A novel small molecule antagonist of choline kinase-α that simultaneously suppresses MAPK and PI3K/AKT signaling

B. F. Clem, A. L. Clem, A. Yalcin, U. Goswami, S. Arumugam, S. Telang, J. O. Trent, J. Chesney

Research output: Contribution to journalArticlepeer-review

60 Scopus citations

Abstract

Choline kinase-α expression and activity are increased in multiple human neoplasms as a result of growth factor stimulation and activation of cancer-related signaling pathways. The product of choline kinase-α, phosphocholine, serves as an essential metabolic reservoir for the production of phosphatidylcholine, the major phospholipid constituent of membranes and substrate for the production of lipid second messengers. Using in silico screening for small molecules that may interact with the choline kinase-α substrate binding domain, we identified a novel competitive inhibitor, N-(3,5-dimethylphenyl)-2-[[5-(4-ethylphenyl)-1H-1,2,4-triazol-3-yl]sulfanyl] acetamide (termed CK37) that inhibited purified recombinant human choline kinase-α activity, reduced the steady-state concentration of phosphocholine in transformed cells, and selectively suppressed the growth of neoplastic cells relative to normal epithelial cells. Choline kinase-α activity is required for the downstream production of phosphatidic acid, a promoter of several Ras signaling pathways. CK37 suppressed mitogen-activated protein kinase and phosphatidylinositol 3-kinase/AKT signaling, disrupted actin cytoskeletal organization, and reduced plasma membrane ruffling. Finally, administration of CK37 significantly decreased tumor growth in a lung tumor xenograft mouse model, suppressed tumor phosphocholine, and diminished activating phosphorylations of extracellular signal-regulated kinase and AKT in vivo. Together, these results further validate choline kinase-α as a molecular target for the development of agents that interrupt Ras signaling pathways, and indicate that receptor-based computational screening should facilitate the identification of new classes of choline kinase-α inhibitors.

Original languageEnglish (US)
Pages (from-to)3370-3380
Number of pages11
JournalOncogene
Volume30
Issue number30
DOIs
StatePublished - Jul 28 2011

Bibliographical note

Funding Information:
Lipidomic analysis was performed as a fee for service by the Kansas Lipidomics Research Center at Kansas State University. Briefly, cell lipids were extracted in methanol, dried under continuous nitrogen and then sent for analysis. The Kansas Lipidomics Research Center Analytical Laboratory is supported from the National Science Foundation’s EPSCoR program, under Grant no. EPS-0236913 with matching support from the State of Kansas through Kansas Technology Enterprise Corporation and Kansas State University.

Funding Information:
We acknowledge Deanna Siow and Binks Wattenburg for assistance with the thin layer chromatography protocol, Erin Brock for assisting with the confocal microscopy experiments, Bennet Jenson for histopathology assistance, and Andrew Lane for NMR interpretation. We also thank Dr Arnon Lavie for providing the D49N-hCKa2 plasmid for the expression of recombinant choline kinase. NMR experiments were carried out at the James Graham Brown Cancer Center NMR facility, supported in part by the Brown Foundation and NCCRR Grant 1P20 RR18733. This work was supported by institutional funds from the James Graham Brown Cancer Center and by grants from the Ky Lung Cancer Research Program (JC & BFC) and the National Cancer Institute (JC: 2R56CA116428-0509).

Keywords

  • chemotherapy
  • choline kinase
  • in silico
  • metabolism
  • phosphocholine

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