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Gene Expression

Glycogen Synthase Kinase 3β-Mediated Apoptosis of Primary Cortical Astrocytes Involves Inhibition of Nuclear Factor κB Signaling

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Pages 4649-4662 | Received 11 Feb 2003, Accepted 25 Mar 2003, Published online: 27 Mar 2023

REFERENCES

  • Abbott, K. L., A. M. Robida, M. E. Davis, G. K. Pavlath, J. M. Camden, J. T. Turner, and T. J. Murphy. 2000. Differential regulation of vascular smooth muscle nuclear factor kappa-B by G alpha q-coupled and cytokine receptors. J. Mol. Cell. Cardiol. 32: 391–403.
  • Allport, V. C., D. M. Slater, R. Newton, and P. R. Bennett. 2000. NF-κB and AP-1 are required for cyclo-oxygenase 2 gene expression in amnion epithelial cell line (WISH). Mol. Hum. Reprod. 6: 561–565.
  • Barbin, G., M. P. Roisin, and B. Zalc. 2001. Tumor necrosis factor alpha activates the phosphorylation of ERK, SAPK/JNK, and P38 kinase in primary cultures of neurons. Neurochem. Res. 26: 107–112.
  • Beals, C. R., C. M. Sheridan, C. W. Turck, P. Gardner, and G. R. Crabtree. 1997. Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science 275: 1930–1934.
  • Beg, A. A., and D. Baltimore. 1996. An essential role for NF-κB in preventing TNF-alpha-induced cell death. Science 274: 782–784.
  • Bertrand, F., A. Atfi, A. Cadoret, G. L'Allemain, H. Robin, O. Lascols, J. Capeau, and G. Cherqui. 1998. A role for nuclear factor κB in the antiapoptotic function of insulin. J. Biol. Chem. 273: 2931–2938.
  • Bezzi, P., M. Domercq, L. Brambilla, R. Galli, D. Schols, E. De Clercq, A. Vescovi, G. Bagetta, G. Kollias, J. Meldolesi, and A. Volterra. 2001. CXCR4-activated astrocyte glutamate release via TNFα: amplification by microglia triggers neurotoxicity. Nat. Neurosci. 4: 702–710.
  • Bezzi, P., M. Domercq, S. Vesce, and A. Volterra. 2001. Neuron-astrocyte cross-talk during synaptic transmission: physiological and neuropathological implications. Prog. Brain. Res. 132: 255–265.
  • Bijur, G. N., P. De Sarno, and R. S. Jope. 2000. Glycogen synthase kinase-3β facilitates staurosporine- and heat shock-induced apoptosis. Protection by lithium. J. Biol. Chem. 275: 7583–7590.
  • Bournat, J. C., A. M. Brown, and A. P. Soler. 2000. Wnt-1 dependent activation of the survival factor NF-κB in PC12 cells. J. Neurosci. Res. 61: 21–32.
  • Boyle, W. J., T. Smeal, L. H. Defize, P. Angel, J. R. Woodgett, M. Karin, and T. Hunter. 1991. Activation of protein kinase C decreases phosphorylation of c-Jun at sites that negatively regulate its DNA-binding activity. Cell 64: 573–584.
  • Brambilla, R., and M. P. Abbracchio. 2001. Modulation of cyclooxygenase-2 and brain reactive astrogliosis by purinergic P2 receptors. Ann. N. Y. Acad. Sci. 939: 54–62.
  • Caivano, M., B. Gorgoni, P. Cohen, and V. Poli. 2001. The induction of cyclooxygenase-2 mRNA in macrophages is biphasic and requires both CCAAT enhancer-binding protein beta (C/EBP beta) and C/EBP delta transcription factors. J. Biol. Chem. 276: 48693–48701.
  • Carbott, D. E., L. Duan, and M. A. Davis. 2002. Phosphoinositol 3 kinase inhibitor, LY294002 increases bcl-2 protein and inhibits okadaic acid-induced apoptosis in Bcl-2 expressing renal epithelial cells. Apoptosis 7: 69–76.
  • Chen, G., L. D. Huang, Y. M. Jiang, and H. K. Manji. 1999. The mood-stabilizing agent valproate inhibits the activity of glycogen synthase kinase-3. J. Neurochem. 72: 1327–1330.
  • Cross, D. A., A. A. Culbert, K. A. Chalmers, L. Facci, S. D. Skaper, and A. D. Reith. 2001. Selective small-molecule inhibitors of glycogen synthase kinase-3 activity protect primary neurones from death. J. Neurochem. 77: 94–102.
  • Crowder, R. J., and R. S. Freeman. 2000. Glycogen synthase kinase-3 beta activity is critical for neuronal death caused by inhibiting phosphatidylinositol 3-kinase or Akt but not for death caused by nerve growth factor withdrawal. J. Biol. Chem. 275: 34266–34271.
  • Deininger, M. H., R. Meyermann, K. Trautmann, M. Morgalla, F. Duffner, E. H. Grote, J. Wickboldt, and H. J. Schluesener. 2000. Cyclooxygenase (COX)-1 expressing macrophages/microglial cells and COX-2 expressing astrocytes accumulate during oligodendroglioma progression. Brain Res. 885: 111–116.
  • Di Iorio, P., S. Kleywegt, R. Ciccarelli, U. Traversa, C. M. Andrew, C. E. Crocker, E. S. Werstiuk, and M. P. Rathbone. 2002. Mechanisms of apoptosis induced by purine nucleosides in astrocytes. Glia 38: 179–190.
  • DiDonato, J. A., M. Hayakawa, D. M. Rothwarf, E. Zandi, and M. Karin. 1997. A cytokine-responsive IκB kinase that activates the transcription factor NF-κB. Nature 388: 548–554.
  • Diehl, J. A., M. Cheng, M. F. Roussel, and C. J. Sherr. 1998. Glycogen synthase kinase-3β regulates cyclin D1 proteolysis and subcellular localization. Genes Dev. 12: 3499–3511.
  • Embi, N., D. B. Rylatt, and P. Cohen. 1980. Glycogen synthase kinase-3 from rabbit skeletal muscle. Separation from cyclic-AMP-dependent protein kinase and phosphorylase kinase. Eur. J. Biochem. 107: 519–527.
  • Foehr, E. D., J. Bohuslav, L. F. Chen, C. DeNoronha, R. Geleziunas, X. Lin, A. O'Mahony, and W. C. Greene. 2000. The NF-kappa B-inducing kinase induces PC12 cell differentiation and prevents apoptosis. J. Biol. Chem. 275: 34021–34024.
  • Frame, S., P. Cohen, and R. M. Biondi. 2001. A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation. Mol. Cell 7: 1321–1327.
  • Fraser, E., N. Young, R. Dajani, J. Franca-Koh, J. Ryves, R. S. Williams, M. Yeo, M. T. Webster, C. Richardson, M. J. Smalley, L. H. Pearl, A. Harwood, and T. C. Dale. 2002. Identification of the Axin and Frat binding region of glycogen synthase kinase-3. J. Biol. Chem. 277: 2176–2185.
  • Ghosh, S., and M. Karin. 2002. Missing pieces in the NF-κB puzzle. Cell 109(Suppl.): S81–S96.
  • Ghosh, S., M. J. May, and E. B. Kopp. 1998. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16: 225–260.
  • Ginger, R. S., E. C. Dalton, W. J. Ryves, M. Fukuzawa, J. G. Williams, and A. J. Harwood. 2000. Glycogen synthase kinase-3 enhances nuclear export of a Dictyostelium STAT protein. EMBO J. 19: 5483–5491.
  • Grimes, C. A., and R. S. Jope. 2001. CREB DNA binding activity is inhibited by glycogen synthase kinase-3 beta and facilitated by lithium. J. Neurochem. 78: 1219–1232.
  • Grimes, C. A., and R. S. Jope. 2001. The multifaceted roles of glycogen synthase kinase 3β in cellular signaling. Prog. Neurobiol. 65: 391–426.
  • Hazell, A. S. 2002. Astrocytes and manganese neurotoxicity. Neurochem. Int. 41: 271–277.
  • He, T. C., S. Zhou, L. T. da Costa, J. Yu, K. W. Kinzler, and B. Vogelstein. 1998. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 95: 2509–2514.
  • Hetman, M., J. E. Cavanaugh, D. Kimelman, and Z. Xia. 2000. Role of glycogen synthase kinase-3β in neuronal apoptosis induced by trophic withdrawal. J. Neurosci. 20: 2567–2574.
  • Hoeflich, K. P., J. Luo, E. A. Rubie, M. S. Tsao, O. Jin, and J. R. Woodgett. 2000. Requirement for glycogen synthase kinase-3β in cell survival and NF-κB activation. Nature 406: 86–90.
  • Hostettler, M. E., P. E. Knapp, and S. L. Carlson. 2002. Platelet-activating factor induces cell death in cultured astrocytes and oligodendrocytes: involvement of caspase-3. Glia 38: 228–239.
  • Hu, Y., V. Baud, M. Delhase, P. Zhang, T. Deerinck, M. Ellisman, R. Johnson, and M. Karin. 1999. Abnormal morphogenesis but intact IKK activation in mice lacking the IKKκ subunit of IκB kinase. Science 284: 316–320.
  • Karin, M., and Y. Ben-Neriah. 2000. Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu. Rev. Immunol. 18: 621–663.
  • Kaul, M., G. A. Garden, and S. A. Lipton. 2001. Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410: 988–994.
  • Kawamura, N., L. Singer, R. A. Wetsel, and H. R. Colten. 1992. Cis- and trans-acting elements required for constitutive and cytokine-regulated expression of the mouse complement C3 gene. Biochem. J. 283: 705–712.
  • Kim, M. S., Y. P. Cheong, H. S. So, K. M. Lee, T. Y. Kim, J. Oh, Y. T. Chung, Y. Son, B. R. Kim, and R. Park. 2001. Protective effects of morphine in peroxynitrite-induced apoptosis of primary rat neonatal astrocytes: potential involvement of G protein and phosphatidylinositol 3-kinase (PI3 kinase). Biochem. Pharmacol. 61: 779–786.
  • Leclerc, S., M. Garnier, R. Hoessel, D. Marko, J. A. Bibb, G. L. Snyder, P. Greengard, J. Biernat, Y. Z. Wu, E. M. Mandelkow, G. Eisenbrand, and L. Meijer. 2001. Indirubins inhibit glycogen synthase kinase-3 beta and CDK5/p25, two protein kinases involved in abnormal tau phosphorylation in Alzheimer's disease. A property common to most cyclin-dependent kinase inhibitors? J. Biol. Chem. 276: 251–260.
  • Lezoualc'h, F., Y. Sagara, F. Holsboer, and C. Behl. 1998. High constitutive NF-κB activity mediates resistance to oxidative stress in neuronal cells. J. Neurosci. 18: 3224–3232.
  • Li, M., X. Wang, M. K. Meintzer, T. Laessig, M. J. Birnbaum, and K. A. Heidenreich. 2000. Cyclic AMP promotes neuronal survival by phosphorylation of glycogen synthase kinase 3β. Mol. Cell. Biol. 20: 9356–9363.
  • Li, Q., Q. Lu, J. Y. Hwang, D. Buscher, K. F. Lee, J. C. Izpisua-Belmonte, and I. M. Verma. 1999. IKK1-deficient mice exhibit abnormal development of skin and skeleton. Genes Dev. 13: 1322–1328.
  • Li, Z. W., W. Chu, Y. Hu, M. Delhase, T. Deerinck, M. Ellisman, R. Johnson, and M. Karin. 1999. The IKKβ subunit of IκB kinase (IKK) is essential for nuclear factor κB activation and prevention of apoptosis. J. Exp. Med. 189: 1839–1845.
  • Maggirwar, S. B., S. Ramirez, N. Tong, H. A. Gelbard, and S. Dewhurst. 2000. Functional interplay between nuclear factor-κB and c-Jun integrated by coactivator p300 determines the survival of nerve growth factor-dependent PC12 cells. J. Neurochem. 74: 527–539.
  • Maggirwar, S. B., N. Tong, S. Ramirez, H. A. Gelbard, and S. Dewhurst. 1999. HIV-1 Tat-mediated activation of glycogen synthase kinase-3β contributes to Tat-mediated neurotoxicity. J. Neurochem. 73: 578–586.
  • Makris, C., V. L. Godfrey, G. Krahn-Senftleben, T. Takahashi, J. L. Roberts, T. Schwarz, L. Feng, R. S. Johnson, and M. Karin. 2000. Female mice heterozygous for IKK gamma/NEMO deficiencies develop a dermatopathy similar to the human X-linked disorder incontinentia pigmenti. Mol. Cell 5: 969–979.
  • Mattson, M. P. 2000. Apoptosis in neurodegenerative disorders. Nat. Rev. Mol. Cell. Biol. 1: 120–129.
  • May, M. J., F. D'Acquisto, L. A. Madge, J. Glockner, J. S. Pober, and S. Ghosh. 2000. Selective inhibition of NF-κB activation by a peptide that blocks the interaction of NEMO with the IκB kinase complex. Science 289: 1550–1554.
  • Moule, S. K., G. I. Welsh, N. J. Edgell, E. J. Foulstone, C. G. Proud, and R. M. Denton. 1997. Regulation of protein kinase B and glycogen synthase kinase-3 by insulin and beta-adrenergic agonists in rat epididymal fat cells. Activation of protein kinase B by wortmannin-sensitive and -insensitive mechanisms. J. Biol. Chem. 272: 7713–7719.
  • Nakao, S., Y. Ogata, E. Shimizu-Sasaki, M. Yamazaki, S. Furuyama, and H. Sugiya. 2000. Activation of NFκB is necessary for IL-1β-induced cyclooxygenase-2 (COX-2) expression in human gingival fibroblasts. Mol. Cell. Biochem. 209: 113–118.
  • Nedergaard, M. 1994. Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science 263: 1768–1771.
  • O'Connell, M. A., B. L. Bennett, F. Mercurio, A. M. Manning, and N. Mackman. 1998. Role of IKK1 and IKK2 in lipopolysaccharide signaling in human monocytic cells. J. Biol. Chem. 273: 30410–30414.
  • Ozes, O. N., L. D. Mayo, J. A. Gustin, S. R. Pfeffer, L. M. Pfeffer, and D. B. Donner. 1999. NF-κB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 401: 82–85.
  • Pap, M., and G. M. Cooper. 1998. Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-kinase/Akt cell survival pathway. J. Biol. Chem. 273: 19929–19932.
  • Pap, M., and G. M. Cooper. 2002. Role of translation initiation factor 2B in control of cell survival by the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3β signaling pathway. Mol. Cell. Biol. 22: 578–586.
  • Parpura, V., T. A. Basarsky, F. Liu, K. Jeftinija, S. Jeftinija, and P. G. Haydon. 1994. Glutamate-mediated astrocyte-neuron signalling. Nature 369: 744–747.
  • Pfrieger, F. W., and B. A. Barres. 1997. Synaptic efficacy enhanced by glial cells in vitro. Science 277: 1684–1687.
  • Ramirez, S. H., J. F. Sanchez, C. A. Dimitri, H. A. Gelbard, S. Dewhurst, and S. B. Maggirwar. 2001. Neurotrophins prevent HIV Tat-induced neuronal apoptosis via a nuclear factor-κB (NF-κB)-dependent mechanism. J. Neurochem. 78: 874–889.
  • Reuther, J. Y., and A. S. Baldwin, Jr. 1999. Apoptosis promotes a caspase-induced amino-terminal truncation of IκBα that functions as a stable inhibitor of NF-κB. J. Biol. Chem. 274: 20664–20670.
  • Rothwarf, D. M., E. Zandi, G. Natoli, and M. Karin. 1998. IKK-gamma is an essential regulatory subunit of the IκB kinase complex. Nature 395: 297–300.
  • Rudolph, D., W. C. Yeh, A. Wakeham, B. Rudolph, D. Nallainathan, J. Potter, A. J. Elia, and T. W. Mak. 2000. Severe liver degeneration and lack of NF-κB activation in NEMO/IKKγ-deficient mice. Genes Dev. 14: 854–862.
  • Saas, P., J. Boucraut, A. L. Quiquerez, V. Schnuriger, G. Perrin, S. Desplat-Jego, D. Bernard, P. R. Walker, and P. Y. Dietrich. 1999. CD95 (Fas/Apo-1) as a receptor governing astrocyte apoptotic or inflammatory responses: a key role in brain inflammation? J. Immunol. 162: 2326–2333.
  • Schouten, G. J., A. C. Vertegaal, S. T. Whiteside, A. Israel, M. Toebes, J. C. Dorsman, A. J. van der Eb, and A. Zantema. 1997. IκBα is a target for the mitogen-activated 90 kDa ribosomal S6 kinase. EMBO J. 16: 3133–3144.
  • Schwabe, R. F., and D. A. Brenner. 2002. Role of glycogen synthase kinase-3 in TNF-alpha-induced NF-κB activation and apoptosis in hepatocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 283: G204–G211.
  • Song, H., C. F. Stevens, and F. H. Gage. 2002. Astroglia induce neurogenesis from adult neural stem cells. Nature 417: 39–44.
  • Takeda, K., O. Takeuchi, T. Tsujimura, S. Itami, O. Adachi, T. Kawai, H. Sanjo, K. Yoshikawa, N. Terada, and S. Akira. 1999. Limb and skin abnormalities in mice lacking IKKα. Science 284: 313–316.
  • Tamatani, M., Y. H. Che, H. Matsuzaki, S. Ogawa, H. Okado, S. Miyake, T. Mizuno, and M. Tohyama. 1999. Tumor necrosis factor induces Bcl-2 and Bcl-x expression through NFκB activation in primary hippocampal neurons. J. Biol. Chem. 274: 8531–8538.
  • Tanaka, M., M. E. Fuentes, K. Yamaguchi, M. H. Durnin, S. A. Dalrymple, K. L. Hardy, and D. V. Goeddel. 1999. Embryonic lethality, liver degeneration, and impaired NF-κB activation in IKK-β-deficient mice. Immunity 10: 421–429.
  • Tanji, C., H. Yamamoto, N. Yorioka, N. Kohno, K. Kikuchi, and A. Kikuchi. 2002. A-kinase anchoring protein AKAP220 binds to glycogen synthase kinase-3β (GSK-3β) and mediates protein kinase A-dependent inhibition of GSK-3β. J. Biol. Chem. 277: 36955–36961.
  • Thomas, G. M., S. Frame, M. Goedert, I. Nathke, P. Polakis, and P. Cohen. 1999. A GSK3-binding peptide from FRAT1 selectively inhibits the GSK3-catalysed phosphorylation of axin and beta-catenin. FEBS Lett. 458: 247–251.
  • Thomas, L. B., D. J. Gates, E. K. Richfield, T. F. O'Brien, J. B. Schweitzer, and D. A. Steindler. 1995. DNA end labeling (TUNEL) in Huntington's disease and other neuropathological conditions. Exp. Neurol. 133: 265–272.
  • Thompson, K. A., J. C. McArthur, and S. L. Wesselingh. 2001. Correlation between neurological progression and astrocyte apoptosis in HIV-associated dementia. Ann. Neurol. 49: 745–752.
  • Tibbles, L. A., J. C. Spurrell, G. P. Bowen, Q. Liu, M. Lam, A. K. Zaiss, S. M. Robbins, M. D. Hollenberg, T. J. Wickham, and D. A. Muruve. 2002. Activation of p38 and ERK signaling during adenovirus vector cell entry lead to expression of the C-X-C chemokine IP-10. J. Virol. 76: 1559–1568.
  • Tong, N., J. F. Sanchez, S. B. Maggirwar, S. H. Ramirez, H. Guo, S. Dewhurst, and H. A. Gelbard. 2001. Activation of glycogen synthase kinase 3 beta (GSK-3β) by platelet activating factor mediates migration and cell death in cerebellar granule neurons. Eur. J. Neurosci. 13: 1913–1922.
  • Traenckner, E. B., H. L. Pahl, T. Henkel, K. N. Schmidt, S. Wilk, and P. A. Baeuerle. 1995. Phosphorylation of human I kappa B-alpha on serines 32 and 36 controls I kappa B-alpha proteolysis and NF-kappa B activation in response to diverse stimuli. EMBO J. 14: 2876–2883.
  • Van Antwerp, D. J., S. J. Martin, T. Kafri, D. R. Green, and I. M. Verma. 1996. Suppression of TNF-alpha-induced apoptosis by NF-κB. Science 274: 787–789.
  • van Weeren, P. C., K. M. de Bruyn, A. M. de Vries-Smits, J. van Lint, and B. M. Burgering. 1998. Essential role for protein kinase B (PKB) in insulin-induced glycogen synthase kinase 3 inactivation. Characterization of dominant-negative mutant of PKB. J. Biol. Chem. 273: 13150–13156.
  • von Knethen, A., D. Callsen, and B. Brune. 1999. Superoxide attenuates macrophage apoptosis by NF-kappa B and AP-1 activation that promotes cyclooxygenase-2 expression. J. Immunol. 163: 2858–2866.
  • Wachtel, M., M. F. Bolliger, H. Ishihara, K. Frei, H. Bluethmann, and S. M. Gloor. 2001. Down-regulation of occludin expression in astrocytes by tumour necrosis factor (TNF) is mediated via TNF type-1 receptor and nuclear factor-κB activation. J. Neurochem. 78: 155–162.
  • Wang, Q. M., C. J. Fiol, A. A. DePaoli-Roach, and P. J. Roach. 1994. Glycogen synthase kinase-3 beta is a dual specificity kinase differentially regulated by tyrosine and serine/threonine phosphorylation. J. Biol. Chem. 269: 14566–14574.
  • Wood, L. D., and A. Richmond. 1995. Constitutive and cytokine-induced expression of the melanoma growth stimulatory activity/GRO alpha gene requires both NF-kappa B and novel constitutive factors. J. Biol. Chem. 270: 30619–30626.
  • Woronicz, J. D., X. Gao, Z. Cao, M. Rothe, and D. V. Goeddel. 1997. IκB kinase-beta: NF-κB activation and complex formation with IκB kinase-alpha and NIK. Science 278: 866–869.
  • Yamamoto, Y., D. W. Kim, Y. T. Kwak, S. Prajapati, U. Verma, and R. B. Gaynor. 2001. IKKγ/NEMO facilitates the recruitment of the IκB proteins into the IκB kinase complex. J. Biol. Chem. 276: 36327–36336.
  • Yamaoka, S., G. Courtois, C. Bessia, S. T. Whiteside, R. Weil, F. Agou, H. E. Kirk, R. J. Kay, and A. Israel. 1998. Complementation cloning of NEMO, a component of the IκB kinase complex essential for NF-κB activation. Cell 93: 1231–1240.
  • Yost, C., M. Torres, J. R. Miller, E. Huang, D. Kimelman, and R. T. Moon. 1996. The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev. 10: 1443–1454.
  • Zamanian-Daryoush, M., T. H. Mogensen, J. A. DiDonato, and B. R. Williams. 2000. NF-κB activation by double-stranded-RNA-activated protein kinase (PKR) is mediated through NF-κB-inducing kinase and IκB kinase. Mol. Cell. Biol. 20: 1278–1290.

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