G9a regulates group 2 innate lymphoid cell development by repressing the group 3 innate lymphoid cell program

Journal of Experimental Medicine

Volumn 213, Issue 7, 2016, Pages 1153-1162

  Antignano, Frann ^a   Braam, Mitchell ^a   Hughes, Michael R ^a   Chenery, Alistair L ^a   Burrows, Kyle ^a   Gold, Matthew J ^a   Oudhoff, Menno J ^a   Rattray, David ^a   Halim, Timotheus Y ^b   Cait, Alissa ^a   Takei, Fumio ^b   Rossi, Fabio M ^a   McNagny, Kelly M ^a   Zaph, Colby ^a,c  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b BRITISH COLUMBIA CANCER AGENCY   (Canada)

^c MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE 3 LYSINE 9; HISTONE H3; LYSINE METHYLTRANSFERASE G9A; METHYLTRANSFERASE; UNCLASSIFIED DRUG; G9A PROTEIN, MOUSE; HISTONE; HISTONE LYSINE METHYLTRANSFERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL FUNCTION; CELL MATURATION; CELL POPULATION; CELL SPECIFICITY; CONTROLLED STUDY; DEMETHYLATION; ENZYME ACTIVITY; EPIGENETICS; GENE; GENE EXPRESSION; GENE LOCUS; GENE REPRESSION; GENE SILENCING; HEMATOPOIETIC CELL; HISTONE METHYLATION; INFLAMMATION; LYMPHOID CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; ANIMAL; GENE DELETION; GENETIC EPIGENESIS; GENETICS; HEMATOPOIETIC STEM CELL; IMMUNOLOGY; INNATE IMMUNITY; KNOCKOUT MOUSE; LYMPHOCYTE; PHYSIOLOGY;

ANIMALS; EPIGENESIS, GENETIC; GENE DELETION; HEMATOPOIETIC STEM CELLS; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; IMMUNITY, INNATE; LYMPHOCYTES; MICE; MICE, KNOCKOUT;

EID: 84977605156     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20151646     Document Type: Article

References (34)

1. Antignano, F., K. Burrows, M.R. Hughes, J.M. Han, K.J. Kron, N.M. Penrod, M.J. Oudhoff, S.K. Wang, P.H. Min, M.J. Gold, et al. 2014. Methyltransferase G9A regulates T cell differentiation during murine intestinal inflammation. J. Clin. Invest. 124:1945-1955. http://dx.doi.org/10.1172/JCI69592
2. Califano, D., J.J. Cho, M.N. Uddin, K.J. Lorentsen, Q. Yang, A. Bhandoola, H. Li, and D. Avram. 2015. Transcription factor Bcl11b controls identity and function of mature type 2 innate lymphoid cells. Immunity. 43:354-368. http://dx.doi.org/10.1016/j.immuni.2015.07.005
3. Chen, J., H. Liu, J. Liu, J. Qi, B. Wei, J. Yang, H. Liang, Y. Chen, J. Chen, Y. Wu, et al. 2012. H3K9 methylation is a barrier during somatic cell reprogramming into iPSCs. Nat. Genet. 45:34-42. http://dx.doi.org/10.1038/ng.2491
4. Cherrier, M., S. Sawa, and G. Eberl. 2012. Notch, Id2, and RORγt sequentially orchestrate the fetal development of lymphoid tissue inducer cells. J. Exp. Med. 209:729-740. http://dx.doi.org/10.1084/jem.20111594
5. Constantinides, M.G., B.D. McDonald, P.A. Verhoef, and A. Bendelac. 2014. A committed precursor to innate lymphoid cells. Nature. 508:397-401. http://dx.doi.org/10.1038/nature13047
6. Dong, K.B., I.A. Maksakova, F. Mohn, D. Leung, R. Appanah, S. Lee, H.W. Yang, L.L. Lam, D.L. Mager, D. Schübeler, et al. 2008. DNA methylation in ES cells requires the lysine methyltransferase G9a but not its catalytic activity. EMBO J. 27:2691-2701. http://dx.doi.org/10.1038/emboj.2008.193
7. Duan, Z., A. Zarebski, D. Montoya-Durango, H.L. Grimes, and M. Horwitz. 2005. Gfi1 coordinates epigenetic repression of p21Cip/WAF1 by recruitment of histone lysine methyltransferase G9a and histone deacetylase 1. Mol. Cell. Biol. 25:10338-10351. http://dx.doi.org/10.1128/MCB.25.23.10338-10351.2005
8. Eberl, G., S. Marmon, M.J. Sunshine, P.D. Rennert, Y. Choi, and D.R. Littman. 2004. An essential function for the nuclear receptor RORγt in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 5:64-73. http://dx.doi.org/10.1038/ni1022
9. H2-inducing allergen exposures. J. Allergy Clin. Immunol. 133:1142-1148.e5. http://dx.doi.org/10.1016/j.jaci.2014.02.033
10. Halim, T.Y., R.H. Krauss, A.C. Sun, and F. Takei. 2012a. Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergeninduced airway inflammation. Immunity. 36:451-463. http://dx.doi.org/10.1016/j.immuni.2011.12.020
11. Halim, T.Y., A. MacLaren, M.T. Romanish, M.J. Gold, K.M. McNagny, and F. Takei. 2012b. Retinoic-acid-receptor-related orphan nuclear receptor alpha is required for natural helper cell development and allergic inflammation. Immunity. 37:463-474. http://dx.doi.org/10.1016/j.immuni.2012.06.012
12. Halim, T.Y., C.A. Steer, L. Mathä, M.J. Gold, I. Martinez-Gonzalez, K.M. McNagny, A.N. McKenzie, and F. Takei. 2014. Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity. 40:425-435. http://dx.doi.org/10.1016/j.immuni.2014.01.011
13. Hoyler, T., C.S. Klose, A. Souabni, A. Turqueti-Neves, D. Pfeifer, E.L. Rawlins, D. Voehringer, M. Busslinger, and A. Diefenbach. 2012. The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity. 37:634-648. http://dx.doi.org/10.1016/j.immuni.2012.06.020
14. Klose, C.S., M. Flach, L. Möhle, L. Rogell, T. Hoyler, K. Ebert, C. Fabiunke, D. Pfeifer, V. Sexl, D. Fonseca-Pereira, et al. 2014. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell. 157:340-356. http://dx.doi.org/10.1016/j.cell.2014.03.030
15. Kurebayashi, S., E. Ueda, M. Sakaue, D.D. Patel, A. Medvedev, F. Zhang, and A.M. Jetten. 2000. Retinoid-related orphan receptor γ (RORγ) is essential for lymphoid organogenesis and controls apoptosis during thymopoiesis. Proc. Natl. Acad. Sci. USA. 97:10132-10137. http://dx.doi.org/10.1073/pnas.97.18.10132
16. Lehnertz, B., J.P. Northrop, F. Antignano, K. Burrows, S. Hadidi, S.C. Mullaly, F.M. Rossi, and C. Zaph. 2010. Activating and inhibitory functions for the histone lysine methyltransferase G9a in T helper cell differentiation and function. J. Exp. Med. 207:915-922. http://dx.doi.org/10.1084/jem.20100363
17. + lymphoid cells. Nature. 463:540-544. http://dx.doi.org/10.1038/nature08636
18. Neill, D.R., S.H. Wong, A. Bellosi, R.J. Flynn, M. Daly, T.K. Langford, C. Bucks, C.M. Kane, P.G. Fallon, R. Pannell, et al. 2010. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature. 464:1367-1370. http://dx.doi.org/10.1038/nature08900
19. Oboki, K., T. Ohno, N. Kajiwara, K. Arae, H. Morita, A. Ishii, A. Nambu, T. Abe, H. Kiyonari, K. Matsumoto, et al. 2010. IL-33 is a crucial amplifier of innate rather than acquired immunity. Proc. Natl. Acad. Sci. USA. 107:18581-18586. http://dx.doi.org/10.1073/pnas.1003059107
20. + innate lymphoid cells. Nat. Immunol. 12:949-958. http://dx.doi.org/10.1038/ni.2105
21. Price, A.E., H.E. Liang, B.M. Sullivan, R.L. Reinhardt, C.J. Eisley, D.J. Erle, and R.M. Locksley. 2010. Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc. Natl. Acad. Sci. USA. 107:11489-11494. http://dx.doi.org/10.1073/pnas.1003988107
22. Robinette, M.L., A. Fuchs, V.S. Cortez, J.S. Lee, Y. Wang, S.K. Durum, S. Gilfillan, and M. Colonna. Immunological Genome Consortium. 2015. Transcriptional programs define molecular characteristics of innate lymphoid cell classes and subsets. Nat. Immunol. 16:306-317. http://dx.doi.org/10.1038/ni.3094
23. + cells. Nat. Immunol. 10:83-91. http://dx.doi.org/10.1038/ni.1684
24. + cell subsets from Id2-dependent precursors. J. Exp. Med. 207:273-280. http://dx.doi.org/10.1084/jem.20092029
25. + group 3 innate lymphoid cells. J. Exp. Med. 211:199-208. http://dx.doi.org/10.1084/jem.20131038
26. Spooner, C.J., J. Lesch, D. Yan, A.A. Khan, A. Abbas, V. Ramirez-Carrozzi, M. Zhou, R. Soriano, J. Eastham-Anderson, L. Diehl, et al. 2013. Specification of type 2 innate lymphocytes by the transcriptional determinant Gfi1. Nat. Immunol. 14:1229-1236. http://dx.doi.org/10.1038/ni.2743
27. Sun, Z., D. Unutmaz, Y.R. Zou, M.J. Sunshine, A. Pierani, S. Brenner-Morton, R.E. Mebius, and D.R. Littman. 2000. Requirement for RORγ in thymocyte survival and lymphoid organ development. Science. 288:2369-2373. http://dx.doi.org/10.1126/science.288.5475.2369
28. Tachibana, M., K. Sugimoto, M. Nozaki, J. Ueda, T. Ohta, M. Ohki, M. Fukuda, N. Takeda, H. Niida, H. Kato, and Y. Shinkai. 2002. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 16:1779-1791. http://dx.doi.org/10.1101/gad.989402
29. Vedadi, M., D. Barsyte-Lovejoy, F. Liu, S. Rival-Gervier, A. Allali-Hassani, V. Labrie, T.J. Wigle, P.A. Dimaggio, G.A. Wasney, A. Siarheyeva, et al. 2011. A chemical probe selectively inhibits G9a and GLP methyltransferase activity in cells. Nat. Chem. Biol. 7:566-574. http://dx.doi.org/10.1038/nchembio.599
30. Wen, B., H. Wu, Y. Shinkai, R.A. Irizarry, and A.P. Feinberg. 2009. Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nat. Genet. 41:246-250. http://dx.doi.org/10.1038/ng.297
31. Wong, S.H., J.A. Walker, H.E. Jolin, L.F. Drynan, E. Hams, A. Camelo, J.L. Barlow, D.R. Neill, V. Panova, U. Koch, et al. 2012. Transcription factor RORa is critical for nuocyte development. Nat. Immunol. 13:229-236. http://dx.doi.org/10.1038/ni.2208
32. Yagi, R., C. Zhong, D.L. Northrup, F. Yu, N. Bouladoux, S. Spencer, G. Hu, L. Barron, S. Sharma, T. Nakayama, et al. 2014. The transcription factor GATA3 is critical for the development of all IL-7Rα-expressing innate lymphoid cells. Immunity. 40:378-388. http://dx.doi.org/10.1016/j.immuni.2014.01.012
33. Yang, Q., L.A. Monticelli, S.A. Saenz, A.W. Chi, G.F. Sonnenberg, J. Tang, M.E. De Obaldia, W. Bailis, J.L. Bryson, K. Toscano, et al. 2013. T cell factor 1 is required for group 2 innate lymphoid cell generation. Immunity. 38:694-704. http://dx.doi.org/10.1016/j.immuni.2012.12.003
34. Younesy, H., T. Möller, M.C. Lorincz, M.M. Karimi, and S.J. Jones. 2015. VisRseq: R-based visual framework for analysis of sequencing data. BMC Bioinformatics. 16:S2. http://dx.doi.org/10.1186/1471-2105-16-S11-S2