COMMENTARY
Do anaphase chromosomes chew their way to the pole or are they pulled by
actin?
ARTHUR FORER
Biology' Department, York University, Dotvnsvietu, Ontario, M3J 1P3, Canada
Introduction
In a current model of anaphase chromosome movement it
is envisaged that depolymerization of microtubules at the
kinetochore produces the force to move a chromosome to
the pole. The chromosome itself generates the force for
chromosome movement by 'chewing' its way to the pole
along stationary microtubules, behaving as does 'PacMan'
in the video game of the same name (reviews by Cassimeris et al. 1987; Nicklas, 1988; Nicklas, 1988a; Wolniak, 1988). [This model is a re-statement of a model
presented much earlier (Gruzdev, 1972).] I describe
herein data that are not consistent with the PacMan
model and present an alternative view on how chromosomes move to the poles during anaphase. I first look at
the evidence for the model.
Evidence for the model
The PacMan model derives from three kinds of experiment, all of which were interpreted as evidence that the
chromosomes chew their way to the pole along stationary
kinetochore microtubules.
FRAP (Fluorescence Redistribution After
Photobleachirig) experiments
Fluorescently labelled tubulin was injected into dividing
cells, a local region of the spindle between chromosomes
and poles was photobleached, and the bleached region
either rapidly regained fluorescence, while remaining
stationary and not moving polewards (Salmon et al.
1984; Wadsworth & Salmon, 1986), or remained visible,
without gaining fluorescence, as the chromosomes moved
into and past the bleached region (Gorbsky et al. 1987,
1988).
Biotinylated tubulin experiments
Biotinylated tubulin was injected into living cells and the
incorporation of tubulin monomers into kinetochore
microtubules was followed by immunoelectron microscopy. Tubulin monomers appeared at the kinetochore ends of kinetochore microtubules during metaJournnl of Cell Science 91, 449-453 (1988)
Printed in Great Britain © The Company of Biologists Limited 1988
phase, but the same microtubules lost their labelled
subunits during anaphase (Mitchison et al. 1986).
Experiments on miovtubules in vitro
Microtubules polymerized in vitro from microtubuleassociated protein (MAP)-free tubulin were captured by
isolated chromosomes, and under appropriate conditions
the captured microtubules shortened. Those captured
with the same structural polarities as found in spindles;'/;
vivo shortened from the kinetochore ends, as determined
from microtubules labelled differently in different
portions of the microtubule (Koshland et al. 1988).
None of these interpretations is without flaws. With
respect to the FRAP experiments, the bleached region of
the spindle was not stationary in sea-urchin zygotes
(Hamaguchi et al. 1987), in either metaphase or anaphase. Further, the tubulin that was bleached was not
shown to be in kinetochore microtubules - it might have
been primarily in non-kinetochore microtubules or in
oligomeric tubulin. Until one is certain that the results
pertain to kinetochore microtubules one does not know if
the results from the FRAP experiments are relevant to
chromosome-to-pole motion.
With respect to the experiments using biotinylated
tubulin, the interpretation of events in anaphase is not
secure. There was variability in that after injection of
labelled tubulin in metaphase some cells in anaphase still
had label associated with kinetochore microtubules, and
some injections in anaphase resulted in incorporation of
labelled tubulin at the kinetochore. Serial-section analysis
was not performed, so there is uncertainty about which
microtubules were or were not labelled. Anaphase in the
cells studied consists primarily of spindle elongation chromosome-to-pole motion is a very minor component
of that particular anaphase, having been described as
being completed in 20-100 s (Mitchison et al. 1986) - so
the results, even if completely accurate, may not be
relevant to the movement of chromosomes to the poles.
With respect to the experiments on in vitro microtubules, there was indeed depolymerization of microtubules at their kinetochore ends for that set of
microtubules studied, but it is not at all clear that the
shortening in vitro of uncapped, MAP-free microtubules
449
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Distance along fibre
B
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00
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Birel
is relevant to the shortening in vivo of microtubules
which are capped at both ends and associated with MAPs.
Even if all the experiments discussed above unambiguously showed that kinetochore microtubules shortened at
the kinetochore in vivo as the chromosome moved to the
pole, there is no evidence that this has anything to do
with producing the force to move that chromosome to the
pole of a spindle.
I conclude that the evidence that suggests that kinetochore microtubules shorten at the kinetochore during
anaphase chromosome-to-pole motion is only suggestive,
and therefore that this interpretation of where kinetochore microtubules depolymerize during anaphase cannot be accepted without reservation. For purposes of
discussion I will assume that kinetochore microtubules
do depolymerize at the kinetochore in anaphase; but
there is no evidence that this depolymerization of microtubules produces the force that moves a chromosome to
the pole.
K
K,
1
•
1
;
\
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Distance along fibre
P
Data that the PacMan model Is inconsistent with
There are a variety of data with which the PacMan model
is inconsistent. I summarize some of those that are
particularly persuasive to me:
(1) The birefringence along the length of an individual
chromosomal spindle fibre is constant from the kinetochore half-way to the pole and then it decreases linearly
from there to the pole (Forer, 1976; Salmon & Begg,
1980; Schaap & Forer, 1984a,b), as illustrated in
Fig. 1A. If the microtubules between chromosome and
pole remain static in anaphase as they are depolymerized
at the chromosomal end, then, if the birefringence is due
to microtubules (Inoue\ 1981), the PacMan model predicts that (a) as the chromosome chews its way along the
microtubules the length of the region of constant birefringence should get shorter and shorter, and that (b)
after the chromosome reaches the region of the fibre in
which the birefringence linearly declines the birefringence at the kinetochore should get smaller and smaller as
the chromosome chews its way closer and closer to the
pole, as illustrated in Fig. IB. The actual events indeed
satisfy the prediction up to the point at which the
chromosomal spindle fibre birefringence decreases
linearly to the pole; after that the predicted changes do
not occur: the birefringence at the kinetochore remains
constant rather than decreasing (fig. 4 of Forer (1976);
fig. 5 of Salmon & Begg (1980); C. J. Schaap & A. Forer,
unpublished results), as illustrated in Fig. 1C. What
actually occurs in mid- to late-anaphase, then, is not
consistent with the basic postulate of the PacMan model
that chromosome-to-pole microtubules are depolymerized in anaphase at their kinetochore ends.
(2) The force on a chromosome is proportional to the
length of the chromosomal spindle fibre to which that
chromosome is attached (e.g. see Wise, 1978; Hays et al.
1982; Nicklas, 19886). This is inconsistent with the
PacMan model: the length of the fibre would not
determine the amount of force if the driving force for
motion were depolymerization of microtubules at the
kinetochore.
450
A. Forer
CQ
Distance along fibre
Fig. 1. Birefringence of an individual chromosomal spindle
fibre (ordinate) during metaphase measured at different
positions along the length of the fibre (abscissa), and the
changes in this pattern of birefringence during anaphase as
predicted by the PacMan model (B) and as actually measured
(C). P, position of the pole; K, position of the kinetochore in
metaphase; Kj and Kz, positions of the kinetochores at
successively later stages of anaphase. Based on data from
Forer (1976), Salmon & Begg (1980) and Schaap & Forer
(1984a, b).
(3) Various ultraviolet (u.v.) microbeam experiments
are also inconsistent with the PacMan model. In order to
explain the implications of these data I first summarize
some of the basic results.
u.v. microbeam irradiation of a single chromosomal
spindle fibre can produce an area of reduced birefringence (ARB) at the site of the irradiation; the ARB is a
region in which there is local depolymerization (absence)
of microtubules and thus the ARB is a discontinuity in
the kinetochore microtubules (Wilson & Forer, 1988).
u.v. microbeam irradiation of a single chromosomal
spindle fibre can also block (temporarily) the movement
of the associated chromosome, but the blocking of
movement is completely independent of effects on
spindle fibre birefringence (Forer, 1966; Sillers, 1983):
the wavelength sensitivities for producing ARBs are
different from those for blocking chromosome movement
(Fig. 2). Thus, by controlling wavelength and dose one
can predictably produce an ARB with no effect on
chromosome movement, or can block chromosome movement with no effect on spindle fibre birefringence, or
simultaneously can get an ARB and block chromosome
movement (Sillers & Forer, 1983). These experiments
are relevant to the PacMan model as follows.
Chromosome movement can be blocked by irradiations
0-6'
0-5-
£? 0-3-
Fig. 3. A model for chromosome movement in which the
microtubules (straight lines) are separate from the forceproducing component(s) of the spindle fibre (zig-zag lines),
and in which both components are attached to the
kinetochore (bottom, dark) and extend along the length of the
spindle fibre.
0-1-
260
270
280
nm
290
300
Fig. 2. The energy per area (ordinate) necessary to produce
either an ARB ( + ) or block chromosome movement (closed
circles) at various wavelengths (abscissa), after individual
chromosomal spindle fibres in crane fly spermatocytes were
irradiated with a u.v. microbeam. Based on data in Sillers &
Forer (1983) and Hughes et al. (1988).
along the length of the chromosomal spindle fibre (e.g.
Forer, 1969); this should not occur were the kinetochore
the site of force production. One can produce ARBs that
are immediately adjacent to the kinetochore, yet chromosome movement is normal (e.g. Forer, 1966): this should
not occur were the PacMan model correct, for irradiations that destroy all microtubules at the kinetochore
should block chromosome movement. Consider a cell in
which an ARB is produced several micrometres from the
kinetochore and chromosome movement is blocked: the
ARB immediately moves poleward (while the chromosome does not), and the chromosome resumes movement
before the ARB reaches the pole (e.g. Forer, 1966). In
this experiment not only is movement blocked by irradiation at a site distant from the chromosome, but the
poleward motion of the ARB also shows that nothing is
wrong with the kinetochore microtubules - indeed, the
resumption of chromosome motion before the ARB
reaches the pole shows that there is no need to 'repair' the
microtubules in the irradiated region in order for
chromosome movement to resume. All of these observations suggest that the force for movement does not arise
at the kinetochore-spindle fibre junction, and thus these
observations are inconsistent with the PacMan model.
(4) Observations on metaphase are inconsistent with
the PacMan model. Metaphase chromosomes are subject
to forces to both poles, as indicated by u.v. microbeam
irradiation of spindle fibres (Sillers et al. 1983) or laser
microbeam ablation of kinetochores (McNeill & Berns,
1981; Rieder et al. 1986). Oppositely directed poleward
forces in metaphase can not be due to depolymerization at
the kinetochore, as required by the PacMan model,
because in metaphase there is incorporation of tubulin at
the kinetochore, as indicated by localized release from
inhibition by colcemid (Czaban & Forer, 1985a,6), by
incorporation of biotinylated tubulin (Mitchison et al.
1986), and by poleward movement of a bleached region in
spindles labelled with fluorescent tubulin (Hamaguchi et
al. 1987). Unless one argues that force production at
metaphase is by a mechanism completely different from
that responsible for force production at anaphase, these
observations are inconsistent with the PacMan model.
(5) After an anaphase half-bivalent is pushed polewards using micromanipulation techniques, the chromosome sits and does not move until the other chromosomes
nearly catch up to it, as if it had to wait for the pushed
spindle fibre to be shortened (fig. 3 of Nicklas & Staehly,
1967). Were the force for chromosome movement to be
produced by depolymerization at the kinetochore, the
chromosome would continue to move as the fibre
shortened. Thus this observation is not consistent with
the PacMan model.
These are persuasive reasons, to me, for rejecting the
PacMan model. There is a simple alternative.
An alternative model for force production during
anaphase
I propose that something other than microtubules produces the force to move a chromosome to the pole
(Fig. 3). The role of the kinetochore microtubules is not
specified, but microtubules might act as "governor"
(Forer, 1974; Nicklas, 1975). The force-producing component is present along the length of the fibre, so
irradiations along the fibre could interfere with the forceproducing component at any position. Length could
matter because the force-producing component is distributed along the length of the fibre. And the model is
independent of wherever kinetochore microtubules depolymerize in anaphase.
What might the force-producing component(s) be?
Cellular motile systems are based either on microtubules
or on actin filaments (e.g. Forer, 1978), so if microtubules do not produce the force for chromosome motion
one would expect that actin filaments do. There is indeed
evidence implicating actin filaments. First, there are no
solid data that rule out actin or myosin as producing the
force to move a chromosome to the pole in anaphase
(reviewed by Forer, 1985). Second, actin is present in
chromosomal spindle fibres, with consistent structural
Anaphase chivmosome movement
451
0-6H
0-5-
0-4-
0-3-
0-2-
0-1-
260
270
280
nm
290
300
Fig. 4. The energy per area (ordinate) necessary to block
chromosome movement (closed circles) at various
wavelengths (abscissa) after individual chromosomal spindle
fibres were irradiated with a u.v. microbeam, in comparison
with the energies per area necessary to block myofibril
contraction after u.v. microbeam irradiation of the A band
(open circle) or I band (open square). Data on chromosome
movement are from Sillers & Forer (1983) and on myofibrils
from Wilson & Forer (1987).
polarity (Forer et al. 1979; reviewed by Forer, 1985;
additional evidence from staining with fluorescent phalloidin, see Seagull et al. 1987; Traas et al. 1987; Sheldon
& Hawes, 1988). Third, actin is implicated experimentally, as follows.
When chromosomal spindle fibres are irradiated with a
u.v. microbeam the peak sensitivities for blocking
chromosome movement are at wavelengths of 270 nm and
290 nm (Fig. 2); these match the peak sensitivities for
blocking contraction of myofibrils but are quite different
from those for blocking ciliary beating (Sillers & Forer,
1981). The peaks at 270 nm and 290 nm match absorption
peaks of actin (270 nm) and heavy meromyosin (290 nm)
but are quite different from the absorption peaks of
tubulin or microtubules (Forer, 1985).
Carrying further the comparisons of spindle fibres with
muscle proteins, the energies per area required to block
chromosome movement when a spindle fibre is irradiated
with u.v. light of wavelength 270nm or 290 nm match
exactly those needed to block myofibril contraction by
irradiating the actin filaments in the I band with u.v. light
of wavelength 270 nm or the A band with u.v. light of
wavelength 290 nm (Wilson & Forer, 1987), as illustrated
in Fig. 4. All these comparisons show a remarkable
coincidence between effects on chromosome movement
and effects on muscle proteins. Considering effects on
birefringence, however, the peak sensitivities for producing ARBs in vivo, 260 nm and 280 nm (Fig. 2), and the
452
A. Forer
doses, are the same as those for production of ARBs on
microtubules in vittv (Hughes et al. 1988). Hence the
effects on birefringence are indeed directly on chromosomal spindle fibre microtubules (Hughes et al. 1988);
since these are independent of effects on force production
(Fig. 2), this strongly argues that microtubules do not
produce the force that moves the chromosome to the
pole.
I conclude that these data are consistent with and
provide strong support for the suggestion that actin
filaments are involved in force production; they are
difficult to explain on any hypothesis other than that the
microtubules do not produce the force for chromosome
movement.
While the arguments for my view of force production
are not airtight, the model is testable. One test is to see if
there is a correlation between local depolymerization of
the putative non-microtubule force producer - actin
filaments - and blocking of chromosome movement, the
kind of correlation that does not exist between production
of ARBs (depolymerization of microtubules) and
blocking of chromosome movement. A second test is to
see if agents, such as phalloidin, that selectively stabilize
actin filaments will protect the chromosomal spindle fibre
against u.v. microbeam irradiation, that otherwise would
have blocked chromosome movement. Agents, such as
taxol, that selectively stabilize microtubules, however,
might protect the chromosomal spindle fibre against
production of ARBs. These are the kinds of experiments
that we will be doing to test this alternative view of
anaphase chromosome movement.
In sum, the evidence used to support the PacMan
model is not compelling. I described evidence that
persuades me that the site of force production is not at the
kinetochore but along the chromosomal spindle fibre. In
my view, even if it is substantiated that the kinetochore
microtubules depolymerize at the kinetochores as the
chromosomes move poleward, this does not mean that
the depolymerization generates the force that moves the
chromosome - microtubule depolymerization may only
be the governor, the rate-limiting step that controls the
velocity of the chromosomes. I argue that the force that
causes the chromosome to move most likely arises from a
non-microtubule component of the spindle fibre, probably actin.
I thank Paula Wilson for a tough, critical reading of the
manuscript. This work was supported by a grant from the
Natural Sciences and Engineering Research Council of Canada.
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Anaphase chivmosome movement
453