Targeting the splicing isoforms of spleen tyrosine kinase affects the viability of colorectal cancer cells

PLoS One. 2022 Sep 14;17(9):e0274390. doi: 10.1371/journal.pone.0274390. eCollection 2022.

Abstract

Spleen tyrosine kinase (Syk) expression have been both positively and negatively associated with tumorigenesis. Our goal was to evaluate the contribution of Syk and its two splice variants, full length Syk (L) and short isoform Syk (S), in the tumor biology of colorectal cancer cells (CRC). The analysis of Syk expression in primary human colorectal tumors, as well as the analysis of TCGA database, revealed a high Syk mRNA expression score in colorectal cancer tumors, suggesting a tumor promotor role of Syk in CRC. Our analysis showed that Syk (L) isoform is highly expressed in the majority of the tumor tissues and that it remains expressed in tumors in which global Syk expression is downregulated, suggesting the dependence of tumors to Syk (L) isoform. We also identified a small cluster of tumor tissues, which express a high proportion of Syk (S) isoform. This specific cluster is associated with overexpressed genes related to translation and mitochondria, and down regulated genes implicated in the progression of mitosis. For our functional studies, we used short hairpin RNA tools to target the expression of Syk in CRC cells bearing the activating K-Ras (G13D) mutation. Our results showed that while global Syk knock down increases cell proliferation and cell motility, Syk (L) expression silencing affects the viability and induces the apoptosis of the cells, confirming the dependence of cells on Syk (L) isoform for their survival. Finally, we report the promising potential of compound C-13, an original non-enzymatic inhibitor of Syk isolated in our group. In vitro studies showed that C-13 exerts cytotoxic effects on Syk-positive CRC cells by inhibiting their proliferation and their motility, and by inducing their apoptosis, while Syk-negative cell lines viability was not affected. Moreover, the oral and intraperitoneal administration of C-13 reduced the tumor growth of CRC DLD-1 cells xenografts in Nude mice in vivo.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Colorectal Neoplasms* / genetics
  • Colorectal Neoplasms* / pathology
  • Humans
  • Mice
  • Mice, Nude
  • Protein Isoforms / genetics
  • Protein Isoforms / metabolism
  • RNA Splicing*
  • Syk Kinase / genetics
  • Syk Kinase / metabolism

Substances

  • Protein Isoforms
  • Syk Kinase

Grants and funding

This study was funded by the French National Research Agency under the program Investissements d'Avenir Grant Agreement LabEx MAbImprove (grant no. ANR‐10‐LABX‐53), and the SIte de Recherche Intégrée sur le Cancer (SIRIC) Montpellier‐Cancer (grant no. INCa‐DGOS‐Inserm 6045).