Fibre-type specific concentration of focal adhesion kinase at the sarcolemma: influence of fibre innervation and regeneration
1 M. E. Müller-Institute for Biomechanics, University of Bern,
Bühlestrasse 26, 3000 Bern 9, Switzerland
2 Institute of Anatomy, University of Bern, Bühlestrasse 26, 3000 Bern
9, Switzerland
3 Department of Clinical Research, University of Bern, Bühlestrasse 26,
3000 Bern 9, Switzerland
4 School of Biomedical Sciences, University of Leeds, Leeds LS2 9NQ,
UK
5 Institute of Anatomy, University of Zürich-Irchel and Department of
Applied Biosciences ETH, Zürich, Switzerland
* Author for correspondence at address 2 (e-mail: flueck{at}ana.unibe.ch )
Accepted 13 May 2002
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Summary |
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Key words: focal adhesion complex, costamere, skeletal muscle, focal adhesion kinase, nerve, regeneration, myosin
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Introduction |
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There is sparse evidence indicating the fibre-type specificity of costamere
components in, for example, the chicken
(Bozyczko et al., 1989;
Shear and Bloch, 1985
).
However, the extent to which sarcolemmal components contribute to
fibre-type-specific properties is poorly understood
(Shear and Bloch, 1985
).
Recently, the integrin-associated tyrosine kinase focal adhesion kinase
(FAK) was found in an irregular pattern in association with the sarcolemma of
chicken slow tonic muscle fibres
(Flück et al., 1999); it
was concentrated in slow-twitch soleus (SOL) rather than fast-twitch rat
muscles (plantaris and gastrocnemius)
(Gordon et al., 2001
).
Intriguingly, FAK was also demonstrated to be associated with the
dystrophin/glycoprotein complex (Cavaldesi
et al., 1999
) and to localize to the sarcomeric Z-line of cardiac
myocytes (Kovacic-Milivojevic et al.,
2001
). In cultured mesodermal cells, FAK is known to play a
central role in the formation and turnover of focal adhesion complexes (FACs)
(Cary and Guan, 1999
;
Ilic et al., 1995
;
Schlaepfer and Hunter, 1998
),
which link, in a manner analogous to costameres, the outside of a cell to the
extracellular matrix and interact with cytoskeletal elements in its interior
(Fig. 1) (Burridge and Chrzanowska-Wodnicka,
1996
). Interaction between integrins and the ECM induces rapid
phosphorylation of the integrin-associated FAK on distinct tyrosine residues
(Cary and Guan, 1999
). Such
modifications create docking sites for the subsequent recruitment of
cytoskeletal and signalling molecules to FACs
(Fig. 1)
(Giancotti, 1997
;
Miyamoto et al., 1995
). It has
also been suggested that FAK controls the cell cycle of myoblasts in culture
and is involved in the attachment of muscle fibres to laminin
(Disatnik and Rando, 1999
;
Oktay et al., 1999
;
Sastry et al., 1999
).
Furthermore, FAK protein and FAK kinase activity are induced during the
formation of muscle fibres in culture and during muscle hypertrophy, as well
as in myopathy (Flück et al.,
1999
; Saher and Hildt,
1999
). Thus, FAK plays a critical role in the formation of muscle
fibres and could conceivably contribute to the mechanisms that control the
fibre-type-specific distribution of sarcolemmal FACs.
Changes in the muscle fibre recruitment pattern, as a consequence of
changed innervation, cause transformations of fibre types
(Buller et al., 1960;
Jolesz and Sreter, 1981
;
Pette and Staron, 1997
; for
further references, see Lu et al.,
1999
). In addition to fibre-type transformation, fibres in
transplanted muscle undergo, after an initial degeneration, a regeneration
process on the scaffold of the basal lamina
(Marshall et al., 1977
) that
is sometimes accompanied by the deposition of a new basement membrane
(Gulati et al., 1983
). We have
explored the hypothesis that the expression of FAK protein and its association
with the sarcolemma in rat skeletal muscle corresponds with fibre types and is
affected by the remodelling of the basement membrane during fibre
regeneration.
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Materials and methods |
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Animals and muscles
The muscle samples originated from a previous experiment, described in
detail by Lu et al. (1999),
and had been stored for approximately 5 years at -70°C. All surgical
procedures were performed on male rats (strain Zur:SIV; Institute of
Laboratory Animal Science, University of Zürich, Switzerland) at the
Institute of Anatomy, University of Zürich-Irchel, with the permission of
the State Animal Protection Commission. Animals were anaesthetised by
injection with 0.25 ml kg-1 body mass Innovar-Vet (Pitman-Moore
GMBH, Germany) intramuscularly combined with 2.5 mg of Valium (Roche, Reinach,
Switzerland) and 7.5 mg of Nembutal (Abbott, Baar, Switzerland)
intraperitoneally (for details, see Lu et
al., 1999
). The following muscles were analysed in the present
investigation: (i) soleus (SOL) muscles, which were cross-reinnervated by the
extensor digitorum longus (EDL) nerve, termed X-SOL, (ii) SOL muscle grafted
into the site of the EDL muscles with foreign reinnervation by the EDL nerve,
termed T-SOL, (iii) EDL muscles transplanted into the site of the SOL muscles
with foreign reinnervation by the SOL nerve, termed T-EDL, and (iv) normal SOL
and EDL muscles, termed N-SOL and N-EDL, respectively. For each treatment,
muscles from at least five animals were analysed. X-SOL, T-SOL and T-EDL
muscles were analysed only after the muscle fibre transformation process was
considered to be complete, i.e. at least 6 months after innervation by the
foreign nerve.
Protein extraction and immunoprecipitation
The preparation and denaturing of deoxycholate extracts in SDSPAGE
loading buffer was as described in Flück et al.
(2000).
For immunoprecipitation, proteins were extracted from cryosections of the
belly portion of the muscle with 500 µl of cold immunoprecipitation buffer
(10 mmol l-1 Tris-HCl, pH 7.4, 1 % Triton X-100, 150 mmol
l-1 NaCl, 1 mmol l-1 EDTA, 1 mmol l-1 EGTA,
1.5 mmol l-1 MgCl2, 1 mmol l-1 Na3
VO4, 0.2 mmol l-1 phenylmethylsulphonyl fluoride, 2.5
µg ml-1 aprotinin, 2.5 µg ml-1 leupeptin), and the
soluble fraction resulting after centrifugation (3 min, 10 000
g at 8 °C; termed the Triton X-100 extract) was divided
into three parts. Each part was incubated with a different rabbit serum (2 h,
8 °C), followed by reaction for 1 h at 4 °C with 100 µl of a 10 %
slurry of Protein A crosslinked to agarose (Sigma Chemical, Buchs,
Switzerland). The isolation, washing and denaturing of the precipitated
antigen/antibody complexes in SDSPAGE loading buffer were carried out
as described previously (Flück et
al., 1999).
SDSPAGE and immunoblotting
Denatured SDSPAGE loading buffer samples of deoxycholate extracts
(20 µg) or immunoprecipitates were separated on 7.5 % and 5 %
SDSPAGE gels, respectively, and processed for immunoblotting
essentially as described previously
(Flück et al., 2000).
Blots were stained with Ponceau S (Serva Electrophoresis GMBH, Heidelberg,
Germany) to verify equal loading and transfer and were subsequently incubated
with primary antibodies and secondary peroxidase-conjugated goat anti-rabbit
IgG at a dilution of 1:1000 and 1:5000, respectively, in TTBS (20
mmoll-1 Tris base, pH7.5, 150 mmoll-1 NaCl, 0.05 %
Tween-20) containing 2.5 % non-fat dry milk and 1 % bovine serum albumin
(BSA). After washing, bound secondary antibody was detected by enhanced
chemoluminescence (ECL; SuperSignal®West Pico from Pierce, Socochim SA,
Switzerland) and recorded on X-ray film. The detection of
tyrosine-phosphorylated proteins with antibody RC20:HRPO was carried out in a
similar manner, but the addition of milk powder to the solution was omitted
and the ECL reaction was carried out directly.
Immunocytochemistry
Cryosections (12 µm thick) were prepared from the belly portion of the
muscle, mounted on glass slides (SuperFrost®Plus; Menzel-Gläser,
Germany), air-dried and stored (for 0.5-5 days) at -20 °C. Detection of
FAK with different antibodies was carried out using different protocols.
Visualization of FAK immunoreactivity with antiserum A-17 was carried out
using a two-step detection protocol as described by Flück et al.
(2000) but with the following
modifications. Thawed sections were fixed in cold acetone and wetted in
phosphate-buffered saline (PBS); tissue peroxidase activity was then quenched
(10 min, 3 % H2O2 in methanol), and sections were washed
in PBS and blocked with 3 % BSA in PBS for 0.5 h. Subsequently the sections
were incubated for 1 h at room temperature (20 °C) with antibody A-17
(diluted 1:100 in 0.3 % BSA/PBS) and, following brief washing in PBS, reacted
for 30 min with peroxidase-conjugated goat anti-rabbit IgG (diluted 1:2000 in
0.3 % BSA/PBS) and again washed with PBS. Immunoreactivity was detected with
3-amino-9-ethylcarbazole substrate (Sigma Chemicals, Buchs, Switzerland); the
nuclei were counterstained with haematoxylin, and the sections were embedded
in Aquamount (BDH Laboratory Supplies Poole, UK). The stain was visualised on
film (Ektachrome 64T, Kodak) using a microscope/photograph system (Vanox-S,
Olympus). The slides were scanned using a Nikon SF-200 slide scanner operated
by a Power Macintosh G3 using the Nikon Scan 2.0 interface and imported in
JPEG format into Adobe Photoshop version 5.0.
Detection of FAK with monoclonal antibody 2A7 and slow and fast myosin isoforms with specific antibodies were performed as follows. Sections were quenched and blocked as described above, incubated with a 1:100 dilution of the respective specific antibodies followed by goat anti-mouse whole IgG (dilution 1:500) and then with mouse anti-peroxidase complex (dilution 1:5000) with intermittent washing steps in PBS. Immunoreactivity and nuclei were visualised as described above. For each of the individual protocols, a control reaction was carried out with normal rabbit serum.
Fibre analysis
Histochemical analysis of myofibrillar ATPase activity was carried out on
consecutive cryosections to those analysed immunocytochemically for expression
of type I or type II myosin isoforms and for FAK immunoreactivity
(Lu et al., 1999). Micrographs
were taken from corresponding fields of the stained sections, and the fibre
types were classified. Type I and II fibres were differentiated on the basis
of the presence of immunoreactivity for either type I or type II myosin
isoforms. Intermediate (hybrid) type I/II (type IIC) fibres were identified by
the simultaneous presence of type I and II myosin. Type II fibres were further
differentiated into type IIA and IIB fibres by the more robust alkali-stable
myofibrillar ATPase activity of type IIA fibres. The presence of alkali-stable
ATPase was demonstrated by pre-incubation of sections at pH 10.4 and 10.5
combined with incubation at pH 9.5 or 9.6
(Baker et al., 1994
),
respectively. Using these criteria, type IIX fibres could not be
differentiated and were, if present, ranked with IIB fibres.
For each fibre type, the total number of fibres and the number of
sarcolemmal FAK-positive fibres per field were counted. Fibres were
arbitrarily assigned as FAK-positive when at least two boundaries of the
sarcolemma showed distinct positive (orange-red) FAK immunoreactivity. An
average of 150 fibres was counted per section. Data from different fields were
pooled, and the mean percentage and standard error of sarcolemmal FAK-positive
fibres per fibre type were calculated. Differences in percentage of
sarcolemmal FAK-positive fibres among fibre types and muscles were verified
using a bilateral two-by-two 2-test for statistical
significance (Microsoft Excel 97).
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Results |
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FAK localises to the sarcolemma of slow-twitch fibres
Having established that the antisera recognise the FAK isoform of rat
skeletal muscle, we performed experiments to localise the FAK protein in rat
skeletal muscle. Immunohistochemical experiments using antiserum A-17 (N
terminus) indicated that FAK immunoreactivity in slow-twitch N-SOL muscle was
associated with the sarcolemma of most fibres
(Fig. 4). Normal SOL muscle
contains 97% of slow-twitch (type I) and 3% of fast-twitch type IIA fibres.
Using histochemical criteria, i.e. the expression of the slow myosin isoform
and ATPase activity, type I fibres of N-SOL muscle were identified and
compared with the distribution of FAK-immunoreactive staining. Of type I
fibres, 89% were FAK-positive at the sarcolemma, as were 74% of type IIA
fibres (see Fig. 9A).
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|
FAK localisation to the sarcolemma in fast-twitch fibres
We characterised the expression of FAK in normal rat EDL muscle (N-EDL),
which contains up to 98% of fast-twitch fibres
(Lu et al., 1999). Using
antiserum A-17 (N terminus), FAK immunoreactivity was detected at the
sarcolemma in only approximately half the muscle fibres
(Fig. 5A).
|
To verify the absence of sarcolemmal FAK immunoreactivity in certain fibres
of fast-twitch N-EDL muscle, we used a C-terminal FAK-reactive monoclonal
antibody, 2A7. This antibody has been used previously to detect FAK in
skeletal muscle of non-mammalian species
(Baker et al., 1994;
Flück et al., 1999
;
Kanner et al., 1990
); it
detects FAK protein in extracts of rat skeletal muscle
(Fig. 2). Staining revealed
expression of FAK along the sarcolemma of the same fibres that reacted with
antibody A-17 (Fig. 5B). In
addition, punctate staining outside the muscle fibres, which presumably
reflects capillaries, was detected with antibody 2A7
(Polte et al., 1994
).
The fibres that exhibited sarcolemmal FAK immunoreactivity were fast-twitch
type IIA fibres, as detected by myosin isoform staining and myofibrillar
ATPase staining (Fig. 6). These
fibres comprise up to 43% of all N-EDL fibres. The rest of the fibres of N-EDL
muscle are made up mostly (55%) of fast-twitch type IIB with approximately 2%
of type I fibres (Lu et al.,
1999). Quantitative assessment revealed that approximately 90% of
type IIA and 10% of type IIB fibres showed sarcolemmal FAK-immunoreactive
staining (see Fig. 9B).
|
Sarcolemmal localisation of FAK in transformed muscle fibres
In cross-reinnervated soleus (X-SOL), the proportion of type I fibres was
reduced to 15-25% (N-SOL, 93-97%), whereas the proportion of type IIA fibres
was increased to 72-85% (N-SOL 3-6%) (Lu
et al., 1999). After cross-reinnervation, FAK expression at the
sarcolemma was reduced to 61% in the remaining type I fibres and was 28% in
newly transformed type IIA fibres (Fig.
7; see Fig.
9A).
|
Sarcolemmal localisation of FAK in regenerated and transformed muscle
fibres
The slow-to-fast fibre-type transformation in SOL muscle that had been
transplanted into the EDL bed (T-SOL) was more pronounced than in X-SOL muscle
cross-reinnervated with the fast EDL nerve
(Lu et al., 1999). After
several months of recovery, the proportion of type I fibres decreased from
more than 90% to approximately 11%, while the proportion of type IIA fibres
increased from less than 10% to approximately 89%. Sarcolemmal FAK expression
was observed in 90% of remaining type I fibres and in 84% of (new) type IIA
fibres (see Fig. 9). Thus,
compared with X-SOL muscle, the levels of sarcolemmal FAK immunoreactivity in
type I and IIA fibres were significantly increased in fibres of the
transplanted and regenerated T-SOL muscle.
In T-EDL that had regenerated after transplantation into the SOL bed, the proportion of type I and type I/II fibres increased to 93-97 % (N-EDL 2.0-3.5 %), while the proportion of type IIA fibres decreased to 3-7 % (N-EDL 34-50 %); less than 1 % of type IIB fibres persisted (N-EDL 47-55 %). In transplanted T-EDL muscles, FAK expression at the sarcolemma appeared in newly formed intermediate (hybrid) type I/II and type I fibres and was strongly associated with the expression of slow-type myosin (Fig. 8). Of the intermediate (hybrid) type I/II fibres, 88 % showed FAK immunoreactivity; 83 % of type I fibres showed FAK immunoreactivity. A lower percentage (9 %) of FAK immunoreactivity was seen in the remaining type IIA fibres (Fig. 9). The percentage of sarcolemmal FAK immunoreactivity in persisting, normally sized type IIB fibres was low (approximately 11 %), but was increased in small type IIB fibres (to more than 90 %).
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Discussion |
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Immunocytochemical analysis with antibodies against the N and C termini of FAK demonstrated significant FAK immunoreactivity in muscle fibres exclusively in the vicinity of the sarcolemma, suggesting that, in muscle fibres, FAK protein is primarily concentrated at the fibre's periphery.
The muscle fibre types of N-SOL and N-EDL muscles could be divided into two
populations according to sarcolemmal FAK immunoreactivity. A high percentage
of type I and IIA muscle fibres in N-SOL muscle and type IIA fibres in N-EDL
muscle (74 %) showed sarcolemmal localisation of FAK. In contrast, only a
small proportion (<15 %) of the type IIB and type I muscle fibres of N-EDL
muscle revealed sarcolemmal FAK expression. The punctate sarcolemmal FAK
staining in longitudinal sections of type I fibres of N-SOL
(Fig. 4) indicates that a
sampling error may explain the lack of FAK immunoreactivity in a proportion of
type I and IIA muscle fibres of N-SOL muscle and type IIA fibres of N-EDL.
The levels of FAK protein at the sarcolemma in individual muscle fibre
types of rat N-SOL and N-EDL muscle are in good agreement with the firing
pattern of the innervating motoneurones during normal motor behaviour of adult
rats (Hennig and Lomo, 1985).
Recruitment of type I motor units in SOL muscle during free movement and
during quiet standing (Armstrong and
Laughlin, 1985
) is frequent, and these units are active 22-35 % of
the total time (Hennig and Lomo,
1985
). During free movement, the recruitment of type IIA motor
units in EDL muscle was also recorded for a significant fraction of the total
time (1.6-5 %), while type IIB units were recruited much less frequently, i.e.
0.04-0.22 % of the total time. To our knowledge, no data have been published
on the recruitment pattern of the low-abundance type I fibres of EDL muscle
during normal cage activity of laboratory rats. Since, during daily life in
cages, control laboratory rats do not perform any type of endurance exercise
activity, we speculate that the type I fibres of the EDL, in contrast to their
complete recruitment during the `unusual' locomotory activity of swimming
(Yoshimura et al., 1992
), are
only rarely recruited. It is possible that the recruitment pattern and firing
rate of the motoneurons are the main determinants of the localisation of FAK
protein at the sarcolemma.
To test this hypothesis, soleus muscles were cross-reinnervated with the
nerve of the fast-twitch EDL muscle. The sarcolemmal concentration of FAK in
such X-SOL muscles was significantly reduced in type I and IIA fibres
(Fig. 9A). These reciprocal
changes in sarcolemmal FAK expression after foreign reinnervation of
slow-twitch SOL with a nerve supply of higher firing frequency are in good
agreement with the presumed decreased recruitment of muscle fibres in X-SOL
(Hennig and Lomo, 1985).
Similarly, the percentage of sarcolemmal FAK immunoreactivity decreased in IIA
fibres and remained low in normal-sized IIB fibres of transplanted T-EDL
muscle that had undergone a fast-to-slow fibre transformation as a result of
foreign reinnervation with the slow SOL nerve. The remaining type IIB and the
IIA fibre types in T-EDL are expected to show a reduced recruitment to
compensate for the preferential activation of the newly formed type I fibres.
Correspondingly, sarcolemmal FAK immunoreactivity occurred in a high
proportion of newly formed intermediate (hybrid) type I/II (88 %) and type I
(83 %) fibres in T-EDL, supporting our hypothesis that the firing rate of the
innervating nerve, by determining the recruitment pattern, controls FAK
localisation at the sarcolemma.
Conversely, FAK immunoreactivity increased in small type IIB fibres of
T-EDL, which represent newly regenerated myotubes
(Gulati et al., 1983).
Similarly, transplanted T-SOL muscle undergoing a slow-to-fast fibre
transformation maintained its percentage of fibres with sarcolemmal FAK
immunoreactivity in type I and type IIA fibres
(Fig. 9). This increase in the
percentage of sarcolemmal FAK-positive fibres may be related to changes in the
basement membrane zone. Transplantation of rat EDL muscle results initially in
fibre degeneration and the disappearance of basement membrane components, i.e.
type IV and V collagen and laminin. Over time, a new basement membrane appears
and persists in the regenerated fibres
(Bassaglia and Gautron, 1995
;
Gulati et al., 1983
). Several
laminin chains are re-expressed during regeneration of muscle fibres and
probably contribute to induced reconstruction of the basal lamina
(Patton et al., 1999
). The
presence of laminin isoforms, through binding to their integrin receptors, has
been shown to trigger the formation of focal adhesion structures in cultured
cells (Sondermann et al.,
1999
). Such basal lamina remodelling may cause occupancy of
integrins with new ECM ligands and induce the formation of FACs involving
upregulation of sarcolemmal FAK expression. In the first 2 weeks after injury
to rat gastrocnemius and soleus muscle, the FAC component vinculin, together
with the extracellular matrix proteins type IV collagen, fibronectin and
laminin, accumulate in regenerating (small) fibres in regions corresponding to
the costamere (Kaariainen et al.,
2000
; Kami et al.,
1993
). This suggests that some fibres showing a high(er)
percentage of sarcolemmal FAK immunoreactivity in transplanted compared with
normal muscles, i.e. small type IIB fibres in T-EDL and type I and IIA fibres
in T-SOL, reflect regenerating fibres that show an increased turnover or
density of FACs as a result of changes in basal lamina composition.
Alternatively, the reduced sarcolemmal FAK immunoreactivity in type IIA fibres
of T-EDL could reflect fibres with reduced costamere density, similar to the
situation observed in injured rat muscle after regeneration
(Kaariainen et al., 2000
).
The association of FAK with integrin-based focal adhesions of cultured
cells is through paxillin-mediated interaction between the C-terminal (focal
adhesion targeting) domain of FAK. It is negatively regulated by the level of
specific C-terminal products of the FAK gene, which are derived from
alternative transcriptional initiation or postranslational processing
(Cary and Guan, 1999).
Immunoblotting experiments did not indicate enhanced expression of proteins
related to the FAK C terminus in N-EDL versus N-SOL muscle
(Fig. 3). In contrast,
immunoblotting analyses indicated that the level of full-length 125 kDa FAK
protein was elevated in slow-twitch N-SOL relative to fast-twitch N-EDL muscle
(Fig. 3). These latter
differences are in agreement with the different percentages of sarcolemmal
FAK-positive fibres in normal muscles. For example, only 45 % of fibres in
N-EDL muscle (the product of the percentage of sarcolemmal FAK-positive fibres
in a fibre type and the abundance of fibre type relative to total fibres)
versus 89 % of total fibres in N-SOL muscle were sarcolemmal
FAK-positive. These data suggest that an increased level of FAK protein,
rather than modification of FAK localisation by FAK C-terminal products,
causes the high level of sarcolemmal expression of FAK in rat fibre types.
A major biological function of FAK is the control of FAC turnover, and
localisation of FAK is in many cell types restricted to FACs
(Cary and Guan, 1999;
Ilic et al., 1995
;
Schlaepfer and Hunter, 1998
).
Thus, the sarcolemmal concentration of FAK in rat muscles probably reflects
the concentration of FAK to sarcolemmal focal adhesions
(Pardo et al., 1983
). It has
been proposed that the costameres transmit physical forces laterally to the
connective tissue and to adjacent muscle fibres
(Huijing, 1999
;
Monti et al., 1999
;
Patel and Lieber, 1997
). Fast-
and slow-twitch skeletal muscle fibres contract at different velocities
(Burke et al., 1971
;
Close, 1965
). It is therefore
conceivable that focal adhesions of the sarcolemma of fast- and slow-twitch
fibres are subjected to different profiles of mechanical forces. Intriguingly,
mechanical forces induce FAK phosphorylation in many cells, and physical load
has recently been shown to induce phosphorylation and expression of FAK in
skeletal muscle (Flück et al.,
1999
; Gordon et al.,
2001
; Li et al.,
1997
; Tang et al.,
1999
). We speculate that the higher sarcolemmal FAK
immunoreactivity in frequently recruited fibres of normal rat muscle reflects
an adaptive increase in costamer density or turnover needed to stabilise the
fibres against the higher overall mechanical load. However, increased
sarcolemmal FAK immunoreactivity in transplanted rat muscles may reflect
increased turnover and the formation of new costameres during remodelling of
the basement membrane in regenerating fibres
(Fig. 10). This is consistent
with the hypothesis that FAK is involved in the fibre-type-specific assembly
of sarcolemmal integrin receptor complexes and in their eventual modulation
through fibre regeneration and fibre recruitment pattern.
|
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Acknowledgments |
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