INTRODUCTION
The extracellular matrix glycoprotein laminin mediates
adhesion events that are critical to a number of fundamental
biological phenomena, including cell migration, neurite
outgrowth and angiogenesis (see for review Yamada and
Kleinman, 1992). Although these events take hours for com-
pletion, they may be composed of a series of rapid and
reversible cellular interactions with laminin. Such reversible or
dynamic interactions are suggested, for example, by the rapid
lamellipod extensions that occur during translocation of
myoblasts on laminin (Goodman et al., 1989). The mechanisms
that regulate the dynamic interactions of cells with laminin or
other matrix proteins have not been examined. Based on
existing data, it can be postulated that dynamic interactions
involve a cycle of integrin-mediated attachment to and detach-
ment from matrix proteins and that this cycle is regulated by
the rapid modulation of integrin function (Regen and Horwitz,
1992).
The principal epithelial and carcinoma cell surface adhesion
receptors that interact with laminin are integrins α
2
β
1
, α
6
β
1
and α
6
β
4
(Sonnenberg et al., 1990; Lotz et al., 1990; Lee et al.,
1992). Although some carcinoma cells also express α
3
β
1
, an
established laminin and collagen receptor (Carter et al., 1990;
Kramer et al., 1990; Hynes, 1992), they do not appear to use
it in adhesion to laminin (Lotz et al., 1990). The α
2
β
1
integrin
laminin receptor functions as a collagen receptor in a number
of epithelial and carcinoma cells (Carter et al., 1990; Elices and
Hemler, 1989; Lotz et al., 1990). Integrins α
6
β
4
and α
6
β
1
bind
to laminin and to laminin subfragment E8, the distal stem and
proximal half of the large globule of the long arm (Kramer et
al., 1990; Elices et al., 1991; Lee et al., 1992). The β
4
integrin
subunit, which is probably the most structurally complex of all
integrins associates with variants of the α
6
integrin (Quaranta
and Jones, 1991). The α
6
integrin subunit has a higher binding
affinity for β
4
than for β
1
integrin (Giancotti et al., 1992). As
a result, in cells expressing both β
1
and β
4
integrins, α
6
integrin
preferentially associates with β
4
integrin (Hemler et al., 1989;
Kajiji et al., 1989; Simon-Assmann et al., 1994).
In a variety of cell types that express large amounts of the
α
6
β
4
integrin, it has not been possible to assign a distinct
adhesive function to α
6
β
4
using conventional adhesion tests
(Sonnenberg et al., 1990). Only recently, with the use of clone
A colon carcinoma cells that express α
6
β
4
but not α
6
β
1
and are
highly motile on laminin, was integrin α
6
β
4
shown to be a
laminin receptor (Lee et al., 1992). These authors also illus-
trated that carcinoma cell lines that express both α
6
β
4
and α
6
β
1
or exclusively α
6
β
1
(RKO human rectal carcinoma cells)
adhere to laminin with slower kinetics than the clone A cells.
The capacity for rapid attachment and motility on laminin
suggests a dynamic mode of interaction that is distinct and
perhaps more significant biologically than from more static
3153
We present here a novel form of dynamic adhesion in
which both the integrin receptor and the ligand supporting
dynamic adhesion have been identified. Laminar flow
assays showed that laminin supported attachment of α
6
β
4
-
positive cells in the presence of fluid shear stress (τ≤2
dyn/cm
2
), indicating that these cells adhered to laminin
within a fraction of a second. Further increases in flow rate
(3.5 dyn/cm
2
≤τ≤100 dyn/cm
2
) initiated rolling of attached
cells in the direction of flow, suggesting that rapidly formed
adhesion is reversible and repeatable. Laminin fragment
E8, which interacts with α
6
integrins, supported dynamic
attachment and rolling but extracellular matrix glycopro-
tein fibronectin did not. In cell lines that express α
6
β
4
but
not α
6
β
1
an anti-α
6
monoclonal antibody inhibited attach-
ment to laminin in the presence of flow and following 5
minutes of static incubation. Infusion of this antibody onto
cells adherent to laminin-coated slides led to rapid detach-
ment of cells from the substratum. An anti-β
1
monoclonal
antibody diminished adhesion strength following static
incubation but did not inhibit rapid attachment and flow-
initiated rolling. These results indicate that in some α
6
β
4
-
expressing epithelial and carcinoma cell lines, integrin α
6
β
4
mediates rapidly formed dynamic interactions with
laminin.
Key words: laminin, integrin, α6β4, dynamics, adhesion
SUMMARY
Integrin α
6
β
4
mediates dynamic interactions with laminin
Aydin Tözeren
1,
*, Hynda K. Kleinman
2
, Stephen Wu
1
, Arthur M. Mercurio
3
and Stephen W. Byers
4
1
Department of Mechanical Engineering, The Catholic University of America, Washington, DC 20064, USA
2
Laboratory of Developmental Biology, National Institute of Dental Research, National Institutes of Health, Bethesda, MD 20892,
USA
3
Laboratory of Cancer Biology, Deaconess Hospital, Harvard Medical School, Boston, MA 02115, USA
4
Department of Cell Biology and Lombardi Cancer Research Center, Georgetown University, Washington, DC 20007, USA
*Author for correspondence
Journal of Cell Science 107, 3153-3163 (1994)
Printed in Great Britain © The Company of Biologists Limited 1994