Palmitoylation regulates epidermal homeostasis and hair follicle differentiation
Palmitoylation is a key post-translational modification mediated by a family of DHHC-containing palmitoyl acyl-transferases (PATs). Unlike other lipid modifications, palmitoylation is reversible and thus often regulates dynamic protein interactions. We find that the mouse hair loss mutant, depilated...
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| Published in | PLoS genetics Vol. 5; no. 11; p. e1000748 |
|---|---|
| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.11.2009
Public Library of Science (PLoS) |
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| Online Access | Get full text |
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| Abstract | Palmitoylation is a key post-translational modification mediated by a family of DHHC-containing palmitoyl acyl-transferases (PATs). Unlike other lipid modifications, palmitoylation is reversible and thus often regulates dynamic protein interactions. We find that the mouse hair loss mutant, depilated, (dep) is due to a single amino acid deletion in the PAT, Zdhhc21, resulting in protein mislocalization and loss of palmitoylation activity. We examined expression of Zdhhc21 protein in skin and find it restricted to specific hair lineages. Loss of Zdhhc21 function results in delayed hair shaft differentiation, at the site of expression of the gene, but also leads to hyperplasia of the interfollicular epidermis (IFE) and sebaceous glands, distant from the expression site. The specific delay in follicle differentiation is associated with attenuated anagen propagation and is reflected by decreased levels of Lef1, nuclear beta-catenin, and Foxn1 in hair shaft progenitors. In the thickened basal compartment of mutant IFE, phospho-ERK and cell proliferation are increased, suggesting increased signaling through EGFR or integrin-related receptors, with a parallel reduction in expression of the key differentiation factor Gata3. We show that the Src-family kinase, Fyn, involved in keratinocyte differentiation, is a direct palmitoylation target of Zdhhc21 and is mislocalized in mutant follicles. This study is the first to demonstrate a key role for palmitoylation in regulating developmental signals in mammalian tissue homeostasis. |
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| AbstractList | Palmitoylation is a key post-translational modification mediated by a family of DHHC-containing palmitoyl acyl- transferases (PATS). Unlike other lipid modifications, palmitoylation is reversible and thus often regulates dynamic protein interactions. We find that the mouse hair loss mutant, depilated, (dep) is due to a single amino acid deletion in the PAT, Zdhhc21, resulting in protein mislocalization and loss of palmitoylation activity. We examined expression of Zdhhc21 protein in skin and find it restricted to specific hair lineages. Loss of Zdhhc21 function results in delayed hair shaft differentiation, at the site of expression of the gene, but also leads to hyperplasia of the interfollicular epidermis (IFE) and sebaceous glands, distant from the expression site. The specific delay in follicle differentiation is associated with attenuated anagen propagation and is reflected by decreased levels of Left, nuclear β-catenin, and Foxn1 in hair shaft progenitors. In the thickened basal compartment of mutant IFE, phospho-ERK and cell proliferation are increased, suggesting increased signaling through EGFR or integrin-related receptors, with a parallel reduction in expression of the key differentiation factor Gata3. We show that the Src-family kinase, Fyn, involved in keratinocyte differentiation, is a direct palmitoylation target of Zdhhc21 and is mislocalized in mutant follicles. This study is the first to demonstrate a key role for palmitoylation in regulating developmental signals in mammalian tissue homeostasis. Palmitoylation is a key post-translational modification mediated by a family of DHHC-containing palmitoyl acyl-transferases (PATs). Unlike other lipid modifications, palmitoylation is reversible and thus often regulates dynamic protein interactions. We find that the mouse hair loss mutant, depilated, (dep) is due to a single amino acid deletion in the PAT, Zdhhc21, resulting in protein mislocalization and loss of palmitoylation activity. We examined expression of Zdhhc21 protein in skin and find it restricted to specific hair lineages. Loss of Zdhhc21 function results in delayed hair shaft differentiation, at the site of expression of the gene, but also leads to hyperplasia of the interfollicular epidermis (IFE) and sebaceous glands, distant from the expression site. The specific delay in follicle differentiation is associated with attenuated anagen propagation and is reflected by decreased levels of Lef1, nuclear I2-catenin, and Foxn1 in hair shaft progenitors. In the thickened basal compartment of mutant IFE, phospho-ERK and cell proliferation are increased, suggesting increased signaling through EGFR or integrin-related receptors, with a parallel reduction in expression of the key differentiation factor Gata3. We show that the Src-family kinase, Fyn, involved in keratinocyte differentiation, is a direct palmitoylation target of Zdhhc21 and is mislocalized in mutant follicles. This study is the first to demonstrate a key role for palmitoylation in regulating developmental signals in mammalian tissue homeostasis. Author Summary During embryonic development, growth and patterning are regulated at many levels. Signals that mediate transcriptional activity, where and when genes are expressed, are a primary level of regulation. However, developmental signals can be further fine-tuned by modulating protein stability, localization, and activity via post-translational modifications. One such modification is the reversible addition of the fatty acid palmitate to proteins. This modification mediates dynamic trafficking of target proteins to specific subdomains of the cell. A large family of enzymes carries out this palmitoylation process, where each family member has specificity towards particular targets. However, the functional significance of palmitoylation during mammalian development is unclear. We present evidence of a critical role for palmitoylation during mouse development using a mutation of a specific palmitoylating enzyme, whose loss of function leads to hair loss and skin defects in depilated (dep) mice. Despite its restricted expression in hair follicles, loss of function of this enzyme results in developmental defects in nearby structures. We show that palmitoylation plays an important regulatory role in hair growth and epidermal homeostasis. Palmitoylation is a key post-translational modification mediated by a family of DHHC-containing palmitoyl acyl-transferases (PATs). Unlike other lipid modifications, palmitoylation is reversible and thus often regulates dynamic protein interactions. We find that the mouse hair loss mutant, depilated, (dep) is due to a single amino acid deletion in the PAT, Zdhhc21, resulting in protein mislocalization and loss of palmitoylation activity. We examined expression of Zdhhc21 protein in skin and find it restricted to specific hair lineages. Loss of Zdhhc21 function results in delayed hair shaft differentiation, at the site of expression of the gene, but also leads to hyperplasia of the interfollicular epidermis (IFE) and sebaceous glands, distant from the expression site. The specific delay in follicle differentiation is associated with attenuated anagen propagation and is reflected by decreased levels of Lef1, nuclear beta-catenin, and Foxn1 in hair shaft progenitors. In the thickened basal compartment of mutant IFE, phospho-ERK and cell proliferation are increased, suggesting increased signaling through EGFR or integrin-related receptors, with a parallel reduction in expression of the key differentiation factor Gata3. We show that the Src-family kinase, Fyn, involved in keratinocyte differentiation, is a direct palmitoylation target of Zdhhc21 and is mislocalized in mutant follicles. This study is the first to demonstrate a key role for palmitoylation in regulating developmental signals in mammalian tissue homeostasis. Palmitoylation is a key post-translational modification mediated by a family of DHHC-containing palmitoyl acyl-transferases (PATs). Unlike other lipid modifications, palmitoylation is reversible and thus often regulates dynamic protein interactions. We find that the mouse hair loss mutant, depilated, ( dep ) is due to a single amino acid deletion in the PAT, Zdhhc21, resulting in protein mislocalization and loss of palmitoylation activity. We examined expression of Zdhhc21 protein in skin and find it restricted to specific hair lineages. Loss of Zdhhc21 function results in delayed hair shaft differentiation, at the site of expression of the gene, but also leads to hyperplasia of the interfollicular epidermis (IFE) and sebaceous glands, distant from the expression site. The specific delay in follicle differentiation is associated with attenuated anagen propagation and is reflected by decreased levels of Lef1, nuclear β-catenin, and Foxn1 in hair shaft progenitors. In the thickened basal compartment of mutant IFE, phospho-ERK and cell proliferation are increased, suggesting increased signaling through EGFR or integrin-related receptors, with a parallel reduction in expression of the key differentiation factor Gata3. We show that the Src-family kinase, Fyn, involved in keratinocyte differentiation, is a direct palmitoylation target of Zdhhc21 and is mislocalized in mutant follicles. This study is the first to demonstrate a key role for palmitoylation in regulating developmental signals in mammalian tissue homeostasis. During embryonic development, growth and patterning are regulated at many levels. Signals that mediate transcriptional activity, where and when genes are expressed, are a primary level of regulation. However, developmental signals can be further fine-tuned by modulating protein stability, localization, and activity via post-translational modifications. One such modification is the reversible addition of the fatty acid palmitate to proteins. This modification mediates dynamic trafficking of target proteins to specific subdomains of the cell. A large family of enzymes carries out this palmitoylation process, where each family member has specificity towards particular targets. However, the functional significance of palmitoylation during mammalian development is unclear. We present evidence of a critical role for palmitoylation during mouse development using a mutation of a specific palmitoylating enzyme, whose loss of function leads to hair loss and skin defects in depilated ( dep ) mice. Despite its restricted expression in hair follicles, loss of function of this enzyme results in developmental defects in nearby structures. We show that palmitoylation plays an important regulatory role in hair growth and epidermal homeostasis. Palmitoylation is a key post-translational modification mediated by a family of DHHC-containing palmitoyl acyl-transferases (PATs). Unlike other lipid modifications, palmitoylation is reversible and thus often regulates dynamic protein interactions. We find that the mouse hair loss mutant, depilated, (dep) is due to a single amino acid deletion in the PAT, Zdhhc21, resulting in protein mislocalization and loss of palmitoylation activity. We examined expression of Zdhhc21 protein in skin and find it restricted to specific hair lineages. Loss of Zdhhc21 function results in delayed hair shaft differentiation, at the site of expression of the gene, but also leads to hyperplasia of the interfollicular epidermis (IFE) and sebaceous glands, distant from the expression site. The specific delay in follicle differentiation is associated with attenuated anagen propagation and is reflected by decreased levels of Lef1, nuclear β-catenin, and Foxn1 in hair shaft progenitors. In the thickened basal compartment of mutant IFE, phospho-ERK and cell proliferation are increased, suggesting increased signaling through EGFR or integrin-related receptors, with a parallel reduction in expression of the key differentiation factor Gata3. We show that the Src-family kinase, Fyn, involved in keratinocyte differentiation, is a direct palmitoylation target of Zdhhc21 and is mislocalized in mutant follicles. This study is the first to demonstrate a key role for palmitoylation in regulating developmental signals in mammalian tissue homeostasis. Palmitoylation is a key post-translational modification mediated by a family of DHHC-containing palmitoyl acyl-transferases (PATs). Unlike other lipid modifications, palmitoylation is reversible and thus often regulates dynamic protein interactions. We find that the mouse hair loss mutant, depilated, (dep) is due to a single amino acid deletion in the PAT, Zdhhc21, resulting in protein mislocalization and loss of palmitoylation activity. We examined expression of Zdhhc21 protein in skin and find it restricted to specific hair lineages. Loss of Zdhhc21 function results in delayed hair shaft differentiation, at the site of expression of the gene, but also leads to hyperplasia of the interfollicular epidermis (IFE) and sebaceous glands, distant from the expression site. The specific delay in follicle differentiation is associated with attenuated anagen propagation and is reflected by decreased levels of Lef1, nuclear b-catenin, and Foxn1 in hair shaft progenitors. In the thickened basal compartment of mutant IFE, phospho-ERK and cell proliferation are increased, suggesting increased signaling through EGFR or integrin-related receptors, with a parallel reduction in expression of the key differentiation factor Gata3. We show that the Src-family kinase, Fyn, involved in keratinocyte differentiation, is a direct palmitoylation target of Zdhhc21 and is mislocalized in mutant follicles. This study is the first to demonstrate a key role for palmitoylation in regulating developmental signals in mammalian tissue homeostasis. |
| Audience | Academic |
| Author | Tsutsumi, Ryouhei Porter, Rebecca M Fukata, Yuko Mill, Pleasantine Fukata, Masaki Lee, Angela W S Smyth, Ian Keighren, Margaret McKie, Lisa Jackson, Ian J |
| AuthorAffiliation | 2 National Institute for Physiological Sciences, National Institutes of Natural Sciences, Okazaki, Japan 3 Precursory Research for Embryonic Science and Technology, Japan Science and Technology Agency, Chiyoda, Tokyo, Japan Harvard Medical School, United States of America 1 Medical Research Council, Human Genetics Unit, Edinburgh, United Kingdom 5 Cutaneous Developmental Biology Lab, Department of Biochemistry and Molecular Biology, Department of Anatomy and Developmental Biology, Monash University, Melbourne, Australia 4 Department of Dermatology, School of Medicine, Cardiff University, Cardiff, United Kingdom |
| AuthorAffiliation_xml | – name: 2 National Institute for Physiological Sciences, National Institutes of Natural Sciences, Okazaki, Japan – name: 3 Precursory Research for Embryonic Science and Technology, Japan Science and Technology Agency, Chiyoda, Tokyo, Japan – name: 5 Cutaneous Developmental Biology Lab, Department of Biochemistry and Molecular Biology, Department of Anatomy and Developmental Biology, Monash University, Melbourne, Australia – name: 1 Medical Research Council, Human Genetics Unit, Edinburgh, United Kingdom – name: 4 Department of Dermatology, School of Medicine, Cardiff University, Cardiff, United Kingdom – name: Harvard Medical School, United States of America |
| Author_xml | – sequence: 1 givenname: Pleasantine surname: Mill fullname: Mill, Pleasantine organization: Medical Research Council, Human Genetics Unit, Edinburgh, United Kingdom – sequence: 2 givenname: Angela W S surname: Lee fullname: Lee, Angela W S – sequence: 3 givenname: Yuko surname: Fukata fullname: Fukata, Yuko – sequence: 4 givenname: Ryouhei surname: Tsutsumi fullname: Tsutsumi, Ryouhei – sequence: 5 givenname: Masaki surname: Fukata fullname: Fukata, Masaki – sequence: 6 givenname: Margaret surname: Keighren fullname: Keighren, Margaret – sequence: 7 givenname: Rebecca M surname: Porter fullname: Porter, Rebecca M – sequence: 8 givenname: Lisa surname: McKie fullname: McKie, Lisa – sequence: 9 givenname: Ian surname: Smyth fullname: Smyth, Ian – sequence: 10 givenname: Ian J surname: Jackson fullname: Jackson, Ian J |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/19956733$$D View this record in MEDLINE/PubMed https://www.osti.gov/servlets/purl/1627280$$D View this record in Osti.gov |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2009 Public Library of Science Mill et al. 2009 2009 Mill et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Mill P, Lee AWS, Fukata Y, Tsutsumi R, Fukata M, et al. (2009) Palmitoylation Regulates Epidermal Homeostasis and Hair Follicle Differentiation. PLoS Genet 5(11): e1000748. doi:10.1371/journal.pgen.1000748 |
| Copyright_xml | – notice: COPYRIGHT 2009 Public Library of Science – notice: Mill et al. 2009 – notice: 2009 Mill et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Mill P, Lee AWS, Fukata Y, Tsutsumi R, Fukata M, et al. (2009) Palmitoylation Regulates Epidermal Homeostasis and Hair Follicle Differentiation. PLoS Genet 5(11): e1000748. doi:10.1371/journal.pgen.1000748 |
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| Notes | ObjectType-Article-2 SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 23 ObjectType-Article-1 ObjectType-Feature-2 USDOE Office of Science (SC), Fusion Energy Sciences (FES) Current address: (AWSL) Medical Research Council, Mammalian Genetics Unit, Harwell Science and Innovation Campus, London, United Kingdom These authors are joint senior authors on this work. Conceived and designed the experiments: PM AWSL MF IS IJJ. Performed the experiments: PM AWSL YF RT MK LM IS. Analyzed the data: PM AWSL MF RMP IS. Wrote the paper: PM IJJ. |
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| SubjectTerms | Acyltransferases - genetics Animals BASIC BIOLOGICAL SCIENCES Cell Differentiation Councils Dermatology Developmental Biology/Molecular Development Developmental Biology/Organogenesis Developmental Biology/Stem Cells Embryonic development Epidermal Cells Fatty acids Frameshift Mutation Genetics & Heredity Genetics and Genomics/Functional Genomics Genetics and Genomics/Gene Function Hair Follicle - cytology Homeostasis Kinases Lipids Lipoylation - physiology Mice Palmitoylation Post-translational modification Propagation Protein Processing, Post-Translational Proteins Proto-Oncogene Proteins c-fyn - metabolism Rodents |
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| Title | Palmitoylation regulates epidermal homeostasis and hair follicle differentiation |
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