Autophosphorylation sites participate in the activation of the double- stranded-RNA-activated protein kinase PKR

Molecular and Cellular Biology

Volumn 16, Issue 11, 1996, Pages 6295-6302

  Taylor, Deborah R ^a,b   Lee, Sean Bong ^c,f   Romano, Patrick R ^d   Marshak, Daniel R ^a,g   Hinnebusch, Alan G ^d   Esteban, Mariano ^c,h   Mathews, Michael B ^a,e  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c SUNY DOWNSTATE MEDICAL CENTER   (United States)

^d EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^e RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^f MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

^g OSIRIS THERAPEUTICS INC   (United States)

^h CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; PROTEIN KINASE;

AMINO ACID SEQUENCE; ARTICLE; AUTOPHOSPHORYLATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; NONHUMAN; PRIORITY JOURNAL; RNA BINDING; SACCHAROMYCES CEREVISIAE;

MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 10244257563     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.16.11.6295     Document Type: Article

References (71)

1. Ausubel, F. M., R. Brent, R. E. Kingsion, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Strahl. 1991. Current protocols in molecular biology. John Wiley & Sons, Inc., New York.
2. Barber, G. N., S. Edelhoff, M. G. Katze, and C. M. Disteche. 1993. Chromosomal assignment of the interferon-inducible double-stranded RNA-dependent protein kinase (PRKR) to human chromosome 2p21-p22 and mouse chromosome 17 E2. Genomics 16:765-767.
3. Berry, M. J., G. S. Knutson, S. R. Lasky, S. M. Munemitsu, and C. E. Samuel. 1985. Purification and substrate specificities of the double-stranded RNA-dependent protein kinase from untreated and interferon-treated mouse fibroblasts. J. Biol. Chem. 260:11240-11247.
4. 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.
5. Brand, S. R., R. Kobayashi, and M. B. Mathews. The Tat protein of human immunodeficiency virus type 1 is a substrate and inhibitor of the interferon-induced, virus-activated protein kinase, PKR. Submitted for publication.
6. Brasier, A. R., J. E. Tate, and J. F. Habener. 1989. Optimized use of the firefly luciferase assay as a reporter gene in mammalian cell lines. BioTechniques 7:1116-1122.
7. Bycroft, M., S. Grünert, A. G. Murzin, M. Proctor, and D. St Johnston. 1995. NMR solution structure of a dsRNA binding domain from Drosophila staufen protein reveals homology to the N-terminal domain of ribosomal protein S5. EMBO J. 14:3563-3571.
8. Chen, J.-J., M. S. Throop, L. Gehrke, I. Kuo, J. K. Pal, M. Brodsky, and I. M. London. 1991. Cloning of the cDNA of the home-regulated eukaryotic initiation factor 2a (eIF-2a) kinase of rabbit reticulocytes: homology to yeast GCN2 protein kinase and human double-stranded-RNA-dependent eIF-2a kinase. Proc. Natl. Acad. Sci. USA 88:7729-7733.
9. 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.
10. Clemens, M. J. 1996. Protein kinases that phosphorylate eIF2 and eIF2B, and their role in eukaryotic cell translational control, p. 139-172. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
11. Dever, T. E., 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 2a kinases functionally substitute for GCN2 protein kinase in the GCN4 translational control mechanism of yeast. Proc. Natl. Acad. Sci. USA 90:4616-4620.
12. Dever, T. E., L. Feng, R. C. Wek, A. M. Cigan, T. F. Donahue, and A. G. Hinnebusch. 1992. Phosphorylation of initiation factor 2a by protein kinase GCN2 mediates gene-specific translational control of GCN4 in yeast. Cell 68:585-596.
13. Ellis, L., E. Clauser, D. O. Morgan, M. Edery, R. A. Roth, and W. J. Rutter. 1986. Replacement of insulin receptor tyrosine residues 1162 and 1163 compromises insulin-stimulated kinase activity and uptake of 2-deoxyglucose. Cell 45:721-732.
14. Farrell, P. J., K. Balkow, T. Hunt, R. J. Jackson, and H. Trachsel. 1977. Phosphorylation of initiation factor cIF-2 and the control of reticulocyte protein synthesis. Cell 11:187-200.
15. Feng, G.-S., K. Chong, A. Kumar, and B. R. G. Williams. 1992. Identification of double-stranded RNA-binding domains in the interferon-induced double-stranded RNA-activated p68 kinase. Proc. Natl. Acad. Sci. USA 89:5447-5451.
16. Flint, A. J., R. D. Paladini, and D. E. J. Koshland. 1990. Autophosphorylation of protein kinase C at three separated regions of its primary sequence. Science 249:408-411.
17. Galabru, J., and A. Hovanessian. 1985. Two interferon-induced proteins are involved in the protein kinase complex dependent on double-stranded RNA. Cell 43:685-694.
18. Galabru, J., and A. Hovanessian. 1987. Autophosphorylation of the protein kinase dependent on double-stranded RNA. J. Biol. Chem. 262:15538-15544.
19. Galabru, J., B. Krust, and A. G. Hovanessian. 1984. Interferon-mediated protein kinase activity in different fractions of mouse L-929 cells. J. Interferon Res. 4:469-480.
20. Green, S. R., L. Manche, and M. B. Mathews. 1995. Two functionally distinct RNA-binding motifs in the regulatory domain of the protein kinase DAI. Mol. Cell. Biol. 15:358-364.
21. Green, S. R., and M. B. Mathews. 1992. Two RNA binding motifs in the double-stranded RNA activated protein kinase, DAI. Genes Dev. 6:2478-2490.
22. Hanks, S. K., A. M. Quinn, and T. Hunter. 1988. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42-52.
23. Herrera, R., and O. M. Rosen. 1986. Autophosphorylation of the insulin receptor in vitro. J. Biol. Chem. 261:11980-1985.
24. Hinnebusch, A. G. 1990. Involvement of an initiation factor and protein phosphorylation in translational control of GCN4 mRNA. Trends Biochem. Sci. 15:148-152.
25. Hinnebusch, A. G. 1996. Translational control of GCN4: gene-specific regulation by phosphorylation of eIF2, p. 199-244. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
26. Katze, M. G. 1996. Translational control in cells infected with influenza virus and reovirus, p. 607-630. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
27. r protein kinase in a cell-free system. Mol. Cell. Biol. 11:5497-5505.
28. c-src transforming ability by mutation of its primary sites of tyrosine phosphorylation. Cell 49:65-73.
29. 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-dependnnt protein kinase. Science 257:1685-1689.
30. 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.
31. Kumar, A., J. Haque, J. Lacoste, J. Hiscott, and B. R. G. Williams. 1994. Double-stranded RNA-dependent protein kinase activates transcription factor NF-κB by phosphorylating IκB. Proc. Natl. Acad. Sci. USA 91:6288-6292.
32. Laemmli, E. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
33. Lasky, S. R., B. L. Jacobs, and C. E. Samuel. 1982. Characterization of the sites of phosphorylation in the interferon-induced phosphoprotein P1 from mouse fibroblasts: evidence for two forms of P1. J. Biol. Chem. 257:11087-11093.
34. Laurent, A. G., B. Krust, J. Galabru, J. Svab, and A. G. Hovanessian. 1985. Monoclonal antibodies to an interferon-induced Mr 68,000 protein and their use for the detection of double-stranded RNA-dependent protein kinase in human cells. Proc. Natl. Acad. Sci. USA 82:4341-4345.
35. Lee, S. B., and M. Esteban. 1994. The interferon-induced double-stranded RNA-activated protein kinase induces apoptosis. Virology 199:491-496.
36. Lee, S. B., S. R. Green, M. B. Mathews, and M. Esteban. 1994. Activation of the double-stranded RNA-activated human protein kinase in vivo in the absence of its dsRNA binding domain. Proc. Natl. Acad. Sci. USA 91:10551-10555.
37. Lee, S. B., Z. Melkova, W. Yan, B. R. G. Williams, A. G. Hovanessian, and M. Esteban. 1993. The interferon-induced double-stranded RNA-activated human p68 protein kinase potently inhibits protein synthesis in cultured cells. Virology 192:380-385.
38. Manche, L., S. R. Green, C. Schmedt, and M. B. Mathews. 1992. Interactions between double-stranded RNA regulators and the protein kinase DAI. Mol. Cell. Biol. 12:5238-5248.
39. 1. Virology 164: 106-113.
40. Mathews, M. B. 1996. Interactions between viruses and the cellular machinery for protein synthesis. p. 505-548. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
41. Mathews, M. B., and T. Shenk. 1991. Adenovirus virus-associated RNA and translational control. J. Virol. 65:5657-5662.
42. McMillan, N. A. J., R. F. Chun, D. P. Siderovski, J. Galabru, W. M. Toone, C. E. Samuel, T. W. Mak, A. G. Hovanessian, K. Jeang, and B. R. G. Williams. 1995. HIV-1 Tat directly interacts with the interferon-induced, double-stranded RNA-dependent kinase, PKR. Virology 213:413-424.
43. Merrick, W. C., and J. W. B. Hershey. 1996. The pathway and mechanism of eukaryotic protein synthesis, p. 31-69. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
44. Meurs, E., K. Chong, J. Galabru, N. S. B. Thomas, I. M. Kerr, B. R. G. Williams, and A. G. Hovanessian. 1990. Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon. Cell 62:379-390.
45. 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.
46. Mochly-Rosen, D., and D. E. J. Koshland. 1987. Domain structure and phosphorylation of protein kinase C. J. Biol. Chem. 262:2291-2297.
47. Mohammadi, M., I. Dikic, A. Sorokin, W. H. Burgess, M. Jaye, and J. Schlessinger. 1996. Identification of six novel autophosphorylation sites on fibroblast growth factor receptor 1 and elucidation of their importance in receptor activation and signal transduction. Mol. Cell. Biol. 16:977-989.
48. Mundschau, L. J., and D. V. Faller. 1995. Platelet-derived growth factor signal transduction through the interferon-inducible kinase PKR. Immediate early gene induction. J. Biol. Chem. 270:3100-3106.
49. Offermann, M. K., J. Zimring, K. H. Mellits M. K. Hagan, R. Shaw, R. M. Medford, M. B. Mathews, S. Goodbourn, and R. Jagus. 1995. Activation of the double-stranded-RNA-activated protein kinase and induction of vascular cell adhesion molecule-1 by poly(I) X poly(C) in endothelial cells. Eur. J. Biochem. 232:28-36.
50. Patel, R. C., and G. C. Sen. 1992. Identification of the double-stranded RNA-binding domain of the human interferon-inducible protein kinase. J. Biol. Chem. 267:7671-7676.
51. Petryshyn, R., J.-J. Chen, and I. M. London. 1984. Growth-related expression of a double-stranded RNA-dependent protein kinase in 3T3 cells. J. Biol. Chem. 259:14736-14742.
52. c-src. Cell 49:75-82.
53. Proud, C. G. 1995. PKR: a new name and new roles. Trends Biochem. Sci. 20:241-246.
54. Proud, C. G., D. R. Colthurst, S. Ferrari, and L. A. Pinna. 1990. The substrate specificity of protein kinases which phosphorylate the α subunit of eukaryotic initiation factor 2. Eur. J. Biochem. 195:771-779.
55. 1 and is phosphorylated by the double-stranded RNA dependent protein kinase. J. Biol. Chem. 264:20632-20637.
56. Rodriguez, J. F., D. Rodriguez, J. Rodriguez, E. B. McGowan, and M. Esteban. 1988. Expression of the firefly luciferase gene in vaccinia virus: a highly sensitive gene marker to follow virus dissemination in tissues of infected animals. Proc. Natl. Acad. Sci. USA 85:1667-1671.
57. Rodriguez, J. F., and G. L. Smith. 1990. Inducible gene expression from vaccinia virus vectors. Virology 177:239-250.
58. 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.
59. cdc2 kinase in G1 phase of the HeLa cell division cycle. J. Biol. Chem. 267:20317-20325.
60. Samuel, C. E. 1979. Mechanism of interferon action: phosphorylation of protein synthesis initiation factor eIF-2 in interferon-treated human cells by a ribosome-associated kinase processing site specificity similar to hemin-regulated rabbit reticulocyte kinase. Proc. Natl. Acad. Sci. USA 76:600-604.
61. Schägger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
62. Schneider, R. J. 1996. Adenovirus and vaccinia virus translational control, p. 575-605. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational conrol. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
63. St Johnston, D., N. H. Brown, J. G. Gall, and M. Jantsch. 1992. A conserved double-stranded RNA-binding domain. Proc. Natl. Acad. Sci. USA 89:10979-t0983.
64. 63a. Taylor, D. R., and M. B. Mathews. Unpublished data.
65. Thomis, D. C., J. P. Doohan, and C. E. Samuel. 1992. Mechanism of interferon action: cDNA structure, expression, and regulation of the interferon-induced, RNA-dependent P1/eIF-2a protein kinase from human cells. Virology 188:33-46.
66. Thomis, D. C., and C. E. Samuel. 1993. Mechanism of interferon action: evidence of intermolecular autophosphorylation and autoactivation of the interferon-induced, RNA-dependent protein kinase PKR. J. Virol. 67:7695-7700.
67. 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.
68. gag-fps shows a strict specificity for tyrosine residues. J. Biol. Chem. 261:328-333.
69. 32P-labeled phosphopeptides at picomole and subpicomole levels. Methods Enzymol. 201:186-199.
70. Yang, Y., F. L. Reis, J. Pavlovic, A. Aguzzi, R. Schafer, A. Kumar, B. R. G. Williams, M. Aguet, and C. Weissmann. 1995. Deficient signaling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO J. 14: 6095-6106.
71. Zoller, M. J., and M. Smith. 1984. Oligonucleotide-directed mutagenesis: a simple method using two oligonucleotide primers and a single-stranded DNA template. DNA 3:479-488.