Starvation-Induced Decrease in the Maximal Binding Capacity
for Triiodothyronine of the Thyroid Hormone Receptor Is Due to a Decrease
in the Receptor Protein
Tetsuya Tagami, Hirotoshi Nakamura, Sigekazu Sasaki, Yoji Miyoshi, and Kazuwa Nakao
Biological responses to thyroid hormones are mediated by the nuclear thyroid hormone receptor (TR). Alterations in the
maximal triiodothyronine (T3)-binding capacity (Cmax) of TR measured using a ligand binding assay have been reported under
some pathophysiological conditions. Northern blot analysis has indicated that TR mRNA concentrations do not necessarily
correlate with Cmax levels. For example, although the decrease in Cmax in rat liver induced by prolonged fasting is well
established, TR mRNA concentrations have been reported to be constant. In the present study, we examined starvation-
induced changes in TR by Western blot with anti-TR(al + [3) antiserum and by Scatchard plot analysis. Starvation of rats for 72
hours decreased Cmax in the liver to 72.5% of control levels. The 47- and 55-kd TR proteins detected in hepatic nuclear extract
by Western blotting also decreased to 64% and 66% of control values, respectively. The starvation-induced changes in Cmax
and TR protein levels paralleled the change in total hepatic nuclear protein concentration. These results suggest that the
decrease in T3-binding activity of the TR is due to a reduction of the TR protein itself,
Copyright © 1996 by W,B. Saunders Company
T
HYROID HORMONE RECEPTORS (TRs) are li-
gand-dependent transcription factors. Tissue respon-
siveness to triiodothyronine (T3) is related to TR content.
Many studies have reported that the maximal T3-binding
capacity (Cmax) of TR changes under physiological and
pathological conditions. Tumor growth, ~ uremia, 2 and dia-
betes mellitus3 have been reported to reduce TR Cmax. In
particular, a starvation-induced decrease in Cmax in rat
liver has been well established. This reduction in receptor
number, in combination with reduced serum T3 concentra-
tion, is assumed to protect cells from the catabolic effects of
thyroid hormone during acute caloric and amino acid
deficiency. 4-7 The mechanism responsible for the starvation-
induced Cmax decrease is still unknown.
There are three mRNAs encoding rat TRs with T3-
binding activity: al, [31, and [32. 8-1° TRal and TR[31
mRNAs are expressed ubiquitously in rat tissues, u-~3
whereas TR[32 mRNA is mainly found in the pituitary. 1°a4
When the amounts of individual TR mRNAs in several rat
tissues were determined by Northern blot analysis in
conjunction with solution hybridization, TR[31 mRNA was
the predominant receptor in the liver.15 Lane et a116
reported that the level of hepatic TR[31 mRNA did not
change by prolonged fasting despite a decrease in Cmax.
Discrepancies between TRod and TRI31 mRNA levels and
Cmax have also been found in some tissues and at specific
stages in development. 15,17 These results raise a question as
From the Second Division, Department of Internal Medicine, Kyoto
University School of Medicine, Kyoto; and the Second Division,
Department of Internal Medicine, Hamamatsu Medical School,
Hamamatsu, Japan.
SubmittedAugust 29, 1995;accepted February 1, 1996.
Supported in part by Grants-in-Aid for Scientific Research from
Fellowships of the Japan Society for the Promotion of Science for
Japanese Junior Scientists (no. 2037 in 1993 to ZT.) and from the
Ministry of Education of Japan (no. 06671018in 1994 to H.N.).
Address reprint requests to Tetsuya Tagami, MD, Endocrinology,
Metabolism and Molecular Medicine, Tarry 15, Northwestern Univer-
sity Medical School, 303 E Chicago Ave, Chicago, IL 60611.
Copyright © 1996 by W.B. Saunders Company
0026-0495/96/4508-0010503.00/0
to whether starvation-induced alterations of Cmax corre-
late with changes in TR protein levels.
Previously, we have measured TR protein content in rat
tissues using Western blot analysis with an anti-TR antise-
rum that recognizes TRal and TR[3.18 The 47- and 55-kd
proteins were identified as TR proteins. Although discrep-
ancies between levels of functional TR mRNA and Cmax
were known to exist in rat liver and brain, we demonstrated
that the relative concentration of TR proteins correlated
with Cmax in both tissues.
In the present study, we measured Cmax and TR protein
level by a T3-binding assay and Western blot analysis,
respectively, and examined whether the decrease in Cmax
induced by starvation was due to a reduction of TR protein
content.
MATERIALS AND METHODS
Preparation of Nuclear Extracts
Wistar male rats (150 g body weight) purchased from Shimizu
(Kyoto, Japan) were fed a laboratory diet (Oriental Yeast Indus-
trial, Chiba, Japan) for a few days. The manipulated group of rats
were fasted for 72 hours before killing. All rats were allowed
unlimited access to water. After the animals were killed by
exsanguination through the abdominal aorta, the liver was immedi-
ately removed and nuclear extracts were prepared as described
previously. 19 The nuclear proteins were fractionated by high-
performance liquid chromatography (HPLC) using a gel-filtration
column (G3000SW; Tosoh, Tokyo, Japan) in 0.05 mol/L sodium
phosphate buffer, pH 7.4, with 1 mmol/L MgClz. The TR fraction
was obtained by measurement of T3-binding activity in each
fractionJ 8
Protein concentration was measured using Coomassie brilliant
blue G-250 (Bio-Rad Laboratories, Hercules, CA) with bovine
serum albumin as the standard. DNA content was determined by
Burton's method. 2°
Western Blot Analysis
The procedure for raising the anti-TR antiserum, 4BII, and its
characteristics have been described previously. 19,21 4BII recognizes
functional TRs (cd and [31) but not the variant form (a2)
biochemicallyand immunohistochemicaUy. 19,21,22
TR proteins were analyzed by Western blotting as described
previously. TM Briefly, proteins (20 to 60 Ixg per lane) in the nuclear
970 Metabolism, Vo145,No 8 (August),1996: pp 970-973