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Tissue-resident memory CD8 T cell diversity is spatiotemporally imprinted.

Nature · 2025 · Vol. 639 (8054) · pp. 483-492

Abstract

Tissue-resident memory CD8 T (T<sub>RM</sub>) cells provide protection from infection at barrier sites. In the small intestine, T<sub>RM</sub> cells are found in at least two distinct subpopulations: one with higher expression of effector molecules and another with greater memory potential<sup>1</sup>. However, the origins of this diversity remain unknown. Here we proposed that distinct tissue niches drive the phenotypic heterogeneity of T<sub>RM</sub> cells. To test this, we leveraged spatial transcriptomics of human samples, a mouse model of acute systemic viral infection and a newly established strategy for pooled optically encoded gene perturbations to profile the locations, interactions and transcriptomes of pathogen-specific T<sub>RM</sub> cell differentiation at single-transcript resolution. We developed computational approaches to capture cellular locations along three anatomical axes of the small intestine and to visualize the spatiotemporal distribution of cell types and gene expression. Our study reveals that the regionalized signalling of the intestinal architecture supports two distinct T<sub>RM</sub> cell states: differentiated T<sub>RM</sub> cells and progenitor-like T<sub>RM</sub> cells, located in the upper villus and lower villus, respectively. This diversity is mediated by distinct ligand-receptor activities, cytokine gradients and specialized cellular contacts. Blocking TGFβ or CXCL9 and CXCL10 sensing by antigen-specific CD8 T cells revealed a model consistent with anatomically delineated, early fate specification. Ultimately, our framework for the study of tissue immune networks reveals that T cell location and functional state are fundamentally intertwined.

Publication Types

["Journal Article"]

Keywords

[]

MeSH Terms

["Animals", "CD8-Positive T-Lymphocytes", "Mice", "Immunologic Memory", "Humans", "Cell Differentiation", "Transforming Growth Factor beta", "Female", "Intestine, Small", "Male", "Mice, Inbred C57BL", "Chemokine CXCL10", "Transcriptome", "Memory T Cells"]

Funding

P30 DK120515 NIDDK NIH HHS (United States)
R01 AI150282 NIAID NIH HHS (United States)
P01 AI132122 NIAID NIH HHS (United States)
S10 OD025052 NIH HHS (United States)
F31 AI176705 NIAID NIH HHS (United States)
P30 NS047101 NINDS NIH HHS (United States)
I01 CX002396 CSRD VA (United States)
R01 AI072117 NIAID NIH HHS (United States)
R37 AI067545 NIAID NIH HHS (United States)
R01 AI179952 NIAID NIH HHS (United States)
R01 CA273432 NCI NIH HHS (United States)
K00 CA222711 NCI NIH HHS (United States)

Linked Datasets (3)

GSE279255 GSE via ncbi_elink
GEO

Tissue-resident memory CD8 T Cell Diversity is Spatiotemporally Imprinted

Mus musculus
2 data files
FileTypeSize
44_R_S2_L001_I1_001.fastq.gz OTHER 4.7 GB
44_R_S2_L002_I1_001.fastq.gz OTHER 4.7 GB
GSE280895 GSE via ncbi_elink
GEO

Tissue-resident memory CD8 T Cell Diversity is Spatiotemporally Imprinted

Mus musculus
GSE279254 GSE via ncbi_elink
GEO

Tissue-resident memory CD8 T Cell Diversity is Spatiotemporally Imprinted [snRNA-Seq]

Mus musculus
16 data files
FileTypeSize
JC_EL_10XNuclei_c_dist_M1_S12_L002_R1_001.fastq.gz RNA-Seq 19.8 GB
JC_EL_10XNuclei_c_dist_M1_S8_L002_R1_001.fastq.gz RNA-Seq 17.6 GB
JC_EL_10XNuclei_c_prox_M1_S11_L002_R1_001.fastq.gz RNA-Seq 19.6 GB
JC_EL_10XNuclei_c_prox_M1_S7_L002_R1_001.fastq.gz RNA-Seq 20.6 GB
JC_EL_10XNuclei_si_dist_M1_S5_L002_R1_001.fastq.gz RNA-Seq 25.3 GB
JC_EL_10XNuclei_si_dist_M1_S9_L002_R1_001.fastq.gz RNA-Seq 10.7 GB
JC_EL_10XNuclei_si_dist_M2_S10_L002_R1_001.fastq.gz RNA-Seq 17.3 GB
JC_EL_10XNuclei_si_dist_M2_S6_L002_R1_001.fastq.gz RNA-Seq 21.2 GB
JC_EL_10XNuclei_si_mid_M1_S3_L002_R1_001.fastq.gz RNA-Seq 20.3 GB
JC_EL_10XNuclei_si_mid_M1_S7_L002_R1_001.fastq.gz RNA-Seq 21.6 GB
JC_EL_10XNuclei_si_mid_M2_S4_L002_R1_001.fastq.gz RNA-Seq 29.3 GB
JC_EL_10XNuclei_si_mid_M2_S8_L002_R1_001.fastq.gz RNA-Seq 10.2 GB
JC_EL_10XNuclei_si_prox_M1_S1_L002_R1_001.fastq.gz RNA-Seq 21.1 GB
JC_EL_10XNuclei_si_prox_M1_S5_L002_R1_001.fastq.gz RNA-Seq 17.1 GB
JC_EL_10XNuclei_si_prox_M2_S2_L002_R1_001.fastq.gz RNA-Seq 20.4 GB
JC_EL_10XNuclei_si_prox_M2_S6_L002_R1_001.fastq.gz RNA-Seq 20.9 GB

Potentially Related Datasets (3)

These accessions were text-mined from the PMC full text. They may be referenced for comparison, cited from other studies, or otherwise mentioned without being primary data for this paper.

Tissue-resident memory CD8 T Cell Diversity is Spatiotemporally Imprinted

Tissue-resident memory CD8 T Cell Diversity is Spatiotemporally Imprinted [snRNA-Seq]

Tissue-resident memory CD8 T Cell Diversity is Spatiotemporally Imprinted

Analysis Pipelines (3)

snRNA-seq geo_data_processing GSE279254
Spatial transcriptomics geo_data_processing GSE279255
Spatial transcriptomics geo_data_processing GSE280895