Article

Ras inhibitor farnesylthiosalicylic acid conjugated with IR783 dye exhibits improved tumor-targeting and altered anti-breast cancer mechanisms in mice

Qiu-ju Huang1,2, Guo-chao Liao1, Xue-rong Zhuang1, Meng-lan Yang1, Jing-jing Yao1, Jian-hua Deng1, Yan-min Zhang1, Ying Wang1, Xiao-xiao Qi1, Dong-feng Pan3, Yang Guan1, Zhi-ying Huang1, Feng-xue Zhang2, Zhong-qiu Liu1,4, Lin-lin Lu1,4
1 Joint Laboratory for Translational Cancer Research of Chinese Medicine of the Ministry of Education of the People’s Republic of China, International Institute for Translational Chinese Medicine, Guangzhou University of Chinese Medicine, Guangzhou 510006, China
2 School of Basic Medical Sciences, Guangzhou University of Chinese Medicine, Guangzhou 510006, China
3 Department of Radiology and Medical Imaging, University of Virginia, Charlottesville, VA 22903, USA
4 State Key Laboratory of Quality Research in Chinese Medicine/ Macau Institute for Applied Research in Medicine and Health, Macau University of Science and Technology, Macao, SAR, China
Correspondence to: Zhong-qiu Liu: liuzq@gzucm.edu.cn, Lin-lin Lu: lllu@gzucm.edu.cn,
DOI: 10.1038/s41401-021-00775-5
Received: 6 April 2021
Accepted: 5 September 2021
Advance online: 29 November 2021

Abstract

Ras has long been viewed as a promising target for cancer therapy. Farnesylthiosalicylic acid (FTS), as the only Ras inhibitor has ever entered phase II clinical trials, has yielded disappointing results due to its strong hydrophobicity, poor tumor-targeting capacity, and low therapeutic efficiency. Thus, enhancing hydrophilicity and tumor-targeting capacity of FTS for improving its therapeutic efficacy is of great significance. In this study we conjugated FTS with a cancer-targeting small molecule dye IR783 and characterized the anticancer properties of the conjugate FTS-IR783. We showed that IR783 conjugation greatly improved the hydrophilicity, tumor-targeting and therapeutic potential of FTS. After a single oral administration in Balb/c mice, the relative bioavailability of FTS- IR783 was increased by 90.7% compared with FTS. We demonstrated that organic anion transporting polypeptide (OATP) and endocytosis synergistically drove the uptake of the FTS-IR783 conjugate in breast cancer MDA-MB-231 cells, resulting in superior tumor-targeting ability of the conjugate both in vitro and in vivo. We further revealed that FTS-IR783 conjugate could bind with and directly activate AMPK rather than affecting Ras, and subsequently regulate the TSC2/mTOR signaling pathway, thus achieving 2–10-fold increased anti-cancer therapeutic efficacy against 6 human breast cancer cell lines compared to FTS both in vivo and in vitro. Overall, our data highlights a promising approach for the modification of the anti-tumor drug FTS using IR783 and makes it possible to return FTS back to the clinic with a better efficacy.
Keywords: Ras inhibitor; Farnesylthiosalicylic acid; IR783; tumor-targeting; breast neoplasm; AMPK; mTOR

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