μ-Opioid receptor-induced Ca2+ mobilization and astroglial development: Morphine inhibits DNA synthesis and stimulates cellular hypertrophy through a Ca2+-dependent mechanism

Brain Research

Volumn 720, Issue 1-2, 1996, Pages 191-203

  Hauser, Kurt F ^a   Stiene Martin, Anne ^a   Mattson, Mark P ^a   Elde, Robert P ^b   Ryan, S Eric ^a   Godleske, Chrystal C ^a  

^a UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Cell division; Dantrolene; Endogenous opioid system; Fura 2; Intracellular calcium; Neural development; Nifedipine; Thapsigargin; Opioid receptor

Indexed keywords

ANTIMETABOLITE; BROXURIDINE; CALCIUM; DIAGNOSTIC AGENT; DNA; GLIAL FIBRILLARY ACIDIC PROTEIN; MORPHINE; MU OPIATE RECEPTOR; NARCOTIC AGENT; NUCLEIC ACID SYNTHESIS INHIBITOR; CALCIMYCIN; CALCIUM CHANNEL BLOCKING AGENT; DANTROLENE; FURA 2; GLUTAMIC ACID; MORPHICEPTIN[3 (N METHYLPHENYLALANINE) 4 DEXTRO PROLINAMIDE]; NIFEDIPINE; OPIATE AGONIST; THAPSIGARGIN;

ANIMAL; ARTICLE; ASTROCYTE; BIOSYNTHESIS; CELL CULTURE; CELL DIVISION; CELL SIZE; DRUG EFFECT; DRUG POTENTIATION; IMMUNOHISTOCHEMISTRY; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; MOUSE; PHYSIOLOGY; ULTRASTRUCTURE; ANIMAL CELL; CALCIUM TRANSPORT; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; IMMUNOCYTOCHEMISTRY; INTRACELLULAR RECORDING; NEWBORN; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTIMETABOLITES; ASTROCYTES; BROMODEOXYURIDINE; CALCIUM; CELL DIVISION; CELL SIZE; CELLS, CULTURED; DNA; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED ICR; MORPHINE; NARCOTICS; NUCLEIC ACID SYNTHESIS INHIBITORS; RECEPTORS, OPIOID, MU;

EID: 0029665311     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/0006-8993(96)00103-5     Document Type: Article

References (64)

1. Arvidsson, U., Riedl, M., Chakrabarti, S., Lee, J.-H., Nakano, A.H., Dado, R.J., Loh, H.H., Law. P.-Y., Wessendorf, M.W. and Elde, R., Distribution and targeting of a μ-opioid receptor (MOR1) in brain and spinal cord, J. Neurosci., 15 (1995) 3328-3341.
2. Barg, J., Belcheva, M.M. and Coscia, C.J., Evidence for the implication of phosphoinositol signal transduction in μ-opioid inhibition of DNA synthesis, J. Neurochem., 59 (1992) 1145-1152.
3. 3H]thymidine incorporation into DNA: Evidence for the involvement of pertussis toxin-sensitive G protein-coupled phosphoinositide turnover. J. Neurochem., 60 (1993) 1505-1511.
4. 2+ mobilization in rat C6 glioma cells, J. Neurosci., 14 (1994) 5858-5864.
5. Berridge, M.J., Inositol trisphosphate and calcium signalling. Nature, 361 (1993) 315-325.
6. Boersma, C.J.C., Van Leeuwen, F.W., O'Brien, W.G., Law, G.J., Mason, W.T. and Bicknell, R.J., Dynorphin 1-17 delays the vasopressin induced mobilization of intracellular calcium in cultured astrocytes from the rat neural lobe. J. Neuroendocrinol., 5 (1993) 583-590.
7. Cameron, R.S. and Rakic, P., Glial cell lineage in the cerebral cortex: a review and synthesis, Glia, 4 (1991) 124-137.
8. Charles, A.C., Dirksen, E.R., Merrill, J.E. and Sanderson, M.J., Mechanisms of intercellular calcium signaling in glial cells studied with dantrolene and thapsigargin, Glia, 7 (1993) 134-145.
9. Cheng, B., McMahon, D.G. and Mattson, M.P., Modulation of calcium current, intracellular calcium levels and cell survival by glucose deprivation and growth factors in hippocampal neurons, Brain Res., 607 (1993) 275-285.
10. Cornell-Bell, A.M., Finkbeiner, S.M., Cooper, M.S. and Smith, S.J., Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling, Science, 247 (1990) 470-473.
11. Crain, S.M. and Shen, K.F., Opioids can evoke direct receptor-mediated excitatory effects on sensory neurons, Trends. Pharmacol. Sci., 11 (1990) 77-81.
12. Duggan, A.W. and North, R.A., Electrophysiology of opioids, Pharmacol Rev., 35 (1984) 219-281.
13. 1) receptor adenylate cyclase, Neuropharmacology, 30 (1991) 1233-1239.
14. Eriksson, P.S., Hansson, E. and Rönnbäck, L., δ- and Κ-opiate receptors in primary astroglial cultures. Part II: Receptor sets in cultures from various brain regions and interactions with β-receptor activated cyclic AMP, Neurochem. Res., 17 (1992) 545-551.
15. 2+ channels. Neuroscience, 54 (1993) 401-407.
16. 2+ influx: how many mechanisms for how many channels?, Trends Pharmacol. Sci., 15 (1994) 77-83.
17. Finch, E.A., Turner, T.J. and Goldin, S.M., Calcium as a coagonist of inositol 1,4,5-trisphosphate-inducd calcium release, Science, 252 (1991) 443-446.
18. Finkbeiner, S.M., Glial calcium, Glia, 9 (1993) 83-104.
19. Gosztonyi, G., Schmidt, V., Nickel, R., Rothschild, M.A., Camacho, S., Siegel, G., Zill, E., Pauli, G. and Schneider, V., Neuropathologic analysis of postmortal brain samples of HIV-seropositive and -seronegative i.v. drug addicts. Forensic Sci. Int., 62 (1993) 101-105.
20. Grynkiewicz, G., Poenie, M. and Tsien, R.Y., A new generation of calcium indicators with greatly improved fluorescence properties, J. Biol. Chem., 260 (1985) 3440-3450.
21. Gurwell, J.A., Duncan, M.J. and Hauser, K.F., Role of K-opioid receptors in type 1 astrocyte growth, Soc. Neurosci. Abstr., 19 (1993) 672.
22. Hauser, K.F., Osborne, J.G., Stiene-Martin, A. and Melner, M.H., Cellular localization of proenkephalin mRNA and enkephalin peptide products in cultured astrocytes, Brain Res., 522 (1990) 347-353.
23. Hauser, K.F. and Stiene-Martin, A., Characterization of opioid-dependent glial development in dissociated and organotypic cultures of mouse central nervous system: Critical periods and target specificity, Dev. Brain Res., 62 (1991) 245-255.
24. Hauser, K.F. and Stiene-Martin, A., Opiates and the regulation of nervous system development: Evidence from in vitro studies. In R.P. Hammer, Jr. (Ed.) Neurobiology of Opiates, CRC Press, Boca Raton, Florida, 1993, pp. 23-61.
25. Jin, W., Lee, N.M., Loh, H.H. and Thayer, S.A., Opioid-induced inhibition of voltage-gated calcium channels parallels expression of omega-conotoxin-sensitive channel subtype during differentiation of NG108-15 cells, Brain Res., 607 (1993) 17-22.
26. Jin, W., Lee, N.M., Loh, H.H. and Thayer, S.A., Opioids mobilize calcium from inositol 1,4,5-trisphosphate-sensitive stores in NG108-15 cells, J. Neurosci., 14 (1994) 1920-1929.
27. Johnson, S.M. and Fleming, W.W., Mechanisms of cellular adaptive sensitivity changes: applications to opioid tolerance and dependence, Pharmacol Rev., 41 (1989) 435-487.
28. 2+-mobilizing opioid receptors in Xenopus oocytes injected with rat brain mRNA, Mol. Brain Res., 22 (1994) 69-75.
29. Kater, S.B., Mattson, M.P., Cohan, C. and Connor, J., Calcium regulation of the neuronal growth cone, Trends. Neurosci., 11 (1988) 315-321.
30. Kim, W.T., Rioult, M.G. and Cornell-Bell, A.H., Glutamate-induced calcium signaling in astrocytes, Glia, 11 (1994) 173-184.
31. Maderspach, K. and Solomonia, R., Glial and neuronal opioid receptors: apparent positive cooperativity observed in intact cultured cells, Brain Res., 441 (1988) 41-47.
32. Mangoura, D., Sogos, V., Pelletiere, C. and Dawson, G., Differential regulation of phospholipase C and D by phorbol esters and the physiological activators carbachol and glutamate in astrocytes from chicken embryo cerebrum and cerebellum, Dev. Brain Res., 87 (1995) 12-21.
33. Mattson, M.P., Calcium as sculptor and destroyer of neural circuitry, Exp. Gerontol., 27 (1992) 29-49.
34. Mattson, M.P. and Barger, S.W., Roles for calcium signaling in structural plasticity and pathology in the hippocampal system, Hippocampus, 3 (1993) 73-87.
35. Means, A.R. and Rasmussen, C.D., Calcium, calmodulin and cell proliferation, Cell Calcium, 9 (1988) 313-319.
36. Melner, M.H., Low, K.G., Allen, R.G., Nielson, C.P., Young, S.L. and Saneto, R.P., The regulation of proenkephalin expression in a distinct population of glial cells. EMBO J., 9 (1990) 791-796.
37. Millan, M.J., Kappa-opioid receptors and analgesia, Trends. Pharmacol. Sci., 11 (1990) 70-76.
38. Nicoletti, F., Magrì, G., Ingrao, F., Bruno, V., Catania, M.V., Dell'Albani, P., Condorelli, D.F. and Avola, R., Excitatory amino acids stimulate inositol phospholipid hydrolysis and reduce proliferation in cultured astrocytes, J. Neurochem., 54 (1990) 771-777.
39. 2+ release from sarcoplasmic reticulum in guinea pig skeletal muscle, Eur. J. Pharmacol, 178 (1990) 11-19.
40. a subunit and is similar to that of other opioid receptors, Mol. Brain Res., 29 (1995) 336-346.
41. Reddy, G.P., Cell cycle: regulatory events in G1 → S transition of mammalian cells, J. Cell Biochem., 54 (1994) 379-386.
42. 2+ homeostasis, cell death, proliferation, and differentiation, Chem. Biol. Interact., 77 (1991) 1-23.
43. Ruzicka, B.B., Fox, C.A., Thompson, R.C., Akil, H. and Watson, S.J., Opioid receptor mRNA expression in primary cultures of glial cells derived from different rat brain regions, Reg. Peptides, 54 (1994) 251-252.
44. Ruzicka, B.B., Thompson, R.C., Watson, S.J. and Akil, H., The regulation of astroglial proenkephalin and opioid receptor mRNA expression by interleukin-1β, Soc. Neurosci. Abstr., 21 (1995) 1358.
45. Schmahl, W., Funk, R., Miaskowski, U. and Plendl, J., Long-lasting effects of naltrexone, an opioid receptor antagonist, on cell proliferation in developing rat forebrain, Brain Res., 486 (1989) 297-300.
46. Schwartz, J.P., Nishiyama, N., Wilson, D. and Taniwaki, T., Receptor-mediated regulation of neuropeptide gene expression in astrocytes, Glia, 11 (1994) 185-190.
47. Shao, Y. and McCarthy, K.D., Regulation of astroglial responsiveness to neuroligands in primary culture, Neuroscience, 55 (1993) 991-1001.
48. Shao, Y. and McCarthy, K.D., Plasticity of astrocytes, Glia, 11 (1994) 147-155.
49. Shinoda, H., Marini, A.M., Cosi, C. and Schwartz, J.P., Brain region and gene specificity of neuropeptides gene expression in cultured astrocytes, Science, 245 (1989) 415-417.
50. Shinoda, H., Marini, A.M. and Schwartz, J.P., Developmental expression of the proenkephalin and prosomatostatin genes in cultured cortical and cerebellar astrocytes, Dev. Brain Res., 67 (1992) 205-210.
51. Slotkin, T., Perinatal exposure to methadone: how do early biochemical alterations cause neurofunctional disturbances? Prog. Brain Res., 73 (1988) 265-279.
52. Sontheimer, H., Voltage-dependent ion channels in glial cells, Glia, 11 (1994) 156-172.
53. Spruce, B.A., Curtis, R., Wilkin, G.P. and Glover, D.M., A neuropeptide precursor in cerebellum: Proenkephalin exists in subpopulations of both neurons and astrocytes, EMBO J., 9 (1990) 1787-1795.
54. Stiene-Martin, A., Elde, R.P. and Hauser, K.F., Regional and temporal differences in μ, δ-, and Κ-opioid receptor expression by murine type 1 astrocytes from the cerebral cortex, hippocampus, cerebellum, and striatum in vitro, Soc. Neurosci. Abstr., 21 (1995) 1360.
55. Stiene-Martin, A., Gurwell, J.A. and Hauser, K.F., Morphine alters astrocyte growth in primary cultures of mouse glial cells: Evidence for a direct effect of opiates on neural maturation, Dev. Brain Res., 60 (1991) 1-7.
56. Stiene-Martin, A. and Hauser, K.F., Opioid-dependent growth of glial cultures: Suppression of astrocyte DNA synthesis by Met-enkephalin, Life Sci., 46 (1990) 91-98.
57. Stiene-Martin, A., Mattson, M.P. and Hauser, K.F., Opiates selectively increase intracellular calcium in developing type 1 astrocytes: Role of calcium in morphine-dependent morphologic differentiation, Dev. Brain Res., 76 (1993) 189-196.
58. αi2 protein a-subunit sequence inhibits an opioid-induced increase in intracellular free calcium in ND8-47 neuroblastoma × DRG hybrid cells, FASEB J., 9 (1995) A97.
59. 2+-ATPase, Proc. Natl. Acad. Sci. USA, 87 (1990) 2466-2470.
60. Thorlin, T., Eriksson, P.S., Nilsson, M., Hansson, E. and Rönnbäck, L., Co-localized opioid and glutamate receptors on astroglial cells-Possible regulators of synaptic transmission, Soc. Neurosci. Abstr., 20 (1994) 1731.
61. Vaysse, P.J.-J., Zukin, R.S., Fields, K.L. and Kessler, J.A., Characterization of opioid receptors in cultured neurons, J. Neurochem., 55 (1990) 624-631.
62. Vogel, Z., Nah, S.-Y., Saya, D., Levy, R., Attali, B. and Barg, J., Signal transduction of opiate receptors in spinal cord cells, J. Toxicol. Toxin Rev., 13 (1994) 115-123.
63. Wang, L. and Gintzler, A.R., Bimodal opioid regulation of cyclic AMP formation: Implications for positive and negative coupling of opiate receptors to adenylyl cyclase, J. Neurochem., 63 (1994) 1726-1730.
64. Zagon, I.S. and McLaughlin, P.J., Identification of opioid peptides regulating proliferation of neurons and glia in the developing nervous system, Brain Res., 542 (1991) 318-323.