Multiplex Identification of Human Papillomavirus 16 DNA Integration Sites in Cervical Carcinomas

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Xu, Bo ^a   Chotewutmontri, Sasithorn ^a   Wolf, Stephan ^a   Klos, Ursula ^a   Schmitz, Martina ^b,c   Dürst, Matthias ^b   Schwarz, Elisabeth ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b JENA UNIVERSITY HOSPITAL   (Germany)

^c Oncgnostics GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; VIRUS DNA;

3' UNTRANSLATED REGION; ADULT; AGED; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; DNA FRAGMENTATION; DNA INTEGRATION; DNA REPLICATION; DNA TRANSPOSITION; EARLY DIAGNOSIS; EPISOME; GENE EXPRESSION REGULATION; GENE LOCUS; GENE MAPPING; GENE SEQUENCE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN TISSUE; INTRON; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; POLYMERASE CHAIN REACTION; RESTRICTION SITE; UTERINE CERVIX CARCINOMA; ALPHAPAPILLOMAVIRUS; FEMALE; GENETICS; HIGH THROUGHPUT SEQUENCING; SITE DIRECTED MUTAGENESIS; UTERINE CERVIX TUMOR; VIROLOGY; VIRUS DNA CELL DNA INTERACTION;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS - 16; HUMAN PAPILLOMAVIRUS TYPE 16; PAPILLOMAVIRIDAE;

ALPHAPAPILLOMAVIRUS; DNA, VIRAL; FEMALE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MUTAGENESIS, SITE-DIRECTED; UTERINE CERVICAL NEOPLASMS; VIRUS INTEGRATION;

EID: 84879135702     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066693     Document Type: Article

References (77)

1. Schiffman M, Castle PE, Jeronimo J, Rodriguez AC, Wacholder S, (2007) Human papillomavirus and cervical cancer. Lancet 370: 890-907.
2. Arbyn M, Castellsague X, de Sanjose S, Bruni L, Saraiya M, et al. (2011) Worldwide burden of cervical cancer in 2008. Annals of oncology: official journal of the European Society for Medical Oncology/ESMO 22: 2675-2686.
3. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, et al. (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. International journal of cancer 127: 2893-2917.
4. Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, et al. (2009) A review of human carcinogens-Part B: biological agents. Lancet Oncol 10: 321-322.
5. Castellsague X, (2008) Natural history and epidemiology of HPV infection and cervical cancer. Gynecol Oncol 110: S4-7.
6. de Sanjose S, Quint WG, Alemany L, Geraets DT, Klaustermeier JE, et al. (2010) Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol 11: 1048-1056.
7. Li N, Franceschi S, Howell-Jones R, Snijders PJ, Clifford GM, (2011) Human papillomavirus type distribution in 30,848 invasive cervical cancers worldwide: Variation by geographical region, histological type and year of publication. International journal of cancer 128: 927-935.
8. Yamada T, Wheeler CM, Halpern AL, Stewart AC, Hildesheim A, et al. (1995) Human papillomavirus type 16 variant lineages in United States populations characterized by nucleotide sequence analysis of the E6, L2, and L1 coding segments. J Virol 69: 7743-7753.
9. Casas L, Galvan SC, Ordonez RM, Lopez N, Guido M, et al. (1999) Asian-american variants of human papillomavirus type 16 have extensive mutations in the E2 gene and are highly amplified in cervical carcinomas. Int J Cancer 83: 449-455.
10. Richard C, Lanner C, Naryzhny SN, Sherman L, Lee H, et al. (2010) The immortalizing and transforming ability of two common human papillomavirus 16 E6 variants with different prevalences in cervical cancer. Oncogene 29: 3435-3445.
11. Howie HL, Katzenellenbogen RA, Galloway DA, (2009) Papillomavirus E6 proteins. Virology 384: 324-334.
12. McLaughlin-Drubin ME, Munger K, (2009) The human papillomavirus E7 oncoprotein. Virology 384: 335-344.
13. Moody CA, Laimins LA, (2010) Human papillomavirus oncoproteins: pathways to transformation. Nat Rev Cancer 10: 550-560.
14. Doorbar J, (2006) Molecular biology of human papillomavirus infection and cervical cancer. Clin Sci (Lond) 110: 525-541.
15. Bodily J, Laimins LA, (2011) Persistence of human papillomavirus infection: keys to malignant progression. Trends Microbiol 19: 33-39.
16. Snijders PJ, Steenbergen RD, Heideman DA, Meijer CJ, (2006) HPV-mediated cervical carcinogenesis: concepts and clinical implications. J Pathol 208: 152-164.
17. Badaracco G, Venuti A, Sedati A, Marcante ML, (2002) HPV16 and HPV18 in genital tumors: Significantly different levels of viral integration and correlation to tumor invasiveness. J Med Virol 67: 574-582.
18. Hopman AH, Smedts F, Dignef W, Ummelen M, Sonke G, et al. (2004) Transition of high-grade cervical intraepithelial neoplasia to micro-invasive carcinoma is characterized by integration of HPV 16/18 and numerical chromosome abnormalities. J Pathol 202: 23-33.
19. Boshart M, Gissmann L, Ikenberg H, Kleinheinz A, Scheurlen W, et al. (1984) A new type of papillomavirus DNA, its presence in genital cancer biopsies and in cell lines derived from cervical cancer. Embo J 3: 1151-1157.
20. Corden SA, Sant-Cassia LJ, Easton AJ, Morris AG, (1999) The integration of HPV-18 DNA in cervical carcinoma. Mol Pathol 52: 275-282.
21. Klaes R, Woerner SM, Ridder R, Wentzensen N, Duerst M, et al. (1999) Detection of high-risk cervical intraepithelial neoplasia and cervical cancer by amplification of transcripts derived from integrated papillomavirus oncogenes. Cancer Res 59: 6132-6136.
22. Schwarz E, Freese UK, Gissmann L, Mayer W, Roggenbuck B, et al. (1985) Structure and transcription of human papillomavirus sequences in cervical carcinoma cells. Nature 314: 111-114.
23. Pett M, Coleman N, (2007) Integration of high-risk human papillomavirus: a key event in cervical carcinogenesis? J Pathol 212: 356-367.
24. Gray E, Pett MR, Ward D, Winder DM, Stanley MA, et al. (2010) In vitro progression of human papillomavirus 16 episome-associated cervical neoplasia displays fundamental similarities to integrant-associated carcinogenesis. Cancer Res 70: 4081-4091.
25. Wagatsuma M, Hashimoto K, Matsukura T, (1990) Analysis of integrated human papillomavirus type 16 DNA in cervical cancers: amplification of viral sequences together with cellular flanking sequences. J Virol 64: 813-821.
26. Baker CC, Phelps WC, Lindgren V, Braun MJ, Gonda MA, et al. (1987) Structural and transcriptional analysis of human papillomavirus type 16 sequences in cervical carcinoma cell lines. J Virol 61: 962-971.
27. Van Tine BA, Kappes JC, Banerjee NS, Knops J, Lai L, et al. (2004) Clonal selection for transcriptionally active viral oncogenes during progression to cancer. J Virol 78: 11172-11186.
28. Kraus I, Driesch C, Vinokurova S, Hovig E, Schneider A, et al. (2008) The majority of viral-cellular fusion transcripts in cervical carcinomas cotranscribe cellular sequences of known or predicted genes. Cancer Res 68: 2514-2522.
29. Schneider-Gadicke A, Schwarz E, (1986) Different human cervical carcinoma cell lines show similar transcription patterns of human papillomavirus type 18 early genes. Embo J 5: 2285-2292.
30. Wentzensen N, Ridder R, Klaes R, Vinokurova S, Schaefer U, et al. (2002) Characterization of viral-cellular fusion transcripts in a large series of HPV16 and 18 positive anogenital lesions. Oncogene 21: 419-426.
31. Jeon S, Lambert PF, (1995) Integration of human papillomavirus type 16 DNA into the human genome leads to increased stability of E6 and E7 mRNAs: implications for cervical carcinogenesis. Proc Natl Acad Sci U S A 92: 1654-1658.
32. Bechtold V, Beard P, Raj K, (2003) Human papillomavirus type 16 E2 protein has no effect on transcription from episomal viral DNA. J Virol 77: 2021-2028.
33. Romanczuk H, Howley PM, (1992) Disruption of either the E1 or the E2 regulatory gene of human papillomavirus type 16 increases viral immortalization capacity. Proc Natl Acad Sci U S A 89: 3159-3163.
34. Kalantari M, Karlsen F, Kristensen G, Holm R, Hagmar B, et al. (1998) Disruption of the E1 and E2 reading frames of HPV 16 in cervical carcinoma is associated with poor prognosis. Int J Gynecol Pathol 17: 146-153.
35. Vernon SD, Unger ER, Miller DL, Lee DR, Reeves WC, (1997) Association of human papillomavirus type 16 integration in the E2 gene with poor disease-free survival from cervical cancer. Int J Cancer 74: 50-56.
36. Popescu NC, DiPaolo JA, (1989) Preferential sites for viral integration on mammalian genome. Cancer Genet Cytogenet 42: 157-171.
37. Thorland EC, Myers SL, Gostout BS, Smith DI, (2003) Common fragile sites are preferential targets for HPV16 integrations in cervical tumors. Oncogene 22: 1225-1237.
38. Wentzensen N, Vinokurova S, von Knebel Doeberitz M, (2004) Systematic review of genomic integration sites of human papillomavirus genomes in epithelial dysplasia and invasive cancer of the female lower genital tract. Cancer Res 64: 3878-3884.
39. Couturier J, Sastre-Garau X, Schneider-Maunoury S, Labib A, Orth G, (1991) Integration of papillomavirus DNA near myc genes in genital carcinomas and its consequences for proto-oncogene expression. J Virol 65: 4534-4538.
40. Durst M, Croce CM, Gissmann L, Schwarz E, Huebner K, (1987) Papillomavirus sequences integrate near cellular oncogenes in some cervical carcinomas. Proc Natl Acad Sci U S A 84: 1070-1074.
41. Ferber MJ, Thorland EC, Brink AA, Rapp AK, Phillips LA, et al. (2003) Preferential integration of human papillomavirus type 18 near the c-myc locus in cervical carcinoma. Oncogene 22: 7233-7242.
42. Peter M, Rosty C, Couturier J, Radvanyi F, Teshima H, et al. (2006) MYC activation associated with the integration of HPV DNA at the MYC locus in genital tumors. Oncogene 25: 5985-5993.
43. Reuter S, Bartelmann M, Vogt M, Geisen C, Napierski I, et al. (1998) APM-1, a novel human gene, identified by aberrant co-transcription with papillomavirus oncogenes in a cervical carcinoma cell line, encodes a BTB/POZ-zinc finger protein with growth inhibitory activity. Embo J 17: 215-222.
44. Schmitz M, Driesch C, Beer-Grondke K, Jansen L, Runnebaum IB, et al. (2012) Loss of gene function as a consequence of human papillomavirus DNA integration. International journal of cancer 131: E593-602.
45. Ziegert C, Wentzensen N, Vinokurova S, Kisseljov F, Einenkel J, et al. (2003) A comprehensive analysis of HPV integration loci in anogenital lesions combining transcript and genome-based amplification techniques. Oncogene 22: 3977-3984.
46. Ferber MJ, Montoya DP, Yu C, Aderca I, McGee A, et al. (2003) Integrations of the hepatitis B virus (HBV) and human papillomavirus (HPV) into the human telomerase reverse transcriptase (hTERT) gene in liver and cervical cancers. Oncogene 22: 3813-3820.
47. Thorland EC, Myers SL, Persing DH, Sarkar G, McGovern RM, et al. (2000) Human papillomavirus type 16 integrations in cervical tumors frequently occur in common fragile sites. Cancer Res 60: 5916-5921.
48. Luft F, Klaes R, Nees M, Durst M, Heilmann V, et al. (2001) Detection of integrated papillomavirus sequences by ligation-mediated PCR (DIPS-PCR) and molecular characterization in cervical cancer cells. Int J Cancer 92: 9-17.
49. Kalantari M, Blennow E, Hagmar B, Johansson B, (2001) Physical state of HPV16 and chromosomal mapping of the integrated form in cervical carcinomas. Diagn Mol Pathol 10: 46-54.
50. Schmitz M, Driesch C, Jansen L, Runnebaum IB, Durst M, (2012) Non-random integration of the HPV genome in cervical cancer. PLoS One 7: e39632.
51. Adey A, Morrison HG, Asan, Xun X, Kitzman JO, et al. (2010) Rapid, low-input, low-bias construction of shotgun fragment libraries by high-density in vitro transposition. Genome Biol 11: R119.
52. Caruccio N, (2011) Preparation of next-generation sequencing libraries using Nextera technology: simultaneous DNA fragmentation and adaptor tagging by in vitro transposition. Methods in molecular biology 733: 241-255.
53. Yee C, Krishnan-Hewlett I, Baker CC, Schlegel R, Howley PM, (1985) Presence and expression of human papillomavirus sequences in human cervical carcinoma cell lines. Am J Pathol 119: 361-366.
54. Smits HL, Cornelissen MT, Jebbink MF, van den Tweel JG, Struyk AP, et al. (1991) Human papillomavirus type 16 transcripts expressed from viral-cellular junctions and full-length viral copies in CaSki cells and in a cervical carcinoma. Virology 182: 870-873.
55. Cornet I, Gheit T, Franceschi S, Vignat J, Burk RD, et al. (2012) Human papillomavirus type 16 genetic variants: phylogeny and classification based on E6 and LCR. J Virol 86: 6855-6861.
56. Swan DC, Rajeevan M, Tortolero-Luna G, Follen M, Tucker RA, et al. (2005) Human papillomavirus type 16 E2 and E6/E7 variants. Gynecol Oncol 96: 695-700.
57. Yamada T, Manos MM, Peto J, Greer CE, Munoz N, et al. (1997) Human papillomavirus type 16 sequence variation in cervical cancers: a worldwide perspective. J Virol 71: 2463-2472.
58. Zehbe I, Wilander E, Delius H, Tommasino M, (1998) Human papillomavirus 16 E6 variants are more prevalent in invasive cervical carcinoma than the prototype. Cancer Res 58: 829-833.
59. Grodzki M, Besson G, Clavel C, Arslan A, Franceschi S, et al. (2006) Increased risk for cervical disease progression of French women infected with the human papillomavirus type 16 E6-350G variant. Cancer Epidemiol Biomarkers Prev 15: 820-822.
60. el Awady MK, Kaplan JB, O'Brien SJ, Burk RD, (1987) Molecular analysis of integrated human papillomavirus 16 sequences in the cervical cancer cell line SiHa. Virology 159: 389-398.
61. Mincheva A, Gissmann L, zur Hausen H, (1987) Chromosomal integration sites of human papillomavirus DNA in three cervical cancer cell lines mapped by in situ hybridization. Med Microbiol Immunol 176: 245-256.
62. Peter M, Stransky N, Couturier J, Hupe P, Barillot E, et al. (2010) Frequent genomic structural alterations at HPV insertion sites in cervical carcinoma. J Pathol 221: 320-330.
63. Yu T, Ferber MJ, Cheung TH, Chung TK, Wong YF, et al. (2005) The role of viral integration in the development of cervical cancer. Cancer Genet Cytogenet 158: 27-34.
64. Einstein MH, Cruz Y, El-Awady MK, Popescu NC, DiPaolo JA, et al. (2002) Utilization of the human genome sequence localizes human papillomavirus type 16 DNA integrated into the TNFAIP2 gene in a fatal cervical cancer from a 39-year-old woman. Clin Cancer Res 8: 549-554.
65. Krivega I, Dean A, (2012) Enhancer and promoter interactions-long distance calls. Curr Opin Genet Dev 22: 79-85.
66. Stratton MR, (2011) Exploring the genomes of cancer cells: progress and promise. Science 331: 1553-1558.
67. Zhao X, Liu Q, Cai Q, Li Y, Xu C, et al. (2012) Dr.VIS: a database of human disease-related viral integration sites. Nucleic Acids Res 40: D1041-1046.
68. Gadducci A, Guerrieri ME, Greco C, (2013) Tissue biomarkers as prognostic variables of cervical cancer. Crit Rev Oncol Hematol 86: 104-129.
69. Campitelli M, Jeannot E, Peter M, Lappartient E, Saada S, et al. (2012) Human papillomavirus mutational insertion: specific marker of circulating tumor DNA in cervical cancer patients. PLoS One 7: e43393.
70. Schmitz M, Scheungraber C, Herrmann J, Teller K, Gajda M, et al. (2009) Quantitative multiplex PCR assay for the detection of the seven clinically most relevant high-risk HPV types. J Clin Virol 44: 302-307.
71. Seedorf K, Krammer G, Durst M, Suhai S, Rowekamp WG, (1985) Human papillomavirus type 16 DNA sequence. Virology 145: 181-185.
72. Van Doorslaer K, Tan Q, Xirasagar S, Bandaru S, Gopalan V, et al. (2013) The Papillomavirus Episteme: a central resource for papillomavirus sequence data and analysis. Nucleic Acids Res 41: D571-578.
73. Li H, Durbin R, (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
74. Li H, Durbin R, (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26: 589-595.
75. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
76. Thorvaldsdottir H, Robinson JT, Mesirov JP, (2013) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14: 178-192.
77. Kohany O, Gentles AJ, Hankus L, Jurka J, (2006) Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics 7: 474.