The role of cell-cell and cell-matrix junctional complexes in sebaceous gland homeostasis and differentiation.
Cell–cell adhesion
Cell–matrix adhesion
Junctional complexes
Sebaceous glands
Sebum
Journal
Cell communication and signaling : CCS
ISSN: 1478-811X
Titre abrégé: Cell Commun Signal
Pays: England
ID NLM: 101170464
Informations de publication
Date de publication:
23 Sep 2024
23 Sep 2024
Historique:
received:
09
08
2024
accepted:
17
09
2024
medline:
24
9
2024
pubmed:
24
9
2024
entrez:
24
9
2024
Statut:
epublish
Résumé
Sebaceous glands (SG) are essential for maintaining skin integrity, as their lipid-rich secretion (sebum) lubricates and protects the epidermis and hairs. In addition, these glands have an emerging role in immunomodulation and may affect whole-body energy metabolism, besides being an appealing model for research in topics as lipogenesis, stem cell biology and tumorigenesis. In spite of the increasing interest in studying SGs pathophysiology, sebocyte cell-cell and cell-matrix adhesion processes have been only superficially examined, and never in a systematic way. This is regrettable considering the key role of cellular adhesion in general, the specific expression pattern of indivdual junctional complexes, and the reports of structural changes in SGs after altered expression of adhesion-relevant proteins. Here, we review the available information on structural and functional aspects of cell-cell and cell-matrix junctions in sebocytes, and how these processes change under pathological conditions. This information will contribute for better understanding sebocyte differentiation and sebum secretion, and may provide hints for novel therapeutic strategies for skin diseases.
Identifiants
pubmed: 39313816
doi: 10.1186/s12964-024-01835-z
pii: 10.1186/s12964-024-01835-z
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
445Informations de copyright
© 2024. The Author(s).
Références
Smith KR, Thiboutot DM. Thematic review series: skin lipids. Sebaceous gland lipids: friend or foe? J Lipid Res. 2008;49:271–81.
doi: 10.1194/jlr.R700015-JLR200
pubmed: 17975220
Schneider MR, Paus R. Sebocytes, multifaceted epithelial cells: lipid production and holocrine secretion. Int J Biochem Cell Biol. 2010;42:181–5.
doi: 10.1016/j.biocel.2009.11.017
pubmed: 19944183
Butovich IA. Meibomian glands, meibum, and meibogenesis. Exp Eye Res. 2017;163:2–16. https://doi.org/10.1016/j.exer.2017.06.020 .
doi: 10.1016/j.exer.2017.06.020
pubmed: 28669846
pmcid: 5728685
Nicolaides N. Skin lipids: their biochemical uniqueness. Science. 1974;186:19–26.
doi: 10.1126/science.186.4158.19
pubmed: 4607408
Pappas A. Epidermal surface lipids. Dermatoendocrinol. 2009;1:72–6.
doi: 10.4161/derm.1.2.7811
pubmed: 20224687
pmcid: 2835894
Layton AM, Ravenscroft J. Adolescent acne vulgaris: current and emerging treatments. Lancet Child Adolesc Health. 2023;7:136–44. https://doi.org/10.1016/S2352-4642(22)00314-5 .
doi: 10.1016/S2352-4642(22)00314-5
pubmed: 36525984
van Steensel MAM. Acne in the 21st century. Br J Dermatol. 2019;181:647–8. https://doi.org/10.1111/bjd.18202 .
doi: 10.1111/bjd.18202
pubmed: 31576571
Zouboulis CC, Picardo M, Ju Q, Kurokawa I, Torocsik D, Biro T, Schneider MR. Beyond acne: current aspects of sebaceous gland biology and function. Rev Endocr Metab Disord. 2016;17:319–34. https://doi.org/10.1007/s11154-016-9389-5 .
doi: 10.1007/s11154-016-9389-5
pubmed: 27726049
Sipilä K, Rognoni E, Jokinen J, Tewary M, Vietri Rudan M, Talvi S, et al. Embigin is a fibronectin receptor that affects sebaceous gland differentiation and metabolism. Dev Cell. 2022;57:1453–1465.e7. https://doi.org/10.1016/j.devcel.2022.05.011 .
doi: 10.1016/j.devcel.2022.05.011
pubmed: 35671757
pmcid: 9616737
Yosefzon Y, Soteriou D, Feldman A, Kostic L, Koren E, Brown S, et al. Caspase-3 regulates YAP-dependent cell proliferation and organ size. Mol Cell. 2018;70:573–587.e4. https://doi.org/10.1016/j.molcel.2018.04.019 .
doi: 10.1016/j.molcel.2018.04.019
pubmed: 29775577
Exner T, Romero-Brey I, Yifrach E, Rivera-Monroy J, Schrul B, Zouboulis CC, et al. An alternative membrane topology permits lipid droplet localization of peroxisomal fatty acyl-CoA reductase 1. J Cell Sci. 2019. https://doi.org/10.1242/jcs.223016 .
doi: 10.1242/jcs.223016
pubmed: 30745342
Kobayashi T, Voisin B, Kim DY, Kennedy EA, Jo J-H, Shih H-Y, et al. Homeostatic control of sebaceous glands by innate lymphoid cells regulates commensal bacteria equilibrium. Cell. 2019;176:982–997.e16. https://doi.org/10.1016/j.cell.2018.12.031 .
doi: 10.1016/j.cell.2018.12.031
pubmed: 30712873
pmcid: 6532063
Choa R, Tohyama J, Wada S, Meng H, Hu J, Okumura M, et al. Thymic stromal lymphopoietin induces adipose loss through sebum hypersecretion. Science. 2021. https://doi.org/10.1126/science.abd2893 .
doi: 10.1126/science.abd2893
pubmed: 34326208
pmcid: 8917823
Oulès B, Rognoni E, Hoste E, Goss G, Fiehler R, Natsuga K, et al. Mutant Lef1 controls Gata6 in sebaceous gland development and cancer. EMBO J. 2019. https://doi.org/10.15252/embj.2018100526 .
doi: 10.15252/embj.2018100526
pubmed: 30886049
pmcid: 6484415
Canse C, Yildirim E, Yaba A. Overview of junctional complexes during mammalian early embryonic development. Front Endocrinol (Lausanne). 2023;14: 1150017. https://doi.org/10.3389/fendo.2023.1150017 .
doi: 10.3389/fendo.2023.1150017
pubmed: 37152932
Simpson CL, Patel DM, Green KJ. Deconstructing the skin: cytoarchitectural determinants of epidermal morphogenesis. Nat Rev Mol Cell Biol. 2011;12:565–80. https://doi.org/10.1038/nrm3175 .
doi: 10.1038/nrm3175
pubmed: 21860392
pmcid: 3280198
Évora AS, Adams MJ, Johnson SA, Zhang Z. Corneocytes: relationship between structural and biomechanical properties. Skin Pharmacol Physiol. 2021;34:146–61. https://doi.org/10.1159/000513054 .
doi: 10.1159/000513054
pubmed: 33780956
Haftek M. Epidermal barrier disorders and corneodesmosome defects. Cell Tissue Res. 2015;360:483–90. https://doi.org/10.1007/s00441-014-2019-1 .
doi: 10.1007/s00441-014-2019-1
pubmed: 25378284
Haftek M, Simon M, Kanitakis J, Maréchal S, Claudy A, Serre G, Schmitt D. Expression of corneodesmosin in the granular layer and stratum corneum of normal and diseased epidermis. Br J Dermatol. 1997;137:864–73.
doi: 10.1046/j.1365-2133.1997.19792087.x
pubmed: 9470901
Simon M, Tazi-Ahnini R, Jonca N, Caubet C, Cork MJ, Serre G. Alterations in the desquamation-related proteolytic cleavage of corneodesmosin and other corneodesmosomal proteins in psoriatic lesional epidermis. Br J Dermatol. 2008;159:77–85. https://doi.org/10.1111/j.1365-2133.2008.08578.x .
doi: 10.1111/j.1365-2133.2008.08578.x
pubmed: 18460028
Ilarslan H, Lathrop WF, Dobkowski B, Hawkins SS, Scott J, Bajor J, Mayes AE. Effects of eczema calming lotion on the stratum corneum in atopic dermatitis: corneodesmosin and intercellular lipid lamellae. Int J Cosmet Sci. 2024;46:516–25. https://doi.org/10.1111/ics.12962 .
doi: 10.1111/ics.12962
pubmed: 39113306
Ehrmann C, Schneider MR. Genetically modified laboratory mice with sebaceous glands abnormalities. Cell Mol Life Sci. 2016;73:4623–42. https://doi.org/10.1007/s00018-016-2312-0 .
doi: 10.1007/s00018-016-2312-0
pubmed: 27457558
pmcid: 11108334
Leclerc EA, Huchenq A, Mattiuzzo NR, Metzger D, Chambon P, Ghyselinck NB, et al. Corneodesmosin gene ablation induces lethal skin-barrier disruption and hair-follicle degeneration related to desmosome dysfunction. J Cell Sci. 2009;122:2699–709.
doi: 10.1242/jcs.050302
pubmed: 19596793
Gat U, DasGupta R, Degenstein L, Fuchs E. De novo hair follicle morphogenesis and hair tumors in mice expressing a truncated beta-catenin in skin. Cell. 1998;95:605–14.
doi: 10.1016/S0092-8674(00)81631-1
pubmed: 9845363
Lo Celso C, Prowse DM, Watt FM. Transient activation of beta-catenin signalling in adult mouse epidermis is sufficient to induce new hair follicles but continuous activation is required to maintain hair follicle tumours. Development. 2004;131:1787–99.
doi: 10.1242/dev.01052
pubmed: 15084463
Atsugi T, Yokouchi M, Hirano T, Hirabayashi A, Nagai T, Ohyama M, et al. Holocrine secretion occurs outside the tight junction barrier in multicellular glands: lessons from claudin-1-deficient mice. J Invest Dermatol. 2020;140:298–308.e5. https://doi.org/10.1016/j.jid.2019.06.150 .
doi: 10.1016/j.jid.2019.06.150
pubmed: 31445004
Niessen MT, Scott J, Zielinski JG, Vorhagen S, Sotiropoulou PA, Blanpain C, et al. aPKClambda controls epidermal homeostasis and stem cell fate through regulation of division orientation. J Cell Biol. 2013;202:887–900. https://doi.org/10.1083/jcb.20130700 .
Osada S-I, Minematsu N, Oda F, Akimoto K, Kawana S, Ohno S. Atypical protein kinase C isoform, aPKCλ, is essential for maintaining hair follicle stem cell quiescence. J Invest Dermatol. 2015;135:2584–92. https://doi.org/10.1038/jid.2015.222 .
doi: 10.1038/jid.2015.222
pubmed: 26076315
Ali NJA, Dias Gomes M, Bauer R, Brodesser S, Niemann C, Iden S. Essential role of polarity protein Par3 for epidermal homeostasis through regulation of barrier function, keratinocyte differentiation, and stem cell maintenance. J Invest Dermatol. 2016;136:2406–16. https://doi.org/10.1016/j.jid.2016.07.011 .
doi: 10.1016/j.jid.2016.07.011
pubmed: 27452221
Bosen F, Schütz M, Beinhauer A, Strenzke N, Franz T, Willecke K. The Clouston syndrome mutation connexin30 A88V leads to hyperproliferation of sebaceous glands and hearing impairments in mice. FEBS Lett. 2014;588:1795–801. https://doi.org/10.1016/j.febslet.2014.03.040 .
doi: 10.1016/j.febslet.2014.03.040
pubmed: 24685692
Mese G, Sellitto C, Li L, Wang H-Z, Valiunas V, Richard G, et al. The Cx26-G45E mutation displays increased hemichannel activity in a mouse model of the lethal form of keratitis-ichthyosis-deafness syndrome. Mol Biol Cell. 2011;22:4776–86. https://doi.org/10.1091/mbc.E11-09-0778 .
doi: 10.1091/mbc.E11-09-0778
pubmed: 22031297
pmcid: 3237621
Essayem S, Kovacic-Milivojevic B, Baumbusch C, McDonagh S, Dolganov G, Howerton K, et al. Hair cycle and wound healing in mice with a keratinocyte-restricted deletion of FAK. Oncogene. 2006;25:1081–9. https://doi.org/10.1038/sj.onc.1209130 .
doi: 10.1038/sj.onc.1209130
pubmed: 16247468
pmcid: 2710133
Ilic D, Kanazawa S, Nishizumi H, Aizawa S, Kuroki T, Mori S, Yamamoto T. Skin abnormality in aged fyn-/- fak+/- mice. Carcinogenesis. 1997;18:1473–6.
doi: 10.1093/carcin/18.8.1473
pubmed: 9276618
Altstätter J, Hess MW, Costell M, Montanez E. α-parvin is required for epidermal morphogenesis, hair follicle development and basal keratinocyte polarity. PLoS One. 2020;15:e0230380. https://doi.org/10.1371/journal.pone.0230380 .
doi: 10.1371/journal.pone.0230380
pubmed: 32163511
pmcid: 7067437
Coulson-Thomas VJ, Gesteira TF, Esko J, Kao W. Heparan sulfate regulates hair follicle and sebaceous gland morphogenesis and homeostasis. J Biol Chem. 2014;289:25211–26. https://doi.org/10.1074/jbc.M114.572511 .
doi: 10.1074/jbc.M114.572511
pubmed: 25053416
pmcid: 4155684
Schneider MR, Schmidt-Ullrich R, Paus R. The hair follicle as a dynamic miniorgan. Curr Biol. 2009;19:R132–42.
doi: 10.1016/j.cub.2008.12.005
pubmed: 19211055
Geueke A, Niemann C. Stem and progenitor cells in sebaceous gland development, homeostasis and pathologies. Exp Dermatol. 2021;30:588–97. https://doi.org/10.1111/exd.14303 .
doi: 10.1111/exd.14303
pubmed: 33599012
Zouboulis CC, Coenye T, He L, Kabashima K, Kobayashi T, Niemann C, et al. Sebaceous immunobiology - skin homeostasis, pathophysiology, coordination of innate immunity and inflammatory response and disease associations. Front Immunol. 2022;13:1029818. https://doi.org/10.3389/fimmu.2022.1029818 .
doi: 10.3389/fimmu.2022.1029818
pubmed: 36439142
pmcid: 9686445
Jensen KB, Collins CA, Nascimento E, Tan DW, Frye M, Itami S, Watt FM. Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell. 2009;4:427–39.
doi: 10.1016/j.stem.2009.04.014
pubmed: 19427292
pmcid: 2698066
Andersen MS, Hannezo E, Ulyanchenko S, Estrach S, Antoku Y, Pisano S, et al. Tracing the cellular dynamics of sebaceous gland development in normal and perturbed states. Nat Cell Biol. 2019;21:924–32. https://doi.org/10.1038/s41556-019-0362-x .
doi: 10.1038/s41556-019-0362-x
pubmed: 31358966
pmcid: 6978139
Thody AJ, Shuster S. Control and function of sebaceous glands. Physiol Rev. 1989;69:383–416.
doi: 10.1152/physrev.1989.69.2.383
pubmed: 2648418
Schneider MR. Lipid droplets and associated proteins in sebocytes. Exp Cell Res. 2016;340:205–8.
doi: 10.1016/j.yexcr.2015.11.008
pubmed: 26571075
Jenkinson DM, Elder HY, Montgomery I, Moss VA. Comparative studies of the ultrastructure of the sebaceous gland. Tissue Cell. 1985;17:683–98.
doi: 10.1016/0040-8166(85)90004-7
pubmed: 4060144
Veniaminova NA, Jia YY, Hartigan AM, Huyge TJ, Tsai S-Y, Grachtchouk M, et al. Distinct mechanisms for sebaceous gland self-renewal and regeneration provide durability in response to injury. Cell Rep. 2023;42:113121. https://doi.org/10.1016/j.celrep.2023.113121 .
doi: 10.1016/j.celrep.2023.113121
pubmed: 37715952
pmcid: 10591672
Schmidt M, Hansmann F, Loeffler-Wirth H, Zouboulis CC, Binder H, Schneider MR. A spatial portrait of the human sebaceous gland transcriptional program. J Biol Chem. 2024;300:107442. https://doi.org/10.1016/j.jbc.2024.107442 .
doi: 10.1016/j.jbc.2024.107442
pubmed: 38838779
pmcid: 11261126
Schneider MR. Fifty years of the asebia mouse: origins, insights and contemporary developments. Exp Dermatol. 2015;24:340–1.
doi: 10.1111/exd.12664
pubmed: 25683366
Kottke MD, Delva E, Kowalczyk AP. The desmosome: cell science lessons from human diseases. J Cell Sci. 2006;119:797–806.
doi: 10.1242/jcs.02888
pubmed: 16495480
Delva E, Tucker DK, Kowalczyk AP. The desmosome. Cold Spring Harb Perspect Biol. 2009;1:a002543. https://doi.org/10.1101/cshperspect.a002543 .
doi: 10.1101/cshperspect.a002543
pubmed: 20066089
pmcid: 2742091
Hatzfeld M, Keil R, Magin TM. Desmosomes and intermediate filaments: their consequences for tissue mechanics. Cold Spring Harb Perspect Biol. 2017. https://doi.org/10.1101/cshperspect.a029157 .
doi: 10.1101/cshperspect.a029157
pubmed: 28096266
pmcid: 5453391
Angulo-Urarte A, van der Wal T, Huveneers S. Cell-cell junctions as sensors and transducers of mechanical forces. Biochim Biophys Acta Biomembr. 2020;1862:183316. https://doi.org/10.1016/j.bbamem.2020.183316 .
doi: 10.1016/j.bbamem.2020.183316
pubmed: 32360073
Takeichi M. Dynamic contacts: rearranging adherens junctions to drive epithelial remodelling. Nat Rev Mol Cell Biol. 2014;15:397–410.
doi: 10.1038/nrm3802
pubmed: 24824068
Schneider MR, Kolligs FT. E-cadherin’s role in development, tissue homeostasis and disease: insights from mouse models. BioEssays. 2015;37:294–304.
doi: 10.1002/bies.201400141
pubmed: 25449798
Miroshnikova YA, Le HQ, Schneider D, Thalheim T, Rübsam M, Bremicker N, et al. Adhesion forces and cortical tension couple cell proliferation and differentiation to drive epidermal stratification. Nat Cell Biol. 2018;20:69–80. https://doi.org/10.1038/s41556-017-0005-z .
doi: 10.1038/s41556-017-0005-z
pubmed: 29230016
Yoshida K, Yokouchi M, Nagao K, Ishii K, Amagai M, Kubo A. Functional tight junction barrier localizes in the second layer of the stratum granulosum of human epidermis. J Dermatol Sci. 2013;71:89–99. https://doi.org/10.1016/j.jdermsci.2013.04.021 .
doi: 10.1016/j.jdermsci.2013.04.021
pubmed: 23712060
Citi S. The mechanobiology of tight junctions. Biophys Rev. 2019;11:783–93. https://doi.org/10.1007/s12551-019-00582-7 .
doi: 10.1007/s12551-019-00582-7
pubmed: 31586306
pmcid: 6815314
Nielsen MS, Axelsen LN, Sorgen PL, Verma V, Delmar M, Holstein-Rathlou NH. Gap junctions. Compr Physiol. 2012;2:1981–2035. https://doi.org/10.1002/cphy.c110051 .
doi: 10.1002/cphy.c110051
pubmed: 23723031
Goodenough DA, Paul DL. Gap junctions. Cold Spring Harb Perspect Biol. 2009;1:a002576. https://doi.org/10.1101/cshperspect.a002576 .
doi: 10.1101/cshperspect.a002576
pubmed: 20066080
pmcid: 2742079
Berrier AL, Yamada KM. Cell-matrix adhesion. J Cell Physiol. 2007;213:565–73. https://doi.org/10.1002/jcp.21237 .
doi: 10.1002/jcp.21237
pubmed: 17680633
Di Wu, Yamada KM, Wang S. Tissue morphogenesis through dynamic cell and matrix interactions. Annu Rev Cell Dev Biol. 2023;39:123–44. https://doi.org/10.1146/annurev-cellbio-020223-031019 .
doi: 10.1146/annurev-cellbio-020223-031019
Walma DAC, Yamada KM. The extracellular matrix in development. Development. 2020. https://doi.org/10.1242/dev.175596 .
doi: 10.1242/dev.175596
pubmed: 32467294
pmcid: 7272360
Kanchanawong P, Calderwood DA. Organization, dynamics and mechanoregulation of integrin-mediated cell-ECM adhesions. Nat Rev Mol Cell Biol. 2023;24:142–61. https://doi.org/10.1038/s41580-022-00531-5 .
doi: 10.1038/s41580-022-00531-5
pubmed: 36168065
Zuidema A, Wang W, Sonnenberg A. Crosstalk between cell adhesion complexes in regulation of mechanotransduction. BioEssays. 2020;42:e2000119. https://doi.org/10.1002/bies.202000119 .
doi: 10.1002/bies.202000119
pubmed: 32830356
Joost S, Zeisel A, Jacob T, Sun X, La Manno G, Lönnerberg P, et al. Single-cell transcriptomics reveals that differentiation and spatial signatures shape epidermal and hair follicle heterogeneity. Cell Syst. 2016;3:221–237.e9. https://doi.org/10.1016/j.cels.2016.08.010 .
doi: 10.1016/j.cels.2016.08.010
pubmed: 27641957
pmcid: 5052454
Cheng JB, Sedgewick AJ, Finnegan AI, Harirchian P, Lee J, Kwon S, et al. Transcriptional programming of normal and inflamed human epidermis at single-cell resolution. Cell Rep. 2018;25:871–83. https://doi.org/10.1016/j.celrep.2018.09.006 .
doi: 10.1016/j.celrep.2018.09.006
pubmed: 30355494
pmcid: 6367716
Thalheim T, Schneider MR. Skin single-cell transcriptomics reveals a core of sebaceous gland-relevant genes shared by mice and humans. BMC Genomics. 2024;25:137. https://doi.org/10.1186/s12864-024-10008-8 .
doi: 10.1186/s12864-024-10008-8
pubmed: 38310227
pmcid: 10837983
Schäbitz A, Hillig C, Mubarak M, Jargosch M, Farnoud A, Scala E, et al. Spatial transcriptomics landscape of lesions from non-communicable inflammatory skin diseases. Nat Commun. 2022;13:7729. https://doi.org/10.1038/s41467-022-35319-w .
doi: 10.1038/s41467-022-35319-w
pubmed: 36513651
pmcid: 9747967
Seiringer P, Hillig C, Schäbitz A, Jargosch M, Pilz AC, Eyerich S, et al. Spatial transcriptomics reveals altered lipid metabolism and inflammation-related gene expression of sebaceous glands in psoriasis and atopic dermatitis. Front Immunol. 2024;15:1334844. https://doi.org/10.3389/fimmu.2024.1334844 .
doi: 10.3389/fimmu.2024.1334844
pubmed: 38433843
pmcid: 10904577
Hibbs RG. Electron microscopy of human axillary sebaceous glands. J Invest Dermatol. 1962;38:329–36.
doi: 10.1038/jid.1962.60
pubmed: 13907171
Cashion PD, Skobe Z, Nalbandian J. Ultrastructural observations on sebaceous glands of the human oral mucosa (fordyce’s “disease”). J Invest Dermatol. 1969;53:208–16. https://doi.org/10.1038/jid.1969.135 .
doi: 10.1038/jid.1969.135
pubmed: 5809824
Bell M. A comparative study of the ultrastructure of the sebaceous glands of man and other primates. J Invest Dermatol. 1974;62:132–43. https://doi.org/10.1111/1523-1747.ep12676777 .
doi: 10.1111/1523-1747.ep12676777
pubmed: 4361982
Taha AA. Ultrastructure of the sebaceous glands of the camel (Camelus dromedarius). J Anat. 1988;156:157–68.
pubmed: 3417542
pmcid: 1261919
Liu Y, Butovich IA, Garreis F, Zahn I, Scholz M, Gaffling S, et al. Comparative characterization of human meibomian glands, free sebaceous glands, and hair-associated sebaceous glands based on biomarkers, analysis of secretion composition, and gland morphology. Int J Mol Sci. 2024. https://doi.org/10.3390/ijms25063109 .
doi: 10.3390/ijms25063109
pubmed: 39273704
pmcid: 11396332
Brennan D, Hu Y, Kljuic A, Choi Y, Joubeh S, Bashkin M, et al. Differential structural properties and expression patterns suggest functional significance for multiple mouse desmoglein 1 isoforms. Differentiation; research in biological diversity. 2004;72:434–49. https://doi.org/10.1111/j.1432-0436.2004.07208009.x .
doi: 10.1111/j.1432-0436.2004.07208009.x
pubmed: 15606502
Lee JYW, McGrath JA. Mutations in genes encoding desmosomal proteins: spectrum of cutaneous and extracutaneous abnormalities. Br J Dermatol. 2021;184:596–605. https://doi.org/10.1111/bjd.19342 .
doi: 10.1111/bjd.19342
pubmed: 32593191
Vanslembrouck B, Chen J-H, Larabell C, van Hengel J. Microscopic visualization of cell-cell adhesion complexes at micro and nanoscale. Frontiers in cell and developmental biology. 2022;10:819534. https://doi.org/10.3389/fcell.2022.819534 .
doi: 10.3389/fcell.2022.819534
pubmed: 35517500
pmcid: 9065677
Tinkle CL, Lechler T, Pasolli HA, Fuchs E. Conditional targeting of E-cadherin in skin: insights into hyperproliferative and degenerative responses. Proc Natl Acad Sci U S A. 2004;101:552–7.
doi: 10.1073/pnas.0307437100
pubmed: 14704278
pmcid: 327185
Kitson N, van Lennep EW, Young JA. Gap junctions in human sebaceous glands. Cell Tissue Res. 1978;190:115–21. https://doi.org/10.1007/BF00210041 .
doi: 10.1007/BF00210041
pubmed: 688331
Kitson N, van Lennep EW. Intercellular junctions and the permeability barrier in human sebaceous glands. Br J Dermatol. 1984;110:601–6. https://doi.org/10.1111/j.1365-2133.1984.tb04684.x .
doi: 10.1111/j.1365-2133.1984.tb04684.x
pubmed: 6722029
Raschperger E, Engstrom U, Pettersson RF, Fuxe J. CLMP, a novel member of the CTX family and a new component of epithelial tight junctions. J Biol Chem. 2004;279:796–804. https://doi.org/10.1074/jbc.M308249200 .
doi: 10.1074/jbc.M308249200
pubmed: 14573622
Eguchi J, Wada J, Hida K, Zhang H, Matsuoka T, Baba M, et al. Identification of adipocyte adhesion molecule (ACAM), a novel CTX gene family, implicated in adipocyte maturation and development of obesity. Biochem J. 2005;387:343–53. https://doi.org/10.1042/BJ20041709 .
doi: 10.1042/BJ20041709
pubmed: 15563274
pmcid: 1134962
Ahmed SM, Macara IG. Mechanisms of polarity protein expression control. Curr Opin Cell Biol. 2016;42:38–45. https://doi.org/10.1016/j.ceb.2016.04.002 .
doi: 10.1016/j.ceb.2016.04.002
pubmed: 27092866
pmcid: 5064826
Martin PE, Easton JA, Hodgins MB, Wright CS. Connexins: sensors of epidermal integrity that are therapeutic targets. FEBS Lett. 2014;588:1304–14. https://doi.org/10.1016/j.febslet.2014.02.048 .
doi: 10.1016/j.febslet.2014.02.048
pubmed: 24607543
Salomon D, Masgrau E, Vischer S, Ullrich S, Dupont E, Sappino P, et al. Topography of mammalian connexins in human skin. J Invest Dermatol. 1994;103:240–7. https://doi.org/10.1111/1523-1747.ep12393218 .
doi: 10.1111/1523-1747.ep12393218
pubmed: 7518858
Faniku C, Wright CS, Martin PE. Connexins and pannexins in the integumentary system: the skin and appendages. Cell Mol Life Sci. 2015;72:2937–47. https://doi.org/10.1007/s00018-015-1969-0 .
doi: 10.1007/s00018-015-1969-0
pubmed: 26091749
pmcid: 11113313
Masgrau-Peya E, Salomon D, Saurat JH, Meda P. In vivo modulation of connexins 43 and 26 of human epidermis by topical retinoic acid treatment. The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society. 1997;45:1207–15. https://doi.org/10.1177/002215549704500904 .
doi: 10.1177/002215549704500904
pubmed: 9283608
Cowan KN, Langlois S, Penuela S, Cowan BJ, Laird DW. Pannexin1 and Pannexin3 exhibit distinct localization patterns in human skin appendages and are regulated during keratinocyte differentiation and carcinogenesis. Cell Commun Adhes. 2012;19:45–53. https://doi.org/10.3109/15419061.2012.712575 .
doi: 10.3109/15419061.2012.712575
pubmed: 22947051
Brakebusch C, Grose R, Quondamatteo F, Ramirez A, Jorcano JL, Pirro A, et al. Skin and hair follicle integrity is crucially dependent on beta 1 integrin expression on keratinocytes. EMBO J. 2000;19:3990–4003.
doi: 10.1093/emboj/19.15.3990
pubmed: 10921880
pmcid: 306586
Le Coq J, Acebrón I, Rodrigo Martin B, López Navajas P, Lietha D. New insights into FAK structure and function in focal adhesions. J Cell Sci. 2022. https://doi.org/10.1242/jcs.259089 .
doi: 10.1242/jcs.259089
pubmed: 36239192
Jung YR, Hwang C, Ha J-M, Choi D-K, Sohn K-C, Lee Y, et al. Hyaluronic acid decreases lipid synthesis in sebaceous glands. J Invest Dermatol. 2017;137:1215–22. https://doi.org/10.1016/j.jid.2017.01.017 .
doi: 10.1016/j.jid.2017.01.017
pubmed: 28163068
Buechner S, Erne P, Resink TJ. T-cadherin expression in the epidermis and adnexal structures of normal skin. Dermatopathology (Basel). 2016;3:68–78. https://doi.org/10.1159/000451024 .
doi: 10.1159/000451024
pubmed: 27904857
Colas C, Ung PMU, Schlessinger A. SLC transporters: structure, function, and drug discovery. Medchemcomm. 2016;7:1069–81. https://doi.org/10.1039/C6MD00005C .
doi: 10.1039/C6MD00005C
pubmed: 27672436