Advancement of leading lamellae of a migratory cell inevitably causes a strain inside the cell body. We investigated the effect of the tension arisen inside a mesodermal cell on its behavior by pulling the cell body unidirectionally along the substratum. Chick gastrula mesodermal cells, known as highly migratory, were dissociated into single cells in sodium citrate buffer, conjugated with paramagnetic beads activated by tosyl-residue (4.5 microns in diameter) and seeded onto coverglasses coated with fibronectin. After the cells spread on the substratum and protruded cellular processes in all directions, they were exposed to a non-uniform magnetic field by a magnet. Thus the cells bearing the beads were pulled with a force in the order of 10(−10) N. The behavior of such cells was recorded with a time-lapse video taperecorder and assessed quantitatively. Shortly after the magnetic force was applied, the beads stuck to the cells were aligned in tandem along the line of magnetic force at the site for the magnet. Subsequently, they frequently came to extend their leading lamella precisely counter to the traction on the line of the beads. Observation with scanning electron microscope revealed that a large part of the beads attached to the cells were wrapped in the cell membrane. In this condition, the cells were stretched locally between the attachment site of the beads and adhesion plaques beneath the leading edge, which was formed in a direction away from the traction. It was proved statistically that such cells tended to locomote away from the magnet at the 0.1% significance level with Hotelling's T2-test. In contrast, the mesodermal cells free of the artificial traction in three kinds of control experiments did not show such a preference in the direction of locomotion. These results proved that migratory cells tended to move in the direction away from the tractive force parallel to the substratum, suggesting that advancement of a leading lamella is accelerated when it is stretched along the direction of projection by a mechanical force of sufficient strength. Implication of this finding to the mechanism of cell locomotion will be discussed.

REFERENCES

Abercrombie
M.
,
Heaysman
J. E.
,
Pegrum
S. M.
(
1970
).
The locomotion of fibroblasts in culture. III. Movements of particles on the dorsal surface of the leading lamella.
Exp. Cell Res
62
,
389
398
Abercrombie
M.
(
1980
).
The crawling movement of metazoan cells.
Proc. Roy. Soc. Lond. B
207
,
129
147
Beloussov
L. V.
,
Dorfman
J. G.
,
Cherdantzev
V. G.
(
1975
).
Mechanical stresses and morphological patterns in amphibian embryos.
J. Embryol. Exp. Morph
34
,
559
574
Boucaut
J. C.
,
Darribere
T.
(
1983
).
Fibronectin in early amphibian embryos: migrating mesodermal cells are in contact with a fibronectin-rich fibrillar matrix established prior to gastrulation.
Cell Tiss. Res
234
,
135
145
Buck
R. C.
(
1980
).
Reorientation response of cells to repeated stretch and recoil of the substratum.
Exp. Cell Res
127
,
470
474
Buck
R. C.
(
1983
).
Behavior of vascular smooth muscle cells during repeated stretching of substratum in vitro.
Atherosclerosis
46
,
217
223
Buckley
M. J.
,
Banes
A. J.
,
Levin
L. G.
,
Sumpio
B. E.
,
Sato
M.
,
Jordan
R.
,
Gilbert
J.
,
Link
G. W.
,
Tran Son Tay
R.
(
1988
).
Osteoblasts increase their rate of division and align in response to cyclic, mechanical tension in vitro.
Bone Miner
4
,
225
236
Critchley
D. R.
,
England
M. A.
,
Wakely
J.
,
Hynes
R. O.
(
1979
).
Distribution of fibronectin in the ectoderm of gastrulating chick embryos.
Nature
280
,
498
500
Dartsch
P. C.
,
Hammerle
H.
(
1986
).
Orientation response of arterial smooth muscle cells to mechanical stimulation.
Eur. J. Cell Biol
41
,
339
346
Dembo
M.
,
Harris
A. K.
(
1981
).
Motion of particles adhering to the leading lamella of crawling cells.
J. Cell Biol
91
,
528
536
Dewey
C. F.
,
Bussolari
S. R.
,
Gimbrone
M. A.
,
Davies
P. F.
(
1981
).
The dynamic response of vascular endothelial cells to fluid shear stress.
J. Biomech. Eng
103
,
177
185
Doroszewski
J.
,
Lewandowska
K.
,
Wierzbicki
W.
(
1986
).
Locomotion of granulocytes on an inclined plane.
Acta Physiol. Pol
37
,
79
91
Duband
J. L.
,
Volberg
T.
,
Sabanay
I.
,
Thiery
J. P.
,
Geiger
B.
(
1988
).
Spatial and temporal distribution of the adherence-junction-associated adhesion molecule A-CAM during avian embryogenesis.
Development
103
,
325
344
Duband
J. L.
,
Thiery
J. P.
(
1990
).
Spatio-temporal distribution of the adherence-junction associated molecules vinculin and talin in the early avian embryo.
Cell Differ
30
,
55
76
Franke
R.-P.
,
Grafe
M.
,
Schnittler
H.
,
Seiffge
D.
,
Mittermayer
G.
,
Drenckhahn
D.
(
1984
).
Induction of human vascular endothelial stress fibers by fluid shear stress.
Nature
307
,
648
649
Hamburger
V.
,
Hamilton
H. L.
(
1951
).
A series of normal stages in the development of the chick embryo.
J. Morphol
88
,
49
92
Harrisson
F.
,
Andries
L.
,
Vakaet
L.
(
1988
).
The chicken blastoderm: current views on cell biological events guiding intracellular communication.
Cell Diff
22
,
83
106
Hashimoto
K.
,
Fujimoto
H.
,
Nakatsuji
N.
(
1987
).
An ECM substratum allows mouse mesodermal cells isolated from the primitive streak to exhibit motility similar to that inside the embryo and reveals a deficiency in the T/T mutant cells.
Development
100
,
587
598
Hatta
K.
,
Takeichi
M.
(
1986
).
Expression of N-cadherin adhesion molecules associated with early morphogenic events in chick development.
Nature
320
,
447
449
Isenberg
G.
,
Rathke
P. C.
,
Hulsmann
N.
,
Franke
W. W.
,
Botterman
K. E. W.
(
1976
).
Cytoplasmic actomyosin fibrils in tissue culture cells. Direct proof of contractility by visualization of ATP-induced contraction in fibrils isolated by laser microbeam dissection.
Cell Tiss. Res
166
,
427
443
Ishijima
A.
,
Doi
T.
,
Sakurada
K.
,
Yanagida
T.
(
1991
).
Sub-piconewton force fluctuations of actomyosin in vitro.
Nature
352
,
301
306
Izzard
C. S.
,
Lochner
L. R.
(
1976
).
Cell-to-substrate contacts in living fibroblasts: an interference reflection study with an evaluation of the technique.
J. Cell Sci
21
,
129
159
Korega
G.
(
1986
).
Effects of mechanical tension on protrusive activity and microfilament and intermediate filament organization in an epidermal epithelium moving in culture.
J. Cell Biol
102
,
1400
1411
Korohoda
W.
,
Vöth
M.
,
Bereiter-Hahn
J.
(
1992
).
Biphasic response of human polymorphonuclear leucocytes and keratinocytes (epitheliocytes) from Xenopus laevis to mechanical stimulation.
Protoplasma
167
,
169
174
Lotz
M. M.
,
Burdsal
C. A.
,
Erickson
H. P.
,
McClay
D. R.
(
1989
).
Cell adhesion to fibronectin and tenascin: Quantitative measurements of initial binding and subsequent strengthening response.
J. Cell Biol
109
,
1795
1805
Margolis
L. B.
(
1991
).
Induction of cell processes by local force.
J. Cell Sci
98
,
369
373
Nakatsuji
N.
,
Johnson
K. E.
(
1984
).
Experimental manipulation of a contact guidance system in amphibian gastrulation by mechanical tension.
Nature
307
,
453
455
Oiwa
K.
,
Chaen
S.
,
Kamitubo
E.
,
Shimmen
T.
,
Sugi
H.
(
1990
).
Steady-state force-velocity relation in the ATP-dependent sliding movement of myosin-coated beads on actin cables in vitro studied with a centrifuge microscope.
Proc. Nat. Acad. Sci. USA
87
,
7893
7897
Oster
G.
,
Murray
J.
,
Harris
A.
(
1983
).
Mechanical aspects of mesenchymal morphogenesis.
J. Embryol. Exp. Morphol
78
,
83
125
Pender
N.
,
McCulloch
C. A. G.
(
1991
).
Quantitation of actin polymerization in two human fibroblast sub-types sub-types responding to mechanical stretching.
J. Cell Sci
100
,
187
193
Sato
M.
,
Schwarz
W. H.
,
Pollard
T. D.
(
1987
).
Dependence of the mechanical properties of actin/alpha-actinin gels on the deformation rate.
Nature
325
,
828
830
Shirinsky
V. P.
,
Antonov
A. S.
,
Birukov
K. G.
,
Sobolevsky
A. V.
,
Romanov
Y. A.
,
Kavaeva
N. V.
,
Antonova
G. N.
,
Simirnov
V. N.
(
1989
).
Mechano-chemical control of human endothelium orientation and size.
J. Cell Biol
109
,
331
339
Takeuchi
S.
(
1979
).
Wound healing in the cornea of the chick embryo.
Dev. Biol
70
,
232
240
Takeuchi
S.
(
1984
).
Mesoblastic cells in the early phase of primitive streak formation in chick embryos. Observation by scanning electron microscopy in ovo and time-lapse cinematography in vitro.
Dev. Growth Differ
26
,
235
247
Toyoizumi
R.
,
Shiokawa
K.
,
Takeuchi
S.
(
1991
).
The behavior and cytoskeletal system of chick gastrula mesodermal cells on substrata coated with lines of fibronectin.
J. Exp. Zool
260
,
345
353
Truskey
G. A.
,
Pirone
J. S.
(
1990
).
The effect of fluid shear stress upon cell adhesion to fibronectin-treated surfaces.
J. Biomed. Mat. Res
24
,
1333
1353
Vakaet
L.
(
1970
).
Cinephotomicrographic investigations of gastrulation in the chick blastoderm.
Archives de Biologie
81
,
387
426
Wang
N.
,
Butler
J. P.
,
Ingber
D. E.
(
1993
).
Mechanotransduction across the cell surface and through the cytoskeleton.
Science
260
,
1124
1127
Winklbauer
R.
(
1990
).
Mesodermal cell migration during Xenopus gastrulation.
Dev. Biol
142
,
155
168
Wong
A. J.
,
Pollard
T. D.
,
Herman
I. M.
(
1983
).
Actin filament stress fibers in vascular endothelial cell in vivo.
Science
219
,
867
869
Yanagida
T.
,
Arata
T.
,
Oosawa
F.
(
1985
).
Sliding distance of actin filament induced by a myosin cross bridge during one ATP hydrolysis cycle.
Nature
316
,
366
–.
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