Fundam, appl, NemalOl" 1993, 16 (3), 193-198

Fomm article

CHEMOSENSORY PHYSIOLOGY OF

Jens AuMANN !nslilute ofPhylopalhology, University of Kiel, Hermann-Rodewald-Slrasse 9, 2300 Kiel l, Germany, Accepted for publication 20 October 1992, Key-words: Nematodes, chemosensory physiology, chemoreception, transduction, transmission,

Little is yet known about the subject of this paper. Morphology and distribution of cht. Several sciences like deve!opmental biology have profit­ mosensilla ed from the use of as a mode! (Wood, 1988), Although the neuroanatomy of nema­ Nematode chemosensilla are composed of neurons, todes has been weil examined in this model, the neu­ gland cells and supporting cells. The neurons connect rosciences made progress with other , The se­ the outer surface with the nerve ring, Their dendritic quencing of the C. elegans genome as part of the Human nerve extensions are located in body pores and are thus Genome Project (Sulston el al., 1992) may, however, in contact with the external environment. The pores are lead to the structural and functional identification of filled with exudates that are produced in gland cells. many yet unknown molecules, and our knowledge of the Using these criteria, several sensilla can be cIassified as physiological processes involved in the recognition of chemosensitive. In the anterior region, amphids are gen­ chernical stimuli in nematodes may progress rapidly. erally considered to have a chemosensitive function. Other approaches appear more complicated. Despite Other anterior sensilla inside body pores with the same successful attempts by Jones el al. (1991) to record elec­ function are the inner labial sensilla, the outer labial trical activity of chemosensory neurons in nematodes, sensilla and the cephalic sensilla. In the posterior region, difficulties in the application of electrophysiological the phasmids of the and the spicule recep­ methods are imposed by the small size of plant-parasitic tors of males probably act as chemosensilla. Nematode and free-living nematodes and by the preparation of chemosensilla have been described in detail (McLaren, suitable environmental conditions for -parasitic 1976a, b; Coomans, 1979; Wright, 1980, 1983; and species. Coomans & De Grisse, 1981), whereas Chalfie and The senses of taste and smell can be differentiated in White (1988) confined their description to C, elegans. vertebrates and in insects, but this differentiation ap­ A model ofvertebrate and insect olfaction pears meaningless for animais like nematodes that live in aquatic habitats (Schmidt-Nielsen, 1990). 1 will there­ The following model is based on various publications fore use the terms " chemosensilla " for the chemical (Augustine el al., 1987; Vogt el al., 1990; Bruch, 1990; sense organs and" chemosensitive " for their function. Burchell, 1991; Korsching, 1991) according to which The foIlowing paragraphs fust describe briefly the olfactory signaIs bind to the extracellular side of trans­ morphology and distribution of nematode chemosen­ membrane receptor proteins of dendritic nerve exten­ silla and present a model of vertebrate and insect olfac­ sions after they have passed the mucus layer of the ver­ tion. The conformity of this model with our present tebrate olfactory epithelium or the insect sensillum knowledge of nematode chemosensory physiology is Iymph. Binding is followed by the dissociation of the then discussed in the next five paragraphs. They are signal molecules from their receptors. The receptor pro­ arranged in the sequence of events that start with the teins activate G (or guanosine triphosphate-binding) diffusion of signal molecules into the chemosensillum­ proteins on the inner side of the cell membrane, which in associated exudates, i.e. pre-interactive events, receptor turn activate enzymes (adenylate cyclase or phospholi­ events, post-interactive events, transduction, and trans­ pase C) that catalyze the fonnation of secondary mess­ mission. Finally, the prospects for nematode control are engers (cyclic AMP or inositol trisphosphate, respec­ outlined from the data and hypotheses presented in the tively), These messengers then open secondary preceeding paragraphs. This paper is based on an idea messenger-gated ion channels. A rapid ion flux through expressed by Dodd and Castellucci (1991) :" ... ail sen­ the channels changes the e!ectric potential on the mem­ sory systems rely on the same basic principles of proc­ brane surface. This causes the opening of voltage-gated essing and organization not only in humans, but ion channe!s and the generation of an action potential. throughout much of phylogeny, " When the action potential has arrived at the chernical

/SSN 1164-5571193/031l 93 06 S 2.60/ © Gaulhie1'-Villars - ORSTOM 193

r- l 2 HAl 1993 J. Aumann

synapse between the sensory neuron and a neighbouring Receptor events 2 2 neuron, Ca +-channels are opened. The Ca +influx near Odorant receptor mo1ecules were probably identified the synapse causes the secretion of neurotransmitters at for the first time by Buck and Axel (1991). They the presynaptic side of the synaptic cleft. They bind to showed that these molecules from rat olfactory tissue receptors at the postsynaptic side of the cleft. Finally the belong to a family of G protein-coupled receptor pro­ animal reacts to the olfactory signal, for instance by the teins with seven trans-membrane spanning regions. One activation of motoneurons. of the most intensively studied members of this family is the 13-adrenergic receptor of vertebrates (Kobilka, Pre-interactive events 1992). Nematode receptor molecu]es are probably located In vertebrates and insects, the passage of hydrophobic on the surface of the dendritic nerve extensions of che­ olfactory signais through the aqueous mucus layer of the mosensilla. Little is known about their properties Gans­ vertebrate olfactory epithelium or through the aqueous son, 1987). Lectins, more or less specific carbohydrate­ insect sensillum Iymph may be aided by the binding of binding proteins or glycoproteins, have been shown to the signais to olfactory binding proteins, e.g. the odor­ inhibit the recognition of chemical signals in P. redivivus ant-binding proteins (OBP) of vertebrates and the phe­ Gansson & Nordbring-Hertz, 1984), C. elegans Geya­ romone-binding proteins (PBP) of insects (Carr el al., prakash el al., 1985) and Trichoslrongylus colubriformis 1990; Getchell & Getchell, 1990; Lerner el al., 1990; (Bone & Bottjer, 1985). It was assumed that inhibition Pelosi & Maida, 1990; Pevsner & Snyder, 1990). In ne­ resulted from lectin binding to receptor molecules, in­ matodes, however, signal molecules appear to be hydro­ dicating the occurrence of carbohydrate chains in these philic, because these animais live in aqueous environ­ molecules Gansson, 1987). However, the recognition of ments. Molecules with a function similar to the odorant­ chemical signais by males of Helerodera schachlii could and pheromone-binding proteins of vertebrates and not be inhibited by lectins (Aumann el al., 1990). These insects, respectively, therefore seem to be useless for ne­ differences between species are confirmed by the obser­ matodes. Neverthe1ess, this question is still unresolved, vation of Aumann and Wyss (1992) that severa] lectins since results of Jones el al. (1992) indicate that genes diffused into the amphidial pores of P. redivivus but not coding for proteins similar to insect olfactory binding of H. schachlii. An inhibition of chemorecognition of proteins are present in nematodes. H. schachlii males after treatrnent with the extracellulari­ The composition of gland cell-secreted exudates fill­ Iy acting sulfhydryl reagent mersalyl acid points to the ing the pores of nematode chemosensilla is important, occurrence of disulfide bridges in these molecules (Au­ because signal molecules have to pass the exudates on mann, 1991). Chalfie and Wolinsky (1990) suggested their way toward the receptors. These exudates have that the deg-l gene of C. elegans may encode ion chan­ been identified as glycoproteins in the amphids of Hele­ nels or membrane receptors in the nervous system. rodera schachlii males (Aumann, 1989). Several exper­ iments with other species from ail major trophic groups Post-interactive events have shown that lectins bind specifical!y to the exudates (Forrest & Robertson, 1986; McClure & Stynes, 1988; After binding of signais and the fol!owing transduc­ Aumann & Wyss, 1989; Aumann el al., 1991; Ibrahim, tion, a signal accumulation in the chemosensillum-asso­ 1991) or in the pore region of chemosensilla (Bowman ciated exudates has to be prevented; otherwise a sensi­ el al., 1988; Davis el a!., 1988; Forrest el al., 1988a, b; tive recognition of concentration gradients is not Bird el al., 1989; Robertson el al., 1989), indicating that guarameed (Stengl el al., 1992). Several mechanisms the sensillum exudates contain carbohydrates. It was preventing an accumulation of odorants have been dis­ postulated that sorne of these carbohydrates are sialic cussed : i) uptake into the vertebrate olfactory epitheli­ acids with a function in chemoreception (e.g. Zucker­ um and a subsequent enzymatic degradation (Lazard el man, 1983). They have been proposed to occur at the al., 1991); il) enzymatic degradation in the insect sensil­ chemosensilla of Panagrellus redivivus Gansson lum Iymph r:vogt el al., 1985); iil) binding to phero­ & N ordbring-Hertz, 1983, 1984) and Melozdogyne spp. mone-binding proteins in the insect sensillum Iymph (Davis el al., 1988.) However, analyses using chemical (Vogt & Riddiford, 1981); and iv) desorption from ver­ and biochemical methods did not conftrm the occur­ tebrate mucus exudates back into air (Hornung & Mo­ rence of siatic acids in P. redivivus (Bacic el al., 1990; zel!, 1981). The identification ofodorant degradation by Reuter el al., 1991) and C. elegans (Bacic el al., 1990). UDP-glucuronosyl transferase in bovine olfactory epi­ Exudate proteins have been labelled with Coomassie thelium (Lazard el al., 1991) and of a pheromone-de­ Brilliant Blue by Premachandran el al. (1988) and Au­ grading esterase in moth sensillum lymph (Vogt el al., mann and Wyss (1989). Since mucous glycoproteins 1985) point to a significam role of the frrst and second form stable, intertangled networks in solution Gentoft, mechanism in vertebrates and insects, respectively. 1990), signais may reach the receptors exclusively by However, in nematodes the second and third mecha­ diffusion. nism, enzymatic degradation and binding to signal-

194 Fundam. appl. Nemalol. C/umosensory physiology of nemaLOdes binding proteins in the sensillum exudates, respectively, transduction have been identified as cyclic AMP (Na­ are unlikely to occur because they do not aUow a dis­ kamura & Gold, 1987) and inositol trisphosphate crimination between signal molecules before and after (Boekhoff et al.) 1990). No such messenger and none of binding to their receptors; under the condition that en­ the enzymes generating them (adenylate cyclase and zymes and signal-binding proteins are equally distrib­ phospholipase C, respectively) have yet been found in uted in the sensillum exudates, every molecule in the nematode chemosensilla. However, Ward (1973) has sensillum pore will equally be affected by these proteins. shown that C. elegans is attracted by cyclic AMP, indica­ An increasing efficiency of signal removal after binding ting that it may function as a secondary messenger in the will therefore decrease the probability of receptor bind­ transduction of chemical signaIs in nematodes. ing for signaIs that diffuse from the exterior toward the Nothing is known about ion channels of nematode receptors. Hence the ftrst and the last of the above­ sensory neurons. In other organisms, these channels mentioned mechanisms, uptake inta the underlying tis­ control the membrane influx and efflux of ions. In ver­ sue and desorption from exudates into the exterior, re­ tebrate and insect olfaction, ligand-gated ion channels spectively, are more likely to occur in nematodes. In are opened directly by binding of cyclic AMP (Naka­ insects, however, pre-interactive and post-interactive mura & Gold, 1987). In frog taste receptor ceUs, ion events may be spatially separated. According to Kaiss­ channels are opened indirectly through the activation ling (1986), odorants may reach the receptors through ofprotein kinases by secondary messengers and the sub­ pore tubules that contact the dendritic membrane. The sequent ion channel phosphorylation (Avenet et al.) odorants may thus not pass the sensillum Iymph and 1988). However, a definitive role for protein kinases in they may not be affected by enzymes and signal-binding olfactory transduction has yet to be shown (Firestein, proteins (Schneider, 1992). 1991). The ion flux through the ligand-gated channels The assumption that in nematades olfactory binding causes the opening of voltage-gated ion channels and proteins like GBP and PBP are not involved in pre­ the generation of an action potential (Augustine et al.) interactive events and that the signais reach the recep­ 1987). Lu et al. (1990) found cAMP-dependent protein tors exclusively by diffusion leads ta the following hy­ kinases in the amphidial region of C. elegans) supporting pothesis: According ta Fick's principle (see e.g. the sequence cyclic AMP - protein kinase - ion channel Schmidt-Nielsen, 1990), diffusion depends among in nematode chemosensory neurons. other factors on solvent viscosity. The viscosity of the glycoprotein exudates of chemosensilla is possibly high­ Transm.ission er than that of the aqueous environment. This may cause an accumulation of signal molecules in the exu­ The arrivai of the action potential near the synapse dates. However, as mentioned above, a signal accumu­ causes the opening of Ca2+-channels and the influx of lation has ta be prevented in order ta guarantee a sensi­ Ca2+. This leads ta the secretion or neurotransrrutters, tive recognition of concentration gradients. Nematodes which transmit information between neurons at chem­ may thus possess active mechanisms for the removal of ical synapses (Augustine et al.) 1987). In C. elegans) sen­ signais from the exudates. Such a mechanism could be sory neurons terminate in the nerve ring, where they are the production of exudates that transport the accumu­ connected with other neurons via synapses (White et al., lated signal molecules into the exterior (Hornung & Mo­ 1986). Acetylcholinesterase, the enzyme that metabo­ zell, 1981). The observation of Aumann et al. (1990) lizes the neurotransmitter acetylcholine, has been identi­ that exudate production is enhanced when H. schachtii fied in the nerve ring region ofseveral nematode species males move in a female sex pheromone gradient may (Wright & Awan, 1976; Culotti et al.) 1981; Matsuura, support this hypothesis. The capacity of exudate pro­ 1986). Furthermore, carbamate and organophosphate duction in plant parasitic nematades has been demon­ pesticides, which inhibit acetylcholinesterase by revers­ strated by Premachandran et al. (1988) and Aumann ible and irreversible binding, respectively, have been and Wyss (1989). shown to inhibit the orientation behaviour of different nematode species (Di Sanzo, 1973; Marban-Mendoza Transduction & Viglierchio, 1980; Cuany et al., 1984; Gaugler & Campbell, 1991; Sikora & Hartwig, 1991). These da­ G Proteins are coupled to many different receptor ta indicate that acetylcholine works as a neurotransmit­ molecules in animaIs, fungi and plants. They activate ter at the synapses of sensory neurons in the nerve ring. enzymes that catalyze the formation of secondary mess­ In addition to acetylcholinesterase, catecholaminergic engers (Kaziro et al.) 1991; Simon et al.) 1991). Specific structures have been identified in the nerve ring of sev­ G proteins, named Golf' were isolated from rat olfactory eral nematode species (Goh & Davey, 1976; Sharpe et tissue Gones & Reed, 1989). G proteins have been al., 1980). Aumann and Hashem (1993) showed that found in C. elegans (Lochrie et al.) 1991), but their loca­ chlordimeform, an acaricide that blocks octapamine re­ tion is unknown. ceptors, specifically inhibits the recognition of chemical Secondary messengers that play a role in olfactory signais in H. schachtii males, indicating that the neu-

Vol. 16) n° 3 - 1993 195 J. Aumann

rotransmitter octopamine plays also a role at the nerve AUMANN,J, & WYSS, U. (1992). Permeabiliry ofchemorecep­ ring synapses of sensory neurons. tor-associated exudates of Panagrellus redivivus and Het.ero­ dera schachlii. Europ. Soc. NemaLOlogisls, 21 Si in!. NemaLOI. Prospects for nematode control Symp., Albufeira, Porlugal, 11-17April 1992. 7 [Abstr.]. The porential of a specific inhibition of chemosensory AVENET, P., HOFMAl'-.'N, F. & LINDEMANN, B. (1988). Trans­ mechanisms for nematode control has been stressed by duction in taste receptor cells requires cAMP-dependent several authors Ce.g. Zuckerman, 1983; Zuckerman & protein kinase. Nalure, 331 : 351-354. Jansson, 1984; Bone, 1987; Dusenbery, 1987; Jansson, BACIC, A, KAHANE, 1. & ZUCKERMAN, B. M. (1990). Pa­ 1987; MacKinnon, 1987; Haseeb & Fried, 1988). It nagrellus redivivus and Caenorhabdilis elegans : evidence for may be concluded from the previous paragraphs that the absence of sialic acids. Exp. Parasil., 71 : 483-488 this goal is difficult to achieve. No nematode-specific BIRD, A. F., BON1G, 1. & BACle, A (1989). Factors affecting molecules have yet been identified in chemosensilla. the adhesion of micro-organisms to the surfaces of plant­ The similarities of transduction and transmission mech­ parasitic nematodes. Parasilology, 98: 155-164. anisms between vertebrates and insects point to the pos­ BOEKHOFF, 1., T ARElLUS, E., STROTMANN, J, & BREER, H. sibility that the ooly specific targets for control mech­ (1990). Rapid activation of alternative second messenger anisms may be the receptor molecules. They may be pathways in olfactory cilia from rats by different odorants. blockable by the irreversible binding of signal deriv­ EMBO JI, 9 : 2453-2458. atives. Goly one signal molecule has so far been identi­ BONE, L. W. (1987). Pheromone communication in nema­ fied: the sex pheromonal substance vanillic acid for todes. ln: Veech, J, A & Dickson, D. W. (Eds). Vislas on Helerodem glycines Gaffe el al., 1989). The future identi­ nemaLOlogy. Hyattsville, MD, USA, Soc. Nematologists fication of sex pheromones and root exudate attractants Inc.. 147-152. may lead to the development of irreversibly binding sig­ BONE., L. W. & BOTTIER, K. P. (1985). Cuticular carbo­ naI derivatives and thus to environmentally safer control hydrates of three nematode species and chemoreception by methods. Tn'choslrongylus colubriformis. J. Parasil., 71 : 235-238. BOWMAN, D. D., ABRAHAM, D., MlKA-GRlEVE, M. Acknowledgment & GRIEVE, R. B. (1988). Binding ofconcanavalin A to areas 1 thank Professor U. Wyss for helpful suggestions and the compatible with the locations of the amphids and phasmids Deutsche Forschungsgemeinschaft for financial support (Au of larvae of Dirofilaria immilis (Nematoda : Filarioidea) and 100/1-1 ). Toxocara canis (Nematoda : Ascaridoidea). Proc. helmimh. Soc. Wash., 55 : 94-96. References BRUCH, R. C. (1990). 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