Expression of pokeweed antiviral protein in mammalian cells activates c-Jun NH2-terminal kinase without causing apoptosis

International Journal of Biochemistry and Cell Biology

Volumn 40, Issue 11, 2008, Pages 2452-2461

  Chan Tung, Kelvin W ^a   Mansouri, Sheila ^a   Hudak, Katalin A ^a  

^a YORK UNIVERSITY   (Canada)

Author keywords

Apoptosis; c Jun NH2 terminal kinase; Pokeweed antiviral protein; Ribosome inactivating protein; Ribotoxic stress response

Indexed keywords

CASPASE 3; POKEWEED ANTIVIRUS PROTEIN; POLY(ADENOSINE DIPHOSPHATE RIBOSE); RIBOSOME RNA; STRESS ACTIVATED PROTEIN KINASE;

ANTIVIRAL ACTIVITY; APOPTOSIS; ARTICLE; CELL DEATH; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MAMMAL CELL; MEMBRANE PERMEABILITY; PROTEIN EXPRESSION; RIBOSOME; SIGNAL TRANSDUCTION; STAINING; STRESS;

ANIMALS; APOPTOSIS; CELL LINE; ENZYME ACTIVATION; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; PEPTIDE ELONGATION FACTOR 2; PHYTOLACCA AMERICANA; PLANT PROTEINS; PROTEIN BIOSYNTHESIS; PROTEIN SYNTHESIS INHIBITORS; RIBOSOME INACTIVATING PROTEINS, TYPE 1; RIBOSOMES; RNA, RIBOSOMAL, 28S;

MAMMALIA; PHYTOLACCA AMERICANA; PHYTOLACCACEAE;

EID: 48349120147     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2008.04.021     Document Type: Article

References (50)

1. Almeida E.A., Ilić D., Han Q., Hauck C.R., Jin F., Kawakatsu H., Schlaepfer D.D., and Damsky C.H. Matrix survival signaling: from fibronectin via focal adhesion kinase to c-Jun NH(2)-terminal kinase. Journal of Cell Biology 149 (2000) 741-754
2. Anderson P. Kinase cascades regulating entry into apoptosis. Microbiology and Molecular Biology Reviews 61 (1997) 33-46
3. Battelli M.G. Cytotoxicity and toxicity to animals and humans of ribosome-inactivating proteins. Mini Reviews in Medicinal Chemistry 4 (2004) 513-521
4. Boatright K.M., Renatus M., Scott F.L., Sperandio S., Shin H., Pedersen I.M., Ricci J.E., Edris W.A., Sutherlin D.P., Green D.R., and Salvesen G.S. A unified model for apical caspase activation. Molecular Cell 11 (2003) 529-541
5. Boulares A.H., Yakovlev A.G., Ivanova V., Stoica B.A., Wang G., Iyer S., and Smulson M. Role of poly(ADP-ribose) polymerase (PARP) cleavage in apoptosis. Caspase 3-resistant PARP mutant increases rates of apoptosis in transfected cells. Journal of Biological Chemistry 274 (1999) 22932-22940
6. Brigotti M., Rambelli F., Zamboni M., Montanaro L., and Sperti S. Effect of alpha sarcin and ribosome-inactivating proteins on the interaction of elongation factors with ribosomes. Biochemical Journal 257 (1989) 723-727
7. Carlberg U., Nilsson A., and Nygård O. Functional properties of phosphorylated elongation factor 2. European Journal of Biochemistry 191 (1990) 639-645
8. Chen C.A., and Okayama H. Calcium phosphate-mediated gene transfer: a highly efficient transfection system for stably transforming cells with plasmid DNA. Biotechniques 6 (1988) 632-638
9. Chow C.-W., Rincon M., Cavanagh J., Dickens M., and Davis R.J. Nuclear accumulation of NFAT4 opposed by the JNK signal transduction pathway of special interest. Science 278 (1997) 1638-1641
10. Davis R.J. Signal transduction by the JNK group of MAP kinases. Cell 103 (2000) 239-252
11. Endo Y., Tsurugi K., and Lambert J.M. The site of action of six different ribosome-inactivating proteins from plants on eukaryotic ribosomes: the RNA N-glycosidase activity of the proteins. Biochemical and Biophysical Research Communications 150 (1988) 1032-1036
12. Er E., Oliver L., Cartron P.F., Juin P., Manon S., and Vallette F.M. Mitochondria as the target of the pro-apoptotic protein Bax. Biochimica et Biophysica Acta 1757 (2006) 1301-1311
13. Foa-Tomasi L., Campadelli-Fiume G., Barbieri L., and Stirpe F. Effect of ribosome-inactivating proteins on virus-infected cells. Inhibition of virus multiplication and of protein synthesis. Archives of Virology 71 (1982) 323-332
14. Gan Y.H., Peng S.Q., and Liu H.Y. Molecular mechanism of apoptosis induced by ricin in HeLa cells. Acta Pharmacologia Sinica 21 (2000) 243-248
15. Gessner S.L., and Irvin J.D. Inhibition of elongation factor 2-dependent translocation by the pokeweed antiviral protein and ricin. Journal of Biological Chemistry 255 (1980) 3251-3253
16. Griffiths G.D., Leek M.D., and Gee D.J. The toxic plant proteins ricin and abrin induce apoptotic changes in mammalian lymphoid tissues and intestine. Journal of Pathology 151 (1987) 221-229
17. Hudak K.A., Wang P., and Tumer N.E. A novel mechanism for inhibition of translation by pokeweed antiviral protein: depurination of the capped RNA template. RNA 6 (2000) 369-380
18. Hur Y., Hwang D.J., Zoubenko O., Coetzer C., Uckun F.M., and Tumer N.E. Isolation and characterization of pokeweed antiviral protein mutations in Saccharomyces cerevisiae: identification of residues important for toxicity. Proceedings of the National Academy of Sciences of the United States of America 92 (1995) 8448-8452
19. Ip Y.T., and Davis R.J. Signal transduction by the c-Jun N-terminal kinase (JNK)-from inflammation to development. Current Opinion in Cell Biology 10 (1998) 205-219
20. Iordanov M.S., Pribnow D., Magun J.L., Dinh T.-H., Pearson J.A., Chen S.L.-Y., and Magun B.E. Ribotoxic stress response: activation of the stress-activated protein kinase JNK1 by inhibitors of the peptidyl transferase reaction and by sequence-specific RNA damage to the α-sarcin/ricin loop in the 28S rRNA. Molecular and Cellular Biology 17 (1997) 3373-3381
21. Iordanov M.S., Pribnow D., Magun J.L., Dinh T.H., Pearson J.A., and Magun B.E. Ultraviolet radiation triggers the ribotoxic stress response in mammalian cells. Journal of Biological Chemistry 273 (1998) 15794-157803
22. Kawasaki H., Schiltz L., Chiu R., Itakura K., Taira K., Nakatani Y., and Yokoyama K.K. ATF-2 has intrinsic histone acetyltransferase activity which is modulated by phosphorylation. Nature 405 (2000) 195-200
23. Knebel A., Morrice N., and Cohen P. A novel method to identify protein kinase substrates: eEF2 kinase is phosphorylated and inhibited by SAPK4/p38delta. EMBO Journal 20 (2001) 4360-4369
24. Lee K.H., Nishimura S., Matsunaga S., Fusetani N., Horinouchi S., and Yoshida M. Inhibition of protein synthesis and activation of stress-activated protein kinases by onnamide A and theopederin B, antitumor marine natural products. Cancer Science 96 (2005) 357-364
25. Liu J., and Lin A. Role of JNK activation in apoptosis: a double-edged sword. Cell Research 15 (2005) 36-42
26. Lodge J.K., Kaniewski W.K., and Tumer N.E. Broad-spectrum virus resistance in transgenic plants expressing pokeweed antiviral protein. Proceedings of the National Academy of Sciences of the United States of America 90 (1993) 7089-7093
27. Mansouri S., Nourollahzadeh E., and Hudak K.A. Pokeweed antiviral protein depurinates the sarcin/ricin loop of the rRNA prior to binding of aminoacyl-tRNA to the ribosomal A-site. RNA 12 (2006) 1683-1692
28. Moazed D., Robertson J.M., and Noller H.F. Interaction of elongation factors EF-G and EF-Tu with a conserved loop in 23S RNA. Nature 334 (1988) 362-364
29. Narayanan S., Surolia A., and Karande A.A. Ribosome-inactivating protein and apoptosis: abrin causes cell death via mitochondrial pathway in Jurkat cells. Biochemical Journal 377 (2004) 233-240
30. Nilsson L., and Nygard O. The mechanism of the protein-synthesis elongation cycle in eukaryotes. Effect of ricin on the ribosomal interaction with elongation factors. European Journal of Biochemistry 161 (1986) 111-117
31. Obrig T.G., Irvin J.D., and Hardesty B. The effect of an antiviral peptide on the ribosomal reactions of the peptide elongation enzymes, EF-I and EF-II. Archives of Biochemistry and Biophysics 155 (1973) 278-289
32. Ouyang D.Y., Wang Y.Y., and Zheng Y.T. Activation of c-Jun N-terminal kinases by ribotoxic stresses. Cellular and Molecular Immunology 2 (2005) 419-425
33. Parikh B.A., Coetzer C., and Tumer N.E. Pokeweed antiviral protein regulates the stability of its own mRNA by a mechanism that requires depurination but can be separated from depurination of the alpha-sarcin/ricin loop of rRNA. Journal of Biological Chemistry 277 (2002) 41428-41437
34. Pearson G., Robinson F., Beers Gibson T., Xu B.E., Karandikar M., Berman K., and Cobb M.H. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocrine Reviews 22 (2001) 153-183
35. Picard D., Kao C.C., and Hudak K.A. Pokeweed antiviral protein inhibits brome mosaic virus replication in plant cells. Journal of Biological Chemistry 280 (2005) 20069-20075
36. Pulverer B.J., Kyriakis J.M., Avruch J., Nikolakaki E., and Woodgett J.R. Phosphorylation of c-jun mediated by MAP kinases. Nature 353 (1991) 670-674
37. Rajamohan F., Venkatachalam T.K., Irvin J.D., and Uckun F.M. Pokeweed antiviral protein isoforms PAP-I, PAP-II, and PAP-III depurinate RNA of human immunodeficiency virus (HIV)-1. Biochemical and Biophysical Research Communications 260 (1999) 453-458
38. Reinhard C., Shamoon B., Shyamala V., and Williams L.T. Tumor necrosis factor alpha-induced activation of c-jun N-terminal kinase is mediated by TRAF2. EMBO Journal 16 (1997) 1080-1092
39. Rodnina M.V., Savelsbergh A., Katunin V.I., and Wintermeyer W. Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome. Nature 385 (1997) 37-41
40. Ryazanov A.G., and Davydova E.K. Mechanism of elongation factor 2 (EF-2) inactivation upon phosphorylation. Phosphorylated EF-2 is unable to catalyze translocation. FEBS Letters 251 (1989) 187-190
41. Shaw P.C., Lee K.M., and Wong K.B. Recent advances in trichosanthin, a ribosome-inactivating protein with multiple pharmacological properties. Toxicon 45 (2005) 683-689
42. Shifrin V.I., and Anderson P. Trichothecene mycotoxins trigger a ribotoxic stress response that activates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase and induces apoptosis. Journal of Biological Chemistry 274 (1999) 13985-13992
43. Stirpe F., Bailey S., Miller S.P., and Bodley J.W. Modification of ribosomal RNA by ribosome-inactivating proteins from plants. Nucleic Acids Research 16 (1988) 405-412
44. Teltow G.J., Irvin J.D., and Aron G.M. Inhibition of herpes simplex virus DNA synthesis by pokeweed antiviral protein. Antimicrobial Agents and Chemotherapy 23 (1983) 390-396
45. Tomlinson J.A., Walker V.M., Flewtett T.H., and Barclay G.R. The inhibition of infection by cucumber mosaic virus and influenza virus by extracts from Phytolacca americana. Journal of General Virology 22 (1974) 225-232
46. Tournier C., Whitmarsh A.J., Cavanagh J., Barrett T., and Davis R.J. Mitogen-activated protein kinase kinase 7 is an activator of the c-Jun NH2-terminal kinase. Proceedings of the National Academy of Sciences of the United States of America 94 (1997) 7337-7342
47. Tumer N.E., Hwang D.J., and Bonness M. C-terminal deletion mutant of pokeweed antiviral protein inhibits viral infection but does not depurinate host ribosomes. Proceedings of the National Academy of Sciences of the United States of America 94 (1997) 3866-3871
48. Ussery M.A., Irvin J.D., and Hardesty B. Inhibition of poliovirus replication by a plant antiviral peptide. Annals of the New York Academy of Sciences 284 (1977) 431-440
49. VanBogelen R., and Neidhardt F.C. Ribosomes as sensors of heat and cold shock in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 87 (1990) 5589-5593
50. Zarling J.M., Moran P.A., Haffar O., Sias J., Richman D.D., Spina C.A., Myers D.E., Kuebelbeck V., Ledbetter J.A., and Uckun F.M. Inhibition of HIV replication by pokeweed antiviral protein targeted to CD4+ cells by monoclonal antibodies. Nature 347 (1990) 92-95