Periostin directly and indirectly promotes tumor lymphangiogenesis of head and neck cancer

PLoS One. 2012;7(8):e44488. doi: 10.1371/journal.pone.0044488. Epub 2012 Aug 30.

Abstract

Background: Metastasis to regional lymph nodes via lymphatic vessels plays a key role in cancer progression. Tumor lymphangiogenesis is known to promote lymphatic metastasis, and vascular endothelial growth factor C (VEGF-C) is a critical activator of tumor lymphangiogenesis during the process of metastasis. We previously identified periostin as an invasion- and angiogenesis-promoting factor in head and neck squamous cell carcinoma (HNSCC). In this study, we discovered a novel role for periostin in tumor lymphangiogenesis.

Methods and findings: Periostin overexpression upregulated VEGF-C mRNA expression in HNSCC cells. By using conditioned media from periostin-overexpressing HNSCC cells, we examined tube formation of lymphatic endothelial cells. Conditioned media from periostin-overexpressing cells promoted tube formation. To know the correlation between periostin and VEGF-C, we compared Periostin expression with VEGF-C expression in 54 HNSCC cases by immunohistochemistry. Periostin expression was correlated well with VEGF-C expression in HNSCC cases. Moreover, correlation between periostin and VEGF-C secretion was observed in serum from HNSCC patients. Interestingly, periostin itself promoted tube formation of lymphatic endothelial cells independently of VEGF-C. Periostin-promoted lymphangiogenesis was mediated by Src and Akt activity. Indeed possible correlation between periostin and lymphatic status in periostin-overexpressing xenograft tumors and HNSCC cases was observed.

Conclusions: Our findings suggest that periostin itself as well as periostin-induced upregulation of VEGF-C may promote lymphangiogenesis. We suggest that periostin may be a marker for prediction of malignant behaviors in HNSCC and a potential target for future therapeutic intervention to obstruct tumoral lymphatic invasion and lymphangiogenesis in HNSCC patients.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Adhesion Molecules / genetics
  • Cell Adhesion Molecules / metabolism*
  • Cell Movement
  • Cell Proliferation
  • Endothelial Cells / pathology
  • Gene Expression Regulation, Neoplastic
  • Head and Neck Neoplasms / blood supply
  • Head and Neck Neoplasms / genetics
  • Head and Neck Neoplasms / metabolism*
  • Head and Neck Neoplasms / pathology
  • Humans
  • Lymphangiogenesis* / genetics
  • Models, Biological
  • Neovascularization, Pathologic

Substances

  • Cell Adhesion Molecules
  • POSTN protein, human

Grants and funding

This work was supported by Grants-in-Aid from the Ministry of Education, Science, and Culture of Japan (Y. Kudo and T. Takata), a Research Fellowship for Young Scientists and the Excellent Young Researchers Overseas Visit Program from the Japan Society for the Promotion of Science (S. Iizuka), and a Kurozumi Memorial Foundation grant (Y. Kudo). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.