Male mating (Caenorhabditis elegans)

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4, 7, 10, 1113121PKD-2/PC-212P66KEYPhosphorylatesIFT Complex A poly peptides DAF-10 and CHE-11 move at the same rate as IFT Complex B polypeptides OSM-5, OSM-1, and OSM-6.TranslocationOSM-5 undergoes anterograde and retrograde transport.ciliummale sensory neuronLOV-1/PC-19PKD-2/PC-29, 13, 14UNC-1013KIN-3/CK26STAM-1/STAM13RAB-513HGSRS-1/Hrs13PKD-2/PC-23CIL-1UnknownASB-18OSM-1PI(3,5)P2DAF-10PI3POSM-51LOV-1/PC-18, 9, 12, 14CHE-11OSM-61KAP-11CWP-52PKD-2/PC-23, 6, 9, 12, 14ATP-28ASG-18ASG-18ASB-1811KIN-10/CK26TAX-6/Calcineurin6ciliary transition zone1412STAM-1/STAM13PKD-2/PC-23PKD-2/PC-23UNC-1013KIN-3/CK26KIN-10/CK26KIN-3/CK26KIN-10/CK26KIN-3/CK26KIN-10/CK26PKD-2/PC-26PDephosphorylates2Sends for degradationPKD-2/PC-26


Description

Caenorhabditis elegans males exhibit sterotypic and invariant mating behavior starting the moment the animal senses a hermaphrodite and ending with insemination. This complex behavior has been broken down into six steps or sub behaviors: male response to hermaphrodite contact, backwards movement along her body, sharply turning in a ventral coil upon reaching the head or tail, continued backing until his tail contacts the vulva (vulval location), spicule insertion, and ejaculation into the hermaphrodite uterus. Each of these sub behaviors have been molecularly dissected and it has been found that two of these sub behaviors, male response to hermaphrodite contact and vulval location involve similar molecules. In particular these behaviors involve cell autonomous signaling through LOV-1 and PKD-2, which are homologs of human polycystin kidney disease (PKD) associated genes PC-1 and PC-2 respectively. Studies in C. elegans have shown that these genes likely have a sensory function rather than structural or development role in the cilia of male sensory neurons. The identification and characterization of LOV-1 and PKD-2 in C. elegans has lead to insights and new avenues of inquiry in the study of human PKD polycystin pathways.

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Bibliography

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  1. Qin H, Rosenbaum JL, Barr MM; ''An autosomal recessive polycystic kidney disease gene homolog is involved in intraflagellar transport in C. elegans ciliated sensory neurons.''; Curr Biol, 2001 PubMed Europe PMC Scholia
  2. Miller RM, Portman DS; ''A latent capacity of the C. elegans polycystins to disrupt sensory transduction is repressed by the single-pass ciliary membrane protein CWP-5.''; Dis Model Mech, 2010 PubMed Europe PMC Scholia
  3. Bae YK, Qin H, Knobel KM, Hu J, Rosenbaum JL, Barr MM; ''General and cell-type specific mechanisms target TRPP2/PKD-2 to cilia.''; Development, 2006 PubMed Europe PMC Scholia
  4. Barr MM, Garcia LR; ''Male mating behavior.''; WormBook, 2006 PubMed Europe PMC Scholia
  5. Bae YK, Kim E, L'hernault SW, Barr MM; ''''; ,
  6. Hu J, Bae YK, Knobel KM, Barr MM; ''Casein kinase II and calcineurin modulate TRPP function and ciliary localization.''; Mol Biol Cell, 2006 PubMed Europe PMC Scholia
  7. Winyard P, Jenkins D; ''Putative roles of cilia in polycystic kidney disease.''; Biochim Biophys Acta, 2011 PubMed Europe PMC Scholia
  8. Hu J, Barr MM; ''ATP-2 interacts with the PLAT domain of LOV-1 and is involved in Caenorhabditis elegans polycystin signaling.''; Mol Biol Cell, 2005 PubMed Europe PMC Scholia
  9. Barr MM, Sternberg PW; ''A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans.''; Nature, 1999 PubMed Europe PMC Scholia
  10. Lipton J; ''Mating worms and the cystic kidney: Caenorhabditis elegans as a model for renal disease.''; Pediatr Nephrol, 2005 PubMed Europe PMC Scholia
  11. Müller RU, Zank S, Fabretti F, Benzing T; ''Caenorhabditis elegans, a model organism for kidney research: from cilia to mechanosensation and longevity.''; Curr Opin Nephrol Hypertens, 2011 PubMed Europe PMC Scholia
  12. Bae YK, Kim E, L'hernault SW, Barr MM; ''The CIL-1 PI 5-phosphatase localizes TRP Polycystins to cilia and activates sperm in C. elegans.''; Curr Biol, 2009 PubMed Europe PMC Scholia
  13. Hu J, Wittekind SG, Barr MM; ''STAM and Hrs down-regulate ciliary TRP receptors.''; Mol Biol Cell, 2007 PubMed Europe PMC Scholia
  14. Barr MM, DeModena J, Braun D, Nguyen CQ, Hall DH, Sternberg PW; ''The Caenorhabditis elegans autosomal dominant polycystic kidney disease gene homologs lov-1 and pkd-2 act in the same pathway.''; Curr Biol, 2001 PubMed Europe PMC Scholia

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External references

DataNodes

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NameTypeDatabase referenceComment
ASB-1GeneProductF35G12.10 (WormBase) ASB-1 and ASG-2 localize to male-specific sensory cilia as well as mitochondria.
ASG-1GeneProductK07A12.3 (WormBase) ASB-1 and ASG-2 localize to male-specific sensory cilia as well as mitochondria.
ATP-2GeneProductC34E10.6 (WormBase)
  • ATP-2 is identified as one candidate that physically interacts with the PLAT domain of LOV-1
  • ATP-2 and other ATP synthase components were found to localize to the cilia of male-specific sensory neurons.
  • ATP-2::GFP clearly colocalizes with PKD-2::DsRed2 in CEM cilia.
  • ATP-2 physically interacts with LOV-1
CHE-11GeneProductC27A7.4 (WormBase)
CIL-1GeneProductC50C3.7 (WormBase)
CWP-5GeneProductF48C11.2 (WormBase)
DAF-10GeneProductF23B2.4 (WormBase)
HGSRS-1/HrsGeneProductC07G1.5 (WormBase) STAM-1 and HGRS-1 expression completely overlaps in cell bodies and ciliary bases of polysystin-expressing neurons.
KAP-1GeneProductF08F8.3 (WormBase) IFT Complex A poly peptides , DAF-10 and CHE-11 move and that motility is at the same rate as IFT Complex B polypeptides, OSM-1, OSM-5 and OSM-6, and KAP (a subunit of the kinesin motor).
KIN-10/CK2GeneProductT01G9.6 (WormBase)
  • kin-3 and kin-10 are coexpressed with lov-1 and pkd-2 in the male-specific CEM head neurons and ray RnB and hook HOB tail neurons
  • KIN-3::GFP and KIN-10 GFP are enriched in cilia and also found in cell bodies (including nuclei), dendrites, and axons.
KIN-3/CK2GeneProductB0205.7 (WormBase)
  • kin-3 and kin-10 are coexpressed with lov-1 and pkd-2 in the male-specific CEM head neurons and ray RnB and hook HOB tail neurons
  • KIN-3::GFP and KIN-10 GFP are enriched in cilia and also found in cell bodies (including nuclei), dendrites, and axons.
LOV-1/PC-1GeneProductZK945.9 (WormBase)
  • LOV-1 localized to cilia by CIL-1
  • LOV-1 is expressed in male specific sensory neurons...with basodendritic subcellular localization in cell body and sensory endings
  • lov-1 is exclusively expressed in three categories of adult male sensory neurons: the rays, the hook, and the head CEMs
  • lov-1 and pkd-2 are expressed in male-specific sensory neurons and are localized to the similar region of the same cell.
  • lov-1 and atp-2 are coexpressed in the tail ray B neurons and HOB hook neuron...as well as the male-specific CEM head neurons.
OSM-1GeneProductT27B1.1 (WormBase)
OSM-5GeneProductY41G9A.1 (WormBase) OSM-5 localizes to cilia through its TPR repeats through intraflagellar transport
OSM-6GeneProductR31.3 (WormBase)
PI(3,5)P2Metabolite
PI3PMetabolite
PKD-2/PC-2GeneProductY73F8A.1 (WormBase)
  • PKD-2 phosphorylation state appears to modulate its function and ciliary localization, with S534A and S534D reflecting two extreme states.
  • CK2-phosphorylated PKD-2 is dephosphorylated by calcineurin.
RAB-5GeneProductF26H9.6 (WormBase) STAM-1 and RAB-5 collocate in the cell bodies and ciliary bases of polycystin-expressing neurons.
STAM-1/STAMGeneProductC34G6.7 (WormBase) GFP-tagged STAM-1 fusion protein localized to cytoplasmic and dendritic puncta resembling endosomes
TAX-6/CalcineurinGeneProductC02F4.2 (WormBase)
  • TAX-6::GFP also localizes to cilia of these polycystin-expressing neurons
  • CK and calcineurin/protein phosphatase 2B(PP2B) modulate PKD-2 function and ciliary localization
  • CK2 and calcineurin function antagonistically to regulate PKD-2 phosphorylation state
  • CK2 phosphorylated PKD-2 is dephosphorylated by calcineurin
  • In the male, we observed tax-6 expression in the CEM, HOB, and ray RnB neurons, with expression noticeably absent from ray 6, which is very similar to lov-1 and pkd-2 expression patterns
UNC-101GeneProductK11D2.3 (WormBase) UNC-101 acts at a somatodendritic sorting step to restrict PKFD-2, along with other ciliary receptors, to the dendritic compartment.
Unknown

Annotated Interactions

SourceTargetTypeDatabase referenceComment
TAX-6/Calcineurinmim-modificationdephosphorylation (KEGG Reaction) CK2 phosphorylated PKD-2 is dephosphorylated by calcineurin
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