Opposite regulation of adenylyl cyclase by protein kinase C in astrocyte and microglia cultures

Journal of Neurochemistry

Volumn 69, Issue 3, 1997, Pages 1267-1277

  Patrizio, Mario ^a   Slepko, Natalia ^a   Levi, Giulio ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Calphostin C; Cyclic AMP; G proteins; Phorbol ester; Phosphodiesterases; Staurosporine

Indexed keywords

ADENYLATE CYCLASE; CYCLIC AMP; PROTEIN KINASE C;

ANIMAL CELL; ARTICLE; ASTROCYTE; ENZYME ACTIVATION; ENZYME REGULATION; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0030857352     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1997.69031267.x     Document Type: Article

References (78)

1. Agresti C., Aloisi F., and Levi G. (1991) Heterotypic and homotypic cellular interactions influencing the growth and differentiation of bipotential oligodendrocyte-type-2 astrocyte progenitors in culture. Dev. Biol. 144, 16-29.
2. Aloisi F., Rosa S., Testa U., Bonsi P., Russo G., Peschle C., and Levi G. (1994) Regulation of leukemia inhibitory factor synthesis in cultured human astrocytes. J. Immunol. 152, 5022-5031.
3. Azuma Y., Onishi Y., Hirata C, Tanimoto Y., Yamada T., and Kizaki H. (1995) Staurosporine-induced thymocyte apoptosis is inhibited by herbimycin A, a specific inhibitor of protein tyrosine kinase. Biochem. Mol. Biol. Int. 37, 635-643.
4. Ballestas M. E. and Benveniste E. N. (1995) Interleukin-1β- and tumor necrosis factor-α-mediated regulation of ICAM-1 gene expression in astrocytes requires protein kinase C activity. Glia 14, 267-278.
5. Barres B. A., Chun L. L. Y., and Corey D. P. (1989) Calcium current in cortical astrocytes: induction by cAMP and neurotransmitters and permissive effect of serum factors. J. Neurosci. 9, 3169-3175.
6. Bell J. D. and Brunton L. L. (1987) Multiple effects of phorbol esters on hormone-sensitive adenylate cyclase activity in S49 lymphoma cells. Am. J. Physiol. Endocrinol. Metab. 252, E783-E789.
7. + entry. J. Biol. Chem. 266, 18119-18126.
8. Bernardo A., Patrizio M., Levi G., and Petrucci T. C. (1994) Human immunodeficiency virus protein gp120 interferes with β-adrenergic receptor-mediated protein phosphorylation in cultured rat cortical astrocytes. Cell. Mol. Neurobiol. 14, 159-173.
9. Bouvier M. (1992) Cross-talk between second messengers. Ann. NY Acad. Sci. 39, 120-129.
10. Bressler J. P. and Tinsely P. (1990) Regulation of cAMP levels by protein kinase C in C6 rat glioma cells. J. Neurosci. Res. 25, 81-86.
11. Bridoux A.-M., Fages C., Couchie D., Nunez J., and Tardy M. (1986) Protein synthesis in astrocytes: "Spontaneous" and cyclic AMP-induced differentiation. Dev. Neurosci. 8, 31-43.
12. Brooker G., Harper J. F., Terasaky W. L., and Moylan R. D. (1979) Radioimmunoassay of cyclic AMP and cyclic GMP, in Advances in Cyclic Nucleotide Research, Vol. 11 (Greengard P. and Robinson G. A., eds), pp. 1-33. Raven Press, New York.
13. Busto R., Globus M. Y.-T., Neary J. T., and Ginsberg M. D. (1994) Regional alterations of protein kinase C activity following transient cerebral ischemia: effects of intraischemic brain temperature modulation. J. Neurochem. 63, 1095-1103.
14. Carroll P., Sendtner M., Meyer M., and Thoenen H. (1993) Rat ciliary neurotrophic factor (CNTF): gene structure and regulation of mRNA levels in glial cell cultures. Glia 9, 176-187.
15. Cassel D. and Pfeuffer T. (1978) Mechanism of cholera toxin action: covalent modification of the guanyl nucleotide-binding protein of the adenylate cyclase system. Proc. Natl. Acad. Sci. USA 75, 2669-2673.
16. Castagna M., Takai Y., Kaibuchi K., Sano K., Kikkawa U., and Nishizuka Y. (1982) Direct activation of calcium-activated, phospholipid-dependent protein kinase by tumor-promoting phorbol esters. J. Biol. Chem. 257, 7847-7851.
17. Chao C. C., Hu S., and Peterson P. K. (1995) Modulation of human microglial cell superoxide production by cytokines. J. Leukocyte Biol. 58, 65-70.
18. Chida K., Kato N., and Kuroki T. (1986) Down regulation of phorbol diester receptors by proteolytic degradation of protein kinase C in a cultured cell line of fetal skin keratinocytes. J. Biol. Chem. 261, 13013-13018.
19. Cielsielski-Treska J., Ulrich G., and Aunis D. (1991) Protein kinase C-induced redistribution of cytoskeleton and phosphorylation of vimentin in cultured brain macrophages. J. Neurosci. Res. 29, 362-378.
20. Cole G., Dobkins K. R., Hansen L. A., Terry R. D., and Saitoh T. (1988) Decreased level of protein kinase C in Alzheimer brain. Brain Res. 452, 165-174.
21. Eddleston M. and Mucke L. (1993) Molecular profile of reactive astrocytes: implications for their role in neurologic disease. Neuroscience 54, 15-36.
22. 2+/calmodulin-insensitive adenylyl cyclase from rat brain. Proc. Natl. Acad. Sci. USA 88, 10173-10177.
23. Frohman E. M., Vayuvegula B., Gupta S., and van den Noort S. (1988) Norepinephrine inhibits γ-interferon-induced major histocompatibility class II (Ia) antigen expression on cultured astrocytes via β2-adrenergic signal transduction mechanisms. Proc. Natl. Acad. Sci. USA 85, 1292-1296.
24. Gebicke-Haerter P. J., Seregi A., Schobert A., and Hertting G. (1994) The phorbol ester TPA potentiates cholera toxin- and isoproterenol-stimulated cyclic AMP-synthesis in primary astrocyte cultures. Neurochem. Int. 24, 1-12.
25. Gehrmann J., Matsumoto Y., and Kreutzberg G. W. (1995) Microglia: intrinsic immuneffector cell of the brain. Brain Res. Rev. 20, 269-287.
26. Genain C. P., Roberts T., Davis R. L., Nguyen M.-H., Uccelli A., Faulds D., Li Y., Hedgpeth J., and Hauser S. L. (1995) Prevention of autoimmune demyelination in non-human primates by a cAMP-specific phosphodiesterase inhibitor. Proc. Natl. Acad. Sci. USA 92, 3601-3605.
27. Grimaldi M., Pozzoli G., Navarra P., Preziosi P., and Schettini G. (1994) Vasoactive intestinal peptide and forskolin stimulate interleukin 6 production by rat cortical astrocytes in culture via a cyclic AMP-dependent, prostaglandin-independent mechanism. J. Neurochem. 63, 344-350.
28. Harrison B. C. and Mobley P. L. (1989) Protein phosphorylation in astrocytes mediated by protein kinase C: comparison with phosphorylation by cyclic AMP-dependent protein kinase. J. Neurochem. 53, 1245-1251.
29. Harrison B. C. and Mobley P. L. (1990) Phorbol ester-induced change in astrocyte morphology: correlation with protein kinase C activation and protein phosphorylation. J. Neurosci. Res. 25, 71-80.
30. Hellevuo K., Hoffman P. L., and Tabakoff B. (1996) Adenylyl cyclase: mRNA and characteristics of enzyme activity in three areas of brain. J. Neurochem. 67, 177-185.
31. Hetier E., Ayala J., Bousseau A., and Prochiantz A. (1991) Modulation of interleukin-1 and tumor necrosis factor expression by β-adrenergic agonists in mouse ameboid microglial cells. Exp. Brain Res. 86, 407-413.
32. Hoffman J., Whittle S., and Toews M. (1996) Modulation of cyclic AMP accumulation in glial cells by exogenous phospholipase C. J. Lipid Mediat. Cell Signal. 13, 51-62.
33. Hulley P., Hartikka J., Abdel'Al S., Engels P., Buerki H. R., Wiederhold K. H., Müller T., Kelly P., Lowe D., and Lübbert H. (1995) Inhibitors of type IV phosphodiesterases reduce the toxicity of MPTP in substantia nigra neurons in vivo. Eur. J. Neurosci. 7, 2431-2440.
34. Jacobowitz O. and Iyengar R. (1994) Phorbol ester-induced stimulation and phosphorylation of adenylyl cyclase 2. Proc. Natl. Acad. Sci. USA 91, 10630-10634.
35. Ji L., Zhang G., Uematsu S., Akahori Y., and Hirabayashi Y. (1995) Induction of apoptotic DNA fragmentation and cell death by natural ceramide. FEBS Lett. 358, 211-214.
36. Kato H., Araki T., Itoyama Y., and Kogure K. (1995) Rolipram, a cyclic AMP-selective phosphodiesterase inhibitor, reduces neuronal damage following cerebral ischemia in the gerbil. Eur. J. Pharmacol. 272, 107-110.
37. Kawabe J., Iwami G., Ebina T., Ohno S., Katada T., Ueda Y., Homcy C. J., and Ishikawa Y. (1994) Differential activation of adenylyl cyclase by protein kinase C isoenzymes. J. Biol. Chem. 269, 16554-16558.
38. Kettenmann H. and Ransom B. R., eds (1995) Neuroglia. Oxford University Press, New York.
39. Kikkawa U., Takai Y., Tanaka Y., Miyake R., and Nishizuka Y. (1983) Protein kinase C as a possible receptor protein of tumor-promoting phorbol esters. J. Biol. Chem. 258, 11442-11445.
40. Kobayashi E., Nakano H., Morimoto M., and Tamaoki T. (1989) Calphostin C (UCN-1028C), a novel microbial compound, is a highly potent and specific inhibitor of protein kinase C. Biochem. Biophys. Res. Commun. 159, 548-553.
41. Koh J. Y., Wie M. B., Gwag B. J., Sensi S. L., Canzoniero L. M. T., Demaro J., Csernansky C., and Choi D. W. (1995) Staurosporine-induced neuronal apoptosis. Exp. Neurol. 135, 153-159.
42. Kreutzberg G. W. (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19, 312-318.
43. Levi G., Patrizio M., Bernardo A., Petrucci T. C., and Agresti C. (1993) Human immunodeficiency virus coat protein gp120 inhibits the β-adrenergic regulation of astroglial and microglial functions. Proc. Natl. Acad. Sci. USA 90, 1541-1545.
44. Mangoura D., Sogos V., and Dawson G. (1995) Phorbol esters and PKC signaling regulate proliferation, vimentin cytoskeleton assembly and glutamine synthetase activity of chick embryo cerebrum astrocytes in culture. Dev. Brain Res. 87, 1-11.
45. 2+-independent protein kinase C changes in the brains of patients with Alzheimer's disease. J. Neurochem. 67, 317-323.
46. 2, cyclic AMP and non-steroidal anti-inflammatory drugs. Eur. J. Neurosci. (in press).
47. 2 and by cyclooxygenase inhibitors. Glia 19, 152-160.
48. Moore S. and Thanos S. (1996) The concept of microglia in relation to central nervous system disease and regeneration. Prog. Neurobiol. 48, 441-460.
49. Mosmann T. R. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63.
50. Munn D. H., Beall A. C., Song D., Wrenn R. W., and Throckmorton D. C. (1995) Activation-induced apoptosis in human macrophages: developmental regulation of a novel cell death pathway by macrophage colony-stimulating factor and interferon gamma. J. Exp. Med. 181, 127-136.
51. Murphy S., ed (1993) Astrocytes. Pharmacology and Function. Academic Press, San Diego.
52. Nakadate T., Jeng A. Y., and Blumberg P. M. (1988) Comparison of protein kinase C functional assays to clarify mechanisms of inhibitor action. Biochem. Pharmacol. 37, 1541-1545.
53. Neary J. T., Norenberg L. O. B., and Norenberg M. D. (1988) Protein kinase C in primary astrocyte cultures: cytoplasmic localization and translocation by a phorbol ester. J. Neurochem. 50, 1179-1184.
54. Norris J. G., Tang L.-P., Sparacio S. M., and Benveniste E. N. (1994) Signal transduction pathways mediating astrocyte IL-6 induction by IL-1β and tumor necrosis factor-α. J. Immunol. 152, 841-850.
55. 2 in rat cultured astrocytes. J. Biol. Chem. 266, 9956-9960.
56. Patrizio M., Costa T., and Levi G. (1995) Interferon-γ and lipopolysaccharide reduce cAMP responses in cultured glial cells: reversal by a type IV phosphodiesterase inhibitor. Glia 14, 94-100.
57. Pearce B. and Murphy S. (1993) Protein kinase C down-regulation in astrocytes: differential effects on agonist-stimulated inositol phosphate accumulation. Neurochem. Int. 23, 407-412.
58. Priller J., Haas C. A., Reddington M., and Kreutzberg G. W. (1995) Calcitonin gene-related peptide and ATP induce immediate early gene expression in cultured rat microglial cells. Glia 15, 447-457.
59. Rozengurt E., Murray M., Zachary I., and Collins M. (1987) Protein kinase C activation enhances cAMP accumulation in Swiss 3T3 cells: inhibition by pertussis toxin. Proc. Natl. Acad. Sci. USA 84, 2282-2286.
60. Rudge J. S., Morrissey D., Lindsay R. M., and Pasnikowski E. M. (1994) Regulation of ciliary neurotrophic factor in cultured rat hippocampal astrocytes. Eur. J. Neurosci. 6, 218-229.
61. Sasaki A., Levison S. W., and Ting J. P.-Y. (1990) Differential suppression of interferon-γ-induced Ia antigen expression on cultured rat astroglia and microglia by second messengers. J. Neuroimmunol. 29, 213-222.
62. Savio T. and Levi G. (1993) Neurotoxicity of HIV coat protein gp120, NMDA receptors, and protein kinase C: a study with rat cerebellar granule cell cultures. J. Neurosci. Res. 34, 265-272.
63. Schwartz J. P. and Mishler K. (1990) β-Adrenergic receptor regulation, through cyclic AMP, of nerve growth factor expression in rat cortical and cerebellar astrocytes. Cell. Mol. Neurobiol. 10, 447-457.
64. Shain W., Madelian V., and Martin D. L. (1989) Inactivation of cyclic AMP-dependent taurine release from astroglia. J. Neurochem. 52, 1455-1460.
65. Sibley D. R., Jeffs R. A., Daniel K., Nambi P., and Lefkowitz R. J. (1986) Phorbol diester treatment promotes enhanced adenylate cyclase activity in frog erythrocytes. Arch. Biochem. Biophys. 244, 373-381.
66. Simmons M. L. and Murphy S. (1994) Roles for protein kinases in the induction of nitric oxide synthase in astrocytes. Glia 11, 227-234.
67. Sommer N., Löschmann P.-A., Northoff G. H., Weller M., Steinbrecher A., Steinbach J. P., Lichtenfels R., Meyermann R., Riethmüller A., Fontana A., Dichgans J., and Martin R. (1995) The antidepressant rolipram suppresses cytokine production and prevents autoimmune encephalomyelitis. Nat. Med. 1, 244-248.
68. Sunahara R. K., Dessauer C. W., and Gilman A. G. (1996) Complexity and diversity of mammalian adenylyl cyclase. Annu. Rev. Pharmacol. Toxicol. 36, 461-480.
69. Tapia-Arancibia L., Veria S., Pares-Herbute N., and Astier H. (1988) Activators of protein kinase C enhance cyclic AMP accumulation in cerebral cortical and diencephalic neurons in primary culture. J. Neurosci. Res. 20, 195-201.
70. Tomozawa Y., Yabuuchi K., Inoue T., and Satoh M. (1995) Participation of cAMP and cAMP-dependent protein kinase in β-adrenoceptor-mediated interleukin-1β mRNA induction in cultured microglia. Neurosci. Res. 22, 399-409.
71. Ui M. (1984) Islet-activating protein, pertussis toxin: a probe for functions of the inhibitory guanine nucleotide regulatory component of adenylate cyclase. Trends Pharmacol. Sci. 5, 277-279.
72. Vachon L., Costa T., and Herz A. (1987) GTPase and adenylate cyclase desensitize at different rates in NG108-15 cells. Mol. Pharmacol. 31, 159-168.
73. Wiesner D. A. and Dawson G. (1996) Staurosporine induces programmed cell death in embryonic neurons and activation of the ceramide pathway. J. Neurochem. 66, 1418-1425.
74. Yamashita A., Kurokawa T., Une Y., and Ishibashi S. (1988) Phorbol ester regulates stimulatory and inhibitory pathways of the hormone-sensitive adenylate cyclase system in rat reticulocytes. Eur. J. Pharmacol. 151, 167-175.
75. Yokota M., Peterson J. W., Kaoutzanis M., and Kowall N. W. (1992) Immunohistochemical distribution of protein kinase-C isozymes is differentially altered in ischemic gerbil hippocampus. Brain Res. 587, 123-129.
76. Yoshimasa T., Sibley D. R., Bouvier M., Lefkowitz R. J., and Caron M. G. (1987) Cross-talk between cellular signaling pathways suggested by phorbol-ester-induced adenylate cyclase phosphorylation. Nature 327, 67-70.
77. Yoshimura M. and Cooper D. M. F. (1993) Type-specific stimulation of adenylyl cyclase by protein kinase C. J. Biol. Chem. 268, 4604-4607.
78. Zielke H. R., Tildon J. T., Landry M. E., and Max S. R. (1990) Effect of 8-bromo-cAMP and dexamethasone on glutamate metabolism in rat astrocytes. Neurochem. Res. 15, 1115-1122.