Requirement for Dicer in survival of proliferating thymocytes experiencing DNA double-strand breaks

Journal of Immunology

Volumn 190, Issue 7, 2013, Pages 3256-3266

  Brady, Brenna L ^a,b,c,d   Rupp, Levi J ^a,b,c   Bassing, Craig H ^a,b,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DICER; LYMPHOCYTE ANTIGEN RECEPTOR; PROTEIN BCL 2; T LYMPHOCYTE RECEPTOR BETA CHAIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; GENE DELETION; GENE LOCUS; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; T LYMPHOCYTE RECEPTOR BETA GENE; THYMOCYTE;

ANIMALS; CELL SURVIVAL; DNA BREAKS, DOUBLE-STRANDED; MICE; MICE, KNOCKOUT; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECOMBINATION, GENETIC; RIBONUCLEASE III; THYMOCYTES;

EID: 84875431073     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200957     Document Type: Article

References (50)

1. Grewal, S. I., and S. Jia. 2007. Heterochromatin revisited. Nat. Rev. Genet. 8: 35-46.
2. Bushati, N., and S. M. Cohen. 2007. microRNA functions. Annu. Rev. Cell Dev. Biol. 23: 175-205.
3. Bernstein, E., S. Y. Kim, M. A. Carmell, E. P. Murchison, H. Alcorn, M. Z. Li, A. A. Mills, S. J. Elledge, K. V. Anderson, and G. J. Hannon. 2003. Dicer is essential for mouse development. Nat. Genet. 35: 215-217.
4. Xiao, C., and K. Rajewsky. 2009. MicroRNA control in the immune system: basic principles. Cell 136: 26-36.
5. Tam, O. H., A. A. Aravin, P. Stein, A. Girard, E. P. Murchison, S. Cheloufi, E. Hodges, M. Anger, R. Sachidanandam, R. M. Schultz, and G. J. Hannon. 2008. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453: 534-538.
6. Watanabe, T., Y. Totoki, A. Toyoda, M. Kaneda, S. Kuramochi-Miyagawa, Y. Obata, H. Chiba, Y. Kohara, T. Kono, T. Nakano, et al. 2008. Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453: 539-543.
7. Brady, B. L., N. C. Steinel, and C. H. Bassing. 2010. Antigen receptor allelic exclusion: an update and reappraisal. J. Immunol. 185: 3801-3808.
8. Cobb, B. S., T. B. Nesterova, E. Thompson, A. Hertweck, E. O'Connor, J. Godwin, C. B. Wilson, N. Brockdorff, A. G. Fisher, S. T. Smale, and M. Merkenschlager. 2005. T cell lineage choice and differentiation in the absence of the RNase III enzyme Dicer. J. Exp. Med. 201: 1367-1373.
9. Chong, M. M., G. Zhang, S. Cheloufi, T. A. Neubert, G. J. Hannon, and D. R. Littman. 2010. Canonical and alternate functions of the microRNA biogenesis machinery. Genes Dev. 24: 1951-1960.
10. Koralov, S. B., S. A. Muljo, G. R. Galler, A. Krek, T. Chakraborty, C. Kanellopoulou, K. Jensen, B. S. Cobb, M. Merkenschlager, N. Rajewsky, and K. Rajewsky. 2008. Dicer ablation affects antibody diversity and cell survival in the B lymphocyte lineage. Cell 132: 860-874.
11. Chakraborty, T., D. Chowdhury, A. Keyes, A. Jani, R. Subrahmanyam, I. Ivanova, and R. Sen. 2007. Repeat organization and epigenetic regulation of the DH-Cmu domain of the immunoglobulin heavy-chain gene locus. Mol. Cell 27: 842-850.
12. Giallourakis, C., F. W. Alt, and C. H. Bassing. 2004. V(D)J recombinational accessibility-heading in the opposite direction? Nat. Immunol. 5: 561-562.
13. Belver, L., V. G. de Yébenes, and A. R. Ramiro. 2010. MicroRNAs prevent the generation of autoreactive antibodies. Immunity 33: 713-722.
14. Shinkai, Y., G. Rathbun, K. P. Lam, E. M. Oltz, V. Stewart, M. Mendelsohn, J. Charron, M. Datta, F. Young, A. M. Stall, et al. 1992. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68: 855-867.
15. Mombaerts, P., J. Iacomini, R. S. Johnson, K. Herrup, S. Tonegawa, and V. E. Papaioannou. 1992. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68: 869-877.
16. Xu, Y., L. Davidson, F. W. Alt, and D. Baltimore. 1996. Function of the pre-Tcell receptor α chain in T-cell development and allelic exclusion at the T-cell receptor β locus. Proc. Natl. Acad. Sci. USA 93: 2169-2173.
17. Fehling, H. J., A. Krotkova, C. Saint-Ruf, and H. von Boehmer. 1995. Crucial role of the pre-T-cell receptor α gene in development of αβ but not γδ T cells. Nature 375: 795-798.
18. Yang-Iott, K. S., A. C. Carpenter, M. A. Rowh, N. Steinel, B. L. Brady, K. Hochedlinger, R. Jaenisch, and C. H. Bassing. 2010. TCR β feedback signals inhibit the coupling of recombinationally accessible Vβ14 segments with DJβ complexes. J. Immunol. 184: 1369-1378.
19. Steinel, N. C., B. L. Brady, A. C. Carpenter, K. S. Yang-Iott, and C. H. Bassing. 2010. Posttranscriptional silencing of VßDJβCβ genes contributes to TCRβ allelic exclusion in mammalian lymphocytes. J. Immunol. 185: 1055-1062.
20. Brady, B. L., and C. H. Bassing. 2011. Differential regulation of proximal and distal Vβ segments upstream of a functional VDJβ1 rearrangement upon β-selection. J. Immunol. 187: 3277-3285.
21. Brady, B. L., M. A. Oropallo, K. S. Yang-Iott, T. Serwold, K. Hochedlinger, R. Jaenisch, I. L. Weissman, and C. H. Bassing. 2010. Position-dependent silencing of germline Vβ segments on TCRβ alleles containing preassembled VßDJβCβ1 genes. J. Immunol. 185: 3564-3573.
22. Lee, P. P., D. R. Fitzpatrick, C. Beard, H. K. Jessup, S. Lehar, K. W. Makar, M. Pérez-Melgosa, M. T. Sweetser, M. S. Schlissel, S. Nguyen, et al. 2001. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15: 763-774.
23. Strasser, A., A. W. Harris, and S. Cory. 1991. Bcl-2 transgene inhibits T cell death and perturbs thymic self-censorship. Cell 67: 889-899.
24. Carpenter, A. C., K. S. Yang-Iott, L. H. Chao, B. Nuskey, S. Whitlow, F. W. Alt, and C. H. Bassing. 2009. Assembled DJβ complexes influence TCRβ chain selection and peripheral Vβ repertoire. J. Immunol. 182: 5586-5595.
25. Shinkai, Y., S. Koyasu, K. Nakayama, K. M. Murphy, D. Y. Loh, E. L. Reinherz, and F. W. Alt. 1993. Restoration of T cell development in RAG-2-deficient mice by functional TCR transgenes. Science 259: 822-825.
26. Godfrey, D. I., J. Kennedy, T. Suda, and A. Zlotnik. 1993. A developmental pathway involving four phenotypically and functionally distinct subsets of CD3- CD4-CD8- triple-negative adult mouse thymocytes defined by CD44 and CD25 expression. J. Immunol. 150: 4244-4252.
27. Bredemeyer, A. L., G. G. Sharma, C. Y. Huang, B. A. Helmink, L. M. Walker, K. C. Khor, B. Nuskey, K. E. Sullivan, T. K. Pandita, C. H. Bassing, and B. P. Sleckman. 2006. ATM stabilizes DNA double-strand-break complexes during V(D)J recombination. Nature 442: 466-470.
28. Strasser, A., A. W. Harris, H. von Boehmer, and S. Cory. 1994. Positive and negative selection of T cells in T-cell receptor transgenic mice expressing a bcl-2 transgene. Proc. Natl. Acad. Sci. USA 91: 1376-1380.
29. von Boehmer, H. 2004. Selection of the T-cell repertoire: receptor-controlled checkpoints in T-cell development. Adv. Immunol. 84: 201-238.
30. Wilson, A., C. Maréchal, and H. R. MacDonald. 2001. Biased Vβ usage in immature thymocytes is independent of DJβ proximity and pTα pairing. J. Immunol. 166: 51-57.
31. Sicinska, E., I. Aifantis, L. Le Cam, W. Swat, C. Borowski, Q. Yu, A. A. Ferrando, S. D. Levin, Y. Geng, H. von Boehmer, and P. Sicinski. 2003. Requirement for cyclin D3 in lymphocyte development and T cell leukemias. Cancer Cell 4: 451-461.
32. Baldwin, T. A., M. M. Sandau, S. C. Jameson, and K. A. Hogquist. 2005. The timing of TCRα expression critically influences T cell development and selection. J. Exp. Med. 202: 111-121.
33. Kraemer, A., N. Anastasov, M. Angermeier, K. Winkler, M. J. Atkinson, and S. Moertl. 2011. MicroRNA-mediated processes are essential for the cellular radiation response. Radiat. Res. 176: 575-586.
34. Bassing, C. H., H. Suh, D. O. Ferguson, K. F. Chua, J. Manis, M. Eckersdorff, M. Gleason, R. Bronson, C. Lee, and F. W. Alt. 2003. Histone H2AX: a dosagedependent suppressor of oncogenic translocations and tumors. Cell 114: 359-370.
35. Baek, D., J. Villén, C. Shin, F. D. Camargo, S. P. Gygi, and D. P. Bartel. 2008. The impact of microRNAs on protein output. Nature 455: 64-71.
36. Selbach, M., B. Schwanhäusser, N. Thierfelder, Z. Fang, R. Khanin, and N. Rajewsky. 2008. Widespread changes in protein synthesis induced by microRNAs. Nature 455: 58-63.
37. Wan, G., R. Mathur, X. Hu, X. Zhang, and X. Lu. 2011. miRNA response to DNA damage. Trends Biochem. Sci. 36: 478-484.
38. Cannell, I. G., Y. W. Kong, S. J. Johnston, M. L. Chen, H. M. Collins, H. C. Dobbyn, A. Elia, T. R. Kress, M. Dickens, M. J. Clemens, et al. 2010. p38 MAPK/MK2-mediated induction of miR-34c following DNA damage prevents Myc-dependent DNA replication. Proc. Natl. Acad. Sci. USA 107: 5375-5380.
39. Pedraza-Alva, G., M. Koulnis, C. Charland, T. Thornton, J. L. Clements, M. S. Schlissel, and M. Rincón. 2006. Activation of p38 MAP kinase by DNA double-strand breaks in V(D)J recombination induces a G2/M cell cycle checkpoint. EMBO J. 25: 763-773.
40. Dujka, M. E., N. Puebla-Osorio, O. Tavana, M. Sang, and C. Zhu. 2010. ATM and p53 are essential in the cell-cycle containment of DNA breaks during V(D)J recombination in vivo. Oncogene 29: 957-965.
41. Francia, S., F. Michelini, A. Saxena, D. Tang, M. de Hoon, V. Anelli, M. Mione, P. Carninci, and F. d'Adda di Fagagna. 2012. Site-specific DICER and DROSHA RNA products control the DNA-damage response. Nature 488: 231-235.
42. Wei, W., Z. Ba, M. Gao, Y. Wu, Y. Ma, S. Amiard, C. I. White, J. M. Rendtlew Danielsen, Y. G. Yang, and Y. Qi. 2012. A role for small RNAs in DNA doublestrand break repair. Cell 149: 101-112.
43. Mak, T. W., A. Hakem, J. P. McPherson, A. Shehabeldin, E. Zablocki, E. Migon, G. S. Duncan, D. Bouchard, A. Wakeham, A. Cheung, et al. 2000. Brca1 required for T cell lineage development but not TCR loci rearrangement. Nat. Immunol. 1: 77-82.
44. Cheung, A. M., M. P. Hande, F. Jalali, M. S. Tsao, B. Skinnider, A. Hirao, J. P. McPherson, J. Karaskova, A. Suzuki, A. Wakeham, et al. 2002. Loss of Brca2 and p53 synergistically promotes genomic instability and deregulation of T-cell apoptosis. Cancer Res. 62: 6194-6204.
45. Babbe, H., N. Chester, P. Leder, and B. Reizis. 2007. The Bloom's syndrome helicase is critical for development and function of the αβ T-cell lineage. Mol. Cell. Biol. 27: 1947-1959.
46. Muljo, S. A., K. M. Ansel, C. Kanellopoulou, D. M. Livingston, A. Rao, and K. Rajewsky. 2005. Aberrant T cell differentiation in the absence of Dicer. J. Exp. Med. 202: 261-269.
47. Cobb, B. S., A. Hertweck, J. Smith, E. O'Connor, D. Graf, T. Cook, S. T. Smale, S. Sakaguchi, F. J. Livesey, A. G. Fisher, and M. Merkenschlager. 2006. A role for Dicer in immune regulation. J. Exp. Med. 203: 2519-2527.
48. Zhang, N., and M. J. Bevan. 2010. Dicer controls CD8+ T-cell activation, migration, and survival. Proc. Natl. Acad. Sci. USA 107: 21629-21634.
49. Chong, M. M., J. P. Rasmussen, A. Y. Rudensky, and D. R. Littman. 2008. The RNAseIII enzyme Drosha is critical in T cells for preventing lethal inflammatory disease. J. Exp. Med. 205: 2005-2017.
50. Zhou, X., L. T. Jeker, B. T. Fife, S. Zhu, M. S. Anderson, M. T. McManus, and J. A. Bluestone. 2008. Selective miRNA disruption in T reg cells leads to uncontrolled autoimmunity. J. Exp. Med. 205: 1983-1991.