Male mating (WP2287)

Caenorhabditis elegans

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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.

Authors

Karen Yook , Stefan Raats , Finterly Hu , and Egon Willighagen

Activity

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Organisms

Caenorhabditis elegans

Communities

WormBase

Annotations

Pathway Ontology

protein sorting pathway lysosomes based pathway of protein degradation

Disease Ontology

autosomal dominant polycystic kidney disease

Cell Type Ontology

ciliated cell

Participants

Label Type Compact URI Comment
PKD-2/PC-2 GeneProduct wormbase:Y73F8A.1 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.
LOV-1/PC-1 GeneProduct ensembl:WBGene00003058 LOV-1 localizes to intracellular membranes
PKD-2/PC-2 GeneProduct wormbase:Y73F8A.1 PKD-2 localizes to intracellular membranes
Functional localization of PKD-2 is in the ciliary plasma membrane and in intracellular membrane
PKD-2 degradation does not require K48 polyubiquitination and is likely due to STAM-1-Hrs-mediated degradation.
UNC-101 GeneProduct ensembl:WBGene00006829 UNC-101 acts at a somatodendritic sorting step to restrict PKFD-2, along with other ciliary receptors, to the dendritic compartment.
KIN-3/CK2 GeneProduct ensembl:WBGene00002191 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.
STAM-1/STAM GeneProduct ensembl:WBGene00004109 STAM-1A specifically associates with the LOV-1 C-tail
stam-1 and pkd-2 are clearly coexpressed in male-specific ciliated CEM, ray B-type(RnB), and hook HOB sensory neurons
STAM-1A::GFP labels puncta and accumulates at ciliary bases, but is obviously excluded from the cilium proper of CEM, RnB and HOB neurons
STAM-1A co-localizes at the ciliary base with LOV-1 and PKD-2
STAM-1 and HGRS-1 expression completely overlaps in cell bodies and ciliary bases of polysystin-expressing neurons
STAM-1A. but not STAM-1B, specifically acts in the polycystin down-regulation process.
STAM-1A binds, sorts, and targets the polycystin complex for lysosomal degradation
RAB-5 GeneProduct ensembl:WBGene00004268 STAM-1 and RAB-5 collocate in the cell bodies and ciliary bases of polycystin-expressing neurons.
HGSRS-1/Hrs GeneProduct ensembl:WBGene00004101 STAM-1 and HGRS-1 expression completely overlaps in cell bodies and ciliary bases of polysystin-expressing neurons.
PKD-2/PC-2 GeneProduct wormbase:Y73F8A.1 PKD-2 is synthesized in the ER and packaged into vesicles that are transported to the ciliary base and inserted onto the ciliary membrane.
CIL-1 GeneProduct ensembl:WBGene00086546
ASB-1 GeneProduct ensembl:WBGene00000206 ASB-1 and ASG-2 localize to male-specific sensory cilia as well as mitochondria.
OSM-1 GeneProduct ensembl:WBGene00003883
DAF-10 GeneProduct ensembl:WBGene00000906
OSM-5 GeneProduct ensembl:WBGene00003885 OSM-5 localizes to cilia through its TPR repeats through intraflagellar transport
LOV-1/PC-1 GeneProduct ensembl:WBGene00003058 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.
CHE-11 GeneProduct ensembl:WBGene00000490
OSM-6 GeneProduct ensembl:WBGene00003886
KAP-1 GeneProduct ensembl:WBGene00002182 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).
CWP-5 GeneProduct wormbase:F48C11.2
PKD-2/PC-2 GeneProduct wormbase:Y73F8A.1 PKD-2 localized to cilia by CIL-1
PKD-2 GFP accumulates in a ring around the ciliary transition zones.
Functional localization of PKD-2 is in the ciliary plasma membrane and in intracellular membrane
PKD-2 protein is hghly enriched in sensory cilia that are directly exposed to the environment
Within the ciliary region, PKD-2::GFP is distributed throughout the cilium, but primarily concentrated at the ciliary base, which corresponds to the distal-most dendrite and transition zone regions.
In wild-type adult males, PKD-2 is distributed along the ciliary axoneme and accumulates in the transition zone between the cilium and dendrite. In ray neurons of wild-type late L4 males, the magority of the PKD-2 protein localizes to the tip of the cilium and around the transition zone, whereas the staining along the ciliary axoneme is weak.
anti PKD-2 antibodies only label male-specific neurons
lov-1 and pkd-2 are expressed in male-specific sensory neurons and are localized to the similar region of the same cell.
ATP-2 GeneProduct ensembl:WBGene00000229 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
ASG-1 GeneProduct ensembl:WBGene00000209 ASB-1 and ASG-2 localize to male-specific sensory cilia as well as mitochondria.
KIN-10/CK2 GeneProduct ensembl:WBGene00002196 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.
CK2-phosphorylated PKD-2 is dephosphorylated by calcineurin
CK2, lov-1, and pkd-2 act in the same genetic pathway regulating mating behavior.
CK2 modulates PKD-2 function.
PKD-2(S534) is one but not the only in vitro CK2 phosphorylation site.
TAX-6/Calcineurin GeneProduct ensembl:WBGene00006527 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
STAM-1/STAM GeneProduct ensembl:WBGene00004109 GFP-tagged STAM-1 fusion protein localized to cytoplasmic and dendritic puncta resembling endosomes
KIN-10/CK2 GeneProduct ensembl:WBGene00002196 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.

References

  1. A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans. Barr MM, Sternberg PW. Nature. 1999 Sep 23;401(6751):386–9. PubMed Europe PMC Scholia
  2. An autosomal recessive polycystic kidney disease gene homolog is involved in intraflagellar transport in C. elegans ciliated sensory neurons. Qin H, Rosenbaum JL, Barr MM. Curr Biol. 2001 Mar 20;11(6):457–61. PubMed Europe PMC Scholia
  3. The Caenorhabditis elegans autosomal dominant polycystic kidney disease gene homologs lov-1 and pkd-2 act in the same pathway. Barr MM, DeModena J, Braun D, Nguyen CQ, Hall DH, Sternberg PW. Curr Biol. 2001 Sep 4;11(17):1341–6. PubMed Europe PMC Scholia
  4. ATP-2 interacts with the PLAT domain of LOV-1 and is involved in Caenorhabditis elegans polycystin signaling. Hu J, Barr MM. Mol Biol Cell. 2005 Feb;16(2):458–69. PubMed Europe PMC Scholia
  5. Mating worms and the cystic kidney: Caenorhabditis elegans as a model for renal disease. Lipton J. Pediatr Nephrol. 2005 Nov;20(11):1531–6. PubMed Europe PMC Scholia
  6. Casein kinase II and calcineurin modulate TRPP function and ciliary localization. Hu J, Bae YK, Knobel KM, Barr MM. Mol Biol Cell. 2006 May;17(5):2200–11. PubMed Europe PMC Scholia
  7. General and cell-type specific mechanisms target TRPP2/PKD-2 to cilia. Bae YK, Qin H, Knobel KM, Hu J, Rosenbaum JL, Barr MM. Development. 2006 Oct;133(19):3859–70. PubMed Europe PMC Scholia
  8. STAM and Hrs down-regulate ciliary TRP receptors. Hu J, Wittekind SG, Barr MM. Mol Biol Cell. 2007 Sep;18(9):3277–89. PubMed Europe PMC Scholia
  9. Male mating behavior. Barr MM, Garcia LR. WormBook. 2006 Jun 19;1–11. PubMed Europe PMC Scholia
  10. The CIL-1 PI 5-phosphatase localizes TRP Polycystins to cilia and activates sperm in C. elegans. Bae YK, Kim E, L’hernault SW, Barr MM. Curr Biol. 2009 Oct 13;19(19):1599–607. PubMed Europe PMC Scholia
  11. A latent capacity of the C. elegans polycystins to disrupt sensory transduction is repressed by the single-pass ciliary membrane protein CWP-5. Miller RM, Portman DS. Dis Model Mech. 2010;3(7–8):441–50. PubMed Europe PMC Scholia
  12. Caenorhabditis elegans, a model organism for kidney research: from cilia to mechanosensation and longevity. Müller RU, Zank S, Fabretti F, Benzing T. Curr Opin Nephrol Hypertens. 2011 Jul;20(4):400–8. PubMed Europe PMC Scholia
  13. Putative roles of cilia in polycystic kidney disease. Winyard P, Jenkins D. Biochim Biophys Acta. 2011 Oct;1812(10):1256–62. PubMed Europe PMC Scholia