1 INSERM U.384, Faculté de Médecine, 28 Place Henri Dunant, 63001
Clermont Ferrand, France
2 Department of General Zoology, Wroclaw University, 21 Sienkiewicza Street,
50-335 Wroclaw, Poland
* Author for correspondence (e-mail: christophe.jagla{at}u-clermont1.fr)
Accepted 12 October 2004
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SUMMARY |
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Key words: Leg myogenesis, Tendons, Founder cells, Drosophila
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Introduction |
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Like those in the larva, adult muscles also derive from
twi-expressing cells. The adult abdominal body wall musculature
originates from a subset of twi-positive cells associated with larval
nerves (Currie and Bate, 1991;
Dutta et al., 2004
), whereas
the flight and leg muscles develop from a subpopulation of
twi-expressing cells, the so-called adepithelial cells, of wing and
leg imaginal discs (Bate et al.,
1991
; Broadie and Bate,
1991
).
Two principal types of flight muscles have been described: the direct
flight muscles (DFMs) and the indirect flight muscles (IFMs)
(Fernandes et al., 1991;
Miller, 1950
). The DFMs are
the small tubular muscles that arise from the most distal,
cut-expressing adepithelial cells of the notum part of wing disc
(Sudarsan et al., 2001
). As
some of these cells express the founder cell marker duf and the
muscle identity gene apterous (ap), it has been proposed
that DFMs form de novo using a myogenic pathway similar to that described for
larval muscles (Ghazi et al.,
2000
; Kozopas and Nusse,
2002
). Formation of IFMs consisting of three dorsoventral muscles
(DVMs) and 6 dorsal longitudinal muscles (DLMs) involves the proximal
myoblasts of the imaginal notum, which express a low level of cut and
a high level of vestigial (vg)
(Sudarsan et al., 2001
), and
is based on two different developmental strategies. DLMs use persistent larval
muscles as a scaffold to form (Fernandes
et al., 1991
; Fernandes and
Keshishian, 1996
), whereas the DVMs form de novo.
In contrast to larval and flight muscles, practically nothing is known
about the mechanism governing Drosophila leg myogenesis.
Surprisingly, no systematic analysis of the development and morphology of
appendicular Drosophila muscles has been performed since Miller's
work, published more than 50 years ago
(Miller, 1950). Here, we
exploited a set of GFP-expressing Drosophila lines to follow the
formation of appendicular muscles and tendons during larval and pupal stages.
Intriguingly, the presumptive leg muscle founders segregate close to tendon
precursors, and then keep contact with the invaginating internal tendons to
reach the position at which the corresponding muscle fibres will develop. The
confocal microscopy-based analysis reveals the multifibre, vertebrate-like
organisation of Drosophila leg muscles, making appendicular
Drosophila musculature an attractive model with which to study the
genetic control of multifibre muscle formation.
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Materials and methods |
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To visualise muscles and tendons simultaneously, the MHC-tauGFP strain was combined with the 1151-Gal4 driver and the resulting flies crossed with the UAS-dsRED line, generously provided by S. Heuser (Meunster, Germany).
Dissections and mounting
All larvae and pupae were grown and staged at 25°C. Larvae and prepupae
(up to 5 hours after pupae formation, APF) were dissected in
phosphate-buffered saline (PBS), fixed for 15 minutes in 4% paraformaldehyde
in PBS and stained with appropriate antibodies. Pupae older than 5 hours APF
and adult flies were fixed in 4% paraformaldehyde for about 5 hours, dissected
and fixed again overnight before final dissection of the developing legs.
Muscle fibres from the adult legs were dissected directly in 4%
paraformaldehyde, maintained for 15 minutes in the initial fixation solution
and stained to visualise myoblast nuclei. All the preparations were mounted in
50% glycerol.
Immunostaining and 3D modelling
The following primary antibodies were used: rabbit anti-Twi, dilution
1/2500 (from F. Perrin-Schmit, Strasbourg, France); rabbit anti-Stripe,
dilution 1/200 (from T. Volk, Reohovot, Israel); rabbit anti-Histone H3
Phosporylated (H3P), dilution 1/200 (Upstate); monoclonal anti-Wingless (Wg)
(DHSB); monoclonal anti-Dl, dilution1/100 (DHSB); monoclonal anti-LacZ,
dilution 1/500 (DHSB). Anti-rabbit and anti-mouse secondary antibodies
(Jackson) conjugated to CY3 or CY5 fluorochromes were used (dilution 1/300) to
reveal the staining. Nuclei of dissected muscle fibres were stained using
propidium iodide (Molecular Probes). All the preparations were analysed on an
Olympus Fluoview FV300 confocal microscope. 3D modelling was performed using
the ImarisTM Bitplane software.
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Results |
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Major events of appendicular myogenesis during pupal metamorphosis
Starting from mid-pupation secretion of the cuticle makes pupal legs
inaccessible for antibody staining and thus refractory to the analysis of
muscle and tendon development by immunostaining-based methods. To overcome
this technical problem, we took advantage of two GFP-expressing
Drosophila lines (1151-GFP and Stripe-GFP) that enabled us to
visualise appendicular muscles and tendons during metamorphosis
(Fig. 4). Importantly, this
analysis confirms the presence of internal tendons in all leg segments
(Fig. 4, see also Fig. S1 in
supplementary material). At 8 hours APF, string-like tendon precursors are
detected in the Stripe-GFP and the 1151-GFP-expressing leg discs
(Fig. 4A,B). Analysis of the
proximodistal and dorsoventral positions of the detected tendons (Figs
3,
4) shows from which previously
described sr-expressing domain
(Fig. 2) they arise (to better
understand the morphological changes that occur during leg disc eversion refer
to the scheme presented in Fig. S1 in supplementary material). In the femur,
the a and b domains give rise to the dorsal and ventral tendons, respectively
(compare Fig. 2H with Fig. S1
and Fig. 4A). Similarly, the
dorsal and the ventral tibia tendons arise from the c and g domains,
respectively. In addition to these tendons, the long tendon originating from
the d domain can be detected in the tarsus, tibia and femur
(Fig. 4A-D and Fig. S1 in
supplementary material). Thus, unlike the embryonic muscle attachment sites
(Volk, 1999), the
sr-expressing progenitors of appendicular tendons give rise to
internal string-like tendons. As revealed by the analysis of everting leg
discs (data not shown), sr expression diminishes and is no longer
detected in the long tendon starting from 25 hours APF. By contrast, all the
internal tendons, including the long tendon, are detected in the 1151-GFP
pupae (Fig. 4D and data not
shown).
Importantly, the 1151-GFP line also allows the monitoring of the position of myoblasts with respect to the developing internal tendons. At 8 hours APF, most myoblasts are dispersed within the everting leg segments, and only some of them (most likely those corresponding to the founder cells) are closely associated with extending tendons (Fig. 4A). The myoblast distribution changes during the next few hours so that, at 20 hours APF (Fig. 4C), nearly all the 1151-GFP-positive myoblasts are aligned around the internal tendons. We estimate that the non-associated myoblasts seen within the tibia and femur represent no more than 5% of the total number of 1151-GFP-positive adepithelial cells. At the beginning of pupation, some dispersed 1151-positive cells are also present in the tarsus (Fig. 4A). They most probably correspond to myoblasts that have stopped expressing Twi (Figs 2, 3).
At the time the tarsal 1151-GFP-expressing cells disappear (at about 20 hours APF), 1151-GFP-expressing cells in other leg segments start to form prefusion complexes (Fig. 4C,F). Thus at 25 hours APF, we can discern the first precursors of syncytial muscle fibres, composed of 5 to 10 myoblast nuclei (Fig. 4D,G), which indicates that fusion processes are initiated between 20 and 25 hours APF. Newly formed muscle fibres are tightly arranged around the internal tendons and are not yet attached to the epithelium (Fig. 4G). Interestingly, at the same time we observe that the number of dispersed 1151-GFP-positive cells increases (Fig. 4D), suggesting that they have proliferated to generate a new pool of myoblasts. In the next 10 hours, these myoblasts most probably ensure the second wave of fusion, giving rise to the multinucleated muscle fibres (Fig. 4E,H). The newly formed myotubes appear to be associated on their distal sides with the internal tendons. The establishment of the contact between the proximal extremity of a myotube and the corresponding apodeme takes place between 40 and 55 hours APF (Fig. 4G,I,J). As in embryos, precursors of apodemes in the leg epithelium express sr (Fig. 4I,J), suggesting that a similar genetic pathway controls the differentiation of larval and adult muscle attachment sites. In parallel to the establishment of epithelial insertion, appendicular myotubes enter the phase of terminal myogenic differentiation marked by the expression of myofibrillar proteins, here evidenced by the progressively stronger fluorescence of muscle fibres from MHC-tauGFP pupae (Fig. 4G,H).
Muscles and tendons of the adult leg
To identify individual muscles and tendons and assign their position, we
analysed a double-fluorescent Drosophila line that expresses
1151-driven DsRED in the tendons and MHC-tauGFP in the muscles. Our
observations indicate that a robust muscle morphogenesis takes place between
40 and 50 hours APF (Fig. 4 and
data not shown), establishing a final pattern of muscles and tendons as early
as 55 hours APF. As the tendon-specific 1151-DsRED expression is stronger in
the pupae than in the adult, we decided to use 55-hour APF pupae to revisit
the appendicular musculature. The general muscle organisation is independent
of sex and leg pair (data not shown). except for the jump muscle, which is
specific to the second leg pair (Miller,
1950).
Two major multifibre muscle types are present in the tibia, femur and coxa
(Fig. 5A,B,H,I and Fig. S2A-C
in supplementary material). These are the levator and the depressor muscles.
The levator muscles, designated talm (tarsus levator muscle), tilm (tibia
levator muscle) and trlm (trochanter levator muscle) (Figs
5,
6 and Fig. S2 in supplementary
material), are located dorsally. They are organised around the levator
tendons, designated talt, tilt and trlt, respectively (Figs
5,
6 and Fig. S2 in supplementary
material). The ventral sides of the tibia, femur and coxa harbour the
depressor muscles, tadm, tidm and trdm, organised around the corresponding
tadt, tidt and trdt depressor tendons (see
Table 1 for abbreviations). As
these tendons have not been described previously
(Fig. 6C), the morphology of
the levator and the depressor muscles described here differs from that
described by Miller (Miller,
1950). The depressors and the levators in the same leg segment
display distinct features. This results primarily from the different lengths
and diameters of the internal tendons to which the depressor and levator
muscle fibres are attached (Fig.
6A,B). In tibia and coxa segments, the diameter of the depressor
tendons is greater than that of the levator tendons, whereas the comparatively
thicker levator tendon is present in the femur (schematised in
Fig. 6B). Moreover, depressor
tendons are generally longer than levator tendons, and this is particularly
notable in the tibia. As a consequence of the marked differences in tendon
morphology, the number of muscle fibres that build tadm is higher than of talm
(Table 1). In contrast to the
tibia, the number of muscle fibres constituting depressors and levators in
femur and coxa segments is more balanced
(Table 1). Taken together, we
interpret the described differences in depressor and levator morphology as
reflecting the potential efforts to which these muscles are dedicated. Our
GFP-based simultaneous detection of muscles and tendons also identified two
muscles in the trochanter (Fig.
6 and Fig. S2A-D in supplementary material). These are the femur
depressor (fedm) and the femur reductor (ferm) muscles, making the trochanter
the only leg segment with different muscle organisation.
|
Finally, we propose a new nomenclature for the appendicular muscles and
tendons (Table 1,
Fig. 6) with respect to the
dorsoventral, anteroposterior and proximodistal axes of the leg. The presence,
previously identified by Miller (Miller,
1950), of nine appendicular muscles labelled 35 to 44
(Fig. 6C), including depressors
and levators, is confirmed (Fig.
6A,B). Our analysis also identifies five leg muscles that were not
described by Miller (compare Fig. 6B with
6C, see Table 1).
These are two tarsus reductor muscles, tarm1 and tarm2, the femur depressor
muscle, fedm, and two long tendon muscles, one in the tibia and one in the
femur, which we designate ltm1 and ltm2, respectively
(Fig. 5A,B,H,I,
Fig. 6B,D, Table 1). Tarm1 and tarm2 are
the only leg muscles that are not associated with the internal tendons. Tarm1
is composed of five, and tarm2 of three, short aligned fibres attached on both
sides to the epithelial apodemes (Fig.
5A,B). Tarm1 is located on the posterior, and tarm2 on the
anterior, side of the tibia/tarsus junction
(Fig. 5A,B,
Fig. 6D). Fibres forming the
long tendon muscles are attached on the posterior sides of the tibia and femur
(Fig. 5B,I,
Fig. 6D).
For a better characterisation of muscle fibres constituting appendicular musculature, we dissected individual muscles from different leg segments of the adult MHC-tauGFP flies (Fig. 5C-G,J-P, Fig. S2D-I in supplementary material). The analysis of dissected adult leg muscles confirms the general muscle and tendon organisation from the 55-hour APF pupae (compare Fig. 5A with 5C,D). Dissection revealed the striated character of syncytial muscle fibres. Depending on muscle type, appendicular fibres were found to contain 10 to 25 nuclei (Fig. 5E,L,O,P, Fig. S2D-F) arranged in two rows (Fig. 5P, Fig. S2E). Interestingly, within the tibia and femur, the levator muscles display comparatively stronger MHC-tauGFP expression than the depressors (Fig. 5F,G,J), whereas the opposite is observed in coxa (Fig. S2I in supplementary material). Moreover our analysis by transmitted light and electron microscopy revealed a classic sarcomeric organisation of muscle fibres with a canonical succession of Z, I, H and M bands (Fig. S3A-C in supplementary material). Interestingly, when comparing the depressor and the levator muscle ultrastructure, marked differences in sarcomere size and the number of mitochondria were found (see Fig. S3 for more details).
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Discussion |
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Appendicular myogenesis versus larval and flight muscle formation
A common feature of all Drosophila muscles is that they arise from
twi-expressing non-differentiated cells. Leg muscles originate from a
restricted subpopulation of such cells (5-10 myoblasts) associated with the
embryonic leg disc primordia. These cells start to proliferate in the second
instar larvae to form a population of about 500 myoblasts that are randomly
deployed on the disc epithelium and also are known as adepithelial cells
(Bate et al., 1991;
Broadie and Bate, 1991
).
Unlike the embryonic promuscular cells, they do not seem to be organised into
clusters of cells from which progenitors of individual muscles segregate
(Carmena et al., 1995
), but
rather to follow the segmental subdivision of the leg disc within the
proximodistal axis. This leads to the early loss of twi expression in
adepithelial cells from the tarsal segments. The main feature of all
Drosophila muscles that form de novo, including the larval body wall
and the adult direct flight muscles, is that they develop from the specialised
myoblasts named muscle founder cells (Bate,
1990
; Baylies et al.,
1998
; Kozopas and Nusse,
2002
; Dutta et al.,
2004
). The leg muscles belong to this category of muscle, and our
study shows that their formation is preceded by the specification of cells
expressing the muscle founder marker duf-lacZ. How the
duf-lacZ-expressing cells segregate from the population of
adepithelial cells and how they become muscle founders remains unclear, but
their association with sr-positive tendon progenitors suggests that
interactions between these two cell types may promote their
differentiation.
Interestingly, in third instar leg discs, duf-lacZ cells segregate
in around only one out of five sr-expressing epithelial domains. This
domain, termed the a domain, is located in the dorsal Dpp-dependent portion of
the disc, suggesting that Dpp signalling may be involved in eliciting this
group of presumptive founders. Similar to the leg tendon precursors described
here, sr-expressing domains have been reported in the notum of the
third instar wing discs (Fernandes et al.,
1996; Ghazi et al.,
2000
; Ghazi et al.,
2003
). These sr-positive domains have been reported to be
involved in flight muscle patterning
(Ghazi et al., 2003
).
In spite of all the similarities, marked differences in appendicular versus flight and larval body wall musculatures exist that can be explained by the specific properties of leg tendons. As demonstrated by our analyses of Stripe-GFP-expressing leg discs, at the end of third instar, concomitant with disc evagination, the epithelial domains of tendon progenitors start to invaginate inside the disc. This leads to the formation of internal tendons that have not been described in other body parts of the adult fly. Importantly, the presumptive founder cells associated with the invaginating tendon precursors are vectored and deployed throughout the proximodistal axis of the leg segments. Such a system provides an effective way to generate multifibre muscles in an invertebrate leg devoid of internal skeleton.
The mechanisms governing the formation of internal tendons remain to be
elucidated; however, the co-expression of sr with odd in
invaginating tendon precursors suggests a potential involvement of Notch.
odd was previously described as an important element of the
Notch-dependent cascade that controls the invagination of segmental joints
(Bischop et al., 1999; Hao et al.,
2003). Thus, it is possible that a similar set of genes controls
the different epithelial invagination events that occur in the developing
leg.
Using transgenic lines that express GFP in tendon precursors (Stripe-GFP),
in myoblasts and in tendons (1151-GFP), and in developing myotubes
(MHC-tauGFP), we were able, for the first time, to monitor appendicular
myogenesis during pupa metamorphosis. At 20 hours APF, a large number of
myoblasts are associated with the internal tendons, suggesting that the
founder cells that are initially linked to tendons have attracted
fusion-competent myoblasts to form prefusion complexes. Five hours later we
can discern muscle precursors composed of 5 to 10 nuclei, indicating that the
first wave of fusion takes place between 20 and 25 hours APF. Shortly after,
at 35 hours APF, the second fusion wave occurs, giving rise to the
multinucleated myotubes that are attached on one side to the internal tendons.
The timing of the observed fusion events is comparable to that reported
previously for the de novo forming DFMs
(Ghazi et al., 2000). The next
myogenic steps, including myotube growth, recognition of cognate
sr-expressing epithelial attachment sites and induction of expression
of myofibrillar proteins, are similar to the previously described events that
lead to the formation of the flight and body wall muscles
(Becker et al., 1997
;
Frommer et al., 1996
;
Vorbruggen and Jackle, 1997
;
Yarnitzky et al., 1997
). The
most important, unique, feature of leg muscle fibres that makes them different
from other Drosophila muscles is their association with the internal
tendons.
General organisation and nomenclature of the Drosophila leg muscles
The appendicular muscle pattern revealed by our study, with two principal
muscles (levator and depressor) in each leg segment, resembles that described
by Miller (Miller, 1950).
However, the organisation of the muscle fibres composing levators and
depressors is different, as they are attached to internal tendons that have
not been described previously. The only tendon reported by Miller was the long
tendon of the tarsus. Our analysis shows that this tendon extends to the femur
and harbours two previously undescribed muscles, which we designate ltm1 and
ltm2.
Overall, the computer-assisted reconstruction of the leg musculature
enabled us to identify all the appendicular muscles and tendons, to define
their anteroposterior, dorsoventral and proximodistal positions, and to
determine the number of muscle fibres that compose the individual muscles. As
this is the first reported systematic analysis of the Drosophila leg
musculature, we propose designations and their corresponding abbreviations
(see Table 1) for all the
identified muscles and tendons. In general, the proposed designations reflect
the muscle and tendon functions. For example, muscles located in the femur
that ensure movements of the adjacent tibia are named tibia levator (tilm) and
tibia depressor (tidm) muscle. This nomenclature is largely based on that of
Miller (Miller, 1950).
Our observations also indicate that the general pattern of appendicular muscles is invariant in males and females. However, muscle fibres that contribute to depressors and levators display distinct characteristics, suggesting differences in the genetic programme that ensures their specification. Most specifically, they differ at the ultrastructural level, displaying variations in sarcomere size and number of mitochondria. As determined by the analyses of dissected appendicular muscles, the number of nuclei that contribute to the mature fibres differs in the different types of muscle, but is relatively invariant when the same muscles from two different legs are compared. This suggests a precise control mechanism that sets up the complex events of appendicular myogenesis in Drosophila.
The association of muscle and tendon precursors in the imaginal leg discs
of Drosophila reported here resembles the temporally and spatially
linked development of avian tendons and muscles described in the chick hind
limb (Kardon, 1998). In
addition, as demonstrated recently (Brent
et al., 2003
), the specification of tendon progenitors in
vertebrate embryos takes place very early in development, in a compartment
immediately adjacent to the myotome. Thus it seems that conserved mechanisms
may control the co-ordinated development of muscles and tendons in both the
Drosophila leg and vertebrate embryos. An attractive possibility is
that the muscle and tendon progenitors mutually promote each other's
specification. The existence of such a mechanism could be easily tested in the
future using Drosophila as a model system.
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ACKNOWLEDGMENTS |
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Footnotes |
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Supplementary material for this article is available at http://dev.biologists.org/cgi/content/full/131/24/6041/DC1
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