Natriuretic peptide binding sites were examined in the gills of the hagfish Eptatretus cirrhatus (Class Agnatha, subfamily Eptatretinae) using radio-ligand binding techniques, molecular cloning and guanylyl cyclase assays. Iodinated rat atrial natriuretic peptide ((125)I-rANP) and iodinated porcine C-type natriuretic peptide ((125)I-pCNP) bound specifically to the lamellar folds and cavernous tissue of E. cirrhatus gills, and 0.3 nmol l(−1) rat ANP competed for 50 % of specific (125)I-rANP binding sites. Affinity cross-linking of (125)I-rANP to gill membranes followed by sodium dodecylsulphate-polyacrylamide gel electrophoresis revealed a single binding site of 150 kDa. In the presence of Mn(2+), 0.1 nmol l(−1) rANP inhibited cGMP production, whereas 1 micromol l(−1) rANP stimulated cGMP production rates. At 1 micromol l(−1), pCNP also stimulated cGMP production. The production of cGMP was also measured in the presence and absence of ATP with either Mn(2+) or Mg(2+). Reverse transcriptase polymerase chain reaction (RT-PCR) of hagfish gill RNA, followed by cloning and sequencing of PCR products, produced a partial cDNA sequence of a natriuretic peptide guanylyl cyclase receptor. The deduced amino acid sequence indicated 87–91 % homology with other natriuretic peptide guanylyl cyclase receptors. This study indicates the presence of a natriuretic peptide guanylyl cyclase receptor in the gills of E. cirrhatus that is similar to the natriuretic peptide guanylyl cyclase receptors in higher vertebrates. These observations demonstrate that the coupling of natriuretic peptide receptors with guanylyl cyclase has a long evolutionary history.

REFERENCES

Anand-Srivastava
M. B.
,
Sairam
M. R.
,
Cantin
M.
(
1990
).
Ring-deleted analogs of atrial natriuretic factor inhibit adenylate cyclase/cyclic AMP system
.
J. Biol. Chem
265
,
8566
–.
Anand-Srivastava
M. B.
,
Trachte
G. J.
(
1993
).
Atrial natriuretic factor receptors and signal transduction mechanisms
.
Pharmac. Rev
45
,
455
–.
Awazu
M.
,
Ichikawa
I.
(
1993
).
Biological significance of atrial natriuretic peptide in the kidney
.
Nephron
63
,
1
–.
Barr
C. S.
,
Rhodes
P.
,
Struthers
A. D.
(
1996
).
C-type natriuretic peptide
.
Peptides
17
,
1243
–.
Brenner
B. M.
,
Ballerman
B. J.
,
Gunning
M. E.
,
Zeidel
M. L.
(
1990
).
Diverse biological actions of atrial natriuretic peptide
.
Physiol. Rev
70
,
665
–.
Cerra
M. C.
,
Canonaco
M.
,
Tota
B.
(
1992
).
A quantitative autoradiographical study of 125I atrial natriuretic factor in the heart of a teleost fish (Conger conger)
.
J. Exp. Zool
263
,
215
–.
Chomczynski
P.
,
Sacchi
N.
(
1987
).
Single-step method of RNA isolation by acid guanidinium thiocyanate—phenol—chloroform extraction
.
Analyt. Biochem
162
,
156
–.
Donald
J. A.
,
Toop
T.
,
Evans
D. H.
(
1994
).
Localization and analysis of natriuretic peptide receptors in the gills of the toadfish Opsanus beta (Teleostei)
.
Am. J. Physiol
267
,
1437
–.
Donald
J. A.
,
Vomachka
A. J.
,
Evans
D. H.
(
1992
).
Immunohistochemical localisation of natriuretic peptides in the brains and hearts of the spiny dogfish Squalus acanthias and the Atlantic hagfish Myxine glutinosa
.
Cell. Tissue Res
270
,
535
–.
Duda
T.
,
Goraczniak
R.
,
Sharma
R. K.
(
1996
).
Distinct inhibitory ATP-regulated modulatory domain (ARM24i) in membrane guanylate cyclases
.
Biochem. J
319
,
279
–.
Duff
D. W.
,
Olson
K. R.
(
1992
).
Atrial natriuretic peptide clearance receptors in trout; effects of receptor inhibition in vivo
.
J. Exp. Zool
262
,
343
–.
Elger
M.
(
1987
).
The branchial circulation and the gill epithelia in the Atlantic hagfish, Myxine glutinosa L
.
Anat. Embryol
175
,
489
–.
Evans
D. H.
(
1990
).
An emerging role for cardiac peptide hormone in fish osmoregulation
.
Annu. Rev. Physiol
52
,
43
–.
Evans
D. H.
(
1991
).
Rat atriopeptin dilates vascular smooth muscle of the ventral aorta from the shark (Squalus acanthias) and the hagfish (Myxine glutinosa)
.
J. Exp. Biol
157
,
551
–.
Evans
D. H.
,
Chipouras
E.
,
Payne
J. A.
(
1989
).
Immunoreactive atriopeptin in plasma of fishes: its potential role in gill hemodynamics
.
Am. J. Physiol
257
,
939
–.
Forey
P.
,
Janvier
P.
(
1993
).
Agnathans and the origins of jawed vertebrates
.
Nature
361
,
129
–.
Hagiwara
H.
,
Hirose
S.
,
Takei
Y.
(
1995
).
Natriuretic peptides and their receptors
.
Zool. Sci
12
,
141
–.
Inagami
T.
(
1989
).
Atrial natriuretic factor
.
J. Biol. Chem
264
,
3043
–.
Kashiwagi
M.
,
Katafuchi
T.
,
Kato
A.
,
Inuyama
H.
,
Ito
T.
,
Hagiwara
H.
,
Takei
Y.
,
Hirose
S.
(
1995
).
Cloning and properties of a novel natriuretic peptide receptor, NPR-D
.
Eur. J. Biochem
233
,
102
–.
Kashiwagi
M.
,
Miyamoto
K.
,
Takei
Y.
,
Hirose
S.
(
1999
).
Cloning, properties and tissue distribution of natriuretic peptide receptor-A of euryhaline eel, Anguilla japonica
.
Eur. J. Biochem
259
,
204
–.
Katafuchi
T.
,
Takashima
A.
,
Kashiwagi
M.
,
Hagiwara
H.
,
Takei
Y.
,
Hirose
S.
(
1994
).
Cloning and expression of eel natriuretic peptide B and comparison with its mammalian counterparts
.
Eur. J. Biochem
222
,
835
–.
Levin
E. R.
(
1993
).
Natriuretic peptide C-receptor: more than a clearance receptor
.
Am. J. Physiol
264
,
483
–.
Maack
T.
(
1992
).
Receptors of atrial natriuretic factor
.
Annu. Rev. Physiol
54
,
11
–.
Maack
T.
,
Suzuki
M.
,
Almeida
F. A.
,
Nussenzveig
D.
,
Scarborough
R. M.
,
McEnroe
G. A.
,
Lewicki
J. A.
(
1987
).
Physiological role of silent receptors of atrial natriuretic factor
.
Science
238
,
675
–.
Mishina
S.
,
Takei
Y.
(
1997
).
Characterisation of natriuretic peptide receptors in eel gill
.
J. Endocr
154
,
415
–.
Morel
G.
,
Chabot
J. G.
,
Garcia-Cabellero
T.
,
Gossard
F.
,
Oihl
F.
,
Belles-Isles
M.
,
Heisler
S.
(
1988
).
Synthesis, internalization and localization of atrial natriuretic peptide in rat adrenal medulla
.
Endocrinol
123
,
149
–.
Morel
G.
,
Mesguich
P.
,
Chabot
J. G.
,
Belles-Isles
M.
,
Jeandel
L.
,
Heisler
S.
(
1989
).
Internalization of atrial natriuretic peptide by adrenal glomerulosa cells
.
Biol. Cell
65
,
181
–.
Nicholls
M. G.
(
1994
).
Minisymposium: the natriuretic peptide hormones. Editorial and historical review
.
J. Int. Med
235
,
507
–.
Olson
K. R.
,
Conklin
D. J.
,
Farrell
A. P.
,
Keen
J. E.
,
Takei
Y.
,
Weaver
L. J.
,
Smith
M. P.
,
Zhang
Y.
(
1997
).
Effects of natriuretic peptides and nitroprusside on venous function in trout
.
Am. J. Physiol
273
,
527
–.
Olson
K. R.
,
Duff
D. W.
(
1993
).
Single-pass gill extraction and tissue distribution of atrial natriuretic peptide in trout
.
Am. J. Physiol
265
,
124
–.
Rambotti
M. G.
,
Ercolani
P.
,
Spreca
A.
(
1993
).
Ultracytochemical localization of particulate guanylate cyclase in rat adrenal gland exposed to stimulation by porcine brain natriuretic peptide
.
Histochem. J
25
,
384
–.
Rambotti
M. G.
,
Giambanco
I.
,
Spreca
A.
(
1997
).
Detectionof guanylate cyclases A and B stimulated by natriuretic peptides in gastrointestinal tract of rat
.
Histochem. J
29
,
117
–.
Rambotti
M. G.
,
Mughetti
D.
,
Spreca
A.
(
1994
).
Detection of particulate guanylate cyclase in rat neurohypophysis after stimulation with ANF and BNP — an ultracytochemical study
.
Brain Res
644
,
52
–.
Redondo
J.
,
Bishop
J. E.
,
Wilkins
M. R.
(
1998
).
Effect of atrial natriuretic peptide and cyclic GMP phosphodiesterase inhibition on collagen synthesis by adult cardiac fibroblasts
.
Brit. J. Pharmac
124
,
1455
–.
Reinecke
M.
,
Betzler
D.
,
Forssmann
W. G.
(
1987
).
Immunocytochemistry of cardiac polypeptide hormones (Cardiodilatin/atrial natriuretic polypeptide) in brain and hearts of Myxine glutinosa (Cyclostomata)
.
Histochem
86
,
233
–.
Reinecke
M.
,
Nehls
M.
,
Forssmann
W. G.
(
1985
).
Phylogenetic aspects of cardiac hormones as revealed by immunocytochemistry, electronmicroscopy and bioassay
.
Peptides
6
,
3
–.
Rosenzweig
A.
,
Seidman
C. E.
(
1991
).
Atrial natriuretic factor and related peptide hormones
.
Annu. Rev. Biochem
60
,
229
–.
Sakaguchi
H.
,
Katafuchi
T.
,
Hagiwara
H.
,
Takei
Y.
,
Hirose
S.
(
1993
).
High-density localization of ANP receptors in chondrocytes of eel gill cartilage
.
Am. J. Physiol
265
,
474
–.
Stenslokken
K. O.
,
Sundin
L.
,
Nilsson
G. E.
(
1999
).
Cardiovascular and gill microcirculatory effects of endothelin-1 in Atlantic cod: evidence for pillar cell contraction
.
J. Exp. Biol
202
,
1151
–.
Takashima
A.
,
Katafuchi
T.
,
Shibasaki
M.
,
Kashiwagi
M.
,
Hagiwara
H.
,
Takei
Y.
,
Hirose
S.
(
1995
).
Cloning, properties, site-directed mutagenesis analysis of the subunit structure, tissue distribution and regulation of expression of the type-C eel natriuretic peptide receptor
.
Eur. J. Biochem
227
,
673
–.
Tei
S.
,
Santarella
B.
,
Farnesi
R. M.
,
Vagnetti
D.
(
2000
).
Ultrastructural analysis and cytochemical localization of atrial natriuretic peptide-stimulated guanylate cyclase in internal gills of Bufo bufo tadpoles
.
Eur. J. Morph
38
,
41
–.
Toop
T.
,
Donald
J. A.
,
Evans
D. H.
(
1995
).
Localisation and characterisation of natriuretic peptide receptors in the gills of the Atlantic hagfish Myxine glutinosa (Agnatha)
.
J. Exp. Biol
198
,
117
–.
Toop
T.
,
Donald
J. A.
,
Evans
D. H.
(
1995
).
Natriuretic peptide receptors in the kidney and the ventral and dorsal aortae of the Atlantic hagfish Myxine glutinosa (Agnatha)
.
J. Exp. Biol
198
,
1875
–.
Woods
R. L.
(
1998
).
Vasoconstrictor actions of atrial natriuretic peptide in the splanchnic circulation of anaesthetised dogs
.
Am. J. Physiol
275
,
1822
–.
Woods
R. L.
(
1999
).
Atrial, B-type and C-type natriuretic peptides cause mesenteric vasoconstriction in conscious dogs
.
Am. J. Physiol
276
,
1443
–.
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