1887

Abstract

Ankyrin-repeat (ANK) protein-interaction domains are common in cellular proteins but are relatively rare in viruses. Chordopoxviruses, however, encode a large number of ANK domain-containing ORFs of largely unknown function. Recently, a second protein-interaction domain, an F-box-like motif, was identified in several poxvirus ANK proteins. Cellular F-box proteins recruit substrates to the ubiquitination machinery of the cell, a putative function for ANK/poxviral F-box proteins. Using publicly available genome sequence data we examined all 328 predicted ANK proteins encoded by 27 chordopoxviruses that represented the eight vertebrate poxvirus genera whose members encode ANK proteins. Within these we identified 15 putative ANK protein orthologue groups within orthopoxviruses, five within parapoxviruses, 23 within avipoxviruses and seven across members of the genera , , , and . Sequence comparisons showed that members of each of these four clusters of orthologues were not closely related to members of any of the other clusters. Of these ORFs, 67 % encoded a C-terminal poxviral F-box-like motif, whose absence could largely be attributed to fragmentation of ORFs. Our findings suggest that the large family of poxvirus ANK proteins arose by extensive gene duplication and divergence that occurred independently in four major genus-based groups after the groups diverged from each other. It seems likely that the ancestor ANK proteins of poxviruses contained both the N-terminal ANK repeats and a C-terminal F-box-like domain, with the latter domain subsequently being lost in a small subset of these proteins.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.033654-0
2011-11-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/92/11/2596.html?itemId=/content/journal/jgv/10.1099/vir.0.033654-0&mimeType=html&fmt=ahah

References

  1. Afonso C. L., Tulman E. R., Lu Z., Zsak L., Kutish G. F., Rock D. L. 2000; The genome of fowlpox virus. J Virol 74:3815–3831 [View Article][PubMed]
    [Google Scholar]
  2. Afonso C. L., Tulman E. R., Lu Z., Zsak L., Osorio F. A., Balinsky C., Kutish G. F., Rock D. L. 2002; The genome of swinepox virus. J Virol 76:783–790 [View Article][PubMed]
    [Google Scholar]
  3. Afonso C. L., Delhon G., Tulman E. R., Lu Z., Zsak A., Becerra V. M., Zsak L., Kutish G. F., Rock D. L. 2005; Genome of deerpox virus. J Virol 79:966–977 [View Article][PubMed]
    [Google Scholar]
  4. Bai C., Sen P., Hofmann K., Ma L., Goebl M., Harper J. W., Elledge S. J. 1996; SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 86:263–274 [View Article][PubMed]
    [Google Scholar]
  5. Blanié S., Mortier J., Delverdier M., Bertagnoli S., Camus-Bouclainville C. 2009; M148R and M149R are two virulence factors for myxoma virus pathogenesis in the European rabbit. Vet Res 40:11 [View Article][PubMed]
    [Google Scholar]
  6. Bolte A. L., Meurer J., Kaleta E. F. 1999; Avian host spectrum of avipoxviruses. Avian Pathol 28:415–432 [View Article]
    [Google Scholar]
  7. Bork P. 1993; Hundreds of ankyrin-like repeats in functionally diverse proteins: mobile modules that cross phyla horizontally?. Proteins 17:363–374 [View Article][PubMed]
    [Google Scholar]
  8. Boyle D. B. 2007; Genus Avipoxvirus . In Poxviruses pp. 217–251 Edited by Mercer A. A., Schmidt A., Weber O. Basel, Switzerland: Birkhauser Verlag; [View Article]
    [Google Scholar]
  9. Bradley R. R., Terajima M. 2005; Vaccinia virus K1L protein mediates host-range function in RK-13 cells via ankyrin repeat and may interact with a cellular GTPase-activating protein. Virus Res 114:104–112 [View Article][PubMed]
    [Google Scholar]
  10. Brunetti C. R., Amano H., Ueda Y., Qin J., Miyamura T., Suzuki T., Li X., Barrett J. W., McFadden G. 2003; Complete genomic sequence and comparative analysis of the tumorigenic poxvirus Yaba monkey tumor virus. J Virol 77:13335–13347 [View Article][PubMed]
    [Google Scholar]
  11. Cameron C., Hota-Mitchell S., Chen L., Barrett J., Cao J. X., Macaulay C., Willer D., Evans D., McFadden G. 1999; The complete DNA sequence of myxoma virus. Virology 264:298–318 [View Article][PubMed]
    [Google Scholar]
  12. Chang S. J., Hsiao J. C., Sonnberg S., Chiang C. T., Yang M. H., Tzou D. L., Mercer A. A., Chang W. 2009; Poxvirus host range protein CP77 contains an F-box-like domain that is necessary to suppress NF-κB activation by tumor necrosis factor alpha but is independent of its host range function. J Virol 83:4140–4152 [View Article][PubMed]
    [Google Scholar]
  13. Chen N., Danila M. I., Feng Z., Buller R. M., Wang C., Han X., Lefkowitz E. J., Upton C. 2003; The genomic sequence of ectromelia virus, the causative agent of mousepox. Virology 317:165–186 [View Article][PubMed]
    [Google Scholar]
  14. Clewley J. P., Arnold C. 1997; Megalign. The multiple alignment Module of Lasergene. Methods Moi Biol 70:112–129
    [Google Scholar]
  15. Damon I. K. 2007; Poxviruses. In Field's Virology, 5th edn. pp. 2947–2975 Edited by Knipe D. M., Howley P. M., Griffin D. E., Lamb R. A., Martin M. A., Roizman B., Straus S. E. Philadelphia, PA: Lippincott Williams & Wilkins;
    [Google Scholar]
  16. Delhon G., Tulman E. R., Afonso C. L., Lu Z., de la Concha-Bermejillo A., Lehmkuhl H. D., Piccone M. E., Kutish G. F., Rock D. L. 2004; Genomes of the parapoxviruses ORF virus and bovine papular stomatitis virus. J Virol 78:168–177 [View Article][PubMed]
    [Google Scholar]
  17. Esposito J. J., Sammons S. A., Frace A. M., Osborne J. D., Olsen-Rasmussen M., Zhang M., Govil D., Damon I. K., Kline R. et al. 2006; Genome sequence diversity and clues to the evolution of variola (smallpox) virus. Science 313:807–812 [View Article][PubMed]
    [Google Scholar]
  18. Finn R. D., Mistry J., Schuster-Böckler B., Griffiths-Jones S., Hollich V., Lassmann T., Moxon S., Marshall M., Khanna A. et al. 2006; Pfam: clans, web tools and services. Nucleic Acids Res 34:Database issueD247–D251 [View Article][PubMed]
    [Google Scholar]
  19. Goebel S. J., Johnson G. P., Perkus M. E., Davis S. W., Winslow J. P., Paoletti E. 1990; The complete DNA sequence of vaccinia virus. Virology 179:247–266, 517–563 [View Article][PubMed]
    [Google Scholar]
  20. Gubser C., Smith G. L. 2002; The sequence of camelpox virus shows it is most closely related to variola virus, the cause of smallpox. J Gen Virol 83:855–872[PubMed]
    [Google Scholar]
  21. Gubser C., Hué S., Kellam P., Smith G. L. 2004; Poxvirus genomes: a phylogenetic analysis. J Gen Virol 85:105–117 [View Article][PubMed]
    [Google Scholar]
  22. Hautaniemi M., Ueda N., Tuimala J., Mercer A. A., Lahdenperä J., McInnes C. J. 2010; The genome of pseudocowpoxvirus: comparison of a reindeer isolate and a reference strain. J Gen Virol 91:1560–1576 [View Article][PubMed]
    [Google Scholar]
  23. He J. G., Deng M., Weng S. P., Li Z., Zhou S. Y., Long Q. X., Wang X. Z., Chan S.-M. 2001; Complete genome analysis of the mandarin fish infectious spleen and kidney necrosis iridovirus. Virology 291:126–139 [View Article][PubMed]
    [Google Scholar]
  24. Hendrickson R. C., Wang C., Hatcher E. L., Lefkowitz E. J. 2010; Orthopoxvirus genome evolution: the role of gene loss. Viruses 2:1933–1967 [View Article]
    [Google Scholar]
  25. Ho M. S., Ou C., Chan Y. R., Chien C. T., Pi H. 2008; The utility F-box for protein destruction. Cell Mol Life Sci 65:1977–2000 [View Article][PubMed]
    [Google Scholar]
  26. Hsiao J. C., Chung C. S., Drillien R., Chang W. 2004; The cowpox virus host range gene, CP77, affects phosphorylation of eIF2 alpha and vaccinia viral translation in apoptotic HeLa cells. Virology 329:199–212 [View Article][PubMed]
    [Google Scholar]
  27. Hsiao J. C., Chao C. C., Young M. J., Chang Y. T., Cho E. C., Chang W. 2006; A poxvirus host range protein, CP77, binds to a cellular protein, HMG20A, and regulates its dissociation from the vaccinia virus genome in CHO-K1 cells. J Virol 80:7714–7728 [View Article][PubMed]
    [Google Scholar]
  28. Hughes A. L., Irausquin S., Friedman R. 2010; The evolutionary biology of poxviruses. Infect Genet Evol 10:50–59 [View Article][PubMed]
    [Google Scholar]
  29. Jarmin S., Manvell R., Gough R. E., Laidlaw S. M., Skinner M. A. 2006; Avipoxvirus phylogenetics: identification of a PCR length polymorphism that discriminates between the two major clades. J Gen Virol 87:2191–2201 [View Article][PubMed]
    [Google Scholar]
  30. Jin J., Cardozo T., Lovering R. C., Elledge S. J., Pagano M., Harper J. W. 2004; Systematic analysis and nomenclature of mammalian F-box proteins. Genes Dev 18:2573–2580 [View Article][PubMed]
    [Google Scholar]
  31. Johnston J. B., Wang G., Barrett J. W., Nazarian S. H., Colwill K., Moran M., McFadden G. 2005; Myxoma virus M-T5 protects infected cells from the stress of cell cycle arrest through its interaction with host cell cullin-1. J Virol 79:10750–10763 [View Article][PubMed]
    [Google Scholar]
  32. Kipreos E. T., Pagano M. 2000; The F-box protein family. Genome Biol 1:reviews3002.1–reviews3002.7 [View Article][PubMed]
    [Google Scholar]
  33. Kroemer J. A., Webb B. A. 2005; Iκβ-related vankyrin genes in the Campoletis sonorensis ichnovirus: temporal and tissue-specific patterns of expression in parasitized Heliothis virescens lepidopteran hosts. J Virol 79:7617–7628 [View Article][PubMed]
    [Google Scholar]
  34. Lee H. J., Essani K., Smith G. L. 2001; The genome sequence of Yaba-like disease virus, a yatapoxvirus. Virology 281:170–192 [View Article][PubMed]
    [Google Scholar]
  35. Li J., Mahajan A., Tsai M.-D. 2006; Ankyrin repeat: a unique motif mediating protein–protein interactions. Biochemistry 45:15168–15178 [View Article][PubMed]
    [Google Scholar]
  36. Likos A. M., Sammons S. A., Olson V. A., Frace A. M., Li Y., Olsen-Rasmussen M., Davidson W., Galloway R., Khristova M. L. et al. 2005; A tale of two clades: monkeypox viruses. J Gen Virol 86:2661–2672 [View Article][PubMed]
    [Google Scholar]
  37. Lu Z., Li Y., Zhang Y., Kutish G. F., Rock D. L., Van Etten J. L. 1995; Analysis of 45 kb of DNA located at the left end of the chlorella virus PBCV-1 genome. Virology 206:339–352 [View Article][PubMed]
    [Google Scholar]
  38. Massung R. F., Liu L. I., Qi J., Knight J. C., Yuran T. E., Kerlavage A. R., Parsons J. M., Venter J. C., Esposito J. J. 1994; Analysis of the complete genome of smallpox variola major virus strain Bangladesh-1975. Virology 201:215–240 [View Article][PubMed]
    [Google Scholar]
  39. Mercer A. A., Wise L. M., Scagliarini A., McInnes C. J., Büttner M., Rziha H. J., McCaughan C. A., Fleming S. B., Ueda N., Nettleton P. F. 2002; Vascular endothelial growth factors encoded by Orf virus show surprising sequence variation but have a conserved, functionally relevant structure. J Gen Virol 83:2845–2855[PubMed]
    [Google Scholar]
  40. Mercer A. A., Fleming S. B., Ueda N. 2005; F-box-like domains are present in most poxvirus ankyrin repeat proteins. Virus Genes 31:127–133 [View Article][PubMed]
    [Google Scholar]
  41. Mercer A. A., Ueda N., Friederichs S. M., Hofmann K., Fraser K. M., Bateman T., Fleming S. B. 2006; Comparative analysis of genome sequences of three isolates of Orf virus reveals unexpected sequence variation. Virus Res 116:146–158 [View Article][PubMed]
    [Google Scholar]
  42. Meyer H., Neubauer H., Pfeffer M. 2002; Amplification of ‘variola virus-specific’ sequences in German cowpox virus isolates. J Vet Med B Infect Dis Vet Public Health 49:17–19[PubMed] [CrossRef]
    [Google Scholar]
  43. Mohamed M. R., Rahman M. M., Lanchbury J. S., Shattuck D., Neff C., Dufford M., van Buuren N., Fagan K., Barry M. et al. 2009a; Proteomic screening of variola virus reveals a unique NF-κB inhibitor that is highly conserved among pathogenic orthopoxviruses. Proc Natl Acad Sci U S A 106:9045–9050 [View Article][PubMed]
    [Google Scholar]
  44. Mohamed M. R., Rahman M. M., Rice A., Moyer R. W., Werden S. J., McFadden G. 2009b; Cowpox virus expresses a novel ankyrin repeat NF-κB inhibitor that controls inflammatory cell influx into virus-infected tissues and is critical for virus pathogenesis. J Virol 83:9223–9236 [View Article][PubMed]
    [Google Scholar]
  45. Mosavi L. K., Cammett T. J., Desrosiers D. C., Peng Z.-Y. 2004; The ankyrin repeat as molecular architecture for protein recognition. Protein Sci 13:1435–1448 [View Article][PubMed]
    [Google Scholar]
  46. Moss B. 2007; Poxviridae: the viruses and their replication. In Field’s Virology, 5th edn. pp. 2905–2945 Edited by Knipe D. M., Howley P. M., Griffin D. E., Lamb R. A., Martin M. A., Roizman B., Straus S. E. Philadelphia, PA: Lippincott Williams & Wilkins;
    [Google Scholar]
  47. Perkus M. E., Goebel S. J., Davis S. W., Johnson G. P., Limbach K., Norton E. K., Paoletti E. 1990; Vaccinia virus host range genes. Virology 179:276–286 [View Article][PubMed]
    [Google Scholar]
  48. Ramsey-Ewing A. L., Moss B. 1996; Complementation of a vaccinia virus host-range K1L gene deletion by the nonhomologous CP77 gene. Virology 222:75–86 [View Article][PubMed]
    [Google Scholar]
  49. Raoult D., Audic S., Robert C., Abergel C., Renesto P., Ogata H., La Scola B., Suzan M., Claverie J. M. 2004; The 1.2-megabase genome sequence of Mimivirus. Science 306:1344–1350 [View Article][PubMed]
    [Google Scholar]
  50. Schulman B. A., Carrano A. C., Jeffrey P. D., Bowen Z., Kinnucan E. R., Finnin M. S., Elledge S. J., Harper J. W., Pagano M., Pavletich N. P. 2000; Insights into SCF ubiquitin ligases from the structure of the Skp1-Skp2 complex. Nature 408:381–386 [View Article][PubMed]
    [Google Scholar]
  51. Shchelkunov S. N., Safronov P. F., Totmenin A. V., Petrov N. A., Ryazankina O. I., Gutorov V. V., Kotwal G. J. 1998; The genomic sequence analysis of the left and right species-specific terminal region of a cowpox virus strain reveals unique sequences and a cluster of intact ORFs for immunomodulatory and host range proteins. Virology 243:432–460 [View Article][PubMed]
    [Google Scholar]
  52. Shchelkunov S. N., Totmenin A. V., Loparev V. N., Safronov P. F., Gutorov V. V., Chizhikov V. E., Knight J. C., Parsons J. M., Massung R. F., Esposito J. J. 2000; Alastrim smallpox variola minor virus genome DNA sequences. Virology 266:361–386 [View Article][PubMed]
    [Google Scholar]
  53. Shchelkunov S., Totmenin A., Kolosova I. 2002; Species-specific differences in organization of orthopoxvirus kelch-like proteins. Virus Genes 24:157–162 [View Article][PubMed]
    [Google Scholar]
  54. Shisler J. L., Jin X. L. 2004; The vaccinia virus K1L gene product inhibits host NF-κB activation by preventing IκBα degradation. J Virol 78:3553–3560 [View Article][PubMed]
    [Google Scholar]
  55. Skowyra D., Craig K. L., Tyers M., Elledge S. J., Harper J. W. 1997; F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91:209–219 [View Article][PubMed]
    [Google Scholar]
  56. Sonnberg S., Seet B. T., Pawson T., Fleming S. B., Mercer A. A. 2008; Poxvirus ankyrin repeat proteins are a unique class of F-box proteins that associate with cellular SCF1 ubiquitin ligase complexes. Proc Natl Acad Sci U S A 105:10955–10960 [View Article][PubMed]
    [Google Scholar]
  57. Sperling K. M., Schwantes A., Schnierle B. S., Sutter G. 2008; The highly conserved orthopoxvirus 68k ankyrin-like protein is part of a cellular SCF ubiquitin ligase complex. Virology 374:234–239 [View Article][PubMed]
    [Google Scholar]
  58. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 [CrossRef]
    [Google Scholar]
  59. Tulman E. R., Afonso C. L., Lu Z., Zsak L., Kutish G. F., Rock D. L. 2001; Genome of lumpy skin disease virus. J Virol 75:7122–7130 [View Article][PubMed]
    [Google Scholar]
  60. Tulman E. R., Afonso C. L., Lu Z., Zsak L., Sur J. H., Sandybaev N. T., Kerembekova U. Z., Zaitsev V. L., Kutish G. F., Rock D. L. 2002; The genomes of sheeppox and goatpox viruses. J Virol 76:6054–6061 [View Article][PubMed]
    [Google Scholar]
  61. Tulman E. R., Afonso C. L., Lu Z., Zsak L., Kutish G. F., Rock D. L. 2004; The genome of canarypox virus. J Virol 78:353–366 [View Article][PubMed]
    [Google Scholar]
  62. Tulman E. R., Delhon G., Afonso C. L., Lu Z., Zsak L., Sandybaev N. T., Kerembekova U. Z., Zaitsev V. L., Kutish G. F., Rock D. L. 2006; Genome of horsepox virus. J Virol 80:9244–9258 [View Article][PubMed]
    [Google Scholar]
  63. van Buuren N., Couturier B., Xiong Y., Barry M. 2008; Ectromelia virus encodes a novel family of F-box proteins that interact with the SCF complex. J Virol 82:9917–9927 [View Article][PubMed]
    [Google Scholar]
  64. Werden S. J., Barrett J. W., Wang G., Stanford M. M., McFadden G. 2007; M-T5, the ankyrin repeat, host range protein of myxoma virus, activates Akt and can be functionally replaced by cellular PIKE-A. J Virol 81:2340–2348 [View Article][PubMed]
    [Google Scholar]
  65. Werden S. J., Lanchbury J., Shattuck D., Neff C., Dufford M., McFadden G. 2009; The myxoma virus m-t5 ankyrin repeat host range protein is a novel adaptor that coordinately links the cellular signaling pathways mediated by Akt and Skp1 in virus-infected cells. J Virol 83:12068–12083 [View Article][PubMed]
    [Google Scholar]
  66. Willems A. R., Schwab M., Tyers M. 2004; A hitchhiker’s guide to the cullin ubiquitin ligases: SCF and its kin. Biochim Biophys Acta 1695:133–170 [View Article][PubMed]
    [Google Scholar]
  67. Willer D. O., McFadden G., Evans D. H. 1999; The complete genome sequence of shope (rabbit) fibroma virus. Virology 264:319–343 [View Article][PubMed]
    [Google Scholar]
  68. Xing K., Deng R. Q., Wang J. W., Feng J. H., Huang M. S., Wang X. Z. 2006; Genome-based phylogeny of poxvirus. Intervirology 49:207–214 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.033654-0
Loading
/content/journal/jgv/10.1099/vir.0.033654-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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