Type I interferon controls propagation of long interspersed element-1

Journal of Biological Chemistry

Volumn 290, Issue 16, 2015, Pages 10191-10199

  Yu, Qiujing ^a   Carbone, Christopher J ^a   Katlinskaya, Yuliya V ^a   Zheng, Hui ^a   Zheng, Ke ^a   Luo, Mengcheng ^a   Wang, P Jeremy ^a   Greenberg, Roger A ^b   Fuchs, Serge Y ^a  

^a UNIVERSITY OF PENNSYLVANIA SCHOOL OF VETERINARY MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; CELL CULTURE; GENE EXPRESSION; GLYCOPROTEINS; INTERFERONS; MAMMALS; MOBILE SECURITY; TISSUE; VIRUSES;

ADDITIONAL EXPERIMENTS; GENOME STABILITY; INTERSPERSED ELEMENTS; ISOGENIC CELLS; PRE-TREATMENT; RNA HELICASES; SIGNALING PATHWAYS; TYPE I INTERFERONS;

CELL SIGNALING;

BETA INTERFERON; INTERFERON; INTERFERON RECEPTOR; ALPHA BETA INTERFERON RECEPTOR; ALPHA INTERFERON; IFNAR1 PROTEIN, MOUSE; MOV10L1 PROTEIN, MOUSE; RNA HELICASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; DNA STRUCTURE; GENE ACTIVATION; GENE MUTATION; GENETIC STABILITY; GENETIC VARIABILITY; GERM CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; LONG INTERSPERSED ELEMENT 1; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETROPOSON; UPREGULATION; 3T3 CELL LINE; ANIMAL; ANIMAL EMBRYO; C57BL MOUSE; CYTOLOGY; DEFICIENCY; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; GENOMIC INSTABILITY; HELA CELL LINE; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; LONG INTERSPERSED REPEAT; MALE; METABOLISM; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION; TESTIS;

MUS;

ANIMALS; EMBRYO, MAMMALIAN; FIBROBLASTS; GENE EXPRESSION REGULATION; GENOMIC INSTABILITY; HELA CELLS; HUMANS; INTERFERON-ALPHA; INTERFERON-BETA; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NIH 3T3 CELLS; PRIMARY CELL CULTURE; RECEPTOR, INTERFERON ALPHA-BETA; RNA HELICASES; SIGNAL TRANSDUCTION; TESTIS;

EID: 84927720839     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.612374     Document Type: Article

References (51)

1. Katze, M. G., He, Y., and Gale, M., Jr. (2002) Viruses and interferon: a fight for supremacy. Nature Reviews. Immunology 2, 675-687
2. Fuchs, S. Y. (2013) Hope and fear for interferon: the receptor-centric outlook on the future of interferon therapy. J. Interferon and Cytokine 33, 211-225
3. Fuchs, S. Y. (2012) Ubiquitination-mediated regulation of interferon responses. Growth Factors 30, 141-148
4. Piehler, J., Thomas, C., Garcia, K. C., and Schreiber, G. (2012) Structural and dynamic determinants of type I interferon receptor assembly and their functional interpretation. Immunol. Rev. 250, 317-334
5. Trinchieri, G. (2010) Type I interferon: friend or foe? J. Exp. Med. 207, 2053-2063
6. Platanias, L. C. (2005) Mechanisms of type-I- and type-II-interferon-mediated signalling. Nature Reviews. Immunology 5, 375-386
7. Bhattacharya, S., Katlinski, K. V., Reichert, M., Takano, S., Brice, A., Zhao, B., Yu, Q., Zheng, H., Carbone, C. J., Katlinskaya, Y. V., Leu, N. A., Mc-Corkell, K. A., Srinivasan, S., Girondo, M., Rui, H., May, M. J., Avadhani, N. G., Rustgi, A. K., and Fuchs, S. Y. (2014) Triggering ubiquitination of IFNAR1 protects tissues from inflammatory injury. EMBO Mol. Med. 6, 384-397
8. Zheng, H., Gupta, V., Patterson-Fortin, J., Bhattacharya, S., Katlinski, K., Wu, J., Varghese, B., Carbone, C. J., Aressy, B., Fuchs, S. Y., and Greenberg, R. A. (2013) A BRISC-SHMT complex deubiquitinates IFNAR1 and regulates interferon responses. Cell Reports 5, 180-193
9. Weitzman, M. D., Lilley, C. E., and Chaurushiya, M. S. (2010) Genomes in conflict: maintaining genome integrity during virus infection. Annu. Rev. Microbiol. 64, 61-81
10. Kumar, A., and Bennetzen, J. L. (1999) Plant retrotransposons. Annu. Rev. Genet 33, 479-532
11. Kazazian, H. H., Jr. (2004) Mobile elements: drivers of genome evolution. Science 303, 1626-1632
12. 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., 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., and Chen, Y. J. (2001) Initial sequencing and analysis of the human genome. Nature 409, 860-921
13. Symer, D. E., Connelly, C., Szak, S. T., Caputo, E. M., Cost, G. J., Parmigiani, G., and Boeke, J. D. (2002) Human l1 retrotransposition is associated with genetic instability in vivo. Cell 110, 327-338
14. Zheng, K., and Wang, P. J. (2012) Blockade of pachytene piRNA biogenesis reveals a novel requirement for maintaining post-meiotic germline genome integrity. PLoS Genet 8, e1003038
15. Prak, E. T., Dodson, A. W., Farkash, E. A., and Kazazian, H. H., Jr. (2003) Tracking an embryonic L1 retrotransposition event. Proc. Natl. Acad. Sci. U. S.A. 100, 1832-1837
16. Rangwala, S. H., and Kazazian, H. H., Jr. (2009) The L1 retrotransposition assay: a retrospective and toolkit. Methods 49, 219-226
17. Liu, J., HuangFu, W. C., Kumar, K. G., Qian, J., Casey, J. P., Hamanaka, R. B., Grigoriadou, C., Aldabe, R., Diehl, J. A., and Fuchs, S. Y. (2009) Virus-induced unfolded protein response attenuates antiviral defenses via phosphorylation-dependent degradation of the type I interferon receptor. Cell Host Microbe 5, 72-83
18. Gauzzi, M. C., Velazquez, L., McKendry, R., Mogensen, K. E., Fellous, M., and Pellegrini, S. (1996) Interferon-alpha-dependent activation of Tyk2 requires phosphorylation of positive regulatory tyrosines by another kinase. J. Biol. Chem. 271, 20494-20500
19. Marijanovic, Z., Ragimbeau, J., Kumar, K. G., Fuchs, S. Y., and Pellegrini, S. (2006) TYK2 activity promotes ligand-induced IFNAR1 proteolysis. Biochem. J. 397, 31-38
20. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J. Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., and Cardona, A. (2012) Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682
21. Belgnaoui, S. M., Gosden, R. G., Semmes, O. J., and Haoudi, A. (2006) Human LINE-1 retrotransposon induces DNA damage and apoptosis in cancer cells. Cancer Cell Int. 6, 13
22. Frost, R. J., Hamra, F. K., Richardson, J. A., Qi, X., Bassel-Duby, R., and Olson, E. N. (2010) MOV10L1 is necessary for protection of spermatocytes against retrotransposons by Piwi-interacting RNAs. Proc. Natl. Acad. Sci. U. S.A. 107, 11847-11852
23. Zheng, K., Xiol, J., Reuter, M., Eckardt, S., Leu, N. A., McLaughlin, K. J., Stark, A., Sachidanandam, R., Pillai, R. S., and Wang, P. J. (2010) Mouse MOV10L1 associates with Piwi proteins and is an essential component of the Piwi-interacting RNA (piRNA) pathway. Proc. Natl. Acad. Sci. U. S.A. 107, 11841-11846
24. Wallace, N. A., Belancio, V. P., and Deininger, P. L. (2008) L1 mobile element expression causes multiple types of toxicity. Gene 419, 75-81
25. Gilbert, N., Lutz, S., Morrish, T. A., and Moran, J. V. (2005) Multiple fates of L1 retrotransposition intermediates in cultured human cells. Mol. Cell. Biol. 25, 7780-7795
26. Gasior, S. L., Wakeman, T. P., Xu, B., and Deininger, P. L. (2006) The human LINE-1 retrotransposon creates DNA double-strand breaks. J. Mol. Biol. 357, 1383-1393
27. Kim, T., Kim, T. Y., Song, Y. H., Min, I. M., Yim, J., and Kim, T. K. (1999) Activation of interferon regulatory factor 3 in response to DNA-damaging agents. J. Biol. Chem. 274, 30686-30689
28. Brzostek-Racine, S., Gordon, C., Van Scoy, S., and Reich, N. C. (2011) The DNA damage response induces IFN. J. Immunol. 187, 5336-5345
29. Morrish, T. A., Garcia-Perez, J. L., Stamato, T. D., Taccioli, G. E., Sekiguchi, J., and Moran, J. V. (2007) Endonuclease-independent LINE-1 retrotransposition at mammalian telomeres. Nature 446, 208-212
30. Farkash, E. A., Kao, G. D., Horman, S. R., and Prak, E. T. (2006) Gamma radiation increases endonuclease-dependent L1 retrotransposition in a cultured cell assay. Nucleic Acids Res. 34, 1196-1204
31. Schoggins, J. W., Wilson, S. J., Panis, M., Murphy, M. Y., Jones, C. T., Bieniasz, P., and Rice, C. M. (2011) A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472, 481-485
32. Goodier, J. L., Cheung, L. E., and Kazazian, H. H., Jr. (2012) MOV10 RNA helicase is a potent inhibitor of retrotransposition in cells. PLoS Genet 8, e1002941
33. Zhang, A., Dong, B., Doucet, A. J., Moldovan, J. B., Moran, J. V., and Silverman, R. H. (2014) RNase L restricts the mobility of engineered retrotransposons in cultured human cells. Nucleic Acids Res. 42, 3803-3820
34. Bridge, A. J., Pebernard, S., Ducraux, A., Nicoulaz, A. L., and Iggo, R. (2003) Induction of an interferon response by RNAi vectors in mammalian cells. Nature Genetics 34, 263-264
35. McKendry, R., John, J., Flavell, D., Müller, M., Kerr, I. M., and Stark, G. R. (1991) High-frequency mutagenesis of human cells and characterization of a mutant unresponsive to both α and γ interferons. Proc. Natl. Acad. Sci. U. S.A. 88, 11455-11459
36. Galligan, C. L., Murooka, T. T., Rahbar, R., Baig, E., Majchrzak-Kita, B., and Fish, E. N. (2006) Interferons and viruses: signaling for supremacy. Immunol. Res. 35, 27-40
37. Furano, A. V. (2000) The biological properties and evolutionary dynamics of mammalian LINE-1 retrotransposons. Progr. Nucleic Acid Res. Mol. Biol. 64, 255-294
38. Leonova, K. I., Brodsky, L., Lipchick, B., Pal, M., Novototskaya, L., Chenchik, A. A., Sen, G. C., Komarova, E. A., and Gudkov, A. V. (2013) p53 cooperates with DNA methylation and a suicidal interferon response to maintain epigenetic silencing of repeats and noncoding RNAs. Proc. Natl. Acad. Sci. U. S.A. 110, E89-E98
39. Moiseeva, O., Mallette, F. A., Mukhopadhyay, U. K., Moores, A., and Ferbeyre, G. (2006) DNA damage signaling and p53-dependent senescence after prolonged β-interferon stimulation. Mol. Biol. Cell 17, 1583-1592
40. Takaoka, A., Hayakawa, S., Yanai, H., Stoiber, D., Negishi, H., Kikuchi, H., Sasaki, S., Imai, K., Shibue, T., Honda, K., and Taniguchi, T. (2003) Integration of interferon-α/β signalling to p53 responses in tumour suppression and antiviral defence. Nature 424, 516-523
41. Muñoz-Fontela, C., Macip, S., Martínez-Sobrido, L., Brown, L., Ashour, J., García-Sastre, A., Lee, S. W., and Aaronson, S. A. (2008) Transcriptional role of p53 in interferon-mediated antiviral immunity. J. Exp. Med. 205, 1929-1938
42. Bonvin, M., Achermann, F., Greeve, I., Stroka, D., Keogh, A., Inderbitzin, D., Candinas, D., Sommer, P., Wain-Hobson, S., Vartanian, J. P., and Greeve, J. (2006) Interferon-inducible expression of APOBEC3 editing enzymes in human hepatocytes and inhibition of hepatitis B virus replication. Hepatology 43, 1364-1374
43. Tanaka, Y., Marusawa, H., Seno, H., Matsumoto, Y., Ueda, Y., Kodama, Y., Endo, Y., Yamauchi, J., Matsumoto, T., Takaori-Kondo, A., Ikai, I., and Chiba, T. (2006) Anti-viral protein APOBEC3G is induced by interferon-α stimulation in human hepatocytes. Biochem. Biophys. Res. Commun. 341, 314-319
44. Lovsin, N., and Peterlin, B. M. (2009) APOBEC3 proteins inhibit LINE-1 retrotransposition in the absence of ORF1p binding. Ann. N.Y. Acad. Sci. 1178, 268-275
45. Niewiadomska, A. M., Tian, C., Tan, L., Wang, T., Sarkis, P. T., and Yu, X. F. (2007) Differential inhibition of long interspersed element 1 by APOBEC3 does not correlate with high-molecular-mass-complex formation or P-body association. J. Virol. 81, 9577-9583
46. Esnault, C., Heidmann, O., Delebecque, F., Dewannieux, M., Ribet, D., Hance, A. J., Heidmann, T., and Schwartz, O. (2005) APOBEC3G cytidine deaminase inhibits retrotransposition of endogenous retroviruses. Nature 433, 430-433
47. Peng, G., Lei, K. J., Jin, W., Greenwell-Wild, T., and Wahl, S. M. (2006) Induction of APOBEC3 family proteins, a defensive maneuver underlying interferon-induced anti-HIV-1 activity. J. Exp. Med. 203, 41-46
48. Nakkuntod, J., Avihingsanon, Y., Mutirangura, A., and Hirankarn, N. (2011) Hypomethylation of LINE-1 but not Alu in lymphocyte subsets of systemic lupus erythematosus patients. Clin. Chim. Acta 412, 1457-1461
49. Crow, M. K. (2010) Long interspersed nuclear elements (LINE-1): potential triggers of systemic autoimmune disease. Autoimmunity 43, 7-16
50. Bronson, P. G., Chaivorapol, C., Ortmann, W., Behrens, T. W., and Graham, R. R. (2012) The genetics of type I interferon in systemic lupus erythematosus. Curr. Opin. Immunol. 24, 530-537
51. Elkon, K. B., and Wiedeman, A. (2012) Type I IFN system in the development and manifestations of SLE. Curr. Opin. Rheumatol. 24, 499-505