Mobile elements and viral integrations prompt considerations for bacterial DNA integration as a novel carcinogen

Cancer Letters

Volumn 352, Issue 2, 2014, Pages 137-144

  Robinson, Kelly M ^a   Dunning Hotopp, Julie C ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Bacteria; Lateral gene transfer; Mobile elements; Parasites; Viruses

Indexed keywords

BACTERIAL DNA; CARCINOGEN; VIRUS DNA;

ALU SEQUENCE; CANCER RISK; CARCINOGENESIS; DNA INTEGRATION; DNA REPAIR; EPSTEIN BARR VIRUS; GENE INSERTION; GENE MUTATION; GENE SEQUENCE; GENE TRANSFER; GENETIC ASSOCIATION; HEPATITIS B VIRUS; HUMAN; LEUKEMIA; LONG INTERSPERSED REPEAT; MERKEL CELL POLYOMAVIRUS; NONHUMAN; PRIORITY JOURNAL; RISK REDUCTION; SHORT INTERSPERSED REPEAT; SHORT SURVEY; VARIABLE NUMBER OF TANDEM REPEAT; VIRAL INTEGRATION; VIRAL PHENOMENA AND FUNCTIONS; WART VIRUS;

BACTERIA (MICROORGANISMS); BACTEROIDES FRAGILIS; HELICOBACTER PYLORI; HEPATITIS B VIRUS; HUMAN HERPESVIRUS 4; HUMAN PAPILLOMAVIRUS; POLYOMAVIRUS;

BACTERIA; LATERAL GENE TRANSFER; MOBILE ELEMENTS; PARASITES; VIRUSES;

ANIMALS; BACTERIAL INFECTIONS; CELL TRANSFORMATION, VIRAL; DNA, BACTERIAL; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INTERSPERSED REPETITIVE SEQUENCES; MUTAGENESIS, INSERTIONAL; NEOPLASMS; PHENOTYPE; RISK FACTORS; TUMOR VIRUS INFECTIONS; VIRUS INTEGRATION;

EID: 84906053075     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.05.021     Document Type: Review

References (133)

1. Abend J.R., Jiang M., Imperiale M.J. BK virus and human cancer: innocent until proven guilty. Semin. Cancer Biol. 2009, 19:252-260.
2. Ansari K.I., Mandal S.S. Mixed lineage leukemia: roles in gene expression, hormone signaling and mRNA processing. FEBS J. 2010, 277:1790-1804.
3. Arzumanyan A., Reis H.M., Feitelson M.A. Pathogenic mechanisms in HBV- and HCV-associated hepatocellular carcinoma. Nat. Rev. Cancer 2013, 13:123-135.
4. Astier Y., Braha O., Bayley H. Toward single molecule DNA sequencing: direct identification of ribonucleoside and deoxyribonucleoside 5'-monophosphates by using an engineered protein nanopore equipped with a molecular adapter. J. Am. Chem. Soc. 2006, 128:1705-1710.
5. Beal M.A., Glenn T.C., Somers C.M. Whole genome sequencing for quantifying germline mutation frequency in humans and model species: cautious optimism. Mutat. Res. 2012, 750:96-106.
6. Bechtold V., Beard P., Raj K. Human papillomavirus type 16 E2 protein has no effect on transcription from episomal viral DNA. J. Virol. 2003, 77:2021-2028.
7. Beiko R.G., Harlow T.J., Ragan M.A. Highways of gene sharing in prokaryotes. Proc. Natl. Acad. Sci. USA 2005, 102:14332-14337.
8. Benard A., van de Velde C.J., Lessard L., Putter H., Takeshima L., Kuppen P.J., Hoon D.S. Epigenetic status of LINE-1 predicts clinical outcome in early-stage rectal cancer. Br. J. Cancer 2013, 109:3073-3083.
9. Benchimol S., Fuks A., Jothy S., Beauchemin N., Shirota K., Stanners C.P. Carcinoembryonic antigen, a human tumor marker, functions as an intercellular adhesion molecule. Cell 1989, 57:327-334.
10. Biarc J., Nguyen I.S., Pini A., Gosse F., Richert S., Thierse D., Van Dorsselaer A., Leize-Wagner E., Raul F., Klein J.P., Scholler-Guinard M. Carcinogenic properties of proteins with pro-inflammatory activity from Streptococcus infantarius (formerly S.bovis). Carcinogenesis 2004, 25:1477-1484.
11. Boyer S.N., Wazer D.E., Band V. E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res. 1996, 56:4620-4624.
12. Brechot C., Pourcel C., Louise A., Rain B., Tiollais P. Presence of integrated hepatitis B virus DNA sequences in cellular DNA of human hepatocellular carcinoma. Nature 1980, 286:533-535.
13. Brouha B., Schustak J., Badge R.M., Lutz-Prigge S., Farley A.H., Moran J.V., Kazazian H.H. Hot L1s account for the bulk of retrotransposition in the human population. Proc. Natl. Acad. Sci. USA 2003, 100:5280-5285.
14. Carreira P.E., Richardson S.R., Faulkner G.J. L1 retrotransposons, cancer stem cells and oncogenesis. FEBS J. 2014, 281:63-73.
15. Castellarin M., Warren R.L., Freeman J.D., Dreolini L., Krzywinski M., Strauss J., Barnes R., Watson P., Allen-Vercoe E., Moore R.A., Holt R.A. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res. 2012, 22:299-306.
16. Chakraborty P.R., Ruiz-Opazo N., Shouval D., Shafritz D.A. Identification of integrated hepatitis B virus DNA and expression of viral RNA in an HBsAg-producing human hepatocellular carcinoma cell line. Nature 1980, 286:531-533.
17. Corden S.A., Sant-Cassia L.J., Easton A.J., Morris A.G. The integration of HPV-18 DNA in cervical carcinoma. Mol. Pathol. 1999, 52:275-282.
18. Das P., Thomas A., Mahantshetty U., Shrivastava S.K., Deodhar K., Mulherkar R. HPV genotyping and site of viral integration in cervical cancers in Indian women. PLoS ONE 2012, 7:e41012.
19. de Martel C., Ferlay J., Franceschi S., Vignat J., Bray F., Forman D., Plummer M. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol. 2008, 13(2012):607-615.
20. Dunning Hotopp J.C. Horizontal gene transfer between bacteria and animals. Trends Genet. 2011, 27:157-163.
21. Dunning Hotopp J.C. Lateral gene transfer in multicellular organisms. Lateral Gene Transfer in Evolution 2013, 161-179. Springer Science. U. Gophna (Ed.).
22. Dunning Hotopp J.C., Clark M.E., Oliveira D.C., Foster J.M., Fischer P., Munoz Torres M.C., Giebel J.D., Kumar N., Ishmael N., Wang S., Ingram J., Nene R.V., Shepard J., Tomkins J., Richards S., Spiro D.J., Ghedin E., Slatko B.E., Tettelin H., Werren J.H. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 2007, 317:1753-1756.
23. Dutta U., Garg P.K., Kumar R., Tandon R.K. Typhoid carriers among patients with gallstones are at increased risk for carcinoma of the gallbladder. Am. J. Gastroenterol. 2000, 95:784-787.
24. Edman J.C., Gray P., Valenzuela P., Rall L.B., Rutter W.J. Integration of hepatitis B virus sequences and their expression in a human hepatoma cell. Nature 1980, 286:535-538.
25. Edwards T.G., Helmus M.J., Koeller K., Bashkin J.K., Fisher C. Human papillomavirus episome stability is reduced by aphidicolin and controlled by DNA damage response pathways. J. Virol. 2013, 87:3979-3989.
26. Elinav E., Nowarski R., Thaiss C.A., Hu B., Jin C., Flavell R.A. Inflammation-induced cancer: crosstalk between tumours, immune cells and microorganisms. Nat. Rev. Cancer 2013, 13:759-771.
27. Feitelson M.A., Duan L.X. Hepatitis B virus X antigen in the pathogenesis of chronic infections and the development of hepatocellular carcinoma. Am. J. Pathol. 1997, 150:1141-1157.
28. Feitelson M.A., Lee J. Hepatitis B virus integration, fragile sites, and hepatocarcinogenesis. Cancer Lett. 2007, 252:157-170.
29. Feng H., Shuda M., Chang Y., Moore P.S. Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 2008, 319:1096-1100.
30. Fried B., Reddy A., Mayer D. Helminths in human carcinogenesis. Cancer Lett. 2011, 305:239-249.
31. Gold D.V., Stein R., Burton J., Goldenberg D.M. Enhanced expression of CD74 in gastrointestinal cancers and benign tissues. Int. J. Clin. Exp. Pathol. 2010, 4:1-12.
32. Goldstein M.J., Mitchell E.P. Carcinoembryonic antigen in the staging and follow-up of patients with colorectal cancer. Cancer Invest. 2005, 23:338-351.
33. Gozuacik D., Murakami Y., Saigo K., Chami M., Mugnier C., Lagorce D., Okanoue T., Urashima T., Brechot C., Paterlini-Brechot P. Identification of human cancer-related genes by naturally occurring Hepatitis B Virus DNA tagging. Oncogene 2001, 20:6233-6240.
34. Gubanova E., Brown B., Ivanov S.V., Helleday T., Mills G.B., Yarbrough W.G., Issaeva N. Downregulation of SMG-1 in HPV-positive head and neck squamous cell carcinoma due to promoter hypermethylation correlates with improved survival. Clin. Cancer Res. 2012, 18:1257-1267.
35. Hacker G., Redecke V., Hacker H. Activation of the immune system by bacterial CpG-DNA. Immunology 2002, 105:245-251.
36. Hadler H.I., Devadas K., Mahalingam R. Selected nuclear LINE elements with mitochondrial-DNA-like inserts are more plentiful and mobile in tumor than in normal tissue of mouse and rat. J. Cell. Biochem. 1998, 68:100-109.
37. Han S.U., Kwak T.H., Her K.H., Cho Y.H., Choi C., Lee H.J., Hong S., Park Y.S., Kim Y.S., Kim T.A., Kim S.J. CEACAM5 and CEACAM6 are major target genes for Smad3-mediated TGF-beta signaling. Oncogene 2008, 27:675-683.
38. Hancks D.C., Kazazian H.H. Active human retrotransposons: variation and disease. Curr. Opin. Genet. Dev. 2012, 22:191-203.
39. Henkler F., Koshy R. Hepatitis B virus transcriptional activators: mechanisms and possible role in oncogenesis. J. Viral Hepatitis 1996, 3:109-121.
40. Hohne M., Schaefer S., Seifer M., Feitelson M.A., Paul D., Gerlich W.H. Malignant transformation of immortalized transgenic hepatocytes after transfection with hepatitis B virus DNA. EMBO J. 1990, 9:1137-1145.
41. Hollingsworth R.E., Chen P.L., Lee W.H. Integration of cell cycle control with transcriptional regulation by the retinoblastoma protein. Curr. Opin. Cell Biol. 1993, 5:194-200.
42. Husnik F., Nikoh N., Koga R., Ross L., Duncan R.P., Fujie M., Tanaka M., Satoh N., Bachtrog D., Wilson A.C., von Dohlen C.D., Fukatsu T., McCutcheon J.P. Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 2013, 153:1567-1578.
43. Ilantzis C., Demarte L., Screaton R.A., Stanners C.P. Deregulated expression of the human tumor marker CEA and CEA family member CEACAM6 disrupts tissue architecture and blocks colonocyte differentiation. Neoplasia 2002, 4:151-163.
44. Iskow R.C., McCabe M.T., Mills R.E., Torene S., Pittard W.S., Neuwald A.F., Van Meir E.G., Vertino P.M., Devine S.E. Natural mutagenesis of human genomes by endogenous retrotransposons. Cell 2010, 141:1253-1261.
45. Kazazian H.H., Wong C., Youssoufian H., Scott A.F., Phillips D.G., Antonarakis S.E. Haemophilia A resulting from de novo insertion of L1 sequences represents a novel mechanism for mutation in man. Nature 1988, 332:164-166.
46. Khaiboullina S.F., Morzunov S.P., Hall M.R., De Meirleir K.L., Rizvanov A.A., Lombardi V.C. Human dendritic cells transfected with a human papilloma virus-18 construct display decreased mobility and upregulated cytokine production. Int. J. Oncol. 2013, 43:1701-1709.
47. Kim C.M., Koike K., Saito I., Miyamura T., Jay G. HBx gene of hepatitis B virus induces liver cancer in transgenic mice. Nature 1991, 351:317-320.
48. Kim S.S., Ruiz V.E., Carroll J.D., Moss S.F. Helicobacter pylori in the pathogenesis of gastric cancer and gastric lymphoma. Cancer Lett. 2011, 305:228-238.
49. Klein G. The role of gene dosage and genetic transpositions in carcinogenesis. Nature 1981, 294:313-318.
50. Koike K., Moriya K., Iino S., Yotsuyanagi H., Endo Y., Miyamura T., Kurokawa K. High-level expression of hepatitis B virus HBx gene and hepatocarcinogenesis in transgenic mice. Hepatology 1994, 19:810-819.
51. Konkel M.K., Batzer M.A. A mobile threat to genome stability: the impact of non-LTR retrotransposons upon the human genome. Semin. Cancer Biol. 2010, 20:211-221.
52. Kostic A.D., Chun E., Robertson L., Glickman J.N., Gallini C.A., Michaud M., Clancy T.E., Chung D.C., Lochhead P., Hold G.L., El-Omar E.M., Brenner D., Fuchs C.S., Meyerson M., Garrett W.S. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 2013, 14:207-215.
53. Kostic A.D., Gevers D., Pedamallu C.S., Michaud M., Duke F., Earl A.M., Ojesina A.I., Jung J., Bass A.J., Tabernero J., Baselga J., Liu C., Shivdasani R.A., Ogino S., Birren B.W., Huttenhower C., Garrett W.S., Meyerson M. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res. 2012, 22:292-298.
54. Kuespert K., Pils S., Hauck C.R. CEACAMs: their role in physiology and pathophysiology. Curr. Opin. Cell Biol. 2006, 18:565-571.
55. Kunik T., Tzfira T., Kapulnik Y., Gafni Y., Dingwall C., Citovsky V. Genetic transformation of HeLa cells by Agrobacterium. Proc. Natl. Acad. Sci. USA 2001, 98:1871-1876.
56. Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C., Baldwin J., Devon K., Dewar K., Doyle M., FitzHugh W., Funke R., Gage D., Harris K., Heaford A., Howland J., Kann L., Lehoczky J., LeVine R., McEwan P., McKernan K., Meldrim J., Mesirov J.P., Miranda C., Morris W., Naylor J., Raymond C., Rosetti M., Santos R., Sheridan A., Sougnez C., Stange-Thomann N., Stojanovic N., Subramanian A., Wyman D., Rogers J., Sulston J., Ainscough R., Beck S., Bentley D., Burton J., Clee C., Carter N., Coulson A., Deadman R., Deloukas P., Dunham A., Dunham I., Durbin R., French L., Grafham D., Gregory S., Hubbard T., Humphray S., Hunt A., Jones M., Lloyd C., McMurray A., Matthews L., Mercer S., Milne S., Mullikin J.C., Mungall A., Plumb R., Ross M., Shownkeen R., Sims S., Waterston R.H., Wilson R.K., Hillier L.W., McPherson J.D., Marra M.A., Mardis E.R., Fulton L.A., Chinwalla A.T., Pepin K.H., Gish W.R., Chissoe S.L., Wendl M.C., Delehaunty K.D., Miner T.L., Delehaunty A., Kramer J.B., Cook L.L., Fulton R.S., Johnson D.L., Minx P.J., Clifton S.W., Hawkins T., Branscomb E., Predki P., Richardson P., Wenning S., Slezak T., Doggett N., Cheng J.F., Olsen A., Lucas S., Elkin C., Uberbacher E., Frazier M., Gibbs R.A., Muzny D.M., Scherer S.E., Bouck J.B., Sodergren E.J., Worley K.C., Rives C.M., Gorrell J.H., Metzker M.L., Naylor S.L., Kucherlapati R.S., Nelson D.L., Weinstock G.M., Sakaki Y., Fujiyama A., Hattori M., Yada T., Toyoda A., Itoh T., Kawagoe C., Watanabe H., Totoki Y., Taylor T., Weissenbach J., Heilig R., Saurin W., Artiguenave F., Brottier P., Bruls T., Pelletier E., Robert C., Wincker P., Smith D.R., Doucette-Stamm L., Rubenfield M., Weinstock K., Lee H.M., Dubois J., Rosenthal A., Platzer M., Nyakatura G., Taudien S., Rump A., Yang H., Yu J., Wang J., Huang G., Gu J., Hood L., Rowen L., Madan A., Qin S., Davis R.W., Federspiel N.A., Abola A.P., Proctor M.J., Myers R.M., Schmutz J., Dickson M., Grimwood J., Cox D.R., Olson M.V., Kaul R., Raymond C., Shimizu N., Kawasaki K., Minoshima S., Evans G.A., Athanasiou M., Schultz R., Roe B.A., Chen F., Pan H., Ramser J., Lehrach H., Reinhardt R., McCombie W.R., de la Bastide M., Dedhia N., Blocker H., Hornischer K., Nordsiek G., Agarwala R., Aravind L., Bailey J.A., Bateman A., Batzoglou S., Birney E., Bork P., Brown D.G., Burge C.B., Cerutti L., Chen H.C., Church D., Clamp M., Copley R.R., Doerks T., Eddy S.R., Eichler E.E., Furey T.S., Galagan J., Gilbert J.G., Harmon C., Hayashizaki Y., Haussler D., Hermjakob H., Hokamp K., Jang W., Johnson L.S., Jones T.A., Kasif S., Kaspryzk A., Kennedy S., Kent W.J., Kitts P., Koonin E.V., Korf I., Kulp D., Lancet D., Lowe T.M., McLysaght A., Mikkelsen T., Moran J.V., Mulder N., Pollara V.J., Ponting C.P., Schuler G., Schultz J., Slater G., Smit A.F., Stupka E., Szustakowski J., Thierry-Mieg D., Thierry-Mieg J., Wagner L., Wallis J., Wheeler R., Williams A., Wolf Y.I., Wolfe K.H., Yang S.P., Yeh R.F., Collins F., Guyer M.S., Peterson J., Felsenfeld A., Wetterstrand K.A., Patrinos A., Morgan M.J., de Jong P., Catanese J.J., Osoegawa K., Shizuya H., Choi S., Chen Y.J. Initial sequencing and analysis of the human genome. Nature 2001, 409:860-921.
57. Langmead B., Trapnell C., Pop M., Salzberg S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009, 10:R25.
58. Lax A.J., Thomas W. How bacteria could cause cancer: one step at a time. Trends Microbiol. 2002, 10:293-299.
59. Li H., Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760.
60. Li J., Wang X., Diaz J., Tsang S.H., Buck C.B., You J. Merkel cell polyomavirus large T antigen disrupts host genomic integrity and inhibits cellular proliferation. J. Virol. 2013, 87:9173-9188.
61. Li L., McVety S., Younan R., Liang P., Du Sart D., Gordon P.H., Hutter P., Hogervorst F.B., Chong G., Foulkes W.D. Distinct patterns of germ-line deletions in MLH1 and MSH2: the implication of Alu repetitive element in the genetic etiology of Lynch syndrome (HNPCC). Hum. Mutat. 2006, 27:388.
62. Littman A.J., White E., Jackson L.A., Thornquist M.D., Gaydos C.A., Goodman G.E., Vaughan T.L. Chlamydia pneumoniae infection and risk of lung cancer. Cancer Epidemiol. Biomar. Prev. 2004, 13:1624-1630.
63. Lotteau V., Teyton L., Peleraux A., Nilsson T., Karlsson L., Schmid S.L., Quaranta V., Peterson P.A. Intracellular transport of class II MHC molecules directed by invariant chain. Nature 1990, 348:600-605.
64. Luckey T.D. Introduction to the ecology of the intestinal flora. Am. J. Clin. Nutr. 1970, 23:1430-1432.
65. Malina A., Mills J.R., Cencic R., Yan Y., Fraser J., Schippers L.M., Paquet M., Dostie J., Pelletier J. Repurposing CRISPR/Cas9 for in situ functional assays. Genes Dev. 2013, 27:2602-2614.
66. Marion P.L., Salazar F.H., Alexander J.J., Robinson W.S. State of hepatitis B viral DNA in a human hepatoma cell line. J. Virol. 1980, 33:795-806.
67. Markowitz S.D., Bertagnolli M.M. Molecular origins of cancer: molecular basis of colorectal cancer. N. Engl. J. Med. 2009, 361:2449-2460.
68. Martin H.M., Campbell B.J., Hart C.A., Mpofu C., Nayar M., Singh R., Englyst H., Williams H.F., Rhodes J.M. Enhanced Escherichia coli adherence and invasion in Crohn's disease and colon cancer. Gastroenterology 2004, 127:80-93.
69. Matza D., Wolstein O., Dikstein R., Shachar I. Invariant chain induces B cell maturation by activating a TAFII105-NF-κB-dependent transcription program. J. Biol. Chem. 2001, 276:27203-27206.
70. McCabe M.T., Low J.A., Imperiale M.J., Day M.L. Human polyomavirus BKV transcriptionally activates DNA methyltransferase 1 through the pRb/E2F pathway. Oncogene 2006, 25:2727-2735.
71. Melsheimer P., Vinokurova S., Wentzensen N., Bastert G., von Knebel M. Doeberitz, DNA aneuploidy and integration of human papillomavirus type 16 e6/e7 oncogenes in intraepithelial neoplasia and invasive squamous cell carcinoma of the cervix uteri. Clin. Cancer Res. 2004, 10:3059-3063.
72. Miki Y., Katagiri T., Kasumi F., Yoshimoto T., Nakamura Y. Mutation analysis in the BRCA2 gene in primary breast cancers. Nat. Genet. 1996, 13:245-247.
73. Miki Y., Nishisho I., Horii A., Miyoshi Y., Utsunomiya J., Kinzler K.W., Vogelstein B., Nakamura Y. Disruption of the APC gene by a retrotransposal insertion of L1 sequence in a colon cancer. Cancer Res. 1992, 52:643-645.
74. Miller R.W., Rabkin C.S. Merkel cell carcinoma and melanoma: etiological similarities and differences. Cancer Epidemiol. Biomar. Prev. 1999, 8:153-158.
75. Mills R.E., Bennett E.A., Iskow R.C., Devine S.E. Which transposable elements are active in the human genome?. Trends Genet. 2007, 23:183-191.
76. Mitchell R.J., Farrington S.M., Dunlop M.G., Campbell H. Mismatch repair genes hMLH1 and hMSH2 and colorectal cancer: a HuGE review. Am. J. Epidemiol. 2002, 156:885-902.
77. Molyneux E.M., Rochford R., Griffin B., Newton R., Jackson G., Menon G., Harrison C.J., Israels T., Bailey S. Burkitt's lymphoma. Lancet 2012, 379:1234-1244.
78. Montagna M., Santacatterina M., Torri A., Menin C., Zullato D., Chieco-Bianchi L., D'Andrea E. Identification of a 3 kb Alu-mediated BRCA1 gene rearrangement in two breast/ovarian cancer families. Oncogene 1999, 18:4160-4165.
79. Moore P.S., Chang Y. Why do viruses cause cancer? Highlights of the first century of human tumour virology. Nat. Rev. Cancer 2010, 10:878-889.
80. Mooren J.J., Gultekin S.E., Straetmans J.M., Haesevoets A., Peutz-Kootstra C.J., Huebbers C.U., Dienes H.P., Wieland U., Ramaekers F.C., Kremer B., Speel E.J., Klussmann J.P. P16(INK4A) immunostaining is a strong indicator for high-risk-HPV-associated oropharyngeal carcinomas and dysplasias, but is unreliable to predict low-risk-HPV-infection in head and neck papillomas and laryngeal dysplasias. Int. J. Cancer 2014, 134:2108-2117.
81. Mukherjee S., Mukhopadhyay A., Banerjee D., Chandak G.R., Ray K. Molecular pathology of haemophilia B: identification of five novel mutations including a LINE 1 insertion in Indian patients. Haemophilia 2004, 10:259-263.
82. Murakami Y., Saigo K., Takashima H., Minami M., Okanoue T., Brechot C., Paterlini-Brechot P. Large scaled analysis of hepatitis B virus (HBV) DNA integration in HBV related hepatocellular carcinomas. Gut 2005, 54:1162-1168.
83. Niedobitek G., Agathanggelou A., Rowe M., Jones E.L., Jones D.B., Turyaguma P., Oryema J., Wright D.H., Young L.S. Heterogeneous expression of Epstein-Barr virus latent proteins in endemic Burkitt's lymphoma. Blood 1995, 86:659-665.
84. Oien K.A., Vass J.K., Downie I., Fullarton G., Keith W.N. Profiling, comparison and validation of gene expression in gastric carcinoma and normal stomach. Oncogene 2003, 22:4287-4300.
85. Oldenburg M., Kruger A., Ferstl R., Kaufmann A., Nees G., Sigmund A., Bathke B., Lauterbach H., Suter M., Dreher S., Koedel U., Akira S., Kawai T., Buer J., Wagner H., Bauer S., Hochrein H., Kirschning C.J. TLR13 recognizes bacterial 23S rRNA devoid of erythromycin resistance-forming modification. Science 2012, 337:1111-1115.
86. Oldridge M., Zackai E.H., McDonald-McGinn D.M., Iseki S., Morriss-Kay G.M., Twigg S.R.F., Johnson D., Wall S.A., Jiang W., Theda C., Jabs E.W., Wilkie A.O.M. De novo Alu-element insertions in FGFR2 identify a distinct pathological basis for Apert syndrome. Am. J. Hum. Genet. 1999, 64:446-461.
87. Pace J.K., Feschotte C. The evolutionary history of human DNA transposons: evidence for intense activity in the primate lineage. Genome Res. 2007, 17:422-432.
88. Parkin D.M. The global health burden of infection-associated cancers in the year 2002. Int. J. Cancer 2006, 118:3030-3044.
89. Paterlini-Brechot P., Saigo K., Murakami Y., Chami M., Gozuacik D., Mugnier C., Lagorce D., Brechot C. Hepatitis B virus-related insertional mutagenesis occurs frequently in human liver cancers and recurrently targets human telomerase gene. Oncogene 2003, 22:3911-3916.
90. Peek R.M., Blaser M.J. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat. Rev. Cancer 2002, 2:28-37.
91. Peixoto A., Pinheiro M., Massena L., Santos C., Pinto P., Rocha P., Pinto C., Teixeira M.R. Genomic characterization of two large Alu-mediated rearrangements of the BRCA1 gene. J Hum Genet 2013, 58:78-83.
92. Plottel C.S., Blaser M.J. Microbiome and malignancy. Cell Host Microbe 2011, 10:324-335.
93. Purtilo D.T., Manolov G., Manolova Y., Harada S., Lipscomb H., Tatsumi E. Role of Epstein-Barr virus in the etiology of Burkitt's lymphoma. IARC Sci. Publ. 1985, 231-247.
94. Rawat S., Clippinger A., Bouchard M. Modulation of apoptotic signaling by the hepatitis B virus X protein. Viruses 2012, 4:2945-2972.
95. Riley D.R., Sieber K.B., Robinson K.M., White J.R., Ganesan A., Nourbakhsh S., Dunning Hotopp J.C. Bacteria-human somatic cell lateral gene transfer is enriched in cancer samples. PLoS Comput. Biol. 2013, 9:e1003107.
96. Robinson K.M., Sieber K.B., Dunning Hotopp J.C. A review of bacteria-animal lateral gene transfer may inform our understanding of diseases like cancer. PLoS Genet. 2013, 9:e1003877.
97. Robinson W.S., Klote L., Aoki N. Hepadnaviruses in cirrhotic liver and hepatocellular carcinoma. J. Med. Virol. 1990, 31:18-32.
98. Romanczuk H., Howley P.M. Disruption of either the E1 or the E2 regulatory gene of human papillomavirus type 16 increases viral immortalization capacity. Proc. Natl. Acad. Sci. USA 1992, 89:3159-3163.
99. Roy A.M., Carroll M.L., Nguyen S.V., Salem A.H., Oldridge M., Wilkie A.O., Batzer M.A., Deininger P.L. Potential gene conversion and source genes for recently integrated Alu elements. Genome Res. 2000, 10:1485-1495.
100. Rubinstein M.R., Wang X., Liu W., Hao Y., Cai G., Han Y.W. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/beta-catenin signaling via its FadA adhesin. Cell Host Microbe 2013, 14:195-206.
101. Saigo K., Yoshida K., Ikeda R., Sakamoto Y., Murakami Y., Urashima T., Asano T., Kenmochi T., Inoue I. Integration of hepatitis B virus DNA into the myeloid/lymphoid or mixed-lineage leukemia (MLL4) gene and rearrangements of MLL4 in human hepatocellular carcinoma. Hum. Mutat. 2008, 29:703-708.
102. Sander L.E., Davis M.J., Boekschoten M.V., Amsen D., Dascher C.C., Ryffel B., Swanson J.A., Muller M., Blander J.M. Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 2011, 474:385-389.
103. Sarid R., Gao S.J. Viruses and human cancer: from detection to causality. Cancer Lett. 2011, 305:218-227.
104. Sastre-Garau X., Peter M., Avril M.F., Laude H., Couturier J., Rozenberg F., Almeida A., Boitier F., Carlotti A., Couturaud B., Dupin N. Merkel cell carcinoma of the skin: pathological and molecular evidence for a causative role of MCV in oncogenesis. J. Pathol. 2009, 218:48-56.
105. Scheffner M., Huibregtse J.M., Vierstra R.D., Howley P.M. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 1993, 75:495-505.
106. Schichman S.A., Caligiuri M.A., Gu Y., Strout M.P., Canaani E., Bloomfield C.D., Croce C.M. ALL-1 partial duplication in acute leukemia. Proc. Natl. Acad. Sci. USA 1994, 91:6236-6239.
107. Schichman S.A., Caligiuri M.A., Strout M.P., Carter S.L., Gu Y., Canaani E., Bloomfield C.D., Croce C.M. ALL-1 tandem duplication in acute myeloid leukemia with a normal karyotype involves homologous recombination between Alu elements. Cancer Res. 1994, 54:4277-4280.
108. Schmitz M., Driesch C., Beer-Grondke K., Jansen L., Runnebaum I.B., Durst M. Loss of gene function as a consequence of human papillomavirus DNA integration. Int. J. Cancer 2012, 131:E593-602.
109. Schneider G.F., Dekker C. DNA sequencing with nanopores. Nat. Biotechnol. 2012, 30:326-328.
110. Schröder G., Schuelein R., Quebatte M., Dehio C. Conjugative DNA transfer into human cells by the VirB/VirD4 type IV secretion system of the bacterial pathogen Bartonella henselae. Proc. Natl. Acad. Sci. USA 2011.
111. Schulz T.F., Boshoff C.H., Weiss R.A. HIV infection and neoplasia. Lancet 1996, 348:587-591.
112. Schwabe R.F., Jobin C. The microbiome and cancer. Nat. Rev. Cancer 2013, 13:800-812.
113. Sears C.L. Enterotoxigenic Bacteroides fragilis: a rogue among symbiotes. Clin. Microbiol. Rev. 2009, 22:349-369.
114. Sears C.L., Pardoll D.M. Perspective: alpha-bugs, their microbial partners, and the link to colon cancer. J. Infect. Dis. 2011, 203:306-311.
115. Shuda M., Arora R., Kwun H.J., Feng H., Sarid R., Fernandez-Figueras M.T., Tolstov Y., Gjoerup O., Mansukhani M.M., Swerdlow S.H., Chaudhary P.M., Kirkwood J.M., Nalesnik M.A., Kant J.A., Weiss L.M., Moore P.S., Chang Y. Human Merkel cell polyomavirus infection I. MCV T antigen expression in Merkel cell carcinoma, lymphoid tissues and lymphoid tumors. Int. J. Cancer 2009, 125:1243-1249.
116. Shuda M., Feng H., Kwun H.J., Rosen S.T., Gjoerup O., Moore P.S., Chang Y. T antigen mutations are a human tumor-specific signature for Merkel cell polyomavirus. Proc. Natl. Acad. Sci. USA 2008, 105:16272-16277.
117. Society A.C. Cancer Facts & Figures 2013. Atlanta 2013, American Cancer Society.
118. Solyom S., Ewing A.D., Rahrmann E.P., Doucet T., Nelson H.H., Burns M.B., Harris R.S., Sigmon D.F., Casella A., Erlanger B., Wheelan S., Upton K.R., Shukla R., Faulkner G.J., Largaespada D.A., Kazazian H.H. Extensive somatic L1 retrotransposition in colorectal tumors. Genome Res. 2012, 22:2328-2338.
119. Sribenja S., Li M., Wongkham S., Wongkham C., Yao Q., Chen C. Advances in thymosin beta10 research: differential expression, molecular mechanisms, and clinical implications in cancer and other conditions. Cancer Invest. 2009, 27:1016-1022.
120. Stein R., Mattes M.J., Cardillo T.M., Hansen H.J., Chang C.-H., Burton J., Govindan S., Goldenberg D.M. CD74: a new candidate target for the immunotherapy of B-cell neoplasms. Clin. Cancer Res. 2007, 13:5556s-5563s.
121. Sung W.K., Zheng H., Li S., Chen R., Liu X., Li Y., Lee N.P., Lee W.H., Ariyaratne P.N., Tennakoon C., Mulawadi F.H., Wong K.F., Liu A.M., Poon R.T., Fan S.T., Chan K.L., Gong Z., Hu Y., Lin Z., Wang G., Zhang Q., Barber T.D., Chou W.C., Aggarwal A., Hao K., Zhou W., Zhang C., Hardwick J., Buser C., Xu J., Kan Z., Dai H., Mao M., Reinhard C., Wang J., Luk J.M. Genome-wide survey of recurrent HBV integration in hepatocellular carcinoma. Nat. Genet. 2012, 44:765-769.
122. Taub R., Kirsch I., Morton C., Lenoir G., Swan D., Tronick S., Aaronson S., Leder P. Translocation of the c-myc gene into the immunoglobulin heavy chain locus in human Burkitt lymphoma and murine plasmacytoma cells. Proc. Natl. Acad. Sci. USA 1982, 79:7837-7841.
123. Teugels E., De Brakeleer S., Goelen G., Lissens W., Sermijn E., De Grève J. De novo Alu element insertions targeted to a sequence common to the BRCA1 and BRCA2 genes. Hum. Mutat. 2005, 26:284.
124. Tournier I., Paillerets B.B., Sobol H., Stoppa-Lyonnet D., Lidereau R., Barrois M., Mazoyer S., Coulet F., Hardouin A., Chompret A., Lortholary A., Chappuis P., Bourdon V., Bonadona V., Maugard C., Gilbert B., Nogues C., Frebourg T., Tosi M. Significant contribution of germline BRCA2 rearrangements in male breast cancer families. Cancer Res 2004, 64:8143-8147.
125. Theelen W., Litjens R.J., Vinokurova S., Haesevoets A., Reijans M., Simons G., Smedts F., Herrington C.S., Ramaekers F.C., von Knebel Doeberitz M., Speel E.J., Hopman A.H. Human papillomavirus multiplex ligation-dependent probe amplification assay for the assessment of viral load, integration, and gain of telomerase-related genes in cervical malignancies. Hum. Pathol. 2013, 44:2410-2418.
126. Wang G.C., Wang Y. Frequency of formation of chimeric molecules as a consequence of PCR coamplification of 16S rRNA genes from mixed bacterial genomes. Appl. Environ. Microbiol. 1997, 63:4645-4650.
127. Wang G.C.Y., Wang Y. The frequency of chimeric molecules as a consequence of PCR co-amplification of 16S rRNA genes from different bacterial species. Microbiology 1996, 142:1107-1114.
128. Wentzensen N., Vinokurova S., von Knebel Doeberitz M. Systematic review of genomic integration sites of human papillomavirus genomes in epithelial dysplasia and invasive cancer of the female lower genital tract. Cancer Res. 2004, 64:3878-3884.
129. Whitman S.P., Liu S., Vukosavljevic T., Rush L.J., Yu L., Liu C., Klisovic M.I., Maharry K., Guimond M., Strout M.P., Becknell B., Dorrance A., Klisovic R.B., Plass C., Bloomfield C.D., Marcucci G., Caligiuri M.A. The MLL partial tandem duplication: evidence for recessive gain-of-function in acute myeloid leukemia identifies a novel patient subgroup for molecular-targeted therapy. Blood 2005, 106:345-352.
130. Wu S., Lim K.C., Huang J., Saidi R.F., Sears C.L. Bacteroides fragilis enterotoxin cleaves the zonula adherens protein, E-cadherin. Proc. Natl. Acad. Sci. USA 1998, 95:14979-14984.
131. Wu S., Morin P.J., Maouyo D., Sears C.L. Bacteroides fragilis enterotoxin induces c-Myc expression and cellular proliferation. Gastroenterology 2003, 124:392-400.
132. You X., Liu F., Zhang T., Li Y., Ye L., Zhang X. Hepatitis B virus X protein upregulates oncogene Rab18 to result in the dysregulation of lipogenesis and proliferation of hepatoma cells. Carcinogenesis 2013, 34:1644-1652.
133. Yu F.X., Lin S.C., Morrison-Bogorad M., Atkinson M.A., Yin H.L. Thymosin beta 10 and thymosin beta 4 are both actin monomer sequestering proteins. J. Biol. Chem. 1993, 268:502-509.