Post-translational modifications of Abutilon mosaic virus movement protein (BC1) in fission yeast

Virus Research

Volumn 131, Issue 1, 2008, Pages 86-94

  Kleinow, Tatjana ^a   Holeiter, Gerlinde ^a   Nischang, Marc ^a   Stein, Monika ^a   Karayavuz, Miriam ^a   Wege, Christina ^a   Jeske, Holger ^a  

^a UNIVERSITY OF STUTTGART   (Germany)

Author keywords

Geminivirus; In vivo labelling; Schizosaccharomyces pombe

Indexed keywords

ACETIC ACID; ALKALINE PHOSPHATASE; DODECYL SULFATE SODIUM; MOVEMENT PROTEIN BC1; PHOSPHATE; PHOSPHORUS 32; POLYACRYLAMIDE; UNCLASSIFIED DRUG; UREA; VIRUS PROTEIN;

ABUTILON MOSAIC VIRUS; ARTICLE; ELECTROPHORETIC MOBILITY; GEL ELECTROPHORESIS; GEMINIVIRUS; MOLECULAR WEIGHT; NONHUMAN; PHOSPHORYLATION; PLANT DISEASE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; SACCHAROMYCES; SACCHAROMYCES POMBE; SEPARATION TECHNIQUE; WESTERN BLOTTING;

ELECTROPHORESIS, POLYACRYLAMIDE GEL; GEMINIVIRIDAE; PLANT VIRAL MOVEMENT PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; SCHIZOSACCHAROMYCES; VIRAL PROTEINS;

ABUTILON MOSAIC VIRUS; GEMINIVIRIDAE; SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

EID: 36849069900     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2007.08.011     Document Type: Article

References (71)

1. Aberle H.J., Rütz M.L., Karayavuz M., Frischmuth S., Wege C., Hülser D., and Jeske H. Localizing BC1 movement proteins of Abutilon mosaic geminivirus in yeasts by subcellular fractionation and freeze-fracture immunolabelling. Arch. Virol. 147 (2002) 103-107
2. Abouzid A.M., Barth A., and Jeske H. Immunogold labeling of the Abutilon mosaic virus in ultrathin sections of epoxy resin embedded leaf tissue. J. Ultrastruct. Res. 99 (1988) 39-47
3. Ausubel F.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., and Struhl K. Current Protocols in Molecular Biology (1999), Green Publishing Associates John Wiley and Sons-Interscience, New York
4. Bhalerao R.P., Salchert K., Bako L., Okresz L., Szabados L., Muranaka T., Machida Y., Schell J., and Koncz C. Regulatory interaction of PRL1 WD protein with Arabidopsis SNF1-like protein kinases. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 5322-5327
5. Bisaro D.M. Silencing suppression by geminivirus proteins. Virology 344 (2006) 158-168
6. Blom N., Gammeltoft S., and Brunak S. Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 294 (1999) 1351-1362
7. Boulikas T. Electrophoretic separation of histones and high-mobility-group proteins on acid-urea-Triton gels. Anal. Biochem. 149 (1985) 379-386
8. Brough C.L., Hayes R.J., Coutts R.H.A., and Buck K.W. Effect of mutagenesis in vitro on the ability of cloned tomato golden mosaic virus DNA to infect Nicotiana benthamiana plants. J. Gen. Virol. 69 (1988) 481-492
9. Citovsky V., McLean B.G., Zupan J.R., and Zambryski P. Phosphorylation of tobacco mosaic virus cell-to-cell movement protein by a developmentally regulated plant cell wall-associated protein kinase. Genes Dev. 7 (1993) 904-910
10. Duan Y.P., Powell C.A., Purcifull D.E., Broglio P., and Hiebert E. Phenotypic variation in transgenic tobacco expressing mutated geminivirus movement/pathogenicity (BC1) proteins. Mol. Plant-Microbe Interact. 10 (1997) 1065-1074
11. Etessami P., Callis R., Ellwood S., and Stanley J. Delimitation of essential genes of cassava latent virus DNA 2. Nucleic Acids Res. 16 (1988) 4811-4829
12. Evans D., and Jeske H. DNA B facilitates, but is not essential for, the spread of Abutilon mosaic virus in agroinoculated Nicotiana benthamiana. Virology 194 (1993) 752-757
13. Florentino L.H., Santos A.A., Fontenelle M.R., Pinheiro G.L., Zerbini F.M., Baracat-Pereira M.C., and Fontes E.P. A PERK-like receptor kinase interacts with the geminivirus nuclear shuttle protein and potentiates viral infection. J. Virol. 80 (2006) 6648-6656
14. Fontes E.P., Santos A.A., Luz D.F., Waclawovsky A.J., and Chory J. The geminivirus nuclear shuttle protein is a virulence factor that suppresses transmembrane receptor kinase activity. Genes Dev. 18 (2004) 2545-2556
15. Francis D., and Halford N.G. Nutrient sensing in plant meristems. Plant Mol. Biol. 60 (2006) 981-993
16. Frischmuth S., Kleinow T., Aberle H.-J., Wege C., Hülser D., and Jeske H. Yeast two-hybrid systems confirm the membrane-association and oligomerization of BC1 but do not detect an interaction of the movement proteins BC1 and BV1 of Abutilon mosaic geminivirus. Arch. Virol. 149 (2004) 2349-2364
17. Frischmuth S., Wege C., Hülser D., and Jeske H. The movement protein BC1 promotes redirection of the nuclear shuttle protein BV1 of Abutilon mosaic geminivirus to the plasma membrane in fission yeast. Protoplasma. 230 (2007) 117-123
18. Gafni Y., and Epel B.L. The role of host and viral proteins in intra- and inter-cellular trafficking of geminiviruses. Physiol. Mol. Plant Pathol. 60 (2002) 231-241
19. Haley A., Hunter T., Kiberstis P., and Zimmern D. Multiple serine phosphorylation sites on the 30 kDa TMV cell-to-cell movement protein synthesized in tobacco protoplasts. Plant J. 8 (1995) 715-724
20. Halford N.G., and Hardie D.G. SNF1-related protein kinases: global regulators of carbon metabolism in plants?. Plant Mol. Biol. 37 (1998) 735-748
21. Hao L., Wang H., Sunter G., and Bisaro D.M. Geminivirus AL2 and L2 proteins interact with and inactivate SNF1 kinase. Plant Cell 15 (2003) 1034-1048
22. Hartitz M.D., Sunter G., and Bisaro D.M. The tomato golden mosaic virus transactivator (TrAP) is a single-stranded DNA and zinc-binding phosphoprotein with an acidic activation domain. Virology 263 (1999) 1-14
23. Hehnle S., Wege C., and Jeske H. Interaction of DNA with the movement proteins of geminiviruses revisited. J. Virol. 78 (2004) 7698-7706
24. Horns T., and Jeske H. Localization of Abutilon mosaic virus DNA within leaf tissue by in situ hybridization. Virology 181 (1991) 580-588
25. Hou Y.M., Sanders R., Ursin V.M., and Gilbertson R.L. Transgenic plants expressing geminivirus movement proteins: abnormal phenotypes and delayed infection by tomato mottle virus in transgenic tomatoes expressing the bean dwarf mosaic virus BV1 or BC1 proteins. Mol. Plant-Microbe Interact. 13 (2000) 297-308
26. Ingham D.J., Pascal E., and Lazarowitz S.G. Both bipartite geminivirus movement proteins define viral host range, but only BL1 determines viral pathogenicity. Virology 207 (1995) 191-204
27. Karger E.M., Frolova O.Y., Fedorova N.V., Baratova L.A., Ovchinnikova T.V., Susi P., Makinen K., Ronnstrand L., Dorokhov Y.L., and Atabekov J.G. Dysfunctionality of a tobacco mosaic virus movement protein mutant mimicking threonine 104 phosphorylation. J. Gen. Virol. 84 (2003) 727-732
28. Karpova O.V., Ivanov K.I., Rodionova N.P., Dorokhov Yu L., and Atabekov J.G. Nontranslatability and dissimilar behavior in plants and protoplasts of viral RNA and movement protein complexes formed in vitro. Virology 230 (1997) 11-21
29. Karpova O.V., Rodionova N.P., Ivanov K.I., Kozlovsky S.V., Dorokhov Y.L., and Atabekov J.G. Phosphorylation of tobacco mosaic virus movement protein abolishes its translation repressing ability. Virology 261 (1999) 20-24
30. Kawakami S., Padgett H.S., Hosokawa D., Okada Y., Beachy R.N., and Watanabe Y. 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 (1999) 6831-6840
31. Kleinow T., Bhalerao R., Breuer F., Umeda M., Salchert K., and Koncz C. Functional identification of an Arabidopsis Snf4 ortholog by screening for heterologous multicopy suppressors of Snf4 deficiency in yeast. Plant J. 23 (2000) 115-122
32. Kong L.J., and Hanley-Bowdoin L. A geminivirus replication protein interacts with a protein kinase and a motor protein that display different expression patterns during plant development and infection. Plant Cell 14 (2002) 1817-1832
33. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
34. Lee J.Y., Taoka K., Yoo B.C., Ben-Nissan G., Kim D.J., and Lucas W.J. Plasmodesmal-associated protein kinase in tobacco and Arabidopsis recognizes a subset of non-cell-autonomous proteins. Plant Cell 17 (2005) 2817-2831
35. Mariano A.C., Andrade M.O., Santos A.A., Carolino S.M., Oliveira M.L., Baracat-Pereira M.C., Brommonshenkel S.H., and Fontes E.P. Identification of a novel receptor-like protein kinase that interacts with a geminivirus nuclear shuttle protein. Virology 318 (2004) 24-31
36. Matsushita Y., Hanazawa K., Yoshioka K., Oguchi T., Kawakami S., Watanabe Y., Nishiguchi M., and Nyunoya H. In vitro phosphorylation of the movement protein of tomato mosaic tobamovirus by a cellular kinase. J. Gen. Virol. 81 (2000) 2095-2102
37. Matsushita Y., Yoshioka K., Shigyo T., Takahashi H., and Nyunoy H. Phosphorylation of the movement protein of cucumber mosaic virus in transgenic tobacco plants. Virus Genes 24 (2002) 231-234
38. Maundrell K. Thiamine-repressible expression vectors pREP and pRIP for fission yeast. Gene 123 (1993) 127-130
39. Noueiry A.O., Lucas W.J., and Gilbertson R.L. Two proteins of a plant DNA virus coordinate nuclear and plasmodesmatal transport. Cell 76 (1994) 925-932
40. Pascal E., Goodlove P.E., Wu L.C., and Lazarowitz S.G. Transgenic tobacco plants expressing the geminivirus BL1 protein exhibit symptoms of viral disease. Plant Cell 5 (1993) 795-807
41. Pascal E., Sanderfoot A.A., Ward B.M., Medville R., Turgeon R., and Lazarowitz S.G. The geminivirus BR1 movement protein binds single-stranded DNA and localizes to the cell nucleus. Plant Cell 6 (1994) 995-1006
42. Polge C., and Thomas M. SNF1/AMPK/SnRK1 kinases, global regulators at the heart of energy control?. Trends Plant Sci. 12 (2006) 20-28
43. Rojas M.R., Noueiry A.O., Lucas W.J., and Gilbertson R.L. Bean dwarf mosaic geminivirus movement proteins recognize DNA in a form- and size-specific manner. Cell 95 (1998) 105-113
44. Rojas M.R., Hagen C., Lucas W.J., and Gilbertson R.L. Exploiting chinks in the plant's armor: evolution and emergence of geminiviruses. Annu. Rev. Phytopathol. 43 (2005) 361-394
45. Rolland F., Baena-Gonzalez E., and Sheen J. Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu. Rev. Plant Biol. 57 (2006) 675-709
46. Sanderfoot A.A., and Lazarowitz S.G. Cooperation in viral movement: the geminivirus BL1 movement protein interacts with BR1 and redirects it from the nucleus to the cell periphery. Plant Cell 7 (1995) 1185-1194
47. Sanderfoot A.A., Ingham D.J., and Lazarowitz S.G. A viral movement protein as a nuclear shuttle: the geminivirus BR1 movement protein contains domains essential for interaction with BL1 and nuclear localization. Plant Physiol. 110 (1996) 23-33
48. Saunders K., Wege C., Karuppannan V., Jeske H., and Stanley J. The distinct disease phenotypes of the common and yellow vein strains of Tomato golden mosaic virus are determined by nucleotide differences in the 3′-terminal region of the gene encoding the movement protein. J. Gen. Virol. 82 (2001) 45-51
49. Seron K., Bernasconi L., Allet B., and Haenni A.L. Expression of the 69K movement protein of turnip yellow mosaic virus in insect cells. Virology 219 (1996) 274-278
50. Shen W., and Hanley-Bowdoin L. Geminivirus infection up-regulates the expression of two arabidopsis protein kinases related to yeast Snf1 and mammalian AMPK activating kinases. Plant Physiol. 142 (2006) 1642-1655
51. Sokolova M., Prufer D., Tacke E., and Rohde W. 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 (1997) 201-205
52. Stanley J., Bisaro D.M., Briddon R.W., Brown J.K., Fauquet C.M., Harrison B.D., Rybicki E.P., and Stenger D.C. Geminiviridae. In: Fauquet C.M., Mayo M.A., Maniloff J., Desselberger U., and Ball L.A. (Eds). Virus Taxonomy. VIIIth Report of the International Commitee on Taxonomy of Viruses (2005), Elsevier/Academic Press, London pp. 301-326
53. Trutnyeva K., Bachmaier R., and Waigmann E. Mimicking carboxyterminal phosphorylation differentially effects subcellular distribution and cell-to-cell movement of Tobacco mosaic virus movement protein. Virology 332 (2005) 563-577
54. Unseld S., Höhnle M., Ringel M., and Frischmuth T. Subcellular targeting of the coat protein of African cassava mosaic geminivirus. Virology 286 (2001) 373-383
55. Unseld S., Frischmuth T., and Jeske H. Short deletions in nuclear targeting sequences of African cassava mosaic virus coat protein prevent geminivirus twinned particle formation. Virology 318 (2004) 89-100
56. von Arnim A., and Stanley J. Determinants of tomato golden mosaic virus symptom development located on DNA B. Virology 186 (1992) 286-293
57. von Arnim A., Frischmuth T., and Stanley J. Detection and possible functions of African cassava mosaic virus DNA B gene products. Virology 192 (1993) 264-272
58. Waigmann E., Chen M.H., Bachmaier R., Ghoshroy S., and Citovsky V. Regulation of plasmodesmal transport by phosphorylation of tobacco mosaic virus cell-to-cell movement protein. EMBO J. 19 (2000) 4875-4884
59. Waigmann E., Ueki S., Trtneyeva K., and Citovsky V. The ins and outs of nondestructive cell-to-cell and systemic movement of plant viruses. Crit. Rev. Plant Sci. 23 (2004) 195-250
60. Wang M.S., Pang J.S., and Selsted M.E. Semidry electroblotting of peptides and proteins from acid-urea polyacrylamide gels. Anal. Biochem. 253 (1997) 225-230
61. Wang H., Hao L., Shung C.Y., Sunter G., and Bisaro D.M. Adenosine kinase is inactivated by geminivirus AL2 and L2 proteins. Plant Cell 15 (2003) 3020-3032
62. Wang H., Buckley K.J., Yang X., Buchmann R.C., and Bisaro D.M. Adenosine kinase inhibition and suppression of RNA silencing by geminivirus AL2 and L2 proteins. J. Virol. 79 (2005) 7410-7418
63. Ward A., Etessami P., and Stanley J. Expression of a bacterial gene in plants mediated by infectious geminivirus DNA. EMBO J. 7 (1988) 1583-1587
64. Watanabe Y., Ogawa T., and Okada Y. In vivo phosphorylation of the 30-kDa protein of tobacco mosaic virus. FEBS Lett. 313 (1992) 181-184
65. Wege C., and Jeske H. Abutilon mosaic geminivirus proteins expressed and phosphorylated in Escherichia coli. J. Phytopathol. 146 (1998) 613-621
66. Wege C., and Pohl D. Abutilon mosaic virus DNA B component supports mechanical virus transmission, but does not counteract begomoviral limitation in transgenic plants. Virology 365 (2007) 173-186
67. Wege C., Gotthardt R.D., Frischmuth T., and Jeske H. Fulfilling Koch's postulates for Abutilon mosaic virus. Arch. Virol. 145 (2000) 2217-2225
68. Wege C., Saunders K., Stanley J., and Jeske H. Comparative analysis of tissue tropism of bipartite geminiviruses. J. Phytopathol. 149 (2001) 359-368
69. Zhang S.C., Wege C., and Jeske H. Movement proteins (BC1 and BV1) of Abutilon mosaic geminivirus are cotransported in and between cells of sink but not of source leaves as detected by green fluorescent protein tagging. Virology 290 (2001) 249-260
70. Zhang S.C., Ghosh R., and Jeske H. Subcellular targeting domains of Abutilon mosaic geminivirus movement protein BC1. Arch. Virol. 147 (2002) 2349-2363
71. Zweidler A. Resolution of histones by polyacrylamide gel electrophoresis in presence of nonionic detergents. Methods Cell Biol. 17 (1978) 223-233