Single-cell protein activity analysis identifies recurrence-associated renal tumor macrophages

Cell. 2021 May 27;184(11):2988-3005.e16. doi: 10.1016/j.cell.2021.04.038. Epub 2021 May 20.

Abstract

Clear cell renal carcinoma (ccRCC) is a heterogeneous disease with a variable post-surgical course. To assemble a comprehensive ccRCC tumor microenvironment (TME) atlas, we performed single-cell RNA sequencing (scRNA-seq) of hematopoietic and non-hematopoietic subpopulations from tumor and tumor-adjacent tissue of treatment-naive ccRCC resections. We leveraged the VIPER algorithm to quantitate single-cell protein activity and validated this approach by comparison to flow cytometry. The analysis identified key TME subpopulations, as well as their master regulators and candidate cell-cell interactions, revealing clinically relevant populations, undetectable by gene-expression analysis. Specifically, we uncovered a tumor-specific macrophage subpopulation characterized by upregulation of TREM2/APOE/C1Q, validated by spatially resolved, quantitative multispectral immunofluorescence. In a large clinical validation cohort, these markers were significantly enriched in tumors from patients who recurred following surgery. The study thus identifies TREM2/APOE/C1Q-positive macrophage infiltration as a potential prognostic biomarker for ccRCC recurrence, as well as a candidate therapeutic target.

Keywords: CD8 T cell; Treg; clear cell renal carcinoma; clustering; gene regulatory networks; immunotherapy; post-surgical recurrence; protein activity inference; single-cell RNA sequencing; tumor microenvironment; tumor-infiltrating macrophage.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adult
  • Apolipoproteins E / genetics
  • Apolipoproteins E / metabolism
  • Biomarkers, Tumor / genetics
  • Carcinoma, Renal Cell / genetics
  • Carcinoma, Renal Cell / metabolism*
  • Carcinoma, Renal Cell / pathology
  • Cohort Studies
  • Female
  • Gene Expression / genetics
  • Gene Expression Regulation, Neoplastic / genetics
  • Humans
  • Kidney / metabolism
  • Kidney Neoplasms / pathology
  • Lymphocytes, Tumor-Infiltrating / pathology
  • Macrophages / metabolism
  • Male
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism
  • Middle Aged
  • Neoplasm Recurrence, Local / genetics*
  • Neoplasm Recurrence, Local / metabolism
  • Prognosis
  • Receptors, Complement / genetics
  • Receptors, Complement / metabolism
  • Receptors, Immunologic / genetics
  • Receptors, Immunologic / metabolism
  • Sequence Analysis, RNA / methods
  • Single-Cell Analysis / methods
  • Tumor Microenvironment
  • Tumor-Associated Macrophages / metabolism*
  • Tumor-Associated Macrophages / physiology

Substances

  • ApoE protein, human
  • Apolipoproteins E
  • Biomarkers, Tumor
  • Membrane Glycoproteins
  • Receptors, Complement
  • Receptors, Immunologic
  • TREM2 protein, human
  • complement 1q receptor