The inducible tissue-specific expression of the human IL-3/GM-CSF locus is controlled by a complex array of developmentally regulated enhancers

Journal of Immunology

Volumn 189, Issue 9, 2012, Pages 4459-4469

  Baxter, Euan W ^a   Mirabella, Fabio ^a,d   Bowers, Sarion R ^a,e   James, Sally R ^a   Bonavita, Aude Marine ^a   Bertrand, Elisabeth ^a   Strogantsev, Ruslan ^b,f   Hawwari, Abbas ^c,g   Bert, Andrew G ^c   Gonzalez De Arce, Andrea ^a   West, Adam G ^b   Bonifer, Constanze ^a,h   Cockerill, Peter N ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c CENTRE FOR CANCER BIOLOGY   (Australia)

^d INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^e UNIVERSITY OF CONNECTICUT   (United States)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^g KING FAISAL SPECIALIST HOSPITAL AND RESEARCH CENTER   (Saudi Arabia)

^h UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 3;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; ENHANCER REGION; GENE ACTIVATION; GENE CLUSTER; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE LOCUS; GM CSF GENE; HUMAN; HUMAN CELL; IL 3 GENE; MACROPHAGE; MAST CELL; MONOCYTE; MOUSE; MYELOID PROGENITOR CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY SEQUENCE; T LYMPHOCYTE; TISSUE SPECIFICITY; TRANSGENIC MOUSE;

ANIMALS; CELL LINE; CELL LINE, TUMOR; CELLS, CULTURED; DEOXYRIBONUCLEASE I; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC LOCI; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; INTERLEUKIN-3; JURKAT CELLS; MICE; MICE, TRANSGENIC; TISSUE DISTRIBUTION;

EID: 84867911442     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1201915     Document Type: Article

References (40)

1. Cockerill, P. N. 2004. Mechanisms of transcriptional regulation of the human IL- 3/GM-CSF locus by inducible tissue-specific promoters and enhancers. Crit. Rev. Immunol. 24: 385-408. (Pubitemid 40397318)
2. Alexander, W. S. 1998. Cytokines in hematopoiesis. Int. Rev. Immunol. 16: 651-682. (Pubitemid 28286189)
3. Nicola, N. A. 1989. Hemopoietic cell growth factors and their receptors. Annu. Rev. Biochem. 58: 45-77. (Pubitemid 19172964)
4. Robin, C., K. Ottersbach, C. Durand, M. Peeters, L. Vanes, V. Tybulewicz, and E. Dzierzak. 2006. An unexpected role for IL-3 in the embryonic development of hematopoietic stem cells. Dev. Cell 11: 171-180. (Pubitemid 44138501)
5. He, W. Y., Y. Lan, H. Y. Yao, Z. Li, X. Y. Wang, X. S. Li, J. Y. Zhang, Y. Zhang, B. Liu, and N. Mao. 2010. Interleukin-3 promotes hemangioblast development in mouse aorta-gonad-mesonephros region. Haematologica 95: 875-883.
6. Gasson, J. C. 1991. Molecular physiology of granulocyte-macrophage colonystimulating factor. Blood 77: 1131-1145.
7. Basu, S., A. R. Dunn, M. W. Marino, H. Savoia, G. Hodgson, G. J. Lieschke, and J. Cebon. 1997. Increased tolerance to endotoxin by granulocyte-macrophage colony-stimulating factor-deficient mice. J. Immunol. 159: 1412-1417. (Pubitemid 127484120)
8. Frazer, K. A., Y. Ueda, Y. Zhu, V. R. Gifford, M. R. Garofalo, N. Mohandas, C. H. Martin, M. J. Palazzolo, J. F. Cheng, and E. M. Rubin. 1997. Computational and biological analysis of 680 kb of DNA sequence from the human 5q31 cytokine gene cluster region. Genome Res. 7: 495-512. (Pubitemid 27232012)
9. Lee, G. R., C. G. Spilianakis, and R. A. Flavell. 2005. Hypersensitive site 7 of the TH2 locus control region is essential for expressing TH2 cytokine genes and for long-range intrachromosomal interactions. Nat. Immunol. 6: 42-48. (Pubitemid 40136694)
10. Spilianakis, C. G., M. D. Lalioti, T. Town, G. R. Lee, and R. A. Flavell. 2005. Interchromosomal associations between alternatively expressed loci. Nature 435: 637-645. (Pubitemid 40825504)
11. Bowers, S. R., F. Mirabella, F. J. Calero-Nieto, S. Valeaux, S. Hadjur, E. W. Baxter, M. Merkenschlager, and P. N. Cockerill. 2009. A conserved insulator that recruits CTCF and cohesin exists between the closely related but divergently regulated interleukin-3 and granulocyte-macrophage colony-stimulating factor genes. Mol. Cell. Biol. 29: 1682-1693.
12. Hawwari, A., J. Burrows, M. A. Vadas, and P. N. Cockerill. 2002. The human IL- 3 locus is regulated cooperatively by two NFAT-dependent enhancers that have distinct tissue-specific activities. J. Immunol. 169: 1876-1886. (Pubitemid 34857650)
13. Bert, A. G., J. Burrows, A. Hawwari, M. A. Vadas, and P. N. Cockerill. 2000. Reconstitution of T cell-specific transcription directed by composite NFAT/Oct elements. J. Immunol. 165: 5646-5655.
14. Duncliffe, K. N., A. G. Bert, M. A. Vadas, and P. N. Cockerill. 1997. A T cell-specific enhancer in the interleukin-3 locus is activated cooperatively by Oct and NFAT elements within a DNase I-hypersensitive site. Immunity 6: 175-185. (Pubitemid 27145562)
15. Cockerill, P. N., A. G. Bert, D. Roberts, and M. A. Vadas. 1999. The human GM-CSF gene is autonomously regulated in vivo by an inducible tissue-specific enhancer. Proc. Natl. Acad. Sci. USA 96: 15097-15102. (Pubitemid 30019771)
16. Cockerill, P. N., M. F. Shannon, A. G. Bert, G. R. Ryan, and M. A. Vadas. 1993. The granulocyte-macrophage colony-stimulating factor/interleukin 3 locus is regulated by an inducible cyclosporin A-sensitive enhancer. Proc. Natl. Acad. Sci. USA 90: 2466-2470. (Pubitemid 23078648)
17. Osborne, C. S., M. A. Vadas, and P. N. Cockerill. 1995. Transcriptional regulation of mouse granulocyte-macrophage colony-stimulating factor/IL-3 locus. J. Immunol. 155: 226-235.
18. Wurster, A. L., P. Precht, and M. J. Pazin. 2011. NF-κB and BRG1 bind a distal regulatory element in the IL-3/GM-CSF locus. Mol. Immunol. 48: 2178-2188.
19. Johnson, B. V., A. G. Bert, G. R. Ryan, A. Condina, and P. N. Cockerill. 2004. GM-CSF enhancer activation requires cooperation between NFAT and AP-1 elements and is associated with extensive nucleosome reorganization. Mol. Cell. Biol. 24: 7914-7930. (Pubitemid 39167442)
20. Russell, N. H. 1992. Autocrine growth factors and leukaemic haemopoiesis. Blood Rev. 6: 149-156.
21. Jiang, X., A. Lopez, T. Holyoake, A. Eaves, and C. Eaves. 1999. Autocrine production and action of IL-3 and granulocyte colony-stimulating factor in chronic myeloid leukemia. Proc. Natl. Acad. Sci. USA 96: 12804-12809. (Pubitemid 29513583)
22. Jiang, X., E. Ng, C. Yip, W. Eisterer, Y. Chalandon, M. Stuible, A. Eaves, and C. J. Eaves. 2002. Primitive interleukin 3 null hematopoietic cells transduced with BCR-ABL show accelerated loss after culture of factor-independence in vitro and leukemogenic activity in vivo. Blood 100: 3731-3740. (Pubitemid 35303945)
23. Holyoake, T. L., X. Jiang, H. G. Jorgensen, S. Graham, M. J. Alcorn, C. Laird, A. C. Eaves, and C. J. Eaves. 2001. Primitive quiescent leukemic cells from patients with chronic myeloid leukemia spontaneously initiate factor-independent growth in vitro in association with up-regulation of expression of interleukin-3. Blood 97: 720-728. (Pubitemid 32113406)
24. Mirabella, F., E. W. Baxter, M. Boissinot, S. R. James, and P. N. Cockerill. 2010. The human IL-3/granulocyte-macrophage colony-stimulating factor locus is epigenetically silent in immature thymocytes and is progressively activated during T cell development. J. Immunol. 184: 3043-3054.
25. Bert, A. G., B. V. Johnson, E. W. Baxter, and P. N. Cockerill. 2007. A modular enhancer is differentially regulated by GATA and NFAT elements that direct different tissue-specific patterns of nucleosome positioning and inducible chromatin remodeling. Mol. Cell. Biol. 27: 2870-2885. (Pubitemid 46581303)
26. Butterfield, J. H., and D. A. Weiler. 1989. In vitro sensitivity of immature human mast cells to chemotherapeutic agents. Int. Arch. Allergy Appl. Immunol. 89: 297-300. (Pubitemid 19209655)
27. Bert, A. G., J. Burrows, C. S. Osborne, and P. N. Cockerill. 2000. Generation of an improved luciferase reporter gene plasmid that employs a novel mechanism for high-copy replication. Plasmid 44: 173-182.
28. Dickson, J., H. Gowher, R. Strogantsev, M. Gaszner, A. Hair, G. Felsenfeld, and A. G. West. 2010. VEZF1 elements mediate protection from DNA methylation. PLoS Genet. 6: e1000804.
29. Anderson, M. K., G. Hernandez-Hoyos, R. A. Diamond, and E. V. Rothenberg. 1999. Precise developmental regulation of Ets family transcription factors during specification and commitment to the T cell lineage. Development 126: 3131-3148. (Pubitemid 29378177)
30. Liu, C., A. Calogero, G. Ragona, E. Adamson, and D. Mercola. 1996. EGR-1, the reluctant suppression factor: EGR-1 is known to function in the regulation of growth, differentiation, and also has significant tumor suppressor activity and a mechanism involving the induction of TGF-beta1 is postulated to account for this suppressor activity. Crit. Rev. Oncog. 7: 101-125.
31. Skerka, C., E. L. Decker, and P. F. Zipfel. 1995. A regulatory element in the human interleukin 2 gene promoter is a binding site for the zinc finger proteins Sp1 and EGR-1. J. Biol. Chem. 270: 22500-22506.
32. Khachigian, L. M., and T. Collins. 1997. Inducible expression of Egr-1- dependent genes: a paradigm of transcriptional activation in vascular endothelium. Circ. Res. 81: 457-461. (Pubitemid 27432731)
33. Wijgerde, M., F. Grosveld, and P. Fraser. 1995. Transcription complex stability and chromatin dynamics in vivo. Nature 377: 209-213.
34. Dillon, N., and F. Grosveld. 1993. Transcriptional regulation of multigene loci: multilevel control. Trends Genet. 9: 134-137. (Pubitemid 23098781)
35. Mätlik, K., K. Redik, and M. Speek. 2006. L1 antisense promoter drives tissue-specific transcription of human genes. J. Biomed. Biotechnol. 2006: 71753.
36. Smith, A. M., M. J. Sanchez, G. A. Follows, S. Kinston, I. J. Donaldson, A. R. Green, and B. Göttgens. 2008. A novel mode of enhancer evolution: the Tal1 stem cell enhancer recruited a MIR element to specifically boost its activity. Genome Res. 18: 1422-1432.
37. Lamprecht, B., K. Walter, S. Kreher, R. Kumar, M. Hummel, D. Lenze, K. Kochert, M. A. Bouhlel, J. Richter, E. Soler, et al. 2010. Derepression of an endogenous long terminal repeat activates the CSF1R proto-oncogene in human lymphoma. Nat. Med. 16: 571-579, 1p following 579.
38. Cockerill, P. N., A. G. Bert, F. Jenkins, G. R. Ryan, M. F. Shannon, and M. A. Vadas. 1995. Human GM-CSF enhancer function is associated with cooperative interactions between AP-1 and NFATp/c. Mol. Cell. Biol. 15: 2071-2079.
39. Wilson, N. K., S. D. Foster, X. Wang, K. Knezevic, J. Schütte, P. Kaimakis, P. M. Chilarska, S. Kinston, W. H. Ouwehand, E. Dzierzak, et al. 2010. Combinatorial transcriptional control in blood stem/progenitor cells: genomewide analysis of ten major transcriptional regulators. Cell Stem Cell 7: 532-544.
40. Taylor, D. S., J. P. Laubach, D. G. Nathan, and B. Mathey-Prevot. 1996. Cooperation between core binding factor and adjacent promoter elements contributes to the tissue-specific expression of interleukin-3. J. Biol. Chem. 271: 14020-14027. (Pubitemid 26190293)