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Blood, 1 May 2002, Vol. 99, No. 9, pp. 3111-3118
CHEMOKINES
Signaling through ZAP-70 is required for CXCL12-mediated T-cell
transendothelial migration
Michel Ticchioni,
Céline Charvet,
Nelly Noraz,
Laurence Lamy,
Marcos Steinberg,
Alain Bernard, and
Marcel Deckert
From INSERM U343 and Laboratoire d'Immunologie,
Hôpital de l'Archet, Nice; and UMR 5535, Institut de
Génétique Moléculaire, Montpellier, France.
Transendothelial migration of activated lymphocytes from the blood
into the tissues is an essential step for immune functions. The
housekeeping chemokine CXCL12 (or stroma cell-derived factor-1 ), a
highly efficient chemoattractant for T lymphocytes, drives lymphocytes to sites where they are highly likely to encounter antigens. This suggests that cross-talk between the T-cell receptor (TCR) and CXCR4
(the CXCL12 receptor) might occur within these sites. Here we show that
the zeta-associated protein 70 (ZAP-70), a key element in TCR
signaling, is required for CXCR4 signal transduction. The pharmacologic
inhibition of ZAP-70, or the absence of ZAP-70 in Jurkat T cells and in
primary CD4+ T cells obtained from a patient with ZAP
deficiency, resulted in an impairment of transendothelial migration
that was rescued by the transfection of ZAP-70. Moreover, the
overexpression of mutated forms of ZAP-70, whose kinase domain was
inactivated, also abrogated the migratory response of Jurkat T cells to
CXCL12. In contrast, no involvement of ZAP-70 in T-cell arrest on
inflammatory endothelium under flow conditions or in CXCL12-induced
actin polymerization was observed. Furthermore, CXCL12 induced
time-dependent phosphorylation of ZAP-70, Vav1, and extracellular
signal-regulated kinases (ERKs); the latter were
reduced in the absence of functional ZAP-70. However, though a dominant-negative Vav1 mutant (Vav1 L213A) blocked
CXCL12-induced T-cell migration, pharmacologic inhibition of the ERK
pathway did not affect migration, suggesting that ERK activation is
dispensable for T-cell chemotaxis. We conclude that cross-talk between
the ZAP-70 signaling pathway and the chemokine receptor CXCR4 is
required for T-cell migration.
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