Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1993 Feb;13(2):1290–1295. doi: 10.1128/mcb.13.2.1290

Inhibition of protein kinase C zeta subspecies blocks the activation of an NF-kappa B-like activity in Xenopus laevis oocytes.

I Dominguez 1, L Sanz 1, F Arenzana-Seisdedos 1, M T Diaz-Meco 1, J L Virelizier 1, J Moscat 1
PMCID: PMC359014  PMID: 8423794

Abstract

Nuclear factor kappa B (NF-kappa B) plays a critical role in the regulation of a large variety of cellular genes. However, the mechanism whereby this nuclear factor is activated remains to be determined. In this report, we present evidence that in oocytes from Xenopus laevis, (i) ras p21- and phospholipase C (PLC)-mediated phosphatidylcholine (PC) hydrolysis activates NF-kappa B and (ii) protein kinase C zeta subspecies is involved in the activation of NF-kappa B in response to insulin/ras p21/PC-PLC. Thus, the microinjection of either ras p21 or PC-PLC, or the exposure of oocytes to insulin, promotes a significant translocation to the nucleus of an NF-kappa B-like activity. This effect is not observed when oocytes are incubated with phorbol myristate acetate or progesterone, both of which utilize a ras p21-independent pathway for oocyte activation. These data strongly suggest a critical role of the insulin/ras p21/PC-PLC/protein kinase C zeta pathway in the control of NF-kappa B activation.

Full text

PDF

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arenzana-Seisdedos F., Israël N., Bachelerie F., Hazan U., Alcami J., Dautry F., Virelizier J. L. c-Ha-ras transfection induces human immunodeficiency virus (HIV) transcription through the HIV-enhancer in human fibroblasts and astrocytes. Oncogene. 1989 Nov;4(11):1359–1362. [PubMed] [Google Scholar]
  2. Bachelerie F., Alcami J., Arenzana-Seisdedos F., Virelizier J. L. HIV enhancer activity perpetuated by NF-kappa B induction on infection of monocytes. Nature. 1991 Apr 25;350(6320):709–712. doi: 10.1038/350709a0. [DOI] [PubMed] [Google Scholar]
  3. Baeuerle P. A., Baltimore D. A 65-kappaD subunit of active NF-kappaB is required for inhibition of NF-kappaB by I kappaB. Genes Dev. 1989 Nov;3(11):1689–1698. doi: 10.1101/gad.3.11.1689. [DOI] [PubMed] [Google Scholar]
  4. Baeuerle P. A., Baltimore D. Activation of DNA-binding activity in an apparently cytoplasmic precursor of the NF-kappa B transcription factor. Cell. 1988 Apr 22;53(2):211–217. doi: 10.1016/0092-8674(88)90382-0. [DOI] [PubMed] [Google Scholar]
  5. Baeuerle P. A., Baltimore D. I kappa B: a specific inhibitor of the NF-kappa B transcription factor. Science. 1988 Oct 28;242(4878):540–546. doi: 10.1126/science.3140380. [DOI] [PubMed] [Google Scholar]
  6. Birchmeier C., Broek D., Wigler M. ras proteins can induce meiosis in Xenopus oocytes. Cell. 1985 Dec;43(3 Pt 2):615–621. doi: 10.1016/0092-8674(85)90233-8. [DOI] [PubMed] [Google Scholar]
  7. Diaz-Meco M. T., Quiñones S., Municio M. M., Sanz L., Bernal D., Cabrero E., Saus J., Moscat J. Protein kinase C-independent expression of stromelysin by platelet-derived growth factor, ras oncogene, and phosphatidylcholine-hydrolyzing phospholipase C. J Biol Chem. 1991 Nov 25;266(33):22597–22602. [PubMed] [Google Scholar]
  8. Dominguez I., Diaz-Meco M. T., Municio M. M., Berra E., García de Herreros A., Cornet M. E., Sanz L., Moscat J. Evidence for a role of protein kinase C zeta subspecies in maturation of Xenopus laevis oocytes. Mol Cell Biol. 1992 Sep;12(9):3776–3783. doi: 10.1128/mcb.12.9.3776. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dominguez I., Marshall M. S., Gibbs J. B., García de Herreros A., Cornet M. E., Graziani G., Diaz-Meco M. T., Johansen T., McCormick F., Moscat J. Role of GTPase activating protein in mitogenic signalling through phosphatidylcholine-hydrolysing phospholipase C. EMBO J. 1991 Nov;10(11):3215–3220. doi: 10.1002/j.1460-2075.1991.tb04884.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Downward J., Graves J. D., Warne P. H., Rayter S., Cantrell D. A. Stimulation of p21ras upon T-cell activation. Nature. 1990 Aug 23;346(6286):719–723. doi: 10.1038/346719a0. [DOI] [PubMed] [Google Scholar]
  11. Dressler K. A., Mathias S., Kolesnick R. N. Tumor necrosis factor-alpha activates the sphingomyelin signal transduction pathway in a cell-free system. Science. 1992 Mar 27;255(5052):1715–1718. doi: 10.1126/science.1313189. [DOI] [PubMed] [Google Scholar]
  12. Duh E. J., Maury W. J., Folks T. M., Fauci A. S., Rabson A. B. Tumor necrosis factor alpha activates human immunodeficiency virus type 1 through induction of nuclear factor binding to the NF-kappa B sites in the long terminal repeat. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5974–5978. doi: 10.1073/pnas.86.15.5974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fauci A. S. The human immunodeficiency virus: infectivity and mechanisms of pathogenesis. Science. 1988 Feb 5;239(4840):617–622. doi: 10.1126/science.3277274. [DOI] [PubMed] [Google Scholar]
  14. García de Herreros A., Dominguez I., Diaz-Meco M. T., Graziani G., Cornett M. E., Guddal P. H., Johansen T., Moscat J. Requirement of phospholipase C-catalyzed hydrolysis of phosphatidylcholine for maturation of Xenopus laevis oocytes in response to insulin and ras p21. J Biol Chem. 1991 Apr 15;266(11):6825–6829. [PubMed] [Google Scholar]
  15. Ghosh S., Baltimore D. Activation in vitro of NF-kappa B by phosphorylation of its inhibitor I kappa B. Nature. 1990 Apr 12;344(6267):678–682. doi: 10.1038/344678a0. [DOI] [PubMed] [Google Scholar]
  16. Gilmore T. D. NF-kappa B, KBF1, dorsal, and related matters. Cell. 1990 Sep 7;62(5):841–843. doi: 10.1016/0092-8674(90)90257-f. [DOI] [PubMed] [Google Scholar]
  17. Hazan U., Thomas D., Alcami J., Bachelerie F., Israel N., Yssel H., Virelizier J. L., Arenzana-Seisdedos F. Stimulation of a human T-cell clone with anti-CD3 or tumor necrosis factor induces NF-kappa B translocation but not human immunodeficiency virus 1 enhancer-dependent transcription. Proc Natl Acad Sci U S A. 1990 Oct;87(20):7861–7865. doi: 10.1073/pnas.87.20.7861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hohmann H. P., Remy R., Aigner L., Brockhaus M., van Loon A. P. Protein kinases negatively affect nuclear factor-kappa B activation by tumor necrosis factor-alpha at two different stages in promyelocytic HL60 cells. J Biol Chem. 1992 Jan 25;267(3):2065–2072. [PubMed] [Google Scholar]
  19. Kao K. R., Hopwood N. D. Expression of a mRNA related to c-rel and dorsal in early Xenopus laevis embryos. Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2697–2701. doi: 10.1073/pnas.88.7.2697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Korn L. J., Siebel C. W., McCormick F., Roth R. A. Ras p21 as a potential mediator of insulin action in Xenopus oocytes. Science. 1987 May 15;236(4803):840–843. doi: 10.1126/science.3554510. [DOI] [PubMed] [Google Scholar]
  21. Larrodera P., Cornet M. E., Diaz-Meco M. T., Lopez-Barahona M., Diaz-Laviada I., Guddal P. H., Johansen T., Moscat J. Phospholipase C-mediated hydrolysis of phosphatidylcholine is an important step in PDGF-stimulated DNA synthesis. Cell. 1990 Jun 15;61(6):1113–1120. doi: 10.1016/0092-8674(90)90074-o. [DOI] [PubMed] [Google Scholar]
  22. Lenardo M. J., Baltimore D. NF-kappa B: a pleiotropic mediator of inducible and tissue-specific gene control. Cell. 1989 Jul 28;58(2):227–229. doi: 10.1016/0092-8674(89)90833-7. [DOI] [PubMed] [Google Scholar]
  23. Lopez-Barahona M., Kaplan P. L., Cornet M. E., Diaz-Meco M. T., Larrodera P., Diaz-Laviada I., Municio A. M., Moscat J. Kinetic evidence of a rapid activation of phosphatidylcholine hydrolysis by Ki-ras oncogene. Possible involvement in late steps of the mitogenic cascade. J Biol Chem. 1990 Jun 5;265(16):9022–9026. [PubMed] [Google Scholar]
  24. Meichle A., Schütze S., Hensel G., Brunsing D., Krönke M. Protein kinase C-independent activation of nuclear factor kappa B by tumor necrosis factor. J Biol Chem. 1990 May 15;265(14):8339–8343. [PubMed] [Google Scholar]
  25. Meyer R., Hatada E. N., Hohmann H. P., Haiker M., Bartsch C., Röthlisberger U., Lahm H. W., Schlaeger E. J., van Loon A. P., Scheidereit C. Cloning of the DNA-binding subunit of human nuclear factor kappa B: the level of its mRNA is strongly regulated by phorbol ester or tumor necrosis factor alpha. Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):966–970. doi: 10.1073/pnas.88.3.966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nabel G., Baltimore D. An inducible transcription factor activates expression of human immunodeficiency virus in T cells. Nature. 1987 Apr 16;326(6114):711–713. doi: 10.1038/326711a0. [DOI] [PubMed] [Google Scholar]
  27. Nishizuka Y. The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature. 1988 Aug 25;334(6184):661–665. doi: 10.1038/334661a0. [DOI] [PubMed] [Google Scholar]
  28. Nolan G. P., Ghosh S., Liou H. C., Tempst P., Baltimore D. DNA binding and I kappa B inhibition of the cloned p65 subunit of NF-kappa B, a rel-related polypeptide. Cell. 1991 Mar 8;64(5):961–969. doi: 10.1016/0092-8674(91)90320-x. [DOI] [PubMed] [Google Scholar]
  29. Ono Y., Fujii T., Ogita K., Kikkawa U., Igarashi K., Nishizuka Y. Protein kinase C zeta subspecies from rat brain: its structure, expression, and properties. Proc Natl Acad Sci U S A. 1989 May;86(9):3099–3103. doi: 10.1073/pnas.86.9.3099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Osada S., Mizuno K., Saido T. C., Akita Y., Suzuki K., Kuroki T., Ohno S. A phorbol ester receptor/protein kinase, nPKC eta, a new member of the protein kinase C family predominantly expressed in lung and skin. J Biol Chem. 1990 Dec 25;265(36):22434–22440. [PubMed] [Google Scholar]
  31. Ruben S. M., Dillon P. J., Schreck R., Henkel T., Chen C. H., Maher M., Baeuerle P. A., Rosen C. A. Isolation of a rel-related human cDNA that potentially encodes the 65-kD subunit of NF-kappa B. Science. 1991 Mar 22;251(5000):1490–1493. doi: 10.1126/science.2006423. [DOI] [PubMed] [Google Scholar]
  32. Ruberti I., Beccari E., Bianchi E., Carnevali F. Large scale isolation of nuclei from oocytes of Xenopus laevis. Anal Biochem. 1989 Jul;180(1):177–180. doi: 10.1016/0003-2697(89)90108-5. [DOI] [PubMed] [Google Scholar]
  33. Schmitz M. L., Baeuerle P. A. The p65 subunit is responsible for the strong transcription activating potential of NF-kappa B. EMBO J. 1991 Dec;10(12):3805–3817. doi: 10.1002/j.1460-2075.1991.tb04950.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Schütze S., Berkovic D., Tomsing O., Unger C., Krönke M. Tumor necrosis factor induces rapid production of 1'2'diacylglycerol by a phosphatidylcholine-specific phospholipase C. J Exp Med. 1991 Nov 1;174(5):975–988. doi: 10.1084/jem.174.5.975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sen R., Baltimore D. Multiple nuclear factors interact with the immunoglobulin enhancer sequences. Cell. 1986 Aug 29;46(5):705–716. doi: 10.1016/0092-8674(86)90346-6. [DOI] [PubMed] [Google Scholar]
  36. Shirakawa F., Mizel S. B. In vitro activation and nuclear translocation of NF-kappa B catalyzed by cyclic AMP-dependent protein kinase and protein kinase C. Mol Cell Biol. 1989 Jun;9(6):2424–2430. doi: 10.1128/mcb.9.6.2424. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES