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The KLP-6 Kinesin Is Required for Male Mating Behaviors and Polycystin Localization in Caenorhabditis elegans

The KLP-6 Kinesin Is Required for Male Mating Behaviors and Polycystin Localization in Caenorhabditis elegans,10.1016/j.cub.2004.12.073,Current Biolog

The KLP-6 Kinesin Is Required for Male Mating Behaviors and Polycystin Localization in Caenorhabditis elegans   (Citations: 29)
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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.
Journal: Current Biology - CURR BIOL , vol. 15, no. 5, pp. 394-404, 2005
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    • ... cha-1 expression driven by the klp-6 promoter, which is specifically expressed in IL2 also rescued the nictation defect in cha-1 (n2411) mutant...

    Harksun Leeet al. Nictation, a dispersal behavior of the nematode Caenorhabditis elegans...

    • ...channels in male-specific ciliated sensory neurons and are implicated in polycystic kidney disease [112]...

    Michael A. Silvermanet al. Intraflagellar transport and the generation of dynamic, structurally a...

    • ...Next, the ciliary sorting step, which involves KLP-6 (Peden and Barr, 2005), intraflagellar transport (IFT) (Bae et al., 2006), calcineurin (Hu et al., 2006), and the Hrs-STAM ubiquitin-sorting complex (Hu et al., 2007), regulates PKD-2 access to and abundance in the cilium...
    • ...To determine if abnormal PKD-2 localization alters male reproductive abilities, we measured male response behavior efficiency (RE) and mating efficiency (ME) of the cil mutants (Table 1). A response efficiency (RE) assay measures in minutes the male’s behavioral ability to respond to hermaphrodite contact (Liu and Sternberg, 1995; Barr et al., 2001; Peden and Barr, 2005)...
    • ...Similarly, klp-6 and IFT mutant males exhibit similar accumulation of PKD-2::GFP in ray dendrites and response defects (Peden and Barr, 2005; Bae et al., 2006)...
    • ...PKD-2 ciliary abundance is tightly regulated via post-translational modifications (Hu et al., 2006), other polycystins (Bae et al., 2006), the kinesin-3 KLP-6 (Peden and Barr, 2005), intraflagellar transport (IFT) (Qin et al., 2005), and the STAM-Hrs ubiquitin degradation machinery (Hu et al., 2007)...

    Young-Kyung Baeet al. Identification of genes involved in the ciliary trafficking of C. eleg...

    • ...The precise topographic arrangement and compartmentalization of cell-specific sensory receptors and signaling molecules in the cilia are essential for accurate and sensitive detection and signal transduction of external cues (Young and Droz, 1968; Kulaga et al, 2004; Nishimura et al, 2004; Corbit et al, 2005; Haycraft et al, 2005; Peden and Barr, 2005; Qin et al, 2005; Flannery et al, 2006; Wang et al, 2006)...

    Saikat Mukhopadhyayet al. Distinct IFT mechanisms contribute to the generation of ciliary struct...

    • ...Response is mediated by signaling through the polycystin-class TRP channels LOV-1 and PKD-2, which may act as mechanosensors (Barr and Sternberg, 1999), though other sensory pathways are likely to be involved (Barr et al., 2001; Peden and Barr, 2005; R. M. Miller and D. S. P., unpublished data)...

    Douglas S. Portman. Genetic Control of Sex Differences in C. elegans Neurobiology and Beha...

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