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Cystathionine γ-lyase mediates cell proliferation, migration, and invasion of nasopharyngeal carcinoma

Oncogene volume 41, pages 5238–5252 (2022)Cite this article

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Abstract

Nasopharyngeal carcinoma (NPC) is an epithelia-derived malignancy with a distinctive geographic distribution. Cystathionine γ-lyase (CSE) is involved in cancer development and progression. Nevertheless, the role of CSE in the growth of NPC is unknown. In this study, we found that CSE levels in human NPC cells were higher than those in normal nasopharyngeal cells. CSE overexpression enhanced the proliferative, migrative, and invasive abilities of NPC cells and CSE downregulation exerted reverse effects. Overexpression of CSE decreased the expressions of cytochrome C, cleaved caspase (cas)-3, cleaved cas-9, and cleaved poly-ADP-ribose polymerase, whereas CSE knockdown exhibited reverse effects. CSE overexpression decreased reactive oxygen species (ROS) levels and the expressions of phospho (p)-extracellular signal-regulated protein kinase 1/2, p-c-Jun N-terminal kinase, and p-p38, but promoted the expressions of p-phosphatidylinositol 3-kinase (PI3K), p-AKT, and p-mammalian target of rapamycin (mTOR), whereas CSE knockdown showed oppose effects. In addition, CSE overexpression promoted NPC xenograft tumor growth and CSE knockdown decreased tumor growth by modulating proliferation, angiogenesis, cell cycle, and apoptosis. Furthermore, DL-propargylglycine (an inhibitor of CSE) dose-dependently inhibited NPC cell growth via ROS-mediated mitogen-activated protein kinase (MAPK) and PI3K/AKT/mTOR pathways without significant toxicity. In conclusion, CSE could regulate the growth of NPC cells through ROS-mediated MAPK and PI3K/AKT/mTOR cascades. CSE might be a novel tumor marker for the diagnosis and prognosis of NPC. Novel donors/drugs that inhibit the expression/activity of CSE can be developed in the treatment of NPC.

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Fig. 1: The expression levels of CSE, CBS, and 3-MST in human NPC cells were detected and CSE overexpression and knockdown experiments were performed.
Fig. 2: Effects of CSE on the proliferation and viability of human NPC cells.
Fig. 3: Effects of CSE on the migration and invasion of human NPC cells.
Fig. 4: Effects of CSE on the apoptosis in human NPC cells.
Fig. 5: Effects of CSE on ROS-mediated MAPK and PI3K/AKT/mTOR signaling pathways in human NPC cells.
Fig. 6: Effects of CSE on NPC xenograft tumor growth in nude mice.
Fig. 7: Effects of PAG on NPC xenograft tumor growth in nude mice.
Fig. 8: Effects of PAG on the toxicity in nude mice.

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Data availability

The data of the study are available from the corresponding author on reasonable request.

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Funding

This work was supported by grants from the National Natural Science Foundation of China (Nos. 81802718, U1504817), the Foundation of Science & Technology Department of Henan Province, China (Nos. 202102310480, 192102310151), the Training Program for Young Backbone Teachers of Institutions of Higher Learning in Henan Province, China (No. 2020GGJS038), and the Science Foundation for Young Talents of Henan University College of Medicine, China (No. 2019013).

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  1. These authors contributed equally: Qianqian Zhang, Yingran Gao.

Authors and Affiliations

  1. School of Basic Medical Sciences, Henan University, Kaifeng, Henan, 475004, China

    Qianqian Zhang, Yingran Gao, Yanxia Zhang, Mirong Jing, Di Wang, Yizhen Wang, Huiwen Qi, Chunbo Cai, Jing Zhang, Tao Li, Ailing Ji, Qiying Jiang, Xinying Ji, Yanzhang Li & Dongdong Wu

  2. Henan International Joint Laboratory for Nuclear Protein Regulation, Henan University, Kaifeng, Henan, 475004, China

    Qianqian Zhang, Yingran Gao, Yanxia Zhang, Mirong Jing, Di Wang, Yizhen Wang, Saadullah Khattak, Huiwen Qi, Chunbo Cai, Jing Zhang, Ebenezeri Erasto Ngowi, Nazeer Hussain Khan, Tao Li, Ailing Ji, Qiying Jiang, Xinying Ji, Yanzhang Li & Dongdong Wu

  3. School of Life Sciences, Henan University, Kaifeng, Henan, 475004, China

    Saadullah Khattak & Nazeer Hussain Khan

  4. Kaifeng Municipal Key Laboratory of Cell Signal Transduction, Henan Provincial Engineering Centre for Tumor Molecular Medicine, Henan University, Kaifeng, Henan, 475004, China

    Ebenezeri Erasto Ngowi & Xinying Ji

  5. Department of Biological Sciences, Faculty of Science, Dar es Salaam University College of Education, Dar es Salaam, 2329, Tanzania

    Ebenezeri Erasto Ngowi

  6. School of Stomatology, Henan University, Kaifeng, Henan, 475004, China

    Dongdong Wu

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Contributions

DDW, YZL and XYJ conceived the study and drafted the manuscript. DDW, QQZ, YRG, YXZ, MRJ, DW, YZW, SK, HWQ, CBC, JZ, EEN, NHK, TL, ALJ and QYJ designed and performed the experiments. DDW, QQZ and YRG analyzed the data and prepared the figures. All authors read and approved the final manuscript.The data of the study are available from the corresponding author on reasonable request.

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Correspondence to Xinying Ji, Yanzhang Li or Dongdong Wu.

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Animal experiments were approved by the Committee of Medical Ethics and Welfare for Experimental Animals of Henan University School of Medicine (HUSOM-2017-191) in compliance with the Experimental Animal Regulations formulated by the National Science and Technology Commission, China.

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Zhang, Q., Gao, Y., Zhang, Y. et al. Cystathionine γ-lyase mediates cell proliferation, migration, and invasion of nasopharyngeal carcinoma. Oncogene 41, 5238–5252 (2022). https://doi.org/10.1038/s41388-022-02512-6

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