Effect of MAP2, MAP2c, and tau on kinesin-dependent microtubule motility
SUSANNE HEINS, YOUNG-HWA SONG, HOLGER WILLE, ECKHARD MANDELKOW
and EVA-MARIA MANDELKOW*
Max-Planck-Unit for Structural Molecular Biology, c/o DESY, Notkestrasse 85, D-2000 Hamburg 52, Germany
* Corresponding author
Summary
By making use of DIC video microscopy to monitor
microtubule motility we have studied the effect of
several MAPs (MAP2, MAP2c, tau) on microtubule-
kinesin interactions and microtubule gliding. Of the
three M APs tested, M AP2 interferes most strongly
with kinesin-dependent microtubule motility.
Key words: kinesin, microtubules, motility, MAPs.
Introduction
The transport of vesicles and organelles in nerve cells
depends on microtubules and their motor proteins (Allen
et al. 1985; Brady et al. 1985; Vale et al. 1985). These cells
also contain a variety of microtubule-associated proteins
(MAPs) which tightly bind to and stabilize the micro-
tubules. Some of the MAPs (e.g. MAP2) are fairly large,
have elongated shapes and can protrude for several tens of
nanometres from the microtubule surface. The crowding of
proteins in the axoplasm poses some problems; for
example, how can a motor protein move along a micro-
tubule in spite of the MAPs present? What is the influence
of MAPs on axonal transport?
The analogue of anterograde axonal transport can be
studied in vitro by observing microtubules gliding over a
surface covered with the motor protein kinesin, using
video-enhanced DIC microscopy (Allen et al. 1985; Vale et
al. 1985). The visualization of the microtubules depends
not only on the optical parameters and image enhance-
ment, but also, because of the small depth of field, on the
confinement of the microtubules to a region just above the
surface. If the microtubules detach from the surface and
diffuse into the solution they become essentially invisible.
Thus the image contains information both on microtubule
attachment and on motility. It can therefore be used to
study factors that affect these two parameters.
We have recently reported on the interference of MAP2
with microtubule attachment and kinesin-dependent
motility (von Massow et al. 1989). The experiments (see
diagrams in Fig. 1) showed that (1) pure microtubules
attach to the surface and are therefore visible, (2) a surface
covered with MAP2 prevents the attachment of micro-
tubules which are therefore invisible and (3) kinesin
attached to the surface binds and moves microtubules.
However (4) when the surface is covered with both kinesin
and MAP2, the effect of MAP2 dominates, i.e. micro-
tubules neither attach nor move, and thus are not visible;
(5) when MAP2 is present both on the surface and on
microtubules, microtubules attach to the surface again, in
contrast to (2), as if the MAP2 molecules coming from
Journal of Cell Science, Supplement 14, 121-124 (1991)
Printed in Great Britain © The Company of Biologists Limited 1991
opposite directions interlocked with one another; in this
case kinesin cannot induce movement either.
These effects depend on certain concentration ratios
between kinesin, MAPs, and microtubules, which we have
now studied in more detail. In addition we were interested
to determine if other MAPs had effects similar to MAP2.
We have now tested two proteins which are homologous
with MAP2 (1828 residues) in the C-terminal region,
which contains the internal repeats responsible for
microtubule binding (Lewis et al. 1988). They are tau
(around 400 residues, depending on isoform; Lee et al.
1988; Goedert et al. 1988), which has a much shorter N-
terminal domain than MAP2 and shows no homology to it,
and MAP2c (467 residues), a juvenile form of MAP2,
arising from alternative splicing, which is homologous to
MAP2 but lacks most of the N-terminal region (Papan-
drikopoulou et al. 1989). The results reported below show
that their effects are much less pronounced than those of
MAP2 in terms of the above assays, suggesting that only
the full length MAP2 contains special regions, presumably
in the N-terminal domain, that are responsible for the
repulsion of microtubules from the surface or the MAP-
2-MAP2 interlocking.
Materials and methods
Preparation of microtubules
PC-tubulin was prepared as previously described (Mandelkow et
al. 1985). MAP-free microtubules were polymerized in assembly
buffer (0.1 m PIPES, pH 6.9, ImM each of MgS04, EGTA, DTT,
and GTP) and stabilized by 10 /iM taxol.
Preparation of kinesin
Kinesin was prepared after Kuznetsov and Gelfand (1986) or Vale
et al. (1985), with modifications (von Massow et al. 1989; Song,
unpublished).
Preparation of MAPs
MAP2 and tau were prepared from porcine brain as described
(Hagestedt et al. 1989), involving a boiling step, separation on
Mono S HPLC (Pharmacia), and their differential solubility in
perchloric acid. MAP2c was prepared similarly and separated
from MAP2 by gel filtration (Superose 12 column, Pharmacia).
Motility assay and sample preparation
Microtubules and their movement by kinesin were observed by
DIC video microscopy following the method of Allen et al. (1985).
The effects of MAPs on microtubule attachment and gliding were
performed as previously described (von Massow et al. 1989).
Briefly, the samples are prepared in two steps: (1) coating of the
glass surface by pre-incubation with kinesin, MAPs, or both, (2)
addition of microtubules, made either from PC-tubulin and
stabilized by taxol, or with re-attached purified MAPs. The pre-
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