FRINK Linked Data Fragments server

Matches in SemOpenAlex for { <https://semopenalex.org/work/W2039220265> ?p ?o ?g. }

• W2039220265 endingPage "219" @default.
• W2039220265 startingPage "207" @default.
• W2039220265 abstract "Somites are transient, mesodermally derived structures that give rise to a number of different cell types within the vertebrate embryo. To achieve this, somitic cells are partitioned into lineage-restricted domains, whose fates are determined by signals secreted from adjacent tissues. While the molecular nature of many of the inductive signals that trigger formation of different cell fates within the nascent somite has been identified, less is known about the processes that coordinate the formation of the subsomitic compartments from which these cells arise. Utilizing a combination of vital dye-staining and lineage-tracking techniques, we describe a previously uncharacterized, lineage-restricted compartment of the zebrafish somite that generates muscle progenitor cells for the growth of appendicular, hypaxial, and axial muscles during development. We also show that formation of this compartment occurs via whole-somite rotation, a process that requires the action of the Sdf family of secreted cytokines. Somites are transient, mesodermally derived structures that give rise to a number of different cell types within the vertebrate embryo. To achieve this, somitic cells are partitioned into lineage-restricted domains, whose fates are determined by signals secreted from adjacent tissues. While the molecular nature of many of the inductive signals that trigger formation of different cell fates within the nascent somite has been identified, less is known about the processes that coordinate the formation of the subsomitic compartments from which these cells arise. Utilizing a combination of vital dye-staining and lineage-tracking techniques, we describe a previously uncharacterized, lineage-restricted compartment of the zebrafish somite that generates muscle progenitor cells for the growth of appendicular, hypaxial, and axial muscles during development. We also show that formation of this compartment occurs via whole-somite rotation, a process that requires the action of the Sdf family of secreted cytokines. Within vertebrate embryos, segmentation of the paraxial mesoderm during somitogenesis results in the formation of distinct anterior/posterior cellular compartments within the early somite, defined by differential gene expression. A secondary series of cellular rearrangements generates morphologically distinct, lineage-restricted somitic compartments that are, in turn, induced to form the progenitors of distinct tissues during embryogenesis. Fate-mapping studies, chiefly in the chick embryo, indicate that the dorsal aspect of the amniote somite produces an epithelial intermediary structure, the dermomyotome, that gives rise to the progenitors for skeletal muscle of the axis (the myotome) and to progenitors at limb levels, which are precursors of the appendicular muscles. The dermomyotome is also the source of resident adult skeletal muscle stem cells, the satellite cells (Christ and Ordahl, 1995Christ B. Ordahl C.P. Early stages of chick somite development.Anat. Embryol. (Berl.). 1995; 191: 381-396Crossref PubMed Scopus (613) Google Scholar, Gros et al., 2005Gros J. Manceau M. Thome V. Marcelle C. A common somitic origin for embryonic muscle progenitors and satellite cells.Nature. 2005; 435: 954-958Crossref PubMed Scopus (418) Google Scholar, Relaix et al., 2005Relaix F. Rocancourt D. Mansouri A. Buckingham M. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells.Nature. 2005; 435: 948-953Crossref PubMed Scopus (748) Google Scholar, Kassar-Duchossoy et al., 2005Kassar-Duchossoy L. Giacone E. Gayraud-Morel B. Jory A. Gomes D. Tajbakhsh S. Pax3/Pax7 mark a novel population of primitive myogenic cells during development.Genes Dev. 2005; 19: 1426-1431Crossref PubMed Scopus (364) Google Scholar, Schienda et al., 2006Schienda J. Engleka K.A. Jun S. Hansen M.S. Epstein J.A. Tabin C.J. Kunkel L.M. Kardon G. Somitic origin of limb muscle satellite and side population cells.Proc. Natl. Acad. Sci. USA. 2006; 103: 945-950Crossref PubMed Scopus (153) Google Scholar). Dorsally, the dermomyotome generates the dermal layer of the forming skin of the back (reviewed in Brand-Saberi and Christ, 2000Brand-Saberi B. Christ B. Evolution and development of distinct cell lineages derived from somites.Curr. Top. Dev. Biol. 2000; 48: 1-42Crossref PubMed Scopus (136) Google Scholar, Olivera-Martinez et al., 2000Olivera-Martinez I. Coltey M. Dhouailly D. Pourquie O. Mediolateral somitic origin of ribs and dermis determined by quail-chick chimeras.Development. 2000; 127: 4611-4617PubMed Google Scholar, Ben-Yair and Kalcheim, 2005Ben-Yair R. Kalcheim C. Lineage analysis of the avian dermomyotome sheet reveals the existence of single cells with both dermal and muscle progenitor fates.Development. 2005; 132: 689-701Crossref PubMed Scopus (140) Google Scholar). The ventral aspect of the amniote somite gives rise both to sclerotome, the progenitors of the axial skeleton, and the syndetome, which generates the tendons of the body axis (Brent et al., 2003Brent A.E. Schweitzer R. Tabin C.J. A somitic compartment of tendon progenitors.Cell. 2003; 113: 235-248Abstract Full Text Full Text PDF PubMed Scopus (395) Google Scholar, Christ and Ordahl, 1995Christ B. Ordahl C.P. Early stages of chick somite development.Anat. Embryol. (Berl.). 1995; 191: 381-396Crossref PubMed Scopus (613) Google Scholar). By contrast, zebrafish somites show little overt morphological compartmentalization, and cell lineage analysis has defined the origins of only a subset of the cell types derived from the amniote somite. The best-described zebrafish somitic lineage is that of the embryonic myotome. Myoblast-specific gene expression is initiated coincidently with the anterior/posterior restriction of segmental gene expression with zebrafish somites (Weinberg et al., 1996Weinberg E.S. Allende M.L. Kelly C.S. Abdelhamid A. Murakami T. Andermann P. Doerre O.G. Grunwald D.J. Riggleman B. Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos.Development. 1996; 122: 271-280PubMed Google Scholar, Coutelle et al., 2001Coutelle O. Blagden C.S. Hampson R. Halai C. Rigby P.W. Hughes S.M. Hedgehog signalling is required for maintenance of myf5 and myoD expression and timely terminal differentiation in zebrafish adaxial myogenesis.Dev. Biol. 2001; 236: 136-150Crossref PubMed Scopus (121) Google Scholar). Two distinct myogenic compartments are discernable within presegmentation- and segmentation-stage zebrafish embryos and are generated by different processes. Adaxial cells are early differentiating progenitors of the slow twitch muscle lineage that arise from the most medial portion of the paraxial mesoderm and migrate to form a subcutaneous layer of slow twitch muscle at the lateral-most surface of the myotome (Devoto et al., 1996Devoto S.H. Melancon E. Eisen J.S. Westerfield M. Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation.Development. 1996; 122: 3371-3380Crossref PubMed Google Scholar, Cortes et al., 2003Cortes F. Daggett D. Bryson-Richardson R.J. Neyt C. Maule J. Gautier P. Hollway G.E. Keenan D. Currie P.D. Cadherin-mediated differential cell adhesion controls slow muscle cell migration in the developing zebrafish myotome.Dev. Cell. 2003; 5: 865-876Abstract Full Text Full Text PDF PubMed Scopus (74) Google Scholar). A second identifiable compartment is constituted by the cells of the lateral somitic mesoderm, which are induced to undergo myogenesis by a distinct set of signals from those that regulate adaxial cell myogenesis (Groves et al., 2005Groves J.A. Hammond C.L. Hughes S.M. Fgf8 drives myogenic progression of a novel lateral fast muscle fibre population in zebrafish.Development. 2005; 132: 4211-4222Crossref PubMed Scopus (105) Google Scholar). Fate-mapping studies (Devoto et al., 1996Devoto S.H. Melancon E. Eisen J.S. Westerfield M. Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation.Development. 1996; 122: 3371-3380Crossref PubMed Google Scholar) have revealed that lateral somitic cells contain progenitors of the fast twitch muscle lineage, although this previous analysis failed to provide evidence for any anterior/posterior restriction of the fast twitch muscle precursors within nascent somites, suggested by the restricted onset of myogenesis within the posterior domain of the lateral somite (Devoto et al., 1996Devoto S.H. Melancon E. Eisen J.S. Westerfield M. Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation.Development. 1996; 122: 3371-3380Crossref PubMed Google Scholar, Weinberg et al., 1996Weinberg E.S. Allende M.L. Kelly C.S. Abdelhamid A. Murakami T. Andermann P. Doerre O.G. Grunwald D.J. Riggleman B. Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos.Development. 1996; 122: 271-280PubMed Google Scholar). Sclerotomal cells are generated from ventral somitic regions, as in the amniote somite, but they represent a much-reduced proportion of the somitic derivatives (Morin-Kensicki and Eisen, 1997Morin-Kensicki E.M. Eisen J.S. Sclerotome development and peripheral nervous system segmentation in embryonic zebrafish.Development. 1997; 124: 159-167PubMed Google Scholar). Despite these studies, the embryonic origins of other fish somitic derivatives remained undefined, leading to the suggestion that the lineage-restricted compartments evident within the amniote somite may be innovations that arose during tetrapod evolution (Brand-Saberi and Christ, 2000Brand-Saberi B. Christ B. Evolution and development of distinct cell lineages derived from somites.Curr. Top. Dev. Biol. 2000; 48: 1-42Crossref PubMed Scopus (136) Google Scholar, Stickney et al., 2000Stickney H.L. Barresi M.J. Devoto S.H. Somite development in zebrafish.Dev. Dyn. 2000; 219: 287-303Crossref PubMed Scopus (208) Google Scholar, Sporle, 2001Sporle R. Epaxial-adaxial-hypaxial regionalisation of the vertebrate somite: evidence for a somitic organiser and a mirror-image duplication.Dev. Genes Evol. 2001; 211: 198-217Crossref PubMed Scopus (42) Google Scholar, Hollway and Currie, 2003Hollway G.E. Currie P.D. Myotome meanderings. Cellular morphogenesis and the making of muscle.EMBO Rep. 2003; 4: 855-860Crossref PubMed Scopus (31) Google Scholar). In such a scenario, the increased reliance on the use of appendicular muscle evident in tetrapod, limb-dominant, locomotor strategies and the necessity for a defined embryonic dermal layer as an adaptation to terrestrial environs may have driven the evolution of a distinct dermomyotomal compartment. Conversely, other authors have argued, based only on the expression of specific genes, that an equivalent of the amniote dermomyotome does exist in fish species (Devoto et al., 2006Devoto S.H. Stoiber W. Hammond C.L. Steinbacher P. Haslett J.R. Barresi M.J. Patterson S.E. Adiarte E.G. Hughes S.M. Generality of vertebrate developmental patterns: evidence for a dermomyotome in fish.Evol. Dev. 2006; 8: 101-110Crossref PubMed Scopus (104) Google Scholar, Steinbacher et al., 2006Steinbacher P. Haslett J.R. Six M. Gollmann H.P. Sanger A.M. Stoiber W. Phases of myogenic cell activation and possible role of dermomyotome cells in teleost muscle formation.Dev. Dyn. 2006; 235: 3132-3143Crossref PubMed Scopus (41) Google Scholar, Feng et al., 2006Feng X. Adiarte E.G. Devoto S.H. Hedgehog acts directly on the zebrafish dermomyotome to promote myogenic differentiation.Dev. Biol. 2006; 300: 736-746Crossref PubMed Scopus (77) Google Scholar, Hammond et al., 2006Hammond C.L. Hinits Y. Osborn D.P. Minchin J.E. Tettamanti G. Hughes S.M. Signals and myogenic regulatory factors restrict pax3 and pax7 expression to dermomyotome-like tissue in zebrafish.Dev. Biol. 2006; (in press)PubMed Google Scholar). Equally unclear is the cellular basis for the prodigious growth evident within the larval zebrafish myotome, and it remains unknown if cells directly analogous to satellite cells exist within the zebrafish myotome. More generally, while the concept of recognizable, lineage-restricted compartments within the somites of different model systems is well defined, the molecular mechanisms by which these compartments arise from nascent somites is far from understood in any context. In this study, we define a distinct lineage-restricted domain within the zebrafish somite, the anterior somitic compartment, which gives rise secondarily to a number of different cell types, including a series of muscle progenitor populations that are required during different phases of muscle growth. Generation of these somitic subdomains occurs through the mechanism of whole-somite rotation, a process that we show to require the activity of the secreted cytokine Sdfla and its receptors. Analyses of the expression of the myogenic marker gene myoD within the zebrafish embryo reveals that it is initially restricted to the posterior region of newly formed somites, but by late somitogenesis encompasses the entire anterior/posterior extent of the somite, an expression profile shared by a number of other myogenic regulatory genes (Figure S1; see the Supplemental Data available with this article online) (Weinberg et al., 1996Weinberg E.S. Allende M.L. Kelly C.S. Abdelhamid A. Murakami T. Andermann P. Doerre O.G. Grunwald D.J. Riggleman B. Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos.Development. 1996; 122: 271-280PubMed Google Scholar, Coutelle et al., 2001Coutelle O. Blagden C.S. Hampson R. Halai C. Rigby P.W. Hughes S.M. Hedgehog signalling is required for maintenance of myf5 and myoD expression and timely terminal differentiation in zebrafish adaxial myogenesis.Dev. Biol. 2001; 236: 136-150Crossref PubMed Scopus (121) Google Scholar). This suggests that the anterior somitic domain does not contribute to the initial phase of myogenesis within the zebrafish somite. Furthermore, the expression of zebrafish orthologs of pax3 pax7 and dachshundD (dacD), genes known to be expressed within amniote dermomyotome and hypaxial muscle progenitors (Gros et al., 2005Gros J. Manceau M. Thome V. Marcelle C. A common somitic origin for embryonic muscle progenitors and satellite cells.Nature. 2005; 435: 954-958Crossref PubMed Scopus (418) Google Scholar, Relaix et al., 2005Relaix F. Rocancourt D. Mansouri A. Buckingham M. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells.Nature. 2005; 435: 948-953Crossref PubMed Scopus (748) Google Scholar, Sporle, 2001Sporle R. Epaxial-adaxial-hypaxial regionalisation of the vertebrate somite: evidence for a somitic organiser and a mirror-image duplication.Dev. Genes Evol. 2001; 211: 198-217Crossref PubMed Scopus (42) Google Scholar, Bober et al., 1994Bober E. Franz T. Arnold H.H. Gruss P. Tremblay P. Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells.Development. 1994; 120: 603-612Crossref PubMed Google Scholar, Heanue et al., 1999Heanue T.A. Reshef R. Davis R.J. Mardon G. Oliver G. Tomarev S. Lassar A.B. Tabin C.J. Synergistic regulation of vertebrate muscle development by Dach2, Eya2, and Six1, homologs of genes required for Drosophila eye formation.Genes Dev. 1999; 13: 3231-3243Crossref PubMed Scopus (297) Google Scholar), is restricted to the cells of the anterior somitic compartment (Figure 1). The anterior restriction of the expression of these genes is followed by a shift of expression domains. Both pax3 and pax7 come to be expressed in a single layer of cells superficial to the myotome at the end of somitogenesis, an expression profile that resembles the “external cell” population previously noted by other authors (Waterman, 1969Waterman R.E. Development of the lateral musculature in the teleost, Brachydanio rerio: a fine structural study.Am. J. Anat. 1969; 125: 457-493Crossref PubMed Scopus (151) Google Scholar, Groves et al., 2005Groves J.A. Hammond C.L. Hughes S.M. Fgf8 drives myogenic progression of a novel lateral fast muscle fibre population in zebrafish.Development. 2005; 132: 4211-4222Crossref PubMed Scopus (105) Google Scholar, Devoto et al., 2006Devoto S.H. Stoiber W. Hammond C.L. Steinbacher P. Haslett J.R. Barresi M.J. Patterson S.E. Adiarte E.G. Hughes S.M. Generality of vertebrate developmental patterns: evidence for a dermomyotome in fish.Evol. Dev. 2006; 8: 101-110Crossref PubMed Scopus (104) Google Scholar, Feng et al., 2006Feng X. Adiarte E.G. Devoto S.H. Hedgehog acts directly on the zebrafish dermomyotome to promote myogenic differentiation.Dev. Biol. 2006; 300: 736-746Crossref PubMed Scopus (77) Google Scholar, Hammond et al., 2006Hammond C.L. Hinits Y. Osborn D.P. Minchin J.E. Tettamanti G. Hughes S.M. Signals and myogenic regulatory factors restrict pax3 and pax7 expression to dermomyotome-like tissue in zebrafish.Dev. Biol. 2006; (in press)PubMed Google Scholar) (Figures 1A–1H; Movie S1 [available in the Supplemental Data]). A distinct laterally progressing expression pattern for both of these genes precedes expression within the external cell layer, which suggests that pax7/pax3-expressing anterior somitic cells undergo an anterior-to-lateral rotation (Figures 1A, 1B, and 1L and Figures 5Q, 5T, and 5W). Furthermore, mitotically active Pax7-positive nuclei can be found at the external cell position, concentrating toward the horizontal myosepta, throughout larval, juvenile, and adult stages (Figures 1I–1K; Figure S2; data not shown). Pax7-positive nuclei can also be found localized between myofibers deep within the myotome from 3 days postfertilization (dpf) onward, underneath the basal lamina of individual fibers (Figures 1K; Figure S2). The majority of these cells are mitotically inactive, suggesting that fiber-associated Pax7 cells are quiescent (Figure S2). An identical niche and proliferative behavior is exhibited by mammalian satellite cells, which similarly express and also require Pax7 for their maintenance (Gros et al., 2005Gros J. Manceau M. Thome V. Marcelle C. A common somitic origin for embryonic muscle progenitors and satellite cells.Nature. 2005; 435: 954-958Crossref PubMed Scopus (418) Google Scholar, Oustanina et al., 2004Oustanina S. Hause G. Braun T. Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification.EMBO J. 2004; 23: 3430-3439Crossref PubMed Scopus (358) Google Scholar, Relaix et al., 2005Relaix F. Rocancourt D. Mansouri A. Buckingham M. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells.Nature. 2005; 435: 948-953Crossref PubMed Scopus (748) Google Scholar, Seale et al., 2000Seale P. Sabourin L.A. Girgis-Gabardo A. Mansouri A. Gruss P. Rudnicki M.A. Pax7 is required for the specification of myogenic satellite cells.Cell. 2000; 102: 777-786Abstract Full Text Full Text PDF PubMed Scopus (1501) Google Scholar). The expression of dacD differs from that of the two pax gene orthologs, and this expression is restricted to the ventral/lateral edge of rostral somites (Figure 1U). This region has been shown to contain pectoral fin and hypaxial myoblast precursors, suggesting that the expression of dacD may specifically mark the progenitors of these cells (Neyt et al., 2000Neyt C. Jagla K. Thisse C. Thisse B. Haines L. Currie P.D. Evolutionary origins of vertebrate appendicular muscle.Nature. 2000; 408: 82-86Crossref PubMed Scopus (141) Google Scholar) (Figures 1Q–1U). In support of this notion, both pax3 and a second dac ortholog, dacA, are expressed in migrating pectoral fin and hypaxial muscle precursors (Hammond et al., 2002Hammond K.L. Hill R.E. Whitfield T.T. Currie P.D. Isolation of three zebrafish dachshund homologues and their expression in sensory organs, the central nervous system and pectoral fin buds.Mech. Dev. 2002; 112: 183-189Crossref PubMed Scopus (30) Google Scholar) (Figures 1M–1P). To summarize, the zebrafish orthologs of amniote genes expressed within the dermomyotome, hypaxial and migratory limb muscle precursors and muscle-specific stem cells are initially expressed in the anterior domain of the zebrafish somite. In order to investigate the morphogenetic movements that control formation of the external cell layer, we undertook whole-somite imaging by using the vital fluorophore BODIPY-Ceramide, followed by confocal laser scanning microscopy of the intact cells of the myotome over a time course that encompassed two periods of somite development (Figure 2). The cells of newly segmented somites undergo little, if any, rearrangement relative to their neighbors (Figures 2A–2F). However, by mid-somitogenesis, somitic cells have initiated a set of morphogenetic behaviors that ultimately result in the rotation of the entire somite 90° from its initial position. As a result of this cellular rearrangement, anterior somitic compartment cells come to lie in a lateral external cell position, a process confirmed by lineage tracing of individual anterior somitic compartment cells (Figures 2G–2N; Movie S2). Furthermore, individual labeled cells can rotate at different rates, even when comparing neighboring cells that share an immediate lineage relationship (Figures 2M and 2N). We next followed the fate of individual cells of the anterior somitic compartment, derived from different rostral/caudal levels within the embryo. Anterior somite cells derived from somite 4 migrate to contribute to pectoral fin muscle formation (Figures 3A–3F). Similarly, the anterior cells of somite 5 contribute to the posterior hypaxial muscle (PHM), which we previously showed is derived from the ventral regions of somites 5 and 6 (Haines et al., 2004Haines L. Neyt C. Gautier P. Keenan D.G. Bryson-Richardson R.J. Hollway G.E. Cole N.J. Currie P.D. Met and Hgf signaling controls hypaxial muscle and lateral line development in the zebrafish.Development. 2004; 131: 4857-4869Crossref PubMed Scopus (68) Google Scholar) (Table S1). However, at these somitic levels, and at all other levels examined, a second fate was identified as originating from the anterior somite. Labeled cells migrate laterally to generate large, flat, Pax7-positive cells of the external cell layer ( Figures 3G–3I and 4A–4F; Movies S3A and S3B; Table S1).Figure 4Anterior Somitic Compartment Cells Contribute to the Pax7-Positive External Cell LayerShow full caption(A) Iontophoretic injection of two row 1 cells at the 10-somite stage located within somite 5.(B and C) A total of 24 hr later, at 36 hpf, these cells have migrated laterally and externally to the myotome to form large, flattened cells of the external cell layer. (A and C) Dorsal views; anterior is oriented toward the top. (B) Lateral view; anterior is oriented toward the left.(D–F) Same embryo as in (A)–(C) stained for Pax7-positive nuclei (green) and streptavidin (red) to reveal the Rhodamine/Biotin dextran-injected cell at 36 hpf. Confocal rendering of the external cell layer and the superficial aspect of the myotome (movies of the 3D rendering are provided as Movies S3A and S3B). Coincident Biotin dextran and Pax7 localization (arrows) indicates that anterior somitic cells contribute to the external cell layer.(G–N) Fate mapping extended to 7 days of development. (G) Anterior somitic cells labeled at the 10-somite stage; dorsal view, anterior is oriented toward the top. (H and I) (H) Lateral and (I) dorsal views of the same embryo as (G) at 36 hpf, revealing that the injected cell has rotated to the external cell layer and occupies a superficial position. (J) At 7 days, the injected cell has migrated to a deeper, fiber-adjacent position, revealed by the presence of z-bands of differentiated muscle fibers. Lateral view; anterior is oriented toward the left. (K–M) Single confocal scans of the identical larvae in (G)–(J), fixed at 7 dpf and stained for Pax7-positive nuclei (green) and streptavidin (red) to further reveal the Rhodamine/Biotin dextran-injected cell. Coincident Biotin dextran and Pax7 localization (arrow) indicates that the injected external cell undergoes self-renewal and remains Pax7 positive up to 1 week in development, despite contributing daughter muscle fibers (MF, arrows) to the myotome over this period of time. (N) MFs are evident in single confocal scans deeper in the myotome. (K)–(N) Lateral views; anterior is oriented toward the left, dorsal is oriented toward the top of single confocal scans. The insets in (K)–(M) reveal the colabeled cell at high magnification in a 3D total projection rendering of a z-stack through the entire cell.View Large Image Figure ViewerDownload Hi-res image Download (PPT) (A) Iontophoretic injection of two row 1 cells at the 10-somite stage located within somite 5. (B and C) A total of 24 hr later, at 36 hpf, these cells have migrated laterally and externally to the myotome to form large, flattened cells of the external cell layer. (A and C) Dorsal views; anterior is oriented toward the top. (B) Lateral view; anterior is oriented toward the left. (D–F) Same embryo as in (A)–(C) stained for Pax7-positive nuclei (green) and streptavidin (red) to reveal the Rhodamine/Biotin dextran-injected cell at 36 hpf. Confocal rendering of the external cell layer and the superficial aspect of the myotome (movies of the 3D rendering are provided as Movies S3A and S3B). Coincident Biotin dextran and Pax7 localization (arrows) indicates that anterior somitic cells contribute to the external cell layer. (G–N) Fate mapping extended to 7 days of development. (G) Anterior somitic cells labeled at the 10-somite stage; dorsal view, anterior is oriented toward the top. (H and I) (H) Lateral and (I) dorsal views of the same embryo as (G) at 36 hpf, revealing that the injected cell has rotated to the external cell layer and occupies a superficial position. (J) At 7 days, the injected cell has migrated to a deeper, fiber-adjacent position, revealed by the presence of z-bands of differentiated muscle fibers. Lateral view; anterior is oriented toward the left. (K–M) Single confocal scans of the identical larvae in (G)–(J), fixed at 7 dpf and stained for Pax7-positive nuclei (green) and streptavidin (red) to further reveal the Rhodamine/Biotin dextran-injected cell. Coincident Biotin dextran and Pax7 localization (arrow) indicates that the injected external cell undergoes self-renewal and remains Pax7 positive up to 1 week in development, despite contributing daughter muscle fibers (MF, arrows) to the myotome over this period of time. (N) MFs are evident in single confocal scans deeper in the myotome. (K)–(N) Lateral views; anterior is oriented toward the left, dorsal is oriented toward the top of single confocal scans. The insets in (K)–(M) reveal the colabeled cell at high magnification in a 3D total projection rendering of a z-stack through the entire cell. Fate-mapping strategies extended to later developmental periods also revealed that a subset of the external cell population generates muscle fibers 1 week after cells were initially labeled (Figures 3J–3M and 4G–4N; Table S1). Within lineage-related cell clusters, it is also possible to detect the original undifferentiated cell at the site of muscle fiber generation, an observation suggestive of stem cell self-renewal (Figures 3L and 4K–4N). A subset of the cells of the external cell layer generate larval muscle fibers and transit to fiber-associated positions deeper within the myotome, where they maintain Pax7 expression (Figures 4K–4N). The position of these Pax7-positive cells, medial to the superficial horizontal myosepta-associated external cell layer, suggests that these cells are satellite cells (Figures 1J, 1K, and 4K–4N; Figure S2). The remainder of labeled cells stay undifferentiated within the external cell layer at least 10 days after injection, the latest point at which labeled cells could still be identified. This is consistent with the observation that Pax7-positive external cells are evident within the postlarval myotome, suggesting that they represent a resident progenitor cell population required for muscle growth through the entire life of the fish (Figures 1I and 1J; Figure S2). A third set of labeled anterior somitic cells migrated both dorsally and ventrally to a distinct subepidermal/epidermal-intercalated position consistent with a dermal layer (Figures 3R–3U; Table S1). Anterior somitic compartment cells also contributed to the formation of the dorsal fin when labels were made within somites inclusive and caudal to somite 6 (Figures 3N–3Q; Table S1). Collectively, these results suggest that the anterior somitic cells of rostral somites generate seven distinct fates; external cells, appendicular and hypaxial muscle precursors, muscle progenitor cells that generate fibers during a secondary period of larval muscle growth, satellite cells, dermal cells of the skin, and cells contributing to the dorsal fin. We also examined the fates of anterior somitic compartment cells derived from caudal somitic levels. Anterior somitic cells derived from somites 14–16 of 16-somite-stage embryos do not contribute to hypaxial muscle, although external cells, larval muscle fibers, and dermal and dorsal fin contributions are observed similarly to labels made within anterior somitic cells of rostral somites (Table S1). A distinct fate is derived from anterior cells of caudal somites, superficial embryonic fast twitch muscle fibers, evident 24 hr after labeling (Figures 3V–3Y). These results suggest that at caudal somitic levels, anterior somitic cells contribute to the embryonic growth of the myotome by generating fast twitch muscle fibers after somite rotation, a situation not evident in rostral somitic regions, where progenitors are required to generate hypaxial muscle duri" @default.
• W2039220265 created "2016-06-24" @default.
• W2039220265 creator A5006397040 @default.
• W2039220265 creator A5029395389 @default.
• W2039220265 creator A5035901267 @default.
• W2039220265 creator A5036164082 @default.
• W2039220265 creator A5073121053 @default.
• W2039220265 creator A5085304568 @default.
• W2039220265 date "2007-02-01" @default.
• W2039220265 modified "2023-10-15" @default.
• W2039220265 title "Whole-Somite Rotation Generates Muscle Progenitor Cell Compartments in the Developing Zebrafish Embryo" @default.
• W2039220265 cites W1518124127 @default.
• W2039220265 cites W1522882412 @default.
• W2039220265 cites W1859346747 @default.
• W2039220265 cites W1888475523 @default.
• W2039220265 cites W1967016048 @default.
• W2039220265 cites W1968802624 @default.
• W2039220265 cites W1977911977 @default.
• W2039220265 cites W1985445926 @default.
• W2039220265 cites W1986994638 @default.
• W2039220265 cites W1988060154 @default.
• W2039220265 cites W1988744406 @default.
• W2039220265 cites W1997638149 @default.
• W2039220265 cites W2006254080 @default.
• W2039220265 cites W2008787016 @default.
• W2039220265 cites W2009701699 @default.
• W2039220265 cites W2016278733 @default.
• W2039220265 cites W2023424615 @default.
• W2039220265 cites W2025182546 @default.
• W2039220265 cites W2029914169 @default.
• W2039220265 cites W2034486165 @default.
• W2039220265 cites W2041622114 @default.
• W2039220265 cites W2042601922 @default.
• W2039220265 cites W2045595107 @default.
• W2039220265 cites W2049731453 @default.
• W2039220265 cites W2083457899 @default.
• W2039220265 cites W2083898995 @default.
• W2039220265 cites W2085205835 @default.
• W2039220265 cites W2086756183 @default.
• W2039220265 cites W2087862328 @default.
• W2039220265 cites W2089045623 @default.
• W2039220265 cites W2090486853 @default.
• W2039220265 cites W2095056735 @default.
• W2039220265 cites W2103656923 @default.
• W2039220265 cites W2105669185 @default.
• W2039220265 cites W2106081693 @default.
• W2039220265 cites W2109686700 @default.
• W2039220265 cites W2111629550 @default.
• W2039220265 cites W2118963105 @default.
• W2039220265 cites W2125295969 @default.
• W2039220265 cites W2143025255 @default.
• W2039220265 cites W2143777555 @default.
• W2039220265 cites W2161699162 @default.
• W2039220265 cites W2168842654 @default.
• W2039220265 doi "https://doi.org/10.1016/j.devcel.2007.01.001" @default.
• W2039220265 hasPubMedId "https://pubmed.ncbi.nlm.nih.gov/17276339" @default.
• W2039220265 hasPublicationYear "2007" @default.
• W2039220265 type Work @default.
• W2039220265 sameAs 2039220265 @default.
• W2039220265 citedByCount "163" @default.
• W2039220265 countsByYear W20392202652012 @default.
• W2039220265 countsByYear W20392202652013 @default.
• W2039220265 countsByYear W20392202652014 @default.
• W2039220265 countsByYear W20392202652015 @default.
• W2039220265 countsByYear W20392202652016 @default.
• W2039220265 countsByYear W20392202652017 @default.
• W2039220265 countsByYear W20392202652018 @default.
• W2039220265 countsByYear W20392202652019 @default.
• W2039220265 countsByYear W20392202652020 @default.
• W2039220265 countsByYear W20392202652021 @default.
• W2039220265 countsByYear W20392202652022 @default.
• W2039220265 countsByYear W20392202652023 @default.
• W2039220265 crossrefType "journal-article" @default.
• W2039220265 hasAuthorship W2039220265A5006397040 @default.
• W2039220265 hasAuthorship W2039220265A5029395389 @default.
• W2039220265 hasAuthorship W2039220265A5035901267 @default.
• W2039220265 hasAuthorship W2039220265A5036164082 @default.
• W2039220265 hasAuthorship W2039220265A5073121053 @default.
• W2039220265 hasAuthorship W2039220265A5085304568 @default.
• W2039220265 hasBestOaLocation W20392202651 @default.
• W2039220265 hasConcept C104317684 @default.
• W2039220265 hasConcept C105702510 @default.
• W2039220265 hasConcept C15729860 @default.
• W2039220265 hasConcept C196843134 @default.
• W2039220265 hasConcept C201750760 @default.
• W2039220265 hasConcept C2524010 @default.
• W2039220265 hasConcept C2776878037 @default.
• W2039220265 hasConcept C2779018604 @default.
• W2039220265 hasConcept C28328180 @default.
• W2039220265 hasConcept C33923547 @default.
• W2039220265 hasConcept C54355233 @default.
• W2039220265 hasConcept C74050887 @default.
• W2039220265 hasConcept C86803240 @default.
• W2039220265 hasConcept C87073359 @default.
• W2039220265 hasConcept C95444343 @default.
• W2039220265 hasConceptScore W2039220265C104317684 @default.
• W2039220265 hasConceptScore W2039220265C105702510 @default.
• W2039220265 hasConceptScore W2039220265C15729860 @default.

• next