Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1998 Jan;148(1):187–200. doi: 10.1093/genetics/148.1.187

Analysis of osm-6, a gene that affects sensory cilium structure and sensory neuron function in Caenorhabditis elegans.

J Collet 1, C A Spike 1, E A Lundquist 1, J E Shaw 1, R K Herman 1
PMCID: PMC1459801  PMID: 9475731

Abstract

Mutation in the Caenorhabditis elegans gene osm-6 was previously shown to result in defects in the ultrastructure of sensory cilia and defects in chemosensory and mechanosensory behaviors. We have cloned osm-6 by transposon tagging and transformation rescue and have identified molecular lesions associated with five osm-6 mutations. The osm-6 gene encodes a protein that is 40% identical in amino acid sequence to a predicted mammalian protein of unknown function. We fused osm-6 with the gene for green fluorescent protein (GFP); the fusion gene rescued the osm-6 mutant phenotype and showed accumulation of GFP in ciliated sensory neurons exclusively. The OSM-6::GFP protein was localized to cytoplasm, including processes and dendritic endings where sensory cilia are situated. Mutations in other genes known to cause ciliary defects led to changes in the appearance of OSM-6::GFP in dendritic endings or, in the case of daf-19, reduced OSM-6::GFP accumulation. We conclude from an analysis of genetic mosaics that osm-6 acts cell autonomously in affecting cilium structure.

Full Text

The Full Text of this article is available as a PDF (259.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adzhubei A. A., Sternberg M. J. Left-handed polyproline II helices commonly occur in globular proteins. J Mol Biol. 1993 Jan 20;229(2):472–493. doi: 10.1006/jmbi.1993.1047. [DOI] [PubMed] [Google Scholar]
  2. Albert P. S., Brown S. J., Riddle D. L. Sensory control of dauer larva formation in Caenorhabditis elegans. J Comp Neurol. 1981 May 20;198(3):435–451. doi: 10.1002/cne.901980305. [DOI] [PubMed] [Google Scholar]
  3. Albertson D. G., Thomson J. N. The pharynx of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci. 1976 Aug 10;275(938):299–325. doi: 10.1098/rstb.1976.0085. [DOI] [PubMed] [Google Scholar]
  4. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  5. Aroian R. V., Levy A. D., Koga M., Ohshima Y., Kramer J. M., Sternberg P. W. Splicing in Caenorhabditis elegans does not require an AG at the 3' splice acceptor site. Mol Cell Biol. 1993 Jan;13(1):626–637. doi: 10.1128/mcb.13.1.626-637.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bargmann C. I., Hartwieg E., Horvitz H. R. Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell. 1993 Aug 13;74(3):515–527. doi: 10.1016/0092-8674(93)80053-h. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. 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]
  9. Bargmann C. I., Thomas J. H., Horvitz H. R. Chemosensory cell function in the behavior and development of Caenorhabditis elegans. Cold Spring Harb Symp Quant Biol. 1990;55:529–538. doi: 10.1101/sqb.1990.055.01.051. [DOI] [PubMed] [Google Scholar]
  10. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974 May;77(1):71–94. doi: 10.1093/genetics/77.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cassada R. C., Russell R. L. The dauerlarva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Dev Biol. 1975 Oct;46(2):326–342. doi: 10.1016/0012-1606(75)90109-8. [DOI] [PubMed] [Google Scholar]
  12. Chalfie M., Sulston J. Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Dev Biol. 1981 Mar;82(2):358–370. doi: 10.1016/0012-1606(81)90459-0. [DOI] [PubMed] [Google Scholar]
  13. Chalfie M., Tu Y., Euskirchen G., Ward W. W., Prasher D. C. Green fluorescent protein as a marker for gene expression. Science. 1994 Feb 11;263(5148):802–805. doi: 10.1126/science.8303295. [DOI] [PubMed] [Google Scholar]
  14. Chow K. L., Hall D. H., Emmons S. W. The mab-21 gene of Caenorhabditis elegans encodes a novel protein required for choice of alternate cell fates. Development. 1995 Nov;121(11):3615–3626. doi: 10.1242/dev.121.11.3615. [DOI] [PubMed] [Google Scholar]
  15. Cohen G. B., Ren R., Baltimore D. Modular binding domains in signal transduction proteins. Cell. 1995 Jan 27;80(2):237–248. doi: 10.1016/0092-8674(95)90406-9. [DOI] [PubMed] [Google Scholar]
  16. Coulson A., Huynh C., Kozono Y., Shownkeen R. The physical map of the Caenorhabditis elegans genome. Methods Cell Biol. 1995;48:533–550. doi: 10.1016/s0091-679x(08)61402-8. [DOI] [PubMed] [Google Scholar]
  17. Culotti J. G., Russell R. L. Osmotic avoidance defective mutants of the nematode Caenorhabditis elegans. Genetics. 1978 Oct;90(2):243–256. doi: 10.1093/genetics/90.2.243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Daniels M. P., Hamprecht B. The ultrastructure of neuroblastoma glioma somatic cell hybrids. Expression of neuronal characteristics stimulated by dibutyryl adenosine 3',5' cyclic monophosphate. J Cell Biol. 1974 Nov;63(2 Pt 1):691–699. doi: 10.1083/jcb.63.2.691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Feng S., Chen J. K., Yu H., Simon J. A., Schreiber S. L. Two binding orientations for peptides to the Src SH3 domain: development of a general model for SH3-ligand interactions. Science. 1994 Nov 18;266(5188):1241–1247. doi: 10.1126/science.7526465. [DOI] [PubMed] [Google Scholar]
  20. Greene L. A., Tischler A. S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2424–2428. doi: 10.1073/pnas.73.7.2424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Hedgecock E. M., Culotti J. G., Thomson J. N., Perkins L. A. Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes. Dev Biol. 1985 Sep;111(1):158–170. doi: 10.1016/0012-1606(85)90443-9. [DOI] [PubMed] [Google Scholar]
  23. Hedgecock E. M., Herman R. K. The ncl-1 gene and genetic mosaics of Caenorhabditis elegans. Genetics. 1995 Nov;141(3):989–1006. doi: 10.1093/genetics/141.3.989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Henikoff S. Unidirectional digestion with exonuclease III in DNA sequence analysis. Methods Enzymol. 1987;155:156–165. doi: 10.1016/0076-6879(87)55014-5. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. 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]
  27. Kaplan J. M., Horvitz H. R. A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2227–2231. doi: 10.1073/pnas.90.6.2227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kenyon C. A gene involved in the development of the posterior body region of C. elegans. Cell. 1986 Aug 1;46(3):477–487. doi: 10.1016/0092-8674(86)90668-9. [DOI] [PubMed] [Google Scholar]
  29. Krause M. Transcription and translation. Methods Cell Biol. 1995;48:483–512. [PubMed] [Google Scholar]
  30. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  31. Lee C. H., Saksela K., Mirza U. A., Chait B. T., Kuriyan J. Crystal structure of the conserved core of HIV-1 Nef complexed with a Src family SH3 domain. Cell. 1996 Jun 14;85(6):931–942. doi: 10.1016/s0092-8674(00)81276-3. [DOI] [PubMed] [Google Scholar]
  32. Lee N. H., Weinstock K. G., Kirkness E. F., Earle-Hughes J. A., Fuldner R. A., Marmaros S., Glodek A., Gocayne J. D., Adams M. D., Kerlavage A. R. Comparative expressed-sequence-tag analysis of differential gene expression profiles in PC-12 cells before and after nerve growth factor treatment. Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8303–8307. doi: 10.1073/pnas.92.18.8303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Lewis J. A., Hodgkin J. A. Specific neuroanatomical changes in chemosensory mutants of the nematode Caenorhabditis elegans. J Comp Neurol. 1977 Apr 1;172(3):489–510. doi: 10.1002/cne.901720306. [DOI] [PubMed] [Google Scholar]
  34. Li W., Herman R. K., Shaw J. E. Analysis of the Caenorhabditis elegans axonal guidance and outgrowth gene unc-33. Genetics. 1992 Nov;132(3):675–689. doi: 10.1093/genetics/132.3.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Lim W. A., Richards F. M., Fox R. O. Structural determinants of peptide-binding orientation and of sequence specificity in SH3 domains. Nature. 1994 Nov 24;372(6504):375–379. doi: 10.1038/372375a0. [DOI] [PubMed] [Google Scholar]
  36. Mello C. C., Kramer J. M., Stinchcomb D., Ambros V. Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 1991 Dec;10(12):3959–3970. doi: 10.1002/j.1460-2075.1991.tb04966.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Mello C., Fire A. DNA transformation. Methods Cell Biol. 1995;48:451–482. [PubMed] [Google Scholar]
  38. Miller L. M., Waring D. A., Kim S. K. Mosaic analysis using a ncl-1 (+) extrachromosomal array reveals that lin-31 acts in the Pn.p cells during Caenorhabditis elegans vulval development. Genetics. 1996 Jul;143(3):1181–1191. doi: 10.1093/genetics/143.3.1181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Mori I., Moerman D. G., Waterston R. H. Analysis of a mutator activity necessary for germline transposition and excision of Tc1 transposable elements in Caenorhabditis elegans. Genetics. 1988 Oct;120(2):397–407. doi: 10.1093/genetics/120.2.397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Nelson G. A., Ward S. Vesicle fusion, pseudopod extension and amoeboid motility are induced in nematode spermatids by the ionophore monensin. Cell. 1980 Feb;19(2):457–464. doi: 10.1016/0092-8674(80)90520-6. [DOI] [PubMed] [Google Scholar]
  41. 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]
  42. Reisine T., Bell G. I. Molecular biology of opioid receptors. Trends Neurosci. 1993 Dec;16(12):506–510. doi: 10.1016/0166-2236(93)90194-q. [DOI] [PubMed] [Google Scholar]
  43. Rosenzweig B., Liao L. W., Hirsh D. Target sequences for the C. elegans transposable element Tc1. Nucleic Acids Res. 1983 Oct 25;11(20):7137–7140. doi: 10.1093/nar/11.20.7137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Rost B. PHD: predicting one-dimensional protein structure by profile-based neural networks. Methods Enzymol. 1996;266:525–539. doi: 10.1016/s0076-6879(96)66033-9. [DOI] [PubMed] [Google Scholar]
  45. Rushforth A. M., Anderson P. Splicing removes the Caenorhabditis elegans transposon Tc1 from most mutant pre-mRNAs. Mol Cell Biol. 1996 Jan;16(1):422–429. doi: 10.1128/mcb.16.1.422. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Schackwitz W. S., Inoue T., Thomas J. H. Chemosensory neurons function in parallel to mediate a pheromone response in C. elegans. Neuron. 1996 Oct;17(4):719–728. doi: 10.1016/s0896-6273(00)80203-2. [DOI] [PubMed] [Google Scholar]
  48. Starich T. A., Herman R. K., Kari C. K., Yeh W. H., Schackwitz W. S., Schuyler M. W., Collet J., Thomas J. H., Riddle D. L. Mutations affecting the chemosensory neurons of Caenorhabditis elegans. Genetics. 1995 Jan;139(1):171–188. doi: 10.1093/genetics/139.1.171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Starich T. A., Herman R. K., Shaw J. E. Molecular and genetic analysis of unc-7, a Caenorhabditis elegans gene required for coordinated locomotion. Genetics. 1993 Mar;133(3):527–541. doi: 10.1093/genetics/133.3.527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. 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]
  51. Sulston J. E., Horvitz H. R. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol. 1977 Mar;56(1):110–156. doi: 10.1016/0012-1606(77)90158-0. [DOI] [PubMed] [Google Scholar]
  52. Sulston J. E., Schierenberg E., White J. G., Thomson J. N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol. 1983 Nov;100(1):64–119. doi: 10.1016/0012-1606(83)90201-4. [DOI] [PubMed] [Google Scholar]
  53. Tabish M., Siddiqui Z. K., Nishikawa K., Siddiqui S. S. Exclusive expression of C. elegans osm-3 kinesin gene in chemosensory neurons open to the external environment. J Mol Biol. 1995 Mar 31;247(3):377–389. doi: 10.1006/jmbi.1994.0146. [DOI] [PubMed] [Google Scholar]
  54. Thomas J. H. Chemosensory regulation of development in C. elegans. Bioessays. 1993 Dec;15(12):791–797. doi: 10.1002/bies.950151204. [DOI] [PubMed] [Google Scholar]
  55. Ward S., Thomson N., White J. G., Brenner S. Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans.?2UU. J Comp Neurol. 1975 Apr 1;160(3):313–337. doi: 10.1002/cne.901600305. [DOI] [PubMed] [Google Scholar]
  56. Waterston R. H. A second informational suppressor, SUP-7 X, in Caenorhabditis elegans. Genetics. 1981 Feb;97(2):307–325. doi: 10.1093/genetics/97.2.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Waterston R. H., Brenner S. A suppressor mutation in the nematode acting on specific alleles of many genes. Nature. 1978 Oct 26;275(5682):715–719. doi: 10.1038/275715a0. [DOI] [PubMed] [Google Scholar]
  58. Wick M. J., Ann D. K., Loh H. H. Molecular cloning of a novel protein regulated by opioid treatment of NG108-15 cells. Brain Res Mol Brain Res. 1995 Aug;32(1):171–175. doi: 10.1016/0169-328x(95)00090-f. [DOI] [PubMed] [Google Scholar]
  59. Wilson R., Ainscough R., Anderson K., Baynes C., Berks M., Bonfield J., Burton J., Connell M., Copsey T., Cooper J. 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature. 1994 Mar 3;368(6466):32–38. doi: 10.1038/368032a0. [DOI] [PubMed] [Google Scholar]
  60. Wolf N., Hirsh D., McIntosh J. R. Spermatogenesis in males of the free-living nematode, Caenorhabditis elegans. J Ultrastruct Res. 1978 May;63(2):155–169. doi: 10.1016/s0022-5320(78)80071-9. [DOI] [PubMed] [Google Scholar]
  61. Zhang H., Blumenthal T. Functional analysis of an intron 3' splice site in Caenorhabditis elegans. RNA. 1996 Apr;2(4):380–388. [PMC free article] [PubMed] [Google Scholar]
  62. de Both N. J., Vermey M., van't Hull E., Klootwijk-van-Dijke E., van Griensven L. J., Mol J. N., Stoof T. J. A new erythroid cell line induced by Rauscher murine leukaemia virus. Nature. 1978 Apr 13;272(5654):626–628. doi: 10.1038/272626a0. [DOI] [PubMed] [Google Scholar]
  63. van Luenen H. G., Plasterk R. H. Target site choice of the related transposable elements Tc1 and Tc3 of Caenorhabditis elegans. Nucleic Acids Res. 1994 Feb 11;22(3):262–269. doi: 10.1093/nar/22.3.262. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES