The KLP-6 kinesin is required for male mating behaviors and polycystin localization in Caenorhabditis elegans
- PMID: 15753033
- DOI: 10.1016/j.cub.2004.12.073
The KLP-6 kinesin is required for male mating behaviors and polycystin localization in Caenorhabditis elegans
Abstract
Background: Male mating behavior of the nematode Caenorhabditis elegans offers an intriguing model to study the genetics of sensory behavior, cilia function, and autosomal dominant polycystic kidney disease (ADPKD). The C. elegans polycystins LOV-1 and PKD-2 act in male-specific sensory cilia required for response and vulva-location mating behaviors.
Results: Here, we identify and characterize a new mating mutant, sy511. sy511 behavioral phenotypes were mapped to a mutation in the klp-6 locus, a gene encoding a member of the kinesin-3 family (previously known as the UNC-104/Kif1A family). KLP-6 has a single homolog of unknown function in vertebrate genomes, including fish, chicken, mouse, rat, and human. We show that KLP-6 expresses exclusively in sensory neurons with exposed ciliated endings and colocalizes with the polycystins in cilia of male-specific neurons. Cilia of klp-6 mutants appear normal, suggesting a defect in sensory neuron function but not development. KLP-6 structure-function analysis reveals that the putative cargo binding domain directs the motor to cilia. Consistent with a motor-cargo association between KLP-6 and the polycystins, klp-6 is required for PKD-2 localization and function within cilia. Genetically, we find klp-6 regulates behavior through polycystin-dependent and -independent pathways.
Conclusion: Multiple ciliary transport pathways dependent on kinesin-II, OSM-3, and KLP-6 may act sequentially to build cilia and localize sensory ciliary membrane proteins such as the polycystins. We propose that KLP-6 and the polycystins function as an evolutionarily conserved ciliary unit. KLP-6 promises new routes to understanding cilia function, behavior, and ADPKD.
Similar articles
-
Mating behavior, male sensory cilia, and polycystins in Caenorhabditis elegans.Semin Cell Dev Biol. 2014 Sep;33:25-33. doi: 10.1016/j.semcdb.2014.06.001. Epub 2014 Jun 27. Semin Cell Dev Biol. 2014. PMID: 24977333 Free PMC article. Review.
-
ATP-2 interacts with the PLAT domain of LOV-1 and is involved in Caenorhabditis elegans polycystin signaling.Mol Biol Cell. 2005 Feb;16(2):458-69. doi: 10.1091/mbc.e04-09-0851. Epub 2004 Nov 24. Mol Biol Cell. 2005. PMID: 15563610 Free PMC article.
-
Functional characterization of the C. elegans nephrocystins NPHP-1 and NPHP-4 and their role in cilia and male sensory behaviors.Exp Cell Res. 2005 May 1;305(2):333-42. doi: 10.1016/j.yexcr.2005.01.008. Exp Cell Res. 2005. PMID: 15817158
-
Towards understanding the polycystins.Nephron Exp Nephrol. 2003 Jan;93(1):e9-17. doi: 10.1159/000066650. Nephron Exp Nephrol. 2003. PMID: 12411744
-
Mating worms and the cystic kidney: Caenorhabditis elegans as a model for renal disease.Pediatr Nephrol. 2005 Nov;20(11):1531-6. doi: 10.1007/s00467-005-1958-x. Epub 2005 Jun 10. Pediatr Nephrol. 2005. PMID: 15947985 Review.
Cited by
-
Kinesin-2 motors differentially impact biogenesis of extracellular vesicle subpopulations shed from sensory cilia.iScience. 2022 Oct 4;25(11):105262. doi: 10.1016/j.isci.2022.105262. eCollection 2022 Nov 18. iScience. 2022. PMID: 36304122 Free PMC article.
-
Unraveling the hierarchical structure of posture and muscle activity changes during mating of Caenorhabditis elegans.PNAS Nexus. 2024 Jan 24;3(2):pgae032. doi: 10.1093/pnasnexus/pgae032. eCollection 2024 Feb. PNAS Nexus. 2024. PMID: 38312221 Free PMC article.
-
Function and dynamics of PKD2 in Chlamydomonas reinhardtii flagella.J Cell Biol. 2007 Nov 5;179(3):501-14. doi: 10.1083/jcb.200704069. J Cell Biol. 2007. PMID: 17984324 Free PMC article.
-
The LIM and POU homeobox genes ttx-3 and unc-86 act as terminal selectors in distinct cholinergic and serotonergic neuron types.Development. 2014 Jan;141(2):422-35. doi: 10.1242/dev.099721. Epub 2013 Dec 18. Development. 2014. PMID: 24353061 Free PMC article.
-
Mating behavior, male sensory cilia, and polycystins in Caenorhabditis elegans.Semin Cell Dev Biol. 2014 Sep;33:25-33. doi: 10.1016/j.semcdb.2014.06.001. Epub 2014 Jun 27. Semin Cell Dev Biol. 2014. PMID: 24977333 Free PMC article. Review.
Publication types
MeSH terms
Substances
Grants and funding
LinkOut - more resources
Full Text Sources
Other Literature Sources
Molecular Biology Databases
Miscellaneous