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. 2001 Mar 15;354(Pt 3):635–643. doi: 10.1042/0264-6021:3540635

Mitogen-stimulated TIS21 protein interacts with a protein-kinase-Calpha-binding protein rPICK1.

W J Lin 1, Y F Chang 1, W L Wang 1, C Y Huang 1
PMCID: PMC1221695  PMID: 11237868

Abstract

TIS21 is induced transiently by PMA and a number of extracellular stimuli. Yeast two-hybrid screening has identified three TIS21 interacting clones from a rat cDNA library [Lin, Gary, Yang, Clarke and Herschman (1996) J. Biol. Chem 271, 15034-15044]. The amino acid sequence deduced from clone 5A shows 96.9% identity with the murine PICK1, a protein kinase Calpha (PKCalpha)-binding protein postulated to act as an intracellular receptor for PKC. A fusion protein of glutathione S-transferase and rPICK1 associates with the TIS21 translated in vitro, suggesting a direct physical interaction between these two proteins. TIS21 and rPICK1 are co-immunoprecipitated from NIH 3T3 cells overexpressing these two proteins. This indicates that the interaction also occurs in mammalian cells. Deletion of the PDZ domain at the N-terminus of rPICK1 abolishes its interaction with TIS21. A putative carboxylate-binding loop required for PICK1 to bind PKCalpha [Staudinger, Lu and Olson (1997) J. Biol. Chem 272, 32019-32024] is within this deleted region. Our results suggest a potential competition between TIS21 and PKC for binding to PICK1. We show that recombinant TIS21 is phosphorylated by PKC in vitro. The catalytic activity of PKC towards TIS21 is significantly decreased in the presence of rPICK1, whereas phosphorylation of histone by PKC is not affected. rPICK1 seems to modulate the phosphorylation of TIS21 through specific interactions between these two proteins. TIS21 might have a role in PKC-mediated extracellular signal transduction through its interaction with rPICK1.

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Selected References

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  1. Bogdan J. A., Adams-Burton C., Pedicord D. L., Sukovich D. A., Benfield P. A., Corjay M. H., Stoltenborg J. K., Dicker I. B. Human carbon catabolite repressor protein (CCR4)-associative factor 1: cloning, expression and characterization of its interaction with the B-cell translocation protein BTG1. Biochem J. 1998 Dec 1;336(Pt 2):471–481. doi: 10.1042/bj3360471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bradbury A., Possenti R., Shooter E. M., Tirone F. Molecular cloning of PC3, a putatively secreted protein whose mRNA is induced by nerve growth factor and depolarization. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3353–3357. doi: 10.1073/pnas.88.8.3353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Coghlan V. M., Perrino B. A., Howard M., Langeberg L. K., Hicks J. B., Gallatin W. M., Scott J. D. Association of protein kinase A and protein phosphatase 2B with a common anchoring protein. Science. 1995 Jan 6;267(5194):108–111. doi: 10.1126/science.7528941. [DOI] [PubMed] [Google Scholar]
  4. Cohen N. A., Brenman J. E., Snyder S. H., Bredt D. S. Binding of the inward rectifier K+ channel Kir 2.3 to PSD-95 is regulated by protein kinase A phosphorylation. Neuron. 1996 Oct;17(4):759–767. doi: 10.1016/s0896-6273(00)80207-x. [DOI] [PubMed] [Google Scholar]
  5. Cortes U., Moyret-Lalle C., Falette N., Duriez C., Ghissassi F. E., Barnas C., Morel A. P., Hainaut P., Magaud J. P., Puisieux A. BTG gene expression in the p53-dependent and -independent cellular response to DNA damage. Mol Carcinog. 2000 Feb;27(2):57–64. [PubMed] [Google Scholar]
  6. Fanning A. S., Anderson J. M. PDZ domains: fundamental building blocks in the organization of protein complexes at the plasma membrane. J Clin Invest. 1999 Mar;103(6):767–772. doi: 10.1172/JCI6509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Faux M. C., Rollins E. N., Edwards A. S., Langeberg L. K., Newton A. C., Scott J. D. Mechanism of A-kinase-anchoring protein 79 (AKAP79) and protein kinase C interaction. Biochem J. 1999 Oct 15;343(Pt 2):443–452. [PMC free article] [PubMed] [Google Scholar]
  8. Faux M. C., Scott J. D. More on target with protein phosphorylation: conferring specificity by location. Trends Biochem Sci. 1996 Aug;21(8):312–315. [PubMed] [Google Scholar]
  9. Goodnight J. A., Mischak H., Kolch W., Mushinski J. F. Immunocytochemical localization of eight protein kinase C isozymes overexpressed in NIH 3T3 fibroblasts. Isoform-specific association with microfilaments, Golgi, endoplasmic reticulum, and nuclear and cell membranes. J Biol Chem. 1995 Apr 28;270(17):9991–10001. doi: 10.1074/jbc.270.17.9991. [DOI] [PubMed] [Google Scholar]
  10. Guardavaccaro D., Corrente G., Covone F., Micheli L., D'Agnano I., Starace G., Caruso M., Tirone F. Arrest of G(1)-S progression by the p53-inducible gene PC3 is Rb dependent and relies on the inhibition of cyclin D1 transcription. Mol Cell Biol. 2000 Mar;20(5):1797–1815. doi: 10.1128/mcb.20.5.1797-1815.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Guéhenneux F., Duret L., Callanan M. B., Bouhas R., Hayette S., Berthet C., Samarut C., Rimokh R., Birot A. M., Wang Q. Cloning of the mouse BTG3 gene and definition of a new gene family (the BTG family) involved in the negative control of the cell cycle. Leukemia. 1997 Mar;11(3):370–375. doi: 10.1038/sj.leu.2400599. [DOI] [PubMed] [Google Scholar]
  12. Hall R. A., Premont R. T., Chow C. W., Blitzer J. T., Pitcher J. A., Claing A., Stoffel R. H., Barak L. S., Shenolikar S., Weinman E. J. The beta2-adrenergic receptor interacts with the Na+/H+-exchanger regulatory factor to control Na+/H+ exchange. Nature. 1998 Apr 9;392(6676):626–630. doi: 10.1038/33458. [DOI] [PubMed] [Google Scholar]
  13. Henry M. F., Silver P. A. A novel methyltransferase (Hmt1p) modifies poly(A)+-RNA-binding proteins. Mol Cell Biol. 1996 Jul;16(7):3668–3678. doi: 10.1128/mcb.16.7.3668. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Herschman H. R., Kujubu D. A., Fletcher B. S., Ma Q., Varnum B. C., Gilbert R. S., Reddy S. T. The tis genes, primary response genes induced by growth factors and tumor promoters in 3T3 cells. Prog Nucleic Acid Res Mol Biol. 1994;47:113–148. doi: 10.1016/s0079-6603(08)60251-2. [DOI] [PubMed] [Google Scholar]
  15. Lim R. W., Varnum B. C., Herschman H. R. Cloning of tetradecanoyl phorbol ester-induced 'primary response' sequences and their expression in density-arrested Swiss 3T3 cells and a TPA non-proliferative variant. Oncogene. 1987;1(3):263–270. [PubMed] [Google Scholar]
  16. Lin W. J., Gary J. D., Yang M. C., Clarke S., Herschman H. R. The mammalian immediate-early TIS21 protein and the leukemia-associated BTG1 protein interact with a protein-arginine N-methyltransferase. J Biol Chem. 1996 Jun 21;271(25):15034–15044. doi: 10.1074/jbc.271.25.15034. [DOI] [PubMed] [Google Scholar]
  17. Mesner P. W., Epting C. L., Hegarty J. L., Green S. H. A timetable of events during programmed cell death induced by trophic factor withdrawal from neuronal PC12 cells. J Neurosci. 1995 Nov;15(11):7357–7366. doi: 10.1523/JNEUROSCI.15-11-07357.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mochly-Rosen D. Localization of protein kinases by anchoring proteins: a theme in signal transduction. Science. 1995 Apr 14;268(5208):247–251. doi: 10.1126/science.7716516. [DOI] [PubMed] [Google Scholar]
  19. Montagnoli A., Guardavaccaro D., Starace G., Tirone F. Overexpression of the nerve growth factor-inducible PC3 immediate early gene is associated with growth inhibition. Cell Growth Differ. 1996 Oct;7(10):1327–1336. [PubMed] [Google Scholar]
  20. Nishizuka Y. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science. 1992 Oct 23;258(5082):607–614. doi: 10.1126/science.1411571. [DOI] [PubMed] [Google Scholar]
  21. Rouault J. P., Falette N., Guéhenneux F., Guillot C., Rimokh R., Wang Q., Berthet C., Moyret-Lalle C., Savatier P., Pain B. Identification of BTG2, an antiproliferative p53-dependent component of the DNA damage cellular response pathway. Nat Genet. 1996 Dec;14(4):482–486. doi: 10.1038/ng1296-482. [DOI] [PubMed] [Google Scholar]
  22. Rouault J. P., Prévôt D., Berthet C., Birot A. M., Billaud M., Magaud J. P., Corbo L. Interaction of BTG1 and p53-regulated BTG2 gene products with mCaf1, the murine homolog of a component of the yeast CCR4 transcriptional regulatory complex. J Biol Chem. 1998 Aug 28;273(35):22563–22569. doi: 10.1074/jbc.273.35.22563. [DOI] [PubMed] [Google Scholar]
  23. Rouault J. P., Rimokh R., Tessa C., Paranhos G., Ffrench M., Duret L., Garoccio M., Germain D., Samarut J., Magaud J. P. BTG1, a member of a new family of antiproliferative genes. EMBO J. 1992 Apr;11(4):1663–1670. doi: 10.1002/j.1460-2075.1992.tb05213.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Saras J., Heldin C. H. PDZ domains bind carboxy-terminal sequences of target proteins. Trends Biochem Sci. 1996 Dec;21(12):455–458. doi: 10.1016/s0968-0004(96)30044-3. [DOI] [PubMed] [Google Scholar]
  25. Songyang Z., Fanning A. S., Fu C., Xu J., Marfatia S. M., Chishti A. H., Crompton A., Chan A. C., Anderson J. M., Cantley L. C. Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science. 1997 Jan 3;275(5296):73–77. doi: 10.1126/science.275.5296.73. [DOI] [PubMed] [Google Scholar]
  26. Staudinger J., Lu J., Olson E. N. Specific interaction of the PDZ domain protein PICK1 with the COOH terminus of protein kinase C-alpha. J Biol Chem. 1997 Dec 19;272(51):32019–32024. doi: 10.1074/jbc.272.51.32019. [DOI] [PubMed] [Google Scholar]
  27. Staudinger J., Zhou J., Burgess R., Elledge S. J., Olson E. N. PICK1: a perinuclear binding protein and substrate for protein kinase C isolated by the yeast two-hybrid system. J Cell Biol. 1995 Feb;128(3):263–271. doi: 10.1083/jcb.128.3.263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Torres R., Firestein B. L., Dong H., Staudinger J., Olson E. N., Huganir R. L., Bredt D. S., Gale N. W., Yancopoulos G. D. PDZ proteins bind, cluster, and synaptically colocalize with Eph receptors and their ephrin ligands. Neuron. 1998 Dec;21(6):1453–1463. doi: 10.1016/s0896-6273(00)80663-7. [DOI] [PubMed] [Google Scholar]
  29. Tsunoda S., Sierralta J., Sun Y., Bodner R., Suzuki E., Becker A., Socolich M., Zuker C. S. A multivalent PDZ-domain protein assembles signalling complexes in a G-protein-coupled cascade. Nature. 1997 Jul 17;388(6639):243–249. doi: 10.1038/40805. [DOI] [PubMed] [Google Scholar]
  30. Varnum B. C., Reddy S. T., Koski R. A., Herschman H. R. Synthesis, degradation, and subcellular localization of proteins encoded by the primary response genes TIS7/PC4 and TIS21/PC3. J Cell Physiol. 1994 Jan;158(1):205–213. doi: 10.1002/jcp.1041580125. [DOI] [PubMed] [Google Scholar]
  31. Wang S., Dibenedetto A. J., Pittman R. N. Genes induced in programmed cell death of neuronal PC12 cells and developing sympathetic neurons in vivo. Dev Biol. 1997 Aug 15;188(2):322–336. doi: 10.1006/dbio.1997.8655. [DOI] [PubMed] [Google Scholar]
  32. Xia J., Zhang X., Staudinger J., Huganir R. L. Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1. Neuron. 1999 Jan;22(1):179–187. doi: 10.1016/s0896-6273(00)80689-3. [DOI] [PubMed] [Google Scholar]
  33. Yoshida Y., Matsuda S., Ikematsu N., Kawamura-Tsuzuku J., Inazawa J., Umemori H., Yamamoto T. ANA, a novel member of Tob/BTG1 family, is expressed in the ventricular zone of the developing central nervous system. Oncogene. 1998 May;16(20):2687–2693. doi: 10.1038/sj.onc.1201805. [DOI] [PubMed] [Google Scholar]

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