CD39 is the dominant Langerhans cell–associated ecto-NTPDase: Modulatory roles in inflammation and immune responsiveness
Abstract
CD39, the endothelial ecto-nucleoside triphosphate diphosphohydrolase (NTPDase), regulates vascular inflammation and thrombosis by hydrolyzing ATP and ADP. Although ecto-NTPDase activities have been used as a marker of epidermal dendritic cells (DCs) known as Langerhans cells, the identity and function of these activities remain unknown. Here we report that Langerhans cells in CD39-/- mice express no detectable ecto-NTPDase activity. Irritant chemicals triggered rapid ATP and ADP release from keratinocytes and caused exacerbated skin inflammation in CD39-/- mice. Paradoxically, T cell-mediated allergic contact hypersensitivity was severely attenuated in CD39-/- mice. As to mechanisms, T cells increased pericellular ATP concentrations upon activation, and CD39-/- DCs showed ATP unresponsiveness (secondary to P2-receptor desensitization) and impaired antigen-presenting capacity. Our results show opposing outcomes of CD39 deficiency in irritant versus allergic contact dermatitis, reflecting its diverse roles in regulating extracellular nucleotide-mediated signaling in inflammatory responses to environmental insults and DC-T cell communication in antigen presentation.
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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 [54]
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BackgroundThe Therapeutic Potential of Modifying Inflammasomes and NOD-Like Receptors
Virgilio, F. D. (2013) · Pharmacological Reviews · doi:10.1124/pr.112.006171 · Cited by 158 · see citing works
“Many agents reported to drive NLRP3 activation via ROS generation are also potent triggers of ATP release (Ab, hyperglycemia, skin irritants, infections, ultraviolet light) (Mizumoto et al., 2002; Solini et al., 2004; Inoue et al., 2007; Sanz et al., 2009; Weber et al., 2010).”
BackgroundP2 receptors and extracellular ATP a novel homeostatic pathway in inflammation
Bours, M. J. L. (2011) · Frontiers in Bioscience-Scholar · doi:10.2741/235 · Cited by 160 · see citing works
“This was likely due to P2 receptor desensitization, since responsiveness of CD39/dendritic cells to ATP was restored by apyrase treatment (28).”
InfluentialThe Environment of Regulatory T Cell Biology: Cytokines, Metabolites, and the Microbiome
Hoeppli, R. E., Wu, D., Cook, L., & Levings, M. K. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00061 · Cited by 157 · see citing works
Tanaka, H., Matsushima, H., Mizumoto, N., & Takashima, A. (2009) · Cancer Research · doi:10.1158/0008-5472.can-09-1101 · Cited by 157 · see citing works
“(BM)–derived DC cultures were propagated as before (18, 19).”
Self-citationBehavioral Responses of Epidermal Langerhans Cells In Situ to Local Pathological Stimuli
Nishibu, A., Ward, B. R., Jester, J. V., Ploegh, H. L., Boes, M. L., & Takashima, A. (2006) · Journal of Investigative Dermatology · doi:10.1038/sj.jid.5700107 · Cited by 147 · see citing works
“5% DNFB in acetone/olive oil (3/1) to the ear skin as described before (Kumamoto et al., 2002; Mizumoto et al., 2002).”
MethodInfluentialSelf-citationImpact of Ectoenzymes on P2 and P1 Receptor Signaling
Kukulski, F., Lévesque, S. A., & Sévigny, J. (2011) · Advances in pharmacology · doi:10.1016/b978-0-12-385526-8.00009-6 · Cited by 143 · 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
Conversion of extracellular ATP into adenosine: a master switch in renal health and disease
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“The relative duration of signaling by these extracellular nucleotides is determined largely by nucleotide degrading ecto-enzymes such as the transmembrane ecto-enzymes CD38 and CD39 (21, 39, 59).”
BackgroundAddi, A. B., Lefort, A., Hua, X., Libert, F., Communi, D., Ledent, C. A., Macours, P., Tilley, S. L., Boeynaems, J., & Robaye, B. (2008) · European Journal of Immunology · doi:10.1002/eji.200737781 · Cited by 136 · see citing works
Connexin 26 regulates epidermal barrier and wound remodeling and promotes psoriasiform response
Djalilian, A. R. (2006) · Journal of Clinical Investigation · doi:10.1172/jci27186 · Cited by 132 · 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
“Ado derives from the dephosphorylation of ATP, catalyzed by different enzymes: the ectonucleoside triphosphate diphosphohydrolase 1 (CD39) and the ecto-5’-nucleotidase (CD73) (37, 38).”
BackgroundSchnurr, M. M., Toy, T., Stoitzner, P., Cameron, P. U., Shin, A., Beecroft, T., Davis, I. D., Cebon, J. S., & Maraskovsky, E. (2003) · Blood · doi:10.1182/blood-2002-12-3745 · Cited by 125 · see citing works
Adenosine A2A receptor antagonists: blockade of adenosinergic effects and T regulatory cells
Sitkovsky, M. V., Lukashev, D. E., Deaglio, S., Dwyer, K. M., Robson, S. C., & Ohta, A. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.23 · Cited by 124 · see citing works
“…extend their potential applications with many more diseases (Cassada et al., 2001; Hogan et al., 2001; Okusa et al., 2001; Feoktistov et al., 2002; Montesinos et al., 2002; Dhalla et al., 2003; Awad et al., 2006; Nemeth et al., 2007; Rivo et al., 2007), but also served as an elegant tool to…”
BackgroundSelf-citationOgawa, Y., Kawamura, T., & Shimada, S. (2016) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2016.06.003 · Cited by 123 · see citing works
Extracellular nucleotides as negative modulators of immunity
Virgilio, F. D., Boeynaems, J., & Robson, S. C. (2009) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2009.06.021 · Cited by 121 · see citing works
Self-citationEltzschig, H. K., MacManus, C. F., & Colgan, S. P. (2008) · Trends in Cardiovascular Medicine · doi:10.1016/j.tcm.2008.01.006 · Cited by 120 · see citing works
“Rather, these studies identified the ecto-nucleoside triphosphate diphosphohydrolase (NTPDase)(Wang and Guidotti 1996), previously identified as ecto-ATPase, ecto-ATPDase or CD39 (Gendron et al. 2002, Mizumoto et al. 2002) as the central surface enzyme in this reaction.”
BackgroundNTPDase1 governs P2X7‐dependent functions in murine macrophages
Lévesque, S. A., Kukulski, F., Enjyoji, K., Robson, S. C., & Sévigny, J. (2010) · European Journal of Immunology · doi:10.1002/eji.200939741 · Cited by 112 · see citing works
Self-citationRing, S., Oliver, S. J., Cronstein, B. N., Enk, A., & Mahnke, K. (2009) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2009.03.022 · Cited by 111 · see citing works
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“Our initial ex vivo experiments in which we injected cutaneous explants with BzATP confirmed human in vitro and murine results (8, 9, 12, 13, 17) by demonstrating a significant”
NTPDase1 (CD39) controls nucleotide-dependent vasoconstriction in mouse
Kauffenstein, G., Drouin, A., Thorin‐Trescases, N., Bachelard, H., Robaye, B., D’Orléans-Juste, P., Marceau, F., Thorin, É., & Sévigny, J. (2009) · Cardiovascular Research · doi:10.1093/cvr/cvp265 · Cited by 108 · see citing works
Self-citationRedox Imbalance Induced by Contact Sensitizers Triggers the Maturation of Dendritic Cells
Mizuashi, M., Ohtani, T., Nakagawa, S., & Aiba, S. (2005) · Journal of Investigative Dermatology · doi:10.1111/j.0022-202x.2005.23624.x · Cited by 107 · see citing works
“Recently, it has been demonstrated that irritant chemicals induced the release of ATP from keratinocytes”
BackgroundInflammasome Activation of IL‐1 Family Mediators in Response to Cutaneous Photodamage†
Nasti, T. H., & Timares, L. (2012) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.2012.01182.x · Cited by 106 · see citing works
“showed that ATP released from keratinocytes also stimulated Langerhans cells to produce inflammatory cytokines (72), but IL-1b”
BackgroundCD1a and langerin: acting as more than Langerhans cell markers
Mizumoto, N., & Takashima, A. (2004) · Journal of Clinical Investigation · doi:10.1172/jci21140 · Cited by 104 · see citing works
Self-citationDeletion of Cd39/Entpd1 Results in Hepatic Insulin Resistance
Enjyoji, K., Kotani, K., Thukral, C., Blumel, B., Sun, X., Wu, Y., Imai, M., Friedman, D. J., Csizmadia, E., Bleibel, W., et al. (2008) · Diabetes · doi:10.2337/db07-1265 · Cited by 101 · see citing works
“We have previously shown that deletion of Cd39/Entpd1 results in disordered purinergic signaling responses that compromise vascular thromboregulation and augment inflammatory responses(3;5;12).”
BackgroundSelf-citationBönner, F., Borg, N., Burghoff, S., & Schrader, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034730 · Cited by 98 · see citing works
“For example, it was shown that ATP activates dendritic cells in lung [31] and skin [32] and is involved in the recruitment of phagocytotic cells [33].”
BackgroundJacobse, J., Li, J., Rings, E. H. H. M., Samsom, J. N., & Goettel, J. A. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.716499 · Cited by 98 · see citing works
Purinergic mechanism in the immune system: A signal of danger for dendritic cells
Virgilio, F. D. (2005) · Purinergic Signalling · doi:10.1007/s11302-005-6312-z · Cited by 96 · see citing works
“As of now there are no reports of an in vivo modulatory activity of extracellular ATP on dendritic cell function, but the observations reported in mice deleted of the main ecto-ATPase of immune cells (CD39) point in this direction [23].”
BackgroundChanging Paradigms in Cutaneous Immunology: Adapting with Dendritic Cells
Larregina, A. T., & Falo, L. D. (2005) · Journal of Investigative Dermatology · doi:10.1111/j.1523-1747.2004.23554.x · Cited by 95 · see citing works
Weissmüller, T., Campbell, E. L., Rosenberger, P., Scully, M. M., Beck, P. L., Furuta, G. T., & Colgan, S. P. (2008) · Journal of Clinical Investigation · doi:10.1172/jci35874 · Cited by 95 · see citing works
“One family member, NTPDase-1, also called CD39, has been extensively studied on vascular endothelial cells (27).”
BackgroundInfluentialMummert, M. E., Mummert, D. I., Edelbaum, D., Hui, F., Matsue, H., & Takashima, A. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.8.4322 · Cited by 94 · see citing works
“T cell proliferation was measured by [(3)H]thymidine uptake on day 3 as previously described (30, 31, 33).”
BackgroundMethodInfluentialSelf-citationTsai, S. H., Kinoshita, M., Kusu, T., Kayama, H., Okumura, R., Ikeda, K., Shimada, Y., Takeda, A., Yoshikawa, S., Obata‐Ninomiya, K., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.01.015 · Cited by 93 · see citing works
CD39/NTPDase-1 activity and expression in normal leukocytes
Pulte, D. D., Broekman, M. J., Olson, K. E., Drosopoulos, J. H. F., Kizer, J. R., Islam, N., & Marcus, A. J. (2007) · Thrombosis Research · doi:10.1016/j.thromres.2007.04.008 · Cited by 93 · see citing works
“CD39 in leukocytes has been demonstrated to have other effects as well, including modulation of cytokine expression and the inflammatory response, as well as cell-cell adhesion [4,6,15,16].”
BackgroundSowa, N. A., Taylor‐Blake, B., & Zylka, M. J. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5324-09.2010 · Cited by 92 · see citing works
“ENTPD1 (CD39, NTPDase1) is found on epidermal Langerhans cells and hydrolyzes keratinocyte-derived ATP and ADP to AMP (Mizumoto et al., 2002).”
BackgroundBeldi, G., Wu, Y., Banz, Y., Nowak, M. A., Miller, L., Enjyoji, K., Haschemi, A., Yegutkin, G. G., Candinas, D., Exley, M. A., et al. (2008) · Hepatology · doi:10.1002/hep.22401 · Cited by 91 · see citing works
Self-citationSevere dermatitis with loss of epidermal Langerhans cells in human and mouse zinc deficiency
Kawamura, T., Ogawa, Y., Nakamura, Y., Nakamizo, S., Ohta, Y., Nakano, H., Kabashima, K., Katayama, I., Koizumi, S., Kodama, T., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci58618 · Cited by 91 · see citing works
“Because the P2-receptor signaling pathway is negatively regulated by NTPDase-dependent hydrolysis of ATP, LC-associated CD39 plays a protective role against ATPmediated inflammatory signals by hydrolyzing extracellular nucleotides released by keratinocytes in ICD responses (28).”
BackgroundResultInfluentialLiao, H., Hyman, M. C., Baek, A. E., Fukase, K., & Pinsky, D. J. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.116905 · Cited by 89 · see citing works
Fontana, M. C., Rezer, J. F. P., Coradini, K., Leal, D. B. R., & Beck, R. C. R. (2011) · European Journal of Pharmaceutics and Biopharmaceutics · doi:10.1016/j.ejpb.2011.05.002 · Cited by 88 · see citing works
Sansom, F. M., Robson, S. C., & Hartland, E. L. (2008) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00013-08 · Cited by 88 · see citing works
“Furthermore, CD39 plays a role in modulating inflammation and the immune response by affecting the extracellular concentrations of ATP; this nucleotide serves as an immunostimulant of the immune system operative via P2 receptor pathways (105, 119).”
BackgroundSelf-citationda Silva, E. D. A. M., de Oliveira, J. C., Figueiredo, A. B., Lima-Junior, D. S., Carneiro, C. M., Fietto, J. L. R., & Afonso, L. (2008) · Microbes and Infection · doi:10.1016/j.micinf.2008.04.016 · Cited by 85 · see citing works
Kurashima, Y., Amiya, T., Fujisawa, K., Shibata, N., Suzuki, Y., Kogure, Y., Hashimoto, E., Otsuka, A., Kabashima, K., Sato, S., et al. (2014) · Immunity · doi:10.1016/j.immuni.2014.01.014 · Cited by 79 · see citing works
“Furthermore, ATP amounts are increased in the extracellular compartment in irritant contact dermatitis associatedwith zinc-deficiency (Kawamura et al., 2012;Mizumoto et al., 2002).”
BackgroundBeldi, G., Wu, Y., Sun, X., Imai, M., Enjyoji, K., Csizmadia, E., Candinas, D., Erb, L., & Robson, S. C. (2008) · Gastroenterology · doi:10.1053/j.gastro.2008.07.025 · Cited by 81 · see citing works
Self-citationMarteau, F., Communi, D., Boeynaems, J., & Gonzalez, N. S. (2004) · Journal of Leukocyte Biology · doi:10.1189/jlb.0104032 · Cited by 81 · see citing works
“As DC express ecto-nucleotidases such as CD39 [13, 17], ADP is likely to be generated following release of ATP from necrotic cells or from CD4 T lymphocytes [13].”
BackgroundInfluentialThompson, E. A., & Powell, J. D. (2020) · Annual Review of Medicine · doi:10.1146/annurev-med-060619-023155 · Cited by 80 · see citing works
The Alterations in Mitochondrial Dynamics Following Cerebral Ischemia/Reperfusion Injury
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The sixth sense: hematopoietic stem cells detect danger through purinergic signaling
Rossi, L., Salvestrini, V., Ferrari, D., Virgilio, F. D., & Lemoli, R. M. (2012) · Blood · doi:10.1182/blood-2012-04-422378 · Cited by 80 · see citing works
Structural insight into signal conversion and inactivation by NTPDase2 in purinergic signaling
Zebisch, M., & Sträter, N. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802535105 · Cited by 80 · see citing works
Guido, G. (2007) · Frontiers in bioscience · doi:10.2741/2868 · Cited by 79 · see citing works
“Consequently, in Cd39 null mice, defects in dendrititc cell function, antigen presentation, T cell responses to haptens (type IV hypersensitivity reactions) and delayed cellular rejection responses are observed (8, 131, 134).”
BackgroundAeby, P., Ashikaga, T., Bessou‐Touya, S., Schepky, A. G., Gerberick, F., Kern, P., Marrec-Fairley, M., Maxwell, G., Ovigne, J. ‐., Sakaguchi, H., et al. (2010) · Toxicology in Vitro · doi:10.1016/j.tiv.2010.07.005 · Cited by 78 · see citing works
The Role of Endothelial Cells in the Resolution of Acute Inflammation
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Idzko, M., Panther, E., Bremer, H., Sorichter, S., Luttmann, W., Virchow, C., Virgilio, F. D., Herouy, Y., Norgauer, J., & Ferrari, D. (2003) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0705145 · Cited by 77 · see citing works
“Virtually all cell types express ecto-nucleotidases (Zimmer- mann, 1992; Mizumoto et al., 2002); therefore, responses to extracellular nucleotides could also be due to stimulation of adenosine receptors by nucleotide degradation products.”
BackgroundDeletion of Cd39 on Natural Killer Cells Attenuates Hepatic Ischemia/Reperfusion Injury in Mice
Beldi, G., Banz, Y., Kroemer, A., Sun, X., Wu, Y., Graubardt, N., Rellstab, A., Nowak, M., Enjyoji, K., Li, X. C., et al. (2009) · Hepatology · doi:10.1002/hep.23510 · Cited by 76 · see citing works
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Ectonucleotidases in Acute and Chronic Inflammation
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“…ectonucleotidase, widely expressed on different immune cell types, e.g., monocytes, dendritic cells (DCs), T regulatory (Treg) cells and natural killer (NK) cells, besides vascular endothelial cells (Mizumoto et al., 2002; Deaglio et al., 2007; Deaglio and Robson, 2011; Kishore et al., 2018).”
BackgroundPhenotypical and functional alterations of CD8 regulatory T cells in primary biliary cirrhosis
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“The CD39 antigen is a nucleosidase present at the cell surface whose activity has been strictly correlated with normal Treg function [52,53].”
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“Previous estimates of ADP [35,36,45,47] and adenosine [21,22,47] made in various cells, tissue slices and blood plasma also reported purine levels from low nanomolar to submicromolar range.”
BackgroundSantos, R. F., Pôssa, M. A. S., Bastos, M. S. E., Guedes, P. M. D. M., de Almeida, M. R., Demarco, R. C., Verjovski‐Almeida, S., Bahia, M. T., & Fietto, J. L. R. (2009) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0000387 · Cited by 72 · see citing works
“The role of ecto-nucleotidases as the major biomolecules involved in the control of purinergic signaling were demonstrated in various models, such as the dominant role of CD39 in the modulation of inflammation and immune response in the Langerhans cells [5] and in cardioprotection and protective responses to hypoxia/i…”
BackgroundCui, M., Ding, H., Chen, F., Zhao, Y., Yang, Q., & Dong, Q. (2014) · Molecular Neurobiology · doi:10.1007/s12035-014-9002-4 · Cited by 70 · see citing works
- Authors
- Mizumoto, N., Kumamoto, T., Robson, S. C., Sévigny, J., Matsue, H., Enjyoji, K., & Takashima, A.
- Affiliations
- The University of Texas Southwestern Medical Center (US)
- Beth Israel Deaconess Medical Center (US)
- Corresponding author
- Takashima, Akira
- Venue
- Nature Medicine
- Published
- 2002-04
- Volume
- 8
- Issue
- 4
- Pages
- 358-365
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- OpenAlex
- W1988951550
- Cited by
- 327
- References
- 41
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 8 · 2023: 16 · 2022: 7 · 2021: 9 · 2020: 7 · 2019: 12 · 2018: 15 · 2017: 13 · 2016: 15 · 2015: 14 · 2014: 18 · 2013: 14 · 2012: 23
- FWCI
- 8.48
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Adenosine and Purinergic Signaling
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Molecular Research
- Health Sciences › Medicine › Dermatology › Dermatology and Skin Diseases
- Keywords
- CD39, Langerhans cells, ATP hydrolysis, ADP, purinergic P2 receptors, contact dermatitis, contact allergy, irritant contact dermatitis, keratinocytes, antigen presentation, skin inflammation, thrombosis
- MeSH terms
- Adenosine Triphosphatases, Adenosine Triphosphate, Animals, Apyrase, Female, Immunity, Inflammation, Irritants, Langerhans Cells, Male, Signal Transduction, Antigens, CD, Receptors, Purinergic P2, Mice, Knockout, Mice
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