Molecular methods for identification and characterization of novel papillomaviruses

Clinical Microbiology and Infection

Volumn 21, Issue 9, 2015, Pages 808-816

  Kocjan, B J ^a   Bzhalava, D ^b   Forslund, O ^c   Dillner, J ^b   Poljak, Mario ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b KAROLINSKA INSTITUTE   (Sweden)

^c LUND UNIVERSITY   (Sweden)

Author keywords

Discovery; Human Papillomavirus Reference Center; Next generation sequencing; Papillomaviruses; Polymerase chain reaction; Rolling circle amplification

Indexed keywords

GENE AMPLIFICATION; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 120; HUMAN PAPILLOMAVIRUS TYPE 125; HUMAN PAPILLOMAVIRUS TYPE 150; HUMAN PAPILLOMAVIRUS TYPE 151; HUMAN PAPILLOMAVIRUS TYPE 153; HUMAN PAPILLOMAVIRUS TYPE 154; HUMAN PAPILLOMAVIRUS TYPE 155; HUMAN PAPILLOMAVIRUS TYPE 159; HUMAN PAPILLOMAVIRUS TYPE 174; HUMAN PAPILLOMAVIRUS TYPE 175; HUMAN PAPILLOMAVIRUS TYPE 178; HUMAN PAPILLOMAVIRUS TYPE 179; HUMAN PAPILLOMAVIRUS TYPE 180; HUMAN PAPILLOMAVIRUS TYPE 184; HUMAN PAPILLOMAVIRUS TYPE 197; HUMAN PAPILLOMAVIRUS TYPE 198; HUMAN PAPILLOMAVIRUS TYPE 199; HUMAN PAPILLOMAVIRUS TYPE 200; HUMAN PAPILLOMAVIRUS TYPE 201; HUMAN PAPILLOMAVIRUS TYPE 202; HUMAN PAPILLOMAVIRUS TYPE 203; HUMAN PAPILLOMAVIRUS TYPE 204; NEXT GENERATION SEQUENCING; NONHUMAN; PAPILLOMAVIRIDAE; PHODOPUS SUNGORUS PAPILLOMAVIRUS TYPE 1; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REVIEW; ROLLING CIRCLE AMPLIFICATION; SLOVENIA; SWEDEN; VIRUS CHARACTERIZATION; VIRUS IDENTIFICATION; ANIMAL; CLASSIFICATION; DNA SEQUENCE; GENETICS; GENOTYPE; ISOLATION AND PURIFICATION; PAPILLOMAVIRUS INFECTION; VETERINARY; VIROLOGY; VIRUS GENOME;

ANIMALIA; DNA VIRUSES; HUMAN PAPILLOMAVIRUS; PAPILLOMAVIRIDAE; VERTEBRATA;

ANIMALS; GENOME, VIRAL; GENOTYPE; HUMANS; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; SEQUENCE ANALYSIS, DNA; SLOVENIA; SWEDEN;

EID: 84940614340     PISSN: 1198743X     EISSN: 14690691     Source Type: Journal    
DOI: 10.1016/j.cmi.2015.05.011     Document Type: Review

References (78)

1. Bernard H.U., Burk R.D., Chen Z., van Doorslaer K., zur Hausen H., de Villiers E.M. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 2010, 401:70-79.
2. Cubie H.A. Diseases associated with human papillomavirus infection. Virology 2013, 445:21-34.
3. Rector A., Van Ranst M. Animal papillomaviruses. Virology 2013, 445:213-223.
4. de Villiers E.M., Fauquet C., Broker T.R., Bernard H.U., zur Hausen H. Classification of papillomaviruses. Virology 2004, 324:17-27.
5. de Villiers E.M. Cross-roads in the classification of papillomaviruses. Virology 2013, 445:2-10.
6. Bzhalava D., Eklund C., Dillner J. International standardization and classification of human papillomavirus types. Virology 2015, 476:341-344.
7. Van Doorslaer K., Tan Q., Xirasagar S., Bandaru S., Gopalan V., Mohamoud Y., et al. The Papillomavirus Episteme: a central resource for papillomavirus sequence data and analysis. Nucleic Acids Res 2013, 41:D571-D578.
8. Bottalico D., Chen Z., Dunne A., Ostoloza J., McKinney S., Sun C., et al. The oral cavity contains abundant known and novel human papillomaviruses from the Betapapillomavirus and Gammapapillomavirus genera. JInfect Dis 2011, 204:787-792.
9. Forslund O., Johansson H., Madsen K.G., Kofoed K. The nasal mucosa contains a large spectrum of human papillomavirus types from the Betapapillomavirus and Gammapapillomavirus genera. JInfect Dis 2013, 208:1335-1341.
10. Sichero L., Pierce Campbell C.M., Ferreira S., Sobrinho J.S., Luiza Baggio M., Galan L., et al. for the HIM Study Group. Broad HPV distribution in the genital region of men from the HPV infection in men (HIM) study. Virology 2013, 443:214-217.
11. Mlakar B., Kocjan B.J., Hošnjak L., Fujs Komloš K., Milošević M., Poljak M. Betapapillomaviruses in the anal canal of HIV positive and HIV negative men who have sex with men. JClin Virol 2014, 61:237-241.
12. Köhler A., Gottschling M., Förster J., Röwert-Huber J., Stockfleth E., Nindl I. Genomic characterization of a novel human papillomavirus (HPV-117) with a high viral load in a persisting wart. Virology 2010, 399:129-133.
13. Kovanda A., Kocjan B.J., Potočnik M., Poljak M. Characterization of a novel cutaneous human papillomavirus genotype HPV-125. PLoS One 2011, 6:e22414.
14. Mitsuishi T., Ohsawa I., Kato T., Egawa N., Kiyono T. Molecular cloning and characterisation of a novel type of human papillomavirus 160 isolated from a flat wart of an immunocompetent patient. PLoS One 2013, 8:e79592.
15. Silling S., Wieland U., Werner M., Pfister H., Potthoff A., Kreuter A. Resolution of novel human papillomavirus-induced warts after HPV vaccination. Emerg Infect Dis 2014, 20:142-145.
16. Hošnjak L., Kocjan B.J., Pirš B., Seme K., Poljak M. Characterization of two novel Gammapapillomaviruses, HPV179 and HPV184, isolated from common warts of a renal-transplant recipient. PLoS One 2015, 10:e0119154.
17. Forslund O., Antonsson A., Nordin P., Stenquist B., Hansson B.G. Abroad range of human papillomavirus types detected with a general PCR method suitable for analysis of cutaneous tumours and normal skin. JGen Virol 1999, 80:2437-2443.
18. Forslund O., Ly H., Higgins G. Improved detection of cutaneous human papillomavirus DNA by single tube nested 'hanging droplet' PCR. JVirol Methods 2003, 110:129-136.
19. Chouhy D., Gorosito M., Sánchez A., Serra E.C., Bergero A., Fernandez Bussy R., et al. New generic primer system targeting mucosal/genital and cutaneous human papillomaviruses leads to the characterization of HPV 115, a novel Beta-papillomavirus species 3. Virology 2010, 397:205-216.
20. Staheli J.P., Ryan J.T., Bruce A.G., Boyce R., Rose T.M. Consensus-degenerate hybrid oligonucleotide primers (CODEHOPs) for the detection of novel viruses in non-human primates. Methods 2009, 49:32-41.
21. Tieben L.M., ter Schegget J., Minnaar R.P., Bouwes Bavinck J.N., Berkhout R.J., Vermeer B.J., et al. Detection of cutaneous and genital HPV types in clinical samples by PCR using consensus primers. JVirol Methods 1993, 42:265-279.
22. Boxman I.L., Berkhout R.J., Mulder L.H., Wolkers M.C., Bouwes Bavinck J.N., Vermeer B.J., et al. Detection of human papillomavirus DNA in plucked hairs from renal transplant recipients and healthy volunteers. JInvest Dermatol 1997, 108:712-715.
23. Boxman I.L., Hogewoning A., Mulder L.H., Bouwes Bavinck J.N., Schegget J. Detection of human papillomavirus types 6 and 11 in pubic and perianal hair from patients with genital warts. JClin Microbiol 1999, 37:2270-2273.
24. Rector A., Van Doorslaer K., Bertelsen M., Barker I.K., Olberg R.A., Lemey P., et al. Isolation and cloning of the raccoon (Procyon lotor) papillomavirus type 1 by using degenerate papillomavirus-specific primers. JGen Virol 2005, 86:2029-2033.
25. Harwood C.A., Spink P.J., Surentheran T., Leigh I.M., de Villiers E.M., McGregor J.M., et al. Degenerate and nested PCR: a highly sensitive and specific method for detection of human papillomavirus infection in cutaneous warts. JClin Microbiol 1999, 37:3545-3555.
26. Rector A., Stevens H., Lacave G., Lemey P., Mostmans S., Salbany A., et al. Genomic characterization of novel dolphin papillomaviruses provides indications for recombination within the Papillomaviridae. Virology 2008, 378:151-161.
27. Chouhy D., Bolatti E.M., Piccirilli G., Sánchez A., Fernandez Bussy R., Giri A.A. Identification of human papillomavirus type 156, the prototype of a new human gammapapillomavirus species, by a generic and highly sensitive PCR strategy for long DNA fragments. JGen Virol 2013, 94:524-533.
28. Rector A., Tachezy R., Van Ranst M. Asequence-independent strategy for detection and cloning of circular DNA virus genomes by using multiply primed rolling-circle amplification. JVirol 2004, 78:4993-4998.
29. Li J., Pan Y., Xu Z., Wang Q., Hang D., Shen N., et al. Improved detection of human papillomavirus harbored in healthy skin with FAP6085/64 primers. JVirol Methods 2013, 193:633-638.
30. Ekström J., Mühr L.S., Bzhalava D., Söderlund-Strand A., Hultin E., Nordin P., et al. Diversity of human papillomaviruses in skin lesions. Virology 2013, 447:300-311.
31. Claus M.P., Lunardi M., Alfieri A.F., Ferracin L.M., Fungaro M.H., Alfieri A.A. Identification of unreported putative new bovine papillomavirus types in Brazilian cattle herds. Vet Microbiol 2008, 132:396-401.
32. Ure A.E., Elfadl A.K., Khalafalla A.I., Gameel A.A., Dillner J., Forslund O. Characterization of the complete genomes of Camelus dromedarius papillomavirus types 1 and 2. JGen Virol 2011, 92:1769-1777.
33. Stevens H., Heylen E., De Keyser K., Maes R., Kiupel M., Wise A., et al. Complete Genome Sequence of the Crocuta crocuta Papillomavirus Type 1 (CcrPV1) from a spotted hyena, the first papillomavirus characterized in a member of the Hyaenidae. Genome Announc 2013, 1. e00062-12.
34. Kocjan B.J., Hošnjak L., Račnik J., Zadravec M., Poljak M. Complete genome sequence of Phodopus sungorus Papillomavirus Type 1 (PsPV1), a novel member of the pipapillomavirus genus, isolated from a Siberian hamster. Genome Announc 2014, 2:e00311-e00314.
35. Munday J.S., Tucker R.S., Kiupel M., Harvey C.J. Multiple oral carcinomas associated with a novel papillomavirus in a dog. JVet Diagn Invest 2015, pii:1040638714567191. 10.1177/1040638714567191.
36. Marincevic-Zuniga Y., Gustavsson I., Gyllensten U. Multiply-primed rolling circle amplification of human papillomavirus using sequence-specific primers. Virology 2012, 432:57-62.
37. Johne R., Müller H., Rector A., van Ranst M., Stevens H. Rolling-circle amplification of viral DNA genomes using phi29 polymerase. Trends Microbiol 2009, 17:205-211.
38. Bzhalava D., Mühr L.S., Lagheden C., Ekström J., Forslund O., Dillner J., et al. Deep sequencing extends the diversity of human papillomaviruses in human skin. Sci Rep 2014, 4:5807.
39. Bahassi E.M., Stambrook P.J. Next-generation sequencing technologies: breaking the sound barrier of human genetics. Mutagenesis 2014, 29:303-331.
40. Huang T. Next generation sequencing to characterize mitochondrial genomic DNA heteroplasmy. Curr Protoc Hum Genet 2011, 71:19.8.1-19.8.12.
41. Ekström J., Bzhalava D., Svenback D., Forslund O., Dillner J. High throughput sequencing reveals diversity of human papillomaviruses in cutaneous lesions. Int J Cancer 2011, 129:2643-2650.
42. Arroyo Mühr L.S., Hultin E., Bzhalava D., Eklund C., Lagheden C., Ekström J., et al. Human papillomavirus type 197 is commonly present in skin tumors. Int J Cancer 2015, 136:2546-2555.
43. Bzhalava D., Johansson H., Ekström J., Faust H., Möller B., Eklund C., et al. Unbiased approach for virus detection in skin lesions. PLoS One 2013, 8:e65953.
44. Johansson H., Bzhalava D., Ekström J., Hultin E., Dillner J., Forslund O. Metagenomic sequencing of "HPV-negative" condylomas detects novel putative HPV types. Virology 2013, 440:1-7.
45. Phan T.G., Vo N.P., Aronen M., Jartti L., Jartti T., Delwart E. Novel human gammapapillomavirus species in a nasal swab. Genome Announc 2013, 2:e0002213.
46. Smits S.L., Schapendonk C.M., van Leeuwen M., Kuiken T., Bodewes R., Stalin Raj V., et al. Identification and characterization of two novel viruses in ocular infections in reindeer. PLoS One 2013, 8:e69711.
47. Canuti M., Deijs M., Jazaeri Farsani S.M., Holwerda M., Jebbink M.F., de Vries M., et al. Metagenomic analysis of a sample from a patient with respiratory tract infection reveals the presence of a γ-papillomavirus. Front Microbiol 2014, 5:347.
48. Varsani A., Porzig E.L., Jennings S., Kraberger S., Farkas K., Julian L., et al. Identification of an avian polyomavirus associated with Adélie penguins (Pygoscelis adeliae). JGen Virol 2014, pii:vir.0.000038. 10.1099/vir.0.000038.
49. Kim K.H., Bae J.W. Amplification methods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses. Appl Environ Microbiol 2011, 77:7663-7668.
50. Bzhalava D., Ekström J., Lysholm F., Hultin E., Faust H., Persson B., et al. Phylogenetically diverse TT virus viremia among pregnant women. Virology 2012, 432:427-434.
51. Binga E.K., Lasken R.S., Neufeld J.D. Something from (almost) nothing: the impact of multiple displacement amplification on microbial ecology. ISME J 2008, 2:233-241.
52. Lasken R.S. Genomic DNA amplification by the multiple displacement amplification (MDA) method. Biochem Soc Trans 2009, 37:450-453.
53. Yilmaz S., Allgaier M., Hugenholtz P. Multiple displacement amplification compromises quantitative analysis of metagenomes. Nat Methods 2010, 7:943-944.
54. Phan T.G., Kapusinszky B., Wang C., Rose R.K., Lipton H.L., Delwart E.L. The fecal viral flora of wild rodents. PLoS Pathog 2011, 7:e1002218.
55. Foulongne V., Sauvage V., Hebert C., Dereure O., Cheval J., Gouilh M.A. Human skin microbiota: high diversity of DNA viruses identified on the human skin by high throughput sequencing. PLoS One 2012, 7:e38499.
56. Tse H., Tsang A.K., Tsoi H.W., Leung A.S., Ho C.C., Lau S.K., et al. Identification of a novel bat papillomavirus by metagenomics. PLoS One 2012, 7:e43986.
57. Mokili J.L., Dutilh B.E., Lim Y.W., Schneider B.S., Taylor T., Haynes M.R., et al. Identification of a novel human papillomavirus by metagenomic analysis of samples from patients with febrile respiratory illness. PLoS One 2013, 8:e58404.
58. Yu J.M., Zhao G., Ao Y.Y., Li L.L., Wang D., Duan Z.J. Complete genome sequence of a novel human papillomavirus identified by metagenomic analysis from a child with diarrhea in China. Arch Virol 2015, 160:549-552.
59. Kocjan B.J., Poljak M., Seme K., Potocnik M., Fujs K., Babic D.Z. Distribution of human papillomavirus genotypes in plucked eyebrow hairs from Slovenian males with genital warts. Infect Genet Evol 2005, 5:255-259.
60. Kovanda A., Kocjan B.J., Luzar B., Bravo I.G., Poljak M. Characterization of novel cutaneous human papillomavirus genotypes HPV-150 and HPV-151. PLoS One 2011, 6:e22529.
61. Bottalico D., Chen Z., Kocjan B.J., Seme K., Poljak M., Burk R.D. Characterization of human papillomavirus type 120: a novel betapapillomavirus with tropism for multiple anatomical niches. JGen Virol 2012, 93:1774-1779.
62. Potočnik M., Kocjan B.J., Seme K., Luzar B., Babic D.Z., Poljak M. Beta-papillomaviruses in anogenital hairs plucked from healthy individuals. JMed Virol 2006, 78:1673-1678.
63. Kocjan B.J., Hosnjak L., Seme K., Poljak M. Complete genome sequence of a novel human betapapillomavirus, HPV-159. Genome Announc 2013, 1. e00298-13.
64. Kocjan B.J., Steyer A., Sagadin M., Hosnjak L., Poljak M. Novel human papillomavirus type 174 from a cutaneous squamous cell carcinoma. Genome Announc 2013, 1. e00445-13.
65. Iwasaki T., Maeda H., Kameyama Y., Moriyama M., Kanai S., Kurata T. Presence of a novel hamster oral papillomavirus in dysplastic lesions of hamster lingual mucosa induced by application of dimethylbenzanthracene and excisional wounding: molecular cloning and complete nucleotide sequence. JGen Virol 1997, 78:1087-1093.
66. Sturegård E., Johansson H., Ekström J., Hansson B.G., Johnsson A., Gustafsson E., et al. Human papillomavirus typing in reporting of condyloma. Sex Transm Dis 2013, 40:123-129.
67. Ure A.E., Forslund O. Characterization of human papillomavirus type 154 and tissue tropism of gammapapillomaviruses. PLoS One 2014, 9:e89342.
68. Antonsson A., Karanfilovska S., Lindqvist P.G., Hansson B.G. General acquisition of human papillomavirus infections of skin occurs in early infancy. JClin Microbiol 2003, 41:2509-2514.
69. Johansson H., Forslund O. Complete genome sequences of three novel human papillomavirus types, 175, 178, and 180. Genome Announc 2014, 2. e00443-14.
70. Chen Z., de Freitas L.B., Burk R.D. Evolution and classification of oncogenic human papillomavirus types and variants associated with cervical cancer. Methods Mol Biol 2015, 1249:3-26.
71. Eklund C., Zhou T., Dillner J. Global proficiency study of human papillomavirus genotyping. WHO Human Papillomavirus Laboratory Network. JClin Microbiol 2010, 48:4147-4155.
72. Eklund C., Forslund O., Wallin K.L., Dillner J. Global improvement in genotyping of human papillomavirus DNA: the 2011 HPV LabNet International Proficiency Study. JClin Microbiol 2014, 52:449-459.
73. Köhler A., Gottschling M., Manning K., Lehmann M.D., Schulz E., Krüger-Corcoran D., et al. Genomic characterization of ten novel cutaneous human papillomaviruses from keratotic lesions of immunosuppressed patients. JGen Virol 2011, 92:1585-1594.
74. Vasiljević N., Hazard K., Dillner J., Forslund O. Four novel human betapapillomaviruses of species 2 preferentially found in actinic keratosis. JGen Virol 2008, 89:2467-2474.
75. Vasiljević N., Hazard K., Eliasson L., Ly H., Hunziker A., de Villiers E.M., et al. Characterization of two novel cutaneous human papillomaviruses, HPV93 and HPV96. JGen Virol 2007, 88:1479-1483.
76. de Villiers E.M., Gunst K. Characterization of seven novel human papillomavirus types isolated from cutaneous tissue, but also present in mucosal lesions. JGen Virol 2009, 90:1999-2004.
77. Ekstrom J., Forslund O., Dillner J. Three novel papillomaviruses (HPV109, HPV112 and HPV114) and their presence in cutaneous and mucosal samples. Virology 2010, 397:331-336.
78. Forslund O., Antonsson A., Higgins G., Ly H., Delius H., Hunziker A., et al. Nucleotide sequence and phylogenetic classification of candidate human papilloma virus type 92. Virology 2003, 312:255-260.