Guanylyl cyclases are usually characterized as being either soluble (sGCs) or receptor (rGCs). We have recently cloned a novel guanylyl cyclase, MsGC-I, from the developing nervous system of the hawkmoth Manduca sexta that cannot be classified as either an sGC or an rGC. MsGC-I shows highest sequence identity with receptor guanylyl cyclases throughout its catalytic and dimerization domains, but does not contain the ligand-binding, transmembrane or kinase-like domains characteristic of receptor guanylyl cyclases. In addition, MsGC-I contains a C-terminal extension of 149 amino acid residues. In this paper, we report the expression of MsGC-I in the adult. Northern blots show that it is expressed preferentially in the nervous system, with high levels in the pharate adult brain and antennae. In the antennae, immunohistochemical analyses show that it is expressed in the cell bodies and dendrites, but not axons, of olfactory receptor neurons. In the brain, it is expressed in a variety of sensory neuropils including the antennal and optic lobes. It is also expressed in structures involved in higher-order processing including the mushroom bodies and central complex. This complicated expression pattern suggests that this novel guanylyl cyclase plays an important role in mediating cyclic GMP levels in the nervous system of Manduca sexta.
REFERENCES
Chinkers
M.
, Wilson
E. M.
(1992
). Ligand-independent oligomerization of natriuretic peptide receptors. Identification of heteromeric receptors and a dominant negative mutant.
J. Biol. Chem
267
, 18589
–.Davis
N. T.
, Veenstra
J. A.
, Feyereisen
R.
, Hildebrand
J. G.
(1997
). Allatostatin-like-immunoreactive neurons of the tobacco hornworm, Manduca sexta and isolation and identification of a new neuropeptide related to cockroach allatostatins.
J. Comp. Neurol
385
, 265
–.Davis
R. L.
(1993
). Mushroom bodies and Drosophila learning.
Neuron
11
, 1
–.Denninger
J. W.
, Marletta
M. A.
(1999
). Guanylate cyclase and the NO/cGMP signaling pathway.
Biochim. Biophys. Acta
1411
, 334
–.Ewer
J.
, Truman
J. W.
(1996
). Increases in cyclic 3,5 -guanosine monophosphate (cGMP) occur at ecdysis in an evolutionarily conserved crustacean cardioactive peptide-immunoreactive insect neuronal network.
J. Comp. Neurol
370
, 330
–.Foster
D. C.
, Wedel
B. J.
, Robinson
S. W.
, Garbers
D. L.
(1999
). Mechanisms of regulation and functions of guanylyl cyclases.
Rev. Physiol. Biochem. Pharmac
135
, 1
–.Gelperin
A.
(1999
). Oscillatory dynamics and information processing in olfactory systems.
J. Exp. Biol
202
, 1855
–.Gronenberg
W.
(1999
). Modality-specific segregation of input to ant mushroom bodies.
Brain Behav. Evol
54
, 85
–.Han
P. L.
, Levin
L. R.
, Reed
R. R.
, Davis
R. L.
(1992
). Preferential expression of the Drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects.
Neuron
9
, 619
–.Heinbockel
T.
, Christensen
T. A.
, Hildebrand
J. G.
(1999
). Temporal tuning of odor responses in pheromone-responsive projection neurons in the brain of the sphinx moth Manduca sexta.
J. Comp. Neurol
409
, 1
–.Hildebrand
J. G.
, Shepherd
G. M.
(1997
). Mechanisms of olfactory discrimination: converging evidence for common principles across phyla.
Annu. Rev. Neurosci
20
, 595
–.Homberg
U.
, Vitzthum
H.
, Muller
M.
, Binkle
U.
(1999
). Immunocytochemistry of GABA in the central complex of the locust Schistocerca gregaria: identification of immunoreactive neurons and colocalization with neuropeptides.
J. Comp. Neurol
409
, 495
–.Ilius
M.
, Wolf
R.
, Heisenberg
M.
(1994
). The central complex of Drosophila melanogaster is involved in flight control: studies on mutants and mosaics of the gene ellipsoid body open.
J. Neurogenet
9
, 189
–.Lowe
D. G.
(1992
). Human natriuretic peptide receptor-A guanylyl cyclase is self-associated prior to hormone binding.
Biochemistry
31
, 10421
–.McBride
S. M.
, Giuliani
G.
, Choi
C.
, Krause
P.
, Correale
D.
, Watson
K.
, Baker
G.
, Siwicki
K. K.
(1999
). Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in Drosophila melanogaster.
Neuron
24
, 967
–.Mizunami
M.
, Weibrecht
J. M.
, Strausfeld
N. J.
(1998
). Mushroom bodies of the cockroach: their participation in place memory.
J. Comp. Neurol
402
, 520
–.Muller
U.
, Hildebrandt
H.
(1995
). The nitric oxide/cGMP system in the antennal lobe of Apis mellifera is implicated in integrative processing of chemosensory stimuli.
Eur. J. Neurosci
7
, 2240
–.Nighorn
A.
, Gibson
N. J.
, Morton
D. B.
, Hildebrand
J. G.
(1998
). The NO/cGMP pathway may mediate communication between sensory afferents and projection neurons in the antennal lobe of Manduca sexta.
J. Neurosci
8
, 7244
–.Nighorn
A.
, Healy
M. J.
, Davis
R. L.
(1991
). The cyclic AMP phosphodiesterase encoded by the Drosophila dunce gene is concentrated in the mushroom body neuropil.
Neuron
6
, 455
–.O'Shea
M.
, Colbert
R.
, Williams
L.
, Dunn
S.
(1998
). Nitric oxide compartments in the mushroom bodies of the locust brain.
Neuroreport
9
, 333
–.Olshevskaya
E. V.
, Ermilov
A. N.
, Dizhoor
A. M.
(1999
). Dimerization of guanylyl cyclase-activating protein and a mechanism of photoreceptor guanylyl cyclase activation.
J. Biol. Chem
274
, 25583
–.Simpson
P. J.
, Nighorn
A.
, Morton
D. B.
(1999
). Identification of a novel guanylyl cyclase that is related to receptor guanylyl cyclases, but lacks extracellular and transmembrane domains.
J. Biol. Chem
274
, 4440
–.Skoulakis
E. M.
, Kalderon
D.
, Davis
R. L.
(1993
). Preferential expression in mushroom bodies of the catalytic subunit of protein kinase A and its role in learning and memory.
Neuron
11
, 197
–.Stengl
M.
, Zufall
F.
, Hatt
H.
, Hildebrand
J. G.
(1992
). Olfactory receptor neurons from antennae of developing male Manduca sexta respond to components of the species-specific sex pheromone in vitro.
J. Neurosci
12
, 2523
–.Stopfer
M.
, Laurent
G.
(1999
). Short-term memory in olfactory network dynamics.
Nature
402
, 664
–.Strausfeld
N. J.
, Li
Y.
(1999
). Organization of olfactory and multimodal afferent neurons supplying the calyx and pedunculus of the cockroach mushroom bodies.
J. Comp. Neurol
409
, 603
–.Sun
X. J.
, Tolbert
L. P.
, Hildebrand
J. G.
(1997
). Synaptic organization of the uniglomerular projection neurons of the314antennal lobe of the moth Manduca sexta: a laser scanning confocal and electron microscopic study.
J. Comp. Neurol
379
, 2
–.Tolbert
L. P.
, Matsumoto
S. G.
, Hildebrand
J. G.
(1983
). Development of synapses in the antennal lobes of the moth Manduca sexta during metamorphosis.
J. Neurosci
3
, 1158
–.Wilson
E. M.
, Chinkers
M.
(1995
). Identification of sequences mediating guanylyl cyclase dimerization.
Biochemistry
34
, 4696
–.Zhao
Y.
, Marletta
M. A.
(1997
). Localization of the heme binding region in soluble guanylate cyclase.
Biochemistry
36
, 15959
–.Zufall
F.
, Leinders-Zufall
T.
(1997
). Identification of a long-lasting form of odor adaptation that depends on the carbon monoxide/cGMP second-messenger system.
J. Neurosci
17
, 2703
–.
This content is only available via PDF.
© 2001 by Company of Biologists
2001
