Tenascin-C Expressing Touch Dome Keratinocytes Exhibit Characteristics of All Epidermal Lineages

Overview

Journal Sci Adv

Specialties Biology
Science

Date 2024 Jan 19

PMID 38241368

Authors

Minh Binh Nguyen

Pooja Flora

Meagan C Branch

Madison Weber

Xiang Yu Zheng

Unnikrishnan Sivan

Simon Joost

Karl Annusver

Deyou Zheng

Maria Kasper

Elena Ezhkova

Affiliations

Soon will be listed here.

Abstract

The touch dome (TD) keratinocytes are specialized epidermal cells that intimately associate with the light touch sensing Merkel cells (MCs). The TD keratinocytes function as a niche for the MCs and can induce de novo hair follicles upon stimulation; however, how the TD keratinocytes are maintained during homeostasis remains unclear. scRNA-seq identified a specific TD keratinocyte marker, (TNC). Lineage tracing of -expressing TD keratinocytes revealed that these cells maintain themselves as an autonomous epidermal compartment and give rise to MCs upon injury. Molecular characterization uncovered that, while the transcriptional and chromatin landscape of the TD keratinocytes is remarkably similar to that of the interfollicular epidermal keratinocytes, it also shares certain molecular signatures with the hair follicle keratinocytes. Our study highlights that the TD keratinocytes in the adult skin have molecular characteristics of keratinocytes of diverse epidermal lineages.

Citing Articles

Screening and expression validation of key proteins for secondary hair follicle growth in cashmere goats based on iTRAQ quantitative proteomics technology.

Chang J, Meng F, Zhang R, Feng J, Liu Y, Zhang J Front Vet Sci. 2024; 11:1441074.

PMID: 39474271 PMC: 11520223. DOI: 10.3389/fvets.2024.1441074.

References

Hoffman B, Baba Y, Griffith T, Mosharov E, Woo S, Roybal D . Merkel Cells Activate Sensory Neural Pathways through Adrenergic Synapses. Neuron. 2018; 100(6):1401-1413.e6. PMC: 6347413. DOI: 10.1016/j.neuron.2018.10.034. View

Ieda M, Fukuda K, Hisaka Y, Kimura K, Kawaguchi H, Fujita J . Endothelin-1 regulates cardiac sympathetic innervation in the rodent heart by controlling nerve growth factor expression. J Clin Invest. 2004; 113(6):876-84. PMC: 362115. DOI: 10.1172/JCI19480. View

Brose K, Bland K, Wang K, Arnott D, Henzel W, Goodman C . Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell. 1999; 96(6):795-806. DOI: 10.1016/s0092-8674(00)80590-5. View

Nunzi M, Pisarek A, Mugnaini E . Merkel cells, corpuscular nerve endings and free nerve endings in the mouse palatine mucosa express three subtypes of vesicular glutamate transporters. J Neurocytol. 2004; 33(3):359-76. DOI: 10.1023/B:NEUR.0000044196.45602.92. View

Ghuwalewala S, Lee S, Jiang K, Baidya J, Chovatiya G, Kaur P . Binary organization of epidermal basal domains highlights robustness to environmental exposure. EMBO J. 2022; 41(18):e110488. PMC: 9475544. DOI: 10.15252/embj.2021110488. View

Weber M, Nguyen M, Li M, Flora P, Shuda M, Ezhkova E . Merkel Cell Polyomavirus T Antigen-Mediated Reprogramming in Adult Merkel Cell Progenitors. J Invest Dermatol. 2023; 143(11):2163-2176.e6. PMC: 10592583. DOI: 10.1016/j.jid.2023.04.031. View

Li B, Dewey C . RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011; 12:323. PMC: 3163565. DOI: 10.1186/1471-2105-12-323. View

Ahn S, Joyner A . Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell. 2004; 118(4):505-16. DOI: 10.1016/j.cell.2004.07.023. View

Feng J, Zhao Y, Xie Z, Zang K, Sviben S, Hu X . Miswiring of Merkel cell and pruriceptive C fiber drives the itch-scratch cycle. Sci Transl Med. 2022; 14(653):eabn4819. PMC: 9888006. DOI: 10.1126/scitranslmed.abn4819. View

10.

Xiao Y, Thoresen D, Williams J, Wang C, Perna J, Petrova R . Neural Hedgehog signaling maintains stem cell renewal in the sensory touch dome epithelium. Proc Natl Acad Sci U S A. 2015; 112(23):7195-200. PMC: 4466733. DOI: 10.1073/pnas.1504177112. View

11.

Van Keymeulen A, Mascre G, Youseff K, Harel I, Michaux C, De Geest N . Epidermal progenitors give rise to Merkel cells during embryonic development and adult homeostasis. J Cell Biol. 2009; 187(1):91-100. PMC: 2762088. DOI: 10.1083/jcb.200907080. View

12.

Mardaryev A, Meier N, Poterlowicz K, Sharov A, Sharova T, Ahmed M . Lhx2 differentially regulates Sox9, Tcf4 and Lgr5 in hair follicle stem cells to promote epidermal regeneration after injury. Development. 2011; 138(22):4843-52. PMC: 4067271. DOI: 10.1242/dev.070284. View

13.

He W, Xie Q, Wang Y, Chen J, Zhao M, Davis L . Generation of a tenascin-C-CreER2 knockin mouse line for conditional DNA recombination in renal medullary interstitial cells. PLoS One. 2013; 8(11):e79839. PMC: 3823583. DOI: 10.1371/journal.pone.0079839. View

14.

Rosenblum M, Olasz E, Yancey K, Woodliff J, Lazarova Z, Gerber K . Expression of CD200 on epithelial cells of the murine hair follicle: a role in tissue-specific immune tolerance?. J Invest Dermatol. 2004; 123(5):880-7. DOI: 10.1111/j.0022-202X.2004.23461.x. View

15.

Feng J, Luo J, Yang P, Du J, Kim B, Hu H . Piezo2 channel-Merkel cell signaling modulates the conversion of touch to itch. Science. 2018; 360(6388):530-533. PMC: 6114129. DOI: 10.1126/science.aar5703. View

16.

Chanda K, Das S, Chakraborty J, Bucha S, Maitra A, Chatterjee R . Altered Levels of Long NcRNAs Meg3 and Neat1 in Cell And Animal Models Of Huntington's Disease. RNA Biol. 2018; 15(10):1348-1363. PMC: 6284602. DOI: 10.1080/15476286.2018.1534524. View

17.

Woo S, Stumpfova M, Jensen U, Lumpkin E, Owens D . Identification of epidermal progenitors for the Merkel cell lineage. Development. 2010; 137(23):3965-71. PMC: 2976280. DOI: 10.1242/dev.055970. View

18.

Feng J, Liu T, Qin B, Zhang Y, Liu X . Identifying ChIP-seq enrichment using MACS. Nat Protoc. 2012; 7(9):1728-40. PMC: 3868217. DOI: 10.1038/nprot.2012.101. View

19.

Wright M, Logan G, Bolock A, Kubicki A, Hemphill J, Sanders T . Merkel cells are long-lived cells whose production is stimulated by skin injury. Dev Biol. 2016; 422(1):4-13. PMC: 5253117. DOI: 10.1016/j.ydbio.2016.12.020. View

20.

Ploner M, Schmitz F, Freund H, Schnitzler A . Differential organization of touch and pain in human primary somatosensory cortex. J Neurophysiol. 2000; 83(3):1770-6. DOI: 10.1152/jn.2000.83.3.1770. View