![[Feedback]](/icons/banner/feedbackACT.gif){kind=icon}
![[For Subscribers]](/icons/banner/subscriberACT.gif){kind=icon}
![[Archive]](/icons/banner/archiveACT.gif){kind=icon}
![[Search]](/icons/banner/searchACT.gif){kind=icon}
![[Contents]](/icons/banner/tocACT.gif){kind=icon}
|
|
|
|
|
||
Vol. 9, Issue 8, 1951-1959, August 1998
Department of Molecular and Cell Biology, University of California, Berkeley, California 94720-3202
Submitted February 9, 1998; Accepted June 5, 1998  |
INTRODUCTION |
|---|
Top
Introduction
Conclusions
References
|
|---|
Genome sequencing projects have dramatically increased the amount of sequence data available in public databases, providing an opportunity to identify new protein families. The definition of new protein families allows knowledge from studies of one or a few members of a protein family to be applied to many other proteins in the family. The analysis presented here defines an actin-binding module, the actin-depolymerizing factor homology (ADF-H) domain, which is present in each member of a newly identified, extensive protein family. This family consists of three phylogenetically distinct classes: the ADF/cofilins, the twinfilins, and the drebrin/Abp1s. Each class has been used by eukaryotic organisms for more than 1 billion years, since before the divergence of fungi and animals. The ADF-H domain can be considered a functional building block that is arranged differently in each of the three protein classes in the family. In addition to being evolutionarily distinguishable, proteins in each class seem to possess distinct biochemical properties. Thus, ancient duplication of the ADF-H domain allowed the development of functional diversity.
| |
THE ADF-H DOMAIN PROTEIN FAMILY |
|---|
To regulate the structure and dynamics of the actin cytoskeleton,
a plethora of actin-binding proteins has evolved. As the sequence,
structural and biochemical data on actin-binding proteins has
accumulated, it has become evident that many actin-binding proteins
have evolved through the duplication and mutation of DNA sequences
encoding a relatively small number of protein motifs or modules (for
definitions of motifs and modules, see Henikoff et al.,
1997
) that interact with monomeric (G) or filamentous (F) actin in a
specific manner. Three widely occurring actin-binding motifs and
modules that govern the structure and dynamics of the actin
cytoskeleton have been described to date: 1) the calponin homology
domain, 2) the thymosin-
4 motif, and 3) the gelsolin homology domain
(Van Troys et al., 1996, Puius et al.,
1998).
A fourth group of widely occurring actin-binding proteins with sequence
and biochemical similarity is the ADF/cofilin group, which facilitates
the rapid in vivo disassembly of actin filaments (for a recent review,
see Theriot, 1997). Using a comprehensive sequence database search, we
have identified 39 proteins that contain a module (an ADF-H domain)
with sequence similarity to ADF/cofilins. Examination of the primary
structures of these proteins shows that the ADF-H domain protein family
can be subdivided into three structurally distinct classes, which we
have termed the ADF/cofilins, the twinfilins, and the drebrin/Abp1s
(Figure 1).
|
ADF/Cofilins
The ADF/cofilins are composed of a single ADF-H domain (Figure 1)
and include ADF, cofilin, destrin, actophorin, coactosin, and depactin.
ADF/cofilin proteins can interact with both actin monomers and
filaments with dissociation constants in the submicromolar range
(reviewed by Moon and Drubin, 1995; Theriot, 1997). Furthermore, upon
binding to actin filaments, cofilin increases filament twist (McGough
et al., 1997) and promotes the turnover of the filaments by
increasing the koff rate of the monomers at the
minus end of actin filaments (Carlier et al., 1997).
Cofilin-induced filament depolymerization provides an essential element
of actin dynamics in vivo (Lappalainen and Drubin, 1997), and thus
these proteins are required for viability in yeast, worms, and flies
(Moon et al., 1993, McKim et al., 1994, Gunsalus
et al., 1995).
Twinfilins
To our surprise, sequence database searches revealed proteins that
are remarkable in that they are composed of two ADF-H domains (Figure
1). Genes encoding these proteins, which we have named the twinfilins,
are found in humans, mice, and yeast (and recently a cDNA clone
encoding a probable twinfilin has been obtained from Dictyostelium discoideum [R. Insall, personal communication
regarding the University of Tsukuba Dictyostelium cDNA
project]). Human twinfilin had been originally identified by screening
an embryonic fibroblast expression library with an anti-phosphotyrosine
antibody and was named A6. Bacterially expressed A6 was reported to
phosphorylate exogenous substrates on tyrosine residues (Beeler
et al., 1994). This protein, however, lacks any of the
motifs commonly conserved in the catalytic domains of protein kinases,
raising doubts about its identification as a protein kinase. Our recent
studies have shown that yeast twinfilin localizes to the cortical actin
cytoskeleton and that purified twinfilin sequesters actin monomers by
forming a tight 1:1 complex with actin monomers (Goode et
al., 1998). Thus, twinfilin is indeed a bona fide actin-binding
protein. We find no evidence for cross-linking of actin filaments by
twinfilin. However, the presence of both ADF-H domains confers tighter
actin monomer binding than is observed when only the first domain is expressed (Goode et al., 1998).
Drebrin/Abp1s
Proteins of the drebrin/Abp1 class have a single ADF-H domain at
their N-termini, followed by a nonconserved central region and a
C-terminal Src homology 3 (SH3) domain (Figure 1). All available biochemical data to date indicate that members of this class bind to
F-actin but not G-actin. Yeast Abp1 is linked to the Ras/adenylate cyclase signaling pathway via interactions with Srv2/CAP (Freeman et al., 1996, Lila and Drubin, 1997). A related
protein in mouse, found in our database searches, is expressed in all
tissues and binds to F-actin (Kessels, unpublished results). This
protein was independently discovered by screening for SH3
domain-containing proteins and was named SH3P7 (Sparks et
al., 1996). The drebrins are neuron-specific F-actin-binding
proteins proposed to provide plasticity to the cytoskeleton and to
serve as intracellular regulators of morphogenesis (Ishikawa et
al., 1994, Shirao 1995).
| |
EVOLUTION OF THE ADF-H DOMAIN |
|---|
A protein sequence alignment and subsequent phylogenetic analysis
of all ADF-H domains currently present in the public databases group
these domains in a manner (Figures 2 and
3A) that agrees with the classification
described above, which was based on the domain arrangement of each
class of ADF-H domain protein (Figure 1). Based on this analysis, the
ADF-H family consists of three phylogenetically distinct classes, the
ADF/cofilin class, the drebrin/Abp1 class, and the twinfilin class.
Interestingly, members of each class are found in organisms as diverse
as mammals and yeast, indicating that each was already present in the
common ancestor of all of these organisms. Coactosin from D. discoideum and depactin from Asterias amurensis, which
are each composed of a single ADF-H domain, are the only proteins whose
phylogenetic classification remains somewhat ambiguous. Statistical
analysis of the phylogenetic tree ("bootstrapping") indicates that
coactosin and depactin are, in terms of sequence, more closely related
to the drebrin/Abp1 class, whereas their biochemical activities (F- and
G-actin binding) appear to be more similar to the members of the
ADF/cofilin class (Takagi et al., 1988; de Hostos et
al., 1993).
|
|
It is important to note that repeats 1 and 2 of twinfilins are distinct from one another and form separate subbranches in the tree (Figure 3). Because each branch contains sequences from such evolutionarily distant organisms as yeast and mammals, it can be concluded that the duplication of the ADF homology domain and the creation of a twinfilin protein was an ancient event that took place (probably only once in evolution) before the divergence of the yeast and animal lineages.
Examination of the phylogenetic trees shown in Figure 3 reveals that all members of ADF/cofilin class have evolved from a single ancestral protein. In multicellular organisms, such as plants and animals, as many as three ADF/cofilin proteins per species have been found. For example, cofilin, destrin 1, and destrin 2 have been identified in Homo sapiens, and ADFs 1-3 have been found in Zea mays. In contrast, there is only a single cofilin in Saccharomyces cerevisiae (and probably in Schizosaccharomyces pombe). These multiple members also arose from single ancestral proteins, distinct examples of which appeared after divergence of the plant and animal kingdoms. In mammals and chicken, the multiple ADF/cofilin proteins fall into at least three distinct subclasses (muscle cofilin, nonmuscle cofilin, and destrin). The gene duplications that gave rise to these three subclasses of vertebrate cofilins took place before divergence of birds and mammals, because the same subclasses exist in both chicken and mammals. Although only up to two of these subclasses have been found to date in a given mammalian species or in chicken, our analysis enables us to predict that at least one member from each of these subclasses will be present in all mammals and all birds. There is an additional subclass of vertebrate ADF/cofilins, made up of two ADF-H proteins, in the toad, Xenopus laevis. It is almost certain that further ADF/cofilins are present in this species as well as members of the drebrin/Abp1 and twinfilin classes.
A simplification of the evolutionary path taken by the ADF-H domain proteins, as determined from the phylogenetic tree, is depicted in Figure 3B. All three classes of these proteins were already present before the divergence of yeast and animals. This implies that each class has performed an important role in eukaryotes for more than 1 billion years. After the emergence of vertebrates, further gene duplication events took place providing additional proteins in the drebrin/Abp1 and the ADF/cofilin classes. These additional proteins presumably helped in the creation of the more complex actin cytoskeletons of multicellular organisms.
| |
STRUCTURE AND FUNCTION OF THE ADF-H DOMAIN |
|---|
To date, three high-resolution structures of ADF homology domains
have been reported. The structure of human destrin was determined by
nuclear magnetic resonance (Hatanaka et al., 1996)
and was followed by the 2.3-Å resolution x-ray crystal structures of
yeast cofilin (Fedorov et al., 1997) and
Acanthamoeba actophorin (Leonard et al., 1997).
All three structures display a very similar fold, with a central
six-stranded mixed -sheet sandwiched between two pairs of
-helices, one on each face (Figure
4a). The only significant difference
between these structures is the presence of an additional -helix in
human destrin between -strands 1 and 2 (Figures 2 and 4a).
|
A surprising and remarkable feature of the three-dimensional structures
of ADF/cofilin proteins is the similarity of their overall fold to
another actin-binding module, the gelsolin homology domain. Members of
both actin-binding protein families are built around a central mixed
-sheet and show the same topological connections of secondary
structure elements (McLaughlin et al., 1993; Hatanaka et al., 1996).
Because gelsolin consists of multiple segments, and because it appears
that different gelsolin segments interact with actin through different
interfaces, it is possible that at least one of the gelsolin segments
interacts with actin in a manner similar to that of ADF/cofilin
proteins. In support of this hypothesis, recent studies have suggested
that cofilin and gelsolin segment 2 might interact with actin in a
similar manner (Van Troys et al., 1997). In contrast, it
appears that the actin-binding surfaces of cofilin and gelsolin segment
1 are significantly different from each other. The gelsolin segment
1-actin interface has been identified from x-ray crystallography
studies (McLaughlin et al., 1993). Systematic mutagenesis
studies of yeast cofilin suggested that the actin-binding site of
cofilin is more extended than the actin-binding site of gelsolin
segment 1 and is not as clearly built around the "long" -helix
(-3 in yeast cofilin) (Lappalainen et al., 1997; Figure
4B). Furthermore, electron microscopy studies on cofilin-decorated
actin filaments indicate that the cofilin-binding site on an actin
filament is significantly different from the gelsolin segment 1-binding
site (McGough et al., 1997). Finally, it should be noted
that whereas gelsolin segment 1 is able to interact only with actin
monomers (Weeds and Maciver, 1993), members of the ADF/cofilin class of
proteins interact tightly with both actin monomers and actin filaments.
Based on the structural homology and the similarity of their
biochemical activities (actin binding), it has been proposed that
ADF/cofilin proteins and gelsolins have evolved from a common ancestral
actin-binding protein (Hatanaka et al., 1996). Primary sequence alignments of ADF/cofilins with gelsolins, however, do not
reveal sequence identity between these groups of proteins higher than
would be expected between two unrelated proteins. The inclusion of
gelsolins in the ADF-H protein family is therefore not justified at
this stage, and a meaningful phylogenetic analysis that included
gelsolin would be impossible. It must be noted that convergent, as well
as divergent, evolution could have given rise to the structural
similarities between the proteins. For these reasons, we have in this
essay focused only on the three classes of ADF-H domain proteins that
clearly evolved from a common ancestral gene.
From the sequence alignment shown in Figure 2 and the structure in Figure 4a, it can be predicted that all ADF-H domains have a similar overall fold. Although, for example, the sequence homology between members of the drebrin/Abp1 and ADF/cofilin classes is low (13-15% identity within and between species), the predicted secondary structure elements identified in the ADF-H domain structural models are well conserved throughout the entire family. Furthermore, predicted loop regions connecting secondary structure elements are less conserved, and insertions are located in the predicted loop regions. Finally, the hydrophobic core elements are well conserved (see below; Figure 4a, residues indicated in yellow).
The sequence alignment also suggests that all ADF-H domains probably
interact with actin through a similar interface. The residues essential
for the interaction of yeast cofilin with actin (Figures 2, asterisks,
and 4b, red) are relatively well conserved in all three classes of
ADF-H domain proteins. More specifically, residues Arg96,
Lys98, Asp123, and Glu126
(numbering based on positions in yeast cofilin), which are essential for actin monomer and actin filament binding in yeast cofilin (Lappalainen et al., 1997), show extremely high conservation
throughout the three protein families. Furthermore, the five N-terminal
residues of yeast cofilin, which have been shown to be essential for
actin monomer and filament binding, are relatively well conserved in the ADF-H domains (Lappalainen et al., 1997). The most
highly conserved residues in this region are Ser4 and
Gly5 (numbering based on positions in yeast cofilin),
suggesting that these two residues might form an important
actin-binding sequence within the N-terminal region of ADF-H domains
(the first five residues of cofilin are not shown in Figure 4, because
they were found to be disordered in the x-ray crystal structure
determination). Interestingly, in vertebrate ADF/cofilin proteins,
interactions with actin can be down-regulated by phosphorylation of the
aforementioned serine (Agnew et al., 1995). The suggestion
that the F-actin interface is conserved, at least between the
ADF/cofilin and drebrin/Abp1 classes, is also supported by biochemical
data that show that both ADF (Bernstein and Bamburg, 1982) and drebrin
(Ishikawa et al., 1994) compete with tropomyosin for actin
filament binding.
In addition to the highly conserved residues that have already been
shown to be important for the interaction between cofilin and actin,
there are also a number of other residues that are well conserved
throughout ADF homology domains. These residues fall approximately into
two different categories. The first category consists of residues
located in the hydrophobic core of cofilin, and these therefore appear
to be important for protein stability or correct folding. These
residues include Tyr64, Phe85,
Trp88, Pro90, and Tyr101 (numbers
based on positions in yeast cofilin; Figure 4a, yellow). A critical
role of maize ADF residues Tyr82 and Tyr117
(corresponding to residues Tyr64 and Tyr101 in
yeast cofilin) in proper protein folding has recently been demonstrated
by site-directed mutagenesis (Jiang et al., 1997). The
second category of highly conserved residues are those that, because
they are exposed on the surface of the protein, may be involved in
protein-protein interactions. All of these residues (Met99, Ala102, Ser103, and
Gly114) except Ser45 are located close to the
actin-binding site as identified by Lappalainen et al.,
(1997), indicating that these residues might take part in interactions
with actin (Figure 4b). Ser45 is located at the opposite
side of the molecule. Because this residue is at the end of the
-strand-3 and because this position is in most cases occupied by
either serine or glycine, it is possible that a residue lacking a bulky
side chain is required at this position for steric reasons.
Gln120, which is conserved in all but one of the
ADF/cofilin proteins and is replaced by asparagine in drebrins and
mSH3P7, but which is not conserved in twinfilins, coactosin, and
depactin, is also located close to the actin-binding site of cofilin.
An interesting and instructive sequence (and, by inference, structural)
variance among the ADF-H domains is revealed by the alignment. There
are two insertions present in the vertebrate ADF/cofilins but not in
any other members of the ADF-H domain family. The first insertion is
located between -helix 1 and -strand-2, and the second insertion
is between -strand-2 and -strand-3 (Figures 2 and 4a, green and
blue loops, respectively). The first insertion forms a short -helix
in human destrin and is always followed by a putative nuclear
localization signal (KKRKK) found only in vertebrate ADF/cofilin
proteins (Figure 2; note that human destrin-2 is a pseudogene and
contains the sequence KKRTK in this region). Nuclear localization of
ADF/cofilin has been demonstrated in mammalian cells placed under
stress (Ohta et al., 1989). Conceivably, these insertions
may play a role in a nuclear function of mammalian cofilins. It is
important, however, to note that an identical KKRKK sequence is also
found in ActA, a protein that plays central role in the actin-based
motility of the intracellular pathogen Listeria
monocytogenes. Mutagenesis studies have shown that this lysine-rich sequence in ActA plays an important role in actin filament
nucleation (Lasa et al., 1997). It is therefore formally possible that this sequence might have a similar role in mammalian cofilins.
A second structural difference within the ADF-H domain family revealed
by our sequence alignment is that -strand-4 and -strand-5 within
the drebrin/Abp1 class are shortened and/or disrupted by prolines. The
cluster of three charged residues preceding Lys81 (based on
position in S. cerevisiae) found in all mammalian and avian
cofilins is replaced by hydrophobic but flexible amino acids in the
drebrin/Abp1 class. Thus, it seems that the rigid handle protruding
from the main body of ADF/cofilin is shortened in the entire
drebrin/Abp1 family and probably has a different tertiary structure,
the functional implications of which need to be explored.
Finally, our sequence alignment shows that the C-terminal regions
following -strand-6 in all twinfilin ADF-H domains are longer and
align poorly with other members of ADF-H domain family (Figure 2). It
is possible that this region imparts a unique function to these
proteins, such as the reported kinase activity (Beeler et
al., 1994). Alternatively, the extension that separates the two
tandem ADF-H domains in twinfilin might serve as a linker, thereby
conferring an appropriate spatial relationship between the two domains.
| |
CONCLUSIONS |
|---|
|
Top
Introduction
Conclusions
References
|
|---|
In recent years, with the explosive increase in accessible sequence data, it has become apparent that within the sequences of many proteins can be found motifs and modules that are shared with a number of otherwise unrelated proteins. The availability of sequence data for 39 ADF-H domain proteins has provided us with an opportunity to examine the sequence similarities and the evolutionary relationships within this important family of actin-binding proteins. Further such analysis for other cytoskeleton proteins will provide a better appreciation for which protein motifs and modules were the fundamental cytoskeletal building blocks, and how cytoskeletal complexity evolved from these.
We have shown that the ADF-H domain family is made up of at least three different classes of proteins: the ADF/cofilins, the drebrin/Abp1s, and the twinfilins. Each class was represented in organisms existing before the divergence of the animal, plant, and fungal kingdoms. Multiple examples within each class subsequently arose from gene duplication events after this split and may have fulfilled the needs particular to multicellular lifestyles. Only one member of each of these three classes is present in the unicellular yeast S. cerevisiae, whereas several different members of drebrin/Abp1 and ADF/cofilin proteins are found in more complex organisms.
The sequence alignment of ADF-H domain proteins presented in Figure 2 indicates that it is likely that all ADF-H domains have a similar three-dimensional fold because the extra insertions found in some of these proteins are found only between major secondary structural elements and not within them. Furthermore, the residues that have been shown to be essential for actin interactions in the ADF/cofilin family are also well conserved in the other classes, leading to the prediction that all ADF-H domain proteins interact with actin. This conserved module, however, has provided a framework for three subclasses of actin-binding proteins with differing biochemical properties. Although ADF/cofilins are capable of binding both monomeric and filamentous actin, the drebrin/Abp1s seem to bind to filamentous actin only, and S. cerevisiae twinfilin appears to bind to actin monomers only. Crystal structures of members of the twinfilin and drebrin/Abp1 classes should enhance our understanding how this specificity is achieved.
The actin interactions of the members of the ADF/cofilin family and their role in the regulation of actin filament turnover are well established. It is now important to further elucidate the properties of the other two classes and to elucidate their in vivo functions.
| |
ACKNOWLEDGMENTS |
|---|
We thank Keith Kozminski for comments on the manuscript. This work was supported by grants from the Human Frontier Science Program (to P.L and M.J.T.V.C), Deutsche Forschungsgemeinschaft (to M.M.K) and the National Institutes of General Medical Sciences (grant GM-42759 to D.G.D).
| |
FOOTNOTES |
|---|
* Corresponding author. E-mail address: drubin{at}uclink4.berkeley.edu.
| |
REFERENCES |
|---|
|
Top
Introduction
Conclusions
References
|
|---|
implications for structure and function.
Structure
15, 969-987.an approach using the bootstrap.
Evolution
39, 783-791.systematic isolation of SH3 domain-containing proteins.
Nat. Biotechnol.
14, 741-744[Medline].improving the sensitivity Of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
Nucleic Acids Res.
22, 4673-46804 mapped by mutational analysis.
EMBO J.
15, 201-210[Medline].This article has been cited by other articles:
|
|
 |
|
  V. O. Paavilainen, M. Hellman, E. Helfer, M. Bovellan, A. Annila, M.-F. Carlier, P. Permi, and P. Lappalainen Structural basis and evolutionary origin of actin filament capping by twinfilin PNAS, February 27, 2007; 104(9): 3113 - 3118. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. B. Moseley, K. Okada, H. I. Balcer, D. R. Kovar, T. D. Pollard, and B. L. Goode Twinfilin is an actin-filament-severing protein and promotes rapid turnover of actin structures in vivo J. Cell Sci., April 15, 2006; 119(8): 1547 - 1557. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D.-H. Jang, J.-H. Han, S.-H. Lee, Y.-S. Lee, H. Park, S.-H. Lee, H. Kim, and B.-K. Kaang Cofilin expression induces cofilin-actin rod formation and disrupts synaptic structure and function in Aplysia synapses PNAS, November 1, 2005; 102(44): 16072 - 16077. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Schuler, A.-K. Mueller, and K. Matuschewski A Plasmodium Actin-depolymerizing Factor That Binds Exclusively to Actin Monomers Mol. Biol. Cell, September 1, 2005; 16(9): 4013 - 4023. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. S. Chew, C. T. Okamoto, X. Chen, and R. Thomas Drebrin E2 is differentially expressed and phosphorylated in parietal cells in the gastric mucosa Am J Physiol Gastrointest Liver Physiol, August 1, 2005; 289(2): G320 - G331. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
O. Quintero-Monzon, A. A. Rodal, B. Strokopytov, S. C. Almo, and B. L. Goode Structural and Functional Dissection of the Abp1 ADFH Actin-binding Domain Reveals Versatile In Vivo Adapter Functions Mol. Biol. Cell, July 1, 2005; 16(7): 3128 - 3139. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Le Bras, I. Foucault, A. Foussat, C. Brignone, O. Acuto, and M. Deckert Recruitment of the Actin-binding Protein HIP-55 to the Immunological Synapse Regulates T Cell Receptor Signaling and Endocytosis J. Biol. Chem., April 9, 2004; 279(15): 15550 - 15560. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. Qualmann, T. M. Boeckers, M. Jeromin, E. D. Gundelfinger, and M. M. Kessels Linkage of the Actin Cytoskeleton to the Postsynaptic Density via Direct Interactions of Abp1 with the ProSAP/Shank Family J. Neurosci., March 10, 2004; 24(10): 2481 - 2495. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. C. Kay-Jackson, L. C. Goatley, L. Cox, J. E. Miskin, R. M. E. Parkhouse, J. Wienands, and L. K. Dixon The CD2v protein of African swine fever virus interacts with the actin-binding adaptor protein SH3P7 J. Gen. Virol., January 1, 2004; 85(1): 119 - 130. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. K. Vartiainen, E. M. Sarkkinen, T. Matilainen, M. Salminen, and P. Lappalainen Mammals Have Two Twinfilin Isoforms Whose Subcellular Localizations and Tissue Distributions Are Differentially Regulated J. Biol. Chem., September 5, 2003; 278(36): 34347 - 34355. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Mulder, M. Poland, M. F. B. G. Gebbink, J. Calafat, W. H. Moolenaar, and O. Kranenburg p116Rip Is A Novel Filamentous Actin-binding Protein J. Biol. Chem., July 11, 2003; 278(29): 27216 - 27223. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. D. Fenster, M. M. Kessels, B. Qualmann, W. J. Chung, J. Nash, E. D. Gundelfinger, and C. C. Garner Interactions between Piccolo and the Actin/Dynamin-binding Protein Abp1 Link Vesicle Endocytosis to Presynaptic Active Zones J. Biol. Chem., May 23, 2003; 278(22): 20268 - 20277. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Kim, E. C. Snesrud, B. Haas, F. Cheung, C. D. Town, and J. Quackenbush Gene Expression Analyses of Arabidopsis Chromosome 2 Using a Genomic DNA Amplicon Microarray Genome Res., March 1, 2003; 13(3): 327 - 340. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. K. Mattila, M. Salminen, T. Yamashiro, and P. Lappalainen Mouse MIM, a Tissue-specific Regulator of Cytoskeletal Dynamics, Interacts with ATP-Actin Monomers through Its C-terminal WH2 Domain J. Biol. Chem., February 28, 2003; 278(10): 8452 - 8459. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. O. Paavilainen, M. C. Merckel, S. Falck, P. J. Ojala, E. Pohl, M. Wilmanns, and P. Lappalainen Structural Conservation between the Actin Monomer-binding Sites of Twinfilin and Actin-depolymerizing Factor (ADF)/Cofilin J. Biol. Chem., November 1, 2002; 277(45): 43089 - 43095. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. J. Ojala, V. O. Paavilainen, M. K. Vartiainen, R. Tuma, A. G. Weeds, and P. Lappalainen The Two ADF-H Domains of Twinfilin Play Functionally Distinct Roles in Interactions with Actin Monomers Mol. Biol. Cell, November 1, 2002; 13(11): 3811 - 3821. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Fazi, M. J. T. V. Cope, A. Douangamath, S. Ferracuti, K. Schirwitz, A. Zucconi, D. G. Drubin, M. Wilmanns, G. Cesareni, and L. Castagnoli Unusual Binding Properties of the SH3 Domain of the Yeast Actin-binding Protein Abp1. STRUCTURAL AND FUNCTIONAL ANALYSIS J. Biol. Chem., February 8, 2002; 277(7): 5290 - 5298. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Palmgren, M. Vartiainen, and P. Lappalainen Twinfilin, a molecular mailman for actin monomers J. Cell Sci., January 3, 2002; 115(5): 881 - 886. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. L. Goode, A. A. Rodal, G. Barnes, and D. G. Drubin Activation of the Arp2/3 Complex by the Actin Filament Binding Protein Abp1p J. Cell Biol., April 30, 2001; 153(3): 627 - 634. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. M. Kessels, A. E.Y. Engqvist-Goldstein, D. G. Drubin, and B. Qualmann Mammalian Abp1, a Signal-responsive F-Actin-binding Protein, Links the Actin Cytoskeleton to Endocytosis Via the GTPase Dynamin J. Cell Biol., April 16, 2001; 153(2): 351 - 366. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. Ouellet, E. Carpentier, M. J. T.V. Cope, A. F. Monroy, and F. Sarhan Regulation of a Wheat Actin-Depolymerizing Factor during Cold Acclimation Plant Physiology, January 1, 2001; 125(1): 360 - 368. [Abstract] [Full Text]
|
|
|
|
 |
|
 M. Vartiainen, P. J. Ojala, P. Auvinen, J. Peränen, and P. Lappalainen Mouse A6/Twinfilin Is an Actin Monomer-Binding Protein That Localizes to the Regions of Rapid Actin Dynamics Mol. Cell. Biol., March 1, 2000; 20(5): 1772 - 1783. [Abstract] [Full Text]
|
|
|
|
|
|
B. Keon, P. Jedrzejewski, D. Paul, and D. Goodenough Isoform specific expression of the neuronal F-actin binding protein, drebrin, in specialized cells of stomach and kidney epithelia J. Cell Sci., January 1, 2000; 113(2): 325 - 336. [Abstract] [PDF]
|
|
|
|
|
|
M. M. Kessels, A. E. Y. Engqvist-Goldstein, and D. G. Drubin Association of Mouse Actin-binding Protein 1 (mAbp1/SH3P7), an Src Kinase Target, with Dynamic Regions of the Cortical Actin Cytoskeleton in Response to Rac1 Activation Mol. Biol. Cell, January 1, 2000; 11(1): 393 - 412. [Abstract] [Full Text]
|
|
|
|
