دورية أكاديمية
Universal recording of immune cell interactions in vivo.
العنوان: | Universal recording of immune cell interactions in vivo. |
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المؤلفون: | Nakandakari-Higa S; Laboratory of Lymphocyte Dynamics, The Rockefeller University, New York, NY, USA., Walker S; Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ, USA.; Department of Quantitative and Computational Biology, Princeton University, Princeton, NJ, USA., Canesso MCC; Laboratory of Lymphocyte Dynamics, The Rockefeller University, New York, NY, USA.; Laboratory of Mucosal Immunology, The Rockefeller University, New York, NY, USA., van der Heide V; Marc and Jennifer Lipschultz Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Tisch Cancer Center, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA., Chudnovskiy A; Laboratory of Lymphocyte Dynamics, The Rockefeller University, New York, NY, USA., Kim DY; Laboratory of Mucosal Immunology, The Rockefeller University, New York, NY, USA., Jacobsen JT; Laboratory of Lymphocyte Dynamics, The Rockefeller University, New York, NY, USA.; Institute for Immunology and Transfusion Medicine, Rikshospitalet, University of Oslo, Oslo, Norway., Parsa R; Laboratory of Mucosal Immunology, The Rockefeller University, New York, NY, USA., Bilanovic J; Laboratory of Lymphocyte Dynamics, The Rockefeller University, New York, NY, USA., Parigi SM; Laboratory of Mammalian Cell Biology and Development, The Rockefeller University, New York, NY, USA., Fiedorczuk K; Laboratory of Membrane Biology and Biophysics, The Rockefeller University, New York, NY, USA., Fuchs E; Laboratory of Mammalian Cell Biology and Development, The Rockefeller University, New York, NY, USA.; Howard Hughes Medical Institute, The Rockefeller University, New York, NY, USA., Bilate AM; Laboratory of Mucosal Immunology, The Rockefeller University, New York, NY, USA., Pasqual G; Laboratory of Synthetic Immunology, Department of Surgery, Oncology and Gastroenterology, University of Padova, Padua, Italy., Mucida D; Laboratory of Mucosal Immunology, The Rockefeller University, New York, NY, USA.; Howard Hughes Medical Institute, The Rockefeller University, New York, NY, USA., Kamphorst AO; Marc and Jennifer Lipschultz Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Tisch Cancer Center, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA., Pritykin Y; Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ, USA. pritykin@princeton.edu.; Department of Computer Science, Princeton University, Princeton, NJ, USA. pritykin@princeton.edu., Victora GD; Laboratory of Lymphocyte Dynamics, The Rockefeller University, New York, NY, USA. victora@rockefeller.edu. |
المصدر: | Nature [Nature] 2024 Mar; Vol. 627 (8003), pp. 399-406. Date of Electronic Publication: 2024 Mar 06. |
نوع المنشور: | Journal Article |
اللغة: | English |
بيانات الدورية: | Publisher: Nature Publishing Group Country of Publication: England NLM ID: 0410462 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1476-4687 (Electronic) Linking ISSN: 00280836 NLM ISO Abbreviation: Nature Subsets: MEDLINE |
أسماء مطبوعة: | Publication: Basingstoke : Nature Publishing Group Original Publication: London, Macmillan Journals ltd. |
مواضيع طبية MeSH: | CD8-Positive T-Lymphocytes*/cytology , CD8-Positive T-Lymphocytes*/immunology , Cell Communication*/immunology , Dendritic Cells*/cytology , Dendritic Cells*/immunology , T-Lymphocytes, Regulatory*/cytology , T-Lymphocytes, Regulatory*/immunology , T Follicular Helper Cells*/cytology , T Follicular Helper Cells*/immunology , B-Lymphocytes*/cytology , B-Lymphocytes*/immunology , Epithelial Cells*/cytology , Epithelial Cells*/immunology, Ligands ; Germinal Center/cytology ; Single-Cell Gene Expression Analysis ; Intestinal Mucosa/cytology ; Intestinal Mucosa/immunology ; Lymphocytic choriomeningitis virus/immunology ; Lymphocytic Choriomeningitis/immunology ; Lymphocytic Choriomeningitis/virology ; Organ Specificity |
مستخلص: | Immune cells rely on transient physical interactions with other immune and non-immune populations to regulate their function 1 . To study these 'kiss-and-run' interactions directly in vivo, we previously developed LIPSTIC (labelling immune partnerships by SorTagging intercellular contacts) 2 , an approach that uses enzymatic transfer of a labelled substrate between the molecular partners CD40L and CD40 to label interacting cells. Reliance on this pathway limited the use of LIPSTIC to measuring interactions between CD4 + T helper cells and antigen-presenting cells, however. Here we report the development of a universal version of LIPSTIC (uLIPSTIC), which can record physical interactions both among immune cells and between immune and non-immune populations irrespective of the receptors and ligands involved. We show that uLIPSTIC can be used, among other things, to monitor the priming of CD8 + T cells by dendritic cells, reveal the steady-state cellular partners of regulatory T cells and identify germinal centre-resident T follicular helper cells on the basis of their ability to interact cognately with germinal centre B cells. By coupling uLIPSTIC with single-cell transcriptomics, we build a catalogue of the immune populations that physically interact with intestinal epithelial cells at the steady state and profile the evolution of the interactome of lymphocytic choriomeningitis virus-specific CD8 + T cells in multiple organs following systemic infection. Thus, uLIPSTIC provides a broadly useful technology for measuring and understanding cell-cell interactions across multiple biological systems. (© 2024. The Author(s), under exclusive licence to Springer Nature Limited.) |
References: | Dustin, M. L. The immunological synapse. Cancer Immunol. Res. 2, 1023–1033 (2014). (PMID: 25367977469205110.1158/2326-6066.CIR-14-0161) Pasqual, G. et al. Monitoring T cell-dendritic cell interactions in vivo by intercellular enzymatic labelling. Nature 553, 496–500 (2018). (PMID: 29342141585312910.1038/nature25442) Greenwald, I. & Rubin, G. M. Making a difference: the role of cell-cell interactions in establishing separate identities for equivalent cells. Cell 68, 271–281 (1992). (PMID: 136540210.1016/0092-8674(92)90470-W) Sudhof, T. C. & Malenka, R. C. Understanding synapses: past, present, and future. Neuron 60, 469–476 (2008). (PMID: 18995821324374110.1016/j.neuron.2008.10.011) Victora, G. D. & Nussenzweig, M. C. Germinal centers. Annu. Rev. Immunol. 30, 429–457 (2012). (PMID: 2222477210.1146/annurev-immunol-020711-075032) Bilate, A. M. et al. T cell receptor is required for differentiation, but not maintenance, of intestinal CD4 + intraepithelial lymphocytes. Immunity 53, 1001–1014 (2020). (PMID: 33022229767718210.1016/j.immuni.2020.09.003) Niec, R. E., Rudensky, A. Y. & Fuchs, E. Inflammatory adaptation in barrier tissues. Cell 184, 3361–3375 (2021). (PMID: 34171319833667510.1016/j.cell.2021.05.036) Mempel, T. R., Henrickson, S. E. & Von Andrian, U. H. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427, 154–159 (2004). (PMID: 1471227510.1038/nature02238) Moses, L. & Pachter, L. Museum of spatial transcriptomics. Nat. Methods 19, 534–546 (2022). (PMID: 3527339210.1038/s41592-022-01409-2) Efremova, M., Vento-Tormo, M., Teichmann, S. A. & Vento-Tormo, R. CellPhoneDB: inferring cell–cell communication from combined expression of multi-subunit ligand–receptor complexes. Nat. Protoc. 15, 1484–1506 (2020). (PMID: 3210320410.1038/s41596-020-0292-x) Liu, D. S., Loh, K. H., Lam, S. S., White, K. A. & Ting, A. Y. Imaging trans-cellular neurexin-neuroligin interactions by enzymatic probe ligation. PLoS ONE 8, e52823 (2013). (PMID: 23457442357304610.1371/journal.pone.0052823) Ombrato, L. et al. Metastatic-niche labelling reveals parenchymal cells with stem features. Nature 572, 603–608 (2019). (PMID: 31462798679749910.1038/s41586-019-1487-6) Zhang, S. et al. Monitoring of cell-cell communication and contact history in mammals. Science 378, eabo5503 (2022). (PMID: 3645484810.1126/science.abo5503) Bechtel, T. J., Reyes-Robles, T., Fadeyi, O. O. & Oslund, R. C. Strategies for monitoring cell–cell interactions. Nat. Chem. Biol. 17, 641–652 (2021). (PMID: 3403551410.1038/s41589-021-00790-x) Yassin, M. et al. Upregulation of PD-1 follows tumour development in the AOM/DSS model of inflammation-induced colorectal cancer in mice. Immunology 158, 35–46 (2019). (PMID: 31429085670046710.1111/imm.13093) Weizman, O. E. et al. Developing synthetic tools to decipher the tumor-immune interactome. Proc. Natl Acad. Sci. USA 120, e2306632120 (2023). (PMID: 378712021062292510.1073/pnas.2306632120) Dorr, B. M., Ham, H. O., An, C., Chaikof, E. L. & Liu, D. R. Reprogramming the specificity of sortase enzymes. Proc. Natl Acad. Sci. USA 111, 13343–13348 (2014). (PMID: 25187567416994310.1073/pnas.1411179111) Guimaraes, C. P. et al. Site-specific C-terminal and internal loop labeling of proteins using sortase-mediated reactions. Nat. Protoc. 8, 1787–1799 (2013). (PMID: 23989673394346110.1038/nprot.2013.101) Dustin, M. L. & Depoil, D. New insights into the T cell synapse from single molecule techniques. Nat. Rev. Immunol. 11, 672–684 (2011). (PMID: 21904389388920010.1038/nri3066) Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133–140 (2010). (PMID: 2002365310.1038/nn.2467) Robertson, J. M., Jensen, P. E. & Evavold, B. D. DO11.10 and OT-II T cells recognize a C-terminal ovalbumin 323-339 epitope. J. Immunol. 164, 4706–4712 (2000). (PMID: 1077977610.4049/jimmunol.164.9.4706) Merkenschlager, J. et al. Dynamic regulation of T Stoll, S., Delon, J., Brotz, T. M. & Germain, R. N. Dynamic imaging of T cell-dendritic cell interactions in lymph nodes. Science 296, 1873–1876 (2002). (PMID: 1205296110.1126/science.1071065) Frederico, B. et al. DNGR-1-tracing marks an ependymal cell subset with damage-responsive neural stem cell potential. Dev. Cell 57, 1957–1975 (2022). (PMID: 35998585961680010.1016/j.devcel.2022.07.012) Rubtsov, Y. P. et al. Stability of the regulatory T cell lineage in vivo. Science 329, 1667–1671 (2010). (PMID: 20929851426215110.1126/science.1191996) Aghajani, K., Keerthivasan, S., Yu, Y. & Gounari, F. Generation of CD4CreER T2 transgenic mice to study development of peripheral CD4-T-cells. Genesis 50, 908–913 (2012). (PMID: 22887772353556110.1002/dvg.22052) Shulman, Z. et al. T follicular helper cell dynamics in germinal centers. Science 341, 673–677 (2013). (PMID: 23887872394146710.1126/science.1241680) Dogan, I. et al. Multiple layers of B cell memory with different effector functions. Nat. Immunol. 10, 1292–1299 (2009). (PMID: 1985538010.1038/ni.1814) McDonald, B. D., Jabri, B. & Bendelac, A. Diverse developmental pathways of intestinal intraepithelial lymphocytes. Nat. Rev. Immunol. 18, 514–525 (2018). (PMID: 29717233606379610.1038/s41577-018-0013-7) el Marjou, F. et al. Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 39, 186–193 (2004). (PMID: 1528274510.1002/gene.20042) Mucida, D. et al. Transcriptional reprogramming of mature CD4 + helper T cells generates distinct MHC class II-restricted cytotoxic T lymphocytes. Nat. Immunol. 14, 281–289 (2013). (PMID: 23334788358108310.1038/ni.2523) London, M., Bilate, A. M., Castro, T. B. R., Sujino, T. & Mucida, D. Stepwise chromatin and transcriptional acquisition of an intraepithelial lymphocyte program. Nat. Immunol. 22, 449–459 (2021). (PMID: 33686285825170010.1038/s41590-021-00883-8) Cepek, K. L. et al. Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin. Nature 372, 190–193 (1994). (PMID: 796945310.1038/372190a0) Zen, K. et al. Neutrophil migration across tight junctions is mediated by adhesive interactions between epithelial coxsackie and adenovirus receptor and a junctional adhesion molecule-like protein on neutrophils. Mol. Biol. Cell 16, 2694–2703 (2005). (PMID: 15800062114241710.1091/mbc.e05-01-0036) Cohen, C. J. et al. The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. Proc. Natl Acad. Sci. USA 98, 15191–15196 (2001). (PMID: 117346286500510.1073/pnas.261452898) Pazirandeh, A. et al. Multiple phenotypes in adult mice following inactivation of the Coxsackievirus and Adenovirus Receptor (Car) gene. PLoS ONE 6, e20203 (2011). (PMID: 21674029310858510.1371/journal.pone.0020203) Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545–15550 (2005). (PMID: 16199517123989610.1073/pnas.0506580102) Oldstone, M. B. et al. Virus and immune responses: lymphocytic choriomeningitis virus as a prototype model of viral pathogenesis. Br. Med. Bull. 41, 70–74 (1985). (PMID: 388219010.1093/oxfordjournals.bmb.a072029) Olson, M. R., McDermott, D. S. & Varga, S. M. The initial draining lymph node primes the bulk of the CD8 T cell response and influences memory T cell trafficking after a systemic viral infection. PLoS Pathog. 8, e1003054 (2012). (PMID: 23236277351655410.1371/journal.ppat.1003054) Jakubzick, C. et al. Minimal differentiation of classical monocytes as they survey steady-state tissues and transport antigen to lymph nodes. Immunity 39, 599–610 (2013). (PMID: 2401241610.1016/j.immuni.2013.08.007) Puglielli, M. T. et al. In vivo selection of a lymphocytic choriomeningitis virus variant that affects recognition of the GP33-43 epitope by H-2Db but not H-2Kb. J. Virol. 75, 5099–5107 (2001). (PMID: 1133389111491510.1128/JVI.75.11.5099-5107.2001) Stevens, A. J. et al. Programming multicellular assembly with synthetic cell adhesion molecules. Nature 614, 144–152 (2022). (PMID: 36509107989200410.1038/s41586-022-05622-z) Giladi, A. et al. Dissecting cellular crosstalk by sequencing physically interacting cells. Nat. Biotechnol. 38, 629–637 (2020). (PMID: 3215259810.1038/s41587-020-0442-2) Sujino, T. et al. Tissue adaptation of regulatory and intraepithelial CD4 + T cells controls gut inflammation. Science 352, 1581–1586 (2016). (PMID: 27256884496807910.1126/science.aaf3892) Shin, K. S. et al. Monocyte-derived dendritic cells dictate the memory differentiation of CD8 + T cells during acute infection. Front. Immunol. 10, 1887 (2019). (PMID: 31474983670681610.3389/fimmu.2019.01887) Engels, B. et al. Retroviral vectors for high-level transgene expression in T lymphocytes. Hum. Gene Ther. 14, 1155–1168 (2003). (PMID: 1290896710.1089/104303403322167993) Kim, J. H. et al. High cleavage efficiency of a 2A peptide derived from porcine teschovirus-1 in human cell lines, zebrafish and mice. PLoS ONE 6, e18556 (2011). (PMID: 21602908308470310.1371/journal.pone.0018556) Argos, P. An investigation of oligopeptides linking domains in protein tertiary structures and possible candidates for general gene fusion. J. Mol. Biol. 211, 943–958 (1990). (PMID: 231370110.1016/0022-2836(90)90085-Z) Lee, P. P. et al. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15, 763–774 (2001). (PMID: 1172833810.1016/S1074-7613(01)00227-8) Schraml, B. U. et al. Genetic tracing via DNGR-1 expression history defines dendritic cells as a hematopoietic lineage. Cell 154, 843–858 (2013). (PMID: 2395311510.1016/j.cell.2013.07.014) Shinnakasu, R. et al. Regulated selection of germinal-center cells into the memory B cell compartment. Nat. Immunol. 17, 861–869 (2016). (PMID: 2715884110.1038/ni.3460) Barnden, M. J., Allison, J., Heath, W. R. & Carbone, F. R. Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and beta-chain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 76, 34–40 (1998). (PMID: 955377410.1046/j.1440-1711.1998.00709.x) Danciu, C. et al. A characterization of four B16 murine melanoma cell sublines molecular fingerprint and proliferation behavior. Cancer Cell Int. 13, 75 (2013). (PMID: 23890195375023310.1186/1475-2867-13-75) Sanchez, A. B. & de la Torre, J. C. Rescue of the prototypic Arenavirus LCMV entirely from plasmid. Virology 350, 370–380 (2006). (PMID: 1647646110.1016/j.virol.2006.01.012) Emonet, S. F., Garidou, L., McGavern, D. B. & de la Torre, J. C. Generation of recombinant lymphocytic choriomeningitis viruses with trisegmented genomes stably expressing two additional genes of interest. Proc. Natl Acad. Sci. USA 106, 3473–3478 (2009). (PMID: 19208813265127010.1073/pnas.0900088106) Iwasaki, M., Ngo, N., Cubitt, B., Teijaro, J. R. & de la Torre, J. C. General molecular strategy for development of arenavirus live-attenuated vaccines. J. Virol. 89, 12166–12177 (2015). (PMID: 26401045464531810.1128/JVI.02075-15) van der Heide, V. et al. Functional impairment of “helpless” CD8+ memory T cells is transient and driven by prolonged but finite cognate antigen presentation. Preprint at bioRxiv https://doi.org/10.1101/2024.01.22.576725 (2024). Pasqual, G., Angelini, A. & Victora, G. D. Triggering positive selection of germinal center B cells by antigen targeting to DEC-205. Methods Mol. Biol. 1291, 125–134 (2015). (PMID: 2583630610.1007/978-1-4939-2498-1_10) Bilate, A. M. et al. Tissue-specific emergence of regulatory and intraepithelial T cells from a clonal T cell precursor. Sci. Immunol. 1, eaaf7471 (2016). (PMID: 28783695629646110.1126/sciimmunol.aaf7471) Wolf, F. A., Angerer, P. & Theis, F. J. SCANPY: large-scale single-cell gene expression data analysis. Genome Biol. 19, 15 (2018). (PMID: 29409532580205410.1186/s13059-017-1382-0) Sturm, G. et al. Scirpy: a Scanpy extension for analyzing single-cell T-cell receptor-sequencing data. Bioinformatics 36, 4817–4818 (2020). (PMID: 32614448775101510.1093/bioinformatics/btaa611) Franzen, O., Gan, L. M. & Bjorkegren, J. L. M. PanglaoDB: a web server for exploration of mouse and human single-cell RNA sequencing data. Database 2019, baz046 (2019). (PMID: 30951143645003610.1093/database/baz046) Setty, M. et al. Wishbone identifies bifurcating developmental trajectories from single-cell data. Nat. Biotechnol. 34, 637–645 (2016). (PMID: 27136076490089710.1038/nbt.3569) Storey, J. D. & Tibshirani, R. Statistical significance for genomewide studies. Proc. Natl Acad. Sci. USA 100, 9440–9445 (2003). (PMID: 1288300517093710.1073/pnas.1530509100) Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021). (PMID: 34265844837160510.1038/s41586-021-03819-2) Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126–2132 (2004). (PMID: 1557276510.1107/S0907444904019158) Ko, J., Park, H., Heo, L. & Seok, C. GalaxyWEB server for protein structure prediction and refinement. Nucleic Acids Res. 40, W294–W297 (2012). (PMID: 22649060339431110.1093/nar/gks493) Jo, S., Kim, T., Iyer, V. G. & Im, W. CHARMM-GUI: a web-based graphical user interface for CHARMM. J. Comput. Chem. 29, 1859–1865 (2008). (PMID: 1835159110.1002/jcc.20945) Paulick, M. G. & Bertozzi, C. R. The glycosylphosphatidylinositol anchor: a complex membrane-anchoring structure for proteins. Biochemistry 47, 6991–7000 (2008). (PMID: 1855763310.1021/bi8006324) Goddard, T. D. et al. UCSF ChimeraX: meeting modern challenges in visualization and analysis. Protein Sci. 27, 14–25 (2018). (PMID: 2871077410.1002/pro.3235) PyMOL v.2.4.0 (Schrödinger & DeLano, 2020). Butler, A., Hoffman, P., Smibert, P., Papalexi, E. & Satija, R. Integrating single-cell transcriptomic data across different conditions, technologies, and species. Nat. Biotechnol. 36, 411–420 (2018). (PMID: 29608179670074410.1038/nbt.4096) |
معلومات مُعتمدة: | R01 AI173086 United States AI NIAID NIH HHS; R37 AR027883 United States AR NIAMS NIH HHS; R01 AI153363 United States AI NIAID NIH HHS; R01 AR050452 United States AR NIAMS NIH HHS; DP2 AI171161 United States AI NIAID NIH HHS; T32 HG003284 United States HG NHGRI NIH HHS; R01 AR027883 United States AR NIAMS NIH HHS; United Kingdom WT_ Wellcome Trust; DP1 AI144248 United States AI NIAID NIH HHS |
المشرفين على المادة: | 0 (Ligands) |
تواريخ الأحداث: | Date Created: 20240306 Date Completed: 20240315 Latest Revision: 20240605 |
رمز التحديث: | 20240606 |
مُعرف محوري في PubMed: | PMC11078586 |
DOI: | 10.1038/s41586-024-07134-4 |
PMID: | 38448581 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1476-4687 |
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DOI: | 10.1038/s41586-024-07134-4 |