INTRODUCTION
Cell migration involves interactions of the cell with the
surrounding extracellular matrix and requires a coordinated
series of steps, including attachment to the substrate,
generation of force and subsequent detachment from the
substrate (Lee et al., 1993). Cell attachment to the substrate
is mediated by adhesion receptors such as integrins (for
review on adhesion receptors see Aplin et al., 1998). The
nature of integrin-induced transmembrane signals controlling
cell migration is still unclear. Changes of [Ca
2+
]
i
are of
particular interest, since such modifications may well
modulate various stages of the migration process. Indeed,
many of the key proteins involved in migration can be
regulated by [Ca
2+
]
i
, including protein kinase C, myosin light
chain kinase, actin cytoskeleton regulating proteins such as
gelsolin (Cunningham et al., 1991) or fodrin (Harris and
Morrow, 1990) and integrins, whose affinity for extracellular
matrix proteins can be decreased by increases in [Ca
2+
]
i
(Hendey et al., 1992).
The relationship between changes in [Ca
2+
]
i
and cell
migration has been studied only in a few cell types. Multiple
transient increases in [Ca
2+
]
i
have been observed in response
to the chemoattractant f-Met-Leu-Phe (fMLP) in neutrophils
migrating on vitronectin or fibronectin (Jaconi et al., 1991;
Marks et al., 1991). Similar calcium transients during
migration were observed in the MDCK-F cell line (Wojnowski
et al., 1994) or in granule cells migrating from cerebellar
microexplant cultures (Komuro and Rakic, 1996).
The migration of vascular smooth muscle cells (VSMC) is
one important component in the formation of atherosclerotic
plaques (Ross, 1993). The mechanisms that govern this
function in this cell type are largely unexplored. Collagens are
the dominant surrounding extracellular matrix proteins for
VSMC in blood vessels and α
2
β
1
integrin has been shown to
be the adhesion receptor implicated in in vitro migration on
collagen (Pickering et al., 1997). However, the role of [Ca
2+
]
i
changes in any cell type migrating on collagen has, to our
knowledge, never been studied, although it has been reported
that α
2
β
1
integrin-mediated adhesion of human platelets to
collagen is associated with an increase of [Ca
2+
]
i
(Poole and
Watson, 1995). We have thus investigated the importance of
changes in [Ca
2+
]
i
in human VSMC migrating on type I
collagen.
MATERIALS AND METHODS
Materials
Cell culture media RPMI 1640 and M199, Hepes, L-glutamine,
penicillin, streptomycin, amphotericin B and trypsin-EDTA solution
(trypsin 0.5 g/l, EDTA 0.2 g/l) were from Gibco (Paisley, UK).
653 Journal of Cell Science 113, 653-662 (2000)
Printed in Great Britain © The Company of Biologists Limited 2000
JCS0822
Migration of vascular smooth muscle cells (VSMC) is a key
event in the formation of neointima during atherosclerosis.
Fura-2 loaded VSMCs were used to investigate calcium
homeostasis during cell migration. Multiple spontaneous
transient increases in cytosolic free calcium [Ca
2+
]
i
were
observed in single human VSMCs migrating on type I
collagen. Such [Ca
2+
]
i
transients were dependent on the
presence of serum or PDGF-BB. Removal of serum, or
loading cells with BAPTA, abolished the transients and
decreased cell migration speed. The transients were
not affected by disruption of cell polarization by
dihydrocytochalasin B. Adhesion was used to investigate
the specific role of cell-substrate interactions in the
generation of transients. Transients are seen in VSMCs
adhering either on collagen or on poly-L-lysine, suggesting
that generation of transients is not strictly dependent
on integrins. Buffering [Ca
2+
]
i
with BAPTA led to
accumulation of β1 integrins at the cellular tail, and to
increased release of integrin on the extracellular matrix.
These results demonstrate a role for [Ca
2+
]
i
transients in
the rapid, serum-dependent migration of VSMCs. These
[Ca
2+
]
i
transients are present in migrating VSMCs only
when two simultaneous events occur: (1) substrate
independent spreading and (2) stimulation of cells by
serum components such as PDGF-BB.
Key words: Migration, Smooth muscle, Integrin, Calcium, Collagen
SUMMARY
Migration of human vascular smooth muscle cells involves serum-dependent
repeated cytosolic calcium transients
Arnaud Scherberich, Manuel Campos-Toimil, Philippe Rondé, Kenneth Takeda and Alain Beretz*
Pharmacologie et Physico-Chimie des Interactions Cellulaires et Moléculaires, UMR CNRS 7034, Faculté de Pharmacie,
Université Louis Pasteur de Strasbourg, Illkirch, France
*Author for correspondence (e-mail: aberetz@pharma.u-strasbg.fr)
Accepted 2 December 1999; published on WWW 31 January 2000