Emergence of division of labor in tissues through cell interactions and spatial cues

Miri Adler; Noa Moriel; Aleksandrina Goeva; Inbal Avraham-Davidi; Simon Mages; Taylor S. Adams; Naftali Kaminski; Evan Z. Macosko; Aviv Regev; Ruslan Medzhitov; Mor Nitzan

Cell Reports (May 2023)

Emergence of division of labor in tissues through cell interactions and spatial cues

Miri Adler,
Noa Moriel,
Aleksandrina Goeva,
Inbal Avraham-Davidi,
Simon Mages,
Taylor S. Adams,
Naftali Kaminski,
Evan Z. Macosko,
Aviv Regev,
Ruslan Medzhitov,
Mor Nitzan

Affiliations

Miri Adler: Broad Institute of Massachusetts Institute of Technology and Harvard, Cambridge, MA, USA; Tananbaum Center for Theoretical and Analytical Human Biology, Yale University School of Medicine, New Haven, CT, USA
Noa Moriel: School of Computer Science and Engineering, The Hebrew University of Jerusalem, Jerusalem, Israel
Aleksandrina Goeva: Broad Institute of Massachusetts Institute of Technology and Harvard, Cambridge, MA, USA
Inbal Avraham-Davidi: Broad Institute of Massachusetts Institute of Technology and Harvard, Cambridge, MA, USA
Simon Mages: Broad Institute of Massachusetts Institute of Technology and Harvard, Cambridge, MA, USA; Gene Center and Department of Biochemistry, Ludwig-Maximilians-University Munich, Munich, Germany
Taylor S. Adams: Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, CT, USA
Naftali Kaminski: Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, CT, USA
Evan Z. Macosko: Broad Institute of Massachusetts Institute of Technology and Harvard, Cambridge, MA, USA; Massachusetts General Hospital, Department of Psychiatry, Boston, MA, USA
Aviv Regev: Broad Institute of Massachusetts Institute of Technology and Harvard, Cambridge, MA, USA; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA; Corresponding author
Ruslan Medzhitov: Tananbaum Center for Theoretical and Analytical Human Biology, Yale University School of Medicine, New Haven, CT, USA; Howard Hughes Medical Institute, Department of Immunobiology, Yale University School of Medicine, New Haven, CT, USA; Corresponding author
Mor Nitzan: School of Computer Science and Engineering, The Hebrew University of Jerusalem, Jerusalem, Israel; Racah Institute of Physics, The Hebrew University of Jerusalem, Jerusalem, Israel; Faculty of Medicine, The Hebrew University of Jerusalem, Jerusalem, Israel; Corresponding author

Journal volume & issue: Vol. 42, no. 5
p. 112412

Abstract

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Summary: Most cell types in multicellular organisms can perform multiple functions. However, not all functions can be optimally performed simultaneously by the same cells. Functions incompatible at the level of individual cells can be performed at the cell population level, where cells divide labor and specialize in different functions. Division of labor can arise due to instruction by tissue environment or through self-organization. Here, we develop a computational framework to investigate the contribution of these mechanisms to division of labor within a cell-type population. By optimizing collective cellular task performance under trade-offs, we find that distinguishable expression patterns can emerge from cell-cell interactions versus instructive signals. We propose a method to construct ligand-receptor networks between specialist cells and use it to infer division-of-labor mechanisms from single-cell RNA sequencing (RNA-seq) and spatial transcriptomics data of stromal, epithelial, and immune cells. Our framework can be used to characterize the complexity of cell interactions within tissues.

CP: Developmental biology

Published in Cell Reports

ISSN: 2211-1247 (Online)
Publisher: Elsevier
Country of publisher: Netherlands
LCC subjects: Science: Biology (General)
Website: http://www.cell.com/cell-reports/home

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