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The Mec-8 Gene of Caenorhabditis Elegans Affects Muscle and Sensory Neuron Function and Interacts with Three Other Genes: Unc-52, Smu-1 and Smu-2

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The Mec-8 Gene of Caenorhabditis Elegans Affects Muscle and Sensory Neuron Function and Interacts with Three Other Genes: Unc-52, Smu-1 and Smu-2 Copyright 0 1994 by the Genetics Society of America The mec-8 Gene of Caenorhabditis elegans Affects Muscle and Sensory Neuron Function and Interacts With Three Other Genes: unc-52, smu-1 and smu-2 Erik A. Lundquist and Robert K. Herman Department of Genetics and Cell Biology, University of Minnesota, St. Paul, Minnesota 55108 Manuscript received March 14, 1994 Accepted for publication May 23, 1994 ABSTRACT Mutations in the Caenorhabditis elegans gene mec-8 were previously shown to cause defects in mech- anosensation and in the structure and dye filling of certain chemosensory neurons. Using noncomple- mentation screens, we have identified eight new mec-8 alleles and a deficiency that uncovers the locus. Strong mec-8 mutants exhibit an incompletely penetrant cold-sensitiveembryonic and larval arrest, which we have correlated with defects in the attachmentof body muscleto the hypodermis and cuticle. Mutations in mec-8 strongly enhance the mutant phenotypeof unc-52(uiable) mutations; double mutants exhibit an unconditional arrestand paralysis at thetwofold stage ofembryonic elongation, a phenotype characteristic of lethal alleles of unc-52, a gene previously shown to encode a homolog of the core protein of heparan sulfate proteogylcan, found in basement membrane, and to be involved in the anchorageof myofilament lattice to the muscle cell membrane. We have identified and characterized four extragenic recessive suppressors of a mec-8; unc-52(uiable) synthetic lethality. The suppressors, which define the genes smu-1 and smu-2, can weakly suppress all mec-8 mutant phenes. They also suppress the muscular dystrophy conferred by an unc-52(uiable) mutation. UTANT analysishas proved to bevery useful in the 1991). It is presumed that mec-8 mutants are defective M study of the development and function of both in touch cell function, although no morphological de- the nervous system and the musculature of the nema- fects in the touch cells of mec-8 animals have been dis- tode Caenorhabditis elegans. Many genes identified by cerned by electron microscopy (CHALFIEand SULSTON mutations that affect animal movement, mechanosen- 1981; CHALFIEand Au 1989).The results of temperature- sation, egg-laying, chemosensation,thermosensation, shift experiments with mec-8(~218ts), a temperature- feeding or defecation have been shown to be important sensitive allele, suggest that only a small amount of mec-8 in nervous system development (forreviews, see CHALFIE product is required fortouch cell function; theMec phe- and WHITE 1988; BARGMANN1993), and among theclass notype can be rescued if the mutants aregrown at per- of mutants affected in movement, manyhave been missive temperature either duringembryogenesis or for shown to have defects in muscle development, structure a time during larval development (CHALFIEand Au or function (WATERSTON 1988; WILLIAMSand WATERSTON 1989). 1994). Mutations in mec-8 also cause defects in chemosen- Mutations in the mec-8 gene were originally identified sory neurons (PERKINSet al. 1986). Neurons required in a screen for mechanosensory-defective (Mec) mu- for various chemosensory behaviors have been identi- tants (CHALFIEand SULSTON 1981; CHALFIEand Au 1989). fied by laser ablation studies (BARGMANNet al. 1990, When a fine hair is drawn gently across the body of a 1993; BARGMANNand HORVITZ1991a,b). All of the im- wild-type worm in the region of the head or tail, the plicated neurons belongto a pairof bilaterally symmet- animal moves quickly backwardor forward, respectively. ric sensilla in the head called amphids. Each wild-type Mec mutants do not respond to this gentle touch, al- amphid consists of the ciliated dendrites of 12 neurons though they do recoil to a prod with a wire and move plus two non-neuronal support cells, a sheath cell and with apparently wild-type coordination. Laser ablation a socket cell (WARDet al. 1975; WAREet al. 1975; WHITE studies have shown that the wild-type response to light et al. 1986; PERKINSet al. 1986). PERKINSet al. (1986) touch is mediated by a set of six sensory neurons, the showed by serial section electron microscopy that mu- touch cells, which havelong, anteriorly directed, longi- tation in mec-8 disrupts the fasciculation of the amphid tudinal processes (CHALFIEand SULSTON1981). The pro- cilia. A convenient method for scoring chemosensory cesses of the touch cells are embedded in the animal’s defects in mec-8 mutants (as well as many other chemo- hypodermis and lie near thecuticle; associatedwith each sensory mutants) has been described (PEFUUNSet al. process is extracellular material called the mantle,which (1986). When living wild-type,animals are bathed in a appears to be connected to the cuticle by fibrous bodies solution of fluorescein isothiocyanate (FITC), the cell (CHALFIEand SULSTON1981; FRANCISand WATERSTON bodies and processes of six neurons of each amphid, Genetics 138: 83-101 (September, 1994) 84 E. A. Lundquist and R. K. Herman which are exposed to the external environment via a ning at the third or fourth larval stage; the disruption pore, fill with dyeand can be readily visualized by fluo- of muscle is correlated with a progressiveparalysis rescence microscopy (HEDGECOCKet al. 1985). Two neu- (MACKENZIE et al. 1978; WATERSTON 1988; GILCHIUST and rons belongingto each of a bilaterally symmetric pair of MOERMAN1992). Other unc-52 alleles cause a paralysis sensilla in the tail, called phasmids (SULSTONet al. 1980; and arrest at thetwofold stage of embryonic elongation WHITEet al. 1986; HALL and RUSSELL1991), arealso ex- (ROGALSKIet al. 1993; WILLIAMSand WATERSTON1994), posed to the outside and fill with dye. PERKINS et al. which is a phenotype characteristic of mutations in other (1986) reported that each of two different mec-8 muta- muscle-affecting genes (WATERSTON1989; VENOLIAand tions invariably block FITC filling of both phasmid neu- WATERSTON1990; BARSTEADand WATERSTON1991; rons and all but two amphid neurons, a phenotype we WILLIAMSand WATERSTON1994). We have found that refer to as Dyf, for abnormal dye filling. when viable unc-52 mutations are combinedwith anyof In this report we further characterize mec-8 mutants. several mec-8 mutations, the phenotype of the double We have identified eight new mec-8 alleles and a defi- mutant is very similar to that of an embryonic lethal ciency of the locus by noncomplementation screens, unc-52 mutant. and we have analyzed the Mec and Dyf phenes caused Suppression of a mutant phenotype by mutation in by all alleles to try to determine the mec-8 null pheno- another geneprovides a second method for identifylng type. We have also discovered that strong mec-8 muta- interactions between genes. We have identified extra- tions cause a cold-sensitive embryonic and larval lethality genic suppressors of mec-8; unc-52 synthetic lethality at low penetrance and cold-sensitive disruptions in the that define two loci, smu-1 and smu-2. We show that structure of body wallmuscle. C. elegam body wall mutations in these two loci are capable of suppressing muscle cells are located in four longitudinal strips that three distinct mec-8 phenes as well as the paralysis con- run the length of the animal, subventrally and subdor- ferred by certain viable unc-52 alleles. sally. To generate animal movement, the contractile force of the body wall muscles must be transmitted to the MATERIALS AND METHODS external cuticle (WATERSTON1988). Interposedbetween General genetic methods: Nematodes were cultured as de- the body muscle cells and the cuticle are a basement scribed by BRENNER(1974). The wild-type strain was N2. We membrane and a thin layer of hypodermis, which is re- havefollowed standard C. elegans genetic nomenclature sponsible for secreting the cuticle. The muscle cells are (HORVITZet al. 1979). Unless otherwise noted, all genetic ex- attached to the adjoining basement membrane, which periments were done at 20". Genes, mutations and chromo- some rearrangements used in this work werethe following (for in turn is anchored to thecuticle via filament-associated references, see HODCKINet al. 1988): LG (linkage group) I: structures called fibrous organelles that bridge the thin dpy-5(e61),unc-40(e271), mec-6(e1342), unc-l3(e51), unc- hypodermal layer and thus complete the mechanical 55(e402),unc-29(eI93), mec-8fe398, u303, 1174, u391, coupling of muscle to cuticle (FRANCISand WATERSTON u218 ts, u456, u314) (CHALFIEand Au 1989), mec-8(rh170) 1991; HRESKOet al. 1994). We have found that mec-8 (E. HEDGECOCK,personal communication), dpy-24(s 71), unc- 75(e950),unc-lOl(ml), unc-59(e261), unc-95(su33), unc- animals grown at 16" frequently exhibit defects in at- 54(e190), nDf23, nDf24, nDf25, nDp4.LGII: sqt-2(sc3), mup- tachment of the myofilament lattice to the hypodermis 1(e2346),unc-85(e1414), dpy-lO(e128), unc-4(e120), and cuticle. In sum, mec-8 mutations cause defects in the sqt-1 (scl3), unc-52(e669, e669su250, e444, e998, e1421, functions of at least three distinct types of cells: mech- su54, su200) and mnC1. LGIII: dpy-l8(e364). LGW. dpy- 13(mn278),emb-9(hc70), bli-6(sc16), mec-3(e1338), him- anosensory and chemosensory neuronsand body 8(e1491). LGV unc-60(e667), mec-1 (el 066), unc-23(e324), muscle. mec-9(el494), him-5(e1467).LGX: unc-l(e538), lon-2(e678), One of the virtues of C. elegans genetics is its suit- mec-2(e75),unc-97(su110), unc-6(ev400), mec-7(e1343), ability for identifylng interacting genesthrough the mec-lO(e1515),him-4(e1267), unc-3(el51), daf-6(e1377), analysis of the phenotypes of double mutants. We report unc-7(bx5),mec-S(e1340), let-2(6246), osm-l(p808), mec-4(e1497). here two types of genetic interaction involving mec-8. Genetic mapping of mec-8 We have refined the map po- The first is a synthetic enhancement of an unc-52 mu- sition of mec-8, which earlier was mapped to the rightof dpy-5 tantphenotype by mec-8 mutation.Products of the Z (CHALFIEand SULSTON1981).
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