Biology Reference
In-Depth Information
The modern understanding of the periodic movement of the cell body can be
traced conceptually to the earlier work on muscle and flagella oscillations. Pringle
(
1949
) proposed that insect flight muscles were activated by stretch, and that this
leads to autonomous oscillations in the antagonistic muscle pairs. The indepen-
dence of this emergent mechanical behavior from the control by the nervous system
provides, on the organ level, an analogy to the subject of systems biomechanics of
the cell. Subsequently Brokaw (
1975
) showed theoretically that if disengagement of
cross-bridges increased with the load, then coupled antagonistic pairs could develop
and sustain oscillations. Indeed, the load-induced disengagement introduces the
feedback that further weakens the losing side in the tug of war. This principle was
applicable equally to myosin cross-bridges in muscle and dynein cross-bridges in
flagella, and equally to pairs of flight muscles and diametrically opposite microtu-
bule doublets in a flagellum. It mechanistically and quantitatively resolved the prob-
lem of the time delay requirement, which was implicit in Pringle's proposal.
The idea of the load-induced disengagement of molecular motors was applied to
oscillations of the cell body by Grill et al. (
2005
). Their one-dimensional model was
developed for the motion of the posterior spindle pole during the first division in
C.
elegans
. Force generators exhibiting the stretch-induced disengagement were pos-
tulated to act on astral microtubules reaching the opposite sides of the cell boundary
orthogonally to the spindle axis. The restoring force necessary for the oscillations
was assumed to arise from the bending elasticity of the microtubules, which was
modeled as amounting collectively to a simple Hookean spring tying the centro-
some to the central position. The pulling strength must be sufficiently strong in this
model relative to the strength of the restoring spring for the oscillations to arise and
to be sustained. This prediction was further elaborated theoretically and tested
experimentally (Pecreaux et al.
2006
).
Subsequent work of Kozlowski et al. (
2007
) put the load-dependent force gen-
erators in a theoretical framework that included explicitly computed deformations
of the astral microtubules in
Caenorhabditis
. The new model resolved mechanisti-
cally the problem of the physical conditions of the microtubule contact with the
pulling cortex, which was implicit in the previous model. Kozlowski et al. demon-
strated experimentally that the microtubules in this experimental system transition
to disassembly upon contact with the cell boundary, and showed theoretically that
the oscillatory dynamics can be sustained despite the brevity of each individual
contact. As the authors note, the model was constructed to be representative of the
conditions during anaphase B, when the oscillations take place in the
Caenorhabditis
egg, and would not be correct for the telophase, when the microtubules emanating
from the former spindle pole become greatly deformed against the boundary of the
posterior daughter cell.
The conditions of the very large deformations that are established at the end of
the first division prevail also during the second division in
Caenorhabditis
, when the
spindle pole oscillations are again observed (Keating and White
1998
). They simi-
larly prevail in lymphocytes conjugated with target cells (Kuhn and Poenie
2002
),
where the single interphase centrosome oscillates in close proximity to the cell-cell
interface. [Structural and biomechanical similarities of these two systems have been
reviewed in detail before (Maly
2011
)]. The difficulty in applying the previously
