105
Views
196
CrossRef citations to date
0
Altmetric
Gene Expression

Autophosphorylation in the Activation Loop Is Required for Full Kinase Activity In Vivo of Human and Yeast Eukaryotic Initiation Factor 2α Kinases PKR and GCN2

, , , , , , , , & show all
Pages 2282-2297 | Received 24 Oct 1997, Accepted 22 Dec 1997, Published online: 27 Mar 2023

REFERENCES

  • Adams, J. A., M. L. McGlone, R. Gibson, and S. S. Taylor 1995. Phosphorylation modulates catalytic function and regulation in the cAMP-dependent protein kinase. Biochemistry 34: 2447–2454.
  • Barber, G. N., M. Wambach, M. L. Wong, T. E. Dever, A. G. Hinnebusch, and M. G. Katze 1993. Translational regulation by the interferon-induced double-stranded RNA-activated 68-kDa protein kinase. Proc. Natl. Acad. Sci. USA 90: 4621–4625.
  • Bischoff, J. R., and C. E. Samuel 1985. Mechanism of interferon action: the interferon-induced phosphoprotein P1 possesses a double-stranded RNA-dependent ATP-binding site. J. Biol. Chem. 260: 8237–8239.
  • Boyle, W. J., P. van der Geer, and T. Hunter 1991. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 201: 110–149.
  • Brill, J. A., E. A. Elion, and G. R. Fink 1994. A role for autophosphorylation revealed by activated alleles of FUS3, the yeast MAP kinase homolog. Mol. Biol. Cell. 5: 297–312.
  • Bushman, J. L., M. Foiani, A. M. Cigan, C. J. Paddon, and A. G. Hinnebusch 1993. Guanine nucleotide exchange factor for eukaryotic translation initiation factor 2 in Saccharomyces cerevisiae: interactions between the essential subunits GCD2, GCD6, and GCD7 and the regulatory subunit GCN3. Mol. Cell. Biol. 13: 4618–4631.
  • Canagarajah, B. J., A. Khokhlatchev, M. H. Cobb, and E. J. Goldsmith 1997. Activation mechanism of the MAP kinase ERK2 by dual phosphorylation. Cell 90: 859–869.
  • Chiu, Y. S., and M. Tao 1978. Autophosphorylation of rabbit skeletal muscle cyclic AMP-dependent protein kinase I catalytic subunit. J. Biol. Chem. 253: 7145–7148.
  • Chong, K. L., L. Feng, K. Schappert, E. Meurs, T. F. Donahue, J. D. Friesen, A. G. Hovanessian, and B. R. G. Williams 1992. Human p68 kinase exhibits growth suppression in yeast and homology to the translational regulator GCN2. EMBO J. 11: 1553–1562.
  • Cobb, M. H., and E. J. Goldsmith 1995. How MAP kinases are regulated. J. Biol. Chem. 270: 1483–1486.
  • Cosentino, G. P., S. Venkatesan, F. C. Serluca, S. R. Green, M. B. Mathews, and N. Sonenberg 1995. Double-stranded-RNA-dependent protein kinase and TAR RNA-binding protein form homo- and heterodimers in vivo. Proc. Natl. Acad. Sci. USA 92: 9445–9449.
  • De Bondt, H. L., J. Rosenblatt, J. Jancarik, H. D. Jones, D. O. Morgan, and S. H. Kim 1993. Crystal structure of cyclin-dependent kinase 2. Nature 363: 595–602.
  • Dever, T. E., J. J. Chen, G. N. Barber, A. M. Cigan, L. Feng, T. F. Donahue, I. M. London, M. G. Katze, and A. G. Hinnebusch 1993. Mammalian eukaryotic initiation factor 2α kinases functionally substitute for GCN2 in the GCN4 translational control mechanism of yeast. Proc. Natl. Acad. Sci. USA 90: 4616–4620.
  • Dever, T. E., L. Feng, R. C. Wek, A. M. Cigan, T. D. Donahue, and A. G. Hinnebusch 1992. Phosphorylation of initiation factor 2α by protein kinase GCN2 mediates gene-specific translational control of GCN4 in yeast. Cell 68: 585–596.
  • Diallinas, G., and G. Thireos 1994. Genetic and biochemical evidence for yeast GCN2 protein kinase polymerization. Gene 143: 21–27.
  • Dong, J., X. Zhang, A. G. Hinnebusch, and J. Qin. Unpublished observations.
  • Galabru, J., and A. Hovanessian 1987. Autophosphorylation of the protein kinase dependent on double-stranded RNA. J. Biol. Chem. 262: 15538–15544.
  • Galabru, J., M. G. Katze, N. Robert, and A. G. Hovanessian 1989. The binding of double-stranded RNA and adenovirus VAI RNA to the interferon-induced protein kinase. Eur. J. Biochem. 178: 581–589.
  • Green, S. R., and M. B. Mathews 1992. Two RNA-binding motifs in double-stranded RNA-activated protein kinase DAI. Genes Dev. 6: 2478–2490.
  • Hanks, S. K., and T. Hunter 1995. The eukaryotic protein kinase superfamily The protein kinase facts book. In: Hardie, G., and S. Hanks7–47Academic Press, Inc., San Diego, Calif.
  • Hinnebusch, A. G. 1996. Translational control of GCN4: gene-specific regulation by phosphorylation of eIF2 Translational control. In: Hershey, J. W. B., M. B. Mathews, and N. Sonenberg199–244Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
  • Johnson, L. N., M. E. M. Noble, and D. J. Owen 1996. Active and inactive protein kinases: structural basis for regulation. Cell 85: 149–158.
  • Kamps, M. P. 1991. Determination of phosphoamino acid composition by acid hydrolysis of protein blotted to immobilon. Methods Enzymol. 201: 21–27.
  • Knighton, D. R., J. Zheng, L. F. Ten Eyck, N. H. Xuong, S. S. Taylor, and J. M. Sowadski 1991. Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253: 407–414.
  • Koerner, T. J., J. E. Hill, A. M. Myers, and A. Tzagoloff 1991. High-expression vectors with multiple cloning sites for construction of trpE fusion genes: pATH vectors. Methods Enzymol. 194: 477–490.
  • Koromilas, A. E., S. Roy, G. N. Barber, M. G. Katze, and N. Sonenberg 1992. Malignant transformation by a mutant of the IFN-inducible dsRNA-dependent protein kinase. Science 257: 1685–1689.
  • Kostura, M., and M. B. Mathews 1989. Purification and activation of the double-stranded RNA-dependent eIF-2 kinase DAI. Mol. Cell. Biol. 9: 1576–1586.
  • Laemmli, U. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685.
  • Langland, J. O., and B. L. Jacobs 1992. Cytosolic double-stranded RNA-dependent protein kinase is likely a dimer of partially phosphorylated Mr=66,000 subunits. J. Biol. Chem. 267: 10729–10736.
  • Madhusudan, E., A. T., N.-H. Xuong, J. A. Adams, L. F. ten Eyck, S. S. Taylor, and J. M. Sowadski 1994. cAMP-dependent protein kinase: crystallographic insights into substrate recognition and phosphotransfer. Protein Sci. 3: 176–187.
  • Mathews, M. B. 1993. Viral evasion of cellular defense mechanisms: regulation of the protein kinase DAI by RNA effectors. Semin. Virol. 4: 247–257.
  • Meurs, E. F., J. Galabru, G. N. Barber, M. G. Katze, and A. G. Hovanessian 1993. Tumor suppressor function of the interferon-induced double-stranded RNA-activated protein kinase. Proc. Natl. Acad. Sci. USA 90: 232–236.
  • Parent, S. A., C. M. Fenimore, and K. A. Bostian 1985. Vector systems for the expression, analysis and cloning of DNA sequences in S. cerevisiae. Yeast 1: 83–138.
  • Patel, R. C., P. Stanton, N. M. J. McMillan, B. R. G. Williams, and G. C. Sen 1995. The interferon-inducible double-stranded RNA-activated protein kinase self-associates in vitro and in vivo. Proc. Natl. Acad. Sci. USA 92: 8283–8287.
  • Patel, R. C., P. Stanton, and G. C. Sen 1996. Specific mutations near the amino terminus of double-stranded RNA-dependent protein kinase (PKR) differentially affect its double-stranded RNA binding and dimerization properties. J. Biol. Chem. 271: 25657–25663.
  • Pavitt, G. D., W. Yang, and A. G. Hinnebusch 1996. Identification of amino acids in homologous segments of 3 subunits of the guanine nucleotide exchange factor eIF2B required for translational regulation by phosphorylation of eukaryotic translation initiation factor 2. Mol. Cell. Biol. 17: 1298–1313.
  • Qin, J., D. Fenyo, Y. Zhao, W. W. Hall, D. M. Chao, C. J. Wilson, R. A. Young, and B. T. Chait 1997. A strategy for rapid, high-confidence protein identification. Anal. Chem. 69: 3995–4001.
  • Ramirez, M., R. C. Wek, C. R. Vazquez de Aldana, B. M. Jackson, B. Freeman, and A. G. Hinnebusch 1992. Mutations activating the yeast eIF-2α kinase GCN2: isolation of alleles altering the domain related to histidyl-tRNA synthetases. Mol. Cell. Biol. 12: 5801–5815.
  • Romano, P. R., S. R. Green, G. N. Barber, M. B. Mathews, and A. G. Hinnebusch 1995. Structural requirements for double-stranded RNA binding, dimerization, and activation of the human eIF-2α kinase DAI in Saccharomyces cerevisiae. Mol. Cell. Biol. 15: 365–378.
  • Sambrook, J., E. F. Fritsch, and T. Maniatis 1989. Molecular cloning: a laboratory manual2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
  • Santoyo, J., J. Alcalde, R. Mendez, D. Pulido, and C. de Haro 1997. Cloning and characterization of a cDNA encoding a protein synthesis initiation factor-2α (eIF-2α) kinase from Drosophila melanogaster. J. Biol. Chem. 272: 12544–12550.
  • Shoji, S., K. Titani, J. Demaille, and E. H. Fischer 1979. Sequences of two phosphorylated sites in the catalytic subunit of bovine cardiac muscle adenosine 3′:5′-monophosphate-dependent protein kinase. J. Biol. Chem. 254: 6211–6214.
  • Taylor, D. R., S. B. Lee, P. R. Romano, D. R. Marshak, A. G. Hinnebusch, M. Esteban, and M. B. Mathews 1996. Autophosphorylation sites participate in the activation of the double-stranded RNA-activated protein kinase PKR. Mol. Cell. Biol. 16: 6295–6302.
  • Taylor, D. R., and M. B. Mathews. Unpublished observations.
  • Thomis, D. C., and C. E. Samuel 1992. Mechanism of interferon action: autoregulation of RNA-dependent P1/eIF-2α protein kinase (PKR) expression in transfected mammalian cells. Proc. Natl. Acad. Sci. USA 89: 10837–10841.
  • Thomis, D. C., and C. E. Samuel 1995. Mechanism of interferon action: characterization of the intermolecular autophosphorylation of PKR, the interferon-inducible, RNA-dependent protein kinase. J. Virol. 69: 5195–5198.
  • Wek, R. C., M. Ramirez, B. M. Jackson, and A. G. Hinnebusch 1990. Identification of positive-acting domains in GCN2 protein kinase required for translational activation of GCN4 expression. Mol. Cell. Biol. 10: 2820–2831.
  • Wek, S. A., S. Zhu, and R. C. Wek 1995. The histidyl-tRNA synthetase-related sequence in the eIF-2α protein kinase GCN2 interacts with tRNA and is required for activation in response to starvation for different amino acids. Mol. Cell. Biol. 15: 4497–4506.
  • Wu, S., and R. J. Kaufman 1996. Double-stranded (ds) RNA binding and not dimerization correlates with the activation of the dsRNA-dependent protein kinase (PKR). J. Biol. Chem. 271: 1756–1763.
  • Wu, S., and R. J. Kaufman 1997. A model for the double-stranded RNA (dsRNA)-dependent dimerization and activation of the dsRNA-activated protein kinase PKR. J. Biol. Chem. 272: 1291–1296.
  • Yon, J., and M. Fried 1988. Precise gene fusion by PCR. Nucleic Acids Res. 17: 4895.
  • Zhang, F., A. Strand, D. Robbins, M. H. Cobb, and E. J. Goldsmith 1994. Atomic structure of the MAP kinase ERK2 at 2.3 A resolution. Nature 367: 704–710.
  • Zhang, X., C. Herring, P. R. Romano, J. Szczepanowska, H. Brzeska, A. G. Hinnebusch, and J. Qin. Submitted for publication.
  • Zhu, S., P. R. Romano, and R. C. Wek 1997. Ribosome targeting of PKR is mediated by two double-stranded RNA-binding domains and facilitates in vivo phosphorylation of eukaryotic initiation factor-2. J. Biol. Chem. 272: 14434–14441.
  • Zhu, S., A. Y. Sobolev, and R. C. Wek 1996. Histidyl-tRNA synthetase-related sequences in GCN2 protein kinase regulate in vitro phosphorylation of eIF-2. J. Biol. Chem. 271: 24989–24994.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.