Long interspersed element-1 is differentially regulated by food-borne carcinogens via the aryl hydrocarbon receptor

Oncogene

Volumn 32, Issue 41, 2013, Pages 4903-4912

  Okudaira, N ^a,b   Okamura, T ^a,e   Tamura, M ^a   Iijma, K ^a   Goto, M ^a   Matsunaga, A ^a   Ochiai, M ^c   Nakagama, H ^c   Kano, S ^a,b   Fujii Kuriyama, Y ^d   Ishizaka, Y ^a  

^a NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e Department of Infectious Diseases   (Japan)

Author keywords

aryl hydrocarbon receptor; breast carcinomas; ERa; MeIQx; PhIP

Indexed keywords

2 AMINO 1 METHYL 6 PHENYLIMIDAZO[4,5 B]PYRIDINE; 2 AMINO 3,8 DIMETHYLIMIDAZO[4,5 F]QUINOXALINE; AROMATIC HYDROCARBON RECEPTOR; AROMATIC HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR 1; AROMATIC HYDROCARBON RECEPTOR REPRESSOR; CCAAT ENHANCER BINDING PROTEIN BETA; ESTROGEN RECEPTOR ALPHA; HETEROCYCLIC AMINE; HYPOXIA INDUCIBLE FACTOR 1BETA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BREAST CARCINOGENESIS; BREAST CARCINOMA; BREAST MILK; CONTROLLED STUDY; DNA DAMAGE; GENE EXPRESSION; GENOMIC INSTABILITY; LONG INTERSPERSED ELEMENT 1; LONG INTERSPERSED REPEAT; MOUSE; NONHUMAN; PRIORITY JOURNAL; RETROPOSON; SOMATIC CELL; TRANSPOSON;

ANIMALS; CARCINOGENESIS; CARCINOGENS; CELL LINE, TUMOR; FEMALE; FOOD; GENOMIC INSTABILITY; HUMANS; IMIDAZOLES; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MICE; QUINOXALINES; RECEPTORS, ARYL HYDROCARBON;

MUS MUSCULUS;

EID: 84885666342     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.516     Document Type: Article

References (77)

1. Bannert N, Kurth R. Retroelements and the human genome: new perspectives on an old relation. Proc Natl Acad Sci USA 2004; 101: 14572-14579. (Pubitemid 39346726)
2. Brouha B, Schustak J, Badge RM, Lutz-Prigge S, Farley AH, Moran JV et al. Hot L1s account for the bulk of retrotransposition in the human population. Proc Natl Acad Sci USA 2003; 100: 5280-5285. (Pubitemid 36542696)
3. Goodier JL, Kazazian HH Jr. Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 2008; 135: 23-35.
4. Babushok DV, Kazazian HH Jr. Progress in understanding the biology of the human mutagen LINE-1. Hum Mutat 2007; 28: 527-539. (Pubitemid 46744283)
5. Hohjoh H, Singer MF. Cytoplasmic ribonucleoprotein complexes containing human LINE-1 protein and RNA. EMBO J 1996; 15: 630-639. (Pubitemid 26044576)
6. Goodier JL, Zhang L, Vetter MR, Kazazian HH Jr. LINE-1 ORF1 protein localizes in stress granules with other RNA-binding proteins, including components of RNA interference RNA-induced silencing complex. Mol Cell Biol 2007; 27: 6469-6483. (Pubitemid 47435752)
7. Wei W, Gilbert N, Ooi SL, Lawler JF, Ostertag EM, Kazazian HH Jr et al. Human L1 retrotransposition: cis preference versus trans complementation. Mol Cell Biol 2001; 21: 1429-1439. (Pubitemid 32114989)
8. Martin SL, Cruceanu M, Branciforte D, Wai-Lun Li P, Kwok SC, Hodges RS et al. LINE-1 retrotransposition requires the nucleic acid chaperone activity of the ORF1 protein. J Mol Biol 2005; 348: 549-561. (Pubitemid 40520490)
9. Mathias SL, Scott AF, Kazazian HH Jr, Boeke JD, Gabriel A. Reverse transcriptase encoded by a human transposable element. Science 1991; 254: 1808-1810. (Pubitemid 21917534)
10. Feng Q, Moran JV, Kazazian HH Jr, Boeke JD. Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 1996; 87: 905-916. (Pubitemid 26404289)
11. Jurka J. Sequence patterns indicate an enzymatic involvement in integration of mammalian retroposons. Proc Natl Acad Sci USA 1997; 94: 1872-1877. (Pubitemid 27113929)
12. Gilbert N, Luts S, Morrish TA, Moran JV. Multiple fates of L1 retrotransposition intermediates in cultured human cells. Mol Cell Biol 2005; 25: 7780-7795. (Pubitemid 41170138)
13. Gasior SL, Wakeman TP, Xu B, Deininger PL. The human LINE-1 retrotransposon creates DNA double-strand breaks. J Mol Biol 2006; 357: 1383-1393.
14. Dewannieux M, Esnault C, Heidmann T. LINE-mediated retrotransposition of marked Alu sequences. Nat Genet 2003; 35: 41-48. (Pubitemid 37048594)
15. Wallace N, Wagstaff BJ, Deininger PL, Roy-Engel AM. LINE-1 ORF1 protein enhances Alu SINE retrotrasposition. Gene 2008; 419: 1-6.
16. Raiz J, Damert A, Chira S, Held U, Klawitter S, Hamdorf M et al. The non-autonomous retrotransposon SVA is trans-mobilized by the human LINE-1 protein machinery. Nucleic Acids Res 2012; 40: 1666-1683.
17. Vitullo P, Sciamanna I, Baiocchi M, Sinibaldi-Vallebona P, Spadafora C. LINE-1 retrotransposon copies are amplified during murine early embryo development. Mol Reprod Dev 2012; 79: 118-127.
18. Beraldi R, Pittoggi C, Sciamanna I, Mattei E, Spadafora C. Expression of LINE-1 retroposons is essential for murine preimplantation development. Mol Reprod Dev 2006; 73: 279-287. (Pubitemid 43262042)
19. Belancio VP, Hedges DJ, Deininger P. Mammalian non-LTR retrotransposons: for better or worse, in sickness and in health. Genome Res 2008; 18: 343-358. (Pubitemid 351347078)
20. Hancks DC, Kazazian HH Jr. Active human retrotransposons: variation and disease. Curr Opin Genet Dev 2012; 22: 191-203.
21. Georgiou I, Noutsopoulos D, Dimitriadou E, Markopoulos G, Apergi A, Lazaros L et al. Retrotransposon RNA expression and evidence for retrotransposition events in human oocytes. Hum Mol Genet 2009; 18: 1221-1228.
22. Kano H, Godoy I, Courtney C, Vetter MR, Gerton GL, Ostertag EM et al. L1 retro-transposition occurs mainly in embryogenesis and creates somatic mosaicism. Genes Dev 2009; 23: 1303-1312.
23. Macia A, Muñoz-Lopez M, Cortes JL, Hastings RK, Morell S, Lucena-Aguilar G et al. Epigenetic control of retrotransposon expression in human embryonic stem cells. Mol Cell Biol 2011; 31: 300-316.
24. Coufal NG, Garcia-Perez JL, Peng GE, Yeo GW, Mu Y, Lovci MT et al. L1 retro-transposition in human neural progenitor cells. Nature 2009; 460: 1127-1131.
25. Baillie JK, Barnett MW, Upton KR, Gerhardt DJ, Richmond TA, De Sapio F et al. Somatic retrotransposition alters the genetic landscape of the human brain. Nature 2011; 479: 534-537.
26. Coufal NG, Garcia-Perez JL, Peng GE, Marchetto MC, Muotri AR, Mu Y et al. Ataxia telangiectasia mutated (ATM) modulates long interspersed element-1 (L1) retro-transposition in human neural stem cells. Proc Natl Acad Sci USA 2011; 108: 20382-20387.
27. Morse B, Rotherg PG, South VJ, Spandorfer JM, Astrin SM. Insertional mutagenesis of the myc locus by a LINE-1 sequence in a human breast carcinoma. Nature 1988; 333: 87-90.
28. Miki Y, Nishisho I, Horii A, Miyoshi Y, Utsunomiya J, Kinzler KW et al. Disruption of the APC gene by a retrotransposal insertion of L1 sequence in a colon cancer. Cancer Res 1992; 52: 643-645.
29. Iskow RC, McCabe MT, Mills RE, Torene S, Pittard WS, Neuwald AF et al. Natural mutagenesis of human genomes by endogenous retrotransposons. Cell 2010; 141: 1253-1261.
30. Ting DT, Lipson D, Paul S, Brannigan BW, Akhavanfard S, Coffman EJ et al. Aberrant overexpression of satellite repeats in pancreatic and other epithelial cancers. Science 2011; 331: 593-596.
31. Kazazian HH Jr. Mobile DNA transposition in somatic cells. BMC Biol 2011; 29: 62.
32. Lee E, Iskow R, Yang L, Gokcumen O, Haseley P, Luquette LJ 3rd et al. Landscape of Somatic Retrotransposition in Human Cancers. Science 2012; 337: 967-971.
33. Farkash EA, Kao GD, Horman SR, Prak ET. Gamma radiation increases endonu-clease-dependent L1 retrotransposition in a cultured cell assay. Nucleic Acids Res 2006; 34: 1196-1204.
34. Kale SP, Moore L, Deininger PL, Roy-Engel AM. Heavy metals stimulate human LINE-1 retrotransposition. Int J Environ Res Public Health 2005; 2: 14-23. (Pubitemid 40973381)
35. Stribinskis V, Ramos KS. Activation of human long interspersed nuclear element 1 retrotransposition by benzo(a)pyrene, an ubiquitous environmental carcinogen. Cancer Res 2006; 66: 2616-2620.
36. Okudaira N, Iijima K, Koyama T, Minemoto Y, Kano S, Mimori A et al. Induction of long interspersed nucleotide element-1 (L1) retrotransposition by 6-for-mylindolo[3, 2-b]carbazole (FICZ), a tryptophan photoproduct. Proc Natl Acad Sci USA 2010; 107: 18487-18492.
37. Okudaira N, Goto M, Yanobu-Takanashi R, Tamura M, An A, Abe Y et al. Involvement of retrotransposition of long interspersed nucleotide element-1 in skin tumorigenesis induced by 7, 12-dimethylbenz[a]anthracene and 12-O-tetra-decanoylphorbol-13-acetate. Cancer Sci 2011; 102: 2000-2006.
38. Hoffman EC, Reyes H, Chu FF, Sander F, Conley LH, Brooks BA et al. Cloning of a factor required for activity of the Ah (dioxin) receptor. Science 1991; 252: 954-958. (Pubitemid 21917012)
39. Hahn ME. Aryl hydrocarbon receptors: diversity and evolution. Chem Biol Interact 2002; 141: 131-160. (Pubitemid 35223209)
40. Beischlag TV, Luis Morales J, Hollingshead BD, Perdew GH. The aryl hydrocarbon receptor complex and the control of gene expression. Crit Rev Eukaryot Gene Expr 2008; 18: 207-250. (Pubitemid 351620286)
41. McIntosh BE, Hogenesch JB, Bradfield CA. Mammalian Per-Arnt-Sim proteins in environmental adaptation. Annu Rev Physiol 2010; 72: 625-645.
42. Eguchi H, Ikuta T, Tachibana T, Yoneda Y, Kawajiri K. A nuclear localization signal of human aryl hydrocarbon receptor nuclear translocator/hypoxia-inducible factor 1beta is a novel bipartite type recognized by the two components of nuclear pore-targeting complex. J Biol Chem 1997; 272: 17640-17647. (Pubitemid 27311200)
43. Wiseman M. The second World Cancer Research Fund/American Institute for Cancer Research expert report. Food, nutrition, physical activity, and the prevention of cancer: a global perspective. Proc Nutr Soc 2008; 67: 253-256.
44. Sugimura T, Wakabayashi K, Nakagama H, Nagao M. Heterocyclic amines: muta-gens/carcinogens produced during cooking of meat and fish. Cancer Sci 2004; 95: 290-299. (Pubitemid 38519467)
45. Layton DW, Bogen KT, Knize MG, Hatch FT, Johnson VM, Felton JS. Cancer risk of heterocyclic amines in cooked foods: an analysis and implications for research. Carcinogenesis 1995; 16: 39-52.
46. Scott KA, Turesky RJ, Wainman BC, Josephy PD. Hplc/electrospray ionization mass spectrometric analysis of the heterocyclic aromatic amine carcinogen 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine in human milk. Chem Res Toxicol 2007; 20: 88-94. (Pubitemid 46220158)
47. Ito N, Hasegawa R, Sano M, Tamano S, Esumi H, Takayama S et al. A new colon and mammary carcinogen in cooked food, 2-amino-1-methyl-6-phenylimi- dazo[4, 5-b]pyridine (PhIP). Carcinogenesis 1991; 12: 1503-1506.
48. Shirai T, Sano M, Tamano S, Takahashi S, Hirose M, Futakuchi M et al. The prostate: a target for carcinogenicity of 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine (PhIP) derived from cooked foods. Cancer Res 1997; 57: 195-198. (Pubitemid 27036591)
49. Nakai Y, Nelson WG, De Marzo AM. The dietary charred meat carcinogen 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine acts as both a tumor initiator and promoter in the rat ventral prostate. Cancer Res 2007; 67: 1378-1384.
50. Nishikawa A, Imazawa T, Kuroiwa Y, Kitamura Y, Kanki K, Ishii Y et al. Induction of colon tumors in C57BL/6J mice fed MeIQx, IQ, or PhIP followed by dextran sulfate sodium treatment. Toxicol sci 2005; 84: 243-248. (Pubitemid 40542283)
51. Ohgaki H, Hasegawa H, Suenaga M, Sato S, Takayama S, Sugimura T. Carcino-genicity in mice of a mutagenic compound, 2-amino-3, 8-dimethylimidazo [4, 5-f]quinoxaline (MeIQx) from cooked foods. Carcinogenesis 1987; 8: 665-668. (Pubitemid 17127900)
52. Lauber SN, Ali S, Gooderham NJ. The cooked food derived carcinogen 2-amino-1-methyl-6-phenylimidazo[4, 5-b] pyridine is a potent oestrogen: a mechanistic basis for its tissue-specific carcinogenicity. Carcinogenesis 2004; 25: 2509-2517. (Pubitemid 39625193)
53. Ema M, Morita M, Ikawa S, Tanaka M, Matsuda Y, Gotoh O et al. Two new members of the murine Sim gene family are transcriptional repressors and show different expression patterns during mouse embryogenesis. Mol Cell Biol 1996; 16: 5865-5875. (Pubitemid 26315108)
54. Gilbert N, Lutz-Prigge S, Moran JV. Genomic deletions created upon LINE-1 retrotransposition. Cell 2002; 110: 315-325.
55. Wei W, Morrish TA, Alisch RS, Moran JV. A transient assay reveals that cultured human cells can accommodate multiple LINE-1 retrotransposition events. Anal Biochem 2000; 284: 435-438.
56. Schut HA, Snyderwine EG. DNA adducts of heterocyclic amine food mutagens: implications for mutagenesis and carcinogenesis. Carcinogenesis 1999; 20: 353-368. (Pubitemid 29112620)
57. Kleman MI, Overvik E, Mason GG, Gustafsson JA. In vitro activation of the dioxin receptor to a DNA-binding form by food-borne heterocyclic amines. Carcino-genesis 1992; 13: 1619-1624.
58. Fritsche E, Schäfer C, Calles C, Bernsmann T, Bernshausen T, Wurm M et al. Lightening up the UV response by identification of the arylhydrocarbon receptor as a cytoplasmic target for ultraviolet B radiation. Proc Natl Acad Sci USA 2007; 104: 8851-8856. (Pubitemid 47175400)
59. Wincent E, Bengtsson J, Mohammadi Bardbori A, Alsberg T, Luecke S, Rannug U et al. Inhibition of cytochrome P4501-dependent clearance of the endogenous agonist FICZ as a mechanism for activation of the aryl hydrocarbon receptor. Proc Natl Acad Sci USA 2012; 109: 4479-4484.
60. Karchner SI, Jenny MJ, Tarrant AM, Evans BR, Kang HJ, Bae I et al. The active form of human aryl hydrocarbon receptor (AHR) repressor lacks exon 8, and its Pro 185 and Ala 185 variants repress both AHR and hypoxia-inducible factor. Mol Cell Biol 2009; 29: 3465-3477.
61. Osborne CK, Wakeling A, Nicholson RI. Fulvestrant: an oestrogen receptor antagonist with a novel mechanism of action. Br J Cancer 2004; 90: S2-S6. (Pubitemid 38482618)
62. Weiss C, Faust D, Dürk H, Kolluri SK, Pelzer A, Schneider S et al. TCDD induces c-jun expression via a novel Ah (dioxin) receptor-mediated p38-MAPK-dependent pathway. Oncogene 2005; 24: 4975-4983. (Pubitemid 41129101)
63. Ishizaka Y, Okudaira N, Okamura T. Regulation of retrotransposition of long interspersed element-1 by mitogen-activated protein kinases. In: Da Silva Xavier G (ed). Protein Kinases/Book 1. InTecOpen: Croatia, pp 187-198(http://www.intechopen.com/books/protein-kinases)).
64. Puig O, Caspary F, Rigaut G, Rutz B, Bouveret E, Bragado-Nilsson E et al. The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 2001; 24: 218-229. (Pubitemid 32846428)
65. Mimura J, Yamashita K, Nakamura K, Morita M, Takagi TN, Nakao K et al. Loss of teratogenic response to 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD) in mice lacking the Ah (dioxin) receptor. Genes Cells 1997; 2: 645-654. (Pubitemid 127688610)
66. Hahn ME, Allan LL, Sherr DH. Regulation of constitutive and inducible AHR signaling: complex interactions involving the AHR repressor. Biochem Pharmacol 2009; 77: 485-497.
67. Woodcock DM, Lawler CB, Linsenmeyer ME, Doherty JP, Warren WD. Asymmetric methylation in the hypermethylated CpG promoter region of the human L1 retrotransposon. J Biol Chem 1997; 272: 7810-7816. (Pubitemid 27137338)
68. Muotri AR, Marchetto MC, Coufal NG, Oefner R, Yeo G, Nakashima K et al. L1 retrotransposition in neurons is modulated by MeCP2. Nature 2010; 468:443-446.
69. Herman JG, Graff JR, Myöhänen S, Nelkin BD, Baylin SB. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA 1996; 93: 9821-9826. (Pubitemid 26296693)
70. Quintana FJ, Basso AS, Iglesias AH, Korn T, Farez MF, Bettelli E et al. Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor. Nature 2008; 453: 65-71. (Pubitemid 351630328)
71. Veldhoen M, Hirota K, Westendorf AM, Buer J, Dumoutier L, Renauld JC et al. The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 2008; 453: 106-109. (Pubitemid 351630329)
72. Shimizu Y, Nakatsuru Y, Ichinose M, Takahashi Y, Kume H, Mimura J et al. Ben-zo[a]pyrene carcinogenicity is lost in mice lacking the aryl hydrocarbon receptor. Proc Natl Acad Sci USA 2000; 97: 779-782. (Pubitemid 30070386)
73. Symer DE, Connelly C, Szak ST, Caputo EM, Cost GJ, Parmigiani G et al. Human L1 retrotransposition is associated with genetic instability in vivo. Cell 2002; 110: 327-338.
74. Belancio VP, Roy-Engel AM, Deininger PL. All y'all need to know 'bout retro-elements in cancer. Semin Cancer Biol 2010; 20: 200-210.
75. Konkel MK, Batzer MA. A mobile threat to genome stability: the impact of non-LTR retrotransposons upon the human genome. Semin Cancer Biol 2010; 20: 211-221.
76. Oricchio E, Sciamanna I, Beraldi R, Tolstonog GV, Schumann GG, Spadafora C. Distinct roles for LINE-1 and HERV-K retroelements in cell proliferation, differentiation and tumor progression. Oncogene 2007; 26: 4226-4233. (Pubitemid 46975802)
77. Lauber SN, Gooderham NJ. The cooked meat derived genotoxic carcinogen 2-amino-3-methylimidazo[4, 5-b]pyridine has potent hormone-like activity: mechanistic support for a role in breast cancer. Cancer Res 2007; 67: 9597-9602. (Pubitemid 47535952)