Comparative transcriptomics coupled to developmental grading via transgenic zebrafish reporter strains identifies conserved features in neutrophil maturation

Stefanie Kirchberger (), Mohamed R. Shoeb, Daria Lazic, Andrea Wenninger-Weinzierl, Kristin Fischer, Lisa E. Shaw, Filomena Nogueira, Fikret Rifatbegovic, Eva Bozsaky, Ruth Ladenstein, Bernd Bodenmiller, Thomas Lion, David Traver, Matthias Farlik, Christian Schöfer, Sabine Taschner-Mandl, Florian Halbritter () and Martin Distel ()
Additional contact information
Stefanie Kirchberger: St. Anna Children’s Cancer Research Institute (CCRI)
Mohamed R. Shoeb: St. Anna Children’s Cancer Research Institute (CCRI)
Daria Lazic: St. Anna Children’s Cancer Research Institute (CCRI)
Andrea Wenninger-Weinzierl: St. Anna Children’s Cancer Research Institute (CCRI)
Kristin Fischer: St. Anna Children’s Cancer Research Institute (CCRI)
Lisa E. Shaw: Medical University of Vienna, Department of Dermatology
Filomena Nogueira: St. Anna Children’s Cancer Research Institute (CCRI)
Fikret Rifatbegovic: St. Anna Children’s Cancer Research Institute (CCRI)
Eva Bozsaky: St. Anna Children’s Cancer Research Institute (CCRI)
Ruth Ladenstein: St. Anna Children’s Cancer Research Institute (CCRI)
Bernd Bodenmiller: University of Zurich
Thomas Lion: St. Anna Children’s Cancer Research Institute (CCRI)
David Traver: University of California
Matthias Farlik: Medical University of Vienna, Department of Dermatology
Christian Schöfer: Medical University of Vienna, Division of Cell and Developmental Biology, Center for Anatomy and Cell Biology
Sabine Taschner-Mandl: St. Anna Children’s Cancer Research Institute (CCRI)
Florian Halbritter: St. Anna Children’s Cancer Research Institute (CCRI)
Martin Distel: St. Anna Children’s Cancer Research Institute (CCRI)

Nature Communications, 2024, vol. 15, issue 1, 1-18

Abstract: Abstract Neutrophils are evolutionarily conserved innate immune cells playing pivotal roles in host defense. Zebrafish models have contributed substantially to our understanding of neutrophil functions but similarities to human neutrophil maturation have not been systematically characterized, which limits their applicability to studying human disease. Here we show, by generating and analysing transgenic zebrafish strains representing distinct neutrophil differentiation stages, a high-resolution transcriptional profile of neutrophil maturation. We link gene expression at each stage to characteristic transcription factors, including C/ebp-β, which is important for late neutrophil maturation. Cross-species comparison of zebrafish, mouse, and human samples confirms high molecular similarity of immature stages and discriminates zebrafish-specific from pan-species gene signatures. Applying the pan-species neutrophil maturation signature to RNA-sequencing data from human neuroblastoma patients reveals association between metastatic tumor cell infiltration in the bone marrow and an overall increase in mature neutrophils. Our detailed neutrophil maturation atlas thus provides a valuable resource for studying neutrophil function at different stages across species in health and disease.

Date: 2024
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DOI: 10.1038/s41467-024-45802-1

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