Research Paper Volume 12, Issue 21 pp 21758—21776

Caspase-3 knockout attenuates radiation-induced tumor repopulation via impairing the ATM/p53/Cox-2/PGE2 pathway in non-small cell lung cancer

Minghui Zhao1, *, , Yiwei Wang1, *, , Yucui Zhao1, *, , Sijia He1, , Ruyi Zhao1, , Yanwei Song1, , Jin Cheng1, , Yanping Gong1, , Jianzhu Xie1, , Yulan Wang1, , Binjie Hu1, , Ling Tian2,3, , Qian Huang1, ,

  • 1 Cancer Center, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 201620, China
  • 2 Shanghai Key Laboratory for Pancreatic Diseases, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 201620, China
  • 3 Department of Central Laboratory, Shanghai Chest Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200030, China
* Equal contribution

Received: May 15, 2020       Accepted: July 14, 2020       Published: November 7, 2020      

https://doi.org/10.18632/aging.103984
How to Cite

Copyright: © 2020 Zhao et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Abstract

Radiotherapy is an effective treatment for non-small cell lung cancer (NSCLC). However, irradiated, dying tumor cells generate potent growth stimulatory signals during radiotherapy that promote the repopulation of adjacent surviving tumor cells to cause tumor recurrence. We investigated the function of caspase-3 in NSCLC repopulation after radiotherapy. We found that radiotherapy induced a DNA damage response (DDR), activated caspase-3, and promoted tumor repopulation in NSCLC cells. Unexpectedly, caspase-3 knockout attenuated the ataxia-telangiectasia mutated (ATM)/p53-initiated DDR by decreasing nuclear migration of endonuclease G (EndoG), thereby reducing the growth-promoting effect of irradiated, dying tumor cells. We also identified p53 as a regulator of the Cox-2/PGE2 axis and its involvement in caspase-3-induced tumor repopulation after radiotherapy. In addition, injection of caspase-3 knockout NSCLC cells impaired tumor growth in a nude mouse model. Our findings reveal that caspase-3 promotes tumor repopulation in NSCLC cells by activating DDR and the downstream Cox-2/PGE2 axis. Thus, caspase-3-induced ATM/p53/Cox-2/PGE2 signaling pathway could provide potential therapeutic targets to reduce NSCLC recurrence after radiotherapy.

Abbreviations

AA: arachidonic acid; ATM: ataxia-telangiectasia mutated; Chk2: checkpoint kinase 2; DDR: DNA damage response; DSBs: DNA double-strand breaks; ELISA: enzyme-linked immunosorbent assay; EndoG: endonuclease G; Fluc: firefly luciferase; GFP: green fluorescent protein; H&E: hematoxylin and eosin; HR: homologous recombination; IHC: immunohistochemistry; iPLA2: calcium-independent phospholipase A2; NHEJ: non-homologous end joining; NSCLC: non-small cell lung cancer; PARP: poly (ADP-ribose) polymerase; PGE2: prostaglandin E2; qPCR: quantitative real-time polymerase chain reaction.