|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online November 2, 2007
Journal of Experimental Biology 210, 3970-3978 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.010645
Area postrema, a brain circumventricular organ, is the site of antidipsogenic action of circulating atrial natriuretic peptide in eels
Laboratory of Physiology, Ocean Research Institute, The University of Tokyo, Tokyo 164-8639, Japan
* Author for correspondence at present address: Department of Cell Biology and Anatomy, The University of Arizona, 1656 E. Mabel-MRB330, Tucson, AZ 85724, USA (e-mail: tsukada{at}email.arizona.edu)
Accepted 3 September 2007
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Key words: blood–brain barrier, ANP receptor (NPR-A), fish osmoregulation, drinking behaviour, circumvetricular organ
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
;
Loretz and Pollina, 2000;
Takei and Hirose, 2002;
Toop and Donald, 2004). In
eels, ANP promotes adaptation to seawater (SW) by reducing excess
Na+ uptake from the environment
(Tsukada et al., 2005). The
reduced Na+ uptake is accomplished by decreases in both drinking of
environmental SW and subsequent absorption of Na+ ions by the
intestine, while renal and branchial excretion of Na+ are unchanged
by ANP infusion. In fact, removal of endogenous ANP and ventricular
natriuretic peptide, which also binds to the type A ANP receptor (NPR-A) with
similar affinity, from plasma by immunoneutralization increased plasma
Na+ concentration with a concomitant increase in drinking rate in
SW eels (Tsukada and Takei,
2006). These results strongly support the hypo-osmoregulatory
roles of ANP in SW. Despite such an important effect of ANP on drinking, the
proximate mechanisms and the site of action of ANP in the brain have not been
examined in detail.
The mechanisms regulating drinking have been intensively and extensively
investigated in mammals, reflecting its important role in body fluid
regulation (Fitzsimons, 1998;
Balment, 2002). Accumulating
evidence has shown that the central nervous system (CNS) controls drinking by
integrating neuronal and chemical signals originating in the brain and from
the periphery. Circulating hormones are major controllers of drinking through
their actions on the brain; these factors include angiotensin II (ANG II),
relaxin, bradykinin and ANP (Fitzsimons and
Simons, 1968; Katsuura et al.,
1986; Fregly and Rowland,
1991; Sinnayah et al.,
1999). However, since circulating hormones do not cross the
blood–brain barrier (BBB), they must act on the target sites outside the
BBB such as circumventricular organs (CVOs)
(Ferguson and Bains, 1996;
McKinley et al., 1999). In
mammals, the CVOs such as the subfornical organ (SFO), area postrema (AP) and
organum vasculosum of the lamina terminalis (OVLT) serve as a
blood–brain interface for the action of circulating hormones
(Ferguson and Bains, 1996). In
particular, forebrain CVOs, including the SFO and OVLT, are known to be
primary sites for the central regulation of body fluid balance in mammals
(Johnson and Gross, 1993;
McKinley et al., 1999) and in
birds (Simon et al., 1992).
For instance, administration of ANP and ANG II into the SFO influences the
neuronal activities within the structure
(Gutman et al., 1988) and
modifies drinking behaviour in mammals and birds
(Simpson and Routenberg, 1973;
Lin and Hubbard, 1992;
Takei, 1977). Further,
receptors for ANP (NPR-A type) and ANG II (AT1 subtype) are densely
localised in the SFO of mammals and birds
(Saavedra et al., 1986;
Quirion, 1989;
Gehlert et al., 1990;
Simon et al., 1992). Thus,
CVOs are the most probable sites of action of circulating hormones in the
brain.
In contrast to mammals and birds, fishes are unique in that the hindbrain
rather than the forebrain may be involved in the elicitation of drinking,
since eels without forebrain and midbrain (`decerebrated' eels) respond to SW
transfer (Hirano et al., 1972)
and to peripheral injection of ANG II
(Takei et al., 1979) by
copious drinking. Furthermore, direct injection of ANG II into the third
ventricle (Takei, 1992) or
fourth ventricle (Kozaka et al.,
2003) of eels induced drinking at much lower doses than peripheral
injections, suggesting that the ANG II acts on the brain to induce drinking in
fishes. Kozaka et al. further showed that ANP injection into the ventricle at
the level of medulla oblongata (MO) inhibits drinking in SW eels
(Kozaka et al., 2003), but the
effect was rather weak compared with the potent inhibition after peripheral
injection (Tsuchida and Takei,
1998). Reflecting on all the results obtained thus far, it is
likely that the major route of ANP action is from the periphery, and that
circulating ANP acts on the brain, probably at the level of MO, in eels. The
regulatory motor signals generated from the hindbrain may be transmitted
via the vagus nerves, since in the eel bilateral vagotomy abolished
drinking induced by SW transfer (Hirano et
al., 1972) and by peripheral ANG II injection
(Takei et al., 1979).
The present study was undertaken to determine the central receptor sites
for the antidipsogenic effect of ANP in the eel. Initially, the cellular
localization of NPR-A, a specific receptor for biological actions of ANP, was
determined in the brain nuclei by immunohistochemistry using an antiserum
specific for eel NPR-A. The BBB-deficient structures were identified in the
eel brain by peripheral injection of Trypan Blue, which is impermeable to the
BBB after binding to albumin (Clasen et
al., 1970). Since the AP was the only site possessing ANP
receptors and lacks a functional BBB, heat-coagulative lesions or chemical
lesions with kainic acid were made topically to the AP, and effects of the
lesioning on the antidipsogenic effect of peripherally injected ANP were
examined.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Immunohistochemistry
The eel brain sections were stained to determine the cells possessing NPR-A
using the Elite avidin-biotin-peroxidase complex kit (Vector Laboratories,
Burlingame, CA, USA). After anesthetizing eels (N=7) in 0.1% (w/v)
tricaine methanesulfonate (Sigma-Aldrich, St Louis, MO, USA) for 15 min, the
skull was opened and the exposed brain was fixed by 4% paraformaldehyde in
0.01 mol l–1 phosphate-buffered saline (PBS, pH 7.3) for 1 h
in situ. The brain was then dissected out of the skull and immersed
in the same fixative solution for 48 h at 4°C. The brain was immersed in
30% sucrose in PBS overnight at 4°C for cryoprotection and embedded in
Tissue-Tek OCT compound (Sakura Finetechnical, Tokyo, Japan) at
–20°C. Serial cross sections (10 µm thick) were cut and mounted
onto gelatin-coated slides and dried overnight at 4°C. For
immunohistochemistry, the sections were incubated sequentially with (1) 0.6%
H2O2 in methanol for 30 min at room temperature, (2) 2%
normal goat serum in PBS (NGS-PBS) containing 0.01% sodium azide for 1 h at
room temperature, (3) the affinity-purified antiserum for NPR-A diluted at
1:9000 with NGS-PBS for 48 h at 4°C, (4) biotinylated, goat anti-rabbit
IgG for 30 min at room temperature, (5) avidin-biotin-peroxidase complex for
45 min at room temperature, and (6) 0.05% diaminobenzidine tetrahydrochloride
and 0.01% hydrogen peroxidase in 50 mmol l–1 Tris buffer (pH
7.2) for 10 min at room temperature. Specificity of immunoreactive signals was
confirmed by preabsorption of the antibody with antigen-conjugated
CNBr-activated Sepharose 4B (GE Healthcare, Bucks, UK). The specificity of
this antiserum in eel tissue was confirmed by western blotting of membrane
fractions prepared from the gills as previously reported
(Healy et al., 2005).
Immunostained sections were counterstained with Haematoxylin and then
dehydrated and cleared, and coverslips placed on top for observation with a
light microscope (E800, Nikon, Tokyo, Japan). The brain loci were determined
in the present study based on the brain atlas of Japanese eel
(Mukuda and Ando, 2003a)
(Fig. 1).
|
Effect of AP lesioning on ANP-induced antidipsogenesis
Since the AP was identified as a probable target site for circulating ANP
(see Results), the involvement of the AP in ANP-induced antidipsogenesis was
evaluated in vivo. For this purpose, eels (N=49) were
anesthetized and cannulated with a polyethylene tube (o.d. 0.8 mm) in the
ventral aorta for injection of ANP. Then, vinyl tubes (o.d. 1.5 mm) were
inserted into the esophagus and stomach of eels for continuous measurement of
drinking rate as described previously
(Takei et al., 1998).
|
|
|
After surgery, eels were immediately placed, according to their individual
size, in a PlexiglasTM trough through which aerated SW continuously
circulated at 18°C to avoid deterioration of physiological conditions. The
trough was covered with a black vinyl sheet to minimize visual stress to the
animal during the experiments. Beginning at least 18 h after lesioning, each
eel received an injection of saline as control via aortic cannula in
a volume of 50 µl, followed by a flush of cannula with 50 µl saline.
Subsequently, 50 µl of ANP containing 100 pmol kg–1 eel
mass was injected in the same fashion. This dose is sufficient for the
antidipsogenic action of ANP (Takei and
Tsukada, 2001). The saline and ANP injections were separated by an
interval of at least 45 min. Drinking rate was measured throughout the
experimental period. After the experiment, eels were anesthetized and
decapitated for histological verification of the lesion sites
(Fig. 2).
Chemical lesioning to neurons
In addition to heat-coagulative lesioning by electric cautery, chemical
lesioning with kainic acid was undertaken to confirm that effect was due to
the lesion of AP neurons (Fig.
3). Kainic acid is an excitotoxic glutamate agonist that
specifically induces degeneration of neurons
(Tomioka et al., 2002). To
perform a topical microinjection of kainic acid to the AP, a glass capillary
injector was prepared from the glass capillary stock (o.d. 0.9 mm) with a
puller and a microgrinder (Narishige, Tokyo, Japan). The capillary injector
was connected to a 0.5 µl Hamilton microsyringe via polyethylene
tubing (o.d. 0.61 mm) (Fig.
3B). After exposure of the AP as described above, anesthetized
eels were placed on a stereotaxic apparatus (Narishige), and then the glass
capillary filled with kainic acid (4 mmol l–1, Sigma-Aldrich)
containing 1% Chicago Sky Blue 6B (Sigma-Aldrich) in PBS was inserted into the
AP to a depth of 0.1 mm by the manipulator of the stereotaxic apparatus.
Kainic acid solution (50 nl) was injected into the AP (N=7; AP-lesion
eels) or into an adjacent area (N=7; lesion control). Control
injection was also performed into the AP with 1% Chicago Sky Blue 6B in PBS
(N=7; sham control). The injections were accomplished within 1 min,
but the capillary remained in place for 3 min to insure complete injection of
volume. Beginning at least 18 h post-operatively, the eels were anesthetized
and cannulae were inserted into the dorsal aorta for injection of ANP and into
the esophagus and stomach for continuous measurement of drinking rate as
mentioned above. On the next day of cannulation, ANP was injected into the
dorsal aorta and the effect of AP lesioning on the ANP-induced
antidipsogenesis was examined. After the experiment, the distribution of
kainic acid was confirmed by staining with Chicago Sky Blue 6B
(Fig. 3C).
|
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Brain loci outside the blood–brain barrier
Intraperitoneally injected Trypan Blue was taken up into the blood stream
and stained almost all peripheral tissues. In contrast, no staining was
observed in the brain parenchyma except for the pineal gland and surrounding
saccus dorsalis (SD), parvocellular and magnocellular part of preoptic
nucleus, SV and AP (Fig.
5A–C). In addition to these loci, some RF and GVC neurons
were stained, but the signals were much weaker than other Trypan Blue-positive
loci (Table 1).
|
Effect of AP lesioning on ANP-induced antidipsogenesis
As the AP is the sole brain structure that is positive to both NPR-A
immunohistochemical staining and vital staining with Trypan Blue
(Table 1), it is the most
probable target site of circulating ANP. Therefore, the effect of AP lesioning
on antidipsogenesis caused by peripheral ANP injection was examined. Effects
of the heat-coagulative and chemical lesions to the AP on drinking are
summarized as changes in 20 min water intake before and after ANP injection
(Table 2), since the effect of
100 pmol kg–1 of ANP was usually continued for 20 min. After
heat-coagulative lesioning of the AP, ANP injection into the circulation no
longer inhibited drinking, although the inhibition was apparent in sham
controls and lesion controls. In addition, the AP lesioning also reduced basal
drinking in eels (Table 2).
Since heat coagulation not only destroys neurons in the AP but also neural
circuitry that traverses the AP, chemical lesioning that damages only AP
neurons was attempted with kainic acid. Average basal drinking rate of the
AP-lesioned eels with kainic acid was not different from those of sham
controls and lesion controls (Table
2). Furthermore, the antidipsogenic effect of ANP was
significantly suppressed by kainic acid lesioning of the AP, although slight
inhibition of drinking still remained after ANP injection
(Table 2). In order to
highlight the effect of AP lesions on the ANP effects, the time course of
changes in drinking rate was normalized to percentage change in drinking rate
after intravascular injection of ANP (Fig.
6). In sham-operated eels and lesion controls with intact AP,
drinking was strongly inhibited by ANP within 5 min after injection. However,
total destruction of the AP by electric cauterization abolished the
antidipsogenic effect of ANP injected into the circulation in SW eels
(Fig. 6A). After chemical
lesioning with kainic acid, the normalized time-course changes clearly shows
that AP-lesioned group significantly attenuated the antidipsogenic effect of
ANP compared with sham controls and lesion controls
(Fig. 6B).
|
|
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
). Although several ANP-binding sites are identified in the
mammalian brains (Saavedra et al.,
1986; Quirion,
1989), little is known about the mechanisms of how circulating ANP
acts on the brain to inhibit drinking compared with the many studies on the
cerebral mechanisms for elicitation of drinking by ANG II
(Fitzsimons, 1998). In contrast
to the relatively weak antidipsogenic effect of ANP in mammals, ANP potently
inhibits drinking in the eel, even more potently than the dipsogenic effect of
ANG II (Tsuchida and Takei,
1998; Takei,
2002). Furthermore, ANP is highly potent for inhibition of
drinking when injected systemically, which is in contrast to the much greater
potency of ANG II after intracranial injection compared with peripheral
injection. Therefore, the eel is an excellent model animal to investigate the
cerebral mechanisms underlying the antidipsogenic effect of circulating ANP.
In the present study, we pursued the site of action of peripherally generated
ANP in the brain by the two histological methods. The immunohistochemical
study using specific antiserum raised against eel NPR-A found immunoreactive
neurons only in MO loci, such as the RF, GVC, NCC and AP. Furthermore, the AP
was intensively stained by intraperitoneally injected Trypan Blue in eels, as
previously reported using Evans Blue
(Mukuda et al., 2005). These
results show that circulating ANP can act on NPR-A in the BBB-deficient
circumventricular structure in the MO. Therefore, the AP appears to be
directly involved in the potent antidipsogenic action of ANP delivered from
the periphery in the eel.
In addition to the histological approach, the ANP target site was also
pursued by physiological studies in vivo. Heat-coagulation of the AP
by electric cautery completely nullified the antidipsogenic effect of systemic
injection of ANP, whereas ANP delivered by the same route strikingly inhibited
drinking in sham-operated eels and in eels with lesions outside the AP. These
results strongly suggest that the AP is involved in the antidipsogenic effect
of circulating ANP in eel. However, heat-coagulative lesions to the AP
considerably decreased basal drinking compared with sham controls and with
controls experiencing lesions outside the AP. Since heat coagulation by
electric cautery destroyed not only AP neurons, but also nerve fibres running
through the AP, it is possible that the extensive destruction of the AP may
have affected the neural circuitry that is responsible for basal drinking in
eels. As an alternative method, therefore, the AP neurons were chemically
destroyed by microinjection of kainic acid into the AP. Kainic acid has been
successfully used to block the AP neurons in the cat
(Bonigut et al., 1997). With
this method, the AP lesion itself did not decrease basal drinking of SW eels.
As observed after heat-coagulative lesioning, the chemical lesioning
significantly attenuated ANP-induced inhibition of drinking in SW eels. Since
injection of kainic acid to other sites in the MO did not affect the ANP
effect, the AP neurons are most likely to be involved in ANP-induced
antidipsogenesis. Compared with heat-coagulative lesioning, however, the
inhibition of the ANP effect by kainic acid was partial in AP-lesioned eels.
This partial inhibition is most probably due to the partial destruction of the
AP, since Chicago Sky Blue 6B dye did not spread throughout the entire AP
(Fig. 3C). Although there are
technical limitations with the two methods employed in the present study,
these data evaluated by two distinct methods clearly showed that the AP is the
responsible locus for the antidipsogenic action of circulating ANP in
eels.
The mechanisms of ANG II-induced drinking in terrestrial species have been
well documented. In mammals and birds, the SFO and OVLT are forebrain CVOs
important for controlling drinking by systemic hormones
(Takei, 1992;
Fitzsimons, 1998). The SFO and
OVLT are the target sites for circulating ANG II
(Kobayashi and Takei, 1996;
Ferguson and Bains, 1996;
Fitzsimons, 1998), since local
injection of femtomolar doses of ANG II into these sites induces drinking, and
since local lesioning of these structures eliminates the dipsogenic effects of
systemic injection of ANG II (Simpson and
Routenberg, 1973; Takei,
1977; Ehrlich and Fitts,
1990; Schmid and Simon,
1992; Li and Ferguson,
1993). Further, the ANG II subtype 1 receptor (AT1) is localized
in the SFO (Song et al., 1992)
and ANG II enhances neuronal activities of SFO
(Gutman et al., 1988;
Hattori et al., 1988) in the
rat. Since autoradiographic study showed that ANP-binding neurons are located
in the SFO in the rat (Saavedra et al.,
1986), a similar cerebral mechanism may be applicable to the
antidipsogenic action of ANP in terrestrial vertebrates (Antunes-Rodorigues et
al., 1986), although the exact site of action of ANP has not been identified
in mammals. In fishes, on the other hand, the site of action of ANG II is
thought to be in the hindbrain, since `decerebration' of the entire forebrain
does not influence ANG II-induced drinking in eels
(Takei et al., 1979). ANP and
ANG II injection into the ventricle near the AP inhibited and stimulated
drinking, respectively, in a dose-related manner in eels
(Kozaka et al., 2003).
However, the exact target sites for circulating ANP and ANG II have not been
determined yet for fishes. Since the site of action of ANP in the brain has
also not been determined in mammals, the present study on eel is the first
report to show the cerebral target site for the antidipsogenic action of
circulating ANP in vertebrates, which is localized in the AP, a hindbrain
CVO.
Although the SFO and OVLT have not been identified in eels, the
magnocellular preoptic nuclei (PON) in the forebrain appears to be outside the
BBB as its neurons were stained by Trypan Blue in the present study and by
Evans Blue in a previous study (Mukuda et
al., 2005). However, the NPR-A antibody did not stain neurons in
the PON and thus this nucleus may not be a target site for circulating ANP. We
show in the present study that the GVC and RF, as well as AP, were stained by
Trypan Blue vital staining in the eel brain, although the intensity of
staining was weaker and the number of positive neurons was smaller in the RF
and GVC than those of the AP. It is possible that the RF and GVC neurons have
taken up the dye from the peripheral tissues. Indeed, when Evans Blue, a
retrograde tracer of neurons and structural isomer of Trypan Blue, is injected
into the esophageal muscles, some neurons in the GVC and spino-occipital motor
nucleus (NSO) within the RF are stained
(Mukuda and Ando, 2003b).
The functional role of the AP in drinking regulation in fishes remains
largely unknown at present. However, previous histological studies showed that
the sinus capillaries in the AP are fenestrated, and the dendrites of AP
neurons extend dorsally to reach the basal lamina of the capillaries in
goldfish (Morita and Finger,
1987), suggesting that teleost AP serves as an avenue for
endocrine signals such as ANP and ANG II to communicate with the CNS.
Furthermore, it has been shown that the GVC neurons project directly to the
striated muscles of the opercular membrane, pharynx, upper esophageal
sphincter and esophageal body, all of which are implicated in swallowing
(Mukuda and Ando, 2003b). It
was also shown that the AP neurons project ventrally to the GVC
(Ito et al., 2006). Although
further experiments are required to identify precise neuronal networks that
are involved in ANP-induced inhibition of drinking, it is possible that the AP
acts as a center for integrating the information of dipsogenic and
antidipsogenic hormones from the periphery and that it regulates the
coordinated behaviour of swallowing through the vagus nerves in eels.
List of abbreviations
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Antunes-Rodrigues, J., McCann, S. M. and Samson, W. K. (1986). Central administration of atrial natriuretic factor inhibits saline preference in the rat. Endocrinology 118,1726 -1728.[Abstract]
Balment, R. J. (2002). Control of water balance in mammals. In Osmoregulation and Drinking in Vertebrates (ed. N. Hazon and G. Flik), pp.153 -168. Oxford: BIOS Scientific Publisher.
Bonigut, S., Bonham, A. C. and Stebbins, C. L. (1997). Area postrema-induced inhibition of the exercise pressor reflex. Am. J. Physiol. 272,H1650 -H1655.[Medline]
Clasen, R. A., Pandolfi, S. and Hass, G. M. (1970). Vital staining, serum albumin and the blood-brain barrier. J. Neuropathol. Exp. Neurol. 29,266 -284.[Medline]
Ehrlich, K. J. and Fitts, D. A. (1990). Atrial natriuretic peptide in the subfornical organ reduces drinking induced by angiotensin or in response to water deprivation. Behav. Neurosci. 104,365 -372.[CrossRef][Medline]
Farrell, A. P. and Olson, K. R. (2000). Cardiac natriuretic peptides: a physiological lineage of cardioprotective hormones? Physiol. Biochem. Zool. 73, 1-11.[CrossRef][Medline]
Ferguson, A. V. and Bains, J. S. (1996). Electrophysiology of the circumventricular organs. Front. Neuroendocrinol. 17,440 -475.[CrossRef][Medline]
Fitzsimons, J. T. (1998). Angiotensin, thirst,
and sodium appetite. Physiol. Rev.
78,583
-686.
Fitzsimons, J. T. and Simons, B. J. (1968). The effect of angiotensin on drinking in the rat. J. Physiol. 196,39 -41.
Fregly, M. J. and Rowland, N. E. (1991). Bradykinin-induced dipsogenesis in captopril-treated rats. Brain Res. Bull. 26,169 -172.[CrossRef][Medline]
Gehlert, D. R., Gackenheimer, S. L., Reel, J. K., Lin, H. and Steinberg, M. I. (1990). Non-peptide angiotensin II receptor antagonists discriminate subtypes of 125I-angiotensin II binding sites in the rate brain. Eur. J. Pharmacol. 187,123 -126.[CrossRef][Medline]
Gutman, M. B., Ciriello, J. and Mogenson, G. J. (1988). Effects of plasma angiotensin II and hypernatremia on subfornical organ neurons. Am. J. Physiol. 254,R746 -R754.[Medline]
Hattori, Y., Kasai, M., Uesugi, S., Kawata, M. and Yamashita, H. (1988). Atrial natriuretic polypeptide depresses angiotensin II induced excitation of neurons in the rat subfornical organ in vitro. Brain Res. 443,355 -359.[CrossRef][Medline]
Healy, J. M., Donald, J. A., Hyodo, S., Toop, T. and Takei, Y. (2005). Natriuretic peptide guanylyl cyclase receptors in the kidney of the Japanese eel, Anguilla japonica. Cell Tissue Res. 320,311 -322.[CrossRef][Medline]
Hirano, T., Satou, M. and Utida, S. (1972). Central nervous system control of osmoregulation in the eel (Anguilla japonica). Comp. Biochem. Physiol. 43A,537 -544.
Ito, S., Mukuda, T. and Ando, M. (2006). Catecholamines inhibit neuronal activity in the glossopharyngeal-vagal motor complex of the Japanese eel: significance for controlling swallowing water. J. Exp. Zool. 305A,499 -506.
Johnson, A. K. and Gross, P. M. (1993). Sensory circumventricular organs and brain homeostatic pathways. FASEB J. 7,678 -686.[Abstract]
Katsuura, G., Nakamura, M., Inouye, K., Kono, M., Nakao, K. and Imura, H. (1986). Regulatory role of atrial natriuretic polypeptide in water drinking in rats. Eur. J. Pharmacol. 121,285 -287.[CrossRef][Medline]
Kobayashi, H. and Takei, Y. (1996). Sites of action of angiotensin in drinking. In The Renin-Angiotensin System – Comparative Aspects. Zoophysiology, Vol.35 , pp. 144-154. Berlin: Springer.
Kozaka, T., Fujii, Y. and Ando, M. (2003).
Central effects of various ligands on drinking behavior in eels acclimated to
seawater. J. Exp. Biol.
206,687
-692.
Li, Z. and Ferguson, A. V. (1993). Angiotensin II responsiveness of rat paraventricular and subfornical organ neurons in vitro. Neuroscience 55,197 -207.[CrossRef][Medline]
Lin, N. and Hubbard, J. I. (1992). ANP and naloxone reduce postdeprivation drinking after subfornical organ lesions. Brain Res. Bull. 28,769 -774.[CrossRef][Medline]
Loretz, C. A. and Pollina, C. (2000). Natriuretic peptides in fish physiology. Comp. Biochem. Physiol. 125A,169 -187.[CrossRef][Medline]
McKinley, M. J., Gerstberger, R., Mathai, M. L., Oldfield, B. J. and Schmid, H. (1999). The lamina terminalis and its role in fluid and electrolyte homeostasis. J. Clin. Neurosci. 6, 289-301.[CrossRef][Medline]
Morita, Y. and Finger, T. E. (1987). Area postrema of the goldfish, Carassius auratus: ultrastructure, fiber connections, and immunocytochemistry. J. Comp. Neurol. 256,104 -116.[CrossRef][Medline]
Mukuda, T. and Ando, M. (2003a). Brain atlas of the Japanese eel: comparison to other fishes. Mem. Fac. Integrated Arts Sci. Hiroshima Univ. Ser. IV 29, 1-25.
Mukuda, T. and Ando, M. (2003b). Medullary motor neurons associated with drinking behaviour of Japanese eel. J. Fish Biol. 62,1 -12.[CrossRef]
Mukuda, T., Matsunaga, Y., Kawamoto, K., Yamaguchi, K. and Ando, M. (2005). `Blood-contacting neurons' in the brain of the Japanese eel Anguilla japonica. J. Exp. Zool. 303,366 -376.
Quirion, R. (1989). Receptor sites for atrial natriuretic factors in brain and associated structures: an overview. Cell. Mol. Neurobiol. 9,45 -55.[CrossRef][Medline]
Saavedra, J. M., Correa, F. M. A., Plunkett, L. M., Israel, A., Kurihama, M. and Shigematsu, K. (1986). Binding of angiotensin and atrial natriuretic peptide in brain of hypertensive rats. Nature 320,758 -760.[CrossRef][Medline]
Schmid, H. A. and Simon, E. (1992). Effect of angiotensin II and atrial natriuretic factor on neurons in the subfornical organ of duck and rats in vitro. Brain Res. 588,324 -328.[CrossRef][Medline]
Simon, E., Gerstburger, R. and Gray, D. A. (1992). Central nervous angiotensin II responsiveness in birds. Progr. Neurobiol. 39,179 -207.[CrossRef][Medline]
Simpson, J. B. and Routenberg, A. (1973).
Subfornical organ: site of drinking elicitation by angiotensin II.
Science 181,1172
-1174.
Sinnayah, P., Burns, P., Wada, J. D., Weisinger, R. S. and
McKinley, M. J. (1999). Water drinking in rats resulting from
intravenous relaxin and its modification by other dipsogenic factors.
Endocrinology 140,5082
-5086.
Song, K., Allen, A. M., Paxinos, G. and Mendelsohn, F. A. (1992). Mapping of angiotensin II receptor subtype heterogeneity in rat brain. J. Comp. Neurol. 316,467 -484.[CrossRef][Medline]
Takei, Y. (1977). The role of the subfornical organ in drinking induced by angiotensin in the Japanese quail, Coturnix coturnix japonica. Cell Tissue Res. 185,175 -181.[Medline]
Takei, Y. (1992). Vasoactive hormones and body fluid homeostasis: a phylogenetic consideration. In Phylogenetic Models in Functional Coupling of the CNS and the Cardiovascular System (Molecular Comparative Physiology). Vol.11 (ed. K. Kuwasawa, R. B. Hill, R. B. McMahon and T. Kuramoto), pp. 239-249. Basel: Karger.
Takei, Y. (2002). Hormonal control of drinking in eels: an evolutionary approach. In Osmoregulation and Drinking in Vertebrates (ed. N. Hazon and G. Flik), pp.61 -82. Oxford: BIOS Scientific.
Takei, Y. and Hirose, S. (2002). The natriuretic peptide system in eels: a key endocrine system for euryhalinity? Am. J. Physiol. 282,R940 -R951.
Takei, Y. and Tsukada, T. (2001). Ambient temperature regulates drinking and arterial pressure in eels. Zool. Sci. 18,963 -967.[CrossRef]
Takei, Y., Hirano, T. and Kobayashi, H. (1979). Angiotensin and water intake in the Japanese eel, Anguilla japonica.Gen. Comp. Endocrinol. 38,466 -475.[CrossRef][Medline]
Takei, Y., Tsuchida, T. and Tanakadate, A. (1998). Evaluation of water intake in seawater adaptation in eels using synchronized drop counter and pulse injector system. Zool. Sci. 15,677 -682.[CrossRef]
Tomioka, M., Shirotani, K., Iwata, N., Lee, H. J., Yang, F., Cole, G. M., Seyama, Y. and Saido, T. C. (2002). In vivo role of caspases in excitotoxic neuronal death: generation and analysis of transgenic mice expressing baculoviral caspase inhibitor, p35, in postnatal neurons. Mol. Brain Res. 108, 18-32.[Medline]
Toop, T. and Donald, J. A. (2004). Comparative aspects of natriuretic peptide physiology in non-mammalian vertebrates: a review. J. Comp. Physiol. B 174,189 -204.[CrossRef][Medline]
Tsuchida, T. and Takei, Y. (1998). Effects of homologous atrial natriuretic peptide on drinking and plasma ANG II level in eels. Am. J. Physiol. 275,R1605 -R1610.[Medline]
Tsukada, T. and Takei, Y. (2006). Integrative approach to osmoregulatory action of atrial natriuretic peptide in seawater eels. Gene. Comp. Endocrinol. 147, 31-38.[CrossRef]
Tsukada, T., Rankin, J. C. and Takei, Y. (2005). Involvement of drinking and intestinal sodium absorption in hyponatremic effect of atrial natriuretic peptide in seawater eels. Zool. Sci. 22,77 -85.[CrossRef][Medline]
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
