Chicken sine oculis binding protein homolog (sobp), a novel gene
that may regulate feather development
W. Liu and N. Li1
State Key Laboratory for Agrobiotechnology, College of Biological Sciences,
China Agricultural University, Beijing 100193, China
ABSTRACT Feathers are appendages of skin in avians and provide a model for analyzing skin appendage morphogenesis. The feathers of Chinese Silky
(CS) and White Leghorn (WL) chickens have distinct
phenotypes. Based on preliminary genetic results, we
cloned the chicken gene sobp (encoding sine oculis binding protein homolog, which is expressed at a higher
level in the dorsal skin and in the feather follicle in the
WL compared with the CS. The reverse-transcription
PCR and quantitative real-time PCR indicated that
sobp was expressed in many tissues and was continuously expressed during embryonic development in both
strains. Northern and Western blotting indicated that
the mRNA of sobp was approximately 5 kb and the
SOBP protein was approximately 96 kDa. The expressions of signaling molecules that affect feather development were similar. This study is the first report of sobp
expression in chickens. Our results suggest that sobp
might regulate distinct feather type.
Key words: sobp, sine oculis binding protein homolog, differential expression, skin, chicken
2012 Poultry Science 91:1950–1955
http://dx.doi.org/10.3382/ps.2011-02114
INTRODUCTION
Avian feathers are derived from skin and play important roles in flying, protection, and communication.
There are many different forms, sizes, and colors of
feathers among birds. Feather development includes
processes such as induction, molting, differentiation,
and cell death. Feathers are composed of rachis, branches, and barbules (Widelitz et al., 2003). Several molecular signaling molecules affect feather morphogenesis, including wnts, bone morphogenic proteins (bmps), and
noggin (Lin et al., 2006). The bmps enhance the size
of the rachis, and noggin increases branching (Yu et
al., 2002). Several genes affect feather development; for
example, the expression of hex plays an important role
in the initiation of feather bud development (Obinata
and Akimoto, 2005), and chick delta-1 expression is associated with formation of feather primordia (Viallet
et al., 1998).
The chicken is an important avian model system and
is a powerful tool for studying development and disease
(Brown et al., 2003). In particular, the avian integument provides a model for analyzing skin appendage
morphogenesis (Chen and Chuong, 1999). The Chinese
Silky (CS) chicken strain, a Chinese local breed, has
©2012 Poultry Science Association Inc.
Received December 20, 2011.
Accepted April 3, 2012.
1 Corresponding author: [email protected]
a “silky” feather type, and the White Leghorn (WL)
chicken strain has a sheet-like feather type. The silky
feather is inherited as an autosomal complete recessive
characteristic and has been studied for almost 100 yr.
The fluffy type of feathers is caused by defective microscopic hooklets and can be found on the whole body
of Silky fowl. In our previous study, we located the
silkiness locus on chicken chromosome 3 and found no
recombination between the marker CAU0006 and the
silkiness locus. Marker CAU0006 is located within the
sobp gene (Gao, 2006; Gao et al., 2006). Based on these
results, we proposed sobp as a candidate gene associated with feather development.
The sobp gene (encoding sine oculis binding protein
homolog), also named jxc1, was first identified and
studied in mice. Spontaneous mutation of sobp in mice
increases the sound threshold, resulting in abnormal
hearing. The sobp gene also controls development of the
mouse organ of Corti (Chen et al., 2008). In mice, sobp
is expressed in many tissues, including the brain, lung,
and heart (Chen et al., 2008). In addition, mutated
sobp is highly expressed in the brain limbic system and
causes intellectual disability (Birk et al., 2010). Other
functions of sobp have not been described, and there
are no reports of sobp expression or function in other
species. The sobp gene has 6 exons, spanning a region of
chromosome 3 from 70.35 Mb to 70.47 Mb. Twelve gene
records of sobp-like sequences have been recorded in
GenBank, including sequences from mouse, rat, human,
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DIFFERENTIAL EXPRESSION OF sobp IN CHICKENS
dog, chicken, fly, Xenopus, horse, chimpanzee, cattle,
monkey, and Monodelphis domestica.
In this study, we describe the chicken sobp gene, including its homologous relationship among several species and its mRNA and protein size. We also report that
sobp expression is approximately 1-fold higher in the
dorsal skin of WL than in the dorsal skin of CS, during
all stages of incubation. In addition, sobp expression
is also 1-fold higher in the feather follicle of WL compared with the feather follicle of CS in adult chickens.
The expression of signaling molecules affecting feather
development, such as WNT5A, β-CATENIN, and SHH
was similar. Our results suggest the differential expression of sobp could be the reason for the distinct feather
types of WL and CS chickens.
MATERIALS AND METHODS
Experimental Birds
Thirty WL chicken eggs and 30 CS eggs were incubated and sampled at various developmental times
[embryonic day (E) 1, 2, 3, 4, 5, 6, 7, 8, 10, 12, 14,
16, and postnatal day (P) 1]. At E1, 2, 3, 4, 5, 6, and
7, whole embryos were collected from 3 chickens (WL
chicken and CS chicken) and kept in liquid nitrogen for
RNA extraction and real-time PCR. At E8, 10, 12, 14,
and 16, dorsal skin was collected from 3 chickens (WL
chicken and CS chicken) and kept in liquid nitrogen for
RNA extraction and real-time PCR.
sobp Gene Isolation
by Reverse-Transcription PCR
Total RNA was extracted from tissues (heart, brain,
lung, kidney, eye, and skin) from newborn WL and
CS using Trizol reagent (Tiagen, Beijing, China). The
chicken sobp gene was amplified by reverse-transcription (RT) PCR. Approximately 1 μg of total RNA was
used in first strand cDNA synthesis (M-MLV reverse
transcriptase, Invitrogen, Carlsbad, CA) with oligo
d(T)18 primers. The primers, 5′-AATGAGCTCCTTGGCTGGTA-3′ (forward) and 5′-ATA TGCTCTTCGGCA AGCTG-3′ (reverse), were used to amplify sobp.
The PCR conditions were denaturation at 94°C for 5
min, 32 cycles of denaturation at 94°C for 30 s, renaturation at 60°C for 30 s, extension at 72°C for 30 s,
and a final extension at 72°C for 7 min. The length of
the amplified fragment was 441 bp. The gapdh gene was
used as a control (gapdh forward primer: 5′-TGGGTGTCAACCATGAGAAA-3′; reverse primer: 5′-CAG
CAGCCTTCACTACCCTC-3′). The PCR procedure
was the same as for sobp.
Western Blot Analysis
Antigenic peptides, corresponding to the SOBP amino acid sequence from 504 to 729, were expressed in
Escherichia coli using vector pET-30a (Novagen, Ger-
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many). Polyclonal rabbit anti-chicken SOBP antibodies
were generated in our laboratory. To analyze the expression of SOBP, protein was extracted from the skin
of WL and CS chickens using cell lysis buffer for Western blot analysis and immunoprecipitation (Beyotime,
Shanghai, China). Concentrations were determined using a BCA protein assay kit (Beyotime). Protein (200
μg) was electrophoresed on a 10% SDS-PAGE gel, and
the separated proteins were transferred to a PVDF
membrane. The membrane was blocked with 5% skim
milk powder in TBST overnight at 4°C. The anti-SOBP
polyclonal antibody was diluted to 1:1,000, added to
the skim milk solution, and incubated for 1 h. Anti-βactin monoclonal antibody (Santa Cruz Biotechnology,
Santa Cruz, CA) was diluted to 1:1,000 and used as the
control. After washing with TBST 3 times, the blots
were incubated with horseradish peroxidase-conjugated secondary antibody diluted to 1:5,000 (Zhongshan
GoldenBridge Biotechnology Co. Ltd., Beijing, China).
The proteins were visualized with SuperSignal West
Pico (Thermo Scientific, Waltham, MA).
Analysis of sobp Expression
by Quantitative Real-Time PCR
Using the RNeasy fibrous tissue mini kit (Qiagen,
Germany), total RNA was extracted from WL and CS
chick embryos at E1 to E7, and total RNA from the
skin was separately extracted from chick embryos at E8,
E10, E12, E14, and E16. Approximately 300 ng of total
RNA was used for first strand cDNA synthesis (M-MLV
reverse transcriptase, Invitrogen), using oligo d(T)18
primers. β-actin was used as an internal reference to
verify successful reverse transcription and to normalize
the amount of cDNA amplified. Quantitative real-time
PCR was performed on an ABI 7900HT real-time PCR
system machine (Applied Biosystems Inc., Foster City,
CA). The cDNA in each sample was amplified 3 times
with SYBR Green PCR master mix (Applied Biosystems). The fold expression was determined as 2–∆∆Ct.
The primers for β-actin were 5′-GCCCATCTATGAAGGCTACG-3′ (forward) and reverse 5′-TCCTTGATGTCACGCACAAT-3′ (reverse). The primers for
sobp were 5′-CGCCAGCACATTTCTGTTCTC-3′ (forward) and 5′-AGCCCTGGGTAGCTT GTGTTT-3′
(reverse). Using the software Primer3 (Applied Biosystems), PCR primers were designed to amplify the
target cDNA.
Northern Blot Analysis
Total RNA was extracted from WL and CS tissues
with Trizol reagent (Invitrogen). A total of 30 μg of
RNA was fractionated on a denaturing 1% agarose gel
containing formaldehyde, transferred to Hybond N+
membrane with the capillary method and Northernmax transfer buffer (Ambion, Austin, TX) and fixed
with UV cross-linking. The membrane was probed with
32P-labeled standard DNA that was complementary to
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Liu and Li
the target RNA. Template DNA (50 ng) was labeled
with [α-32P]dCTP with Klenow DNA polymerase and
random primers (Promega, Fitchburg, WI). Prehybridization and hybridization were carried out in ultra-sensitive hybridization buffer (Ambion) at 45°C for 24 h
in total. After hybridization, membranes were washed
at low stringency in 2× saline sodium citrate (SSC),
0.1% SDS at 45°C for 10 min, at medium stringency
in 1× SSC, 0.1% SDS at 45°C for 10 min, and at high
stringency in 0.5× SSC, 0.1% SDS at 45°C for 10 min.
18s rRNA was used in the Northern blot analysis as
an internal RNA loading control. The gray level was
calculated with Quantity One software (Bio-Rad, Hercules, CA).
In Situ Hybridization
The sobp hybridization probe was amplified from
cDNA by PCR and cloned into the pGEM-T easy vector (Promega). The primers were 5′-AAGCTTCCTTGGCTGGTA TGG TTA TG-3′ (forward) and
5′-GGATCCTCTTCTGCTGGTGGCTTTAT-3′ (reverse). The underlined sequences represent the restriction enzyme sites of HindIII and BamHI. The dorsal
skin at P38 was collected and immediately stored in
liquid nitrogen. In situ hybridization was performed on
4% paraformaldehyde-fixed 8-μm frozen sections with
DIG-labeled sobp probes (Roche, Switzerland). Images
were acquired with a Leica 2500 microscope.
Immunohistochemical Analysis
The antibodies used were as follows anti-SOBP
(1:50), anti-β-CATENIN (1:50; Abcam), anti-SHH
(1:50; Abcam), anti-WNT5A (1:50; Abcam). Secondary antibodies and labeled streptavidin-peroxidase were
purchased from Zhongshan Goldbridge Biotechnology
Co. Ltd. (Beijing, China). Images were acquired with
the Image Plus system (Olympus Corp., Ina, Japan).
The expression levels of every targeted gene were calculated using the software Image-Pro Plus (Media Cybernetics, Bethesda, MD).
RESULTS
RT-PCR Analysis of sobp Expression
and Differential Expression
in Skin by Western Blotting
The expression level and relative mRNA abundance
of sobp in tissues were measured. The RT-PCR analysis
showed that sobp was expressed in the heart, brain,
lung, kidney, eye, and skin (Figure 1B). The sobp gene
was expressed at its highest level in the brain, lung, and
skin of WL and the heart and brain of CS. However,
the expression profile of sobp in other tissues was different between the 2 strains. The level of sobp in skin
was higher in WL than in CS (Figure 1B). Using our
Figure 1. Expression analysis by reverse-transcription (RT) PCR
and Western blotting. A) RT-PCR analysis of sobp expression in tissues. The upper panel shows sobp expression profiles in different tissues between White Leghorn and Chinese Silky chickens. The lower
panel shows gapdh expression as a control. B) Western blot analysis
of SOBP in the skin of both chicken types. The SOBP protein was
detected in the skin of both chicken strains, and SOBP was expressed
differentially between White Leghorn and Chinese Silky chickens. The
size of SOBP was approximately 96 kDa.
polyclonal antibody, SOBP was detected in the skin of
both WL and CS. In addition, SOBP was differentially expressed in skin between WL and CS. The size of
SOBP was approximately 96 kDa, which matched that
deduced from the predicted translation of the cDNA
sequence (Figure 1C).
sobp Expression Levels in Embryos, Skin,
and Other Tissues During Development
We investigated the relative expression levels of sobp
mRNA in whole embryos, skin, and other tissues at
different developmental stages. Expression of sobp transcripts in whole embryos differed between WL and CS.
At E3 and E5, sobp expression levels between WL and
CS chickens were significantly different (Figure 2A). In
skin, sobp expression levels were significantly different
at E8, E12, and E14, and sobp was expressed at least
approximately 1-fold higher in the skin of WL than
in the skin of CS during embryo development (Figure
2B). The distribution of sobp expression and relative
mRNA abundance in embryonic tissues were also assessed using Northern blot analysis. The sobp gene was
expressed in the heart, brain, lung, kidney, and eye in
both WL and CS (Figure 3A). The sobp gene expression was highest in CS heart tissue, and its expression
in skin during embryonic development was different between the 2 strains. Expression in WL skin was clearly
higher than the expression in CS skin (Figure 3B). Using gray level analysis, the values for WL were almost
DIFFERENTIAL EXPRESSION OF sobp IN CHICKENS
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Immunohistochemistry of Signaling
Molecules Associated with Feather
Development
Several signaling molecules are associated with feather development, including sonic hedgehog (shh), wnt5a, and β-catenin (Lin et al., 2006). We located and
examined the expression of these molecules in dorsal
skin using immunohistochemistry on tissues collected
at P38. The tissues sections represent approximately
the same section for every gene examined. The SOBP
and WNT5A proteins were localized similarly, and were
expressed in the whole feather follicle, including the
stratum corneum, germinal layer, feather pulp, the wall
of the feather follicle, and the feather bulb. The SHH
protein is expressed in the stratum corneum, germinal
layer and the feather bulb. The β-CATENIN protein
is mainly expressed in the wall of feather follicle. The
expression level of SOBP was 1-fold higher in feather
follicle of WL than in the CS (Figure 5). Although
SOBP expression levels differed between strains, the
expression levels of WNT5A, β-CATENIN, and SHH
did not differ (Figure 5).
DISCUSSION
Following the result of genetic mapping, the chicken
gene sobp was cloned and characterized. Skin development is initiated at E8 in chickens (Widelitz et al.,
Figure 2. Quantitative real-time PCR analysis of sobp expression
during development. A) sobp expression levels in embryos at different
developmental stages. At embryo day (E)3 and E5, sobp expression
levels between White Leghorn and Chinese Silky chickens were significantly different (*P < 0.05, **P < 0.01). B) sobp expression levels in
skin at different developmental stages. Embryo skin was collected at
E8, E10, E12, E14, and E16 from White Leghorn and Chinese Silky
chickens. At E8 and E14, the difference in expression was significant
(**P < 0.01). At E12, the difference in expression was borderline
significant (*P < 0.05). The data are the means ± SD from triplicate
samples in 3 separate experiments. A statistical t-test was used to
compare the sobp mRNA levels between the White Leghorn and Chinese Silky chickens. Color version available in the online PDF.
1-fold higher than in CS. The size of the sobp mRNA
detected in these studies was approximately 5 kb.
Differential Expression of sobp in Feather
Follicles Between WL and CS Chickens
After the first molting, the covered feathers were obviously different between the 2 types of chicken, whereas those in the primary regimens region were similar.
The feather of dorsal skin at P38 was clearly different
between the strains (Figure 4A). At later stages, differences in expression were verified with in situ hybridization, and differences in skin were clearly seen (Figure
4B). The sobp gene was localized similarly between WL
and CS, and it was expressed in the whole feather follicle, including the stratum corneum, germinal layer,
feather pulp, the wall of the feather follicle, and the
feather bulb (Figure 4B).
Figure 3. Northern blot analysis of tissue sobp expression in White
Leghorn chickens compared with Chinese Silky chickens. A) sobp expression profiles of White Leghorn and Chinese Silky tissues. B) Expression of sobp in White Leghorn and Chinese Silky skin at embryo
day (E)10, E12, E14, and E16 and in the newborn (E21). The last panel shows analysis of the gray scale between White Leghorn and Chinese
Silky chickens. The size of sobp mRNA detected in these studies was
approximately 5 kb. 18S rRNA was used as the internal control.
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Liu and Li
Figure 4. Differential sobp expression in skin between White Leghorn chickens and Chinese Silky chickens using in situ hybridization
of feather follicles. A) Feather phenotype varieties on the dorsum in
White Leghorn and Chinese Silky chickens at P38. B) In situ hybridization of feather follicles in White Leghorn and Chinese Silky chickens. The sobp gene was localized similarly between White Leghorn and
Chinese Silky and expressed in the whole feather follicle, including
the stratum corneum germinal layer, the feather pulp, the wall of the
feather follicle, and the feather bulb. Key: 1 = the wall of the feather
follicle; 2 = the stratum corneum and germinal layer; 3 = the feather
pulp; and 4 = the feather bulb. The brown-yellow signal is the positive signal.
2003). At E8, E12, E14, sobp was expressed at least
approximately 1-fold higher in the skin of WL than in
the skin of CS during embryo development and was expressed 1-fold higher in the feather follicle of WL than
in CS in the adult chicken.
At the RNA and protein levels, differences in sobp
expression were clearly seen. Given that the shape of
WL and CS feathers are quite distinct, our results suggest that the differential expression of sobp may be the
reason for the distinct feather shapes.
Does the differential expression of sobp affect the expression of other genes? Several signaling molecules are
involved in feather morphogenesis, such as WNT5A,
SHH, and β-CATENIN. The SHH protein mediates
key interactions between the epithelium and the mesenchyme during early feather development (Ting-Berreth and Chuong, 1996). Furthermore, wnt genes have
roles in hair follicle development (Chuong et al., 1996;
Figure 5. Immunohistochemical analysis of signaling molecules.
A) Expressions of SOBP and signaling molecules that affect feather
development were analyzed by immunohistochemistry. Key: 1 = the
wall of the feather follicle; 2 = the stratum corneum and germinal
layer; 3 = the feather pulp; and 4 = the feather bulb. The brownyellow signal is the positive signal. B) The expression levels of SOBP
and signaling molecules that affect feather development were analyzed
using the software Image-Pro Plus (Media Cybernetics, Bethesda,
MD). The expression of SOBP was significantly different between the
2 strains (*P < 0.05). The expression of SOBP was twice as high in the
feather follicle of White Leghorns as in the feather follicle of Chinese
Silkies. However, signaling molecules that affect feather development
(WNT5A, SHH, and β-CATENIN) do not differ significantly between
White Leghorns and Chinese Silkies. The data are the means ± SD
from triplicate samples in 3 separate experiments. A statistical t-test
was used to compare the expression level between the White Leghorn
and Chinese Silky chickens.
DIFFERENTIAL EXPRESSION OF sobp IN CHICKENS
Olivera-Martinez et al., 2001; Tanda et al., 1995), and
WNT5A is a target of SHH in hair follicles (Reddy et
al., 2001). β-CATENIN signaling can initiate feather
bud development (Noramly et al., 1999) and is associated with the conversion of part of the avian foot scales
into feather buds (Widelitz et al., 2000). In this study,
the expression of WNT5A, SHH, and β-CATENIN
were examined by immunohistochemistry. However, no
differences were observed between the 2 strains tested.
Other signaling molecules involved in feather morphogenesis, such as bmps (Harris et al., 2002; Botchkarev
and Sharov, 2004) and FGFs (Tao et al., 2002; Mandler
and Neubüser, 2004; Song et al., 2004), may interact
with sobp directly or indirectly, leading to the distinct
feather phenotype.
In a recent study, a genomic region showing significant association with silky feathers was identified
on chicken chromosome 3, between the SNP markers
rs16287115 and rs14371625, spanning the genome from
64.5 Mb to 69.7 Mb (Dorshorst et al., 2010). The map
location of sobp is close to, but outside of, the mapping
interval indicated by Dorshorst, which suggests the
presence of another gene affecting feather morphology.
Whether sobp indeed regulates feather development
should be the subject of further studies. For example,
functional complementation assays should be performed by knockdown of sobp expression in WL and
overexpression of sobp in CS and their effect on feather
phenotype recorded.
ACKNOWLEDGMENTS
This study was supported by research grants from
the National Program on Key Basic Research Project
(973 Program; Grant No. 2006CB102100).
REFERENCES
Birk, E., A. H. Zahav, C. M. Manzini, M. P. Chor, L. Kornreich, C.
A. Walsh, K. N. Trauth, A. A. A. J. Simon, L. Colleaux, Y. M.
L. Rainshtein, D. J. Tischfield, P. Wang, N. Magal, I. Maya, N.
Shoshani, G. Rechavi, D. Gothelf, G. Maydan, M. Shohat, and L.
B. Vanagaite. 2010. SOBP is mutated in syndromic and nonsyndromic intellectual disability and is highly expressed in the brain
limbic system. Am. J. Hum. Genet. 87:694–700.
Botchkarev, V. A., and A. A. Sharov. 2004. BMP signaling in the
control of skin development and hair follicle growth. Differentiation 72:512–526.
Brown, W. R. A., S. J. Hubbard, C. Tickle, and S. A. Wilson. 2003.
The chicken as a model for large scale analysis of vertebrate gene
function. Nat. Rev. Genet. 4:87–98.
Chen, C. W., and C. M. Chuong. 1999. Avian integument provides
multiple possibilities to analyze different phases of skin appendage morphogenesis. J. Investig. Dermatol. Symp. Proc. 4:333–
337.
Chen, Z., M. Montcouquiol, R. Calderon, N. A. Jenkins, N. G. Copeland, M. W. Kelle, and K. N. Trauth. 2008. Jxc1/Sobp, encoding
1955
a nuclear zinc finger protein, is critical for cochlear growth, cell
fate, and patterning of the organ of Corti. J. Neurosci. 28:6633–
6641.
Chuong, C. M., R. Widelitz, S. Ting Berreth, and T. Jiang. 1996.
Early events during avian skin appendage regeneration: dependence on epithelial-mesenchymal interaction and order of molecular reappearance. J. Invest. Dermatol. 107:639–646.
Dorshorst, B., R. Okimoto, and C. Ashwell. 2010. Genomic regions
associated with dermal hyperpigmentation, polydactyly and other
morphological traits in the silkie chicken. J. Hered. 101:339–350.
Gao, Y. 2006. Mapping and candidate gene analysis for important
traits loci in chicken. PhD Diss. China Agricultural University,
Beijing, China.
Gao, Y., Z. Du, X. Hu, X. Deng, Y. Huang, and N. Li. 2006. Fine
mapping the silkiness locus of the chicken with microsatellite
molecular markers to chromosome 3. Proceedings of the 30th International Conference on Animal Genetics. Section B:49. Porto
Seguro, BA, Brazil.
Harris, M. P., J. F. Fallon, and R. O. Prum. 2002. Shh-Bmp2 signaling module and the evolutionary origin and diversification of
feathers. J. Exp. Zool. 294:160–176.
Lin, C. M., T. X. Jiang, R. B. Widelitz, and C. M. Chuong. 2006.
Molecular signaling in feather morphogenesis. Curr. Opin. Cell
Biol. 18:730–741.
Mandler, M., and A. Neubüser. 2004. FGF signaling is required for
initiation of feather placode. Development 131:3333–3343.
Noramly, S., A. Freeman, and B. Morgan. 1999. Beta-catenin signaling can initiate feather bud development. Development
126:3509–3521.
Obinata, A., and Y. Akimoto. 2005. Expression of Hex during feather bud development. Int. J. Dev. Biol. 49:885–890.
Olivera-Martinez, I., J. Thélu, M. Teillet, and D. Dhouailly. 2001.
Dorsal dermis development depends on a signal from the dorsal
neural tube, which can be substituted by Wnt-1. Mech. Dev.
100:233–244.
Reddy, S., T. Andla, A. Bagasraa, M. M. Lub, D. J. Epsteinc, E. E.
Morriseyb, and S. E. Millar. 2001. Characterization of Wnt gene
expression in developing and postnatal hair follicles and identification of Wnt5a as a target of Sonic hedgehog in hair follicle
morphogenesis. Mech. Dev. 107:69–82.
Song, H. K., S. H. Lee, and P. F. Goetinck. 2004. FGF-2 signaling is
sufficient to induce dermal condensations during feather development. Dev. Dyn. 231:741–749.
Tanda, N., H. Ohuchi, H. Yoshioka, S. Noji, and T. Nohno. 1995.
A chicken Wnt gene, Wnt-11, is involved in dermal development.
Biochem. Biophys. Res. Commun. 211:123–129.
Tao, H., Y. Yoshimoto, H. Yoshioka, T. Nohno, S. Noji, and H.
Ohuchi. 2002. FGF10 is a mesenchymally derived stimulator for
epidermal development in the chick embryonic skin. Mech. Dev.
116:39–49.
Ting-Berreth, S. A., and C. M. Chuong. 1996. Sonic hedgehog in
feather morphogenesis: Induction of mesenchymal condensation
and association with cell death. Dev. Dyn. 207:157–170.
Viallet, J. P., F. Prin, I. Oliviera-Martinez, E. Hirsinger, O. Pourquié,
and D. Dhouailly. 1998. Chick Delta-1 gene expression and the
formation of the feather primordia. Mech. Dev. 72:159–168.
Widelitz, R. B., T. Jiang, J. Lu, and C. Chuong. 2000. Beta-catenin
in epithelial morphogenesis: Conversion of part of avian foot
scales into feather buds with a mutated beta-catenin. Dev. Biol.
219:98–114.
Widelitz, R. B., T. X. Jiang, M. Yu, T. Shen, J. Y. Shen, P. Wu, Z.
Yu, and C. M. Chuong. 2003. Molecular biology of feather morphogenesis: A testable model for evo-devo research. J. Exp. Zool.
Mol. Dev. Evol. 298:109–122.
Yu, M., P. Wu, R. B. Widelitz, and C. M. Chuong. 2002. The morphogenesis of feathers. Nature 420:308–312.