Introduction
Abercrombie formulated: a cell’s relationship to the substratum
is the key to cell crawling, and it is the changing adhesion of
a cell to the substratum that moves a cell along (Abercrombie,
1978). Movement itself also requires traction, and the need for
contractility to provide traction for cell movement was clear to
the earliest investigators (Weiss, 1959). We now know that
traction is exerted on the substrate via specialised adhesion
sites that interface with the actin cytoskeleton. At least two
classes of adhesion sites can be distinguished: focal adhesions,
which interface with actin stress fibre bundles, and smaller,
focal complexes, which are associated with actin filament
networks and filopodia (reviewed in Burridge and
Chrzanowska-Wodnicka, 1996; Small et al., 1999a). Focal
complexes can serve as precursors of focal adhesions through
a transition effected by changes in the balance of activities of
members of the Rho GTPase family (Nobes and Hall, 1995;
Rottner et al., 1999a). And both focal complexes and focal
adhesions require contractility in the actin cytoskeleton for
their formation and maintenance (Chrzanowska-Wodnicka and
Burridge, 1996; Rottner et al., 1999a). Contractility, in turn,
probably plays an important part in inside-out signalling events
(Shyy and Chien, 1997), possibly through force-induced
conformational changes in molecules of the extracellular
matrix (Zhong et al., 1998), integrins (Vinogradova et al.,
2000; Takagi et al., 2001) and cytoskeleton-associated
components (Yamada and Geiger, 1997).
Cell locomotion not only involves the mutual and dynamic
reorganisation of the actin cytoskeleton and its associated
adhesion sites but also mechanisms that confer polarity on
these structural changes. Only then can traction forces in the
actin cytoskeleton be converted into net movement (e.g.
Beningo et al., 2001). Earlier findings attributed this polarising
function to microtubules (Vasiliev and Gelfand, 1976), and
more recent studies have revealed how they may achieve this
role (Kaverina et al., 1998; Kaverina et al., 1999; Kaverina et
al., 2000). It has been shown in fibroblasts that microtubules
specifically target substrate adhesion sites and that these
targeting events are followed by the turnover of adhesion sites
or their dislocation from the substrate (Kaverina et al., 1998;
Kaverina et al., 1999). Given the dependence of adhesion site
maintenance on contractility, it was speculated that
microtubules destabilise adhesions by delivering signals that
antagonise the contractility pathway. This contention was
supported by the demonstration that dissociation of adhesion
sites at the cell edge could be mimicked by the local application
of inhibitors of actomyosin contractility (Kaverina et al., 2000).
The question addressed in the present study is what is the
mechanism by which microtubules are guided to adhesion
sites. We formerly showed that the local application of
contractility inhibitors to a cell edge produced a rapid and local
depolymerisation of microtubules towards the cell centre. In
the present work, we have used alternative approaches to
modulate radial stress at the cell periphery. By this means, we
demonstrate that microtubules specifically invade regions
where stress is locally increased. These findings highlight a
stress-dependent feedback mechanism that presumably plays
an important role in the selection of adhesion sites for targeted
modulation via microtubules.
Materials and Methods
Cells and expression constructs
Cells of the mouse melanoma line B16F1 (ATCC) were maintained
2283
Cell motility is driven by the sum of asymmetric traction
forces exerted on the substrate through adhesion foci
that interface with the actin cytoskeleton. Establishment
of this asymmetry involves microtubules, which exert a
destabilising effect on adhesion foci via targeting events.
Here, we demonstrate the existence of a mechano-sensing
mechanism that signals microtubule polymerisation and
guidance of the microtubules towards adhesion sites under
increased stress. Stress was applied either by manipulating
the body of cells moving on glass with a microneedle or by
stretching a flexible substrate that cells were migrating on.
We propose a model for this mechano-sensing
phenomenon whereby microtubule polymerisation is
stimulated and guided through the interaction of a
microtubule tip complex with actin filaments under
tension.
Movies available on-line
Key words: Microtubules, Actin cytoskeleton, Adhesion, Tension,
Mechanosensor
Summary
Tensile stress stimulates microtubule outgrowth in
living cells
Irina Kaverina
1
, Olga Krylyshkina
1
, Karen Beningo
2
, Kurt Anderson
3
, Yu-Li Wang
2
and J. Victor Small
1,
*
1
Institute of Molecular Biology of the Austrian Academy of Sciences, A-5020, Austria
2
Department of Physiology, University of Massachusetts Medical School, Worcester, Massachusetts 01605, USA
3
Max Planck Institute for Molecular Cell Biology and Genetics, Pfotenhauerstr. 108, Dresden, D-01307, Germany
*Author for correspondence (e-mail: jvsmall@imb.oeaw.ac.at)
Accepted 21 March 2002
Journal of Cell Science 115, 2283-2291(2002) © The Company of Biologists Ltd
Research Article