Bidirectional activation of stem-like programs between metastatic cancer and alveolar type 2 cells within the niche

Dev Cell. 2024 Sep 23;59(18):2398-2413.e8. doi: 10.1016/j.devcel.2024.05.020. Epub 2024 Jun 11.

Abstract

A key step for metastatic outgrowth involves the generation of a deeply altered microenvironment (niche) that supports the malignant behavior of cancer cells. The complexity of the metastatic niche has posed a significant challenge in elucidating the underlying programs driving its origin. Here, by focusing on early stages of breast cancer metastasis to the lung in mice, we describe a cancer-dependent chromatin remodeling and activation of developmental programs in alveolar type 2 (AT2) cells within the niche. We show that metastatic cells can prime AT2 cells into a reprogrammed multilineage state. In turn, this cancer-induced reprogramming of AT2 cells promoted stem-like features in cancer cells and enhanced their initiation capacity. In conclusion, we propose the concept of "reflected stemness" as an early phenomenon during metastatic niche initiation, wherein metastatic cells reprogram the local tissue into a stem-like state that enhances intrinsic cancer-initiating potential, creating a positive feedback loop where tumorigenic programs are amplified.

Keywords: Metastasis; Sox9; alveolar type 2 cells; breast cancer; lung stem cells; metastasis-initiating cells; metastatic niche; multilineage state; tissue reprogramming.

MeSH terms

  • Alveolar Epithelial Cells / metabolism
  • Alveolar Epithelial Cells / pathology
  • Animals
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / pathology
  • Cell Line, Tumor
  • Cellular Reprogramming
  • Chromatin Assembly and Disassembly
  • Female
  • Humans
  • Lung Neoplasms* / metabolism
  • Lung Neoplasms* / pathology
  • Lung Neoplasms* / secondary
  • Mice
  • Neoplasm Metastasis / pathology
  • Neoplastic Stem Cells* / metabolism
  • Neoplastic Stem Cells* / pathology
  • Stem Cell Niche
  • Tumor Microenvironment*