- Research article
- Open Access
Gene expression profiling of the hyperplastic growth zones of the late trout embryo myotome using laser capture microdissection and microarray analysis
© Rescan et al.; licensee BioMed Central Ltd. 2013
- Received: 20 September 2012
- Accepted: 8 March 2013
- Published: 14 March 2013
A unique feature of fish is that new muscle fibres continue to be produced throughout much of the life cycle; a process termed muscle hyperplasia. In trout, this process begins in the late embryo stage and occurs in both a discrete, continuous layer at the surface of the primary myotome (stratified hyperplasia) and between existing muscle fibres throughout the myotome (mosaic hyperplasia). In post-larval stages, muscle hyperplasia is only of the mosaic type and persists until 40% of the maximum body length is reached. To characterise the genetic basis of myotube neoformation in trout, we combined laser capture microdissection and microarray analysis to compare the transcriptome of hyperplastic regions of the late embryo myotome with that of adult myotomal muscle, which displays only limited hyperplasia.
Gene expression was analysed using Agilent trout oligo microarrays. Our analysis identified more than 6800 transcripts that were significantly up-regulated in the superficial hyperplastic zones of the late embryonic myotome compared to adult myotomal muscle. In addition to Pax3, Pax7 and the fundamental myogenic basic helix-loop-helix regulators, we identified a large set of up-regulated transcriptional factors, including Myc paralogs, members of Hes family and many homeobox-containing transcriptional regulators. Other cell-autonomous regulators overexpressed in hyperplastic zones included a large set of cell surface proteins belonging to the Ig superfamily. Among the secreted molecules found to be overexpressed in hyperplastic areas, we noted growth factors as well as signalling molecules. A novel finding in our study is that many genes that regulate planar cell polarity (PCP) were overexpressed in superficial hyperplastic zones, suggesting that the PCP pathway is involved in the oriented elongation of the neofibres.
The results obtained in this study provide a valuable resource for further analysis of novel genes potentially involved in hyperplastic muscle growth in fish. Ultimately, this study could yield insights into particular genes, pathways or cellular processes that may stimulate muscle regeneration in other vertebrates.
- Muscle growth
- Muscle hyperplasia
- Gene expression
- Laser capture microdissection
In the myotome of teleost fish, new muscle fibres continue to be produced far into adulthood, whereas in mammals postnatal growth depends only on the hypertrophy of muscle fibres that are formed during embryonic development . The post-embryonic formation of muscle fibres in fish generally occurs in two successive phases . In the first phase, which takes place in the late embryo stage and/or in larvae, new fibres are formed at the surface of the primary myotome. This regionalised phase of myogenesis, termed stratified hyperplasia, results from the differentiation of myogenic precursor cells that derive from the dermomyotome-like epithelium that surrounds the myotome [3–6]. In the second phase of neomyogenesis, termed mosaic hyperplasia, new muscle fibres are formed on the surface of existing muscle fibres throughout the entire myotome, producing the typical mosaic appearance observed in a muscle cross section. Mosaic hyperplasia is responsible for the robust increase in muscle mass in larvae and in juveniles . Myogenic precursor cells that underlie the basal lamina of mature muscle fibres power mosaic hyperplasia . These resident quiescent cells, which are the equivalent of mammalian satellite cells, express FoxK1 protein , a member of the forkhead/winged helix family of transcription factors and one of the few known markers of quiescent satellite cells in mammalian muscle . Although it has not been formally demonstrated, it is likely that these satellite cells in fish also originate from the dermomyotome . In most teleost species, the onset of mosaic hyperplasia follows stratified hyperplasia and begins only in the advanced larval stages . In contrast, in trout, mosaic hyperplasia and stratified hyperplasia occur simultaneously, immediately following the differentiation of the embryonic myotome . This mode of growth likely accounts for the intense embryonic body growth observed in salmonids . Little is known about the genetic mechanisms regulating the formation of new myofibres in fish, primarily as a result of the difficulty of accessing the zones of myotube neoformation. In this study we have combined laser capture microdissection  with microarray analysis to compare the transcriptome of hyperplastic subdomains of the late embryo myotome with that of adult myotomal muscle, which displays only limited muscle hyperplasia.
This work used early trout embryos. All experiments performed in this study followed the recommendations of the “Comité National de Reflexion Ethique sur l’Experimentation Animale” of the Ministry of Higher Education and Research and were approved by Local Animal Care and Use Committee (approval n° 7I12).
Animals and sampling
All experiments were performed using rainbow trout Oncorhynchus mykiss (Walbaum). Laser capture microdissection of myotome subdomains was carried out on 19 day-old prehatching trout embryos. RNA extraction of adult myotomal muscle was carried out using three distinct animals from a mixed-sex trout population and weighing approximately 500 grams. The trout were rapidly anaesthetised with phenoxyethanol (Sigma; 4 ml/10 litres fresh water) before sacrificing. A transverse slice of fast muscle situated just beneath the dorsal fin was then sampled and was stored at −80°C prior to RNA extraction using using TRIzol reagent (Invitrogen, Carlsbad, CA).
Selective isolation of superficial and deep domains of the myotome of the late embryo by Laser Capture Microscopy (LCM)
Superficial growth zones under the slow muscle layer and subjacent primary myotome-derived muscle mass were separately isolated using laser capture microdissection. For this purpose, late trout embryos were frozen in liquid nitrogen-cooled isopentane. Ten-micron- thick transverse frozen sections were cut using a cryostat (Leica, Milton Keynes, UK), mounted onto uncoated glass slides, fixed at −20°C in 70% ethanol for 1 min, washed briefly in 70% ethanol and sequentially dehydrated in 100% ethanol and xylene. The sections were then microdissected using a Veritas Laser Capture Microdissection system (LCM) (Arcturus). The infrared laser was used with the following parameters: spot diameter, 20 μm; pulse duration, 3500 ms; power, 90 mW. All areas were selected and collected within 30 min of the preparation of the slide. A total of 20–30 laser-captured area obtained from 2–3 late embryos were pooled for each RNA extraction. Total RNA was isolated using the PicoPureRNA isolation kit (Arcturus) and had an RNA integrity number of 7.5 (Agilent).
Microarray experiments were performed using an Agilent-based microarray platform with 8 × 60 K probes per slide (GEO platform record: GPL15840). This platform, which is based on a rainbow trout resource designed by Salem et al. , has been enriched with oligonucleotides designed using recent NGS data from trout . The microarray gene annotations were reanalysed by Sigenae (Institut National de la Recherche Agronomique, Toulouse, France). Microarray data sets have been submitted to the GEO-NCBI with the accession number GSE40410.
RNA labelling and hybridisation
RNA from (i) four distinct pools of laser-captured superficial area of late trout embryo myotome, (ii) three distinct pools of laser-captured deep area of late trout myotome and (iii) three distinct adult fast muscles were used for labelling and hybridisation. RNA samples were Cy3-labelled according to the manufacturer’s instructions (Agilent). Briefly, RNA was first reverse transcribed, using a polyDT-T7 primer, Cy3 was incorporated by a T7 polymerase-mediated transcription and excess dye was removed using an RNeasy kit (Quiagen). The level of dye incorporation was evaluated using a spectrophotometer (Nanodrop ND1000, LabTech). Labelled RNA was then fragmented in the appropriate buffer (Agilent) for 30 minutes at 60°C before dilution (v/v) in hybridisation buffer. Hybridisations were performed in a microarray hybridisation Oven (Agilent) overnight at 65°C, using two Agilent 8 × 60 K high-density oligonucleotide microarray slides. Following hybridisation, the slides were rinsed in gene expression wash buffers 1 and 2 (Agilent).
Data acquisition and analysis
Hybridised slides were scanned at a 3-μm resolution using an Agilent G2505 microscanner. Data were extracted using the standard procedures contained in the Agilent Feature Extraction (FE) software version 10.7. Arrays were normalised using GeneSpring software. A t-test (p < 0.01) and an average fold change of >3 were used as the criteria for defining genes as differentially expressed between hyperplastic areas of the late embryonic myotome and adult myotomal muscle. For clustering analysis, data were log transformed, median-centred and an average linkage clustering was carried out using CLUSTER software. The results were visualised using TREEVIEW . Biological functions and pathways were generated and analysed using Ingenuity Pathway Analysis software (IPA, Ingenuity Systems, CA).
In situ hybridisation
Recombinant bacterial clones were obtained from the CRB GADIE resource centre (Jouy-en-Josas, France) or the USDA (Washington D.C., USA). Plasmid were extracted and cDNA inserts were amplified by PCR using vector-specific primers. PCR products were purified and used as templates for digoxigenin (DIG)-labeled probe synthesis using the Riboprobe Combination system - T3/T7 RNA polymerase (Promega).
In situ hybridisation experiments were performed in 17 day-old trout embryos. Briefly trout embryos were dechorionated with fine forceps and were fixed overnight at 4°C with paraformaldehyde in phosphate buffered saline (PBS). Specimens were dehydrated and stored in methanol at −20°C. After rehydration in graded methanol-PBS, embryos were processed according to established automated procedures  with minor modifications.
Muscle hyperplasia in the late trout embryo
Gene expression profiling overview
Identifying genes associated with myotube formation
Muscle fibre hyperplasia involves the proliferation, fusion and differentiation of myogenic cells. These events are regulated by an interplay of intrinsic factors and extrinsic signals. Therefore, to further identify candidate genes of specific relevance in the regulation of muscle hyperplasia, we focused on transcripts encoding cell-autonomous (intrinsic) factors such as transcriptional regulators and membrane associated proteins, and on transcripts encoding extrinsic factors such as secreted factors, including growth factors and signalling molecules.
Transcriptional regulators: DNA-binding transcriptional regulators
More than 100 DNA-binding transcriptional regulators were found to be up-regulated in the superficial hyperplastic areas of the late embryonic myotome when compared to adult fast muscle (Additional file 2). Among these factors were well known regulators of muscle-specific transcription such as the paired-box transcription factors, Pax3 and Pax7, which mark immature myogenic cells, and the myogenic bHLH transcription factors such as MyoD (Myod1b and MyoD1c), Myf5, mrf4 and myogenin, which act downstream of the pax3/7 genes to trigger myogenic differentiation (Figure 3A). In addition to these canonical myogenic regulators, we found a large set of genes encoding homeobox motif-containing transcriptional regulators such as members of the meis family (meis1 and meis3), activity-dependent neuroprotector homeobox protein, Lbx1 and ARX (Aristaless-related homeobox gene) (Figure 3B). Several genes found to be up-regulated in our analysis encode transcriptional regulators of the Sox family, such as Sox5, sox8 and sox11. Also were found the winged helix factor Foxc1 as well as Tbx2 and Tbx3 which are members of the T-box DNA binding-containing protein family. Among the transcriptional regulators with zinc finger motifs, we identified Gli2 and snail2, as well as Zic2 and Zic4. A salient feature of the hyperplastic zones was the strong enrichment of genes encoding members of Hairy/enhancer of split (Hes) family proteins such as hairy and enhancer of split 6, as well as Hes-related transcriptional factors including hairy enhancer of split with YRPW motif protein 1 (Hey1) and 2 (Hey2) (Figure 3C). Seven distinct c-Myc paralogs were up-regulated in hyperplastic areas (Figure 3D) along with their associated factor Max and the upstream transcriptional regulators the FUSE binding proteins FUBP1, FUBP2 and FUBP3. Finally, we observed an enrichment for members of the AP-2 family (alpha, alpha-2, epsilon and sigma) in hyperplastic zones.
Transcriptional regulators: epigenetic factors
Signalling environment components and other secreted factors
In situ hybridisation of transcripts up-regulated in laser-captured peripheral hyperplastic domains of the myotome
By taking advantage of laser capture microdissection and microarray technologies we aimed in this study to discover genes that potentially regulate myotube neoformation in fish. Combining these experimental approaches we identified nearly 7000 genes that were up-regulated in superficial growth (hyperplastic) zones of the late trout embryo myotome compared to adult myotomal muscle. In these zones, our transcriptomic analysis revealed the up-regulation of canonical genes known to have a role in controlling myogenesis, such as Pax3, Pax7 and the four bHLH myogenic factors. This observation indicates that muscle hyperplasia depends on the genetic regulatory pathways that regulate the initial (embryonic) myogenesis. The overexpression of the muscle progenitor markers Pax3 and Pax7 is likely the result of undifferentiated dermomyotome-derived myogenic cells, which are transiently stockpiled in the lateral fast muscle before they differentiate into new myofibers (Steinbacher et al., 2008), in the captured material. Along with MRF genes, we observed the up-regulation of Tsh3, ARX, meis1 and the homeodomain containing protein pbx1, all of which have been reported to modulate the activity of MRF during skeletal muscle differentiation [19–22]. Interestingly, we observed the overexpression of a variety of transcriptional regulators for which a function in myogenesis has not been shown or is poorly documented; for example, we noted the up-regulation of seven distinct members of the Myc family. Using in situ hybridisation, we further showed that c-myc transcript is detectable in differentiating myotubes indicating that c-Myc not only regulates cell growth, apoptosis and metabolism as classically reported , but may also activate, at least in myogenic cells, the differentiation machinery. Among the Hes gene family members overexpressed in hyperplastic zones, we found Her6, hey1 and hey2 which are transcribed in the developing primary myotome of zebrafish . In addition, we showed in this study that Hes6 and hairy related-9 transcripts are detectable in superficial hyperplastic zones using in situ hybridisation. In keeping with a possible role for Hes6 in trout muscle hyperplasia, it is worth noting that the microinjection of Hes6 RNA into Xenopus embryos induces an impairment of terminal differentiation and an expansion of the myotome . Sox5 and Sox11 transcripts were also up-regulated in laser-captured samples from the peripheral domain of the myotome. We have recently shown that Sox5 is expressed in myogenic cells from the dermomyotome-like epithelium notably at the level of the dorsal and ventral lips . We report in this study a similar pattern of sox11 expression, indicating that these two genes are transcribed in dermomyotome-derived cells prior their differentiation. In addition to DNA-binding transcriptional regulators, we observed the up-regulation in hyperplasic area of a large set of genes involved in chromatin remodelling. Specifically, we observed the up-regulation of Ezh2, an essential component of the polycomb-repressive complex, which has been recently reported to control self-renewal and preservation of the transcriptional identity of skeletal muscle stem cells . Additionally, we report the overexpression of histone modifying enzymes including protein arginine methyltransferase 4 (PRTM4/CARM1) and 5 (PRTM5), which, in zebrafish, have a major role in controlling MRF expression and proper myogenesis . Among the SWI/SNF chromatin remodelling enzymes overexpressed in our analysis it is worth noting that Brg1/Smarca4 has been shown to alter chromatin structure at myogenic loci facilitating transcription .
Myoblast fusion is required for muscle fibre formation. This step depends on cell-cell contact that is mediated by proteins present at the surface of the myoblats  (Krauss et al., 2005). Among the large set of membrane proteins up-regulated in hyperplastic zones were found many genes encoding Ig-domain containing transmembrane proteins such as Kin of irre 3, Ncam, N-cadherin, M-cadherin and Brother of CDO, all of which are known to influence cell-cell interactions during myoblast differentiation or fusion . Surprisingly, in contrast to M-cadherin, which is expressed in differentiating myoblasts located at the periphery of the expanding myotome , Kin of Irre 3 and brother of CDO were found to be transcribed primarily in the external dermomyotome-like epithelium, similar to what is observed for N-cadherin . This indicates that the transcription of Kin of Irre 3 and brother of CDO takes place early in the myogenic progenitor cells that participate in the second wave of myofibre formation and does not depend on MRF activity. Interestingly, we found that Junctional adhesion molecule Jam2b which is closely related to jam2a (Jam-B) and Jam3b (JAM-C), both critical for myocyte fusion , was also up-regulated along with protogenin which is closely related to the promyogenic transmembrane protein Neogenin . The Ig superfamily members CD 166 and CD 276, which were up-regulated in our microarray, have also been detected at the surface of mouse C2C12 myoblasts , suggesting a role for these two proteins in early myoblast-myoblast interactions. Other membrane proteins that were both up-regulated in superficial hyperplastic zones in our study and that have been detected at the surface of C2C12 cells included cleft lip and palate transmembrane protein1, trophoblast glycoprotein, tissue factor/CD142, Ephrin type A receptor 2, tetraspanin 3 and 4 and fibroblast growth factor 4 (FGFR4) . FGFR4 is highly expressed during chick embryo muscle differentiation  (Marics et al., 2002) and muscle regeneration . Our data further support the involvement of FGFR4 in fish muscle hyperplasia as FGF6, a secreted ligand that binds to FGFR4 , is overexpressed in laser-captured hyperplastic zones. Other secreted factors that may act in an autocrine and/or paracrine manner to regulate muscle hyperplasia included anteriorgradient protein 2 which acts as a growth factor for blastema cells during regeneration of salamander limbs , and Neurotrophin 4, which acts as a regulator of the development, maintenance and regeneration of skeletal muscle fibres . In addition, the expression of both Hepatoma-derived growth factor and Hepatoma-derived growth factor-related protein 2 was up-regulated in hyperplastic zones. Hepatoma derived growth factor is a heparin binding protein that promotes the proliferation, differentiation and migration of various cell types, such as vascular smooth muscle cells .
The Sema3D and sema7A proteins that were up-regulated in our microarray, are also produced by C2C12 differentiating myogenic cells . These secreted proteins were initially identified as regulators of axon guidance  and, subsequently, were shown to participate in myogenic differentiation [42, 43]. Superficial growth zones exhibits high levels of expression of various morphogens or secreted antagonists of morphogens, suggesting that these areas are subjected to complex overlapping morphogenic signals. An example of this from our analysis is the up-regulation of both Gremlin-1 and SFRP2. Gremlin-1 is known to inhibit Tgfβ/BMP activity and thus favours myogenic cell differentiation . However, SFRP2, by inhibiting the myogenic activity of Wnt, is predicted to prevent precocious myogenic differentiation. Interestingly, the expression of Wnt5 and Wnt11 is up-regulated in hyperplastic zones along with the transmembrane receptors frizzled 3 and 7, the protocadherin Fat1, the dishevelled interactor dact1 and the planar cell polarity effectors Vang-like1 and Vang-like2. This suggests that a pathway similar to planar cell polarity , which is notably involved in the oriented elongation of early muscle fibres , may regulate the formation of new muscle fibres at the surface of the trout primary myotome.
In the present study, LCM and microarray analysis were used as tools to characterise the transcriptomal landscape of the superficial growth zones of the early fish myotome. Our data provide a valuable resource for the further characterisation of individual genes, sets of genes and signalling pathways that may control the neoformation of myotubes in fish. In addition, this work serves as a potentially useful source of information for the identification of novel genes that regulate muscle regeneration in vertebrates.
The research leading to these results received funding from the European Community’s Seventh Framework Programme (FP7/2007-2013) under grant agreement no. 222719 - LIFECYCLE, and from the French National Research Agency (ANR 08 GENM 035 01). We would like to thank Cecile Melin and Jean-Luc Thomas for obtaining and rearing the trout embryos.
- Goldspink G: Postembryonic growth and differentiation of striated skeletal muscle. The structure and Function of Muscle. Edited by: Bourne GH. 1972, New York: Academic Press, 179-236.View ArticleGoogle Scholar
- Rowlerson A, Veggetti A: Cellular mechanisms of post-embryonic muscle growth inaquaculture species. Muscle development and growth. Fish Physiology series, Volume 18. Edited by: Johnston IA. 2001, San Diego: Academic Press, 103-140.Google Scholar
- Hollway GE, Bryson-Richardson R, Berger S, Cole NJ, Hall TE, Currie PD: Whole somite rotation generates muscle progenitor cell compartments in the developing embryo. Dev Cell. 2007, 12: 207-219. 10.1016/j.devcel.2007.01.001.View ArticlePubMedGoogle Scholar
- Stellabotte F, Dobbs-McAuliffe B, Fernandez DA, Feng X, Devoto SH: Dynamic somite cell rearrangements lead to distinct waves of myotome growth. Development. 2007, 134: 1253-1257. 10.1242/dev.000067.View ArticlePubMedGoogle Scholar
- Steinbacher P, Stadlmayr V, Marschallinger J, Sänger AM, Stoiber W: Lateral fast muscle fibers originate from the posterior lip of the teleost dermomyotome. Dev Dyn. 2008, 237: 3233-3239. 10.1002/dvdy.21745.PubMed CentralView ArticlePubMedGoogle Scholar
- Marschallinger J, Obermayer A, Sänger AM, Stoiber W, Steinbacher P: Postembryonic fast muscle growth of teleost fish depends upon a nonuniformly distributed population of mitotically active Pax7+ precursor cells. Dev Dyn. 2009, 238: 2442-2448. 10.1002/dvdy.22049.PubMed CentralView ArticlePubMedGoogle Scholar
- Johnston IA, Bower NI, Macqueen DJ: Growth and the regulation of myotomal muscle mass in teleost fish. J Exp Biol. 2011, 214: 1617-1628. 10.1242/jeb.038620.View ArticlePubMedGoogle Scholar
- Koumans JTM, Akster HA: Myogenic cells in development and growth of fish. Comp Biochem Physiol. 1995, 110A: 3-20.View ArticleGoogle Scholar
- Fernandes JM, MacKenzie MG, Kinghorn JR, Johnston IA: FoxK1 splice variants show developmental stage-specific plasticity of expression with temperature in the tiger pufferfish. J Exp Biol. 2007, 210: 3461-3472. 10.1242/jeb.009183.View ArticlePubMedGoogle Scholar
- Garry DJ, Yang Q, Bassel-Duby R, Williams RS: Persistent expression of MNF identifies myogenic stem cells in postnatal muscles. Dev Biol. 1997, 188: 280-294. 10.1006/dbio.1997.8657.View ArticlePubMedGoogle Scholar
- Steinbacher P, Haslett JR, Obermayer A, Marschallinger J, Bauer HC, Sänger AM, Stoiber W: MyoD and Myogenin expression during myogenic phases in brown trout: a precocious onset of mosaic hyperplasia is a prerequisite for fast somatic growth. Dev Dyn. 2007, 236: 1106-1114. 10.1002/dvdy.21103.View ArticlePubMedGoogle Scholar
- Espina V, Wulfkuhle JD, Calvert VS, VanMeter A, Zhou W, Coukos G, Geho DH, Petricoin EF, Liotta LA: Laser-capture microdissection. Nat Protoc. 2006, 1: 586-603. 10.1038/nprot.2006.85.View ArticlePubMedGoogle Scholar
- Salem M, Kenney PB, Rexroad CE, Yao J: Development of a 37 k high-density oligonucleotide microarray: a new tool for functional genome research in rainbow trout. J Fish Biol. 2008, 72: 2187-2206. 10.1111/j.1095-8649.2008.01860.x.View ArticleGoogle Scholar
- Public Sigenae Contig Browser trout. http://www.sigenae.org/,
- Eisen MB, Spellman PT, Brown PO, Botstein D: Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA. 1998, 95: 14863-14868. 10.1073/pnas.95.25.14863.PubMed CentralView ArticlePubMedGoogle Scholar
- Quiring R, Wittbrodt B, Henrich T, Ramialison M, Burgtorf C, Lehrach H, Wittbrodt J: Large-scale expression screening by automated whole-mount in situ hybridization. Mech Dev. 2004, 121: 971-976. 10.1016/j.mod.2004.03.031.View ArticlePubMedGoogle Scholar
- Browseable file containing the supervised clustering of the genes differentially expressed between laser-captured growth zones and adult muscle. http://www.sigenae.org/fileadmin/_temp_/TreeView/overexpressed_in_growth_zone.html,
- Sauvageau M, Sauvageau G: Polycomb group proteins: multi-faceted regulators of somatic stem cells and cancer. Cell Stem Cell. 2010, 7: 299-313. 10.1016/j.stem.2010.08.002.View ArticlePubMedGoogle Scholar
- Faralli H, Martin E, Coré N, Liu QC, Filippi P, Dilworth FJ, Caubit X, Fasano L: Teashirt-3, a novel regulator of muscle differentiation, associates with BRG1-associated factor 57 (BAF57) to inhibit myogenin gene expression. J Biol Chem. 2011, 286: 23498-23510. 10.1074/jbc.M110.206003.PubMed CentralView ArticlePubMedGoogle Scholar
- Biressi S, Messina G, Collombat P, Tagliafico E, Monteverde S, Benedetti L, Cusella De Angelis MG, Mansouri A, Ferrari S, Tajbakhsh S, Broccoli V, Cossu G: The homeobox gene Arx is a novel positive regulator of embryonic myogenesis. Cell Death Differ. 2008, 15: 94-104. 10.1038/sj.cdd.4402230.View ArticlePubMedGoogle Scholar
- Heidt AB, Rojas A, Harris IS, Black BL: Determinants of myogenic specificity within MyoD are required for noncanonical E box binding. Mol Cell Biol. 2007, 27: 5910-5920. 10.1128/MCB.01700-06.PubMed CentralView ArticlePubMedGoogle Scholar
- de la Serna IL, Ohkawa Y, Berkes CA, Bergstrom DA, Dacwag CS, Tapscott SJ, Imbalzano AN: MyoD targets chromatin remodeling complexes to the myogenin locus prior to forming a stable DNA-bound complex. Mol Cell Biol. 2005, 25: 3997-4009. 10.1128/MCB.25.10.3997-4009.2005.PubMed CentralView ArticlePubMedGoogle Scholar
- Dang CV: c-Myc target genes involved in cell growth, apoptosis, and metabolism. Mol Cell Biol. 1999, 19: 1-11.PubMed CentralView ArticlePubMedGoogle Scholar
- Thisse B, Thisse C: Fast Release Clones: A High Throughput Expression Analysis. 2004, ZFIN Direct Data Submission, http://zfin.org,Google Scholar
- Cossins J, Vernon AE, Zhang Y, Philpott A, Jones PH: Hes6 regulates myogenic differentiation. Development. 2002, 129: 2195-2207.PubMedGoogle Scholar
- Rescan PY, Ralliere C: A Sox5 gene is expressed in the myogenic lineage during trout embryonic development. Int J Dev Biol. 2010, 54: 913-918. 10.1387/ijdb.092893pr.View ArticlePubMedGoogle Scholar
- Juan AH, Derfoul A, Feng X, Ryall JG, Dell’Orso S, Pasut A, Zare H, Simone JM, Rudnicki MA, Sartorelli V: Polycomb EZH2 controls self-renewal and safeguards the transcriptional identity of skeletal muscle stem cells. Genes Dev. 2011, 25: 789-794. 10.1101/gad.2027911.PubMed CentralView ArticlePubMedGoogle Scholar
- Batut J, Duboé C, Vandel L: The methyltransferases PRMT4/CARM1 and PRMT5 control differentially myogenesis in zebrafish. PLoS One. 2011, 6: e25427-10.1371/journal.pone.0025427.PubMed CentralView ArticlePubMedGoogle Scholar
- Ohkawa Y, Yoshimura S, Higashi C, Marfella CG, Dacwag CS, Tachibana T, Imbalzano AN: Myogenin and the SWI/SNF ATPase Brg1 maintain myogenic gene expression at different stages of skeletal myogenesis. J Biol Chem. 2007, 282: 6564-6570.View ArticlePubMedGoogle Scholar
- Krauss RS, Cole F, Gaio U, Takaesu G, Zhang W, Kang JS: Close encounters: regulation of vertebrate skeletal myogenesis by cell-cell contact. J Cell Sci. 2005, 118: 2355-2362. 10.1242/jcs.02397.View ArticlePubMedGoogle Scholar
- Rescan PY, Ralliere C, Lebret V: N-cadherin and M-cadherin are sequentially expressed in myoblast populations contributing to the first and second waves of myogenesis in the trout (Oncorhynchus mykiss). J Exp Zool B Mol Dev Evol. 2012, 318: 71-77.View ArticlePubMedGoogle Scholar
- Powell GT, Wright GJ: Jamb and jamc are essential for vertebrate myocyte fusion. PLoS Biol. 2011, 12: e1001216-View ArticleGoogle Scholar
- Gundry RL, Raginski K, Tarasova Y, Tchernyshyov I, Bausch-Fluck D, Elliott ST, Boheler KR, Van Eyk JE, Wollscheid B: The mouse C2C12 myoblast cell surface N-linked glycoproteome: identification, glycosite occupancy, and membrane orientation. Mol Cell Proteomics. 2009, 8: 2555-2569. 10.1074/mcp.M900195-MCP200.PubMed CentralView ArticlePubMedGoogle Scholar
- Marics I, Padilla F, Guillemot JF, Scaal M, Marcelle C: FGFR4 signaling is a necessary step in limb muscle differentiation. Development. 2002, 129: 4559-4569.PubMedGoogle Scholar
- Zhao P, Hoffman EP: Embryonic myogenesis pathways in muscle regeneration. Dev Dyn. 2004, 229: 380-392. 10.1002/dvdy.10457.View ArticlePubMedGoogle Scholar
- Armand AS, Laziz I, Chanoine C: FGF6 in myogenesis. Biochim Biophys Acta. 2006, 1763: 773-778. 10.1016/j.bbamcr.2006.06.005.View ArticlePubMedGoogle Scholar
- Kumar A, Godwin JW, Gates PB, Garza-Garcia AA, Brockes JP: Molecular Basis for the Nerve Dependence of Limb Regeneration in an Adult Vertebrate. Science. 2007, 318: 772-778. 10.1126/science.1147710.PubMed CentralView ArticlePubMedGoogle Scholar
- Sakuma K, Yamaguchi A: The recent understanding of the neurotrophin’s role in skeletal muscle adaptation. J Biomed Biotechnol. 2011, 2011: 201696-PubMed CentralView ArticlePubMedGoogle Scholar
- Everett AD, Stoops T, McNamara CA: Nuclear targeting is required for hepatoma-derived growth factor-stimulated mitogenesis in vascular smooth muscle cells. J Biol Chem. 2001, 276: 37564-37578. 10.1074/jbc.M105109200.View ArticlePubMedGoogle Scholar
- Henningsen J, Rigbolt KT, Blagoev B, Pedersen BK, Kratchmarova I: Dynamics of the skeletal muscle secretome during myoblast differentiation. Mol Cell Proteomics. 2010, 9: 2482-2496. 10.1074/mcp.M110.002113.PubMed CentralView ArticlePubMedGoogle Scholar
- de Wit J, Verhaagen J: Role of semaphorins in the adult nervous system. Prog Neurobiol. 2003, 71: 249-267. 10.1016/j.pneurobio.2003.06.001.View ArticlePubMedGoogle Scholar
- Wu H, Wang X, Liu S, Wu Y, Zhao T, Chen X, Zhu L, Wu Y, Ding X, Peng X, Yuan J, Wang X, Fan W, Fan M: Sema4C participates in myogenic differentiation in vivo and in vitro through the p38 MAPK pathway. Eur J Cell Biol. 2007, 86: 331-344. 10.1016/j.ejcb.2007.03.002.View ArticlePubMedGoogle Scholar
- Tatsumi R, Sankoda Y, Anderson JE, Sato Y, Mizunoya W, Shimizu N, Suzuki T, Yamada M, Rhoads RP, Ikeuchi Y, Allen RE: Possible implication of satellite cells in regenerative motoneuritogenesis: HGF upregulates neural chemorepellent Sema3A during myogenic differentiation. Am J Physiol Cell Physiol. 2009, 297: C238-C252. 10.1152/ajpcell.00161.2009.View ArticlePubMedGoogle Scholar
- Kollias HD, McDermott JC: Transforming growth factor-beta and myostatin signaling in skeletal muscle. J Appl Physiol. 2008, 104: 579-587.View ArticlePubMedGoogle Scholar
- Torban E, Kor C, Gros P: Van Gogh-like2 (Strabismus) and its role in planar cell polarity and convergent extension in vertebrates. Trends Genet. 2004, 20: 570-577. 10.1016/j.tig.2004.09.003.View ArticlePubMedGoogle Scholar
- Gros J, Serralbo O, Marcelle C: WNT11 acts as a directional cue to organize the elongation of early muscle fibres. Nature. 2009, 457: 589-593. 10.1038/nature07564.View ArticlePubMedGoogle Scholar
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