New insights on the transcriptional regulation of CD69 gene through a potent enhancer located in the conserved non-coding sequence 2

Molecular Immunology

Volumn 66, Issue 2, 2015, Pages 171-179

  Laguna, Teresa ^a   Notario, Laura ^a   Pippa, Raffaella ^b   Fontela, Miguel G ^a   Vázquez, Berta N ^a,d   Maicas, Miren ^b,e   Aguilera Montilla, Noemí ^c   Corbí, Ángel L ^c   Odero, María D ^b   Lauzurica, Pilar ^a  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b UNIVERSITY OF NAVARRA   (Spain)

^c CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^d Life Sciences Building Rutgers University   (United States)

^e INSTITUTO DE BIOMECÁNICA DE VALENCIA   (Spain)

Author keywords

CD69; CNS; Enhancer; Gene regulation; Transcription regulation

Indexed keywords

CD69 ANTIGEN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RUNX1; LECTIN; LEUKOCYTE ANTIGEN; LUCIFERASE; PROTEIN BINDING; RUNX1 PROTEIN, HUMAN; T LYMPHOCYTE ANTIGEN;

ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; COMPUTER MODEL; ENHANCER REGION; GENE SILENCING; GENETIC TRANSCRIPTION; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; T LYMPHOCYTE; TRANSCRIPTION REGULATION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; DNA FLANKING REGION; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; JURKAT CELL LINE; K562 CELL LINE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; REPORTER GENE; TRANSGENE; TUMOR CELL LINE;

MAMMALIA;

5' FLANKING REGION; AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; BINDING SITES; CELL LINE, TUMOR; CONSERVED SEQUENCE; CORE BINDING FACTOR ALPHA 2 SUBUNIT; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION; GENES, REPORTER; HUMANS; JURKAT CELLS; K562 CELLS; LECTINS, C-TYPE; LUCIFERASES; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; TRANSCRIPTION, GENETIC; TRANSFECTION; TRANSGENES;

EID: 84925063184     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2015.02.031     Document Type: Article

References (44)

1. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489(7414):57-74.
2. Avots A., Hoffmeyer A., Flory E., Cimanis A., Rapp U.R., Serfling E. GABP factors bind to a distal interleukin 2 (IL-2) enhancer and contribute to c-Raf-mediated increase in IL-2 induction. Mol. Cell. Biol. 1997, 17(8):4381-4389.
3. Bannert N., Avots A., Baier M., Serfling E., Kurth R. GA-binding protein factors, in concert with the coactivator CREB binding protein/p300, control the induction of the interleukin 16 promoter in T lymphocytes. Proc. Natl. Acad. Sci. 1999, 96(4):1541-1546.
4. Cartharius K., Frech K., Grote K., Klocke B., Haltmeier M., Klingenhoff A., et al. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 2005, 21(13):2933-2942.
5. Castellanos M.C., Muñoz C., Montoya M.C., Lara-Pezzi E., López-Cabrera M., de Landázuri M.O. Expression of the leukocyte early activation antigen CD69 is regulated by the transcription factor AP-1. J. Immunol. 1997, 159(11):5463-5473.
6. Collins A., Littman D.R., Taniuchi I. RUNX proteins in transcription factor networks that regulate T-cell lineage choice. Nat. Rev. Immunol. 2009, 9(2):106-115.
7. del Carmen Castellanos M., López-Giral S., López-Cabrera M., de Landázuri O.M. Multiple cis-acting elements regulate the expression of the early T cell activation antigen CD69. Eur. J. Immunol. 2002, 32(11):3108-3117.
8. Don R.H., Cox P.T., Wainwright B.J., Baker K., Mattick J.S. 'Touchdown' PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res. 1991, 19(14):4008.
9. Egawa T., Tillman R.E., Naoe Y., Taniuchi I., Littman D.R. The role of the Runx transcription factors in thymocyte differentiation and in homeostasis of naive T cells. J. Exp. Med. 2008, 205(8):1939.
10. Fullard N., Wilson C.L., Oakley F. Roles of c-Rel signalling in inflammation and disease. Int. J. Biochem. Cell Biol. 2012, 44(6):851-860.
11. Gilmore T.D., Kalaitzidis D., Liang M.-C., Starczynowski D.T. The c-Rel transcription factor and B-cell proliferation: a deal with the devil. Oncogene 2004, 23(13):2275-2286.
12. Gottschalk L.R., Leiden J.M. Identification and functional characterization of the human T-cell receptor beta gene transcriptional enhancer: common nuclear proteins interact with the transcriptional regulatory elements of the T-cell receptor alpha and beta genes. Mol. Cell. Biol. 1990, 10(10):5486-5495.
13. Hara T., Jung L.K., Bjorndahl J.M., Fu S.M. Human T cell activation III. Rapid induction of a phosphorylated 28 kD/32 kD disulfide-linked early activation antigen (EA 1) by 12-o-tetradecanoyl phorbol-13-acetate, mitogens, and antigens. J. Exp. Med. 1986, 164(6):1988-2005.
14. Hatton R.D., Harrington L.E., Luther R.J., Wakefield T., Janowski K.M., Oliver J.R., et al. A distal conserved sequence element controls Ifng gene expression by T cells and NK cells. Immunity 2006, 25(5):717-729.
15. Higuchi R., Krummel B., Saiki R. A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res. 1988, 16(15):7351-7367.
16. Kasza A., Wyrzykowska P., Horwacik I., Tymoszuk P., Mizgalska D., Palmer K., et al. Transcription factors Elk-1 and SRF are engaged in IL1-dependent regulation of ZC3H12A expression. BMC Mol. Biol. 2010, 11:14.
17. Kulaeva O.I., Nizovtseva E.V., Polikanov Y.S., Ulianov S.V., Studitsky V.M. Distant activation of transcription: mechanisms of enhancer action. Mol. Cell. Biol. 2012, 32(24):4892-4897.
18. Li L., Zhang J.A., Dose M., Kueh H.Y., Mosadeghi R., Gounari F., et al. A far downstream enhancer for murine Bcl11b controls its T-cell specific expression. Blood 2013, 122(6):902-911.
19. López-Cabrera M., Muñoz E., Blázquez M.V., Ursa M.A., Santis A.G., Sánchez-Madrid F. Transcriptional regulation of the gene encoding the human C-type lectin leukocyte receptor AIM/CD69 and functional characterization of its tumor necrosis factor-α-responsive elements. J. Biol. Chem. 1995, 270(37):21545-21551.
20. Macian F. NFAT proteins: key regulators of T-cell development and function. Nat. Rev. Immunol. 2005, 5(6):472-484.
21. Maicas M., Vazquez I., Vicente C., Garcia-Sanchez M.A., Marcotegui N., Urquiza L., et al. Functional characterization of the promoter region of the human EVI1 gene in acute myeloid leukemia: RUNX1 and ELK1 directly regulate its transcription. Oncogene 2013, 32(16):2069-2078.
22. Marzio R., Jirillo E., Ransijn A., Mauël J., Corradin S.B. Expression and function of the early activation antigen CD69 in murine macrophages. J. Leukoc. Biol. 1997, 62(3):349-355.
23. Naito T., Tanaka H., Naoe Y., Taniuchi I. Transcriptional control of T-cell development. Int. Immunol. 2011, 23(11):661-668.
24. Ochiai K., Kagami M., Nakazawa T., Sugiyama T., Sueishi M., Ito M., et al. Regulation of CD69 expression on eosinophil precursors by interferon-γ. Int. Arch. Allergy Immunol. 2000, 122(Suppl. 1):28-32.
25. Paun A., Pitha P.M. The IRF family, revisited. Biochimie 2007, 89(6-7):744-753.
26. Pippa R., Espinosa L., Gundem G., Garcia-Escudero R., Dominguez A., Orlando S., et al. p27Kip1 represses transcription by direct interaction with p130/E2F4 at the promoters of target genes. Oncogene 2012, 31(38):4207-4220.
27. Prosser H.M., Wotton D., Gegonne A., Ghysdael J., Wang S., Speck N.A., et al. A phorbol ester response element within the human T-cell receptor beta-chain enhancer. Proc. Natl. Acad. Sci. U. S. A. 1992, 89(20):9934-9938.
28. Rao A., Luo C., Hogan P.G. Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol. 1997, 15(1):707-747.
29. Sancho D., Gómez M., Sánchez-Madrid F. CD69 is an immunoregulatory molecule induced following activation. Trends Immunol. 2005, 26(3):136-140.
30. Schönheit J., Kuhl C., Gebhardt M.L., Klett F.F., Riemke P., Scheller M., et al. PU.1 level-directed chromatin structure remodeling at the Irf8 Gene drives dendritic cell commitment. Cell Rep. 2013, 3(5):1617-1628.
31. Spitz F., Furlong E.E.M. Transcription factors: from enhancer binding to developmental control. Nat. Rev. Genet. 2012, 13(9):613-626.
32. Swat W., Dessing M., Boehmer H.V., Kisielow P. CD 69 expression during selection and maturation of CD4+8+ thymocytes. Eur. J. Immunol. 1993, 23(3):739-746.
33. Takeda J., Cheng A., Mauxion F., Nelson C.A., Newberry R.D., Sha W.C., et al. Functional analysis of the murine T-cell receptor beta enhancer and characteristics of its DNA-binding proteins. Mol. Cell. Biol. 1990, 10(10):5027-5035.
34. Tsytsykova A.V., Rajsbaum R., Falvo J.V., Ligeiro F., Neely S.R., Goldfeld A.E. Activation-dependent intrachromosomal interactions formed by the TNF gene promoter and two distal enhancers. Proc. Natl. Acad. Sci. 2007, 104(43):16850-16855.
35. Urasaki T., Takasaki J., Nagasawa T., Ninomiya H. Induction of the activation-related antigen CD69 on human eosinophils by type IIA phospholipase A2. Inflamm. Res. 2000, 49(4):177-183.
36. Vazquez B.N., Laguna T., Carabana J., Krangel M.S., Lauzurica P. CD69 gene is differentially regulated in T and B cells by evolutionarily conserved promoter-distal elements. J. Immunol. 2009, 183(10):6513-6521.
37. Vazquez B.N., Laguna T., Notario L., Lauzurica P. Evidence for an intronic cis-regulatory element within CD69 gene. Genes Immun. 2012, 13(4):356-362.
38. Visekruna A., Volkov A., Steinhoff U. A key role for NF-kappaB transcription factor c-Rel in T-lymphocyte-differentiation and effector functions. Clin. Dev. Immunol. 2012, 2012:239368.
39. Wang H., Zhang Y., Cheng Y., Zhou Y., King D.C., Taylor J., et al. Experimental validation of predicted mammalian erythroid cis-regulatory modules. Genome Res. 2006, 16(12):1480-1492.
40. Wong W.F., Kohu K., Chiba T., Sato T., Satake M. Interplay of transcription factors in T-cell differentiation and function: the role of Runx. Immunology 2011, 132(2):157-164.
41. Wotton D., Ghysdael J., Wang S., Speck N.A., Owen M.J. Cooperative binding of Ets-1 and core binding factor to DNA. Mol. Cell. Biol. 1994, 14(1):840-850.
42. Yang X.O., Pappu B.P., Nurieva R., Akimzhanov A., Kang H.S., Chung Y., et al. T helper 17 lineage differentiation is programmed by orphan nuclear receptors RORα and RORγ. Immunity 2008, 28(1):29-39.
43. Yoshimura C., Yamaguchi M., Iikura M., Izumi S., Kudo K., Nagase H., et al. Activation markers of human basophils: CD69 expression is strongly and preferentially induced by IL-3. J. Allergy Clin. Immunol. 2002, 109(5):817-823.
44. Ziegler S.F., Levin S.D., Johnson L., Copeland N.G., Gilbert D.J., Jenkins N.A., et al. The mouse CD69 gene. Structure, expression, and mapping to the NK gene complex. J. Immunol. 1994, 152(3):1228-1236.