Transcription factor repertoire of homeostatic eosinophilopoiesis

Journal of Immunology

Volumn 195, Issue 6, 2015, Pages 2683-2695

  Bouffi, Carine ^a   Kartashov, Andrey V ^a   Schollaert, Kaila L ^a   Chen, Xiaoting ^b   Bacon, W Clark ^a   Weirauch, Matthew T ^a   Barski, Artem ^a   Fulkerson, Patricia C ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b 705 Engineering Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AIOLOS TRANSCRIPTION FACTOR; BINDING PROTEIN; DNA; EPIGENOME; HELIOS TRANSCRIPTION FACTOR; IKAROS TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTOME; UNCLASSIFIED DRUG; CHROMATIN; DNA BINDING PROTEIN; IKZF3 PROTEIN, MOUSE; TRANSACTIVATOR PROTEIN; ZFPN1A2 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EOSINOPHILOPOIESIS; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; HEMATOPOIESIS; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FUNCTION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL CULTURE; CELL GRANULE; CHROMATIN; CYTOLOGY; EOSINOPHIL; GENETICS; GRANULOCYTE PRECURSOR; IMMUNOLOGY; METABOLISM;

ANIMALS; BINDING SITES; CELL LINEAGE; CELLS, CULTURED; CHROMATIN; CYTOPLASMIC GRANULES; DNA-BINDING PROTEINS; EOSINOPHILS; GENE EXPRESSION REGULATION; GRANULOCYTE PRECURSOR CELLS; HEMATOPOIESIS; MICE; MICE, INBRED BALB C; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84941770152     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500510     Document Type: Article

References (77)

1. Lee, J., and H. F. Rosenberg. 2013. Eosinophils in Health and Disease. Elsevier/ Academic Press, London.
2. Rosenberg, H. F., K. D. Dyer, and P. S. Foster. 2013. Eosinophils: changing perspectives in health and disease. Nat. Rev. Immunol. 13: 9-22.
3. Iwasaki, H., S. Mizuno, R. Mayfield, H. Shigematsu, Y. Arinobu, B. Seed, M. F. Gurish, K. Takatsu, and K. Akashi. 2005. Identification of eosinophil lineage-committed progenitors in the murine bone marrow. J. Exp. Med. 201: 1891-1897.
4. Mori, Y., H. Iwasaki, K. Kohno, G. Yoshimoto, Y. Kikushige, A. Okeda, N. Uike, H. Niiro, K. Takenaka, K. Nagafuji, et al. 2009. Identification of the human eosinophil lineage-committed progenitor: revision of phenotypic definition of the human common myeloid progenitor. J. Exp. Med. 206: 183-193.
5. Duffin, R., A. E. Leitch, S. Fox, C. Haslett, and A. G. Rossi. 2010. Targeting granulocyte apoptosis: mechanisms, models, and therapies. Immunol. Rev. 236: 28-40.
6. Simon, H. U. 2006. Molecules involved in the regulation of eosinophil apoptosis. Chem. Immunol. Allergy 91: 49-58.
7. Yoshida, T., K. Ikuta, H. Sugaya, K. Maki, M. Takagi, H. Kanazawa, S. Sunaga, T. Kinashi, K. Yoshimura, J. Miyazaki, et al. 1996. Defective B-1 cell development and impaired immunity against Angiostrongylus cantonensis in IL-5R alpha-deficient mice. Immunity 4: 483-494.
8. Takagi, M., T. Hara, M. Ichihara, K. Takatsu, and A. Miyajima. 1995. Multicolony stimulating activity of interleukin 5 (IL-5) on hematopoietic progenitors from transgenic mice that express IL-5 receptor alpha subunit constitutively. J. Exp. Med. 181: 889-899.
9. Nishinakamura, R., N. Nakayama, Y. Hirabayashi, T. Inoue, D. Aud, T. McNeil, S. Azuma, S. Yoshida, Y. Toyoda, K. Arai, et al. 1995. Mice deficient for the IL-3/GM-CSF/IL-5 beta c receptor exhibit lung pathology and impaired immune response, while beta IL3 receptor-deficient mice are normal. Immunity 2: 211-222.
10. Kopf, M., F. Brombacher, P. D. Hodgkin, A. J. Ramsay, E. A. Milbourne, W. J. Dai, K. S. Ovington, C. A. Behm, G. Köhler, I. G. Young, and K. I. Matthaei. 1996. IL-5-deficient mice have a developmental defect in CD5+ B-1 cells and lack eosinophilia but have normal antibody and cytotoxic T cell responses. Immunity 4: 15-24.
11. Dent, L. A., M. Strath, A. L. Mellor, and C. J. Sanderson. 1990. Eosinophilia in transgenic mice expressing interleukin 5. J. Exp. Med. 172: 1425-1431.
12. Dent, L. A., G. H. Munro, K. P. Piper, C. J. Sanderson, D. A. Finlay, R. K. Dempster, L. P. Bignold, D. G. Harkin, and P. Hagan. 1997. Eosinophilic interleukin 5 (IL-5) transgenic mice: eosinophil activity and impaired clearance of Schistosoma mansoni. Parasite Immunol. 19: 291-300.
13. Fulkerson, P. C., C. A. Fischetti, M. L. McBride, L. M. Hassman, S. P. Hogan, and M. E. Rothenberg. 2006. A central regulatory role for eosinophils and the eotaxin/CCR3 axis in chronic experimental allergic airway inflammation. Proc. Natl. Acad. Sci. USA 103: 16418-16423.
14. Byström, J., T. A. Wynn, J. B. Domachowske, and H. F. Rosenberg. 2004. Gene microarray analysis reveals interleukin-5-dependent transcriptional targets in mouse bone marrow. Blood 103: 868-877.
15. Fulkerson, P. C., K. L. Schollaert, C. Bouffi, and M. E. Rothenberg. 2014. IL-5 triggers a cooperative cytokine network that promotes eosinophil precursor maturation. J. Immunol. 193: 4043-4052.
16. Schollaert, K. L., M. R. Stephens, J. K. Gray, and P. C. Fulkerson. 2014. Generation of eosinophils from cryopreserved murine bone marrow cells. PLoS One 9: e116141.
17. Edgar, R., M. Domrachev, and A. E. Lash. 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30: 207-210.
18. Kartashov, A. V., and A. Barski. 2015. BioWardrobe: an integrated platform for analysis of epigenomics and transcriptomics data. Genome Biol. In press.
19. Dobin, A., C. A. Davis, F. Schlesinger, J. Drenkow, C. Zaleski, S. Jha, P. Batut, M. Chaisson, and T. R. Gingeras. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29: 15-21.
20. Anders, S., and W. Huber. 2010. Differential expression analysis for sequence count data. Genome Biol. 11: R106.
21. Chen, J., E. E. Bardes, B. J. Aronow, and A. G. Jegga. 2009. ToppGene Suite for gene list enrichment analysis and candidate gene prioritization. Nucleic Acids Res. 37: W305-W311.
22. Heinz, S., C. Benner, N. Spann, E. Bertolino, Y. C. Lin, P. Laslo, J. X. Cheng, C. Murre, H. Singh, and C. K. Glass. 2010. Simple combinations of lineagedetermining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38: 576-589.
23. Zhang, J., A. F. Jackson, T. Naito, M. Dose, J. Seavitt, F. Liu, E. J. Heller, M. Kashiwagi, T. Yoshida, F. Gounari, et al. 2012. Harnessing of the nucleosome-remodeling-deacetylase complex controls lymphocyte development and prevents leukemogenesis. Nat. Immunol. 13: 86-94.
24. Stormo, G. D. 2000. DNA binding sites: representation and discovery. Bioinformatics 16: 16-23.
25. Barski, A., S. Cuddapah, K. Cui, T. Y. Roh, D. E. Schones, Z. Wang, G. Wei, I. Chepelev, and K. Zhao. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837.
26. Wang, Z., C. Zang, J. A. Rosenfeld, D. E. Schones, A. Barski, S. Cuddapah, K. Cui, T. Y. Roh, W. Peng, M. Q. Zhang, and K. Zhao. 2008. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 40: 897-903.
27. Ernst, J., P. Kheradpour, T. S. Mikkelsen, N. Shoresh, L. D. Ward, C. B. Epstein, X. Zhang, L. Wang, R. Issner, M. Coyne, et al. 2011. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473: 43-49.
28. Immunological Genome Project Consortium. 2008. The Immunological Genome Project: networks of gene expression in immune cells. Nat. Immunol. 9: 1091-1094.
29. Barrett, T., S. E. Wilhite, P. Ledoux, C. Evangelista, I. F. Kim, M. Tomashevsky, K. A. Marshall, K. H. Phillippy, P. M. Sherman, M. Holko, et al. 2013. NCBI GEO: archive for functional genomics data sets-update. Nucleic Acids Res. 41: D991-D995.
30. Allantaz, F., D. T. Cheng, T. Bergauer, P. Ravindran, M. F. Rossier, M. Ebeling, L. Badi, B. Reis, H. Bitter, M. D'Asaro, et al. 2012. Expression profiling of human immune cell subsets identifies miRNA-mRNA regulatory relationships correlated with cell type specific expression. PLoS One 7: e29979.
31. Logan, M. R., P. Lacy, B. Bablitz, and R. Moqbel. 2002. Expression of eosinophil target SNAREs as potential cognate receptors for vesicle-associated membrane protein-2 in exocytosis. J. Allergy Clin. Immunol. 109: 299-306.
32. Park, Y. M., and B. S. Bochner. 2010. Eosinophil survival and apoptosis in health and disease. Allergy Asthma Immunol. Res. 2: 87-101.
33. Wen, T., J. A. Besse, M. K. Mingler, P. C. Fulkerson, and M. E. Rothenberg. 2013. Eosinophil adoptive transfer system to directly evaluate pulmonary eosinophil trafficking in vivo. Proc. Natl. Acad. Sci. USA 110: 6067-6072.
34. Farahi, N., N. R. Singh, S. Heard, C. Loutsios, C. Summers, C. K. Solanki, K. Solanki, K. K. Balan, P. Ruparelia, A. M. Peters, et al. 2012. Use of 111-Indium-labeled autologous eosinophils to establish the in vivo kinetics of human eosinophils in healthy subjects. Blood 120: 4068-4071.
35. Ohnmacht, C., A. Pullner, N. van Rooijen, and D. Voehringer. 2007. Analysis of eosinophil turnover in vivo reveals their active recruitment to and prolonged survival in the peritoneal cavity. J. Immunol. 179: 4766-4774.
36. Geering, B., C. Stoeckle, S. Conus, and H. U. Simon. 2013. Living and dying for inflammation: neutrophils, eosinophils, basophils. Trends Immunol. 34: 398-409.
37. Tomaki, M., L. L. Zhao, J. Lundahl, M. Sjöstrand, M. Jordana, A. Lindén, P. O'Byrne, and J. Lötvall. 2000. Eosinophilopoiesis in a murine model of allergic airway eosinophilia: involvement of bone marrow IL-5 and IL-5 receptor alpha. J. Immunol. 165: 4040-4050.
38. Mattes, J., M. Yang, S. Mahalingam, J. Kuehr, D. C. Webb, L. Simson, S. P. Hogan, A. Koskinen, A. N. McKenzie, L. A. Dent, et al. 2002. Intrinsic defect in T cell production of interleukin (IL)-13 in the absence of both IL-5 and eotaxin precludes the development of eosinophilia and airways hyperreactivity in experimental asthma. J. Exp. Med. 195: 1433-1444.
39. Hogan, S. P., A. Koskinen, and P. S. Foster. 1997. Interleukin-5 and eosinophils induce airway damage and bronchial hyperreactivity during allergic airway inflammation in BALB/c mice. Immunol. Cell Biol. 75: 284-288.
40. Wirths, S., S. Bugl, and H. G. Kopp. 2014. Neutrophil homeostasis and its regulation by danger signaling. Blood 123: 3563-3566.
41. May, G., S. Soneji, A. J. Tipping, J. Teles, S. J. McGowan, M. Wu, Y. Guo, C. Fugazza, J. Brown, G. Karlsson, et al. 2013. Dynamic analysis of gene expression and genome-wide transcription factor binding during lineage specification of multipotent progenitors. Cell Stem Cell 13: 754-768.
42. Laslo, P., J. M. Pongubala, D. W. Lancki, and H. Singh. 2008. Gene regulatory networks directing myeloid and lymphoid cell fates within the immune system. Semin. Immunol. 20: 228-235.
43. Bochner, B. S. 2009. Siglec-8 on human eosinophils and mast cells, and Siglec-F on murine eosinophils, are functionally related inhibitory receptors. Clin. Exp. Allergy 39: 317-324.
44. Hudson, S. A., H. Herrmann, J. Du, P. Cox, B. Haddad, B. Butler, P. R. Crocker, S. J. Ackerman, P. Valent, and B. S. Bochner. 2011. Developmental, malignancyrelated, and cross-species analysis of eosinophil, mast cell, and basophil siglec-8 expression. J. Clin. Immunol. 31: 1045-1053.
45. Dyer, K. D., K. E. Garcia-Crespo, K. E. Killoran, and H. F. Rosenberg. 2011. Antigen profiles for the quantitative assessment of eosinophils in mouse tissues by flow cytometry. J. Immunol. Methods 369: 91-97.
46. Lei, J. T., andM.Martinez-Moczygemba. 2008. Separate endocytic pathways regulate IL-5 receptor internalization and signaling. J. Leukoc. Biol. 84: 499-509.
47. Hellman, C., G. Halldén, B. Hylander, and J. Lundahl. 2003. Regulation of the interleukin-5 receptor alpha-subunit on peripheral blood eosinophils from healthy subjects. Clin. Exp. Immunol. 131: 75-81.
48. Gregory, B., A. Kirchem, S. Phipps, P. Gevaert, C. Pridgeon, S. M. Rankin, and D. S. Robinson. 2003. Differential regulation of human eosinophil IL-3, IL-5, and GM-CSF receptor alpha-chain expression by cytokines: IL-3, IL-5, and GM-CSF down-regulate IL-5 receptor alpha expression with loss of IL-5 responsiveness, but up-regulate IL-3 receptor alpha expression. J. Immunol. 170: 5359-5366.
49. Gruart, V., M. J. Truong, J. Plumas, M. Zandecki, J. P. Kusnierz, L. Prin, D. Vinatier, A. Capron, and M. Capron. 1992. Decreased expression of eosinophil peroxidase and major basic protein messenger RNAs during eosinophil maturation. Blood 79: 2592-2597.
50. Doyle, A. D., E. A. Jacobsen, S. I. Ochkur, M. P. McGarry, K. G. Shim, D. T. Nguyen, C. Protheroe, D. Colbert, J. Kloeber, J. Neely, et al. 2013. Expression of the secondary granule proteins major basic protein 1 (MBP-1) and eosinophil peroxidase (EPX) is required for eosinophilopoiesis in mice. Blood 122: 781-790.
51. Melo, R. C., L. A. Spencer, A. M. Dvorak, and P. F.Weller. 2008. Mechanisms of eosinophil secretion: large vesiculotubular carriers mediate transport and release of granule-derived cytokines and other proteins. J. Leukoc. Biol. 83: 229-236.
52. Phipps, S., C. E. Lam, S. Mahalingam, M. Newhouse, R. Ramirez, H. F. Rosenberg, P. S. Foster, and K. I. Matthaei. 2007. Eosinophils contribute to innate antiviral immunity and promote clearance of respiratory syncytial virus. Blood 110: 1578-1586.
53. Malm-Erjefält, M., C. G. Persson, and J. S. Erjefält. 2001. Degranulation status of airway tissue eosinophils in mouse models of allergic airway inflammation. Am. J. Respir. Cell Mol. Biol. 24: 352-359.
54. Spencer, L. A., K. Bonjour, R. C. Melo, and P. F. Weller. 2014. Eosinophil secretion of granule-derived cytokines. Front. Immunol. 5: 496.
55. Iwasaki, H., S. Mizuno, Y. Arinobu, H. Ozawa, Y. Mori, H. Shigematsu, K. Takatsu, D. G. Tenen, and K. Akashi. 2006. The order of expression of transcription factors directs hierarchical specification of hematopoietic lineages. Genes Dev. 20: 3010-3021.
56. McNagny, K., and T. Graf. 2002. Making eosinophils through subtle shifts in transcription factor expression. J. Exp. Med. 195: F43-F47.
57. Du, J., M. J. Stankiewicz, Y. Liu, Q. Xi, J. E. Schmitz, J. A. Lekstrom-Himes, and S. J. Ackerman. 2002. Novel combinatorial interactions of GATA-1, PU.1, and C/EBPepsilon isoforms regulate transcription of the gene encoding eosinophil granule major basic protein. J. Biol. Chem. 277: 43481-43494.
58. Gombart, A. F., S. H. Kwok, K. L. Anderson, Y. Yamaguchi, B. E. Torbett, and H. P. Koeffler. 2003. Regulation of neutrophil and eosinophil secondary granule gene expression by transcription factors C/EBP epsilon and PU.1. Blood 101: 3265-3273.
59. Fu, W., A. Ergun, T. Lu, J. A. Hill, S. Haxhinasto, M. S. Fassett, R. Gazit, S. Adoro, L. Glimcher, S. Chan, et al. 2012. A multiply redundant genetic switch 'locks in' the transcriptional signature of regulatory T cells. Nat. Immunol. 13: 972-980.
60. Quintana, F. J., H. Jin, E. J. Burns, M. Nadeau, A. Yeste, D. Kumar, M. Rangachari, C. Zhu, S. Xiao, J. Seavitt, et al. 2012. Aiolos promotes TH17 differentiation by directly silencing Il2 expression. Nat. Immunol. 13: 770-777.
61. Evans, H. G., U. Roostalu, G. J. Walter, N. J. Gullick, K. S. Frederiksen, C. A. Roberts, J. Sumner, D. L. Baeten, J. G. Gerwien, A. P. Cope, et al. 2014. TNF-a blockade induces IL-10 expression in human CD4+ T cells. Nat. Commun. 5: 3199.
62. Kim, J., S. Sif, B. Jones, A. Jackson, J. Koipally, E. Heller, S. Winandy, A. Viel, A. Sawyer, T. Ikeda, et al. 1999. Ikaros DNA-binding proteins direct formation of chromatin remodeling complexes in lymphocytes. Immunity 10: 345-355.
63. Thompson, E. C., B. S. Cobb, P. Sabbattini, S. Meixlsperger, V. Parelho, D. Liberg, B. Taylor, N. Dillon, K. Georgopoulos, H. Jumaa, et al. 2007. Ikaros DNA-binding proteins as integral components of B cell developmental-stagespecific regulatory circuits. Immunity 26: 335-344.
64. Schwickert, T. A., H. Tagoh, S. Gültekin, A. Dakic, E. Axelsson, M. Minnich, A. Ebert, B.Werner, M. Roth, L. Cimmino, et al. 2014. Stage-specific control of early B cell development by the transcription factor Ikaros. Nat. Immunol. 15: 283-293.
65. Tagari, P., E. I. Pecheur, M. Scheid, P. Brown, A. W. Ford-Hutchinson, and D. Nicholson. 1993. Activation of human eosinophils and differentiated HL-60 cells by interleukin-5. Int. Arch. Allergy Immunol. 101: 227-233.
66. Ishihara, K., J. Hong, O. Zee, and K. Ohuchi. 2004. Possible mechanism of action of the histone deacetylase inhibitors for the induction of differentiation of HL-60 clone 15 cells into eosinophils. Br. J. Pharmacol. 142: 1020-1030.
67. Fischkoff, S. A. 1988. Graded increase in probability of eosinophilic differentiation of HL-60 promyelocytic leukemia cells induced by culture under alkaline conditions. Leuk. Res. 12: 679-686.
68. Fischkoff, S. A., and M. E. Condon. 1985. Switch in differentiative response to maturation inducers of human promyelocytic leukemia cells by prior exposure to alkaline conditions. Cancer Res. 45: 2065-2069.
69. Zimmermann, N., B. L. Daugherty, J. M. Stark, and M. E. Rothenberg. 2000. Molecular analysis of CCR-3 events in eosinophilic cells. J. Immunol. 164: 1055-1064.
70. John, L. B., and A. C. Ward. 2011. The Ikaros gene family: transcriptional regulators of hematopoiesis and immunity. Mol. Immunol. 48: 1272-1278.
71. Kelley, C. M., T. Ikeda, J. Koipally, N. Avitahl, L. Wu, K. Georgopoulos, and B. A. Morgan. 1998. Helios, a novel dimerization partner of Ikaros expressed in the earliest hematopoietic progenitors. Curr. Biol. 8: 508-515.
72. Hahm, K., B. S. Cobb, A. S. McCarty, K. E. Brown, C. A. Klug, R. Lee, K. Akashi, I. L. Weissman, A. G. Fisher, and S. T. Smale. 1998. Helios, a T cellrestricted Ikaros family member that quantitatively associates with Ikaros at centromeric heterochromatin. Genes Dev. 12: 782-796.
73. Morgan, B., L. Sun, N. Avitahl, K. Andrikopoulos, T. Ikeda, E. Gonzales, P. Wu, S. Neben, and K. Georgopoulos. 1997. Aiolos, a lymphoid restricted transcription factor that interacts with Ikaros to regulate lymphocyte differentiation. EMBO J. 16: 2004-2013.
74. Rao, K. N., C. Smuda, G. D. Gregory, B. Min, and M. A. Brown. 2013. Ikaros limits basophil development by suppressing C/EBP-a expression. Blood 122: 2572-2581.
75. Heinz, S., and C. K. Glass. 2012. Roles of lineage-determining transcription factors in establishing open chromatin: lessons from high-throughput studies. Curr. Top. Microbiol. Immunol. 356: 1-15.
76. Rothenberg, E. V. 2013. Epigenetic mechanisms and developmental choice hierarchies in T-lymphocyte development. Brief. Funct. Genomics 12: 512-524.
77. Krönke, J., N. D. Udeshi, A. Narla, P. Grauman, S. N. Hurst, M. McConkey, T. Svinkina, D. Heckl, E. Comer, X. Li, et al. 2014. Lenalidomide causes selective degradation of IKZF1 and IKZF3 in multiple myeloma cells. Science 343: 301-305.