P52rIPK regulates the molecular cochaperone P58IPK to mediate control of the RNA-dependent protein kinase in response to cytoplasmic stress

Biochemistry

Volumn 41, Issue 39, 2002, Pages 11878-11887

  Gale Jr , Michael ^a   Blakely, Collin M ^a,b   Darveau, André ^c   Romano, Patrick R ^d   Korth, Marcus J ^a   Katze, Michael G ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITÉ LAVAL   (Canada)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHORYLATION;

AMINO ACIDS; PROTEINS; RNA;

BIOCHEMISTRY;

CHAPERONE; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; PROTEIN KINASE; PROTEIN P52 RIPK; PROTEIN P58 IPK; UNCLASSIFIED DRUG; CARRIER PROTEIN; DNAJC3 PROTEIN, HUMAN; DNAJC3 PROTEIN, MOUSE; HEAT SHOCK PROTEIN 40; PEPTIDE FRAGMENT; PRKRIR PROTEIN, HUMAN; PROTEIN KINASE R; REPRESSOR PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL CELL; ARTICLE; CELL DAMAGE; CELL GROWTH; ENZYME ACTIVITY; ENZYME REGULATION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RNA TRANSLATION; SEQUENCE HOMOLOGY; AMINO ACID SEQUENCE; ANIMAL; CATTLE; CELL LINE; CELL STRAIN 3T3; CELL STRAIN COS1; CYTOPLASM; DRUG ANTAGONISM; ELECTRICITY; ENZYMOLOGY; GENETICS; HELA CELL; ISOELECTRIC FOCUSING; METABOLISM; MOUSE; OXIDATIVE STRESS; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

ANIMALIA;

3T3 CELLS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CARRIER PROTEINS; CATTLE; CELL LINE; COS CELLS; CYTOPLASM; EIF-2 KINASE; ELECTROSTATICS; HELA CELLS; HSP40 HEAT-SHOCK PROTEINS; HUMANS; ISOELECTRIC FOCUSING; MICE; MOLECULAR CHAPERONES; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, AMINO ACID; REPRESSOR PROTEINS;

EID: 0036771789     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi020397e     Document Type: Article

References (57)

1. Brostrom, C. O., and Brostrom, M. A. (1998) Regulation of translational initiation during cellular responses to stress, Prog. Nucleic Acid Res. Mol. Biol. 58, 79-125.
2. Sheikh, M. S., and Fornance, A. J., Jr. (1999) Regulation of translation initiation following stress, Oncogene 18, 6121-6128.
3. Gale, M., Jr., Tan, S.-L., and Katze, M. G. (2000) Translational control of viral gene expression in eukaryotes, Microbiol. Mol. Biol. Rev. 64, 239-280.
4. Frederickson, R. M., and Sonenberg, N. (1992) Signal transduction and regulation of translation initiation, Semin. Cell Biol. 3, 107-115.
5. Merrick, W. C., and Hershey, J. W. B. (1996) The pathway and mechanism of eukaryotic protein synthesis, in Translational control (Hershey, J., Mathews, M., and Sonenberg, N., Eds.) pp 31-70, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
6. Clemens, M. J. (1996) Protein kinases that phosphorylate eIF-2 and eIF-2B, and their role in eukaryotic cell translational control, in Translational control (Hershey, J., Mathews, M., and Sonenberg, N., Eds.) pp 139-172, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
7. Silverman, R. H., and Williams, B. R. G. (1999) Translational control perks up, Nature 397, 208-211.
8. Hinnebusch, A. G. (1994) The eIF-2α kinases: regulators of protein synthesis in starvation and stress, Semin. Cell Biol. 5, 417-426.
9. Chen, J.-J. (2000) Heme-regulated eIF2α kinase, in Translational control of gene expression (Sonenberg, N., Hershey, J. W. B., and Mathews, M. B., Eds.) pp 529-546, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
10. Hinnebusch, A. G. (1996) Translational control of GCN4: gene-specific regulation by phosphorylation of eIF2, in Translational control (Hershey, J., Mathews, M., and Sonenberg, N., Eds.) pp 199-244, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
11. Sood, R., Porter, A. C., Olsen, D., Cavener, D. R., and Wek, R. C. (2000) A mammalian homologue of GCN2 protein kinase important for translational control by phosphorylation of eukaryotic initiation factor-2α, Genetics 154, 787-801.
12. Olsen, D. S., Jordan, B., Chen, D., Wek, R. C., and Cavener, D. R. (1998) Isolation of the gene encoding the Drosophila melanogaster homologue of the Saccharomyces cerevisiae GCN2 eIF-2α kinase, Genetics 149, 1495-1509.
13. Berlanga, J. J., Santoyo, J., and de Haro, C. (1998) Characterization of a mammalian homologue of the GCN2 eukaryotic initiation factor 2α kinase, Eur. J. Biochem. 265, 754-762.
14. Ron, D., and Harding, H. P. (2000) Perk and translational control by stress in the endoplasmic reticulum, in Translational control of gene expression (Sonenberg, N., Hershey, J. W. B., and Mathews, M. B., Eds.) pp 547-560, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
15. Harding, H. P., Zhang, Y., Bertolotti, A., Zeng, H., and Ron, D. (2000) Perk is essential for translational regulation and cell survival during the unfolded protein response, Mol. Cell 5, 897-904.
16. Williams, B. R. G. (1997) Role of the double-stranded RNA-activated protein kinase (PKR) in cell regulation, Biochem. Soc. Trans. 25.
17. Clemens, M. J., and Elia, A. (1997) The double-stranded RNA-dependent protein kinase PKR: structure and function, J. Interferon Cytokine Res. 17, 503-524.
18. Gale, M., Jr., and Katze, M. G. (1998) Molecular mechanisms of interferon resistance mediated by viral-directed inhibition of PKR, the interferon-induced protein kinase, Pharmacol. Ther. 78, 29-46.
19. Kumar, A., Yang, Y.-L., Flati, V., Der, S., Kadereit, S., Deb, A., Haque, J., Reis, L., Weissmann, C., and Williams, B. R. G. (1997) Deficient cytokine signaling in mouse embryo fibroblasts with a targeted deletion in the PKR gene: role of IRF-1 and NF-κB, EMBO J. 16, 406-416.
20. Kaufman, R. J. (2000) Double-stranded RNA-activated protein kinase PKR, in Translational control of gene expression (Sonenberg, N., Hershey, J. W. B., and Mathews, M. B., Eds.) pp 503-528, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
21. Lee, T. G., Tang, N., Thompson, S., Miller, J., and Katze, M. G. (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.
22. IPK inhibitor, Mol. Cell. Biol. 18, 2431-2443.
23. IPK, is an influenza virus-activated co-chaperone that modulates heat shock protein 70 activity, J. Biol. Chem. 274, 3797-3803.
24. IPK and vaccinia virus K3L is mediated by unique domains: implications for kinase regulation, Mol. Cell. Biol. 16, 4172-4181.
25. Tang, N. M., Ho, C. Y., and Katze, M. G. (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.
26. IPK does not require J-domain function, Biochemistry 41, 4938-4945.
27. IPK, the cellular inhibitor of PKR, Proc. Natl. Acad. Sci. U.S.A. 94, 97-102.
28. Barber, G. N., Thompson, S., Lee, T. G., Strom, T., Jagus, R., Darveau, A., and Katze, M. G. (1994) The 58-kilodalton inhibitor of the interferon-induced double-stranded RNA-activated protein kinase is a tetratricopeptide repeat protein with oncogenic properties, Proc. Natl. Acad. Sci. U.S.A. 91, 4278-4282.
29. IPK, Mol. Cell. Biol. 19, 4757-4765.
30. rIPK, Mol. Cell. Biol. 18, 859-871.
31. Cesareni, G., and Murray, J. A. H. (1987) Plasmid vectors carrying the replication origin of filamentous single-stranded phages, in Genetic engineering: principles and methods (Setlow, J., Ed.) 1st ed., pp 135-154, Plenum Publishing Corp., New York.
32. Laurent, A. G., Krust, B., Galabru, J., Svab, J., and Hovanessian, A. G. (1985) Monoclonal antibodies to interferon induced 68,000 Mr protein and their use for the detection of double-stranded RNA dependent protein kinase in human cells, Proc. Natl. Acad. Sci. U.S.A. 82, 4341-4345.
33. Harlow, E., and Lane, D. (1988) Antibodies: a laboratory manual, pp 310-310, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
34. Romano, P. R., Green, S. R., Barber, G. N., Mathews, M. B., and Hinnebusch, A. G. (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.
35. Dever, T. E., Chen, J.-J., Barber, G. N., Cigan, A. M., Feng, L., Donahue, T. F., London, I. M., Katze, M. G., and Hinnebusch, A. G. (1993) Mammalian eukaryotic initiation factor eIF2α kinases functionally substitute for GCN2 protein kinase in the GCN4 translational control mechanism of yeast, Proc. Natl. Acad. Sci. U.S.A. 90, 4616-4620.
36. Hickey, E., Brandon, S. E., Smale, G., Lloyd, D., and Weber, L. A. (1989) Sequence and regulation of a gene encoding a human 89 kilodalton heat shock protein, Mol. Cell. Biol. 9, 2615-2626.
37. Stebbins, C. E., Russo, A. A., Schneider, C., Rosen, N., Hartl, F. U., and Pavletich, N. P. (1997) Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent, Cell 89, 239-250.
38. Ramsey, A. J., Russell, L. C., Whitt, S. R., and Chinkers, M. (2000) Overlapping sites of tetratricopeptide repeat protein binding and chaperone activity in heat shock protein 90, J. Biol. Chem. 275, 17857-17862.
39. Russell, L. C., Whitt, S. R., Chen, M. S., and Chinkers, M. (1999) Identification of conserved residues required for the binding of tetratricopeptide repeat domain to heat shock protein 90, J. Biol. Chem. 274, 20060-20063.
40. Chen, S., Sullivan, W. P., Toft, D. O., and Smith, D. F. (2000) Differential interactions of p23 and the TPR-containing proteins Hop, Cyp40, FKBP52, and FKBP51 with Hsp90 mutants, Cell Stress Chaperones 3, 118-129.
41. Blatch, G. L., and Lässle, M. (1999) The tetratricopeptide repeat: a structural motif mediating protein-protein interactions, BioEssays 21, 932-939.
42. Gale, M., Jr., Korth, M. J., Tang, N. M., Tan, S.-L., Hopkins, D. A., Dever, T. E., Polyak, S. J., Gretch, D. R., and Katze, M. G. (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.
43. McLauchlan, J. (2000) Properties of the hepatitis C virus core protein: a structural protein that modulates cellular processes, J. Viral Hepatitis 7, 2-14.
44. Sikorski, R. S., Michaud, W. A., Wootton, J. C., Boguski, M. S., Connelly, C., and Hieter, P. (1991) TPR proteins as essential components of the yeast cell cycle, Cold Spring Harbor Symp. Quant. Biol. 56, 663-673.
45. Stepanova, L., Leng, X., and Harper, J. W. (1997) Analysis of mammalian Cdc37, a protein kinase targeting subunit of heat shock protein 90, Methods Enzymol. 283, 220-229.
46. Prodromou, C., Siligardi, G., O'Brien, R., Woolfson, D. N., Regan, L., Panaretou, B., Ladbury, J. E., Piper, P. W., and Pearl, L. H. (1999) Regulation of Hsp90 ATPase activity by tetratricopeptide repeat (TPR)-domain co-chaperones, EMBO J. 18, 754-762.
47. Carrello, A., Ingley, E., Minchin, R. F., Tsai, S., and Ratajczak, T. (1999) The common tetratricopeptide repeat acceptor site for steroid receptor-associated immunophilins and hop is located in the dimerization domain of Hsp90, J. Biol. Chem. 274, 2682-2689.
48. Young, J. C., Oberman, W. M. J., and Hartl, F. U. (1998) Specific binding of tetratricopeptide repeat proteins to the C-terminal 12-kDa domain of hsp90, J. Biol. Chem. 273, 18007-18010.
49. Leverson, J. D., and Ness, S. A. (1998) Point mutations in v-Myb disrupt a cyclophilin-catalyzed negative regulatory mechanism, Mol. Cell 1, 203-211.
50. Callahan, M. A., Handley, M. A., Lee, Y. H., Talbot, K. J., Harper, J. W., and Panganiban, A. T. (1998) Functional interaction of human immunodeficiency virus type 1 Vpu and Gag with a novel member of the tetratricopeptide repeat protein family, J. Virol. 72, 5189-5197.
51. Scheuner, D., Song, B., McEwen, E., Liu, C., Laybutt, R., Gillespie, P., Saunders, T., Bonner-Weir, S., and Kaufman, R. J. (2001) Translational control is required for the unfolded protein response and in vivo glucose homeostasis, Mol. Cell 7, 1165-1176.
52. Patel, C. V., Handy, I., Goldsmith, T., and Patel, R. C. (2000) PACT, a stress-modulated cellular activator of interferon-induced double-stranded RNA-activated protein kinase, PKR, J. Biol. Chem. 275, 37993-37998.
53. Koromilas, A. E., Roy, S., Barber, G. N., Katze, M. G., and Sonenberg, N. (1992) Malignant transformation by a mutant of the IFN-inducible dsRNA-dependent protein kinase, Science 257, 1685-1689.
54. Barber, G. N., Wambach, M., Thompson, S., Jagus, R., and Katze, M. G. (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.
55. Balachandran, S., Kim, C. N., Yeh, W.-C., Mak, T. W., and Barber, G. N. (1998) Activation of the dsRNA-dependent protein kinase, PKR, induces apoptosis through FADD-mediated death signaling, EMBO J. 17, 6888-6902.
56. Benkirane, M., Neuveut, C., Chun, R. F., Smith, S. M., Samuel, C. E., Gatignol, A., and Jeang, K.-T. (1997) Oncogenic potential of TAR RNA binding protein TRBP and its regulatory interaction with RNA-dependent protein kinase PKR, EMBO J. 16, 611-624.
57. Gale, M., Jr., Kwieciszewski, B., Dossett, M., Nakao, H., and Katze, M. G. (1999) Antiapoptotic and oncogenic potentials of hepatitis C virus are linked to interferon resistance by viral repression of the PKR protein kinase, J. Virol. 73, 6506-6516.