Slide-tags enables single-nucleus barcoding for multimodal spatial genomics

Nature. 2024 Jan;625(7993):101-109. doi: 10.1038/s41586-023-06837-4. Epub 2023 Dec 13.

Abstract

Recent technological innovations have enabled the high-throughput quantification of gene expression and epigenetic regulation within individual cells, transforming our understanding of how complex tissues are constructed1-6. However, missing from these measurements is the ability to routinely and easily spatially localize these profiled cells. We developed a strategy, Slide-tags, in which single nuclei within an intact tissue section are tagged with spatial barcode oligonucleotides derived from DNA-barcoded beads with known positions. These tagged nuclei can then be used as an input into a wide variety of single-nucleus profiling assays. Application of Slide-tags to the mouse hippocampus positioned nuclei at less than 10 μm spatial resolution and delivered whole-transcriptome data that are indistinguishable in quality from ordinary single-nucleus RNA-sequencing data. To demonstrate that Slide-tags can be applied to a wide variety of human tissues, we performed the assay on brain, tonsil and melanoma. We revealed cell-type-specific spatially varying gene expression across cortical layers and spatially contextualized receptor-ligand interactions driving B cell maturation in lymphoid tissue. A major benefit of Slide-tags is that it is easily adaptable to almost any single-cell measurement technology. As a proof of principle, we performed multiomic measurements of open chromatin, RNA and T cell receptor (TCR) sequences in the same cells from metastatic melanoma, identifying transcription factor motifs driving cancer cell state transitions in spatially distinct microenvironments. Slide-tags offers a universal platform for importing the compendium of established single-cell measurements into the spatial genomics repertoire.

MeSH terms

  • Animals
  • Brain / cytology
  • Brain / metabolism
  • Chromatin / genetics
  • Chromatin / metabolism
  • DNA Barcoding, Taxonomic* / methods
  • Epigenesis, Genetic
  • Gene Expression Profiling
  • Genomics* / methods
  • Hippocampus / cytology
  • Hippocampus / metabolism
  • Humans
  • Ligands
  • Melanoma / genetics
  • Melanoma / pathology
  • Mice
  • Organ Specificity
  • Palatine Tonsil / cytology
  • Palatine Tonsil / metabolism
  • RNA / genetics
  • Receptors, Antigen, T-Cell / genetics
  • Response Elements / genetics
  • Single-Cell Analysis / methods
  • Single-Cell Gene Expression Analysis
  • Transcription Factors / metabolism
  • Transcriptome / genetics
  • Tumor Microenvironment

Substances

  • Chromatin
  • Receptors, Antigen, T-Cell
  • RNA
  • Ligands
  • Transcription Factors