Wild type and tailless CD8 display similar interaction with microfilaments
during capping
PASCALE ANDRE
1
, JEAN GABERT
2
'*, ANNE MARIE BENOLIEL
1
, CHRISTIAN CAPO
1
, CLAUDE
BOYER
2
, ANNE MARIE SCHMITT-VERHULST
2
, BERNARD MALISSEN
2
and PIERRE BONGRAND
1
1
Laboratoire d'Immunologie, Hdpital de Sainte-Marguerite, BP 29, 13277 Marseille Cedex 09, France
2
Centre d'Immunologie de Marseille Luminy, Case 906, 13288 Marseille Cedex 9, France
* Present address: Institut Paoli-Calmettes, BP 156, 13273 Marseille Cedex 9, France
Summary
We examined the influence of the intracytoplasmic
region of CD8a on capping and interaction with
microfilaments. We used cell clones obtained by
transfecting a CD4+ T-cell hybridoma with (a) T-cell
receptor (TCR) a and fi chains from a cytolytic clone
and (b) CD8« genes that were either native or
modified by extensive deletion of the intracytoplas-
mic region or replacement of the transmembrane and
intracytoplasmic domains with those of a class I
major histocompatibility complex gene (Letourneur
et al. (1990). Proc. natn. Acad. Sci. U.S.A. 87,
2339—2343). Different cell surface structures were
cross-linked with anti-T-cell receptor, anti-CD8 or
anti-class I monoclonal antibodies and anti-immuno-
globulin (Fab')
2
. Double labeling and quantitative
image analysis were combined to monitor fluor-
escence anisotropy and correlation between differ-
ent markers. Microfilaments displayed maximal
polarization within two minutes. The correlation
between these structures and surface markers was
then maximal and started decreasing, whereas the
redistribution of surface markers remained stable or
continued. Furthermore, wild type and altered CD8«
exhibited similar ability to be capped and to induce
co-capping of TCR and MHC (major histocompati-
bility complex) class I: the fraction of cell surface
label redistributed into a localized cap ranged
between 40% and 80%. Finally, cytochalasin D
dramatically decreased CD8 capping in all tested
clones.
It is concluded that the transmembrane and/or
intracellular domains of CD8 molecules are able to
drive the extensive redistributions of membrane
structures and cytoskeletal elements that are trig-
gered by CD8 cross-linking.
Key words: membrane, molecular motion, cytoplasmic domain,
cytoskeleton, CD8.
Introduction
Since the elaboration of the fluid mosaic model of the
plasma membrane by Singer and Nicolson (1972), it has
become clear that many cell functions are affected by
lateral movements of membrane molecules. Cell adhesion
is thus highly dependent on the lateral mobility of ligand
molecules (Rutishauser and Sachs, 1974). Clearly, the
formation of strong intercellular bonds may require that
ligand molecules be concentrated in adhesion areas (Bell
et al. 1984), and this concentration was indeed observed in
several experimental studies using different method-
ologies such as electron microscopy (Singer, 1975), micro-
fluorometry (Poo and McCloskey, 1986) and conventional
(Kupfer and Singer, 1989) or computer-assisted (Andre et
al. 1990a,b)fluorescencemicroscopy. Also, the microaggre-
gation of cell surface receptors was found to enhance their
adhesive capacity (Detmers et al. 1987).
However, the mechanisms of molecular motion in the
plasma membrane remain incompletely understood.
When the mobility of cell surface proteins was studied
with the fluorescence photobleaching recovery (Schless-
inger et al. 1976) or post electric field relaxation (Poo et al.
1978) method, the diffusion coefficient of concanavalin A
Journal of Cell Science 100, 329-337 (1991)
Printed in Great Britain © The Company of Biologists Limited 1991
'receptors' (Schlessinger et al. 1976; Poo et al. 1978; Smith
et al. 1979), class I histocompatibility molecules (Edidin
and Zuniga, 1984; Bierer et al. 1987; Wier and Edidin,
1986) or lymphocyte surface immunoglobulins (Dragsten
et al. 1979; Barisas, 1984) varied between less than 10~
12
and about 2xlO~
9
cm
2
s~
1
. The latter value was roughly
consistent with theoretical estimates for free diffusion in a
thick viscous sheet (Wiegel, 1984). Thus, it appeared
reasonable to view the motion of cell surface proteins as a
hindered-diffusion process. In addition, these proteins may
undergo active displacements as exemplified by the
capping process (Taylor et al. 1971; Bourguignon and
Bourguignon, 1984).
Strong experimental evidence suggests that interac-
tions between cytoskeletal elements and membrane
intrinsic proteins are dynamic events (Flanagan and
Koch, 1978; Burn et al. 1988) that may hinder random
diffusion (Koppel et al. 1981; Tank et al. 1982). Further,
active movements may be affected by cytoskeletal inhibi-
tors (Taylor et al. 1971; Bourguignon and Bourguignon,
1984). However, the precise molecular interactions in-
volved in these phenomena remain incompletely under-
stood and it is not well known whether cytoskeletal
elements are bound to many membrane proteins or
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