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. 2007 Apr 10;360(2):447-53.
doi: 10.1016/j.virol.2006.10.022. Epub 2006 Nov 22.

Human papillomavirus (HPV) types 101 and 103 isolated from cervicovaginal cells lack an E6 open reading frame (ORF) and are related to gamma-papillomaviruses

Zigui Chen  1 , Mark Schiffman, Rolando Herrero, Rob Desalle, Robert D Burk
Affiliations

Human papillomavirus (HPV) types 101 and 103 isolated from cervicovaginal cells lack an E6 open reading frame (ORF) and are related to gamma-papillomaviruses

Zigui Chen et al. Virology. .

Abstract

Complete genomes of HPV101 and HPV103 were PCR amplified and cloned from cervicovaginal cells of a 34-year-old female with cervical intraepithelial neoplasia grade 3 (CIN 3) and a 30-year-old female with a normal Pap test, respectively. HPV101 and HPV103 contain 4 early genes (E7, E1, E2, and E4) and 2 late genes (L2 and L1), but both lack the canonical E6 ORF. Pairwise alignment similarity of the L1 ORF nucleotide sequences of HPV101 and HPV103 indicated that they are at least 30% dissimilar to each other and all known PVs. However, similarities of the other ORFs (E7, E1, E2, and L2) indicated that HPV101 and HPV103 are most related to each other. Phylogenetic analyses revealed that these two types form a monophyletic clade, clustering together with the gamma- and pi-PV groups. These data demonstrated that HPV genomes closely related to papillomaviruses identified from cutaneous epithelia can be isolated from the genital mucosal region. Moreover, this is the first report of HPVs lacking an E6 ORF and phylogenetic evidence suggests this occurred subsequent to their emergence from the gamma-/pi-PVs.

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Figures

Fig. 1
Fig. 1
Bayesian tree of 125 papillomavirus types inferred from the concatenated amino acids and nucleotide sequences of six ORFs (E6, E7, E1, E2, L2 and L1). The ORF sequence was left blank if unavailable. Classification at the “genus” level is according to de Villiers (10). The number at the ends of each of the branches identifies an HPV type. All other abbreviations refer to animal PVs but the RTRX7. Two novel HPV types in this work (HPV101 and HPV103) form a monophyletic clade at the root of the gamma-PV genus. PV genomes representing main clades of papillomaviruses that were used in Table 1 are were highlighted in gray. All complete genome sequences of PVs were obtained from NCBI / GenBank database (with their accession numbers): HPV01a (NC_001356), HPV02a (NC_001352), HPV03 (NC_001588), HPV04 (NC_001457), HPV05 (NC_001531), HPV06 (NC_000904), HPV07 (NC_001595), HPV08 (NC_001532), HPV09 (NC_001596), HPV10 (NC_001576), HPV11 (NC_001525), HPV12 (NC_001577), HPV13 (NC_001349), HPV14D (NC_001578), HPV15 (NC_001579), HPV16R (AY686581), HPV17 (NC_001580), HPV18R (AY262282), HPV19 (NC_001581), HPV20 (NC_001679), HPV21 (NC_001680), HPV22 (NC_001681), HPV23 (NC_001682), HPV24 (NC_001683), HPV25 (NC_001582), HPV26 (NC_001583), HPV27 (NC_001584), HPV28 (NC_001684), HPV29 (NC_001685), HPV30 (NC_001585), HPV31 (NC_001527), HPV32 (NC_001586), HPV33 (NC_001528), HPV34 (NC_001587), HPV35 (NC_001529), HPV36 (NC_001686), HPV37 (NC_001687), HPV38 (NC_001688), HPV39 (NC_001535), HPV40 (NC_001589), HPV41 (NC_001354), HPV42 (NC_001534), HPV43 (NC_005349), HPV44 (NC_001689), HPV45 (NC_001590), HPV47 (NC_001530), HPV48 (NC_001690), HPV49 (NC_001591), HPV50 (NC_001691), HPV51 (NC_001533), HPV52 (NC_001592), HPV53 (NC_001593), HPV54 (NC_001676), HPV55 (NC_001692), HPV56 (NC_001594), HPV57 (NC_001353), HPV58 (NC_001443), HPV59 (NC_001635), HPV60 (NC_001693), HPV61 (NC_001694), HPV62 (NC_006357), HPV63 (NC_001458), HPV65 (NC_001459), HPV66 (NC_001695), HPV67 (NC_004710), HPV68 (DQ080079), HPV69 (NC_002171), HPV70 (NC_001711), HPV71 (NC_002644), HPV72 (NC_006164), HPV73 (NC_006165), HPV74 (NC_004501), HPV75 (NC_006166), HPV76 (NC_006167), HPV77 (NC_006168), HPV78 (unpublished), HPV80 (NC_006169), HPV81 (NC_005351), HPV82 (NC_002172), HPV83 (NC_000856), HPV84 (NC_002676), HPV85 (NC_004762), HPV86 (NC_003115), HPV87 (NC_002627), HPV89 (NC_004103), HPV90 (NC_004104), HPV91 (NC_004085), HPV92 (NC_004500), HPV93 (NC_005133), HPV94 (NC_005352), HPV95 (AJ620210), HPV96 (NC_005134), HPV101 (DQ080081 ), HPV103 (DQ080078), bovine BPV1 (X02346), BPV2 (NC_001521), BPV3 (NC_004197), BPV4 (NC_004711), BPV5 (NC_004195), BPV6 (NC_005350), canine oral CoPV (NC_001619), commom chimpanzee ChPV (NC_001838), cottontail rabbit CRPV (NC_001541), deer DPV (NC_001523), Erethizon dorsatum EdPV-1(AY684126), Equinus caballus EquiPV (NC_004194), European elk EEPV (NC_001524), feline FdPV (NC_004765), Fringilla coelebs FPV (NC_004068), Hamster oral HaOPV (E15111), multimammate rat MnPV (NC_001605), ovine OvPV1 (NC_001789), ovine OvPV2 (NC_001790), Procyon lotor PIPV-1 (AY763115), Phocoena spinipinnis PsPV (NC_003348), Psittacus erithacus PePV (NC_003973), pygmy chimpanzee PcPV (NC_006163), Trichechus manatus latirostris TmPV1 (NC_006563), rabbit oral ROPV (NC_002232), reindeer RPV (NC_004196), and rhesus monkey RhPV (NC_001678).
Fig. 2
Fig. 2
Bayesian trees inferred from the concatenated amino acids and nucleotide sequences of early (E6, E7, E1 and E2) and late (L2 and L1) ORFs. The ORF sequence was left blank if unavailable. Numbers on or near branches indicate support indices from multiple algorithms in the following order: Bayesian credibility value using MrBayes; maximum parsimony (MP) bootstrap percentage and neighbor joining (NJ) bootstrap percentage using PAUP. An asterisk (*) indicates complete agreement between methods. “n” reflects disagreement between a method and the reference Bayesian tree at a given node. HPV101 and HPV103 genomes are highlighted in gray.
Fig. 3
Fig. 3
Molecular tree topology of representative papillomaviruses combined with dating of the phylogenetic nodes. Branch lengths are proportional to divergence times. Numbers above the nodes are the mean estimated divergence time (in million years, Mya). The bars in grey represent the 95% highest posterior density (HPD) interval for the divergence times. A Bayesian Markov chain Monte Carlo (MCMC) method was used to calculate divergence times in the BEAST program by selecting the uncorrelated lognormal distribution (UCLD) model. The node of the most recent common ancestor (MRCA) between the clade of HPV101/103 and the Gamma HPVs is denoted with a black circle.
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