Role of the soluble epoxide hydrolase in the hair follicle stem cell homeostasis and hair growth.


Journal

Pflugers Archiv : European journal of physiology
ISSN: 1432-2013
Titre abrégé: Pflugers Arch
Pays: Germany
ID NLM: 0154720

Informations de publication

Date de publication:
09 2022
Historique:
received: 15 03 2022
accepted: 19 05 2022
revised: 18 05 2022
pubmed: 2 6 2022
medline: 24 8 2022
entrez: 1 6 2022
Statut: ppublish

Résumé

Polyunsaturated fatty acids (PUFAs) are used as traditional remedies to treat hair loss, but the mechanisms underlying their beneficial effects are not well understood. Here, we explored the role of PUFA metabolites generated by the cytochrome P450/soluble epoxide hydrolase (sEH) pathway in the regulation of the hair follicle cycle. Histological analysis of the skin from wild-type and sEH

Identifiants

pubmed: 35648219
doi: 10.1007/s00424-022-02709-4
pii: 10.1007/s00424-022-02709-4
pmc: PMC9393123
doi:

Substances chimiques

Epoxide Hydrolases EC 3.3.2.-
Ephx2 protein, mouse EC 3.3.2.10

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1021-1035

Subventions

Organisme : NIEHS NIH HHS
ID : P42 ES004699
Pays : United States
Organisme : NIEHS NIH HHS
ID : R35 ES030443
Pays : United States

Informations de copyright

© 2022. The Author(s).

Références

Atone J, Wagner K, Hashimoto K et al (2020) Cytochrome P450 derived epoxidized fatty acids as a therapeutic tool against neuroinflammatory diseases. Prostaglandins Other Lipid Mediat 147:106385. https://doi.org/10.1016/j.prostaglandins.2019.106385
doi: 10.1016/j.prostaglandins.2019.106385 pubmed: 31698143
Dos Santos LRB, Fleming I (2020) Role of cytochrome P450-derived, polyunsaturated fatty acid mediators in diabetes and the metabolic syndrome. Prostaglandins Other Lipid Mediat 148:106407. https://doi.org/10.1016/j.prostaglandins.2019.106407
doi: 10.1016/j.prostaglandins.2019.106407 pubmed: 31899373
Imig JD (2018) Prospective for cytochrome P450 epoxygenase cardiovascular and renal therapeutics. Pharmacol Ther 192:1–19. https://doi.org/10.1016/j.pharmthera.2018.06.015
doi: 10.1016/j.pharmthera.2018.06.015 pubmed: 29964123 pmcid: 6263841
Fleming I (2014) The pharmacology of the cytochrome P450 epoxygenase/soluble epoxide hydrolase axis in the vasculature and cardiovascular disease. Pharmacol Rev 66:1106–1140. https://doi.org/10.1124/pr.113.007781
doi: 10.1124/pr.113.007781 pubmed: 25244930
McReynolds C, Morisseau C, Wagner K et al (2020) Epoxy fatty acids are promising targets for treatment of pain, cardiovascular disease and other indications characterized by mitochondrial dysfunction, endoplasmic stress and inflammation. Adv Exp Med Biol 1274:71–99. https://doi.org/10.1007/978-3-030-50621-6_5
doi: 10.1007/978-3-030-50621-6_5 pubmed: 32894508 pmcid: 7737916
Larsen MC, Almeldin A, Tong T et al. (2020) Cytochrome P4501B1 in bone marrow is co-expressed with key markers of mesenchymal stem cells. BMS2 cell line models PAH disruption of bone marrow niche development functions. Toxicol Appl Pharmacol 401:115111. https://doi.org/10.1016/j.taap.2020.115111
Park H-J, Choi Y-J, Kim JW et al (2015) Differences in the epigenetic regulation of cytochrome P450 genes between human embryonic stem cell-derived hepatocytes and primary hepatocytes. PLoS ONE 10:e0132992. https://doi.org/10.1371/journal.pone.0132992
doi: 10.1371/journal.pone.0132992 pubmed: 26177506 pmcid: 4503736
Rashid MA, Haque M, Akbar M (2016) Role of polyunsaturated fatty acids and their metabolites on stem cell proliferation and differentiation. Adv Neurobiol 12:367–380. https://doi.org/10.1007/978-3-319-28383-8_20
doi: 10.1007/978-3-319-28383-8_20 pubmed: 27651264
Okano J, Levy C, Lichti U et al (2012) Cutaneous retinoic acid levels determine hair follicle development and downgrowth. J Biol Chem 287:39304–39315. https://doi.org/10.1074/jbc.M112.397273
doi: 10.1074/jbc.M112.397273 pubmed: 23007396 pmcid: 3501026
Hao P-P, Lee M-J, Yu G-R et al (2013) Isolation of EpCAM(+)/CD133 (-) hepatic progenitor cells. Mol Cells 36:424–431. https://doi.org/10.1007/s10059-013-0190-y
doi: 10.1007/s10059-013-0190-y pubmed: 24293012 pmcid: 3887933
Kino J, Ichinohe N, Ishii M et al (2019) Isolation and expansion of rat hepatocytic progenitor cells. Methods Mol Biol 1905:29–41. https://doi.org/10.1007/978-1-4939-8961-4_4
doi: 10.1007/978-1-4939-8961-4_4 pubmed: 30536088
Frömel T, Jungblut B, Hu J et al (2012) Soluble epoxide hydrolase regulates hematopoietic progenitor cell function via generation of fatty acid diols. Proc Natl Acad Sci USA 109:9995–10000. https://doi.org/10.1073/pnas.1206493109
doi: 10.1073/pnas.1206493109 pubmed: 22665795 pmcid: 3382493
Murayama E, Kissa K, Zapata A et al (2006) Tracing hematopoietic precursor migration to successive hematopoietic organs during zebrafish development. Immunity 25:963–975. https://doi.org/10.1016/j.immuni.2006.10.015
doi: 10.1016/j.immuni.2006.10.015 pubmed: 17157041
Gonzales KAU, Fuchs E (2017) Skin and its regenerative powers: an alliance between stem cells and their niche. Dev Cell 43:387–401. https://doi.org/10.1016/j.devcel.2017.10.001
doi: 10.1016/j.devcel.2017.10.001 pubmed: 29161590
Decker M, Adamska M, Cronin A et al (2012) EH3 (ABHD9): the first member of a new epoxide hydrolase family with high activity for fatty acid epoxides. J Lipid Res 53:2038–2045. https://doi.org/10.1194/jlr.M024448
doi: 10.1194/jlr.M024448 pubmed: 22798687 pmcid: 3435537
Du L, Yermalitsky V, Ladd PA et al (2005) Evidence that cytochrome P450 CYP2B19 is the major source of epoxyeicosatrienoic acids in mouse skin. Arch Biochem Biophys 435:125–133. https://doi.org/10.1016/j.abb.2004.11.023
doi: 10.1016/j.abb.2004.11.023 pubmed: 15680914
Enayetallah AE, French RA, Thibodeau MS et al (2004) Distribution of soluble epoxide hydrolase and of cytochrome P450 2C8, 2C9, and 2J2 in human tissues. J Histochem Cytochem 52:447–454. https://doi.org/10.1177/002215540405200403
doi: 10.1177/002215540405200403 pubmed: 15033996
Winder BS, Nourooz-Zadeh J, Isseroff R et al (1993) Properties of enzymes hydrating epoxides in human epidermis and liver. Int J Biochem 25:1291–1301. https://doi.org/10.1016/0020-711x(93)90081-o
doi: 10.1016/0020-711x(93)90081-o pubmed: 8224376
Yamanashi H, Boeglin WE, Morisseau C et al (2018) Catalytic activities of mammalian epoxide hydrolases with cis and trans fatty acid epoxides relevant to skin barrier function. J Lipid Res 59:684–695. https://doi.org/10.1194/jlr.M082701
doi: 10.1194/jlr.M082701 pubmed: 29459481 pmcid: 5880498
Riccio G, Sommella E, Badolati N et al (2018) Annurca apple polyphenols protect murine hair follicles from taxane induced dystrophy and hijacks polyunsaturated fatty acid metabolism toward β-oxidation. Nutrients 10:1808. https://doi.org/10.3390/nu10111808
doi: 10.3390/nu10111808 pmcid: 6267362
Hoopes SL, Gruzdev A, Edin ML et al (2017) Generation and characterization of epoxide hydrolase 3 (EPHX3)-deficient mice. PLoS ONE 12:e0175348. https://doi.org/10.1371/journal.pone.0175348
doi: 10.1371/journal.pone.0175348 pubmed: 28384353 pmcid: 5383309
Muñoz-Garcia A, Thomas CP, Keeney DS et al (2014) The importance of the lipoxygenase-hepoxilin pathway in the mammalian epidermal barrier. Biochim Biophys Acta 1841:401–408. https://doi.org/10.1016/j.bbalip.2013.08.020
doi: 10.1016/j.bbalip.2013.08.020 pubmed: 24021977
DasGupta R, Fuchs E (1999) Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126:4557–4568. https://doi.org/10.1242/dev.126.20.4557
doi: 10.1242/dev.126.20.4557 pubmed: 10498690
Hu J, Popp R, Frömel T et al (2014) Müller glia cells regulate Notch signaling and retinal angiogenesis via the generation of 19,20-dihydroxydocosapentaenoic acid. J Exp Med 211:281–295. https://doi.org/10.1084/jem.20131494
doi: 10.1084/jem.20131494 pubmed: 24446488 pmcid: 3920554
Yano K, Brown LF, Detmar M (2001) Control of hair growth and follicle size by VEGF-mediated angiogenesis. J Clin Invest 107:409–417. https://doi.org/10.1172/JCI11317
doi: 10.1172/JCI11317 pubmed: 11181640 pmcid: 199257
Hardy MH (1992) The secret life of the hair follicle. Trends Genet 8:55–61. https://doi.org/10.1016/0168-9525(92)90350-D
doi: 10.1016/0168-9525(92)90350-D pubmed: 1566372
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Meth 9:671–675. https://doi.org/10.1038/nmeth.2089
doi: 10.1038/nmeth.2089
Han Y, Mora J, Huard A et al (2019) IL-38 Ameliorates skin inflammation and limits IL-17 production from γδ T cells. Cell Rep 27:835-846.e5. https://doi.org/10.1016/j.celrep.2019.03.082
doi: 10.1016/j.celrep.2019.03.082 pubmed: 30995480
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
doi: 10.1093/bioinformatics/btu170 pubmed: 24695404 pmcid: 4103590
Dobin A, Davis CA, Schlesinger F et al (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15–21. https://doi.org/10.1093/bioinformatics/bts635
doi: 10.1093/bioinformatics/bts635 pubmed: 23104886
Liao Y, Smyth GK, Shi W (2014) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923–930. https://doi.org/10.1093/bioinformatics/btt656
doi: 10.1093/bioinformatics/btt656 pubmed: 24227677
Müller-Röver S, Handjiski B, van der Veen C et al (2001) A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J Invest Dermatol 117:3–15. https://doi.org/10.1046/j.0022-202x.2001.01377.x
doi: 10.1046/j.0022-202x.2001.01377.x pubmed: 11442744
Nishimura EK, Jordan SA, Oshima H et al (2002) Dominant role of the niche in melanocyte stem-cell fate determination. Nature 416:854–860. https://doi.org/10.1038/416854a
doi: 10.1038/416854a pubmed: 11976685
Qiu W, Chuong C-M, Lei M (2019) Regulation of melanocyte stem cells in the pigmentation of skin and its appendages: biological patterning and therapeutic potentials. Exp Dermatol 28:395–405. https://doi.org/10.1111/exd.13856
doi: 10.1111/exd.13856 pubmed: 30537004 pmcid: 6488374
Rabbani P, Takeo M, Chou W et al (2011) Coordinated activation of Wnt in epithelial and melanocyte stem cells initiates pigmented hair regeneration. Cell 145:941–955. https://doi.org/10.1016/j.cell.2011.05.004
doi: 10.1016/j.cell.2011.05.004 pubmed: 21663796 pmcid: 3962257
Hsu Y-C, Pasolli HA, Fuchs E (2011) Dynamics between stem cells, niche, and progeny in the hair follicle. Cell 144:92–105. https://doi.org/10.1016/j.cell.2010.11.049
doi: 10.1016/j.cell.2010.11.049 pubmed: 21215372 pmcid: 3050564
Hsu Y-C, Li L, Fuchs E (2014) Transit-amplifying cells orchestrate stem cell activity and tissue regeneration. Cell 157:935–949. https://doi.org/10.1016/j.cell.2014.02.057
doi: 10.1016/j.cell.2014.02.057 pubmed: 24813615 pmcid: 4041217
Mesler AL, Veniaminova NA, Lull MV et al (2017) Hair follicle terminal differentiation is orchestrated by distinct early and late matrix progenitors. Cell Rep 19:809–821. https://doi.org/10.1016/j.celrep.2017.03.077
doi: 10.1016/j.celrep.2017.03.077 pubmed: 28445731 pmcid: 5482241
Yang H, Adam RC, Ge Y et al (2017) Epithelial-mesenchymal micro-niches govern stem cell lineage choices. Cell 169:483-496.e13. https://doi.org/10.1016/j.cell.2017.03.038
doi: 10.1016/j.cell.2017.03.038 pubmed: 28413068 pmcid: 5510744
Le Floc’h C, Cheniti A, Connétable S et al (2015) Effect of a nutritional supplement on hair loss in women. J Cosmet Dermatol 14:76–82. https://doi.org/10.1111/jocd.12127
doi: 10.1111/jocd.12127 pubmed: 25573272
Munkhbayar S, Jang S, Cho A-R et al (2016) Role of arachidonic acid in promoting hair growth. Ann Dermatol 28:55–64. https://doi.org/10.5021/ad.2016.28.1.55
doi: 10.5021/ad.2016.28.1.55 pubmed: 26848219 pmcid: 4737836
Ryu HS, Jeong J, Lee CM et al (2021) Activation of hair cell growth factors by linoleic acid in Malva verticillata seed. Molecules 26:2117. https://doi.org/10.3390/molecules26082117
doi: 10.3390/molecules26082117 pubmed: 33917070 pmcid: 8067726
Cotsarelis G, Sun T-T, Lavker RM (1990) Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 61:1329–1337. https://doi.org/10.1016/0092-8674(90)90696-C
doi: 10.1016/0092-8674(90)90696-C pubmed: 2364430
Cronin A, Mowbray S, Dürk H et al (2003) The N-terminal domain of mammalian soluble epoxide hydrolase is a phosphatase. Proc Natl Acad Sci USA 100:1552–1557. https://doi.org/10.1073/pnas.0437829100
doi: 10.1073/pnas.0437829100 pubmed: 12574508 pmcid: 149870
Newman JW, Morisseau C, Harris TR et al (2003) The soluble epoxide hydrolase encoded by EPXH2 is a bifunctional enzyme with novel lipid phosphate phosphatase activity. Proc Natl Acad Sci USA 100:1558–1563. https://doi.org/10.1073/pnas.0437724100
doi: 10.1073/pnas.0437724100 pubmed: 12574510 pmcid: 149871
Hwang SH, Tsai H-J, Liu J-Y et al (2007) Orally bioavailable potent soluble epoxide hydrolase inhibitors. J Med Chem 50:3825–3840. https://doi.org/10.1021/jm070270t
doi: 10.1021/jm070270t pubmed: 17616115 pmcid: 2596069
Imig JD, Cervenka L, Neckar J (2022) Epoxylipids and soluble epoxide hydrolase in heart diseases. Biochem Pharmacol 195:114866. https://doi.org/10.1016/j.bcp.2021.114866
doi: 10.1016/j.bcp.2021.114866 pubmed: 34863976
Hildreth K, Kodani SD, Hammock BD et al (2020) Cytochrome P450-derived linoleic acid metabolites EpOMEs and DiHOMEs: a review of recent studies. J Nutr Biochem 86:108484. https://doi.org/10.1016/j.jnutbio.2020.108484
doi: 10.1016/j.jnutbio.2020.108484 pubmed: 32827665 pmcid: 7606796
Ocampo-Garza J, Griggs J, Tosti A (2019) New drugs under investigation for the treatment of alopecias. Expert Opin Investig Drugs 28:275–284. https://doi.org/10.1080/13543784.2019.1568989
doi: 10.1080/13543784.2019.1568989 pubmed: 30642204
Yazdanian N, Mozafarpoor S, Goodarzi A (2021) Phosphodiesterase inhibitors and prostaglandin analogues in dermatology: a comprehensive review. Dermatol Ther 34:e14669. https://doi.org/10.1111/dth.14669
doi: 10.1111/dth.14669 pubmed: 33314552
Sato N, Leopold PL, Crystal RG (1999) Induction of the hair growth phase in postnatal mice by localized transient expression of Sonic hedgehog. J Clin Invest 104:855–864. https://doi.org/10.1172/JCI7691
doi: 10.1172/JCI7691 pubmed: 10510326 pmcid: 408560
Zhang B, Hsu Y-C (2017) Emerging roles of transit-amplifying cells in tissue regeneration and cancer. Wiley Interdiscip Rev Dev Biol 6 https://doi.org/10.1002/wdev.282.10.1002/wdev.282
Huang W-Y, Lai S-F, Chiu H-Y et al (2017) Mobilizing tansit-amplifying cell-derived ectopic progenitors prevents hair loss from chemotherapy or radiation therapy. Cancer Res 77:6083–6096. https://doi.org/10.1158/0008-5472.CAN-17-0667
doi: 10.1158/0008-5472.CAN-17-0667 pubmed: 28939680 pmcid: 5756475
Sinal CJ, Miyata M, Tohkin M et al (2000) Targeted disruption of soluble epoxide hydrolase reveals a role in blood pressure regulation. J Biol Chem 275:40504–40510. https://doi.org/10.1074/jbc.M008106200
doi: 10.1074/jbc.M008106200 pubmed: 11001943
Wagner K, Gilda J, Yang J et al (2017) Soluble epoxide hydrolase inhibition alleviates neuropathy in Akita (Ins2 Akita) mice. Behav Brain Res 326:69–76. https://doi.org/10.1016/j.bbr.2017.02.048
doi: 10.1016/j.bbr.2017.02.048 pubmed: 28259677 pmcid: 5409858
Edin ML, Yamanashi H, Boeglin WE et al (2020) Epoxide hydrolase 3 (Ephx3) gene disruption reduces ceramide linoleate epoxide hydrolysis and impairs skin barrier function. J Biol Chem. https://doi.org/10.1074/jbc.RA120.016570
doi: 10.1074/jbc.RA120.016570

Auteurs

Zumer Naeem (Z)

Institute for Vascular Signalling, Centre for Molecular Medicine, Goethe University, Theodor-Stern-Kai 7, 60590, Frankfurt am Main, Germany.

Sven Zukunft (S)

Institute for Vascular Signalling, Centre for Molecular Medicine, Goethe University, Theodor-Stern-Kai 7, 60590, Frankfurt am Main, Germany.

Stephan Günther (S)

Bioinformatics and Deep Sequencing Platform, Max Planck Institute for Heart and Lung Research, 61231, Bad Nauheim, Germany.

Stefan Liebner (S)

Institute of Neurology (Edinger-Institute), Goethe-University Frankfurt, 60528, Frankfurt am Main, Germany.

Andreas Weigert (A)

Institute of Biochemistry I, Goethe-University Frankfurt, 60590, Frankfurt am Main, Germany.

Bruce D Hammock (BD)

Department of Entomology and Nematology and Comprehensive Cancer Center, University of California, Davis, CA, USA.

Timo Frömel (T)

Institute for Vascular Signalling, Centre for Molecular Medicine, Goethe University, Theodor-Stern-Kai 7, 60590, Frankfurt am Main, Germany.

Ingrid Fleming (I)

Institute for Vascular Signalling, Centre for Molecular Medicine, Goethe University, Theodor-Stern-Kai 7, 60590, Frankfurt am Main, Germany. fleming@em.uni-frankfurt.de.
German Center of Cardiovascular Research (DZHK), Partner site RheinMain, Frankfurt am Main, Germany. fleming@em.uni-frankfurt.de.

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