вход по аккаунту


Effect of the Photoperiod and Administration of Melatonin on the Pars Tuberalis of Viscacha Lagostomus maximus maximusAn Ultrastructural Study.

код для вставкиСкачать
THE ANATOMICAL RECORD 293:871–878 (2010)
Effect of the Photoperiod and
Administration of Melatonin on the
Pars Tuberalis of Viscacha
(Lagostomus maximus maximus):
An Ultrastructural Study
Cátedra de Anatomı́a Humana, Bioquı́mica y Farmacia, Universidad Nacional
de San Luis, San Luis, Argentina
Cátedra de Histologı́a y Embriologı́a, Facultad de Quı́mica, Bioquı́mica y Farmacia,
Universidad Nacional de San Luis, San Luis, Argentina
Instituto de Histologı́a y Embriologı́a (IHEM), Universidad Nacional de Cuyo, Consejo
Nacional de Investigaciones (CONICET), Argentina
The pituitary pars tuberalis (PT) is a glandular zone exhibiting welldefined structural characteristics. Morphologically, it is formed by specific
secretory cells, folliculostellate cells, and migratory cells coming from the
pars distalis. The purpose of this work was to investigate differences in specific cellular characteristics in the PT of viscachas captured in summer
(long photoperiod) and winter (short photoperiod), as well as the effects of
chronic melatonin administration in viscachas captured in summer and
kept under long photoperiod. In summer, the PT-specific cells exhibited celllike characteristics with an important secretory activity and a moderate
amount of glycogen. In winter, the PT-specific granulated cells showed ultrastructural variations with signs of a reduced synthesis activity. Also, PT
showed a high amount of glycogen and a great number of cells in degeneration. After melatonin administration, the ultrastructural characteristics
were similar to those observed in winter, but the amount of glycogen was
higher. These results suggest possible functional implications as a result of
morphological differences between long and short photoperiods, and are in
agreement with the variations of the pituitary-gonadal axis, probably in
response to the natural photoperiod changes through the pineal melatonin.
The ultrastructural differences observed in PT, after melatonin administration, were similar to those observed in the short photoperiod, thus supporting the hypothesis that these cytological changes are induced by melatonin.
C 2010 Wiley-Liss, Inc.
Anat Rec, 293:871–878, 2010. V
Key words: Lagostomus maximus maximus; pars tuberalis;
ultrastructure; photoperiod; melatonin
Grant sponsor: Universidad Nacional de San Luis; Contract
grant number: Proyecto 22/Q603 CyT.
*Correspondence to: Edith Perez Romera, Cátedra de Anatomı́a Humana, Facultad de Quı́mica, Bioquı́mica y Farmacia,
Universidad Nacional de San Luis, Av. Ejército de los Andes
950–2 Piso, (5700) San Luis, Argentina. Fax: 54-2652-422644/
430224. E-mail:
Received 25 June 2009; Accepted 15 October 2009
DOI 10.1002/ar.21083
Published online in Wiley InterScience (www.interscience.wiley.
The pituitary pars tuberalis (PT) is a glandular zone
exhibiting well-defined structural characteristics (Dellmann et al., 1974; Fitzgerald, 1979; Gross, 1984; Stoeckel
and Porte, 1984). Its abundant irrigation and the presence of cells containing dense secretory vesicles demonstrate its important secretory activity. In all the studied
mammals, the PT is a thin cellular sheath surrounding
the pituitary stalk and extending along the basal surface
of the median eminence. Morphologically, it is constituted
by specific secretory cells (the so-called PT-specific cells),
folliculostellate cells and migratory cells coming from the
pars distalis (PD) (Oota and Kurosomi, 1966; Cameron
and Foster, 1972; Stoeckel and Porte, 1984).
The viscacha pituitary PT exhibits a parenchyma with
a well-defined histoarchitecture and a well-developed
capillary plexus, probably belonging to the hypothalamus-pituitary portal system. The capillaries extend all
along the pituitary zone. The PT cells are arranged longitudinally in cords and separated by blood capillaries.
Observation with the transmission electron microscope
reveals the presence of specific granulated cells (PT-specific cells), agranulated cells and folliculostellate cells.
Two types of specific granulated cells can be distinguished: cells with large secretory granules ranging
from 150 to 500 nm (PT-specific cells Type I), and cells
with small secretory granules between 65 and 200 nm
(PT-specific cells Type II). Agranulated cells are distributed along the entire PT. Folliculostellate cells are
arranged in follicles. The plasma membrane exhibits microvilli that project into the lumen, which displays colloidal-like material. All the described cellular types exhibit
deposits of cytoplasmic glycogen. Numerous nerve endings in contact with the plasma membrane are observed
in the secretory cells (Perez Romera et al., 2005).
The PT is characterized by the presence of melatonin
receptors. Numerous studies have shown that the highest density of melatonin receptors has been found in the
pituitary PT and in a projection from this region extending over the anteroventral PD, known as zona tuberalis
(ZT) (Skinner and Robinson, 1995) of all the studied animals (Vanecek et al., 1987; Williams and Morgan 1988;
Masson-Pevet et al., 1996; Morgan and Williams, 1996),
including humans (Von Gall C et al., 2002; Wu YH et al.,
2006). The PT-specific cells constitute the melatonin-responsive cell group (Morgan et al., 1991, 1994).
Studies carried out in some species such as the hibernating garden door mouse (Dellmann et al., 1974) and
the hedgehog (Rütten et al., 1988) have demonstrated
circannual morphological changes in the PT-specific
cells. Wittkowski et al. (1984) examined the ultrastructural aspects of the pituitary PT of the Djungarian hamsters maintained under long and short photoperiods, and
Böckers et al. (1995) studied the effects of melatonin in
the same species. Both studies showed changes in the
ultrastructure of PT-specific cells.
In our laboratory, previous studies have been conducted to determine the structural and ultrastructural
characteristics of pituitary PD (Mohamed et al., 1995;
2000), pars intermedia (Scardapane, 1990) and PT of the
viscacha (Perez Romera et al., 2005). However, studies
on the influence of the photoperiod and melatonin
administration on the PT have not been carried out in
this species.
TABLE 1. Environmental conditions during
summer and winter
P (mm)
T ( C)
Summer (January–February)
Winter (June-July)
The viscacha (Lagostomus maximus maximus) is a
subterranean rodent belonging to the family Chinchillidae, living in the central zone of Argentina. These herbivorous animals, nocturnally active, emerge from their
burrows during periods of darkness from dawn to dusk
to feed on the surrounding vegetation (Llanos and
Crespo, 1952). It has a seasonal reproductive cycle
(Fuentes et al., 1991), with important participation of
the pineal gland (Dominguez et al., 1987; Cernuda-Cernuda et al., 2003). Its reproductive activity occurs during
the long days of summer and early autumn whereas on
short winter days, these animals experience an important testicular regression. These changes at the central
level affect the testicular and epididymal histophysiology
(Muñoz et al., 1997, 2001; Aguilera Merlo et al., 2005).
This study was performed to investigate differences in
the ultrastructural characteristics of the pituitary PT of
viscachas captured and killed in summer (long photoperiod, maximal gonadal activity) and winter (short photoperiod, minimal gonadal activity), as well as to
determine the effects of chronic melatonin administration in viscachas captured in summer and kept under
long photoperiod, in order to provide new data about the
PT and its relation with the pineal-pituitary-gonadal
axis in this photoperiod-dependent seasonal reproduction
Animals and Tissue Preparation
Seasonal study. Twelve adult male viscachas
(Lagostomus maximus maximus) weighing 4–8 kg were
captured in their natural habitat (six in summer; February–March and six in winter; July–August), near San
Luis, Argentina (33 20’south latitude and 760 m altitude). Values of solar irradiation expressed as heliophany (H) and mean values of precipitations (P) and
temperature (T) were provided by the Servicio Meteorológico Nacional San Luis (Table 1). The animals were
captured at night (between 24:00 and 05:00 hr) using
traps placed in their burrows and taken to the laboratory. Then, the viscachas were anesthetized with Nembutal (pentobarbital) and quickly decapitated (between
07:00 and 08:00 hr). The skull was opened, and the basal
hypothalamus and pituitary gland were rapidly dissected out en bloc and fixed by immersion. The specimens were fixed in Karnovsky’s fluid (Karnovsky, 1965),
post-fixed in 1% osmium tetroxide 2 hr at 4 C, washed
in phosphate buffer, pH 7.2–7.4, dehydrated in acetone
and embedded in Spurr plastic resin. Consecutive 1 lmthick sections were stained with 1% toluidine blue for
morphological orientation. For electron microscopy,
ultrathin sections were cut with a Porter-Blum ultramicrotome, contrasted with lead citrate and uranyl acetate
(Millonig, 1961). The ultrastructural characteristics of
PT were studied in detail under a Siemens Elmiscop I
electron microscope, and micrographs were captured for
morphometric analysis.
The reproductive condition of viscachas was carefully
assessed on the basis of observations by light microscopy
of testes. All male viscachas captured in winter were in
the gonadal regression period. These results were similar to those previously found in our laboratory (Muñoz,
1998). The experimental design was approved by the
local Ethics Committee and was in agreement with the
guidelines of the National Institutes of Health (NIH,
USA) for the use of experimental animals.
Melatonin administration. Eight adult male viscachas captured during the month of February (summer)
were used. The rodents were kept in isolated boxes with
free access to water and food at 20 C 2 C. They were
maintained under long photoperiods with a controlled
light regimen (14L:10D, lights-on from 10:00 to 24:00
hr). The experimental group received two daily subcutaneous injections of melatonin (Sigma, 100 lg/kg body
weight in oil solution) at 09:00 hr (lights-off), and 17:00
hr (lights-on), for 9 weeks. The control group received
only the diluent. The animals were anesthetized with
Nembutal (pentobarbital) and killed by decapitation at
08:00 hr (lights-off). Tissues were treated with the same
histological techniques used for the seasonal study. The
experimental design was carried out according to protocols previously used in viscachas in our laboratory (Scardapane et al., 1983; Muñoz, 1998; Mohamed et al., 2000;
Filippa et al., 2005; Filippa and Mohamed, 2006a,b,
2008). In addition, in both groups, the histological study
of the testes was carried out to confirm the effect of melatonin on the reproductive status. In the melatonintreated viscachas an inhibitory effect of this hormone on
the spermatogenic activity was observed. These results
were similar to those previously found in this rodent
(Muñoz, 1998).
Morphometric analysis. Glycogen: A computerassisted image analysis system was used to measure the
cytoplasmic area occupied by the glycogen in PT cells.
The images were captured by a Siemens Elmiscop I electron microscope, scanned at resolutions yielding 800 dpi
and processed with Image Pro Plus 5.0 software under
control of a Pentium IV computer. The software allowed
the following processes: automatic analogous adjust,
thresholding, background subtraction, distance calibration, and area measuring. The image was displayed on a
color monitor, and the cytoplasmic glycogen areas were
measured. Before counting, the distance calibration was
performed in lm, considering the magnification of the
electronic micrographs and the number of pixels per
inch. Twenty-five electronic micrographs were analyzed
in each PT for the morphometric study. Finally, 300
micrographs were used for the seasonal study and 200,
for the melatonin study. The percentage of cytoplasmic
glycogen area
P (%
P GA) was calculated
P using the formula
% GA ¼ Ag/ At 100, where PAg was the sum of
the cytoplasmic glycogen area and At was the sum of
the cellular cytoplasmic area. The number of cells with
degenerative processes was determined in the same
micrographs previously described for the glycogen determination. The results were expressed as percentage of
degenerating cells (%DC).
Statistical analysis. The results were expressed as
% means standard error of the mean (SEM) for all
data sets. Differences between summer-winter groups
and experimental-control groups were evaluated using
unpaired Student’s t test. A probability of less than 0.05
was assumed to be significant.
Pars Tuberalis in Long Photoperiod (Summer)
The ultrastructural study showed that both PT-specific
cells types (Type I and II) exhibited an eccentric nucleus
with regular edges and finely dispersed chromatin. They
showed large round, oval and elongated mitochondria,
rough endoplasmic reticulum, Golgi complex and glycogen particles which were scattered throughout the cytoplasm (Fig. 1b,c). Agranulated cells had nuclei with
smooth contours of the nuclear membrane and finely distributed chromatin. A voluminous cytoplasm exhibited
numerous oval and elongated mitochondria, Golgi complex and scarce rough endoplasmic reticulum, phagosomes and glycogen deposits (Fig. 1a). The cytoplasmic
glycogen area was 2.7% 0.28%. Folliculostellate cells
were characterized by dark and irregularly shaped
nuclei, moderately condensed chromatin and elongated
Pars Tuberalis in Short Photoperiod (Winter)
The ultrastructural analysis showed that the PT-specific granulated cells Type I exhibited a cytoplasm with
a great amount of large round and elongated mitochondria, a well-developed and often expanded rough endoplasmic reticulum and secretory granules with
heterogeneous electronic density (Fig. 2b). They frequently exhibited great cytoplasmic vacuolization and
irregularly shaped nuclei with clotted chromatin (Figs.
1e, 2d). Besides, a higher percentage of cells with degenerative processes (%DC) was observed in winter (17.6%
0.13%) in relation to summer (2.93% 0.08%, P <
0.001; Figs. 1e, 2c). The PT-specific granulated cells
Type II showed light nuclei with smooth contours. The
amount of mitochondria and rough endoplasmic reticulum was markedly reduced. Most of these cells exhibited
a scarce amount of secretory granules (Fig. 2a).
High amounts of glycogen either aggregated in clusters or scattered throughout the cytoplasm were
observed in many cells (Fig. 1f). The cytoplasmic glycogen area was 6.32% 0.3%, showing significant differences in relation to summer (P < 0.001). Few changes in
the ultrastructural appearance of the agranulated cells
were detected. Phagosomes, however, were more abundant (Fig. 1d). Apparent morphological differences of the
folliculostellate cells were not found.
Pars Tuberalis: Melatonin Administration
The PT of the control group exhibited cell-like characteristics with an important secretory activity, a moderate
amount of glycogen (3.5% 0.15%) and low %DC (3.13%
0.07%). These ultrastructural characteristics were
similar to those observed in summer (Fig. 3a,b).
In melatonin-treated animals, the PT-specific granulated cells showed ultrastructural differences similar to
those observed in winter, with signs of a reduced
Fig. 1. (a–c) Electronic micrographs of pituitary pars tuberalis (PPT)
of viscacha captured in the long photoperiod (summer). The glandular
cells exhibit regular nuclei (N) of smooth edges with finely distributed
chromatin. g, glycogen particles; m, mitochondria. (d–f) PPT of viscacha captured in the short photoperiod (winter). d. Note the abundant
accumulation of lysosome-like bodies (arrow); g, glycogen. e. degen-
erating PT-specific cell. This image is frequent in winter. *, dilated cisternae of rough endoplasmic reticulum. f. Cell with numerous deposits
of glycogen aggregated in clusters (arrowhead). Magnification: a, d ¼
2,000. Scale Bar ¼ 5 lm; b, e ¼ 2,500. Scale Bar ¼ 4 lm; c ¼
5,000. Scale Bar ¼ 2 lm; f ¼ 4,000. Scale Bar ¼ 2.5 lm.
Fig. 2. (a–d) Images of PT of viscacha captured in winter (short
photoperiod). a. I, type I PT-specific cell; II, type II PT-specific cell. b.
junction complex (arrow) among type I PT-specific cell and folliculostellate cells (F). c. follicular cavity filled with amorphous electron dense
material. c. Cells in advanced state of degeneration. d. vacuoles
formed by the great dilation of rough endoplasmic reticulum (*). N,
irregular nucleus with condensed chromatin. Magnification: a ¼
5,000. Scale Bar ¼ 2 lm; b, c ¼ 4,000. Scale Bar ¼ 2.5 lm; d ¼
8,000. Scale Bar ¼ 1.25 lm.
synthesis activity. The morphometric study of the cytoplasmic glycogen area in melatonin-treated animals
showed a significant increase in relation to the control
group 7.5% 0.3% (P < 0.001). Nevertheless, the PT
showed a higher amount of glycogen particles than in
winter (Fig. 3b,c). Besides, the %DC was significantly
higher in relation to the control (17.2% 0.12%, P <
from the neuroendocrine neurons of the hypothalamus,
suggesting a probable modulation of PT secretory cells on
the PD glandular cells (Wittkowski et al., 1999).
Morgan et al. (1992) studied the synthesis and secretion of proteins by using [35S] methionine in primary
cultures of ovine PT specific cells. These authors showed
that the accumulation of these proteins was enhanced
by stimulation of PT cells with forskolin, and this effect
was blocked by melatonin.
Dellmann et al. (1974) carried out a comparative ultrastructural study of the PT of several species and
observed regressive changes in the secretory cells of the
garden door mouse during hibernation. This hibernating
species showed a decrease in the secretory granules, a
decrease in the rough endoplasmic reticulum and an
aggregation of increasing amounts of glycogen granules.
These findings suggested that the photoperiod might
have some influence on the PT histophysiology.
Wittkowski et al. (1984) studied the influence of the
photoperiod on the PT ultrastructure of the Djungarian
Studies on different species have shown that the PT is
a well-developed pituitary area with an important secretory activity, made evident by the presence of secretory
granules and abundant irrigation (Oota and Kurosomi,
1966; Dellmann et al., 1974; Fitzgerald, 1979; Perez
Romera et al., 2005).
The secretory cells are in close contact with the primary plexus capillaries of the portal hypothalamic-pituitary system, together with nerve endings of fibers coming
hamster and found alterations in the specific secretory
cells of the animals exposed to short photoperiods.
In the present work, the ultrastructural aspects of the
viscacha PT were studied during the long (summer) and
short (winter) photoperiods and after melatonin-chronic
administration. The PT of viscacha has two types of PTspecific cells: Type I and Type II. These cells do not react
with antibodies directed against the PD hormones (Perez
Romera et al., 2005). Both cell types showed ultrastructural differences in relation to the photoperiod length. In
winter, the PT specific cells type I showed great dilation of
the endoplasmic reticulum. The abundant amount of cytoplasmic vacuoles and the presence of secretory granules in
clusters observed in a great number of cells in different
degradation stages are indicative of a local cytoplasmic
degeneration known as crinophagy (Farquhar, 1977). The
PT-specific cells type II showed signs of a reduced synthesis activity in winter. The marked glycogen increase indicated an energy reserve state, probably due to a decrease
in the cellular activity. The PT of viscacha showed a
higher number of lysosome-like bodies in winter in relation to summer, unlike the Djungarian hamster, which
showed a decrease in the number of dense lysosome-like
bodies in winter (Wittkowski et al., 1984). The changes
are also comparable to those reported by an investigation
of the hedgehog (Rütten et al., 1988). Chronic melatonin
administration induced variations in PT of viscacha similar to those observed in winter.
These ultrastructural characteristics found in viscacha
are suggestive of functional differences of the PT in
summer and in winter, and after the administration of
melatonin. The high affinity of melatonin receptors found
in the PT-specific cells of several species (Vanecek et al.,
1987; Williams and Morgan, 1988; Masson-Pevet et al.,
1996; Morgan and Williams, 1996) suggested that the pineal melatonin might be involved in these differences.
In other seasonal breeders, pronounced photoperioddriven seasonal changes occur in the levels of prolactin
secretion, and these effects are thought to be mediated by
the pineal hormone melatonin, which acts as a humoral
indicator of the photoperiod. Therefore, factors released by
the PT might regulate the activity of lactotrophs in the
PD (Wittkowski et al., 1992; Morgan et al., 1996). Hazlerigg et al. (1996) investigated this hypothesis using a range
of co-culture and medium-conditioning experiments on primary cultures of ovine PT and PD cells. They reported
that PT cells secreted an unidentified factor that is a
potent stimulus of prolactin secretion by PD cells. Lafarque et al. (1998) reported that the active factor/s should
have a molecular weight higher than 30 kDa.
Melatonin might directly regulate the synthesis and liberation of this unidentified factor, which acts on the PD
cells, mainly the lactotrophs, thus regulating the synthesis
and liberation of prolactin (Wittkowski et al., 1999). This
hypothesis is structurally supported by the studies on the
hypothalamus–pituitary disconnected ram. These studies
suggest that photoperiodic modulation of prolactin
Fig. 3. a. Characteristic aspect of pars tuberalis of viscacha maintained under long photoperiod (control). PT-specific cell with typical
smooth outlines of nucleus (N). The cytoplasm shows a well-developed rough endoplasmic reticulum, mitochondria and secretory granules. (b, c) Characteristic aspect of pars tuberalis of melatonin-treated
viscachas. b. Nucleus of secretory cell (N) is irregularly formed and
shows deep invaginations. High amounts of glycogen aggregated in
clusters and scattered throughout the cytoplasm (arrow). c. Typical aspect of secretory cells of PT. Cytoplasm filled with dense accumulation of glycogen particles (arrow); N, nucleus. Magnification: a ¼
5,000. Scale Bar ¼ 2 lm; b ¼ 5,500. Scale Bar ¼ 1.82 lm; c ¼
4,000. Scale Bar ¼ 2.5 lm.
secretion can occur independently from the hypothalamus,
presumably due to melatonin direct effects on the anterior
pituitary (Lincoln and Clarke, 1994, 1995).
It has also been demonstrated in most species that the
PT-specific cells express the common alpha chain of glycoprotein hormones (Böckers et al., 1994; Stoeckel et al.,
1994) and thyrotrophin beta chain (TSHb). The PT TSHpositive cells were indeed different from PD TSH-positive
cells (Sakai et al., 1999; Wittkowski et al., 1999; Bockman
et al., 1997). Recent studies have demonstrated that the
TSHb secreted by PT controls the expression of type II
and type III thyroid hormone deiodinase (Dio2) and (Dio3)
in the ependymal cell layer of the infundibular recess
(EC) via TSH receptors (TSHr) (Nakao et al., 2008). Melatonin-dependent regulation of thyroid hormone levels in
the mediobasal hypothalamus appears to involve TSH in
mammals. There is clear evidence in mice that TSH participates in this photoperiodic signal transduction (Ono
et al., 2008). Hanon et al. (2008) demonstrated in Soay
sheep that the TSH-expressing cells of the PT play an ancestral role in seasonal reproductive control in vertebrates. In mammals, this role provides the missing link
between the pineal melatonin signal and thyroid-dependent seasonal biology. It has recently been suggested that
melatonin affects the expression of Dio2 and Dio3 in EC
due to the action on the receptor MT1 localized in the PT.
(Yasuo et al., 2009). Unfried et al. (2009) postulated a
model depicting the autocrine/paracrine pathway of TSH
derived from the PT. Melatonin acts through the MT1 receptor and activates expression of the TSHr in the PT.
The expression of TSHb mRNA in the PT is inhibited by
melatonin and the molecular clockwork. Thyroid-stimulatin hormone acts retrogradely in the EC in which it activates Dio2 expression via phosphorylated cAMP response
element-binding protein (pCREB) signaling. DIO2 converts T4 into T3, which facilitates the release of gonadotropin-releasing hormone (GnRH) into the hypothalamopituitary portal system. This mechanism might be important for fine-tuning of seasonal reproduction.
Previous studies have demonstrated that the viscacha
showed maximal pineal activity in winter and minimal
activity in summer (Dominguez et al, 1987; Fuentes et
al, 2003). Also, it exhibited in its photoperiod-dependent
reproductive cycle maximal gonadal activity in summer
and minimal in winter (Fuentes et al., 1991; Muñoz
et al., 1997, 2001). In PD, the LH gonadotrophs, somatotrophs, corticotrophs, thyrotrophs, and lactotrophs
showed lower cellular activity in winter. In addition, LH
gonadotrophs, corticotrophs, somatotrophs, and lactotrophs decreased their activity after melatonin administration (Filippa et al., 2005; Filippa and Mohamed,
2006a,b, 2008; Filippa V, 2008).
In this work, we demonstrate that seasonal ultrastructural differences occur in the PT of the viscacha and
that melatonin-chronic administration induces variations in the PT similar to those occurring during the
short photoperiod (winter). These results are in agreement with the variations of the pituitary-gonadal axis,
probably in response to the changes in the natural photoperiod through the pineal melatonin. In addition, our
results allow us to propose the viscacha (Lagostomus
maximus maximus) as a new and interesting model for
future studies of the PT and its participation in the complex mechanism of reproduction regulation through the
environmental signals.
The authors wish to thank Mr. J. Arroyuelo and Mr.
N. Perez for their technical participation.
Aguilera-Merlo C, Muñoz E, Dominguez S, Scardapane L, Piezzi R.
2005. Epididymis of viscacha (Lagostomus maximus maximus):
morphological changes during the annual reproductive cycle.
Anat Rec A Discov Mol Cell Evol Biol 282A:83–92.
Böckers TM, Bockman J, Fauteck JD, Kreutz MR, Bock R, Wittkowski W. 1994. Pars tuberalis-specific cells in the ovine pituitary do
express the common a-chain of glycoprotein hormones: an in situ
hybridization and immunocytochemical study. Eur J Endocrinol
Böckers TM, Niklowitz P, Bockmann J, Fauteck JD, Wittkowski W,
Kreutz MR. 1995. Daily melatonin injections induce cytological
changes in pars tuberalis specific cells similar to short photoperiod. J Neuroendocrinol 7:607–613.
Bockmann J, Böckers TM, Winter C, Wittkowski W, Winterhoff H,
Deufel T, Kreutz MR. 1997. Thyrotropin expression in hypophyseal pars tuberalis-specific cells is 3,5,30 -triiodothyronine, thyrotropin-releasing hormone, and pit-1 independent. Endocrinology
Cameron E, Foster CL. 1972. Some light and electron microscopical
observations on the pars tuberalis of the pituitary gland of the
rabbit. J Endocrinol 54:505–511.
Cernuda-Cernuda R, Piezzi RS, Dominguez S, Alvarez-Urı́a M.
2003. Cell populations in the pineal gland of the viscacha (Lagostomus maximus maximus). Seasonal variations. Histol Histopathol 18:827–836.
Dellmann HD, Stoeckel ME, Hindelang-Gertner C, Porte A, Stutinsky F. 1974. A comparative ultrastructural study of the pars
tuberalis of various mammals, the chicken and the newt. Cell Tissue Res 148:313–329.
Dominguez S, Piezzi R S, Scardapane L, Guzmán JA. 1987. A light
and electron microscopic study of the pineal gland of the vizcacha
(Lagostomus maximus maximus). J Pineal Res 4:211–219.
Farquhar MG. 1977. Secretion and crinophagy in prolactin cells. In:
Dellmann D, Johnson JA, Klachko DM. Comparative endocrinology of prolactin. Plenum: New York, p 37–94.
Filippa V. 2008. Histofisiologı́a de la pars distalis hipofisiaria del
Lagostomus maximus maximus: relación con el fotoperı́odo, edad
y sexo. Doctoral Thesis, Biblioteca Central Universidad Nacional
de San Luis, San Luis, Argentina.
Filippa V, Mohamed F. 2006a. ACTH cells of pituitary pars distalis
of viscachas (Lagostomus maximus maximus): immunohistochemical study in relation to season, sex, and growth. Gen Comp Endocrinol 146:217–225.
Filippa V, Mohamed F. 2006b. Immunohistochemical study of somatotrophs in pituitary pars distalis of viscachas (Lagostomus maximus maximus) in relation to the gonadal activity. Cell Tissues
Organs 184:188–197.
Filippa V, Mohamed F. 2008. Immunohistochemical and morphometric study of pituitary pars distalis thyrotrophs of male viscacha
(Lagostomus maximus maximus): Seasonal variations and effect
of melatonin and castration. Anat Rec (Hoboken) 291:400–409.
Filippa V, Penissi A, Mohamed F. 2005. Seasonal variations of
gonadotropins in the pars distalis male viscachas pituitary. Effect
of chronic melatonin treatment. Eur J Histochem 49:291–300.
Fitzgerald KT. 1979. The structure and function of the pars tuberalis of the vertebrate adenohypophysis. Gen Comp Endocrinol
Fuentes LB, Caravaca N, Pelzer LE, Scardapane L, Piezzi RS, Guzmán JA. 1991. Seasonal variations in the testis and epididimys of
viscacha (Lagostomus maximus maximus). Biol Reproduction
Fuentes LB, Moller M, Muñoz E, Calderón C, Pelzer L. 2003. Seasonal variations in the expression of the mRNA encoding b1-adrenoceptor and AA-NAT enzyme, and in the AA-NAT activity in the
pineal gland of vizcacha (Lagostomus maximus maximus). Correlation with serum melatonin. Biol Rhythm Res 34:193–206.
Gross DS. 1984. The mammalian hypophyseal pars tuberalis: a
comparative immunocytochemical study. Gen Comp Endocrinol
Hanon EA, Lincoln GA, Fustin JM, Dardente H, Masson-Pevet M,
Morgan PJ, Hazlerigg DG. 2008. Ancestral TSH mechanism signals summer in a photoperiodic mammal. Curr Biol 18:1147–
Hazlerigg DG, Hastings MH, Morgan PJ. 1996. Production of a prolactin releasing factor by the ovine pars tuberalis. J Neuroendocrinol 8:489–492.
Karnovsky MJ. 1965. A formaldehyde-glutaraldehyde fixate of high
osmolarity for use in electron microscopy. J Cell Biol 27:137–8A.
Lafarque M, Oliveros L, Aguado L. 1998. Efecto de secreciones de
pars tuberalis de la adenohipofisis sobre la liberación de prolactina desde pars distalis. Medicina 58:36–40.
Lincoln GA, Clarke IJ. 1994. Photoperiodically-induced cycles in the
secretion of prolactin in hypothalamo-pituitary disconnected
rams: evidence for translation of the melatonin signal in the pituitary gland. J Neuroendocrinol 6:251–260.
Lincoln GA, Clarke IJ. 1995. Evidence that melatonin acts in the pituitary gland through a dopamine-independent mechanism to
mediate effects of daylength on the secretion of prolactin in the
ram. J Neuroendocrinol 7:637–643.
Llanos AC, Crespo JA. 1952. Ecologia de la vizcacha (Lagostomus
maximus maximus) en el nordeste de la provincia de Entre Rios.
Rev Invest Agric 10:5–95.
Masson-Pevet M, Gauer F, Recio J. 1996. Melatonin receptors, pars
tuberalis and photoperiodic response. Front Horm Res 21:84–89.
Millonig GA. 1961. A modified procedure for lead staining of thin
sections. J Biophys Biochem Cytol 11:736–739.
Mohamed F, Fogal T, Dominguez S, Scardapane L, Guzmán J,
Piezzi RS. 1995. Ultrastructure of pars distalis of viscacha (Lagostomus maximus maximus). Pituitary cellular types. Biocell
Mohamed F, Fogal T, Dominguez S, Scardapane L, Guzmán J,
Piezzi RS. 2000. Colloid accumulations in the pituitary pars distalis of viscacha (Lagostomus maximus maximus). A numeric study
in relation to season, sex and growth. Anat Rec 258:252–261.
Morgan PJ, Barrett P, Davidson G, Lawson W. 1992. Melatonin regulates the synthesis and secretion of several proteins by pars-tuberalis cells of the ovine pituitary. J Neuroendocrinol 4:557–563.
Morgan PJ, Barrett P, Howell HE, Helliwell R. 1994. Melatonin
receptors: localization, molecular pharmacology and physiological
significance. Neurochem Int 24:101–146.
Morgan PJ, King TP, Lawson W, Slater D, Davidson G. 1991. Ultrastructure of melatonin-responsive cells in the ovine pars tuberalis. Cell Tissue Res 263:529–534.
Morgan PJ, Webster CA, Mercer JG, Ross AW, Hazlerigg DG, MacLean A, Barrett P. 1996. The ovine pars tuberalis secretes a factor(s) that regulates gene expression in both lactotropic and
nonlactotropic pituitary cells. Endocrinology 137:4018–4026.
Morgan PJ, Williams LM. 1996. The pars tuberalis of the pituitary:
a gateway for neuroendocrine output. Rev Reprod 1:153–161.
Muñoz E. 1998. Estudio estacional del compartimiento tubular e
intersticial del testı́culo de vizcacha (Lagostomus maximus maximus): papel de la melatonina en la ciclicidad reproductiva y su
relación con el fotoperı́odo. Doctoral Thesis, Biblioteca Central
Universidad Nacional de San Luis, San Luis, Argentina.
Muñoz E, Fogal T, Dominguez S, Scardapane L, Guzmán J, Piezzi
R. 1997. Seasonal changes of the Leydig cells of viscacha (Lagostomus maximus maximus). A ligth and electron microscopy study.
Tissue Cell 29:119–128.
Muñoz E, Fogal T, Dominguez S, Scardapane L, Piezzi R. 2001. Ultrastructural and morphometric study of the Sertoli cell of the
viscacha (Lagostomus maximus maximus) during the annual
reproductive cycle. Anat Rec 262:176–185.
Nakao N, Ono H, Yamamura T, Anraku T, Takagi T, Higashi K,
Yasuo S, Katou Y, Kageyama S, Uno Y, Kasukawa T, Iigo M,
Sharp PJ, Iwasawa A, Suzuki Y, Sugano S, Niimi T, Mizutani M,
Namikawa T, Ebihara S, Ueda HR, Yoshimura T. 2008. Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature
Ono H, Hoshino Y, Yasuo S, Watanabe M, Nakane Y, Murai A, Ebihara S, Korf HW, Yoshimura T. 2008. Involvement of thyrotropin
in photoperiodic signal transduction in mice. Proc Natl Acad Sci
USA 105:18238–18242.
Oota Y, Kurosomi K. 1966. Electron microscopic studies on the pars
tuberalis of the rat hypophysis. Arch Histol Jpn 27:501–520.
Perez Romera E, Mohamed F, Filippa V, Fogal T, Dominguez S,
Scardapane L, Piezzi RS. 2005. Ultrastructural and immunocytochemical studies of the viscacha (Lagostomus maximus maximus)
pituitary pars tuberalis. Anat Rec A Discov Mol Cell Evol Biol
Rütten A, Hewing M, Wittkowski W. 1988. Seasonal ultrastructural
changes of the hypophyseal pars tuberalis in the hedgehog (Erinaceus europaeus L.) Acta Anat 133:217–223.
Sakai T, Sakamoto S, Ijima K, Matsubara K, Kato Y, Inoue K. 1999.
Characterization of TSH-positive cells in foetal rat pars tuberalis
that fail to express Pit-1 factor and thyroid hormone beta2 receptors. J Neuroendocrinol 11:187–193.
Scardapane L. 1990. Aspectos histofisiológicos de la pars intermedia hipofisiaria del Lagostomus maximus maximus. Doctoral Thesis, Biblioteca Central Universidad Nacional de San Luis, San
Luis, Argentina.
Scardapane L, Lucero J B, Dominguez S, Piezzi RS, Guzmán JA.
1983. Effect of chronic administration of melatonin on viscacha
pars intermedia (Lagostomus maximus maximus). Com Biol
Skinner DC, Robinson JE. 1995. Melatonin-binding sites in the
gonadotroph enriched zona tuberalis of ewes. J Reprod Fertility
Stoeckel ME, Hindelang C, Klein MJ, Poissonnier M, Felix JM.
1994. Expression of the alpha-subunit of glycoprotein homones in
the pars tuberalis-specific glandular cells in rat, mouse and
guinea-pig. Cell Tissue Res 278:617–624.
Stoeckel ME, Porte A. 1984. Ultrastructure and development of the
pars tuberalis of the mammals. In: Motta PM, editor. Ultrastructure of endocrine cells and tissues. Nijhoff: Boston. p 29–38.
Unfried C, Ansari N, Yasuo S, Korf HW, von Gall C. 2009. Impact
of melatonin and molecular clockwork components on the expression of thyrotropin beta chain (Tshb) and the Tsh receptor in the
mouse pars tuberalis. Endocrinology 150:4653–4662.
Vanecek J, Pavlik A, Illnerova H. 1987. Hypothalamic melatonin
receptor sites revealed by autoradiography. Brain Res 435(1–2):
Von Gall C, Stehle JH, Weaver DR. 2002. Mammalian melatonin
receptors: molecular biology and signal transduction. Cell Tissue
Res 309:151–162.
Williams LM, Morgan PJ. 1988. Demonstration of melatonin-binding sites on the pars tuberalis of the rat. J Endocrinol 119:Rl–R3.
Wittkowski W, Bockman J, Kreutz MR, Böckers TM. 1999. Cell and
molecular biology of the pars tuberalis of the pituitary. Int Rev
Cytol 185:157–194.
Wittkowski W, Hewing M, Hoffmann K, Bergmann M, Fechner J.
1984. Influence of photoperiod on the structure of the hypophyseal pars tuberalis of the Djungarian hamster, Phodopus sungorus. Cell Tissue Res 238:213–216.
Wittkowski W, Schulze-Bonhage A, Böckers T. 1992. The pars tuberalis of the hypophyis: a modulador of the pars distalis? Acta
Endocrinol (Copenh) 126:285–290.
Wu YH, Zhou JN, Balesar R, Unmehopa U, Bao A, Jockers R, Van
Heerikhuize J, Swaab DF. 2006. Distribution of MT1 melatonin
receptor immunoreactivity in the human hypothalamus and pituitary gland: colocalization of MT1 with vasopressin, oxytocin, and
corticotrophin releasing hormone. J Comp Neurol 499:897–910.
Yasuo S, Yoshimura T, Ebihara S, Korf HW. 2009. Melatonin transmits photoperiodic signals through the MT1 melatonin receptor.
J Neurosci 29:2885–2889.
Без категории
Размер файла
855 Кб
ultrastructure, lagostomus, effect, photoperiod, tuberalis, maximum, stud, maximusan, administration, viscacha, melatonin, pars
Пожаловаться на содержимое документа