Essential Role of PACT-Mediated PKR Activation in Tunicamycin-Induced Apoptosis

Journal of Molecular Biology

Volumn 385, Issue 2, 2009, Pages 457-468

  Singh, Madhurima ^a   Fowlkes, Vennece ^a   Handy, Indhira ^a   Patel, Chandrashekhar V ^b   Patel, Rekha C ^a  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

apoptosis; eIF2 ; interferon; PACT; PKR

Indexed keywords

GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; PACT PROTEIN; PROTEIN KINASE R; TRANSCRIPTION FACTOR; TUNICAMYCIN; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME RECONSTITUTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NULL CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

EID: 58149104379     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.10.068     Document Type: Article

References (79)

1. Meurs E., Chong K., Galabru J., Thomas N.S., Kerr I.M., Williams B.R., and Hovanessian A.G. Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon. Cell 62 (1990) 379-390
2. Williams B.R. PKR; a sentinel kinase for cellular stress. Oncogene 18 (1999) 6112-6120
3. Garcia M.A., Gil J., Ventoso I., Guerra S., Domingo E., Rivas C., and Esteban M. Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol. Mol. Biol. Rev. 70 (2006) 1032-1060
4. Hovanessian A.G., and Galabru J. The double-stranded RNA-dependent protein kinase is also activated by heparin. Eur. J. Biochem. 167 (1987) 467-473
5. Sadler A.J., and Williams B.R. Structure and function of the protein kinase R. Curr. Top. Microbiol. Immunol. 316 (2007) 253-292
6. Garcia M.A., Meurs E.F., and Esteban M. The dsRNA protein kinase PKR: virus and cell control. Biochimie 89 (2007) 799-811
7. Samuel C.E. The eIF-2 alpha protein kinases, regulators of translation in eukaryotes from yeasts to humans. J. Biol. Chem. 268 (1993) 7603-7606
8. Katze M.G. Regulation of the interferon-induced PKR: can viruses cope?. Trends Microbiol. 3 (1995) 75-78
9. Williams B.R.G. The role of the dsRNA-activated kinase, PKR, in signal transduction. Semin. Virol. 6 (1995) 191-202
10. Williams B.R. Signal integration via PKR. Sci. STKE 2001 (2001) RE2
11. Patel R.C., and Sen G.C. Identification of the double-stranded RNA-binding domain of the human interferon-inducible protein kinase. J. Biol. Chem. 267 (1992) 7671-7676
12. Feng G.S., Chong K., Kumar A., and Williams B.R. Identification of double-stranded RNA-binding domains in the interferon-induced double-stranded RNA-activated p68 kinase. Proc. Natl Acad. Sci. USA 89 (1992) 5447-5451
13. Katze M.G., Wambach M., Wong M.L., Garfinkel M., Meurs E., Chong K., et al. Functional expression and RNA binding analysis of the interferon-induced, double-stranded RNA-activated, 68,000-Mr protein kinase in a cell-free system. Mol. Cell. Biol. 11 (1991) 5497-5505
14. Green S.R., and Mathews M.B. Two RNA-binding motifs in the double-stranded RNA-activated protein kinase, DAI. Genes Dev. 6 (1992) 2478-2490
15. McCormack S.J., Thomis D.C., and Samuel C.E. Mechanism of interferon action: identification of a RNA binding domain within the N-terminal region of the human RNA-dependent P1/eIF-2 alpha protein kinase. Virology 188 (1992) 47-56
16. Nanduri S., Carpick B.W., Yang Y., Williams B.R., and Qin J. Structure of the double-stranded RNA-binding domain of the protein kinase PKR reveals the molecular basis of its dsRNA-mediated activation. EMBO J. 17 (1998) 5458-5465
17. Nanduri S., Rahman F., Williams B.R., and Qin J. A dynamically tuned double-stranded RNA binding mechanism for the activation of antiviral kinase PKR. EMBO J. 19 (2000) 5567-5574
18. Cole J.L. Activation of PKR: an open and shut case?. Trends Biochem. Sci. 32 (2007) 57-62
19. Patel R.C., Stanton P., McMillan N.M., Williams B.R., and Sen G.C. The interferon-inducible double-stranded RNA-activated protein kinase self-associates in vitro and in vivo. Proc. Natl Acad. Sci. USA 92 (1995) 8283-8287
20. Patel R.C., and Sen G.C. Requirement of PKR dimerization mediated by specific hydrophobic residues for its activation by double-stranded RNA and its antigrowth effects in yeast. Mol. Cell. Biol. 18 (1998) 7009-7019
21. Patel R.C., Vestal D.J., Xu Z., Bandyopadhyay S., Guo W., Erme S.M., et al. DRBP76, a double-stranded RNA-binding nuclear protein, is phosphorylated by the interferon-induced protein kinase, PKR. J. Biol. Chem. 274 (1999) 20432-20437
22. Cosentino G.P., Venkatesan S., Serluca F.C., Green S.R., Mathews M.B., and Sonenberg N. Double-stranded-RNA-dependent protein kinase and TAR RNA-binding protein form homo- and heterodimers in vivo. Proc. Natl Acad. Sci. USA 92 (1995) 9445-9449
23. Benkirane M., Neuveut C., Chun R.F., Smith S.M., Samuel C.E., Gatignol A., and Jeang K.T. Oncogenic potential of TAR RNA binding protein TRBP and its regulatory interaction with RNA-dependent protein kinase PKR. EMBO J. 16 (1997) 611-624
24. Mittelstadt M., Frump A., Khuu T., Fowlkes V., Handy I., Patel C.V., and Patel R.C. Interaction of human tRNA-dihydrouridine synthase-2 with interferon-induced protein kinase PKR. Nucleic Acids Res. 36 (2008) 998-1008
25. Patel R.C., and Sen G.C. PACT, a protein activator of the interferon-induced protein kinase, PKR. EMBO J. 17 (1998) 4379-4390
26. Patel C.V., Handy I., Goldsmith T., and Patel R.C. PACT, a stress-modulated cellular activator of interferon-induced double-stranded RNA-activated protein kinase, PKR. J. Biol. Chem. 275 (2000) 37993-37998
27. Peters G.A., Hartmann R., Qin J., and Sen G.C. Modular structure of PACT: distinct domains for binding and activating PKR. Mol. Cell. Biol. 21 (2001) 1908-1920
28. Huang X., Hutchins B., and Patel R.C. The C-terminal, third conserved motif of the protein activator PACT plays an essential role in the activation of double-stranded-RNA-dependent protein kinase (PKR). Biochem. J. 366 (2002) 175-186
29. Ito T., Yang M., and May W.S. RAX, a cellular activator for double-stranded RNA-dependent protein kinase during stress signaling. J. Biol. Chem. 274 (1999) 15427-15432
30. Bennett R.L., Blalock W.L., Abtahi D.M., Pan Y., Moyer S.A., and May W.S. RAX, the PKR activator, sensitizes cells to inflammatory cytokines, serum withdrawal, chemotherapy, and viral infection. Blood 108 (2006) 821-829
31. Bennett R.L., Blalock W.L., and May W.S. Serine 18 phosphorylation of RAX, the PKR activator, is required for PKR activation and consequent translation inhibition. J. Biol. Chem. 279 (2004) 42687-42693
32. Peters G.A., Li S., and Sen G.C. Phosphorylation of specific serine residues in the PKR activation domain of PACT is essential for its ability to mediate apoptosis. J. Biol. Chem. 281 (2006) 35129-35136
33. Harding H.P., Zhang Y., and Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397 (1999) 271-274
34. Harding H.P., Calfon M., Urano F., Novoa I., and Ron D. Transcriptional and translational control in the mammalian unfolded protein response. Annu. Rev. Cell Dev. Biol. 18 (2002) 575-599
35. Kincaid M.M., and Cooper A.A. ERADicate ER stress or die trying. Antioxid. Redox Signal. 9 (2007) 2373-2387
36. Ng D.T., Spear E.D., and Walter P. The unfolded protein response regulates multiple aspects of secretory and membrane protein biogenesis and endoplasmic reticulum quality control. J. Cell. Biol. 150 (2000) 77-88
37. Wek R.C., and Cavener D.R. Translational control and the unfolded protein response. Antioxid. Redox Signal. 9 (2007) 2357-2371
38. Oyadomari S., and Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 11 (2004) 381-389
39. Wek R.C., Jiang H.Y., and Anthony T.G. Coping with stress: eIF2 kinases and translational control. Biochem. Soc. Trans. 34 (2006) 7-11
40. Szegezdi E., Logue S.E., Gorman A.M., and Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 7 (2006) 880-885
41. Zinszner H., Kuroda M., Wang X., Batchvarova N., Lightfoot R.T., Remotti H., et al. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12 (1998) 982-995
42. Oyadomari S., Koizumi A., Takeda K., Gotoh T., Akira S., Araki E., and Mori M. Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J. Clin. Invest. 109 (2002) 525-532
43. Ron D., and Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8 (2007) 519-529
44. Kozutsumi Y., Segal M., Normington K., Gething M.J., and Sambrook J. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature 332 (1988) 462-464
45. Schroder M., and Kaufman R.J. The mammalian unfolded protein response. Annu. Rev. Biochem. 74 (2005) 739-789
46. Kaufman R.J. Orchestrating the unfolded protein response in health and disease. J. Clin. Invest. 110 (2002) 1389-1398
47. Wu J., and Kaufman R.J. From acute ER stress to physiological roles of the Unfolded Protein Response. Cell Death Differ. 13 (2006) 374-384
48. Harding H.P., Novoa I., Bertolotti A., Zeng H., Zhang Y., Urano F., et al. Translational regulation in the cellular response to biosynthetic load on the endoplasmic reticulum. Cold Spring Harbor Symp. Quant. Biol. 66 (2001) 499-508
49. Ron D. Translational control in the endoplasmic reticulum stress response. J. Clin. Invest. 110 (2002) 1383-1388
50. Delepine M., Nicolino M., Barrett T., Golamaully M., Lathrop G.M., and Julier C. EIF2AK3, encoding translation initiation factor 2-alpha kinase 3, is mutated in patients with Wolcott-Rallison syndrome. Nat. Genet. 25 (2000) 406-409
51. Zhang W., Feng D., Li Y., Iida K., McGrath B., and Cavener D.R. PERK EIF2AK3 control of pancreatic beta cell differentiation and proliferation is required for postnatal glucose homeostasis. Cell Metab. 4 (2006) 491-497
52. Shi Y., Taylor S.I., Tan S.L., and Sonenberg N. When translation meets metabolism: multiple links to diabetes. Endocr. Rev. 24 (2003) 91-101
53. Zhang P., McGrath B., Li S., Frank A., Zambito F., Reinert J., et al. The PERK eukaryotic initiation factor 2 alpha kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas. Mol. Cell. Biol. 22 (2002) 3864-3874
54. Harding H.P., and Ron D. Endoplasmic reticulum stress and the development of diabetes: a review. Diabetes 51 Suppl. 3 (2002) S455-S461
55. Harding H.P., Zhang Y., Bertolotti A., Zeng H., and Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5 (2000) 897-904
56. Scheuner D., Song B., McEwen E., Liu C., Laybutt R., Gillespie P., et al. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7 (2001) 1165-1176
57. Jousse C., Oyadomari S., Novoa I., Lu P., Zhang Y., Harding H.P., and Ron D. Inhibition of a constitutive translation initiation factor 2alpha phosphatase, CReP, promotes survival of stressed cells. J. Cell. Biol. 163 (2003) 767-775
58. Lu P.D., Jousse C., Marciniak S.J., Zhang Y., Novoa I., Scheuner D., et al. Cytoprotection by pre-emptive conditional phosphorylation of translation initiation factor 2. EMBO J. 23 (2004) 169-179
59. Srivastava S.P., Davies M.V., and Kaufman R.J. Calcium depletion from the endoplasmic reticulum activates the double-stranded RNA-dependent protein kinase (PKR) to inhibit protein synthesis. J. Biol. Chem. 270 (1995) 16619-16624
60. Srivastava S.P., Kumar K.U., and Kaufman R.J. Phosphorylation of eukaryotic translation initiation factor 2 mediates apoptosis in response to activation of the double-stranded RNA-dependent protein kinase. J. Biol. Chem. 273 (1998) 2416-2423
61. Brostrom C.O., Prostko C.R., Kaufman R.J., and Brostrom M.A. Inhibition of translational initiation by activators of the glucose-regulated stress protein and heat shock protein stress response systems. Role of the interferon-inducible double-stranded RNA-activated eukaryotic initiation factor 2alpha kinase. J. Biol. Chem. 271 (1996) 24995-25002
62. Scheuner D., Patel R., Wang F., Lee K., Kumar K., Wu J., et al. Double-stranded RNA-dependent protein kinase phosphorylation of the alpha-subunit of eukaryotic translation initiation factor 2 mediates apoptosis. J. Biol. Chem. 281 (2006) 21458-21468
63. Onuki R., Bando Y., Suyama E., Katayama T., Kawasaki H., Baba T., et al. An RNA-dependent protein kinase is involved in tunicamycin-induced apoptosis and Alzheimer's disease. EMBO J. 23 (2004) 959-968
64. Tang N.M., Korth M.J., Gale Jr. M., Wambach M., Der S.D., Bandyopadhyay S.K., et al. Inhibition of double-stranded RNA- and tumor necrosis factor alpha-mediated apoptosis by tetratricopeptide repeat protein and cochaperone P58(IPK). Mol. Cell. Biol. 19 (1999) 4757-4765
65. Gil J., Alcami J., and Esteban M. Induction of apoptosis by double-stranded-RNA-dependent protein kinase (PKR) involves the alpha subunit of eukaryotic translation initiation factor 2 and NF-kappaB. Mol. Cell. Biol. 19 (1999) 4653-4663
66. Balachandran S., Kim C.N., Yeh W.C., Mak T.W., Bhalla K., and Barber G.N. Activation of the dsRNA-dependent protein kinase, PKR, induces apoptosis through FADD-mediated death signaling. EMBO J. 17 (1998) 6888-6902
67. Baltzis D., Qu L.K., Papadopoulou S., Blais J.D., Bell J.C., Sonenberg N., and Koromilas A.E. Resistance to vesicular stomatitis virus infection requires a functional cross talk between the eukaryotic translation initiation factor 2alpha kinases PERK and PKR. J. Virol. 78 (2004) 12747-12761
68. Bando Y., Onuki R., Katayama T., Manabe T., Kudo T., Taira K., and Tohyama M. Double-strand RNA dependent protein kinase (PKR) is involved in the extrastriatal degeneration in Parkinson's disease and Huntington's disease. Neurochem. Int. 46 (2005) 11-18
69. Peel A.L., Rao R.V., Cottrell B.A., Hayden M.R., Ellerby L.M., and Bredesen D.E. Double-stranded RNA-dependent protein kinase, PKR, binds preferentially to Huntington's disease (HD) transcripts and is activated in HD tissue. Hum. Mol. Genet. 10 (2001) 1531-1538
70. Peel A.L., and Bredesen D.E. Activation of the cell stress kinase PKR in Alzheimer's disease and human amyloid precursor protein transgenic mice. Neurobiol. Dis. 14 (2003) 52-62
71. Peel A.L. PKR activation in neurodegenerative disease. J. Neuropathol. Exp. Neurol. 63 (2004) 97-105
72. Shimazawa M., and Hara H. Inhibitor of double stranded RNA-dependent protein kinase protects against cell damage induced by ER stress. Neurosci. Lett. 409 (2006) 192-195
73. Lee E.S., Yoon C.H., Kim Y.S., and Bae Y.S. The double-strand RNA-dependent protein kinase PKR plays a significant role in a sustained ER stress-induced apoptosis. FEBS Lett. 581 (2007) 4325-4332
74. Clemens M.J. Regulation of eukaryotic protein synthesis by protein kinases that phosphorylate initiation factor eIF-2. Mol. Biol. Rep. 19 (1994) 201-210
75. Clemens M.J. Initiation factor eIF2 alpha phosphorylation in stress responses and apoptosis. Prog. Mol. Subcell. Biol. 27 (2001) 57-89
76. Proud C.G. eIF2 and the control of cell physiology. Semin. Cell Dev. Biol. 16 (2005) 3-12
77. Wek R.C. eIF-2 kinases: regulators of general and gene-specific translation initiation. Trends Biochem. Sci. 19 (1994) 491-496
78. Marques J.T., White C.L., Peters G.A., Williams B.R., and Sen G.C. The role of PACT in mediating gene induction, PKR activation, and apoptosis in response to diverse stimuli. J. Interferon Cytokine Res. 28 (2008) 469-476
79. Vindelov L.L., Christensen I.J., and Nissen N.I. A detergent-trypsin method for the preparation of nuclei for flow cytometric DNA analysis. Cytometry 3 (1983) 323-327