Spatial interactions modulate tumor growth and immune infiltration

NPJ Syst Biol Appl. 2024 Sep 30;10(1):106. doi: 10.1038/s41540-024-00438-1.

Abstract

Direct observation of tumor-immune interactions is unlikely in tumors with currently available technology, but computational simulations based on clinical data can provide insight to test hypotheses. It is hypothesized that patterns of collagen evolve as a mechanism of immune escape, but the exact nature of immune-collagen interactions is poorly understood. Spatial data quantifying collagen fiber alignment in squamous cell carcinomas indicates that late-stage disease is associated with highly aligned fibers. Our computational modeling framework discriminates between two hypotheses: immune cell migration that moves (1) parallel or (2) perpendicular to collagen fiber orientation. The modeling recapitulates immune-extracellular matrix interactions where collagen patterns provide immune protection, leading to an emergent inverse relationship between disease stage and immune coverage. Here, computational modeling provides important mechanistic insights by defining a kernel cell-cell interaction function that considers a spectrum of local (cell-scale) to global (tumor-scale) spatial interactions. Short-range interaction kernels provide a mechanism for tumor cell survival under conditions with strong Allee effects, while asymmetric tumor-immune interaction kernels lead to poor immune response. Thus, the length scale of tumor-immune interaction kernels drives tumor growth and infiltration.

MeSH terms

  • Carcinoma, Squamous Cell / immunology
  • Carcinoma, Squamous Cell / pathology
  • Cell Communication / immunology
  • Cell Movement / immunology
  • Collagen
  • Computer Simulation*
  • Extracellular Matrix / immunology
  • Extracellular Matrix / metabolism
  • Humans
  • Models, Biological
  • Neoplasms / immunology
  • Neoplasms / pathology
  • Tumor Microenvironment / immunology

Substances

  • Collagen