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. 1994 Sep;138(1):83–101. doi: 10.1093/genetics/138.1.83

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

E A Lundquist 1, R K Herman 1
PMCID: PMC1206141  PMID: 8001796

Abstract

Mutations in the Caenorhabditis elegans gene mec-8 were previously shown to cause defects in mechanosensation and in the structure and dye filling of certain chemosensory neurons. Using noncomplementation 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-sensitive embryonic and larval arrest, which we have correlated with defects in the attachment of body muscle to the hypodermis and cuticle. Mutations in mec-8 strongly enhance the mutant phenotype of unc-52(viable) mutations; double mutants exhibit an unconditional arrest and paralysis at the twofold stage of embryonic 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 anchorage of myofilament lattice to the muscle cell membrane. We have identified and characterized four extragenic recessive suppressors of a mec-8; unc-52(viable) 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(viable) mutation.

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Selected References

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  1. Bargmann C. I. Genetic and cellular analysis of behavior in C. elegans. Annu Rev Neurosci. 1993;16:47–71. doi: 10.1146/annurev.ne.16.030193.000403. [DOI] [PubMed] [Google Scholar]
  2. Bargmann C. I., Horvitz H. R. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron. 1991 Nov;7(5):729–742. doi: 10.1016/0896-6273(91)90276-6. [DOI] [PubMed] [Google Scholar]
  3. Bargmann C. I., Horvitz H. R. Control of larval development by chemosensory neurons in Caenorhabditis elegans. Science. 1991 Mar 8;251(4998):1243–1246. doi: 10.1126/science.2006412. [DOI] [PubMed] [Google Scholar]
  4. Culotti J. G., Von Ehrenstein G., Culotti M. R., Russell R. L. A second class of acetylcholinesterase-deficient mutants of the nematode Caenorhabditis elegans. Genetics. 1981 Feb;97(2):281–305. doi: 10.1093/genetics/97.2.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ferguson E. L., Horvitz H. R. The multivulva phenotype of certain Caenorhabditis elegans mutants results from defects in two functionally redundant pathways. Genetics. 1989 Sep;123(1):109–121. doi: 10.1093/genetics/123.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Francis G. R., Waterston R. H. Muscle organization in Caenorhabditis elegans: localization of proteins implicated in thin filament attachment and I-band organization. J Cell Biol. 1985 Oct;101(4):1532–1549. doi: 10.1083/jcb.101.4.1532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Francis R., Waterston R. H. Muscle cell attachment in Caenorhabditis elegans. J Cell Biol. 1991 Aug;114(3):465–479. doi: 10.1083/jcb.114.3.465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gilchrist E. J., Moerman D. G. Mutations in the sup-38 gene of Caenorhabditis elegans suppress muscle-attachment defects in unc-52 mutants. Genetics. 1992 Oct;132(2):431–442. doi: 10.1093/genetics/132.2.431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Goh P. Y., Bogaert T. Positioning and maintenance of embryonic body wall muscle attachments in C. elegans requires the mup-1 gene. Development. 1991 Mar;111(3):667–681. doi: 10.1242/dev.111.3.667. [DOI] [PubMed] [Google Scholar]
  10. Guarente L. Synthetic enhancement in gene interaction: a genetic tool come of age. Trends Genet. 1993 Oct;9(10):362–366. doi: 10.1016/0168-9525(93)90042-g. [DOI] [PubMed] [Google Scholar]
  11. Guo X. D., Johnson J. J., Kramer J. M. Embryonic lethality caused by mutations in basement membrane collagen of C. elegans. Nature. 1991 Feb 21;349(6311):707–709. doi: 10.1038/349707a0. [DOI] [PubMed] [Google Scholar]
  12. Hall D. H., Russell R. L. The posterior nervous system of the nematode Caenorhabditis elegans: serial reconstruction of identified neurons and complete pattern of synaptic interactions. J Neurosci. 1991 Jan;11(1):1–22. doi: 10.1523/JNEUROSCI.11-01-00001.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Herman R. K., Hedgecock E. M. Limitation of the size of the vulval primordium of Caenorhabditis elegans by lin-15 expression in surrounding hypodermis. Nature. 1990 Nov 8;348(6297):169–171. doi: 10.1038/348169a0. [DOI] [PubMed] [Google Scholar]
  14. Hirsh D., Vanderslice R. Temperature-sensitive developmental mutants of Caenorhabditis elegans. Dev Biol. 1976 Mar;49(1):220–235. doi: 10.1016/0012-1606(76)90268-2. [DOI] [PubMed] [Google Scholar]
  15. Hodgkin J. Male Phenotypes and Mating Efficiency in CAENORHABDITIS ELEGANS. Genetics. 1983 Jan;103(1):43–64. doi: 10.1093/genetics/103.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hodgkin J., Papp A., Pulak R., Ambros V., Anderson P. A new kind of informational suppression in the nematode Caenorhabditis elegans. Genetics. 1989 Oct;123(2):301–313. doi: 10.1093/genetics/123.2.301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Horvitz H. R., Brenner S., Hodgkin J., Herman R. K. A uniform genetic nomenclature for the nematode Caenorhabditis elegans. Mol Gen Genet. 1979 Sep;175(2):129–133. doi: 10.1007/BF00425528. [DOI] [PubMed] [Google Scholar]
  18. Hoyt M. A., Stearns T., Botstein D. Chromosome instability mutants of Saccharomyces cerevisiae that are defective in microtubule-mediated processes. Mol Cell Biol. 1990 Jan;10(1):223–234. doi: 10.1128/mcb.10.1.223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hresko M. C., Williams B. D., Waterston R. H. Assembly of body wall muscle and muscle cell attachment structures in Caenorhabditis elegans. J Cell Biol. 1994 Feb;124(4):491–506. doi: 10.1083/jcb.124.4.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ishii N., Wadsworth W. G., Stern B. D., Culotti J. G., Hedgecock E. M. UNC-6, a laminin-related protein, guides cell and pioneer axon migrations in C. elegans. Neuron. 1992 Nov;9(5):873–881. doi: 10.1016/0896-6273(92)90240-e. [DOI] [PubMed] [Google Scholar]
  21. Johnson C. D., Rand J. B., Herman R. K., Stern B. D., Russell R. L. The acetylcholinesterase genes of C. elegans: identification of a third gene (ace-3) and mosaic mapping of a synthetic lethal phenotype. Neuron. 1988 Apr;1(2):165–173. doi: 10.1016/0896-6273(88)90201-2. [DOI] [PubMed] [Google Scholar]
  22. Kenan D. J., Query C. C., Keene J. D. RNA recognition: towards identifying determinants of specificity. Trends Biochem Sci. 1991 Jun;16(6):214–220. doi: 10.1016/0968-0004(91)90088-d. [DOI] [PubMed] [Google Scholar]
  23. Kondo K., Makovec B., Waterston R. H., Hodgkin J. Genetic and molecular analysis of eight tRNA(Trp) amber suppressors in Caenorhabditis elegans. J Mol Biol. 1990 Sep 5;215(1):7–19. doi: 10.1016/S0022-2836(05)80090-7. [DOI] [PubMed] [Google Scholar]
  24. Lambie E. J., Kimble J. Two homologous regulatory genes, lin-12 and glp-1, have overlapping functions. Development. 1991 May;112(1):231–240. doi: 10.1242/dev.112.1.231. [DOI] [PubMed] [Google Scholar]
  25. Mackenzie J. M., Jr, Garcea R. L., Zengel J. M., Epstein H. F. Muscle development in Caenorhabditis elegans: mutants exhibiting retarded sarcomere construction. Cell. 1978 Nov;15(3):751–762. doi: 10.1016/0092-8674(78)90261-1. [DOI] [PubMed] [Google Scholar]
  26. Miller D. M., 3rd, Ortiz I., Berliner G. C., Epstein H. F. Differential localization of two myosins within nematode thick filaments. Cell. 1983 Sep;34(2):477–490. doi: 10.1016/0092-8674(83)90381-1. [DOI] [PubMed] [Google Scholar]
  27. Novick P., Osmond B. C., Botstein D. Suppressors of yeast actin mutations. Genetics. 1989 Apr;121(4):659–674. doi: 10.1093/genetics/121.4.659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Perkins L. A., Hedgecock E. M., Thomson J. N., Culotti J. G. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol. 1986 Oct;117(2):456–487. doi: 10.1016/0012-1606(86)90314-3. [DOI] [PubMed] [Google Scholar]
  29. Priess J. R., Hirsh D. I. Caenorhabditis elegans morphogenesis: the role of the cytoskeleton in elongation of the embryo. Dev Biol. 1986 Sep;117(1):156–173. doi: 10.1016/0012-1606(86)90358-1. [DOI] [PubMed] [Google Scholar]
  30. Query C. C., Bentley R. C., Keene J. D. A common RNA recognition motif identified within a defined U1 RNA binding domain of the 70K U1 snRNP protein. Cell. 1989 Apr 7;57(1):89–101. doi: 10.1016/0092-8674(89)90175-x. [DOI] [PubMed] [Google Scholar]
  31. Rose A. M., Baillie D. L. The Effect of Temperature and Parental Age on Recombination and Nondisjunction in CAENORHABDITIS ELEGANS. Genetics. 1979 Jun;92(2):409–418. doi: 10.1093/genetics/92.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sulston J. E., Albertson D. G., Thomson J. N. The Caenorhabditis elegans male: postembryonic development of nongonadal structures. Dev Biol. 1980 Aug;78(2):542–576. doi: 10.1016/0012-1606(80)90352-8. [DOI] [PubMed] [Google Scholar]
  33. Thomas J. H. Thinking about genetic redundancy. Trends Genet. 1993 Nov;9(11):395–399. doi: 10.1016/0168-9525(93)90140-d. [DOI] [PubMed] [Google Scholar]
  34. Venolia L., Waterston R. H. The unc-45 gene of Caenorhabditis elegans is an essential muscle-affecting gene with maternal expression. Genetics. 1990 Oct;126(2):345–353. doi: 10.1093/genetics/126.2.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Waterston R. H. The minor myosin heavy chain, mhcA, of Caenorhabditis elegans is necessary for the initiation of thick filament assembly. EMBO J. 1989 Nov;8(11):3429–3436. doi: 10.1002/j.1460-2075.1989.tb08507.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Williams B. D., Waterston R. H. Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations. J Cell Biol. 1994 Feb;124(4):475–490. doi: 10.1083/jcb.124.4.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wood W. B., Hecht R., Carr S., Vanderslice R., Wolf N., Hirsh D. Parental effects and phenotypic characterization of mutations that affect early development in Caenorhabditis elegans. Dev Biol. 1980 Feb;74(2):446–469. doi: 10.1016/0012-1606(80)90445-5. [DOI] [PubMed] [Google Scholar]
  38. Yandell M. D., Edgar L. G., Wood W. B. Trimethylpsoralen induces small deletion mutations in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1381–1385. doi: 10.1073/pnas.91.4.1381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Zengel J. M., Epstein H. F. Identification of genetic elements associated with muscle structure in the nematode Caenorhabditis elegans. Cell Motil. 1980;1(1):73–97. doi: 10.1002/cm.970010107. [DOI] [PubMed] [Google Scholar]

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