Spalt mediates an evolutionarily conserved switch to fibrillar muscle fate in insects

Schönbauer, Cornelia; Distler, Jutta; Jährling, Nina; Radolf, Martin; Dodt, Hans‐Ulrich; Frasch, Manfred; Schnorrer, Frank

doi:10.1038/nature10559

Cited by 111 publications

(186 citation statements)

References 35 publications

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“…4A,B,E), demonstrating that, even though the abdominal muscle pattern at 50 hours APF was completed (Bate et al, 1991), muscles sustain significant growth during late pupal development. Tubular muscles contain an internal lumen devoid of actin where nuclei are found (Peckham et al, 1990; Schönbauer et al, 2011). Our studies showed that the lumen was maintained constant in size along development (supplementary material Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Morphologically, there are two major muscle types in the Drosophila adult: fibrillar muscles, which are present exclusively as indirect flight muscles, and tubular muscles, which include the jump, leg and abdominal muscles (Peckham et al, 1990; Schönbauer et al, 2011). In this work, we used the adult abdominal muscles as our model system to study adult myogenesis in vivo .…”

Section: Introductionmentioning

confidence: 99%

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The conserved transmembrane proteoglycan Perdido/Kon-tiki is essential for myofibrillogenesis and sarcomeric structure in Drosophila

Pérez-Moreno¹,

Bischoff²,

Martín-Bermudo³

et al. 2014

Journal of Cell Science

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Muscle differentiation requires the assembly of high-order structures called myofibrils, composed of sarcomeres. Even though the molecular organization of sarcomeres is well known, the mechanisms underlying myofibrillogenesis are poorly understood. It has been proposed that integrin-dependent adhesion nucleates myofibrils at the periphery of the muscle cell to sustain sarcomere assembly. Here, we report a role for the gene perdido (perd, also known as kon-tiki, a transmembrane chondroitin proteoglycan) in myofibrillogenesis. Expression of perd RNAi in muscles, prior to adult myogenesis, can induce misorientation and detachment of Drosophila adult abdominal muscles. In comparison to controls, perd-depleted muscles contain fewer myofibrils, which are localized at the cell periphery. These myofibrils are detached from each other and display a defective sarcomeric structure. Our results demonstrate that the extracellular matrix receptor Perd has a specific role in the assembly of myofibrils and in sarcomeric organization. We suggest that Perd acts downstream or in parallel to integrins to enable the connection of nascent myofibrils to the Z-bands. Our work identifies the Drosophila adult abdominal muscles as a model to investigate in vivo the mechanisms behind myofibrillogenesis.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The conserved transmembrane proteoglycan Perdido/Kon-tiki is essential for myofibrillogenesis and sarcomeric structure in Drosophila

Pérez-Moreno¹,

Bischoff²,

Martín-Bermudo³

et al. 2014

Journal of Cell Science

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“…with Mef2RNAi(15550) at 25°C, and could be linked to the different genetic programs in fibrillar and tubular muscle (Schonbauer et al, 2011).…”

Section: Research Reportmentioning

confidence: 99%

The conserved transcription factor Mef2 has multiple roles in adult Drosophila musculature formation

2012

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SUMMARYMuscle is an established paradigm for analysing the cell differentiation programs that underpin the production of specialised tissues during development. These programs are controlled by key transcription factors, and a well-studied regulator of muscle gene expression is the conserved transcription factor Mef2. In vivo, Mef2 is essential for the development of the Drosophila larval musculature: Mef2-null embryos have no differentiated somatic muscle. By contrast, a similar phenotype has not been seen in analyses of the function of Mef2 genes in other examples of myogenesis. These include using conditional mutant mice, using morpholinos in zebrafish and using hypomorphic mutants in Drosophila adult development. However, we show here that Mef2 is absolutely required for a diverse range of Drosophila adult muscle types. These include the dorso-longitudinal muscles (DLMs), the largest flight muscles, which are produced by tissue remodelling. Furthermore, we demonstrate that Mef2 has temporally separable functions in this remodelling and in muscle maintenance. Drosophila adult muscles are multi-fibre and physiologically diverse, in common with vertebrate skeletal muscles, but in contrast to Drosophila larval muscles. These results therefore establish the importance of Mef2 in multiple roles in examples of myogenesis that have parallels in vertebrates and are distinct from that occurring in Drosophila embryogenesis.

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“…Importantly, recent evidence in the model organism, Drosophila, demonstrated a direct link between myonuclei positioning and proper muscle function, emphasizing the physiological significance of correct myonuclear positioning in proper movement of the organism. [7][8][9] Striated muscle fibers are multinucleated cells of variable size, morphology and physiology (e.g., fast or slow muscles), [10][11][12] but in each of the distinct muscle types, the nuclei, as well as other cytoplasmic organelles are evenly distributed along the entire cytoplasm, suggesting a mechanism capable of sensing muscle dimensions, which is coupled to the cellular machinery capable of moving and/or anchoring organelles within the cell. Surprisingly, information regarding such mechanisms is extremely limited, possibly due to the inability to follow the dynamics of organelle positioning within contracting muscles in live organisms.…”

Section: Positioning Nuclei Within the Cytoplasm Of Striated Muscle Fmentioning

confidence: 99%

Positioning nuclei within the cytoplasm of striated muscle fiber

Volk

2013

Nucleus

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S triated muscles contain a tightly ordered cytoplasm in which the shape and size of the nuclei are comparable and nuclear distribution is uniform. These features were recently shown to be essential for muscle function. In an attempt to elucidate mechanisms regulating the position and shape of myonuclei, we analyzed the function of the two KASH proteins that are uniquely present in the Drosophila genome, MSP-300 and Klarsicht, both expressed in striated muscles. We demonstrated that both KASH proteins cooperate to construct a unique ring composed of MSP-300 protein that surrounds and attached to the nuclear envelope. The MSP-300 nuclear ring structure recruits and associates with a network of polarized astral microtubules that enables the dynamic movement and uniform spacing between the nuclei in each muscle fiber.

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Spalt mediates an evolutionarily conserved switch to fibrillar muscle fate in insects

Cited by 111 publications

References 35 publications

The conserved transmembrane proteoglycan Perdido/Kon-tiki is essential for myofibrillogenesis and sarcomeric structure in Drosophila

The conserved transmembrane proteoglycan Perdido/Kon-tiki is essential for myofibrillogenesis and sarcomeric structure in Drosophila

The conserved transcription factor Mef2 has multiple roles in adult Drosophila musculature formation

Positioning nuclei within the cytoplasm of striated muscle fiber

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