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PMID: 9312025 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Protein phosphatase 2A is a critical regulator of protein kinase C zeta signaling targeted by SV40 small t to promote cell growth and NF-kappaB activation.

The EMBO journal ·Vol. 16 ·No. 18 ·1997-09-15 ·Pages 5662-71

Sontag E, Sontag JM, Garcia A

Abstract

We have reported that inhibition of protein phosphatase 2A (PP2A) by expression of SV40 small t stimulates the mitogenic MAP kinase cascade. Here, we show that SV40 small t can substitute for tumor necrosis factor-alpha (TNF-alpha) or serum and stimulate atypical protein kinase C zeta (PKC zeta) activity, resulting in MEK activation, cell proliferation and NF-kappaB-dependent gene transcriptional activation in CV-1 and NIH 3T3 cells. These effects were abrogated by co-expression of kinase-deficient PKC zeta and inhibition of phosphatidylinositol 3-kinase p85alpha-p110 by wortmannin, LY294002 and a dominant-negative mutant of p85alpha. In contrast, expression of kinase-inactive ERK2 inhibited small t-dependent cell growth but was unable to abolish small t-induced NF-kappaB transactivation. Our results provide the first in vivo evidence for a critical regulatory role of PP2A in bifunctional PKC zeta signaling pathways controlled by phosphatidylinositol 3-kinase. Constitutive activation of PKC zeta and NF-kappaB following inhibition of PP2A supports new mechanisms by which SV40 small t promotes cell growth and transformation. By establishing PP2A as a key player in the response of cells to growth factors and stress signals like TNF-alpha, our findings could explain why PP2A is a primary target utilized during SV40 infection to alter cellular behavior.

MeSH Terms
3T3 Cells Androstadienes/pharmacology Animals Antigens, Viral, Tumor/metabolism Blood Calcium-Calmodulin-Dependent Protein Kinases/metabolism Cell Division Cell Line Cells, Cultured Chlorocebus aethiops Enzyme Inhibitors/pharmacology Genes, Reporter Luciferases/metabolism MAP Kinase Kinase 1 Mice Mitogen-Activated Protein Kinase Kinases NF-kappa B/metabolism Phosphatidylinositol 3-Kinases/metabolism Phosphoprotein Phosphatases/metabolism Protein Kinase C/metabolism Protein Phosphatase 2 Protein Serine-Threonine Kinases/metabolism Protein-Tyrosine Kinases/metabolism Recombinant Proteins/metabolism Signal Transduction Simian virus 40/immunology Transfection Wortmannin
Chemicals
Androstadienes Antigens, Viral, Tumor Enzyme Inhibitors NF-kappa B Recombinant Proteins Luciferases Protein-Tyrosine Kinases Protein Serine-Threonine Kinases protein kinase C zeta Protein Kinase C Calcium-Calmodulin-Dependent Protein Kinases MAP Kinase Kinase 1 Map2k1 protein, mouse Mitogen-Activated Protein Kinase Kinases Phosphoprotein Phosphatases Protein Phosphatase 2 Wortmannin
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Sontag E
Department of Pathology, University of Texas Southwestern Medical Center, Dallas, TX 75235, USA. esonta@mednet.swmed.edu
Sontag J M
Garcia A
References (39)
39 references, click to expand
  1. The roles of the simian virus 40 tumor antigens in transformation of Chinese hamster lung cells.
    Cell. 1979 Jul;17(3):635-43 PMID: 225037
  2. Role of diacylglycerol-regulated protein kinase C isotypes in growth factor activation of the Raf-1 protein kinase.
    Mol Cell Biol. 1997 Feb;17(2):732-41 PMID: 9001227
  3. Control of protein phosphatase 2A by simian virus 40 small-t antigen.
    Mol Cell Biol. 1991 Apr;11(4):1988-95 PMID: 1706474
  4. HIV enhancer activity perpetuated by NF-kappa B induction on infection of monocytes.
    Nature. 1991 Apr 25;350(6320):709-12 PMID: 2023633
  5. Induction of NF-kappa B DNA-binding activity during the G0-to-G1 transition in mouse fibroblasts.
    Mol Cell Biol. 1991 Oct;11(10):4943-51 PMID: 1922027
  6. Cellular transcription factors involved in the regulation of HIV-1 gene expression.
    AIDS. 1992 Apr;6(4):347-63 PMID: 1616633
  7. Activation of the zeta isozyme of protein kinase C by phosphatidylinositol 3,4,5-trisphosphate.
    J Biol Chem. 1993 Jan 5;268(1):13-6 PMID: 8380153
  8. Inhibition of protein kinase C zeta subspecies blocks the activation of an NF-kappa B-like activity in Xenopus laevis oocytes.
    Mol Cell Biol. 1993 Feb;13(2):1290-5 PMID: 8423794
  9. A dominant negative protein kinase C zeta subspecies blocks NF-kappa B activation.
    Mol Cell Biol. 1993 Aug;13(8):4770-5 PMID: 8336714
  10. Protein kinase C zeta isoform is critical for mitogenic signal transduction.
    Cell. 1993 Aug 13;74(3):555-63 PMID: 7688666
  11. Inhibition of histamine secretion by wortmannin through the blockade of phosphatidylinositol 3-kinase in RBL-2H3 cells.
    J Biol Chem. 1993 Dec 5;268(34):25846-56 PMID: 7503989
  12. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002).
    J Biol Chem. 1994 Feb 18;269(7):5241-8 PMID: 8106507
  13. Simian virus 40 small-t antigen stimulates viral DNA replication in permissive monkey cells.
    J Virol. 1994 May;68(5):3138-44 PMID: 8151779
  14. zeta PKC induces phosphorylation and inactivation of I kappa B-alpha in vitro.
    EMBO J. 1994 Jun 15;13(12):2842-8 PMID: 8026469
  15. Protein kinase C zeta isoform is critical for kappa B-dependent promoter activation by sphingomyelinase.
    J Biol Chem. 1994 Jul 29;269(30):19200-2 PMID: 8034680
  16. Simian virus 40 small tumor antigen inhibits dephosphorylation of protein kinase A-phosphorylated CREB and regulates CREB transcriptional stimulation.
    Mol Cell Biol. 1994 Sep;14(9):5881-90 PMID: 8065321
  17. Simian virus 40 small t antigen cooperates with mitogen-activated kinases to stimulate AP-1 activity.
    Mol Cell Biol. 1994 Sep;14(9):6244-52 PMID: 8065356
  18. The phosphatidylinositol 3-kinase alpha is required for DNA synthesis induced by some, but not all, growth factors.
    Proc Natl Acad Sci U S A. 1994 Sep 13;91(19):9185-9 PMID: 8090789
  19. Phosphatidic acid activation of protein kinase C-zeta overexpressed in COS cells: comparison with other protein kinase C isotypes and other acidic lipids.
    Biochem J. 1994 Dec 15;304 ( Pt 3):1001-8 PMID: 7818462
  20. Control of I kappa B-alpha proteolysis by site-specific, signal-induced phosphorylation.
    Science. 1995 Mar 10;267(5203):1485-8 PMID: 7878466
  21. Activation of protein kinases and the inactivation of protein phosphatase 2A in tumour necrosis factor and interleukin-1 signal-transduction pathways.
    Eur J Biochem. 1995 Apr 15;229(2):503-11 PMID: 7744073
  22. Overexpression of PKC zeta in NIH3T3 cells does not induce cell transformation nor tumorigenicity and does not alter NF kappa B activity.
    Oncogene. 1995 Jun 1;10(11):2213-20 PMID: 7784066
  23. 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. 1995 Jun 15;14(12):2876-83 PMID: 7796813
  24. Activation of NF-kappa B by phosphatase inhibitors involves the phosphorylation of I kappa B alpha at phosphatase 2A-sensitive sites.
    J Biol Chem. 1995 Aug 4;270(31):18347-51 PMID: 7629157
  25. Evidence for a bifurcation of the mitogenic signaling pathway activated by Ras and phosphatidylcholine-hydrolyzing phospholipase C.
    J Biol Chem. 1995 Sep 8;270(36):21299-306 PMID: 7673165
  26. Ras target proteins in eukaryotic cells.
    FASEB J. 1995 Oct;9(13):1311-8 PMID: 7557021
  27. Protein kinase C-zeta mediates NF-kappa B activation in human immunodeficiency virus-infected monocytes.
    J Virol. 1996 Jan;70(1):223-31 PMID: 8523529
  28. Platelet-derived growth factor activates protein kinase C epsilon through redundant and independent signaling pathways involving phospholipase C gamma or phosphatidylinositol 3-kinase.
    Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):151-5 PMID: 8552594
  29. Evidence for a role of MEK and MAPK during signal transduction by protein kinase C zeta.
    EMBO J. 1995 Dec 15;14(24):6157-63 PMID: 8557035
  30. EGF or PDGF receptors activate atypical PKClambda through phosphatidylinositol 3-kinase.
    EMBO J. 1996 Feb 15;15(4):788-98 PMID: 8631300
  31. Protein kinase C-zeta reverts v-raf transformation of NIH-3T3 cells.
    Genes Dev. 1996 Jun 15;10(12):1455-66 PMID: 8666230
  32. The NF-kappa B and I kappa B proteins: new discoveries and insights.
    Annu Rev Immunol. 1996;14:649-83 PMID: 8717528
  33. Protein kinase C is regulated in vivo by three functionally distinct phosphorylations.
    Curr Biol. 1995 Dec 1;5(12):1394-1403 PMID: 8749392
  34. Phosphoinositide kinases.
    Curr Opin Cell Biol. 1996 Apr;8(2):153-8 PMID: 8791418
  35. Overexpression of protein kinase C-zeta (PKC-zeta) inhibits invasive and metastatic abilities of Dunning R-3327 MAT-LyLu rat prostate cancer cells.
    Cancer Res. 1996 Sep 15;56(18):4137-41 PMID: 8797581
  36. NF-kappa B: ten years after.
    Cell. 1996 Oct 4;87(1):13-20 PMID: 8858144
  37. Functions of ceramide in coordinating cellular responses to stress.
    Science. 1996 Dec 13;274(5294):1855-9 PMID: 8943189
  38. Altered susceptibility to tumor necrosis factor alpha-induced apoptosis of mouse cells expressing polyomavirus middle and small T antigens.
    J Virol. 1997 Jan;71(1):276-83 PMID: 8985347
  39. A synthetic peptide substrate for selective assay of protein kinase C.
    Biochem Biophys Res Commun. 1990 Feb 14;166(3):1220-7 PMID: 1689574
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1997-09-15
Pages
5662-71
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1170198
Subset
IM
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