|
|
||||||||
Short Communication |
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 |
|---|
|
|
|---|
The GenBank/EMBL/DDBJ accession number for the complete genome sequence of BPV-7 is DQ217793.
| MAIN TEXT |
|---|
|
|
|---|
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., 1986
). 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., 1996
; Morgan & Campo, 2000
). 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., 2001
; Dahiya et al., 2000
; Dick & Dyson, 2002
). However, the E7 proteins of BPV-1, -2 and -5 lack this motif (Narechania et al., 2004
).
Recently, the multiple-primed rolling-circle amplification (RCA) method has been optimized for rapid amplification of circular DNA (Dean et al., 2001
) and used for PV DNA amplification (Rector et al., 2004a
, b
, 2005
). 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., 2004
). DNA was amplified by PCR using primer pairs FAP59/MY09 (Forslund et al., 1999
; Manos et al., 1989
) 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. 1a
). The length of the ELR was 205 bp. However, the genome lacked the E5 ORF, which is known to encode a small transforming protein.
|
Recently, numerous PV types representing novel, as-yet-unnamed PV genera have been published in GenBank: canine CPV2 and CPV3 (Tobler et al., 2006
), goat ChPV-1 (Van Doorslaer et al., 2006
), multimammate mouse MCPV2, harvest mouse MmPV, Egyptian fruit bat RaPV-1 and bottlenose dolphin TtPV2 (Rehtanz et al., 2006
). 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 5758 % 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 5253 % (Table 1
). The L1 ORFs of novel PV types ChPV-1 and MmPV showed similarities of 5456 % 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., 2004
). 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. 2
). These results suggest that BPV-7 represents a novel genus in the family Papillomaviridae.
|
|
It has been reported that the ELR of BPV-1 and other ungulate PVs contain an E5 ORF (de Villiers et al., 2004
). The E5 ORF of BPV-1 (Schiller et al., 1986
), the E9 ORFs of other transforming ungulate PVs (Eriksson et al., 1994
) 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., 1993
; Conrad et al., 1993
). 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., 1999
; Morgan & Campo, 2000
).
In the absence of the E5 ORF, fibroblast transformation may be mediated by cooperation between the E6 and E7 ORFs (Neary & Dimaio, 1989
). The E6 ORFs of most PVs contain two CxxC(x)29CxxC domains, separated by 3537 aa. These domains bind zinc through cysteine residues and can act as dimerization/multimerization domains of E6 proteins (Barbosa et al., 1989
; Grossman & Laimins, 1989
). The CxxC(x)29CxxC domain found in most of the E7 proteins can also act as a dimerization/multimerization domain (Barbosa et al., 1989
; Clemens et al., 1995
; McIntyre et al., 1993
). 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., 2001
; Dahiya et al., 2000
; Dick & Dyson, 2002
). 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, 2003
). 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., 2004
), 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, 2002
; Antonsson et al., 2003
; Astori et al., 1998
; Ogawa et al., 2004
). 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 |
|---|
|
|
|---|
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, 18811886.
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, 752755.[CrossRef][Medline]
Barbosa, M. S., Lowy, D. R. & Schiller, J. T. (1989). Papillomavirus polypeptides E6 and E7 are zinc-binding proteins. J Virol 63, 14041407.
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, 255264.
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, 180182.[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, 323335.[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, 61526163.[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, 529534.[CrossRef][Medline]
Clemens, K. E., Brent, R., Gyuris, J. & Munger, K. (1995). Dimerization of the human papillomavirus E7 oncoprotein in vivo. Virology 214, 289293.[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, 61706178.
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, 67996805.
de Villiers, E.-M., Fauquet, C., Broker, T. R., Bernard, H.-U. & zur Hausen, H. (2004). Classification of papillomaviruses. Virology 324, 1727.[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, 10951099.
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, 62246234.
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, 83658373.
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, 24372443.
Grossman, S. R. & Laimins, L. A. (1989). E6 protein of human papillomavirus type 18 binds zinc. Oncogene 4, 10891096.[Medline]
Helt, A. M. & Galloway, D. A. (2003). Mechanisms by which DNA tumor virus oncoproteins target the Rb family of pocket proteins. Carcinogenesis 24, 159169.
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, 11891199.
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, 255264.[CrossRef][Medline]
Kumar, S., Tamura, K. & Nei, M. (2004). MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5, 150163.
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. 209214. 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, 31423150.
Morgan, I. M. & Campo, M. S. (2000). Recent developments in bovine papillomaviruses. Papillomavirus Rep 11, 127132.
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, 12431250.
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, 259266.
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, 385394.[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, 21912197.
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, 18.[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, 49934998.
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, 1269812702.
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, 449456.[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, 35593565.
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, 16.
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, 45214532.
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, 35513557.
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, 164169.[CrossRef][Medline]
Wingender, E. (1988). Compilation of transcription regulating proteins. Nucleic Acids Res 16, 18791902.
Received 14 December 2006;
accepted 23 March 2007.
This article has been cited by other articles:
![]() |
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] |
||||
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| INT J SYST EVOL MICROBIOL | MICROBIOLOGY | J GEN VIROL |
| J MED MICROBIOL | ALL SGM JOURNALS | |