Spatiotemporal immune zonation of the human kidney

Benjamin J. Stewart, John R. Ferdinand, Matthew D. Young, Thomas J. Mitchell, Kevin W. Loudon, Alexandra M. Riding, Nathan Richoz, Gordon L. Frazer, Joy U. L. Staniforth, Felipe A. Vieira Braga, Rachel A. Botting, Dorin-Mirel Popescu, Roser Vento-Tormo, Emily Stephenson, Alex Cagan, Sarah J. Farndon, Krzysztof Polanski, Mirjana Efremova, Kile Green, Martin Del Castillo Velasco-Herrera, Charlotte Guzzo, Grace Collord, Lira Mamanova, Tevita Aho, James N. Armitage, Antony C. P. Riddick, Imran Mushtaq, Stephen Farrell, Dyanne Rampling, James Nicholson, Andrew Filby, Johanna Burge, Steven Lisgo, Susan Lindsay, Marc Bajenoff, Anne Y. Warren, Grant D. Stewart, Neil Sebire, Nicholas Coleman, Muzlifah Haniffa, Sarah A. Teichmann, Sam Behjati, Menna R. Clatworthy

Abstract

Tissue-resident immune cells are important for organ homeostasis and defense. The epithelium may contribute to these functions directly or by cross-talk with immune cells. We used single-cell RNA sequencing to resolve the spatiotemporal immune topology of the human kidney. We reveal anatomically defined expression patterns of immune genes within the epithelial compartment, with antimicrobial peptide transcripts evident in pelvic epithelium in the mature, but not fetal, kidney. A network of tissue-resident myeloid and lymphoid immune cells was evident in both fetal and mature kidney, with postnatal acquisition of transcriptional programs that promote infection-defense capabilities. Epithelial-immune cross-talk orchestrated localization of antibacterial macrophages and neutrophils to the regions of the kidney most susceptible to infection. Overall, our study provides a global overview of how the immune landscape of the human kidney is zonated to counter the dominant immunological challenge.

Datasets

1. Mature kidney dataset: full
Metadata
donor_id
donor_age
self_reported_ethnicity_ontology_term_id
organism_ontology_term_id
sample_uuid
tissue_ontology_term_id
development_stage_ontology_term_id
suspension_uuid
suspension_type
library_uuid
assay_ontology_term_id
mapped_reference_annotation
cell_type_ontology_term_id
author_cell_type
cell_state
disease_ontology_term_id
reported_diseases
sex_ontology_term_id
Short_Sample
Project
Experiment
compartment
broad_celltype
tissue_type
cell_type
assay
disease
organism
sex
tissue
self_reported_ethnicity
development_stage
TTx15065 cells
TxK45793 cells
RCC13546 cells
RCC23269 cells
VHL3231 cells
Wilms32325 cells
RCC32277 cells
Wilms11948 cells
TxK11678 cells
Wilms2586 cells
TxK3324 cells
TxK2164 cells
pRCC62 cells
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Spatiotemporal immune zonation of the human kidney
2. Fetal kidney dataset: full
Metadata
donor_id
self_reported_ethnicity_ontology_term_id
organism_ontology_term_id
sample_uuid
tissue_ontology_term_id
development_stage_ontology_term_id
suspension_depletion_factors
suspension_enriched_cell_types
suspension_enrichment_factors
suspension_uuid
suspension_type
library_uuid
assay_ontology_term_id
mapped_reference_annotation
cell_type_ontology_term_id
author_cell_type
cell_state
disease_ontology_term_id
sex_ontology_term_id
Short_Sample
Experiment
Selection
compartment
tissue_type
cell_type
assay
disease
organism
sex
tissue
self_reported_ethnicity
development_stage
F356050 cells
F385998 cells
F415618 cells
F454709 cells
F173280 cells
F161542 cells
Preview
Spatiotemporal immune zonation of the human kidney

Analyze this study

Dataset 1
Dataset 2
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Source data

https://cellxgene.cziscience.com/collections/120e86b4-1195-48c5-845b-b98054105eec

Alias names

PMID31604275, PMC7343525

Cite this study

Stewart, B.J., Ferdinand, J.R., Young, M.D., Mitchell, T.J., Loudon, K.W., Riding, A.M., Richoz, N., Frazer, G.L., Staniforth, J.U., Vieira Braga, F.A. and Botting, R.A., 2019. Spatiotemporal immune zonation of the human kidney. Science, 365(6460), pp.1461-1466. https://doi.org/10.1126/science.aat5031