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Laboratory of Animal Genetics and Breeding, College of Animal Science and Technology, Jilin Agricultural University, Changchun 130118, P. R. China
1 Corresponding author: rufusxu{at}yahoo.com.cn
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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Key Words: β-catenin gene • feather bud development • goose embryo • messenger ribonucleic acid expression
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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β-Catenin was originally identified as a cytoplasmic ligand required for cadherin-mediated extracellular adhesion (Nagafuchi and Takeichi, 1988; Ozawa et al., 1989). It is a vertebrate homolog of the Drosophila segment polarity gene product armadillo (McCrea et al., 1991). β-Catenin was previously confirmed to be involved in Wnt family signal transduction (Gumbiner, 1995), which was found not only to be associated with the determination of embryonic axis (Funayama et al., 1995) but also to be a crucial component in the Wnt/β-catenin signaling pathway controlling the expression of specific target genes that regulate cell proliferation, cell fate, and differentiation (Wodarz and Nusse, 1998; Novak and Dedhar, 1999; Akiyama, 2000; Sakanaka et al., 2000). The pathway was found to be involved in skin follicle morphogenesis, embryonic development, pancreas growth, and cancer (Waltzer and Bienz, 1999; Chodankar et al., 2003; Chang et al., 2004; Heiser et al., 2006). The avian β-catenin gene was first isolated and characterized in chicken (Lu et al., 1997). Further studies showed that intercellular signaling by a subset of Wnt is mediated by the stabilization of cytoplasmic β-catenin and its translocation to the nucleus and that the activation of the β-catenin pathway initiates feather follicle development in embryonic skin and plays an important role in the subsequent morphogenesis of the buds (Hsu et al., 1998; Noramly et al., 1999). The β-catenin pathway has been reported involved in modulating chicken epithelial morphogenesis. The β-catenin mRNA was initially expressed at homogeneous levels in the epithelia over a skin appendage tract field, and then the expression became transformed into a periodic pattern corresponding to individual primordia (Widelitz et al., 2000). More related studies have shown that β-catenin is an essential molecule in Wnt/wingless signaling (Merriam et al., 1997; Knowles et al., 2003; Lloyd et al., 2003), and when β-catenin is mutated during embryogenesis, the formation of placodes that generate hair follicles is blocked (Huelsken et al., 2001). Upon Wnt signaling, β-catenin accumulates in the cytoplasm and is transported to the nucleus, where it interacts with members of the LEF/TCF family of transcription factors and activates gene expression, which plays a role in the development of skin, hair, and feathers (Behrens et al., 1996; Widelitz et al., 1999; Tetsu and McCormick, 1999; Barker et al., 2000). However, the expression pattern of the β-catenin gene and its cooperative signals in the developmental skin of the goose embryo still remains unknown. As a consequence, the molecular mechanisms controlling the early stages of feather bud development in geese is also poorly defined. In this work, we performed semiquantitative reverse transcription PCR (RT-PCR), Northern blot analyses, and in situ hybridization spatially and temporally in the dorsal skin of goose embryo to determine how the β-catenin gene is involved in the feather morphogenesis.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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Semiquantitative RT-PCR
To measure the mRNA expression level of goose β-catenin, semiquantitative RT-PCR analysis of β-catenin and constitutively expressed β-actin was carried out as described previously (Botchkarev et al., 2000). Total RNA was isolated from dorsal skin samples of embryonic geese at E10, E12, E18, E20, E25, and E30, based on the methods above. Complementary DNA was synthesized by reverse transcriptase using 1 µg of total RNA and the BcaBEST RNA PCR Kit (Takara Bio Inc., Otsu, Japan). The following RT-PCR conditions were used: 65°C for 1 min, 30°C for 5 min, 65°C for 25 min, 98°C for 5 min, followed by 35 cycles of 94°C for 15 s and 60°C for 1 min. Polymerase chain reaction was performed in a volume of 20 µL consisting of 1 µL of RT-PCR product, 1 x PCR buffer, 1.5 mM MgCl2, 0.2 mM deoxynucleoside triphosphate, 0.3µM each primer, and 1 U Taq DNA polymerase (MBI Fermentas, Vilnius, Lithuania). The PCR conditions were at 95°C for 5 min followed by 30 cycles of a denaturing at 95°C for 30 s, annealing at 59°C for 30 s, an extension at 72°C for 30 s, and a final extension at 72°C for 4 min, finally kept at 4°C. The amplification was performed on a PTC-100 programmable thermal controller (MJ Research Inc., Waltham, MA). The β-actin gene was used as an internal control. The following sets of oligonucleotide primers were used: for β-catenin, 5'-CATCTCGCCATGC-TATTA-3' and 5'-AAGGTGGAGTCCTAAAGC-3'; for β-actin, 5'-ATCAGCAAGCAGGAATACGA-3' and 5'-CGGCAGCAACAGAAGTGGA-3'. The primers were designed according to the published sequences of goose β-catenin (submitted in this paper) and β-actin (M26111) mRNA in the GenBank databases. The reaction products (4 µL) at each embryonic time point were visualized and photographed following electrophoresis on 2% agarose gels stained with 0.25 µg/mL of ethidium bromide, and the expected product was extracted and verified by direct DNA sequencing. Semiquantitative analysis of β-catenin expression was done by the densitometry scan analysis program from a photographic system (GeneSnap from SynGene, Frederick, MD). The density ratio of the β-catenin RT-PCR band to the β-actin RT-PCR band was used as a measure of β-catenin mRNA level in the tissue. To verify the specificity of the bands shown, a negative control was performed using an aliquot of a cDNA synthesis reaction in which no reverse transcriptase enzyme was added.
Northern Blot Analysis and In Situ Hybridization
Northern blot analysis was performed according to the method by Leung et al. (2002), to detect β-catenin mRNA transcripts of the dorsal skin of goose embryos at E10, E12, E18, E20, E25, and E30. Complementary DNA probes were prepared using the 563-bp β-catenin fragment, and the β-actin cDNA probe (461 bp) was used as a loading control. The RT-PCR product probes were confirmed by sequencing, and the probes were randomly labeled with [
32P] deoxycytidine triphosphate using Rediprime (Invitrogen, Paisley, UK) and hybridized to the membrane with RapidHyb Buffer (Invitrogen) according to the protocol of the manufacturer. The RNA was transferred to a nylon membrane and hybridized to the probe by random priming. The amounts of mRNA loaded in each gel lane were normalized by staining with methylene blue.
Dorsal skin sections of the embryonic goose at varied stages and RNA probes corresponding to the 563-bp sense and antisense strand of the goose β-catenin cDNA and Shh cDNA (368 bp) were prepared for in situ hybridization as previously described (Nakamura et al., 1989; Mackem and Mahon, 1991). Hybridization was performed at 50°C in 50% formamide, 5 x 0.75 M NaCl, 0.075 M sodium citrate, 0.1 M Na-K phosphate pH 7.0, l x Denhardt’s solution, 5% dextran sulfate, 100 mM dithiothreitol, and 100 µg/mL of Escherichia coli transfer RNA overnight. Following the hybridization, sections were washed with high stringency and then treated with RNase A (15 µg/mL). The sections were dehydrated in ethanol solutions (containing ammonium acetate), then dried and dipped in Kodak NTB-2 nuclear track emulsion (Eastman Kodak, Rochester, NY). After exposure for 2 wk, the slides were developed and stained with toluidine blue. The skin tissue sections were examined at E10, E12, E18, E20, E25, and E30, respectively. The sections were air-dried and photographed with numarski optics using a Zeiss Axiophot microscope (Carl Zeiss, Thornwood, NY), equipped with an automatic camera, using Kodacolor Gold film (Kodak). Quantification of β-catenin and Shh grain density was performed using MetaMorph image analysis system (UIC, Dowington, PA).
Data Analysis
Eight and 5 birds at each stage were used for semiquantitative RT-PCR analysis and Northern blot, respectively, and 4 syntheses products from independent reactions per individual were quantified densitometrically. For in situ hybridization analysis, 5 birds at each stage were used, and the representative microscopic fields were selected. Six serial sections per biopsy were examined. All statistical calculations were completed by the software package SPSS11.0 (Lin et al., 2002). The quantified results above are expressed as mean ± SD. Due to the small sample sizes, comparisons among different age groups were assessed using the Kruskall-Wallis nonparametric test (Conover, 1999). Statistical significance was indicated with P < 0.05.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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Semiquantitation of β-catenin mRNA Expression by RT-PCR
As shown in Figure 1
, during feather bud development, the highest β-catenin mRNA expression levels were shown at E18 and E20 (98.22 ± 5.31 and 101.74 ± 7.29%), and the lowest levels were observed at E25 and E30 (67.91 ± 6.24 and 62.51 ± 7.11%). The expression levels at E10 and E12 ranked second (82.02 ± 7.47 and 80.31 ± 9.03%). The negative control performed using an aliquot of a cDNA synthesis reaction in which no reverse transcriptase enzyme was added gave no β-catenin band, thus verifying the specificity of the bands shown. These results confirmed that the levels of β-catenin expression were most prominent at the early stage from E18 to E20 and then significantly declined with the embryonic development. Our study on feather follicle development in embryonic geese has shown that most feather primordia evolved initially at E10 to E12 on the spinal feather tract, and then the buds elongated with anterior-posterior and proximal-distal asymmetries until at E18 to E20, the density of the primary feather follicles reached the maximum, and the secondary follicles started to increase; up to E26, the density of secondary follicles exceeded the primary follicles (Xu et al., 2007). This indicates that the higher expression of β-catenin mRNA seems to be associated with the initiation of feather follicles; the varied levels of β-catenin expression in the skin may influence the density of different kinds of feather follicles. Although the β-catenin function was studied extensively in chicken embryos and revealed that it contributes to the induction of feather bud formation, the activation of the β-catenin pathway also initiates feather follicle development in embryonic skin and plays an important role in the subsequent morphogenesis of the buds (Noramly et al., 1999; Widelitz et al., 2000; Chodankar et al., 2003; Chang et al., 2004). How exactly β-catenin controls the development of feather buds remains to be identified. Recent studies have revealed that the function of β-catenin is not only determined by its stabilization in the cellular compartments but also by the nuclear location of the β-catenin for signal transduction (Kemler et al., 2004; Tolwinski and Wieschaus, 2004; Itoh et al., 2005; Waldrop et al., 2006).
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that a single 3.5-kb transcript was observed at every stage and that no alternative splicing variant was found; the mRNA transcripts were abundantly expressed in the dorsal skins of embryonic geese from E10 to E20 (Figure 2A). In chicken, β-catenin transcripts were 3.6 kb (Lu et al., 1997), and in Drosophila, armadillo transcripts were 3.2 kb (Riggleman et al., 1989). Here, we simultaneously quantitated the expression levels at the varied stages after normalization to β-actin signal using densitometry. It was verified that the expressions seemed to be the strongest at stages E10, E18, and E20 and then significantly decreased at E25 and E30 (Figure 2B). Although Northern blot analysis is less sensitive, the changes of β-catenin expression levels at the varied stages were almost consistent with the patterns of the mRNA detected by semi-quantitative RT-PCR above. Immunolocalization of β-catenin in developing chick skin has shown that the β-catenin signaling pathway is active in a dynamic pattern from the earliest stages of feather bud development (Noramly et al., 1999). In this study, the high mRNA expression levels of the β-catenin gene in developing embryonic goose skin indicated that this signaling regulation is stable and active from the earliest stages of feather bud development to the maturation of feather follicles. However, the forced activation of this pathway by expression of a stabilized β-catenin in the ectoderm results in the ectopic formation of feather buds (Noramly et al., 1999).
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). As the feather bud develops with an anterior-posterior orientation, strong expression was seen in the ectoderm and dense dermis besides the periderm layer, with a diffuse distribution within the internal area of the buds. Furthermore, stronger dermal staining was observed in the posterior lateral of the bud and in the interplacodal cells, which may form a novel bud (Figure 3B). This result was consistent with the localization of endogenous β-catenin protein detected in the anterior and posterior of a bud of chicken skin during tract formation (Noramly et al., 1999). But, the expression levels of β-catenin mRNA is relatively low at this stage (Figure 4). As the bud develops, the stronger staining is seen in the barb ridges having differentiated into 3 longitudinal plates involving the marginal plate, the barbule plate, and the axial plate than in the center pulp of the feather follicles at E18 and E20. At the same time, quantitative analysis has confirmed the expressions of β-catenin mRNA were the highest among the samples at the varied stages (Figure 4A). This result corroborated the measurements detected by semiquantitative RT-PCR above. In the case of mature primary feather follicles, weak staining of β-catenin transcripts was observed at the region of barb ridges, whereas the sharp grains were restricted to the ramogenic and proliferation zones and dermal papilla within the follicles (marked with the arrowhead, Figure 3F). No expression was detected with the use of β-catenin and Shh sense probe (Figure 3B'' and 3G').
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, a similar observation to β-catenin (Figure 3A), but not continuously distributed as observed in Figure 3A. It was also observed that Shh signals mainly appear at the sites to form feather primordia. At E12, the grains of Shh transcripts tended to concentrate on the distal area of the short feather buds (Figure 3H), and then the intense expression of Shh was seen at the marginal and barbule plates inside the feather follicles (Figure 3I and 3J), unlike the expression pattern of β-catenin in feather buds at E18. However, at the later stages of feather bud development, expression patterns of Shh were almost similar spatially and temporally to those of β-catenin mRNA as observed in Figure 3E and 3F (plates not shown). Meanwhile, the quantitative analysis of β-catenin mRNA expression has shown that higher expression levels were observed at E18 and E20 than at the other stages, and there were no statistically significant differences in optical density measurements in grain areas of the β-catenin transcripts among the stages E10, E12, E25, and E30 (Figure 4A). Corresponding to it, expressions of Shh were measured, and the significant higher Shh mRNA levels were observed from E18 and E30 (Figure 4B). Previously, it was shown that Shh is expressed in the ectodermal placode of the feather bud only after initial differentiation of this structure has restricted responsiveness to Shh in the ectoderm (Morgan et al., 1998). Expression of Shh in the epidermis correlates with the initiation of hair and feather follicle formation; Shh mutant skin gave rise to large abnormal follicles containing a small dermal papilla (St-Jacques et al., 1998; McKinnell et al., 2004). The Shh signaling molecule as well as Wnt and fibroblast growth factor families are expressed during cutaneous appendage development and have been shown to play important roles in the communication between epithelial and mesenchymal cells (Ting-Berreth and Chuong, 1996; Millar, 2002). The misexpression of Shh signaling within the skin and hair follicle leads to highly abnormal development (Oro et al., 1997). Furthermore, the forced expression of Shh at a level similar to that observed during normal development has profoundly different effects on feather buds at different times in embryogenesis (Morgan et al., 1998), which can either lead to formation of large, disorganized ectodermal growths or induce ectopic feather bud development. In this study, compared with the expression patterns and functions of Shh in feather morphogenesis, the variety of β-catenin expression in the goose dorsal skin indicated that the expression pattern of β-catenin mRNA may be essential for promoting the normal development of embryonic feather bud. Further studies on the association of the spatial and temporal diversity of β-catenin expression with its regulating functions in the feather follicle development of geese are ongoing.
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ACKNOWLEDGMENTS |
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Received for publication May 17, 2007. Accepted for publication August 31, 2007.
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