The Nitric Oxide–cGMP Pathway May Mediate Communication between Sensory Afferents and Projection Neurons in the Antennal Lobe of<i>Manduca Sexta</i>

Nighorn, Alan; Gibson, Nicholas J.; Rivers, David M.; Hildebrand, John G.; Morton, David B.

doi:10.1523/jneurosci.18-18-07244.1998

Cited by 115 publications

(132 citation statements)

References 44 publications

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“…Two of these have been described previously (19), appear to be the Manduca homologues of the mammalian soluble guanylyl cyclase subunits, ␣1 and ␤1, and have been named MsGC-␣1 and MsGC-␤1, respectively. In the course of this earlier study, we isolated an additional cDNA fragment that also had high sequence similarity to mammalian ␤ subunits.…”

Section: Resultsmentioning

confidence: 99%

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Identification and Characterization of a Novel β Subunit of Soluble Guanylyl Cyclase That Is Active in the Absence of a Second Subunit and Is Relatively Insensitive to Nitric Oxide

Nighorn

Byrnes

Morton

1999

Journal of Biological Chemistry

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Previously characterized soluble guanylyl cyclases form ␣-␤ heterodimers that can be activated by the gaseous messenger, nitric oxide. In mammals, four subunits have been cloned, named ␣1, ␣2, ␤1, and ␤2. We have identified a novel soluble guanylyl cyclase isoform from the nervous system of the insect Manduca sexta that we have named M. sexta guanylyl cyclase ␤3 (MsGC-␤3). It is most closely related to the mammalian ␤ subunits but has several features that distinguish it from previously identified soluble cyclases. Most importantly, MsGC-␤3 does not need to form heterodimers to form an active enzyme because guanylyl cyclase activity can be measured when it is expressed alone in COS-7 cells. Moreover, this activity is only weakly enhanced in the presence of the nitric oxide donor, sodium nitroprusside. Several of the amino acids in rat ␤1 subunits, previously identified as being important in heme binding or necessary for nitric oxide activation, are substituted with nonsimilar amino acids in MsGC-␤3. There are also an additional 315 amino acids C-terminal to the catalytic domain of MsGC-␤3 that have no sequence similarity to any known protein. Northern blot analysis shows that MsGC-␤3 is primarily expressed in the nervous system of Manduca.The intracellular messenger cGMP mediates a wide variety of cellular and physiological processes. It functions as the primary messenger in visual transduction (1, 2), is an important regulator in vascular smooth muscle and kidney function (3, 4), and has been implicated in a number of forms of neuronal plasticity (5-7).The enzymes that regulate the synthesis of cGMP fall into two major classes: the cytoplasmically localized, soluble guanylyl cyclases and the membrane associated, receptor guanylyl cyclases (4). Soluble guanylyl cyclases are obligate heterodimers composed of an ␣ and a ␤ subunit. Two ␣ (␣1 and ␣2) and two ␤ (␤1 and ␤2) subunits have been cloned from mammalian tissues (8 -13). The active heterodimer requires and binds heme as a prosthetic group and can be potently activated by the gaseous messenger, nitric oxide (NO) 1 (14). The soluble cyclases are found in the cytosol of cells, although the mammalian ␤2 subunit has a consensus isoprenylation site, suggesting that it might be associated with membranes. The receptor guanylyl cyclases, by contrast, are integral membrane proteins with transmembrane and extracellular domains (4).We have been using the insect Manduca sexta as a model system to study cGMP regulation and have previously shown that a neuropeptide, eclosion hormone, is a potent stimulator of cGMP levels in the central nervous system (15). Biochemical characterization of the eclosion hormone-stimulated cGMP increase suggested that eclosion hormone might activate a NOinsensitive, soluble guanylyl cyclase (15-18). In an attempt to identify the pathway for eclosion hormone-stimulated cGMP levels, we used reverse transcription-polymerase chain reaction (RT-PCR) to identify guanylyl cyclases from Manduca nervous tissue. This approach has yielded a number of dif...

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Section: Resultsmentioning

confidence: 99%

“…This approach has yielded a number of different guanylyl cyclases. We have previously described the cloning and expression characteristics of the Manduca homologues of the ␣1 and ␤1 subunits, named MsGC-␣1 and MsGC-␤1 (19). Here we describe the cloning and preliminary characterization of a novel ␤ subunit, MsGC-␤3.…”

mentioning

confidence: 98%

Identification and Characterization of a Novel β Subunit of Soluble Guanylyl Cyclase That Is Active in the Absence of a Second Subunit and Is Relatively Insensitive to Nitric Oxide

Nighorn

Byrnes

Morton

1999

Journal of Biological Chemistry

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“…Such phenomena have been well described in the mollusk where increased NO in the procerebral lobe is thought to aid in encoding the odor's identity through modifications in the frequency of field potential oscillations (Gelperin 1994). However, in the mollusk, NO (and sGC) are distributed across all procerebral lobe neurons (Fujie et al 2002(Fujie et al , 2005, whereas in M. sexta, NO is restricted only to the ORNs (Nighorn et al 1998;Collmann et al 2004). The differences in the functional anatomy might confer differences in the function of NO signaling in the two systems.…”

Section: A Role For No In Shaping the Odor Responsementioning

confidence: 99%

“…The pervasive effects on basal activity strongly suggest that a certain level of NO is present at all times and is therefore in a position to act as a tonic regulator of AL neuron function. Since expression of NOS has only been documented in ORNs (Nighorn et al 1998;Collmann et al 2004), this suggests that these neurons have spontaneous activity that results in a tonic level of NO in all olfactory glomeruli. This need not be classic synaptic activity.…”

Section: A Role For No As a Tonic Neuromodulatormentioning

confidence: 99%

“…Over the past 15 years, nitric oxide synthase (NOS) immunohistochemistry and/or NADPH diaphorase staining of the olfactory pathway has provided indirect anatomical evidence for NO modulation in every animal model examined (Bredt et al 1991;Elphick et al 1995;Müller and Hildebrandt 1995;Hopkins et al 1996;Kendrick et al 1997;Alonso et al 1998;Nighorn et al 1998;Fujie et al 2002). A wellcharacterized target of NO, soluble guanylyl cyclase (sGC) has also been localized to neurons within the olfactory pathway (Bicker et al 1996;Hopkins et al 1996;Kendrick et al 1997;…”

Section: Introductionmentioning

confidence: 99%

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Inhibition of nitric oxide and soluble guanylyl cyclase signaling affects olfactory neuron activity in the moth, Manduca sexta

2007

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Nitric oxide is emerging as an important modulator of many physiological processes including olfaction, yet the function of this gas in the processing of olfactory information remains poorly understood. In the antennal lobe of the moth, Manduca sexta, nitric oxide is produced in response to odor stimulation, and many interneurons express soluble guanylyl cyclase, a well-characterized nitric oxide target. We used intracellular recording and staining coupled with pharmacological manipulation of nitric oxide and soluble guanylyl cyclase to test the hypothesis that nitric oxide modulates odor responsiveness in olfactory interneurons through soluble guanylyl cyclase-dependent pathways. Nitric oxide synthase inhibition resulted in pronounced effects on the resting level of firing and the responses to odor stimulation in most interneurons. Effects ranged from bursting to strong attenuation of activity and were often accompanied by membrane depolarization coupled with a change in input resistance. Blocking nitric oxide activation of soluble guanylyl cyclase signaling mimicked the effects of nitric oxide synthase inhibitors in a subset of olfactory neurons, while other cells were differentially affected by this treatment. Together, these results suggest that nitric oxide is required for proper olfactory function, and likely acts through soluble guanylyl cyclase-dependent and -independent mechanisms in different subsets of neurons.

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Neurons involved in nitric oxide-mediated cGMP signaling in the tobacco hornworm,Manduca sexta

et al. 2000

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Recently, both nitric oxide synthase (NOS), and nitric oxide (NO)‐sensitive guanylyl cyclase were cloned in Manduca sexta and implicated in several cellular, developmental, and behavioral processes (Nighorn et al. [1998] J Neurosci 18:7244–7255). However, NO is a highly diffusive gas, and little is known about the range and specificity of its actions on neurons. To begin examining the role of NO as a neurotransmitter in the central nervous system (CNS) of larval Manduca, we have mapped potential NO‐producing neurons using fixation‐resistant NADPH‐diaphorase staining and antisera that recognize a NOS‐specific epitope. In addition, to detect NO‐responsive neurons, we treated the CNS with NO donors and used antibodies that recognize elevated levels of cyclic 3`,5`‐guanosine monophosphate (cGMP). Many potential NO‐producing neurons were mapped, including the ventral unpaired median cells and three pairs of lateral cells in each abdominal ganglion. Additional neurons in the dorsal midline of ganglia A5‐7 (PM2) appear to express NOS in a segment‐specific manner. At the larval‐to‐pupal transition, this staining pattern changes; the PM2 neurons stain weakly or are undetectable and there is novel expression of NOS in cell 27. In response to NO donors, a small number of neurons produce detectable cGMP accumulation in a segment‐specific pattern. These include a pair of posteriodorsally positioned interneurons (IN505) in all the abdominal ganglia, PM2 neurons in A5, and PM1 and PM2 neurons in A7. Hence, PM2 neurons in A5 and A7 are potentially capable of producing and responding to NO. These identified NO‐producing and responding neurons provide a tractable model system for studying the dynamics and specificity of NO signaling in the CNS. J. Comp. Neurol. 419:422–438, 2000. © 2000 Wiley‐Liss, Inc.

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

Cited by 115 publications

References 44 publications

Identification and Characterization of a Novel β Subunit of Soluble Guanylyl Cyclase That Is Active in the Absence of a Second Subunit and Is Relatively Insensitive to Nitric Oxide

Identification and Characterization of a Novel β Subunit of Soluble Guanylyl Cyclase That Is Active in the Absence of a Second Subunit and Is Relatively Insensitive to Nitric Oxide

Inhibition of nitric oxide and soluble guanylyl cyclase signaling affects olfactory neuron activity in the moth, Manduca sexta

Neurons involved in nitric oxide-mediated cGMP signaling in the tobacco hornworm,Manduca sexta

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