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Neuropeptides are ubiquitous chemical mediators: Using the stomatogastric nervous system as a model system

Petra Skiebe^*

Freie Universität Berlin, Fachbereich Biologie, Chemie, Pharmazie, Neurobiologie, Königin-Luise-Straße 28–30, D-14195 Berlin, Germany

View larger version (24K): [in a new window]   Fig. 1. Schematic drawings showing the stomatogastric nervous system (STNS), stomach, heart and pericardial organs. (A) Location within Cherax destructor. (B) Enlarged view: The STNS consists of four ganglia, the paired commissural ganglia (CoGs), the oesophageal ganglion (OG) and the stomatogastric ganglion (STG), together with their connecting and motor nerves. The STNS is located between the brain and the suboesophageal ganglion (SOG), which are connected by the circumoesophageal connective (coc) surrounding the oesophagus. The post-oesophageal commissure (poc) links both cocs close to the SOG. The STG lies within the ophthalmic artery, which carries haemolymph containing hormones released by the pericardial organs to the brain. Another important neurohaemal organ, the X-organ/sinus gland complex, is located in the eystalks. (C) Schematic diagram of an isolated STNS and the location of nerves discussed in the review. dvn, dorsal ventricular nerve; ion, inferior oesophageal nerve; ivn, inferior ventricular nerve; lvn, lateral ventricular nerve; on, oesophageal nerve; son, superior oesophageal nerve; stn, stomatogastric nerve. Not drawn to scale (modified from Skiebe, 1999).

View larger version (53K): [in a new window]   Fig. 2. Summary of the neuroactive mediators present in the neuropile of the stomatogastric ganglion (STG) and neurohaemal organs identified either biochemically and/or by immunocytochemistry. (A) Neuroactive mediators in the STG of the crab Cancer borealis, the lobsters Homarus americanus and Homarus gammarus, the spiny lobster Panulirus interruptus and the crayfish Cherax destructor. Large circles in the drawing represent the STG somata. Mediators shown to be present are marked by a plus sign, those not present by a minus sign. The classical transmitters of the STG neurones are acetylcholine and glutamate. Only in a few cell bodies were other mediators found in both adults (a) and during development (d; see also Table 1). The source of the serotonin is the gastropyloric receptor cells (*). ACh, acetylcholine (Marder, 1987); Glu, glutamate (Marder, 1987); GABA, -aminobutyric acid (Nusbaum et al., 1989; Cournil et al., 1990; Swensen et al., 2000); DA, dopamine (Barker et al., 1979; Kushner and Barker, 1983; Marder, 1987; Cournil et al., 1994; Cournil et al., 1995); HA, histamine (Claiborne and Selverston, 1984a; Mulloney and Hall, 1991); 5-HT, serotonin (Beltz et al., 1984; Katz et al., 1989; Kilman et al., 1999; P. Skiebe, unpublished data); Oct, octopamine (Barker et al., 1979); NO, nitric oxide (Scholz et al., 1998); AST, allatostatin (Skiebe and Schneider, 1994; Kilman et al., 1999; Skiebe, 1999); ATR, allatotropin (A. E. Christie, unpublished data); ß-PDH, ß-pigment dispersing hormone (Mortin and Marder, 1991); Buc, buccalin (Christie et al., 1994); CabTRP, Cancer borealis tachykinin-related peptide (Goldberg et al., 1988; Blitz et al., 1995; Christie et al., 1997b; Fénelon et al., 1999); CCAP, crustacean cardioactive peptide (Christie et al., 1995b; Kilman, 1998; Skiebe et al., 1999); CCK, cholecystokinin (Turrigiano and Selverston, 1991; Christie et al., 1995a; Meyrand et al., 2000; subscripts indicate different antibodies against CCK); Cor, corazonin (Christie and Nusbaum, 1995); FLRF, FLRFamide-related peptides (only FLRFamides have been isolated from crustaceans) (Marder et al., 1987; Weimann et al., 1993; Fénelon et al., 1998; Kilman et al., 1999); Myo, myomodulin (Christie et al., 1994); Proc, proctolin (Marder et al., 1986; Fénelon et al., 1998; Fénelon et al., 1999; Kilman et al., 1999; Skiebe et al., 1999); RPCH, red pigment-concentrating hormone (Nusbaum and Marder, 1988; Dickinson and Marder, 1989; Fénelon et al., 1999). (B) Summary of the neuroactive mediators present in the STG (excluding the classical transmitters ACh and Glu of STG neurones), in the pericardial organs (PO) and in the X-organ/sinus gland complex (SG) of the crab Cancer borealis and on the post-oesophageal commissure (poc), the STG and the PO of the crayfish Cherax destructor (Cancer borealis) (Christie et al., 1995b) (Cherax destructor) (Skiebe, 1999; Skiebe et al., 1999) (P. Skiebe, unpublished data). Fig.2A, left, is modified from Marder et al., 1994; Fig.2B, left, is modified from Christie et al., 1995b. stn, stomatogastric nerve; dvn, dorsal ventricular nerve.

View larger version (71K): [in a new window]   Fig. 3. Putative neurohaemal release zone on the surface of the circumoesophageal connective (coc) and the post-oesophageal commissure (poc). (A) Drawing of allatostatin-like immunoreactivity on the surface of the cocs and the poc found only in Cherax destructor. Similar staining was found with antibodies generated against crustacean cardioactive peptide and proctolin. Other stained structures, including axons in the coc and cell bodies and neuropile in the commissural ganglia (CoGs) were not drawn. ion, inferior oesophageal nerve; son, superior oesophageal nerve. (B) Transmission electron micrograph of a cross section through the poc showing a large profile in the perineural sheath that contains dense-core vesicles (arrowheads) and electron-dense granules (arrows) close to a glial cell (g) process. The profile is separated from the haemolymph space (h) only by a thin extracellular matrix (em) representing a basal lamina. m, mitochondrion. Scale bar, 0.5µm. A is modified from Skiebe, 1999; B is modified from Skiebe et al., 1999.

View larger version (38K): [in a new window]   Fig. 4. Schematic drawing of the interactions between identified interneurones, sensory neurones and motor networks of the stomatogastric ganglion (STG). (Left) In the crab Cancer borealis, three pairs of proctolin (Proc)-like immunoreactive neurones are present (coloured in different shades of grey), which each elicit a different motor pattern. The two modulatory proctolin neurones (MPN) are located in the oesophageal ganglion (OG) or the oesophageal nerve and elicit a pyloric motor pattern (pyloric patterns coloured in different shades of orange) via excitatory synapses (symbolised by triangles). MPN inhibits, via the release of -aminobutyric acid (GABA; inhibitory synapses symbolised by small circles), two pairs of modulatory neurones located in the commissural ganglia, which are called commissural projection neurones 2 (CPN2) and modulatory commissural neurones 1 (MCN1), thereby preventing a gastric mill rhythm, which the latter neurones normally initiate. Stimulating MCN1 (containing proctolin, Cancer borealis tachykinin-related peptide, CabTRP, and GABA) alone elicits a gastropyloric motor pattern (gastric mill motor patterns are coloured in different shades of green, gastropyloric motor patterns are drawn in stripes of orange and green). After blocking the action of CabTRP, MCN1 does not elicit a gastric mill rhythm and the pyloric rhythm it initiates is more similar but still not identical to that elicited by MPN. Co-stimulation of the MCN1 and CPN2 elicits a different type of gastropyloric pattern. MCN1 receives rhythmic inhibition from the lateral gastric neurone (LG) in the STG. This does not influence the MCN1 synapses in the commissural ganglia (CoGs), demonstrating that activity of synapses can vary with the output region. Modulatory commissural neurones 7 (MCN7) also elicit a pyloric motor pattern that differs from that elicited by the MPNs. (Right) In the lobster Homarus gammarus, the anterior gastric receptor (AGR) excites two pairs of modulatory interneurones in the CoGs: the commissural gastric (CG) neurones and the gastric inhibitor (GI) neurones. AGR, which is a mechanoreceptor activated by the movements of the gastric mill muscle 1 (gm1), has its soma in the dorsal ventricular nerve (dvn) and projects through the STG without any arborization to innervate the CoGs. When AGR fires weakly, one gastric mill pattern is elicited. When AGR fires strongly, a second gastric mill pattern is elicited, demonstrating that the activity of a feedback loop is able to select different motor patterns (modified from Blitz et al., 1999; Blitz and Nusbaum, 1997; Coleman and Nusbaum, 1994; Coleman et al., 1995; Combes et al., 1999a; Combes et al., 1999b).

View larger version (29K): [in a new window]   Fig. 5. Example of peptidergic innervation of muscles in Cherax destructor. (A) Schematic diagram of the branching pattern of the neurone labelled with an FMRFamide antibody in the oesophageal ganglion (OG), presumably the cardiac dilator neurone 1 (CD1). (B) Schematic diagram of the distribution of FLRFamide-like immunoreactivity on the muscles: regions of the muscles that show FLRFamide-like immunoreactivity are coloured orange; the regions without immunoreactivity are shown in white. (C) An example of the actual FLRFamide-like immunoreactivity on the c5a muscle, which is covered with strongly stained varicosities (montage of two confocal micrographs). Unstained muscles are also present (asterisks). acdn, anterior cardiac dilator nerve; c1 to c5, cardiac sac muscles; cv1, cardiac valve muscle; vcdn, ventral cardiac dilator nerve (for other abbreviations see Fig.1). Scale bar, 200µm (modified from Skiebe et al., 1999). Arrows denote the main axon; the double-headed arrow marks axon collaterals.