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Pelota regulates epidermal differentiation by modulating BMP and PI3K/AKT signaling pathways

Pelota regulates epidermal differentiation by modulating BMP and PI3K/AKT signaling pathways
Pelota regulates epidermal differentiation by modulating BMP and PI3K/AKT signaling pathways

The depletion of evolutionarily conserved pelota protein causes impaired differentiation of embryonic and spermatogonial stem cells. In this study, we show that temporal deletion of pelota protein before epidermal barrier acquisition leads to neonatal lethality due to perturbations in permeability barrier formation. Further analysis indicated that this phenotype is a result of failed processing of profilaggrin into filaggrin monomers, which promotes the formation of a protective epidermal layer. Molecular analyses showed that pelota protein negatively regulates the activities of bone morphogenetic protein and phosphoinositide 3-kinase (PI3K)/protein kinase B (AKT) signaling pathways in the epidermis. To address whether elevated activities of bone morphogenetic protein and PI3K/AKT signaling pathways were the cause for the perturbed epidermal barrier in Pelo-deficient mice, we made use of organotypic cultures of skin explants from control and mutant embryos at embryonic day 15.5. Inhibition of PI3K/AKT signaling did not significantly affect the bone morphogenetic protein activity. However, inhibition of bone morphogenetic protein signaling caused a significant attenuation of PI3K/AKT activity in mutant skin and, more interestingly, the restoration of profilaggrin processing and normal epidermal barrier function. Therefore, increased activity of the PI3K/AKT signaling pathway in Pelo-deficient skin might conflict with the dephosphorylation of profilaggrin and thereby affect its proper processing into filaggrin monomers and ultimately the epidermal differentiation.

Alleles, Animals, Body Weight, Bone Morphogenetic Proteins/metabolism, Cell Cycle Proteins/metabolism, Cell Differentiation, Cell Proliferation, Endonucleases, Epidermis/metabolism, Female, Filaggrin Proteins, Gene Deletion, Gene Expression Regulation, Developmental, Intermediate Filament Proteins/metabolism, Keratinocytes/cytology, Mice, Mice, Knockout, Microfilament Proteins/metabolism, Microscopy, Electron, Transmission, Permeability, Phosphatidylinositol 3-Kinases/metabolism, Phosphorylation, Proto-Oncogene Proteins c-akt/metabolism, Signal Transduction
0022-202X
1664-1671
Elkenani, Manar
c28f50d8-b9dd-445f-824f-f9c532079a03
Nyamsuren, Gunsmaa
84c93f64-9bc0-4eef-83a3-042a76838705
Raju, Priyadharsini
8380f0f3-3f38-4e34-a7a4-868e180a8a77
Liakath-Ali, Kifayathullah
8d5a020c-e976-4901-9195-68f4bc0de74e
Hamdaoui, Aicha
64d272d5-7952-4def-9fe3-82745ccbb9a7
Kata, Aleksandra
28034ddf-d474-4b55-86a1-18d82b86f8be
Dressel, Ralf
4fa404ce-9474-4032-a24d-3617ff97025e
Klonisch, Thomas
3553a615-a5a3-4d52-97c8-b565629087de
Watt, Fiona M.
24fff937-94b0-4127-8cbb-e8bd6e01fa29
Engel, Wolfgang
8ef6f39d-b6c7-49d1-9c5a-94ba43ecf127
Thliveris, James A.
66af077f-2dbd-4a6b-a21b-4a0711092629
Krishna Pantakani, D.V.
d07ff6a0-ee73-48d3-be62-7b066d32d9db
Adham, Ibrahim M.
bc85d396-ba08-4bee-8416-1cf6b8335341
Elkenani, Manar
c28f50d8-b9dd-445f-824f-f9c532079a03
Nyamsuren, Gunsmaa
84c93f64-9bc0-4eef-83a3-042a76838705
Raju, Priyadharsini
8380f0f3-3f38-4e34-a7a4-868e180a8a77
Liakath-Ali, Kifayathullah
8d5a020c-e976-4901-9195-68f4bc0de74e
Hamdaoui, Aicha
64d272d5-7952-4def-9fe3-82745ccbb9a7
Kata, Aleksandra
28034ddf-d474-4b55-86a1-18d82b86f8be
Dressel, Ralf
4fa404ce-9474-4032-a24d-3617ff97025e
Klonisch, Thomas
3553a615-a5a3-4d52-97c8-b565629087de
Watt, Fiona M.
24fff937-94b0-4127-8cbb-e8bd6e01fa29
Engel, Wolfgang
8ef6f39d-b6c7-49d1-9c5a-94ba43ecf127
Thliveris, James A.
66af077f-2dbd-4a6b-a21b-4a0711092629
Krishna Pantakani, D.V.
d07ff6a0-ee73-48d3-be62-7b066d32d9db
Adham, Ibrahim M.
bc85d396-ba08-4bee-8416-1cf6b8335341

Elkenani, Manar, Nyamsuren, Gunsmaa, Raju, Priyadharsini, Liakath-Ali, Kifayathullah, Hamdaoui, Aicha, Kata, Aleksandra, Dressel, Ralf, Klonisch, Thomas, Watt, Fiona M., Engel, Wolfgang, Thliveris, James A., Krishna Pantakani, D.V. and Adham, Ibrahim M. (2016) Pelota regulates epidermal differentiation by modulating BMP and PI3K/AKT signaling pathways. Journal of Investigative Dermatology, 136 (8), 1664-1671. (doi:10.1016/j.jid.2016.04.020).

Record type: Article

Abstract

The depletion of evolutionarily conserved pelota protein causes impaired differentiation of embryonic and spermatogonial stem cells. In this study, we show that temporal deletion of pelota protein before epidermal barrier acquisition leads to neonatal lethality due to perturbations in permeability barrier formation. Further analysis indicated that this phenotype is a result of failed processing of profilaggrin into filaggrin monomers, which promotes the formation of a protective epidermal layer. Molecular analyses showed that pelota protein negatively regulates the activities of bone morphogenetic protein and phosphoinositide 3-kinase (PI3K)/protein kinase B (AKT) signaling pathways in the epidermis. To address whether elevated activities of bone morphogenetic protein and PI3K/AKT signaling pathways were the cause for the perturbed epidermal barrier in Pelo-deficient mice, we made use of organotypic cultures of skin explants from control and mutant embryos at embryonic day 15.5. Inhibition of PI3K/AKT signaling did not significantly affect the bone morphogenetic protein activity. However, inhibition of bone morphogenetic protein signaling caused a significant attenuation of PI3K/AKT activity in mutant skin and, more interestingly, the restoration of profilaggrin processing and normal epidermal barrier function. Therefore, increased activity of the PI3K/AKT signaling pathway in Pelo-deficient skin might conflict with the dephosphorylation of profilaggrin and thereby affect its proper processing into filaggrin monomers and ultimately the epidermal differentiation.

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More information

Accepted/In Press date: 4 April 2016
e-pub ahead of print date: 7 May 2016
Published date: 20 July 2016
Keywords: Alleles, Animals, Body Weight, Bone Morphogenetic Proteins/metabolism, Cell Cycle Proteins/metabolism, Cell Differentiation, Cell Proliferation, Endonucleases, Epidermis/metabolism, Female, Filaggrin Proteins, Gene Deletion, Gene Expression Regulation, Developmental, Intermediate Filament Proteins/metabolism, Keratinocytes/cytology, Mice, Mice, Knockout, Microfilament Proteins/metabolism, Microscopy, Electron, Transmission, Permeability, Phosphatidylinositol 3-Kinases/metabolism, Phosphorylation, Proto-Oncogene Proteins c-akt/metabolism, Signal Transduction

Identifiers

Local EPrints ID: 491576
URI: http://eprints.soton.ac.uk/id/eprint/491576
ISSN: 0022-202X
PURE UUID: 6dbaa8df-14c9-46f1-ba71-1cecba3b3d00
ORCID for Kifayathullah Liakath-Ali: ORCID iD orcid.org/0000-0001-9047-7424

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Date deposited: 27 Jun 2024 16:36
Last modified: 28 Jun 2024 02:09

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Contributors

Author: Manar Elkenani
Author: Gunsmaa Nyamsuren
Author: Priyadharsini Raju
Author: Kifayathullah Liakath-Ali ORCID iD
Author: Aicha Hamdaoui
Author: Aleksandra Kata
Author: Ralf Dressel
Author: Thomas Klonisch
Author: Fiona M. Watt
Author: Wolfgang Engel
Author: James A. Thliveris
Author: D.V. Krishna Pantakani
Author: Ibrahim M. Adham

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