The CIL-1 PI 5-Phosphatase Localizes TRP Polycystins to Cilia and Activates Sperm in C. elegans

Young Kyung Bae; Eunsoo Kim; Steven W. L'Hernault; Maureen M. Barr

doi:10.1016/j.cub.2009.08.045

The CIL-1 PI 5-Phosphatase Localizes TRP Polycystins to Cilia and Activates Sperm in C. elegans

Young Kyung Bae, Eunsoo Kim, Steven W. L'Hernault, Maureen M. Barr

Department of Life Science

Research output: Contribution to journal › Article › peer-review

46 Scopus citations

Abstract

Background: C. elegans male sexual behaviors include chemotaxis and response to hermaphrodites, backing, turning, vulva location, spicule insertion, and sperm transfer, culminating in cross-fertilization of hermaphrodite oocytes with male sperm. The LOV-1 and PKD-2 transient receptor potential polycystin (TRPP) complex localizes to ciliated endings of C. elegans male-specific sensory neurons and mediates several aspects of male mating behavior. TRPP complex ciliary localization and sensory function are evolutionarily conserved. A genetic screen for C. elegans mutants with PKD-2 ciliary localization (Cil) defects led to the isolation of a mutation in the cil-1 gene. Results: Here, we report that a phosphoinositide (PI) 5-phosphatase, CIL-1, regulates TRPP complex ciliary receptor localization and sperm activation. cil-1 does not regulate the localization of other ciliary proteins, including intraflagellar transport (IFT) components, sensory receptors, or other TRP channels in different cell types. Rather, cil-1 specifically controls TRPP complex trafficking in male-specific sensory neurons and does so in a cell-autonomous fashion. In these cells, cil-1 is required for normal PI(3)P distribution, indicating that a balance between PI(3,5)P2 and PI(3)P is important for TRPP localization. cil-1 mutants are infertile because of sperm activation and motility defects. In sperm, the CIL-1 5-phosphatase and a wortmannin-sensitive PI 3-kinase act antagonistically to regulate the conversion of sessile spermatids into motile spermatozoa, implicating PI(3,4,5)P3 signaling in nematode sperm activation. Conclusion: Our studies identify the CIL-1 5-phosphatase as a key regulator of PI metabolism in cell types that are important in several aspects of male reproductive biology.

Original language	English
Pages (from-to)	1599-1607
Number of pages	9
Journal	Current Biology
Volume	19
Issue number	19
DOIs	https://doi.org/10.1016/j.cub.2009.08.045
State	Published - 13 Oct 2009

Bibliographical note

Funding Information:
Nancy L'Hernault provided assistance with electron microscopy. We thank Natalia Morsci, Jinghua Hu, and members of Barr laboratory for help throughout the course of this project; John Archibald, Ching Kung, and Andy Singson for helpful discussion; David Sherwood and Joshua Ziel for critical reading of the manuscript; Barth Grant for intestinal PI markers, Shawn X.-Y. Xu for the anti-TRP-3 antibody; and Sam Ward for sharing unpublished data. Some nematode strains used in this work were provided by the Caenorhabditis Genetics Center, which is funded by the National Institutes of Health (NIH) National Center for Research Resources (NCRR), and by Shohei Mitani of the National Bioresource Project for the Nematode (Japan). This work was supported by the NIH (DK059418 and DK074746 to M.M.B.; GM082932 to S.W.L.H.), the National Science Foundation (0131532 to S.W.L.H.), and the Polycystic Kidney Disease (PKD) Foundation (to M.M.B.).

Keywords

CELLBIO

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10.1016/j.cub.2009.08.045

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title = "The CIL-1 PI 5-Phosphatase Localizes TRP Polycystins to Cilia and Activates Sperm in C. elegans",

abstract = "Background: C. elegans male sexual behaviors include chemotaxis and response to hermaphrodites, backing, turning, vulva location, spicule insertion, and sperm transfer, culminating in cross-fertilization of hermaphrodite oocytes with male sperm. The LOV-1 and PKD-2 transient receptor potential polycystin (TRPP) complex localizes to ciliated endings of C. elegans male-specific sensory neurons and mediates several aspects of male mating behavior. TRPP complex ciliary localization and sensory function are evolutionarily conserved. A genetic screen for C. elegans mutants with PKD-2 ciliary localization (Cil) defects led to the isolation of a mutation in the cil-1 gene. Results: Here, we report that a phosphoinositide (PI) 5-phosphatase, CIL-1, regulates TRPP complex ciliary receptor localization and sperm activation. cil-1 does not regulate the localization of other ciliary proteins, including intraflagellar transport (IFT) components, sensory receptors, or other TRP channels in different cell types. Rather, cil-1 specifically controls TRPP complex trafficking in male-specific sensory neurons and does so in a cell-autonomous fashion. In these cells, cil-1 is required for normal PI(3)P distribution, indicating that a balance between PI(3,5)P2 and PI(3)P is important for TRPP localization. cil-1 mutants are infertile because of sperm activation and motility defects. In sperm, the CIL-1 5-phosphatase and a wortmannin-sensitive PI 3-kinase act antagonistically to regulate the conversion of sessile spermatids into motile spermatozoa, implicating PI(3,4,5)P3 signaling in nematode sperm activation. Conclusion: Our studies identify the CIL-1 5-phosphatase as a key regulator of PI metabolism in cell types that are important in several aspects of male reproductive biology.",

keywords = "CELLBIO",

author = "Bae, {Young Kyung} and Eunsoo Kim and L'Hernault, {Steven W.} and Barr, {Maureen M.}",

note = "Funding Information: Nancy L'Hernault provided assistance with electron microscopy. We thank Natalia Morsci, Jinghua Hu, and members of Barr laboratory for help throughout the course of this project; John Archibald, Ching Kung, and Andy Singson for helpful discussion; David Sherwood and Joshua Ziel for critical reading of the manuscript; Barth Grant for intestinal PI markers, Shawn X.-Y. Xu for the anti-TRP-3 antibody; and Sam Ward for sharing unpublished data. Some nematode strains used in this work were provided by the Caenorhabditis Genetics Center, which is funded by the National Institutes of Health (NIH) National Center for Research Resources (NCRR), and by Shohei Mitani of the National Bioresource Project for the Nematode (Japan). This work was supported by the NIH (DK059418 and DK074746 to M.M.B.; GM082932 to S.W.L.H.), the National Science Foundation (0131532 to S.W.L.H.), and the Polycystic Kidney Disease (PKD) Foundation (to M.M.B.). ",

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T1 - The CIL-1 PI 5-Phosphatase Localizes TRP Polycystins to Cilia and Activates Sperm in C. elegans

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AU - Kim, Eunsoo

AU - L'Hernault, Steven W.

AU - Barr, Maureen M.

N1 - Funding Information: Nancy L'Hernault provided assistance with electron microscopy. We thank Natalia Morsci, Jinghua Hu, and members of Barr laboratory for help throughout the course of this project; John Archibald, Ching Kung, and Andy Singson for helpful discussion; David Sherwood and Joshua Ziel for critical reading of the manuscript; Barth Grant for intestinal PI markers, Shawn X.-Y. Xu for the anti-TRP-3 antibody; and Sam Ward for sharing unpublished data. Some nematode strains used in this work were provided by the Caenorhabditis Genetics Center, which is funded by the National Institutes of Health (NIH) National Center for Research Resources (NCRR), and by Shohei Mitani of the National Bioresource Project for the Nematode (Japan). This work was supported by the NIH (DK059418 and DK074746 to M.M.B.; GM082932 to S.W.L.H.), the National Science Foundation (0131532 to S.W.L.H.), and the Polycystic Kidney Disease (PKD) Foundation (to M.M.B.).

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N2 - Background: C. elegans male sexual behaviors include chemotaxis and response to hermaphrodites, backing, turning, vulva location, spicule insertion, and sperm transfer, culminating in cross-fertilization of hermaphrodite oocytes with male sperm. The LOV-1 and PKD-2 transient receptor potential polycystin (TRPP) complex localizes to ciliated endings of C. elegans male-specific sensory neurons and mediates several aspects of male mating behavior. TRPP complex ciliary localization and sensory function are evolutionarily conserved. A genetic screen for C. elegans mutants with PKD-2 ciliary localization (Cil) defects led to the isolation of a mutation in the cil-1 gene. Results: Here, we report that a phosphoinositide (PI) 5-phosphatase, CIL-1, regulates TRPP complex ciliary receptor localization and sperm activation. cil-1 does not regulate the localization of other ciliary proteins, including intraflagellar transport (IFT) components, sensory receptors, or other TRP channels in different cell types. Rather, cil-1 specifically controls TRPP complex trafficking in male-specific sensory neurons and does so in a cell-autonomous fashion. In these cells, cil-1 is required for normal PI(3)P distribution, indicating that a balance between PI(3,5)P2 and PI(3)P is important for TRPP localization. cil-1 mutants are infertile because of sperm activation and motility defects. In sperm, the CIL-1 5-phosphatase and a wortmannin-sensitive PI 3-kinase act antagonistically to regulate the conversion of sessile spermatids into motile spermatozoa, implicating PI(3,4,5)P3 signaling in nematode sperm activation. Conclusion: Our studies identify the CIL-1 5-phosphatase as a key regulator of PI metabolism in cell types that are important in several aspects of male reproductive biology.

AB - Background: C. elegans male sexual behaviors include chemotaxis and response to hermaphrodites, backing, turning, vulva location, spicule insertion, and sperm transfer, culminating in cross-fertilization of hermaphrodite oocytes with male sperm. The LOV-1 and PKD-2 transient receptor potential polycystin (TRPP) complex localizes to ciliated endings of C. elegans male-specific sensory neurons and mediates several aspects of male mating behavior. TRPP complex ciliary localization and sensory function are evolutionarily conserved. A genetic screen for C. elegans mutants with PKD-2 ciliary localization (Cil) defects led to the isolation of a mutation in the cil-1 gene. Results: Here, we report that a phosphoinositide (PI) 5-phosphatase, CIL-1, regulates TRPP complex ciliary receptor localization and sperm activation. cil-1 does not regulate the localization of other ciliary proteins, including intraflagellar transport (IFT) components, sensory receptors, or other TRP channels in different cell types. Rather, cil-1 specifically controls TRPP complex trafficking in male-specific sensory neurons and does so in a cell-autonomous fashion. In these cells, cil-1 is required for normal PI(3)P distribution, indicating that a balance between PI(3,5)P2 and PI(3)P is important for TRPP localization. cil-1 mutants are infertile because of sperm activation and motility defects. In sperm, the CIL-1 5-phosphatase and a wortmannin-sensitive PI 3-kinase act antagonistically to regulate the conversion of sessile spermatids into motile spermatozoa, implicating PI(3,4,5)P3 signaling in nematode sperm activation. Conclusion: Our studies identify the CIL-1 5-phosphatase as a key regulator of PI metabolism in cell types that are important in several aspects of male reproductive biology.

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The CIL-1 PI 5-Phosphatase Localizes TRP Polycystins to Cilia and Activates Sperm in C. elegans

Abstract

Bibliographical note

Keywords

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