Transcriptional Atlas of Intestinal Immune Cells Reveals that Neuropeptide α-CGRP Modulates Group 2 Innate Lymphoid Cell Responses
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Signaling abnormalities in immune responses in the small intestine can trigger chronic type 2 inflammation involving interaction of multiple immune cell types. To systematically characterize this response, we analyzed 58,067 immune cells from the mouse small intestine by single-cell RNA sequencing (scRNA-seq) at steady state and after induction of a type 2 inflammatory reaction to ovalbumin (OVA). Computational analysis revealed broad shifts in both cell-type composition and cell programs in response to the inflammation, especially in group 2 innate lymphoid cells (ILC2s). Inflammation induced the expression of exon 5 of Calca, which encodes the alpha-calcitonin gene-related peptide (α-CGRP), in intestinal KLRG1+ ILC2s. α-CGRP antagonized KLRG1+ ILC2s proliferation but promoted IL-5 expression. Genetic perturbation of α-CGRP increased the proportion of intestinal KLRG1+ ILC2s. Our work highlights a model where α-CGRP-mediated neuronal signaling is critical for suppressing ILC2 expansion and maintaining homeostasis of the type 2 immune machinery.
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Neuromedin U initiates type 2 immunity, while αCGRP antagonizes type 2 immunity in the gut mucosa.
“For example, activation of type 2 innate lymphoid cells (ILC2) in the gut mucosa is regulated by neuronally-derived peptides, with neuromedin U initiating102, and α-calcitonin gene-related peptide (αCGRP) antagonizing, type 2 immunity103.”
From Central regulation of stress-evoked peripheral immune responses (2023) · cites this paper as [103]
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NIH Image to ImageJ: 25 years of image analysis
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012) · Nature Methods · doi:10.1038/nmeth.2089 · Cited by 64,638 · see citing works
Fast gapped-read alignment with Bowtie 2
Langmead, B., & Salzberg, S. L. (2012) · Nature Methods · doi:10.1038/nmeth.1923 · Cited by 56,400 · see citing works
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709 · see citing works
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364 · see citing works
(2003) · Journal of Machine Learning Research · doi:10.5555/944919.944937 · Cited by 32,337 · see citing works
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
Liao, Y., Smyth, G. K., & Shi, W. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btt656 · Cited by 27,219 · see citing works
RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome
Li, B., & Dewey, C. N. (2011) · BMC Bioinformatics · doi:10.1186/1471-2105-12-323 · Cited by 22,179 · see citing works
Fast unfolding of communities in large networks
Blondel, V. D., Guillaume, J.-L., Lambiotte, R., & Lefebvre, E. (2008) · Journal of Statistical Mechanics: Theory and Experiment · doi:10.1088/1742-5468/2008/10/p10008 · Cited by 21,424 · see citing works
Model-based Analysis of ChIP-Seq (MACS)
Zhang, Y., Liu, T., Meyer, C. A., Eeckhoute, J., Johnson, D. S., Bernstein, B. E., Nusbaum, C., Myers, R. M., Brown, M., Li, W., et al. (2008) · Genome Biology · doi:10.1186/gb-2008-9-9-r137 · Cited by 18,386 · see citing works
Integrating single-cell transcriptomic data across different conditions, technologies, and species
Butler, A., Hoffman, P., Smibert, P., Papalexi, E., & Satija, R. (2018) · Nature Biotechnology · doi:10.1038/nbt.4096 · Cited by 13,174 · see citing works
Indexing by latent semantic analysis
Deerwester, S. C., Dumais, S., Furnas, G. W., Landauer, T. K., & Harshman, R. A. (1990) · Journal of the American Society for Information Science · doi:10.1002/(sici)1097-4571(199009)41:6 · Cited by 12,758 · see citing works
Blei, D. M., Ng, A. Y., & Jordan, M. I. (2002) · The MIT Press eBooks · doi:10.7551/mitpress/1120.003.0082 · Cited by 12,649 · see citing works
Fast, sensitive and accurate integration of single-cell data with Harmony
Korsunsky, I., Millard, N., Fan, J., Slowikowski, K., Zhang, F., Wei, K., Baglaenko, Y., Brenner, M., Loh, P.-R., & Raychaudhuri, S. (2019) · Nature Methods · doi:10.1038/s41592-019-0619-0 · Cited by 10,488 · see citing works
Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y., & Greenleaf, W. J. (2013) · Nature Methods · doi:10.1038/nmeth.2688 · Cited by 6,422 · see citing works
GREAT improves functional interpretation of cis-regulatory regions
McLean, C. Y., Bristor, D., Hiller, M., Clarke, S. L., Schaar, B. T., Lowe, C. B., Wenger, A. M., & Bejerano, G. (2010) · Nature Biotechnology · doi:10.1038/nbt.1630 · Cited by 4,502 · see citing works
Finak, G., McDavid, A., Yajima, M., Deng, J., Gersuk, V., Shalek, A. K., Slichter, C. K., Miller, H. W., McElrath, M. J., Prlic, M., et al. (2015) · Genome Biology · doi:10.1186/s13059-015-0844-5 · Cited by 3,159 · see citing works
Molecular Architecture of the Mouse Nervous System
Zeisel, A., Hochgerner, H., Lönnerberg, P., Johnsson, A., Memic, F., van der Zwan, J., Häring, M., Braun, E., Borm, L. E., La Manno, G., et al. (2018) · Cell · doi:10.1016/j.cell.2018.06.021 · Cited by 2,995 · see citing works
Scrublet: computational identification of cell doublets in single-cell transcriptomic data
Wolock, S. L., Lopez, R., & Klein, A. M. (2019) · Cell Systems · doi:10.1016/j.cels.2018.11.005 · Cited by 2,758 · see citing works
Scrublet: computational identification of cell doublets in single-cell transcriptomic data
Wolock, S. L., Lopez, R., & Klein, A. M. (2018) · doi:10.1101/357368 · Cited by 2,758 · see citing works
Deep generative modeling for single-cell transcriptomics
Lopez, R., Regier, J., Cole, M. B., Jordan, M. I., & Yosef, N. (2018) · Nature Methods · doi:10.1038/s41592-018-0229-2 · Cited by 2,530 · see citing works
Batch effects in single-cell RNA-sequencing data are corrected by matching mutual nearest neighbors
Haghverdi, L., Lun, A. T. L., Morgan, M. D., & Marioni, J. C. (2018) · Nature Biotechnology · doi:10.1038/nbt.4091 · Cited by 2,416 · see citing works
Smart-seq2 for sensitive full-length transcriptome profiling in single cells
Picelli, S., Björklund, Å. K., Faridani, O. R., Sagasser, S., Winberg, G., & Sandberg, R. (2013) · Nature Methods · doi:10.1038/nmeth.2639 · Cited by 2,358 · see citing works
Data-Driven Phenotypic Dissection of AML Reveals Progenitor-like Cells that Correlate with Prognosis
Levine, J. H., Simonds, E. F., Bendall, S. C., Davis, K. L., Amir, E.-A. D., Tadmor, M. D., Litvin, O., Fienberg, H. G., Jager, A., Zunder, E. R., et al. (2015) · Cell · doi:10.1016/j.cell.2015.05.047 · Cited by 2,303 · see citing works
Amara, S. G., Jonas, V., Rosenfeld, M. G., Ong, E. S., & Evans, R. M. (1982) · Nature · doi:10.1038/298240a0 · Cited by 2,105 · see citing works
Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity
Neill, D. R., Wong, S. H., Bellosi, A., Flynn, R. J., Daly, M. G., Langford, T. K. A., Bucks, C. M., Kane, C. M., Fallon, P. G., Pannell, R., et al. (2010) · Nature · doi:10.1038/nature08900 · Cited by 2,079 · see citing works
The Immunological Genome Project: networks of gene expression in immune cells
The Immunological Genome Project Consortium, Heng, T. S. P., Painter, M. W., Elpek, K., Lukacs-Kornek, V., Mauermann, N., Turley, S. J., Koller, D., Kim, F. S., Wagers, A. J., et al. (2008) · Nature Immunology · doi:10.1038/ni1008-1091 · Cited by 1,864 · see citing works
Regional specialization within the intestinal immune system
Mowat, A. M., & Agace, W. W. (2014) · Nature reviews. Immunology · doi:10.1038/nri3738 · Cited by 1,769 · see citing works
A single-cell survey of the small intestinal epithelium
Haber, A. L., Biton, M., Rogel, N., Herbst, R. H., Shekhar, K., Smillie, C., Burgin, G., Delorey, T. M., Howitt, M. R., Katz, Y., et al. (2017) · Nature · doi:10.1038/nature24489 · Cited by 1,750 · see citing works
Self-citationchromVAR: inferring transcription-factor-associated accessibility from single-cell epigenomic data
Schep, A. N., Wu, B., Buenrostro, J. D., & Greenleaf, W. J. (2017) · Nature Methods · doi:10.1038/nmeth.4401 · Cited by 1,680 · see citing works
The biology of innate lymphoid cells
Artis, D., & Spits, H. (2015) · Nature · doi:10.1038/nature14189 · Cited by 1,624 · see citing works
A Cancer Cell Program Promotes T Cell Exclusion and Resistance to Checkpoint Blockade
Jerby-Arnon, L., Shah, P., Cuoco, M. S., Rodman, C., Su, M.-J., Melms, J. C., Leeson, R., Kanodia, A., Mei, S., Lin, J.-R., et al. (2018) · Cell · doi:10.1016/j.cell.2018.09.006 · Cited by 1,429 · see citing works
Self-citationTuft-cell-derived IL-25 regulates an intestinal ILC2-epithelial response circuit
von Moltke, J., Ji, M., Liang, H.-E., & Locksley, R. M. (2016) · Nature · doi:10.1038/nature16161 · Cited by 1,230 · see citing works
Single-Cell Multi-omic Integration Compares and Contrasts Features of Brain Cell Identity
Welch, J. D., Kozareva, V., Ferreira, A., Vanderburg, C., Martin, C., & Macosko, E. Z. (2019) · Cell · doi:10.1016/j.cell.2019.05.006 · Cited by 1,193 · see citing works
Systemically dispersed innate IL-13–expressing cells in type 2 immunity
Price, A. E., Liang, H.-E., Sullivan, B. M., Reinhardt, R. L., Eisley, C. J., Erle, D. J., & Locksley, R. M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1003988107 · Cited by 1,134 · see citing works
Type 2 innate lymphoid cells control eosinophil homeostasis
Nussbaum, J. C., Dyken, S. J. V., von Moltke, J., Cheng, L. E., Mohapatra, A., Molofsky, A. B., Thornton, E. E., Krummel, M. F., Chawla, A., Liang, H.-E., et al. (2013) · Nature · doi:10.1038/nature12526 · Cited by 1,069 · see citing works
Type 2 immunity in tissue repair and fibrosis
Gieseck, R. L., Wilson, M. S., & Wynn, T. A. (2018) · Nature Reviews Immunology · doi:10.1038/nri.2017.90 · Cited by 1,055 · see citing works
Intestinal epithelial tuft cells initiate type 2 mucosal immunity to helminth parasites
Gerbe, F., Sidot, E., Smyth, D. J., Ohmoto, M., Matsumoto, I., Dardalhon, V., Cesses, P., Garnier, L., Pouzolles, M., Brulin, B., et al. (2016) · Nature · doi:10.1038/nature16527 · Cited by 944 · see citing works
Tuft cells, taste-chemosensory cells, orchestrate parasite type 2 immunity in the gut
Howitt, M. R., Lavoie, S., Michaud, M., Blum, A. M., Tran, S. V., Weinstock, J. V., Gallini, C. A., Redding, K., Margolskee, R. F., Osborne, L. C., et al. (2016) · Science · doi:10.1126/science.aaf1648 · Cited by 904 · see citing works
Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation
Stork, P. A., & Schmitt, J. (2002) · Trends in Cell Biology · doi:10.1016/s0962-8924(02)02294-8 · Cited by 897 · see citing works
Barrier Epithelial Cells and the Control of Type 2 Immunity
Hammad, H., & Lambrecht, B. N. (2015) · Immunity · doi:10.1016/j.immuni.2015.07.007 · Cited by 847 · see citing works
Scaling single-cell genomics from phenomenology to mechanism
Tanay, A., & Regev, A. (2017) · Nature · doi:10.1038/nature21350 · Cited by 792 · see citing works
Self-citationInnate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria
Hepworth, M. R., Monticelli, L. A., Fung, T. C., Ziegler, C. G. K., Grunberg, S., Sinha, R., Mantegazza, A. R., Ma, H., Crawford, A., Angelosanto, J., et al. (2013) · Nature · doi:10.1038/nature12240 · Cited by 780 · see citing works
Bias, robustness and scalability in single-cell differential expression analysis
Soneson, C., & Robinson, M. D. (2018) · Nature Methods · doi:10.1038/nmeth.4612 · Cited by 770 · see citing works
Huang, Y., Guo, L., Qiu, J., Chen, X., Hu‐Li, J., Siebenlist, U. K., Williamson, P. R., Urban, J. F., & Paul, W. E. (2014) · Nature Immunology · doi:10.1038/ni.3078 · Cited by 648 · see citing works
Robinette, M. L., Fuchs, A. G., Cortez, V. S., Lee, J. S., Wang, Y., Durum, S. K., Gilfillan, S., & Colonna, M. (2015) · Nature Immunology · doi:10.1038/ni.3094 · Cited by 644 · see citing works
The neuropeptide NMU amplifies ILC2-driven allergic lung inflammation
Wallrapp, A., Riesenfeld, S. J., Burkett, P. R., Abdulnour, R.-E. E., Nyman, J., Dionne, D. A., Hofree, M., Cuoco, M. S., Rodman, C., Farouq, D., et al. (2017) · Nature · doi:10.1038/nature24029 · Cited by 641 · see citing works
Self-citationInterleukin-33 in tissue homeostasis, injury, and inflammation
Molofsky, A. B., Savage, A. K., & Locksley, R. M. (2015) · Immunity · doi:10.1016/j.immuni.2015.06.006 · Cited by 638 · see citing works
Revealing the vectors of cellular identity with single-cell genomics
Wagner, A., Regev, A., & Yosef, N. (2016) · Nature Biotechnology · doi:10.1038/nbt.3711 · Cited by 632 · see citing works
Self-citationNeuronal regulation of type 2 innate lymphoid cells via neuromedin U
Cardoso, V., Chesné, J., Ribeiro, H., García-Cassani, B., Carvalho, T., Bouchery, T., Shah, K., Barbosa-Morais, N. L., Harris, N., & Veiga-Fernandes, H. (2017) · Nature · doi:10.1038/nature23469 · Cited by 592 · see citing works
T Helper Cell Cytokines Modulate Intestinal Stem Cell Renewal and Differentiation
Biton, M., Haber, A. L., Rogel, N., Burgin, G., Beyaz, S., Schnell, A., Ashenberg, O., Su, C., Smillie, C. S., Shekhar, K., et al. (2018) · Cell · doi:10.1016/j.cell.2018.10.008 · Cited by 580 · see citing works
Self-citationThe neuropeptide neuromedin U stimulates innate lymphoid cells and type 2 inflammation
Klose, C. S. N., Mahlakõiv, T., Moeller, J. B., Rankin, L. C., Flamar, A.-L., Kabata, H., Monticelli, L. A., Moriyama, S., Putzel, G., Rakhilin, N., et al. (2017) · Nature · doi:10.1038/nature23676 · Cited by 570 · see citing works
S1P-dependent interorgan trafficking of group 2 innate lymphoid cells supports host defense
Huang, Y., Mao, K., Chen, X., Sun, M., Kawabe, T., Li, W., Usher, N. T., Zhu, J., Urban, J. F., Paul, W. E., et al. (2018) · Science · doi:10.1126/science.aam5809 · Cited by 551 · see citing works
Chen, C., Grennan, K. S., Badner, J. A., Zhang, D., Gershon, E. S., Li, J., & Liu, C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017238 · Cited by 543 · see citing works
Adaptation of Innate Lymphoid Cells to a Micronutrient Deficiency Promotes Type 2 Barrier Immunity
Spencer, S. P., Wilhelm, C., Yang, Q., Hall, J. A., Bouladoux, N., Boyd, A., Nutman, T. B., Urban, J. F., Wang, J., Ramalingam, T. R., et al. (2014) · Science · doi:10.1126/science.1247606 · Cited by 447 · see citing works
Tissue signals imprint ILC2 identity with anticipatory function
Ricardo-González, R. R., Dyken, S. J. V., Schneider, C., Lee, J., Nussbaum, J. C., Liang, H.-E., Vaka, D., Eckalbar, W. L., Molofsky, A. B., Erle, D. J., et al. (2018) · Nature Immunology · doi:10.1038/s41590-018-0201-4 · Cited by 433 · see citing works
Pulmonary neuroendocrine cells amplify allergic asthma responses
Sui, P., Wiesner, D. L., Xu, J., Zhang, Y., Lee, J., Dyken, S. J. V., Lashua, A. J., Yu, C. D., Klein, B. S., Locksley, R. M., et al. (2018) · Science · doi:10.1126/science.aan8546 · Cited by 433 · see citing works
New Paradigms in Type 2 Immunity
Pulendran, B., & Artis, D. (2012) · Science · doi:10.1126/science.1221064 · Cited by 430 · see citing works
Mast cells are required for experimental oral allergen–induced diarrhea
Brandt, E. B., Strait, R. T., Hershko, D., Wang, Q., Muntel, E. E., Scribner, T. A., Zimmermann, N., Finkelman, F. D., & Rothenberg, M. E. (2003) · Journal of Clinical Investigation · doi:10.1172/jci19785 · Cited by 426 · see citing works
Asthma and Allergic Inflammation
Locksley, R. M. (2010) · Cell · doi:10.1016/j.cell.2010.03.004 · Cited by 405 · see citing works
Mechanism and control of class-switch recombination
Manis, J. P., Tian, M., & Alt, F. W. (2002) · Trends in Immunology · doi:10.1016/s1471-4906(01)02111-1 · Cited by 386 · see citing works
β 2 -adrenergic receptor–mediated negative regulation of group 2 innate lymphoid cell responses
Moriyama, S., Brestoff, J. R., Flamar, A.-L., Moeller, J. B., Klose, C. S. N., Rankin, L. C., Yudanin, N. A., Monticelli, L. A., Putzel, G., Rodewald, H.-R., et al. (2018) · Science · doi:10.1126/science.aan4829 · Cited by 379 · see citing works
Tordesillas, L., Berin, M. C., & Sampson, H. A. (2017) · Immunity · doi:10.1016/j.immuni.2017.07.004 · Cited by 341 · see citing works
Interpretable dimensionality reduction of single cell transcriptome data with deep generative models
Ding, J., Condon, A., & Shah, S. P. (2018) · Nature Communications · doi:10.1038/s41467-018-04368-5 · Cited by 337 · see citing works
Self-citationCalcitonin gene-related peptide is a key neurotransmitter in the neuro-immune axis
Assas, B. M., Pennock, J. I., & Miyan, J. A. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00023 · Cited by 226 · see citing works
PD-1 regulates KLRG1+ group 2 innate lymphoid cells
Taylor, S. R., Huang, Y., Mallett, G., Stathopoulou, C., Felizardo, T. C., Sun, M., Martin, E. L., Zhu, N., Woodward, E. L., Elias, M. S., et al. (2017) · The Journal of Experimental Medicine · doi:10.1084/jem.20161653 · Cited by 203 · see citing works
Fast, sensitive, and accurate integration of single cell data with HarmonyPreprint
Korsunsky, I., Fan, J., Slowikowski, K., et al. (2018) · bioRxiv · doi:10.1101/461954 · Cited by 177 · see citing works
Visualizing the structure of RNA-seq expression data using grade of membership models
Dey, K. K., Hsiao, C. J., & Stephens, M. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006599 · Cited by 161 · see citing works
Elevated Sympathetic Nervous Activity in Mice Deficient in αCGRP
Oh-hashi, Y., Shindo, T., Kurihara, Y., Imai, T., Wang, Y., Morita, H., Imai, Y., Kayaba, Y., Nishimatsu, H., Suematsu, Y., et al. (2001) · Circulation Research · doi:10.1161/hh2301.100812 · Cited by 154 · see citing works
Neuromedin U: A Multifunctional Neuropeptide with Pleiotropic Roles
Martínez, V. G., & O’Driscoll, L. (2015) · Clinical Chemistry · doi:10.1373/clinchem.2014.231753 · Cited by 131 · see citing works
Beta-adrenergic receptor signaling in cardiac function and heart failure.
Madamanchi, A. (2007) · PubMed · Cited by 119 · see citing works
Kotas, M. E., & Locksley, R. M. (2018) · Immunity · doi:10.1016/j.immuni.2018.06.002 · Cited by 116 · see citing works
Transcriptomes of the B and T Lineages Compared by Multiplatform Microarray Profiling
Painter, M. W., Davis, S. P., Hardy, R. R., Mathis, D. J., Benoist, C. O., Zhou, Y., Shinton, S. A., Hardy, R. R., Asinovski, N., Davis, S. P., et al. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1002695 · Cited by 103 · see citing works
Self-citationIncreased H1N1 Infection Rate in Children with Asthma
Kloepfer, K. M., Olenec, J. P., Lee, W. M., Liu, G., Vrtis, R. F., Roberg, K. A., Evans, M. D., Gangnon, R. E., Lemanske, R. F., & Gern, J. E. (2012) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201109-1635oc · Cited by 100 · see citing works
duVerle, D. A., Yotsukura, S., Nomura, S., Aburatani, H., & Tsuda, K. (2016) · BMC Bioinformatics · doi:10.1186/s12859-016-1175-6 · Cited by 92 · see citing works
IgE promotes type 2 innate lymphoid cells in murine food allergy
Burton, O. T., Tamayo, J. M., Stranks, A. J., et al. (2017) · Clinical & Experimental Allergy · doi:10.1111/cea.13075 · Cited by 89 · see citing works
Shao, J., & Sheng, H. (2010) · Endocrinology · doi:10.1210/en.2010-0319 · Cited by 87 · see citing works
Affinity Maturation Is Impaired by Natural Killer Cell Suppression of Germinal Centers
Rydyznski, C. E., Cranert, S. A., Zhou, J. Q., Xu, H., Kleinstein, S. H., Singh, H., & Waggoner, S. N. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.08.075 · Cited by 73 · see citing works
Self-citationRodriguez, G., Ross, J. A., Nagy, Z. S., & Kirken, R. A. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.408765 · Cited by 52 · see citing works
CGRP Antibodies as Prophylaxis in Migraine
Edvinsson, L. I. (2018) · Cell · doi:10.1016/j.cell.2018.11.049 · Cited by 50 · see citing works
Klein, M., Vaeth, M., Scheel, T., Grabbe, S., Baumgrass, R., Berberich‐Siebelt, F., Bopp, T., Schmitt, E., & Becker, C. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1102045 · Cited by 41 · see citing works
Ding, J., Shah, S. P., & Condon, A. (2016) · Bioinformatics · doi:10.1093/bioinformatics/btw227 · Cited by 36 · see citing works
Self-citationRowe, R. K., & Gill, M. A. (2014) · Immunology and Allergy Clinics of North America · doi:10.1016/j.iac.2014.09.012 · Cited by 28 · see citing works
Chatterjee, T. K., MOY, J. A., Cai, J., et al. (1993) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)13596-7 · Cited by 25 · see citing works
Bielecki, P., Riesenfeld, S. J., Kowalczyk, M. S., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/461228 · Cited by 21 · see citing works
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Sanmarco, L. M., Wheeler, M. A., Gutiérrez-Vázquez, C., Polonio, C. M., Linnerbauer, M., Pinho-Ribeiro, F. A., Li, Z., Giovannoni, F., Batterman, K. V., Scalisi, G., et al. (2021) · Nature · doi:10.1038/s41586-020-03116-4 · Cited by 331 · see citing works
Central regulation of stress-evoked peripheral immune responses
Chan, K. L., Poller, W. C., Swirski, F. K., & Russo, S. J. (2023) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00729-2 · Cited by 207 · see citing works
Regulatory T cells in the face of the intestinal microbiota
Ramanan, D., Pratama, A., Zhu, Y., Venezia, O., Sassone-Corsi, M., Chowdhary, K., Galván-Peña, S., Sefik, E., Brown, C., Gélineau, A., et al. (2023) · Nature Reviews Immunology · doi:10.1038/s41577-023-00890-w · Cited by 126 · see citing works
Yonekura, S., Terrisse, S., Alves Costa Silva, C., Lafarge, A., Iebba, V., Ferrere, G., Goubet, A.-G., Fahrner, J.-E., Lahmar, I., Ueda, K., et al. (2022) · Cancer Discovery · doi:10.1158/2159-8290.cd-21-0999 · Cited by 112 · see citing works
Neuroimmune mechanisms of type 2 inflammation in the skin and lung
Tamari, M., & Ver Heul, A. M. (2025) · Allergology International · doi:10.1016/j.alit.2025.02.001 · Cited by 17 · see citing works
- Authors
- Xu, H., Ding, J., Porter, C. B. M., Wallrapp, A., Tabaka, M., Ma, S., Fu, S., Guo, X., Riesenfeld, S. J., Su, C., Dionne, D., Nguyen, L. T., Lefkovith, A., Ashenberg, O., Burkett, P. R., Shi, H. N., Rozenblatt-Rosen, O., Graham, D. B., Kuchroo, V. K., Regev, A., & Xavier, R. J.
- Affiliations
- Broad Institute (US)
- Brigham and Women's Hospital (US)
- Westlake University (CN)
- Harvard University (US)
- Corresponding author
- Xu, Heping
- Regev, Aviv
- Xavier, Ramnik J.
- ORCID
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2019-10
- Volume
- 51
- Issue
- 4
- Pages
- 696-708.e9
- ISSN
- 1074-7613 (ISSN-L)
- PMC
- PMC6991097
- OpenAlex
- W2980389928
- Cited by
- 273
- References
- 84
- Citations by year
- 2026: 36 · 2025: 50 · 2024: 44 · 2023: 38 · 2022: 44 · 2021: 35 · 2020: 21 · 2019: 4
- FWCI
- 10.37
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Immunity (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
- Funders
- National Natural Science Foundation of China
- National Institutes of Health
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › IL-33, ST2, and ILC Pathways
- Life Sciences › Immunology and Microbiology › Immunology › Mast cells and histamine
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Keywords
- alpha-calcitonin gene-related peptide, ILC2, intestinal immune cells, type 2 inflammation, neuronal signaling, IL-5, small intestine, immune homeostasis, single-cell transcriptomics
- MeSH terms
- Animals, Cells, Cultured, Immunity, Innate, Inflammation, Intestines, Lymphocytes, Mice, Inbred BALB C, Mice, Transgenic, Neuropeptides, Receptors, Immunologic, Signal Transduction, Calcitonin Gene-Related Peptide, Interleukin-5, Up-Regulation, Sequence Analysis, RNA, Th2 Cells, Computational Biology, Lectins, C-Type, Mice, Single-Cell Analysis, Transcriptome
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