1887

Abstract

The movement protein (MP) of (ToMV) was reported previously by us to be phosphorylated by a cellular protein kinase(s) that exhibited several characteristics of casein kinase 2 (CK2). To characterize further this CK2-like cellular kinase, we have cloned cDNAs encoding the CK2 catalytic subunit from tobacco and compared the properties of the recombinant protein with those of the CK2-like cellular kinase. The recombinant CK2 catalytic subunit formed a complex with ToMV MP and phosphorylated it, similar to the CK2-like cellular kinase. Phosphoamino acid analyses of various mutant MPs altered near the C terminus revealed that the recombinant CK2 catalytic subunit phosphorylated serine-261, while the CK2-like cellular kinase phosphorylated both serine-261 and threonine-256. Both kinases were suggested to phosphorylate an additional serine residue(s) in regions other than the C-terminal peptide. The results are consistent with our previous prediction of involvement of CK2 in phosphorylation of ToMV MP.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.18839-0
2003-02-01
2020-01-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/84/2/vir840497.html?itemId=/content/journal/jgv/10.1099/vir.0.18839-0&mimeType=html&fmt=ahah

References

  1. Atabekov, J. G. & Taliansky, M. E. ( 1990; ). Expression of a plant virus-coded transport function by different viral genomes. Adv Virus Res 38, 201–248.
    [Google Scholar]
  2. Boyko, V., van der Laak, J., Ferralli, J., Suslova, E., Kwon, M. O. & Heinlein, M. ( 2000; ). Cellular targets of functional and dysfunctional mutants of tobacco mosaic virus movement protein fused to green fluorescent protein. J Virol 74, 11339–11346.[CrossRef]
    [Google Scholar]
  3. Citovsky, V., McLean, B. G., Zupan, J. R. & Zambryski, P. ( 1993; ). Phosphorylation of tobacco mosaic virus cell-to-cell movement protein by a developmentally regulated plant cell wall-associated protein kinase. Genes Dev 7, 904–910.[CrossRef]
    [Google Scholar]
  4. Dobrowolska, G., Boldyreff, B. & Issinger, O. G. ( 1991; ). Cloning and sequencing of the casein kinase 2 alpha subunit from Zea mays. Biochim Biophys Acta 1129, 139–140.[CrossRef]
    [Google Scholar]
  5. Dobrowolska, G., Meggio, F., Szczegielniak, J., Muszynska, G. & Pinna, L. A. ( 1992; ). Purification and characterization of maize seedling casein kinase IIB, a monomeric enzyme immunologically related to the alpha subunit of animal casein kinase-2. Eur J Biochem 204, 299–303.[CrossRef]
    [Google Scholar]
  6. Espunya, M. C., Combettes, B., Dot, J., Chaubet-Gigot, N. & Martinez, M. C. ( 1999; ). Cell-cycle modulation of CK2 activity in tobacco BY-2 cells. Plant J 19, 655–666.[CrossRef]
    [Google Scholar]
  7. Gafny, R., Lapidot, M., Berna, A., Holt, C. A., Deom, C. M. & Beachy, R. N. ( 1992; ). Effects of terminal deletion mutations on function of the movement protein of tobacco mosaic virus. Virology 187, 499–507.[CrossRef]
    [Google Scholar]
  8. Ghoshroy, S., Lartey, R., Sheng, J. & Citovsky, V. ( 1997; ). Transport of proteins and nucleic acids through plasmodesmata. Annu Rev Plant Physiol Plant Mol Biol 48, 27–50.[CrossRef]
    [Google Scholar]
  9. Guerra, B. & Issinger, O. G. ( 1999; ). Protein kinase CK2 and its role in cellular proliferation, development and pathology. Electrophoresis 20, 391–408.[CrossRef]
    [Google Scholar]
  10. Haley, A., Hunter, T., Kiberstis, P. & Zimmern, D. ( 1995; ). Multiple serine phosphorylation sites on the 30 kDa TMV cell-to-cell movement protein synthesized in tobacco protoplasts. Plant J 8, 715–724.[CrossRef]
    [Google Scholar]
  11. Kamps, M. A. & Sefton, B. M. ( 1989; ). Acid and base hydrolysis of phospho-proteins bound to Immobilon: a rapid technique for the analysis of phosphoamino acids in gel-fractionated proteins. Anal Biochem 176, 22–27.[CrossRef]
    [Google Scholar]
  12. Karpova, O. V., Rodionova, N. P., Ivanov, K. I., Kozlovsky, S. V., Dorokhov, Y. L. & Atabekov, J. G. ( 1999; ). Phosphorylation of tobacco mosaic virus movement protein abolishes its translation repressing ability. Virology 261, 20–24.[CrossRef]
    [Google Scholar]
  13. Kawakami, S., Padgett, H. S., Hosokawa, D., Okada, Y., Beachy, R. N. & Watanabe, Y. ( 1999; ). Phosphorylation and/or presence of serine 37 in the movement protein of tomato mosaic tobamovirus is essential for intracellular localization and stability in vivo. J Virol 73, 6831–6840.
    [Google Scholar]
  14. Kingston, R. E. ( 1997; ). Phenol/SDS method for plant RNA preparation. In Current Protocols in Molecular Biology, vol. 1, pp. 4.3.1–4.3.3. Edited by V. B. Chanda. New York: John Wiley & Sons.
  15. Lee, J. Y & Lucas, W. J. ( 2001; ). Phosphorylation of viral movement proteins: regulation of cell-to-cell trafficking. Trends Microbiol 9, 5–8.[CrossRef]
    [Google Scholar]
  16. Lozeman, F. J., Litchfield, D. W., Piening, C., Takio, K., Walsh, K. & Krebs, E. G. ( 1990; ). Isolation and characterization of human cDNA clones encoding the alpha and alpha′ subunits of casein kinase II. Biochemistry 29, 8436–8447.[CrossRef]
    [Google Scholar]
  17. Lucas, W. J. & Gilbertson, R. L. ( 1994; ). Plasmodesmata in relation to viral movement within leaf tissues. Annu Rev Phytopathol 32, 387–411.[CrossRef]
    [Google Scholar]
  18. Marin, O., Sarno, S., Boschetti, M., Pagano, M. A., Meggio, F., Ciminale, V., D'Agostino, D. M. & Pinna, L. A. ( 2000; ). Unique features of HIV-1 Rev protein phosphorylation by protein kinase CK2 (‘casein kinase-2’). FEBS Lett 481, 63–67.[CrossRef]
    [Google Scholar]
  19. Matsushita, Y., Hanazawa, K., Yoshioka, K., Oguchi, T., Kawakami, S., Watanabe, Y., Nishiguchi, M. & Nyunoya, H. ( 2000).; In vitro phosphorylation of the movement protein of tomato mosaic tobamovirus by a cellular kinase. J Gen Virol 81 , 2095 –2102.
    [Google Scholar]
  20. Matsushita, Y., Deguchi, M., Youda, M., Nishiguchi, M. & Nyunoya, H. ( 2001; ). The tomato mosaic tobamovirus movement protein interacts with a putative transcriptional coactivator KELP. Mol Cells 12, 57–66.
    [Google Scholar]
  21. Matsushita, Y., Yoshioka, K., Shigyo, T., Takahashi, H. & Nyunoya, H. ( 2002; ). Phosphorylation of the movement protein of Cucumber mosaic virus in transgenic tobacco plants. Virus Genes 24, 231–234.[CrossRef]
    [Google Scholar]
  22. Meggio, F., Marin, O. & Pinna, L. A. ( 1994; ). Substrate specificity of protein kinase CK2. Cell Mol Biol Res 40, 401–409.
    [Google Scholar]
  23. Melcher, U. ( 2000; ). The ‘30K’ superfamily of viral movement proteins. J Gen Virol 81, 257–266.
    [Google Scholar]
  24. Mizoguchi, T., Yamaguchi-Shinozaki, K., Hayashida, N., Kamada, H. & Shinozaki, K. ( 1993; ). Cloning and characterization of two cDNAs encoding casein kinase II catalytic subunits in Arabidopsis thaliana. Plant Mol Biol 21, 279–289.[CrossRef]
    [Google Scholar]
  25. Nagata, T., Okada, K., Takebe, I. & Matsui, C. ( 1981; ). Delivery of tobacco mosaic virus RNA into plant protoplasts mediated by reverse-phase evaporation vesicles (Liposomes). Mol Gen Genet 184, 161–165.
    [Google Scholar]
  26. Padgett, H. S., Epel, B. L., Kahn, T. W., Heinlein, M., Watanabe, Y. & Beachy, R. N. ( 1996; ). Distribution of tobamovirus movement protein in infected cells and implications for cell-to-cell spread of infection. Plant J 10, 1079–1088.[CrossRef]
    [Google Scholar]
  27. Padmanabha, R., Chen-Wu, J. L.-P., Hanna, D. E. & Glover, C. V. C. ( 1990; ). Isolation, sequencing, and disruption of the yeast CKA2 gene: casein kinase II is essential for viability in Saccharomyces cerevisiae. Mol Cell Biol 10, 4089–4099.
    [Google Scholar]
  28. Pearson, R. B. & Kemp, B. E. ( 1991; ). Protein kinase phosphorylation site sequences and consensus specificity motifs: tabulations. Methods Enzymol 200, 62–81.
    [Google Scholar]
  29. Peracchia, G., Jensen, A. B., Culianez-Macia, F. A., Grosset, J., Goday, A., Issinger, O. G. & Pagès, M. ( 1999; ). Characterization, subcellular localization and nuclear targeting of casein kinase 2 from Zea mays. Plant Mol Biol 40, 199–211.[CrossRef]
    [Google Scholar]
  30. Riera, M., Peracchia, G., de Nadal, E., Ariño, J. & Pagès, M. ( 2001; ). Maize protein kinase CK2: regulation and functionality of three beta regulatory subunits. Plant J 25, 365–374.[CrossRef]
    [Google Scholar]
  31. Sassa, N., Matsushita, Y., Nakamura, T. & Nyunoya, H. ( 2001; ). The molecular characterization and in situ expression pattern of pea SCARECROW gene. Plant Cell Physiol 42, 385–394.[CrossRef]
    [Google Scholar]
  32. Seron, K., Bernasconi, L., Allet, B. & Haenni, A. L. ( 1996; ). Expression of the 69K movement protein of turnip yellow mosaic virus in insect cells. Virology 219, 274–278.[CrossRef]
    [Google Scholar]
  33. Sokolova, M., Prufer, D., Tacke, E. & Rohde, W. ( 1997; ). The potato leafroll virus 17K movement protein is phosphorylated by a membrane-associated protein kinase from potato with biochemical features of protein kinase C. FEBS Lett 400, 201–205.[CrossRef]
    [Google Scholar]
  34. Takahashi, Y., Shomura, A., Sasaki, T. & Yano, M. ( 2001; ). Hd6, a rice quantitative trait locus involved in photoperiod sensitivity, encodes the alpha subunit of protein kinase CK2. Proc Natl Acad Sci U S A 98, 7922–7927.[CrossRef]
    [Google Scholar]
  35. Waigmann, E., Chen, M. H., Bachmaier, R., Ghoshroy, S. & Citovsky, V. ( 2000; ). Regulation of plasmodesmal transport by phosphorylation of tobacco mosaic virus cell-to-cell movement protein. EMBO J 19, 4875–4884.[CrossRef]
    [Google Scholar]
  36. Watanabe, Y., Ogawa, T. & Okada, Y. ( 1992; ). In vivo phosphorylation of the 30-kDa protein of tobacco mosaic virus. FEBS Lett 313, 181–184.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.18839-0
Loading
/content/journal/jgv/10.1099/vir.0.18839-0
Loading

Data & Media loading...

Most cited articles

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error