Program in Cellular Biotechnology, Institute of Biotechnology, PO Box 56, 00014 University of Helsinki, Finland
* Author for correspondence (e-mail: pekka.lappalainen{at}helsinki.fi )
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Summary |
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Key words: Actin, Twinfilin, ADF-H domain, Capping protein, Cytoskeletal dynamics
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Introduction |
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Actin-monomer-binding proteins play an important role in cells by
controlling the size and localization of the cytoplasmic actin-monomer pool
and by regulating the incorporation of actin monomers into filaments. Three
classes of small actin-monomer-binding protein exist in organisms as diverse
as yeasts and mammals: ADF/cofilin, profilin and twinfilin
(Bamburg et al., 1999;
Pollard et al., 2000
;
Lappalainen et al., 1998
). In
addition to these three ubiquitous proteins, a fourth class of small
actin-monomer-binding protein, ß-thymosins, is present in vertebrates.
ß-thymosins are small ATP-actin-monomer-binding proteins whose role is to
sequester a large pool of unpolymerized actin in cells
(Pollard et al., 2000
).
ß-thymosins are expressed typically in highly motile cells such as
platelets and differentiating neurons
(Border et al., 1993
).
ADF/cofilins are small (15-19 kDa) proteins that bind both actin monomers
and filaments. They promote rapid actin dynamics in cells by increasing the
depolymerization rate at the minus end (pointed end) of actin filaments
(Carlier et al., 1997;
Rosenblatt et al., 1997
;
Lappalainen and Drubin, 1997
).
ADF/cofilins may also have a weak actin filament-severing activity, which
would account for the formation of new filament ends
(Chan et al., 2000
).
ADF/cofilins interact with ADP-acin-monomers and filaments with higher
affinities than ATP-actins and inhibit the spontaneous nucleotide exchange on
actin monomers (Bamburg et al.,
1999
). These small actin-binding proteins appear to be essential
for viability in all eukaryotes: null mutations in Saccharomyces
cerevisiae, Caenorhabditis elegans and Drosophila melanogaster
ADF/cofilin genes are lethal (Moon et al.,
1993
; McKim et al.,
1994
; Gunsalus et al.,
1995
).
Profilins are small (13-16 kDa) proteins that bind only actin monomers.
Profilins promote assembly at the plus end (barbed end) of the filament, but
they also suppress spontaneous filament nucleation. Therefore, profilins
function as actin-monomer-sequestering proteins in the absence of free
filament plus ends (Pantaloni and Carlier,
1993; Vinson et al.,
1998
). By contrast with ADF/cofilins, profilins bind
ATP-actin-monomers with higher affinity than ADP-actin (Goldschmidt-Cleremont
et al., 1991; Pantaloni and Carlier,
1993
; Vinson et al.,
1998
). Furthermore, profilins, enhance the nucleotide exchange on
actin monomers and, at least in the yeasts S. cerevisiae and S.
pombe, this activity is essential in vivo
(Wolven et al., 2000
;
Lu and Pollard, 2001
).
The third evolutionarily conserved class of small actin-monomer-binding protein, twinfilins, was identified more recently. The biological roles and actin interactions of twinfilin are less well characterized than those of ADF/cofilins and profilins. Here we review recent advances in our knowledge about this ubiquitous actin-monomer-binding protein and discuss its possible role in actin filament turnover.
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Structure and biochemical properties of twinfilin |
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Twinfilin is a 37-40 kDa protein composed of two ADF/cofilin-like (ADF-H)
domains connected by a short linker region and followed by a C-terminal tail
of 20 residues (Fig. 1A).
The two ADF-H domains are
20% homologous to ADF/cofilin and to each other
(Lappalainen et al., 1998
).
Interestingly, the individual twinfilin ADF-H domains are more similar across
species than are the N- and C-terminal ADF-H domains within a species
(Fig. 1B). This suggests that
the ADF-H domain duplicated once before the divergence of the fungal and
animal lineages. The positions of secondary structural elements are relatively
well conserved between ADF/cofilin and twinfilin; both ADF-H domains probably
therefore have tertiary structures similar to that of ADF/cofilin proteins.
Furthermore, insertions in the twinfilin ADF-H domains are located in the
predicted loop regions (Lappalainen et
al., 1998
).
|
All twinfilins characterized so far are biochemically similar. The human
homologue of twinfilin was originally identified as a tyrosine kinase
(Beeler et al., 1994), but
recent studies have demonstrated that neither mammalian
(Vartiainen et al., 2000
;
Rohwer et al., 1999
) nor
fungal (Goode et al., 1998
)
twinfilins have kinase activity. Twinfilins also lack sequence homology to
known protein kinases. Instead, all twinfilins characterized so far are
actin-monomer-binding proteins (Goode et
al., 1998
; Vartiainen et al.,
2000
;
Wahlström et
al., 2001
). They appear to form a 1:1 complex with actin monomers:
in actin filament sedimentation assays, yeast twinfilin shifts actin monomers
to the supernatant fraction in a
1:1 molar ratio
(Goode et al., 1998
). In
addition, the migration of the mouse twinfilinactinmonomer complex in a
sucrose gradient is consistent with a 1:1 molar ratio
(Vartiainen et al., 2000
). The
ability of twinfilin to prevent actin filament assembly in sedimentation
assays and in kinetic pyrene actin assembly assays shows that twinfilin is an
efficient actin-monomer-sequestering protein
(Goode et al., 1998
;
Vartiainen et al., 2000
;
Wahlström et
al., 2001
). Furthermore, yeast twinfilin inhibits the spontaneous
nucleotide exchange on actin monomers in a manner similar to that of
ADF/cofilins (Goode et al.,
1998
).
The residues important for actin-monomer binding in ADF/cofilins are well
conserved in both twinfilin ADF-H domains
(Lappalainen et al., 1998),
and recent mutagenesis studies on yeast twinfilin demonstrated that these
corresponding residues are important for actin-monomer binding
(Palmgren et al., 2001
). This
suggests that twinfilins and ADF/cofilins interact with actin monomers at
partly or completely overlapping interfaces. Both ADF/cofilin
(Maciver and Weeds, 1994
;
Carlier et al., 1997
) and
twinfilin (Palmgren et al.,
2001
) prefer to interact with ADP-actin-monomers; in contrast, the
actin-monomer-binding proteins profilin and thymosin-ß4 bind
ATP-actin-monomers with higher affinities
(Carlier et al., 1993
;
Pantaloni and Carlier, 1993
;
Vinson et al., 1998
).
Therefore, ADF/cofilin and twinfilin may interact with newly depolymerized,
assembly-incompetent ADP-actin-monomers, whereas profilin and thymosin-ß4
regulate the dynamics of the assembly-competent ATP-actin-monomer pool.
Despite these similarities between twinfilin and ADF/cofilin, the proteins
differ in other aspects. In contrast to ADF/cofilins, twinfilins do not
detectably bind actin filaments and do not promote the depolymerization of
actin filaments (Goode et al.,
1998; Vartiainen et al.,
2000
;
Wahlström et
al., 2001
). Such a lack of actin filament binding is further
supported by the fact that the residues essential for binding of ADF/cofilin
to actin filaments (Lappalainen et al.,
1997
; Ono et al.,
2001
) are not conserved in twinfilins
(Lappalainen et al.,
1998
).
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Localization and biological function of twinfilin |
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The subcellular localization of twinfilin strongly suggests its involvement
in actin filament dynamics. In budding yeast, twinfilin is diffusely
cytoplasmic but is also concentrated at cortical actin patches, which are
sites of rapid actin filament turnover
(Palmgren et al., 2001). In
cultured mammalian cells, twinfilin has a strong punctate cytoplasmic staining
pattern, and a significant proportion is also localized to cellular processes
rich in actin monomers and filaments
(Vartiainen et al., 2000
). In
developing Drosophila bristles, twinfilin is diffusely cytoplasmic
and concentrated at the ends of actin bundles
(Wahlström
et al., 2001
). Further support for the involvement of twinfilin in
actin filament dynamics comes from the observation that overexpressing
twinfilin in yeast and mammalian cells results in the formation of abnormal
actin structures: in yeast the actin cytoskeleton is depolarized and actin
bars accumulate in the cytoplasm (Goode et
al., 1998
), and in mammalian cells there are fewer stress fibers
and worm-like actin filament structures appear
(Vartiainen et al., 2000
).
Deletion of the twinfilin gene in budding yeast does not produce a
clear phenotype, but the twf mutants appear to have somewhat
abnormal cortical actin patches and defects in the bipolar bud-site selection
pattern (Goode et al., 1998
;
Fig. 2B). The role of twinfilin
during the development of a multicellular organism has been investigated in a
Drosophila strain carrying a P-element insertion in the first intron
of the twinfilin gene. These flies show a dramatic decrease in twinfilin mRNA
and protein. The mutants are smaller and less active than wild-type flies.
Furthermore, they have morphological defects such as a rough eye phenotype,
but the most obvious external phenotype is seen in bristles
(Wahlström
et al., 2001
). Drosophila bristles are sensory organs
formed from a single cell as a long extension that is supported by actin
filament bundles. Each bundle is composed of repeated units attached end to
end. As the bristle elongates, actin filaments are formed at the tip of the
bristle and then progressively packed together to form new units that have
maximally crosslinked filaments (Tilney et
al., 2000
). In the twinfilin mutants, the bristles are
shorter than those of wild-type flies and are often bent
(Fig. 2D). The mutant bristles
also have a rough surface morphology: the ridges and grooves of the bristles
are highly irregular. Phalloidin staining of the developing bristles
demonstrated that the actin bundles in the mutant bristles are often twisted
and misoriented and that the twinfilin mutant bristles contain many
abnormal F-actin-containing spots or tiny actin bundles. These abnormal actin
structures explain the defective mutant bristle morphology observed in the
adult
(Wahlström
et al., 2001
).
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The role of twinfilin in actin filament turnover |
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All biochemical data indicate that twinfilin is an actin-monomer-binding
protein, but it localizes to the cortical actin filament structures in yeast
and mammalian cells, and to the ends of the actin filament bundles in
developing Drosophila bristles
(Palmgren et al., 2001;
Vartiainen et al., 2000
;
Wahlström et
al., 2001
). In yeast, the localization of twinfilin to cortical
actin patches is dependent on the presence of intact actin filaments, because
twinfilin is diffusely cytoplasmic in cells treated with the
actin-filament-depolymerizing agent latrunculin-A
(Palmgren et al., 2001
). These
data suggest that twinfilin also interacts with other components of the
cortical actin cytoskeleton.
We screened several yeast strains with mutations in known components of the
cortical actin cytoskeleton and discovered that twinfilin does not localize to
the cortical actin patches in strains carrying deletions in CAP1 and
CAP2, which encode the two subunits of the heterodimeric actin
filament plus end capping protein
(Palmgren et al., 2001).
Deleting either subunit of the capping protein leads to a loss of the other
subunit (Amatruda et al.,
1992
). Twinfilin co-immunoprecipitates with capping protein from
yeast extracts, and the purified proteins directly interact as shown by native
PAGE (Palmgren et al., 2001
).
The twinfilin-capping protein interaction appears to be conserved during
evolution, because mouse twinfilin and
1ß2 capping protein also
interact in vitro (Palmgren et al.,
2001
). Furthermore, in developing Drosophila bristles,
twinfilin localizes to the plus ends of the actin bundles, where capping
protein is reported to be
(Wahlström
et al., 2001
; Hopmann et al.,
1996
). Correct localization of twinfilin to the cortical actin
cytoskeleton also appears to require an interaction with an actin monomer,
because a mutant twinfilin that is unable to interact with actin monomers in
vitro is diffusely cytoplasmic when expressed in yeast
(Palmgren et al., 2001
).
It is possible that the biological role of twinfilin is to recycle actin
monomers, in their `inactive' ADP-form, to the sites of actin filament
assembly in cells (Fig. 3). In
such a model, newly depolymerized ADP-actin-monomers could be delivered to
twinfilin by ADF/cofilin, as suggested by the ability of twinfilin to form a
stable complex with ADP-actin-monomers, and the overlapping actin-binding
interfaces of twinfilin and ADF/cofilin. Twinfilin might keep the delivered
actin monomers in their `inactive' ADP form, because yeast twinfilin inhibits
the spontaneous nucleotide exchange on actin monomers
(Goode et al., 1998).
Therefore, twinfilin would prevent actin filament assembly at undesired
locations in the cells. The twinfilinADP-actin-monomer complexes could
then be concentrated to the cellular sites of rapid actin filament assembly
through interactions between twinfilin and capping protein. After dissociating
from twinfilin, the actin monomer would undergo nucleotide exchange and
assemble into the plus end of the filament either spontaneously or by a
profilin-catalyzed mechanism (Fig.
3). Further support for a role for twinfilin as an
actin-monomer-recycling/localizing protein is provided by the genetic
interactions between twinfilin and cofilin
(Goode et al., 1998
;
Wahlström et
al., 2001
) and between twinfilin and profilin
(Wolven et al., 2000
). In
yeast, the twinfilin-null mutant shows synthetic lethality with the
cofilin mutant cof1-22: an allele that exhibits diminished actin
filament depolymerization activity
(Lappalainen and Drubin, 1997
)
and shows synthetic lethality with the profilin mutant pfy1-4, which
has defects in actin nucleotide exchange activity
(Wolven et al., 2000
). In
combination with possible defects in the actin filament localization activity
of
twf1 cells, either one of these mutations would be expected
to result in a significant decrease in the number of assembly competent
(ATP-actin) monomers at the sites of rapid actin filament assembly.
|
The activities of many actin-binding proteins are regulated by
phosphorylation or by binding to phosphatidylinositols. In mammalian cells,
the activity of twinfilin is regulated by phosphorylation (M.V. and P.L.,
unpublished), whereas phosphorylated twinfilin has not been detected in yeast
(S.P. and P.L., unpublished). However, yeast twinfilin interacts with
phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P2) in
vitro, and this interaction downregulates the actin-monomer-sequestering
activity of twinfilin (Palmgren et al.,
2001). The interaction with PtdIns(4,5)P2
might keep twinfilin from sequestering actin monomers at those cell regions
where the nucleation and assembly of actin filaments is rapid. In general, the
proteins that promote the assembly of actin filaments (e.g. WASP) are
upregulated by PtdIns(4,5)P2
(Rohatgi et al., 2000
;
Higgs and Pollard, 2000
),
whereas the activity of the proteins that promote the disassembly of actin
filaments (e.g. ADF/cofilin) is downregulated
(Yonezawa et al., 1990
).
PtdIns(4,5)P2 also promotes the assembly of actin
filaments under in vivo conditions, as demonstrated by studies of actin
polymerization by PtdIns(4,5)P2-containing vesicles in
cell extracts (Ma et al.,
1998
) and living cells
(Rozelle et al., 2000
;
Tall et al., 2000
). It remains
to be shown whether the interaction between twinfilin and
PtdIns(4,5)P2 takes place in vivo and if this interaction
has any physiological relevance.
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Conclusions and perspectives |
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In the future, it remains to be shown whether twinfilin's role is indeed to localize ADP-actin-monomers in cells, or whether it has a more complex role in actin dynamics. Furthermore, it will be important to elucidate the molecular mechanism of the twinfilinactin-monomer interaction. It is still unclear why twinfilin, which forms a 1:1 complex with actin monomers, has two ADF-H domains. At least in theory, both ADF-H domains of twinfilin should be able to interact with one actin monomer. Further studies must also elucidate how actin monomers are released from twinfilin and whether the interaction with capping protein affects the actin-monomer-binding activity of twinfilin. Finally, it will be interesting to examine how various signal transduction pathways regulate the activity of twinfilin in different cell types and during various cell biological processes.
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Acknowledgments |
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