Neuropilin-2 contributes to tumor progression in preclinical models of small intestinal neuroendocrine tumors

J Pathol. 2019 Nov;249(3):343-355. doi: 10.1002/path.5321. Epub 2019 Sep 3.

Abstract

The identification of novel regulators of tumor progression is a key challenge to gain knowledge on the biology of small intestinal neuroendocrine tumors (SI-NETs). We recently identified the loss of the axon guidance protein semaphorin 3F as a protumoral event in SI-NETs. Interestingly the expression of its receptor neuropilin-2 (NRP-2) was still maintained. This study aimed at deciphering the potential role of NRP-2 as a contributor to SI-NET progression. The role of NRP-2 in SI-NET progression was addressed using an approach integrating human tissue and serum samples, cell lines and in vivo models. Data obtained from human SI-NET tissues showed that membranous NRP-2 expression is present in a majority of tumors, and is correlated with invasion, metastatic abilities, and neovascularization. In addition, NRP-2 soluble isoform was found elevated in serum samples from metastatic patients. In preclinical mouse models of NET progression, NRP-2 silencing led to a sustained antitumor effect, partly driven by the downregulation of VEGFR2. In contrast, its ectopic expression conferred a gain of aggressiveness, driven by the activation of various oncogenic signaling pathways. Lastly, NRP-2 inhibition led to a decrease of tumor cell viability, and sensitized to therapeutic agents. Overall, our results point out NRP-2 as a potential therapeutic target for SI-NETs, and will foster the development of innovative strategies targeting this receptor. © 2019 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.

Keywords: invasion; neuropilin-2; small intestinal neuroendocrine tumors; tumor progression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Animals
  • Antineoplastic Agents / pharmacology
  • Apoptosis
  • Carcinoma, Neuroendocrine / drug therapy
  • Carcinoma, Neuroendocrine / genetics
  • Carcinoma, Neuroendocrine / metabolism*
  • Carcinoma, Neuroendocrine / secondary
  • Cell Line, Tumor
  • Cell Movement
  • Everolimus / pharmacology
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Intestinal Neoplasms / drug therapy
  • Intestinal Neoplasms / genetics
  • Intestinal Neoplasms / metabolism*
  • Intestinal Neoplasms / pathology
  • Intestine, Small / metabolism*
  • Intestine, Small / pathology
  • Male
  • Mice, Nude
  • Neoplasm Invasiveness
  • Neovascularization, Pathologic
  • Neuropilin-2 / blood
  • Neuropilin-2 / genetics
  • Neuropilin-2 / metabolism*
  • Protein Kinase Inhibitors / pharmacology
  • Signal Transduction
  • TOR Serine-Threonine Kinases / antagonists & inhibitors
  • TOR Serine-Threonine Kinases / metabolism
  • Vascular Endothelial Growth Factor Receptor-2 / genetics
  • Vascular Endothelial Growth Factor Receptor-2 / metabolism

Substances

  • Antineoplastic Agents
  • Neuropilin-2
  • Protein Kinase Inhibitors
  • neuropilin-2, human
  • Everolimus
  • MTOR protein, human
  • KDR protein, human
  • Vascular Endothelial Growth Factor Receptor-2
  • TOR Serine-Threonine Kinases