1887

Abstract

The proteasome is a multicatalytic complex involved in many cellular processes in eukaryotes, such as protein and RNA turnover, cell division, signal transduction, transcription and translation. Intracellular pathogens are targets of its enzymic activities, and a number of animal viruses are known to interfere with these activities. The first evidence that a plant virus protein, the helper component-proteinase (HcPro) of (LMV; genus ), interferes with the 20S proteasome ribonuclease is reported here. LMV infection caused an aggregation of the 20S proteasome to high-molecular mass structures , and specific binding of HcPro to the proteasome was confirmed using two different approaches. HcPro inhibited the 20S endonuclease activity , while its proteolytic activities were unchanged or slightly stimulated. This ability of HcPro, a pathogenicity regulator of potyviruses, to interfere with some of the catalytic functions of the 20S proteasome suggests the existence of a novel type of defence and counter-defence interplay in the course of interaction between potyviruses and their hosts.

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2005-09-01
2019-11-22
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References

  1. Anandalakshmi, R., Pruss, G. J., Ge, X., Marathe, R., Mallory, A. C., Smith, T. H. & Vance, V. B. ( 1998; ). A viral suppressor of gene silencing in plants. Proc Natl Acad Sci U S A 95, 13079–13084.[CrossRef]
    [Google Scholar]
  2. Anandalakshmi, R., Marathe, R., Ge, X., Herr, J. M., Jr, Mau, C., Mallory, A., Pruss, G., Bowman, L. & Vance, V. B. ( 2000; ). A calmodulin-related protein that suppresses posttranscriptional gene silencing in plants. Science 290, 142–144.[CrossRef]
    [Google Scholar]
  3. Apcher, G. S., Heink, S., Zantopf, D., Kloetzel, P. M., Schmid, H. P., Mayer, R. J. & Kruger, E. ( 2003; ). Human immunodeficiency virus-1 Tat protein interacts with distinct proteasomal α and β subunits. FEBS Lett 553, 200–204.[CrossRef]
    [Google Scholar]
  4. Aronson, M. N., Meyer, A. D., Gyorgyey, J., Katul, L., Vetten, H. J., Gronenborn, B. & Timchenko, T. ( 2000; ). Clink, a nanovirus-encoded protein, binds both pRB and SKP1. J Virol 74, 2967–2972.[CrossRef]
    [Google Scholar]
  5. Ballut, L., Petit, F., Mouzeyar, S., Le Gall, O., Candresse, T., Schmid, P., Nicolas, P. & Badaoui, S. ( 2003; ). Biochemical identification of proteasome-associated endonuclease activity in sunflower. Biochim Biophys Acta 1645, 30–39.[CrossRef]
    [Google Scholar]
  6. Blanc, S., Ammar, E. D., Garcia-Lampasona, S., Dolja, V. V., Llave, C., Baker, J. & Pirone, T. P. ( 1998; ). Mutations in the potyvirus helper component protein: effects on interactions with virions and aphid stylets. J Gen Virol 79, 3119–3122.
    [Google Scholar]
  7. Brigneti, G., Voinnet, O., Li, W. X., Ji, L. H., Ding, S. W. & Baulcombe, D. C. ( 1998; ). Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J 17, 6739–6746.[CrossRef]
    [Google Scholar]
  8. Carrington, J. C. & Herndon, K. L. ( 1992; ). Characterization of the potyviral HC-pro autoproteolytic cleavage site. Virology 187, 308–315.[CrossRef]
    [Google Scholar]
  9. Carrington, J. C., Freed, D. D. & Sanders, T. C. ( 1989; ). Autocatalytic processing of the potyvirus helper component proteinase in Escherichia coli and in vitro. J Virol 63, 4459–4463.
    [Google Scholar]
  10. Carrington, J. C., Freed, D. D. & Oh, C. S. ( 1990; ). Expression of potyviral polyproteins in transgenic plants reveals three proteolytic activities required for complete processing. EMBO J 9, 1347–1353.
    [Google Scholar]
  11. Ciechanover, A. & Schwartz, A. L. ( 1998; ). The ubiquitin-proteasome pathway: the complexity and myriad functions of proteins death. Proc Natl Acad Sci U S A 95, 2727–2730.[CrossRef]
    [Google Scholar]
  12. Coux, O., Tanaka, K. & Goldberg, A. L. ( 1996; ). Structure and functions of the 20S and 26S proteasomes. Annu Rev Biochem 65, 801–847.[CrossRef]
    [Google Scholar]
  13. Dahlmann, B., Kopp, F., Kuehn, L., Hegerl, R., Pfeifer, G. & Baumeister, W. ( 1991; ). The multicatalytic proteinase (prosome, proteasome): comparison of the eukaryotic and archaebacterial enzyme. Biomed Biochim Acta 50, 465–469.
    [Google Scholar]
  14. Dolja, V. V., Herndon, K. L., Pirone, T. P. & Carrington, J. C. ( 1993; ). Spontaneous mutagenesis of a plant potyvirus genome after insertion of a foreign gene. J Virol 67, 5968–5975.
    [Google Scholar]
  15. Drugeon, G. & Jupin, I. ( 2002; ). Stability in vitro of the 69K movement protein of Turnip yellow mosaic virus is regulated by the ubiquitin-mediated proteasome pathway. J Gen Virol 83, 3187–3197.
    [Google Scholar]
  16. Dunand-Sauthier, I., Walker, C., Wilkinson, C., Gordon, C., Crane, R., Norbury, C. & Humphrey, T. ( 2002; ). Sum1, a component of the fission yeast eIF3 translation initiation complex, is rapidly relocalized during environmental stress and interacts with components of the 26S proteasome. Mol Biol Cell 13, 1626–1640.[CrossRef]
    [Google Scholar]
  17. Gautier-Bert, K., Murol, B., Jarrousse, A. S., Ballut, L., Badaoui, S., Petit, F. & Schmid, H. P. ( 2003; ). Substrate affinity and substrate specificity of proteasomes with RNase activity. Mol Biol Rep 30, 1–7.[CrossRef]
    [Google Scholar]
  18. German-Retana, S., Candresse, T., Alias, E., Delbos, R. P. & Le Gall, O. ( 2000; ). Effects of green fluorescent protein or beta-glucuronidase tagging on the accumulation and pathogenicity of a resistance-breaking Lettuce mosaic virus isolate in susceptible and resistant lettuce cultivars. Mol Plant Microbe Interact 13, 316–324.[CrossRef]
    [Google Scholar]
  19. Govier, D. A., Kassanis, B. & Pirone, T. P. ( 1977; ). Partial purification and characterization of the potato virus Y helper component. Virology 78, 306–314.[CrossRef]
    [Google Scholar]
  20. Guo, D., Spetz, C., Saarma, M. & Valkonen, J. P. ( 2003; ). Two potato proteins, including a novel RING finger protein (HIP1), interact with the potyviral multifunctional protein HCpro. Mol Plant Microbe Interact 16, 405–410.[CrossRef]
    [Google Scholar]
  21. Hazelwood, D. & Zaitlin, M. ( 1990; ). Ubiquitinated conjugates are found in preparations of several plant viruses. Virology 177, 352–356.[CrossRef]
    [Google Scholar]
  22. Hericourt, F., Blanc, S., Redeker, V. & Jupin, I. ( 2000; ). Evidence for phosphorylation and ubiquitinylation of the turnip yellow mosaic virus RNA-dependent RNA polymerase domain expressed in a baculovirus-insect cell system. Biochem J 349, 417–425.[CrossRef]
    [Google Scholar]
  23. Homma, S., Horsch, A., Pouch, M. N., Petit, F., Briand, Y. & Schmid, H. P. ( 1994; ). Proteasomes (prosomes) inhibit the translation of tobacco mosaic virus RNA by preventing the formation of initiation complexes. Mol Biol Rep 20, 57–61.[CrossRef]
    [Google Scholar]
  24. Hu, Z., Zhang, Z., Doo, E., Coux, O., Goldberg, A. L. & Liang, T. J. ( 1999; ). Hepatitis B virus X protein is both a substrate and a potential inhibitor of the proteasome complex. J Virol 73, 7231–7240.
    [Google Scholar]
  25. Janeway, C. A., Jr ( 2001; ). How the immune system works to protect the host from infection: a personal view. Proc Natl Acad Sci U S A 98, 7461–7468.[CrossRef]
    [Google Scholar]
  26. Jockusch, H. & Wiegand, C. ( 2003; ). Misfolded plant virus proteins: elicitors and targets of ubiquitylation. FEBS Lett 545, 229–232.[CrossRef]
    [Google Scholar]
  27. Karsies, A., Merkle, T., Szurek, B., Bonas, U., Hohn, T. & Leclerc, D. ( 2002; ). Regulated nuclear targeting of cauliflower mosaic virus. J Gen Virol 83, 1783–1790.
    [Google Scholar]
  28. Kasschau, K. D. & Carrington, J. C. ( 1998; ). A counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing. Cell 95, 461–470.[CrossRef]
    [Google Scholar]
  29. Kasschau, K. D., Xie, Z., Allen, E., Llave, C., Chapman, E. J., Krizan, K. A. & Carrington, J. C. ( 2003; ). P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev Cell 4, 205–217.[CrossRef]
    [Google Scholar]
  30. Kremp, A., Schliephacke, M., Kull, U. & Schmid, H. P. ( 1986; ). Prosomes exist in plant cells too. Exp Cell Res 166, 553–557.[CrossRef]
    [Google Scholar]
  31. Laemmli, U. K. ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.[CrossRef]
    [Google Scholar]
  32. Llave, C., Kasschau, K. D. & Carrington, J. C. ( 2000; ). Virus-encoded suppressor of posttranscriptional gene silencing targets a maintenance step in the silencing pathway. Proc Natl Acad Sci U S A 97, 13401–13406.[CrossRef]
    [Google Scholar]
  33. Maia, I. G. & Bernardi, F. ( 1996; ). Nucleic acid-binding properties of a bacterially expressed potato virus Y helper component-proteinase. J Gen Virol 77, 869–877.[CrossRef]
    [Google Scholar]
  34. Maia, I. G., Haenni, A.-L. & Bernardi, F. ( 1996; ). Potyviral HC-Pro: a multifunctional protein. J Gen Virol 77, 1335–1341.[CrossRef]
    [Google Scholar]
  35. Mallory, A. C., Reinhart, B. J., Bartel, D., Vance, V. B. & Bowman, L. H. ( 2002; ). A viral suppressor of RNA silencing differentially regulates the accumulation of short interfering RNAs and micro-RNAs in tobacco. Proc Natl Acad Sci U S A 99, 15228–15233.[CrossRef]
    [Google Scholar]
  36. Merits, A., Guo, D., Jarvekulg, L. & Saarma, M. ( 1999; ). Biochemical and genetic evidence for interactions between potato A potyvirus-encoded proteins P1 and P3 and proteins of the putative replication complex. Virology 263, 15–22.[CrossRef]
    [Google Scholar]
  37. Petit, F., Kreutzer-Schmid, C., Gautier, K., Jarrousse, A. S., Badaoui, S. & Schmid, H. P. ( 2000; ). The proteasome in post-transcriptional control: a protease with endonuclease activity? In Proteasomes: the World of the Regulatory Proteolysis, pp. 377–384. Edited by W. Hilt & D. H. Wolf. Georgetown, TX: Landes Bioscience.
  38. Plisson, C., Drücker, M., Blanc, S., German-Retana, S., Le Gall, O., Thomas, D. & Bron, P. ( 2003; ). Structural characterization of HC-Pro, a plant virus multifunctional protein. J Biol Chem 278, 23753–23761.[CrossRef]
    [Google Scholar]
  39. Pollard-Knight, D., Hawkins, E., Yeung, D., Pashby, D. P., Simpson, M., McDougall, A., Buckle, P. & Charles, S. A. ( 1990; ). Immunoassays and nucleic acid detection with a biosensor based on surface plasmon resonance. Ann Biol Clin 48, 642–646.
    [Google Scholar]
  40. Pruss, G., Ge, X., Shi, X. M., Carrington, J. C. & Bowman Vance, V. ( 1997; ). Plant viral synergism: the potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. Plant Cell 9, 859–868.[CrossRef]
    [Google Scholar]
  41. Rechsteiner, M., Realini, C. & Ustrell, V. ( 2000; ). The proteasome activator 11 S REG (PA28) and class I antigen presentation. Biochem J 345, 1–15.[CrossRef]
    [Google Scholar]
  42. Redondo, E., Krause-Sakate, R., Yang, S. J., Lot, H., Le Gall, O. & Candresse, T. ( 2001; ). Lettuce mosaic virus (LMV) pathogenicity determinants in susceptible and tolerant lettuce varieties map to different regions of the viral genome. Mol Plant Microbe Interact 14, 804–810.[CrossRef]
    [Google Scholar]
  43. Reichel, C. & Beachy, R. N. ( 2000; ). Degradation of tobacco mosaic virus movement protein by the 26S proteasome. J Virol 74, 3330–3337.[CrossRef]
    [Google Scholar]
  44. Reinstein, E., Scheffner, M., Oren, M., Ciechanover, A. & Schwartz, A. ( 2000; ). Degradation of the E7 human papillomavirus oncoprotein by the ubiquitin-proteasome system: targeting via ubiquitination of the N-terminal residue. Oncogene 19, 5944–5950.[CrossRef]
    [Google Scholar]
  45. Rojas, M. R., Zerbini, F. M., Allison, R. F., Gilbertson, R. L. & Lucas, W. J. ( 1997; ). Capsid protein and helper component-proteinase function as potyvirus cell-to-cell movement proteins. Virology 237, 283–295.[CrossRef]
    [Google Scholar]
  46. Roudet-Tavert, G., German-Retana, S., Delaunay, T., Delecolle, B., Candresse, T. & Le Gall, O. ( 2002; ). Interaction between potyvirus helper component-proteinase and capsid protein in infected plants. J Gen Virol 83, 1765–1770.
    [Google Scholar]
  47. Saenz, P., Salvador, B., Simon-Mateo, C., Kasschau, K. D., Carrington, J. C. & Garcia, J. A. ( 2002; ). Host-specific involvement of the HC protein in the long-distance movement of potyviruses. J Virol 76, 1922–1931.[CrossRef]
    [Google Scholar]
  48. Schliephacke, M., Kremp, A., Schmid, H. P., Kohler, K. & Kull, U. ( 1991; ). Prosomes (proteasomes) of higher plants. Eur J Cell Biol 55, 114–121.
    [Google Scholar]
  49. Seeger, M., Ferrell, K., Frank, R. & Dubiel, W. ( 1997; ). HIV-1 tat inhibits the 20S proteasome and its 11S regulator-mediated activation. J Biol Chem 272, 8145–8148.[CrossRef]
    [Google Scholar]
  50. Tang, G., Reinhart, B. J., Bartel, D. P. & Zamore, P. D. ( 2003; ). A biochemical framework for RNA silencing in plants. Genes Dev 17, 49–63.[CrossRef]
    [Google Scholar]
  51. Thornbury, D. W., Hellmann, G. M., Rhoads, R. E. & Pirone, T. P. ( 1985; ). Purification and characterization of potyvirus helper component. Virology 144, 260–267.[CrossRef]
    [Google Scholar]
  52. Unno, M., Mizushima, T., Morimoto, Y., Tomisugi, Y., Tanaka, K., Yasuoka, N. & Tsukihara, T. ( 2002; ). The structure of the mammalian 20S proteasome at 2·75 Å resolution. Structure 10, 609–618.[CrossRef]
    [Google Scholar]
  53. Urcuqui-Inchima, S., Walter, J., Drugeon, G., German-Retana, S., Haenni, A. L., Candresse, T., Bernardi, F. & Le Gall, O. ( 1999; ). Potyvirus helper component-proteinase self-interaction in the yeast two-hybrid system and delineation of the interaction domain involved. Virology 258, 95–99.[CrossRef]
    [Google Scholar]
  54. Voinnet, O. ( 2001; ). RNA silencing as a plant immune system against viruses. Trends Genet 17, 449–459.[CrossRef]
    [Google Scholar]
  55. Voss, S. & Skerra, A. ( 1997; ). Mutagenesis of a flexible loop in streptavidin leads to higher affinity for the Strep-tag II peptide and improved performance in recombinant protein purification. Protein Eng 10, 975–982.[CrossRef]
    [Google Scholar]
  56. Wells, S. E., Hillner, P. E., Vale, R. D. & Sachs, A. B. ( 1998; ). Circularization of mRNA by eukaryotic translation initiation factors. Mol Cell 2, 135–140.[CrossRef]
    [Google Scholar]
  57. Yambao, M. L. M., Masuta, C., Nakahara, K. & Uyeda, I. ( 2003; ). The central and C-terminal domains of VPg of Clover yellow vein virus are important for VPg-HCPro and VPg-VPg interactions. J Gen Virol 84, 2861–2869.[CrossRef]
    [Google Scholar]
  58. Yoo, J. Y. & Desiderio, S. ( 2003; ). Innate and acquired immunity intersect in a global view of the acute-phase response. Proc Natl Acad Sci U S A 100, 1157–1162.[CrossRef]
    [Google Scholar]
  59. Zhang, Z., Torii, N., Furusaka, A., Malayaman, N., Hu, Z. & Liang, T. J. ( 2000; ). Structural and functional characterization of interaction between hepatitis B virus X protein and the proteasome complex. J Biol Chem 275, 15157–15165.[CrossRef]
    [Google Scholar]
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