1887

Abstract

(CPMV) moves from cell to cell by transporting virus particles via tubules formed through plasmodesmata by the movement protein (MP). On the surface of protoplasts, a fusion between the MP and the green fluorescent protein forms similar tubules and peripheral punctate spots. Here it was shown by time-lapse microscopy that tubules can grow out from a subset of these peripheral punctate spots, which are dynamic structures that seem anchored to the plasma membrane. Fluorescence resonance energy transfer experiments showed that MP subunits interacted within the tubule, where they were virtually immobile, confirming that tubules consist of a highly organized MP multimer. Fluorescence recovery after photobleaching experiments with protoplasts, transiently expressing fluorescent plasma membrane-associated proteins of different sizes, indicated that tubules made by CPMV MP do not interact directly with the surrounding plasma membrane. These experiments indicated an indirect interaction between the tubule and the surrounding plasma membrane, possibly via a host plasma membrane protein.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.80497-0
2004-12-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/85/12/vir853787.html?itemId=/content/journal/jgv/10.1099/vir.0.80497-0&mimeType=html&fmt=ahah

References

  1. Adams C. L., Chen Y. T., Smith S. J., Nelson W. J. 1998; Mechanisms of epithelial cell–cell adhesion and cell compaction revealed by high-resolution tracking of E-cadherin-green fluorescent protein. J Cell Biol 142:1105–1119 [CrossRef]
    [Google Scholar]
  2. Axelrod D., Koppel D. E., Schlessinger J., Elson E., Webb W. W. 1976; Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys J 16:1055–1069 [CrossRef]
    [Google Scholar]
  3. Bastiaens P. I., Jovin T. M. 1996; Microspectroscopic imaging tracks the intracellular processing of a signal transduction protein: fluorescent-labeled protein kinase C beta I. Proc Natl Acad Sci U S A 93:8407–8412 [CrossRef]
    [Google Scholar]
  4. Bastiaens P. I., Majoul I. V., Verveer P. J., Soling H. D., Jovin T. M. 1996; Imaging the intracellular trafficking and state of the AB5 quaternary structure of cholera toxin. EMBO J 15:4246–4253
    [Google Scholar]
  5. Bertens P., Wellink J., Goldbach R., van Kammen A. 2000; Mutational analysis of the cowpea mosaic virus movement protein. Virology 267:199–208 [CrossRef]
    [Google Scholar]
  6. Bertens P., Heijne W., van der Wel N., Wellink J., van Kammen A. 2003; Studies on the C-terminus of the cowpea mosaic virus movement protein. Arch Virol 148:265–279 [CrossRef]
    [Google Scholar]
  7. Canto T., Palukaitis P. 1999; Are tubules generated by the 3a protein necessary for cucumber mosaic virus movement?. Mol Plant Microbe Interact 12:985–993 [CrossRef]
    [Google Scholar]
  8. Carvalho C. M., Wellink J., Ribeiro S. G. W. G. R., van Lent J. W. M. 2003; The C-terminal region of the movement protein of cowpea mosaic virus is involved in binding to the large but not to the small coat protein. J Gen Virol 84:2271–2277 [CrossRef]
    [Google Scholar]
  9. Dundr M., McNally J. G., Cohen J., Misteli T. 2002; Quantitation of GFP-fusion proteins in single living cells. J Struct Biol 140:92–99 [CrossRef]
    [Google Scholar]
  10. Eggen R., Verver J., Wellink J., Pleij K., van Kammen A., Goldbach R. 1989; Analysis of sequences involved in cowpea mosaic virus RNA replication using site-specific mutants. Virology 173:456–464 [CrossRef]
    [Google Scholar]
  11. Ellenberg J., Siggia E. D., Moreira J. E., Smith C. L., Presley J. F., Worman H. J., Lippincott-Schwartz J. 1997; Nuclear membrane dynamics and reassembly in living cells: targeting of an inner nuclear membrane protein in interphase and mitosis. J Cell Biol 138:1193–1206 [CrossRef]
    [Google Scholar]
  12. Gerlich D., Ellenberg J. 2003; 4D imaging to assay complex dynamics in live specimens. Nat Cell Biol 5:S14–S19
    [Google Scholar]
  13. Gopinath K., Wellink J., Porta C., Taylor K. M., Lomonossoff G. P., van Kammen A. 2000; Engineering cowpea mosaic virus RNA-2 into a vector to express heterologous proteins in plants. Virology 267:159–173 [CrossRef]
    [Google Scholar]
  14. Gopinath K., Bertens P., Pouwels J., Marks H., van Lent J., Wellink J., van Kammen A. 2003; Intracellular distribution of cowpea mosaic virus movement protein as visualised by green fluorescent protein fusions. Arch Virol 148:2099–2114 [CrossRef]
    [Google Scholar]
  15. Haggie P. M., Stanton B. A., Verkman A. S. 2003; Increased diffusional mobility of CFTR at the plasma membrane after deletion of its C-terminus PDZ-binding motif. J Biol Chem 279:5494–5500
    [Google Scholar]
  16. Haywood V., Kragler F., Lucas W. J. 2002; Plasmodesmata: pathways for protein and ribonucleoprotein signaling. Plant Cell 14:S303–S325
    [Google Scholar]
  17. Heinlein M., Padgett H. S., Gens J. S., Pickard B. G., Casper S. J., Epel B. L., Beachy R. N. 1998; Changing patterns of localization of the tobacco mosaic virus movement protein and replicase to the endoplasmic reticulum and microtubules during infection. Plant Cell 10:1107–1120 [CrossRef]
    [Google Scholar]
  18. Huang Z., Han Y., Howell S. H. 2000; Formation of surface tubules and fluorescent foci in Arabidopsis thaliana protoplasts expressing a fusion between the green fluorescent protein and the cauliflower mosaic virus movement protein. Virology 271:58–64 [CrossRef]
    [Google Scholar]
  19. Immink R. G., Gadella T. W. Jr, Ferrario S., Busscher M., Angenent G. C. 2002; Analysis of MADS box protein–protein interactions in living plant cells. Proc Natl Acad Sci U S A 99:2416–2421 [CrossRef]
    [Google Scholar]
  20. Jans D. A., Peters R., Fahrenholz F. 1990; Lateral mobility of the phospholipase C-activating vasopressin V1-type receptor in A7r5 smooth muscle cells: a comparison with the adenylate cyclase-coupled V2-receptor. EMBO J 9:2693–2699
    [Google Scholar]
  21. Karpova T. S., Baumann C. T., He L., Wu X., Grammer A., Lipsky P., Hager G. L., McNally J. G. 2003; Fluorescence resonance energy transfer from cyan to yellow fluorescent protein detected by acceptor photobleaching using confocal microscopy and a single laser. J Microsc 209:56–70 [CrossRef]
    [Google Scholar]
  22. Kasteel D., Wellink J., Verver J., van Lent J., Goldbach R., van Kammen A. 1993; The involvement of cowpea mosaic virus M RNA-encoded proteins in tubule formation. J Gen Virol 74:1721–1724 [CrossRef]
    [Google Scholar]
  23. Kasteel D. T., Perbal M. C., Boyer J. C., Wellink J., Goldbach R. W., Maule A. J., van Lent J. W. 1996; The movement proteins of cowpea mosaic virus and cauliflower mosaic virus induce tubular structures in plant and insect cells. J Gen Virol 77:2857–2864 [CrossRef]
    [Google Scholar]
  24. Kasteel D. T., Wellink J., Goldbach R. W., van Lent J. W. 1997; Isolation and characterization of tubular structures of cowpea mosaic virus. J Gen Virol 78:3167–3170
    [Google Scholar]
  25. Kenworthy A. K. 2001; Imaging protein–protein interactions using fluorescence resonance energy transfer microscopy. Methods 24:289–296 [CrossRef]
    [Google Scholar]
  26. Kim K. S., Fulton J. P. 1971; Tubules with viruslike particles in leaf cells infected with bean pod mottle virus. Virology 43:329–337 [CrossRef]
    [Google Scholar]
  27. Lazarowitz S. G., Beachy R. N. 1999; Viral movement proteins as probes for intracellular and intercellular trafficking in plants. Plant Cell 11:535–548 [CrossRef]
    [Google Scholar]
  28. Mas P., Beachy R. N. 1998; Distribution of TMV movement protein in single living protoplasts immobilized in agarose. Plant J 15:835–842 [CrossRef]
    [Google Scholar]
  29. Meissner O., Haberlein H. 2003; Lateral mobility and specific binding to GABAA receptors on hippocampal neurons monitored by fluorescence correlation spectroscopy. Biochemistry 42:1667–1672 [CrossRef]
    [Google Scholar]
  30. Morris N. R. 2003; Nuclear positioning: the means is at the ends. Curr Opin Cell Biol 15:54–59 [CrossRef]
    [Google Scholar]
  31. Olson K. R., McIntosh J. R., Olmsted J. B. 1995; Analysis of MAP 4 function in living cells using green fluorescent protein (GFP) chimeras. J Cell Biol 130:639–650 [CrossRef]
    [Google Scholar]
  32. Pfaff M., Liu S., Erle D. J., Ginsberg M. H. 1998; Integrin β cytoplasmic domains differentially bind to cytoskeletal proteins. J Biol Chem 273:6104–6109 [CrossRef]
    [Google Scholar]
  33. Phair R. D., Misteli T. 2001; Kinetic modelling approaches to in vivo imaging. Nat Rev Mol Cell Biol 2:898–907 [CrossRef]
    [Google Scholar]
  34. Pouwels J., Carette J. E., Van Lent J., Wellink J. 2002a; Cowpea mosaic virus: effects on host cell processes. Mol Plant Pathol 3:411–418 [CrossRef]
    [Google Scholar]
  35. Pouwels J., van Der Krogt G. N., van Lent J., Bisseling T., Wellink J. 2002b; The cytoskeleton and the secretory pathway are not involved in targeting the cowpea mosaic virus movement protein to the cell periphery. Virology 297:48–56 [CrossRef]
    [Google Scholar]
  36. Pouwels J., Kornet N., van Bers N., Guighelaar T., van Lent J., Bisseling T., Wellink J. 2003; Identification of distinct steps during tubule formation by the movement protein of cowpea mosaic virus. J Gen Virol 84:3485–3494 [CrossRef]
    [Google Scholar]
  37. Salmon E. D., Leslie R. J., Saxton W. M., Karow M. L., McIntosh J. R. 1984; Spindle microtubule dynamics in sea urchin embryos: analysis using a fluorescein-labeled tubulin and measurements of fluorescence redistribution after laser photobleaching. J Cell Biol 99:2165–2174 [CrossRef]
    [Google Scholar]
  38. Satoh H., Matsuda H., Kawamura T., Isogai M., Yoshikawa N., Takahashi T. 2000; Intracellular distribution, cell-to-cell trafficking and tubule-inducing activity of the 50 kDa movement protein of apple chlorotic leaf spot virus fused to green fluorescent protein. J Gen Virol 81:2085–2093
    [Google Scholar]
  39. Sekar R. B., Periasamy A. 2003; Fluorescence resonance energy transfer (FRET) microscopy imaging of live cell protein localizations. J Cell Biol 160:629–633 [CrossRef]
    [Google Scholar]
  40. Shah K., Russinova E., Gadella T. W., Willemse J. Jr, De Vries S. C. 2002; The Arabidopsis kinase-associated protein phosphatase controls internalization of the somatic embryogenesis receptor kinase 1. Genes Dev 16:1707–1720 [CrossRef]
    [Google Scholar]
  41. Starr D. A., Han M. 2003; ANChors away: an actin based mechanism of nuclear positioning. J Cell Sci 116:211–216 [CrossRef]
    [Google Scholar]
  42. Takagi S. 2003; Actin-based photo-orientation movement of chloroplasts in plant cells. J Exp Biol 206:1963–1969 [CrossRef]
    [Google Scholar]
  43. Tardin C., Cognet L., Bats C., Lounis B., Choquet D. 2003; Direct imaging of lateral movements of AMPA receptors inside synapses. EMBO J 22:4656–4665 [CrossRef]
    [Google Scholar]
  44. Umenishi F., Verbavatz J. M., Verkman A. S. 2000; cAMP regulated membrane diffusion of a green fluorescent protein–aquaporin 2 chimera. Biophys J 78:1024–1035 [CrossRef]
    [Google Scholar]
  45. van Bokhoven H., Verver J., Wellink J., van Kammen A. 1993; Protoplasts transiently expressing the 200K coding sequence of cowpea mosaic virus B-RNA support replication of M-RNA. J Gen Virol 74:2233–2241 [CrossRef]
    [Google Scholar]
  46. van der Scheer C., Groenewegen J. 1971; Structure in cells of Vigna unguiculata infected with cowpea mosaic virus. Virology 46:493–497 [CrossRef]
    [Google Scholar]
  47. van Lent J. W., Wellink J., Goldbach R. W. 1990; Evidence for the involvement of the 58K and 48K proteins in the intracellular movement of cowpea mosaic virus. J Gen Virol 71:219–223 [CrossRef]
    [Google Scholar]
  48. van Lent J., Storms M., van der Meer F., Wellink J., Goldbach R. 1991; Tubular structures involved in movement of cowpea mosaic virus are also formed in infected cowpea protoplasts. J Gen Virol 72:2615–2623 [CrossRef]
    [Google Scholar]
  49. Vermeer J. E., van Munster E. B., Vischer N. O., Gadella T. W. Jr 2004; Probing plasma membrane microdomains in cowpea protoplasts using lipidated GFP-fusion proteins and multimode FRET microscopy. J Microsc 214:190–200 [CrossRef]
    [Google Scholar]
  50. Wellink J., van Lent J. W., Verver J., Sijen T., Goldbach R. W., van Kammen A. 1993; The cowpea mosaic virus M RNA-encoded 48-kilodalton protein is responsible for induction of tubular structures in protoplasts. J Virol 67:3660–3664
    [Google Scholar]
  51. Wouters F. S., Bastiaens P. I., Wirtz K. W., Jovin T. M. 1998; FRET microscopy demonstrates molecular association of non-specific lipid transfer protein (nsL-TP) with fatty acid oxidation enzymes in peroxisomes. EMBO J 17:7179–7189 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.80497-0
Loading
/content/journal/jgv/10.1099/vir.0.80497-0
Loading

Data & Media loading...

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