Palmitoylation Regulates Epidermal Homeostasis and Hair Follicle Differentiation

Mill, Pleasantine; Lee, Angela W.  S.; Fukata, Yuko; Tsutsumi, Ryouhei; Fukata, Masaki; Keighren, Margaret; Porter, Rebecca M.; McKie, Lisa; Smyth, Ian; Jackson, Ian J.

doi:10.1371/journal.pgen.1000748

Title: Palmitoylation Regulates Epidermal Homeostasis and Hair Follicle Differentiation

Journal Article · 26 November 2009 · PLoS Genetics

DOI: https://doi.org/10.1371/journal.pgen.1000748 · OSTI ID:1627280

Mill, Pleasantine ^[1]; Lee, Angela W. S. ^[2]; Fukata, Yuko ^[3]; Tsutsumi, Ryouhei ^[4]; Fukata, Masaki ^[3]; Keighren, Margaret ^[2]; Porter, Rebecca M. ^[5]; McKie, Lisa ^[2]; Smyth, Ian ^[6]; Jackson, Ian J. ^[2]

Medical Research Council, Edinburgh, Scotland (United Kingdom). Human Genetics Unit; DOE/OSTI
Medical Research Council, Edinburgh, Scotland (United Kingdom). Human Genetics Unit
National Insts. of Natural Sciences, Okazaki (Japan). National Inst. for Physiological Sciences; Japan Science and Technology Agency, Tokyo (Japan). Precursory Research for Embryonic Science and Technology
National Insts. of Natural Sciences, Okazaki (Japan). National Inst. for Physiological Sciences
Cardiff Univ. (United Kingdom). School of Medicine. Dept. of Dermatology
Medical Research Council, Edinburgh, Scotland (United Kingdom). Human Genetics Unit; Monash Univ., Melbourne, VIC (Australia). Dept. of Anatomy and Developmental Biology. Dept. of biochemistry and Molecular Biology. Cutaneous Developmental Biology Lab.

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Medical Research Council, Edinburgh, Scotland (United Kingdom). Human Genetics Unit

Sponsoring Organization:: USDOE Office of Science (SC), Fusion Energy Sciences (FES)

OSTI ID:: 1627280

Journal Information:: PLoS Genetics, Journal Name: PLoS Genetics Journal Issue: 11 Vol. 5; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (91)

Wntless, a Conserved Membrane Protein Dedicated to the Secretion of Wnt Proteins from Signaling Cells Bänziger, Carla; Soldini, Davide; Schütt, Corina Cell, Vol. 125, Issue 3 https://doi.org/10.1016/j.cell.2006.02.049	journal	May 2006
Global Analysis of Protein Palmitoylation in Yeast Roth, Amy F.; Wan, Junmei; Bailey, Aaron O. Cell, Vol. 125, Issue 5 https://doi.org/10.1016/j.cell.2006.03.042	journal	June 2006
Differential Regulation of AMPA Receptor Subunit Trafficking by Palmitoylation of Two Distinct Sites Hayashi, Takashi; Rumbaugh, Gavin; Huganir, Richard L. Neuron, Vol. 47, Issue 5 https://doi.org/10.1016/j.neuron.2005.06.035	journal	September 2005
Systematic screening for palmitoyl transferase activity of the DHHC protein family in mammalian cells Fukata, Yuko; Iwanaga, Tsuyoshi; Fukata, Masaki Methods, Vol. 40, Issue 2 https://doi.org/10.1016/j.ymeth.2006.05.015	journal	October 2006
Characterization of Wnt gene expression in developing and postnatal hair follicles and identification of Wnt5a as a target of Sonic hedgehog in hair follicle morphogenesis Reddy, Seshamma; Andl, Thomas; Bagasra, Alexander Mechanisms of Development, Vol. 107, Issue 1-2 https://doi.org/10.1016/s0925-4773(01)00452-x	journal	September 2001
A PKC-η/Fyn-Dependent Pathway Leading to Keratinocyte Growth Arrest and Differentiation Cabodi, Sara; Calautti, Enzo; Talora, Claudio Molecular Cell, Vol. 6, Issue 5 https://doi.org/10.1016/s1097-2765(00)00110-6	journal	November 2000
A single type of progenitor cell maintains normal epidermis Clayton, Elizabeth; Doupé, David P.; Klein, Allon M. Nature, Vol. 446, Issue 7132 https://doi.org/10.1038/nature05574	journal	February 2007
Palmitoylation-dependent neurodevelopmental deficits in a mouse model of 22q11 microdeletion Mukai, Jun; Dhilla, Alefiya; Drew, Liam J. Nature Neuroscience, Vol. 11, Issue 11 https://doi.org/10.1038/nn.2204	journal	October 2008
The extracellular matrix gene Frem1 is essential for the normal adhesion of the embryonic epidermis Smyth, I.; Du, X.; Taylor, M. S. Proceedings of the National Academy of Sciences, Vol. 101, Issue 37 https://doi.org/10.1073/pnas.0402760101	journal	September 2004
Genomic anatomy of the Tyrp1 (brown) deletion complex Smyth, I. M.; Wilming, L.; Lee, A. W. Proceedings of the National Academy of Sciences, Vol. 103, Issue 10 https://doi.org/10.1073/pnas.0600199103	journal	February 2006
IKK is a critical coregulator of a Smad4-independent TGF -Smad2/3 signaling pathway that controls keratinocyte differentiation Descargues, P.; Sil, A. K.; Sano, Y. Proceedings of the National Academy of Sciences, Vol. 105, Issue 7 https://doi.org/10.1073/pnas.0712044105	journal	February 2008
Subcellular Distribution of Envoplakin and Periplakin DiColandrea, Teresa; Karashima, Tadashi; Määttä, Arto Journal of Cell Biology, Vol. 151, Issue 3 https://doi.org/10.1083/jcb.151.3.573	journal	October 2000
A developmental conundrum DasGupta, Ramanuj; Rhee, Horace; Fuchs, Elaine Journal of Cell Biology, Vol. 158, Issue 2 https://doi.org/10.1083/jcb.200204134	journal	July 2002
Identification of Golgi-localized acyl transferases that palmitoylate and regulate endothelial nitric oxide synthase Fernández-Hernando, Carlos; Fukata, Masaki; Bernatchez, Pascal N. Journal of Cell Biology, Vol. 174, Issue 3 https://doi.org/10.1083/jcb.200601051	journal	July 2006
Mutations in ZDHHC9, Which Encodes a Palmitoyltransferase of NRAS and HRAS, Cause X-Linked Mental Retardation Associated with a Marfanoid Habitus Raymond, F. Lucy; Tarpey, Patrick S.; Edkins, Sarah The American Journal of Human Genetics, Vol. 80, Issue 5 https://doi.org/10.1086/513609	journal	May 2007
Molecular genetics of the brown (b)-locus region of mouse chromosome 4. II. Complementation analyses of lethal brown deletions. Rinchik, E. M. Genetics, Vol. 137, Issue 3 https://doi.org/10.1093/genetics/137.3.855	journal	July 1994
fyn tyrosine kinase is involved in keratinocyte differentiation control. Calautti, E.; Missero, C.; Stein, P. L. Genes & Development, Vol. 9, Issue 18 https://doi.org/10.1101/gad.9.18.2279	journal	September 1995
Differential expression of nitric oxide synthases in human scalp epidermal and hair follicle pigmentary units: implications for regulation of melanogenesis Sowden, H. M.; Naseem, K. M.; Tobin, D. J. British Journal of Dermatology, Vol. 153, Issue 2 https://doi.org/10.1111/j.1365-2133.2005.06718.x	journal	August 2005
Palmitoylation Controls Recycling in Lysosomal Sorting and Trafficking McCormick, Peter J.; Dumaresq-Doiron, Karine; Pluviose, Anne-Sophie Traffic, Vol. 9, Issue 11 https://doi.org/10.1111/j.1600-0854.2008.00814.x	journal	November 2008
Identification of G Protein α Subunit-Palmitoylating Enzyme Tsutsumi, Ryouhei; Fukata, Yuko; Noritake, Jun Molecular and Cellular Biology, Vol. 29, Issue 2 https://doi.org/10.1128/mcb.01144-08	journal	November 2008
Palmitoylation of Intracellular Signaling Proteins: Regulation and Function Smotrys, Jessica E.; Linder, Maurine E. Annual Review of Biochemistry, Vol. 73, Issue 1 https://doi.org/10.1146/annurev.biochem.73.011303.073954	journal	June 2004
A role for mitogen-activated protein kinase activation by integrins in the pathogenesis of psoriasis Haase, Ingo; Hobbs, Robin M.; Romero, M. Rosario Journal of Clinical Investigation, Vol. 108, Issue 4 https://doi.org/10.1172/jci12153	journal	August 2001
ZDHHC8as a candidate gene for schizophrenia: Analysis of a putative functional intronic marker in case-control and family-based association studies Faul, Thomas; Gawlik, Micha; Bauer, Martin BMC Psychiatry, Vol. 5, Issue 1 https://doi.org/10.1186/1471-244x-5-35	journal	October 2005
Epithelial Bmpr1a regulates differentiation and proliferation in postnatal hair follicles and is essential for tooth development Andl, Thomas; Ahn, Kyung; Kairo, Alladin Development, Vol. 131, Issue 10 https://doi.org/10.1242/dev.01125	journal	May 2004
Patterned acquisition of skin barrier function during development Hardman, M. J.; Sisi, P.; Banbury, D. N. Development, Vol. 125, Issue 8 https://doi.org/10.1242/dev.125.8.1541	journal	April 1998
Protein Palmitoylation Regulates Osteoblast Differentiation through BMP-Induced Osterix Expression Leong, Wai Fook; Zhou, Tielin; Lim, Gek Liang PLoS ONE, Vol. 4, Issue 1 https://doi.org/10.1371/journal.pone.0004135	journal	January 2009
Thecerberus-related gene,Cerr1, is not essential for mouse head formation Shawlot, William; Min Deng, Jian; Wakamiya, Maki genesis, Vol. 26, Issue 4 https://doi.org/10.1002/(SICI)1526-968X(200004)26:4<253::AID-GENE60>3.0.CO;2-D	journal	April 2000
Targeted insertion of alacZ reporter gene into the mouseCer1 locus reveals complex and dynamic expression during embryogenesis Stanley, Edouard G.; Biben, Christine; Allison, Janette genesis, Vol. 26, Issue 4 https://doi.org/10.1002/(SICI)1526-968X(200004)26:4<259::AID-GENE70>3.0.CO;2-V	journal	April 2000
Cerberus-like is a secreted BMP and nodal antagonist not essential for mouse development Belo, Jos� Ant�nio; Bachiller, D.; Agius, E. genesis, Vol. 26, Issue 4 https://doi.org/10.1002/(SICI)1526-968X(200004)26:4<265::AID-GENE80>3.0.CO;2-4	journal	April 2000
Isolation of a novel gene on 8p21.3–22 whose expression is reduced significantly in human colorectal cancers with liver metastasis Oyama, Tsukasa; Miyoshi, Yasuo; Koyama, Kumiko Genes, Chromosomes and Cancer, Vol. 29, Issue 1 https://doi.org/10.1002/1098-2264(2000)9999:9999<::AID-GCC1001>3.0.CO;2-#	journal	September 2000
A comparative transcript map and candidates for mutant phenotypes in the Tyrp1 (brown) deletion complex homologous to human 9p21-23 Simpson, Eleanor H.; Suffolk, Ruth; Bell, Julia A. Mammalian Genome, Vol. 11, Issue 1 https://doi.org/10.1007/s003350010011	journal	January 2000
De Novo Hair Follicle Morphogenesis and Hair Tumors in Mice Expressing a Truncated β-Catenin in Skin Gat, Uri; DasGupta, Ramanuj; Degenstein, Linda Cell, Vol. 95, Issue 5 https://doi.org/10.1016/S0092-8674(00)81631-1	journal	November 1998
Synaptic Strength Regulated by Palmitate Cycling on PSD-95 El-Husseini, Alaa El-Din; Schnell, Eric; Dakoji, Srikanth Cell, Vol. 108, Issue 6 https://doi.org/10.1016/S0092-8674(02)00683-9	journal	March 2002
Characterization of Wnt gene expression in developing and postnatal hair follicles and identification of Wnt5a as a target of Sonic hedgehog in hair follicle morphogenesis Reddy, Seshamma; Andl, Thomas; Bagasra, Alexander Mechanisms of Development, Vol. 107, Issue 1-2 https://doi.org/10.1016/S0925-4773(01)00452-X	journal	September 2001
A PKC-η/Fyn-Dependent Pathway Leading to Keratinocyte Growth Arrest and Differentiation Cabodi, Sara; Calautti, Enzo; Talora, Claudio Molecular Cell, Vol. 6, Issue 5 https://doi.org/10.1016/S1097-2765(00)00110-6	journal	November 2000
Self-Renewal, Multipotency, and the Existence of Two Cell Populations within an Epithelial Stem Cell Niche Blanpain, Cedric; Lowry, William E.; Geoghegan, Andrea Cell, Vol. 118, Issue 5 https://doi.org/10.1016/j.cell.2004.08.012	journal	September 2004
Wntless, a Conserved Membrane Protein Dedicated to the Secretion of Wnt Proteins from Signaling Cells Bänziger, Carla; Soldini, Davide; Schütt, Corina Cell, Vol. 125, Issue 3 https://doi.org/10.1016/j.cell.2006.02.049	journal	May 2006
Global Analysis of Protein Palmitoylation in Yeast Roth, Amy F.; Wan, Junmei; Bailey, Aaron O. Cell, Vol. 125, Issue 5 https://doi.org/10.1016/j.cell.2006.03.042	journal	June 2006
The DHHC Palmitoyltransferase Approximated Regulates Fat Signaling and Dachs Localization and Activity Matakatsu, Hitoshi; Blair, Seth S. Current Biology, Vol. 18, Issue 18 https://doi.org/10.1016/j.cub.2008.07.067	journal	September 2008
β-Catenin and Hedgehog Signal Strength Can Specify Number and Location of Hair Follicles in Adult Epidermis without Recruitment of Bulge Stem Cells Silva-Vargas, Violeta; Lo Celso, Cristina; Giangreco, Adam Developmental Cell, Vol. 9, Issue 1 https://doi.org/10.1016/j.devcel.2005.04.013	journal	July 2005
Identification of PSD-95 Palmitoylating Enzymes Fukata, Masaki; Fukata, Yuko; Adesnik, Hillel Neuron, Vol. 44, Issue 6 https://doi.org/10.1016/j.neuron.2004.12.005	journal	December 2004
Differential Regulation of AMPA Receptor Subunit Trafficking by Palmitoylation of Two Distinct Sites Hayashi, Takashi; Rumbaugh, Gavin; Huganir, Richard L. Neuron, Vol. 47, Issue 5 https://doi.org/10.1016/j.neuron.2005.06.035	journal	September 2005
Systematic screening for palmitoyl transferase activity of the DHHC protein family in mammalian cells Fukata, Yuko; Iwanaga, Tsuyoshi; Fukata, Masaki Methods, Vol. 40, Issue 2 https://doi.org/10.1016/j.ymeth.2006.05.015	journal	October 2006
Wnt proteins are lipid-modified and can act as stem cell growth factors Willert, Karl; Brown, Jeffrey D.; Danenberg, Esther Nature, Vol. 423, Issue 6938 https://doi.org/10.1038/nature01611	journal	April 2003
A single type of progenitor cell maintains normal epidermis Clayton, Elizabeth; Doupé, David P.; Klein, Allon M. Nature, Vol. 446, Issue 7132 https://doi.org/10.1038/nature05574	journal	February 2007
Scratching the surface of skin development Fuchs, Elaine Nature, Vol. 445, Issue 7130 https://doi.org/10.1038/nature05659	journal	February 2007
Neural palmitoyl-proteomics reveals dynamic synaptic palmitoylation Kang, Rujun; Wan, Junmei; Arstikaitis, Pamela Nature, Vol. 456, Issue 7224 https://doi.org/10.1038/nature07605	journal	December 2008
Evidence that the gene encoding ZDHHC8 contributes to the risk of schizophrenia Mukai, Jun; Liu, Hui; Burt, Rachel A. Nature Genetics, Vol. 36, Issue 7 https://doi.org/10.1038/ng1375	journal	June 2004
Palmitoylation-dependent neurodevelopmental deficits in a mouse model of 22q11 microdeletion Mukai, Jun; Dhilla, Alefiya; Drew, Liam J. Nature Neuroscience, Vol. 11, Issue 11 https://doi.org/10.1038/nn.2204	journal	October 2008
Loss of ZDHHC15 expression in a woman with a balanced translocation t(X;15)(q13.3;cen) and severe mental retardation Mansouri, Mahmoud Reza; Marklund, Lena; Gustavsson, Peter European Journal of Human Genetics, Vol. 13, Issue 8 https://doi.org/10.1038/sj.ejhg.5201445	journal	May 2005
Huntingtin interacting protein 14 is an oncogenic human protein: palmitoyl acyltransferase Ducker, Charles E.; Stettler, Erin M.; French, Kevin J. Oncogene, Vol. 23, Issue 57 https://doi.org/10.1038/sj.onc.1208171	journal	October 2004
A Comprehensive Guide for the Accurate Classification of Murine Hair Follicles in Distinct Hair Cycle Stages Müller-Röver, Sven; Foitzik, Kerstin; Paus, Ralf Journal of Investigative Dermatology, Vol. 117, Issue 1 https://doi.org/10.1046/j.0022-202x.2001.01377.x	journal	July 2001
Bone Morphogenetic Proteins and Their Antagonists in Skin and Hair Follicle Biology Botchkarev, Vladimir A. Journal of Investigative Dermatology, Vol. 120, Issue 1 https://doi.org/10.1046/j.1523-1747.2003.12002.x	journal	January 2003
The extracellular matrix gene Frem1 is essential for the normal adhesion of the embryonic epidermis Smyth, I.; Du, X.; Taylor, M. S. Proceedings of the National Academy of Sciences, Vol. 101, Issue 37 https://doi.org/10.1073/pnas.0402760101	journal	September 2004
From The Cover: Long-term renewal of hair follicles from clonogenic multipotent stem cells Claudinot, S.; Nicolas, M.; Oshima, H. Proceedings of the National Academy of Sciences, Vol. 102, Issue 41 https://doi.org/10.1073/pnas.0507250102	journal	October 2005
Genomic anatomy of the Tyrp1 (brown) deletion complex Smyth, I. M.; Wilming, L.; Lee, A. W. Proceedings of the National Academy of Sciences, Vol. 103, Issue 10 https://doi.org/10.1073/pnas.0600199103	journal	February 2006
IKK is a critical coregulator of a Smad4-independent TGF -Smad2/3 signaling pathway that controls keratinocyte differentiation Descargues, P.; Sil, A. K.; Sano, Y. Proceedings of the National Academy of Sciences, Vol. 105, Issue 7 https://doi.org/10.1073/pnas.0712044105	journal	February 2008
Elevated blood pressures in mice lacking endothelial nitric oxide synthase Shesely, E. G.; Maeda, N.; Kim, H. - S. Proceedings of the National Academy of Sciences, Vol. 93, Issue 23 https://doi.org/10.1073/pnas.93.23.13176	journal	November 1996
Identification of a Ras Palmitoyltransferase in Saccharomyces cerevisiae Lobo, Sandra; Greentree, Wendy K.; Linder, Maurine E. Journal of Biological Chemistry, Vol. 277, Issue 43 https://doi.org/10.1074/jbc.M206573200	journal	August 2002
Subcellular Distribution of Envoplakin and Periplakin DiColandrea, Teresa; Karashima, Tadashi; Määttä, Arto Journal of Cell Biology, Vol. 151, Issue 3 https://doi.org/10.1083/jcb.151.3.573	journal	October 2000
A developmental conundrum DasGupta, Ramanuj; Rhee, Horace; Fuchs, Elaine Journal of Cell Biology, Vol. 158, Issue 2 https://doi.org/10.1083/jcb.200204134	journal	July 2002
The yeast DHHC cysteine-rich domain protein Akr1p is a palmitoyl transferase Roth, Amy F.; Feng, Ying; Chen, Linyi The Journal of Cell Biology, Vol. 159, Issue 1 https://doi.org/10.1083/jcb.200206120	journal	October 2002
Defining BMP functions in the hair follicle by conditional ablation of BMP receptor IA Kobielak, Krzysztof; Pasolli, H. Amalia; Alonso, Laura Journal of Cell Biology, Vol. 163, Issue 3 https://doi.org/10.1083/jcb.200309042	journal	November 2003
Identification of Golgi-localized acyl transferases that palmitoylate and regulate endothelial nitric oxide synthase Fernández-Hernando, Carlos; Fukata, Masaki; Bernatchez, Pascal N. Journal of Cell Biology, Vol. 174, Issue 3 https://doi.org/10.1083/jcb.200601051	journal	July 2006
Lipid defect underlies selective skin barrier impairment of an epidermal-specific deletion of Gata-3 de Guzman Strong, Cristina; Wertz, Philip W.; Wang, Chenwei Journal of Cell Biology, Vol. 175, Issue 4 https://doi.org/10.1083/jcb.200605057	journal	November 2006
Mutations in ZDHHC9, Which Encodes a Palmitoyltransferase of NRAS and HRAS, Cause X-Linked Mental Retardation Associated with a Marfanoid Habitus Raymond, F. Lucy; Tarpey, Patrick S.; Edkins, Sarah The American Journal of Human Genetics, Vol. 80, Issue 5 https://doi.org/10.1086/513609	journal	May 2007
Specific Activation of Mitogen-activated Protein Kinase by Transforming Growth Factor-β Receptors in Lipid Rafts Is Required for Epithelial Cell Plasticity Zuo, Wei; Chen, Ye-Guang Molecular Biology of the Cell, Vol. 20, Issue 3 https://doi.org/10.1091/mbc.E08-09-0898	journal	February 2009
Skin abnormality in aged fyn-/- fak+/- mice Ilic, D. Carcinogenesis, Vol. 18, Issue 8 https://doi.org/10.1093/carcin/18.8.1473	journal	August 1997
Molecular genetics of the brown (b)-locus region of mouse chromosome 4. II. Complementation analyses of lethal brown deletions. Rinchik, E. M. Genetics, Vol. 137, Issue 3 https://doi.org/10.1093/genetics/137.3.855	journal	July 1994
DEPILATED (dep), A MUTANT GENE THAT AFFECTS THE COAT OF THE MOUSE AND ACTS IN THE EPIDERMIS Mayer, Thomas C.; Kleiman, Norman J.; Green, Margaret C. Genetics, Vol. 84, Issue 1 https://doi.org/10.1093/genetics/84.1.59	journal	September 1976
CSS-Palm 2.0: an updated software for palmitoylation sites prediction Ren, J.; Wen, L.; Gao, X. Protein Engineering Design and Selection, Vol. 21, Issue 11 https://doi.org/10.1093/protein/gzn039	journal	August 2008
Control of murine hair follicle regression (catagen) by TGF‐β1 in vivo Foitzik, Kerstin; Lindner, Gerd; Mueller‐Roever, Sven The FASEB Journal, Vol. 14, Issue 5 https://doi.org/10.1096/fasebj.14.5.752	journal	April 2000
The segment polarity gene porcupine encodes a putative multitransmembrane protein involved in Wingless processing. Kadowaki, T.; Wilder, E.; Klingensmith, J. Genes & Development, Vol. 10, Issue 24 https://doi.org/10.1101/gad.10.24.3116	journal	December 1996
Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin Merrill, B. J. Genes & Development, Vol. 15, Issue 13 https://doi.org/10.1101/gad.891401	journal	July 2001
fyn tyrosine kinase is involved in keratinocyte differentiation control. Calautti, E.; Missero, C.; Stein, P. L. Genes & Development, Vol. 9, Issue 18 https://doi.org/10.1101/gad.9.18.2279	journal	September 1995
Differential expression of nitric oxide synthases in human scalp epidermal and hair follicle pigmentary units: implications for regulation of melanogenesis Sowden, H. M.; Naseem, K. M.; Tobin, D. J. British Journal of Dermatology, Vol. 153, Issue 2 https://doi.org/10.1111/j.1365-2133.2005.06718.x	journal	August 2005
Palmitoylation Controls Recycling in Lysosomal Sorting and Trafficking McCormick, Peter J.; Dumaresq-Doiron, Karine; Pluviose, Anne-Sophie Traffic, Vol. 9, Issue 11 https://doi.org/10.1111/j.1600-0854.2008.00814.x	journal	November 2008
Identification of G Protein α Subunit-Palmitoylating Enzyme Tsutsumi, Ryouhei; Fukata, Yuko; Noritake, Jun Molecular and Cellular Biology, Vol. 29, Issue 2 https://doi.org/10.1128/MCB.01144-08	journal	November 2008
Palmitoylation of Intracellular Signaling Proteins: Regulation and Function Smotrys, Jessica E.; Linder, Maurine E. Annual Review of Biochemistry, Vol. 73, Issue 1 https://doi.org/10.1146/annurev.biochem.73.011303.073954	journal	June 2004
Barrier function regulates epidermal DNA synthesis. Proksch, E.; Feingold, K. R.; Man, M. Q. Journal of Clinical Investigation, Vol. 87, Issue 5 https://doi.org/10.1172/JCI115183	journal	May 1991
A role for mitogen-activated protein kinase activation by integrins in the pathogenesis of psoriasis Haase, Ingo; Hobbs, Robin M.; Romero, M. Rosario Journal of Clinical Investigation, Vol. 108, Issue 4 https://doi.org/10.1172/JCI12153	journal	August 2001
ZDHHC8as a candidate gene for schizophrenia: Analysis of a putative functional intronic marker in case-control and family-based association studies Faul, Thomas; Gawlik, Micha; Bauer, Martin BMC Psychiatry, Vol. 5, Issue 1 https://doi.org/10.1186/1471-244X-5-35	journal	October 2005
BMPR1A signaling is necessary for hair follicle cycling and hair shaft differentiation in mice Yuhki, Munehiro; Yamada, Masahisa; Kawano, Masako Development, Vol. 131, Issue 8 https://doi.org/10.1242/dev.01079	journal	April 2004
Epithelial Bmpr1a regulates differentiation and proliferation in postnatal hair follicles and is essential for tooth development Andl, Thomas; Ahn, Kyung; Kairo, Alladin Development, Vol. 131, Issue 10 https://doi.org/10.1242/dev.01125	journal	May 2004
Dlx3 is a crucial regulator of hair follicle differentiation and cycling Hwang, Joonsung; Mehrani, Taraneh; Millar, Sarah E. Development, Vol. 135, Issue 18 https://doi.org/10.1242/dev.022202	journal	September 2008
Transcriptome and phenotypic analysis reveals Gata3-dependent signalling pathways in murine hair follicles Kurek, Dorota; Garinis, George A.; van Doorninck, J. Hikke Development, Vol. 134, Issue 2 https://doi.org/10.1242/dev.02721	journal	January 2007
Patterned acquisition of skin barrier function during development Hardman, M. J.; Sisi, P.; Banbury, D. N. Development, Vol. 125, Issue 8 https://doi.org/10.1242/dev.125.8.1541	journal	April 1998
Expression of ΔNLef1 in mouse epidermis results in differentiation of hair follicles into squamous epidermal cysts and formation of skin tumours Niemann, Catherin; Owens, David M.; Hülsken, Jörg Development, Vol. 129, Issue 1 https://doi.org/10.1242/dev.129.1.95	journal	January 2002
p63 is upstream of IKKα in epidermal development Candi, Eleonora; Terrinoni, Alessandro; Rufini, Alessandro Journal of Cell Science, Vol. 119, Issue 22 https://doi.org/10.1242/jcs.03265	journal	November 2006
Protein Palmitoylation Regulates Osteoblast Differentiation through BMP-Induced Osterix Expression Leong, Wai Fook; Zhou, Tielin; Lim, Gek Liang PLoS ONE, Vol. 4, Issue 1 https://doi.org/10.1371/journal.pone.0004135	journal	January 2009
The 2 Subunit of GABAA Receptors Is a Substrate for Palmitoylation by GODZ Keller, C. A. Journal of Neuroscience, Vol. 24, Issue 26 https://doi.org/10.1523/JNEUROSCI.1037-04.2004	journal	June 2004

Cited By (25)

A potential role for protein palmitoylation and zDHHC16 in DNA damage response Cao, Na; Li, Jia-Kai; Rao, Yu-Qing BMC Molecular Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s12867-016-0065-9	journal	May 2016
Quantitative Control of Protein S-Palmitoylation Regulates Meiotic Entry in Fission Yeast Zhang, Mingzi M.; Wu, Pei-Yun Jenny; Kelly, Felice D. PLoS Biology, Vol. 11, Issue 7 https://doi.org/10.1371/journal.pbio.1001597	journal	July 2013
Specificity of Transmembrane Protein Palmitoylation in Yeast González Montoro, Ayelén; Chumpen Ramirez, Sabrina; Quiroga, Rodrigo PLoS ONE, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pone.0016969	journal	February 2011
Role for the Epidermal Growth Factor Receptor in Chemotherapy-Induced Alopecia Bichsel, Kyle J.; Gogia, Navdeep; Malouff, Timothy PLoS ONE, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pone.0069368	journal	July 2013
Attenuated palmitoylation of serotonin receptor 5-HT1A affects receptor function and contributes to depression-like behaviors Gorinski, Nataliya; Sigrist, Stephan; Bijata, Monika Freie Universität Berlin https://doi.org/10.17169/refubium-25302	text	January 2019
Progress toward Understanding Protein S-acylation: Prospective in Plants Li, Yaxiao; Qi, Baoxiu Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00346	journal	March 2017
Additional file 11 of Gene network analysis reveals candidate genes related with the hair follicle development in sheep He, Junmin; Zhao, Bingru; Huang, Xixia figshare https://doi.org/10.6084/m9.figshare.20024784	dataset	January 2022
Additional file 1 of Gene network analysis reveals candidate genes related with the hair follicle development in sheep He, Junmin; Zhao, Bingru; Huang, Xixia figshare https://doi.org/10.6084/m9.figshare.20024787.v1	dataset	January 2022
Additional file 4 of Gene network analysis reveals candidate genes related with the hair follicle development in sheep He, Junmin; Zhao, Bingru; Huang, Xixia figshare https://doi.org/10.6084/m9.figshare.20024796.v1	dataset	January 2022
Additional file 5 of Gene network analysis reveals candidate genes related with the hair follicle development in sheep He, Junmin; Zhao, Bingru; Huang, Xixia figshare https://doi.org/10.6084/m9.figshare.20024799	dataset	January 2022
Additional file 8 of Gene network analysis reveals candidate genes related with the hair follicle development in sheep He, Junmin; Zhao, Bingru; Huang, Xixia figshare https://doi.org/10.6084/m9.figshare.20024808	dataset	January 2022
Additional file 9 of Gene network analysis reveals candidate genes related with the hair follicle development in sheep He, Junmin; Zhao, Bingru; Huang, Xixia figshare https://doi.org/10.6084/m9.figshare.20024811	dataset	January 2022
Protein lipid modifications-More than just a greasy ballast Hentschel, Andreas; Zahedi, René P.; Ahrends, Robert PROTEOMICS, Vol. 16, Issue 5 https://doi.org/10.1002/pmic.201500353	journal	March 2016
Palmitoyl acyltransferase DHHC21 mediates endothelial dysfunction in systemic inflammatory response syndrome Beard, Richard S.; Yang, Xiaoyuan; Meegan, Jamie E. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12823	journal	September 2016
Attenuated palmitoylation of serotonin receptor 5-HT1A affects receptor function and contributes to depression-like behaviors Gorinski, Nataliya; Bijata, Monika; Prasad, Sonal Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-11876-5	journal	September 2019
Protein S-palmitoylation in cellular differentiation Zhang, Mingzi M.; Hang, Howard C. Biochemical Society Transactions, Vol. 45, Issue 1 https://doi.org/10.1042/bst20160236	journal	February 2017
Palmitoyl acyltransferase Aph2 in cardiac function and the development of cardiomyopathy Zhou, Tielin; Li, Jing; Zhao, Peiquan Proceedings of the National Academy of Sciences, Vol. 112, Issue 51 https://doi.org/10.1073/pnas.1518368112	journal	December 2015
Fatty acyl recognition and transfer by an integral membrane S -acyltransferase Rana, Mitra S.; Kumar, Pramod; Lee, Chul-Jin Science, Vol. 359, Issue 6372 https://doi.org/10.1126/science.aao6326	journal	January 2018
The Physiology of Protein S- acylation Chamberlain, Luke H.; Shipston, Michael J. Physiological Reviews, Vol. 95, Issue 2 https://doi.org/10.1152/physrev.00032.2014	journal	April 2015
The Protein Acyl Transferase ZDHHC21 Modulates α1 Adrenergic Receptor Function and Regulates Hemodynamics Marin, Ethan P.; Jozsef, Levente; Di Lorenzo, Annarita Arteriosclerosis, Thrombosis, and Vascular Biology, Vol. 36, Issue 2 https://doi.org/10.1161/atvbaha.115.306942	journal	February 2016
Endothelial Cell Palmitoylproteomic Identifies Novel Lipid-Modified Targets and Potential Substrates for Protein Acyl Transferases Marin, Ethan P.; Derakhshan, Behrad; Lam, TuKiet T. Circulation Research, Vol. 110, Issue 10 https://doi.org/10.1161/circresaha.112.269514	journal	May 2012
A potential role for protein palmitoylation and zDHHC16 in DNA damage response Cao, Na; Li, Jia-Kai; Rao, Yu-Qing BMC Molecular Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s12867-016-0065-9	journal	May 2016
Regulation of dendrite morphology and excitatory synapse formation by zDHHC15 Shah, Bhavin S.; Shimell, Jordan J.; Bamji, Shernaz X. Journal of Cell Science https://doi.org/10.1242/jcs.230052	journal	January 2019
Progress toward Understanding Protein S-acylation: Prospective in Plants Li, Yaxiao; Qi, Baoxiu Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00346	journal	March 2017
Role of fatty acid transporters in epidermis: implications for health and disease Khnykin, Denis; Miner, Jeffrey H.; Jahnsen, Frode Dermato-Endocrinology, Vol. 3, Issue 2 https://doi.org/10.4161/derm.3.2.14816	journal	April 2011

Similar Records

EFFECT OF CYSTAMINE AND CYSTEAMINE ON X-IRRADIATED HAIR FOLLICLES

Journal Article · 1963 · Intern. J. Radiation Biol. · OSTI ID:4022037

Smoliar, V

A new Gsdma3 mutation affecting anagen phase of first hair cycle

Journal Article · 2007 · Biochemical and Biophysical Research Communications · OSTI ID:20991481

Tanaka, Shigekazu; Tamura, Masaru; Aoki, Aya; +4 more

Effects of Wnt-10b on hair shaft growth in hair follicle cultures

Journal Article · 2007 · Biochemical and Biophysical Research Communications · OSTI ID:20991464

Ouji, Yukiteru; Yoshikawa, Masahide; Moriya, Kei; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Genetics & Heredity

Title: Palmitoylation Regulates Epidermal Homeostasis and Hair Follicle Differentiation

Citation Formats

References (91)

Cited By (25)

Similar Records

Related Subjects