Fn-Dps, a novel virulence factor of Fusobacterium nucleatum, disrupts erythrocytes and promotes metastasis in colorectal cancer

PLoS Pathog. 2023 Jan 24;19(1):e1011096. doi: 10.1371/journal.ppat.1011096. eCollection 2023 Jan.

Abstract

Fusobacterium nucleatum (Fn) is a critical colorectal cancer (CRC)-associated bacterium. DNA hunger/stationary phase protective proteins (Dps) are bacterial ferritins that protect DNA from oxidative stress. However, little is known about the regulatory roles of Fn-Dps towards host cellular functions. Here, we identified Fn-Dps from the culture supernatant of Fn by mass spectrometry, and prepared the recombinant of Fn-Dps protein. We show a novel virulence protein of Fn, Fn-Dps, which lyses and disrupts erythrocytes by the competition for iron acquisition. Also, Fn-Dps facilitates intracellular survival of Fn in macrophages by upregulating the expression of the chemokine CCL2/CCL7. In addition, Fn-Dps can elicit a strong humoral immune response, and mucosal immunization with Fn-Dps conferred protection against Fn in the intestinal tract. Moreover, a high level of anti-Fn-Dps antibody was prevalent in populations, and elevated anti-Fn-Dps antibody levels were observed in CRC patients. Furthermore, Fn-Dps promotes the migration of CRC cells via the CCL2/CCL7-induced epithelial-mesenchymal transition (EMT) and promotes CRC metastasis in vivo.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Colorectal Neoplasms*
  • Erythrocytes / metabolism
  • Fusobacterium nucleatum* / genetics
  • Humans
  • Intestines / pathology
  • Virulence Factors / genetics

Substances

  • Virulence Factors

Grants and funding

This work was supported by the National Natural Science Foundation of China [Grant number: 81972289 (GZ)], the Natural Science Foundation of Guangdong Province [Grant number: 2019A1515010500 (GZ)], and the China Postdoctoral Science Foundation [Grant number: 2022M713596 (SG)]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.