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1

White, Elizabeth A. "Manipulation of Epithelial Differentiation by HPV Oncoproteins." Viruses 11, no. 4 (April 22, 2019): 369. http://dx.doi.org/10.3390/v11040369.

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Papillomaviruses replicate and cause disease in stratified squamous epithelia. Epithelial differentiation is essential for the progression of papillomavirus replication, but differentiation is also impaired by papillomavirus-encoded proteins. The papillomavirus E6 and E7 oncoproteins partially inhibit and/or delay epithelial differentiation and some of the mechanisms by which they do so are beginning to be defined. This review will outline the key features of the relationship between HPV infection and differentiation and will summarize the data indicating that papillomaviruses alter epithelial differentiation. It will describe what is known so far and will highlight open questions about the differentiation-inhibitory mechanisms employed by the papillomaviruses.
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2

Lange, Christian E., Mathias Ackermann, Claude Favrot, and Kurt Tobler. "Entire Genomic Sequence of Novel Canine Papillomavirus Type 13." Journal of Virology 86, no. 18 (August 23, 2012): 10226–27. http://dx.doi.org/10.1128/jvi.01553-12.

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Papillomaviruses are associated with benign and malignant neoplasias of the skin and mucous membranes. The sequence of a novel canine papillomavirus was determined from DNA detected in the oral cavity of a dog. The sequence of the novel virus canine papillomavirus type 13 (CPV13) shares the highest levels of similarity with the Tau papillomaviruses CPV2 and CPV7.
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3

Antonsson, Annika, and Nigel A. J. McMillan. "Papillomavirus in healthy skin of Australian animals." Journal of General Virology 87, no. 11 (November 1, 2006): 3195–200. http://dx.doi.org/10.1099/vir.0.82195-0.

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Papillomaviruses are a group of ubiquitous viruses that are often found in normal skin of humans, as well as a range of different vertebrates. In this study, swab samples collected from the healthy skin of 225 Australian animals from 54 species were analysed for the presence of papillomavirus DNA with the general skin papillomavirus primer pair FAP59/FAP64. A total of five putative and potential new animal papillomavirus types were identified from three different animal species. The papillomaviruses were detected in one monotreme and two marsupial species: three from koalas, and one each from an Eastern grey kangaroo and an echidna. The papillomavirus prevalence in the three species was 14 % (10/72) in koalas, 20 % (1/5) in echidnas and 4 % (1/23) in Eastern grey kangaroos. Phylogenetic analysis was performed on the putative koala papillomavirus type that could be cloned and it appears in the phylogenetic tree as a novel putative papillomavirus genus. The data extend the range of species infected by papillomaviruses to the most primitive mammals: the monotremes and the marsupials.
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4

McPhillips, M. G., J. G. Oliveira, J. E. Spindler, R. Mitra, and A. A. McBride. "Brd4 Is Required for E2-Mediated Transcriptional Activation but Not Genome Partitioning of All Papillomaviruses." Journal of Virology 80, no. 19 (October 1, 2006): 9530–43. http://dx.doi.org/10.1128/jvi.01105-06.

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ABSTRACT Bromodomain protein 4 (Brd4) has been identified as the cellular binding target through which the E2 protein of bovine papillomavirus type 1 links the viral genome to mitotic chromosomes. This tethering ensures retention and efficient partitioning of genomes to daughter cells following cell division. E2 is also a regulator of viral gene expression and a replication factor, in association with the viral E1 protein. In this study, we show that E2 proteins from a wide range of papillomaviruses interact with Brd4, albeit with variations in efficiency. Moreover, disruption of the E2-Brd4 interaction abrogates the transactivation function of E2, indicating that Brd4 is required for E2-mediated transactivation of all papillomaviruses. However, the interaction of E2 and Brd4 is not required for genome partitioning of all papillomaviruses since a number of papillomavirus E2 proteins associate with mitotic chromosomes independently of Brd4 binding. Furthermore, mutations in E2 that disrupt the interaction with Brd4 do not affect the ability of these E2s to associate with chromosomes. Thus, while all papillomaviruses attach their genomes to cellular chromosomes to facilitate genome segregation, they target different cellular binding partners. In summary, the E2 proteins from many papillomaviruses, including the clinically important alpha genus human papillomaviruses, interact with Brd4 to mediate transcriptional activation function but not all depend on this interaction to efficiently associate with mitotic chromosomes.
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5

Antonsson, Annika, and Bengt Göran Hansson. "Healthy Skin of Many Animal Species Harbors Papillomaviruses Which Are Closely Related to Their Human Counterparts." Journal of Virology 76, no. 24 (December 15, 2002): 12537–42. http://dx.doi.org/10.1128/jvi.76.24.12537-12542.2002.

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ABSTRACT Papillomaviruses associated with clinical symptoms have been found in many vertebrate species. In this study, we have used an L1 gene consensus PCR test designed to detect a broad spectrum of human skin papillomaviruses to analyze swab samples from healthy skin of 111 animals belonging to 19 vertebrate species. In eight of the species, papillomavirus DNA was found with the following prevalences: chimpanzees, 9 of 11 samples positive; gorillas, 3 of 4; long-tailed macaques, 14 of 16; spider monkeys, 2 of 2; ruffed lemurs, 1 of 2; cows, 6 of 10; European elks, 4 of 4; aurochs, 1 of 1. In total, 53 new putative animal papillomavirus types were found. The results show that skin papillomaviruses can be detected in healthy skin from many different animal species and are sufficiently related genetically to their human counterparts to be identified by a human skin papillomavirus primer set (FAP59 and FAP64).
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6

Varsani, Arvind, Simona Kraberger, Scott Jennings, Elizabeth L. Porzig, Laurel Julian, Melanie Massaro, Annie Pollard, Grant Ballard, and David G. Ainley. "A novel papillomavirus in Adélie penguin (Pygoscelis adeliae) faeces sampled at the Cape Crozier colony, Antarctica." Journal of General Virology 95, no. 6 (June 1, 2014): 1352–65. http://dx.doi.org/10.1099/vir.0.064436-0.

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Papillomaviruses are epitheliotropic viruses that have circular dsDNA genomes encapsidated in non-enveloped virions. They have been found to infect a variety of mammals, reptiles and birds, but so far they have not been found in amphibians. Using a next-generation sequencing de novo assembly contig-informed recovery, we cloned and Sanger sequenced the complete genome of a novel papillomavirus from the faecal matter of Adélie penguins (Pygoscelis adeliae) nesting on Ross Island, Antarctica. The genome had all the usual features of a papillomavirus and an E9 ORF encoding a protein of unknown function that is found in all avian papillomaviruses to date. This novel papillomavirus genome shared ~60 % pairwise identity with the genomes of the other three known avian papillomaviruses: Fringilla coelebs papillomavirus 1 (FcPV1), Francolinus leucoscepus papillomavirus 1 (FlPV1) and Psittacus erithacus papillomavirus 1. Pairwise identity analysis and phylogenetic analysis of the major capsid protein gene clearly indicated that it represents a novel species, which we named Pygoscelis adeliae papillomavirus 1 (PaCV1). No evidence of recombination was detected in the genome of PaCV1, but we did detect a recombinant region (119 nt) in the E6 gene of FlPV1 with the recombinant region being derived from ancestral FcPV1-like sequences. Previously only paramyxoviruses, orthomyxoviruses and avian pox viruses have been genetically identified in penguins; however, the majority of penguin viral identifications have been based on serology or histology. This is the first report, to our knowledge, of a papillomavirus associated with a penguin species.
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7

Carrai, Maura, Kate Van Brussel, Mang Shi, Ci-Xiu Li, Wei-Shan Chang, John S. Munday, Katja Voss, et al. "Identification of a Novel Papillomavirus Associated with Squamous Cell Carcinoma in a Domestic Cat." Viruses 12, no. 1 (January 20, 2020): 124. http://dx.doi.org/10.3390/v12010124.

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Papillomaviruses infect the skin and mucosal surfaces of diverse animal hosts with consequences ranging from asymptomatic colonization to highly malignant epithelial cancers. Increasing evidence suggests a role for papillomaviruses in the most common cutaneous malignancy of domestic cats, squamous cell carcinoma (SCC). Using total DNA sequencing we identified a novel feline papillomavirus in a nasal biopsy taken from a cat presenting with both nasal cavity lymphoma and recurrent squamous cell carcinoma affecting the nasal planum. We designate this novel virus as Felis catus papillomavirus 6 (FcaPV6). The complete FcaPV6 7453 bp genome was similar to those of other feline papillomaviruses and phylogenetic analysis revealed that it was most closely related to FcaPV3, although was distinct enough to represent a new viral type. Classification of FcaPV6 in a new genus alongside FcaPVs 3, 4 and 5 is supported. Archived excisional biopsy of the SCC, taken 20 months prior to presentation, was intensely positive on p16 immunostaining. FcaPV6, amplified using virus-specific, but not consensus, PCR, was the only papillomavirus detected in DNA extracted from the SCC. Conversely, renal lymphoma, sampled at necropsy two months after presentation, tested negative on FcaPV6-specific PCR. In sum, using metagenomics we demonstrate the presence of a novel feline papillomavirus in association with cutaneous squamous cell carcinoma.
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8

Terai, Masanori, Rob DeSalle, and Robert D. Burk. "Lack of Canonical E6 and E7 Open Reading Frames in Bird Papillomaviruses: Fringilla coelebs Papillomavirus and Psittacus erithacus timneh Papillomavirus." Journal of Virology 76, no. 19 (October 1, 2002): 10020–23. http://dx.doi.org/10.1128/jvi.76.19.10020-10023.2002.

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ABSTRACT Determination and analyses of the complete sequence of Fringilla coelebs papillomavirus and Psittacus erithacus timneh papillomavirus indicate that they represent a distinct and distant lineage of papillomaviruses. The lack of canonical E6-E7 open reading frames suggests that they serve adaptive functions during papillomavirus evolution.
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9

Nordin, Peter, Bengt Göran Hansson, Carita Hansson, Ingemar Blohmè, Olle Larkö, and Kristin Andersson. "Human Papilloma Virus in Skin, Mouth and Uterine Cervix in Female Renal Transplant Recipients With or Without a History of Cutaneous Squamous Cell Carcinoma." Acta Dermato-Venereologica 87, no. 3 (February 23, 2007): 219–22. http://dx.doi.org/10.2340/00015555-0235.

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Some human papillomaviruses are thought to be associated with skin cancer. In this pilot study, 21 female renal transplant carriers, 10 with a history of skin squamous cell carcinoma and 11 without, together with 9 age-matched healthy women were investigated for human papillomavirus DNA in sun-exposed (forehead) and less sun-exposed (buttock) skin, mouth and uterine cervix. Paraffin-embedded tumours from 9 of the patients with a history of squamous cell carcinoma were analysed. Healthy skin from both the healthy and the immunosuppressed individuals harboured a wide variety of papillomaviruses. In the healthy individuals, samples from less sun-exposed skin showed a lower prevalence of human papillomavirus DNA than corresponding samples from the immunosuppressed patients (4/9 and 7/9, respectively). Among the immunosuppressed patients, human papillomavirus DNA was found as frequently in buttock samples (17/21) as in forehead samples (17/20). There was no increased prevalence of human papillomavirus in the cervix or mouth samples from the immunosuppressed patients.
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10

White, Elizabeth A., Rebecca E. Kramer, Justin H. Hwang, Arun T. Pores Fernando, Nana Naetar, William C. Hahn, Thomas M. Roberts, Brian S. Schaffhausen, David M. Livingston, and Peter M. Howley. "Papillomavirus E7 Oncoproteins Share Functions with Polyomavirus Small T Antigens." Journal of Virology 89, no. 5 (December 24, 2014): 2857–65. http://dx.doi.org/10.1128/jvi.03282-14.

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ABSTRACTMany of the small DNA tumor viruses encode transforming proteins that function by targeting critical cellular pathways involved in cell proliferation and survival. In this study, we have examined whether some of the functions of the polyomavirus small T antigens (ST) are shared by the E6 and E7 oncoproteins of two oncogenic papillomaviruses. Using three different assays, we have found that E7 can provide some simian virus 40 (SV40) or murine polyomavirus (PyV) ST functions. Both human papillomavirus 16 (HPV16) and bovine papillomavirus (BPV1) E7 proteins are capable of partially substituting for SV40 ST in a transformation assay that also includes SV40 large T antigen, the catalytic subunit of cellular telomerase, and oncogenic Ras. Like SV40 ST, HPV16 E7 has the ability to override a quiescence block induced by mitogen deprivation. Like PyV ST, it also has the ability to inhibit myoblast differentiation. At least two of these activities are dependent upon the interaction of HPV16 E7 with retinoblastoma protein family members. For small T antigens, interaction with PP2A is needed for each of these functions. Even though there is no strong evidence that E6 or E7 share the ability of small T to interact with PP2A, E7 provides these functions related to cellular transformation.IMPORTANCEDNA tumor viruses have provided major insights into how cancers develop. Some viruses, like the human papillomaviruses, can cause cancer directly. Both the papillomaviruses and the polyomaviruses have served as tools for understanding pathways that are often perturbed in cancer. Here, we have compared the functions of transforming proteins from several DNA tumor viruses, including two papillomaviruses and two polyomaviruses. We tested the papillomavirus E6 and E7 oncoproteins in three functional assays and found that E7 can provide some or all of the functions of the SV40 small T antigen, another well-characterized oncoprotein, in two of these assays. In a third assay, papillomavirus E7 has the same effect as the murine polyomavirus small T protein. In summary, we report several new functions for the papillomavirus E7 proteins, which will contribute new insights into the roles of viruses in cancer and the cellular pathways they perturb in carcinogenesis.
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11

Rosenbaum, Claire S., Arno Wünschmann, Aníbal G. Armién, Renee Schott, Vikash K. Singh, and Sunil K. Mor. "Novel papillomavirus in a mallard duck with mesenchymal chondroid dermal tumors." Journal of Veterinary Diagnostic Investigation 34, no. 2 (January 28, 2022): 231–36. http://dx.doi.org/10.1177/10406387221075607.

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Papillomaviruses, which are epitheliotropic and may induce epithelial tumors, have been identified in several avian species, including ducks. An adult female mallard duck ( Anas platyrhynchos) was admitted to a wildlife rehabilitation center with 2 beige, well-demarcated, firm masses: one in the subcutis under a wing, and the other on a digit of the right foot. After euthanasia, the masses were fixed in formalin for histologic examination. Both tumors had a lobular organization with cartilage cores surrounded by densely cellular interlacing bundles of spindle cells. Neoplastic chondroblasts in both masses, particularly the digital mass, contained basophilic intranuclear inclusion bodies, which consisted of assembly complexes of icosahedral virions of 44-nm diameter. Next-generation sequencing allowed whole genome assembly of a novel papillomavirus ( Anas platyrhynchos papillomavirus 2) related most closely to Fulmarus glacialis papillomavirus 1 (59.49% nucleotide identity). Our case supports the observation that certain papillomaviruses can productively infect mesenchymal cells and induce neoplasia.
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12

Li, Ci-Xiu, Wei-Shan Chang, Katerina Mitsakos, James Rodger, Edward C. Holmes, and Bernard J. Hudson. "Identification of a Novel Equine Papillomavirus in Semen from a Thoroughbred Stallion with a Penile Lesion." Viruses 11, no. 8 (August 4, 2019): 713. http://dx.doi.org/10.3390/v11080713.

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Papillomaviruses (PVs) have been identified in a wide range of animal species and are associated with a variety of disease syndromes including classical papillomatosis, aural plaques, and genital papillomas. In horses, 13 PVs have been described to date, falling into six genera. Using total RNA sequencing (meta-transcriptomics) we identified a novel equine papillomavirus in semen taken from a thoroughbred stallion suffering a genital lesion, which was confirmed by nested RT-PCR. We designate this novel virus Equus caballus papillomavirus 9 (EcPV9). The complete 7656 bp genome of EcPV9 exhibited similar characteristics to those of other horse papillomaviruses. Phylogenetic analysis based on concatenated E1-E2-L2-L1 amino acid sequences revealed that EcPV9 clustered with EcPV2, EcPV4, and EcPV5, although was distinct enough to represent a new viral species within the genus Dyoiotapapillomavirus (69.35%, 59.25%, and 58.00% nucleotide similarity to EcPV2, EcPV4, and EcPV5, respectively). In sum, we demonstrate the presence of a novel equine papillomavirus for which more detailed studies of disease association are merited.
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13

Erdélyi, Károly, János Gál, László Sugár, Krisztina Ursu, Petra Forgách, Levente Szeredi, and Theodora Steineck. "Papillomavirus-associated fibropapillomas of red deer ( Cervus elaphus )." Acta Veterinaria Hungarica 57, no. 2 (June 1, 2009): 337–44. http://dx.doi.org/10.1556/avet.57.2009.2.14.

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Oval, firm, cutaneous tumours with a rough, hairless, pigmented surface, exhibiting a moderately pronounced papillary structure were detected on the abdominal skin of two young red deer (Cervus elaphus). One animal was shot in Lower Austria in 2004, the other at a deer farm in Hungary in 2007. Histological examination of both samples classified the tumours as fibropapillomas, showing marked proliferation of fibroblasts and connective tissue, accompanied by hyperkeratosis, parakeratosis and acanthosis of the overlaying epidermis, and occasional foci of inflammation. The distribution of cytokeratin and vimentin was characterised in the lesion. The presence of papillomavirus (PV) antigen was demonstrated by immunohistochemistry in both cases. Papillomavirus-specific DNA was successfully amplified by PCR from one sample. The obtained partial nucleotide sequence of the L2 ORF exhibited the highest critical identity values with the homologous regions of Delta-papillomaviruses, especially the Roe deer papillomavirus (93%). Phylogenetic analysis of the partial L2 ORF sequence alignment of 10 papillomaviruses by both neighbour-joining and maximum parsimony method confirmed that the Red deer PV is very closely related to the Western roe deer papillomavirus (CcPV1).
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14

Muglikar, Dushyant Madhukarrao, Jyoti Chavan, U. M. Tumlam, S. Budhe, and Abijit Barate. "Recent Developments in the Understanding of Bovine Papillomavirus." International Journal of Current Microbiology and Applied Sciences 11, no. 4 (April 10, 2022): 50–55. http://dx.doi.org/10.20546/ijcmas.2022.1104.008.

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Papillomaviruses are epitheliotropic, non-enveloped, double-stranded DNA viruses. The Papillomaviridae family consists of 5 genera affecting cattle, including Delta papillomavirus, Xi papillomavirus, Epsilon papillomavirus, Dyoxi papillomavirus, and Dyokappa papillomavirus. Among these genera, 24 types of bovine papillomaviruses (BPVs) have been reported to date. The BPV genome is almost 8 Kb in size and is organized into three regions: early (E), late (L), and long codon region (LCR), The E region codes for replication proteins (E1, E2, E4) as well as oncoproteins (E5, E6, and E7). The L1 ORF is the most conserved among PVs and for this reason, it is employed in virus classification. The present PV diversity can be explained by multiple evolutionary mechanisms. Virus host-divergence is an important evolutionary force, however this force solely cannot explain the evolution of PVs and their diversity, thus alternative mechanisms such as within-host virus duplication, recombination, viral sorting, or viral adaptation after a host switch, may therefore contribute considerably to explain the PV diversification. This review will provide a quick overview of the genomes and structures of BPV as well as a more detailed description of genotypic diversity.
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15

Paul, Țuțu, Tanase Oana Irina, Daraban Florentina, Dascălu Mihaela Anca, Soreanu Dumitru-Octavian, and Mareș Mihai. "Classification and clinical significance of Papillomavirus infection in domestic cats." Scientific Papers Journal VETERINARY SERIES 66, no. 4 (December 15, 2023): 53–62. http://dx.doi.org/10.61900/spjvs.2023.04.09.

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During the last decades, the infection with papillomavirus in domestic cats gained interest from the veterinary community due to its significant impact on the companion's animal's health. Therefore, in this review, we aim to present a concise classification of feline papillomaviruses and their clinical relevance in domestic felines. Initially, the different types of papillomaviruses affecting domestic cats are described. Here, we emphasize the molecular diversity and transmission ways to better understand each virus type and its clinical implications. Furthermore, we explore the clinical importance of papillomavirus infections, analyzing their various manifestations such as skin or oral lesions. We outline the signs and symptoms of these infections, shedding light on the oncogenic mechanisms used by the virus. The knowledge gained from this analysis holds the potential to refine veterinary medical practices, enabling the effective management of this condition and ultimately enhancing the overall quality of life for our feline companions.
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16

Bravo, Ignacio G., and Marta Félez-Sánchez. "Papillomaviruses." Evolution, Medicine, and Public Health 2015, no. 1 (2015): 32–51. http://dx.doi.org/10.1093/emph/eov003.

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17

Lowy, Douglas R., and John T. Schiller. "Papillomaviruses." Clinics in Dermatology 3, no. 4 (October 1985): 1–7. http://dx.doi.org/10.1016/0738-081x(85)90044-6.

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18

Griffin, Beverly E. "Papillomaviruses." Virus Research 5, no. 4 (September 1986): 407–8. http://dx.doi.org/10.1016/0168-1702(86)90032-8.

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19

Reeves, W. C. "Papillomaviruses." Virus Research 21, no. 2 (October 1991): 166. http://dx.doi.org/10.1016/0168-1702(91)90009-k.

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20

Grint, P. "Papillomaviruses." Journal of Clinical Pathology 40, no. 3 (March 1, 1987): 357. http://dx.doi.org/10.1136/jcp.40.3.357-a.

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Xie, Jian, Pengwei Zhang, Mac Crite, and Daniel DiMaio. "Papillomaviruses Go Retro." Pathogens 9, no. 4 (April 7, 2020): 267. http://dx.doi.org/10.3390/pathogens9040267.

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Human papillomaviruses are important pathogens responsible for approximately 5% of cancer as well as other important human diseases, but many aspects of the papillomavirus life cycle are poorly understood. To undergo genome replication, HPV DNA must traffic from the cell surface to the nucleus. Recent findings have revolutionized our understanding of HPV entry, showing that it requires numerous cellular proteins and proceeds via a series of intracellular membrane-bound vesicles that comprise the retrograde transport pathway. This paper reviews the evidence supporting this unique entry mechanism with a focus on the crucial step by which the incoming virus particle is transferred from the endosome into the retrograde pathway. This new understanding provides novel insights into basic cellular biology and suggests novel rational approaches to inhibit HPV infection.
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Conway, M. J., and C. Meyers. "Replication and Assembly of Human Papillomaviruses." Journal of Dental Research 88, no. 4 (April 2009): 307–17. http://dx.doi.org/10.1177/0022034509333446.

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Human papillomaviruses (HPVs) are small dsDNA tumor viruses, which are the etiologic agents of most cervical cancers and are associated with a growing percentage of oropharyngeal cancers. The HPV capsid is non-enveloped, having a T=7 icosahedral symmetry formed via the interaction among 72 pentamers of the major capsid protein, L1. The minor capsid protein L2 associates with L1 pentamers, although it is not known if each L1 pentamer contains a single L2 protein. The HPV life cycle strictly adheres to the host cell differentiation program, and as such, native HPV virions are only produced in vivo or in organotypic “raft” culture. Research producing synthetic papillomavirus particles—such as virus-like particles (VLPs), papillomavirus-based gene transfer vectors, known as pseudovirions (PsV), and papillomavirus genome-containing quasivirions (QV)—has bypassed the need for stratifying and differentiating host tissue in viral assembly and has allowed for the rapid analysis of HPV infectivity pathways, transmission, immunogenicity, and viral structure.
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Arman, Warda, and Karl Munger. "Mechanistic Contributions of lncRNAs to Cellular Signaling Pathways Crucial to the Lifecycle of Human Papillomaviruses." Viruses 14, no. 11 (November 3, 2022): 2439. http://dx.doi.org/10.3390/v14112439.

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Papillomaviruses are ubiquitous epitheliotropic viruses with double-stranded circular DNA genomes of approximately 8000 base pairs. The viral life cycle is somewhat unusual in that these viruses can establish persistent infections in the mitotically active basal epithelial cells that they initially infect. High-level viral genome replication (“genome amplification”), the expression of capsid proteins, and the formation of infectious progeny are restricted to terminally differentiated cells where genomes are synthesized at replication factories at sites of double-strand DNA breaks. To establish persistent infections, papillomaviruses need to retain the basal cell identity of the initially infected cells and restrain and delay their epithelial differentiation program. To enable high-level viral genome replication, papillomaviruses also need to hold the inherently growth-arrested terminally differentiated cells in a replication-competent state. To provide ample sites for viral genome synthesis, they target the DNA damage and repair machinery. Studies focusing on delineating cellular factors that are targeted by papillomaviruses may aid the development of antivirals. Whilst most of the current research efforts focus on protein targets, the majority of the human transcriptome consists of noncoding RNAs. This review focuses on one specific class of noncoding RNAs, long noncoding RNAs (lncRNAs), and summarizes work on lncRNAs that may regulate the cellular processes that are subverted by papillomavirus to enable persistent infections and progeny synthesis.
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Korsak, K. S., and E. V. Voropaev. "Phylogenetic features of papillomaviruses and their significance in the diagnosis of papillomavirus infection." Health and Ecology Issues, no. 4 (December 28, 2020): 23–28. http://dx.doi.org/10.51523/2708-6011.2020-17-4-3.

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Viruses belonging to the Papillomaviridae family have been isolated from mammals, birds and reptiles. The analysis of the genome structure of more than 240 different types of papillomaviruses has made it possible to better understand their evolutionary path. The existing data indicate that many diverse evolutionary mechanisms have influenced their phylogenetic tree. For more than 400 million years, papillomaviruses have occupied various ecological niches. Niche sorting was followed by extensive periods of host-parasite co-evolution. Adaptation to different host tissues, as well as to changing environmental conditions can explain some features of the members of the Papillomaviridae family, one of which is human papillomavirus (HPV), having an important clinical significance. The study of the driving mechanisms of the evolution will help to change the notions about HPV virulence, character of its spread, epidemiology, as well as the pathogenesis and the course of oncologic diseases caused by it. This review highlights some moments of the evolutionary history of papillomaviruses which created a background for the development of oncogenic features of certain HPV types.
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Lange, Christian E., Elisabeth Vetsch, Mathias Ackermann, Claude Favrot, and Kurt Tobler. "Four novel papillomavirus sequences support a broad diversity among equine papillomaviruses." Journal of General Virology 94, no. 6 (June 1, 2013): 1365–72. http://dx.doi.org/10.1099/vir.0.052092-0.

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Papillomaviruses appear to be species-specific pathogens, and it was suggested that each animal species might harbour its own set of papillomaviruses. However, all approaches addressing the underlying evolutionary phenomena still suffer from very limited data about animal papillomaviruses. In case of the horse for example, only three equine papillomaviruses (EcPVs) have been identified. To further address the situation in this host, suspected papillomavirus-associated lesions were tested for EcPV DNA. Four novel EcPV types were detected and their genomes entirely cloned and sequenced. They display the characteristic organization, with early (E) and late (L) regions harbouring the seven classical open reading frames divided by non-coding regions. They were named EcPVs 4, 5, 6 and 7, according to their dissimilarity to other papillomaviruses. Most L1 nucleotide identities were shared with EcPV2 in case of EcPV4 (62 %) and EcPV5 (60 %) or with EcPV3 in case of EcPV6 (70 %) and EcPV7 (71 %). Thus, EcPVs 4 and 5 may establish novel species within the genus Dyoiota, while EcPVs 6 and 7 might fit into the genus Dyorho and belong to the same species as EcPV3. They were found in genital plaques (EcPV4), aural plaques (EcPV5, EcPV6) or penile masses (EcPV7). Interestingly, PCR analysis revealed the DNA of EcPV2 and EcPV4 as well as of EcPV3 and EcPV6 together in the same tissue samples, respectively. In conclusion, the DNA of four novel EcPV types was identified and cloned. They cluster with the known types and support broad genetic EcPV diversity in at least two of the known clades. Furthermore, PCR assays also provide evidence for EcPV co-infections in horses.
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Tobler, Kurt, Claude Favrot, Gilles Nespeca, and Mathias Ackermann. "Detection of the prototype of a potential novel genus in the family Papillomaviridae in association with canine epidermodysplasia verruciformis." Journal of General Virology 87, no. 12 (December 1, 2006): 3551–57. http://dx.doi.org/10.1099/vir.0.82305-0.

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Epidermodysplasia verruciformis (EV) is a rare human genetic predisposition to develop flat warts, some of which subsequently undergo cancer transformation. Some human papillomaviruses (HPVs), i.e. HPV 5 and 8, have been associated with cancer development as a sequela of EV. As similar diseases have been observed in dogs, it was hypothesized that unknown canine papillomaviruses (CPVs) may exist and that they may be present in cases of canine EV. Consequently, DNA was extracted from a malignant lesion of a dog with EV and circular DNA was amplified by multiple-primed rolling-circle amplification (RCA). Indeed, sequence determination and analysis of the RCA-amplified and cloned DNA from a malignant canine EV lesion resulted in the detection and primary description of a third CPV (CPV3). Typical papillomavirus genes were identified, with deduced amino acid similarities ranging from 20 to 57 % for E1, E2, E6, E7, L1 and L2, respectively. According to the sequence of the L1 gene, which is used for papillomavirus classification, the new isolate meets the majority of criteria needed to declare detection of a novel genus among the papillomaviruses. Thus, CPV3 may represent the prototype of this novel genus. As the novel virus was found in a dog in association with lesions reminiscent of human EV, it should be interesting to test in the future whether this condition can be reproduced in experimental animals. If such were the case, a new model for EV could be established.
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27

Volgareva, G. M., I. N. Mikhaylova, and D. A. Golovina. "Melanoma and human papillomaviruses: is there an outlook for study? Review of the literature." Annals of the Russian academy of medical sciences 71, no. 2 (April 5, 2016): 121–27. http://dx.doi.org/10.15690/vramn654.

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Melanoma is one of the most aggressive human malignant tumors. Its incidence and mortality are growing steadily. Ultraviolet irradiation is the main risk factor for melanoma, however it seems not to be the sole environmental factor involved in melanomagenesis.Probability of viral etiology of melanoma has been discussed for a long time. Human papillomaviruses have been mentioned among candidates for its etiologic agents. Much interest in these viruses is due to the fact that powerful carcinogens causing cervical cancer and some other cancer types are members of this group. The aim of the review is analysis of literature data on association of melanoma with human papillomaviruses.Several groups found papillomaviruses in skin melanomas as well as in mucous ones; viruses if high oncogenic risk were detected in some cases. In majority of the studies in which viral DNA-positive melanomas were found testing for viral genome expression was not done. Objective difficulty of such studies is the problem of negative control as papillomaviruses are being routinely found in normal skin and mucous membranes thus creating justifiable threat of tumor specimen contamination with viral DNA in vivo. Complex approach might become helpful in overcoming this obstacle: detecting of viral DNA, viral oncogenes’ mRNAs and corresponding proteins.There are limited data on aggravation of the disease prognosis in papillomavirus-positive melanomas. However systematic observation of some sizeable patients’ contingents differing in the given tumor character has not been performed yet.The problem of melanoma association with human papillomaviruses remains unsolved
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28

Kim, Kitai, Peter C. Angeletti, Elizabeth C. Hassebroek, and Paul F. Lambert. "Identification of cis-Acting Elements That Mediate the Replication and Maintenance of Human Papillomavirus Type 16 Genomes in Saccharomyces cerevisiae." Journal of Virology 79, no. 10 (May 15, 2005): 5933–42. http://dx.doi.org/10.1128/jvi.79.10.5933-5942.2005.

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ABSTRACT Papillomaviruses contain small double-stranded DNA genomes that are maintained in persistently infected mammalian host epithelia as nuclear plasmids and rely upon the host replication machinery for replication. Papillomaviruses encode a DNA helicase, E1, which can specifically bind to the viral genome and support DNA synthesis. Under some conditions in mammalian cells, E1 is not required for viral DNA synthesis, leading to the hypothesis that papillomavirus DNA can be replicated solely by the host replication machinery. This machinery is highly conserved among eukaryotes. We and others found that papillomavirus DNA could replicate in a simple eukaryote, Saccharomyces cerevisiae. Specifically, papillomavirus DNA could substitute for the function of the autonomously replicating sequence (ARS) and centromere (CEN) elements that are normally both required for the stable replication of extrachromosomal DNAs in yeast. Furthermore, this form of replication in yeast was E1 independent. In this study, we map the elements in the human papillomavirus type 16 (HPV16) genome that can substitute for yeast ARS and CEN elements. A single element, termed rep, was identified that can substitute for ARS, and multiple elements, termed mtc, could substitute for CEN. The location of one of these mtc elements overlaps the location of rep, and this approximately 1,000-bp region of HPV16 was sufficient to support stable replication of a bacterial-yeast shuttle plasmid deleted of both ARS and CEN elements.
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29

Sundberg, J. P., M. K. O'Banion, A. Shima, C. Knupp, and M. E. Reichmann. "Papillomas and Carcinomas Associated with a Papillomavirus in European Harvest Mice (Micromys minutus)." Veterinary Pathology 25, no. 5 (September 1988): 356–61. http://dx.doi.org/10.1177/030098588802500504.

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Papillomaviruses, group-specific papillomavirus antigens, or extrachromosomal papillomavirus DNA were detected in cutaneous, mucocutaneous, and pulmonary tumors affecting a colony of European harvest mice (Micromys minutus). Skin lesions were classified as acanthomatous hyperplasia, epidermal inclusion cysts. squamous papillomas, inverted papillomas, trichoepitheliomas, and sebaceous carcinomas. Cutaneous horns (hyperkeratotic papillomas) were on mucocutaneous junctions of one animal. One mouse, with a cutaneous sebaceous carcinoma, had multiple pulmonary keratinaceous cysts. Papillomavirus antigens, detected by the avidin-biotin technique, were in 20 of 31 lesions tested. In contrast, by Southern blot hybridization all 28 lesions tested contained papillomavirus DNA. Papillomavirus DNA was demonstrated in two often benign cutaneous lesions by in situ hybridization.
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30

McCance, Dennis J. "HUMAN PAPILLOMAVIRUSES." Infectious Disease Clinics of North America 8, no. 4 (December 1994): 751–64. http://dx.doi.org/10.1016/s0891-5520(20)30624-3.

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31

Uberoi, Aayushi, and Paul Lambert. "Rodent Papillomaviruses." Viruses 9, no. 12 (November 27, 2017): 362. http://dx.doi.org/10.3390/v9120362.

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32

CRIPE, TIMOTHY P. "Human papillomaviruses." Pediatric Infectious Disease Journal 9, no. 11 (November 1990): 836–44. http://dx.doi.org/10.1097/00006454-199011000-00012.

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33

Demeter, Lisa M., and Richard C. Reichman. "Human papillomaviruses." Current Opinion in Infectious Diseases 3, no. 6 (December 1990): 796–804. http://dx.doi.org/10.1097/00001432-199012000-00011.

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34

Unger, Elizabeth R., and Eliane Duarte-Franco. "HUMAN PAPILLOMAVIRUSES." Obstetrics and Gynecology Clinics of North America 28, no. 4 (December 2001): 653–66. http://dx.doi.org/10.1016/s0889-8545(05)70227-8.

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35

Rector, Annabel, and Marc Van Ranst. "Animal papillomaviruses." Virology 445, no. 1-2 (October 2013): 213–23. http://dx.doi.org/10.1016/j.virol.2013.05.007.

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36

Jarrett, W. F. H. "Bovine papillomaviruses." Clinics in Dermatology 3, no. 4 (October 1985): 8–19. http://dx.doi.org/10.1016/0738-081x(85)90045-8.

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37

Lange, Christian E., and Claude Favrot. "Canine Papillomaviruses." Veterinary Clinics of North America: Small Animal Practice 41, no. 6 (November 2011): 1183–95. http://dx.doi.org/10.1016/j.cvsm.2011.08.003.

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38

Ostrow, Ronald S., and Anthony J. Faras. "Human papillomaviruses." Clinical Microbiology Newsletter 8, no. 8 (April 1986): 53–56. http://dx.doi.org/10.1016/0196-4399(86)90033-4.

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39

Sanz, Alexandra, Erica Miller, Nikki Harley, and Laura Coffee. "Papillomatosis in a raccoon (<em>Procyon lotor</em>)." Wildlife Rehabilitation Bulletin 40, no. 1 (October 7, 2022): 22–26. http://dx.doi.org/10.53607/wrb.v40.255.

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Papillomaviruses are species-specific double-stranded DNA viruses with at least 50 species of mammals. Although well-studied in humans, papillomaviruses in the raccoon (Procyon lotor) are not well characterized, and few cases have been published. Therefore, when the disease is encountered in a rehabilitation center, definitive diagnosis and treatment in the raccoon can be unclear. This case study outlines the characteristic gross and histologic lesions of an affected individual to facilitate identification and treatment of this disease in the future. In the case of this juvenile raccoon, ulcerated exophytic lesions on the bridge of its nose and right forelimb digit were seen grossly, with the presence of koilocytes and hyperkeratosis observed histologically. These findings are consistent with other documented cases of papillomavirus in raccoons and canines. Affected raccoons do not require extensive treatment, as raccoon papillomatosis is considered self-limiting.
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40

Varsani, Arvind, Eric van der Walt, Livio Heath, Edward P. Rybicki, Anna Lise Williamson, and Darren P. Martin. "Evidence of ancient papillomavirus recombination." Journal of General Virology 87, no. 9 (September 1, 2006): 2527–31. http://dx.doi.org/10.1099/vir.0.81917-0.

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An open question amongst papillomavirus taxonomists is whether recombination has featured in the evolutionary history of these viruses. Since the onset of the global AIDS epidemic, the question is somewhat less academic, because immune-compromised human immunodeficiency virus patients are often co-infected with extraordinarily diverse mixtures of human papillomavirus (HPV) types. It is expected that these conditions may facilitate the emergence of HPV recombinants, some of which might have novel pathogenic properties. Here, a range of rigorous analyses is applied to full-genome sequences of papillomaviruses to provide convincing statistical and phylogenetic evidence that evolutionarily relevant papillomavirus recombination can occur.
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41

Awua, Adolf K., Alberto Severini, Edwin K. Wiredu, Edwin A. Afari, Vanessa A. Zubach, and Richard M. K. Adanu. "Self-Collected Specimens Revealed a Higher Vaccine- and Non-Vaccine-Type Human Papillomavirus Prevalences in a Cross-Sectional Study in Akuse." Advances in Preventive Medicine 2020 (January 22, 2020): 1–13. http://dx.doi.org/10.1155/2020/8343169.

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Background. Population-specific epidemiologic data on human Papillomavirus infection, which are limited in most of the SubSaharan African countries, are necessary for effective cervical cancer prevention. This study aimed to generate population-specific data on human Papillomavirus infections, and determine which of these, self-collected and provider-collected specimens, gives a higher estimate of the prevalence of human Papillomaviruses, including vaccine and non-vaccine-type human Papillomavirus. Methods. In this cross-sectional study, following a questionnaire-based collection of epidemiological data, self-, and provider-collected specimens, obtained from women 15−65 years of age, were analysed for human Papillomavirus types by a nested-multiplex polymerase chain reaction, and for cervical lesions by Pap testing. HPV data were categorised according to risk type and vaccine types for further analysis. Results. The difference between the overall human Papillomavirus infection prevalences obtained with the self-collected specimens, 43.1% (95% CI of 38.0–51.0%) and that with the provider-collected samples, 23.3% (95% CI of 19.0–31.0%) were significant (p≤0.001). The prevalence of quadrivalent vaccine-type human Papillomaviruses was 12.3% with self-collected specimens, but 6.0% with provider-collected specimens. For the nonavalent vaccine-types, the prevalences were 26.6% and 16.7% respectively. There were multiple infections involving both vaccine-preventable and nonvaccine preventable high-risk human Papillomavirus genotypes. Conclusion. The Akuse subdistrict can, therefore, be said to have a high burden of human Papillomavirus infections, which included nonvaccine types, as detected with both self-collected and provider-collected specimens. These imply that self-collection is to be given a higher consideration as a means for a population-based high-risk human Papillomavirus infections burdens assessment/screening. Additionally, even with a successful implementation of the HPV vaccination, if introduced in Ghana, there is still the need to continue with the screening of women.
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42

Arron, Sarah Tuttleton, Peter Skewes-Cox, Phong H. Do, Eric Dybbro, Maria Da Costa, Joel M. Palefsky, and Joseph L. DeRisi. "Validation of a Diagnostic Microarray for Human Papillomavirus: Coverage of 102 Genotypes." Journal of Nucleic Acids 2011 (2011): 1–6. http://dx.doi.org/10.4061/2011/756905.

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Papillomaviruses have been implicated in a variety of human diseases ranging from common warts to invasive carcinoma of the anogenital mucosa. Existing assays for genotyping human papillomavirus are restricted to a small number of types. Here, we present a comprehensive, accurate microarray strategy for detection and genotyping of 102 human papillomavirus types and validate its use in a panel of 91 anal swabs. This array has equal performance to traditional dot blot analysis with the benefits of added genotype coverage and the ability to calibrate readout over a range of sensitivity or specificity values.
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43

Stanley, MA, PJ Masterson, and PK Nicholls. "In vitro and Animal Models for Antiviral Therapy in Papillomavirus Infections." Antiviral Chemistry and Chemotherapy 8, no. 5 (October 1997): 381–400. http://dx.doi.org/10.1177/095632029700800501.

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The need for antiviral therapies for papillomavirus infections is well recognized but the difficulties of reproducing the infectious cycle of papillomaviruses in vitro has hindered our understanding of virus-cell interactions and the regulation of viral gene expression during permissive growth. Recent advances in understanding the temporal expression and function of papillomavirus proteins has enabled consideration of a targeted approach to papillomavirus chemotherapy and in particular the inhibition of viral replication by targeting the E1 and E2 proteins. There are in vitro culture systems available for the screening of new chemotherapeutic agents, since significant advances have been made with culture systems which promote epithelial differentiation in vitro. However, to date, there are no published data which show that virions generated in vitro can infect keratinocytes and initiate another round of replication in vitro. In vivo animal models are therefore necessary to assess the efficacy of antivirals in preventing and treating viral infection, particularly for the low-risk genital viruses which are on the whole refractory to culture in vitro. Although papillomaviruses affect a wide variety of hosts in a species-specific manner, the animals most useful for modelling papillomavirus infections include the rabbit, ox, mouse, dog, horse, primate and sheep. The ideal animal model should be widely available, easy to house and handle, be large enough to allow for adequate tissue sampling, develop lesions on anatomical sites comparable with those in human diseases and these lesions should be readily accessible for monitoring and ideally should yield large amounts of infectious virus particles for use in both in vivo and in vitro studies. The relative merits of the various papillomavirus animal models available in relation to these criteria are discussed.
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44

Rector, Annabel, Ruth Tachezy, and Marc Van Ranst. "A Sequence-Independent Strategy for Detection and Cloning of Circular DNA Virus Genomes by Using Multiply Primed Rolling-Circle Amplification." Journal of Virology 78, no. 10 (May 15, 2004): 4993–98. http://dx.doi.org/10.1128/jvi.78.10.4993-4998.2004.

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ABSTRACT The discovery of novel viruses has often been accomplished by using hybridization-based methods that necessitate the availability of a previously characterized virus genome probe or knowledge of the viral nucleotide sequence to construct consensus or degenerate PCR primers. In their natural replication cycle, certain viruses employ a rolling-circle mechanism to propagate their circular genomes, and multiply primed rolling-circle amplification (RCA) with φ29 DNA polymerase has recently been applied in the amplification of circular plasmid vectors used in cloning. We employed an isothermal RCA protocol that uses random hexamer primers to amplify the complete genomes of papillomaviruses without the need for prior knowledge of their DNA sequences. We optimized this RCA technique with extracted human papillomavirus type 16 (HPV-16) DNA from W12 cells, using a real-time quantitative PCR assay to determine amplification efficiency, and obtained a 2.4 × 104-fold increase in HPV-16 DNA concentration. We were able to clone the complete HPV-16 genome from this multiply primed RCA product. The optimized protocol was subsequently applied to a bovine fibropapillomatous wart tissue sample. Whereas no papillomavirus DNA could be detected by restriction enzyme digestion of the original sample, multiply primed RCA enabled us to obtain a sufficient amount of papillomavirus DNA for restriction enzyme analysis, cloning, and subsequent sequencing of a novel variant of bovine papillomavirus type 1. The multiply primed RCA method allows the discovery of previously unknown papillomaviruses, and possibly also other circular DNA viruses, without a priori sequence information.
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45

Remm, Maido, Anu Remm, and Mart Ustav. "Human Papillomavirus Type 18 E1 Protein Is Translated from Polycistronic mRNA by a Discontinuous Scanning Mechanism." Journal of Virology 73, no. 4 (April 1, 1999): 3062–70. http://dx.doi.org/10.1128/jvi.73.4.3062-3070.1999.

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ABSTRACT Papillomaviruses are small double-stranded DNA viruses that replicate episomally in the nuclei of infected cells. The full-length E1 protein of papillomaviruses is required for the replication of viral DNA. The viral mRNA from which the human papillomavirus type 18 E1 protein is expressed is not known. We demonstrate that in eukaryotic cells, the E1 protein is expressed from polycistronic mRNA containing E6, E7, and E1 open reading frames (ORFs). The translation of adjacent E7 and E1 ORFs is not associated; it is performed by separate populations of ribosomes. The translation of the downstream E1 gene is preceded by ribosome scanning. Scanning happens at least at the 5′ end of the polycistronic mRNA and also approximately 100 bp in front of the E1 gene. Long areas in middle of the mRNA are bypassed by ribosomes, possibly by ribosomal “shunting.” Inactivation of short minicistrons in the upstream area of the E1 gene did not change the expression level of the E1 gene.
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46

Angeletti, Peter C., Kitai Kim, Fiona J. Fernandes, and Paul F. Lambert. "Stable Replication of Papillomavirus Genomes in Saccharomyces cerevisiae." Journal of Virology 76, no. 7 (April 1, 2002): 3350–58. http://dx.doi.org/10.1128/jvi.76.7.3350-3358.2002.

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ABSTRACT Papillomaviruses normally replicate in stratified squamous epithelial tissues of their mammalian hosts, in which the viral genome is found as a nuclear plasmid. Two viral proteins, E1, a helicase, and E2, a transcriptional activator and plasmid maintenance factor, are known to contribute to the episomal replication of the viral genome. Recently, our laboratory discovered that papillomaviruses can also replicate in an E1-independent manner in mammalian cells (K. Kim and P. F. Lambert, Virology, in press; K. Kim and P. F. Lambert, submitted for publication). In this study, we describe experiments investigating the capacity of the human papillomavirus type 16 (HPV16) genome to replicate in yeast (Saccharomyces cerevisiae). The full-length HPV16 genome, when linked in cis to a selectable yeast marker gene, either TRP1 or URA3, could replicate stably as an episome in yeast. The replication of papillomavirus genomes in yeast is not limited to HPV16. Bovine papillomavirus type 1 and HPV6b, -11, -16, -18, and -31 were all capable of replicating in short-term assays over a period of 20 cell doublings. The long-term persistence of viral episomes did not require any one viral gene, as mutant genomes defective in single genes also replicated episomally. These results indicate that the viral episome can replicate in the absence of the E1 DNA helicase. Similarly, E2 was also not required for replication in yeast, and E2 mutant viral genomes were stably maintained in the absence of selection, indicating the existence of an E2-independent mechanism for plasmid maintenance. The episomal replication of papillomavirus genomes in yeast provides a genetically manipulatable system in which to investigate cellular factors required for episomal replication and may provide a novel means for generating infectious papillomavirus.
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47

Strauss, Melvin, and A. Bennett Jenson. "Human Papillomavirus in Various Lesions of the Head and Neck." Otolaryngology–Head and Neck Surgery 93, no. 3 (June 1985): 342–46. http://dx.doi.org/10.1177/019459988509300310.

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The association of human papillomavirus with benign and malignant epithelial lesions of the head and neck has been studied by a peroxidase-antiperoxidase technique having immunospecificity against genus-specific structural antigens of the papillomaviruses. More than 360 specimen blocks from 144 patients were evaluated. There was evidence of human papillomavirus antigen in three out of eight patients with childhood-onset laryngeal papillomas (37.5%) and in four out of eight patients with adult-onset papillomas (50%). A patient with an unusual flat, wartlike lesion appearing as an oral cavity leukoplakia had detectable papillomavirus antigen in it. None of the 13 cases of inverting papilloma or any of the malignant lesions studied showed evidence for the presence of papillomavirus antigen. There is currently only suggestive evidence for the oncogenic potential of human papillomavirus in the head and neck.
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48

McCance, D. J. "News on papillomaviruses." Nature 335, no. 6193 (October 1988): 765–66. http://dx.doi.org/10.1038/335765a0.

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49

McBride, Alison A. "Oncogenic human papillomaviruses." Philosophical Transactions of the Royal Society B: Biological Sciences 372, no. 1732 (September 11, 2017): 20160273. http://dx.doi.org/10.1098/rstb.2016.0273.

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Human papillomaviruses (HPVs) are an ancient group of viruses with small, double-stranded DNA circular genomes. They are species-specific and have a strict tropism for mucosal and cutaneous stratified squamous epithelial surfaces of the host. A subset of these viruses has been demonstrated to be the causative agent of several human cancers. Here, we review the biology, natural history, evolution and cancer association of the oncogenic HPVs. This article is part of the themed issue ‘Human oncogenic viruses’.
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50

de Villiers, Ethel-Michele, Claude Fauquet, Thomas R. Broker, Hans-Ulrich Bernard, and Harald zur Hausen. "Classification of papillomaviruses." Virology 324, no. 1 (June 2004): 17–27. http://dx.doi.org/10.1016/j.virol.2004.03.033.

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