Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Sep 13;91(19):9175–9179. doi: 10.1073/pnas.91.19.9175

The pleckstrin homology domain of Bruton tyrosine kinase interacts with protein kinase C.

L Yao 1, Y Kawakami 1, T Kawakami 1
PMCID: PMC44770  PMID: 7522330

Abstract

Bruton tyrosine kinase (EC 2.7.1.112) [Btk, encoded by Btk in mice and BTK in humans (formerly known as atk, BPK, or emb)], which is variously mutated in chromosome X-linked agammaglobulinemia patients and X-linked immunodeficient (xid) mice, has the pleckstrin homology (PH) domain at its amino terminus. The PH domain of Btk expressed as a bacterial fusion protein directly interacts with protein kinase C in mast cell lysates. Evidence was obtained that Btk is physically associated with protein kinase C in intact murine mast cells as well. Both Ca(2+)-dependent (alpha, beta I, and beta II) and Ca(2+)-independent protein kinase C isoforms (epsilon and zeta) in mast cells interact with the PH domain of Btk in vitro, and protein kinase C beta I is associated with Btk in vivo. Btk served as a substrate of protein kinase C, and its enzymatic activity was down-regulated by protein kinase C-mediated phosphorylation. Furthermore, depletion or inhibition of protein kinase C with pharmacological agents resulted in an enhancement of the tyrosine phosphorylation of Btk induced by mast cell activation.

Full text

PDF
9175

Images in this article

9176Image
on p.9176
9177Image
on p.9177
9177Image
on p.9177
9178Image
on p.9178

Selected References

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

  1. Altman A., Coggeshall K. M., Mustelin T. Molecular events mediating T cell activation. Adv Immunol. 1990;48:227–360. doi: 10.1016/s0065-2776(08)60756-7. [DOI] [PubMed] [Google Scholar]
  2. Arora N., Min K. U., Costa J. J., Rhim J. S., Metcalfe D. D. Immortalization of mouse bone marrow-derived mast cells with Ad12-SV40 virus. Int Arch Allergy Immunol. 1993;100(4):319–327. doi: 10.1159/000236432. [DOI] [PubMed] [Google Scholar]
  3. Beaven M. A., Metzger H. Signal transduction by Fc receptors: the Fc epsilon RI case. Immunol Today. 1993 May;14(5):222–226. doi: 10.1016/0167-5699(93)90167-j. [DOI] [PubMed] [Google Scholar]
  4. Birge R. B., Hanafusa H. Closing in on SH2 specificity. Science. 1993 Dec 3;262(5139):1522–1524. doi: 10.1126/science.7504323. [DOI] [PubMed] [Google Scholar]
  5. Cunha-Melo J. R., Gonzaga H. M., Ali H., Huang F. L., Huang K. P., Beaven M. A. Studies of protein kinase C in the rat basophilic leukemia (RBL-2H3) cell reveal that antigen-induced signals are not mimicked by the actions of phorbol myristate acetate and Ca2+ ionophore. J Immunol. 1989 Oct 15;143(8):2617–2625. [PubMed] [Google Scholar]
  6. Frorath B., Abney C. C., Berthold H., Scanarini M., Northemann W. Production of recombinant rat interleukin-6 in Escherichia coli using a novel highly efficient expression vector pGEX-3T. Biotechniques. 1992 Apr;12(4):558–563. [PubMed] [Google Scholar]
  7. Fukamachi H., Kawakami Y., Takei M., Ishizaka T., Ishizaka K., Kawakami T. Association of protein-tyrosine kinase with phospholipase C-gamma 1 in bone marrow-derived mouse mast cells. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9524–9528. doi: 10.1073/pnas.89.20.9524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fukamachi H., Takei M., Kawakami T. Activation of multiple protein kinases including a MAP kinase upon Fc epsilon RI cross-linking. Int Arch Allergy Immunol. 1993;102(1):15–25. doi: 10.1159/000236546. [DOI] [PubMed] [Google Scholar]
  9. Haslam R. J., Koide H. B., Hemmings B. A. Pleckstrin domain homology. Nature. 1993 May 27;363(6427):309–310. doi: 10.1038/363309b0. [DOI] [PubMed] [Google Scholar]
  10. Hunter T., Ling N., Cooper J. A. Protein kinase C phosphorylation of the EGF receptor at a threonine residue close to the cytoplasmic face of the plasma membrane. Nature. 1984 Oct 4;311(5985):480–483. doi: 10.1038/311480a0. [DOI] [PubMed] [Google Scholar]
  11. Hunter T., Sefton B. M. Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1311–1315. doi: 10.1073/pnas.77.3.1311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kawakami T., Inagaki N., Takei M., Fukamachi H., Coggeshall K. M., Ishizaka K., Ishizaka T. Tyrosine phosphorylation is required for mast cell activation by Fc epsilon RI cross-linking. J Immunol. 1992 Jun 1;148(11):3513–3519. [PubMed] [Google Scholar]
  13. Kawakami Y., Furue M., Kawakami T. Identification of fyn-encoded proteins in normal human blood cells. Oncogene. 1989 Mar;4(3):389–391. [PubMed] [Google Scholar]
  14. Kawakami Y., Yao L., Miura T., Tsukada S., Witte O. N., Kawakami T. Tyrosine phosphorylation and activation of Bruton tyrosine kinase upon Fc epsilon RI cross-linking. Mol Cell Biol. 1994 Aug;14(8):5108–5113. doi: 10.1128/mcb.14.8.5108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Koch C. A., Anderson D., Moran M. F., Ellis C., Pawson T. SH2 and SH3 domains: elements that control interactions of cytoplasmic signaling proteins. Science. 1991 May 3;252(5006):668–674. doi: 10.1126/science.1708916. [DOI] [PubMed] [Google Scholar]
  16. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  17. Liu F. T., Bohn J. W., Ferry E. L., Yamamoto H., Molinaro C. A., Sherman L. A., Klinman N. R., Katz D. H. Monoclonal dinitrophenyl-specific murine IgE antibody: preparation, isolation, and characterization. J Immunol. 1980 Jun;124(6):2728–2737. [PubMed] [Google Scholar]
  18. Mano H., Mano K., Tang B., Koehler M., Yi T., Gilbert D. J., Jenkins N. A., Copeland N. G., Ihle J. N. Expression of a novel form of Tec kinase in hematopoietic cells and mapping of the gene to chromosome 5 near Kit. Oncogene. 1993 Feb;8(2):417–424. [PubMed] [Google Scholar]
  19. Mayer B. J., Ren R., Clark K. L., Baltimore D. A putative modular domain present in diverse signaling proteins. Cell. 1993 May 21;73(4):629–630. doi: 10.1016/0092-8674(93)90244-k. [DOI] [PubMed] [Google Scholar]
  20. Musacchio A., Gibson T., Rice P., Thompson J., Saraste M. The PH domain: a common piece in the structural patchwork of signalling proteins. Trends Biochem Sci. 1993 Sep;18(9):343–348. doi: 10.1016/0968-0004(93)90071-t. [DOI] [PubMed] [Google Scholar]
  21. Nishizuka Y. Studies and perspectives of protein kinase C. Science. 1986 Jul 18;233(4761):305–312. doi: 10.1126/science.3014651. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Ozawa K., Szallasi Z., Kazanietz M. G., Blumberg P. M., Mischak H., Mushinski J. F., Beaven M. A. Ca(2+)-dependent and Ca(2+)-independent isozymes of protein kinase C mediate exocytosis in antigen-stimulated rat basophilic RBL-2H3 cells. Reconstitution of secretory responses with Ca2+ and purified isozymes in washed permeabilized cells. J Biol Chem. 1993 Jan 25;268(3):1749–1756. [PubMed] [Google Scholar]
  24. Pawson T., Gish G. D. SH2 and SH3 domains: from structure to function. Cell. 1992 Oct 30;71(3):359–362. doi: 10.1016/0092-8674(92)90504-6. [DOI] [PubMed] [Google Scholar]
  25. Rawlings D. J., Saffran D. C., Tsukada S., Largaespada D. A., Grimaldi J. C., Cohen L., Mohr R. N., Bazan J. F., Howard M., Copeland N. G. Mutation of unique region of Bruton's tyrosine kinase in immunodeficient XID mice. Science. 1993 Jul 16;261(5119):358–361. doi: 10.1126/science.8332901. [DOI] [PubMed] [Google Scholar]
  26. Ren R., Mayer B. J., Cicchetti P., Baltimore D. Identification of a ten-amino acid proline-rich SH3 binding site. Science. 1993 Feb 19;259(5098):1157–1161. doi: 10.1126/science.8438166. [DOI] [PubMed] [Google Scholar]
  27. Thomas J. D., Sideras P., Smith C. I., Vorechovský I., Chapman V., Paul W. E. Colocalization of X-linked agammaglobulinemia and X-linked immunodeficiency genes. Science. 1993 Jul 16;261(5119):355–358. doi: 10.1126/science.8332900. [DOI] [PubMed] [Google Scholar]
  28. Touhara K., Inglese J., Pitcher J. A., Shaw G., Lefkowitz R. J. Binding of G protein beta gamma-subunits to pleckstrin homology domains. J Biol Chem. 1994 Apr 8;269(14):10217–10220. [PubMed] [Google Scholar]
  29. Tsukada S., Saffran D. C., Rawlings D. J., Parolini O., Allen R. C., Klisak I., Sparkes R. S., Kubagawa H., Mohandas T., Quan S. Deficient expression of a B cell cytoplasmic tyrosine kinase in human X-linked agammaglobulinemia. Cell. 1993 Jan 29;72(2):279–290. doi: 10.1016/0092-8674(93)90667-f. [DOI] [PubMed] [Google Scholar]
  30. Tyers M., Rachubinski R. A., Stewart M. I., Varrichio A. M., Shorr R. G., Haslam R. J., Harley C. B. Molecular cloning and expression of the major protein kinase C substrate of platelets. Nature. 1988 Jun 2;333(6172):470–473. doi: 10.1038/333470a0. [DOI] [PubMed] [Google Scholar]
  31. Vetrie D., Vorechovský I., Sideras P., Holland J., Davies A., Flinter F., Hammarström L., Kinnon C., Levinsky R., Bobrow M. The gene involved in X-linked agammaglobulinaemia is a member of the src family of protein-tyrosine kinases. Nature. 1993 Jan 21;361(6409):226–233. doi: 10.1038/361226a0. [DOI] [PubMed] [Google Scholar]
  32. White J. R., Pluznik D. H., Ishizaka K., Ishizaka T. Antigen-induced increase in protein kinase C activity in plasma membrane of mast cells. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8193–8197. doi: 10.1073/pnas.82.23.8193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. White K. N., Metzger H. Translocation of protein kinase C in rat basophilic leukemic cells induced by phorbol ester or by aggregation of IgE receptors. J Immunol. 1988 Aug 1;141(3):942–947. [PubMed] [Google Scholar]
  34. Yamada N., Kawakami Y., Kimura H., Fukamachi H., Baier G., Altman A., Kato T., Inagaki Y., Kawakami T. Structure and expression of novel protein-tyrosine kinases, Emb and Emt, in hematopoietic cells. Biochem Biophys Res Commun. 1993 Apr 15;192(1):231–240. doi: 10.1006/bbrc.1993.1404. [DOI] [PubMed] [Google Scholar]
  35. Yu H., Chen J. K., Feng S., Dalgarno D. C., Brauer A. W., Schreiber S. L. Structural basis for the binding of proline-rich peptides to SH3 domains. Cell. 1994 Mar 11;76(5):933–945. doi: 10.1016/0092-8674(94)90367-0. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES