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Role of IGFBPs in the morphogenesis of lingual papillae.

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THE ANATOMICAL RECORD PART A 286A:841– 847 (2005)
Role of IGFBPs in the Morphogenesis
of Lingual Papillae
YUKO SUZUKI*
Department of Oral Anatomy, School of Dentistry, Health Sciences University of
Hokkaido, Ishikari-Tobetsu, Japan
ABSTRACT
The expression of insulin-like growth factor binding proteins (IGFBPs)
during the morphogenesis of lingual papillae of mice was examined by in
situ hybridization. Among seven mouse IGFBPs, IGFBP-1, -6, and -7 mRNAs were not expressed in the tongue tissue. At E12, though no papillae
have formed yet, IGFBP-2, -4, and -5 were expressed in the entire tongue
epithelium. At E14, fungiform papillae appeared in the anterior region and
circumvallate papillae were distinguished in the posterior region. Strong
expression of IGFBP-5 was observed in the apical region of both fungiform
and circumvallate papillae. At this stage, the epithelial elevation of filiform
papillae was not clear; but IGFBP-5 was expressed in the apex. At E15,
foliate papillae were distinguished and IGFBP-5 was expressed in the
dorsal epithelium of ridges. In filiform papillae, IGFBP-3 was expressed in
the core of the connective tissue. At E17, the expression of IGFBP-5 disappeared from the apical region of fungiform, filiform, foliate, and circumvallate papillae, whereas that of IGFBP-2 remained. This finding suggests that
IGFBP-5 and -2 function to cause evagination of the epithelium into a raised
structure. In the epithelium of trenches of foliate and circumvallate papillae, strong expression of IGFBP-4 was observed at E15 and E17. As previously suggested from a study on postnatal mice (Suzuki et al. J Comp
Neurol 2005;482:74 – 84), IGFBP-4 acts in the epithelial invagination to
form the trenches, grooves, or furrows of lingual papillae during development. © 2005 Wiley-Liss, Inc.
Key words: insulin-like growth factor binding protein; in situ
hybridization; fungiform papillae; circumvallate
papillae; filiform papillae
The dorsal surface of the mammalian tongue is covered
with four kinds of papillae: fungiform, circumvallate, foliate, and filiform. These papillae are distributed in a specific pattern over the tongue in mice: fungiform and filiform papillae are located on the anterior two-thirds of the
tongue. The fungiform papillae have a mushroom-shaped
structure, composed of a multilayered epithelium and
mesenchymal core (Farbman and Mbiene, 1991). Filiform
papillae are small conical surface projections found in
great numbers among the fungiform papillae (Baratz and
Farbman, 1975). Foliate papillae are located on the posterior lateral margins of the tongue, and circumvallate
papillae on the posterior midline. Foliate papillae consist
of several ridges that alternate with deep grooves in the
mucosa. In mice and rats, single circumvallate papilla is
present in the middle part of the terminal sulcus and it is
surrounded by a deep circular groove into which open the
©
2005 WILEY-LISS, INC.
von Ebner’s glands. Except for the filiform papillae, these
papillae contain taste buds (Nosrat et al., 1997).
Grant sponsor: Academic Frontier Project for Private Universities; Grant sponsor: mathcing fund pubsidy from MEXT (Ministry of Education, Culture, Sports, Science, and Technology),
2002-2006.
*Correspondence to: Yuko Suzuki, Department of Oral Anatomy, School of Dentistry, Health Sciences University of Hokkaido, Ishikari-Tobetsu 061-0293, Japan. Fax: 81-1332-3-1236.
E-mail: suzuki@hoku-iryo-u.ac.jp
Received 21 February 2005; Accepted 11 April 2005
DOI 10.1002/ar.a.20219
Published online 27 July 2005 in Wiley InterScience
(www.interscience.wiley.com).
842
SUZUKI
Several signaling molecules regulate the morphogenesis
of the papillae. For example, sonic hedgehog (Shh) is expressed only in the dorsal surface of fungiform papillae
during embryonic days 13–18 (Hall et al., 1999, 2003;
Jung et al., 2004), and its signal disruption alters the
number and location of fungiform papillae (Hall et al.,
2003; Liu et al., 2004). In pax 9-deficient mice, a cornified
layer is absent, thus filiform papillae lack anterior-posterior polarity (Jonker et al., 2004). In mice knocked out for
brain-derived neurotrophic factor (BDNF) and its receptor
TrkB, fungiform, foliate, and circumvallate papillae are
smaller or have an aberrant morphology or both (Nosrat et
al., 1997; Oakley et al., 1998; Mistretta et al., 1999).
In our previous study, insulin-like growth factor binding
protein (IGFBP)-4, a member of the family of insulin-like
growth factor (IGF) and related molecules, was expressed
in the bottom of the trenches of circumvallate papillae of
postnatal day 2 mice, suggesting that it regulates the
down-growth of grooves (Suzuki et al., 2005). The IGF
family comprises IGF-I, IGF-II, their receptors (IGF-IR,
IGF-IIR), and seven high-affinity IGFBPs. The actions of
these IGFs appear to be regulated and coordinated by a
family of IGFBPs. The IGFBPs are thought to have four
major functions that are essential to the regulation and
coordination of the biological activities of IGFs. That is,
IGFBPs are considered to act as transport proteins in
plasma and to control the efflux of IGFs from the vascular
space; to prevent IGFs from being degraded and to prolong
the half-lives of IGFs; to provide a means of tissue and cell
type-specific localization; and to modulate directly the interaction of the IGFs with their receptors and thereby
indirectly control their biological actions (Duan, 2002).
Recent evidence suggests that the IGFBPs can also have
direct IGF-independent actions on cellular functions
(Zhou et al., 2003). All lingual papillae begin as epithelial
thickenings and then evaginate to form raised papillae
with a mesenchymal core during embryonic development
(cf. Farbman and Mbiene, 1991). Because IGF-I and -II
are known to be expressed in the embryonic tongue in rats
(Ayer-LeLievre et al., 1991) and in mice (Ferguson et al.,
1992; Yamane et al., 2000), the IGF family has been suggested to regulate the morphogenesis of the lingual papillae. The aim of this article was to examine the expression
of IGFBPs during embryonic development of lingual papillae.
MATERIALS AND METHODS
Animals
Timed pregnant ddY mice, were obtained from Sankyo
Laboratories (Tokyo, Japan). They were maintained in a
heat- and humidity-controlled vivarium with food and water provided ad libitum. Experimental protocols concerning animal handling were reviewed and approved by the
Institutional Animal Care Committee of the Health Sciences University of Hokkaido.
Tissue Preparation
The day of appearance of vaginal plug was designated
as E0. The study was conducted on 12 pregnant female
mice. To obtain embryos, mice were killed by cervical
dislocation and their uteri with fetuses (E12–17) carefully
dissected out. For in situ hybridization, the tongues were
fixed with 4% paraformaldehyde in 0.1 M phosphate
buffer (pH 7.4) overnight at 4°C. For immunohistochem-
istry, the tongues were fixed with periodate-lysine-paraformaldehyde (PLP) solution. Each specimen was washed
in phosphate-buffered saline (PBS) solution, cryoprotected
with 25% sucrose, and embedded in OCT compound
(Oken, Tokyo, Japan). The tissues were sectioned coronally at a thickness of 8 –10 ␮m. Sections were collected
and placed on silane-coated slides.
RNA Probes and In Situ Hybridization
cDNA fragments of IGF-IR, IGFBP-2, IGFBP-3, IGFBP-4, IGFBP-5, IGFBP-6, and IGFBP-7 were generated
by reverse transcription-polymerase chain reaction (RTPCR) using total RNA extracted from the tongue and then
used for the synthesis of cRNA probes. The sequences of
the primers were as follows: 5⬘-TCTCTCTCTGGCCGACGAGT-3⬘ and 5⬘-GAGCAGAAGTCACCGAATCG-3⬘ (977
bp; AF056187) for IGF-IR; 5⬘-GACGCTACGCTGCTATCCCA-3⬘ and 5⬘-GTCTCCTGCTGCTCGTTGTA-3⬘ (614 bp;
NM008342) for IGFBP-2; 5⬘-GGAAACATCAGTGAGTCCGA-3⬘ and 5⬘-GCTGAGGCAATGTACGTCGT-3⬘ (458 bp;
X8158.1) for IGFBP-3; 5⬘-GGAGAAGCCCCTGCGTACAT-3⬘ and 5⬘-ACCCCTGTCTTCCGATCCAC-3⬘ (434 bp;
X76066)
for
IGFBP-4;
5⬘-AGTAACGTTGAGTGACGCGT-3⬘ and 5⬘-CAGTGTTGGGGGTGCGTACT-3⬘
(750 bp; L12447) for IGFBP-5; 5⬘-TAATGCTGTTGTTCGCTGCG-3⬘ and 5⬘-CACTGCTGCTTGCGGTAGAA-3⬘
(552 bp; NM008344) for IGFBP-6; and 5⬘-AAGGTCCTTCCATAGTGACG-3⬘ and 5⬘-CAGGGTTATAGCTGTCGGCT-3⬘ (439 bp; NM008048) for IGFBP-7. The PCR was
carried out for 35 cycles. Each resulting fragment was
cloned into HindIII/EcoRI sites of pT7/T3 DH5␣-FT (Invitrogen, Tokyo, Japan) and sequenced. Digoxigenin
(DIG)-labeled antisense and sense probes were produced
by use of an RNA transcription kit (Roche Diagnostics,
Mannheim, Germany). Sections were washed in PBS and
treated for 20 min with 0.2 N HCl and for 15–20 min with
proteinase K (1 ␮g/ml in PBS; Takara, Kyoto, Japan) at
37°C. Next, the sections were washed in PBS and refixed
with 4% paraformaldehyde in 0.1 M phosphate buffer for
20 min. After having been washed twice in PBS, the sections were air-dried and hybridized. Hybridization was
performed at 47°C for 16 hr with an RNA probe in a
hybridization solution containing 50% formamide, 0.3 M
NaCl, 0.02 M Tris-HCl, 1 mM EDTA, 10% dextran sulfate,
1 ⫻ Denhardt’s solution, 1 mg/ml yeast tRNA, and 0.02%
SDS. Hybridized sections were washed at 47°C in a solution containing 50% formamide and 2 ⫻ SSC for 1 hr, and
thereafter twice in 2 ⫻ SSC for 5 min each time. Then they
were treated with 20 ␮g/ml of RNase (TypeII-A; Sigma) at
37°C for 30 min and washed at 47°C in 50% formamide/
2XSSC followed by 50% formamide/1 ⫻ SSC for 1 hr for
each. After having been washed three times in PBS, the
sections were incubated with 1% blocking reagent
(Boeringer Mannheim, Mannheim, Germany) in maleic
acid buffer (pH 7.5) for 1 hr at room temperature. Subsequently, they were incubated overnight at 4°C with alkaline phosphatase-conjugated anti-DIG Fab fragments diluted 1:500 in PBS. After three washes in PBS,
chromogenic reactions were carried out by using NBT/
BCIP (Boeringer).
Immunohistochemistry
The sections were incubated in a blocking solution
(Dako Protein Block Serum-Free; Dako, Carpinteria, CA)
843
ROLE OF IGFBP
for 10 min at room temperature. Then the sections were
incubated overnight at 4°C with antirabbit PGP9.5 antibody (Ultraclone, Isle of Wight, U.K.), diluted 1:100 in
PBS. After having been washed in PBS, the sections were
treated with Alexa Fluor 594-conjugated donkey antirabbit IgG (Molecular Probes, Eugene, OR) for 2 hr at room
temperature. Sections were viewed with a Leica confocal
laser scanning microscope.
RESULTS
Among IGFBPs, it was reported that IGFBP-1 mRNA
was detected only in adult liver tissue (Suzuki et al., 2005)
and so it was not examined in the present study. IGFBP-6
and -7 mRNAs were not expressed in tongue tissue by in
situ hybridization in the present study. Immunohistochemically IGFBP-6 was detected in the nerve fibers innervating the taste buds of circumvallate papillae (Suzuki
et al., 2005). IGFBP-7 was specifically expressed in developing lens (not shown). Therefore, IGFBP-2, -3, -4, and -5
mRNAs were detected in the developing tongue.
At embryonic day (E) 12, the early fetal tongue has a
relatively homogeneous epithelium with no obvious papillary structure. Among IGFBPs, IGFBP-2 was expressed
in the entire lingual epithelium (Fig. 1A); IGFBP-5 was
expressed in the lingual epithelium and in myoblast cells
(Fig. 1B). IGFBP-4 was expressed in the entire lingual
epithelium and mesenchyme (not shown). IGFBP-3 was
not detected in the tongue epithelium but was found in
some mesenchymal cells (Fig. 1C).
Fungiform and Filiform Papillae
At E14, in the anterior region of tongue, the developing
fungiform papillae were small and slightly elevated into
the oral cavity. They also contained a small amount of
connective tissue in their medullary core. IGFBP-2 and -4
were expressed in the epithelium of both fungiform papillae and nonpapilla tongue tissue. IGFBP-4 was expressed
also in the mesenchyme (Fig. 1D). IGF-IR expression was
observed in the tongue epithelium throughout the embryonic stages (Fig. 1E). IGFBP-5 was intensely expressed in
the fungiform papillae (Fig. 1F). Although the surface of
the tongue remained flat, IGFBP-5 was expressed also in
the presumed filiform papillae, which were interspersed
with fungiform papillae (Fig. 1F). At E15, regularly
spaced dermal papillae appeared in the presumptive filiform papillae. Expression of IGFBP-5 was observed in the
apical to middle region of the filiform epithelium (Fig. 1G),
and IGFBP-3 was expressed in mesenchymal core (Fig.
1H). At E17, the filiform papillae start to form a cornified
layer in the epithelium, which exhibit anterior-posterior
polarity. IGFBP-3 was expressed in the core of these papillae (Fig. 1I). In fungiform papillae, expression of IGFBP-3 was weak (Fig. 1I, inset). IGFBP-2 was expressed
in the basal layer of the epithelium in the anterior region
of each filiform papilla (Fig. 1J) and in the apex of the
fungiform papillae (Fig. 1K). The expression of IGFBP-4
and IGFBP-5 had mostly disappeared from the anterior
tongue epithelium by E17 (Fig. 1L and M).
Circumvallate Papillae
At E14 in the posterior region of the tongue, circumvallate papillae were observed to have epithelial elevations
and shallow grooves. IGFBP-2 was expressed in the entire
epithelium of these papillae (Fig. 2A). IGFBP-5 was ex-
pressed in the elevated epithelium of papillae but not in
the grooves (Fig. 2B). At E15, IGFBP-3 was expressed in a
few cells of mesenchymal core (Fig. 2C). IGFBP-4 was
intensely expressed in the bottom of the grooves (Fig. 2D).
IGF-IR expression was observed in the epithelium
throughout the embryonic stages (Fig. 2E). At E17, the
circumvallate papillae were more developed. The trench
grooves had deepened further into the underlying mesenchyme, and IGFBP-2 expression had become restricted to
the elevated epithelium of the papillae (Fig. 2F). Intense
expression of IGFBP-4 was still observed in the epithelium of the bottom of the trenches, and IGFBP-4 was
expressed also in minor salivary glands, von Ebner’s
glands (Fig. 2G). IGFBP-5 expression had mostly disappeared from the epithelium of the circumvallate papillae,
but it was expressed in presumptive taste buds and some
epithelial cells at the boundary with the connective tissue
(Fig. 2H). At this stage, numerous PGP9.5-positive nerve
fibers entered the circumvallate papillae, and a few taste
buds were located at the top of the papillae (Fig. 2I).
Foliate Papillae
At E15, foliate papillae were observed in the margin of
the posterior region of tongue. At this stage, IGFBP-4 was
intensely expressed in the shallow grooves among the
ridges (Fig. 3A). IGFBP-5 was expressed in the dorsal
epithelium of papillae but not in the grooves (Fig. 3B).
IGF-IR expression was observed in the epithelium
throughout the embryonic stages (Fig. 3C). The expression
of IGFBP-2 was observed in the entire epithelium of papillae at E15 and had restricted to the dorsal epithelium of
the papillae at E17 (Fig. 3D). At E17, IGFBP-3 was
weakly expressed in the mesenchyme (Fig. 3E). At this
stage, intense expression of IGFBP-4 was still observed in
the bottom of grooves (Fig. 3F). These results were summarized in Table 1.
DISCUSSION
In the embryonic tongue of mice, IGF-I and -II were
earlier found by immunohistochemical means to be expressed in the dorsal epithelium and muscles (Yamane et
al., 2000). By in situ hybridization, high levels of IGF-II
mRNA were found in the mesenchyme, muscles, and connective tissue of the embryonic tongues of mice (Ferguson
et al., 1992) and rats (Ayer-LeLievre et al., 1991). The
expression of IGF-I mRNA in the embryonic rat tongue
was weak, and thus its localization was not clear (AyerLeLievre et al., 1991). IGF-1 and -II bind to the receptor
IGF-IR. IGF-IIR has no known growth-mediating effects
and may simply act as a cell-surface depot for storage of
ligand (cf. Zhou et al., 2003). In the present study, IGF-IR
mRNA was expressed weakly in lingual epithelium, including the papillae. Therefore, IGFs may function to
cause the morphogenesis of the lingual papillae through
IGF-IR, acting in an autocrine or paracrine manner. However, the expression of these molecules was not restricted
to the lingual papillae. The present study revealed specific
expression patterns of IGFBP-2, -3, -4, and -5 in the lingual papillae at E14 –17. Morphogenesis of lingual papillae includes a series of evaginations and invaginations,
which are coordinated interactions between the epithelium and underlying connective tissue. In fact, proliferating cells were observed in the apex of epithelium, trench
grooves, and core of connective tissue of the developing
844
SUZUKI
Fig. 1. Expression of IGFBP mRNAs in developing fungiform and
filiform papillae of the mouse tongue detected by in situ hybridization
with RNA probes. A–C: E12 tongue showing IGFBP-2 (A), IGFBP-5 (B),
and IGFBP-3 (C) expressions. D–F: E14 tongue showing IGFBP-4 (D),
IGF-IR (E), and IGFBP-5 (F) expressions. Expressions of IGFBP-4 and
IGF-IR are seen in the epithelium and mesenchyme including fungiform
papillae (fu in D and E). Note the intense expression of IGFBP-5 in the
apex of fungiform (fu) and filiform (fi) papillae (F). G and H: E15 tongue
showing mRNA expression of IGFBP-5 (G) and IGFBP-3 (H). IGFBP-3 is
expressed in the mesenchymal core of presumptive filiform papillae (H).
I–M: E17 tongue showing IGFBP-3 (I), IGFBP-2 (J, K), IGFBP-4 (L), and
IGFBP-5 m RNA (M) expression. Cornified surface of each filiform papilla
(fi) is seen (I). IGFBP-3 is expressed in the mesenchymal core of filiform
papillae (I), but very weak in fungiform papillae (I, inset). IGFBP-2 is
expressed in the basal layer of the epithelium of filiform papillae (J) and
at the apex of fungiform papillae (K). Expression of IGFBP-4 is absent in
the epithelium (L). Expression of IGFBP-5 mostly disappears from filiform and fungiform papillae (M). Scale bar ⫽ 20 ␮m.
ROLE OF IGFBP
845
Fig. 2. Expression of IGFBP mRNAs (A–H) and immunohistochemistry for PGP9.5 (I) in developing circumvallate papillae of mouse tongue.
A and B: E14 circumvallate papillae showing mRNA expression of IGFBP-2 (A) and IGFBP-5 (B). Note intense expression of IGFBP-5 in the
apex of circumvallate papillae (B). C: Weak expression of IGFBP-3 is
seen in the core of mesenchyme. E15. D: Intense expression of IGFBP-4
is seen in the epithelium of trench grooves (G). E15. E: Expression of
IGF-IR is seen in the epithelium. E15. F–H: E17. Expressions of IGFBP-2
(F), IGFBP-4 (G), IGFBP-5 (H), and PGP9.5 (I). IGFBP-2 is expressed in
the apex of circumvallate papillae (F), and IGFBP-4 in the grooves of
circumvallate papillae (G). IGFBP-5 expression remains in presumed
taste buds (arrows in H), whose location is limited to the apex of
circumvallate papillae (arrows in I). Scale bar ⫽ 20 ␮m in A–G and I; 10
␮m in H.
lingual papillae (cf. Mbiene and Roberts, 2003). IGFs may
act in this series of evaginations and invaginations, and
this action may be regulated by their interaction with
IGFBPs. Based on the present results, we suggest IGFBP-5 and -2 to be molecules involved in the evagination
to form the raised epithelial papillae. At E12, IGFBP-5
showed broad expression, and at E14 –16, this expression
was observed in the apex of filiform, fungiform, circumvallate, and foliate papillae. At a later embryonic stage
(E17), IGFBP-5 expression remained only in the taste
buds and some epithelial cells. A similar expression pattern of Shh was reported in the taste bud-bearing papillae
of mice (fungiform and circumvallate) (Hall et al., 1999;
Jung et al., 2004; Liu et al., 2004). Also, mature taste buds
expressed Shh (Miura et al., 2001). In fact, in early chick
embryogenesis, embryos cultured in the presence of cyclo-
pamine, a potent inhibitor of Shh signaling (Liu et al.,
2004), showed downregulation of IGFBP-5 expression. IGFBP-5 expression was suggested to be regulated by Shh
(Allan et al., 2003). Moreover, IGFBP-2, which was expressed in the entire epithelium until E15, became restricted to the dorsal epithelium of filiform, fungiform,
foliate, and circumvallate papillae at E17. IGFBP-2 and
IGFBP-5 expression often overlap in the same cells or
tissue or are in adjacent tissues, e.g., taste buds (Suzuki et
al., 2005), lung alveolae (Schuller et al., 1993), ectoderm of
limb buds, astrocytes (Green et al., 1994).
In contrast, IGFBP-4 is related to invagination of the
epithelium to form grooves or furrows. In our previous
study, IGFBP-4 was expressed in the bottom of trenches of
circumvallate papillae at postnatal day 2 (Suzuki et al.,
2005). In the present study, IGFBP-4 was expressed in the
846
SUZUKI
Fig. 3. Expression of IGFBP mRNAs in developing foliate papillae of
mouse tongue. A: Intense expression of IGFBP-4 is seen in the grooves
(G). E15. B: Note the expression of IGFBP-5 in the ridges among the
grooves (G). E15. C: Expression of IGF-IR is seen in the epithelium. E15.
D: Expression of IGFBP-2 is seen in the ridge epithelium. E17. E:
IGFBP-3 is weakly expressed in the core of mesenchyme. E17. F:
Expression of IGFBP-4 is still seen in the grooves (arrows). fi, filiform
papillae; fo, foliate papillae. Scale bar ⫽ 20 ␮m in A–E; 10 ␮m in F.
TABLE 1. IGFBP mRNA expression patterns in
filiform, fungiform, foliate, and circumvallate
papillae of E14-17 mice*
pillae of filiform papillae, but very weakly expressed in
those of other papillae. IGFBP-3 is the major IGF carrier
protein in adult serum (Clemmons, 1992) and is also expressed in peripheral embryonic tissue, such as dermal
papillae of filiform papillae and hair follicle (Batch et al.,
1996).
IGF-1R
IGFBP-2
IGFBP-3
IGFBP-4
IGFBP-5
E14
E15
E17
⫹
⫹⫹
NE
⫹⫹
NE
⫹⫹
⫹
⫹⫹
⫹⫹
⫹
⫹⫹
⫹
⫹ (all four papillae)
⫹⫹ (all four papillae)
⫹⫹ (filiform)
⫺ (filiform, fungiform)
⫹⫹ (groove, foliate, circumvallate)
⫺ (all four papillae)
*Relative levels of expression are based on hybridization intensities of sections. ⫺, signal low to undetectable; NE, not
examined.
entire epithelium until E14 and then became restricted to
the groove of circumvallate and foliate papillae. Among
IGFBPs, IGFBP-4 uniquely inhibits IGF action (Zhou et
al., 2003), and so in circumvallate and foliate papillae, it
may be involved in the down-growth of grooves, with its
activity continuing during early postnatal development.
In filiform papillae, regularly spaced dermal papillae
appeared at E15 in the rat fetus, although the surface of
the tongue remained flat. At E18 of the rat fetus, proliferation in the epithelium overlying the dermal papillae
started and keratinization appeared at the surface of the
epithelium (Baratz and Farbman, 1975), thus giving rise
to anterior-posterior polarity (Jonker et al., 2004). The
presence of IGFBP-2 expression in the anterior epithelium
of each filiform papilla at E17 mice may promote this
polarity. IGFBP-3 was intensely expressed in dermal pa-
LITERATURE CITED
Allan GJ, Zannoni A, McKinnel I, Otto WR, Holzenberger M, Flint DJ,
Patel K. 2003. Major components of the insulin-like growth factor
axis are expressed early in chicken embryogenesis, with IGF binding protein (IGFBP)-5 expression subject to regulation by sonic
hedgehog. Anat Embryol 207:73– 84.
Ayer-LeLievre C, Stahlbom P-A, Sara VR. 1991. Expression of IGF-I
and -II mRNA in the brain and craniofacial region of the rat fetus.
Development 111:105–115.
Baratz RS, Farbman AI. 1975. Morphogenesis of rat lingual filiform
papillae. Am J Anat 143:283–302.
Batch JA, Mercuri FA, Werther GA. 1996. Identification and localization of insulin-like growth factor-binding protein (IGFBP) messenger RNAs in human hair follicle dermal papillae. J Invest Dermatol
106:471– 475.
Clemmons DR. 1992. IGF binding proteins: regulation of cellular
actions. Growth Regul 2:80 – 87.
Duan C. 2002. Specifying cellular responses to IGF signals: roles of
IGF-binding proteins. J Endocrinol 175:41–54.
Farbman AI, Mbiene J-P. 1991. Early development and innervation of
taste bud-bearing papillae on the rat tongue. J Comp Neurol 304:
172–186.
Ferguson MW, Sharpe PM, Thomas BL, Beck F. 1992. Differential
expression of insulin-like growth factors I and II (IGF I and II),
mRNA, peptide and binding protein 1 during mouse palate
development: comparison with TGF␤ peptide distribution. J Anat
181:219 –238.
ROLE OF IGFBP
Green BN, Jones SB, Streck RD, Wood TL, Rotwein P, Pinter JE.
1994. Distinct expression patterns of insulin-like growth factor
binding protein 2 and 5 during fetal and postnatal development.
Endocrinology 134:954 –962.
Hall JM, Hooper JE, Finger TE. 1999. Expression of Sonic hedgehog,
Patched, and Gli1 in developing taste papillae of the mouse. J Comp
Neurol 406:143–155.
Hall JM, Bell ML, Finger TE. 2003. Disruption of sonic hedgehog
signaling alters growth and patterning of lingual taste papillae.
Dev Biol 255:263–277.
Jonker L, Kist R, Aw A, Wappler I, Peters H. 2004. Pax9 is required
for filiform papilla development and suppresses skin-specific differentiation of the mammalian tongue epithelium. Mech Dev 121:
1313–1322.
Jung H-S, Akita K, Kim J-Y. 2004. Spacing patterns on tongue surface-gustatory papilla. Int J Dev Biol 48:157–161.
Liu H-X, MacCallum DK, Edwards C, Gaffield W, Mistretta CM. 2004.
Sonic hedgehog exerts distinct, stage-specific effects on tongue and
taste papilla development. Dev Biol 276:280 –300.
Mbiene J-P, Roberts JD. 2003. Distribution of keratin 8-containing
cell clusters in mouse embryonic tongue: evidence for a prepattern
for taste bud development. J Comp Neurol 457:111–122.
Mistretta CM, Goosens KA, Farinas I, Reichardt LF. 1999. Alternations in size, number, and morphology of gustatory papillae and
847
taste buds in BDNF null mutant mice demonstrate neural dependence of developing taste organs. J Comp Neurol 409:13–24.
Miura H, Kusakabe Y, Sugiyama C, Kawamatsu M, Ninomiya Y,
Motoyama J, Hino A. 2001. Shh and Ptc are associated with taste
bud maintenance in adult mouse. Mech Dev 106:143–145.
Nosrat CA, Blomlf J, Elshamy WM, Ernfors P, Olson L. 1997. Lingual
deficits in BDNF and NT3 mutant mice leading to gustatory and
somato-sensory disturbances, respectively. Development 124:1333–
1342.
Oakley B, Brandemihl A, Cooper D, Lau D, Lawton A, Zhang C. 1998.
The morphogenesis of mouse gustatory vallate epithelium and taste
buds requires BDNF-dependent taste neurons. Dev Brain Res 105:
85–96.
Schuller AGP, Zwarthoff EC, Drop SLS. 1993. Gene expression of the
six insulin-like growth factor binding proteins in the mouse conceptus during mid- and late gestation. Endocrinology 132:2544 –2550.
Suzuki Y, Takeda M, Sakakura Y, Suzuki N. 2005. Distinct expression pattern of insulin-like growth factor family in rodent taste
buds. J Comp Neurol 482:74 – 84.
Yamane A, Mayo ML, Shuler C. 2000. The expression of insulin-like
growth factor-I, II and their cognate receptor 1 and 2 during mouse
tongue embryonic and neonatal development. Zool Sci 17:935–945.
Zhou R, Diehl D, Hoeflich A, Lahm H, Wolf E. 2003. IGF-binding
protein-4: biochemical characteristics and functional consequences.
J Endocrinol 178:177–193.
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