Nerve-muscle interactions during flight muscle development in Drosophila

Development ◽  
1998 ◽  
Vol 125 (9) ◽  
pp. 1769-1779 ◽  
Author(s):  
J.J. Fernandes ◽  
H. Keshishian
Keyword(s):  
Muscle Development ◽  
Synapse Formation ◽  
Muscle Fibers ◽  
Developmental State ◽  
Fiber Formation ◽  
Absolute Dependence ◽  
Flight Muscles ◽  
Nerve Muscle ◽  
Longitudinal Muscles ◽  
Primary Motoneuron

During Drosophila pupal metamorphosis, the motoneurons and muscles differentiate synchronously, providing an opportunity for extensive intercellular regulation during synapse formation. We examined the existence of such interactions by developmentally delaying or permanently eliminating synaptic partners during the formation of indirect flight muscles. When we experimentally delayed muscle development, we found that although adult-specific primary motoneuron branching still occurred, the higher order (synaptic) branching was suspended until the delayed muscle fibers reached a favourable developmental state. In reciprocal experiments we found that denervation caused a decrease in the myoblast pool. Furthermore, the formation of certain muscle fibers (dorsoventral muscles) was specifically blocked. Exceptions were the adult muscles that use larval muscle fibers as myoblast fusion targets (dorsal longitudinal muscles). However, when these muscles were experimentally compelled to develop without their larval precursors, they showed an absolute dependence on the motoneurons for their formation. These data show that the size of the myoblast pool and early events in fiber formation depend on the presence of the nerve, and that, conversely, peripheral arbor development and synaptogenesis is closely synchronized with the developmental state of the muscle.

The development of indirect flight muscle innervation in Drosophila melanogaster

Development ◽  
1993 ◽  
Vol 118 (1) ◽  
pp. 215-227 ◽  
Author(s):  
J. Fernandes ◽  
K. VijayRaghavan
Keyword(s):  
Muscle Development ◽  
Flight Muscle ◽  
Neuromuscular Junctions ◽  
Indirect Flight Muscle ◽  
Larval Life ◽  
Spatial And Temporal Patterns ◽  
Muscle Innervation ◽  
Flight Muscles ◽  
Nerve Muscle ◽  
Longitudinal Muscles

We have examined the development of innervation to the indirect flight muscles of Drosophila. During metamorphosis, the larval intersegmental nerve of the mesothorax is remodelled to innervate the dorsal longitudinal muscles and two of the dorsoventral muscles. Another modified larval nerve innervates the remaining dorsoventral muscle. The dorsal longitudinal muscles develop using modified larval muscles as templates while dorsoventral muscles develop without the use of such templates. The development of innervation to the two groups of indirect flight muscles differs in spatial and temporal patterns, which may reflect the different ways in which these muscles develop. The identification of myoblasts associated with thoracic nerves during larval life and the association of migrating myoblasts with nerves during metamorphosis indicate the existence of nerve-muscle interactions during indirect flight muscle development. In addition, the developing pattern of axonal branching suggests a role for the target muscles in respecifying neuromuscular junctions during metamorphosis.

Fast myosin heavy chains expressed in secondary mammalian muscle fibers at the time of their inception

1994 ◽  
Vol 107 (9) ◽  
pp. 2361-2371 ◽  
Author(s):  
M. Cho ◽  
S.M. Hughes ◽  
I. Karsch-Mizrachi ◽  
M. Travis ◽  
L.A. Leinwand ◽  
...  
Keyword(s):  
Muscle Development ◽  
Muscle Fibers ◽  
Fiber Formation ◽  
Mammalian Skeletal Muscle ◽  
Western Blots ◽  
Mammalian Muscle ◽  
Heavy Chains ◽  
Fast Myosin ◽  
Myhc Isoforms ◽  
Fast Myosin Heavy Chain

Mammalian skeletal muscle is generated by two waves of fiber formation, resulting in primary and secondary fibers. These fibers mature to give rise to several classes of adult muscle fibers with distinct contractile properties. Here we describe fast myosin heavy chain (MyHC) isoforms that are expressed in nascent secondary, but not primary, fibers in the early development of rat and human muscle. These fast MyHCs are distinct from previously described embryonic and neonatal fast MyHCs. To identify these MyHCs, monoclonal antibodies were used whose specificity was determined in western blots of MyHCs on denaturing gels and reactivity with muscle tissue at various stages of development. To facilitate a comparison of our results with those of others obtained using different antibodies or species, we have identified cDNAs that encode the epitopes recognized by our antibodies wherever possible. The results suggest that epitopes characteristic of adult fast MyHCs are expressed very early in muscle fiber development and distinguish newly formed secondary fibers from primary fibers. This marker of secondary fibers, which is detectable at the time of their inception, should prove useful in future studies of the derivation of primary and secondary fibers in mammalian muscle development.

scholarly journals Adult Drosophila muscle morphometry through microCT reveals dynamics during ageing

Open Biology ◽  
2019 ◽  
Vol 9 (6) ◽  
pp. 190087 ◽  
Author(s):  
Dhananjay Chaturvedi ◽  
Sunil Prabhakar ◽  
Aman Aggarwal ◽  
Krishan B. Atreya ◽  
K. VijayRaghavan
Keyword(s):  
Muscle Development ◽  
Imaging Techniques ◽  
Power Stroke ◽  
Tissue Preparation ◽  
Dependent Manner ◽  
Form And Function ◽  
Insect Biodiversity ◽  
Flight Muscles ◽  
And Function ◽  
Longitudinal Muscles

Indirect flight muscles (IFMs) in adult Drosophila provide the key power stroke for wing beating. They also serve as a valuable model for studying muscle development. An age-dependent decline in Drosophila free flight has been documented, but its relation to gross muscle structure has not yet been explored satisfactorily. Such analyses are impeded by conventional histological preparations and imaging techniques that limit exact morphometry of flight muscles. In this study, we employ microCT scanning on a tissue preparation that retains muscle morphology under homeostatic conditions. Focusing on a subset of IFMs called the dorsal longitudinal muscles (DLMs), we find that DLM volumes increase with age, partially due to the increased separation between myofibrillar fascicles, in a sex-dependent manner. We have uncovered and quantified asymmetry in the size of these muscles on either side of the longitudinal midline. Measurements of this resolution and scale make substantive studies that test the connection between form and function possible. We also demonstrate the application of this method to other insect species making it a valuable tool for histological analysis of insect biodiversity.

scholarly journals The Hippo pathway controls myofibril assembly and muscle fiber growth by regulating sarcomeric gene expression

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Aynur Kaya-Çopur ◽  
Fabio Marchiano ◽  
Marco Y Hein ◽  
Daniel Alpern ◽  
Julie Russeil ◽  
...  
Keyword(s):  
Gene Expression ◽  
Muscle Fiber ◽  
Flight Muscle ◽  
Hippo Pathway ◽  
Muscle Fibers ◽  
Muscle Growth ◽  
Fiber Growth ◽  
Flight Muscles ◽  
Sarcomeric Gene ◽  
The Hippo Pathway

Skeletal muscles are composed of gigantic cells called muscle fibers, packed with force-producing myofibrils. During development the size of individual muscle fibers must dramatically enlarge to match with skeletal growth. How muscle growth is coordinated with growth of the contractile apparatus is not understood. Here, we use the large Drosophila flight muscles to mechanistically decipher how muscle fiber growth is controlled. We find that regulated activity of core members of the Hippo pathway is required to support flight muscle growth. Interestingly, we identify Dlg5 and Slmap as regulators of the STRIPAK phosphatase, which negatively regulates Hippo to enable post-mitotic muscle growth. Mechanistically, we show that the Hippo pathway controls timing and levels of sarcomeric gene expression during development and thus regulates the key components that physically mediate muscle growth. Since Dlg5, STRIPAK and the Hippo pathway are conserved a similar mechanism may contribute to muscle or cardiomyocyte growth in humans.

scholarly journals Rapid dispersal of clustered postsynaptic nuclei following dissociation of skeletal muscle fibers.

1996 ◽  
Vol 199 (11) ◽  
pp. 2359-2367
Author(s):  
C Brösamle ◽  
D P Kuffler
Keyword(s):  
Skeletal Muscle ◽  
Synapse Formation ◽  
Contractile Activity ◽  
Muscle Fibers ◽  
Skeletal Muscle Fibers ◽  
Synaptic Region ◽  
Nuclear Clusters ◽  
Specialized Structure

The vertebrate neuromuscular junction is a highly specialized structure containing many unique proteins and an underlying cluster of nuclei. Part of this specialization results from the expression of the genes for these proteins in nuclei clustered in the postsynaptic region. Contractile activity, as well as molecules located in the synaptic extracellular matrix (ECM), have been implicated in the induction of gene expression in these clustered nuclei. The present experiments were aimed at examining whether the presence of the synaptic ECM and presynaptic cells play a role in maintaining the clustering of the nuclei. We describe the normal distribution of nuclei clustered in the synaptic region of intact adult frog, Rana pipiens, skeletal muscle fibers and show that innervation is not required to maintain the nuclear clusters. Even after long-term (4 week) denervation, the clusters remain unchanged. Dissociation of the muscle fibers with proteases that remove ECM, Schwann cells and other satellite cells from the synaptic sites is followed by a rapid (within approximately 1.5 h) and almost complete dispersal of the clustered nuclei. Attempts to recluster the postsynaptic nuclei by the application of ECM components to muscle fibers in vitro were not successful. We propose that a factor or factors, localized in the synaptic ECM as a result of synapse formation and acting via the transmembrane or cytoplasmic domains of their respective receptors, induces the formation of a specialized cytoskeleton in the postsynaptic region that is capable of pulling in or 'trapping' nuclei. The removal of these factors from the ECM by proteases brings about the disorganization of the cytoskeleton and the freeing of the 'trapped' nuclei.

Overlapping functions of the myogenic bHLH genes MRF4 and MyoD revealed in double mutant mice

Development ◽  
1998 ◽  
Vol 125 (13) ◽  
pp. 2349-2358 ◽  
Author(s):  
A. Rawls ◽  
M.R. Valdez ◽  
W. Zhang ◽  
J. Richardson ◽  
W.H. Klein ◽  
...  
Keyword(s):  
Skeletal Muscle ◽  
Double Mutant ◽  
Muscle Development ◽  
Expression Patterns ◽  
Muscle Fibers ◽  
Mutant Mice ◽  
Myoblast Differentiation ◽  
Bhlh Genes ◽  
Bhlh Factors

The myogenic basic helix-loop-helix (bHLH) genes - MyoD, Myf5, myogenin and MRF4 - exhibit distinct, but overlapping expression patterns during development of the skeletal muscle lineage and loss-of-function mutations in these genes result in different effects on muscle development. MyoD and Myf5 have been shown to act early in the myogenic lineage to establish myoblast identity, whereas myogenin acts later to control myoblast differentiation. In mice lacking myogenin, there is a severe deficiency of skeletal muscle, but some residual muscle fibers are present in mutant mice at birth. Mice lacking MRF4 are viable and have skeletal muscle, but they upregulate myogenin expression, which could potentially compensate for the absence of MRF4. Previous studies in which Myf5 and MRF4 null mutations were combined suggested that these genes do not share overlapping myogenic functions in vivo. To determine whether the functions of MRF4 might overlap with those of myogenin or MyoD, we generated double mutant mice lacking MRF4 and either myogenin or MyoD. MRF4/myogenin double mutant mice contained a comparable number of residual muscle fibers to mice lacking myogenin alone and myoblasts from those double mutant mice formed differentiated multinucleated myotubes in vitro as efficiently as wild-type myoblasts, indicating that neither myogenin nor MRF4 is absolutely essential for myoblast differentiation. Whereas mice lacking either MRF4 or MyoD were viable and did not show defects in muscle development, MRF4/MyoD double mutants displayed a severe muscle deficiency similar to that in myogenin mutants. Myogenin was expressed in MRF4/MyoD double mutants, indicating that myogenin is insufficient to support normal myogenesis in vivo. These results reveal unanticipated compensatory roles for MRF4 and MyoD in the muscle differentiation pathway and suggest that a threshold level of myogenic bHLH factors is required to activate muscle structural genes, with this level normally being achieved by combinations of multiple myogenic bHLH factors.

scholarly journals Indirect flight muscles in Drosophila melanogaster as a tractable model to study muscle development and disease

2020 ◽  
Vol 64 (1-2-3) ◽  
pp. 167-173
Author(s):  
Saroj Jawkar ◽  
Upendra Nongthomba
Keyword(s):  
Drosophila Melanogaster ◽  
Muscle Development ◽  
Myoblast Fusion ◽  
Successful Development ◽  
Adult Muscle ◽  
Attachment Sites ◽  
Flight Muscles ◽  
And Function

Myogenesis is a complex multifactorial process leading to the formation of the adult muscle. An amalgamation of autonomous processes including myoblast fusion and myofibrillogenesis, as well as non-autonomous processes, such as innervations from neurons and precise connections with attachment sites, are responsible for successful development and function of muscles. In this review, we describe the development of the indirect flight muscles (IFMs) in Drosophila melanogaster, and highlight the use of the IFMs as a model for studying muscle development and disease, based on recent studies on the development and function of IFMs.

scholarly journals Skeletal muscle development in vertebrate animals

2015 ◽  
Vol 1 (2) ◽  
pp. 139-148
Author(s):  
Md Shahjahan
Keyword(s):  
Skeletal Muscle ◽  
Muscle Development ◽  
Muscle Fibers ◽  
Muscle Growth ◽  
Paraxial Mesoderm ◽  
Meat Production ◽  
Lineage Specification ◽  
Proliferation And Differentiation ◽  
Axial Musculature ◽  
Postnatal Stage

This review covers the pre- and post-natal development of skeletal muscle of vertebrate animals with cellular and molecular levels. The formation of skeletal muscle initiates from paraxial mesoderm during embryogenesis of individuals which develops somites and subsequently forms dermomyotome derived myotome to give rise axial musculature. This process (myogenesis) includes stem and progenitor cell maintenance, lineage specification, and terminal differentiation to form myofibrils consequent muscle fibers which control muscle mass and its multiplication. The main factors of muscle growth are proliferation and differentiation of myogenic cells in prenatal stage and also the growth of satellite cells at postnatal stage. There is no net increase in the number of muscle fibers in vertebrate animals after hatch or birth except fish. The development of muscle is characterized by hyperplasia and hypertrophy in prenatal and postnatal stages of individuals, respectively, through Wnt signalling pathway including environment, nutrition, sex, feed, growth and myogenic regulatory factors. Therefore further studies could elucidate new growth related genes, markers and factors to enhance meat production and enrich knowledge on muscle growth.Asian J. Med. Biol. Res. June 2015, 1(2): 139-148

scholarly journals Flying High—Muscle-Specific Underreplication in Drosophila

Genes ◽  
2020 ◽  
Vol 11 (3) ◽  
pp. 246 ◽  
Author(s):  
J. Spencer Johnston ◽  
Mary E. Zapalac ◽  
Carl E. Hjelmen
Keyword(s):  
Flow Cytometry ◽  
Dna Synthesis ◽  
Salivary Glands ◽  
Genome Size ◽  
Flight Muscle ◽  
S Phase ◽  
The Other ◽  
Tissue Type ◽  
Flight Muscles ◽  
Longitudinal Muscles

Drosophila underreplicate the DNA of thoracic nuclei, stalling during S phase at a point that is proportional to the total genome size in each species. In polytene tissues, such as the Drosophila salivary glands, all of the nuclei initiate multiple rounds of DNA synthesis and underreplicate. Yet, only half of the nuclei isolated from the thorax stall; the other half do not initiate S phase. Our question was, why half? To address this question, we use flow cytometry to compare underreplication phenotypes between thoracic tissues. When individual thoracic tissues are dissected and the proportion of stalled DNA synthesis is scored in each tissue type, we find that underreplication occurs in the indirect flight muscle, with the majority of underreplicated nuclei in the dorsal longitudinal muscles (DLM). Half of the DNA in the DLM nuclei stall at S phase between the unreplicated G0 and fully replicated G1. The dorsal ventral flight muscle provides the other source of underreplication, and yet, there, the replication stall point is earlier (less DNA replicated), and the endocycle is initiated. The differences in underreplication and ploidy in the indirect flight muscles provide a new tool to study heterochromatin, underreplication and endocycle control.

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