Interleukin-1 beta and lipopolysaccharide decrease soluble guanylyl cyclase in brain cells: NO-independent destabilization of protein and NO-dependent decrease of mRNA.
Pedraza, Carlos E; Baltrons, María Antonia; HENEKA, Michaelet al.
2003 • In Journal of Neuroimmunology, 144 (1-2), p. 80 - 90
[en] We previously showed that soluble guanylyl cyclase (sGC) is down-regulated in astroglial cells after exposure to LPS. Here, we show that this effect is not mediated by released IL-1beta but that this cytokine is also able to decrease NO-dependent cGMP accumulation in a time- and concentration-dependent manner. The effect of IL-1beta is receptor-mediated, mimicked by tumor necrosis factor-alpha and involves a decrease in sGC activity and protein. IL-1beta and LPS decrease the half-life of the sGC beta1 subunit by a NO-independent but transcription- and translation-dependent mechanism. Additionally, both agents induce a NO-dependent decrease of sGC subunit mRNA. Decreased sGC subunit protein and mRNA levels are also observed in adult rat brain after focal injection of IL-1beta or LPS.
Disciplines :
Neurology
Author, co-author :
Pedraza, Carlos E; Institute of Biotechnology and Biomedicine V. Villar Palasi, and Department of Biochemistry and Molecular Biology, Autonomous University of Barcelona, 08193 Bellaterra, Spain
Baltrons, María Antonia; Inst. Biotech./Biomed. 'V. V.', Dept. of Biochem./Molecular Biology, Autonomous University of Barcelona, 08193 Bellaterra, Spain
HENEKA, Michael ; Department of Neurology, University of Bonn, 53105 Bonn, Germany
García, Agustina; Inst. Biotech./Biomed. 'V. V.', Dept. of Biochem./Molecular Biology, Autonomous University of Barcelona, 08193 Bellaterra, Spain ; Inst. Biotecnologia/Biomedicina 'V.', Univ. Autónoma de Barcelona, 08193 Bellaterra, Spain
External co-authors :
yes
Language :
English
Title :
Interleukin-1 beta and lipopolysaccharide decrease soluble guanylyl cyclase in brain cells: NO-independent destabilization of protein and NO-dependent decrease of mRNA.
We thank F. Garcı́a for assistance in preparation of cultures and A. Segura for technical assistance. We also thank Dr. D. Feinstein (University of Illinois, USA) for advice in the RT-PCR experiments. This work was supported by SAF2001-2540, SGR2001-212, Fundació La Marató TV3 (1008/97) grants to A.G. and a DFG (SFB 400, A8) grant to M.T.H. C.E. Pedraza was the recipient of a predoctoral fellowship from Ministerio de Educación y Cultura (Spain).
Agulló L., García A. Different receptors mediate stimulation of nitric oxide-dependent cyclic GMP formation in neurons and astrocytes in culture. Biochem. Biophys. Res. Commun. 182:1992;1362-1368.
Agulló L., Baltrons M.A., García A. Calcium-dependent nitric oxide formation in glial cells. Brain Res. 686:1995;160-168.
Araujo D.M., Cotman C.W. β-Amyloid stimulates glial cells in vitro to produce growth factors that accumulate in senile plaques in Alzheimer's disease. Brain Res. 569:1992;141-145.
Ariano M.A., Lewicki J.A., Brandwein H.J., Murad F. Immunohistochemical localization of guanylate cyclase within neurons of rat brain. Proc. Natl. Acad. Sci. U. S. A. 79:1982;1316-1320.
Baltrons M.A., García A. Nitric oxide-independent down-regulation of soluble guanylyl cyclase by bacterial endotoxin in astroglial cells. J. Neurochem. 73:1999;2149-2157.
Baltrons M.A., García A. The nitric oxide/cyclic GMP system in astroglial cells. Castellano B., Nieto-Sampedro M. Progress in Brain Res. 2001;335-347 Elsevier, Amsterdam.
Baltrons M.A., Pedraza C.E., García A. β-Amyloid peptides decrease soluble guanylyl cyclase expression in astroglial cells. Neurobiol. Dis. 10:2002;139-149.
Bellamy T.C., Wood J., Goodwin D.A., Garthwaite J. Rapid desensitization of the nitric oxide receptor, soluble guanylyl cyclase, underlies diversity of cellular cGMP responses. Proc. Natl. Acad. Sci. U. S. A. 97:2000;2928-2933.
Benveniste E.N., Benos D.J. TNF-α and INF-γ-mediated signal transduction pathways: effects on glial cell gene expression and function. FASEB J. 9:1995;1577-1584.
Brooker G., Harper J.F., Terasaki W.L., Moylan R.D. Radioimmunoassay of cyclic AMP and cyclic GMP. Adv. Cycl. Nucleotide Res. 10:1979;1-33.
Bunn St.J., Garthwaite J., Wilkin G.P. Guanylate cyclase activities in enriched preparations of neurones, astroglia and a synaptic complex isolated from rat cerebellum. Neurochem. Int. 8:1986;179-185.
Denninger J.W., Marletta M.A. Guanylate cyclase and the NO/cGMP signaling pathway. Biochim. Biophys. Acta. 1411:1999;334-350.
De Vente J., Steinbusch H.H.W. On the stimulation of soluble and particulate guanylate cyclase in the rat brain and the involvement of nitric oxide as studied by cGMP immuno-cytochemistry. Acta Histochem. 92:1992;13-38.
Filippov G., Bloch D.B., Bloch K.D. Nitric oxide decreases stability of mRNAs encoding soluble guanylate cyclase subunits in rat pulmonary artery smooth muscle cells. J. Clin. Invest. 100:1997;942-948.
Förstermann U., Kleinert H. Nitric oxide synthase: expression and expressional control of the three isoforms. Naunyn-Schmiedeberg's Arch. Pharmacol. 356:1995;351-364.
Furuyama T., Inagaki S., Takagi H. Localizations of α1 and β subunits of soluble guanylate cyclase in the rat brain. Mol. Brain Res. 20:1993;335-344.
Garthwaite J., Boulton C.L. Nitric oxide signalling in the central nervous system. Annu. Rev. Physiol. 57:1995;683-706.
Gibb B.J., Garthwaite J. Subunits of the nitric oxide receptor, soluble guanylyl cyclase, expressed in rat brain. Eur. J. Neurosci. 13:2001;539-544.
Griffiths C., Garthwaite J. The shaping of nitric oxide signals by a cellular sink. J. Physiol. 536:2001;855-862.
Heneka M.T., Feinstein D.L. Expression and function of inducible nitric oxide synthase in neurons. J. Neuroimmunol. 114:2001;8-18.
Heneka M.T., Klockgether T., Feinstein D.L. Peroxixome proliferator-activated receptor-γ ligands reduce neuronal inducible nitric oxide synthase expression and cell death in vivo. J. Neurosci. 20:2000;6862-6867.
Heuschling P. Nitric oxide modulates γ-interferon-induced MHC class II antigen expression on rat astrocytes. J. Neuroimmunol. 57:1995;63-69.
Hewett S.J., Corbett J.A., McDaniel M.L., Choi D.W. Interferon-γ and interleukin-1β induce nitric oxide formation from primary mouse astrocytes. Neurosci. Lett. 164:1993;229-232.
Hobbs A.J. Soluble guanylate cyclase: the forgotten sibling. TIPS. 18:1997;484-491.
Kim Y.M., Chung H.T., Kim S.S., Han J.A., Yoo Y.M., Kim K.M., Lee G.H., Yun H.Y., Green A., Li J., Simmons R.L., Billiar T.R. Nitric oxide protects PC12 cells from serum deprivation-induced apoptosis by cGMP-dependent inhibition of caspase signalling. J. Neurosci. 19:1999;6740-6747.
Klegeris A., McGeer P.L. β-Amyloid protein enhances macrophage production of oxygen free radicals and glutamate. J. Neurosci. Res. 49:1997;229-235.
Knowles R.G., Moncada S. Nitric oxide synthases in mammals. Biochem. J. 298:1994;249-258.
Koesling D., Friebe A. Soluble guanylyl cyclase: structure and regulation. Rev. Physiol., Biochem. Pharmacol. 135:1999;41-65.
Lieberman A.P., Pitha P.M., Shin H.S., Shin M.L. Production of tumor necrosis factor and other cytokines by astrocytes stimulated with lipopolysaccharide or a neurotropic virus. Proc. Natl. Acad. Sci. U. S. A. 86:1989;6348-6352.
Liu H., Force T., Bloch K.D. Nerve growth factor decreases soluble guanylate cyclase in rat pheochromocytoma PC12 cells. J. Biol. Chem. 272:1997;6038-6043.
Loddick S.A., Liu C., Takao T., Hashimoto K., de Souza E.B. Interleukin-1 receptors: cloning studies and role in central nervous system disorders. Brain Res. Rev. 26:1998;306-319.
Loihl A.K., Murphy S. Expression of NOS-2 in glia associated with CNS pathology. Prog. Brain Res. 118:1998;253-267.
Murphy S. Production of nitric oxide by glial cells: regulation and potential roles in the CNS. Glia. 29:2000;1-14.
Nakane M., Ichikawa M., Deguchi T. Light and electron microscopic demonstration of guanylate cyclase in rat brain. Brain Res. 273:1983;9-15.
O'Neill L.A., Dinarello C.A. The IL-1 receptor/toll-like receptor superfamily: crucial receptors for inflammation and host defense. Immunol. Today. 21:2000;206-209.
Pantazis N.J., West J.R., Dai D. The nitric oxide-cyclic GMP pathway plays an essential role in both promoting cell survival of cerebellar granule cells in culture and protecting the cells against ethanol neurotoxicity. J. Neurochem. 70:1998;1826-1838.
Papapetropoulos A., Marczin N., Mora G., Milici A., Murad F., Catravas J.D. Regulation of vascular smooth muscle soluble guanylate cyclase activity, mRNA, and protein levels by cAMP elevating agents. Hypertension. 26:1995;696-704.
Papapetropoulos A., Go C., Murad F., Catravas J.D. Mechanisms of tolerance to sodium nitroprusside in cultured rat aortic smooth muscle cells. Br. J. Pharmacol. 117:1996;147-155.
Papapetropoulos A., Abou-Mohamed G., Marczin N., Murad F., Cadwell W., Catravas J.D. Downregulation of nitrovasodilator-induced cyclic GMP accumulation in cells exposed to endotoxin or interleukin-1β Br. J. Pharmacol. 118:1996;1359-1366.
Park S.K., Lin H.L., Murphy S. Nitric oxide regulates nitric oxide synthase 2 gene expression by inhibiting NFkappa B binding to DNA. Biochem. J. 322:1997;609-613.
Pedraza C.E., Baltrons M.A., García A. Interleukin-1β stimulates cyclic GMP efflux in brain astrocytes. FEBS Lett. 507:2001;303-306.
Rauhala P., Lin A.M., Chiueh C.C. Neuroprotection by S- nitrosoglutathione of brain dopamine neurons from oxidative stress. FASEB J. 12:1998;165-173.
Rothwell N.J., Luheshi G.N. Interleukin 1 in the brain: biology, pathology and therapeutic target. Trends Neurosci. 23:2000;618-625.
Shimouchi S., Janssen St.P., Bloch D.B., Zapol W.M., Bloch K.D. cAMP regulates soluble guanylate cyclase β1-subunit gene expression in RFL-6 rat fetal lung fibroblasts. Am. J. Physiol. 265:1993;L456-L461.
Simmons M.L., Murphy S. Cytokines regulate L-arginine-dependent cyclic GMP production in rat glial cells. Eur. J. Neurosci. 5:1993;825-831.
Szabó C. Physiological and pathological roles of nitric oxide in the central nervous system. Brain Res. Bull. 41:1996;131-141.
Takata M., Filipopov G., Liu H., Ichinose F., Janssens St., Bloch D.B., Bloch K.D. Cytokines decrease sGC in pulmonary artery smooth muscle cells via NO-dependent and NO-independent mechanisms. Am. J. Physiol., Lung Cell. Mol. Physiol. 280:2001;L272-L278.
Tanaka J., Markerink-Van Ittersum M., Steinbusch H.W.M., De Vente J. Nitric oxide-mediated cGMP synthesis in oligodendrocytes in the developing rat brain. Glia. 19:1997;286-297.
Togashi H., Sasaki M., Frohman E., Taira E., Ratan R.R., Dawson T.M., Dawson V.L. Neuronal (type I) nitric oxide synthase regulates nuclear factor kappa B activity and immunologic (type II) nitric oxide synthase expression. Proc. Natl. Acad. Sci. U. S. A. 94:1997;2676-2680.
Tsuchida S., Hiraoka M., Sudo M., Kigoshi S., Muramatsu I. Attenuation of sodium nitroprusside responses after prolonged incubation of rat aorta with endotoxin. Am. J. Physiol. 267:1994;H2305-H2310.
Ujiie K., Hogarth L., Danziger R., Drewett J.G., Yuen P.S.T., Pang I.-H., Star R.A. Homologous and heterologous desensitization of a guanylyl cyclase-linked nitric oxide receptor in cultured rat medullary interstitial cells. J. Pharmacol. Exp. Ther. 270:1994;761-767.
Xie Q.W., Whisnant R., Nathan C. Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. J. Exp. Med. 177:1993;1779-1784.
Xiong H., Yamada K., Jourdi H., Kawamura M., Takei N., Han D., Nabeshima T., Wawa H. Regulation of nerve growth factor release by nitric oxide through cyclic GMP pathway in cortical glial cells. Mol. Pharmacol. 56:1999;339-347.
Zhang J., Snyder S.H. Nitric oxide in the nervous system. Annu. Rev. Pharmacol. Toxicol. 35:1995;213-233.
