- Research article
- Open Access
The chemokine Sdf-1 and its receptor Cxcr4 are required for formation of muscle in zebrafish
© Chong et al; licensee BioMed Central Ltd. 2007
- Received: 28 December 2006
- Accepted: 22 May 2007
- Published: 22 May 2007
During development cell migration takes place prior to differentiation of many cell types. The chemokine receptor Cxcr4 and its ligand Sdf1 are implicated in migration of several cell lineages, including appendicular muscles.
We dissected the role of sdf1-cxcr4 during skeletal myogenesis. We demonstrated that the receptor cxcr4a is expressed in the medial-anterior part of somites, suggesting that chemokine signaling plays a role in this region of the somite. Previous reports emphasized co-operation of Sdf1a and Cxcr4b. We found that during early myogenesis Sdf1a co-operates with the second Cxcr4 of zebrafish – Cxcr4a resulting in the commitment of myoblast to form fast muscle. Disrupting this chemokine signal caused a reduction in myoD and myf5 expression and fast fiber formation. In addition, we showed that a dimerization partner of MyoD and Myf5, E12, positively regulates transcription of cxcr4a and sdf1a in contrast to that of Sonic hedgehog, which inhibited these genes through induction of expression of id2.
We revealed a regulatory feedback mechanism between cxcr4a-sdf1a and genes encoding myogenic regulatory factors, which is involved in differentiation of fast myofibers. This demonstrated a role of chemokine signaling during development of skeletal muscles.
- Additional Figure
- Slow Muscle
- Fast Muscle
- bHLH Protein
- Fast Fiber
Several cell movements are associated with somitogenesis, including the convergence of lateral mesodermal cells into presomitic mesoderm and later its segmentation. During somite epithelialization two types of cells are formed – epithelial border cells and inner mesenchymal cells. As somite matures, presumptive muscle cells start to express characteristic muscle-specific proteins (MSP) and elongate either actively or through fusion to form myofibrils [1–13]. The border cells undergo migration/rearrangement of their position . The fast muscle cell elongation is triggered by migration of slow muscle cells , which in turn is dependent upon Hedgehog (Hh) signaling [15–23]. A high level of Hh induces Engrailed-expressing muscle pioneers, a subset of slow muscle cells located at the horizontal myoseptum, and a small subset of fast fibers, the Engrailed-expressing medial fast fibers. A low level Hh induces superficial slow fibers, which precursors migrate from their initial position adjacent to the notochord laterally through the paraxial mesoderm and become the most superficial muscle fibers [4, 24]. Specification of most fast muscle in zebrafish does not show obvious signs of lineage-specific cell migration besides being involved in more general events of convergence, mesenchyme-to-epithelial transition (MET) during somite epithelialization followed later on by cell elongation during formation of myofibrils. The fast myofibrils differentiate specifically from the lateral aspect of somites and this process involves relatively short distance migration of prospective myoblasts. These cells express a subset of genes linked to cell migration and at certain A-P levels are capable of undergoing epithelial-mesenchymal transition (EMT), migrate and establish appendicular muscles [reviewed in [25, 26]].
Chemokine receptors are members of the superfamily of seven-transmembrane domain, G-protein coupled receptors. The CXC chemokine receptor CXCR4 [27, 28] is used by HIV-1 for binding to the cell membrane [27, 29–31]. SDF-1α [chemokine (C-X-C motif) ligand 12; zebrafish gene nomenclature committee] and its receptor CXCR4 [chemokine (C-X-C motif) receptor 4; zebrafish gene nomenclature committee] bind only each other [32–35]. Importantly, a study of the expression of SDF-1α/CXCR4 in the mouse embryo demonstrated expression of CXCR4 in the presomites . The knockout SDF-1α and CXCR4-mice are the only known chemokine/chemokine receptor mutants that display embryonic lethality . They demonstrate defects of cell migration during formation of the neural tube and heart [38, 39]. The Sdf1-Cxcr4 interaction also plays a role during the chemotaxis of primordial germ cells in zebrafish in mice [40–42], and sensory cells in zebrafish [43–47].
Our previous study demonstrated that the zebrafish Cxcr4 is encoded by two related genes expressed in a complex pattern, including somites . Later on, it was shown that homologous genes are expressed in human muscle satellite cells and play a role in cell migration during tongue and limb myogenesis in mice [49–51]. While this suggests a role for Cxcr4 in late myogenesis, a role of Cxcr4 in early somitogenesis still remains to be elucidated. Since the zebrafish mutant of cxcr4b – ody does not show obvious defects in myogenesis , we analyzed the second receptor – cxcr4a.
Prior to segmentation in zebrafish, myoblasts initiate expression of myogenic regulatory factors (MRFs)  important for skeletal muscle commitment and myotube formation . The highly related bHLH proteins MyoD, Myf5, Myogenin and Mrf4 have a pivotal function in muscle cell specification and differentiation [53–57]. They share a common dimerization domain and DNA binding domain (DBD), the basic helix-loop-helix (bHLH) motif. MRFs regulate myogenesis after forming heterodimers with ubiquitous E proteins. These bind to E box, with core consensus sequence of CANNTG, in the promoter of target genes . How these proteins initiate the program of muscle cell differentiation remains to be deciphered explicitly. Recently, MyoD was shown to have repressive activity in presence of other cofactors .
In this report, we described the involvement of Cxcr4a and Sdf1a during formation of fast muscles in zebrafish and provided in vivo evidence of a role of cxcr4a-sdf1a in the regulation of MRFs during myogenic determination. The lack of Cxcr4a-Sdf1a-mediated signaling leads to reduction in expression of somitic markers and decrease in fast myofibrils. The lack of Cxcr4a-Sdf1a also affects migration of slow muscle. This effect could be indirect. In addition, we show that E12 and MyoD-Myf5 regulate cxcr4a. This suggested a possible feedback loop between cxcr4a-sdf1a axis and myoD/myf5. In addition, we discovered that ectopic Hh represses transcription of cxcr4a and sdf1a through a negative regulator of cell differentiation Id2. Taken together, our data connect MRFs and chemokines in a regulatory relationship during early myogenesis.
cxcr4a and sdf1aare expressed in a dynamic manner during formation of fast muscles
Since SDF-1α is the only known ligand of CXCR4 [32, 34], we examined the expression pattern of the two zebrafish sdf1genes. Both sdf1a and sdf1b are expressed maternally (Figure 1L; Additional Figure A1H (see Additional file 1)). The level of sdf1a transcript increases rapidly from the onset of mid-blastula transition (MBT). In contrast, the level of sdf1b transcript increases from fertilization.
During early somitogenesis sdf1a is expressed in the lateral somitic mesoderm (Figure 1E). Later, sdf1a expression is restricted mainly to the posterior part of somite. However, in the anterior most three somites, sdf1a transcripts cover almost the entire somite (Figure 1D). At mid-somitogenesis, only the posterior somites express sdf1a (Figure 1H). During late segmentation the forming and newly-formed somites express sdf1a at low level (Figure 1I). By 24 h, sdf1a expression is no longer detected by WISH (data not shown).
The expression level of sdf1b in the somites is low (Additional Figure A1D (see Additional file 1)). It is first observed in the adaxial cells and later become restricted to the posterior part of somite similar to that of sdf1a. By mid-somitogenesis, sdf1b transcripts are restricted to the dorsal and ventral parts of somites (Additional Figures A1D-G (see Additional file 1)).
To define how cxcr4 or sdf1are expressed in respect to other markers, we used the two-color WISH. The expression pattern of both cxcr4a and cxcr4b overlaps almost entirely with that of myoD in the forming somite and a few posterior-most somites (cxcr4a), but in more mature somites both cxcr4s are expressed in the anterior part of somite and myoD in the posterior part (Figure 1C; Additional Figure A1C (see Additional file 1)). In contrast to cxcr4a, expression pattern of sdf1a overlaps completely with that of myoD (Figures 1F–G). The expression patterns of cxcr4a and sdf1a are summarized in a diagram (Figures 1J–K). Therefore, cxcr4a and cxcr4b are co-expressed with sdf1a in the forming and newly formed somites, but not in more mature somites. This suggests that the chemokine and its receptor may have both early and late function during myogenesis.
cxcr4a and sdf1afunction is required for formation of fast muscles
Based on the fact that cxcr4 is expressed during early somitogenesis, we hypothesized that deficiency of Cxcr4 or Sdf1 might affect early myogenesis. To test our hypothesis, we examined somite defects in the mutant ody-/-, which represents a loss of function of Cxcr4b . There was no obvious somitic defect in ody-/- (Additional Figures A2A-D (see Additional file 2)). This could be due to redundancy of cxcr4b and cxcr4a (Additional Figures A2E-J (see Additional file 2)) . We therefore concentrated our study on Cxcr4a.
Next we decided to evaluate which of the two ligands, Sdf1a or Sdf1b, co-operates with Cxcr4a during myogenesis. In Sdf1a morphants expression of myoD and myf5 was down-regulated in somites (Figures 2D, H). In contrast, overall expression of myoD and myf5 was unaffected in Sdf1b morphants even although in some of them somites were slightly elongated (data not shown). Furthermore, we designed sdf1a-EI-MO which targets the second intron of sdf1a causing missplicing of sdf1a transcripts as confirmed by electrophoresis and sequencing (Additional Figure A4B (see Additional file 4) and data not shown). The phenotype of sdf1a-EI-MO morphants is similar to that of 5'UTR-sdf1a morphants. In addition, expression of genes encoding myosin light chain (mylz2) and myosin heavy chain (myhz1) decreased in cxcr4a and sdf1a morphants (Figures 2J–K), whereas expression of the early myocyte marker pax7 was relatively normal (data not shown). Taken together, these experiments showed that knockdown of Sdf1a causes reduction in myoD and myf5 transcription, a phenomenon similar to that of Cxcr4a knockdown. Thus, sdf1a is necessary for early myogenesis.
Loss of cxc4a and sdf1afunction affects slow muscle migration
myoD and myf5 are required co-operatively for the expression of cxcr4a and sdf1a
In mammals, the primary MRFs, Myf5 and MyoD, are involved in both myoblast specification and differentiation . The early expression of cxcr4a or sdf1a correlates with that of myoD or myf5. Therefore, we speculated that the knockdown of MyoD or Myf5 could cause a change in cxcr4a/sdf1a transcription. Neither injection of the two different myoD MO designed against distinct regions at 5'-UTR nor the splice site MO against the first intron of myoD (myoD-EI-MO), which effectively inhibits splicing of myoD (Additional Figures A4C-F (see Additional file 4)) caused significant changes in transcription of cxcr4a and sdf1a (data not shown).
myoD and myf5 positively regulate cxcr4atranscription
The negative HLH proteins Id1-4 compete with the positive bHLH factors for dimerization with E12 and E47 by forming inactive dimers. This results in inhibition of transcription of genes – targets of positive MRFs [63, 64]. Overexpression of id2  in a one-sided fashion resulted in the downregulation of cxcr4a or sdf1a transcription (Figures 6F, F', O, P–P"'). Taken together, these data suggest that myoD or myf5 act in parallel with their co-factors to regulate transcription of cxcr4a or sdf1a.
We have demonstrated that expression of chemokine receptor Cxcr4a and its ligand Sdf1a in paraxial mesoderm is required during formation of fast muscles. This defines a much earlier role for these molecules in myogenesis comparing to that described in previous reports on the migration of progenitors of the appendicular muscles [25, 51, 72]. In the gain-of-function (GOF) experiments, based on implantation of SDF1-containing beads into chick limb, the down-regulation of MyoD expression has been observed . Such an outcome differs from that in our observations. This conflict probably demonstrates that an outcome of SDF1 signaling could be the context- and/or concentration-dependent as implied earlier . Furthermore, the different methodological approaches have been used to collect data. We relied on the loss-of-function (LOF) approach, which similar to recent experiments with SDF1 inhibitor  demonstrated a positive regulatory role of SDF1-Cxcr4 axis upstream of MyoD. Taken together, results of LOF experiments in chick  and our results in zebrafish support the positive regulatory role of Cxcr4-Sdf1 upstream of MRFs during commitment of fast myocytes.
Functional differences within pairs of Sdf1s and Cxcr4s
Our data show that the both pairs of genes encoding Sdf1 and Cxcr4 have overlapping expression in somites. Neither cxcr4b nor sdf1b MO alone have obvious effect on formation of fast muscles. There are no defects in this tissue in ody mutant. Thus, it appears that Cxcr4a-Sdf1a axis alone is fully capable of supporting fast myogenesis, whereas Cxcr4b or Sdf1b perhaps can only partially compensate for the loss of this activity.
Cxcr4a-Sdf1a signaling during myogenesis
Both CXCR4 and SDF1 knockout mice exhibit a complex phenotype [74, 75]. Despite the fact that they have been available for analysis for a long time, no defects in trunk muscles were detected . Perhaps potential abnormalities in this tissue are too subtle compared to a plethora of more obvious defects elsewhere. Alternatively, an apparent change in regulatory machinery of Cxcr4 and Sdf1 expression between fish and mice, with respect to these proteins in fast muscle development of fish, could explain the differences that we have detected.
We never observed a complete absence of fast fibers in morphants. This could be due to other factors such as an incomplete knockdown or activity of paralogous genes, cxcr4b and sdf1b, which might partially compensate for the reduction of function of Cxcr4a and Sdf1a. Our data suggest that Cxcr4a-Sdf1a signaling plays no role in tailbud mesoderm and starts to become necessary just before formation of somite border. It has been proposed that Cxcr4b in the lateral line primordium is involved in coordination of internal cell movement . Similarly, Cxcr4a-Sdf1a could be instrumental in coordinating a short distance movement of fast myocytes.
cxcr4a and sdf1a are not expressed in the adaxial cells and these cells express myoD and myf5 normally in the cxcr4a or sdf1a morphants. Thus, the defect of slow myofibrils observed in these morphants is likely an indirect one. It could be caused by abnormality of fast myocytes. This is in line with earlier data suggesting that migration of slow myocytes depends on fast myocytes .
Cxcr4a-Sdf1a and regulation of MRFs expression
The early expression pattern of sdf1a-cxcr4a in somites is very similar to that of myoD and myf5, but later on cxcr4a expression becomes restricted to the less differentiated anterior part of somite in contrast to MRFs expressed in the posterior more differentiated part of somite. This suggested that developmental events involving Cxcr4 precede induction of expression of myoD-myf5. Indeed, our functional analysis illustrated a requirement of Cxcr4 for regulation of expression of MRFs. Thus activation of MRFs expression by sdf1a-cxcr4a signaling during fast myogenesis occurs concurrently with the process of somite epithelialization and may play a role during this process.
MRFs positively regulate expression of cxcr4a and sdf1a
Until now there has been little evidence that MRFs could regulate expression of components of chemokine signaling [76, 77]. Here for a first time we provided evidence that MRFs regulate transcription of cxcr4a and sdf1a. At the same time our results are consistent with previous reports that the MRFs are partially redundant as myogenic determinants . And yet the double MyoD-Myf5 knockdown caused only partial reduction in the expression of cxcr4a and sdf1a. Perhaps some other regulatory factors such as Myocyte Enhancer Factor 2 (MEF2) act in parallel . Alternatively, these data reflect an incomplete knockdown of MyoD-Myf5.
To act, MRFs form a dimer with E12 and E47, which are products of alternative splicing of E2A transcripts. They belong to a distinct class of ubiquitously expressed bHLH proteins of the E-protein family. The MRF/E protein heterodimers bind to a conserved DNA sequence, CANNTG, also known as the E-box, located in regulatory regions of many muscle-specific genes [80–82]. The promoter region of human CXCR4 contains an E-box sequence . Similarly, we found two E-boxes in close proximity within a 2 kb stretch of cxcr4a 5'-untranslated region (our unpublished data). The upstream regulatory sequences of many muscle-specific genes, including MLC1/3 , acetylcholine receptor alpha , MCK  and myoD , contain multiple E-box sites. In general, at least two E-box sites are required for the activation of these genes by the MRFs [88, 89]. These results support an idea that MRFs could directly regulate expression of cxcr4.
Feedback loop between Cxcr4-Sdf1 and MRFs
The expression pattern of Sdf1 genes overlaps with that of MRFs. Since Sdf1a expressed in the posterior part of somite probably interacts with Cxcr4a expressed in the anterior part of somite, this provides a missing link to complete the feedback regulation loop between Cxcr4-MRFs-Sdf1 that could be operating to link cascades of genes involved in chemokine signaling and myogenic differentiation. However, further investigation will be needed to understand the biochemical interactions.
In summary, our analysis of the developmental role of zebrafish Cxcr4-Sdf1 has led to the identification of the ligand-receptor pair essential for development of trunk muscles. This reveals a novel role of Sdf1-Cxcr4 in differentiation of fast myocytes of the trunk. Thus the chemokine signaling mediated by Sdf1-Cxcr4 emerged as an important regulatory pathway involved in myogenesis.
Zebrafish strains and maintenance
Adult zebrafish (Danio rerio) was maintained at 28.5°C as described . The zebrafish AB line (ZIRC) was used as a wild-type fish. The odysseus (odyJ10049/cxcr4b) mutants and myosin light chain 2 (mylz2-GFP) transgenics were described [6, 41]. Pigment formation was blocked with 1-phenyl-2-thiourea (PTU) .
Whole mount in situ hybridization (WISH) and immunohistochemistry
WISH was performed using single-stranded RNA probes labeled with digoxigenin-UTP or fluorescein-UTP (Boehringer Mannheim, Germany) by established protocol. The zebrafish probes cxcr4a, cxcr4b , myoD , myf5 [17, 91], myhz1 and mylz2  have been described previously. Full-length sdf1a and sdf1b cDNA were obtained by RT-PCR using total RNA and primers designed based on sequence of the EST clones (BM184435 and BM070896), respectively. F59 Mab (1:25)  and secondary goat anti-mouse IgG antibody – Alexa Fluor 488 (1:1000; Molecular Probes, USA) was used to detect slow myosin heavy chain.
Total RNA was isolated from 14 h embryos using RNeasy® Mini Kit (Qiagen, Germany). cDNA for reverse transcription (RT)-PCR analysis was synthesized using Qiagen® OneStep RT-PCR kit (Qiagen, Germany) and Peltier Thermal Cycler – 200 (MJ Research, USA) according to the manufacturer's instructions. For mRNA splicing analysis, 25 ng of total RNA samples treated with DNAse I was used. RT-PCR conditions were as follows: Reverse transcription 50°C, 30 mins; PCR activation step 95°C, 15 mins; Denaturation 94°C, 1 min; Annealing 59°C, 1 min; Extension 72°C, 1 min; Cycles from Denaturation to Extension were repeated 39 times; Final Extension 72°C, 15 mins. 10 μl of RT-PCR products were loaded into each well for gel-electrophoresis. The sequences of primers for introns of sdf1a, myoD, myf5 and e12 were as follows: Forward sdf1a-2EI-F 5' ACA GTC AAC ACA GTC CCA CAG 3'; Reverse sdf1a-2EI-R 5' GTT GAT GGC GTT CTT CAG GTA 3'; Forward myoD-1EI-F 5' CTG AGC AAG GTC AAC GAC GCT 3'; Reverse myoD-1EI-R 5' TGA AGT AAG AGC TGT CAT AGC TG 3'; Forward myf5-1EI-F 5' GCA CTA CGC CGC TGC ACC T 3'; Reverse myf5-1EI-R 5' GCG TCA AAG TTG TAG CTA TTC C 3'; Forward EF1aphaF900 5' CGC CCC TGC CAA TGT AAC CA 3'; Reverse EF1alphaR1388 5' TTG CCA GCA CCA CCG ATT TTC 3'.
Morpholino (MO) Injections
MOs were obtained from Gene Tools, LLC (USA). The antisense sequences were designed to bind to the 5'UTR region including the initiation methionine or sequence between exon-intron (EI) junctions. To minimize the possibility of non-specific effects, we designed and used at least two MOs targeting non-overlapping sequences for each gene. MO sequences were as follows: Cr4a-1-MO 5' ATA AGC CAT CTC TAA AAG ACT TCT C 3'; Cr4a-2-MO 5' GAC TTC TCC CGT TCC TTC AGT CTC C 3'; Cr4a-3-MO 5' ACA GTT TAA ATA CCT CTC TCG CGC G 3'; mCr4a-1-MO 5' ATA AAC CAT ATC TAA GAG ACGTCT C3'; S1a-1-MO 5' TGC AGT GTG AAG AAG AGA TCC GCA C3'; S1a-2-MO 5' TTG AGA TCC ATG TTT GCA GTG TGA A3' ; S1a-3-MO 5' ATC ACT TTG AGA TCC ATG TTT GCA 3' ; mS1a-2-MO 5' TTAAGA TAC ATG TTT GAA GTG TAA A3'; S1a-EI-MO 5' GTG CAG ATA CTC ACA TGA CTT GGA A 3'; myoD-1-MO 5' TGC GAT AAC AAG GGG GCG TGA TTT T 3'; myoD-2-MO 5' GTA AGA CAA AGT CCT TCA GAT CCC G 3'; myoD-EI-MO 5' GTT TCT CACCAT GCC ATC AGA GCA G 3'; myf5-EI-MO 5' GTC ATA TTT ACC ATG CTC TCT GAG C3'; e12-1EI-MO 5' GAA AAC ACA CCG GCC ACA TTA GAA G 3'; e12-3EI-MO 5' TTC ACA CTC ACC AGG CCC GGC AGA C 3'; UMO or control MO 5' CCT CTT ACC TCA GTT ACA ATT TAT A 3' . Bold letters either represent base change or region in intron. MOs were diluted using 1× Danieau's solution to 1 mM stock solution or to proper concentration for injection (0.46–1.5 ρmole) and injected into the yolk stream of 1–2 cell stage embryos using a nanoinjecter (WPI, USA). Since several MO give the same results only representative morphants were photographed.
Expression constructs and RNA
cxcr4a (AY057095), cxcr4b (AY057094), sdf1a (BM184435), sdf1b (BM070896), myoD (Z36945), myf5 (AF270789), and id2 (DQ186992) were all cloned into PCRscript (Clontech). Primers used for cloning: Forward cxcr4a (F) 5' ATG GCT TAT TAC GAA CAC ATC GT 3'; Reverse cxcr4a (R) 5' TTA ACT AGA GTG AAA GCT TGA GAT 3'; Forward cxcr4b (F) 5' ATG GAA TTT TAC GAT AGC ATC 3'; Reverse cxcr4b (R) 5' CTA ACT CGT CAG TGC ACT GGA 3'; Forward sdf1a (F) 5' ATG GAT CTC AAA GTG ATC GT 3'; Reverse sdf1a (R) 5' TTA GAC CTG CTG CTG TTG GGC 3'; Forward sdf1b (F) 5' ATG GAT AGC AAA GTA GTA GCG C 3'; Reverse sdf1b (R) 5' TTA CTC TGA GCG TTT CTT CTT TAT 3'; Forward myoD (F) 5' ATG GAG TTG TCG GAT ATC CCC 3'; Reverse myoD (R) 5' GCA CTT GAT AAA TGG TTT CC 3'; Forward myf5 (F) 5' ATG GAC GTA TTC TCC ACA TC 3'; Reverse myf5 (R) 5' TCA CAG TAC GTG GTA AAC TGG T 3'; Forward id2 (F) 5' ATG AAG GCA ATA AGC CCA GTG A 3'; Reverse id2 (R) 5' TTA ACG GTA AAG TGT CCT GCT G 3'. For microinjection of mRNA, constructs were linearized with Sac II and capped mRNA was synthesized by in vitro transcription with T7 RNA polymerase using mMessage mMachine kit (Ambion, USA). Poly-A was added using poly-A polymerase (GE Healthcare, UK). E12 expression construct was provided by Dr. J. Campos-Ortega. Zebrafish sonic hedgehog (Shh) and PKI RNA were transcribed from plasmid pPSP64T-zfshh and pPSP64T-PKI provided by Dr. M. Hammerschmidt. The RNA (100 ρg) was co-injected into the yolk of 1–2-cell stage embryos with lysine fixable Fluorescein Dextran or Texas Red (70 kDa, Molecular Probes, USA).
Cryosectioning and photography
Cryosectioning of embryos was described . Some sections were stained with 1.5 ml of diluted 3.5 μM DAPI (4', 6-diamidine-2-phenylidole-dihydrochloride) for 20 min and washed in PBS 2× 20 min. Axiophot 2 compound microscope or laser scanning confocal microscope LSM 510 (Zeiss, Germany) with software supplied by the manufacturers or AX70 (Olympus, Japan) were used for photography. For image processing Adobe® Photoshop 5.5 and measuring of relative intensities Image-Pro® Plus 4.5.1 software was used.
For analysis of birefringency of the axial skeletal muscle the Olympus Light dissecting microscope equipped with polarizer (Olympus, Japan) was used as described . A plane of polarization was standard in all analysis.
Embryos were processed using standard protocols , embedded in 100% spurr resin and polymerized at 65°C overnight. Ultra-thin sections were cut on a Reichert-Jung ultramicrotome (Germany) and examined under the transmission electron microscope JEM1010 (JEOL, Japan) at 100 kV.
We thank Drs. Philip Ingham, Kathleen Osborne and Ms. Hoon-Hoon Tan for critical reading of the manuscript, Dr. Sudipto Roy for discussion. We are grateful to Drs. Frank Stockdale for F59 antibody, Darren Gilmour for ody mutant, Dmitri Bessarab for myhc1, mylz2 and myogenin probes, Jose Campos-Ortega and Matthias Hammerschmidt for expression constructs, Ms. Yang-Sun Chan for electron microscopy, staff of the IMCB fish facility for fish care. VK and YJJ laboratories are funded by the A*STAR of Singapore.
- Cortes F, Daggett D, Bryson-Richardson RJ, Neyt C, Maule J, Gautier P, Hollway GE, Keenan D, Currie PD: Cadherin-mediated differential cell adhesion controls slow muscle cell migration in the developing zebrafish myotome. Dev Cell. 2003, 5: 865-876. 10.1016/S1534-5807(03)00362-9.View ArticlePubMedGoogle Scholar
- Denetclaw WF, Christ B, Ordahl CP: Location and growth of epaxial myotome precursor cells. Development. 1997, 124: 1601-1610.PubMedGoogle Scholar
- Denetclaw WF, Berdougo E, Venters SJ, Ordahl CP: Morphogenetic cell movements in the middle region of the dermomyotome dorsomedial lip associated with patterning and growth of the primary epaxial myotome. Development. 2001, 128: 1745-1755.PubMedGoogle Scholar
- Devoto SH, Melancon E, Eisen JS, Westerfield M: Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development. 1996, 122: 3371-3380.PubMedGoogle Scholar
- Henry CA, Amacher SL: Zebrafish slow muscle cell migration induces a wave of fast muscle morphogenesis. Dev Cell. 2004, 7: 917-923. 10.1016/j.devcel.2004.09.017.View ArticlePubMedGoogle Scholar
- Ju B, Chong SW, He J, Wang X, Xu Y, Wan H, Tong Y, Yan T, Korzh V, Gong Z: Recapitulation of fast skeletal muscle development in zebrafish by transgenic expression of GFP under the mylz2 promoter. Dev Dyn. 2003, 227: 14-26. 10.1002/dvdy.10273.View ArticlePubMedGoogle Scholar
- Kahane N, Cinnamon Y, Kalcheim C: The cellular mechanism by which the dermomyotome contributes to the second wave of myotome development. Development. 1998, 125: 4259-4271.PubMedGoogle Scholar
- Kalcheim C, Cinnamon Y, Kahane N: Myotome formation: a multistage process. Cell Tissue Res. 1999, 296: 161-173. 10.1007/s004410051277.View ArticlePubMedGoogle Scholar
- Kielbowna L: The formation of somites and early myotomal myogenesis in Xenopus laevis, Bombina variegata and Pelobates fuscus. J Embryol Exp Morphol. 1981, 64: 295-304.PubMedGoogle Scholar
- Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF: Stages of embryonic development of the zebrafish. Dev Dyn. 1995, 203: 253-310.View ArticlePubMedGoogle Scholar
- Neff AW, Malacinski GM, Chung HM: Amphibian (urodele) myotomes display transitory anterior/posterior and medial/lateral differentiation patterns. Dev Biol. 1989, 132: 529-543. 10.1016/0012-1606(89)90248-0.View ArticlePubMedGoogle Scholar
- Venters SJ, Thorsteinsdottir S, Duxson MJ: Early development of the myotome in the mouse. Dev Dyn. 1999, 216: 219-232. 10.1002/(SICI)1097-0177(199911)216:3<219::AID-DVDY1>3.0.CO;2-J.View ArticlePubMedGoogle Scholar
- Xu Y, He J, Wang X, Lim TM, Gong Z: Asynchronous activation of 10 muscle specific protein (MSP) genes during zebrafish somitogenesis. Dev Dyn. 2000, 219: 201-215. 10.1002/1097-0177(2000)9999:9999<::AID-DVDY1043>3.3.CO;2-9.View ArticlePubMedGoogle Scholar
- Henry CA, Hall LA, Hille MB, Solnica-Krezel L, Cooper MS: Somites in zebrafish double mutant for knypek and trilobite form without internal mesenchymal cells or compaction. Curr Biol. 2000, 10: 1063-1066. 10.1016/S0960-9822(00)00677-1.View ArticlePubMedGoogle Scholar
- Barresi MJ, Stickney HL, Devoto SH: The zebrafish slow-muscle-omitted gene product is required for Hedgehog signal transduction and the development of slow muscle identity. Development. 2000, 127: 2189-2199.PubMedGoogle Scholar
- Blagden CS, Currie PD, Ingham PW, Hughes SM: Notochord induction of zebrafish slow muscle mediated by Sonic hedgehog. Genes Dev. 1997, 11: 2163-75.PubMed CentralView ArticlePubMedGoogle Scholar
- Coutelle O, Blagden CS, Hampson R, Halai C, Rigby PW, Hughes M: Hedgehog signalling is required for maintenance of myf5 and myoD expression and timely terminal differentiation in zebrafish adaxial myogenesis. Dev Biol. 2001, 236: 136-50. 10.1006/dbio.2001.0193.View ArticlePubMedGoogle Scholar
- Currie PD, Ingham PW: Induction of a specific muscle cell type by a hedgehog-like protein in zebrafish. Nature. 1996, 382: 452-455. 10.1038/382452a0.View ArticlePubMedGoogle Scholar
- Currie PD, Ingham PW: The generation and interpretation of positional information within the vertebrate myotome. Mech Dev. 1998, 73: 3-21. 10.1016/S0925-4773(98)00036-7.View ArticlePubMedGoogle Scholar
- Du SJ, Devoto SH, Westerfield M, Moon RT: Positive and negative regulation of muscle cell identity by members of the hedgehog and TGF-beta gene families. J Cell Biol. 1997, 139: 145-156. 10.1083/jcb.139.1.145.PubMed CentralView ArticlePubMedGoogle Scholar
- Hirsinger E, Stellabotte F, Devoto SH, Westerfield M: Hedgehog signaling is required for commitment but not initial induction of slow muscle precursors. Dev Biol. 2004, 275: 143-157. 10.1016/j.ydbio.2004.07.030.View ArticlePubMedGoogle Scholar
- Lewis KE, Currie PW, Roy S, Schauerte H, Haffter P, Ingham PW: Control of muscle cell-type specification in the zebrafish embryo by Hedgehog signalling. Dev Biol. 1999, 216: 469-480. 10.1006/dbio.1999.9519.View ArticlePubMedGoogle Scholar
- Roy S, Wolff C, Ingham PW: The u-boot mutation identifies a Hedgehog-regulated myogenic switch for fiber-type diversification in the zebrafish embryo. Genes Dev. 2001, 15: 1563-1576. 10.1101/gad.195801.PubMed CentralView ArticlePubMedGoogle Scholar
- Wolff C, Roy S, Ingham PW: Multiple muscle cell identities induced by distinct levels and timing of hedgehog activity in the zebrafish embryo. Curr Biol. 2003, 13: 1169-1181. 10.1016/S0960-9822(03)00461-5.View ArticlePubMedGoogle Scholar
- Haines L, Currie PD: Morphogenesis and evolution of vertebrate appendicular muscle. J Anat. 2001, 199: 205-209. 10.1017/S0021878201008184.PubMed CentralView ArticlePubMedGoogle Scholar
- Neyt C, Jagla K, Thisse C, Thisse B, Haines L, Currie PD: Evolutionary origins of vertebrate appendicular muscle. Nature. 2000, 408: 82-86. 10.1038/35040549.View ArticlePubMedGoogle Scholar
- Feng Y, Broder CC, Kennedy PE, Berger EA: HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G-protein coupled receptor. Science. 1996, 272: 872-877. 10.1126/science.272.5263.872.View ArticlePubMedGoogle Scholar
- Loetscher M, Geiser T, O'Reilly T, Zwahlen R, Baggiolini M, Bernhard M: Cloning of a human seven-transmembrane domain receptor, LESTR, that is highly expressed in leukocytes. J Biol Chem. 1994, 269: 232-237.PubMedGoogle Scholar
- Berson JF, Long D, Doranz BJ, Rucker J, Jirik FR, Doms RW: A seven-transmembrane domain receptor involved in fusion and entry of T-cell tropic human immunodeficiency virus type 1 strains. J Virol. 1996, 70: 6288-6295.PubMed CentralPubMedGoogle Scholar
- Mackay CR: Chemokine receptors and T cell chemotaxis. J Exp Med. 1996, 184: 799-802. 10.1084/jem.184.3.799.View ArticlePubMedGoogle Scholar
- Moore JP, Trkola A, Dragic T: Co-receptors for HIV-1 entry. Curr Opin Immunol. 1997, 9: 551-562. 10.1016/S0952-7915(97)80110-0.View ArticlePubMedGoogle Scholar
- Baggiolini M, Dewald B, Moser B: Human chemokines: an update. Ann Rev Immunol. 1997, 15: 675-705. 10.1146/annurev.immunol.15.1.675.View ArticleGoogle Scholar
- Bleul CC, Fuhlbrigge RC, Casasnovas JM, Aiuti A, Springer TA: A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor (SDF-1). J Exp Med. 1996, 184: 1101-1109. 10.1084/jem.184.3.1101.View ArticlePubMedGoogle Scholar
- Bleul CC, Farzan M, Choe H, Parolin C, Clark-Lewis I, Sodroski J, Springer TA: The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature. 1996, 382: 829-833. 10.1038/382829a0.View ArticlePubMedGoogle Scholar
- Kim CH, Broxmeyer HE: In vitro behavior of hematopoietic progenitor cells under the influence of chemoattractants: stromal cell-derived factor-1, steel factor, and the bone marrow environment. Blood. 1998, 91: 100-110.PubMedGoogle Scholar
- McGrath KE, Koniski AD, Maltby KM, McGann JK, Palis J: Embryonic expression and function of the chemokine SDF-1 and its receptor, CXCR4. Dev Biol. 1999, 213: 442-456. 10.1006/dbio.1999.9405.View ArticlePubMedGoogle Scholar
- Murphy PM, Baggiolini M, Charo IF, Hebert CA, Horuk R, Matsushima K, Miller LH, Oppenheim JJ, Power CA: International union pharmacology. XXII. Nomenclature for chemokine receptors. Pharmacol Rev. 2000, 52: 145-176.PubMedGoogle Scholar
- Ma Q, Jones D, Borghesani PR, Segal RA, Nagasawa T, Kishimoto T, Bronson RT, Springer TA: Impaired B-lymphopoiesis, myelopoiesis and derailed cerebellar neuron migration in CXCR4 – and SDF-1-deficient mice. Proc Natl Acad Sci USA. 1998, 95: 9448-9453. 10.1073/pnas.95.16.9448.PubMed CentralView ArticlePubMedGoogle Scholar
- Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littamn D: Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature. 1998, 393: 595-599. 10.1038/31269.View ArticlePubMedGoogle Scholar
- Doitsidou M, Reichman-Fried M, Stebler J, Koprunner M, Dorries J, Meyer D, Esguerra CV, Leung T, Raz E: Guidance of primodial germ cell migration by the chemokine SDF-1. Cell. 2002, 111: 647-659. 10.1016/S0092-8674(02)01135-2.View ArticlePubMedGoogle Scholar
- Knaut H, Werz C, Geisler R, Nusslein-Volhard C, Tubingen 2000 Screen Consortium: A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor. Nature. 2003, 421: 279-282. 10.1038/nature01338.View ArticlePubMedGoogle Scholar
- Molyneaux KA, Zinszner H, Kunwar PS, Schaible K, Stebler J, Sunshine MJ, O'Brien W, Raz E, Littman D, Wylie C, Lehmann R: The chemokine SDF1/CXCL12 and its receptor CXCR4 regulate mouse germ cell migration and survival. Development. 2003, 130: 4279-4286. 10.1242/dev.00640.View ArticlePubMedGoogle Scholar
- David NB, Sapede D, Saint-Etienne L, Thisse C, Thisse B, Dambly-Chaudiere C, Rosa FM, Ghysen A: Molecular basis of cell migration in the fish lateral line: role of the chemokine receptor CXCR4 and its ligand, SDF1. Proc Natl Acad Sci USA. 2002, 99: 16297-16302. 10.1073/pnas.252339399.PubMed CentralView ArticlePubMedGoogle Scholar
- Gilmour D, Knaut H, Maischein HM, Nusslein-Volhard C: Towing of sensory axons by their migrating target cells in vivo. Neuron. 2004, 34: 577-588. 10.1016/S0896-6273(02)00683-9.View ArticleGoogle Scholar
- Li Q, Shirabe K, Kuwada JY: Chemokine signaling regulates sensory cell migration in zebrafish. Dev Biol. 2004, 269: 123-136. 10.1016/j.ydbio.2004.01.020.View ArticlePubMedGoogle Scholar
- Li Q, Shirabe K, Thisse C, Thisse B, Okamoto H, Masai I, Kuwada JY: Chemokine signaling guides axons within the retina in zebrafish. J Neurosci. 2005, 25: 1711-1717. 10.1523/JNEUROSCI.4393-04.2005.View ArticlePubMedGoogle Scholar
- Knaut H, Blader P, Strähle U, Schier AF: Assembly of trigeminal sensory ganglia by chemokine signaling. Neuron. 2005, 47: 653-666. 10.1016/j.neuron.2005.07.014.View ArticlePubMedGoogle Scholar
- Chong SW, Emelyanov A, Gong Z, Korzh V: Expression pattern of two zebrafish genes, cxcr4a and cxcr4b. Mech Dev. 2001, 109: 347-54. 10.1016/S0925-4773(01)00520-2.View ArticlePubMedGoogle Scholar
- Pituch-Noworolska A, Majka M, Janowska-Wieczorek A, Baj-Krzyworzeka M, Urbanowicz B, Malec E, Ratajczak MZ: Circulating CXCR4-positive stem/progenitor cells compete for SDF-1-positive niches in bone marrow, muscle and neural tissues: an alternative hypothesis to stem cell plasticity. Folia Histochem Cytobiol. 2003, 41: 13-21.PubMedGoogle Scholar
- Ödemis V, Lamp E, Pezeshki G, Moepps B, Schilling K, Gierschik P, Littman DR, Engele J: Mice deficient in the chemokine receptor CXCR4 exhibit impaired limb innervation and myogenesis. Mol Cell Neurosci. 2005, 30: 494-505. 10.1016/j.mcn.2005.07.019.View ArticlePubMedGoogle Scholar
- Vasyutina E, Stebler J, Brand-Saberi B, Schulz S, Raz E, Birchmeier C: CXCR4 and Gab1 cooperate to control the development of migrating muscle progenitor cells. Genes Dev. 2005, 19: 2187-2198. 10.1101/gad.346205.PubMed CentralView ArticlePubMedGoogle Scholar
- Parker MH, Seale P, Rudnicki MA: Looking back to the embryo: defining transcriptional networks in adult myogenesis. Nat Rev Genet. 2003, 4: 497-507. 10.1038/nrg1109.View ArticlePubMedGoogle Scholar
- Buckingham M, Bajard L, Chang T, Daubas P, Hadchouel J, Meilhac S, Montarras D, Rocancourt D, Relaix F: The formation of skeletal muscle: from somite to limb. J Anat. 2003, 202: 59-68. 10.1046/j.1469-7580.2003.00139.x.PubMed CentralView ArticlePubMedGoogle Scholar
- Molkentin JD, Olson EN: Combinatorial control of muscle development by basic helix-loop-helix and MADS-box transcription factors. Proc Natl Acad Sci USA. 1996, 93: 9366-9373. 10.1073/pnas.93.18.9366.PubMed CentralView ArticlePubMedGoogle Scholar
- Perry RL, Parker MH, Rudnicki MA: Activated MEK1 binds the nuclear MyoD transcriptional complex to repress transactivation. Mol Cell. 2001, 8: 291-301. 10.1016/S1097-2765(01)00302-1.View ArticlePubMedGoogle Scholar
- Pownall ME, Gustafsson MK, Emerson CP: Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. Ann Rev Cell Dev Biol. 2002, 18: 747-783. 10.1146/annurev.cellbio.18.012502.105758.View ArticleGoogle Scholar
- Puri PL, Sartorelli V: Regulation of muscle regulatory factors by DNA-binding, interacting proteins, and post-transcriptional modifications. J Cell Physiol. 2000, 185: 155-173. 10.1002/1097-4652(200011)185:2<155::AID-JCP1>3.0.CO;2-Z.View ArticlePubMedGoogle Scholar
- Blackwell TK, Weintraub H: Differences and similarities in DNA-binding preferences of MyoD and E2A protein complexes revealed by binding site selection. Science. 1990, 250: 1104-1110. 10.1126/science.2174572.View ArticlePubMedGoogle Scholar
- Mal A, Harter ML: MyoD is functionally linked to the silencing of a muscle-specific regulatory gene prior to skeletal myogenesis. Proc Natl Acad Sci USA. 2003, 100: 1735-1739. 10.1073/pnas.0437843100.PubMed CentralView ArticlePubMedGoogle Scholar
- Chong SW, Jiang Y-J: Off limits – Integrins holding boundaries in somitogenesis. Trends Cell Biol. 2005, 15: 453-457. 10.1016/j.tcb.2005.07.008.View ArticlePubMedGoogle Scholar
- Rudnicki MA, Jaenisch R: The MyoD family of transcription factors and skeletal myogenesis. Bioessays. 1995, 17: 203-209. 10.1002/bies.950170306.View ArticlePubMedGoogle Scholar
- Rudnicki MA, Schnegelsberg PN, Stead RH, Braun T, Arnold HH, Jaenisch R: MyoD or Myf5 is required for the formation of skeletal muscle. Cell. 1993, 75: 1351-1359. 10.1016/0092-8674(93)90621-V.View ArticlePubMedGoogle Scholar
- Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H: The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell. 1990, 61: 49-59. 10.1016/0092-8674(90)90214-Y.View ArticlePubMedGoogle Scholar
- Jen Y, Weintraub H, Benezra R: Overexpression of Id protein inhibits the muscle differentiation program: in vivo association of Id with E2A proteins. Genes Dev. 1992, 6: 1466-1479. 10.1101/gad.6.8.1466.View ArticlePubMedGoogle Scholar
- Chong SW, Nguyen TTH, Chu LT, Jiang YJ, Korzh V: Zebrafish id2 developmental expression pattern contains evolutionary conserved and species-specific characteristics. Dev Dyn. 2005, 234: 1055-1063. 10.1002/dvdy.20625.View ArticlePubMedGoogle Scholar
- Borycki A-G, Brunk B, Tajbakhsh S, Buckingham M, Chiang C, Emerson CP: Sonic hedgehog controls epaxial muscle determination through Myf5 activation. Development. 1999, 126: 4053-4063.PubMedGoogle Scholar
- Gustafsson MK, Pan H, Pinney DF, Liu Y, Lewandowski A, Epstein DJ, Emerson CP: Myf5 is a direct target of long-range Shh signaling and Gli regulation for muscle specification. Genes Dev. 2002, 16: 114-126. 10.1101/gad.940702.PubMed CentralView ArticlePubMedGoogle Scholar
- Klein RS, Rubin JB, Gibson HD, DeHaan EN, Alvarez-Hernandez X, Segal RA, Luster AD: SDF-1α induces chemotaxis and enhances Sonic hedgehog-induced proliferation of cerebellar granule cells. Development. 2001, 128: 1971-1981.PubMedGoogle Scholar
- Schauerte HE, van Eeden FJ, Fricke C, Odenthal J, Strahle U, Haffter P: Sonic hedgehog is not required for the induction of medial floor plate cells in the zebrafish. Development. 1998, 125: 2983-2993.PubMedGoogle Scholar
- Concordet JP, Lewis KE, Moore JW, Goodrich LV, Johnson RL, Scott MP, Ingham PW: Spatial regulation of a zebrafish patched homologue reflects the roles of sonic hedgehog and protein kinase A in neural tube and somite patterning. Development. 1996, 122: 2835-2846.PubMedGoogle Scholar
- Hammerschmidt M, Bitgood MJ, McMahon AP: Protein kinase A is a common negative regulator of Hedgehog signaling in the vertebrate embryo. Genes Dev. 1996, 10: 647-658. 10.1101/gad.10.6.647.View ArticlePubMedGoogle Scholar
- Amthor H, Christ B, Weil M, Patel K: The importance of timing differentiation during limb muscle development. Curr Biol. 1998, 8: 642-652. 10.1016/S0960-9822(98)70251-9.View ArticlePubMedGoogle Scholar
- Yusuf F, Rehimi R, Morosan-Puopolo G, Dai F, Zhang X, Brand-Saberi B: Inhibitors of CXCR4 affect the migration and fate of CXCR4-progenitors in the developing limb of chick embryos. Dev Dyn. 2006, 235: 3007-3015. 10.1002/dvdy.20951.View ArticlePubMedGoogle Scholar
- Nagasawa T, Hirota S, Tachibana K, Takakura N, Nishikawa S, Kitamura Y, Yoshida N, Kikutani H, Kishimoto T: Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature. 1996, 382: 635-638. 10.1038/382635a0.View ArticlePubMedGoogle Scholar
- Tachibana K, Hirota S, Lizasa H, Yoshida H, Kawabata K, Kataoka Y, Kitamura Y, Matsushima K, Yoshida N, Nishikawa S, Kishimoto T, Nagasawa T: The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature. 1998, 393: 591-594. 10.1038/31261.View ArticlePubMedGoogle Scholar
- Haas P, Gilmour D: Chemokine signaling mediates self-organizing tissue migration in the zebrafish lateral line. Dev Cell. 2006, 10: 673-680. 10.1016/j.devcel.2006.02.019.View ArticlePubMedGoogle Scholar
- Kury P, Greiner-Petter R, Cornely C, Jurgens T, Muller HW: Mammalian achaete scute homolog 2 is expressed in the adult sciatic nerve and regulates the expression of Krox24, Mob-1, CXCR4, and p57kip2 in Schwann cells. J Neurosci. 2002, 22: 7586-7595.PubMedGoogle Scholar
- Ratajczak MZ, Kucia M, Reca R, Majka M, Janowska-Wieczorek A, Ratajczak J: Stem cell plasticity revisited: CXCR4-positive cells expressing mRNA for early muscle, liver and neural cells 'hide out' in the bone marrow. Leukemia. 2004, 18: 29-40. 10.1038/sj.leu.2403184.View ArticlePubMedGoogle Scholar
- Rudnicki MA, Braun T, Hinuma S, Jaenisch R: Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene give myf5 and results in apparently normal muscle development. Cell. 1992, 71: 383-390. 10.1016/0092-8674(92)90508-A.View ArticlePubMedGoogle Scholar
- Murre C, MaCaw PS, Baltimore D: A nes DNA binding and dimerization motif in immunoglobin enhancer binding, daughterless, MyoD, and myc proteins. Cell. 1989, 56: 777-783. 10.1016/0092-8674(89)90682-X.View ArticlePubMedGoogle Scholar
- Davis RL, Cheng PF, Lassar AB, Weintraub H: The MyoD DNA binding domain contains a recognition code for muscle-specific gene activation. Cell. 1990, 60: 733-746. 10.1016/0092-8674(90)90088-V.View ArticlePubMedGoogle Scholar
- Lassar AB, Davis RL, Wright WE, Kadesch T, Murre C, Voronova A, Baltimore D, Weintraub H: Functional activity of myogenic HLH proteins requires hetero-oligomerization with E12/E47-like proteins in vivo. Cell. 1991, 66: 305-315. 10.1016/0092-8674(91)90620-E.View ArticlePubMedGoogle Scholar
- Moriuchi M, Moriuchi H, Margolis DM, Fauci AS: USF/c-Myc enhances, while Yin-Yang 1 suppresses, the promoter activity of cxcr4, a co-receptor for HIV-1 entry. J Immunol. 1999, 162: 5986-5992.PubMedGoogle Scholar
- Wentworth BM, Donoghue M, Engert JC, Berglund E, Rosenthal N: Paired MyoD-binding sites regulate myosin light chain gene expression. Proc Natl Acad Sci USA. 1991, 88: 1242-1246. 10.1073/pnas.88.4.1242.PubMed CentralView ArticlePubMedGoogle Scholar
- Piette J, Bessereau JL, Huchet M, Changeux JP: Two adjacent MyoD1-binding sites regulate expression of the acetylcholine receptor alpha-subunit gene. Nature. 1990, 345: 353-355. 10.1038/345353a0.View ArticlePubMedGoogle Scholar
- Buskin JN, Hauschka SD: Identification of a myocyte nuclear factor that binds to the muscle-specific enhancer of the mouse muscle creatine kinase gene. Mol Cell Biol. 1989, 9: 2627-2640.PubMed CentralView ArticlePubMedGoogle Scholar
- Goldhamer DJ, Brunk BP, Faerman A, King A, Shani M, Emerson CP: Embryonic activation of the myoD gene is regulated by a highly conserved distal control element. Development. 1995, 121: 637-649.PubMedGoogle Scholar
- Weintraub H, Davis R, Lockshon D, Lassar A: MyoD binds cooperatively to two sites in a target enhancer sequence: occupancy of two sites is required for activation. Proc Natl Acad Sci USA. 1990, 87: 5623-5627. 10.1073/pnas.87.15.5623.PubMed CentralView ArticlePubMedGoogle Scholar
- Bengal E, Flores O, Rangarajan PN, Chen A, Weintraub H, Verma IM: Positive control mutations in the MyoD basic region fail to show cooperative DNA binding and transcriptional activation in vitro. Proc Natl Acad Sci USA. 1994, 91: 6221-6225. 10.1073/pnas.91.13.6221.PubMed CentralView ArticlePubMedGoogle Scholar
- Weinberg E, Allende ML, Kelly CS, Abdelhamid A, Murakami T, Andermann P, Doerre OG, Grunwald DJ, Riggleman B: Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos. Development. 1996, 122: 271-80.PubMedGoogle Scholar
- Chen YH, Lee WC, Liu CF, Tsai HJ: Molecular structure, dynamic expression, and promoter analysis of zebrafish (Danio rerio) myf-5 gene. Genesis. 2001, 29: 22-35. 10.1002/1526-968X(200101)29:1<22::AID-GENE1002>3.0.CO;2-Z.View ArticlePubMedGoogle Scholar
- Miller JB, Teal SB, Stockdale FE: Evolutionarily conserved sequences of striated muscle myosin heavy chain isoforms. Epitope mapping by cDNA expression. J Biol Chem. 1989, 264: 13122-13130.PubMedGoogle Scholar
- Nasevicius A, Ekker SC: Effective targeted gene 'knockdown' in zebrafish. Nat Genet. 2000, 28: 216-220.View ArticleGoogle Scholar
- Felsenfeld AL, Walker C, Westerfield M, Kimmel C, Streisinger G: Mutations affecting skeletal muscle myofibril structure in the zebrafish. Development. 1990, 108: 443-459.PubMedGoogle Scholar
- Spurr AR: A low viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res. 1969, 26: 31-34. 10.1016/S0022-5320(69)90033-1.View ArticlePubMedGoogle Scholar
- Hammond CL, Hinits Y, Osborn DPS, Minchin JEN, Tettamanti G, Hughes SM: Signals and myogenic regulatory factors restrict pax3 and pax7 expression to dermomyotome-like tissue in zebrafish. Dev Biol. 2007, 302: 504-521. 10.1016/j.ydbio.2006.10.009.PubMed CentralView ArticlePubMedGoogle Scholar
- Lee HC, Huang HY, Lin CY, Chen YH, Tsai HJ: Foxd3 mediates zebrafish myf5 expression during early somitogenesis. Dev Biol. 2006, 290: 359-372. 10.1016/j.ydbio.2005.11.032.View ArticlePubMedGoogle Scholar
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