Abstract
As an adhesion receptor, the beta2 integrin lymphocyte function-associated antigen-1 (LFA-1) contributes a strong adhesive force to promote T lymphocyte recirculation and interaction with antigen-presenting cells. As a signaling molecule, LFA-1-mediates transmembrane signaling, which leads to the generation of second messengers and costimulation resulting in T cell activation. We recently have demonstrated that, in costimulatory fashion, LFA-1 activation promotes the induction of T cell membrane urokinase plasminogen activator receptor (uPAR) and that this induced uPAR is functional. To investigate the mechanism(s) of this induction, we used the RNA polymerase II inhibitor 5, 6-dichloro-1-beta-D-ribobenzimidazole and determined that uPAR mRNA degradation is delayed by LFA-1 activation. Cloning of the wild-type, deleted and mutated 3'-untranslated region of the uPAR cDNA into a serum-inducible rabbit beta-globin cDNA reporter construct revealed that the AU-rich elements and, in particular the nonameric UUAUUUAUU sequence, are crucial cis-acting elements in uPAR mRNA degradation. Experiments in which Jurkat T cells were transfected with reporter constructs demonstrated that LFA-1 engagement was able to stabilize the unstable reporter mRNA containing the uPAR 3'-untranslated region. Our study reveals a consequence of adhesion receptor-mediated signaling in T cells, which is potentially important in the regulation of T cell activation, including production of cytokines and expression of proto-oncogenes, many of which are controlled through 3' AU-rich elements.
MeSH Terms
Amino Acid Sequence
Humans
Integrins/genetics,immunology
Jurkat Cells
Leukocytes/immunology
Molecular Sequence Data
RNA Processing, Post-Transcriptional/immunology
RNA, Messenger/analysis,genetics
Receptors, Cell Surface/genetics,immunology
Receptors, Urokinase Plasminogen Activator
T-Lymphocytes/immunology
Urokinase-Type Plasminogen Activator/immunology
Chemicals
Integrins
PLAUR protein, human
RNA, Messenger
Receptors, Cell Surface
Receptors, Urokinase Plasminogen Activator
Urokinase-Type Plasminogen Activator
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Wang G J
Section of Immunobiology, Molecular Cardiobiology, Boyer Center for Molecular Medicine, Yale University School of Medicine, 295 Congress Avenue, New Haven, CT 06536, USA.
Collinge M
Blasi F
Pardi R
Bender J R
References (27)
27 references, click to expand
-
A conserved AU sequence from the 3' untranslated region of GM-CSF mRNA mediates selective mRNA degradation.
Cell. 1986 Aug 29;46(5):659-67
PMID: 3488815
-
Adhesion-dependent regulation of an A+U-rich element-binding activity associated with AUF1.
Mol Cell Biol. 1997 Jul;17(7):3898-906
PMID: 9199324
-
The c-fos transcript is targeted for rapid decay by two distinct mRNA degradation pathways.
Genes Dev. 1989 Jan;3(1):60-72
PMID: 2496006
-
Regulation of lymphokine messenger RNA stability by a surface-mediated T cell activation pathway.
Science. 1989 Apr 21;244(4902):339-43
PMID: 2540528
-
Heterogeneous distribution and transmembrane signaling properties of lymphocyte function-associated antigen (LFA-1) in human lymphocyte subsets.
J Immunol. 1989 Nov 15;143(10):3157-66
PMID: 2553807
-
Regulation of interleukin 3 mRNA expression in mast cells occurs at the posttranscriptional level and is mediated by calcium ions.
Proc Natl Acad Sci U S A. 1990 Jan;87(2):777-81
PMID: 2105489
-
The LFA-1 ligand ICAM-1 provides an important costimulatory signal for T cell receptor-mediated activation of resting T cells.
J Immunol. 1990 Jun 15;144(12):4579-86
PMID: 1972160
-
Expression of the CD4 gene requires a Myb transcription factor.
Mol Cell Biol. 1992 Apr;12(4):1592-604
PMID: 1347906
-
Integrins: versatility, modulation, and signaling in cell adhesion.
Cell. 1992 Apr 3;69(1):11-25
PMID: 1555235
-
Costimulation of T lymphocytes: the role of CD28, CTLA-4, and B7/BB1 in interleukin-2 production and immunotherapy.
Cell. 1992 Dec 24;71(7):1065-8
PMID: 1335362
-
Ca2+ ionophore A23187-dependent stabilization of granulocyte-macrophage colony-stimulating factor messenger RNA in murine thymoma EL-4 cells is mediated through two distinct regions in the 3'-untranslated region.
J Immunol. 1993 May 15;150(10):4386-94
PMID: 8482841
-
CD11a/CD18 (LFA-1) integrin engagement enhances biosynthesis of early cytokines by activated T cells.
Cell Immunol. 1993 Apr 15;148(1):48-59
PMID: 8098668
-
Beta 2-integrin LFA-1 signaling through phospholipase C-gamma 1 activation.
Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7099-103
PMID: 7688472
-
ICAM-3, the third LFA-1 counterreceptor, is a co-stimulatory molecule for both resting and activated T lymphocytes.
Eur J Immunol. 1993 Nov;23(11):2799-806
PMID: 8223855
-
Costimulation of T lymphocytes with integrin ligands intercellular adhesion molecule-1 or vascular cell adhesion molecule-1 induces functional expression of CTLA-4, a second receptor for B7.
J Immunol. 1994 Mar 15;152(6):2686-97
PMID: 7511623
-
AUUUA is not sufficient to promote poly(A) shortening and degradation of an mRNA: the functional sequence within AU-rich elements may be UUAUUUA(U/A)(U/A).
Mol Cell Biol. 1994 Dec;14(12):7984-95
PMID: 7969138
-
The nonamer UUAUUUAUU is the key AU-rich sequence motif that mediates mRNA degradation.
Mol Cell Biol. 1995 Apr;15(4):2219-30
PMID: 7891716
-
Contact-dependent endothelial class II HLA gene activation induced by NK cells is mediated by IFN-gamma-dependent and -independent mechanisms.
J Immunol. 1995 Apr 1;154(7):3222-33
PMID: 7897208
-
Triggering of complement receptors CR1 (CD35) and CR3 (CD11b/CD18) induces nuclear translocation of NF-kappa B (p50/p65) in human monocytes and enhances viral replication in HIV-infected monocytic cells.
J Immunol. 1995 Nov 15;155(10):4861-7
PMID: 7594489
-
A hierarchy of ECM-mediated signalling regulates tissue-specific gene expression.
Curr Opin Cell Biol. 1995 Oct;7(5):736-47
PMID: 8573350
-
AU-rich elements: characterization and importance in mRNA degradation.
Trends Biochem Sci. 1995 Nov;20(11):465-70
PMID: 8578590
-
Extracellular matrix alters PDGF regulation of fibroblast integrins.
J Cell Biol. 1996 Jan;132(1-2):239-49
PMID: 8567727
-
Cloning and characterization of HuR, a ubiquitously expressed Elav-like protein.
J Biol Chem. 1996 Apr 5;271(14):8144-51
PMID: 8626503
-
The regulation of growth and intracellular signaling by integrins.
Endocr Rev. 1996 Jun;17(3):207-20
PMID: 8771356
-
Integrin-dependent induction of functional urokinase receptors in primary T lymphocytes.
J Clin Invest. 1996 Sep 1;98(5):1133-41
PMID: 8787676
-
Posttranscriptional regulation of urokinase receptor mRNA: identification of a novel urokinase receptor mRNA binding protein in human mesothelioma cells.
Mol Cell Biol. 1997 Mar;17(3):1075-83
PMID: 9032234
-
Kinetics of cellular oncogene expression in mouse lymphocytes. II. Regulation of c-fos and c-myc gene expression.
Eur J Immunol. 1987 May;17(5):713-8
PMID: 3556196