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A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans

Nature volume 401, pages 386–389 (1999)Cite this article

Abstract

The stereotyped mating behaviour of the Caenorhabditis elegans male is made up of several substeps: response, backing, turning, vulva location, spicule insertion and sperm transfer. The complexity of this behaviour is reflected in the sexually dimorphic anatomy and nervous system1. Behavioural functions have been assigned to most of the male-specific sensory neurons by means of cell ablations; for example, the hook sensory neurons HOA and HOB are specifically required for vulva location2. We have investigated how sensory perception of the hermaphrodite by the C. elegans male controls mating behaviours. Here we identify a gene, lov-1 (for location of vulva), that is required for two male sensory behaviours: response and vulva location. lov-1 encodes a putative membrane protein with a mucin-like, serine–threonine-rich amino terminus3 followed by two blocks of homology to human polycystins, products of the autosomal dominant polycystic kidney-disease loci PKD1 and PKD2 (ref 4). LOV-1 is the closest C. elegans homologue of PKD1. lov-1 is expressed in adult males in sensory neurons of the rays, hook and head, which mediate response, vulva location, and potentially chemotaxis to hermaphrodites, respectively2,5. PKD-2, the C. elegans homologue of PKD2, is localized to the same neurons as LOV-1, suggesting that they function in the same pathway.

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Figure 1: lov-1 and pkd-2 genomic structures, constructs, rescue data and expression patterns.
Figure 2: LOV-1 structural features and homologies.
Figure 3: LOV-1::GFP1 and PKD-2::GFP2 are colocalized to adult male sensory-neuron cell bodies and dendrites.

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References

  1. Hodgkin,J. in The Nematode C. elegans (ed. Wood, B.) 243–279 (Cold Spring Harbor Laboratory Press, New York, 1988).

    Google Scholar 

  2. Liu,K. S. & Sternberg,P. W. Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron 14, 79–89 (1995).

    Article  CAS  Google Scholar 

  3. Carraway,K. L. & Fregien,N. Mucin structure and function: Insights from molecular biology. Trends Glycosci. Glycotechnol. 7, 31–44 (1995).

    Article  CAS  Google Scholar 

  4. Torres,V. D. New insights into polycystic kidney disease and its treatment. Curr. Opin. Nephrol. Hypertens. 7, 159–169 (1998).

    Article  CAS  Google Scholar 

  5. Ward,S., Thomson,N., White,J. G. & Brenner,S. Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J. Comp. Neurol. 160, 313–337 (1975).

    Article  CAS  Google Scholar 

  6. White,J. G., Southgate,D., Thomson,J. N. & Brenner,S. The structure of the nervous system of Caenorhabditis elegans. Phil. Trans. R. Soc. Lond. B 314, 1–340 (1986).

    Article  ADS  CAS  Google Scholar 

  7. Collet,J., Spike,C. A., Lundquist,E. A., Shaw,J. E. & Herman,R. K. Analysis of osm-6, a gene that affects sensory cilium structure and sensory neuron function in Caenorhabditis elegans. Genetics 148, 187–200 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Kaplan,J. M. & Horvitz,H. R. A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 90, 2227–2231 (1993).

    Article  ADS  CAS  Google Scholar 

  9. Perkins,L. A., Hedgecock,E. M., Thomson,J. N. & Culotti,J. G. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev. Biol. 117, 456–487 (1986).

    Article  CAS  Google Scholar 

  10. Mochizuki,T. et al. PKD2, a gene for polycystic kidney disease that encodes an integral membrane protein. Science 242, 1339–1342 (1996).

    Article  ADS  Google Scholar 

  11. Montell,C. & Rubin,G. M. Molecular characterization of the Drosophila trp locus: a putative integral membrane protein required for phototransduction. Neuron 2, 1313–1323 (1989).

    Article  CAS  Google Scholar 

  12. Sanford,R. et al. Comparative analysis of the polycystic kidney disease 1 (PKD1) gene reveals an integral membrane glycoprotein with multiple evolutionary conserved domains. Hum. Mol. Genet. 9, 1483–1489 (1997).

    Article  Google Scholar 

  13. Nomura,H. et al. Identification of PKDL, a novel polycystic kidney disease 2-like gene whose murine homologue is deleted in mice with kidney and retinal defects. J. Biol. Chem. 273, 25967–25973 (1998).

    Article  CAS  Google Scholar 

  14. Wu,G. et al. Identification of PKD2L, a human PKD2-related gene: Tissue-specific expression and mapping to chromosome 10q25. Genomics 54, 564–568 (1998).

    Article  CAS  Google Scholar 

  15. Qian,F. et al. PKD1 interacts with PKD2 through a probably coiled-coil domain. Nature Genet. 16, 179–183 (1997).

    Article  CAS  Google Scholar 

  16. Tsiokas,L., Kim,E., Arnould,T., Sukhatme,V. P. & Walz,G. Homo- and heterodimeric interactions between the gene products of PKD1 and PKD2. Proc. Natl Acad. Sci. USA 94, 6965–6970 (1997).

    Article  ADS  CAS  Google Scholar 

  17. Arnould,T. et al. The polycystic kidney disease 1 gene product mediates protein kinase C α-dependent and c-Jun N-terminal kinase-dependent activation of the transcription factor AP-1. J. Biol. Chem. 273, 6013-6018 (1998).

    Article  Google Scholar 

  18. Parnell,S. C. et al. The polycystic kidney disease-1 protein, polycystin-1, binds and activates heterotrimeric G-proteins in vitro. Biochem. Biophys. Res. Commun. 251, 625–631 (1998).

    Article  CAS  Google Scholar 

  19. Kim,E. et al. The polycystic kidney kidney disease 1 gene product modulates Wnt signaling. J. Biol. Chem. 274, 4947–4953 (1999).

    Article  CAS  Google Scholar 

  20. Tsiokas,L. et al. Specific association of the gene product of PKD2 with the TRPC1 channel. Proc. Natl Acad. Sci. USA 7, 3934–3939 (1999).

    Article  ADS  Google Scholar 

  21. Sullivan,L. P., Wallace,D. P. & Grantham,J. J. Epithelial transport in polycystic kidney disease. Physiol. Rev. 78, 1165–1191 (1998).

    Article  CAS  Google Scholar 

  22. Hudspeth,A. J. How the ear's works work. Nature 341, 397–404 (1989).

    Article  ADS  CAS  Google Scholar 

  23. Driscoll,M. & Kaplan,J. in C. elegans II (ed. Riddle, D. I., Blumenthal, T., Meyer, B. J. & Priess, J. R.) 645–677 (Cold spring Harbor Laboratory Press, New York, 1997).

    Google Scholar 

  24. Montell,C. TRP trapped in the fly signalling web. Curr. Opin. Neurobiol. 8, 389–397 (1998).

    Article  CAS  Google Scholar 

  25. Brenner,S. The genetics of Caenorhabditis elegans. Genetics 77, 71–94 (1974).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Hodgkin,J. Male phenotypes and mating efficiency in Caenorhabditis elegans. Genetics 103, 43–64 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Hodgkin,J. & Doniach,T. Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics 146, 149–164 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Schnabel,H. & Schnabel,R. An organ-specific differentiation gene, pha-1, from Caenorhabditis elegans. Science 250, 686–688 (1990).

    Article  ADS  CAS  Google Scholar 

  29. Chalfie,M., Tu,Y., Euskirchen,G., Ward,W. W. & Prasher,D. D. Green fluorescent protein as a marker for gene expression. Science 263, 802–805 (1994).

    Article  ADS  CAS  Google Scholar 

  30. Sulston,J. D., Albertson,D. G. & Thomson,J. N. The Caenorhabditis elegans male: Postembryonic development of nongonadal structures. Dev. Biol. 78, 542–576 (1980).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank J. Copeland for help isolating lov-1(sy582Δ); L. Jiang, R. Garcia and R. Ballester for discussions and constructive criticisms; members of our lab, S. Myers and M. Snow for experimental suggestions; D. Sherwood and B. Smith for assistance with confocal microscopy; A. Fire for vectors; and R. Herman for osm-6::gfp. The Caenorhabditis Genetics stock Center and Sanger Center provided numerous strains, cosmids and sequencing data. This work was supported by the Howard Hughes Medical Institute, with which P.W.S. is an investigator and M.M.B. is an associate, and by the Seaver Institute.

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  1. Howard Hughes Medical Institute and Division of Biology, California Institute of Technology, Pasadena, 91125, California, USA

    Maureen M. Barr & Paul W. Sternberg

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  1. Maureen M. Barr
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Correspondence to Paul W. Sternberg.

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Barr, M., Sternberg, P. A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans. Nature 401, 386–389 (1999). https://doi.org/10.1038/43913

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