Cisplatin resistant lung cancer cells promoted M2 polarization of tumor-associated macrophages via the Src/CD155/MIF functional pathway

J Exp Clin Cancer Res. 2019 Apr 29;38(1):180. doi: 10.1186/s13046-019-1166-3.

Abstract

Background: Lung cancer often ranks one of the most prevalent malignancies in the world. One of the most challenging aspects of treating late-stage lung cancer patients is the development of drug resistance, from both conventional chemo- and targeted therapeutic agents. Tumor-associated microphages (TAMs) have been shown to promote the survival and distant metastasis of lung cancer cells.

Methods: This study investigated the TAMs - modulating potential of cisplatin-resistant non-small cell lung cancer (NSCLC) cell lines, A549R and H460R by using bioinformatics approach, immunoblotting, immunofluorescence staining, migration, invasion, colony, lung sphere formation and xenograft tumorigenecity assays.

Results: In this study, we first demonstrated the elevated expression of oncogenic and stemenss markers such as Src, Notch1, macrophage inhibitory factor (MIF) and CD155 in trained cisplatin (CDDP)-resistant A549 and H460 cells (A549R and H460R cells). When co-cultured with TAMs, A549R and H460R cells promoted the M2-polarization in TAMs. In addition, A549R and H460R cells showed an increased self-renewal ability as they formed tumor spheres at higher frequency comparing to their parental counterparts. The increased MIF secretion by the A549R and H460R cells could be suppressed by a multiple kinase inhibitor, dasatinib, which resulted in the decreased of oncogenic network of Src, CD155 and MIF expression. Similarly, dasatinib treatment reduced the M2 polarization in TAMs and suppressed self-renewal ability of the A549R and H460R cells.

Conclusion: In summary, cisplatin resistant lung cancer cells not only showed an increased self-renewal ability but also promoted M2 polarization of TAMs via the secretion of MIF. These findings were linked to the increased Src-associated signaling as dasatinib treatment significantly reversed these phenomena. Thus, kinase inhibitors such as dasatinib may be of potential for treating cisplatin-resistant lung cancer by targeting both tumor and the tumor microenvironment.

Keywords: Cancer stemness; Cisplatin resistance; Lung cancer; M2 tumor-associated macrophages (M2-TAMs); Multiple kinase inhibitor; Src signaling.

MeSH terms

  • A549 Cells
  • Animals
  • Carcinogenesis / drug effects
  • Cisplatin / administration & dosage
  • Cisplatin / adverse effects
  • Dasatinib / administration & dosage
  • Drug Resistance, Neoplasm / genetics*
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Intramolecular Oxidoreductases / genetics*
  • Lung Neoplasms / drug therapy*
  • Lung Neoplasms / genetics
  • Lung Neoplasms / pathology
  • Macrophage Migration-Inhibitory Factors / genetics*
  • Mice
  • Receptors, Virus / genetics*
  • Signal Transduction / drug effects
  • Tumor Microenvironment / drug effects
  • Tumor Microenvironment / genetics
  • Xenograft Model Antitumor Assays
  • src-Family Kinases / genetics

Substances

  • Macrophage Migration-Inhibitory Factors
  • Receptors, Virus
  • poliovirus receptor
  • src-Family Kinases
  • Intramolecular Oxidoreductases
  • MIF protein, human
  • Cisplatin
  • Dasatinib