Collagen IV-conveyed signals can regulate chemokine production and promote liver metastasis

Oncogene. 2018 Jul;37(28):3790-3805. doi: 10.1038/s41388-018-0242-z. Epub 2018 Apr 13.

Abstract

Liver metastases remain a major cause of death from gastrointestinal tract cancers as well as from other malignancies such as breast and lung carcinomas and melanoma. Understanding the underlying biology is essential for the design of effective targeted therapies. We previously reported that collagen IV α1/α2 overexpression in non-metastatic lung carcinoma (M27colIV) cells increased their metastatic ability, specifically to the liver and documented high collagen IV levels in surgical resections of liver metastases from diverse tumor types. Here, we aimed to elucidate the functional relevance of collagen IV to metastatic outgrowth in the liver. Gene expression profiling revealed in M27colIVcells significant increases in the expression of chemokines CCL5 (5.7-fold) and CCL7 (2.6-fold) relative to wild-type cells, and this was validated by qPCR and western blotting. Similarly, in human colon carcinoma KM12C and KM12SM cells with divergent liver-colonizing potentials, CCL7 and CCL5 production correlated with type IV collagen expression and the metastatic phenotype. CCL7 silencing by short hairpin RNA (shRNA) reduced experimental liver metastasis in both cell types, whereas CCL5 silencing reduced metastasis of M27colIV cells, implicating these cytokines in metastatic expansion in the liver. Subsequent functional analyses implicated both MEK/ERK and PI3K signaling upstream of CCL7 upregulation and identified CCL7 (but not CCL5) as a critical migration/invasion factor, acting via the chemokine receptor CCR3. Chemokine CCL5 was identified as a regulator of the T-cell immune response in the liver. Loss of CCL7 in KM12SM cells was also associated with altered E-cadherin and reduced vimentin and Snail expression, implicating it in epithelial-to-mesenchymal transition in these cells. Moreover, in clinical specimens of colon cancer liver metastases analyzed by immunohistochemistry, CCL5 and CCL7 levels paralleled those of collagen IV. The results identify the chemokines CCL5 and CCL7 as type IV collagen-regulated genes that promote liver metastasis by distinct and complementary mechanisms.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cadherins / metabolism
  • Carcinoma, Lewis Lung
  • Cell Line, Tumor
  • Cell Movement / physiology
  • Chemokine CCL5 / metabolism*
  • Chemokine CCL7 / metabolism*
  • Collagen Type IV / metabolism*
  • Epithelial-Mesenchymal Transition / physiology
  • Female
  • Gene Expression Profiling / methods
  • Gene Expression Regulation, Neoplastic / physiology
  • Humans
  • Liver Neoplasms / metabolism*
  • Liver Neoplasms / pathology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Nude
  • Phosphatidylinositol 3-Kinases / metabolism
  • Signal Transduction / physiology
  • Snail Family Transcription Factors / metabolism
  • Up-Regulation / physiology
  • Vimentin / metabolism

Substances

  • Cadherins
  • Chemokine CCL5
  • Chemokine CCL7
  • Collagen Type IV
  • Snail Family Transcription Factors
  • Vimentin
  • Phosphatidylinositol 3-Kinases