Published December 5, 2014
Light exposure during night suppresses nocturnal increase in growth
hormone secretion in Holstein steers1
E. Kasuya,*2 S. Kushibiki,† K. Yayou,* K. Hodate,‡ and M. Sutoh†
*Neurobiology Research Unit, National Institute of Agrobiological Sciences, 2-1-2 Kannondai, Tsukuba, Ibaraki
305-8602, Japan; †Endocrinology and Metabolism Research Team, National Institute of Livestock
and Grassland Science, Tsukuba, Ibaraki 305-0901, Japan; and ‡School of Veterinary Medicine,
Kitasato University, Towada, Aomori 034-8628, Japan
ABSTRACT: To understand the regulatory mechanism of the secretory rhythm of GH and the involvement of melatonin (MEL) in GH regulation in cattle,
daytime and nighttime profiles of GH secretion and the
effect of a photic stimulation on nocturnal GH and MEL
secretion were investigated in Holstein steers. Steers
were kept under a constant lighting condition of 12 h
of light (LIGHT; 500 lx, 0600 to 1800 h):12 h of dark
(DARK; 10 lx, 1800 to 0600 h). In Exp. 1, blood was
taken for 4 h at 15-min intervals during LIGHT (1100
to 1500 h) and DARK (2300 to 0300 h), respectively.
The sampling was also performed from 0500 to 0900
h, with the usual light transition (light onset at 0600
h; morning sampling). In Exp. 2, steers were exposed
to light (500 lx) for 1 h from 0000 to 0100 h. Plasma
GH and MEL concentrations were determined by RIA
and enzyme immunoassay, respectively. Both GH (P
< 0.05) and MEL (P < 0.01) concentrations in plasma
for 4 h during DARK were greater than those during
LIGHT. On the other hand, although MEL concentrations were decreased after the light onset at 0600 during the morning, GH release was not altered. Increased
GH secretion during DARK was suppressed (P < 0.01)
by the 1 h of light exposure, as were MEL concentrations (P < 0.05). Pineal MEL, which was affected by
the photic condition, may play an important role in the
secretory rhythm of GH secretion in cattle.
Key words: cattle, growth hormone, melatonin, photic stimulation, rhythm
©2008 American Society of Animal Science. All rights reserved.
INTRODUCTION
It has been known that spontaneous GH secretion
shows a distinct increase during the night in humans
(Finkelstein et al., 1972; Kostoglou-Athanassiou et al.,
1998), monkeys (Kaler et al., 1986), and rats (Davies
et al., 2004), and the increase in GH is abolished by
photic stimulation during night in humans (KostoglouAthanassiou et al., 1998) and rats (Davies et al., 2004).
Therefore, the photic condition is considered to be one
of the environmental factors affecting GH secretion.
1
This work was supported by a Grant-in-Aid for Scientific Research (19580333 to EK, MS, and SK) from the Japan Society for
the Promotion of Science. We thank the staff of Ruminants and Field
Management Section, Department of Research Planning and Coordination, National Institute of Livestock and Grassland Science, Ibaraki, Japan, H. Morikawa, Y. Okada, A. Furukawa, S. Tamura, and
T. Matsu-ura, for their technical assistance. We are also grateful to
F. Terada and I. Nonaka, National Institute of Livestock and Grassland Science, for their advice for statistical analysis.
2
Corresponding author: [email protected]
Received January 17, 2008.
Accepted March 24, 2008.
J. Anim. Sci. 2008. 86:1799–1807
doi:10.2527/jas.2008-0877
Melatonin (MEL) is a chemical signal substance that
transmits the photoperiodic signal from the eye to various organs, including the hypothalamus and pituitary
gland. Because it has been suggested that MEL affects
GH secretion via the hypothalamus (Richardson et al.,
1981; Valcavi et al., 1993), it is reasonable to speculate
that MEL mediates the photic influence on GH secretion.
In cattle, MEL secretion shows a circadian rhythm in
which the concentrations are low and high during day
and night, respectively (Hedlund et al., 1977; Berthelot
et al., 1990), as in other species. However, the involvement of MEL in the regulation of bovine GH secretion
has not been well defined. Recently, we found that intracerebroventricular injection of MEL significantly
increased GH release in steers (Kasuya et al., 2006).
This indicated that MEL plays an important role in the
regulation of GH secretion in cattle. Although profiles
of GH secretion for 24 h have been reported previously
in cattle (Breier et al., 1986; Miura et al., 2004), the apparent rhythm of GH secretion and the potential photic
effect on GH secretion have not yet been reported in
this species.
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Kasuya et al.
To clarify the participation of the photic condition in
the regulation of GH secretion in cattle, a comparison
of GH secretion during day and night was performed
in steers under strictly controlled lighting conditions.
Furthermore, the effect of a 1-h photic stimulus during
night on GH secretion was determined.
MATERIALS AND METHODS
The experimental procedure used in the present
study was approved by the Institute Committee for
Animal Use and Care at the National Institute of Agrobiological Sciences.
Steers
Holstein steers (n = 9; 6 to 8 mo old) raised on the
farm of the National Institute of Livestock and Grassland Science (Tsukuba, Japan) were used in the present study. The feed (timothy grass hay and concentrate) was sufficient to meet the energy and protein
requirements of the steers to achieve a growth rate of
0.9 kg/d based on the Japanese Feeding Standard (AFFRC, 1999). The steers were fed twice a day at 0830
and 1530 h and were allowed ad libitum access to water. Residual feed was not removed and was available
to the steer any time. To monitor its condition, each
steer was tied to a stanchion stall, and its rectal temperature was measured just before each feeding every
day.
Exp. 1: GH Secretory Pattern During Day
and Night in Steers
First, the spontaneous GH secretory rhythm was
determined in steers under fixed light conditions. All
experiments were performed at the Zootron of the National Institute of Livestock and Grassland Science,
where environmental conditions are strictly controlled
as follows: room temperature, humidity, and lighting
conditions were kept at 20°C, 60%, and 12 h of lightson (500 lx, 0600 to 1800 h; LIGHT):12 h of lights-off
(10 lx, 1800 to 0600 h; DARK), respectively. The steers
were well accustomed to the experimental conditions
(at least 10 d), experimental techniques (including entering the experiment room during day and night randomly), and investigators (including daily animal care
and handling) by the day of the experiment, such that
all procedures did not disturb the physiological conditions of the steers. An indwelling catheter was inserted
into an external jugular vein at least 20 h before the
initiation of the experiment, and blood samples were
taken without any pain. Blood sampling was begun at
1100 h (for LIGHT) or 2300 h (for DARK), and blood
(10 mL) was collected at 15-min intervals for 4 h. Five
hours after the light condition was changed (0600 and
1800 h) was defined as the beginning time of the sampling (1100 and 2300 h) in each period. Furthermore,
blood samples (10 mL) were also collected from 0500 to
0900 h (10 lx from 0500 to 0600 h, 500 lx from 0600 to
0900 h) to observe the secretory patterns of hormones
with the usual light transition in the morning.
For convenience in the sampling procedure during
the DARK period, a flashlight with a red lamp was
used when the blood samples were collected, but a direct flash to the eyes of the steers was avoided as far
as possible to prevent giving a photic stimulus to the
steer. Furthermore, to avert possible artifacts, we followed the same procedure using the same flashlight
even during the morning (0500 to 0900 h) and LIGHT
(1100 to 1500 h) periods. The scheme of the time course
is shown in Figure 1. Blood samples (10 mL) were collected and divided into heparinized (contained 65 U
of heparin, Terumo, Tokyo, Japan; for GH assay) and
EDTA-2Na-containing (3.0 mg of EDTA-2Na, Terumo,
for MEL assay) tubes and immediately put on ice. The
plasma was separated by centrifugation (1,500 × g,
4°C, 30 min) after each experiment was finished and
was stored at −20°C until assayed.
Exp. 2: Effect of Light Exposure for 1 h
on GH and MEL Secretion During Night
in Steers
Because a nocturnal increase in GH concentrations
was observed in Exp. 1, the effect of light exposure on
the increase was investigated. Seven of 9 steers used
in Exp. 1 were used for the light-exposure (EXPO) experiment. Steers were kept under the same light condition as in Exp. 1 until the light-exposure test was performed. On the day of the test, blood samples (10 mL)
were collected at 15-min intervals from 2300 to 0000
h. The light in the experimental room was turned on
right after the sample was taken at 0000 h. Then, blood
samples (10 mL) were taken every 15 min for 3 h. The
light was turned off right after the sample was taken at
0100 h. The scheme of the time course is shown in Figure 1. The sampling process including the method of
blood collection was similar to Exp. 1 other than turning on and off the light.
Hormone Assays and Statistical Analysis
Plasma GH concentrations were determined by a
double-antibody RIA based on the method of Johke
(1978). The intra- and interassay CV were 3.7 and 20%,
respectively; sensitivity was 1.25 ng/mL. Plasma MEL
concentrations were measured using a commercially
available EIA kit (RE54021, Immuno-Biological Laboratories Co. Ltd., Gunma, Japan) following the protocol of the manufacturer. The intra- and interassay CV
were 5.0 and 19%, respectively; sensitivity was 1.6 pg/
mL. Data were represented as the mean ± SE.
In Exp. 1, the area under the curve (AUC) for 4 h for
each period (LIGHT vs. DARK) was used to compare
the difference in total secreted volume of hormones
in each period. A comparison of the AUC between the
LIGHT and DARK periods was performed with a randomized block design ANOVA, with the steers as the
block. For the morning period, AUC for each 1-h pe-
Light alters nocturnal growth hormone in steers
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Figure 1. Schematic illustration of the time course of lighting conditions and blood sampling of Holstein steers.
For Exp. 1 and 2, open and closed squares represent 1-h periods of lights-on and lights-off, respectively. Four-digit
numbers show the time of day (h). The sampling periods of 4 h during each lighting condition [i.e., morning (light
on at 0600 h), continuous light on during the day, continuous darkness during the night, or 1 h of light on from
0000 to 0100 h during the night (darkness)] were expressed as MOR, LIGHT, DARK, or EXPO, respectively.
riod were analyzed as a randomized block design, with
steers as the block, using the GLM procedure of SYSTAT (Version 10.2 for Windows, Systat Software Inc.,
San Jose, CA). In Exp. 2, statistical significance of the
EXPO effect on hormone secretion was analyzed with a
split-plot design, with steers as blocks, sampling time
as the subplot, and treatment as the whole plot using
the GLM procedure of SYSTAT. Comparisons between
treatments at each sampling time were made by posthoc analysis with Fisher’s LSD test only if there was
a significant treatment × time interaction. Statistical
significance was assessed as P < 0.05. The significance
of differences for AUC (1 h) of GH and MEL between
2300 to 0000 h and 0000 to 0100 h time periods was
determined by paired Student’s t-tests.
RESULTS
GH and MEL Secretory Patterns During
LIGHT, DARK, and Morning in Steers
Mean circulating concentrations of GH during the
LIGHT and DARK periods in steers are shown in Figure 2. The greater concentrations of GH were observed
during the DARK compared with LIGHT periods (Figure 2A). The AUC of GH (4 h) during the DARK period
was larger (P < 0.05) than that during LIGHT (Figure
2B).
Figure 3 shows mean plasma MEL concentrations
in steers during LIGHT and DARK sampling periods.
Plasma MEL concentrations during DARK were greater than those during LIGHT (Figure 3A). The AUC of
MEL (4 h) during DARK was larger (P < 0.01) than
that during LIGHT (Figure 3B).
Figure 4 shows the AUC of GH (A) and MEL (B) for
each 1-h period during the morning (0500 to 0900 h).
The AUC of GH did not change before (0500 to 0600 h)
and after (0600 to 0900 h) the light on at 0600 h (Figure 4A). On the other hand, AUC of MEL after light
on were smaller (P < 0.01) than that before light on
(Figure 4B).
Effect of Light Exposure for 1 h on GH
and MEL Secretion During Night in Steers
The effect of a 1-h light exposure on increased GH release during the DARK period is shown in Figure 5. A
treatment × time interaction (P < 0.001) was observed
in the GH release in this experiment. In contrast to
the increased GH release during the DARK period,
mean concentrations of GH did not show such an increase when the steers were exposed to a 1-h period of
light from 0000 to 0100 h. The significant differences
in mean GH between the DARK and EXPO appeared
from 0030 to 0115 h. The plasma concentration of GH
began to rise 30 min after light exposure was terminated, reached its peak level at 0200 h, and then decreased (Figure 5A). The comparisons of 1-h AUC of
GH between 2300 to 0000 h and 0000 to 0100 h in both
DARK and EXPO are shown in Figure 5B. The AUC
of GH after 0000 h was larger (P < 0.01) than that before 0000 during the DARK. The increase of AUC after
0000 was not observed during the EXPO.
The effect of light exposure on MEL release during
the DARK period is shown in Figure 6. Mean MEL concentrations began to decrease 15 min after onset of the
light exposure (0015 h), and the decrease persisted until the end of light exposure (0100 h). Mean concentrations of plasma MEL in EXPO group were less (P < 0.05)
at 0200 and 0215 h and greater at 0230 h, compared
with the corresponding values of the DARK group (Figure 6A). The comparisons of 1-h AUC of MEL between
2300 to 0000 h and 0000 to 0100 h in both DARK and
EXPO are shown in Figure 6B. The AUC of MEL after
0000 h was larger (P < 0.05) than that before 0000 h
during the DARK. In contrast, AUC after 0000 h was
smaller (P < 0.05) than that before 0000 h during the
EXPO (P < 0.05).
DISCUSSION
The present study showed a distinct GH increase
during the night in Holstein steers. These observations
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Kasuya et al.
indicate that the nocturnal increase in GH secretion
exists in cattle as well as in humans (Finkelstein et
al., 1972; Kostoglou-Athanassiou et al., 1998), monkeys (Kaler et al., 1986), and rats (Davies et al., 2004).
Previous experiments performed in cattle did not show
such an increase in GH concentrations during the
night (Breier et al., 1986; Lee et al., 1991; Ozawa et al.,
1991; Miura et al., 2004). The mechanism(s) underlying the nightly increase in GH secretion has not been
completely revealed.
As observed in the present study, and similar to previous reports in cattle (Hedlund et al., 1977; Berthelot
et al., 1990), MEL synthesis or secretion, or both, is
clearly increased during the night. This nocturnal elevation of MEL concentration may be one of those factors mediating the nocturnal increase in GH, given that
MEL has a stimulatory effect on GH secretion when
injected into the third ventricle (Kasuya et al., 2006).
This observation led us to conclude that MEL is one of
the factors regulating GH secretion from the anterior
pituitary gland via the hypothalamus. The involvement
of pineal MEL in the regulation of GH secretion has
been reported previously, mostly in humans for clinical
purposes. Melatonin can stimulate GH release in hu-
Figure 2. The 4-h secretory profile of GH during the day (LIGHT) and night (DARK). (A) Mean plasma concentrations of GH during LIGHT (continuous light on during the day; open circles with solid line; n = 9) and DARK
(continuous darkness during the night; closed circles with solid line; n = 9), respectively. (B) Area under the GH
response curve (AUC) for 4 h of each sampling period. Each value is expressed as the mean ± SE. The asterisk
shows the statistical significance between the AUC during LIGHT and DARK (P < 0.05).
Light alters nocturnal growth hormone in steers
mans (Smythe and Lazarus, 1974; Valcavi et al., 1987,
1993), as we reported in cattle (Kasuya et al., 2006).
However, because the stimulatory effect of MEL on GH
release was obtained by exogenous administration of
MEL, it is possibly different from the physiological role
of MEL in the regulatory system of GH. In the present
study, we determined the GH profile during the night
with maintained darkness and a spontaneous increase
in MEL, as well as the effect of 1 h of light exposure on
GH secretion during the night to further understand
the involvement of MEL in GH secretion. Although the
increased concentrations of MEL already appeared at
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the initiation time of sampling during the night (2300
h), GH concentrations began to increase 1 h after the
initiation of sampling (0000 h). This time lag can be explained by the fact that GH is secreted from the anterior pituitary gland in a pulsatile manner. It is possible
that increased concentrations of MEL after the light off
at 1800 h increased pulsatile, not basal, GH release.
Interestingly, the large peak of GH appeared between
0000 and 0200 h in most steers used in the present
study, although the regularity of pulsatile GH secretion has not been reported in cattle to be different from
other species, such as rats (Tannenbaum and Martin,
Figure 3. The 4-h secretory profile of melatonin (MEL) during the day (LIGHT) and night (DARK). (A) Mean
plasma concentrations of MEL during LIGHT (continuous light on during the day; open circles with solid line; n
= 7) and DARK (continuous darkness during the night; closed circles with solid line; n = 7), respectively. (B) Area
under the MEL response curve (AUC) for 4 h of each sampling period. Each value is expressed as the mean ± SE.
The asterisk shows the statistical significance between AUC during LIGHT and DARK (P < 0.01).
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Kasuya et al.
1976) and goats (Mogi et al., 2004). It is possible that
MEL is one of factors mediating the pulsatility of GH
secretion.
Another interesting finding of the present study was
that 1 h of light exposure during the night clearly inhibited the nocturnal increase in GH secretion in steers.
The increase in GH was suppressed during the exposure and then occurred after the exposure was ended.
This observation is interpreted to mean that a photic
stimulus is able to alter the increase in GH during the
night in cattle. The present result raises the possibility
that MEL may be involved in the secretory pattern of
GH in this species, because MEL has been known as a
signal substance transmitting an ambient photic condition (Reiter, 1991). The 1 h of light exposure during
the night inhibited not only GH secretion but also the
persistent increased concentrations of MEL in the present study. This inhibition of MEL by the light exposure
was consistent with previous reports in rats (Davies
et al., 2004), ewes (Earl et al., 1985), goats (Deveson
et al., 1990), and cattle (Lawson and Kennedy, 2001;
Muthuramalingam et al., 2006).
To consider the mechanism of MEL-mediated GH secretion, it has been reported that somatostatin (SRIF)
plays a more important role than GHRH in MELmediated GH release in rats (Richardson et al., 1981)
and humans (Valcavi et al., 1993). Given that intracerebroventricular injection of MEL could not modify
GHRH-stimulated GH release (Kasuya et al., 2006),
SRIF might also be more important for MEL-induced
GH release in cattle. Although the involvement of MEL
in the regulation of GH release has been suggested as
described above, it has been also reported that photic
stimulation during the night can activate SRIF neurons in the periventricular nucleus to suppress GH increase in rats (Slade et al., 2001; Davies et al., 2004).
The possibility of this direct effect of light on the hypothalamus without the mediation by MEL should also
be evaluated to clarify the relationship between ambient lighting conditions and GH secretion.
It has been reported that light intensity of at least
50 lx is able to suppress plasma MEL concentrations
(Lawson and Kennedy, 2001) and that 10 lx or less is
safe for keeping increased concentrations of MEL during the night (Muthuramalingam et al., 2006) in cattle.
Thus, it is possible that there is a threshold of light
intensity that induces changes in endocrine factors,
including GH. Unfortunately, there is insufficient information about the lighting conditions in the previous
reports performed in cattle (Breier et al., 1986; Lee et
al., 1991; Ozawa et al., 1991; Miura et al., 2004). The
light intensity during the night in the present study
was approximately 2 lx when measured at the top of
the stanchion stall. Although we have not compared
various conditions of light intensity, we assume that
strictly maintained darkness during the night (light intensity less than 10 lx) is necessary to induce the augmentation of GH release in this species.
Figure 4. The changes in area under the (A) GH and
(B) melatonin (MEL) curves (AUC) for 1-h periods during the morning before (closed column) and after (open
column) the light was turned on at 0600. Each value
is expressed as the mean ± SE. An arrow indicates the
time of light on. Asterisks show the statistical significance compared with the 1-h AUC of the dark period in
the morning (0500 to 0600 h; P < 0.01).
Light alters nocturnal growth hormone in steers
On the other hand, the usual light transition in the
morning (light on at 0600 h) did not alter GH release
even though MEL release dramatically decreased after
the lighting condition was changed from dark to light
at 0600 h. It seems that photic stimulation is able to alter GH secretion only when its secretion is augmented
during the night. Furthermore, it is possible that GH
secretion is controlled by not only light onset but also
by other physiological events, such as the sleep-wake
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cycle. It has been reported that the nocturnal increase
in GH secretion is related to the sleep-wake cycle in
humans (Spiegel et al., 2000) monkeys (Quabbe et al.,
1983), and lambs (Laurentie et al., 1989). Because research concerning the sleep-wake cycle using electroencephalograms and the rhythm of the endocrine system has not yet been carefully done in cattle, we cannot
reach any conclusion in regard to the connection between wakefulness and GH secretion in this species at
Figure 5. The 4-h secretory profile of GH during the night (continuous darkness; DARK; n = 7) and before and
after a 1-h light exposure (light on from 0000 to 0100 h; EXPO; n = 7) treatment. (A) Mean plasma concentrations
of GH during DARK (closed circles with solid line) and EXPO (open circles with dotted line), respectively. The
open box indicates the 1-h period during which the light was on in the EXPO group. Each value is expressed as the
mean ± SE. The asterisks show the statistical significance between the corresponding values of DARK and EXPO
(*P < 0.05, **P < 0.01, and ***P < 0.001). (B) Area under the GH response curve (AUC) for 1-h periods (2300 to
0000 and 0000 to 0100 h) of DARK and EXPO. Solid bars indicate AUC during the lights-off period. An open bar
indicates AUC during the lights-on period. The asterisk shows the statistical significance between 2300 to 0000
and 0000 to 0100 h (**P < 0.01).
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Kasuya et al.
Figure 6. The 4-h secretory profile of melatonin (MEL) during the night (continuous darkness; DARK; n =
7) and before and after a 1-h light exposure (light on 0000 to 0100 h; EXPO; n = 7) treatment. (A) Mean plasma
concentrations of MEL during DARK (closed circles with solid line) and EXPO (open circles with dotted line), respectively. The open box indicates the 1-h period during which the light was on in the EXPO group. Each value
is expressed as the mean ± SE. Asterisks show the statistical significance between the corresponding values of
DARK and EXPO (*P < 0.05, **P < 0.01). (B) Area under the MEL response curve (AUC) for 1-h periods (2300 to
0000 and 0000 to 0100 h) of DARK and EXPO. Solid bars indicate AUC during the lights-off period. An open bar
indicates AUC during the lights-on period. The asterisk shows the statistical significance between 2300 to 0000
and 0000 to 0100 h (*P < 0.05).
present. In regard to the possible species differences
in the sleep-wake pattern, it should be noted that the
connection between the GH instantaneous secretion
rate and the state of wakefulness has been reported in
lambs (Laurentie et al., 1989), which may help understand the mechanism in cattle.
In summary, a nocturnal GH increase was observed
in Holstein steers, and the increase was altered by 1 h
of light exposure during the night. The nightly increase
in concentrations of MEL was also inhibited by the exposure. Thus, the pineal MEL, which was affected by
a photic condition, may play an important role in the
secretory rhythm of GH secretion in cattle.
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