Skip to main content
NCBI home page
RNA logoLink to RNA
. 2002 Apr;8(4):478–496. doi: 10.1017/s1355838202022586

The mRNA of the translationally controlled tumor protein P23/TCTP is a highly structured RNA, which activates the dsRNA-dependent protein kinase PKR.

Ulrich-Axel Bommer 1, Anton V Borovjagin 1, Martin A Greagg 1, Ian W Jeffrey 1, Paul Russell 1, Kenneth G Laing 1, Melanie Lee 1, Michael J Clemens 1
PMCID: PMC1370270  PMID: 11991642

Abstract

The dsRNA-activated protein kinase PKR is involved in signal transduction pathways that mediate cellular processes as diverse as cell growth and differentiation, the stress response, and apoptosis. PKR was originally described as an interferon-inducible elF2alpha kinase involved in the antiviral defense mechanism of the cell. The interaction of the kinase with specific viral RNAs has been studied in much detail, but information about cellular mRNAs, which are able to bind and activate PKR, is scarce. In search for such cellular mRNAs, we developed a cloning strategy to identify individual mRNA species from the dsRNA-rich fraction of Daudi cell poly(A)+ RNA. Two out of five cDNA clones we obtained contained sequences derived from the mRNA of the translationally controlled tumor protein P23/TCTP, indicating that this mRNA is present in the dsRNA-rich fraction. Secondary structure predictions and gel electrophoretic mobility investigations on P23/TCTP transcripts confirmed the potential of this mRNA to form extensive secondary structure. A full-length P23 transcript, but not a truncated version thereof, was able to bind to PKR in vitro and in vivo. Transient transfection experiments in human 293 cells showed that coexpression of full-length P23 mRNA leads to partial inhibition of the expression of a beta-galactosidase reporter gene in trans. Additional coexpression of a dominant negative mutant of PKR or of adenovirus VA1 RNA suppressed this inhibition, indicating that it is mediated by PKR. Studies on P23/TCTP expression in cells from PKR-knockout mice suggest that P23/TCTP mRNA translation is regulated by PKR. Hence, our results demonstrate that the mRNA of P23/TCTP may both activate PKR and be subject to translational regulation by this kinase.

Full Text

The Full Text of this article is available as a PDF (1.4 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams M. D., Kerlavage A. R., Fleischmann R. D., Fuldner R. A., Bult C. J., Lee N. H., Kirkness E. F., Weinstock K. G., Gocayne J. D., White O. Initial assessment of human gene diversity and expression patterns based upon 83 million nucleotides of cDNA sequence. Nature. 1995 Sep 28;377(6547 Suppl):3–174. [PubMed] [Google Scholar]
  2. Baudet C., Perret E., Delpech B., Kaghad M., Brachet P., Wion D., Caput D. Differentially expressed genes in C6.9 glioma cells during vitamin D-induced cell death program. Cell Death Differ. 1998 Jan;5(1):116–125. doi: 10.1038/sj.cdd.4400327. [DOI] [PubMed] [Google Scholar]
  3. Ben-Asouli Yitzhak, Banai Yona, Pel-Or Yehuda, Shir Alexei, Kaempfer Raymond. Human interferon-gamma mRNA autoregulates its translation through a pseudoknot that activates the interferon-inducible protein kinase PKR. Cell. 2002 Jan 25;108(2):221–232. doi: 10.1016/s0092-8674(02)00616-5. [DOI] [PubMed] [Google Scholar]
  4. Benndorf R., Nürnberg P., Bielka H. Growth phase-dependent proteins of the Ehrlich ascites tumor analyzed by one- and two-dimensional electrophoresis. Exp Cell Res. 1988 Jan;174(1):130–138. doi: 10.1016/0014-4827(88)90148-6. [DOI] [PubMed] [Google Scholar]
  5. Bhisutthibhan J., Meshnick S. R. Immunoprecipitation of [(3)H]dihydroartemisinin translationally controlled tumor protein (TCTP) adducts from Plasmodium falciparum-infected erythrocytes by using anti-TCTP antibodies. Antimicrob Agents Chemother. 2001 Aug;45(8):2397–2399. doi: 10.1128/AAC.45.8.2397-2399.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bhisutthibhan J., Pan X. Q., Hossler P. A., Walker D. J., Yowell C. A., Carlton J., Dame J. B., Meshnick S. R. The Plasmodium falciparum translationally controlled tumor protein homolog and its reaction with the antimalarial drug artemisinin. J Biol Chem. 1998 Jun 26;273(26):16192–16198. doi: 10.1074/jbc.273.26.16192. [DOI] [PubMed] [Google Scholar]
  7. Bhisutthibhan J., Philbert M. A., Fujioka H., Aikawa M., Meshnick S. R. The Plasmodium falciparum translationally controlled tumor protein: subcellular localization and calcium binding. Eur J Cell Biol. 1999 Sep;78(9):665–670. doi: 10.1016/S0171-9335(99)80052-1. [DOI] [PubMed] [Google Scholar]
  8. Bischoff J. R., Samuel C. E. Mechanism of interferon action. Activation of the human P1/eIF-2 alpha protein kinase by individual reovirus s-class mRNAs: s1 mRNA is a potent activator relative to s4 mRNA. Virology. 1989 Sep;172(1):106–115. doi: 10.1016/0042-6822(89)90112-8. [DOI] [PubMed] [Google Scholar]
  9. Boelens W. C., Jansen E. J., van Venrooij W. J., Stripecke R., Mattaj I. W., Gunderson S. I. The human U1 snRNP-specific U1A protein inhibits polyadenylation of its own pre-mRNA. Cell. 1993 Mar 26;72(6):881–892. doi: 10.1016/0092-8674(93)90577-d. [DOI] [PubMed] [Google Scholar]
  10. Bommer U. A., Lazaris-Karatzas A., De Benedetti A., Nürnberg P., Benndorf R., Bielka H., Sonenberg N. Translational regulation of the mammalian growth-related protein P23: involvement of eIF-4E. Cell Mol Biol Res. 1994;40(7-8):633–641. [PubMed] [Google Scholar]
  11. Bonnet C., Perret E., Dumont X., Picard A., Caput D., Lenaers G. Identification and transcription control of fission yeast genes repressed by an ammonium starvation growth arrest. Yeast. 2000 Jan 15;16(1):23–33. doi: 10.1002/(SICI)1097-0061(20000115)16:1<23::AID-YEA503>3.0.CO;2-A. [DOI] [PubMed] [Google Scholar]
  12. Borovjagin A. V., Ezrokhi M. V., Rostapshov V. M., Ugarova TYu, Bystrova T. F., Shatsky I. N. RNA--protein interactions within the internal translation initiation region of encephalomyocarditis virus RNA. Nucleic Acids Res. 1991 Sep 25;19(18):4999–5005. doi: 10.1093/nar/19.18.4999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Brinegar J. D., Hampel A., Alter G. M., Cruz P. The secondary structure of a fourteen-nucleotide fragment of the hairpin ribozyme. Biochem Biophys Res Commun. 1997 Mar 17;232(2):444–448. doi: 10.1006/bbrc.1997.6305. [DOI] [PubMed] [Google Scholar]
  14. Brostrom C. O., Brostrom M. A. Regulation of translational initiation during cellular responses to stress. Prog Nucleic Acid Res Mol Biol. 1998;58:79–125. doi: 10.1016/s0079-6603(08)60034-3. [DOI] [PubMed] [Google Scholar]
  15. Böhm H., Benndorf R., Gaestel M., Gross B., Nürnberg P., Kraft R., Otto A., Bielka H. The growth-related protein P23 of the Ehrlich ascites tumor: translational control, cloning and primary structure. Biochem Int. 1989 Aug;19(2):277–286. [PubMed] [Google Scholar]
  16. Böhm H., Gross B., Gaestel M., Bommer U. A., Ryffel G., Bielka H. The 5'-untranslated region of p23 mRNA from the Ehrlich ascites tumor is involved in translation control of the growth related protein p23. Biomed Biochim Acta. 1991;50(12):1193–1203. [PubMed] [Google Scholar]
  17. Chu W. M., Ballard R., Carpick B. W., Williams B. R., Schmid C. W. Potential Alu function: regulation of the activity of double-stranded RNA-activated kinase PKR. Mol Cell Biol. 1998 Jan;18(1):58–68. doi: 10.1128/mcb.18.1.58. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Chung S., Kim M., Choi W., Chung J., Lee K. Expression of translationally controlled tumor protein mRNA in human colon cancer. Cancer Lett. 2000 Aug 11;156(2):185–190. doi: 10.1016/s0304-3835(00)00460-2. [DOI] [PubMed] [Google Scholar]
  19. Clarke P. A., Sharp N. A., Arrand J. R., Clemens M. J. Epstein-Barr virus gene expression in interferon-treated cells. Implications for the regulation of protein synthesis and the antiviral state. Biochim Biophys Acta. 1990 Aug 27;1050(1-3):167–173. doi: 10.1016/0167-4781(90)90161-t. [DOI] [PubMed] [Google Scholar]
  20. Clemens M. J., Bommer U. A. Translational control: the cancer connection. Int J Biochem Cell Biol. 1999 Jan;31(1):1–23. doi: 10.1016/s1357-2725(98)00127-7. [DOI] [PubMed] [Google Scholar]
  21. Clemens M. J., Elia A. The double-stranded RNA-dependent protein kinase PKR: structure and function. J Interferon Cytokine Res. 1997 Sep;17(9):503–524. doi: 10.1089/jir.1997.17.503. [DOI] [PubMed] [Google Scholar]
  22. Clemens M. J. PKR--a protein kinase regulated by double-stranded RNA. Int J Biochem Cell Biol. 1997 Jul;29(7):945–949. doi: 10.1016/s1357-2725(96)00169-0. [DOI] [PubMed] [Google Scholar]
  23. Davis S., Watson J. C. In vitro activation of the interferon-induced, double-stranded RNA-dependent protein kinase PKR by RNA from the 3' untranslated regions of human alpha-tropomyosin. Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):508–513. doi: 10.1073/pnas.93.1.508. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. De Benedetti A., Baglioni C. Inhibition of mRNA binding to ribosomes by localized activation of dsRNA-dependent protein kinase. Nature. 1984 Sep 6;311(5981):79–81. doi: 10.1038/311079a0. [DOI] [PubMed] [Google Scholar]
  25. Evstafieva A. G., Ugarova T. Y., Chernov B. K., Shatsky I. N. A complex RNA sequence determines the internal initiation of encephalomyocarditis virus RNA translation. Nucleic Acids Res. 1991 Feb 11;19(3):665–671. doi: 10.1093/nar/19.3.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Gachet Y., Tournier S., Lee M., Lazaris-Karatzas A., Poulton T., Bommer U. A. The growth-related, translationally controlled protein P23 has properties of a tubulin binding protein and associates transiently with microtubules during the cell cycle. J Cell Sci. 1999 Apr;112(Pt 8):1257–1271. doi: 10.1242/jcs.112.8.1257. [DOI] [PubMed] [Google Scholar]
  27. Gast F. U., Kempe D., Spieker R. L., Sänger H. L. Secondary structure probing of potato spindle tuber viroid (PSTVd) and sequence comparison with other small pathogenic RNA replicons provides evidence for central non-canonical base-pairs, large A-rich loops, and a terminal branch. J Mol Biol. 1996 Oct 11;262(5):652–670. doi: 10.1006/jmbi.1996.0543. [DOI] [PubMed] [Google Scholar]
  28. Gingras A. C., Raught B., Sonenberg N. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem. 1999;68:913–963. doi: 10.1146/annurev.biochem.68.1.913. [DOI] [PubMed] [Google Scholar]
  29. Gray N. K., Hentze M. W. Regulation of protein synthesis by mRNA structure. Mol Biol Rep. 1994 May;19(3):195–200. doi: 10.1007/BF00986961. [DOI] [PubMed] [Google Scholar]
  30. Greenhead P., Hayes P., Watts P. S., Laing K. G., Griffin G. E., Shattock R. J. Parameters of human immunodeficiency virus infection of human cervical tissue and inhibition by vaginal virucides. J Virol. 2000 Jun;74(12):5577–5586. doi: 10.1128/jvi.74.12.5577-5586.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Gross B., Gaestel M., Böhm H., Bielka H. cDNA sequence coding for a translationally controlled human tumor protein. Nucleic Acids Res. 1989 Oct 25;17(20):8367–8367. doi: 10.1093/nar/17.20.8367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Guillaume E., Pineau C., Evrard B., Dupaix A., Moertz E., Sanchez J. C., Hochstrasser D. F., Jégou B. Cellular distribution of translationally controlled tumor protein in rat and human testes. Proteomics. 2001 Jul;1(7):880–889. doi: 10.1002/1615-9861(200107)1:7<880::AID-PROT880>3.0.CO;2-2. [DOI] [PubMed] [Google Scholar]
  33. Haghighat N. G., Ruben L. Purification of novel calcium binding proteins from Trypanosoma brucei: properties of 22-, 24- and 38-kilodalton proteins. Mol Biochem Parasitol. 1992 Mar;51(1):99–110. doi: 10.1016/0166-6851(92)90205-x. [DOI] [PubMed] [Google Scholar]
  34. Harding H. P., Zeng H., Zhang Y., Jungries R., Chung P., Plesken H., Sabatini D. D., Ron D. Diabetes mellitus and exocrine pancreatic dysfunction in perk-/- mice reveals a role for translational control in secretory cell survival. Mol Cell. 2001 Jun;7(6):1153–1163. doi: 10.1016/s1097-2765(01)00264-7. [DOI] [PubMed] [Google Scholar]
  35. Harding H. P., Zhang Y., Bertolotti A., Zeng H., Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell. 2000 May;5(5):897–904. doi: 10.1016/s1097-2765(00)80330-5. [DOI] [PubMed] [Google Scholar]
  36. Harding H. P., Zhang Y., Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature. 1999 Jan 21;397(6716):271–274. doi: 10.1038/16729. [DOI] [PubMed] [Google Scholar]
  37. Jagus R., Joshi B., Barber G. N. PKR, apoptosis and cancer. Int J Biochem Cell Biol. 1999 Jan;31(1):123–138. doi: 10.1016/s1357-2725(98)00136-8. [DOI] [PubMed] [Google Scholar]
  38. Kang H. S., Lee M. J., Song H., Han S. H., Kim Y. M., Im J. Y., Choi I. Molecular identification of IgE-dependent histamine-releasing factor as a B cell growth factor. J Immunol. 2001 Jun 1;166(11):6545–6554. doi: 10.4049/jimmunol.166.11.6545. [DOI] [PubMed] [Google Scholar]
  39. Kimball S. R., Clemens M. J., Tilleray V. J., Wek R. C., Horetsky R. L., Jefferson L. S. The double-stranded RNA-activated protein kinase PKR is dispensable for regulation of translation initiation in response to either calcium mobilization from the endoplasmic reticulum or essential amino acid starvation. Biochem Biophys Res Commun. 2001 Jan 12;280(1):293–300. doi: 10.1006/bbrc.2000.4103. [DOI] [PubMed] [Google Scholar]
  40. Kleijn M., Scheper G. C., Voorma H. O., Thomas A. A. Regulation of translation initiation factors by signal transduction. Eur J Biochem. 1998 May 1;253(3):531–544. doi: 10.1046/j.1432-1327.1998.2530531.x. [DOI] [PubMed] [Google Scholar]
  41. Kronfeld-Kinar Y., Vilchik S., Hyman T., Leibkowicz F., Salzberg S. Involvement of PKR in the regulation of myogenesis. Cell Growth Differ. 1999 Mar;10(3):201–212. [PubMed] [Google Scholar]
  42. Kumar K. U., Srivastava S. P., Kaufman R. J. Double-stranded RNA-activated protein kinase (PKR) is negatively regulated by 60S ribosomal subunit protein L18. Mol Cell Biol. 1999 Feb;19(2):1116–1125. doi: 10.1128/mcb.19.2.1116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Laurent A. G., Krust B., Galabru J., Svab J., Hovanessian A. G. 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 U S A. 1985 Jul;82(13):4341–4345. doi: 10.1073/pnas.82.13.4341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Li J., Petryshyn R. A. Activation of the double-stranded RNA-dependent eIF-2 alpha kinase by cellular RNA from 3T3-F442A cells. Eur J Biochem. 1991 Jan 1;195(1):41–48. doi: 10.1111/j.1432-1033.1991.tb15673.x. [DOI] [PubMed] [Google Scholar]
  45. MacDonald M. J., Al-Masri H., Jumelle-Laclau M., Cruz M. O. Oscillations in activities of enzymes in pancreatic islet subcellular fractions induced by physiological concentrations of effectors. Diabetes. 1997 Dec;46(12):1996–2001. doi: 10.2337/diab.46.12.1996. [DOI] [PubMed] [Google Scholar]
  46. MacDonald S. M. Human recombinant histamine-releasing factor. Int Arch Allergy Immunol. 1997 May-Jul;113(1-3):187–189. doi: 10.1159/000237542. [DOI] [PubMed] [Google Scholar]
  47. MacDonald S. M., Paznekas W. A., Jabs E. W. Chromosomal localization of tumor protein, translationally-controlled 1 (TPT1) encoding the human histamine releasing factor (HRF) to 13q12-->q14. Cytogenet Cell Genet. 1999;84(1-2):128–129. doi: 10.1159/000015238. [DOI] [PubMed] [Google Scholar]
  48. MacDonald S. M., Rafnar T., Langdon J., Lichtenstein L. M. Molecular identification of an IgE-dependent histamine-releasing factor. Science. 1995 Aug 4;269(5224):688–690. doi: 10.1126/science.7542803. [DOI] [PubMed] [Google Scholar]
  49. Mellits K. H., Mathews M. B. Effects of mutations in stem and loop regions on the structure and function of adenovirus VA RNAI. EMBO J. 1988 Sep;7(9):2849–2859. doi: 10.1002/j.1460-2075.1988.tb03141.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Mellits K. H., Pe'ery T., Manche L., Robertson H. D., Mathews M. B. Removal of double-stranded contaminants from RNA transcripts: synthesis of adenovirus VA RNAI from a T7 vector. Nucleic Acids Res. 1990 Sep 25;18(18):5401–5406. doi: 10.1093/nar/18.18.5401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Osman F., Jarrous N., Ben-Asouli Y., Kaempfer R. A cis-acting element in the 3'-untranslated region of human TNF-alpha mRNA renders splicing dependent on the activation of protein kinase PKR. Genes Dev. 1999 Dec 15;13(24):3280–3293. doi: 10.1101/gad.13.24.3280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Peel A. L., Rao R. V., Cottrell B. A., Hayden M. R., Ellerby L. M., 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. 2001 Jul 15;10(15):1531–1538. doi: 10.1093/hmg/10.15.1531. [DOI] [PubMed] [Google Scholar]
  53. Petryshyn R. A., Ferrenz A. G., Li J. Characterization and mapping of the double-stranded regions involved in activation of PKR within a cellular RNA from 3T3-F442A cells. Nucleic Acids Res. 1997 Jul 1;25(13):2672–2678. doi: 10.1093/nar/25.13.2672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Pratt G., Galpine A., Sharp N., Palmer S., Clemens M. J. Regulation of in vitro translation by double-stranded RNA in mammalian cell mRNA preparations. Nucleic Acids Res. 1988 Apr 25;16(8):3497–3510. doi: 10.1093/nar/16.8.3497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Prostko C. R., Brostrom M. A., Malara E. M., Brostrom C. O. Phosphorylation of eukaryotic initiation factor (eIF) 2 alpha and inhibition of eIF-2B in GH3 pituitary cells by perturbants of early protein processing that induce GRP78. J Biol Chem. 1992 Aug 25;267(24):16751–16754. [PubMed] [Google Scholar]
  56. Prostko C. R., Dholakia J. N., Brostrom M. A., Brostrom C. O. Activation of the double-stranded RNA-regulated protein kinase by depletion of endoplasmic reticular calcium stores. J Biol Chem. 1995 Mar 17;270(11):6211–6215. doi: 10.1074/jbc.270.11.6211. [DOI] [PubMed] [Google Scholar]
  57. Rastinejad F., Blau H. M. Genetic complementation reveals a novel regulatory role for 3' untranslated regions in growth and differentiation. Cell. 1993 Mar 26;72(6):903–917. doi: 10.1016/0092-8674(93)90579-f. [DOI] [PubMed] [Google Scholar]
  58. Rastinejad F., Conboy M. J., Rando T. A., Blau H. M. Tumor suppression by RNA from the 3' untranslated region of alpha-tropomyosin. Cell. 1993 Dec 17;75(6):1107–1117. doi: 10.1016/0092-8674(93)90320-p. [DOI] [PubMed] [Google Scholar]
  59. Raught B., Gingras A. C. eIF4E activity is regulated at multiple levels. Int J Biochem Cell Biol. 1999 Jan;31(1):43–57. doi: 10.1016/s1357-2725(98)00131-9. [DOI] [PubMed] [Google Scholar]
  60. Robertson H. D., Mathews M. B. The regulation of the protein kinase PKR by RNA. Biochimie. 1996;78(11-12):909–914. doi: 10.1016/s0300-9084(97)86712-0. [DOI] [PubMed] [Google Scholar]
  61. Sage-Ono K., Ono M., Harada H., Kamada H. Dark-induced accumulation of mRNA for a homolog of translationally controlled tumor protein (TCTP) in Pharbitis. Plant Cell Physiol. 1998 Mar;39(3):357–360. doi: 10.1093/oxfordjournals.pcp.a029377. [DOI] [PubMed] [Google Scholar]
  62. Salzberg S., Vilchik S., Cohen S., Heller A., Kronfeld-Kinar Y. Expression of a PKR dominant-negative mutant in myogenic cells interferes with the myogenic process. Exp Cell Res. 2000 Jan 10;254(1):45–54. doi: 10.1006/excr.1999.4721. [DOI] [PubMed] [Google Scholar]
  63. Sanchez J. C., Schaller D., Ravier F., Golaz O., Jaccoud S., Belet M., Wilkins M. R., James R., Deshusses J., Hochstrasser D. Translationally controlled tumor protein: a protein identified in several nontumoral cells including erythrocytes. Electrophoresis. 1997 Jan;18(1):150–155. doi: 10.1002/elps.1150180127. [DOI] [PubMed] [Google Scholar]
  64. Scherly D., Boelens W., van Venrooij W. J., Dathan N. A., Hamm J., Mattaj I. W. Identification of the RNA binding segment of human U1 A protein and definition of its binding site on U1 snRNA. EMBO J. 1989 Dec 20;8(13):4163–4170. doi: 10.1002/j.1460-2075.1989.tb08601.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Scheuner D., Song B., McEwen E., Liu C., Laybutt R., Gillespie P., Saunders T., Bonner-Weir S., Kaufman R. J. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell. 2001 Jun;7(6):1165–1176. doi: 10.1016/s1097-2765(01)00265-9. [DOI] [PubMed] [Google Scholar]
  66. Schroeder J. T., Lichtenstein L. M., MacDonald S. M. An immunoglobulin E-dependent recombinant histamine-releasing factor induces interleukin-4 secretion from human basophils. J Exp Med. 1996 Mar 1;183(3):1265–1270. doi: 10.1084/jem.183.3.1265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Scorsone K. A., Panniers R., Rowlands A. G., Henshaw E. C. Phosphorylation of eukaryotic initiation factor 2 during physiological stresses which affect protein synthesis. J Biol Chem. 1987 Oct 25;262(30):14538–14543. [PubMed] [Google Scholar]
  68. Shama S., Avni D., Frederickson R. M., Sonenberg N., Meyuhas O. Overexpression of initiation factor eIF-4E does not relieve the translational repression of ribosomal protein mRNAs in quiescent cells. Gene Expr. 1995;4(4-5):241–252. [PMC free article] [PubMed] [Google Scholar]
  69. Sharp T. V., Xiao Q., Jeffrey I., Gewert D. R., Clemens M. J. Reversal of the double-stranded-RNA-induced inhibition of protein synthesis by a catalytically inactive mutant of the protein kinase PKR. Eur J Biochem. 1993 Jun 15;214(3):945–948. doi: 10.1111/j.1432-1033.1993.tb17998.x. [DOI] [PubMed] [Google Scholar]
  70. Shi Y., Vattem K. M., Sood R., An J., Liang J., Stramm L., Wek R. C. Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol Cell Biol. 1998 Dec;18(12):7499–7509. doi: 10.1128/mcb.18.12.7499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Srivastava S. P., Davies M. V., 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. 1995 Jul 14;270(28):16619–16624. doi: 10.1074/jbc.270.28.16619. [DOI] [PubMed] [Google Scholar]
  72. Stürzenbaum S. R., Kille P., Morgan A. J. Identification of heavy metal induced changes in the expression patterns of the translationally controlled tumour protein (TCTP) in the earthworm Lumbricus rubellus1. Biochim Biophys Acta. 1998 Jul 9;1398(3):294–304. doi: 10.1016/s0167-4781(98)00077-3. [DOI] [PubMed] [Google Scholar]
  73. Tan S. L., Katze M. G. The emerging role of the interferon-induced PKR protein kinase as an apoptotic effector: a new face of death? J Interferon Cytokine Res. 1999 Jun;19(6):543–554. doi: 10.1089/107999099313677. [DOI] [PubMed] [Google Scholar]
  74. Terenzi F., deVeer M. J., Ying H., Restifo N. P., Williams B. R., Silverman R. H. The antiviral enzymes PKR and RNase L suppress gene expression from viral and non-viral based vectors. Nucleic Acids Res. 1999 Nov 15;27(22):4369–4375. doi: 10.1093/nar/27.22.4369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Thaw P., Baxter N. J., Hounslow A. M., Price C., Waltho J. P., Craven C. J. Structure of TCTP reveals unexpected relationship with guanine nucleotide-free chaperones. Nat Struct Biol. 2001 Aug;8(8):701–704. doi: 10.1038/90415. [DOI] [PubMed] [Google Scholar]
  76. Thiele H., Berger M., Lenzner C., Kühn H., Thiele B. J. Structure of the promoter and complete sequence of the gene coding for the rabbit translationally controlled tumor protein (TCTP) P23. Eur J Biochem. 1998 Oct 1;257(1):62–68. doi: 10.1046/j.1432-1327.1998.2570062.x. [DOI] [PubMed] [Google Scholar]
  77. Thiele H., Berger M., Skalweit A., Thiele B. J. Expression of the gene and processed pseudogenes encoding the human and rabbit translationally controlled tumour protein (TCTP). Eur J Biochem. 2000 Sep;267(17):5473–5481. doi: 10.1046/j.1432-1327.2000.01609.x. [DOI] [PubMed] [Google Scholar]
  78. Thomas G., Thomas G., Luther H. Transcriptional and translational control of cytoplasmic proteins after serum stimulation of quiescent Swiss 3T3 cells. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5712–5716. doi: 10.1073/pnas.78.9.5712. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Thomas G., Thomas G. Translational control of mRNA expression during the early mitogenic response in Swiss mouse 3T3 cells: identification of specific proteins. J Cell Biol. 1986 Dec;103(6 Pt 1):2137–2144. doi: 10.1083/jcb.103.6.2137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Thomis D. C., Samuel C. E. Mechanism of interferon action: evidence for intermolecular autophosphorylation and autoactivation of the interferon-induced, RNA-dependent protein kinase PKR. J Virol. 1993 Dec;67(12):7695–7700. doi: 10.1128/jvi.67.12.7695-7700.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Tian B., White R. J., Xia T., Welle S., Turner D. H., Mathews M. B., Thornton C. A. Expanded CUG repeat RNAs form hairpins that activate the double-stranded RNA-dependent protein kinase PKR. RNA. 2000 Jan;6(1):79–87. doi: 10.1017/s1355838200991544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Walsh B. J., Gooley A. A., Williams K. L., Breit S. N. Identification of macrophage activation associated proteins by two-dimensional gel electrophoresis and microsequencing. J Leukoc Biol. 1995 Mar;57(3):507–512. doi: 10.1002/jlb.57.3.507. [DOI] [PubMed] [Google Scholar]
  83. Williams B. R. PKR; a sentinel kinase for cellular stress. Oncogene. 1999 Nov 1;18(45):6112–6120. doi: 10.1038/sj.onc.1203127. [DOI] [PubMed] [Google Scholar]
  84. Willis A. E. Translational control of growth factor and proto-oncogene expression. Int J Biochem Cell Biol. 1999 Jan;31(1):73–86. doi: 10.1016/s1357-2725(98)00133-2. [DOI] [PubMed] [Google Scholar]
  85. Wu S., Kaufman R. J. A model for the double-stranded RNA (dsRNA)-dependent dimerization and activation of the dsRNA-activated protein kinase PKR. J Biol Chem. 1997 Jan 10;272(2):1291–1296. doi: 10.1074/jbc.272.2.1291. [DOI] [PubMed] [Google Scholar]
  86. Wu S., Kaufman R. J. Double-stranded (ds) RNA binding and not dimerization correlates with the activation of the dsRNA-dependent protein kinase (PKR). J Biol Chem. 1996 Jan 19;271(3):1756–1763. doi: 10.1074/jbc.271.3.1756. [DOI] [PubMed] [Google Scholar]
  87. Wu S., Rehemtulla A., Gupta N. K., Kaufman R. J. A eukaryotic translation initiation factor 2-associated 67 kDa glycoprotein partially reverses protein synthesis inhibition by activated double-stranded RNA-dependent protein kinase in intact cells. Biochemistry. 1996 Jun 25;35(25):8275–8280. doi: 10.1021/bi953028+. [DOI] [PubMed] [Google Scholar]
  88. Xiao Q., Sharp T. V., Jeffrey I. W., James M. C., Pruijn G. J., van Venrooij W. J., Clemens M. J. The La antigen inhibits the activation of the interferon-inducible protein kinase PKR by sequestering and unwinding double-stranded RNA. Nucleic Acids Res. 1994 Jul 11;22(13):2512–2518. doi: 10.1093/nar/22.13.2512. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Xu A., Bellamy A. R., Taylor J. A. Expression of translationally controlled tumour protein is regulated by calcium at both the transcriptional and post-transcriptional level. Biochem J. 1999 Sep 15;342(Pt 3):683–689. [PMC free article] [PubMed] [Google Scholar]
  90. Yan L., Fei K., Bridge D., Sarras M. P., Jr A cnidarian homologue of translationally controlled tumor protein (P23/TCTP). Dev Genes Evol. 2000 Oct;210(10):507–511. doi: 10.1007/s004270000088. [DOI] [PubMed] [Google Scholar]
  91. Yenofsky R., Bergmann I., Brawerman G. Messenger RNA species partially in a repressed state in mouse sarcoma ascites cells. Proc Natl Acad Sci U S A. 1982 Oct;79(19):5876–5880. doi: 10.1073/pnas.79.19.5876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Yenofsky R., Cereghini S., Krowczynska A., Brawerman G. Regulation of mRNA utilization in mouse erythroleukemia cells induced to differentiate by exposure to dimethyl sulfoxide. Mol Cell Biol. 1983 Jul;3(7):1197–1203. doi: 10.1128/mcb.3.7.1197. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from RNA are provided here courtesy of The RNA Society

RESOURCES