PGP-14 establishes a polar lipid permeability barrier within the C. elegans pharyngeal cuticle

Muntasir Kamal; Levon Tokmakjian; Jessica Knox; Duhyun Han; Houtan Moshiri; Lilia Magomedova; Ken C.Q. Nguyen; Hong Zheng; Andrew R. Burns; Brittany Cooke; Jessica Lacoste; May Yeo; David H. Hall; Carolyn L. Cummins; Peter J. Roy

doi:10.1371/journal.pgen.1011008

PGP-14 establishes a polar lipid permeability barrier within the C. elegans pharyngeal cuticle

Muntasir Kamal, Levon Tokmakjian, Jessica Knox, Duhyun Han, Houtan Moshiri, Lilia Magomedova, Ken C.Q. Nguyen, Hong Zheng, Andrew R. Burns, Brittany Cooke, Jessica Lacoste, May Yeo, David H. Hall, Carolyn L. Cummins, Peter J. Roy

Neuroscience

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

Abstract

The cuticles of ecdysozoan animals are barriers to material loss and xenobiotic insult. Key to this barrier is lipid content, the establishment of which is poorly understood. Here, we show that the p-glycoprotein PGP-14 functions coincidently with the sphingomyelin synthase SMS-5 to establish a polar lipid barrier within the pharyngeal cuticle of the nematode C. elegans. We show that PGP-14 and SMS-5 are coincidentally expressed in the epithelium that surrounds the anterior pharyngeal cuticle where PGP-14 localizes to the apical membrane. pgp-14 and sms-5 also peak in expression at the time of new cuticle synthesis. Loss of PGP-14 and SMS-5 dramatically reduces pharyngeal cuticle staining by Nile Red, a key marker of polar lipids, and coincidentally alters the nematode’s response to a wide-range of xenobiotics. We infer that PGP-14 exports polar lipids into the developing pharyngeal cuticle in an SMS-5-dependent manner to safeguard the nematode from environmental insult.

Original language	English (US)
Article number	e1011008
Journal	PLoS genetics
Volume	19
Issue number	11 November
DOIs	https://doi.org/10.1371/journal.pgen.1011008
State	Published - Nov 6 2023

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Molecular Biology
Genetics
Genetics(clinical)
Cancer Research

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1371/journal.pgen.1011008

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Kamal, M., Tokmakjian, L., Knox, J., Han, D., Moshiri, H., Magomedova, L., Nguyen, K. C. Q., Zheng, H., Burns, A. R., Cooke, B., Lacoste, J., Yeo, M., Hall, D. H., Cummins, C. L., & Roy, P. J. (2023). PGP-14 establishes a polar lipid permeability barrier within the C. elegans pharyngeal cuticle. PLoS genetics, 19(11 November), Article e1011008. https://doi.org/10.1371/journal.pgen.1011008

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title = "PGP-14 establishes a polar lipid permeability barrier within the C. elegans pharyngeal cuticle",

abstract = "The cuticles of ecdysozoan animals are barriers to material loss and xenobiotic insult. Key to this barrier is lipid content, the establishment of which is poorly understood. Here, we show that the p-glycoprotein PGP-14 functions coincidently with the sphingomyelin synthase SMS-5 to establish a polar lipid barrier within the pharyngeal cuticle of the nematode C. elegans. We show that PGP-14 and SMS-5 are coincidentally expressed in the epithelium that surrounds the anterior pharyngeal cuticle where PGP-14 localizes to the apical membrane. pgp-14 and sms-5 also peak in expression at the time of new cuticle synthesis. Loss of PGP-14 and SMS-5 dramatically reduces pharyngeal cuticle staining by Nile Red, a key marker of polar lipids, and coincidentally alters the nematode{\textquoteright}s response to a wide-range of xenobiotics. We infer that PGP-14 exports polar lipids into the developing pharyngeal cuticle in an SMS-5-dependent manner to safeguard the nematode from environmental insult.",

author = "Muntasir Kamal and Levon Tokmakjian and Jessica Knox and Duhyun Han and Houtan Moshiri and Lilia Magomedova and Nguyen, {Ken C.Q.} and Hong Zheng and Burns, {Andrew R.} and Brittany Cooke and Jessica Lacoste and May Yeo and Hall, {David H.} and Cummins, {Carolyn L.} and Roy, {Peter J.}",

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AU - Kamal, Muntasir

AU - Tokmakjian, Levon

AU - Knox, Jessica

AU - Han, Duhyun

AU - Moshiri, Houtan

AU - Magomedova, Lilia

AU - Nguyen, Ken C.Q.

AU - Zheng, Hong

AU - Burns, Andrew R.

AU - Cooke, Brittany

AU - Lacoste, Jessica

AU - Yeo, May

AU - Hall, David H.

AU - Cummins, Carolyn L.

AU - Roy, Peter J.

PY - 2023/11/6

Y1 - 2023/11/6

N2 - The cuticles of ecdysozoan animals are barriers to material loss and xenobiotic insult. Key to this barrier is lipid content, the establishment of which is poorly understood. Here, we show that the p-glycoprotein PGP-14 functions coincidently with the sphingomyelin synthase SMS-5 to establish a polar lipid barrier within the pharyngeal cuticle of the nematode C. elegans. We show that PGP-14 and SMS-5 are coincidentally expressed in the epithelium that surrounds the anterior pharyngeal cuticle where PGP-14 localizes to the apical membrane. pgp-14 and sms-5 also peak in expression at the time of new cuticle synthesis. Loss of PGP-14 and SMS-5 dramatically reduces pharyngeal cuticle staining by Nile Red, a key marker of polar lipids, and coincidentally alters the nematode’s response to a wide-range of xenobiotics. We infer that PGP-14 exports polar lipids into the developing pharyngeal cuticle in an SMS-5-dependent manner to safeguard the nematode from environmental insult.

AB - The cuticles of ecdysozoan animals are barriers to material loss and xenobiotic insult. Key to this barrier is lipid content, the establishment of which is poorly understood. Here, we show that the p-glycoprotein PGP-14 functions coincidently with the sphingomyelin synthase SMS-5 to establish a polar lipid barrier within the pharyngeal cuticle of the nematode C. elegans. We show that PGP-14 and SMS-5 are coincidentally expressed in the epithelium that surrounds the anterior pharyngeal cuticle where PGP-14 localizes to the apical membrane. pgp-14 and sms-5 also peak in expression at the time of new cuticle synthesis. Loss of PGP-14 and SMS-5 dramatically reduces pharyngeal cuticle staining by Nile Red, a key marker of polar lipids, and coincidentally alters the nematode’s response to a wide-range of xenobiotics. We infer that PGP-14 exports polar lipids into the developing pharyngeal cuticle in an SMS-5-dependent manner to safeguard the nematode from environmental insult.

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PGP-14 establishes a polar lipid permeability barrier within the C. elegans pharyngeal cuticle

Abstract

ASJC Scopus subject areas

UN SDGs

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