دورية أكاديمية

Screening cell-cell communication in spatial transcriptomics via collective optimal transport.

التفاصيل البيبلوغرافية
العنوان: Screening cell-cell communication in spatial transcriptomics via collective optimal transport.
المؤلفون: Cang Z; Department of Mathematics and Center for Research in Scientific Computation, North Carolina State University, Raleigh, NC, USA., Zhao Y; Department of Mathematics, The George Washington University, Washington, DC, USA., Almet AA; Department of Mathematics, University of California, Irvine, Irvine, CA, USA.; The NSF-Simons Center for Multiscale Cell Fate Research, University of California, Irvine, Irvine, CA, USA., Stabell A; The NSF-Simons Center for Multiscale Cell Fate Research, University of California, Irvine, Irvine, CA, USA.; Department of Developmental and Cell Biology, University of California, Irvine, Irvine, CA, USA., Ramos R; The NSF-Simons Center for Multiscale Cell Fate Research, University of California, Irvine, Irvine, CA, USA.; Department of Developmental and Cell Biology, University of California, Irvine, Irvine, CA, USA., Plikus MV; The NSF-Simons Center for Multiscale Cell Fate Research, University of California, Irvine, Irvine, CA, USA.; Department of Developmental and Cell Biology, University of California, Irvine, Irvine, CA, USA., Atwood SX; The NSF-Simons Center for Multiscale Cell Fate Research, University of California, Irvine, Irvine, CA, USA.; Department of Developmental and Cell Biology, University of California, Irvine, Irvine, CA, USA., Nie Q; Department of Mathematics, University of California, Irvine, Irvine, CA, USA. qnie@uci.edu.; The NSF-Simons Center for Multiscale Cell Fate Research, University of California, Irvine, Irvine, CA, USA. qnie@uci.edu.; Department of Developmental and Cell Biology, University of California, Irvine, Irvine, CA, USA. qnie@uci.edu.
المصدر: Nature methods [Nat Methods] 2023 Feb; Vol. 20 (2), pp. 218-228. Date of Electronic Publication: 2023 Jan 23.
نوع المنشور: Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't; Research Support, U.S. Gov't, Non-P.H.S.
اللغة: English
بيانات الدورية: Publisher: Nature Pub. Group Country of Publication: United States NLM ID: 101215604 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1548-7105 (Electronic) Linking ISSN: 15487091 NLM ISO Abbreviation: Nat Methods Subsets: MEDLINE
أسماء مطبوعة: Original Publication: New York, NY : Nature Pub. Group, c2004-
مواضيع طبية MeSH: Transcriptome* , Cell Communication*/genetics, Humans ; Gene Expression Profiling ; Signal Transduction ; Computer Simulation ; Single-Cell Analysis
مستخلص: Spatial transcriptomic technologies and spatially annotated single-cell RNA sequencing datasets provide unprecedented opportunities to dissect cell-cell communication (CCC). However, incorporation of the spatial information and complex biochemical processes required in the reconstruction of CCC remains a major challenge. Here, we present COMMOT (COMMunication analysis by Optimal Transport) to infer CCC in spatial transcriptomics, which accounts for the competition between different ligand and receptor species as well as spatial distances between cells. A collective optimal transport method is developed to handle complex molecular interactions and spatial constraints. Furthermore, we introduce downstream analysis tools to infer spatial signaling directionality and genes regulated by signaling using machine learning models. We apply COMMOT to simulation data and eight spatial datasets acquired with five different technologies to show its effectiveness and robustness in identifying spatial CCC in data with varying spatial resolutions and gene coverages. Finally, COMMOT identifies new CCCs during skin morphogenesis in a case study of human epidermal development.
(© 2023. The Author(s).)
التعليقات: Comment in: Nat Methods. 2023 Feb;20(2):185-186. (PMID: 36693905)
References: Svensson, V., Vento-Tormo, R. & Teichmann, S. A. Exponential scaling of single-cell RNA-seq in the past decade. Nat. Protoc. 13, 599–604 (2018). (PMID: 10.1038/nprot.2017.14929494575)
Armingol, E., Officer, A., Harismendy, O. & Lewis, N. E. Deciphering cell–cell interactions and communication from gene expression. Nat. Rev. Genet. 22, 71–88 (2021). (PMID: 10.1038/s41576-020-00292-x33168968)
Almet, A. A., Cang, Z., Jin, S. & Nie, Q. The landscape of cell–cell communication through single-cell transcriptomics. Curr. Opin. Syst. Biol. 26, 12–23 (2021). (PMID: 10.1016/j.coisb.2021.03.007339692478104132)
Türei, D. et al. Integrated intra‐ and intercellular signaling knowledge for multicellular omics analysis. Mol. Syst. Biol. 17, e9923 (2021). (PMID: 10.15252/msb.20209923337499937983032)
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: 10.1038/s41596-020-0292-x32103204)
Jin, S. et al. Inference and analysis of cell–cell communication using CellChat. Nat. Commun. 12, 1088 (2021). (PMID: 10.1038/s41467-021-21246-9335975227889871)
Noël, F. et al. Dissection of intercellular communication using the transcriptome-based framework ICELLNET. Nat. Commun. 12, 1089 (2021). (PMID: 10.1038/s41467-021-21244-x335975287889941)
Wang, S., Karikomi, M., Maclean, A. L. & Nie, Q. Cell lineage and communication network inference via optimization for single-cell transcriptomics. Nucleic Acids Res. 47, e66 (2019). (PMID: 10.1093/nar/gkz204309238156582411)
Browaeys, R., Saelens, W. & Saeys, Y. NicheNet: modeling intercellular communication by linking ligands to target genes. Nat. Methods 17, 159–162 (2020). (PMID: 10.1038/s41592-019-0667-531819264)
Hu, Y., Peng, T., Gao, L. & Tan, K. CytoTalk: de novo construction of signal transduction networks using single-cell transcriptomic data. Sci. Adv. 7, eabf1356 (2021). (PMID: 10.1126/sciadv.abf1356338537808046375)
Tsuyuzaki, K., Ishii, M. & Nikaido, I. Uncovering hypergraphs of cell–cell interaction from single cell RNA-sequencing data. Preprint at https://doi.org/10.1101/566182 (2019).
Vento-Tormo, R. et al. Single-cell reconstruction of the early maternal–fetal interface in humans. Nature 563, 347–353 (2018). (PMID: 10.1038/s41586-018-0698-6304295487612850)
Abbasi, S. et al. Distinct regulatory programs control the latent regenerative potential of dermal fibroblasts during wound healing. Cell Stem Cell 27, 396–412 (2020). (PMID: 10.1016/j.stem.2020.07.00832755548)
Armingol, E. et al. Inferring a spatial code of cell–cell interactions across a whole animal body. PLoS Comput. Biol. 18, e1010715 (2022).
Dries, R. et al. Advances in spatial transcriptomic data analysis. Genome Res. 31, 1706–1718 (2021). (PMID: 10.1101/gr.275224.121345990048494229)
Ståhl, P. L. et al. Visualization and analysis of gene expression in tissue sections by spatial transcriptomics. Science 353, 78–82 (2016). (PMID: 10.1126/science.aaf240327365449)
Rodriques, S. G. et al. Slide-seq: a scalable technology for measuring genome-wide expression at high spatial resolution. Science 363, 1463–1467 (2019). (PMID: 10.1126/science.aaw1219309232256927209)
Eng, C.-H. L. et al. Transcriptome-scale super-resolved imaging in tissues by RNA seqFISH+. Nature 568, 235–239 (2019). (PMID: 10.1038/s41586-019-1049-y309111686544023)
Chen, K. H., Boettiger, A. N., Moffitt, J. R., Wang, S. & Zhuang, X. RNA imaging. Spatially resolved, highly multiplexed RNA profiling in single cells. Science 348, aaa6090 (2015). (PMID: 10.1126/science.aaa6090258589774662681)
Wang, X. et al. Three-dimensional intact-tissue sequencing of single-cell transcriptional states. Science 361, eaat5691 (2018). (PMID: 10.1126/science.aat5691299300896339868)
Rao, A., Barkley, D., França, G. S. & Yanai, I. Exploring tissue architecture using spatial transcriptomics. Nature 596, 211–220 (2021). (PMID: 10.1038/s41586-021-03634-9343812318475179)
Palla, G. et al. Squidpy: a scalable framework for spatial omics analysis. Nat. Methods 19, 171–178 (2022). (PMID: 10.1038/s41592-021-01358-2351023468828470)
Dries, R. et al. Giotto: a toolbox for integrative analysis and visualization of spatial expression data. Genome Biol. 22, 78 (2021). (PMID: 10.1186/s13059-021-02286-2336854917938609)
Pham, D. T. et al. stLearn: integrating spatial location, tissue morphology and gene expression to find cell types, cell–cell interactions and spatial trajectories within undissociated tissues. Preprint at https://doi.org/10.1101/2020.05.31.125658 (2020).
Garcia-Alonso, L. et al. Mapping the temporal and spatial dynamics of the human endometrium in vivo and in vitro. Nat. Genet. 53, 1698–1711 (2021). (PMID: 10.1038/s41588-021-00972-2348579548648563)
Arnol, D., Schapiro, D., Bodenmiller, B., Saez-Rodriguez, J. & Stegle, O. Modeling cell–cell interactions from spatial molecular data with spatial variance component analysis. Cell Rep. 29, 202–211 (2019). (PMID: 10.1016/j.celrep.2019.08.077315779496899515)
Tanevski, J., Flores, R. O. R., Gabor, A., Schapiro, D. & Saez-Rodriguez, J. Explainable multiview framework for dissecting spatial relationships from highly multiplexed data. Genome Biol. 23, 97 (2022).
Fischer, D. S., Schaar, A. C. & Theis, F. J. Modeling intercellular communication in tissues using spatial graphs of cells. Nat. Biotechnol. (2022).
Forrow, A. et al. Statistical optimal transport via factored couplings. In Proceedings of the Twenty-Second International Conference on Artificial Intelligence and Statistics (eds. Chaudhuri, K. & Sugiyama, M.) 89 2454–2465 (PMLR, 2019).
Schiebinger, G. et al. Optimal-transport analysis of single-cell gene expression identifies developmental trajectories in reprogramming. Cell 176, 928–943 (2019). (PMID: 10.1016/j.cell.2019.01.006307128746402800)
Cang, Z. & Nie, Q. Inferring spatial and signaling relationships between cells from single cell transcriptomic data. Nat. Commun. 11, 2084 (2020). (PMID: 10.1038/s41467-020-15968-5323502827190659)
Nitzan, M., Karaiskos, N., Friedman, N. & Rajewsky, N. Gene expression cartography. Nature 576, 132–137 (2019). (PMID: 10.1038/s41586-019-1773-331748748)
Peyré, G. & Cuturi, M. Computational optimal transport: with applications to data science. Foundations and Trends in Machine Learning 11, 355–607 (2019). (PMID: 10.1561/2200000073)
Villani, C. Optimal Transport: Old and New (Springer Science & Business Media, 2008).
Ramilowski, J. A. et al. A draft network of ligand–receptor-mediated multicellular signalling in human. Nat. Commun. 6, 7866 (2015). (PMID: 10.1038/ncomms886626198319)
Figalli, A. The optimal partial transport problem. Arch. Rational Mech. Anal. 195, 533–560 (2010). (PMID: 10.1007/s00205-008-0212-7)
Bonneel, N. & Coeurjolly, D. SPOT: sliced partial optimal transport. ACM Transactions on Graphics 38, 89 (2019). (PMID: 10.1145/3306346.3323021)
Chizat, L., Peyré, G., Schmitzer, B. & Vialard, F.-X. Scaling algorithms for unbalanced optimal transport problems. Mathematics of Computation 87, 2563–2609 (2018). (PMID: 10.1090/mcom/3303)
Wang, S. et al. Single cell transcriptomics of human epidermis identifies basal stem cell transition states. Nat. Commun. 11, 4239 (2020). (PMID: 10.1038/s41467-020-18075-7328436407447770)
Choi, Y. S. et al. Distinct functions for Wnt/β-catenin in hair follicle stem cell proliferation and survival and interfollicular epidermal homeostasis. Cell Stem Cell 13, 720–733 (2013). (PMID: 10.1016/j.stem.2013.10.003243154443900235)
Bamberger, C. et al. Activin controls skin morphogenesis and wound repair predominantly via stromal cells and in a concentration-dependent manner via keratinocytes. Am. J. Pathol. 167, 733–747 (2005). (PMID: 10.1016/S0002-9440(10)62047-0161271531698729)
Mou, H. et al. Dual SMAD signaling inhibition enables long-term expansion of diverse epithelial basal cells. Cell Stem Cell 19, 217–231 (2016). (PMID: 10.1016/j.stem.2016.05.012273200414975684)
Moffitt, J. R. et al. Molecular, spatial, and functional single-cell profiling of the hypothalamic preoptic region. Science 362, eaau5324 (2018). (PMID: 10.1126/science.aau5324303854646482113)
Froemke, R. C. & Young, L. J. Oxytocin, neural plasticity, and social behavior. Annu. Rev. Neurosci. 44, 359–381 (2021). (PMID: 10.1146/annurev-neuro-102320-102847338236548604207)
Warfvinge, K., Krause, D. & Edvinsson, L. The distribution of oxytocin and the oxytocin receptor in rat brain: relation to regions active in migraine. J. Headache Pain 21, 10 (2020). (PMID: 10.1186/s10194-020-1079-8320288997006173)
He, Y. et al. ClusterMap for multi-scale clustering analysis of spatial gene expression. Nat. Commun. 12, 5909 (2021). (PMID: 10.1038/s41467-021-26044-x346255468501103)
Bie, C. et al. Insulin-like growth factor 1 receptor drives hepatocellular carcinoma growth and invasion by activating Stat3-Midkine-Stat3 loop. Dig. Dis. Sci. 67, 569–584 (2022). (PMID: 10.1007/s10620-021-06862-133559791)
Sandovici, I. et al. The imprinted Igf2–Igf2r axis is critical for matching placental microvasculature expansion to fetal growth. Dev. Cell 57, 63–79 (2022). (PMID: 10.1016/j.devcel.2021.12.005349630588751640)
Marchese, M. J., Li, S., Liu, B., Zhang, J. J. & Feng, L. Perfluoroalkyl substance exposure and the BDNF pathway in the placental trophoblast. Front. Endocrinol. (Lausanne) 12, 694885 (2021). (PMID: 10.3389/fendo.2021.694885)
Jeyarajah, M. J., Jaju Bhattad, G., Kops, B. F. & Renaud, S. J. Syndecan-4 regulates extravillous trophoblast migration by coordinating protein kinase C activation. Sci. Rep. 9, 10175 (2019). (PMID: 10.1038/s41598-019-46599-6313084096629623)
Bocchi, R. et al. Perturbed Wnt signaling leads to neuronal migration delay, altered interhemispheric connections and impaired social behavior. Nat. Commun. 8, 1158 (2017). (PMID: 10.1038/s41467-017-01046-w290798195660087)
Stickels, R. R. et al. Highly sensitive spatial transcriptomics at near-cellular resolution with Slide-seqV2. Nat. Biotechnol. 39, 313–319 (2021). (PMID: 10.1038/s41587-020-0739-133288904)
Van den Berge, K. et al. Trajectory-based differential expression analysis for single-cell sequencing data. Nat. Commun. 11, 1201 (2020). (PMID: 10.1038/s41467-020-14766-3321396717058077)
Breiman, L. Random forests. Mach. Learn. 45, 5–32 (2001). (PMID: 10.1023/A:1010933404324)
Pedregosa, F. et al. Scikit-learn: machine learning in python. J. Mach. Learn. Res. 12, 2825–2830 (2011).
Meyer, R. C., Giddens, M. M., Coleman, B. M. & Hall, R. A. The protective role of prosaposin and its receptors in the nervous system. Brain Res. 1585, 1–12 (2014). (PMID: 10.1016/j.brainres.2014.08.022251306614529117)
Yaguchi, Y. et al. Fibroblast growth factor (FGF) gene expression in the developing cerebellum suggests multiple roles for FGF signaling during cerebellar morphogenesis and development. Dev. Dyn. 238, 2058–2072 (2009). (PMID: 10.1002/dvdy.2201319544582)
Lécuyer, E. et al. Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131, 174–187 (2007). (PMID: 10.1016/j.cell.2007.08.00317923096)
Tomancak, P. et al. Global analysis of patterns of gene expression during Drosophila embryogenesis. Genome Biol. 8, R145 (2007). (PMID: 10.1186/gb-2007-8-7-r145176458042323238)
Karaiskos, N. et al. The Drosophila embryo at single-cell transcriptome resolution. Science 358, 194–199 (2017). (PMID: 10.1126/science.aan323528860209)
Baruzzo, G., Cesaro, G. & Di Camillo, B. Identify, quantify and characterize cellular communication from single-cell RNA sequencing data with scSeqComm. Bioinformatics https://doi.org/10.1093/bioinformatics/btac036 (2022). (PMID: 10.1093/bioinformatics/btac036351308338822630)
Lander, A. D., Nie, Q. & Wan, F. Y. M. Do morphogen gradients arise by diffusion? Dev. Cell 2, 785–796 (2002). (PMID: 10.1016/S1534-5807(02)00179-X12062090)
Li, Z., Wang, T., Liu, P. & Huang, Y. SpatialDM: Rapid identification of spatially co-expressed ligand-receptor reveals cell–cell communication patterns. Preprint at https://doi.org/10.1101/2022.08.19.504616 (2022).
Shao, X. et al. Knowledge-graph-based cell–cell communication inference for spatially resolved transcriptomic data with SpaTalk. Nat. Commun. 13, 4429 (2022). (PMID: 10.1038/s41467-022-32111-8359080209338929)
Cheng, J., Yan, L., Nie, Q. & Sun, X. Modeling spatial intercellular communication and multilayer signaling regulations using stMLnet. Preprint at https://doi.org/10.1101/2022.06.27.497696 (2022).
Li, H., Ma, T., Hao, M., Wei, L. & Zhang, X. Decoding functional cell–cell communication events by multi-view graph learning on spatial transcriptomics. Preprint at https://doi.org/10.1101/2022.06.22.496105 (2022).
Li, R. & Yang, X. De novo reconstruction of cell interaction landscapes from single-cell spatial transcriptome data with DeepLinc. Genome Biol. 23, 124 (2022). (PMID: 10.1186/s13059-022-02692-0356597229164488)
Longo, S. K., Guo, M. G., Ji, A. L. & Khavari, P. A. Integrating single-cell and spatial transcriptomics to elucidate intercellular tissue dynamics. Nat. Rev. Genet. 22, 627–644 (2021). (PMID: 10.1038/s41576-021-00370-8341454359888017)
Pass, B. Multi-marginal optimal transport: theory and applications. ESAIM Math. Model. Numer. Anal. 49, 1771–1790 (2015). (PMID: 10.1051/m2an/2015020)
Cuturi, M. Sinkhorn distances: lightspeed computation of optimal transportation distances. Adv. Neural Inf. Processing Syst. 26, 2292–2300 (2013).
Moffitt, J. R. et al. Data from: Molecular, spatial and functional single-cell profiling of the hypothalamic preoptic region. Dryad, Dataset, https://doi.org/10.5061/dryad.8t8s248 (2018).
Cang, Z. et al. COMMOT: Screening cell–cell communication in spatial transcriptomics via collective optimal transport (0.0.2). Zenodo https://doi.org/10.5281/zenodo.7272562 (2022).
معلومات مُعتمدة: R01 AR079150 United States AR NIAMS NIH HHS; R01 DE030565 United States DE NIDCR NIH HHS; T32 AR080622 United States AR NIAMS NIH HHS; U01 AR073159 United States AR NIAMS NIH HHS; P30 AR075047 United States AR NIAMS NIH HHS
سلسلة جزيئية: Dryad 10.5061/dryad.8t8s248
تواريخ الأحداث: Date Created: 20230123 Date Completed: 20230213 Latest Revision: 20231012
رمز التحديث: 20231215
مُعرف محوري في PubMed: PMC9911355
DOI: 10.1038/s41592-022-01728-4
PMID: 36690742
قاعدة البيانات: MEDLINE
الوصف
تدمد:1548-7105
DOI:10.1038/s41592-022-01728-4