Embryonic assembly of a complex muscle is directed by a single identified cell in the medicinal leech

Jellies, John; Kristan, WB

doi:10.1523/jneurosci.08-09-03317.1988

Cited by 48 publications

(32 citation statements)

References 27 publications

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“…In cuttlefish, the radial fibres may act as a scaffold for the spatial organization of myocytes that will give rise to the mass of slow and fast circular fibres. The formation of a primary muscle grid and its subsequent use as a template for differentiation of myoblasts are two basic developmental phases that have already been described in vermiform Spiralia such as Platyhelminthes (Ladurner and Rieger, 2000) and Anellids (Jellies and Kristan, 1988), and the patterning of body wall muscles is achieved without using originally positional information of the nervous system (Ladurner and Rieger, 2000).…”

Section: Muscle Fibres Differentiation In Cuttlefish Developmentmentioning

confidence: 99%

A hedgehog homolog is involved in muscle formation and organization of Sepia officinalis (mollusca) mantle

Grimaldi

Tettamanti

Acquati

et al. 2008

Developmental Dynamics

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Our study focuses on the possible involvement of the Hedgehog (Hh) pathway in the differentiation of striated muscle fibres in cuttlefish (Sepia officinalis) mantle. We show here that both an hh-homolog signalling molecule and its receptor Patched (Ptc) are expressed in a specific population of myoblasts which differentiates into the radial fast fibres. To evaluate the functional significance of hh expression in developing cuttlefish, we inhibited the Hedgehog signalling pathway by means of cyclopamine treatment in cuttlefish embryos. In treated embryos, the gross anatomy was considerably compromised, displaying an extremely reduced mantle with a high degree of morphological abnormalities. TUNEL and BrdU assays showed that the absence of an hh signalling induces apoptosis and reduces the proliferation rate of muscle precursors. We therefore hypothesize a possible involvement of Hh and its receptor Ptc in the formation of striated muscle fibres in cuttlefish. Developmental Dynamics 237:659 -671, 2008.

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Section: Muscle Fibres Differentiation In Cuttlefish Developmentmentioning

confidence: 99%

A hedgehog homolog is involved in muscle formation and organization of Sepia officinalis (mollusca) mantle

Grimaldi

Tettamanti

Acquati

et al. 2008

Developmental Dynamics

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“…Studies on pattern formation during embryogenesis to produce these well-defined networks of muscle fibers only exist for a small number of taxa among others, in Platyhelmintha, Sipuncula and Annelida (Jellies and Kristan, 1988a;Ladurner and Rieger, 2000;Wanninger et al, 2005). The available data already indicate that such a functional basic pattern of adult muscle arrangement is achieved by diverse developmental processes.…”

mentioning

confidence: 99%

“…Findings on mesoderm development in oligochaetes are restricted to very early processes, such as cell-lineage studies on m-teloblasts in Tubifex hattai and Eisenia foetida, not covering muscle formation during later embryogenesis (Storey, 1989;Goto et al, 1999a,b). Later development of the threelayered muscle grid (circular, oblique and longitudinal) has been well studied only in leeches (Hirudo medicinalis, Helobdella triserialis, Theromyzon rude), however, focusing on the formation of the oblique muscle layer (Jellies and Kristan, 1988a;Jellies, 1990). Additionally, extensive celllineage analyses have been carried out in those species (reviewed by Shankland, 1991).…”

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confidence: 99%

Pattern of body‐wall muscle differentiation during embryonic development of Enchytraeus coronatus (Annelida: Oligochaeta; Enchytraeidae)

Bergter

Paululat

2007

Journal of Morphology

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The plesiomorphic arrangement of body-wall musculature within the annelids is still under discussion. While polychaete groups show a great variety of patterns in their somatic muscles, the musculature of soil-living oligochaetes was thought to represent the characteristic pattern in annelids. Oligochaete body-wall muscles consist of an outer continuous layer of circular and an inner continuous layer of longitudinal muscles, forming a closed tube. Since designs of adult body musculature are influenced by evolutionary changes, additional patterns found during embryogenesis can give further information about possible plesiomorphic features. In oligochaetes, detailed cell-lineage analyses document the origin of the mesoderm and consequently the muscles, but later processes of muscle formation remain unclear. In the present work, body-wall muscle differentiation was monitored during embryogenesis of thesoil-living oligochaete Enchytraeus coronatus (Annelida) by phalloidin staining. Primary circular muscles form in a discrete anterior-to-posterior segmental pattern, whereas emerging longitudinal muscles are restricted to one ventral and one dorsal pair of primary strands, which continuously elongate towards posterior. These primary muscles establish an initial muscle-template. Secondary circular and longitudinal muscles subsequently differentiate in the previous spaces later in development. The prominent ventral primary longitudinal muscle strands on both sides eventually meet at the ventral midline due to neurulation, which moves the ventral nerve cord into a coelomic position, closing the muscle layers into a complete tube. This early embryonic pattern in E. coronatus resembles the adult body-wall muscle arrangements in several polychaete groups as well as muscle differentiation during embryonic development of the polychaete Capitella sp. I.

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“…Pairs of CCs were found bilaterally near the ventral surface of the body wall, in each somatic segment of the developing medicinal leech (Jellies and Kristan, 1988;Fig. 1).…”

Section: Comb Cell Development and Cytoskeletal Organizationmentioning

confidence: 99%

“…1A). Only later, after somata have elongated and brought segmental homologs into close proximity and the processes themselves have already extended several tens of micrometers, do the processes of each CC begin to assume their characteristic 45°orientation relative to the A-P body axis (Jellies and Kristan, 1988). Beginning at about midembryogenesis, late E10 to early E11, these processes grow rapidly, with those on the lateral surface of the cell extending anterolaterally and those on the medial surface extending posteromedially, with the left and right cells of a segmental pair showing mirror symmetry (Fig.…”

Section: Comb Cell Development and Cytoskeletal Organizationmentioning

confidence: 99%

In vivo imaging of growth cone and filopodial dynamics: Evidence for contact‐mediated retraction of filopodia leading to the tiling of sibling processes

Baker

Macagno

2006

J of Comparative Neurology

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In the leech embryo, the peripheral comb cell (CC) sends out many nonoverlapping, growth cone-tipped processes that grow in parallel and serve as a scaffold for the migrating myocytes of the later-developing oblique muscle layer. To explore how the parallel arrangement is generated we first examined the arrangement of CC cytoskeletal components by expressing a tubulin-binding protein and actin, both tagged with fluorescent reporters. This revealed that the growth cones were compartmentalized into F-actin-rich filopodia and a microtubule-rich central region. Time-lapse analysis with a 2-photon laser scanning microscope revealed that the growth cones of the CC are highly dynamic, undergoing rapid filopodial extension and retraction. Measurements of filopodial lifespan and length revealed that most filopodia at the leading edge of the growth cone achieved significantly longer lifespans and length than lateral filopodia. Furthermore, for the short-lived lateral filopodia, apparent interaction with a neighboring process was found to be a significant predictor of their nearly immediate (within 2-4 minutes) retraction. When contact was experimentally prevented by ablating individual CCs, the filopodia from the growth cones of adjacent segmental neighbors were found to be significantly lengthened in the direction of the removed homolog. Treatment with low doses of cytochalasin D to disrupt F-actin assembly led to filopodial retraction and growth cone collapse and resulted in the bifurcation of many CC processes, numerous crossover errors, and the loss of parallelism. These findings indicate the existence of a contact-mediated repulsive interaction between processes of the CC.

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Embryonic assembly of a complex muscle is directed by a single identified cell in the medicinal leech

Cited by 48 publications

References 27 publications

A hedgehog homolog is involved in muscle formation and organization of Sepia officinalis (mollusca) mantle

A hedgehog homolog is involved in muscle formation and organization of Sepia officinalis (mollusca) mantle

Pattern of body‐wall muscle differentiation during embryonic development of Enchytraeus coronatus (Annelida: Oligochaeta; Enchytraeidae)

In vivo imaging of growth cone and filopodial dynamics: Evidence for contact‐mediated retraction of filopodia leading to the tiling of sibling processes

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