Calcif Tissue Int (1993) 53:180-186
Calcified
Tissue
International
© 1993 Springer-Verlag New York Inc.
Molybdenum-Induced Changes in the Epiphyseal Growth Plate
Nicola M. A. Parry, 1 Michael Phillippo, 1 Martin D. Reid, 1 Brian A. MeGaw, 1 David J. Flint, z and
Nigei Loveridge 1
1Division of Biochemical Sciences, Rowett Research Institute, Greenburn Road, Aberdeen AB2 9SB; and ZHannah Research Institute,
Ayr KA6 5HL Scotland
Received November 4, 1992; and in revised form January 8, 1993.
Summary. Molybdenum (Mo), at high concentrations, in-
duces changes in the epiphyseal growth plate through its
effects on copper (Cu) metabolism but it is unclear whether
or not Mo can induce changes independent of its effects on
copper status. To this end, the effect of Mo on longitudinal
bone growth was examined in rats. Dietary Mo was given
either as ammonium heptamolybdate or as ammonium
tetrathiomolybdate, the latter producing a marked Cu defi-
ciency. There was a significant reduction in longitudinal
bone growth in both groups; however, growth plate width
was increased only in the Cu-deficient animals due to an
increase in the width of the zone of transitional/hypertrophic
chondrocytes. Both glucose 6-phosphate dehydrogenase ac-
tivity and cell proliferation (assessed by bromodeoxyuridine
incorporation) were markedly decreased in the proliferating
zone of the growth plate in both Mo-treated groups. These
changes were not apparently related to changes in circulating
vitamin D metabolites or insulin-like growth factor-1. The
results indicate that excess Mo impairs cell proliferation
within the growth plate, whereas the effects of copper defi-
ciency are more related to chondrocyte differentiation.
Thus, Mo can induce changes in longitudinal bone growth
which are distinct from those resulting from Cu deficiency.
Key words: Growth plate - Molybdenum - Cell proliferation
- Cell differentiation - Chondrocytes.
Certain trace elements such as zinc, manganese, and cooper
are essential for normal growth and development [1, 2] and
there is increasing evidence that other trace elements such as
lead and cadmium affect the skeleton [3, 4] and may play a
role in the etiology of osteoporosis [5, 6]. Skeletal abnormal-
ities due to dietary copper (Cu) deficiency have been ob-
served in many species. Copper deficiency results in thin-
ning of the cortex and a widened epiphyseal growth plate,
along with irregular bone matrix deposition and osteoporosis
associated with reduced osteoblastic activity. These findings
have been consistently reported in pigs [7-9], chickens [10],
and sheep [11]. Similar morphological changes in bone have
also been reported in growing rats fed a diet supplemented
with high concentrations of molybdenum (Mo) (100-500 I~g/g)
[12]. However, bone lesions have been induced in cattle [13]
and sheep [14] with Mo concentrations (5-20 Ixg/g), probably
due to the interaction between dietary Mo and sulfur in the
rumen environment to form thiomolybdate, a potent antag-
Offprint requests to: N. Loveridge
onist of Cu metabolism [15, 16]. Whereas monogastric ani-
mals can tolerate relatively high levels of Mo, the inclusion
of dietary Mo in the form of tetrathiomolybdate (6-20 I~g/g)
induces bone lesions [17, 18]. There is, however, increasing
uncertainty as to whether all the effects of Mo are due to Cu
deficiency or Mo [19].
The aim of this study was to determine the effects of Mo
on the epiphyseal growth plate and to distinguish these ef-
fects from those of Cu deficiency.
Materials and Methods
Animals and Diets
Male Hooded Lister rats of the Rowett strain were weaned at 19
days onto a stock diet for 10 days, followed by ad libitum access to
a semisynthetic, albumin-based trace element diet [20, 21]. Animals
were then group-housed and randomized according to weight into
three different dietary groups. The control group received a basal
diet containing 3 mg Cu/kg without any added Mo; the other groups
received the basal diet supplemented with 6 mg Mo/kg either as
ammonium tetrathiomolybdate (TTM), prepared as described in [22]
or ammonium heptamolybdate (AM) (BDH, Poole, Dorset, UK).
This concentration of TTM was chosen because a previous study
[23] had indicated that this dose induced gross bone lesions but was
not generally toxic.
Diets were fed for 26 days, with six rats from each group being
killed after 13 days, and a further six after 26 days. Mean body
weight in the TTM group was reduced slightly at 13 days (control
160.8 -+ 4.35; TTM 144.3 +- 5.28; AM 158.0 +- 1.32; mean +- SEM)
but markedly reduced at 26 days (control 262.0 + 3.51; TTM 200.5
-+ 6.03; AM 260.2 -+ 6.24).
Tissue Collection and Preparation
Animals were injected intraperitoneally with 25 mg 5-bromo-
2'deoxyuridine (BrdUrd) (Sigma) per kg body weight 1 hour before
death. Blood was taken into heparinized vacutainer tubes after car-
diac puncture under barbiturate anesthesia, centrifuged at 4°C, and
the plasma stored at -20°C. Right tibiae were briefly immersed in
5% polyvinyl alcohol (PVA) and chilled to - 70°C in hexane prior to
mounting in 5% PVA [24] for cutting serial sections of 10 p, thick-
ness on a cryostat (Brights Instruments, Huntingdon, England).
Biochemical Analyses
Four hundred microliters of 10% trichloroacetic acid (TCA) solution
was added to 100 i~1 of plasma and centrifuged for 15 minutes at
3,000 rpm, and the acid-soluble or "available" Cu fraction was an-
alyzed on a Pye Unicam SP9 atomic absorption spectrophotometer.
Freeze-dried liver samples were microwave acid-digested prior to
determination of Cu, Mo, iron (Fe), and zinc (Zn) concentrations by