Genome analysis of non-human primate polyomaviruses

Infection, Genetics and Evolution

Volumn 26, Issue , 2014, Pages 283-294

  Ehlers, Bernhard ^a   Moens, Ugo ^b  

^a ROBERT KOCH INSTITUTE   (Germany)

^b UNIVERSITY OF TROMSØ   (Norway)

Author keywords

Agno; Alto; Large T; Small T; VP1; VP2

Indexed keywords

CAPSID PROTEIN; MICRORNA; PROTEIN VP1; PROTEIN VP2; TUMOR ANTIGEN; VIRUS LARGE T ANTIGEN; REGULATORY RNA SEQUENCE; VIRUS T ANTIGEN;

BASE PAIRING; GENOME ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYOMA VIRUS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; REVIEW; RNA SEQUENCE; UNINDEXED SEQUENCE; VIRUS REPLICATION; ANIMAL; CHEMISTRY; CLASSIFICATION; GENETICS; GENOMICS; GENOTYPE; METABOLISM; OPEN READING FRAME; PHYLOGENY; POLYOMAVIRUS; POLYOMAVIRUS INFECTION; PRIMATE; PRIMATE DISEASE; REGULATORY RNA SEQUENCE; VETERINARY; VIROLOGY; VIRUS GENE; VIRUS GENOME; VIRUS INFECTION;

ANIMALS; ANTIGENS, VIRAL, TUMOR; CAPSID PROTEINS; GENES, VIRAL; GENOME, VIRAL; GENOMICS; GENOTYPE; MICRORNAS; OPEN READING FRAMES; PHYLOGENY; POLYOMAVIRUS; POLYOMAVIRUS INFECTIONS; PRIMATE DISEASES; PRIMATES; REGULATORY SEQUENCES, RIBONUCLEIC ACID; TUMOR VIRUS INFECTIONS;

EID: 84903853539     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2014.05.030     Document Type: Review

References (82)

1. Abend J.R., Joseph A.E., Das D., Campbell-Cecen D.B., Imperiale M.J. A truncated T antigen expressed from an alternatively spliced BK virus early mRNA. J. Gen. Virol. 2009, 90:1238-1245.
2. An P., Saenz Robles M.T., Pipas J.M. Large T antigens of polyomaviruses: amazing molecular machines. Annu. Rev. Microbiol. 2012, 66:213-236.
3. Anisimova M., Gil M., Dufayard J.F., Dessimoz C., Gascuel O. Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Syst. Biol. 2011, 60:685-699.
4. Boyapati A., Wilson M., Yu J., Rundell K. SV40 17KT antigen complements dnaj mutations in large T antigen to restore transformation of primary human fibroblasts. Virology 2003, 315:148-158.
5. Brade L., Muller-Lantzsch N., zur Hausen H. B-lymphotropic papovavirus and possibility of infections in humans. J. Med. Virol. 1981, 6:301-308.
6. Cantalupo P., Doering A., Sullivan C.S., Pal A., Peden K.W., Lewis A.M., Pipas J.M. Complete nucleotide sequence of polyomavirus SA12. J. Virol. 2005, 79:13094-13104.
7. Carter J.J., Daugherty M.D., Qi X., Bheda-Malge A., Wipf G.C., Robinson K., Roman A., Malik H.S., Galloway D.A. Identification of an overprinting gene in Merkel cell polyomavirus provides evolutionary insight into the birth of viral genes. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:12744-12749.
8. Castresana J. Topological variation in single-gene phylogenetic trees. Genome Biol. 2007, 8:216.
9. Chen C.J., Cox J.E., Kincaid R.P., Martinez A., Sullivan C.S. Divergent MicroRNA targetomes of closely related circulating strains of a polyomavirus. J. Virol. 2013, 87:11135-11147.
10. Cicala C., Pompetti F., Carbone M. SV40 induces mesotheliomas in hamsters. Am. J. Pathol. 1993, 142:1524-1533.
11. Coursaget P., Samimi M., Nicol J.T., Gardair C., Touze A. Human Merkel cell polyomavirus: virological background and clinical implications. APMIS 2013, 121:755-769.
12. Daniels R., Sadowicz D., Hebert D.N. A very late viral protein triggers the lytic release of SV40. PLoS Pathog. 2007, 3:e98.
13. Darriba D., Taboada G.L., Doallo R., Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 2011, 27:1164-1165.
14. Deuzing I., Fagrouch Z., Groenewoud M.J., Niphuis H., Kondova I., Bogers W., Verschoor E.J. Detection and characterization of two chimpanzee polyomavirus genotypes from different subspecies. Virol. J. 2010, 7:347.
15. Ehlers B., Wieland U. The novel human polyomaviruses HPyV6, 7, 9 and beyond. APMIS 2013, 121:783-795.
16. Fagrouch Z., Karremans K., Deuzing I., van Gessel S., Niphuis H., Bogers W., Verschoor E.J. Molecular analysis of a novel simian virus 40 (SV40) type in rhesus macaques and evidence for double infections with the classical SV40 type. J. Clin. Microbiol. 2011, 49:1280-1286.
17. Fagrouch Z., Sarwari R., Lavergne A., Delaval M., de Thoisy B., Lacoste V., Verschoor E.J. Novel polyomaviruses in South American bats and their relationship to other members of the family polyomaviridae. J. Gen. Virol. 2012, 93:2652-2657.
18. Fiers W., Contreras R., Haegemann G., Rogiers R., Van de Voorde A., Van Heuverswyn H., Van Herreweghe J., Volckaert G., Ysebaert M. Complete nucleotide sequence of SV40 DNA. Nature 1978, 273:113-120.
19. Fluck M.M., Schaffhausen B.S. Lessons in signaling and tumorigenesis from polyomavirus middle T antigen. Microbiol. Mol. Biol. Rev. 2009, 73:542-563. (Table of Contents).
20. Furuno A., Kanda T., Yoshiike K. Monkey B-lymphotropic papovavirus genome: the entire DNA sequence and variable regions. Jpn. J. Med. Sci. Biol. 1986, 39:151-161.
21. Gardner S.D., Field A.M., Coleman D.V., Hulme B. New human papovavirus (B.K.) isolated from urine after renal transplantation. Lancet 1971, 1:1253-1257.
22. Gerits N., Moens U. Agnoprotein of mammalian polyomaviruses. Virology 2012, 432:316-326.
23. Girardi A.J., Sweet B.H., Slotnick V.B., Hilleman M.R. Development of tumors in hamsters inoculated in the neonatal period with vacuolating virus, SV-40. Proc. Soc. Exp. Biol. Med. 1962, 109:649-660.
24. Gouy M., Guindon S., Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 2010, 27:221-224.
25. Groenewoud M.J., Fagrouch Z., van Gessel S., Niphuis H., Bulavaite A., Warren K.S., Heeney J.L., Verschoor E.J. Characterization of novel polyomaviruses from Bornean and Sumatran orangutans. J. Gen. Virol. 2010, 91:653-658.
26. Gross L. A filterable agent, recovered from Ak leukemic extracts, causing salivary gland carcinomas in C3H mice. Proc. Soc. Exp. Biol. Med. 1953, 83:414-421.
27. Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 2010, 59:307-321.
28. Hausser J., Berninger P., Rodak C., Jantscher Y., Wirth S., Zavolan M. MirZ: an integrated microRNA expression atlas and target prediction resource. Nucleic Acids Res. 2009, 37:W266-272.
29. Johne R., Enderlein D., Nieper H., Muller H. Novel polyomavirus detected in the feces of a chimpanzee by nested broad-spectrum PCR. J. Virol. 2005, 79:3883-3887.
30. Kean J.M., Rao S., Wang M., Garcea R.L. Seroepidemiology of human polyomaviruses. PLoS Pathog. 2009, 5:e1000363.
31. Korup S., Rietscher J., Calvignac-Spencer S., Trusch F., Hofmann J., Moens U., Sauer I., Voigt S., Schmuck R., Ehlers B. Identification of a novel human polyomavirus in organs of the gastrointestinal tract. PLoS One 2013, 8:e58021.
32. Kosugi S., Hasebe M., Tomita M., Yanagawa H. Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:10171-10176.
33. Ishii N., Minami N., Chen E.Y., Medina A.L., Chico M.M., Kasamutsu H. Analysis of a nuclear localization signal of simian virus 40 major capsid protein Vp1. J. Virol. 1996, 70:1317-1322.
34. Lagatie O., Tritsmans L., Stuyver L.J. The miRNA world of polyomaviruses. Virol. J. 2013, 10:268.
35. Leendertz F.H., Scuda N., Cameron K.N., Kidega T., Zuberbuhler K., Leendertz S.A., Couacy-Hymann E., Boesch C., Calvignac S., Ehlers B. African great apes are naturally infected with polyomaviruses closely related to Merkel cell polyomavirus. J. Virol. 2011, 85:916-924.
36. Liddington R.C., Yan Y., Moulai J., Sahli R., Benjamin T.L., Harrison S.C. Structure of simian virus 40 at 3.8-A resolution. Nature 1991, 354:278-284.
37. Lim E.S., Reyes A., Antonio M., Saha D., Ikumapayi U.N., Adeyemi M., Stine O.C., Skelton R., Brennan D.C., Mkakosya R.S., Manary M.J., Gordon J.I., Wang D. Discovery of STL polyomavirus, a polyomavirus of ancestral recombinant origin that encodes a unique T antigen by alternative splicing. Virology 2013, 436:295-303.
38. Malherbe H., Harwin R. The cytopathic effects of vervet monkey viruses. S. Afr. Med. J. 1963, 37:407-411.
39. Misra V., Dumonceaux T., Dubois J., Willis C., Nadin-Davis S., Severini A., Wandeler A., Lindsay R., Artsob H. Detection of polyoma and corona viruses in bats of Canada. J. Gen. Virol. 2009, 90:2015-2022.
40. Moens U., Van Ghelue M., Song X., Ehlers B. Serological cross-reactivity between human polyomaviruses. Rev. Med. Virol. 2013, 23:250-264.
41. Neu U., Allen S.A., Blaum B.S., Liu Y., Frank M., Palma A.S., Stroh L.J., Feizi T., Peters T., Atwood W.J., Stehle T. A structure-guided mutation in the major capsid protein retargets BK polyomavirus. PLoS Pathog. 2013, 9:e1003688.
42. Neu U., Hengel H., Blaum B.S., Schowalter R.M., Macejak D., Gilbert M., Wakarchuk W.W., Imamura A., Ando H., Kiso M., Arnberg N., Garcea R.L., Peters T., Buck C.B., Stehle T. Structures of Merkel cell polyomavirus VP1 complexes define a sialic acid binding site required for infection. PLoS Pathog. 2012, 8:e1002738.
43. Neu U., Khan Z.M., Schuch B., Palma A.S., Liu Y., Pawlita M., Feizi T., Stehle T. Structures of B-lymphotropic polyomavirus VP1 in complex with oligosaccharide ligands. PLoS Pathog. 2013, 9:e1003714.
44. Neu U., Maginnis M.S., Palma A.S., Stroh L.J., Nelson C.D., Feizi T., Atwood W.J., Stehle T. Structure-function analysis of the human JC polyomavirus establishes the LSTc pentasaccharide as a functional receptor motif. Cell Host Microbe 2010, 8:309-319.
45. Neu U., Wang J., Macejak D., Garcea R.L., Stehle T. Structures of the major capsid proteins of the human Karolinska Institutet and Washington University polyomaviruses. J. Virol. 2011, 85:7384-7392.
46. Neu U., Woellner K., Gauglitz G., Stehle T. Structural basis of GM1 ganglioside recognition by simian virus 40. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:5219-5224.
47. Nilsson J., Miyazaki N., Xing L., Wu B., Hammar L., Li T.C., Takeda N., Miyamura T., Cheng R.H. Structure and assembly of a T=1 virus-like particle in BK polyomavirus. J. Virol. 2005, 79:5337-5345.
48. Padgett B.L., Walker D.L., ZuRhein G.M., Eckroade R.J., Dessel B.H. Cultivation of papova-like virus from human brain with progressive multifocal leucoencephalopathy. Lancet 1971, 1:1257-1260.
49. Parrish C.R., Holmes E.C., Morens D.M., Park E.C., Burke D.S., Calisher C.H., Laughlin C.A., Saif L.J., Daszak P. Cross-species virus transmission and the emergence of new epidemic diseases. Microbiol. Mol. Biol. Rev. 2008, 72:457-470.
50. Pastrana D.V., Tolstov Y.L., Becker J.C., Moore P.S., Chang Y., Buck C.B. Quantitation of human seroresponsiveness to Merkel cell polyomavirus. PLoS Pathog. 2009, 5:e1000578.
51. Pawlita M., Clad A., zur Hausen H. Complete DNA sequence of lymphotropic papovavirus: prototype of a new species of the polyomavirus genus. Virology 1985, 143:196-211.
52. Pipas J.M. Common and unique features of T antigens encoded by the polyomavirus group. J. Virol. 1992, 66:3979-3985.
53. Portolani M., Borgatti M. Stable transformation of mouse, rabbit and monkey cells and abortive transformation of human cells by BK virus, a human papovavirus. J. Gen. Virol. 1978, 38:369-374.
54. Purchio A.F., Fareed G.C. Transformation of human embryonic kidney cells by human papovarirus BK. J. Virol. 1979, 29:763-769.
55. Sapp M., Day P.M. Structure, attachment and entry of polyoma- and papillomaviruses. Virology 2009, 384:400-409.
56. Saribas A.S., Mun S., Johnson J., El-Hajmoussa M., White M.K., Safak M. Human polyoma JC virus minor capsid proteins, VP2 and VP3, enhance large T antigen binding to the origin of viral DNA replication: evidence for their involvement in regulation of the viral DNA replication. Virology 2014, 449:1-16.
57. Sauvage V., Foulongne V., Cheval J., Ar Gouilh M., Pariente K., Dereure O., Manuguerra J.C., Richardson J., Lecuit M., Burguiere A., Caro V., Eloit M. Human polyomavirus related to African green monkey lymphotropic polyomavirus. Emerg. Infect. Dis. 2011, 17:1364-1370.
58. Schowalter R.M., Buck C.B. The Merkel cell polyomavirus minor capsid protein. PLoS Pathog. 2013, 9:e1003558.
59. Scuda N., Hofmann J., Calvignac-Spencer S., Ruprecht K., Liman P., Kuhn J., Hengel H., Ehlers B. A novel human polyomavirus closely related to the African green monkey-derived lymphotropic polyomavirus. J. Virol. 2011, 85:4586-4590.
60. Scuda N., Madinda N.F., Akoua-Koffi C., Adjogoua E.V., Wevers D., Hofmann J., Cameron K.N., Leendertz S.A., Couacy-Hymann E., Robbins M., Boesch C., Jarvis M.A., Moens U., Mugisha L., Calvignac-Spencer S., Leendertz F.H., Ehlers B. Novel polyomaviruses of nonhuman primates: genetic and serological predictors for the existence of multiple unknown polyomaviruses within the human population. PLoS Pathog. 2013, 9:e1003429.
61. Shah K.V. SV40 and human cancer: a review of recent data. Int. J. Cancer 2007, 120:215-223.
62. Shuda M., Feng H., Kwun H.J., Rosen S.T., Gjoerup O., Moore P.S., Chang Y. T antigen mutations are a human tumor-specific signature for Merkel cell polyomavirus. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:16272-16277.
63. Stehle T., Gamblin S.J., Yan Y., Harrison S.C. The structure of simian virus 40 refined at 3.1A resolution. Structure 1996, 4:165-182.
64. Stehle T., Harrison S.C. High-resolution structure of a polyomavirus VP1-oligosaccharide complex: implications for assembly and receptor binding. EMBO J. 1997, 16:5139-5148.
65. Stevens H., Bertelsen M.F., Sijmons S., Van Ranst M., Maes P. Characterization of a novel polyomavirus isolated from a fibroma on the trunk of an African elephant (Loxodonta africana). PLoS One 2013, 8:e77884.
66. Sullivan C.S., Grundhoff A.T., Tevethia S., Pipas J.M., Ganem D. SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells. Nature 2005, 435:682-686.
67. Suzuki T., Orba Y., Okada Y., Sunden Y., Kimura T., Tanaka S., Nagashima K., Hall W.W., Sawa H. The human polyoma JC virus agnoprotein acts as a viroporin. PLoS Pathog. 2010, 6:e1000801.
68. Sweet B.H., Hilleman M.R. The vacuolating virus, S.V. 40. Proc. Soc. Exp. Biol. Med. 1960, 105:420-427.
69. Takemoto K.K., Furuno A., Kato K., Yoshiike K. Biological and biochemical studies of African green monkey lymphotropic papovavirus. J. Virol. 1982, 42:502-509.
70. Takemoto K.K., Segawa K. A new monkey lymphotropic papovavirus: characterization of the virus and evidence of a related virus in humans. Prog. Clin. Biol. Res. 1983, 105:87-96.
71. Topalis D., Andrei G., Snoeck R. The large tumor antigen: a "Swiss Army knife" protein possessing the functions required for the polyomavirus life cycle. Antiviral Res. 2013, 97:122-136.
72. Trowbridge P.W., Frisque R.J. Identification of three new JC virus proteins generated by alternative splicing of the early viral mRNA. J. Neurovirol. 1995, 1:195-206.
73. Trusch F., Klein M., Finsterbusch T., Kuhn J., Hofmann J., Ehlers B. Seroprevalence of human polyomavirus 9 and cross-reactivity to African green monkey-derived lymphotropic polyomavirus. J. Gen. Virol. 2012, 93:698-705.
74. Van Ghelue M., Khan M.T., Ehlers B., Moens U. Genome analysis of the new human polyomaviruses. Rev. Med. Virol. 2012, 22:354-377.
75. Verschoor E.J., Groenewoud M.J., Fagrouch Z., Kewalapat A., van Gessel S., Kik M.J., Heeney J.L. Molecular characterization of the first polyomavirus from a new world primate: squirrel monkey polyomavirus. J. Gen. Virol. 2008, 89:130-137.
76. Viscidi R.P., Rollison D.E., Sondak V.K., Silver B., Messina J.L., Giuliano A.R., Fulp W., Ajidahun A., Rivanera D. Age-specific seroprevalence of Merkel cell polyomavirus, BK virus, and JC virus. Clin. Vaccine Immunol. 2011, 18:1737-1743.
77. Viscidi R.P., Rollison D.E., Viscidi E., Clayman B., Rubalcaba E., Daniel R., Major E.O., Shah K.V. Serological cross-reactivities between antibodies to simian virus 40, BK virus, and JC virus assessed by virus-like-particle-based enzyme immunoassays. Clin. Diagn. Lab. Immunol. 2003, 10:278-285.
78. Yamaguchi H., Kobayashi S., Ishii A., Ogawa H., Nakamura I., Moonga L., Hang'ombe B.M., Mweene A.S., Thomas Y., Kimura T., Sawa H., Orba Y. Identification of a novel polyomavirus from vervet monkeys in Zambia. J. Gen. Virol. 2013, 94:1357-1364.
79. Yamaguchi H., Kobayashi S., Maruyama J., Sasaki M., Takada A., Kimura T., Sawa H., Orba Y. Role of the C-terminal region of vervet monkey polyomavirus 1 VP1 in virion formation. J. Vet. Med. Sci. 2014.
80. You X., Zhang Z., Fan J., Cui Z., Zhang X.E. Functionally orthologous viral and cellular microRNAs studied by a novel dual-fluorescent reporter system. PLoS One 2012, 7:e36157.
81. Zerrahn J., Knippschild U., Winkler T., Deppert W. Independent expression of the transforming amino-terminal domain of SV40 large I antigen from an alternatively spliced third SV40 early mRNA. EMBO J. 1993, 12:4739-4746.
82. zur Hausen H., Gissmann L. Lymphotropic papovaviruses isolated from African green monkey and human cells. Med. Microbiol. Immunol. 1979, 167:137-153.