J Gen Virol Faster Access
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
 QUICK SEARCH:   [advanced]


     


J Gen Virol 88 (2007), 1934-1938; DOI 10.1099/vir.0.82794-0

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via CrossRef
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Ogawa, T.
Right arrow Articles by Shirasawa, H.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Ogawa, T.
Right arrow Articles by Shirasawa, H.
Agricola
Right arrow Articles by Ogawa, T.
Right arrow Articles by Shirasawa, H.

Short Communication

Complete genome and phylogenetic position of bovine papillomavirus type 7

Tomoko Ogawa1, Yoshimi Tomita2, Mineyuki Okada1 and Hiroshi Shirasawa2

1 Division of Virology, Chiba Prefectural Institute of Public Health, 666-2 Nitona-cho, Chuou-ku, Chiba 260-8715, Japan
2 Department of Molecular Virology, Graduate School of Medicine, Chiba University, 1-8-1 Inohana, Chuou-ku, Chiba 260-8670, Japan

Correspondence
Yoshimi Tomita
tomita{at}faculty.chiba-u.jp


   ABSTRACT
TOP
ABSTRACT
MAIN TEXT
REFERENCES
 
Six bovine papillomavirus (BPV) types and 16 putative BPV types have been reported previously. Here, the complete genome sequence of BAPV6, a novel putative BPV type isolated from cattle in Japan, was determined by using multiple-primed rolling-circle amplification. The genome consisted of 7412 bp (G+C content of 46 mol%) that encoded five early (E1, E2, E4, E6 and E7) and two late (L1 and L2) genes, but did not encode the E5 gene. The E6 protein contained a non-consensus CxxC(x)33CxxC and a consensus CxxC(x)29CxxC zinc-binding domain, and the E7 protein lacked the LxCxE motif. The nucleotide sequence of the L1 open reading frame (ORF) was related most closely (57–58 %) to the L1 ORF of member(s) of the genera Betapapillomavirus, Gammapapillomavirus and Pipapillomavirus. Phylogenetic analysis based on the complete L1 ORF suggests that BAPV6 should be classified in a novel genus in the family Papillomaviridae as BPV-7.

The GenBank/EMBL/DDBJ accession number for the complete genome sequence of BPV-7 is DQ217793.


   MAIN TEXT
TOP
ABSTRACT
MAIN TEXT
REFERENCES
 
Papillomaviruses (PVs) form a highly diverse group of viruses found in most mammals and birds, and hundreds of PV types have been detected in humans. Recently, PVs have been classified into 18 genera (Alphapapillomavirus to Sigmapapillomavirus) according to nucleotide sequence diversity in the L1 open reading frame (ORF). Different genera share <60 % nucleotide sequence identity in the L1 ORF, whereas complete full-length genomes show >23 %, but <43 % identity when comparing genera of the Papillomaviridae (de Villiers et al., 2004Down). At present, six bovine PV types (BPV-1 to -6) have been characterized (Campo et al., 1980Down, 1981Down; Campo & Coggins, 1982Down; Chen et al., 1982Down; Jarrett et al., 1984Down; Pfister et al., 1979Down) and classified into three genera, Deltapapillomavirus (BPV-1 and -2), Epsilonpapillomavirus (BPV-5) and Xipapillomavirus (BPV-3, -4 and -6). In addition, 16 novel putative BPV types have been identified by PCR-based nucleotide sequence determination of highly conserved regions in the L1 ORFs and by phylogenetic analyses (Antonsson & Hansson, 2002Down; Ogawa et al., 2004Down).

BPV-1 and -2 contain ORFs E6 and E7 in the early region of the genome, whereas ORF E5 is localized between the early and late genes (ERL). These ORFs encode proteins implicated in the transformation of host cells (Schiller et al., 1986Down). However, BPV-3, -4 and -6 lack the E6 and E5 ORFs (generally found in the ERL), but have the E8 or E5 (formerly E8) ORF in place of the E6 ORF (Jackson et al., 1996Down; Morgan & Campo, 2000Down). BPV-5 contains the E6 and E7 ORFs and a putative E5 ORF in the ERL. The E6 proteins of all BPV types contain two zinc-binding or putative zinc-binding domains that seem to be essential for the formation of multimerized complexes. The E7 proteins of most PVs, including BPV-3, -4 and -6, contain the LxCxE motif implicated in the immortalization and transformation of the host cell (Chan et al., 2001Down; Dahiya et al., 2000Down; Dick & Dyson, 2002Down). However, the E7 proteins of BPV-1, -2 and -5 lack this motif (Narechania et al., 2004Down).

Recently, the multiple-primed rolling-circle amplification (RCA) method has been optimized for rapid amplification of circular DNA (Dean et al., 2001Down) and used for PV DNA amplification (Rector et al., 2004aDown, bDown, 2005Down). In this study, the complete genome of BAPV6, a putative novel BPV type, was determined by using PCR and RCA methods. Data from sequencing and phylogenetic analysis suggest that BAPV6 is a novel BPV type that should be classified in a novel genus of the Papillomaviridae; BAPV6 was thus designated BPV-7.

BPV-7 was isolated from a cutaneous papilloma found in cattle and detected in two of the 15 (13 %) papilloma specimens and in eight of the 24 (33 %) healthy teat skin swab samples, suggesting that BPV-7 is the most prevalent PV type found in cattle in Japan. BPV-7 DNA was extracted from the biopsy sample of a teat that did not harbour any other BPV or putative BPV types (Ogawa et al., 2004Down). DNA was amplified by PCR using primer pairs FAP59/MY09 (Forslund et al., 1999Down; Manos et al., 1989Down) and by RCA using a TempliPhi 100 amplification kit (Amersham Biosciences). ORF analysis was performed using the ORF Finder (http://www.ncbi.nlm.nih.gov/gorf/gorf.html) and similarity searches were performed with the NCBI BLAST server (version 2.28) and GenBank. The complete genome of BPV-7 consisted of 7412 bp, and the genome contained E6, E7, E1, E2, E4, L1 and L2 ORFs (Fig. 1aDown). The length of the ELR was 205 bp. However, the genome lacked the E5 ORF, which is known to encode a small transforming protein.


Figure 1
View larger version (29K):
[in this window]
[in a new window]

 
Fig. 1. (a) Schematic representation of BPV-7 genome organization. Each ORF is represented as a rectangle. Numbers represent the nucleotide positions of the start and stop codons of BPV-7. Arrowheads indicate the locations of polyadenylation signals for the early and the late mRNAs. (b) DNA motifs found in the URR. Numbers represent nucleotide positions in the URR of the BPV-7 genome. The rectangle indicates the polyadenylation signal (AATAAA) for the late mRNA. Shaded boxes indicate the E2-binding motif [ACC(N)6GGT]. A single underline indicates the nuclear factor-binding site (TTGGCA). A double underline indicates the TATA box-like sequence (TATATTA).

 
Sequence analysis revealed canonical polyadenylation signals (AATAAA) located at nt 4077–4082 and 7110–7115 for the early and late mRNA, respectively (Fig. 1aUp). In the upstream regulatory region (URR), three E2-binding sites with the consensus sequence [ACC(N)6GGT], which were found in the URRs of BPVs in the genus Xipapillomavirus, were located at nt 45–56, 7129–7140 and 7215–7226. A binding site for nuclear factor 1 (TTGGCA) (Wingender, 1988Down) was also present at nt 7226–7231. A TATA box-like sequence (TATATTA) was found at nt 57–63 (Fig. 1bUp).

Recently, numerous PV types representing novel, as-yet-unnamed PV genera have been published in GenBank: canine CPV2 and CPV3 (Tobler et al., 2006Down), goat ChPV-1 (Van Doorslaer et al., 2006Down), multimammate mouse MCPV2, harvest mouse MmPV, Egyptian fruit bat RaPV-1 and bottlenose dolphin TtPV2 (Rehtanz et al., 2006Down). Pairwise DNA sequence alignments were calculated by using the GAP program of Alignment App (http://genome.cs.mtu.edu/align/align.html). The results showed that closely related PV types, i.e. those that shared 57–58 % similarity with the BPV-7 L1 ORF, were all of the human PV (HPV) types in the genus Betapapillomavirus, HPV-4 in the genus Gammapapillomavirus and hamster oral papillomavirus (HaOPV) in the genus Pipapillomavirus; other members of the genus Gammapapillomavirus had similarities of 52–53 % (Table 1Down). The L1 ORFs of novel PV types ChPV-1 and MmPV showed similarities of 54–56 % with the BPV-7 L1 ORF. Similarities between the full-length sequence of BPV-7 and those of HPV-15, HPV-4, HaOPV and BPV-3 were 40, 41, 41 and 42 %, respectively. A phylogenetic tree of L1 ORF sequences was constructed by using MEGA version 3.1 based on the neighbour-joining method (http:/www.megasoftware.net/mega.html) (Kumar et al., 2004Down). The BPV-7 L1 ORF was related distantly to other L1 ORFs in the phylogenetic tree, which was constructed with 54 PV L1 ORFs, including the L1 ORFs of seven novel PV types (Fig. 2Down). These results suggest that BPV-7 represents a novel genus in the family Papillomaviridae.


View this table:
[in this window]
[in a new window]

 
Table 1. DNA sequence similarity (%) of the L1 ORF and full-length genome of BPV-7 to those of some PVs that are related closely to BPV-7

 

Figure 2
View larger version (42K):
[in this window]
[in a new window]

 
Fig. 2. Phylogenetic tree constructed by using the neighbour-joining method with the L1 ORFs of HPV types and animal PV types. BAPV6 was designated BPV-7 in this tree. GenBank accession numbers are shown in parentheses. Abbreviations: RhPV-1, rhesus monkey PV-1; TmPV-1, Trichechus manatus latirostris PV-1; PsPV1, Phocoena spinipinnis PV-1; PePV, Psittacus erithacus timneh PV; FcPV, Fringilla coelebs PV; MnPV, Mastomys natalensis PV; EdPV-1, Erithizon dorsatum PV-1; FdPV, feline PV; COPV, canine oral PV; ROPV, rabbit oral PV; CRPV, cottontail rabbit PV; OvPV-1, ovine PV-1; EcPV-1, Equus caballus PV-1.

 
The BPV-7 E6 ORF encoded a protein consisting of 142 aa, which contained a non-consensus CxxC(x)33CxxC zinc-binding domain and a consensus CxxC(x)29CxxC zinc-binding domain separated by 38 aa. The E7 ORF encoded a 104 aa protein that lacked the LxCxE motif, but contained a consensus zinc-binding domain, CxxC(x)29CxxC. Lack of the LxCxE motif was also found in E7 ORFs of HaOPV, HPV-4, -50 and -60, and all other members of the genus Gammapapillomavirus. The other non-consensus zinc-binding motifs or domains, CxxxC(x)29CxxC, CxC(x)29CxxC and CxxC(x)30CxxC, were also found in some of these PVs.

It has been reported that the ELR of BPV-1 and other ungulate PVs contain an E5 ORF (de Villiers et al., 2004Down). The E5 ORF of BPV-1 (Schiller et al., 1986Down), the E9 ORFs of other transforming ungulate PVs (Eriksson et al., 1994Down) in the genus Deltapapillomavirus and the E5 ORFs of some HPVs, including HPV-6 and -16 in the genus Alphapapillomavirus, encode a transforming protein containing transmembrane domain(s) (Straight et al., 1993Down; Conrad et al., 1993Down). BPV-3, -4 and -6 lack the E6 ORF and contain an E8 or E5 ORF (formerly E8 ORF) in the position of the E6 ORF. The BPV-4 E5 ORF consists of 42 aa, induces anchorage-independent growth of infected cells and suppresses contact inhibition (O'Brien et al., 1999Down; Morgan & Campo, 2000Down).

In the absence of the E5 ORF, fibroblast transformation may be mediated by cooperation between the E6 and E7 ORFs (Neary & Dimaio, 1989Down). The E6 ORFs of most PVs contain two CxxC(x)29CxxC domains, separated by 35–37 aa. These domains bind zinc through cysteine residues and can act as dimerization/multimerization domains of E6 proteins (Barbosa et al., 1989Down; Grossman & Laimins, 1989Down). The CxxC(x)29CxxC domain found in most of the E7 proteins can also act as a dimerization/multimerization domain (Barbosa et al., 1989Down; Clemens et al., 1995Down; McIntyre et al., 1993Down). BPV-7 lacks the E5 ORF. Thus, it may be assumed that the non-consensus-structured domain CxxC(x)33CxxC of the BPV-7 E6 protein, as well as CxC(x)29CxxC in the BPV-5 E7 protein and CxxxC(x)29CxxC in the HPV-45 E7 protein, could function as zinc-binding domains.

The LxCxE motif found in the E7 protein is a canonical pRb-binding motif and has been implicated in the immortalization and transformation of the host cell (Chan et al., 2001Down; Dahiya et al., 2000Down; Dick & Dyson, 2002Down). Most HPV E7 proteins use a homologous LxCxE motif to bind to the pocket region of pRb, p107 and p130 and prevent interactions with the transcription factor E2F-1 (Helt & Galloway, 2003Down). However, the E7 proteins of artiodactyla PVs, including BPV-1, -2, -5, European elk PV (EEPV), deer PV (DPV) and reindeer PV (RPV) (Narechania et al., 2004Down), and BPV-7 lack this motif.

In addition to the PVs isolated from papilloma specimens, large numbers of putative HPV and animal PV types have been detected by PCR from the healthy skin of humans and other animals (Antonsson & Hansson, 2002Down; Antonsson et al., 2003Down; Astori et al., 1998Down; Ogawa et al., 2004Down). This shows a latent or subclinical infection of skin with PV and their commensal nature. BPV-1, -3, -5 and -6, as well as BPV-7, have been detected in swab samples of healthy teat skin without apparent papilloma, indicating latent or subclinical infections, in addition to papilloma-inducing infections, of these BPV types.

The BPV-7 L1 ORF shows high nucleotide sequence similarity to the L1 ORFs of HPVs of the genera Betapapillomavirus and Gammapapillomavirus and HaOPV of the genus Pipapillomavirus, but appears to have a distant relationship to other PVs in the phylogenetic tree, suggesting that BPV-7 should be classified in a novel genus of the family Papillomaviridae.


   REFERENCES
TOP
ABSTRACT
MAIN TEXT
REFERENCES
 
Antonsson, A. & Hansson, B. G. (2002). Healthy skin of many animal species harbors papillomaviruses which are closely related to their human counterparts. J Virol 76, 12537–12542.[Abstract/Free Full Text]

Antonsson, A., Erfurt, C., Hazard, K., Holmgren, V., Simon, M., Kataoka, A., Hossain, S., Hakangard, C. & Hansson, B. G. (2003). Prevalence and type spectrum of human papillomavirus in healthy skin samples collected in three continents. J Gen Virol 84, 1881–1886.[Abstract/Free Full Text]

Astori, G., Lavergne, D., Benton, C., Hockmayr, B., Egawa, K., Garbe, C. & De Villiers, E.-M. (1998). Human papillomavirus are commonly found in normal skin of immunocompetent hosts. J Invest Dermatol 110, 752–755.[CrossRef][Medline]

Barbosa, M. S., Lowy, D. R. & Schiller, J. T. (1989). Papillomavirus polypeptides E6 and E7 are zinc-binding proteins. J Virol 63, 1404–1407.[Abstract/Free Full Text]

Campo, M. S. & Coggins, L. W. (1982). Molecular cloning of bovine papillomavirus genomes and comparison of their sequence homologies by heteroduplex mapping. J Gen Virol 63, 255–264.[Abstract/Free Full Text]

Campo, M. S., Moar, M. H., Jarrett, W. F. H. & Laird, H. M. (1980). A new papillomavirus associated with alimentary cancer in cattle. Nature 286, 180–182.[CrossRef][Medline]

Campo, M. S., Moar, M. H., Laird, H. M. & Jarrett, W. F. H. (1981). Molecular heterogeneity and lesion site specificity of cutaneous bovine papillomaviruses. Virology 113, 323–335.[CrossRef][Medline]

Chan, H. M., Smith, L. & La Thangue, N. B. (2001). Role of LXCXE motif-dependent interactions in the activity of the retinoblastoma protein. Oncogene 20, 6152–6163.[CrossRef][Medline]

Chen, E. Y., Howley, P. M., Levinson, A. D. & Seeburg, P. H. (1982). The primary structure and genetic organization of the bovine papillomavirus type 1 genome. Nature 299, 529–534.[CrossRef][Medline]

Clemens, K. E., Brent, R., Gyuris, J. & Munger, K. (1995). Dimerization of the human papillomavirus E7 oncoprotein in vivo. Virology 214, 289–293.[CrossRef][Medline]

Conrad, M., Bubb, V. J. & Schlegel, R. (1993). The human papillomavirus type 6 and 16 E5 proteins are membrane-associated proteins which associate with the 16-kilodalton pore-forming protein. J Virol 67, 6170–6178.[Abstract/Free Full Text]

Dahiya, A., Gavin, M. R., Luo, R. X. & Dean, D. C. (2000). Role of the LXCXE binding site in Rb function. Mol Cell Biol 20, 6799–6805.[Abstract/Free Full Text]

de Villiers, E.-M., Fauquet, C., Broker, T. R., Bernard, H.-U. & zur Hausen, H. (2004). Classification of papillomaviruses. Virology 324, 17–27.[CrossRef][Medline]

Dean, F. B., Nelson, J. R., Gesler, T. L. & Lasken, R. S. (2001). Rapid amplification of plasmid and phage DNA using phi29 DNA polymerase and multiply-primed rolling circle amplification. Genome Res 11, 1095–1099.[Abstract/Free Full Text]

Dick, F. A. & Dyson, N. J. (2002). Three regions of the pRB pocket domain affect its inactivation by human papillomavirus E7 proteins. J Virol 76, 6224–6234.[Abstract/Free Full Text]

Eriksson, A., Stewart, A.-C., Moreno-Lopéz, J. & Pettersson, U. (1994). The genomes of the animal papillomaviruses European elk papillomavirus, deer papillomavirus, and reindeer papillomavirus contain a novel transforming gene (E9) near the early polyadenylation site. J Virol 68, 8365–8373.[Abstract/Free Full Text]

Forslund, O., Antonsson, A., Nordin, P., Stenquist, B. & Hansson, B. G. (1999). A broad range of human papillomavirus types detected with a general PCR method suitable for analysis of cutaneous tumors and normal skin. J Gen Virol 80, 2437–2443.[Abstract/Free Full Text]

Grossman, S. R. & Laimins, L. A. (1989). E6 protein of human papillomavirus type 18 binds zinc. Oncogene 4, 1089–1096.[Medline]

Helt, A. M. & Galloway, D. A. (2003). Mechanisms by which DNA tumor virus oncoproteins target the Rb family of pocket proteins. Carcinogenesis 24, 159–169.[Abstract/Free Full Text]

Jackson, M. E., O'Brien, V., Morgan, I. M., Grindlay, G. J. & Campo, M. S. (1996). Bovine papillomavirus type 4: neoplastic cell transformation and control of infection by vaccination. Int J Oncol 9, 1189–1199.

Jarrett, W. F. H., Campo, M. S., O'Neil, B. W., Laird, H. M. & Coggins, L. W. (1984). A novel bovine papillomavirus (BPV-6) causing true epithelial papillomas of the mammary gland skin: a member of a proposed new BPV subgroup. Virology 136, 255–264.[CrossRef][Medline]

Kumar, S., Tamura, K. & Nei, M. (2004). MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5, 150–163.[Abstract/Free Full Text]

Manos, M. M., Ting, Y., Wright, D. K., Lewis, A. J., Broker, T. R. & Wolinsky, S. M. (1989). The use of polymerase chain reaction amplification for the detection of genital human papillomaviruses. In Molecular Diagnostics of Human Cancer: Cancer Cells, vol. 7, pp. 209–214. Edited by M. Furth & M. Greaves. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.

McIntyre, M. C., Frattini, M. G., Grossman, S. R. & Laimins, L. A. (1993). Human papillomavirus type 18 E7 protein requires intact Cys-X-X-Cys motifs for zinc binding, dimerization, and transformation but not for Rb binding. J Virol 67, 3142–3150.[Abstract/Free Full Text]

Morgan, I. M. & Campo, M. S. (2000). Recent developments in bovine papillomaviruses. Papillomavirus Rep 11, 127–132.

Narechania, A., Terai, M., Chen, Z., DeSalle, R. & Burk, R. D. (2004). Lack of the canonical pRB-binding domain in the E7 ORF of artiodactyl papillomaviruses is associated with the development of fibropapillomas. J Gen Virol 85, 1243–1250.[Abstract/Free Full Text]

Neary, K. & Dimaio, D. (1989). Open reading frames E6 and E7 of bovine papillomavirus type 1 are both required for full transformation of mouse C127 cells. J Virol 63, 259–266.[Abstract/Free Full Text]

O'Brien, V., Ashrafi, G. H., Grindlay, G. J., Anderson, R. & Campo, M. S. (1999). Mutational analysis of the transforming functions of the E8 protein of bovine papillomavirus type 4. Virology 255, 385–394.[CrossRef][Medline]

Ogawa, T., Tomita, Y., Okada, M., Shinozaki, K., Kubonoya, H., Kaiho, I. & Shirasawa, H. (2004). Broad-spectrum detection of papillomaviruses in bovine teat papillomas and healthy teat skin. J Gen Virol 85, 2191–2197.[Abstract/Free Full Text]

Pfister, H., Linz, U., Gissmann, L., Huchthausen, B., Hoffman, D. & zur Hausen, H. (1979). Partial characterization of a new type of bovine papillomavirus. Virology 96, 1–8.[CrossRef][Medline]

Rector, A., Tachezy, R. & Van Ranst, M. (2004a). A sequence-independent strategy for detection and cloning of circular DNA virus genomes by using multiply primed rolling-circle amplification. J Virol 78, 4993–4998.[Abstract/Free Full Text]

Rector, A., Bossart, G. D., Ghim, S.-J., Sundberg, J. P., Jenson, A. & Van Ranst, M. (2004b). Characterization of a novel close-to-root papillomavirus from Florida manatee by using multiply primed rolling-circle amplification: Trichechus manatus latirostris papillomavirus type 1. J Virol 78, 12698–12702.[Abstract/Free Full Text]

Rector, A., Tachezy, R., Van Doorslaer, K., MacNamara, T., Burk, R. D., Sundberge, J. P. & Van Ranst, M. V. (2005). Isolation and cloning of a papillomavirus from a North American porcupine by using multiply primed rolling-circle amplification: the Erethizon dorsatum papillomavirus type 1. Virology 331, 449–456.[CrossRef][Medline]

Rehtanz, M., Ghim, S. J., Rector, A., Van Ranst, M., Fair, P. A., Bossart, G. D. & Jenson, A. B. (2006). Isolation and characterization of the first American bottlenose dolphin papillomavirus: Tursiops truncatus papillomavirus type 2. J Gen Virol 87, 3559–3565.[Abstract/Free Full Text]

Schiller, J. T., Vass, W. C., Vousden, K. H. & Lowy, D. R. (1986). E5 open reading frame of bovine papillomavirus type 1 encodes a transforming gene. J Virol 57, 1–6.[Abstract/Free Full Text]

Straight, S. W., Hinkle, P. M., Jewers, R. J. & McCance, D. J. (1993). The E5 oncoprotein of human papillomavirus type 16 transforms fibroblasts and effects the down regulation of the epidermal growth factor receptor in keratinocytes. J Virol 67, 4521–4532.[Abstract/Free Full Text]

Tobler, K., Favrot, C., Nespeca, G. & Ackermann, M. (2006). Detection of the prototype of a potential novel genus in the family Papillomaviridae in association with canine epidermodysplasia verruciformis. J Gen Virol 87, 3551–3557.[Abstract/Free Full Text]

Van Doorslaer, K., Rector, A., Vos, P. & Van Ranst, M. (2006). Genetic characterization of the Capra hircus papillomavirus: a novel close-to-root artiodactyls papillomavirus. Virus Res 118, 164–169.[CrossRef][Medline]

Wingender, E. (1988). Compilation of transcription regulating proteins. Nucleic Acids Res 16, 1879–1902.[Free Full Text]

Received 14 December 2006; accepted 23 March 2007.


This article has been cited by other articles:


Home page
J. Gen. Virol.Home page
S. Hatama, K. Nobumoto, and T. Kanno
Genomic and phylogenetic analysis of two novel bovine papillomaviruses, BPV-9 and BPV-10
J. Gen. Virol., January 1, 2008; 89(1): 158 - 163.
[Abstract] [Full Text] [PDF]


This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via CrossRef
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Ogawa, T.
Right arrow Articles by Shirasawa, H.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Ogawa, T.
Right arrow Articles by Shirasawa, H.
Agricola
Right arrow Articles by Ogawa, T.
Right arrow Articles by Shirasawa, H.


HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
INT J SYST EVOL MICROBIOL MICROBIOLOGY J GEN VIROL
J MED MICROBIOL ALL SGM JOURNALS