GM-CSF Production by Tumor Cells Is Associated with Improved Survival in Colorectal Cancer

Clin Cancer Res. 2014 Jun 15;20(12):3094-106. doi: 10.1158/1078-0432.CCR-13-2774. Epub 2014 Apr 15.

Abstract

Purpose: Colorectal cancer infiltration by CD16(+) myeloid cells correlates with improved prognosis. We addressed mechanistic clues and gene and protein expression of cytokines potentially associated with macrophage polarization.

Experimental design: GM-CSF or M-CSF-stimulated peripheral blood CD14(+) cells from healthy donors were cocultured with colorectal cancer cells. Tumor cell proliferation was assessed by (3)H-thymidine incorporation. Expression of cytokine genes in colorectal cancer and autologous healthy mucosa was tested by quantitative, real-time PCR. A tumor microarray (TMA) including >1,200 colorectal cancer specimens was stained with GM-CSF- and M-CSF-specific antibodies. Clinicopathological features and overall survival were analyzed.

Results: GM-CSF induced CD16 expression in 66% ± 8% of monocytes, as compared with 28% ± 1% in cells stimulated by M-CSF (P = 0.011). GM-CSF but not M-CSF-stimulated macrophages significantly (P < 0.02) inhibited colorectal cancer cell proliferation. GM-CSF gene was expressed to significantly (n = 45, P < 0.0001) higher extents in colorectal cancer than in healthy mucosa, whereas M-CSF gene expression was similar in healthy mucosa and colorectal cancer. Accordingly, IL1β and IL23 genes, typically expressed by M1 macrophages, were expressed to significantly (P < 0.001) higher extents in colorectal cancer than in healthy mucosa. TMA staining revealed that GM-CSF production by tumor cells is associated with lower T stage (P = 0.02), "pushing" growth pattern (P = 0.004) and significantly (P = 0.0002) longer survival in mismatch-repair proficient colorectal cancer. Favorable prognostic effect of GM-CSF production by colorectal cancer cells was confirmed by multivariate analysis and was independent from CD16(+) and CD8(+) cell colorectal cancer infiltration. M-CSF expression had no significant prognostic relevance.

Conclusions: GM-CSF production by tumor cells is an independent favorable prognostic factor in colorectal cancer.

Publication types

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

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Biomarkers, Tumor / genetics
  • Biomarkers, Tumor / metabolism*
  • Case-Control Studies
  • Cell Proliferation
  • Chemokines / genetics
  • Chemokines / metabolism
  • Colorectal Neoplasms / metabolism
  • Colorectal Neoplasms / mortality*
  • Colorectal Neoplasms / pathology
  • Cytokines / genetics
  • Cytokines / metabolism
  • Female
  • Follow-Up Studies
  • Gene Expression Profiling
  • Granulocyte-Macrophage Colony-Stimulating Factor / metabolism*
  • Humans
  • Immunocompetence
  • Immunoenzyme Techniques
  • Macrophage Colony-Stimulating Factor / metabolism
  • Macrophages / metabolism
  • Macrophages / pathology*
  • Male
  • Middle Aged
  • Monocytes / metabolism
  • Monocytes / pathology*
  • Neoplasm Grading
  • Neoplasm Invasiveness
  • Neoplasm Staging
  • Prognosis
  • Real-Time Polymerase Chain Reaction
  • Survival Rate
  • Tissue Array Analysis

Substances

  • Biomarkers, Tumor
  • Chemokines
  • Cytokines
  • Macrophage Colony-Stimulating Factor
  • Granulocyte-Macrophage Colony-Stimulating Factor