Skin-Resident T Cells Sense Ultraviolet Radiation–Induced Injury and Contribute to DNA Repair
Open accessAbstract
Skin-resident T cells have been shown to play important roles in tissue homeostasis and wound repair, but their role in UV radiation (UVR)–mediated skin injury and subsequent tissue regeneration is less clear. In this study, we demonstrate that acute UVR rapidly activates skin-resident T cells in humans and dendritic epidermal γδ T cells (DETCs) in mice through mechanisms involving the release of ATP from keratinocytes. Following UVR, extracellular ATP leads to an increase in CD69 expression, proliferation, and IL-17 production, and to changes in DETC morphology. Furthermore, we find that the purinergic receptor P2X7 and caspase-1 are necessary for UVR-induced IL-1 production in keratinocytes, which increases IL-17 secretion by DETCs. IL-17, in turn, induces epidermal TNF-related weak inducer of apoptosis and growth arrest and DNA damage–associated gene 45, two molecules linked to the DNA repair response. Finally, we demonstrate that DETCs and human skin-resident T cells limit DNA damage in keratinocytes. Taken together, our findings establish a novel role for skin-resident T cells in the UVR-associated DNA repair response and underscore the importance of skin-resident T cells to overall skin regeneration.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Recent mouse studies revealed that murine β-defensin 3 and Reg3γ, but not S100A8, have wound healing-promoting properties as they could rescue defective wound healing in IL-17A−/− mice, which show defective AMP induction.
“In fact, recent mouse studies further revealed that murine β-defensin 3 (the ortholog of hBD2) and Reg3γ (ortholog of REG3A), but not S100A8, have wound healing-promoting properties as they could rescue defective wound healing in IL-17A−/− mice, which show defective AMP induction.6,30”
From The Innate Immune System in Acute and Chronic Wounds (2016) · cites this paper as [30]
Keratinocytes produce large amounts of IL-1α and less IL-1β, whereas epidermal DCs, called Langerhans cells, as well as wound-infiltrating macrophages produce mostly IL-1β, but not IL-1α.
“Keratinocytes produce large amounts of IL-1α and less IL-1β,30,52 whereas epidermal DCs, called Langerhans cells, as well as wound-infiltrating macrophages produce mostly IL-1β, but not IL-1α.”
From The Innate Immune System in Acute and Chronic Wounds (2016) · cites this paper as [30]
Skin-resident T cells produce increased levels of IL-17A early upon skin injury and UV-induced skin damage.
“Skin-resident T cells produce increased levels of IL-17A early upon skin injury and UV-induced skin damage.25,30”
From The Innate Immune System in Acute and Chronic Wounds (2016) · cites this paper as [30]
Skin injury, induced either by UV radiation, skin irritants, or trauma, has been shown to liberate ATP into the extracellular space, which acts as a trigger for NALP3 inflammasome activation and subsequent IL-1β secretion.
“Furthermore, skin injury, induced either by UV radiation, skin irritants, or trauma, has been shown to liberate ATP into the extracellular space, which acts as a trigger for NALP3 inflammasome activation and subsequent IL-1β secretion.30,52,54”
From The Innate Immune System in Acute and Chronic Wounds (2016) · cites this paper as [30]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage
Paull, T. T., Rogakou, E. P., Yamazaki, V., Kirchgessner, C. U., Gellert, M., & Bonner, W. M. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00610-2 · Cited by 2,098 · see citing works
Pivotal Role of Dermal IL-17-Producing γδ T Cells in Skin Inflammation
Cai, Y., Shen, X., Ding, C., Qi, C., Li, K., Li, X., Jala, V. R., Zhang, H., Wang, T., Zheng, J., et al. (2011) · Immunity · doi:10.1016/j.immuni.2011.08.001 · Cited by 1,031 · see citing works
Regulation of Cutaneous Malignancy by γδ T Cells
Girardi, M., Oppenheim, D. E., Steele, C. R., Lewis, J. M., Glusac, E. J., Filler, R. B., Hobby, P., Sutton, B. J., Tigelaar, R. E., & Hayday, A. (2001) · Science · doi:10.1126/science.1063916 · Cited by 1,002 · see citing works
Distribution and compartmentalization of human circulating and tissue-resident memory T cell subsets
Sathaliyawala, T., Kubota, M., Yudanin, N., Turner, D., Camp, P., Thome, J. J. C., Bickham, K. L., Lerner, H., Goldstein, M., Sykes, M., et al. (2013) · Immunity · doi:10.1016/j.immuni.2012.09.020 · Cited by 848 · see citing works
Immune cell regulation by autocrine purinergic signalling
JUNGER, W. G. (2011) · Nature reviews. Immunology · doi:10.1038/nri2938 · Cited by 813 · see citing works
CCL27–CCR10 interactions regulate T cell–mediated skin inflammation
Homey, B., Alenius, H. T., Müller, A., Soto, H., Bowman, E. P., Yuan, W., McEvoy, L. M., Lauerma, A., Assmann, T., Bünemann, E., et al. (2002) · Nature Medicine · doi:10.1038/nm0202-157 · Cited by 807 · see citing works
The Vast Majority of CLA+ T Cells Are Resident in Normal Skin
Clark, R. A., Chong, B., Mirchandani, N., Brinster, N. K., Yamanaka, K.-I., Dowgiert, R. K., & Kupper, T. S. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.7.4431 · Cited by 796 · see citing works
IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice
Cho, J. S., Pietras, E. M., Garcia, N. C., Ramos, R. I., Farzam, D. M., Monroe, H. R., Magorien, J. E., Blauvelt, A., Kolls, J. K., Cheung, A. L., et al. (2010) · Journal of Clinical Investigation · doi:10.1172/jci40891 · Cited by 658 · see citing works
A Role for Skin γδ T Cells in Wound Repair
Jameson, J., Ugarte, K., Chen, N., Yachi, P. P., Fuchs, E. V., Boismenu, R., & Havran, W. L. (2002) · Science · doi:10.1126/science.1069639 · Cited by 639 · see citing works
Self-citationSmith, M. L., Ford, J. M., Hollander, M. C., Bortnick, R. A., Amundson, S. A., Seo, Y. R., Deng, C., Hanawalt, P. C., & Fornace, A. J. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.10.3705-3714.2000 · Cited by 432 · see citing works
Activation of the IL-1β-Processing Inflammasome Is Involved in Contact Hypersensitivity
Watanabe, H., Gaide, O., Pétrilli, V., Martinon, F., Contassot, E., Roques, S., Kummer, J. A., Tschopp, J., & French, L. E. (2007) · Journal of Investigative Dermatology · doi:10.1038/sj.jid.5700819 · Cited by 416 · see citing works
Vries, A. D., van Oostrom, C. T. M., Hofhuis, F. M. A., Dortant, P. M., Berg, R. J. W., Gruijl, F. R. D., Wester, P. W., van Kreijl, C. F., Capel, P. J. A., Steeg, H. V., et al. (1995) · Nature · doi:10.1038/377169a0 · Cited by 406 · see citing works
Tumor Cell Death and ATP Release Prime Dendritic Cells and Efficient Anticancer Immunity
Aymeric, L., Apétoh, L., Ghiringhelli, F., Tesnière, A., Martins, I., Kroemer, G., Smyth, M. J., & Zitvogel, L. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-3566 · Cited by 380 · see citing works
A role for human skin–resident T cells in wound healing
Toulon, A., Breton, L., Taylor, K. R., Tenenhaus, M., Bhavsar, D., Lanigan, C., Rudolph, R., Jameson, J., & Havran, W. L. (2009) · Journal of Experimental Medicine · doi:10.1084/jem.20081787 · Cited by 339 · see citing works
Self-citationBasal Release of ATP: An Autocrine-Paracrine Mechanism for Cell Regulation
Corriden, R., & Insel, P. A. (2010) · Science Signaling · doi:10.1126/scisignal.3104re1 · Cited by 338 · see citing works
Self-citationWoehrle, T., Yip, L., Elkhal, A., Sumi, Y., Chen, Y., Yao, Y., Insel, P. A., & JUNGER, W. G. (2010) · Blood · doi:10.1182/blood-2010-04-277707 · Cited by 315 · see citing works
Burkly, L. C., Michaelson, J. S., Hahm, K., Jakubowski, A., & Zheng, T. S. (2007) · Cytokine · doi:10.1016/j.cyto.2007.09.007 · Cited by 285 · see citing works
Stimulation of P2 receptors causes release of IL-1β–loaded microvesicles from human dendritic cells
Pizzirani, C., Ferrari, D., Chiozzi, P., Adinolfi, E., Sandonà, D., Savaglio, E., & Virgilio, F. D. (2006) · Blood · doi:10.1182/blood-2005-06-031377 · Cited by 280 · see citing works
Gadd45, a p53-Responsive Stress Protein, Modifies DNA Accessibility on Damaged Chromatin
Carrier, F., Georgel, P. T., Pourquier, P., Blake, M., Kontny, H. U., Antinore, M. J., Gariboldi, M. B., Myers, T. G., Weinstein, J. N., Pommier, Y. G., et al. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.3.1673 · Cited by 277 · see citing works
Cutaneous immunosurveillance by self-renewing dermal γδ T cells
Sumaria, N., Roediger, B., Ng, L. G., Qin, J., Pinto, R., Cavanagh, L. L., Shklovskaya, E., Groth, B. F. D. S., Triccas, J. A., & Weninger, W. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20101824 · Cited by 277 · see citing works
Strid, J., Roberts, S. J., Filler, R. B., Lewis, J. M., Kwong, B. Y., Schpero, W. L., Kaplan, D. H., Hayday, A., & Girardi, M. (2008) · Nature Immunology · doi:10.1038/ni1556 · Cited by 266 · see citing works
Muehlhoefer, A., Saubermann, L. J., Gu, X., Lüedtke-Heckenkamp, K., Xavier, R. J., Blumberg, R. S., Podolsky, D. K., MacDermott, R. P., & Reinecker, H. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.164.6.3368 · Cited by 249 · see citing works
Active DNA demethylation by Gadd45 and DNA repair
Niehrs, C., & Schäfer, A. (2012) · Trends in Cell Biology · doi:10.1016/j.tcb.2012.01.002 · Cited by 248 · see citing works
Clark, R. A., Huang, S. J., Murphy, G. F., Mollet, I. G., Hijnen, D., Muthukuru, M., SCHANBACHER, C. F., Edwards, V. L., Miller, D. M., Kim, J. E., et al. (2008) · The Journal of Experimental Medicine · doi:10.1084/jem.20071190 · Cited by 242 · see citing works
Hildesheim, J., Bulavin, D. V., Anver, M. R., Alvord, W. G., Hollander, M. C., Vardanian, L., & Fornace, A. J. (2002) · PubMed · Cited by 240 · see citing works
Analysis of the mammalian gadd45 gene and its response to DNA damage.
Hollander, M. C., Alamo, I., Jackman, J., Wang, M. G., McBride, O. W., & Fornace, A. J. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(20)80537-7 · Cited by 229 · see citing works
P2X7 receptor regulation of non-classical secretion from immune effector cells
Dubyak, G. (2012) · Cellular Microbiology · doi:10.1111/cmi.12001 · Cited by 189 · see citing works
Adenosine and ATP Receptors in the Brain
Burnstock, G., Fredholm, B. B., & Verkhratsky, A. (2011) · Current Topics in Medicinal Chemistry · doi:10.2174/156802611795347627 · Cited by 188 · see citing works
Inflammasome activation and IL-1β target IL-1α for secretion as opposed to surface expression
Fettelschoss‐Gabriel, A., Kistowska, M., LeibundGut‐Landmann, S., Beer, H., Johansen, P., Senti, G., Contassot, E., Bachmann, M. F., French, L. E., Oxenius, A., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1109176108 · Cited by 169 · see citing works
The CD100 Receptor Interacts with Its Plexin B2 Ligand to Regulate Epidermal γδ T Cell Function
Witherden, D. A., Watanabe, M., Garijo, O., Rieder, S., Sarkisyan, G., Cronin, S. J. F., Verdino, P., Wilson, I. A., Kumanogoh, A., Kikutani, H., et al. (2012) · Immunity · doi:10.1016/j.immuni.2012.05.026 · Cited by 165 · see citing works
Self-citationAltemeier, W. A., Matute‐Bello, G., Gharib, S. A., Glenny, R. W., Martin, T. R., & Liles, W. C. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.5.3369 · Cited by 156 · see citing works
Intestinal epithelial cells as mediators of the commensal–host immune crosstalk
Goto, Y., & Ivanov, I. I. (2013) · Immunology and Cell Biology · doi:10.1038/icb.2012.80 · Cited by 153 · see citing works
Jameson, J., Cauvi, G., Witherden, D. A., & Havran, W. L. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.6.3573 · Cited by 152 · see citing works
Self-citationZerbini, L. F., Wang, Y., Czibere, A. G., Correa, R. G., Cho, J., Ijiri, K., Wei, W., Joseph, M. G., Gu, X., Grall, F. T., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402069101 · Cited by 152 · see citing works
Dendritic epidermal T cells regulate skin antimicrobial barrier function
MacLeod, A. S., Hemmers, S., Garijo, O., Chabod, M., Mowen, K., Witherden, D. A., & Havran, W. L. (2013) · Journal of Clinical Investigation · doi:10.1172/jci70064 · Cited by 152 · see citing works
Self-citationPurinergic Signaling in Healthy and Diseased Skin
Burnstock, G., Knight, G. E., & Greig, A. V. H. (2011) · Journal of Investigative Dermatology · doi:10.1038/jid.2011.344 · Cited by 143 · see citing works
Functions of skin-resident γδ T cells
MacLeod, A. S., & Havran, W. L. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0702-x · Cited by 132 · see citing works
Self-citationInterleukin-1, inflammasomes, autoinflammation and the skin
Contassot, E., Beer, H.-D., & French, L. E. (2012) · Swiss Medical Weekly · doi:10.4414/smw.2012.13590 · Cited by 130 · see citing works
Greig, A. V. H., Linge, C., Terenghi, G., McGrouther, D. A., & Burnstock, G. (2003) · Journal of Investigative Dermatology · doi:10.1046/j.1523-1747.2003.12261.x · Cited by 123 · see citing works
Killeen, M. E., Ferris, L. K., Kupetsky, E. A., Falo, L. D., & Mathers, A. R. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1202045 · Cited by 109 · see citing works
Tessari, G., Naldi, L., Boschiero, L., Nacchia, F., Fior, F., Forni, A., Rugiu, C., Faggian, G. G., Sassi, F., Gotti, E., et al. (2010) · Archives of Dermatology · doi:10.1001/archdermatol.2009.377 · Cited by 87 · see citing works
Fu, W., McCormick, T., Qi, X., Luo, L., Zhou, L., Li, X., Wang, B.-C., Gibbons, H. E., Abdul‐Karim, F. W., & Gorodeski, G. I. (2009) · BMC Cancer · doi:10.1186/1471-2407-9-114 · Cited by 85 · see citing works
Shitara, S., Hara, T., Liang, B., Wagatsuma, K., Žuklys, S., Holländer, G. A., Nakase, H., Chiba, T., Tani‐ichi, S., & Ikuta, K. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1202573 · Cited by 85 · see citing works
The P2X1 receptor and platelet function
Mahaut‐Smith, M. P., Jones, S., & Evans, R. J. (2011) · Purinergic Signalling · doi:10.1007/s11302-011-9224-0 · Cited by 73 · see citing works
No formation of DNA double-strand breaks and no activation of recombination repair with UVA
Rizzo, J. L., Dunn, J., Rees, A., & Rünger, T. M. (2011) · Journal of Investigative Dermatology · doi:10.1038/jid.2010.365 · Cited by 50 · see citing works
Befort, K., Karchewski, L. A., Lanoue, C., & Woolf, C. J. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02827.x · Cited by 49 · see citing works
DNA Repair and Cytokine Responses
Schwarz, T., & Schwarz, A. (2009) · Journal of Investigative Dermatology Symposium Proceedings · doi:10.1038/jidsymp.2009.3 · Cited by 49 · see citing works
Alaoui, S. S., Dessirier, V., de Araujo, E., Alexaki, V. I., Pelekanou, V., Lkhider, M., Stathopoulos, E. N., Castanas, E., Bagot, M., Bensussan, A., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033609 · Cited by 47 · see citing works
Takai, E., Tsukimoto, M., Harada, H., & Kojima, S. (2010) · Radiation Research · doi:10.1667/rr2375.1 · Cited by 35 · see citing works
Murine epidermal Langerhans cells and keratinocytes express functional P2X 7 receptors
Tran, J. N. S. N., Pupovac, A., Taylor, R. M., Wiley, J. S., Byrne, S. N., & Sluyter, R. (2010) · Experimental Dermatology · doi:10.1111/j.1600-0625.2009.01029.x · Cited by 33 · see citing works
Milestones in Photocarcinogenesis
Elmets, C. A., & Athar, M. (2013) · Journal of Investigative Dermatology · doi:10.1038/skinbio.2013.179 · Cited by 33 · see citing works
Griswold, D. E., Connor, J. R., Dalton, B. J., Lee, J. C., Simon, P. L., Hillegass, L. M., Sieg, D. J., & Hanna, N. (1991) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12492422 · Cited by 31 · see citing works
Peternel, S., Manestar-Blažić, T., Brajac, I., Massari, L. P., & Kaštelan, M. (2011) · Journal of Cutaneous Pathology · doi:10.1111/j.1600-0560.2011.01762.x · Cited by 28 · see citing works
Genomic Instability in Gadd45a-/- Cells is Coupled with S-Phase Checkpoint Defects
Hollander, M. C., Philburn, R. T., Patterson, A. D., Wyatt, M. A., & Fornace, A. J. (2005) · Cell Cycle · doi:10.4161/cc.4.5.1675 · Cited by 19 · see citing works
Ultraviolet-Induced Immunosuppression: Implications for Photocarcinogenesis
Beissert, S., & Schwarz, T. (2009) · Cancer treatment and research · doi:10.1007/978-0-387-78574-5_10 · Cited by 15 · see citing works
UV Induces GADD45 in a p53-Dependent and -Independent Manner in Human Keratinocytes
Maeda, T., Sim, A. B., Leedel, D. A., Chua, P., Chomey, E. G., Luong, L., & Tron, V. A. (2003) · Journal of Cutaneous Medicine and Surgery · doi:10.1007/s10227-002-0108-3 · Cited by 12 · see citing works
“Validation” of Outcome Measures in Dermatology
Viola, K. V., Nijsten, T. E. C., & Krishnamurthy, K. (2013) · Journal of Investigative Dermatology · doi:10.1038/jid.2013.332 · Cited by 9 · see citing works
UV Induces GADD45 in a p53-Dependent and -Independent Manner in Human Keratinocytes
Maeda, T., Sim, A. B., Leedel, D. A., et al. (2003) · Journal of Cutaneous Medicine and Surgery · doi:10.1177/120347540300700204 · Cited by 4 · see citing works
Flagged first, then by citations
1 of the 59 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
DAMPs from Cell Death to New Life
Vénéreau, E., Ceriotti, C., & Bianchi, M. E. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00422 · Cited by 666 · see citing works
γδ T cells in tissue physiology and surveillance
Ribot, J. C., Lopes, N., & Silva-Santos, B. (2021) · Nature Reviews Immunology · doi:10.1038/s41577-020-00452-4 · Cited by 532 · see citing works
The Innate Immune System in Acute and Chronic Wounds
MacLeod, A. S., & Mansbridge, J. N. (2016) · Advances in Wound Care · doi:10.1089/wound.2014.0608 · Cited by 289 · see citing works
“Skin-resident T cells produce increased levels of IL-17A early upon skin injury and UV-induced skin damage.(25,30) The requirement for IL-17A for the normal wound healing response has been demonstrated in a mouse model, where IL-17A / - mice showed delayed closure of incisional wounds compared with wild-type controls.”
BackgroundSelf-citationFrom Inflammation to Current and Alternative Therapies Involved in Wound Healing
Serra, M. B., Barroso, W. A., da Silva, N. N., Silva, S. D. N., Borges, A. C. R., Abreu, I. C., & Borges, M. O. D. R. (2017) · International Journal of Inflammation · doi:10.1155/2017/3406215 · Cited by 202 · see citing works
Key Role of DAMP in Inflammation, Cancer, and Tissue Repair
Pandolfi, F., Altamura, S., Frosali, S., & Conti, P. (2016) · Clinical Therapeutics · doi:10.1016/j.clinthera.2016.02.028 · Cited by 191 · see citing works
Wang, Z., Zhou, H., Zheng, H., Zhou, X., Shen, G., Teng, X., Liu, X., Zhang, J., Wei, X., Hu, Z., et al. (2020) · Autophagy · doi:10.1080/15548627.2020.1725381 · Cited by 164 · see citing works
Tissue Adaptations of Memory and Tissue-Resident Gamma Delta T Cells
Khairallah, C. F., Chu, T. H., & Sheridan, B. S. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02636 · Cited by 135 · see citing works
Sand, J., Haertel, E., Biedermann, T., Contassot, E., Ernst Reichmann, A., French, L. E., Werner, S., & Beer, H. (2018) · Cell Death and Disease · doi:10.1038/s41419-017-0009-4 · Cited by 130 · see citing works
Exposure to Ultraviolet Radiation in the Modulation of Human Diseases
Hart, P. H., Norval, M., Byrne, S. N., & Rhodes, L. E. (2018) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathmechdis-012418-012809 · Cited by 133 · see citing works
ATP and Its Metabolite Adenosine as Regulators of Dendritic Cell Activity
Silva-Vilches, C., Ring, S., & Mahnke, K. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02581 · Cited by 127 · see citing works
Skopelja‐Gardner, S., An, J., Tai, J., Tanaka, L., Sun, X., Hermanson, P., Baum, R., Kawasumi, M., Green, R. R., Gale, M., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-64865-w · Cited by 127 · see citing works
Epidermal γδ T cells originate from yolk sac hematopoiesis and clonally self-renew in the adult
Gentek, R., Ghigo, C., Hoeffel, G., Jorquera, A., Msallam, R., Wienert, S., Klauschen, F., Ginhoux, F., & Bajénoff, M. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20181206 · Cited by 111 · see citing works
Ultraviolet Radiation, Vitamin D and Multiple Sclerosis
Lucas, R. M., Byrne, S. N., Correale, J. D., Ilschner, S., & Hart, P. H. (2015) · Neurodegenerative Disease Management · doi:10.2217/nmt.15.33 · Cited by 112 · see citing works
Nuclear envelope rupture and NET formation is driven by PKCα‐mediated lamin B disassembly
Li, Y., Li, M., Weigel, B., Mall, M., Werth, V. P., & Liu, M. (2020) · EMBO Reports · doi:10.15252/embr.201948779 · Cited by 106 · see citing works
Patra, V., Wagner, K., Arulampalam, V., & Wolf, P. (2019) · iScience · doi:10.1016/j.isci.2019.04.026 · Cited by 99 · see citing works
Comparing Mouse and Human Tissue-Resident γδ T Cells
Qu, G., Wang, S., Zhou, Z., Jiang, D., Liao, A., & Luo, J. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.891687 · Cited by 87 · see citing works
“Although DETCs are thymically programmed to produce IFN-g rather than IL-17 in wild-type mice, DETCs on a skint-1-deficient background are primarily committed toward an IL-17 effector phenotype (35, 36).”
BackgroundLitvinov, I. V., Netchiporouk, E., Cordeiro, B., Doré, M.-A., Moreau, L., Pehr, K., Gilbert, M. J., Zhou, Y., Sasseville, D., & Kupper, T. S. (2015) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-14-3322 · Cited by 83 · see citing works
Understanding the mechanism of radiation induced fibrosis and therapy options
Ejaz, A., Greenberger, J. S., & Rubin, P. J. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.107399 · Cited by 73 · see citing works
Normality sensing licenses local T cells for innate-like tissue surveillance
McKenzie, D. R., Hart, R., Bah, N. K., Ushakov, D. S., Muñoz‐Ruiz, M., Feederle, R., & Hayday, A. (2022) · Nature Immunology · doi:10.1038/s41590-021-01124-8 · Cited by 71 · see citing works
Wound healing in cutaneous leishmaniasis: A double edged sword of IL-10 and TGF-β
Abdoli, A., Maspi, N., & Ghaffarifar, F. (2017) · Comparative Immunology Microbiology and Infectious Diseases · doi:10.1016/j.cimid.2017.02.001 · Cited by 64 · see citing works
Wolf, S., Estadt, S. N., Theros, J. S., Moore, T., Ellis, J. S., Liu, J. J., Reed, T. J., Jacob, C. O., Gudjonsson, J. E., & Kahlenberg, J. M. (2019) · Journal of Autoimmunity · doi:10.1016/j.jaut.2019.06.002 · Cited by 64 · see citing works
Tissue-resident memory T cells in the skin
Khalil, S., Bardawil, T., Kurban, M., & Abbas, O. M. (2020) · Inflammation Research · doi:10.1007/s00011-020-01320-6 · Cited by 62 · see citing works
Zhang, B., Wu, J., Jiao, Y., Bock, C. B., Dai, M., Chen, B., Chao, N. J. A., Zhang, W., & Zhuang, Y. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1501220 · Cited by 61 · see citing works
IL-27 Facilitates Skin Wound Healing through Induction of Epidermal Proliferation and Host Defense
Yang, B., Suwanpradid, J., Lagunes, R. S., Choi, H. W., Hoang, P., Wang, D., Abraham, S. N., & MacLeod, A. S. (2017) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2017.01.010 · Cited by 55 · see citing works
Self-citationVieyra-Garcia, P. A., & Wolf, P. (2018) · Frontiers in Medicine · doi:10.3389/fmed.2018.00232 · Cited by 47 · see citing works
Suwanpradid, J., Shih, M., Pontius, L. N., Yang, B., Birukova, A., Guttman‐Yassky, E., Corcoran, D. L., Que, L. G., Tighe, R. M., & MacLeod, A. S. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1700739 · Cited by 45 · see citing works
Self-citationLai, C., Coltart, G. S., Shapanis, A. G., Healy, C., Alabdulkareem, A., Selvendran, S., Theaker, J. M., Sommerlad, M., Rose-Zerilli, M. J. J., Al‐Shamkhani, A., et al. (2021) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2020-001807 · Cited by 46 · see citing works
The Role of Tissue-resident γδ T Cells in Stress Surveillance and Tissue Maintenance
Johnson, M. D., Witherden, D. A., & Havran, W. L. (2020) · Cells · doi:10.3390/cells9030686 · Cited by 44 · see citing works
Self-citationPatra, V., Laoubi, L., Nicolas, J.-F., Vocanson, M., & Wolf, P. (2018) · Frontiers in Medicine · doi:10.3389/fmed.2018.00166 · Cited by 42 · see citing works
Human and Murine Evidence for Mechanisms Driving Autoimmune Photosensitivity
Wolf, S., Estadt, S. N., Gudjonsson, J. E., & Kahlenberg, J. M. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02430 · Cited by 41 · see citing works
Mechanisms of Photosensitivity in Autoimmunity
Estadt, S. N., Maz, M. P., Musai, J., & Kahlenberg, J. M. (2021) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2021.05.007 · Cited by 37 · see citing works
Emerging Skin T-Cell Functions in Response to Environmental Insults
Suwanpradid, J., Holcomb, Z. E., & MacLeod, A. S. (2016) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2016.08.013 · Cited by 33 · see citing works
Self-citationLangerhans Cells Facilitate UVB-Induced Epidermal Carcinogenesis
Lewis, J. M., Bürgler, C. D., Freudzon, M., Golubets, K., Gibson, J. F., Filler, R. B., & Girardi, M. (2015) · Journal of Investigative Dermatology · doi:10.1038/jid.2015.207 · Cited by 30 · see citing works
γδT Cells and Related Diseases
Han, L., Li, D., & Jin, L. (2016) · American Journal of Reproductive Immunology · doi:10.1111/aji.12495 · Cited by 27 · see citing works
Sulfation degree not origin of chondroitin sulfate derivatives modulates keratinocyte response
Corsuto, L., Rother, S., Koehler, L., Bedini, E., Moeller, S. J., Schnabelrauch, M., Hintze, V., Schiraldi, C., & Scharnweber, D. (2018) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2018.02.072 · Cited by 27 · see citing works
Current concepts of photosensitivity in cutaneous lupus erythematosus
Klein, B., & Kunz, M. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.939594 · Cited by 23 · see citing works
Dendritic epidermal T cells facilitate wound healing in diabetic mice.
Liu, Z., Xu, Y., Chen, L., Xie, J., Tang, J., Zhao, J., Shu, B., Qi, S., Chen, J., Liang, G., et al. (2016) · PubMed Central · Cited by 22 · see citing works
P2X7 receptor in skin biology and diseases
Geraghty, N. J., Watson, D., Adhikary, S. R., & Sluyter, R. (2016) · World Journal of Dermatology · doi:10.5314/wjd.v5.i2.72 · Cited by 21 · see citing works
Phototherapy in the perspective of the chronicity of psoriasis
van de Kerkhof, P. C. M., & de Gruijl, F. R. (2020) · Journal of the European Academy of Dermatology and Venereology · doi:10.1111/jdv.16245 · Cited by 21 · see citing works
A promising sword of tomorrow: Human γδ T cell strategies reconcile allo-HSCT complications
Hu, Y., Cui, Q., Luo, C., Luo, Y., Shi, J., & Huang, H. (2015) · Blood Reviews · doi:10.1016/j.blre.2015.11.002 · Cited by 20 · see citing works
Patra, V., Strobl, J., Atzmüller, D., Reininger, B., Kleißl, L., Gruber‐Wackernagel, A., Nicolas, J., Stary, G., Vocanson, M., & Wolf, P. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.908047 · Cited by 19 · see citing works
γδ T Cells in Skin Inflammation
Zhang, W., Pajulas, A., & Kaplan, M. H. (2022) · Critical Reviews in Immunology · doi:10.1615/critrevimmunol.2022047288 · Cited by 19 · see citing works
Sil, P., Suwanpradid, J., Muse, G. W., Gruzdev, A., Liu, L., Corcoran, D. L., Willson, C. J., Janardhan, K. S., Grimm, S. A., Myers, P., et al. (2019) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2019.11.041 · Cited by 20 · see citing works
Self-citationRetractedWhitley, M. J., Suwanpradid, J., Lai, C., Jiang, S. W., Cook, J. L., Zelac, D. E., Rudolph, R., Corcoran, D. L., Degan, S., Spasojevic, I., et al. (2021) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2021.02.753 · Cited by 19 · see citing works
Self-citationThe symbiosis of phototherapy and photoimmunology
Matos, T. R., & Sheth, V. M. (2016) · Clinics in Dermatology · doi:10.1016/j.clindermatol.2016.05.003 · Cited by 19 · see citing works
Soares‐da‐Silva, F., Elsaid, R., Peixoto, M. M., Nogueira, G., Pereira, P., Bandeira, A., & Cumano, A. (2023) · Immunological Reviews · doi:10.1111/imr.13187 · Cited by 16 · see citing works
Geraghty, N. J., Mansfield, K. J., Fuller, S. J., Watson, D., & Sluyter, R. (2017) · Purinergic Signalling · doi:10.1007/s11302-017-9569-0 · Cited by 16 · see citing works
Photodistributed toxic epidermal necrolysis in association with lamotrigine and tanning bed exposure
Russomanno, K., DiLorenzo, A. M., Horeczko, J., Deng, M., Cardis, M. A., Petronic-Rosic, V. M., Johnson, L. S., & Pasieka, H. B. (2021) · JAAD Case Reports · doi:10.1016/j.jdcr.2021.05.015 · Cited by 15 · see citing works
Role of Dendritic Epidermal T Cells in Cutaneous Carcinoma
Xiang, J., Qiu, M., & Zhang, H. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01266 · Cited by 11 · see citing works
Koelsch, N. J., & Manjili, M. H. (2025) · British Journal of Cancer · doi:10.1038/s41416-025-03133-y · Cited by 10 · see citing works
Kim, J., Kim, H., Yoo, D., Park, K., Kwon, H., Seo, J., Kim, T. H., Yoon, J., Seong, S. H., Jang, M., et al. (2022) · Photodermatology Photoimmunology & Photomedicine · doi:10.1111/phpp.12848 · Cited by 10 · see citing works
Beserra, F. P., Gushiken, L. F. S., Hussni, M. F., & Pellizzon, C. H. (2018) · Wound Healing - Current Perspectives · doi:10.5772/intechopen.81731 · Cited by 14 · see citing works
Hart, P. H., & Norval, M. (2019) · Immunology · doi:10.1111/imm.13128 · Cited by 8 · see citing works
He, J., Guo, Y., Chen, J., Xu, J., & Zhu, X. (2025) · Journal of Autoimmunity · doi:10.1016/j.jaut.2025.103393 · Cited by 7 · see citing works
Purnami, S., Masneli, L., Suryadi, S., & Syaifudin, M. (2020) · Journal of Physics Conference Series · doi:10.1088/1742-6596/1436/1/012032 · Cited by 7 · see citing works
Inflammation in Wound Repair: Role and Function of Inflammation in Wound Repair
MacLeod, A. S., & Kwock, J. T. (2017) · Wiley eBooks · doi:10.1002/9781119282518.ch14 · Cited by 7 · see citing works
Self-citationThe Role of Extracellular ATP in the Regulation of Functional Cell Activity
Patrakeeva, V. P. (2025) · Cell and Tissue Biology · doi:10.1134/s1990519x25030022 · Cited by 6 · see citing works
Li, J., Tang, Y., Chen, P., Ding, Z., & Zhou, M. (2025) · Radiation Medicine and Protection · doi:10.1016/j.radmp.2025.09.005 · Cited by 4 · see citing works
Perish in the Attempt: Regulated Cell Death in Regenerative and Nonregenerative Tissue
Li, S., & Tao, G. (2023) · Antioxidants and Redox Signaling · doi:10.1089/ars.2022.0166 · Cited by 4 · see citing works
Abbasabadi, O. R., & Farahpour, M. R. (2023) · The International Journal of Lower Extremity Wounds · doi:10.1177/15347346231212331 · Cited by 4 · see citing works
Roles of dendritic epidermal T cells in steady and different pathological states
Hao, J., Zhang, J., & Liu, Y. (2024) · Burns & Trauma · doi:10.1093/burnst/tkae056 · Cited by 3 · see citing works
From neglect to necessity: the role of innate immunity in cutaneous squamous cell carcinoma therapy
He, Y., Tian, T., Li, Y., Zeng, Y., Wang, X., Qian, L., Tian, T., Jiang, M., & Li, L. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1570032 · Cited by 3 · see citing works
γδ T cells monitor tissue health
Subudhi, I., & Naik, S. (2022) · Nature Immunology · doi:10.1038/s41590-022-01139-9 · Cited by 2 · see citing works
Kabbani, M. S., Евгеньевна, Ф. О., Shashkova, E. Y., Men’shikova, M. V., & Shchegoleva, L. S. (2020) · Journal of Medical and Biological Research · doi:10.37482/2687-1491-z027 · Cited by 1 · see citing works
He, Y., Yu, L., Wu, W., Li, Y., Zhu, W., Zhang, X., Ma, Y., & Zhang, L. (2026) · Photochemical & Photobiological Sciences · doi:10.1007/s43630-026-00880-6 · Cited by 1 · see citing works
Gamma-Delta T Cells in the Skin
Tan, S., Tay, S. S., Sumaria, N., Roediger, B., & Weninger, W. (2017) · Springer eBooks · doi:10.1007/978-3-319-29785-9_4 · Cited by 1 · see citing works
ÚLCERA DO PÉ DIABÉTICO (UDP) NO DIABETES MELLITUS 2: UMA ABORDAGEM MOLECULAR
de Carvalho, L. A. N., & Carneiro, M. L. B. (1970) · Hegemonia Revista de Ciências Sociais · doi:10.47695/hegemonia.vi27.290 · Cited by 1 · see citing works
Lilyquist, J. (2015) · UNM’s Digital Repository (University of New Mexico)
The Role of Type I Interferons in TLR7-Mediated Lupus and UVB-Induced Immune Cell Responses
Wolf, S. (2019) · Deep Blue (University of Michigan)
Adipose-derived stem cells for wound healing and fibrosis
Samadi, Y., Egro, F. M., Rodriguez, R. L., & Ejaz, A. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-819376-1.00005-6
The role of extracellular ATP in regulating the functional activity of cells
Patrakeeva, V. P. (2024) · Сибирский научный медицинский журнал · doi:10.18699/ssmj20240506
Gut Microbiota Regulates the Homeostasis of Dendritic Epidermal T Cells
Chung, J., Lee, J.-C., Oh, H., Kim, Y., Lim, S., Lee, C., Shim, Y.-G., Bang, E.-C., & Baek, J.-H. (2024) · Life · doi:10.3390/life14121695
Goudarzi, A. S., Sadraie, S. H., Kaka, G., Aghamolaei, H., & Jalali, B. (2025) · International Immunopharmacology · doi:10.1016/j.intimp.2025.115028
Mécanismes de l'immunothérapie épicutanée des allergies alimentaires
Laoubi, L. (2020) · theses.fr (ABES) · doi:10.70675/848d7714za7e9z43d9zacaez47cd7d35182d
P2X7R in skin diseases: Pathological mechanisms and therapeutic potential
Liu, W. T., Tian, Z., Zhang, L., Ni, B., & Song, Z. (2026) · Genes & Diseases · doi:10.1016/j.gendis.2026.102347
CD8 + Tissue‐Resident Memory T Cells in Health and Disease
Ai, Y.-H., Xu, T., Lin, S., Xiao, M., Lin, Y.-X., Ma, H. Y., Liu, Y., Wang, Y., Yin, L., Huang, M., et al. (2026) · MedComm · doi:10.1002/mco2.70838
Jiao, Z., Wang, H., Meng, X., Yang, M., Dai, C., Zhu, Z., Guo, X., Yang, P., & Lu, Y. (2026) · Veterinary Sciences · doi:10.3390/vetsci13090854
- Authors
- MacLeod, A. S., Rudolph, R., Corriden, R., Ye, I., Garijo, O., & Havran, W. L.
- Affiliations
- Scripps Research Institute (US)
- University of California San Diego (US)
- Corresponding author
- Ye, Ivan
- Garijo, Olivia
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-06
- Volume
- 192
- Issue
- 12
- Pages
- 5695-5702
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- PMC
- PMC4048764
- OpenAlex
- W2146062294
- Cited by
- 77
- References
- 59
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 3 · 2023: 3 · 2022: 7 · 2021: 5 · 2020: 11 · 2019: 7 · 2018: 9 · 2017: 7 · 2016: 6 · 2015: 8
- FWCI
- 7.68
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (T32AI007244, R01AI036964)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (K08AR063729)
- Topics
- Health Sciences › Medicine › Dermatology › Skin Protection and Aging
- Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- skin-resident T cells, ultraviolet radiation, DNA repair, dendritic epidermal T cells, γδ T cells, extracellular ATP, purinergic signaling, P2X7 receptor, caspase-1, interleukin-1, IL-17, keratinocytes, DNA damage, skin regeneration, CD69, TRAF3IP2, DAPK1
- MeSH terms
- CD69 Antigens, Animals, Antigens, Differentiation, T-Lymphocyte, DNA Repair, Epidermis, Female, Gene Expression Regulation, Humans, Male, Regeneration, T-Lymphocytes, Tumor Necrosis Factor-alpha, Ultraviolet Rays, Keratinocytes, Antigens, CD, Receptors, Antigen, T-Cell, gamma-delta, Mice, Knockout, Interleukin-17, Lectins, C-Type, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
