MicroRNA-15/16 antagonizes Myb to control NK cell maturation

Journal of Immunology

Volumn 195, Issue 6, 2015, Pages 2806-2817

  Sullivan, Ryan P ^a   Leong, Jeffrey W ^a   Schneider, Stephanie E ^a   Ireland, Aaron R ^a   Berrien Elliott, Melissa M ^a   Singh, Anvita ^a   Schappe, Timothy ^a   Jewell, Brea A ^a   Sexl, Veronika ^b   Fehniger, Todd A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VETERINARY MEDICINE   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CD27 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 18; LEUKOSIALIN; MESSENGER RNA; MICRORNA; MICRORNA 15; MICRORNA 16; PROTEIN C MYB; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; MIRN15 MICRORNA, MOUSE; MIRN16 MICRORNA, MOUSE; SMALL INTERFERING RNA;

3' UNTRANSLATED REGION; ADOPTIVE TRANSFER; ANIMAL CELL; ARTICLE; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DOWN REGULATION; GENE DELETION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOCUS; GENE OVEREXPRESSION; KNOCKOUT MOUSE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; ONCOGENE MYB; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; UPREGULATION; WILD TYPE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CYTOLOGY; GENETICS; HEK293 CELL LINE; HUMAN; IMMUNOLOGY; RNA INTERFERENCE; TRANSPLANTATION;

3' UNTRANSLATED REGIONS; ADOPTIVE TRANSFER; ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; HEK293 CELLS; HUMANS; INTERFERON-GAMMA; KILLER CELLS, NATURAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; PROTO-ONCOGENE PROTEINS C-MYB; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 84941776166     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500949     Document Type: Article

References (54)

1. Yokoyama, W. M., S. Kim, and A. R. French. 2004. The dynamic life of natural killer cells. Annu. Rev. Immunol. 22: 405-429.
2. Di Santo, J. P. 2006. Natural killer cell developmental pathways: a question of balance. Annu. Rev. Immunol. 24: 257-286.
3. Hesslein, D. G. T., and L. L. Lanier. 2011. Transcriptional control of natural killer cell development and function. Adv. Immunol. 109: 45-85.
4. Elliott, J. M., and W. M. Yokoyama. 2011. Unifying concepts of MHCdependent natural killer cell education. Trends Immunol. 32: 364-372.
5. Kim, S., K. Iizuka, H.-S. P. Kang, A. Dokun, A. R. French, S. Greco, and W. M. Yokoyama. 2002. In vivo developmental stages in murine natural killer cell maturation. Nat. Immunol. 3: 523-528.
6. Chiossone, L., J. Chaix, N. Fuseri, C. Roth, E. Vivier, and T.Walzer. 2009.Maturation of mouse NK cells is a 4-stage developmental program. Blood 113: 5488-5496.
7. Hayakawa, Y., and M. J. Smyth. 2006. CD27 Dissects Mature NK Cells into Two Subsets with Distinct Responsiveness and Migratory Capacity. J. Immunol. 176: 1517-1524.
8. Lanier, L. L. 2008. Up on the tightrope: natural killer cell activation and inhibition. Nat. Immunol. 9: 495-502.
9. Newman, K. C., and E. M. Riley. 2007. Whatever turns you on: accessory-celldependent activation of NK cells by pathogens. Nat. Rev. Immunol. 7: 279-291.
10. Vivier, E., E. Tomasello, M. Baratin, T. Walzer, and S. Ugolini. 2008. Functions of natural killer cells. Nat. Immunol. 9: 503-510.
11. Orange, J. S. 2008. Formation and function of the lytic NK-cell immunological synapse. Nat. Rev. Immunol. 8: 713-725.
12. Russell, J. H., and T. J. Ley. 2002. Lymphocyte-mediated cytotoxicity. Annu. Rev. Immunol. 20: 323-370.
13. Luevano, M., A. Madrigal, and A. Saudemont. 2012. Transcription factors involved in the regulation of natural killer cell development and function: an update. Front. Immunol. 3: 319.
14. Ramirez, K., and B. L. Kee. 2010. Transcriptional regulation of natural killer cell development. Curr. Opin. Immunol. 22: 193-198.
15. Gascoyne, D. M., E. Long, H. Veiga-Fernandes, J. de Boer, O. Williams, B. Seddon, M. Coles, D. Kioussis, and H. J. M. Brady. 2009. The basic leucine zipper transcription factor E4BP4 is essential for natural killer cell development. Nat. Immunol. 10: 1118-1124.
16. Boos, M. D., Y. Yokota, G. Eberl, and B. L. Kee. 2007. Mature natural killer cell and lymphoid tissue-inducing cell development requires Id2-mediated suppression of E protein activity. J. Exp. Med. 204: 1119-1130.
17. Held, W., B. Kunz, B. Lowin-Kropf, M. van de Wetering, and H. Clevers. 1999. Clonal acquisition of the Ly49A NK cell receptor is dependent on the transacting factor TCF-1. Immunity 11: 433-442.
18. Aliahmad, P., B. de la Torre, and J. Kaye. 2010. Shared dependence on the DNAbinding factor TOX for the development of lymphoid tissue-inducer cell and NK cell lineages. Nat. Immunol. 11: 945-952.
19. Firth, M. A., S. Madera, A. M. Beaulieu, G. Gasteiger, E. F. Castillo, K. S. Schluns, M. Kubo, P. B. Rothman, E. Vivier, and J. C. Sun. 2013. Nfil3-independent lineage maintenance and antiviral response of natural killer cells. J. Exp. Med. 210: 2981-2990.
20. Samson, S. I., O. Richard, M. Tavian, T. Ranson, C. A. J. Vosshenrich, F. Colucci, J. Buer, F. Grosveld, I. Godin, and J. P. Di Santo. 2003. GATA-3 promotes maturation, IFN-gamma production, and liver-specific homing of NK cells. Immunity 19: 701-711.
21. Kallies, A., S. Carotta, N. D. Huntington, N. J. Bernard, D. M. Tarlinton, M. J. Smyth, and S. L. Nutt. 2011. A role for Blimp1 in the transcriptional network controlling natural killer cell maturation. Blood 117: 1869-1879.
22. Ramirez, K., K. J. Chandler, C. Spaulding, S. Zandi, M. Sigvardsson, B. J. Graves, and B. L. Kee. 2012. Gene deregulation and chronic activation in natural killer cells deficient in the transcription factor ETS1. Immunity 36: 921-932.
23. Townsend, M. J., A. S. Weinmann, J. L. Matsuda, R. Salomon, P. J. Farnham, C. A. Biron, L. Gapin, and L. H. Glimcher. 2004. T-bet regulates the terminal maturation and homeostasis of NK and Valpha14i NKT cells. Immunity 20: 477-494.
24. Intlekofer, A. M., N. Takemoto, E. J. Wherry, S. A. Longworth, J. T. Northrup, V. R. Palanivel, A. C. Mullen, C. R. Gasink, S. M. Kaech, J. D. Miller, et al. 2005. Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat. Immunol. 6: 1236-1244.
25. Lewis, B. P., C. B. Burge, and D. P. Bartel. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20.
26. Belver, L., F. N. Papavasiliou, and A. R. Ramiro. 2011. MicroRNA control of lymphocyte differentiation and function. Curr. Opin. Immunol. 23: 368-373.
27. Baltimore, D., M. P. Boldin, R. M. O'Connell, D. S. Rao, and K. D. Taganov. 2008. MicroRNAs: new regulators of immune cell development and function. Nat. Immunol. 9: 839-845.
28. Leong, J. W., R. P. Sullivan, and T. A. Fehniger. 2014. microRNA management of NK-cell developmental and functional programs. Eur. J. Immunol. 44: 2862-2868.
29. Beaulieu, A. M., N. A. Bezman, J. E. Lee,M.Matloubian, J. C. Sun, and L. L. Lanier. 2013. MicroRNA function in NK-cell biology. Immunol. Rev. 253: 40-52.
30. Yue, J., and G. Tigyi. 2010. Conservation of miR-15a/16-1 and miR-15b/16-2 clusters. Mamm. Genome 21: 88-94.
31. Basso, K., P. Sumazin, P. Morozov, C. Schneider, R. L. Maute, Y. Kitagawa, J. Mandelbaum, J. Haddad, C.-Z. Chen, A. Califano, and R. Dalla-Favera. 2009. Identification of the human mature B cell miRNome. Immunity 30: 744-752.
32. Fehniger, T. A., T. Wylie, E. Germino, J. W. Leong, V. J. Magrini, S. Koul, C. R. Keppel, S. E. Schneider, D. C. Koboldt, R. P. Sullivan, et al. 2010. Nextgeneration sequencing identifies the natural killer cell microRNA transcriptome. Genome Res. 20: 1590-1604.
33. Klein, U., M. Lia, M. Crespo, R. Siegel, Q. Shen, T. Mo, A. Ambesi-Impiombato, A. Califano, A. Migliazza, G. Bhagat, and R. Dalla-Favera. 2010. The DLEU2/miR-15a/16-1 cluster controls B cell proliferation and its deletion leads to chronic lymphocytic leukemia. Cancer Cell 17: 28-40.
34. Cimmino, A., G. A. Calin, M. Fabbri, M. V. Iorio, M. Ferracin, M. Shimizu, S. E. Wojcik, R. I. Aqeilan, S. Zupo, M. Dono, et al. 2005. miR-15 and miR-16 induce apoptosis by targeting BCL2. [Published erratum appears in 2006. Proc. Natl. Acad. Sci. USA 103: 2464.] Proc. Natl. Acad. Sci. USA 102: 13944-13949.
35. Ramsay, R. G., and T. J. Gonda. 2008. MYB function in normal and cancer cells. Nat. Rev. Cancer 8: 523-534.
36. Biedenkapp, H., and U. Borgmeyer. 1988. Viral myb oncogene encodes a sequence-specific DNA-binding activity. Nature 335: 835-837.
37. Mucenski, M. L., K. McLain, A. B. Kier, S. H. Swerdlow, C. M. Schreiner, T. A. Miller, D. W. Pietryga, W. J. Scott, and S. S. Potter. 1991. A functional c-myb gene is required for normal murine fetal hepatic hematopoiesis. Cell 65: 677-689.
38. Chung, E., M. Dews, and D. Cozma. 2008. c-Myb oncoprotein is an essential target of the dleu2 tumor suppressor microRNA cluster. Cancer Biol. Ther. 7: 1758-1764.
39. Xiao, C., D. P. Calado, G. Galler, T. H. Thai, H. C. Patterson, J. Wang, N. Rajewsky, T. P. Bender, and K. Rajewsky. 2007. MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell 131: 146-159.
40. Bezman, N. A., T. Chakraborty, T. Bender, and L. L. Lanier. 2011. miR-150 regulates the development of NK and iNKT cells. J. Exp. Med. 208: 2717-2731.
41. Eckelhart, E., W. Warsch, E. Zebedin, O. Simma, D. Stoiber, T. Kolbe, T. Rülicke, M. Mueller, E. Casanova, and V. Sexl. 2011. A novel Ncr1-Cre mouse reveals the essential role of STAT5 for NK-cell survival and development. Blood 117: 1565-1573.
42. De Boer, J., A. Williams, G. Skavdis, N. Harker, M. Coles, M. Tolaini, T. Norton, K. Williams, K. Roderick, A. J. Potocnik, and D. Kioussis. 2003. Transgenic mice with hematopoietic and lymphoid specific expression of Cre. Eur. J. Immunol. 33: 314-325.
43. Srinivas, S., T. Watanabe, C.-S. Lin, C. M. William, Y. Tanabe, T. M. Jessell, and F. Costantini. 2001. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1: 4.
44. Narni-mancinelli, E., J. Chaix, A. Fenis, Y. M. Kerdiles, N. Yessaad, A. Reynders, C. Gregoire, H. Luche, S. Ugolini, E. Tomasello, et al. 2011. Fate mapping analysis of lymphoid cells expressing the NKp46 cell surface receptor. Proc. Natl. Acad. Sci. USA 108: 18324-18329.
45. Fehniger, T. A., S. F. Cai, X. Cao, A. J. Bredemeyer, R. M. Presti, A. R. French, and T. J. Ley. 2007. Acquisition of murine NK cell cytotoxicity requires the translation of a pre-existing pool of granzyme B and perforin mRNAs. Immunity 26: 798-811.
46. Sullivan, R. P., J. W. Leong, S. E. Schneider, C. K. R. Keppel, E. Germino, A. R. French, and T. A. Fehniger. 2012. MicroRNA Deficient NK Cells Exhibit Decreased Survival but Enhanced Function. J. Immunol. 188: 3019-3030.
47. Sullivan, R. P., L. A. Fogel, J. W. Leong, S. E. Schneider, R. Wong, R. Romee, T.-H. Thai, V. Sexl, S. J. Matkovich, G. W. Dorn, et al. 2013. miR-155 tunes both the threshold and extent of NK cell activation via targeting of multiple signaling pathways. J. Immunol. 191: 5904-5913.
48. Garcia, D. M., D. Baek, C. Shin, G. W. Bell, A. Grimson, and D. P. Bartel. 2011. Weak seed-pairing stability and high target-site abundance decrease the proficiency of lsy-6 and other microRNAs. Nat Struct Mol Cell Biol 18: 1139-1146.
49. Huang, D. W., B. T. Sherman, and R. A. Lempicki. 2009. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37: 1-13.
50. Shay, T., V. Jojic, O. Zuk, K. Rothamel, D. Puyraimond-Zemmour, T. Feng, E. Wakamatsu, C. Benoist, D. Koller, and A. Regev. 2013. Conservation and divergence in the transcriptional programs of the human and mouse immune systems. Proc. Natl. Acad. Sci. USA 110: 2946-2951.
51. Li, Y., J. Pei, H. Xia, H. Ke, H. Wang, and W. Tao. 2003. Lats2, a putative tumor suppressor, inhibits G1/S transition. Oncogene 22: 4398-4405.
52. Zhao, H., A. Kalota, S. Jin, and A. M. Gewirtz. 2009. The c-myb proto-oncogene and microRNA-15a comprise an active autoregulatory feedback loop in human hematopoietic cells. Blood 113: 505-516.
53. Sankaran, V. G., T. F. Menne, D. Šćepanović, J.-A. Vergilio, P. Ji, J. Kim, P. Thiru, S. H. Orkin, E. S. Lander, and H. F. Lodish. 2011. MicroRNA-15a and -16-1 act via MYB to elevate fetal hemoglobin expression in human trisomy 13. Proc. Natl. Acad. Sci. USA 108: 1519-1524.
54. Karlhofer, B. F. M., M. M. Orihuela, and W. M. Yokoyama. 1995. Ly-49-independent natural killer (NK) cell specificity revealed by NK cell clones derived from p53-deficient mice. J. Exp. Med. 181: 1785-1795.