Natriuretic peptides modulate monocyte-derived Langerhans cell differentiation and promote a migratory phenotype
The interaction between the nervous and immune systems is crucial for maintaining homeostasis and can influence disease progression in inflammatory skin diseases, such as atopic dermatitis (AD). Sensory neurons in the skin can secrete neuropeptides that modulate immune cell activity, including Lange...
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| Vydáno v: | Frontiers in immunology Ročník 16; s. 1593141 |
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| Jazyk: | angličtina |
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Frontiers Media S.A
09.06.2025
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| ISSN: | 1664-3224, 1664-3224 |
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| Abstract | The interaction between the nervous and immune systems is crucial for maintaining homeostasis and can influence disease progression in inflammatory skin diseases, such as atopic dermatitis (AD). Sensory neurons in the skin can secrete neuropeptides that modulate immune cell activity, including Langerhans cells (LCs), one of the primary antigen-presenting cells in the epidermis. In our study we investigated the effects of neuropeptides on the differentiation of monocyte-derived LCs (moLCs), specifically the neuropeptides with the most profound effect, i.e. atrial- and B-type natriuretic peptides (ANP and BNP, respectively).
RNA sequencing and RT-qPCR were used to analyze neuropeptide receptor expression in moLCs and immature dendritic cells (iDCs), and the most translationally relevant, natriuretic peptide receptor A (NPR1) was validated on the protein level using western blotting. Cell surface markers of moLCs were assessed using flow cytometry, and NPR1 functionality was confirmed through intracellular cGMP assays. Confocal microscopy was used to confirm the expression of NPR1
in healthy and AD skin. RNA-Seq analysis was also employed to characterize the phenotypic changes in moLCs differentiated in the presence of BNP.
NPR1 expression was significantly higher in moLCs compared to iDCs, and treatment with ANP and BNP enhanced moLC differentiation, increasing CD207, CD1a, and HLA-DQ expression, while other tested neuropeptides (calcitonin gene-related peptide [CGRP], neurotensin) had no significant effect. NPR1 was functionally active, as evidenced by increased intracellular cGMP levels upon ligand binding. Confocal microscopy revealed NPR1 expression on LC cell bodies in both healthy and AD skin, with reduced intensity in AD. RNA-Seq analysis of BNP-treated moLCs indicated a shift toward a migratory LC phenotype, marked by upregulation of genes associated with cell motility (e.g., CCR7, LAMP3).
These findings demonstrate that NPR1 activation promotes a migratory LC phenotype, highlighting the role of neuropeptides in shaping cutaneous immune responses. The reduced number of LCs in AD skin suggests a potential link between neuropeptide signaling and disease pathology. |
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| AbstractList | IntroductionThe interaction between the nervous and immune systems is crucial for maintaining homeostasis and can influence disease progression in inflammatory skin diseases, such as atopic dermatitis (AD). Sensory neurons in the skin can secrete neuropeptides that modulate immune cell activity, including Langerhans cells (LCs), one of the primary antigen-presenting cells in the epidermis. In our study we investigated the effects of neuropeptides on the differentiation of monocyte-derived LCs (moLCs), specifically the neuropeptides with the most profound effect, i.e. atrial- and B-type natriuretic peptides (ANP and BNP, respectively).MethodsRNA sequencing and RT-qPCR were used to analyze neuropeptide receptor expression in moLCs and immature dendritic cells (iDCs), and the most translationally relevant, natriuretic peptide receptor A (NPR1) was validated on the protein level using western blotting. Cell surface markers of moLCs were assessed using flow cytometry, and NPR1 functionality was confirmed through intracellular cGMP assays. Confocal microscopy was used to confirm the expression of NPR1 in situ in healthy and AD skin. RNA-Seq analysis was also employed to characterize the phenotypic changes in moLCs differentiated in the presence of BNP.ResultsNPR1 expression was significantly higher in moLCs compared to iDCs, and treatment with ANP and BNP enhanced moLC differentiation, increasing CD207, CD1a, and HLA-DQ expression, while other tested neuropeptides (calcitonin gene-related peptide [CGRP], neurotensin) had no significant effect. NPR1 was functionally active, as evidenced by increased intracellular cGMP levels upon ligand binding. Confocal microscopy revealed NPR1 expression on LC cell bodies in both healthy and AD skin, with reduced intensity in AD. RNA-Seq analysis of BNP-treated moLCs indicated a shift toward a migratory LC phenotype, marked by upregulation of genes associated with cell motility (e.g., CCR7, LAMP3).DiscussionThese findings demonstrate that NPR1 activation promotes a migratory LC phenotype, highlighting the role of neuropeptides in shaping cutaneous immune responses. The reduced number of LCs in AD skin suggests a potential link between neuropeptide signaling and disease pathology. The interaction between the nervous and immune systems is crucial for maintaining homeostasis and can influence disease progression in inflammatory skin diseases, such as atopic dermatitis (AD). Sensory neurons in the skin can secrete neuropeptides that modulate immune cell activity, including Langerhans cells (LCs), one of the primary antigen-presenting cells in the epidermis. In our study we investigated the effects of neuropeptides on the differentiation of monocyte-derived LCs (moLCs), specifically the neuropeptides with the most profound effect, i.e. atrial- and B-type natriuretic peptides (ANP and BNP, respectively).IntroductionThe interaction between the nervous and immune systems is crucial for maintaining homeostasis and can influence disease progression in inflammatory skin diseases, such as atopic dermatitis (AD). Sensory neurons in the skin can secrete neuropeptides that modulate immune cell activity, including Langerhans cells (LCs), one of the primary antigen-presenting cells in the epidermis. In our study we investigated the effects of neuropeptides on the differentiation of monocyte-derived LCs (moLCs), specifically the neuropeptides with the most profound effect, i.e. atrial- and B-type natriuretic peptides (ANP and BNP, respectively).RNA sequencing and RT-qPCR were used to analyze neuropeptide receptor expression in moLCs and immature dendritic cells (iDCs), and the most translationally relevant, natriuretic peptide receptor A (NPR1) was validated on the protein level using western blotting. Cell surface markers of moLCs were assessed using flow cytometry, and NPR1 functionality was confirmed through intracellular cGMP assays. Confocal microscopy was used to confirm the expression of NPR1 in situ in healthy and AD skin. RNA-Seq analysis was also employed to characterize the phenotypic changes in moLCs differentiated in the presence of BNP.MethodsRNA sequencing and RT-qPCR were used to analyze neuropeptide receptor expression in moLCs and immature dendritic cells (iDCs), and the most translationally relevant, natriuretic peptide receptor A (NPR1) was validated on the protein level using western blotting. Cell surface markers of moLCs were assessed using flow cytometry, and NPR1 functionality was confirmed through intracellular cGMP assays. Confocal microscopy was used to confirm the expression of NPR1 in situ in healthy and AD skin. RNA-Seq analysis was also employed to characterize the phenotypic changes in moLCs differentiated in the presence of BNP.NPR1 expression was significantly higher in moLCs compared to iDCs, and treatment with ANP and BNP enhanced moLC differentiation, increasing CD207, CD1a, and HLA-DQ expression, while other tested neuropeptides (calcitonin gene-related peptide [CGRP], neurotensin) had no significant effect. NPR1 was functionally active, as evidenced by increased intracellular cGMP levels upon ligand binding. Confocal microscopy revealed NPR1 expression on LC cell bodies in both healthy and AD skin, with reduced intensity in AD. RNA-Seq analysis of BNP-treated moLCs indicated a shift toward a migratory LC phenotype, marked by upregulation of genes associated with cell motility (e.g., CCR7, LAMP3).ResultsNPR1 expression was significantly higher in moLCs compared to iDCs, and treatment with ANP and BNP enhanced moLC differentiation, increasing CD207, CD1a, and HLA-DQ expression, while other tested neuropeptides (calcitonin gene-related peptide [CGRP], neurotensin) had no significant effect. NPR1 was functionally active, as evidenced by increased intracellular cGMP levels upon ligand binding. Confocal microscopy revealed NPR1 expression on LC cell bodies in both healthy and AD skin, with reduced intensity in AD. RNA-Seq analysis of BNP-treated moLCs indicated a shift toward a migratory LC phenotype, marked by upregulation of genes associated with cell motility (e.g., CCR7, LAMP3).These findings demonstrate that NPR1 activation promotes a migratory LC phenotype, highlighting the role of neuropeptides in shaping cutaneous immune responses. The reduced number of LCs in AD skin suggests a potential link between neuropeptide signaling and disease pathology.DiscussionThese findings demonstrate that NPR1 activation promotes a migratory LC phenotype, highlighting the role of neuropeptides in shaping cutaneous immune responses. The reduced number of LCs in AD skin suggests a potential link between neuropeptide signaling and disease pathology. The interaction between the nervous and immune systems is crucial for maintaining homeostasis and can influence disease progression in inflammatory skin diseases, such as atopic dermatitis (AD). Sensory neurons in the skin can secrete neuropeptides that modulate immune cell activity, including Langerhans cells (LCs), one of the primary antigen-presenting cells in the epidermis. In our study we investigated the effects of neuropeptides on the differentiation of monocyte-derived LCs (moLCs), specifically the neuropeptides with the most profound effect, i.e. atrial- and B-type natriuretic peptides (ANP and BNP, respectively). RNA sequencing and RT-qPCR were used to analyze neuropeptide receptor expression in moLCs and immature dendritic cells (iDCs), and the most translationally relevant, natriuretic peptide receptor A (NPR1) was validated on the protein level using western blotting. Cell surface markers of moLCs were assessed using flow cytometry, and NPR1 functionality was confirmed through intracellular cGMP assays. Confocal microscopy was used to confirm the expression of NPR1 in healthy and AD skin. RNA-Seq analysis was also employed to characterize the phenotypic changes in moLCs differentiated in the presence of BNP. NPR1 expression was significantly higher in moLCs compared to iDCs, and treatment with ANP and BNP enhanced moLC differentiation, increasing CD207, CD1a, and HLA-DQ expression, while other tested neuropeptides (calcitonin gene-related peptide [CGRP], neurotensin) had no significant effect. NPR1 was functionally active, as evidenced by increased intracellular cGMP levels upon ligand binding. Confocal microscopy revealed NPR1 expression on LC cell bodies in both healthy and AD skin, with reduced intensity in AD. RNA-Seq analysis of BNP-treated moLCs indicated a shift toward a migratory LC phenotype, marked by upregulation of genes associated with cell motility (e.g., CCR7, LAMP3). These findings demonstrate that NPR1 activation promotes a migratory LC phenotype, highlighting the role of neuropeptides in shaping cutaneous immune responses. The reduced number of LCs in AD skin suggests a potential link between neuropeptide signaling and disease pathology. |
| Author | Bácsi, Attila Pénzes, Zsófia Vereb, György Muzsai, Szabolcs Molnár, Petra Szegedi, Andrea Szántó, Magdolna Rebenku, István Dajnoki, Zsolt Szöllősi, Attila Gábor Pázmándi, Kitti Horváth, Dorottya Fekete, Tünde |
| AuthorAffiliation | 5 Faculty of Pharmacy, University of Debreen , Debrecen , Hungary 3 Department of Biophysics and Cell Biology, Faculty of Medicine, University of Debrecen , Debrecen , Hungary 2 Doctoral School of Molecular Medicine, University of Debrecen , Debrecen , Hungary 6 Department of Medical Chemistry, Faculty of Medicine, University of Debrecen , Debrecen , Hungary 7 Gyula Petrányi Doctoral School of Clinical Immunology and Allergology, University of Debrecen , Debrecen , Hungary 4 HUN-REN-UD Cell Biology and Signaling Research Group, Faculty of Medicine, University of Debrecen , Debrecen , Hungary 8 Department of Dermatology, Centre of Excellence, Faculty of Medicine, University of Debrecen , Debrecen , Hungary 1 Department of Immunology, Faculty of Medicine, University of Debrecen , Debrecen , Hungary 9 HUN-REN-UD, Allergology Research Group, Faculty of Medicine , Debrecen , Hungary |
| AuthorAffiliation_xml | – name: 1 Department of Immunology, Faculty of Medicine, University of Debrecen , Debrecen , Hungary – name: 2 Doctoral School of Molecular Medicine, University of Debrecen , Debrecen , Hungary – name: 6 Department of Medical Chemistry, Faculty of Medicine, University of Debrecen , Debrecen , Hungary – name: 7 Gyula Petrányi Doctoral School of Clinical Immunology and Allergology, University of Debrecen , Debrecen , Hungary – name: 8 Department of Dermatology, Centre of Excellence, Faculty of Medicine, University of Debrecen , Debrecen , Hungary – name: 3 Department of Biophysics and Cell Biology, Faculty of Medicine, University of Debrecen , Debrecen , Hungary – name: 4 HUN-REN-UD Cell Biology and Signaling Research Group, Faculty of Medicine, University of Debrecen , Debrecen , Hungary – name: 5 Faculty of Pharmacy, University of Debreen , Debrecen , Hungary – name: 9 HUN-REN-UD, Allergology Research Group, Faculty of Medicine , Debrecen , Hungary |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/40552299$$D View this record in MEDLINE/PubMed |
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| Copyright | Copyright © 2025 Horváth, Pénzes, Molnár, Rebenku, Vereb, Szántó, Muzsai, Szegedi, Dajnoki, Pázmándi, Fekete, Bácsi and Szöllősi. Copyright © 2025 Horváth, Pénzes, Molnár, Rebenku, Vereb, Szántó, Muzsai, Szegedi, Dajnoki, Pázmándi, Fekete, Bácsi and Szöllősi 2025 Horváth, Pénzes, Molnár, Rebenku, Vereb, Szántó, Muzsai, Szegedi, Dajnoki, Pázmándi, Fekete, Bácsi and Szöllősi |
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| Keywords | B-type natriuretic peptide neurotensin monocyte-derived Langerhans cell atopic dermatitis neuropeptides skin immunology atrial natriuretic peptide calcitonin gene related peptide |
| Language | English |
| License | Copyright © 2025 Horváth, Pénzes, Molnár, Rebenku, Vereb, Szántó, Muzsai, Szegedi, Dajnoki, Pázmándi, Fekete, Bácsi and Szöllősi. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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| SubjectTerms | Adult Atrial Natriuretic Factor - pharmacology atrial natriuretic peptide B-type natriuretic peptide calcitonin gene related peptide Cell Differentiation - drug effects Cell Movement - drug effects Cells, Cultured Dermatitis, Atopic - immunology Dermatitis, Atopic - metabolism Dermatitis, Atopic - pathology Female Humans Immunology Langerhans Cells - cytology Langerhans Cells - drug effects Langerhans Cells - immunology Langerhans Cells - metabolism Male monocyte-derived Langerhans cell Monocytes - cytology Monocytes - immunology Monocytes - metabolism Natriuretic Peptide, Brain - pharmacology Natriuretic Peptides - pharmacology neuropeptides neurotensin Phenotype Receptors, Atrial Natriuretic Factor - genetics Receptors, Atrial Natriuretic Factor - metabolism |
| Title | Natriuretic peptides modulate monocyte-derived Langerhans cell differentiation and promote a migratory phenotype |
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