Endocrinology Vol. 140, No. 4 1869-1874
Copyright © 1999 by The Endocrine Society
Evidence for Stanniocalcin Gene Expression in Mammalian Bone1
Yuji Yoshiko,
Aoi Son,
Shuji Maeda,
Akira Igarashi,
Shoichi Takano,
Jianguo Hu and
Norihiko Maeda
Department of Oral Anatomy (Y.Y., A.S., S.M., N.M.), Hiroshima
University School of Dentistry, Minami-ku, Hiroshima 734-8553, Japan;
and R & D Center, BML, Inc. (A.I., S.T., J.H.), Kawagoe, Saitama
350-1101, Japan
Address all correspondence and requests for reprints to: Norihiko Maeda, Department of Anatomy, Hiroshima University School of Dentistry, Minami-ku, Hiroshima 734-8553, Japan.
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Abstract
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Stanniocalcin (STC) acts as a regulator of calcium and phosphate
homeostasis in an endocrine manner in bony fish. Recently,
complementary DNAs encoding human and mouse STC have been
characterized, and the messenger RNA (mRNA) expression was identified
in various tissues, such as kidney, small intestine, prostate, thyroid,
and ovary. Because previous studies concerning the effects of fish STC
on mammalian bone have been discussed, there is a good possibility that
mammalian STC is a local factor in bone. Here, we demonstrated STC mRNA
expression in neonatal mouse calvaria, the primary cultured mouse
osteoblast-rich fractions, and human and mouse osteoblastic cell lines.
We also mapped the cellular distribution of the STC mRNA in femur and
calvaria in developing mice. Several transcripts with a major 4-kb band
were detected in all samples. The cellular distribution of the mRNA
expression corresponded closely to osteoblasts in both femur and
calvaria. Significant labeling of the STC mRNA was also identified in
chondrocytes but not in osteoclasts and other bone marrow elements.
These results are the first evidence that hormone may be actually
expressed in osteoblasts and chondrocytes, and they strongly implicate
the involvement of local STC in both endochondral and membrane bone as
an autocrine/paracrine factor.
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Introduction
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HUMAN STANNIOCALCIN (STC) was first
identified in a study aimed at identifying genes involved in the
control of cellular proliferation, using a simian virus 40 early
region-transfected human fibroblast culture (1), and in a process of
random sequencing of a human tissue complementary DNA (cDNA) library
(2). Recently, its genomic structure and chromosomal localization have
been determined also in humans (3). It had been widely assumed that STC
is a calcium-regulating hormone presented only in bony fish. Fish STC
is synthesized and secreted by the corpuscles of Stannius (CS), unique
endocrine glands associated with kidney (4, 5) and embryologically
derived from nephric ducts (6). The fish hormone is a homodimeric
glycoprotein with a molecular mass of approximately 50 kDa, and no
sequence similarity with calcitonin (CT), PTH, or other known molecules
in vertebrate had been observed. However, there are interesting
parallels between STC in fish and CT in mammals, with respect to
stimulus-secretion coupling and function (4). The primary function of
fish STC is the prevention of hypercalcemia by targeting gill (7) and
gastrointestinal tract (8) Ca2+ transport. A second
important action of the hormone is stimulation of phosphate
reabsorption by renal proximal tubule (9).
The predicted human STC is 247 amino acids long, and it shares 80%
amino acid sequence similarity with fish STC (1, 2). Human STCs from
both baculovirus-infected insect cells and recombinant Chinese
hamster ovary (CHO) cells are secreted as glycosylated proteins
and as disulfide-linked homodimers, with physiological and chemical
properties similar to those of the fish STC (10). These properties were
identified in native STC derived from human tissue (11). However, the
human STC messenger RNA (mRNA) was expressed in various tissues, with
high levels in ovary, prostate, and thyroid (1). Immunoreactivity,
using a specific antiserum to fish STC and a polyclonal antibody to
bacterial synthesized recombinant human STC, was identified in renal
cortex tubule immediately adjacent to glomerulus and serum in humans
(12) and in the specific segments of renal tubule in rats (13),
respectively. Lastly, native hormone was localized to principal and
-intercalated cells in the distal half of nephron (11). As in human,
mouse STC cDNA was isolated, and it encoded a predicted protein of the
same length as its human counterpart, with a very high level of amino
acid sequence similarity, and the mRNA was also expressed in various
tissues (14). Bacterial or CHO cell-synthesized recombinant human STC
increases phosphate reabsorption in renal cortical brush-border
membrane vesicle of rats (15) and decreases calcium absorption and
increases phosphate absorption in duodenum of swine and rats (16),
respectively. These findings suggest that mammalian STC acts as a
regulator of calcium and phosphate homeostasis and has an
autocrine/paracrine (rather than a specialized) endocrine role.
Possible effects of fish STC or CS extracts on serum calcium levels and
bone metabolism in mammals have been discussed (17, 18, 19, 20, 21). The fish STC
and its N-terminal peptide fragment are similar, in terms of biological
activity, to PTH (17, 18, 19) and CT (20), respectively. If the activities
of fish STC do apply to those of mammalian STC, and if mammalian STC
does act as a regulator of calcium and phosphate homeostasis, there is
a good possibility of STC mRNA expression in bone cells. The present
study provides solid evidence for STC mRNA expression in neonatal mouse
calvaria and its primary cultured osteoblast-rich fractions and human
and mouse osteoblastic cell lines. These results also enabled us to
determine the cellular distribution of the STC mRNA in bone. In
situ hybridization (ISH) analysis revealed that the STC mRNA was
strongly expressed in osteoblasts in both femur and calvaria of
developing mice. Chondrocytes were also stained with ISH
histochemistry. These results suggest that the specific bone cells
actually synthesize STC and that the hormone may act as an
autocrine/paracrine factor in both endochondral and membrane bone.
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Materials and Methods
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Animals
Pregnant or normal ddY mice of appropriate age for the study
were purchased from Shizuoka Laboratory Animal Center (Hamamatsu,
Japan).
Primary bone cell and osteoblastic cell line culture
Bone cell fractions were obtained from calvaria of 20 ddY mice,
at postnatal day 1, by sequential collagenase digestions (22, 23),
which resulted in 6 cell fractions. An identification of the
osteoblastic phenotype in the fractions was made by an assay of
alkaline phosphatase activity, as described (23). Human osteosarcoma
lines, Saos-2, MG-63, and U-2 OS were purchased from American Type Culture Collection (Rockville, MD). HOS human osteogenic
sarcoma line was obtained from Riken Cell Bank (Tsukuba, Japan).
MC3T3-E1 mouse normal osteoblast-like cell line was kindly donated by
Prof. M. Kumegawa (Meikai University, Saitama, Japan). The 6 cell
fractions and the cell lines were cultured in appropriate medium (MEM
for MG-63; DMEM for SAOS-2 and U-2; and MEM- for primary cultured
cells, HOS, and ME3T3-E1 cells, Gibco BRL, Grand Island,
NY) supplemented with 10% FBS (Upstate Biotechnology, Inc. Lake Placid, NY) and antibiotics. Cultures were maintained,
up to confluence, at 37 C in a humidified atmosphere of 5%
CO2.
Northern blot analysis
The riboprobes for STC and alkaline phosphatase (ALP) were
synthesized and labeled by in vitro transcription using
digoxigenin (DIG)-11-uridine 5'-triphosphate (nonradioactive RNA
labeling and detection kit, Boehringer Mannheim, Mannheim, Germany).
Recombinant plasmids, including human STC cDNA and mouse placental ALP
cDNA (positions 628-1258 of the cDNA sequence), were generously
provided by Dr. R. R. Reddel (Children’s Medical Research
Institute, Sydney, Australia) and Dr. Y. Ishizuka (Sumitomo
Pharmaceutical Co., Osaka, Japan), respectively. Total cellular RNA
from calvaria (at postnatal day 1) and kidney, spleen, and liver of
6-week-old ddY mice, as well as cultured cells, were obtained by
acid-guanidinium thiocyanate-phenol-chloroform extraction (24). Total
RNA (20 µg for the tissues and 10 µg for the cultured cells) was
electrophoresed on a 1% agarose-17% formaldehyde gel, then
transferred to a positively charged nylon membrane (Boehringer
Mannheim). After immobilization by baking at 120 C for 30 min, the
membrane was prehybridized, hybridized with 100 ng/ml antisense or
sense riboprobes. Hybridization and washing conditions were as
recommended by the manufacturer. After washing, an ALP-conjugated
anti-DIG antibody was applied, and chemiluminescence detection was
carried out using disodium
3-(4-methoxyspiro{1,2-dioxetane-3,2'(5'-chloro)tricycro[3.3.1.13,7]decan}4-yl)phenyl
phosphate (CSPD) substrate (Boehringer Mannheim). The
signals were determined using Kodak scientific imaging film (BIOMAX MS,
Rochester, NY). The adequacy of RNA loading was assessed by
rehybridization with the ß-actin riboprobe. The data represent
results analyzed from tissues (six independent pools of calvaria, two
independent pools of each of kidney, spleen and liver) and cultured
cells, and analyzed (each in at least two experiments).
Tissue preparation
Twenty- or 30-day-old ddY mice were anesthetized with a 25-mg/kg
ip injection of pentobarbital sodium. Femur and calvaria were preserved
by in vivo vascular perfusion of 0.1 M phosphate
buffer (pH 7.4) for 5 min, followed by perfusion with 4%
paraformaldehyde in the same buffer for 10 min. The femur and calvaria
were then removed, immersed in the fixative overnight at 4 C, and
decalcified with 10% EDTA at 4 C. The specimens were then dehydrated
in a graded series of ethanol, defatted in chloroform, and embedded in
paraffin. Sections, 6-µm thick, were placed on
3-aminopropyltriethoxysilane-treated slides and stored at 4 C.
ISH
ISH analysis was carried out as previously described (25), with
slight modification. In brief, the sections were deparaffinized in
xylene, rehydrated, and treated with proteinase K (5 µg/ml,
Boehringer Mannheim) for 15 min at 37 C. After postfixation with 4%
paraformaldehyde in phosphate buffer for 10 min, further
permiabilization was carried out in 0.1 N HCl for 10 min.
The sections were then acetylated in 0.25% acetic anhydride in 0.1
M triethanolamine-HCl (pH 8.0) for 5 min, dehydrated, and
air dried. Subsequently, the sections were incubated in hybridization
buffer (50% formamide, 200 µg/ml yeast transfer RNA, 1x Denhardt’s
solution, 10% dextran sulfate, 600 mM NaCl, 0.25% SDS,
and 1 mM EDTA in 10 mM Tris-HCl, pH 7.6) for
16 h at 42 C with 1 µg/ml riboprobes. Posthybridization
treatment consisted of washing in 2 x SSC and 50% formamide at
42 C, and incubation in ribonuclease A (RNase A; 1–10 µg/ml;
Sigma Chemical Co., St. Louis, MO) for 20 min at 37 C,
followed by washing once in 2 x SSC for 20 min and twice in
0.2 x SSC for 20 min at 42 C. The sections were then incubated
with blocking reagent (Boehringer Mannheim), followed by an
ALP-congugated anti-DIG antibody (Boehringer Mannheim). Next, they were
washed and incubated in color substrate solution (nitro blue
tetrazolium chloride and 5-bromo-4-chloro-3-indolyl phosphate,
toluidine salt Boehringer Mannheim) for 15–120 min. After the ISH
histochemical procedure, the sections were counterstained with methyl
green. The adjacent sections were hybridized with riboprobe for ALP, as
described above, or stained for tartrate-resistant acid phosphatase
(TRAP) activity, as previously described (26), and counterstained with
hematoxylin. The specificity of antisense riboprobe for STC was
identified by the pretreatment of RNase A (10 µg/ml) before ISH and
by the negative control tissue (liver), in which STC mRNA had not been
detected by Northern blot analysis. The data represent results from
three animals, each analyzed in at least two independent
experiments.
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Results
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Northern blot analysis
We first determined whether STC mRNA is expressed in bone and
identified the size and pattern of the transcripts, compared with those
of kidney or spleen, in which the mRNA transcripts have been
established (14); and Northern blot analysis (on neonatal mouse
calvaria, adult mouse kidney, spleen, and liver) was carried out using
DIG-labeled riboprobes for STC (Fig. 1
).
In all samples except for liver, several transcripts were clearly
detected by the antisense riboprobe, and the 1.4-kb band was most
abundant in the spleen (lane 1) and the 4-kb transcript in the kidney
(lane 2), as previously described (13). The major 4-kb transcript and
fainter bands (smaller transcripts), which were similar in size and
pattern to those of the kidney, were detected in calvaria (lane 3). No
signal was detected in the liver (lane 4) and in all the samples by the
sense riboprobe (the result is represented, in lane 5, by the
calvaria).
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Figure 1. Expression pattern of STC mRNA transcripts in
mouse spleen, kidney, calvaria, and liver. Total RNA from adult mouse
spleen, kidney and liver, and neonatal mouse calvaria was extracted by
a guanidine isothiocyanate method. Twenty micrograms of total RNA was
subjected to Northern blot analysis. The blot was hybridized with a
DIG-labeled antisense (lanes 1–4) and sense (lane 5) riboprobe for
STC. Lane 1, spleen; lane 2, kidney; lanes 3 and 5, neonatal calvaria;
lane 4, liver. Molecular sizes of markers, in kb, are indicated to the
left of the blot.
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We next attempted to identify the specific cell type expressing the STC
mRNA in the primary cultured bone cells. The results are illustrated in
Fig. 2A. Neonatal calvaria was
sequentially digested by collagenase (22, 23), and six bone cell
fractions were obtained. STC mRNA transcripts, in close agreement with
the kidney types, were apparently detected in fractions 1–4. The level
was highest in fractions 2 and 3 (followed by fractions 1 and 4) and
was low in fractions 5 and 6. The high levels of STC mRNA closely
correlated with those of ALP mRNA (Fig. 2A) and its activity (data not
shown), indicating that osteoblast-rich fractions abound in the STC
mRNA accumulation. These results enabled us to estimate that the STC
mRNA expression is specific to osteoblasts. Then, we examined whether
the STC mRNA is expressed in each osteoblastic cell line, in which the
osteoblastic phenotypes differs, or not. Unexpectedly, the STC mRNA was
expressed in all the human and mouse osteoblastic cell lines, MG-63,
SAOS-2, U2-OS, HOS, and MC3T3-E1, similar to the transcripts of primary
cultured bone cells and calvaria (Fig. 2B).
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Figure 2. Expression pattern of STC transcripts in primary
cultured mouse bone cells, and human and mouse osteoblastic cell lines.
Total RNA from primary cultured mouse bone cells and osteoblastic lines
was extracted by a guanidine isothiocyanate method. Ten micrograms of
total RNA was subjected to Northern blot analysis with DIG-labeled STC
(for A and B) or ALP riboprobe (for A), and then reprobed with a
ß-actin riboprobe (for A). A, STC and the ALP mRNA transcripts in the
primary cultured cells: lane 1, fraction 1; lane 2, fraction 2; lane 3,
fraction 3; lane 4, fraction 4; lane 5, fraction 5; lane 6, fraction 6
of enzymatically digested cells from neonatal mouse calvaria. B, STC
mRNA transcripts in human and mouse osteoblastic cell lines: lane 1,
MG-63 cells; lane 2, Saos-2 cells; lane 3, U-2 OS cells; lane 4, HOS
cells; lane 5, MC3T3-E1 cells. Molecular sizes of markers, in kb, are
indicated on the left.
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ISH
We determined STC mRNA expression levels in primary cultured bone
cells and osteoblastic cell lines, as well as neonatal calvaria. These
results suggested that osteoblasts actually express STC mRNA. We,
therefore, examined the cellular distribution of the STC mRNA in femur
and calvaria of developing mice, by ISH histochemistry using the
DIG-labeled riboprobes. The sections were studied with sense and
antisense probes for STC and ALP. Hybridization with the sense
riboprobes, and the pretreatment of RNase A before hybridization with
the antisense riboprobes, did not establish significant labeling of any
structures (data not shown). We also identified the specificity of the
antisense riboprobe for STC by no labeling of liver in which STC mRNA
had not been detected by Northern blot analysis (data not shown).
Hybridization with the antisense riboprobe yielded strong labeling of
both femur (Fig. 3; A, B, D, E, and F)
and calvaria (Fig. 3H). In the femur, signal for STC was rich in
epiphysis and metaphysis. The cellular identification of the strong
labeling corresponded with osteoblasts, in contact with trabecular (A,
B, E, and F) and cortical (D) bone. These findings corresponded to the
labeling patterns of ALP mRNA, as illustrated in C, the adjacent
section of B. As shown in E, significant labeling of the STC mRNA was
also observed in osteoblasts in contact with trabecular bone of
secondary marrow cavity. Furthermore, the same could apply to
chondrocytes in the superficial site of articular cartilage and
epiphyseal plate (E). In subsequent histological and histochemical cell
identification, using adjacent sections, no staining pattern for
TRAP-positive multinucleated cells identical to the labeling of the STC
mRNA was observed (F and G). The signal was relatively poor in
diaphysis because the cavity was filled with STC mRNA-negative bone
marrow cells. The labeling of vascular tissue and other tissue elements
was also not significant. In calvaria, strong labeling was detected in
the layer of osteoblasts in contact with bone at the endocranial site
(Fig. 3I).
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Figure 3. Cellular distribution of STC mRNA in the bone of
20- or 30-day-old developing mice. A–G and H, Femur of 30-day-old mice
and calvaria of 20-day-old mice, respectively. The sections were
hybridized with a DIG-labeled antisense cRNA encoding human STC (A, B,
D, E, F, and H) and mouse ALP (C) and were counterstained with methyl
green. A, Longitudinal section of metaphysis; B, a high magnification
view of trabeculare in the metaphysis; C, the adjacent section
of B; D, a high-magnification view of cortical bone in the metaphysis;
E, longitudinal section of epiphysis; F, a high-magnification view of
multinucleated cells on the trabecular bone surface in the metaphysis;
G, the adjacent section of F, the section was stained for TRAP activity
and counterstained with hematoxylin; H, transverse section of calvaria.
Labeling of STC mRNA is shown in osteoblasts (black
arrows in B, D, and H) and chondrocytes (white
arrows in E) but not in TRAP-positive cells
(asterisks in F and G). Labeling of ALP mRNA was rich in
osteoblasts (black arrows in C), characterized by the
close parallel to STC mRNA expression (B). Bar, 60 µm.
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Discussion
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In this paper, we examined whether STC mRNA is expressed in
mammalian bone, and we mapped the cellular distribution of STC mRNA in
bone using developing mice. We clearly demonstrated that the STC mRNA
was expressed in all neonatal calvaria, primary cultured
osteoblast-rich fractions (which were determined by ALP activity and
mRNA expression) and osteoblastic cell lines (by Northern blot
analysis). There were several transcripts with a high level of 4-kb and
fainter bands common to these samples. For ISH analysis, the labeling
was rich in a specific cell type, characterized by the correlation to
ALP mRNA expression, by contact with bone surface, and by being
TRAP-negative. Osteoblasts show increased ALP expression as they mature
before the mineralization phase (27). Therefore, it is reasonably
suggested that the mRNA is strongly expressed in osteoblasts. This is
the case in both femur and calvaria. Trabecular and cortical bone of
the metaphysis and the endocranial site of calvaria was abounding with
the strong labeling of STC mRNA. In addition, the labeling was
identified in chondrocytes, suggesting that the STC mRNA expression is
involved in cartilage, as well as in bone. No significant labeling was
detected in osteoclasts, blood vessels, or other marrow elements.
STC mRNA expression has been identified in heart, placenta, lung,
skeletal muscle, pancreas, kidney, thymus, prostate, testis, ovary,
thyroid, small intestine, colon, and adrenal cortex in humans (1) and
in heart, spleen, liver, kidney, small intestine, colon, and ovary in
mice (14) but not in brain, liver, spleen, peripheral blood leucocytes,
and adrenal medulla in humans (1) and not in liver in mice (14).
Skeletal results have not been reported on the STC mRNA expression.
Transcripts of 2- and 4-kb, and at least four transcripts have been
reported in human and mouse STC mRNA, respectively. Different STC
transcripts predominate in different tissues, suggesting that
tissue-specific alternative splicing occurs (14). In the present study,
bone was added at one of the possible STC synthesis sites in mice, and
the major 4-kb and fainter bands were similar in size and pattern to
those of kidney but different from those of spleen. These results
suggested that each product of the STC transcripts in bone, kidney,
spleen, and other tissues is restricted to tissue-specific function, as
is shown in a previous report (14). Recently, a second STC (STC-2) cDNA
in mouse and human has been identified (28). STC-2, like STC, is
expressed in a wide variety of tissues, but the predicted amino acid
sequence of STC-2 contains a cluster of histidine residues, which
suggests that STC-2 may interact with metal ions (28).
Milet and co-workers (17) first reported that an extract of eel CS,
which synthesizes and secretes STC, caused an increase in serum levels
of calcium and resulted in the activation of osteoclastic bone
resorption at the periosteum of femur in rats. A bone resorption assay,
using organ culture of rat fetal calvaria, revealed that extracts of
eel (17) and trout (18) CS and purified trout STC (19) stimulated the
release of calcium from the bone in the same manner as PTH. These
effects were not observed in salmon STC (20), but its specific peptide
fragment, which was highly conserved in amino acid sequence of fish
STCs, inhibits a PTH-dependent stimulation in the calvarial bone
resorption and in cAMP production in ROS17/2.8 rat osteoblastic cell
line (21). In the light of the great sequence and structural similarity
between fish and mammalian STC, mammalian STC may prove to be effective
in the regulation of bone cell properties as an autocrine/paracrine
factor. Previous studies in mammalian systems reported that renal
phosphate (15) and intestinal calcium and phosphate transport (16) can
be regulated by recombinant human STC. These observations imply that
STC may play a significant role in mammalian calcium homeostasis, by
reducing net calcium absorption and promoting calcium deposition into
bone in the presence of increased plasma phosphate levels (16). This
hypothesis is well matched to the present results identifying STC mRNA
expression in osteoblasts and chondrocytes in developing mice.
In conclusion, this is the first report of STC mRNA expression in
mammalian bone. STC mRNA in developing mouse bone is expressed with a
pattern similar to that in kidney. Strong signal for the mRNA is
restricted to osteoblasts and chondrocytes. In kidney,
STC-immunoreactive and STC mRNA-expressing cells have been identified
in specific segments of nephron in humans (11) and rats (13), and in
mice (29), respectively. Recombinant STC caused a reduction in
phosphate extraction in rat kidney (15). These results are strong
evidence of a direct effect of STC as an autocrine/paracrine factor on
mammalian tissues. Although the present results cannot reveal whether
STC regulates calcium and phosphate levels or has other functions in
bone, the identification of STC mRNA expression in bone cells supports
the hypothesis that STC acts in an autocrine/paracrine manner during
both endochondral and intramembraneous ossification, and their bone
metabolism in mammals.
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Footnotes
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1 This work was supported, in part, by a grant-in-aid from the Ministry
of Education, Science, and Culture of Japan. 
Received July 3, 1998.
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Abstract
Introduction
