Retrotransposon derepression leads to activation of the unfolded protein response and apoptosis in pro-B cells

Development (Cambridge)

Volumn 143, Issue 10, 2016, Pages 1788-1799

  Pasquarella, Alessandra ^a   Ebert, Anja ^b   de Almeida, Gustavo Pereira ^a   Hinterberger, Maria ^c   Kazerani, Maryam ^a   Nuber, Alexander ^a   Ellwart, Joachim ^d   Klein, Ludger ^c   Busslinger, Meinrad ^b   Schotta, Gunnar ^a  

^a Munich Center for Integrated Protein Science   (Germany)

^b RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^c UNIVERSITY OF MUNICH   (Germany)

^d INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Heterochromatin; Mouse; Retrotransposon; Setdb1; Unfolded protein response

Indexed keywords

DNA; HISTONE H3; HISTONE METHYLTRANSFERASE; HISTONE METHYLTRANSFERASE SETDB1; LYSINE; PROTEIN; UNCLASSIFIED DRUG; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; RETROPOSON; SETDB1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL MATURATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA METHYLATION; GENE EXPRESSION; GENE LOSS; GENE REPRESSION; GENE SEQUENCE; GENE SILENCING; HISTONE METHYLATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MURINE LEUKEMIA VIRUS; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; RETROPOSON; UNFOLDED PROTEIN RESPONSE; VIRUS STRAIN; ANIMAL; CYTOLOGY; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; METHYLATION; NUCLEOTIDE REPEAT;

ANIMALS; APOPTOSIS; GENE EXPRESSION PROFILING; GENE SILENCING; HEK293 CELLS; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; LEUKEMIA VIRUS, MURINE; LYSINE; METHYLATION; MICE; PRECURSOR CELLS, B-LYMPHOID; REPETITIVE SEQUENCES, NUCLEIC ACID; RETROELEMENTS; TRANSCRIPTION, GENETIC; UNFOLDED PROTEIN RESPONSE;

EID: 84968779632     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.130203     Document Type: Article

References (41)

1. Beguelin,W., Popovic, R., Teater, M., Jiang, Y., Bunting, K. L., Rosen, M., Shen, H., Yang, S. N., Wang, L., Ezponda, T. et al. (2013). EZH2 is required for germinal center formation and somatic EZH2 mutations promote lymphoid transformation. Cancer Cell 23, 677-692.
2. Beissbarth, T. and Speed, T. P. (2004). GOstat: find statistically overrepresented Gene Ontologies within a group of genes. Bioinformatics 20, 1464-1465.
3. Bilodeau, S., Kagey, M. H., Frampton, G. M., Rahl, P. B. and Young, R. A. (2009). SetDB1 contributes to repression of genes encoding developmental regulators and maintenance of ES cell state. Genes Dev. 23, 2484-2489.
4. Bourc'his, D. and Bestor, T. H. (2004). Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431, 96-99.
5. Brewer, J.W. and Hendershot, L. M. (2005). Building an antibody factory: a job for the unfolded protein response. Nat. Immunol. 6, 23-29.
6. Brownlie, R. J., Lawlor, K. E., Niederer, H. A., Cutler, A. J., Xiang, Z., Clatworthy, M. R., Floto, R. A., Greaves, D. R., Lyons, P. A. and Smith, K. G. (2008). Distinct cell-specific control of autoimmunity and infection by FcgammaRIIb. J. Exp. Med. 205, 883-895.
7. Bulut-Karslioglu, A., De La Rosa-Velazquez, I. A., Ramirez, F., Barenboim, M., Onishi-Seebacher, M., Arand, J., Galan, C.,Winter, G. E., Engist, B., Gerle, B. et al. (2014). Suv39h-dependent H3K9me3 marks intact retrotransposons and silences LINE elements in mouse embryonic stem cells. Mol. Cell 55, 277-290.
8. Calfon, M., Zeng, H., Urano, F., Till, J. H., Hubbard, S. R., Harding, H. P., Clark, S. G. and Ron, D. (2002). IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415, 92-96.
9. Collins, P. L., Kyle, K. E., Egawa, T., Shinkai, Y. and Oltz, E. M. (2015). The histone methyltransferase SETDB1 represses endogenous and exogenous retroviruses in B lymphocytes. Proc. Natl. Acad. Sci. USA 112, 8367-8372.
10. Dodge, J. E., Kang, Y.-K., Beppu, H., Lei, H. and Li, E. (2004). Histone H3-K9 methyltransferase ESET is essential for early development. Mol. Cell. Biol. 24, 2478-2486.
11. Egle, A., Harris, A. W., Bath, M. L., O'Reilly, L. and Cory, S. (2004). VavP-Bcl2 transgenic mice develop follicular lymphoma preceded by germinal center hyperplasia. Blood 103, 2276-2283.
12. Evans, L. H., Morrison, R. P., Malik, F. G., Portis, J. and Britt, W. J. (1990). A neutralizable epitope common to the envelope glycoproteins of ecotropic, polytropic, xenotropic, and amphotropic murine leukemia viruses. J. Virol. 64, 6176-6183.
13. Finstad, S. L., Rosenberg, N. and Levy, L. S. (2007). Diminished potential for Blymphoid differentiation after murine leukemia virus infection in vivo and in EML hematopoietic progenitor cells. J. Virol. 81, 7274-7279.
14. Gass, J. N., Gunn, K. E., Sriburi, R. and Brewer, J. W. (2004). Stressed-out B cells? Plasma-cell differentiation and the unfolded protein response. Trends Immunol. 25, 17-24.
15. Groenendyk, J., Peng, Z., Dudek, E., Fan, X., Mizianty, M. J., Dufey, E., Urra, H., Sepulveda, D., Rojas-Rivera, D., Lim, Y. et al. (2014). Interplay between the oxidoreductase PDIA6 and microRNA-322 controls the response to disrupted endoplasmic reticulum calcium homeostasis. Sci. Signal. 7, ra54.
16. Hardy, R. R., Carmack, C. E., Shinton, S. A., Kemp, J. D. and Hayakawa, K. (1991). Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J. Exp. Med. 173, 1213-1225.
17. Heng, T. S. P., Painter, M. W. and The Immunological Genome Project Consortium. (2008). The Immunological Genome Project: networks of gene expression in immune cells. Nat. Immunol. 9, 1091-1094.
18. Hobeika, E., Thiemann, S., Storch, B., Jumaa, H., Nielsen, P. J., Pelanda, R. and Reth, M. (2006). Testing gene function early in the B cell lineage in mb1-cre mice. Proc. Natl. Acad. Sci. USA 103, 13789-13794.
19. Holmes, R. and Zuniga-Pflucker, J. C. (2009). The OP9-DL1 system: generation of T-lymphocytes from embryonic or hematopoietic stem cells in vitro. Cold Spring Harb. Protoc. 2009, pdb.prot5156.
20. Jojic, V., Shay, T., Sylvia, K., Zuk, O., Sun, X., Kang, J., Regev, A., Koller, D., The Immunological Genome Project Consortium, Best, A. J. et al. (2013). Identification of transcriptional regulators in the mouse immune system. Nat. Immunol. 14, 633-643.
21. Karimi, M. M., Goyal, P., Maksakova, I. A., Bilenky, M., Leung, D., Tang, J. X., Shinkai, Y., Mager, D. L., Jones, S., Hirst, M. et al. (2011). DNA methylation and SETDB1/H3K9me3 regulate predominantly distinct sets of genes, retroelements, and chimeric transcripts in mESCs. Cell Stem Cell 8, 676-687.
22. Lawson, K. A., Teteak, C. J., Gao, J., Li, N., Hacquebord, J., Ghatan, A., Zielinska-Kwiatkowska, A., Song, G., Chansky, H. A. and Yang, L. (2013). ESET histone methyltransferase regulates osteoblastic differentiation of mesenchymal stem cells during postnatal bone development. FEBS Lett. 587, 3961-3967.
23. Lee, A. S. (2005). The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. Methods 35, 373-381.
24. Lee, E., Iskow, R., Yang, L., Gokcumen, O., Haseley, P., Luquette, L. J., III, Lohr, J. G., Harris, C. C., Ding, L., Wilson, R. K. et al. (2012). Landscape of somatic retrotransposition in human cancers. Science 337, 967-971.
25. Martin, F. J., Xu, Y., Lohmann, F., Ciccone, D. N., Nicholson, T. B., Loureiro, J. J., Chen, T. and Huang, Q. (2015). KMT1E-mediated chromatin modifications at the FcgammaRIIb promoter regulate thymocyte development. Genes Immun. 16, 162-169.
26. Matsui, T., Leung, D., Miyashita, H., Maksakova, I. A., Miyachi, H., Kimura, H., Tachibana, M., Lorincz, M. C. and Shinkai, Y. (2010). Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 464, 927-931.
27. Puthalakath, H., O'Reilly, L. A., Gunn, P., Lee, L., Kelly, P. N., Huntington, N. D., Hughes, P. D., Michalak, E. M., McKimm-Breschkin, J., Motoyama, N. et al. (2007). ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 129, 1337-1349.
28. Regha, K., Sloane, M. A., Huang, R., Pauler, F. M., Warczok, K. E., Melikant, B., Radolf, M., Martens, J. H. A., Schotta, G., Jenuwein, T. et al. (2007). Active and repressive chromatin are interspersed without spreading in an imprinted gene cluster in the mammalian genome. Mol. Cell 27, 353-366.
29. Roulois, D., Loo Yau, H., Singhania, R.,Wang, Y., Danesh, A., Shen, S. Y., Han, H., Liang, G., Jones, P. A., Pugh, T. J. et al. (2015). DNA-demethylating agents target colorectal cancer cells by inducing viral mimicry by endogenous transcripts. Cell 162, 961-973.
30. Sadic, D., Schmidt, K., Groh, S., Kondofersky, I., Ellwart, J., Fuchs, C., Theis, F. J. and Schotta, G. (2015). Atrx promotes heterochromatin formation at retrotransposons. EMBO Rep. 16, 836-850.
31. Santoni de Sio, F. R., Massacand, J., Barde, I., Offner, S., Corsinotti, A., Kapopoulou, A., Bojkowska, K., Dagklis, A., Fernandez, M., Ghia, P. et al. (2012). KAP1 regulates gene networks controlling mouse B-lymphoid cell differentiation and function. Blood 119, 4675-4685.
32. Schwickert, T. A., Tagoh, H., Gultekin, S., Dakic, A., Axelsson, E., Minnich, M., Ebert, A.,Werner, B., Roth, M., Cimmino, L. et al. (2014). Stage-specific control of early B cell development by the transcription factor Ikaros. Nat. Immunol. 15, 283-293.
33. Su, I.-H., Basavaraj, A., Krutchinsky, A. N., Hobert, O., Ullrich, A., Chait, B. T. and Tarakhovsky, A. (2003). Ezh2 controls B cell development through histone H3 methylation and Igh rearrangement. Nat. Immunol. 4, 124-131.
34. Tan, S.-L., Nishi, M., Ohtsuka, T., Matsui, T., Takemoto, K., Kamio-Miura, A., Aburatani, H., Shinkai, Y. and Kageyama, R. (2012). Essential roles of the histone methyltransferase ESET in the epigenetic control of neural progenitor cells during development. Development 139, 3806-3816.
35. Xie, D., Chen, C.-C., Ptaszek, L. M., Xiao, S., Cao, X., Fang, F., Ng, H. H., Lewin, H. A., Cowan, C. and Zhong, S. (2010). Rewirable gene regulatory networks in the preimplantation embryonic development of three mammalian species. Genome Res. 20, 804-815.
36. Xie, M., Hong, C., Zhang, B., Lowdon, R. F., Xing, X., Li, D., Zhou, X., Lee, H. J., Maire, C. L., Ligon, K. L. et al. (2013). DNA hypomethylation within specific transposable element families associates with tissue-specific enhancer landscape. Nat. Genet. 45, 836-841.
37. Yang, L., Lawson, K. A., Teteak, C. J., Zou, J., Hacquebord, J., Patterson, D., Ghatan, A. C., Mei, Q., Zielinska-Kwiatkowska, A., Bain, S. D. et al. (2013). ESET histone methyltransferase is essential to hypertrophic differentiation of growth plate chondrocytes and formation of epiphyseal plates. Dev. Biol. 380, 99-110.
38. Young, G. R., Eksmond, U., Salcedo, R., Alexopoulou, L., Stoye, J. P. and Kassiotis, G. (2012). Resurrection of endogenous retroviruses in antibodydeficient mice. Nature 491, 774-778.
39. Yuan, P., Han, J., Guo, G., Orlov, Y. L., Huss, M., Loh, Y.-H., Yaw, L.-P., Robson, P., Lim, B. and Ng, H.-H. (2009). Eset partners with Oct4 to restrict extraembryonic trophoblast lineage potential in embryonic stem cells. Genes Dev. 23, 2507-2520.
40. Zhang, K.,Wong, H. N., Song, B., Miller, C. N., Scheuner, D. and Kaufman, R. J. (2005). The unfolded protein response sensor IRE1alpha is required at 2 distinct steps in B cell lymphopoiesis. J. Clin. Invest. 115, 268-281.
41. Zhao, X. and Yoshimura, F. K. (2008). Expression of murine leukemia virus envelope protein is sufficient for the induction of apoptosis. J. Virol. 82, 2586-2589.