Bone Vol. 21, No. 3
September 1997:217-223
ELSEVIER ORIGINAL ARTICLES
Circulating and Skeletal Insulin-like Growth Factor-I (IGF-I)
Concentrations in Two Inbred Strains of Mice With Different
Bone Mineral Densities
C. J. ROSEN, 1 H. P. DIMAI, 2 D. VEREAULT, 1 L. R. DONAHUE, 3 W. G. BEAMER, 3 J. FARLEY, 2
S. LINKHART, 2 T. LINKHART, 2 S. MOHAN, 2 and D. J. BAYLINK 2
St. Joseph Hospital, Bc~ngor, ME, USA
2 j. L. Pettis VA Hospital Medical Center, Loma Linda, CA, USA
3 Jackson Laboratory, Bar Harbor, ME, USA
Recent work has demonstrated differences in femoral bone
mineral density between two common inbred strains of mice,
C3H/HeJ (C3H) and C57BL/6J (B6), across a wide age range.
To investigate one possible mechanism that could affect
acquisition and maintenance of bone mass in mice, we stud-
ied circulatory and skeletal insulin-like growth factor-I
(IGF-I) and femoral bone mineral density (F-BMD) by
pQCT in C3H and ]36 progenitor strains, as well as serum
IGF-I obtained from matings between these two strains and
mice bred from subsequent F I intercrosses (F2). Serum IGF-I
measured by radioimmunoassay was more than 35% higher
in virgin progenitor C3H than virgin B6 at I, 4, 8, and I0
months of age, and iin 8-month-old C3H compared with B6
retired breeders (p < 0.001). In the progenitors, there was
also a strong correlation between serum IGF-I and serum
alkaline phosphatase (r - 0.51,p = 0.001). In the 4 month F 1
females IGF-I levels and F-BMD were intermediate between
C3H and B6 progenitors. In contrast, groups of F 2 mice with
the highest or lowest BMD also had the highest or lowest
serum IGF-I (p = 0.0001). IGF-I accounted for >35% of the
variance in F-BMD among the F 2 mice. Conditioned media
from newborn C3H calvarial cultures had higher concentra-
tions of IGF-I than media from B6 cultures, and cell layer
extracts from C3H calvariae exhibited greater alkaline phos-
phatase activity than cultures from B6 calvarial cells (p <
0.0001). The skeletal content of IGF-I in C3H tibiae, femorae,
and calvariae (6-14 weeks of age) was also significantly
higher than IGF-I content in the same bones of the B6 mice
(p < 0.05). These data suggest that a possible mechanism for
the difference in acquisition and maintenance of bone mass
between these two inbred strains is related to systemic and
skeletal IGF-I synthesis. (Bone 21:217-223; 1997) © 1997
by Elsevier Science ][nc. All rights reserved.
Key Words: Insulin-]like growth factors; Femoral bone density.
Address for correspondence and reprints: C. J. Rosen, St. Joseph
Hospital, 360 Broadway, Bangor, ME 04401. E-mail:crosen@maine.
maine.edu
Introduction
Recent studies from our laboratory have demonstrated large
differences (50%) in femoral bone density, measured by periph-
eral quantitative computed tomography (pQCT), between C3H/
HeJ(C3H) and C57BL/6J(B6), two common inbred strains of
mice. 2 These strain differences are noted as early as 4 weeks of
age, a time during peak bone mass acquisition, and are main-
tained through at least 12 months of age. 2't° Moreover, differ-
ences in bone density are not limited to the femur, since C3H
mice compared to B6 mice have consistently higher bone mass
(both cortical and trabecular) at other skeletal sites including the
tibia, vertebrae, and phalanges. 2 Although the mechanisms re-
sponsible for a greater bone mineral density in C3H mice have
yet to be clearly defined, changes in bone resorption or bone
formation must underlie differences in the acquisition of peak
bone mass between these two strains. Preliminary histomorpho-
metrical and biochemical evidence from our laboratory suggests
that bone formation is increased significantly at the time of
acquisition of peak bone mass in C3H mice (Baylink et al.,
unpublished observation).
Osteoblasts mediate bone formation through a series of events
that are regulated by hormonal and skeletal growth factors. 1
Several of these regulatory factors are also operative during
acquisition of bone mass. These include insulin-like growth
factors (IGF-I and -II), transforming growth factor-13 (TGF-13),
bone morphogenic proteins (BMPs), fibroblast growth factors,
numerous interleukins, tumor necrosis factor (TNF), and various
prostaglandins, t Several lines of evidence suggest that IGFs are
important mitogenic and differentiative factors for bone cells.
First, these peptides are found in very high concentrations within
the skeletal matrix, t Second, calciotropic hormones such as
parathyroid hormone (PTH), 1,25-dihydroxyvitamin D, and
growth hormone may mediate their effects on osteoblasts in part
by regulating the synthesis of IGFs and/or their binding pro-
teins. 14'19 Third, studies of growth hormone-deficient patients
have found that serum IGF-I concentrations closely correlate
with reduced bone density, and that growth hormone replacement
increases both serum IGF-I and bone mineral density. 4"13Fourth,
age-associated declines in circulating IGF-I parallel similar drops
in skeletal levels of IGF-I. 3'17 Fifth, several cross-sectional
studies have demonstrated a strong linear relationship between
serum IGF-I and bone mineral density in postmenopausal wom-
en.5"16 These points suggest that IGF-I may play an important
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