Oct4 promotes M2 macrophage polarization through upregulation of macrophage colony-stimulating factor in lung cancer

J Hematol Oncol. 2020 Jun 1;13(1):62. doi: 10.1186/s13045-020-00887-1.

Abstract

Background: Expression of Oct4 maintains cancer stem cell (CSC)-like properties in lung cancer cells and is correlated with poor prognosis of lung adenocarcinoma. M2-type tumor-associated macrophages (TAMs) promote cancer cell migration and metastasis. Tumor microenvironments promote monocyte differentiation into M2 TAMs via a complex cytokine-based connection. We explored the role of Oct4 in cytokine secretion in lung cancer and its impact on M2 TAM polarization.

Methods: Monocytes co-cultured with the conditioned medium from Oct4-overexpressing lung cancer cells were used to investigate M2 TAM differentiation. The inflammatory factors in the conditioned medium of Oct4-overexpressing A549 cells were examined using human inflammation antibody arrays. The correlations of Oct4, macrophage colony-stimulating factor (M-CSF), and M2 TAMs were validated in lung cancer cells, syngeneic mouse lung tumor models, and clinical samples of non-small cell lung cancer (NSCLC).

Results: Oct4-overexpressing A549 cells expressed elevated levels of M-CSF, which contributed to increased M2 macrophages and enhanced tumor migration. Overexpression of Oct4 enhanced tumor growth and reduced the survival of lung tumor-bearing mice, which was correlated with increased number of M2 macrophages in lung cancer. Notably, NSCLC patients with high expression levels of Oct4, M-CSF, and M2 TAMs had the poorest recurrence-free survival. A positive correlation between Oct4, M-CSF, and M2 TAMs was observed in the tumor tissue of NSCLC patient. Treatment with all-trans retinoic acid exerted anti-tumor effects and reduced M2 TAMs in tumor-bearing mice.

Conclusions: Our results indicate that Oct4 expressed by lung cancer cells promotes M2 macrophage polarization through upregulation of M-CSF secretion, leading to cancer growth and metastasis. Our findings also implicate that the Oct4/M-CSF axis in M2 macrophage polarization may be potential therapeutic targets for lung cancer.

Keywords: Lung cancer; M-CSF; M2 macrophage; Oct4; Tumor-associated macrophage.

Publication types

  • Multicenter Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • A549 Cells
  • Adenocarcinoma / pathology
  • Animals
  • Antineoplastic Agents / pharmacology
  • Carcinoma, Non-Small-Cell Lung / mortality
  • Carcinoma, Non-Small-Cell Lung / pathology*
  • Cell Differentiation
  • Cohort Studies
  • Culture Media, Conditioned / pharmacology
  • Cytokines / physiology
  • Genes, Reporter
  • Humans
  • Lung Neoplasms / mortality
  • Lung Neoplasms / pathology*
  • Macrophage Colony-Stimulating Factor / biosynthesis*
  • Macrophage Colony-Stimulating Factor / genetics
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Monocytes / drug effects
  • Neoplasm Proteins / physiology*
  • Octamer Transcription Factor-3 / antagonists & inhibitors
  • Octamer Transcription Factor-3 / genetics
  • Octamer Transcription Factor-3 / pharmacology
  • Octamer Transcription Factor-3 / physiology*
  • Promoter Regions, Genetic
  • RNA Interference
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / pharmacology
  • Recombinant Proteins / pharmacology
  • THP-1 Cells
  • Tretinoin / pharmacology
  • Tumor Microenvironment
  • Tumor-Associated Macrophages / pathology*
  • Up-Regulation / drug effects

Substances

  • Antineoplastic Agents
  • Culture Media, Conditioned
  • Cytokines
  • Neoplasm Proteins
  • Octamer Transcription Factor-3
  • POU5F1 protein, human
  • Pou5f1 protein, mouse
  • RNA, Small Interfering
  • Recombinant Proteins
  • Tretinoin
  • Macrophage Colony-Stimulating Factor