Phylogenetic analysis of the large family of poxvirus ankyrin-repeat proteins reveals orthologue groups within and across chordopoxvirus genera

Journal of General Virology

Volumn 92, Issue 11, 2011, Pages 2596-2607

  Sonnberg, Stephanie ^a,b   Fleming, Stephen B ^a   Mercer, Andrew A ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; F BOX PROTEIN; VIRUS PROTEIN;

ARTICLE; CAPRIPOXVIRUS; CARBOXY TERMINAL SEQUENCE; CERVIDPOXVIRUS; CHORDOPOXVIRINAE; CHORDOPOXVIRUS; F BOX MOTIF; FOWLPOX VIRUS; GENE SEQUENCE; LEPORIPOXVIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; ORTHOPOXVIRUS; PARAPOXVIRUS; PHYLOGENY; POXVIRUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; SUIPOXVIRUS; VIRUS GENE;

ANKYRIN REPEAT; CHORDOPOXVIRINAE; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; PHYLOGENY; POLYMORPHISM, GENETIC; VIRAL PROTEINS;

CAPRIPOXVIRUS; LEPORIPOXVIRUS; POXVIRIDAE; SUIPOXVIRUS; VERTEBRATA; YATAPOXVIRUS;

EID: 80053987096     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.033654-0     Document Type: Article

References (68)

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.
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.
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.
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.
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.
6. Bolte, A. L., Meurer, J. & Kaleta, E. F. (1999). Avian host spectrum of avipoxviruses. Avian Pathol 28, 415-432.
7. Bork, P. (1993). Hundreds of ankyrin-like repeats in functionally diverse proteins: mobile modules that cross phyla horizontally? Proteins 17, 363-374.
8. Boyle, D. B. (2007). Genus Avipoxvirus. In Poxviruses, pp. 217-251.Edited by A. A. Mercer, A. Schmidt & O. Weber. Basel, Switzerland: Birkhauser Verlag
9. Bradley, R. R. & Terajima, M. (2005). Vaccinia virus K1L proteinmediates host-range function in RK-13 cells via ankyrin repeat and may interact with a cellular GTPase-activating protein. Virus Res 114, 104-112.
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.
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.
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-kB activation by tumor necrosis factor alpha but is independent of its host range function. J Virol 83, 4140-4152.
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.
14. Clewley, J. P. & Arnold, C. (1997). MEGALIGN. The multiple alignment Module of Lasergene. Methods Moi Biol 70, 112-129.
15. Damon, I. K. (2007). Poxviruses. In Field's Virology, 5th edn, pp. 2947-2975.Edited by D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman & S. E. Straus. Philadelphia, PA: Lippincott Williams & Wilkins.
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.
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. (2006). Genome sequence diversity and clues to the evolution of variola (smallpox) virus. Science 313, 807-812.
18. Finn, R. D., Mistry, J., Schuster-Böckler, B., Griffiths-Jones, S., Hollich, V., Lassmann, T., Moxon, S., Marshall, M., Khanna, A. (2006). Pfam: clans, web tools and services. Nucleic Acids Res 34 (Database issue), D247-D251.
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.
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.
21. Gubser, C., Hué, S., Kellam, P. & Smith, G. L. (2004). Poxvirus genomes: a phylogenetic analysis. J Gen Virol 85, 105-117.
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.
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.
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.
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.
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.
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.
28. Hughes, A. L., Irausquin, S. & Friedman, R. (2010). The evolutionary biology of poxviruses. Infect Genet Evol 10, 50-59.
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.
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.
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.
32. Kipreos, E. T. & Pagano, M. (2000). The F-box protein family. Genome Biol 1, reviews3002.1-reviews3002.7.
33. Kroemer, J. A. & Webb, B. A. (2005). Ikb-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.
34. Lee, H. J., Essani, K. & Smith, G. L. (2001). The genome sequence of Yaba-like disease virus, a yatapoxvirus. Virology 281, 170-192.
35. Li, J., Mahajan, A. & Tsai, M.-D. (2006). Ankyrin repeat: a unique motif mediating protein-protein interactions. Biochemistry 45, 15168-15178.
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. (2005). A tale of two clades: monkeypox viruses. J Gen Virol 86, 2661-2672.
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.
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.
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.
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.
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.
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.
43. Mohamed, M. R., Rahman, M. M., Lanchbury, J. S., Shattuck, D., Neff, C., Dufford, M., van Buuren, N., Fagan, K., Barry, M. & other authors (2009a). Proteomic screening of variola virus reveals a unique NF-kB inhibitor that is highly conserved among pathogenic orthopoxviruses. Proc Natl Acad Sci U S A 106, 9045-9050.
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-kB inhibitor that controls inflammatory cell influx into virus-infected tissues and is critical for virus pathogenesis. J Virol 83, 9223-9236.
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.
46. Moss, B. (2007). Poxviridae: the viruses and their replication. In Field's Virology, 5th edn, pp. 2905-2945.Edited by D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman & S. E. Straus. Philadelphia, PA: Lippincott Williams & Wilkins.
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.
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.
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.
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.
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.
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.
53. Shchelkunov, S., Totmenin, A. & Kolosova, I. (2002). Species-specific differences in organization of orthopoxvirus kelch-like proteins. Virus Genes 24, 157-162.
54. Shisler, J. L. & Jin, X. L. (2004). The vaccinia virus K1L gene product inhibits host NF-kB activation by preventing IkBa degradation. J Virol 78, 3553-3560.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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 PIKEA. J Virol 81, 2340-2348.
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.
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.
67. Willer, D. O., McFadden, G. & Evans, D. H. (1999). The complete genome sequence of shope (rabbit) fibroma virus. Virology 264, 319-343.
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.