Somatically Acquired LINE-1 Insertions in Normal Esophagus Undergo Clonal Expansion in Esophageal Squamous Cell Carcinoma

Human Mutation

Volumn 37, Issue 9, 2016, Pages 942-954

  Doucet O'Hare, Tara T ^a,b,c   Sharma, Reema ^a   Rodić, Nemanja ^d   Anders, Robert A ^a   Burns, Kathleen H ^a   Kazazian, Haig H ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

esophagus; L1; LINE 1; retrotransposition; squamous cell carcinoma; sub clonal

Indexed keywords

OPEN READING FRAME 1 PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; HUMAN; IMMUNOHISTOCHEMISTRY; INDEL MUTATION; MICRODISSECTION; NEXT GENERATION SEQUENCING; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOMATIC MUTATION;

EID: 84982218114     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.23027     Document Type: Article

References (64)

1. Abedi-Ardekani B, Hainaut P. 2014. Cancers of the upper gastro-intestinal tract: a review of somatic mutation distributions. Arch Iran Med 17:286–292.
2. An O, Dall'Olio GM, Mourikis TP, Ciccarelli FD. 2016. NCG 5.0: updates of a manually curated repository of cancer genes and associated properties from cancer mutational screenings. Nucleic Acids Res 44:D992–D999.
3. Arjan-Odedra S SC, Sherer NM, Wolinsky SM, Malim MH. 2012. Endogenous MOV10 inhibits the retrotransposition of endogenous retroelements but not the replication of exogenous retroviruses. Retrovirology 9.
4. Baba Y, Murata A, Watanabe M, Baba H. 2014. Clinical implications of the LINE-1 methylation levels in patients with gastrointestinal cancer. Surg Today 44:1807–1816.
5. Baillie JK, Barnett MW, Upton KR, Gerhardt DJ, Richmond TA, De Sapio F, Brennan PM, Rizzu P, Smith S, Fell M, Talbot RT, Gustincich S, et al. 2011. Somatic retrotransposition alters the genetic landscape of the human brain. Nature 479:534–537.
6. Bogerd HP, Wiegand HL, Hulme AE, Garcia-Perez JL, O'Shea KS, Moran JV, Cullen BR. 2006. Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. Proc Natl Acad Sci USA 103:8780–8785.
7. Boissinot S, Chevret P, Furano AV. 2000. L1 (LINE-1) retrotransposon evolution and amplification in recent human history. Mol Biol Evol 17:915–928.
8. Chen H, Lilley CE, Yu Q, Lee DV, Chou J, Narvaiza I, Landau NR, Weitzman MD. 2006. APOBEC3A is a potent inhibitor of adeno-associated virus and retrotransposons. Current Biology 16:480–485.
9. Chow JC, Ciaudo C, Fazzari MJ, Mise N, Servant N, Glass JL, Attreed M, Avner P, Wutz A, Barillot E, Greally JM, Voinnet O, et al. 2010. LINE-1 activity in facultative heterochromatin formation during X chromosome inactivation. Cell 141:956–969.
10. Doucet-O'Hare TT, Rodic N, Sharma R, Darbari I, Abril G, Choi JA, Young AJ, Cheng Y, Anders RA, Burns KH, Kazazian HHK. 2015. LINE-1 expression and retrotransposition in Barrett's esophagus and esophageal carcinoma. Proc Natl Acad Sci USA 112:E4894–E4900.
11. Doucet TT, Kazazian HH, Jr. 2016. Long interspersed element sequencing (L1-Seq): a method to identify somatic LINE-1 insertions in the human genome. Methods Mol Biol 1400:79–93.
12. Ecco G, Rowe HM, Trono D. 2016. A Large-Scale Functional Screen to Identify Epigenetic Repressors of Retrotransposon Expression. Methods Mol Biol 1400:403–417.
13. Enzinger PC, Mayer RJ. 2003. Esophageal cancer. N Engl J Med 349:2241–2252.
14. Esnault C, Maestre J, Heidmann T. 2000. Human LINE retrotransposons generate processed pseudogenes. Nat Genet 24:363–367.
15. Evrony GD, Cai X, Lee E, Hills LB, Elhosary PC, Lehmann HS, Parker JJ, Atabay KD, Gilmore EC, Poduri A, Park PJ, Walsh CA. 2012. Single-neuron sequencing analysis of L1 retrotransposition and somatic mutation in the human brain. Cell 151:483–496.
16. Ewing AD, Gacita A, Wood LD, Ma F, Xing D, Kim MS, Manda SS, Abril G, Pereira G, Makohon-Moore A, Looijenga LH, Gillis AJ, et al. 2015.Widespread somatic L1 retrotransposition occurs early during gastrointestinal cancer evolution. Genome Res 25:1536–1545.
17. Ewing AD, Kazazian HH, Jr. 2010. High-throughput sequencing reveals extensive variation in human-specific L1 content in individual human genomes. Genome Res 20:1262–1270.
18. Fanning T, Singer, M. 1987. The LINE-1 DNA sequences in four mammalian orders predict proteins that conserve homologies to retrovirus proteins. Nucleic Acids Res 15:2251–2260.
19. Feng Q, Moran JV, Kazazian HH, Jr., Boeke JD. 1996. Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 87:905–916.
20. Gilbert N, Lutz-Prigge S, Moran JV. 2002. Genomic deletions created upon LINE-1 retrotransposition. Cell 110:315–325.
21. Goodier JL. 2014. Retrotransposition in tumors and brains. Mob DNA 5.
22. Goodier JL, Cheung LE, Kazazian HH, Jr. 2012. MOV10 RNA helicase is a potent inhibitor of retrotransposition in cells. PLoS Genet 8:e1002941.
23. Hancks DC, Kazazian HH. 2012. Active human retrotransposons: variation and disease. Curr Opin Genet Dev 22:191–203.
24. Helman E, Lawrence MS, Stewart C, Sougnez C, Getz G, Meyerson M. 2014. Somatic retrotransposition in human cancer revealed by whole-genome and exome sequencing. Genome Res 24:1053–1063.
25. Heras SR, Macias S, Plass M, Fernandez N, Cano D, Eyras E, Garcia-Perez JL, Caceres JF. 2013. The Microprocessor controls the activity of mammalian retrotransposons. Nat Struct Mol Biol 20:1173–1181.
26. Imbeault M, Trono D. 2014. As time goes by: KRABs evolve to KAP endogenous retroelements. Dev Cell 31:257–258.
27. Irahara N, Nosho K, Baba Y, Shima K, Lindeman NI, Hazra A, Schernhammer ES, Hunter DJ, Fuchs CS, Ogino S. 2010. Precision of pyrosequencing assay to measure LINE-1 methylation in colon cancer, normal colonic mucosa, and peripheral blood cells. J Mol Diagn 12:177–183.
28. Iskow RC, McCabe MT, Mills RE, Torene S, Pittard WS, Neuwald AF, Van Meir EG, Vertino PM, and Devine SE. 2010. Natural mutagenesis of human genomes by endogenous retrotransposons. Cell 141(7):1253-1261.
29. Islami F, Kamangar F, Nasrollahzadeh D, Moller H, Boffetta P, Malekzadeh R. 2009. Oesophageal cancer in Golestan Province, a high-incidence area in northern Iran—a review. Eur J Cancer 45:3156–3165.
30. Iwagami S BY, Watanabe M, Shigaki H, Miyake K, Ishimoto T, Iwatsuki M, Sakamaki K, Ohashi Y, Baba H. 2013. LINE-1 hypomethylation is associated with a poor prognosis among patients with curatively resected esophageal squamous cell carcinoma. Ann Surg 257:449–455.
31. Jacobs FM, Greenberg D, Nguyen N, Haeussler M, Ewing AD, Katzman S, Paten B, Salama SR, Haussler D. 2014. An evolutionary arms race between KRAB zinc-finger genes ZNF91/93 and SVA/L1 retrotransposons. Nature 516:242–245.
32. Jurka J. 1997. Sequence patterns indicate an enzymatic involvement in integration of mammalian retroposons. Proc Natl Acad Sci USA 94:1872–1877.
33. Kamangar F, Malekzadeh R, Dawsey SM, Saidi F. 2007. Esophageal cancer in Northeastern Iran: a review. Arch Iran Med 10:70–82.
34. Kano H, Godoy I, Courtney C, Vetter MR, Gerton GL, Ostertag EM, Kazazian HH Jr. 2010. L1 retrotransposition occurs mainly in embryogenesis and creates somatic mosaicism. Genes Dev 23(11):1303-1312.
35. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D. 2002. The human genome browser at UCSC. Genome Res 12:996–1006.
36. Lambert R, Hainaut P. 2007. The multidisciplinary management of gastrointestinal cancer. Epidemiology of oesophagogastric cancer. Best Pract Res Clin Gastroenterol 21:921–945.
37. Lee E, Iskow R, Yang L, Gokcumen O, Haseley P, Luquette LJ, 3rd, Lohr JG, Harris CC, Ding L, Wilson RK, Wheeler DA, Gibbs RA, et al. 2012. Landscape of somatic retrotransposition in human cancers. Science 337:967–971.
38. Levin HL, Moran JV. 2011. Dynamic interactions between transposable elements and their hosts. Nat Rev Genet 12:615–627.
39. Martin SL. 2006. The ORF1 protein encoded by LINE-1: structure and function during L1 retrotransposition. J Biomed Biotechnol 2006:45621.
40. Martin SL. 2010. Nucleic acid chaperone properties of ORF1p from the non-LTR retrotransposon, LINE-1. RNA Biol 7:706–711.
41. Martin SL, Bushman FD. 2001. Nucleic acid chaperone activity of the ORF1 protein from the mouse LINE-1 retrotransposon. Mol Cell Biol 21:467–475.
42. Mathias SL, Scott AF, Kazazian HH, Jr., Boeke JD, Gabriel A. 1991. Reverse transcriptase encoded by a human transposable element. Science 254:1808–1810.
43. Miki Y, Nishisho I, Horii A, Miyoshi Y, Utsunomiya J, Kinzler KW, Vogelstein B, Nakamura Y. 1992. Disruption of the APC gene by a retrotransposal insertion of L1 sequence in a colon cancer. Cancer Res 52:643–645.
44. Moran JV, Holmes SE, Naas TP, DeBerardinis RJ, Boeke JD, Kazazian HH, Jr. 1996. High frequency retrotransposition in cultured mammalian cells. Cell 87:917–927.
45. Morrish TA, Garcia-Perez JL, Stamato TD, Taccioli GE, Sekiguchi J, Moran JV. 2007. Endonuclease-independent LINE-1 retrotransposition at mammalian telomeres. Nature 446:208–212.
46. Morrish TA, Gilbert N, Myers JS, Vincent BJ, Stamato TD, Taccioli GE, Batzer MA, Moran JV. 2002. DNA repair mediated by endonuclease-independent LINE-1 retrotransposition. Nat Genet 31:159–165.
47. Muotri AR, Marchetto MC, Coufal NG, Oefner R, Yeo G, Nakashima K, Gage FH. 2010. L1 retrotransposition in neurons is modulated by MeCP2. Nature 468:443–446.
48. Ohashi S, Miyamoto S, Kikuchi O, Goto T, Amanuma Y, Muto M. 2015. Recent advances from basic and clinical studies of esophageal squamous cell carcinoma. Gastroenterology 149:1700–1715.
49. Ostertag EM, Kazazian HH, Jr. 2001. Biology of mammalian L1 retrotransposons. Annu Rev Genet 35:501–538.
50. Rodic N, Sharma R, Sharma R, Zampella J, Dai L, Taylor MS, Hruban RH, Iacobuzio-Donahue CA, Maitra A, Torbenson MS, Goggins M, Shih IeM, et al. 2014. Long interspersed element-1 protein expression is a hallmark of many human cancers. Am J Pathol 184:1280–1286.
51. Rodic N, Steranka JP, Makohon-Moore A, Moyer A, Shen P, Sharma R, Kohutek ZA, Huang CR, Ahn D, Mita P, Taylor MS, Barker NJ, et al. 2015. Retrotransposon insertions in the clonal evolution of pancreatic ductal adenocarcinoma. Nat Med 21:1060–1064.
52. Rowe HM, Trono D. 2011. Dynamic control of endogenous retroviruses during development. Virology 411:273–287.
53. Scott AF, Schmeckpeper BJ, Abdelrazik M, Comey CT, O'Hara B, Rossiter JP, Cooley T, Heath P, Smith KD, Margolet L. 1987. Origin of the human L1 elements: proposed progenitor genes deduced from a consensus DNA sequence. Genomics 1:113–125.
54. Shigaki H, Baba Y, Watanabe M, Murata A, Iwagami S, Miyake K, Ishimoto T, Iwatsuki M, Baba H. 2013. LINE-1 hypomethylation in gastric cancer, detected by bisulfite pyrosequencing, is associated with poor prognosis. Gastric Cancer 16:480–487.
55. Shukla R, Upton KR, Munoz-Lopez M, Gerhardt DJ, Fisher ME, Nguyen T, Brennan PM, Baillie JK, Collino A, Ghisletti S, Sinha S, Iannelli F, et al. 2013. Endogenous retrotransposition activates oncogenic pathways in hepatocellular carcinoma. Cell 153:101–111.
56. Skowronski J, Fanning TG, Singer MF. 1988. Unit-length line-1 transcripts in human teratocarcinoma cells. Mol Cell Biol 8:1385–1397.
57. Solyom S, Ewing AD, Rahrmann EP, Doucet T, Nelson HH, Burns MB, Harris RS, Sigmon DF, Casella A, Erlanger B, Wheelan S, Upton KR, et al. 2012. Extensive somatic L1 retrotransposition in colorectal tumors. Genome Res 22:2328–2338.
58. Stenglein MD, Harris RS. 2006. APOBEC3B and APOBEC3F inhibit L1 retrotransposition by a DNA deamination-independent mechanism. J Biol Chem 281:16837–16841.
59. Tran GD, Sun XD, Abnet CC, Fan JH, Dawsey SM, Dong ZW, Mark SD, Qiao YL, Taylor PR. 2005. Prospective study of risk factors for esophageal and gastric cancers in the Linxian general population trial cohort in China. Int J Cancer 113:456–463.
60. Tubio JM, Li Y, Ju YS, Martincorena I, Cooke SL, Tojo M, Gundem G, Pipinikas CP, Zamora J, Raine K, Menzies A, Roman-Garcia P, et al. 2014. Mobile DNA in cancer. Extensive transduction of nonrepetitive DNAmediated by L1 retrotransposition in cancer genomes. Science 345:1251343.
61. Turelli P, Vianin S, Trono D. 2004. The innate antiretroviral factor APOBEC3G does not affect human LINE-1 retrotransposition in a cell culture assay. J Biol Chem 279:43371–43373.
62. Wei W, Gilbert N, Ooi SL, Lawler JF, Ostertag EM, Kazazian HH, Boeke JD, Moran JV. 2001. Human L1 retrotransposition: cis preference versus trans complementation. Mol Cell Biol 21:1429–1439.
63. Yoder JA, Walsh CP, Bestor TH. 1997. Cytosine methylation and the ecology of intragenomic parasites. Trends Genet 13:335–340.
64. Zhang HZ, Jin GF, Shen HB. 2012. Epidemiologic differences in esophageal cancer between Asian and Western populations. Chinese J Cancer 31:281–286.