, F.M. 1987. Pharmacological properties of a proenkephalin A-derived opioid peptide: BAM 18. Eur. J. Pharmacol. 138: 359-366.
26. Isayama, T., McLaughlin, P.J., and Zagon, I.S. 1991. Endogenous opioids regulate cell proliferation in the retina of developing rat. Brain Res. 544: 79-85.
27. Isayama, T., McLaughlin, P.J., and Zagon, I.S. 1996. Ontogeny of preproenkephalin mRNA expression in the rat retina. Visual Neurosci. 13: 695-704.
28. Kent, J.L., Pert, C.B., and Herkenham, M. 1981. Ontogeny of opiate receptors in rat forebrain: visualization by in vitro autoradiography. Brain Res. 254: 487-504.
29. Keshet, E., Polakiewicz, R.D., Itin, A., Ornoy, A., and Rosen, H. 1989. Proenkephalin A is expressed in mesodermal lineages during organogenesis. EMBO J. 8: 2917-2923.
30. Kew, D., and Kilpatrick, D.L. 1990. Widespread organ expression of the rat proenkephalin gene during early postnatal development. Mol. Endocrinol. 4: 337-340.
31. Khachaturian, H., Alessi, N.E., Munfakh, N., and Watson S.J. 1983. Ontogeny of opioid and related peptides in the rat CNS and pituitary: an immunocytochemical study. Life Sci. 33(Suppl. I): 61-64.
32. Law, P.Y., and Bergsbaken, C. 1995. Properties of delta opioid receptor in neuroblastoma NS20Y: receptor activation and neuroblastoma proliferation. J. Pharmacol. Exp. Ther. 272: 322-332.
33. Law, P.Y., McGinn, T.M., Campbell, K.M., Erickson, L.E., and Loh, H.H. 1997. Agonist activation of δ-opioid receptor but not μ-opioid receptor potentiates fetal calf serum or tyrosine kinase receptor-mediated cell proliferation in a cell-line-specific manner. Mol. Pharmacol. 51: 152-160.
34. Leslie, F.M., and Loughlin, S.E. 1993. Ontogeny and plasticity of opioid systems. In The neurobiology of opiates. Edited by R.P. Hammer, Jr. CRC Press, Boca Raton, Fla. pp. 85-123.
35. Linner, K.M., Quist, H.E., and Sharp, B.M. 1995. Met-enkephalin-containing peptides encoded by proenkephalin A mRNA expressed in activated murine thymocytes inhibit thymocyte proliferation. J. Immunol. 154: 5049-5060.
36. Loughlin, S.E., Kornblum, H.I., Massamiri, T., and Leslie F.M. 1991. Transient appearance of beta-endorphin immunoreactive cells within the germinal zone of neonatal rat forebrain. Int. J. Dev. Neurosci. 9: 493-500.
37. Lugo, D.I., and Pintar, J.E. 1996. Ontogeny of basal and regulated secretion from POMC cells of the developing anterior lobe of the rat pituitary gland. Dev. Biol. 173: 95-109.
38. Mansour, A., Fox, C.A., Burke, S., Meng, F., Thompson, R.C., Akil, H., and Watson, S.J. 1994. Mu, delta, and kappa opioid receptor mRNA expression in the rat CNS: an in situ hybridization study. J. Comp. Neurol. 350: 412-438.
39. 5]enkephalin. Am. J. Physiol. 271: R122-R129.
40. Melner, M.H., Low, K.G., Allen, R.G., Nielsen, C.P., Young, S.L., and Saneto, R.P. 1990. The regulation of proenkephalin expression in a distinct population of glial cells. EMBO J. 9: 791-796.
41. Ohkawa, T., Rohde, W., Takeshita, S., Dorner, G., Arai, K., and Okinaga, S. 1991. Effect of an acute maternal stress on the fetal hypothalamo-pituitary-adrenal system in late gestational life of the rat. Exp. Clin. Endocrinol. 98: 123-129.
42. Osborne, J.G., Kindy, M.S., Spruce, B.A., and Hauser, K.F. 1993. Ontogeny of proenkephalin mRNA and enkephalin peptide expression in the cerebellar cortex of the rat: spatial and temporal patterns of expression follow maturational gradients in the external granular layer and in Purkinje cells. Dev. Brain Res. 76: 1-12.
43. Paxinos, G., Törk, I., Tecott, L.H., and Valentino, K.L. 1991. Atlas of the developing rat brain. Academic Press, San Diego, Calif.
44. Rodriguez Vida, M.I., Kleid, M.C., Ase, A., Finkielman, S., Nahmod, V.E., and Vindrola, O. 1994. Synenkephalin processing in embryonic rat brain. Dev. Brain Res. 77: 151-156.
45. Rosen, H., and Bar-Shavit, Z. 1994. Dual role of osteoblastic proenkephalin derived peptides in skeletal tissues. J. Cell. Biochem. 55: 334-339.
46. Ruzicka, B.B., Fox, C.A., Thompson, R.C., Meng, F., Watson, S.J., and Akil, H. 1995. Primary astroglial cultures derived from several rat brain regions differentially express mu, delta and kappa opioid receptor mRNA. Mol. Brain Res. 34: 209-220.
47. Sandman, C.A., Barron, J.L., Demet, E.M., Chicz-Demet, A., Rothenberg, S.J., and Zea, F.J. 1990. Opioid peptides and perinatal development: is beta-endorphin a natural teratogen? Clinical implications. Ann. N.Y. Acad. Sci. 579: 91-108.
48. Schwartzberg, D.G., and Nakane, P.K. 1982. Ontogenesis of adrenocorticotropin-related peptide determinants in the hypothalamus and pituitary gland of the rat. Endocrinology, 110: 855-864.
49. Simmons, D.M., Arriza, J.L., and Swanson, L.W. 1989. A complete protocol for in situ hybridization of messenger RNAs in brain and other tissues with radiolabeled single-stranded RNA probes. J. Histotechnol. 12: 169-181.
50. Song, D.D., and Harlan, R.E. 1993. Ontogeny of the proenkephalin system in the rat corpus striatum: its relationship to dopaminergic innervation and transient compartmental expression. Neuroscience, 52: 883-909.
51. Spruce, B.A., Curtis, R., Wilkin, G.P., and Glover, D.M. 1990. A neuropeptide precursor in cerebellum: proenkephalin exists in subpopulations of both neurons and astrocytes. EMBO J. 9: 1787-1795.
52. Stiene-Martin, A., and Hauser, K.F. 1990. Opioid-dependent growth of glial cultures: suppression of astrocyte DNA synthesis by Metenkephalin. Life Sci. 46: 91-98.
53. Tecott, L.H., Rubenstein, J.L., Paxinos, G., Evans, C.J., Eberwine, J.H., and Valentino, K.L. 1989. Developmental expression of proenkephalin mRNA and peptides in rat striatum. Dev. Brain Res. 49: 75-86.
54. Vertes, Z., Kornyei, J.L., Kovacs, S., and Vertes, M. 1996. Opioids regulate cell proliferation in the developing rat uterus: effects during the period of sexual maturation. J. Steroid Biochem. Mol. Biol. 59: 173-178.
55. Villiger, P.M., and Lotz, M. 1992. Expression of prepro-enkephalin in human articular chondrocytes is linked to cell proliferation. EMBO J. 11: 135-143.
56. Weisinger, G., Zinder, O., and Simantov, R. 1995. Antisense knockout of a neuropeptide gene reduces fibroblast proliferation. Biochem. Biophys. Res. Commun. 214: 530-537.
57. 2B Adrenoceptor mRNA expression during rat brain development. Dev. Brain Res. 100:90-100.
58. Winzer-Serhan, U.H., and Leslie, F.M. 1997b. Codistribution of nicotinic acetylcholine receptor subunit α3 and β4 mRNAs during rat brain development. J. Comp. Neurol. 386: 540-554.
59. Zagon, I.S., and McLaughlin, P.J. 1987. Endogenous opioid systems regulate cell proliferation in the developing rat brain. Brain Res. 412: 68-72.
60. Zagon, I.S., and McLaughlin, P.J. 1991. Identification of opioid peptides regulating proliferation of neurons and glia in the developing nervous system. Brain Res. 542: 318-323.
61. Zagon, I.S., Rhodes, R.E., and McLaughlin, P.J. 1985. Distribution of enkephalin immunoreactivity in germinative cells of developing rat cerebellum. Science (Washington, D.C.), 227: 1049-1051.
62. Zagon, I.S., Goodman, S.R., and McLaughlin, P.J. 1989. Characterization of zeta (ξ): a new opioid receptor involved in growth. Brain Res. 482: 297-305.
63. Zagon, I.S., Isayama, T., and McLaughlin, P.J. 1994. Preproenkephalin mRNA expression in the developing and adult rat brain. Mol. Brain Res. 21: 85-98.
64. Zagon, I.S., Sassani, J.W., and McLaughlin, P.J. 1995. Opioid growth factor modulates corneal epithelial outgrowth in tissue culture. Am. J. Physiol. 268: R942-R950.