Role of the Protein Kinase C Lambda/Iota Isoform in Nuclear Factor-Kappab Activation by Interleukin-1beta or Tumor Necrosis Factor-Alpha: Cell Type Specificities
[en] It has previously been reported that distinct signaling pathways can lead to nuclear factor (NF)-kappaB activation following stimulation of different cell types with inflammatory cytokines. As the role of atypical protein kinase C (PKC) isoforms in NF-kappaB activation remains a matter of controversy, we investigated whether this role might be cell type-dependent. Immunoblots detected atypical PKC expression in all the analyzed cell lines. The PKC inhibitor calphostin C inhibited NF-kappaB activation by tumor necrosis factor (TNF)-alpha or interleukin (IL)-1beta in Jurkat or NIH3T3 cells but not in MCF7 A/Z cells. Cell transfections with a PKC lambda/iota dominant negative mutant abolished TNF-alpha-induced NF-kappaB-dependent transcription in NIH3T3 and Jurkat cells but not in MCF7 A/Z cells. Similarly, the same mutant blocked NF-kappaB-dependent transactivation after IL-1beta stimulation of NIH3T3 cells, but was ineffective after IL-1beta treatment of MCF7 A/Z cells. In MCF7 A/Z cells, however, the PKC lambda/iota dominant negative mutant could abolish transactivation of an AP-1-dependent reporter plasmid after stimulation with TNF-alpha but not with IL-1beta. These data thus confirm that transduction pathways for NF-kappaB activation after cell stimulation with TNF-alpha or IL-1beta are cell-type specific and that atypical PKC isoforms participate in this pathway in NIH3T3 and Jurkat cells.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Bonizzi, G.
Piette, Jacques ; Université de Liège - ULiège > Département des sciences de la vie > Virologie - Immunologie
Haterte, Stéphanie ; Université de Liège - ULiège > Département des sciences de la santé publique > Informatique médicale et biostatistique
Merville, Marie-Paule ; Université de Liège - ULiège > Département de pharmacie > Chimie médicale
Bours, Vincent ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Génétique générale et humaine
Language :
English
Title :
Role of the Protein Kinase C Lambda/Iota Isoform in Nuclear Factor-Kappab Activation by Interleukin-1beta or Tumor Necrosis Factor-Alpha: Cell Type Specificities
Diaz-Meco M.T., Municio M.M., Sanchez P., Lozano J., Moscat J. Lambda-interacting protein, a novel protein that specifically interacts with the zinc finger domain of the atypical protein kinase C isotype λ/ι and stimulates its kinase activity in vitro and in vivo. Mol Cell Biol. 16:1996;105-114.
Akimoto K., Mizumo K., Osada S., Hirai S., Tanuma S., Suzuki K., Ohno S. A new member of the third class in the protein kinase C family, PKCλ, expressed dominantly in an undifferentiated mouse embryonal carcinoma cell line and also in many tissues and cells. J Biol Chem. 269:1994;12677-12683.
Selbie L.A., Schmitz-Peiffer C., Sheng Y., Biden T.J. Molecular cloning and characterization of PKCι, an atypical isoform of protein kinase C derived from insulin-secreting cells. J Biol Chem. 268:1993;24296-24302.
Wooten M.W., Zhou G., Seibenhener M.L., Coleman E.S. A role for ζ protein kinase C in nerve growth factor-induced differentiation of PC12 cells. Cell Growth Diff. 5:1994;395-403.
Ways D.K., Posekany K., de Vente J., Garris T., Chen J., Hooker J., Qin W., Cook P., Fletcher D., Parker P. Overexpression of protein kinase C-ζ stimulates leukemic cell differentiation. Cell Growth Diff. 5:1994;1195-1203.
Ono Y., Fujii T., Ogita K., Kirrawa U., Igarashi K., Nishizuka Y. Protein kinase C ζ subspecies from rat brain Its structure, expression, and properties . Proc Natl Acad Sci USA. 86:1989;3099-3103.
Tsutsumi A., Kubo M., Fujii H., Freire-Monar J., Turck C.W., Ransom J.T. Regulation of protein kinase C isoform proteins in phorbol ester-stimulated Jurkat T lymphoma cells. J Immunol. 150:1993;1746-1754.
Ways D., Cook P.P., Webster C., Parker P.J. Effect of phorbol esters on protein kinase C-ζ J Biol Chem. 267:1992;4799-4805.
Nakanishi H., Exton J.H. Purification and characterization of the ζ isoform of protein kinase C from bovine kidney. J Biol Chem. 267:1992;16347-16354.
Nakanishi H., Brewer K.A., Exton J.H. Activation of the ζ isozyme of protein kinase C by phosphatidylinositol 3,4,5-trisphospate. J Biol Chem. 268:1993;13-16.
Lozano J., Berra E., Municio M.M., Diaz-Meco M.T., Dominguez I., Sanz L., Moscat J. Protein kinase C ζ isoform is critical for κB-dependent promoter activation by sphingomyelinase. J Biol Chem. 269:1994;19200-19202.
Müller G., Ayoub M., Storz P., Rennecke J., Fabbro D., Pfizenmaier K. PKC ζ is a molecular switch in signal transduction of TNF-α, bifunctionally regulated by ceramide and arachidonic acid. EMBO J. 14:1995;1961-1969.
Baldwin A.S. The NF-κB and IκB proteins new discoveries and insights . Annu Rev Immunol. 14:1996;649-681.
Siebenlist U., Franzoso G., Brown K. Structure, regulation, and function of NF-κB. Annu Rev Cell Biol. 10:1994;405-455.
Diaz-Meco M.T., Berra E., Municio M.M., Sanz L., Lozano J., Dominguez I., Diaz-Golpe V., Lain de Lera M.T., Alcami J., Payà C.V., Arenzana-Seisdedos F., Virelizier J.-L., Moscat J. A dominant negative protein kinase C ζ subspecies blocks NF-κB activation. Mol Cell Biol. 13:1993;4770-4775.
Dominguez I., Sanz L., Arenzana-Seisderos F., Diaz-Meco M.T., Virelizier J.-L., Moscat J. Inhibition of protein kinase C ζ subspecies blocks the activation of an NF-κB-like activity in Xenopus laevis oocytes. Mol Cell Biol. 13:1993;1290-1295.
Bjorkoy G., Perander M., Overvatn A., Johansen T. Reversion of ras- and phosphatidylcholine-hydrolyzing phospholipase C-mediated transformation of NIH3T3 cells by a dominant interfering mutant of protein kinase C λ is accompanied by the loss of constitutive nuclear mitogen-activated protein kinase/extracellular signal-regulated kinase activity. J Biol Chem. 272:1997;11557-11565.
Sontag E., Sontag J.-M., Garcia A. Protein phosphatase 2A is a critical regulator of protein kinase C ζ signaling targeted by SV40 small t to promote cell growth and NF-κB activation. EMBO J. 16:1997;5662-5671.
Montaner S., Ramos A., Perona R., Esteve P., Carnero A., Lacal J.C. Overexpression of PKC ζ in NIH3T3 cells does not induce cell transformation nor tumorigenicity and does not alter NF-κB activity. Oncogene. 10:1995;9232-9235.
Diaz-Meco M.T., Dominguez I., Sanz L., Dent P., Lozano J., Municio M.M., Berra E., Hay R.T., Sturgill T.W., Moscat J. ζPKC induces phosphorylation and inactivation of IκB-α in vitro. EMBO J. 13:1994;2842-2848.
DiDonato J.A., Hayakawa M., Rothwarf D.M., Zandi E., Karin M. A cytokine-responsive IκB kinase that activates the transcriptional factor NF-κB. Nature. 388:1997;548-554.
Mercurio F., Zhu H., Murray B.W., Shevchenko A., Bennet B.L., Li J.W., Young D.B., Barbosa M., Mann M., Manning A., Rao A. IKK-1 and IKK-2 Cytokine-activated IκB kinases essential for NF-κB activation . Science. 278:1997;860-865.
Régnier C.H., Song H.Y., Gao X., Goeddel D.V., Cao Z., Rothe M. Identification and characterization of an IκB kinase. Cell. 90:1997;373-383.
Woronicz J.D., Gao X., Cao Z., Rothe M., Goeddel D.V. IκB kinase-β NF-κB activation and complex formation with IκB kinase-α and NIK . Science. 278:1997;866-869.
Zandi E., Rothwarf D.M., Delhasse M., Hayakawa M., Karin M. The IκB kinase complex (IKK) contains two kinase subunits, IKKα and IKKβ, necessary for IκB phosphorylation and NF-κB activation. Cell. 91:1997;243-252.
Bonizzi G., Dejardin E., Piret B., Piette J., Merville M.-P., Bours V. IL-1β induces NF-κB in epithelial cells independently of the production of reactive oxygen intermediates. Eur J Biochem. 242:1996;544-549.
Bonizzi G., Piette J., Merville M.-P., Bours V. Distinct signal transduction pathways mediate nuclear factor-κB induction by IL-1β in epithelial and lymphoid cells. J Immunol. 159:1997;5264-5272.
Piette J., Piret B., Bonizzi G., Schoonbroodt S., Merville M.-P., Legrand-Poels S., Bours V. Multiple redox regulation in NF-κB transcription factor activation. Biol Chem. 378:1997;1237-1245.
Bours V., Burd P.R., Brown K., Villalobos J., Park S., Ryseck R.-P., Bravo R., Kelly K., Siebenlist U. A novel mitogen-inducible gene product related to p50/p105-NF-κB partipates in transactivation through a κB site. Mol Cell Biol. 12:1992;685-695.
Schenk H., Klein M., Erdbrügger W., Dröge W., Schulze-Osthoff K. Distinct effects of thioredoxin and antioxidants on the activation of transcription factors NF-κB and AP1. Proc Natl Acad Sci USA. 91:1994;1672-1676.
Xu J., Clark R.A.F. A three-dimensional collagen lattice induces protein kinase C-ζ activity role in α2 integrin and collagenase mRNA expression . J Cell Biol. 136:1997;473-483.
Rzymkiewicz D.M., Tetsuka T., Daphna-Iken D., Srivasrava S., Morrison A.R. Interleukin-1β activates protein kinase Cζ in renal mesangial cells. J Biol Chem. 271:1996;17241-17246.
Das K.C., White C.W. Activation of NF-κB by antineoplastic agents. J Biol Chem. 272:1997;14914-14920.
Berra E., Diaz-Meco M.T., Lozano J., Frutos S., Municio M.M., Sanchez P., Sanz L., Moscat J. Evidence for a role of MEK and MAPK during signal transduction by protein kinase C ζ EMBO J. 14:1995;6157-6163.
Nishizuka Y. The role of protein kinase C in cell surface signal transduction and tumor promotion. Nature. 308:1984;693-698.
Hirano M., Osada S.-I., Aoki T., Hirai S.-I., Hosaka M., Inoue J.-I., Ohno S. MEK kinase is involved in tumor necrosis factor α-induced NF-κB activation and degradation of IκB-α J Biol Chem. 271:1996;13234-13238.
Malinin N.L., Boldin M.P., Kovalenko A.V., Wallach D. MAP3K-related kinase involved in NF-κB induction by TNF, CD95 and IL-1. Nature. 385:1997;540-544.
Wiegmann K., Schütze S., Machleidt T., Witte D., Krönke M. Functional dichotomy of neutral and acidic sphingomyelinases in tumor necrosis factor signaling. Cell. 78:1994;1005-1015.
Machleidt T., Wiegmann K., Henkel T., Schütze S., Baeuerle P., Krönke M. Sphingomyelinase activates proteolytic IκB-α degradation in a cell-free system. J Biol Chem. 269:1994;13760-13765.
Finco T.S., Baldwin A.S.J. κB site-dependent induction of gene expression by diverse inducers of nuclear factor κB requires Raf-1. J Biol Chem. 268:1993;17676-17679.
Schreck R., Rieber P., Baeuerle P.A. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J. 10:1991;2247-2258.
Diehl J., Tong W., Sun G., Hannink M. TNFα-dependent activation of RelA homodimer in astrocytes increased phosphorylation of RelA and MAD-3 precede activation of RelA . J Biol Chem. 270:1995;2703-2707.
Naumann M., Scheidereit C. Activation of NF-κB in vivo is regulated by multiple phosphorylations. EMBO J. 13:1994;4597-4607.
Hayashi T., Sekine T., Okamoto T. Identification of a new serine kinase that activates NFκB by direct phosphorylation. J Biol Chem. 268:1993;26790-26795.
Vanden Berghe W., Plaisance S., Boone E., De Bosscher K., Schmitz M.L., Fiers W., Haegeman G. p38 and extracellular signal-regulated kinase mitogen-activated protein kinase pathways are required for nuclear factor-κB p65 transactivation mediated by tumor necrosis factor. J Biol Chem. 273:1998;3285-3290.
Beyaert R., Cuenda A., Vanden Berghe W., Plaisance S., Lee J.C., Haegeman G., Cohen P., Fiers W. The p38/RK mitogen-activated protein kinase pathway regulates interleukin-6 synthesis in response to tumour necrosis factor. EMBO J. 15:1996;1914-1923.