1887

Abstract

This study identified the structural proteins of two badnavirus species, (BSMYV) and (BSOLV), and mapped the distribution of continuous B-cell epitopes. Two different capsid protein (CP) isoforms of about 44 and 40 kDa (CP1 and CP2) and the virion-associated protein (VAP) were consistently associated with purified virions. For both viral species, the N terminus of CP2 was successfully sequenced by Edman degradation but that of CP1 was chemically blocked. peptide sequencing of tryptic digests suggested that CP1 and CP2 derive from the same region of the P3 polyprotein but differ in the length of either the N or the C terminus. A three-dimensional model of the BSMYV-CP was constructed, which showed that the CP is a multi-domain structure, containing homologues of the retroviral capsid and nucleocapsid proteins, as well as a third, intrinsically disordered protein region at the N terminus, henceforth called the NID domain. Using the Pepscan approach, the immunodominant continuous epitopes were mapped to the NID domain for five different species of . Anti-peptide antibodies raised against these epitopes in BSMYV were successfully used for detection of native virions and denatured CPs in serological assays. Immunoelectron microscopy analysis of the virion surface using the anti-peptide antibodies confirmed that the NID domain is exposed on the surface of virions, and that the difference in mass of the two CP isoforms is due to variation in length of the NID domain.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000643
2016-12-16
2021-08-02
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/12/3446.html?itemId=/content/journal/jgv/10.1099/jgv.0.000643&mimeType=html&fmt=ahah

References

  1. Bringans S., Kendrick T. S., Lui J., Lipscombe R. 2008; A comparative study of the accuracy of several de novo sequencing software packages for datasets derived by matrix-assisted laser desorption/ionisation and electrospray. Rapid Commun Mass Spectrom 22:3450–3454 [View Article][PubMed]
    [Google Scholar]
  2. Champagne J., Benhamou N., Leclerc D. 2004; Localization of the N-terminal domain of cauliflower mosaic virus coat protein precursor. Virology 324:257–262 [View Article][PubMed]
    [Google Scholar]
  3. Chapdelaine Y., Kirk D., Karsies A., Hohn T., Leclerc D. 2002; Mutation of capsid protein phosphorylation sites abolishes cauliflower mosaic virus infectivity. J Virol 76:11748–11752 [View Article][PubMed]
    [Google Scholar]
  4. Cheng C. P., Lockhart B. E., Olszewski N. E. 1996; The ORF I and II proteins of Commelina yellow mottle virus are virion-associated. Virology 223:263–271 [View Article][PubMed]
    [Google Scholar]
  5. Clark M. F., Adams A. N. 1977; Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. J Gen Virol 34:475–483 [View Article][PubMed]
    [Google Scholar]
  6. Debouck C., Gorniak J. G., Strickler J. E., Meek T. D., Metcalf B. W., Rosenberg M. 1987; Human immunodeficiency virus protease expressed in Escherichia coli exhibits autoprocessing and specific maturation of the gag precursor. Proc Natl Acad Sci U S A 84:8903–8906 [View Article][PubMed]
    [Google Scholar]
  7. Dyson H. J., Wright P. E. 2005; Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6:197–208 [View Article][PubMed]
    [Google Scholar]
  8. Geering A. D., Pooggin M. M., Olszewski N. E., Lockhart B. E., Thomas J. E. 2005; Characterisation of Banana streak Mysore virus and evidence that its DNA is integrated in the B genome of cultivated Musa . Arch Virol 150:787–796 [View Article][PubMed]
    [Google Scholar]
  9. Geysen H. M., Meloen R. H., Barteling S. J. 1984; Use of peptide synthesis to probe viral antigens for epitopes to a resolution of a single amino acid. Proc Natl Acad Sci U S A 81:3998–4002 [View Article][PubMed]
    [Google Scholar]
  10. Guerra-Peraza O., de Tapia M., Hohn T., Hemmings-Mieszczak M. 2000; Interaction of the cauliflower mosaic virus coat protein with the pregenomic RNA leader. J Virol 74:2067–2072 [View Article][PubMed]
    [Google Scholar]
  11. Harper G., Hull R. 1998; Cloning and sequence analysis of banana streak virus DNA. Virus Genes 17:271–278[PubMed] [CrossRef]
    [Google Scholar]
  12. Harper G., Hart D., Moult S., Hull R., Geering A., Thomas J. 2005; The diversity of Banana streak virus isolates in Uganda. Arch Virol 150:2407–2420 [View Article][PubMed]
    [Google Scholar]
  13. Hay J., Grieco F., Druka A., Pinner M., Lee S. C., Hull R. 1994; Detection of rice tungro bacilliform virus gene products in vivo . Virology 205:430–437 [View Article][PubMed]
    [Google Scholar]
  14. Heuzenroeder M. W., Barton M. D., Vanniasinkam T., Phumoonna T. 2009; Linear B-cell epitope mapping using enzyme-linked immunosorbent assay for libraries of overlapping synthetic peptides. In Epitope Mapping Protocols, 2nd edn. pp. 137–144 Edited by Schutkowski M., Reineke U. Totowa, NJ: Humana Press; [CrossRef]
    [Google Scholar]
  15. Hoh F., Uzest M., Drucker M., Plisson-Chastang C., Bron P., Blanc S., Dumas C. 2010; Structural insights into the molecular mechanisms of cauliflower mosaic virus transmission by its insect vector. J Virol 84:4706–4713 [View Article][PubMed]
    [Google Scholar]
  16. Jacquot E., Hagen L. S., Jacquemond M., Yot P. 1996; The open reading frame 2 product of cacao swollen shoot badnavirus is a nucleic acid-binding protein. Virology 225:191–195 [View Article][PubMed]
    [Google Scholar]
  17. Jacquot E., Keller M., Yot P. 1997; A short basic domain supports a nucleic acid-binding activity in the rice tungro bacilliform virus open reading frame 2 product. Virology 239:352–359 [View Article][PubMed]
    [Google Scholar]
  18. Karsies A., Hohn T., Leclerc D. 2001; Degradation signals within both terminal domains of the cauliflower mosaic virus capsid protein precursor. Plant J 27:335–343 [View Article][PubMed]
    [Google Scholar]
  19. 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 [View Article][PubMed]
    [Google Scholar]
  20. Kim D. E., Chivian D., Baker D. 2004; Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res 32:W526–W531 [View Article][PubMed]
    [Google Scholar]
  21. King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J. 2012 Virus Taxonomy: Classification and Nomenclature of Viruses. Ninth Report of the International Committee on Taxonomy of Viruses London, UK: Elsevier;
    [Google Scholar]
  22. Kobayashi K., Tsuge S., Stavolone L., Hohn T. 2002; The cauliflower mosaic virus virion-associated protein is dispensable for viral replication in single cells. J Virol 76:9457–9464 [View Article][PubMed]
    [Google Scholar]
  23. Kringelum J., Nielsen M., Padkjær S. B., Lund O. 2013; Structural analysis of B-cell epitopes in antibody:protein complexes. Mol Immunol 53:24–34 [View Article][PubMed]
    [Google Scholar]
  24. Källberg M., Wang H., Wang S., Peng J., Wang Z., Lu H., Xu J. 2012; Template-based protein structure modeling using the RaptorX web server. Nat Protoc 7:1511–1522 [View Article][PubMed]
    [Google Scholar]
  25. Laco G. S., Beachy R. N. 1994; Rice tungro bacilliform virus encodes reverse transcriptase, DNA polymerase, and ribonuclease H activities. Proc Natl Acad Sci U S A 91:2654–2658 [View Article][PubMed]
    [Google Scholar]
  26. Larsen J. E., Lund O., Nielsen M. 2006; Improved method for predicting linear B-cell epitopes. Immunome Res 2:1–7 [View Article][PubMed]
    [Google Scholar]
  27. Leclerc D., Chapdelaine Y., Hohn T. 1999; Nuclear targeting of the cauliflower mosaic virus coat protein. J Virol 73:553–560[PubMed]
    [Google Scholar]
  28. Marmey P., Bothner B., Jacquot E., de Kochko A., Ong C. A., Yot P., Siuzdak G., Beachy R. N., Fauquet C. M. 1999; Rice tungro bacilliform virus open reading frame 3 encodes a single 37-kDa coat protein. Virology 253:319–326 [View Article][PubMed]
    [Google Scholar]
  29. Marmey P., Rojas-Mendoza A., de Kochko A., Beachy R. N., Fauquet C. M. 2005; Characterization of the protease domain of Rice tungro bacilliform virus responsible for the processing of the capsid protein from the polyprotein. Virol J 2:33 [View Article][PubMed]
    [Google Scholar]
  30. Martinez-Izquierdo J., Hohn T. 1987; Cauliflower mosaic virus coat protein is phosphorylated in vitro by a virion-associated protein kinase. Proc Natl Acad Sci U S A 84:1824–1828 [View Article][PubMed]
    [Google Scholar]
  31. Martinière A., Bak A., Macia J. L., Lautredou N., Gargani D., Doumayrou J., Garzo E., Moreno A., Fereres A. et al. 2013; A virus responds instantly to the presence of the vector on the host and forms transmission morphs. Elife 2: [View Article][PubMed]
    [Google Scholar]
  32. McGuffin L. J., Bryson K., Jones D. T. 2000; The PSIPRED protein structure prediction server. Bioinformatics 16:404–405 [View Article][PubMed]
    [Google Scholar]
  33. Mougeot J. L., Guidasci T., Wurch T., Lebeurier G., Mesnard J. M. 1993; Identification of C-terminal amino acid residues of cauliflower mosaic virus open reading frame III protein responsible for its DNA binding activity. Proc Natl Acad Sci U S A 90:1470–1473 [View Article][PubMed]
    [Google Scholar]
  34. Ndowora T. C. R., Lockhart B. E. L. 2000; Development of a serological assay for detecting serologically diverse banana streak virus isolates. Acta Hortic 540:377–388 [CrossRef]
    [Google Scholar]
  35. Nguyen Ba A. N., Pogoutse A., Provart N., Moses A. M. 2009; NLStradamus: a simple Hidden Markov Model for nuclear localization signal prediction. BMC Bioinformatics 10:202 [View Article][PubMed]
    [Google Scholar]
  36. Pei J., Tang M., Grishin N. V. 2008; PROMALS3D web server for accurate multiple protein sequence and structure alignments. Nucleic Acids Res 36:W30–W34 [View Article][PubMed]
    [Google Scholar]
  37. Pettersen E. F., Goddard T. D., Huang C. C., Couch G. S., Greenblatt D. M., Meng E. C., Ferrin T. E. 2004; UCSF Chimera– a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612 [View Article][PubMed]
    [Google Scholar]
  38. Pinheiro J., DebRoy S., Sarkar D. R Development Core Team 2011; nlme: Linear and nonlinear mixed effects models. R package version 2.15. http://cran.rproject.org/web/packages/nlme/index.html
  39. Plisson C., Uzest M., Drucker M., Froissart R., Dumas C., Conway J., Thomas D., Blanc S., Bron P. 2005; Structure of the mature P3-virus particle complex of cauliflower mosaic virus revealed by cryo-electron microscopy. J Mol Biol 346:267–277 [View Article][PubMed]
    [Google Scholar]
  40. Prabu-Jeyabalan M., Nalivaika E., Schiffer C. A. 2002; Substrate shape determines specificity of recognition for HIV-1 protease: analysis of crystal structures of six substrate complexes. Structure 10:369–381[PubMed] [CrossRef]
    [Google Scholar]
  41. Qu R. D., Bhattacharyya M., Laco G. S., De Kochko A., Rao B. L., Kaniewska M. B., Elmer J. S., Rochester D. E., Smith C. E., Beachy R. N. 1991; Characterization of the genome of rice tungro bacilliform virus: comparison with Commelina yellow mottle virus and caulimoviruses. Virology 185:354–364 [View Article][PubMed]
    [Google Scholar]
  42. Roy A., Zhang Y. 2001; Protein structure prediction. In eLS Chichester: John Wiley & Sons, Ltd;
    [Google Scholar]
  43. Roy A., Kucukural A., Zhang Y. 2010; I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5:725–738 [View Article][PubMed]
    [Google Scholar]
  44. Sandmeyer S. B., Clemens K. A. 2010; Function of a retrotransposon nucleocapsid protein. RNA Biol 7:642–654 [View Article][PubMed]
    [Google Scholar]
  45. Stavolone L., Villani M. E., Leclerc D., Hohn T. 2005; A coiled-coil interaction mediates cauliflower mosaic virus cell-to-cell movement. Proc Natl Acad Sci U S A 102:6219–6224 [View Article][PubMed]
    [Google Scholar]
  46. Takemoto Y., Hibi T. 2001; Genes Ia, II, III, IV and V of Soybean chlorotic mottle virus are essential but the gene Ib product is non-essential for systemic infection. J Gen Virol 82:1481–1489 [View Article][PubMed]
    [Google Scholar]
  47. Tompa P., Fuxreiter M. 2008; Fuzzy complexes: polymorphism and structural disorder in protein-protein interactions. Trends Biochem Sci 33:2–8 [View Article][PubMed]
    [Google Scholar]
  48. Tözsér J. 2010; Comparative studies on retroviral proteases: substrate specificity. Viruses 2:147–165 [View Article][PubMed]
    [Google Scholar]
  49. Uversky V. N. 2013; A decade and a half of protein intrinsic disorder: biology still waits for physics. Protein Sci 22:693–724 [View Article][PubMed]
    [Google Scholar]
  50. Vo J. N., Mahfuz N. N., Lockhart B. E. L., Geering A. D. W. 2015; Improved methods for the purification and enrichment of banana streak virus for antibody production and protein detection. Eur J Plant Pathol 143:619–626 [View Article]
    [Google Scholar]
  51. Ward J. J., McGuffin L. J., Bryson K., Buxton B. F., Jones D. T. 2004a; The DISOPRED server for the prediction of protein disorder. Bioinformatics 20:2138–2139 [View Article][PubMed]
    [Google Scholar]
  52. Ward J. J., Sodhi J. S., McGuffin L. J., Buxton B. F., Jones D. T. 2004b; Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J Mol Biol 337:635–645 [View Article][PubMed]
    [Google Scholar]
  53. Xiong Y., Eickbush T. H. 1990; Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 9:3353–3362[PubMed]
    [Google Scholar]
  54. Xue Z., Xu D., Wang Y., Zhang Y. 2013; ThreaDom: extracting protein domain boundary information from multiple threading alignments. Bioinformatics 29:i247–i256 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000643
Loading
/content/journal/jgv/10.1099/jgv.0.000643
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited this month Most Cited RSS feed

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