Neuroplastin-β mediates S100A8/A9-induced lung cancer disseminative progression

Mol Carcinog. 2019 Jun;58(6):980-995. doi: 10.1002/mc.22987. Epub 2019 Feb 27.

Abstract

Compiling evidence indicates an unusual role of extracellular S100A8/A9 in cancer metastasis. S100A8/A9 secreted from either cancer cells or normal cells including epithelial and inflammatory cells stimulates cancer cells through S100A8/A9 sensor receptors in an autocrine or paracrine manner, leading to cancer cell metastatic progression. We previously reported a novel S100A8/A9 receptor, neuroplastin-β (NPTNβ), which plays a critical role in atopic dermatitis when it is highly activated in keratinocytes by an excess amount of extracellular S100A8/A9 in the inflammatory skin lesion. Interestingly, our expression profiling of NPTNβ showed significantly high expression levels in lung cancer cell lines in a consistent manner. We hence aimed to determine the significance of NPTNβ as an S100A8/A9 receptor in lung cancer. Our results showed that NPTNβ has strong ability to induce cancer-related cellular events, including anchorage-independent growth, motility and invasiveness, in lung cancer cells in response to extracellular S100A8/A9, eventually leading to the expression of a cancer disseminative phenotype in lung tissue in vivo. Mechanistic investigation revealed that binding of S100A8/A9 to NPTNβ mediates activation of NFIA and NFIB and following SPDEF transcription factors through orchestrated upstream signals from TRAF2 and RAS, which is linked to anchorage-independent growth, motility and invasiveness. Overall, our results indicate the importance of the S100A8/A9-NPTNβ axis in lung cancer disseminative progression and reveal a pivotal role of its newly identified downstream signaling, TRAF2/RAS-NFIA/NFIB-SPDEF, in linking to the aggressive development of lung cancers.

Keywords: NFI; NPTNβ; S100 protein; S100A8/A9; SPDEF; lung cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • A549 Cells
  • Animals
  • Calgranulin A / metabolism*
  • Calgranulin B / metabolism*
  • Cell Line, Tumor
  • Cell Movement
  • Disease Progression
  • Female
  • Gene Expression Regulation, Neoplastic
  • HEK293 Cells
  • Humans
  • Lung Neoplasms / metabolism
  • Lung Neoplasms / pathology*
  • Membrane Glycoproteins / metabolism*
  • Mice
  • NFI Transcription Factors / metabolism
  • Protein Isoforms / metabolism
  • Proto-Oncogene Proteins c-ets / metabolism
  • Signal Transduction
  • Up-Regulation*

Substances

  • Calgranulin A
  • Calgranulin B
  • Membrane Glycoproteins
  • NFI Transcription Factors
  • NFIA protein, human
  • NFIB protein, human
  • NPTN protein, human
  • Protein Isoforms
  • Proto-Oncogene Proteins c-ets
  • S100A8 protein, human
  • S100A9 protein, human
  • SPDEF protein, human