Double-stranded RNA-independent dimerization of interferon-induced protein kinase PKR and inhibition of dimerization by the cellular P58(IPK) inhibitor

Molecular and Cellular Biology

Volumn 18, Issue 5, 1998, Pages 2431-2443

  Tan, Seng Lai ^a   Gale Jr , Michael J ^a   Katze, Michael G ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; INHIBITOR PROTEIN; INTERFERON; PROTEIN KINASE;

ARTICLE; DIMERIZATION; ENZYME ACTIVE SITE; ENZYME INDUCTION; ENZYME REGULATION; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; TRANSLATION REGULATION;

EID: 0031897318     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.18.5.2431     Document Type: Article

References (87)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Barber, G. N., R. Jagus, E. F. Meurs, A. G. Hovanessian, and M. G. Katze. 1995. Molecular mechanisms responsible for malignant transformation by regulatory and catalytic domain variants of the interferon-induced enzyme RNA-dependent protein kinase. J. Biol. Chem. 270:17423-17428.
3. Barber, G. N., S. Thompson, T. G. Lee, T. Strom, R. Jagus, A. Darveau, and M. G. Katze. 1994. The 58-kilodalton inhibitor of the interferon-induced double-stranded RNA-activated protein kinase is a tetratricopeptide repeat protein with oncogenic potential. Proc. Natl. Acad. Sci. USA 91:4278-4282.
4. Barber, G. N., J. Tomita, M. S. Garfinkel, E. F. Meurs, A. G. Hovanessian, and M. G. Katze. 1992. Detection of protein kinase homologues and viral RNA-binding domains utilizing polyclonal antiserum prepared against a baculovirus-expressed ds RNA-activated 68,000-Da protein kinase. Virology 191:670-679.
5. Barber, G. N., J. Tomita, A. G. Hovanessian, E. F. Meurs, and M. G. Katze. 1991. Functional expression and characterization of the interferon-induced double-stranded RNA activated P68 protein kinase from Escherichia coli. Biochemistry 30:10356-10361.
6. Barber, G. N., M. Wambach, S. Thompson, R. Jagus, and M. G. Katze. 1995. Mutants of the RNA-dependent protein kinase (PKR) lacking double-stranded RNA binding domain I can act as transdominant inhibitors and induce malignant transformation. Mol. Cell. Biol. 15:3138-3146.
7. 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.
8. Beutner, G., A. Ruck, B. Riede, W. Weite, and D. Brdiczka. 1996. Complexes between kinases, mitochondrial porin and adenylate translocator in rat brain resemble the permeability transition pore. FEBS Lett. 396:189-195.
9. Boldyreff, B., U. Mietens, and O. G. Issinger. 1996. Structure of protein kinase CK2: dimerization of the human beta-subunit. FEBS Lett. 379:153-156.
10. Brand, S. R., R. Kobayashi, and M. B. Mathews. 1997. The Tat protein of human immunodeficiency virus type 1 is a substrate and inhibitor of the interferon-induced, virally activated protein kinase, PKR. J. Biol. Chem. 272:8388-8395.
11. Carpick, B. W., V. Graziano, D. Schneider, R. K. Maitra, X. Lee, and B. R. G. Williams. 1997. Characterization of the solution complex between the interferon-induced, double-stranded RNA-activated protein kinase and HIV-I TAR RNA. J. Biol. Chem. 272:9510-9516.
12. Castagnoli, L., C. Vetriani, and G. Cesareni. 1994. Linking an easily detectable phenotype to the folding of a common structural motif. Selection of rare turn mutations that prevent the folding of Rop. J. Mol. Biol. 237:378-387.
13. Chen, Y. H., L. Hansen, M. X. Chen, C. Bjorbaek, H. Vestergaard, T. Hansen, P. T. Cohen, and O. Pedersen. 1994. Sequence of the human glycogen-associated regulatory subunit of type 1 protein phosphatase and analysis of its coding region and mRNA level in muscle from patients with NIDDM. Diabetes 43:1234-1241.
14. 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.
15. Clemens, M. J. 1996. Protein kinases that phosphorylate eIF2 and eIF2B, and their role in eukaryotic cell translational control, p. 139-172. In J. Hershey, M. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
16. Cosentino, G. P., S. Venkatesan, F. C. Serluca, S. R. Green, M. B. Mathews, and N. Sonenberg. 1995. Double-strandcd-RNA-dependent protein kinase and TAR RNA-binding protein form homo-and heterodimers in vivo. Proc. Natl. Acad. Sci. USA 92:9445-9449.
17. Creasy, C. L., D. M. Ambrose, and J. Chernoff. 1996. The Ste20-like protein kinase, Mst1, dimerizes and contains an inhibitory domain. J. Biol. Chem. 271:21049-21053.
18. Davis, L. J., and T. D. Halazonetis. 1993. Both the helix-loop-helix and the leucine zipper motifs of c-Myc contribute to its dimerization specificity with Max. Oncogene 8:125-132.
19. Denu, J. M., J. A. Stuckey, M. A. Saper, and J. E. Dixon. 1996. Form and function in protein dephosphorylation. Cell 87:361-364.
20. Dubois, M. F., and A. G. Hovanessian. 1990. Modified subcellular localization of interferon-induced p68 kinase during encephalomyocarditis virus infection. Virology 179:591-598.
21. Elledge, S. J., and J. W. Harper. 1994. Cdk inhibitors: on the threshold of checkpoints and development. Curr. Opin. Cell Biol. 6:847-852.
22. Farrar, M. A., J. Alberola-Ila, and R. M. Perlmutter. 1996. Activation of the Raf-1 kinase cascade by coumermycin-induced dimerization. Nature 383: 178-181.
23. Faux, M. C., and J. D. Scott. 1996. Molecular glue: kinase anchoring and scaffold proteins. Cell 85:9-12.
24. Fields, S., and O. Song. 1989. A novel genetic system to detect protein-protein interactions. Nature 340:245-246.
25. IPK and vaccinia virus K3L is mediated by unique domains: implications for kinase regulation. Mol. Cell. Biol. 16:4172-4181.
26. Gale, M., Jr., M. J. Korth, N. M. Tang, S.-L. Tan, D. A. Hopkins, T. E. Dever, S. J. Polyak, D. R. Gretch, and M. G. Katze. 1997. Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by the nonstructural 5A protein. Virology 230:217-227.
27. rIPK. Mol. Cell. Biol. 18:859-871.
28. Gale, M., Jr., C. M. Blakely, N. M. Tang, and M. G. Katze. Unpublished data.
29. Hagman, J., M. J. Gutch, H. Lin, and R. Grosschedl. 1995. EBF contains a novel zinc coordination motif and multiple dimerization and transcriptional activation domains. EMBO J. 14:2907-2916.
30. 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.
31. Heldin, C. H. 1995. Dimerization of cell surface receptors in signal transduction. Cell 80:213-223.
32. Hofer, H. W. 1996. Conservation, evolution, and specificity in cellular control by protein phosphorylation. Experientia 52:449-454.
33. Hu, J. C. 1995. Repressor fusions as a tool to study protein-protein interactions. Structure 3:431-433.
34. Hu, J. C., E. K. O'Shea, P. S. Kim, and R. T. Sauer. 1990. Sequence requirements for coiled-coils: analysis with lambda repressor-GCN4 leucine zipper fusions. Science 250:1400-1403.
35. Hu, Y. F., B. Luscher, A. Admon, N. Mermod, and R. Tjian. 1990. Transcription factor AP-4 contains multiple dimerization domains that regulate dimer specificity. Genes Dev. 4:1741-1752.
36. Hubbard, M. J., and P. Cohen. 1993. On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem. Sci. 18:172-177.
37. Jaffrey, S. R., and S. H. Snyder. 1996. PIN: an associated protein inhibitor of neuronal nitric oxide synthase. Science 274:774-777.
38. Jeffrey, I. W., S. Kadereit, E. F. Meurs, T. Metzger, M. Bachmann, M. Schwemmle, A. G. Hovanessian, and M. J. Clemens. 1995. Nuclear localization of the interferon-inducible protein kinase PKR in human cells and transfected mouse cells. Exp. Cell Res. 218:17-27.
39. Jiménez-García, L. F., S. R. Green, M. B. Mathews, and D. L. Spector. 1993. Organization of the double-stranded RNA-activated protein kinase DAI and virus-associated VA RNAI in adenovirus-2-infected HeLa cells. J. Cell Sci. 106:11-22.
40. Johnson, L. N., M. E. Noble, and D. J. Owen. 1996. Active and inactive protein kinases: structural basis for regulation. Cell 85:149-158.
41. Kalus, W., R. Baumgartner, C. Renner, A. Noegel, F. K. Chan, A. Winoto, and T. A. Holak. 1997. NMR structural characterization of the CDK inhibitor p19INK4d. FEBS Lett. 401:127-132.
42. Katze, M. G. 1995. Regulation of the interferon-induced PKR: can viruses cope? Trends Microbiol. 3:75-78.
43. r protein kinase in a cell-free system. Mol. Cell. Biol. 11:5497-5505.
44. Kemp, B. E., and R. B. Pearson. 1991. Intra-steric regulation of protein kinases and phosphatases. Biochim. Biophys. Acta 1094:67-76.
45. Knighton, D. R., J. H. Zheng, E. L. F. Ten, N. H. Xuong, S. S. Taylor, and J. M. Sowadski. 1991. Structure of a peptide inhibitor bound to the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253:414-420.
46. 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.
47. Kostura, M., and M. B. Mathews. 1989. Purification and activation of the double-stranded eIF-2 kinase DAI. Mol. Cell. Biol. 9:1576-1586.
48. Kumar, A., J. Haque, J. Lacoste, J. Hiscott, and B. R. Williams. 1994. Double-stranded RNA-dependent protein kinase activates transcription factor NF-kappa B by phosphorylating I kappa B. Proc. Natl. Acad. Sci. USA 91:6288-6292.
49. 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.
50. Lee, S. B., S. R. Green, M. B. Mathews, and M. Esteban. 1994. Activation of the double-stranded RNA (dsRNA)-activated human protein kinase in vivo in the absence of its dsRNA binding domain. Proc. Natl. Acad. Sci. USA 91:10551-10555.
51. Lee, T. G., and M. G. Katze. 1994. Cellular inhibitors of the interferon-induced, dsRNA-activated protein kinase. Prog. Mol. Subcell. Biol. 14:48-65.
52. Lee, T. G., N. Tang, S. Thompson, J. Miller, and M. G. Katze. 1994. The 58,000-dalton cellular inhibitor of the interferon-induced double-stranded RNA-activated protein kinase (PKR) is a member of the tetratricopeptide repeat family of proteins. Mol. Cell. Biol. 14:2331-2342.
53. Lee, T. G., J. Tomita, A. G. Hovanessian, and M. G. Katze. 1990. Purification and partial characterization of a cellular inhibitor of the interferon-induced protein kinase of Mr 68,000 from influenza virus-infected cells. Proc. Natl. Acad. Sci. USA 87:6208-6212.
54. Lee, T. G., J. Tomita, A. G. Hovanessian, and M. G. Katze. 1992. Characterization and regulation of the 58,000-dalton cellular inhibitor of the interferon-induced, dsRNA-activated protein kinase. J. Biol. Chem. 267:14238-14243.
55. Longo, F., M. A. Marchetti, L. Castagnoli, P. A. Battaglia, and F. Gigliani. 1995. A novel approach to protein-protein interaction: complex formation between the p53 tumor suppressor and the HIV Tat proteins. Biochem. Biophys. Res. Commun. 206:326-334.
56. Lu, Y., M. Wambach, M. G. Katze, and R. M. Krug. 1995. Binding of the influenza virus NS1 protein to double-stranded RNA inhibits the activation of the protein kinase that phosphorylates the elF-2 translation initiation factor. Virology 214:222-228.
57. MacMillan-Crow, L. A., and T. M. Lincoln. 1994. High-affinity binding and localization of the cyclic GMP dependent protein kinase with the intermediate filament protein vimentin. Biochemistry 33:8035-8043.
58. Mathews, M. B. 1996. Interactions between viruses and the cellular machinery for protein synthesis, p. 505-548. In J. Hershey, M. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
59. Merrick, W. C., and J. W. B. Hershey. 1996. The pathway and mechanism of eukaryotic protein synthesis, p. 31-69. In J. Hershey, M. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
60. Meurs, E., K. Chong, J. Galabru, N. S. Thomas, I. M. Kerr, B. R. 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.
61. Meurs, E., J. Galabru, G. N. Barber, M. G. Katze, and A. G. Hovanessian. 1993. Tumor suppressor function of the interteron-induced double-stranded RNA-activated protein kinase. Proc. Natl. Acad. Sci. USA 90:232-236.
62. Murthy, A. E., A. Bernards, U. Church, J. Wasmuth, and J. F. Gusella. 1996. Identification and characterization of two novel tetratricopeptide repeat-containing genes. DNA Cell. Biol. 15:727-735.
63. Nagaya, T., and J. L. Jameson. 1993. Distinct dimerization domains provide antagonist pathways for thyroid hormone receptor action. J. Biol. Chem. 268:24278-24282.
64. Nishikawa, J., M. Kitaura, M. Imagawa, and T. Nishihara. 1995. Vitamin D receptor contains multiple dimerization interfaces that are functionally different. Nucleic Acids Res. 23:606-611.
65. Olah, G. A., R. D. Mitchell, T. R. Sosnick, D. A. Walsh, and J. Trewhella. 1993. Solution structure of the cAMP-dependent protein kinase catalytic subunit and its contraction upon binding the protein kinase inhibitor peptide. Biochemistry 32:3649-3657.
66. Ortega, L. G., M. D. McCotter, G. L. Henry, S. J. McCormack, D. C. Thomis, and C. E. Samuel. 1996. Mechanism of interferon action. Biochemical and genetic evidence for the intermolecular association of the RNA-dependent protein kinase PKR from human cells. Virology 215:31-39.
67. Patel, R. C., P. Stanton, N. M. McMillan, B. R. 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.
68. 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.
69. Polyak, S. J., N. Tang, M. Wambach, G. N. Barber, and M. G. Katze. 1996. The P58 cellular inhibitor complexes with the interferon-induced, double-stranded RNA-dependent protein kinase, PKR, to regulate its autophosphorylation and activity. J. Biol. Chem. 271:1702-1707.
70. Rice, A. P., M. Kostura, and M. B. Mathews. 1989. Identification of a 90-kDa polypeptide which associates with adenovirus VA RNAI and is phosphorylated by the double-stranded RNA-dependent protein kinase. J. Biol. Chem. 264:20632-20637.
71. 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-2 alpha kinase DAI in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:365-378.
72. Russo, A. A., P. D. Jeffrey, A. K. Patten, J. Massague, and N. P. Pavletich. 1996. Crystal structure of the p27Kip1 cyclin-dependent-kinase inhibitor bound to the cyclin A-Cdk2 complex. Nature 382:325-331.
73. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
74. Samuel, C. E. 1993. The eIF-2 alpha protein kinases, regulators of translation in eukaryotes from yeasts to humans. J. Biol. Chem. 268:7603-7606.
75. Schiestl, R. H., and R. D. Gietz. 1989. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet. 16:339-346.
76. Stock, J. 1996. Receptor signaling: dimerization and beyond. Curr. Biol. 6:825-827.
77. Szyszka, R., W. Kudlicki, G. Kramer, B. Hardesty, J. Galabru, and A. G. Hovanessian. 1989. A type 1 phosphoprotein phosphatase active with phosphorylated Mr = 68,000 initiation factor 2 kinase. J. Biol. Chem. 264:3827-3831.
78. Tan, S.-L., and M. G. Katze. In vitro and in vivo complex formation between the influenza A virus NS1 protein and the interferon-induced PKR protein kinase. Submitted for publication.
79. Tang, N. M., C. Y. Ho, and M. G. Katze. 1996. The 58-kDa cellular inhibitor of the double stranded RNA-dependent protein kinase requires the tetratricopeptide repeat 6 and DnaJ motifs to stimulate protein synthesis in vivo. J. Biol. Chem. 271:28660-28666.
80. 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.
81. Taylor, S. S., J. A. Buechler, and W. Yonemoto. 1990. cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes. Annu. Rev. Biochem. 59:971-1005.
82. Thomis, D. C., and C. E. Samuel. 1992. Mechanism of interferon action: autoregulation of RNA-dependent P1/eIF-2 alpha protein kinase (PKR) expression in transfected mammalian cells. Proc. Natl. Acad. Sci. USA 89: 10837-10841.
83. Thomis, D. C., and C. E. Samuel. 1993. Mechanism of interferon action: evidence for intermolecular autophosphorylation and autoactivation of the interferon-induced. RNA-dependent protein kinase PKR. J. Virol. 67:7695-7700.
84. 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.
85. 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.
86. Zhang, X. F., J. Settleman, J. M. Kyriakis, E. Takeuchi-Suzuki, S. J. Elledge, M. S. Marshall, J. T. Bruder, U. R. Rapp, and J. Avruch. 1993. Normal and oncogenic p21ras proteins bind to the amino-terminal regulatory domain of c-Raf-1. Nature 364:308-313.
87. 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.