Accurate control of dual-receptor-engineered T cell activity through a bifunctional anti-angiogenic peptide

  • J Hematol Oncol. 2018 Mar 20;11(1):44. doi: 10.1186/s13045-018-0591-7.
Erhao Zhang  1 ,  Jieyi Gu  1 ,  Jianpeng Xue  1  2 ,  Chenyu Lin  1 ,  Chen Liu  1 ,  Mengwei Li  1 ,  Jingchao Hao  1  3 ,  Sarra Setrerrahmane  1 ,  Xiaowei Chi  1 ,  Weiyan Qi  1  2 ,  Jialiang Hu  4  5 ,  Hanmei Xu  6  7  8
Affiliations
  • 1. The Engineering Research Center of Peptide Drug Discovery and Development, China Pharmaceutical University, Nanjing, 210009, People's Republic of China.
  • 2. State Key Laboratory of Natural Medicines, Ministry of Education, China Pharmaceutical University, Nanjing, 210009, People's Republic of China.
  • 3. School of Pharmaceutical Sciences and Yunnan Provincial Key Laboratory of Pharmacology for Natural Products, Kunming Medical University, Kunming, 650500, People's Republic of China.
  • 4. The Engineering Research Center of Peptide Drug Discovery and Development, China Pharmaceutical University, Nanjing, 210009, People's Republic of China. [email protected].
  • 5. State Key Laboratory of Natural Medicines, Ministry of Education, China Pharmaceutical University, Nanjing, 210009, People's Republic of China. [email protected].
  • 6. The Engineering Research Center of Peptide Drug Discovery and Development, China Pharmaceutical University, Nanjing, 210009, People's Republic of China. [email protected].
  • 7. State Key Laboratory of Natural Medicines, Ministry of Education, China Pharmaceutical University, Nanjing, 210009, People's Republic of China. [email protected].
  • 8. Nanjing Anji Biotechnology Co., Ltd., Nanjing, 210046, People's Republic of China. [email protected].
Abstract

Background: Chimeric antigen receptors (CARs) presented on T cell surfaces enable redirection of T cell specificity, which has enormous promise in antitumor therapy. However, excessive activity and poor control over such engineered T cells cause significant safety challenges, such as cytokine release syndrome and organ toxicities. To enhance the specificity and controllable activity of CAR-T cells, we report a novel switchable dual-receptor CAR-engineered T (sdCAR-T) cell and a new switch molecule of FITC-HM-3 bifunctional molecule (FHBM) in this study.

Methods: We designed a fusion molecule comprising FITC and HM-3. HM-3, an antitumor peptide including an Arg-Gly-Asp sequence, can specifically target Integrin αvβ3 that is presented on some tumor cells. Moreover, to improve the specificity of CAR-T cells, we also generated the sdCAR-T cell line against cognate tumor cells expressing human Mesothelin (MSLN) and Integrin αvβ3. Finally, the activity of sdCAR-T cell and FHBM is verified via in vitro and in vivo experiments.

Results: In the presence of FHBM, the designed sdCAR-T cells exerted high activity including activation and proliferation and had specific cytotoxicity in a time- and dose-dependent manner in vitro. Furthermore, using a combination of FHBM in nude mice, sdCAR-T cells significantly inhibited the growth of MSLN+ K562 cells and released lower levels of the cytokines (e.g., interleukin-2, interferon γ, interleukin-6, and tumor necrosis factor α) relative to conventional CAR-T cells, obtaining specific, controllable, and enhanced cytotoxicity.

Conclusions: Our data indicate that FHBM can accurately control timing and dose of injected CAR-T cells, and sdCAR-T cells exert significant antitumor activity while releasing lower levels of cytokines for the cognate tumor cells expressing both MSLN and Integrin αvβ3. Therefore, combination therapies using sdCAR-T cells and the switch molecule FHBM have significant potential to treat malignancies.

Keywords
Bifunctional molecule; Cancer immunotherapy; HM-3; K562 cell; Switchable dual-receptor CAR.