The Nitric Oxide–cGMP Pathway May Mediate Communication between Sensory Afferents and Projection Neurons in the Antennal Lobe ofManduca Sexta

The nitric oxide (NO)–cGMP signaling system is thought to play important roles in the function of the olfactory system in both vertebrates and invertebrates. One way of studying the role of NO in the nervous system is to study the distribution and properties of NO synthase (NOS), as well as the soluble guanylyl cyclases (sGCs), which are the best characterized targets of NO. We study NOS and sGC in the relatively simple and well characterized insect olfactory system of the hawkmoth, Manduca sexta. We have cloned Manduca sexta nitric oxide synthase (MsNOS) and two sGCs (MsGCα1 and MsGCβ1), characterized their basic biochemical properties, and studied their expression in the olfactory system. The sequences of theManduca genes are highly similar to their mammalian homologs and show similar biochemical properties when expressed in COS-7 cells. In particular, we find that MsGC functions as an obligate heterodimer that is stimulated significantly by NO. We also find that MsNOS has a Ca2+-sensitive NO-producing activity similar to that of mammalian neuronal NOS. Northern andin situ hybridization analyses show that MsNOS and the MsGCs are expressed in a complementary pattern, with MsNOS expressed at high levels in the antennae and the MsGCs expressed at high levels in a subset of antennal lobe neurons. The expression patterns of these genes suggest that the NO–sGC signaling system may play a role in mediating communication between olfactory receptor neurons and projection neurons in the glomeruli of the antennal lobe.

[1]  D. Wilkinson.  In situ hybridization: a practical approach , 1998 .

[2]  K. Kendrick,et al.  Formation of olfactory memories mediated by nitric oxide , 1997, Nature.

[3]  B. Hovemann,et al.  Drosophila melanogaster NADPH-cytochrome P450 oxidoreductase: pronounced expression in antennae may be related to odorant clearance. , 1997, Gene.

[4]  G. Schultz,et al.  Functions of conserved cysteines of soluble guanylyl cyclase. , 1997, Biochemistry.

[5]  M. Hirai,et al.  cDNA cloning, expression and characterization of nitric-oxide synthase from the salivary glands of the blood-sucking insect Rhodnius prolixus. , 1996, European journal of biochemistry.

[6]  J. Vente,et al.  The Nitric Oxide/Cyclic GMP Messenger System in Olfactory Pathways of the Locust Brain , 1996, The European journal of neuroscience.

[7]  H. Steinbusch,et al.  Nitric oxide synthase, cGMP, and NO‐mediated cGMP production in the olfactory bulb of the rat , 1996, The Journal of comparative neurology.

[8]  S. Snyder,et al.  PIN: An Associated Protein Inhibitor of Neuronal Nitric Oxide Synthase , 1996, Science.

[9]  Stengl,et al.  NADPH diaphorase activity in the antennae of the hawkmoth Manduca sexta , 1996, The Journal of experimental biology.

[10]  P. Pelosi,et al.  Perireceptor events in olfaction. , 1996, Journal of neurobiology.

[11]  D. Bredt,et al.  Interaction of Nitric Oxide Synthase with the Postsynaptic Density Protein PSD-95 and α1-Syntrophin Mediated by PDZ Domains , 1996, Cell.

[12]  D. Morton.  Neuropeptide-stimulated cyclic guanosine monophosphate immunoreactivity in the neurosecretory terminals of a neurohemal organ. , 1996, Journal of neurobiology.

[13]  H. Kaba,et al.  Formation of an olfactory recognition memory in mice: Reassessment of the role of nitric oxide , 1996, Neuroscience.

[14]  U. Müller,et al.  Inhibition of Nitric Oxide Synthase Impairs a Distinct Form of Long-Term Memory in the Honeybee, Apis mellifera , 1996, Neuron.

[15]  M. Marletta,et al.  Heme stoichiometry of heterodimeric soluble guanylate cyclase. , 1995, Biochemistry.

[16]  U. Müller,et al.  The Nitric Oxide/cGMP System in the Antennal Lobe of Apis mellifera is Implicated in Integrative Processing of Chemosensory Stimuli , 1995, The European journal of neuroscience.

[17]  G. Schultz,et al.  Functional Domains of Soluble Guanylyl Cyclase (*) , 1995, The Journal of Biological Chemistry.

[18]  T. Tully,et al.  Molecular and biochemical characterization of dNOS: a Drosophila Ca2+/calmodulin-dependent nitric oxide synthase. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[19]  D. Hyde,et al.  Two Drosophila Genes That Encode the α and β Subunits of the Brain Soluble Guanylyl Cyclase (*) , 1995, The Journal of Biological Chemistry.

[20]  R. Pilz,et al.  Basis of guanylate cyclase activation by carbon monoxide. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[21]  M. Elphick,et al.  Nitric oxide synthesis in locust olfactory interneurones , 1995, The Journal of experimental biology.

[22]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[23]  M. Marletta,et al.  Soluble guanylate cyclase from bovine lung: activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states. , 1994, Biochemistry.

[24]  G. Schultz,et al.  Mutation of His-105 in the beta 1 subunit yields a nitric oxide-insensitive form of soluble guanylyl cyclase. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[25]  F. Murad,et al.  Cloning of Guonylyl Cyclase Isoforms , 1994 .

[26]  F. Murad,et al.  Cloning of guanylyl cyclase isoforms. , 1994, Advances in pharmacology.

[27]  D. Madison,et al.  Nitric oxide and synaptic function. , 1994, Annual review of neuroscience.

[28]  P. Emson,et al.  Localization of Nitric Oxide Synthase in the Mouse Olfactory and Vomeronasal System: a Histochemical, Immunological and In Situ Hybridization Study , 1993, The European journal of neuroscience.

[29]  Gordon M. Shepherd,et al.  Implications of the NO/cGMP system for olfaction , 1993, Trends in Neurosciences.

[30]  D. Garbers.  Guanylyl cyclase receptors and their endocrine, paracrine, and autocrine ligands , 1992, Cell.

[31]  L. Gooding.  Virus proteins that counteract host immune defenses , 1992, Cell.

[32]  D. Morton,et al.  Eclosion Hormone Stimulates Cyclic GMP Levels in Manduca sexta Nervous Tissue via Arachidonic Acid Metabolism with Little or No Contribution from the Production of Nitric Oxide , 1992, Journal of neurochemistry.

[33]  F. Murad,et al.  Mapping of neural nitric oxide synthase in the rat suggests frequent co-localization with NADPH diaphorase but not with soluble guanylyl cyclase, and novel paraneural functions for nitrinergic signal transduction. , 1992, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[34]  E. Kandel,et al.  Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Michael Chinkers,et al.  Signal transduction by guanylyl cyclases. , 1991, Annual review of biochemistry.

[36]  F. Murad,et al.  Molecular cloning and expression of cDNAs coding for soluble guanylate cyclase from rat lung. , 1990, The Journal of biological chemistry.

[37]  J. Hildebrand,et al.  Development of synapses in the antennal lobes of the moth Manduca sexta during metamorphosis , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  J. Truman,et al.  Physiology of Pupal Ecdysis in the Tobacco Hornworm, Manduca Sexta: I. Evidence for Control by Eclosion Hormone , 1980 .

[39]  J. Sanes,et al.  Biochemical and developmental studies of acetylcholine metabolism in the central nervous system of the moth Manduca sexta. , 1977, Comparative biochemistry and physiology. C: Comparative pharmacology.

[40]  J. Sanes,et al.  Structure and development of antennae in a moth, Manduca sexta. , 1976, Developmental biology.