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A high-throughput screening campaign against PFKFB3 identified potential inhibitors with novel scaffolds

Jie Li1, Yan Zhou2, Guy Eelen3, Qing-tong Zhou1, Wen-bo Feng1, Viktorija Labroska2,4, Fen-fen Ma5, Hui-ping Lu5, Mieke Dewerchin3, Peter Carmeliet3, Ming-wei Wang1,2,4,6,7, De-hua Yang2,4,6
1 Department of Pharmacology, School of Basic Medical Sciences, Fudan University, Shanghai 200032, China
2 The National Center for Drug Screening, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai 201203, China
3 Laboratory of Angiogenesis and Vascular Metabolism, Department of Oncology, KU Leuven and Center for Cancer Biology, VIB-KU Leuven, Leuven 3000, Belgium
4 University of Chinese Academy of Sciences, Beijing 100049, China
5 Department of Pharmacy, Pudong Hospital, Fudan University, Shanghai 201300, China
6 Research Center for Deepsea Bioresources, Sanya 572025, China
7 Department of Chemistry, School of Science, The University of Tokyo, Tokyo 113-0033, Japan
Correspondence to: Ming-wei Wang: mwwang@simm.ac.cn, De-hua Yang: dhyang@simm.ac.cn,
DOI: 10.1038/s41401-022-00989-1
Received: 2 April 2022
Accepted: 23 August 2022
Advance online: 16 September 2022

Abstract

The growth of solid tumors depends on tumor vascularization and the endothelial cells (ECs) that line the lumen of blood vessels. ECs generate a large fraction of ATP through glycolysis, and elevation of their glycolytic activity is associated with angiogenic behavior in solid tumors. 6-Phosphofructo-2-kinase/fructose-2,6-bisphosphatase 3 (PFKFB3) positively regulates glycolysis via fructose-2/6-bisphosphate, the product of its kinase activity. Partial inhibition of glycolysis in tumor ECs by targeting PFKFB3 normalizes the otherwise abnormal tumor vessels, thereby reducing metastasis and improving the outcome of chemotherapy. Although a limited number of tool compounds exist, orally available PFKFB3 inhibitors are unavailable. In this study we conducted a high-throughput screening campaign against the kinase activity of PFKFB3, involving 250,240 chemical compounds. A total of 507 initial hits showing >50% inhibition at 20 μM were identified, 66 of them plus 1 analog from a similarity search consistently displayed low IC50 values (<10 μM). In vitro experiments yielded 22 nontoxic hits that suppressed the tube formation of primary human umbilical vein ECs at 10 μM. Of them, 15 exhibited binding affinity to PFKFB3 in surface plasmon resonance assays, including 3 (WNN0403-E003, WNN1352-H007 and WNN1542-F004) that passed the pan-assay interference compounds screening without warning flags. This study provides potential leads to the development of new PFKFB3 inhibitors.
Keywords: solid tumors; angiogenesis; glycolysis; high-throughput screening; PFKFB3 inhibitors

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