Permeabilized mammalian cells as an experimental system for nuclear import geminiviral karyophilic proteins and of synthetic peptides derived from their nuclear localization signal regions

Journal of General Virology

Volumn 87, Issue 9, 2006, Pages 2709-2720

  Kass, Gideon ^a   Arad, Gabriel ^a   Rosenbluh, Joseph ^a   Gafni, Yedidya ^b   Graessmann, Adolf ^c   Rojas, Maria R ^d   Gilbertson, Robert L ^d   Loyter, Abraham ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b VOLCANI CENTER   (Israel)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BOVINE SERUM ALBUMIN; BV1 PROTEIN; CAPSID PROTEIN; KARYOPHERIN ALPHA; KARYOPHERIN BETA; NUCLEAR PROTEIN; RECOMBINANT PROTEIN; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN;

ARTICLE; BEAN DWARF MOSAIC VIRUS; CELL MEMBRANE PERMEABILITY; CELL NUCLEUS; CONTROLLED STUDY; GEMINIVIRUS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR TRANSPORT; MAMMAL CELL; MESOPHYLL; MOSAIC VIRUS; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PLANT LEAF; PLANT VIRUS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; TOBACCO; TOMATO YELLOW LEAF CURL VIRUS; VIRUS CELL INTERACTION; VIRUS GENOME;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; ANIMALS; CATTLE; CELL LINE; GEMINIVIRIDAE; HELA CELLS; HUMANS; KARYOPHERINS; MOLECULAR SEQUENCE DATA; NUCLEAR LOCALIZATION SIGNALS; PLANTS; RECOMBINANT PROTEINS; SERUM ALBUMIN, BOVINE; VIRAL PROTEINS;

BEAN DWARF MOSAIC VIRUS; GEMINIVIRIDAE; MAMMALIA; MIRIDAE; NICOTIANA BENTHAMIANA; TOMATO YELLOW LEAF CURL VIRUS;

EID: 33747335094     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.82021-0     Document Type: Article

References (47)

1. Armon-Omer, A., Graessmann, A. & Loyter, A. (2004). A synthetic peptide bearing the HIV-1 integrase 161-173 amino acid residues mediates active nuclear import and binding to importin α characterization of a functional nuclear localization signal. J Mol Biol 336, 1117-1128.
2. Atmakuri, K., Ding, Z. & Christie, P. J. (2003). VirE2, a type IV secretion substrate, interacts with the VirD4 transfer protein at cell poles of Agrobacterium tumefaciens. Mol Microbiol 49, 1699-1713.
3. Bayer, E. A. & Wilchek M. (1980). The use of the avidin-biotin complex as a tool in molecular biology. Methods Biochem Anal 26, 1-45.
4. Broder, Y. C., Stanhill, A., Zakai, N., Friedler, A., Gilon, C. & Loyter, A. (1997). Translocation of NLS-BSA conjugates into nuclei of permeabilized mammalian cells can be supported by protoplast extract. An experimental system for studying plant cytosolic factors involved in nuclear import. FEBS Lett 412, 535-539.
5. Brown, J. K. (2001). The molecular epidemiology of begomoviruses. In Trends in Plant Virology, pp. 279-316. Edited by J. A. Khan & J. Dykstra. New York: Haworth Press.
6. Citovsky, V., de Vos, G. & Zambryski, P. (1988). Single-stranded DNA binding protein encoded by the virE locus of Agrobacterium tumefaciens. Science 240, 501-504.
7. Citovsky, V., Kapelnikov, A., Oliel, S., Zakai, N., Rojas, M. R., Gilbertson, R. L., Tzfira, T. & Loyter, A. (2004). Protein interactions involved in nuclear import of the Agrobacterium VirE2 protein in vivo and in vitro. J Biol Chem 279, 29528-29533.
8. Cormack, B. P., Bertram, G., Egerton, M., Gow, N. A. R., Falkow, S. & Brown, A. J. P. (1997). Yeast-enhanced green fluorescent protein (yEGFP): a reporter of gene expression in Candida albicans. Microbiology 143, 303-311.
9. Fontes, M. R. M., Teh, T. & Kobe, B. (2000). Structural basis of recognition of monopartite and bipartite nuclear localization sequences by mammalian importin-α. J Mol Biol 297, 1183-1194.
10. Friedler, A., Zakai, N., Karni, O., Broder, Y. C., Baraz, L., Kotler, M., Loyter, A. & Gilon, C. (1998). Backbone cyclic peptide, which mimics the nuclear localization signal of human immunodeficiency virus type 1 matrix protein, inhibits nuclear import and virus production in nondividing cells. Biochemistry 37, 5616-5622.
11. Gafni, Y. & Epel, B. (2002). The role of host and viral proteins in intra- and inter-cellular trafficking of geminiviruses. Physiol Mol Plant Pathol 60, 231-241.
12. Görlich, D. (1997). Nuclear protein import. Curr Opin Cell Biol 9, 412-419.
13. Graessmann, M. & Graessmann, A. (1983). Microinjection of tissue culture cells. Methods Enzymol 101, 482-492.
14. Haley, A., Richardson, K., Zhan, X. & Morris, B. (1995). Mutagenesis of the BC1 and BV1 genes of African cassava mosaic virus identifies conserved amino acids that are essential for spread. J Gen Virol 76, 1291-1298.
15. Hallan, V. & Gafni, Y. (2001). Tomato yellow leaf curl virus (TYLCV) capsid protein (CP) subunit interactions: implications for viral assembly. Arch Virol 146, 1765-1773.
16. Hanley-Bowdoin, L., Settlage, S. B., Orozco, B. M., Nagar, S. & Robertson, D. (2000). Geminiviruses: models for plant DNA replication, transcription, and cell cycle regulation. Crit Rev Biochem Mol Biol 35, 105-140.
17. Hicks, G. R. & Raikhel, N. V. (1995). Nuclear localization signal binding proteins in higher plant nuclei. Proc Natl Acad Sci U S A 92, 734-738.
18. Hu, C.-D. & Kerppola, T. K (2003). Simultaneous visualization of multiple protein interactions in living cells using multicolor fluorescence complementation analysis. Nat Biotechnol 21, 539-545.
19. Hu, C.-D., Chinenov, Y. & Kerppola, T. K. (2002). Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol Cell 9, 789-798.
20. Hübner, S., Smith, H. M. S., Hu, W., Chan, C. K., Rihs, H.-P., Paschal, B. M., Raikhel, N. V. & Jens, D. A. (1999). Plant importin α binds nuclear localization sequences with high affinity and can mediate nuclear import independent of importin β. J Biol Chem 274, 22610-22617.
21. Jans, D. A., Xiao, C.-Y. & Lam, M. H. C. (2000). Nuclear targeting signal recognition: a key control point in nuclear transport? Bioessays 22, 532-544.
22. Jenkins, Y., McEntee, M., Weis, K. & Greene, W. C. (1998). Characterization of HIV-1 Vpr nuclear import: analysis of signals and pathways. J Cell Biol 143, 875-885.
23. Jiang, C.-J., Imamoto, N., Matsuki, R., Yoneda, Y. & Yamamoto, N. (1998). Functional characterization of a plant importin α homologue. Nuclear localization signal (NLS)-selective binding and mediation of nuclear import of NLS proteins in vitro. J Biol Chem 273, 24083-24087.
24. Kalderon, D., Roberts, B. L., Richardson, W. D. & Smith, A. E. (1984). A short amino acid sequence able to specify nuclear location. Cell 39, 499-509.
25. Karni, O., Friedler, A., Zakai, N., Gilon, C. & Loyter, A. (1998). A peptide derived from the N-terminal region of HIV-1 Vpr promotes nuclear import in permeabilized cells: elucidation of the NLS region of the Vpr. FEBS Lett 429, 421-425.
26. Krichevsky, A., Graessmann, A., Nissim, A., Pillar, S. C., Zakai, N. & Loyter, A. (2003). Antibody fragments selected by phage display against the nuclear localization signal of the HIV-1 Vpr protein inhibit nuclear import in permeabilized and intact cultured cells. Virology 305, 77-92.
27. Kunik, T., Palanichelvam, K., Czosnek, H., Citovsky, V. & Gafni, Y. (1998). Nuclear import of the capsid protein of tomato yellow leaf curl virus (TYLCV) in plant and insect cells. Plant J 13, 393-399.
28. Kunik, T., Mizrachy, L., Citovsky, V. & Gafni, Y. (1999). Characterization of a tomato karyopherin α that interacts with the tomato yellow leaf curl virus (TYLCV) capsid protein. J Exp Bot 50, 731-732.
29. Lazarowitz, S. G. & Beachy, R. N. (1999). Viral movement proteins as probes for intracellular and intercellular trafficking in plants. Plant Cell 11, 535-548.
30. Mattaj, I. W. & Englmeier, L. (1998). Nucleocytoplasmic transport: the soluble phase. Annu Rev Biochem 67, 265-306.
31. Melchior, F., Paschal, B., Evans, J. & Gerace, L. (1993). Inhibition of nuclear protein import by nonhydrolyzable analogues of GTP and identification of the small GTPase Ran/TC4 as an essential transport factor. J Cell Biol 123, 1649-1659.
32. Nigg, E. A. (1997). Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature 386, 779-787.
33. Nigg, E. A., Baeuerle, P. A. & Lührmann, R. (1991). Nuclear import-export: in search of signals and mechanisms. Cell 66, 15-22.
34. Noueiry, A. O., Lucas, W. J. & Gilbertson, R. L. (1994). Two proteins of a plant DNA virus coordinate nuclear and plasmodesmal transport. Cell 76, 925-932.
35. Palanichelvam, K., Kunik, T., Citovsky, V. & Gafni, Y. (1998). The capsid protein of tomato yellow leaf curl virus binds cooperatively to single-stranded DNA. J Gen Virol 79, 2829-2833.
36. Pascal, E., Goodlove, P. E., Wu, L. C. & Lazarowitz, S. G. (1993). Transgenic tobacco plants expressing the geminivirus BL1 protein exhibit symptoms of viral disease. Plant Cell 5, 795-807.
37. Pascal, E., Sanderfoot, A. A., Ward, B. M., Medville, R., Turgeon, R. & Lazarowitz, S. G. (1994). The geminivirus BR1 movement protein binds single-stranded DNA and localizes to the cell nucleus. Plant Cell 6, 995-1006.
38. Rojas, M. R., Noueiry, A. O., Lucas, W. J. & Gilbertson, R. L. (1998). Bean dwarf mosaic geminivirus movement proteins recognize DNA in a form-and size-specific manner. Cell 95, 105-113.
39. Rojas, M. R., Jiang, H., Salati, R., Xoconostle-Cizares, B., Sudarshana, M. R., Lucas, W. J. & Gilbertson, R. L. (2001). Functional analysis of proteins involved in movement of the monopartite begomovirus, Tomato yellow leaf curl virus. Virology 291, 110-125.
40. Rojas, M. R., Hagen, C., Lucas, W. J. & Gilbertson, R. L. (2005). Exploiting chinks in the plant's armor: evolution and emergence of geminiviruses. Annu Rev Phytopathol 43, 361-394.
41. Sanderfoot, A. A. & Lazarowitz, S. G. (1995). Cooperation in viral movement: the gerninivirus BL1 movement protein interacts with BR1 and redirects it from the nucleus to the cell periphery. Plant Cell 7, 1185-1194.
42. Sanderfoot, A. A., Ingham, D. J. & Lazarowitz, S. G. (1996). 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, 23-33.
43. Tsuchisaka, A. & Theologis, A. (2004). Heterodimeric interactions among the 1-amino-cyclopropane-1-carboxylate synthase polypeptides encoded by the Arabidopsis gene family. Proc Natl Acad Sci U S A 101, 2275-2280.
44. Tzfira, T. & Citovsky, V. (2001). Comparison between nuclear import of nopaline- and octopine-specific Agrobacterium VirE2 proteins of plant, yeast and mammalian cells. Mol Plant Pathol 2, 171-176.
45. Yoneda, Y., Imamoto-Sonobe, N., Yamalzumi, M. & Uchida, T. (1987). Reversible inhibition of protein import into the nucleus by wheat germ agglutinin injected into cultured cells. Exp Cell Res 173, 586-595.
46. Zhang, S. C., Wage, C. & Jeske, H. (2001). Movement proteins (BC1 and BVI) 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, 249-260.
47. Ziemienowicz, A., Haasen, D., Staiger, D. & Markle, T. (2003). Arabidopsis transportini is the nuclear import receptor for the circadian clock-regulated RNA-binding protein AtGRP7. Plant Mol Biol 53, 201-212.