Journal of Shandong University (Health Sciences) ›› 2022, Vol. 60 ›› Issue (4): 30-37.doi: 10.6040/j.issn.1671-7554.0.2021.1108

Previous Articles    

Deubiquitinase USP35 promotes the cells migration and invasion of non-small cell lung cancer

CHEN Zhaobo1, FANG Min2, XUE Haoran1, LIU Chunyan3   

  1. 1. Department of Clinical Laboratory, Qilu Hospital(Qingdao), Cheeloo College of Medicine, Shandong University, Qingdao 266035, Shandong, China;
    2. Department of Gynaecology, Qingdao Women and Childrens Hospital, Qingdao 266034, Shandong, China;
    3. College of Basic Medicine, Qingdao University, Qingdao 266071, Shandong, China
  • Published:2022-04-22

PDF (PC)

202

Abstract: Objective To investigate the effects of deubiquitinase ubiquitin-speci cproteases 35(USP35)on the migration and invasion of non-small cell lung cancer(NSCLC). Methods The protein expression of USP35 in a panel of 7 human NSCLC cell lines was examined with Western blotting. USP35 overexpression plasmids and control plasmids were transfected into H1299 cells, while USP35 knockdown plasmids and control plasmids were transfected into Anip973 cells according to Lipofectamine 2000 instructions. The migration of NSCLC cells was analyzed using Transwell blank chambers, and the invasion was analyzed using the Transwell chambers containing matrigel substrate gels. The protein expressions of E-cadherin and Vimentin were detected with Western blotting after USP35 overexpressing or silencing in aforementioned cell lines. Results Of the 7 NSCLC cell lines tested, USP35 expression was the lowest in H1299 cells, and the highest in Anip973 cells. Compared with transfected USP35 control plasmids, transfected USP35 overexpression plasmids had significantly increased migration and invasion, down-regulated E-cadherin, and up-regulated Vimentin expressions. Compared with transfected USP35 control plasmids, the Anip973 cells of transfected USP35 knockdown plasmids had significantly reduced migration and invasion, up-regulated E-cadherin, and down-regulated Vimentin expressions. Conclusion USP35 plays a critical role in the migration and invasion of NSCLC cells, hence may become a therapeutic option for NSCLC.

Key words: Ubiquitin-speciı, c proteases 35, Non-small cell lung cancer, Invasion, Migration, Epithelial-mesenchymal transition

CLC Number: 

  • R574
[1] Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015 [J]. CA Cancer J Clin, 2016, 66(2): 115-132.
[2] Siegel RL, Miller KD, Fuchs HE, et al. Cancer Statistics, 2021 [J]. CA Cancer J Clin, 2021, 71(1): 7-33.
[3] Samson P, Keogan K, Crabtree T, et al. Interpreting survival data from clinical trials of surgery versus stereotactic body radiation therapy in operable Stage I non-small cell lung cancer patients [J]. Lung Cancer, 2017, 103: 6-10. doi: 10.1016/j.lungcan.2016.11.005.
[4] Beckett P, Tata LJ, Hubbard RB. Risk factors and survival outcome for non-elective referral in non-small cell lung cancer patients - analysis based on the National Lung Cancer Audit [J]. Lung cancer, 2014, 83(3): 396-400.
[5] Miller KD, Nogueira L, Mariotto AB, et al. Cancer treatment and survivorship statistics, 2019 [J]. CA Cancer J Clin, 2019, 69(5): 363-385.
[6] Xiao Y, Yin C, Wang Y, et al. FBXW7 deletion contributes to lung tumor development and confers resistance to gefitinib therapy [J]. Mol Oncol, 2018, 12(6): 883-895.
[7] 简政, 陈学瑜, 张亚杰, 等. 2022 年 V1 版《NCCN 非小细胞肺癌临床实践指南》更新解读[J]. 中国胸心血管外科临床杂志, 2022, 29(2): 150-157. JIAN Zheng, CHEN Xueyu, ZHANG Yajie, et al. Interpretation of updated NCCN guidelines for non-small cell lung cancer(version 1, 2022)[J]. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2022, 29(2): 150-157.
[8] 周广华, 林琳. 靶向治疗在 NSCLC 中的研究进展[J]. 临床肺科杂志, 2020, 25(4): 602-605.
[9] 戴陈新, 袁健, 郑亚新, 等. 去泛素化酶与肿瘤发生及发展关系的研究进展[J]. 中国癌症杂志, 2013, 23(7): 547-550. DAI Chenxin, YUAN Jian, ZHENG Yaxin, et al. Advances in the study of deubiquitinating enzymes in cancer research [J]. China Oncology, 2013, 23(7): 547-550.
[10] Wang W, Wang M, Xiao Y, et al. USP35 mitigates endoplasmic reticulum stress-induced apoptosis by stabilizing RRBP1 in non-small cell lung cancer [J]. Mol Oncol, 2021. doi: 10.1002/1878-0261.13112.
[11] Park J, Kwon MS, Kim EE, et al. USP35 regulates mitotic progression by modulating the stability of Aurora B [J]. Nat Commun, 2018, 9(1): 688.
[12] Cao J, Wu D, Wu G, et al. USP35, regulated by estrogen and AKT, promotes breast tumorigenesis by stabilizing and enhancing transcriptional activity of estrogen receptor α [J]. Cell Death Dis, 2021, 12(6): 619.
[13] Clague MJ, Urbé S, Komander D. Breaking the chains: deubiquitylating enzyme specificity begets function [J]. Nat Rev Mol Cell Biol, 2019, 20(6): 338-352.
[14] Harrigan JA, Jacq X, Martin NM, et al. Deubiquitylating enzymes and drug discovery: emerging opportunities [J]. Nat Rev Drug Discov, 2018, 17(1): 57-78.
[15] Liu S, González-Prieto R, Zhang M, et al. Deubiquitinase activity profiling identifies UCHL1 as a candidate oncoprotein that promotes TGFβ-induced breast cancer metastasis [J]. Clin Cancer Res, 2020, 26(6): 1460-1473.
[16] Zhang HH, Li C, Ren JW, et al. OTUB1 facilitates bladder cancer progression by stabilizing ATF6 in response to endoplasmic reticulum stress [J]. Cancer Sci, 2021, 112(6): 2199-2209.
[17] Wu X, Luo Q, Zhao P, et al. JOSD1 inhibits mitochondrial apoptotic signalling to drive acquired chemoresistance in gynaecological cancer by stabilizing MCL1 [J]. Cell Death Differ, 2020, 27(1): 55-70.
[18] Khan OM, Carvalho J, Spencer-Dene B, et al. The deubiquitinase USP9X regulates FBW7 stability and suppresses colorectal cancer [J]. J Clin Invest, 2018, 128(4): 1326-1337.
[19] Tanguturi P, Kim KS, Ramakrishna S. The role of deubiquitinating enzymes in cancer drug resistance [J]. Cancer Chemother Pharmacol, 2020, 85(4): 627-639.
[20] Liao XH, Wang Y, Zhong B, et al. USP3 promotes proliferation of non-small cell lung cancer through regulating RBM4 [J]. Eur Rev Med Pharmacol Sci, 2020, 24(6): 3143-3151.
[21] Wu Y, Qin J, Li F, et al. USP3 promotes breast cancer cell proliferation by deubiquitinating KLF5 [J]. J Biol Chem, 2019, 294(47): 17837-17847.
[22] Garcia DA, Baek C, Estrada MV, et al. USP11 enhances TGFβ-induced epithelial-mesenchymal plasticity and human breast cancer metastasis [J]. Mol Cancer Res, 2018, 16(7): 1172-1184.
[23] Sun H, Ou B, Zhao S, et al. USP11 promotes growth and metastasis of colorectal cancer via PPP1CA-mediated activation of ERK/MAPK signaling pathway [J]. EbioMedicine, 2019, 48: 236-247. doi: 10.1016/j.ebiom.2019.08.061.
[24] Zhang C, Xie C, Wang X, et al. Aberrant USP11 expression regulates NF90 to promote proliferation and metastasis in hepatocellular carcinoma [J]. Am J Cancer Res, 2020, 10(5): 1416-1428.
[25] Ha J, Kim M, Seo D, et al. The deubiquitinating enzyme USP20 regulates the TNFα-induced NF-κB signaling pathway through stabilization of p62 [J]. Int J Mol Sci, 2020, 21(9): 3116.
[26] Li W, Shen M, Jiang YZ, et al. Deubiquitinase USP20 promotes breast cancer metastasis by stabilizing SNAI2 [J]. Genes Dev, 2020, 34(19-20): 1310-1315.
[27] Wu C, Luo K, Zhao F, et al. USP20 positively regulates tumorigenesis and chemoresistance through β-catenin stabilization [J]. Cell Death Differ, 2018, 25(10): 1855-1869.
[28] Gan Q, Shao J, Cao Y, et al. USP33 regulates c-Met expression by deubiquitinating SP1 to facilitate metastasis in hepatocellular carcinoma [J]. Life Sci, 2020, 261:118316. doi: 10.1016/j.lfs.2020.118316.
[29] Han PP, Zhang GQ, Li L, et al. Downregulation of USP33 inhibits Slit/Robo signaling pathway and is associated with poor patient survival of glioma [J]. J Neurosurg Sci, 2020. doi: 10.23736/S0390-5616.20.04929-2.
[30] Huang Z, Wen P, Kong R, et al. USP33 mediates Slit-Robo signaling in inhibiting colorectal cancer cell migration [J]. Int J Cancer, 2015, 136(8): 1792-1802.
[31] Xia Y, Wang L, Xu Z, et al. Reduced USP33 expression in gastric cancer decreases inhibitory effects of Slit2-Robo1 signalling on cell migration and EMT [J]. Cell Prolif, 2019, 52(3): e12606.
[32] Dou N, Hu Q, Li L, et al. USP32 promotes tumorigenesis and chemoresistance in gastric carcinoma via upregulation of SMAD2 [J]. Int J Biol Sci, 2020, 16(9): 1648-1657.
[33] Hu W, Wei H, Li K, et al. Downregulation of USP32 inhibits cell proliferation, migration and invasion in human small cell lung cancer [J]. Cell Prolif, 2017, 50(4): e12343.
[34] Liu C, Wang L, Chen W, et al. USP35 activated by miR let-7a inhibits cell proliferation and NF-κB activation through stabilization of ABIN-2 [J]. Oncotarget, 2015, 6(29): 27891-27906.
[35] Wang Y, Serricchio M, Jauregui M, et al. Deubiquitinating enzymes regulate PARK2-mediated mitophagy [J]. Autophagy, 2015, 11(4): 595-606.
[36] Zhang J, Chen Y, Chen X, et al. Deubiquitinase USP35 restrains STING-mediated interferon signaling in ovarian cancer [J]. Cell Death Differ, 2021, 28(1): 139-155.
[37] Tang Z, Jiang W, Mao M, et al. Deubiquitinase USP35 modulates ferroptosis in lung cancer via targeting ferroportin [J]. Clin Transl Med, 2021, 11(4): e390.
[1] WANG Wei, WANG Yi-Feng, ZHANG Ling-Mei, LIN Qiong-Yan, HUANG Ju. umorigenicity and invasion of side population in human ovarian epithelial cancer OVCAR3 cells [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2209, 47(6): 8-11.
[2] ZUO Liping, JIANG Fengyang, ZHOU Binbin, FAN Jinlei, LIANG Yongfeng, DENG Zhanhao, YU Dexin. Value of preoperative multiphase MRI for predicting microvascular invasion and early recurrence of 169 hepatocellular carcinoma [J]. Journal of Shandong University (Health Sciences), 2022, 60(3): 89-95.
[3] ZHONG Lili, SHENG Ying, GUO Jianghong, YANG Shuangjian, HE Yijing. LncRNA-UCA1 effects invasion and metastasis of trophoblast cells by targeting miR-182-5p [J]. Journal of Shandong University (Health Sciences), 2022, 60(3): 76-82.
[4] ZHANG Qian, QIN Mingming, HE Xuejia, CAI Qiujing, ZHANG Yamin, LI Qingsu, ZHU Weiwei. Effects of calcitriol on EMT induced by TGF-β1 in asthma [J]. Journal of Shandong University (Health Sciences), 2021, 59(7): 10-18.
[5] KONG Xue, LI Juan, DUAN Weili, SHI Shuang, LI Peilong, DU Lutao, MAO Haiting, WANG Chuanxin. Effects of lncRNA AC012073.1 on the migration and invasion of human breast cancer cells and its clinical significance [J]. Journal of Shandong University (Health Sciences), 2021, 59(4): 70-78.
[6] XUE Yuan, LIN Xueyan, XU Ge, TIAN Yongjie. Expression of hypoxia-inducible factor-1α in the serum of patients with endometriosis and its effect on epithelial mesenchymal transition of eutopic endometrial stromal cells [J]. Journal of Shandong University (Health Sciences), 2021, 59(2): 41-47.
[7] CHAI Xiaoxue, YE Hui, LYU Xinran, DING Xuchao, ZHEN Qiulai, DU Juan, CAO Lili. Prognostic value of POU4F3 in 118 patients with lung adenocarcinoma and its effect on migration of lung adenocarcinoma cells [J]. Journal of Shandong University (Health Sciences), 2021, 59(11): 8-18.
[8] YANG Jia, ZHANG Man, CHEN Kaiming, CAO Xi. Mechanism of miR-146a accelerating macrophage migration induced arteriosclerosis via TLR4/MyD88 pathway [J]. Journal of Shandong University (Health Sciences), 2021, 59(11): 1-7.
[9] SUN Yifeng, GAO Yu, LIANG Yongyuan, GAO Yang. Expression of CPLX2 and its in vitro effects on the proliferation migration and invasion of hepatocellular carcinoma cells [J]. Journal of Shandong University (Health Sciences), 2020, 1(9): 34-39.
[10] LI Ning, LI Juan, XIE Yan, LI Peilong, WANG Yunshan, DU Lutao, WANG Chuanxin. Expression of LncRNA AL109955.1 in 80 cases of colorectal cancer and its effect on cell proliferation, migration and invasion [J]. Journal of Shandong University (Health Sciences), 2020, 1(7): 38-46.
[11] MA Qingyuan, PU Peidong, HAN Fei, WANG Chao, ZHU Zhoujun, WANG Weishan, SHI Chenhui. Effect of miR-27b-3p regulating SMAD1 on osteosarcoma cell proliferation, migration and invasion [J]. Journal of Shandong University (Health Sciences), 2020, 1(7): 32-37.
[12] WANG Baojin, ZHAO Xinxin, LI Xia, MA Qian, WANG Xinyue, SUN Yang, SHI Zhongna. miR-203 targeting Survivin to inhibit the proliferation, migration and invasion of ovarian cancer cells [J]. Journal of Shandong University (Health Sciences), 2020, 58(12): 23-28.
[13] SHI Li, MA Jing, ZHAO Xiwa, GUAN Yingxia, ZHAO Lianmei, SHAN Baoen. Expression and function of miR-25-3p in endometrial cancer [J]. Journal of Shandong University (Health Sciences), 2020, 58(12): 86-91.
[14] LIU Xiaojing, XIA Xiyan, XIAO Ke, CHEN Wendan, ZHUANG Xuewei. Expression and clinical significance of exosomal long non-coding RNA OGFRP1 in 84 cases of non-small cell lung cancer [J]. Journal of Shandong University (Health Sciences), 2020, 58(11): 71-75.
[15] HONG Jiageng, NIE Yangyang, SU Guoqiang. Effects of propofol on proliferation, migration and expressions of Wnt1 and β-catenin in colon cancer cells [J]. Journal of Shandong University (Health Sciences), 2020, 58(11): 53-58.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
[1] ZHAO Tingting, QI Yana, ZHANG Ying, YUAN Bing, HAN Mingyong. Mouse breast cancer induces changes of the microenvironment in pre-metastatic lung tissue[J]. Journal of Shandong University (Health Sciences), 2022, 60(4): 24 -29 .
[2] XU Ge, LI Qing, ZHANG Cancan, TIAN Yongjie. Expressions and clinical significance of PARP-1 and HIF-1α in adenomyosis tissues and primary cells[J]. Journal of Shandong University (Health Sciences), 0, (): 55 -61 .
[3] LI Honghao, YU Jing, CHEN Yali, GUO Shougang. Evaluation of CD4+CD25+FoxP3+ regulatory T cells and FoxP3 mRNA expression in 20 NMOSD patients[J]. Journal of Shandong University (Health Sciences), 0, (): 50 -54 .
[4] SHAO Na, YIN Hao, LI Yaran, ZHANG Baokun, HUANG Weiwei, LU Shanshan, TANG Jiyou. Study on the mechanism of Suvorexant treatment ameliorates learning and memory impairment in chronic sleep deprivation mice model[J]. Journal of Shandong University (Health Sciences), 2022, 60(4): 17 -23 .
[5] ZHAO Hailong, WANG Hao, FANG Yuqing, MAO Fei, ZHAO Zhangning, TIAN Xiangqi, XU Xinrong, WANG Min, LI Xiuhua. Efficacy of additional idebenone in the treatment of 34 patients with Parkinsons disease with depression[J]. Journal of Shandong University (Health Sciences), 0, (): 38 -44 .
[6] YUAN Hongtao, JI Congshan, KANG Bing, QIN Songnan, YU Xinxin, GAO Lin, WANG Ximing. Diagnostic value of CT radiomics nomogram for adrenal lipid-poor adenoma and nodular hyperplasia[J]. Journal of Shandong University (Health Sciences), 0, (): 68 -75 .
[7] YANG Congpin, LUO Zhuoye, XU Xiuhua, LI Aimin, HAO Guimin. Reproductive choices and pressure in 3,512 women of childbearing age in a hospital in Hebei Province[J]. Journal of Shandong University (Health Sciences), 0, (): 62 -67 .
[8] SHEN Yufei, ZHAO Mei, HU Mi. Help-seeking willingness, help-seeking behaviors and influencing factors in middle school students with suicidal ideation[J]. Journal of Shandong University (Health Sciences), 0, (): 99 -106 .
[9] LIU Liwen, MA Jun, LI Peizheng, ZHANG Xiufang, LIU Yiming. Caregiver burden and influencing factors of 128 patients with Parkinsons disease[J]. Journal of Shandong University (Health Sciences), 0, (): 45 -49 .
[10] SUN Jiye, WANG Ziou, SUN Xiaowei, LI Hongtao. Effects of traditional Chinese medicine fumigation combined with extracorporeal shock wave therapy on 72 cases of femoroacetabular impingement syndrome and serum inflammatory factor[J]. Journal of Shandong University (Health Sciences), 0, (): 76 -81 .
Copyright 2018 © Editorial office of Journal of Shandong University (Health Sciences)
Supported by Beijing Magtech Co.Ltd