Widespread distribution and structural diversity of Type IV IRESs in members of Picornaviridae

Virology

Volumn 478, Issue , 2015, Pages 61-74

  Asnani, Mukta ^a   Kumar, Parimal ^a   Hellen, Christopher U T ^a  

^a SUNY DOWNSTATE MEDICAL CENTER   (United States)

Author keywords

Evolution; IRES; Picornavirus; Recombination; RNA structure

Indexed keywords

CAPSID PROTEIN; RNA 18S; UNTRANSLATED RNA; MESSENGER RNA; VIRUS RNA;

5' UNTRANSLATED REGION; ARTICLE; AVIAN ENCEPHALOMYELITIS ENTEROVIRUS; AVIAN SAPELOVIRUS 1; BINDING SITE; GENETIC CONSERVATION; HEPATITIS A VIRUS; HORIZONTAL GENE TRANSFER; INTERNAL RIBOSOME ENTRY SITE; KOBUVIRUS; LIMNIPIVIRUS; MEGRIVIRUS; NONHUMAN; PARECHOVIRUS; PASIVIRUS; PICORNAVIRIDAE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; RAFIVIRUS; SAPELOVIRUS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; TRANSLATION INITIATION; VIRAL GENETICS; VIRUS GENOME; VIRUS MORPHOLOGY; VIRUS RECOMBINATION; VIRUS STRAIN; X RAY CRYSTALLOGRAPHY; CONFORMATION; CONSERVED SEQUENCE; GENETIC RECOMBINATION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; PROTEIN SYNTHESIS; RIBOSOME;

KOBUVIRUS; PARECHOVIRUS; PICORNAVIRIDAE;

CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; NUCLEIC ACID CONFORMATION; PICORNAVIRIDAE; PROTEIN BIOSYNTHESIS; RECOMBINATION, GENETIC; RIBOSOMES; RNA, MESSENGER; RNA, VIRAL;

EID: 84923668831     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2015.02.016     Document Type: Article

References (94)

1. Bakhshesh M., Groppelli E., Willcocks M.M., Royall E., Belsham G.J., Roberts L.O. The picornavirus avian encephalomyelitis virus possesses a hepatitis C virus-like internal ribosome entry site element. J. Virol. 2008, 82:1993-2003.
2. Barbknecht M., Sepsenwol S., Leis E., Tuttle-Lau M., Gaikowski M., Knowles N.J., Lasee B., Hoffman M.A. Characterization of a new picornavirus isolated from the freshwater fish Lepomis macrochirus. J. Gen. Virol. 2014, 95:601-613.
3. Becher P., Tautz N. RNA recombination in pestiviruses: cellular RNA sequences in viral genomes highlight the role of host factors for viral persistence and lethal disease. RNA Biol. 2011, 8:216-224.
4. Benschop K.S., de Vries M., Minnaar R.P., Stanway G., van der Hoek L., Wolthers K.C., Simmonds P. Comprehensive full-length sequence analyses of human parechoviruses: diversity and recombination. J. Gen. Virol. 2010, 91:145-154.
5. Berry K.E., Waghray S., Doudna J.A. The HCV IRES pseudoknot positions the initiation codon on the 40S ribosomal subunit. RNA 2010, 16:1559-1569.
6. Berry K.E., Waghray S., Mortimer S.A., Bai Y., Doudna J.A. Crystal structure of the HCV IRES central domain reveals strategy for start-codon positioning. Structure 2011, 19:1456-1466.
7. Boehringer D., Thermann R., Ostareck-Lederer A., Lewis J.D., Stark H. Structure of the hepatitis C virus IRES bound to the human 80S ribosome: remodeling of the HCV IRES. Structure 2005, 13:1695-1706.
8. Boerneke M.A., Dibrov S.M., Gu J., Wyles D.L., Hermann T. Functional conservation despite structural divergence in ligand-responsive RNA switches. Proc. Natl. Acad. Sci. USA 2014, 111:15952-15957.
9. Boros Á., Kiss T., Kiss O., Pankovics P., Kapusinszky B., Delwart E., Reuter G. Genetic characterization of a novel picornavirus distantly related to the marine mammal-infecting aquamaviruses in a long-distance migrant bird species, European Roller (Coracias garrulus). J. Gen. Virol. 2013, 94:2029-2035.
10. Boros A., Pankovics P., Knowles N.J., Nemes C., Delwart E., Reuter G. Comparative complete genome analysis of chicken and Turkey megriviruses (family picornaviridae): long 3' untranslated regions with a potential second open reading frame and evidence for possible recombination. J. Virol. 2014, 88:6434-6443.
11. Boros A., Pankovics P., Reuter G. Avian picornaviruses: molecular evolution, genome diversity and unusual genome features of a rapidly expanding group of viruses in birds. Infect. Genet. Evol. 2014, 28C:151-166.
12. Brown E.A., Zajac A.J., Lemon S.M. In vitro characterization of an internal ribosomal entry site (IRES) present within the 5' nontranslated region of hepatitis A virus RNA: comparison with the IRES of encephalomyocarditis virus. J. Virol. 1994, 68:1066-1074.
13. Burbelo P.D., Dubovi E.J., Simmonds P., Medina J.L., Henriquez J.A., Mishra N., Wagner J., Tokarz R., Cullen J.M., Iadarola M.J., Rice C.M., Lipkin W.I., Kapoor A. Serology-enabled discovery of genetically diverse hepaciviruses in a new host. J. Virol. 2012, 86:6171-6178.
14. Byun Y., Han K. PseudoViewer3: generating planar drawings of large-scale RNA structures with pseudoknots. Bioinformatics 2009, 25:1435-1437.
15. Caisová L., Melkonian M. Evolution of helix formation in the ribosomal Internal Transcribed Spacer 2 (ITS2) and its significance for RNA secondary structures. J. Mol. Evol. 2014, 78:324-337.
16. Chard L.S., Bordeleau M.E., Pelletier J., Tanaka J., Belsham G.J. Hepatitis C virus-related internal ribosome entry sites are found in multiple genera of the family Picornaviridae. J. Gen. Virol. 2006, 87:927-936.
17. Chard L.S., Kaku Y., Jones B., Nayak A., Belsham G.J. Functional analyses of RNA structures shared between the internal ribosome entry sites of hepatitis C virus and the picornavirus porcine teschovirus 1 Talfan. J. Virol. 2006, 80:1271-1279.
18. Charini W.A., Todd S., Gutman G.A., Semler B.L. Transduction of a human RNA sequence by poliovirus. J. Virol. 1994, 68:6547-6552.
19. deBreyne S., Yu Y., Pestova T.V., Hellen C.U. Factor requirements for translation initiation on the Simian picornavirus internal ribosomal entry site. RNA 2008, 14:367-380.
20. Easton L.E., Locker N., Lukavsky P.J. Conserved functional domains and a novel tertiary interaction near the pseudoknot drive translational activity of hepatitis C virus and hepatitis C virus-like internal ribosome entry sites. Nucleic Acids Res. 2009, 37:5537-5549.
21. Filbin M.E., Vollmar B.S., Shi D., Gonen T., Kieft J.S. HCV IRES manipulates the ribosome to promote the switch from translation initiation to elongation. Nat. Struct. Mol. Biol. 2013, 20:150-158.
22. Firth C., Bhat M., Firth M.A., Williams S.H., Frye M.J., Simmonds P., Conte J.M., Ng J., Garcia J., Bhuva N.P., Lee B., Che X., Quan P.L., Lipkin W.I. Detection of zoonotic pathogens and characterization of novel viruses carried by commensal Rattus norvegicus in New York City. mBio 2014, 5:e01933-14.
23. Fletcher S.P., Jackson R.J. Pestivirus internal ribosome entry site (IRES) structure and function: elements in the 5' untranslated region important for IRES function. J. Virol. 2002, 76:5024-5033.
24. Friis M.B., Rasmussen T.B., Belsham G.J. Modulation of translation initiation efficiency in classical swine fever virus. J. Virol. 2012, 86:8681-8692.
25. Gmyl A.P., Korshenko S.A., Belousov E.V., Khitrina E.V., Agol V.I. Nonreplicative homologous RNA recombination: promiscuous joining of RNA pieces?. RNA 2003, 9:1221-1231.
26. Greninger A.L., Runckel C., Chiu C.Y., Haggerty T., Parsonnet J., Ganem D., DeRisi J.L. The complete genome of klassevirus-a novel picornavirus in pediatric stool. Virol. J. 2009, 6:82.
27. Hashem Y., des Georges A., Dhote V., Langlois R., Liao H.Y., Grassucci R.A., Pestova T.V., Hellen C.U., Frank J. Hepatitis-C-virus-like internal ribosome entry sites displace eIF3 to gain access to the 40S subunit. Nature 2013, 503:539-543.
28. Hellen C.U. IRES-induced conformational changes in the ribosome and the mechanism of translation initiation by internal ribosomal entry. Biochim. Biophys. Acta 2009, 1789:558-570.
29. Hellen C.U., de Breyne S. A distinct group of hepacivirus/pestivirus-like internal ribosomal entry sites in members of diverse picornavirus genera: evidence for modular exchange of functional noncoding RNA elements by recombination. J. Virol. 2007, 81:5850-5863.
30. Holmblat B., Jégouic S., Muslin C., Blondel B., Joffret M.L., Depeyroux F. Nonhomologous recombination between defective poliovirus and coxsackievirus genomes suggests a new model of genetic plasticity for picornaviruses. mBio 2014, 5:e01119-14.
31. Honda M., Brown E.A., Lemon S.M. Stability of a stem-loop involving the initiator AUG controls the efficiency of internal initiation of translation on hepatitis C virus RNA. RNA 1996, 2:955-968.
32. Honkavuori K.S., Shivaprasad H.L., Briese T., Street C., Hirschberg D.L., Hutchison S.K., Lipkin W.I. Novel picornavirus in turkey poults with hepatitis, California, USA. Emerg. Infect. Dis. 2011, 17:480-487.
33. Hughes P.J., Stanway G. The 2A proteins of three diverse picornaviruses are related to each other and to the H-rev107 family of proteins involved in the control of cell proliferation. J. Gen. Virol. 2000, 81:201-207.
34. Jackson R.J., Kaminski A. Internal initiation of translation in eukaryotes: the picornavirus paradigm and beyond. RNA 1995, 1:985-1000.
35. Janssen S., Giegerich R. The RNA shapes studio. Bioinformatics 2015, 31:423-425.
36. Johansson S., Niklasson B., Maizel J., Gorbalenya A.E., Lindberg A.M. Molecular analysis of three Ljungan virus isolates reveals a new, close-to-root lineage of the Picornaviridae with a cluster of two unrelated 2A proteins. J. Virol. 2002, 76:8920-8930.
37. Kapoor A., Victoria J., Simmonds P., Wang C., Shafer R.W., Nims R., Nielsen O., Delwart E. A highly divergent picornavirus in a marine mammal. J. Virol. 2008, 82:311-320.
38. Kieft J.S., Zhou K., Jubin R., Doudna J.A. Mechanism of ribosome recruitment by hepatitis C IRES RNA. RNA 2001, 7:194-206.
39. Kofstad T., Jonassen C.M. Screening of feral and wood pigeons for viruses harbouring a conserved mobile viral element: characterization of novel astroviruses and picornaviruses. PLoS One 2011, 6:e25964.
40. Kolupaeva V.G., Pestova T.V., Hellen C.U. Ribosomal binding to the internal ribosomal entry site of classical swine fever virus. RNA 2000, 6:1791-1807.
41. Kolupaeva V.G., Pestova T.V., Hellen C.U. An enzymatic footprinting analysis of the interaction of 40S ribosomal subunits with the internal ribosomal entry site of hepatitis C virus. J. Virol. 2000, 74:6242-6250.
42. Lange J., Groth M., Fichtner D., Granzow H., Keller B., Walther M., Platzer M., Sauerbrei A., Zell R. Virus isolate from carp: genetic characterization reveals a novel picornavirus with two aphthovirus 2A-like sequences. J. Gen. Virol. 2014, 95:80-90.
43. Lau S.K., Woo P.C., Lai K.K., Huang Y., Yip C.C., Shek C.T., Lee P., Lam C.S., Chan K.H., Yuen K.Y. Complete genome analysis of three novel picornaviruses from diverse bat species. J. Virol. 2011, 85:8819-8828.
44. Lau S.K., Woo P.C., Yip C.C., Choi G.K., Wu Y., Bai R., Fan R.Y., Lai K.K., Chan K.H., Yuen K.Y. Identification of a novel feline picornavirus from the domestic cat. J. Virol. 2012, 86:395-405.
45. Leontis N.B., Stombaugh J., Westhof E. The non-Watson-Crick base pairs and their associated isostericity matrices. Nucleic Acids Res. 2002, 30:3497-3531.
46. Liao Q., Zheng L., Yuan Y., Shi J., Zhang D. Genomic characterization of a novel picornavirus in Pekin ducks. Vet. Microbiol. 2014, 172:78-91.
47. Locker N., Easton L.E., Lukavsky P.J. HCV and CSFV IRES domain II mediate eIF2 release during 80S ribosome assembly. EMBO J. 2007, 26:795-805.
48. Lomakin I.B., Hellen C.U., Pestova T.V. Physical association of eukaryotic initiation factor 4G (eIF4G) with eIF4A strongly enhances binding of eIF4G to the internal ribosomal entry site of encephalomyocarditis virus and is required for internal initiation of translation. Mol. Cell. Biol. 2000, 20:6019-6029.
49. Lowry K., Woodman A., Cook J., Evans D.J. Recombination in enteroviruses is a biphasic replicative process involving the generation of greater-than genome length 'imprecise' intermediates. PLoS Pathog. 2014, 10:e1004191.
50. Lu H.H., Wimmer E. Poliovirus chimeras replicating under the translational control of genetic elements of hepatitis C virus reveal unusual properties of the internal ribosomal entry site of hepatitis C virus. Proc. Natl. Acad. Sci. USA 1996, 93:1412-1417.
51. Lukavsky P.J., Kim I., Otto G.A., Puglisi J.D. Structure of HCV IRES domain II determined by NMR. Nat. Struct. Biol. 2003, 10:1033-1038.
52. Matsuda D., Mauro V.P. Base pairing between hepatitis C virus RNA and 18S rRNA is required for IRES-dependent translation initiation in vivo. Proc. Natl. Acad. Sci. USA 2014, 111:15385-15389.
53. McIntyre C.L., McWilliam Leitch E.C., Savolainen-Kopra C., Hovi T., Simmonds P. Analysis of genetic diversity and sites of recombination in human rhinovirus species C. J. Virol. 2010, 84:10297-10310.
54. Miras M., Sempere R.N., Kraft J.J., Miller W.A., Aranda M.A., Truniger V. Interfamilial recombination between viruses led to acquisition of a novel translation-enhancing RNA element that allows resistance breaking. New Phytol. 2014, 202:233-246.
55. Moser C., Bosshart A., Tratschin J.D., Hofmann M.A. A recombinant classical swine fever virus with a marker insertion in the internal ribosome entry site. Virus Genes 2001, 23:63-68.
56. Nateri A.S., Hughes P.J., Stanway G. In vivo and in vitro identification of structural and sequence elements of the human parechovirus 5' untranslated region required for internal initiation. J. Virol. 2000, 74:6269-6277.
57. Ng T.F., Mesquita J.R., Nascimento M.S., Kondov N.O., Wong W., Reuter G., Knowles N.J., Vega E., Esona M.D., Deng X., Vinjé J., Delwart E. Feline fecal virome reveals novel and prevalent enteric viruses. Vet. Microbiol. 2014, 171:102-111.
58. Pan M., Yang X., Zhou L., Ge X., Guo X., Liu J., Zhang D., Yang H. Duck Hepatitis A virus possesses a distinct type IV internal ribosome entry site element of picornavirus. J. Virol. 2012, 86:1129-1144.
59. Pankovics P., Boros A., Reuter G. Novel picornavirus in domesticated common quail (Coturnix coturnix) in Hungary. Arch. Virol. 2012, 157:525-530.
60. Pestova T.V., de Breyne S., Pisarev A.V., Abaeva I.S., Hellen C.U. eIF2-dependent and eIF2-independent modes of initiation on the CSFV IRES: a common role of domain II. EMBO J. 2008, 27:1060-1072.
61. Pestova T.V., Hellen C.U. Internal initiation of translation of bovine viral diarrhea virus RNA. Virology 1999, 258:249-256.
62. Pestova T.V., Hellen C.U., Shatsky I.N. Canonical eukaryotic initiation factors determine initiation of translation by internal ribosomal entry. Mol. Cell. Biol. 1996, 16:6859-6869.
63. Pestova T.V., Shatsky I.N., Fletcher S.P., Jackson R.J., Hellen C.U. A prokaryotic-like mode of cytoplasmic eukaryotic ribosome binding to the initiation codon during internal translation initiation of hepatitis C and classical swine fever virus RNAs. Genes Dev. 1998, 12:67-83.
64. Phan T.G., Vo N.P., Boros Á., Pankovics P., Reuter G., Li O.T., Wang C., Deng X., Poon L.L., Delwart E. The viruses of wild pigeon droppings. PLoS One 2013, 8:e72787.
65. Phan T.G., Vo N.P., Simmonds P., Samayoa E., Naccache S., Chiu C.Y., Delwart E. Rosavirus: the prototype of a proposed new genus of the Picornaviridae family. Virus Genes 2013, 47:556-558.
66. Phelps N.B., Mor S.K., Armien A.G., Batts W., Goodwin A.E., Hopper L., McCann R., Ng T.F., Puzach C., Waltzek T.B., Delwart E., Winton J., Goyal S.M. Isolation and molecular characterization of a novel picornavirus from baitfish in the USA. PLoS One 2014, 9:e87593.
67. Pisarev A.V., Chard L.S., Kaku Y., Johns H.L., Shatsky I.N., Belsham G.J. Functional and structural similarities between the internal ribosome entry sites of hepatitis C virus and porcine teschovirus, a picornavirus. J. Virol. 2004, 78:4487-4497.
68. Reeder J., Steffen P., Giegerich R. pknotsRG: RNA pseudoknot folding including near-optimal structures and sliding windows. Nucleic Acids Res. 2007, 35:W320-W324.
69. Reusken C.B., Dalebout T.J., Eerligh P., Bredenbeek P.J., Spaan W.J. Analysis of hepatitis C virus/classical swine fever virus chimeric 5'NTRs: sequences within the hepatitis C virus IRES are required for viral RNA replication. J. Gen. Virol. 2003, 84:1761-1769.
70. Reuter G., Boldizsár A., Pankovics P. Complete nucleotide and amino acid sequences and genetic organization of porcine kobuvirus, a member of a new species in the genus Kobuvirus, family Picornaviridae. Arch. Virol. 2009, 154:101-108.
71. Reuter G., Boros A., Pankovics P., Egyed L. Kobuvirus in domestic sheep, Hungary. Emerg. Infect. Dis. 2010, 16:869-870.
72. Reuter G., Pankovics P., Knowles N.J., Boros Á. Two closely related novel picornaviruses in cattle and sheep in Hungary from 2008 to 2009, proposed as members of a new genus in the family Picornaviridae. J. Virol. 2012, 86:13295-13302.
73. Sato K., Hamada M., Asai K., Mituyama T. CENTROIDFOLD: a web server for RNA secondary structure prediction. Nucleic Acids Res. 2009, 37:W277-W280.
74. Sauvage V., Ar Gouilh M., Cheval J., Muth E., Pariente K., Burguiere A., Caro V., Manuguerra J.C., Eloit M. A member of a new Picornaviridae genus is shed in pig feces. J. Virol. 2012, 86:10036-10046.
75. Sasaki J., Kusuhara Y., Maeno Y., Kobayashi N., Yamashita T., Sakae K., Takeda N., Taniguchi K. Construction of an infectious cDNA clone of Aichi virus (a new member of the family Picornaviridae) and mutational analysis of a stem-loop structure at the 5' end of the genome. J. Virol. 2001, 75:8021-8030.
76. Sizova D.V., Kolupaeva V.G., Pestova T.V., Shatsky I.N., Hellen C.U. Specific interaction of eukaryotic translation initiation factor 3 with the 5' nontranslated regions of hepatitis C virus and classical swine fever virus RNAs. J. Virol. 1998, 72:4775-4782.
77. Smith D.B., Mellor J., Jarvis L.M., Davidson F., Kolberg J., Urdea M., Yap P.L., Simmonds P. Variation of the hepatitis C virus 5' non-coding region: implications for secondary structure, virus detection and typing. The International HCV Collaborative Study Group. J. Gen. Virol. 1995, 76:1749-1761.
78. Smits S.L., Raj V.S., Oduber M.D., Schapendonk C.M., Bodewes R., Provacia L., Stittelaar K.J., Osterhaus A.D., Haagmans B.L. Metagenomic analysis of the ferret fecal viral flora. PLoS One 2013, 8:E71595.
79. Sun C., Querol-Audí J., Mortimer S.A., Arias-Palomo E., Doudna J.A., Nogales E., Cate J.H. Two RNA-binding motifs in eIF3 direct HCV IRES-dependent translation. Nucleic Acids Res. 2013, 41:7512-7521.
80. Sweeney T.R., Abaeva I.S., Pestova T.V., Hellen C.U. The mechanism of translation initiation on type 1 picornavirus IRESs. EMBO J. 2014, 33:76-92.
81. Sweeney T.R., Dhote V., Yu Y., Hellen C.U. A distinct class of internal ribosomal entry site in members of the Kobuvirus and proposed Salivirus and Paraturdivirus genera of the Picornaviridae. J. Virol. 2012, 86:1468-1486.
82. Tengs T., Kristoffersen A.B., Bachvaroff T.R., Jonassen C.M. A mobile genetic element with unknown function found in distantly related viruses. Virol. J. 2013, 10:132.
83. Tseng C.H., Tsai H.J. Sequence analysis of a duck picornavirus isolate indicates that it together with porcine enterovirus type 8 and simian picornavirus type 2 should be assigned to a new picornavirus genus. Virus Res. 2007, 129:104-114.
84. Wang C., Sarnow P., Siddiqui A. A conserved helical element is essential for internal initiation of translation of hepatitis C virus RNA. J. Virol. 1994, 68:7301-7307.
85. Wang X., Liu N., Wang F., Ning K., Li Y., Zhang D. Genetic characterization of a novel duck-origin picornavirus with six 2A proteins. J. Gen. Virol. 2014, 95:1289-1296.
86. Willcocks M.M., Locker N., Gomwalk Z., Royall E., Bakhshesh M., Belsham G.J., Idamakanti N., Burroughs K.D., Reddy P.S., Hallenbeck P.L., Roberts L.O. Structural features of the Seneca Valley virus internal ribosome entry site (IRES) element: a picornavirus with a pestivirus-like IRES. J. Virol. 2011, 85:4452-4461.
87. Wu Z., Ren X., Yang L., Hu Y., Yang J., He G., Zhang J., Dong J., Sun L., Du J., Liu L., Xue Y., Wang J., Yang F., Zhang S., Jin Q. Virome analysis for identification of novel mammalian viruses in bat species from Chinese provinces. J. Virol. 2012, 86:10999-11012.
88. Yamamoto H., Unbehaun A., Loerke J., Behrmann E., Collier M., Bürger J., Mielke T., Spahn C.M. Structure of the mammalian 80S initiation complex with initiation factor 5B on HCV-IRES RNA. Nat. Struct. Mol. Biol. 2014, 21:721-727.
89. Yozwiak N.L., Skewes-Cox P., Gordon A., Saborio S., Kuan G., Balmaseda A., Ganem D., Harris E., DeRisi J.L. Human enterovirus 109: a novel interspecies recombinant enterovirus isolated from a case of acute pediatric respiratory illness in Nicaragua. J. Virol. 2010, 84:9047-9058.
90. Yu J.M., Li X.Y., Ao Y.Y., Li L.L., Liu N., Li J.S., Duan Z.J. Identification of a novel picornavirus in healthy piglets and seroepidemiological evidence of its presence in humans. PLoS One 2013, 8:e70137.
91. Yu Y., Sweeney T.R., Kafasla P., Jackson R.J., Pestova T.V., Hellen C.U. The mechanism of translation initiation on Aichivirus RNA mediated by a novel type of picornavirus IRES. EMBO J. 2011, 30:4423-4436.
92. Zhong X., Leontis N., Qian S., Itaya A., Qi Y., Boris-Lawrie K., Ding B. Tertiary structural and functional analyses of a viroid RNA motif by isostericity matrix and mutagenesis reveal its essential role in replication. J. Virol. 2006, 80:8566-8581.
93. Zoll J., Galama J.M., van Kuppeveld F.J. Identification of potential recombination breakpoints in human parechoviruses. J. Virol. 2009, 83:3379-3383.
94. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003, 31:3406-3415.