Knockdown of neuron-specific enolase suppresses the proliferation and migration of NCI-H209 cells
Identifieur interne : 000751 ( Pmc/Curation ); précédent : 000750; suivant : 000752Knockdown of neuron-specific enolase suppresses the proliferation and migration of NCI-H209 cells
Auteurs : Xia Liu [République populaire de Chine] ; Shousheng Liu [République populaire de Chine] ; Juan Fu [République populaire de Chine] ; Jinsheng Huang [République populaire de Chine] ; Chengyin Weng [République populaire de Chine] ; Xisheng Fang [République populaire de Chine] ; Mingmei Guan [République populaire de Chine] ; Yong Wu [République populaire de Chine] ; Lin Yang [République populaire de Chine] ; Guolong Liu [République populaire de Chine]Source :
- Oncology Letters [ 1792-1074 ] ; 2019.
Abstract
Neuron-specific enolase (NSE) is generally considered as a marker for diagnosis and evaluation of the response to therapy in small cell lung cancer (SCLC). However, the role of NSE in the progression of SCLC remains to be elucidated. In the present study, the functions of NSE in SCLC, in addition to the potential mechanisms, were investigated using a loss-of-function approach with NSE-targeting small interfering (si)RNA. The knockdown of NSE markedly decreased the proliferation of NCI-H209 cells, as indicated by MTT assay (P<0.05). Furthermore, the silencing of NSE resulted in the formation of smaller and fewer colonies compared with that in the control group (P<0.001). Flow cytometric analysis indicated that the silencing of NSE resulted in a decreased S-phase population among NCI-H209 cells (P<0.05). Transwell assay demonstrated that the silencing of NSE suppressed the migration of NCI-H209 cells (P<0.001). NCI-H209 cells transfected with NSE siRNA-1 or negative control were collected and the protein levels of metastasis-associated genes were detected using western blot analysis. The results indicated that the knockdown of NSE led to downregulation of the pro-metastatic gene vascular endothelial growth factor (VEGF; P<0.05) and the upregulation of metastasis suppressor genes NM23 and E-cadherin (P<0.05). Taken together, the results of the present study demonstrated that the silencing of NSE suppressed the migration, proliferation and colony formation ability of SCLC cells and decreased the S-phase population. In addition, the knockdown of NSE resulted in the upregulation of E-cadherin and NM23 and the downregulation of VEGF. Collectively, these results indicated that intracellular NSE may have an important role in the progression of SCLC.
Url:
DOI: 10.3892/ol.2019.10797
PubMed: 31611991
PubMed Central: 6781773
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<author><name sortKey="Liu, Guolong" sort="Liu, Guolong" uniqKey="Liu G" first="Guolong" last="Liu">Guolong Liu</name>
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<series><title level="j">Oncology Letters</title>
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<front><div type="abstract" xml:lang="en"><p>Neuron-specific enolase (NSE) is generally considered as a marker for diagnosis and evaluation of the response to therapy in small cell lung cancer (SCLC). However, the role of NSE in the progression of SCLC remains to be elucidated. In the present study, the functions of NSE in SCLC, in addition to the potential mechanisms, were investigated using a loss-of-function approach with NSE-targeting small interfering (si)RNA. The knockdown of NSE markedly decreased the proliferation of NCI-H209 cells, as indicated by MTT assay (P<0.05). Furthermore, the silencing of NSE resulted in the formation of smaller and fewer colonies compared with that in the control group (P<0.001). Flow cytometric analysis indicated that the silencing of NSE resulted in a decreased S-phase population among NCI-H209 cells (P<0.05). Transwell assay demonstrated that the silencing of NSE suppressed the migration of NCI-H209 cells (P<0.001). NCI-H209 cells transfected with NSE siRNA-1 or negative control were collected and the protein levels of metastasis-associated genes were detected using western blot analysis. The results indicated that the knockdown of NSE led to downregulation of the pro-metastatic gene vascular endothelial growth factor (VEGF; P<0.05) and the upregulation of metastasis suppressor genes NM23 and E-cadherin (P<0.05). Taken together, the results of the present study demonstrated that the silencing of NSE suppressed the migration, proliferation and colony formation ability of SCLC cells and decreased the S-phase population. In addition, the knockdown of NSE resulted in the upregulation of E-cadherin and NM23 and the downregulation of VEGF. Collectively, these results indicated that intracellular NSE may have an important role in the progression of SCLC.</p>
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</author>
<author><name sortKey="Soerjomataram, I" uniqKey="Soerjomataram I">I Soerjomataram</name>
</author>
<author><name sortKey="Dikshit, R" uniqKey="Dikshit R">R Dikshit</name>
</author>
<author><name sortKey="Eser, S" uniqKey="Eser S">S Eser</name>
</author>
<author><name sortKey="Mathers, C" uniqKey="Mathers C">C Mathers</name>
</author>
<author><name sortKey="Rebelo, M" uniqKey="Rebelo M">M Rebelo</name>
</author>
<author><name sortKey="Parkin, Dm" uniqKey="Parkin D">DM Parkin</name>
</author>
<author><name sortKey="Forman, D" uniqKey="Forman D">D Forman</name>
</author>
<author><name sortKey="Bray, F" uniqKey="Bray F">F Bray</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Wistuba, Ii" uniqKey="Wistuba I">II Wistuba</name>
</author>
<author><name sortKey="Gazdar, Af" uniqKey="Gazdar A">AF Gazdar</name>
</author>
<author><name sortKey="Minna, Jd" uniqKey="Minna J">JD Minna</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Van Meerbeeck, Jp" uniqKey="Van Meerbeeck J">JP van Meerbeeck</name>
</author>
<author><name sortKey="Fennell, Da" uniqKey="Fennell D">DA Fennell</name>
</author>
<author><name sortKey="De Ruysscher, Dk" uniqKey="De Ruysscher D">DK De Ruysscher</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Pelayo Alvarez, M" uniqKey="Pelayo Alvarez M">M Pelayo Alvarez</name>
</author>
<author><name sortKey="Westeel, V" uniqKey="Westeel V">V Westeel</name>
</author>
<author><name sortKey="Cortes Jofre, M" uniqKey="Cortes Jofre M">M Cortés-Jofré</name>
</author>
<author><name sortKey="Bonfill Cosp, X" uniqKey="Bonfill Cosp X">X Bonfill Cosp</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Shirasawa, M" uniqKey="Shirasawa M">M Shirasawa</name>
</author>
<author><name sortKey="Fukui, T" uniqKey="Fukui T">T Fukui</name>
</author>
<author><name sortKey="Kusuhara, S" uniqKey="Kusuhara S">S Kusuhara</name>
</author>
<author><name sortKey="Hiyoshi, Y" uniqKey="Hiyoshi Y">Y Hiyoshi</name>
</author>
<author><name sortKey="Ishihara, M" uniqKey="Ishihara M">M Ishihara</name>
</author>
<author><name sortKey="Kasajima, M" uniqKey="Kasajima M">M Kasajima</name>
</author>
<author><name sortKey="Nakahara, Y" uniqKey="Nakahara Y">Y Nakahara</name>
</author>
<author><name sortKey="Otani, S" uniqKey="Otani S">S Otani</name>
</author>
<author><name sortKey="Igawa, S" uniqKey="Igawa S">S Igawa</name>
</author>
<author><name sortKey="Yokoba, M" uniqKey="Yokoba M">M Yokoba</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Qiu, G" uniqKey="Qiu G">G Qiu</name>
</author>
<author><name sortKey="Du, X" uniqKey="Du X">X DU</name>
</author>
<author><name sortKey="Zhou, X" uniqKey="Zhou X">X Zhou</name>
</author>
<author><name sortKey="Bao, W" uniqKey="Bao W">W Bao</name>
</author>
<author><name sortKey="Chen, L" uniqKey="Chen L">L Chen</name>
</author>
<author><name sortKey="Chen, J" uniqKey="Chen J">J Chen</name>
</author>
<author><name sortKey="Ji, Y" uniqKey="Ji Y">Y Ji</name>
</author>
<author><name sortKey="Wang, S" uniqKey="Wang S">S Wang</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Chan, Ba" uniqKey="Chan B">BA Chan</name>
</author>
<author><name sortKey="Coward, Ji" uniqKey="Coward J">JI Coward</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Oze, I" uniqKey="Oze I">I Oze</name>
</author>
<author><name sortKey="Ito, H" uniqKey="Ito H">H Ito</name>
</author>
<author><name sortKey="Nishino, Y" uniqKey="Nishino Y">Y Nishino</name>
</author>
<author><name sortKey="Hattori, M" uniqKey="Hattori M">M Hattori</name>
</author>
<author><name sortKey="Nakayama, T" uniqKey="Nakayama T">T Nakayama</name>
</author>
<author><name sortKey="Miyashiro, I" uniqKey="Miyashiro I">I Miyashiro</name>
</author>
<author><name sortKey="Matsuo, K" uniqKey="Matsuo K">K Matsuo</name>
</author>
<author><name sortKey="Ito, Y" uniqKey="Ito Y">Y Ito</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Harmsma, M" uniqKey="Harmsma M">M Harmsma</name>
</author>
<author><name sortKey="Schutte, B" uniqKey="Schutte B">B Schutte</name>
</author>
<author><name sortKey="Ramaekers, Fc" uniqKey="Ramaekers F">FC Ramaekers</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Bremnes, Rm" uniqKey="Bremnes R">RM Bremnes</name>
</author>
<author><name sortKey="Sundstrom, S" uniqKey="Sundstrom S">S Sundstrom</name>
</author>
<author><name sortKey="Aaseb, U" uniqKey="Aaseb U">U Aasebø</name>
</author>
<author><name sortKey="Kaasa, S" uniqKey="Kaasa S">S Kaasa</name>
</author>
<author><name sortKey="Hatlevoll, R" uniqKey="Hatlevoll R">R Hatlevoll</name>
</author>
<author><name sortKey="Aamdal, S" uniqKey="Aamdal S">S Aamdal</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Ono, A" uniqKey="Ono A">A Ono</name>
</author>
<author><name sortKey="Naito, T" uniqKey="Naito T">T Naito</name>
</author>
<author><name sortKey="Ito, I" uniqKey="Ito I">I Ito</name>
</author>
<author><name sortKey="Watanabe, R" uniqKey="Watanabe R">R Watanabe</name>
</author>
<author><name sortKey="Shukuya, T" uniqKey="Shukuya T">T Shukuya</name>
</author>
<author><name sortKey="Kenmotsu, H" uniqKey="Kenmotsu H">H Kenmotsu</name>
</author>
<author><name sortKey="Tsuya, A" uniqKey="Tsuya A">A Tsuya</name>
</author>
<author><name sortKey="Nakamura, Y" uniqKey="Nakamura Y">Y Nakamura</name>
</author>
<author><name sortKey="Murakami, H" uniqKey="Murakami H">H Murakami</name>
</author>
<author><name sortKey="Kaira, K" uniqKey="Kaira K">K Kaira</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Zhao, Wx" uniqKey="Zhao W">WX Zhao</name>
</author>
<author><name sortKey="Luo, Jf" uniqKey="Luo J">JF Luo</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Sharma, Ra" uniqKey="Sharma R">RA Sharma</name>
</author>
<author><name sortKey="Wotherspoon, Ac" uniqKey="Wotherspoon A">AC Wotherspoon</name>
</author>
<author><name sortKey="Cook, G" uniqKey="Cook G">G Cook</name>
</author>
<author><name sortKey="Morgan, Gj" uniqKey="Morgan G">GJ Morgan</name>
</author>
<author><name sortKey="Huddart, Ra" uniqKey="Huddart R">RA Huddart</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Huang, L" uniqKey="Huang L">L Huang</name>
</author>
<author><name sortKey="Zhou, Jg" uniqKey="Zhou J">JG Zhou</name>
</author>
<author><name sortKey="Yao, Wx" uniqKey="Yao W">WX Yao</name>
</author>
<author><name sortKey="Tian, X" uniqKey="Tian X">X Tian</name>
</author>
<author><name sortKey="Lv, Sp" uniqKey="Lv S">SP Lv</name>
</author>
<author><name sortKey="Zhang, Ty" uniqKey="Zhang T">TY Zhang</name>
</author>
<author><name sortKey="Jin, Sh" uniqKey="Jin S">SH Jin</name>
</author>
<author><name sortKey="Bai, Yj" uniqKey="Bai Y">YJ Bai</name>
</author>
<author><name sortKey="Ma, H" uniqKey="Ma H">H Ma</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Molina, R" uniqKey="Molina R">R Molina</name>
</author>
<author><name sortKey="Auge, Jm" uniqKey="Auge J">JM Auge</name>
</author>
<author><name sortKey="Escudero, Jm" uniqKey="Escudero J">JM Escudero</name>
</author>
<author><name sortKey="Marrades, R" uniqKey="Marrades R">R Marrades</name>
</author>
<author><name sortKey="Vi Olas, N" uniqKey="Vi Olas N">N Viñolas</name>
</author>
<author><name sortKey="Carcereny, E" uniqKey="Carcereny E">E Carcereny</name>
</author>
<author><name sortKey="Ramirez, J" uniqKey="Ramirez J">J Ramirez</name>
</author>
<author><name sortKey="Filella, X" uniqKey="Filella X">X Filella</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Liu, S" uniqKey="Liu S">S Liu</name>
</author>
<author><name sortKey="Guo, H" uniqKey="Guo H">H Guo</name>
</author>
<author><name sortKey="Kong, L" uniqKey="Kong L">L Kong</name>
</author>
<author><name sortKey="Li, H" uniqKey="Li H">H Li</name>
</author>
<author><name sortKey="Zhang, Y" uniqKey="Zhang Y">Y Zhang</name>
</author>
<author><name sortKey="Zhu, H" uniqKey="Zhu H">H Zhu</name>
</author>
<author><name sortKey="Yu, J" uniqKey="Yu J">J Yu</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Buil Bruna, N" uniqKey="Buil Bruna N">N Buil-Bruna</name>
</author>
<author><name sortKey="L Pez Picazo, Jm" uniqKey="L Pez Picazo J">JM López-Picazo</name>
</author>
<author><name sortKey="Moreno Jimenez, M" uniqKey="Moreno Jimenez M">M Moreno-Jiménez</name>
</author>
<author><name sortKey="Martin Algarra, S" uniqKey="Martin Algarra S">S Martín-Algarra</name>
</author>
<author><name sortKey="Ribba, B" uniqKey="Ribba B">B Ribba</name>
</author>
<author><name sortKey="Troc Niz, If" uniqKey="Troc Niz I">IF Trocóniz</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Fizazi, K" uniqKey="Fizazi K">K Fizazi</name>
</author>
<author><name sortKey="Cojean, I" uniqKey="Cojean I">I Cojean</name>
</author>
<author><name sortKey="Pignon, Jp" uniqKey="Pignon J">JP Pignon</name>
</author>
<author><name sortKey="Rixe, O" uniqKey="Rixe O">O Rixe</name>
</author>
<author><name sortKey="Gatineau, M" uniqKey="Gatineau M">M Gatineau</name>
</author>
<author><name sortKey="Hadef, S" uniqKey="Hadef S">S Hadef</name>
</author>
<author><name sortKey="Arriagada, R" uniqKey="Arriagada R">R Arriagada</name>
</author>
<author><name sortKey="Baldeyrou, P" uniqKey="Baldeyrou P">P Baldeyrou</name>
</author>
<author><name sortKey="Comoy, E" uniqKey="Comoy E">E Comoy</name>
</author>
<author><name sortKey="Le Chevalier, T" uniqKey="Le Chevalier T">T Le Chevalier</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Liu, X" uniqKey="Liu X">X Liu</name>
</author>
<author><name sortKey="Zhang, W" uniqKey="Zhang W">W Zhang</name>
</author>
<author><name sortKey="Yin, W" uniqKey="Yin W">W Yin</name>
</author>
<author><name sortKey="Xiao, Y" uniqKey="Xiao Y">Y Xiao</name>
</author>
<author><name sortKey="Zhou, C" uniqKey="Zhou C">C Zhou</name>
</author>
<author><name sortKey="Hu, Y" uniqKey="Hu Y">Y Hu</name>
</author>
<author><name sortKey="Geng, S" uniqKey="Geng S">S Geng</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Liu, S" uniqKey="Liu S">S Liu</name>
</author>
<author><name sortKey="Cai, X" uniqKey="Cai X">X Cai</name>
</author>
<author><name sortKey="Xia, L" uniqKey="Xia L">L Xia</name>
</author>
<author><name sortKey="Jiang, C" uniqKey="Jiang C">C Jiang</name>
</author>
<author><name sortKey="Chen, P" uniqKey="Chen P">P Chen</name>
</author>
<author><name sortKey="Wang, X" uniqKey="Wang X">X Wang</name>
</author>
<author><name sortKey="Zhang, B" uniqKey="Zhang B">B Zhang</name>
</author>
<author><name sortKey="Zhao, Hy" uniqKey="Zhao H">HY Zhao</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Liu, X" uniqKey="Liu X">X Liu</name>
</author>
<author><name sortKey="Lv, Xb" uniqKey="Lv X">XB Lv</name>
</author>
<author><name sortKey="Wang, Xp" uniqKey="Wang X">XP Wang</name>
</author>
<author><name sortKey="Sang, Y" uniqKey="Sang Y">Y Sang</name>
</author>
<author><name sortKey="Xu, S" uniqKey="Xu S">S Xu</name>
</author>
<author><name sortKey="Hu, K" uniqKey="Hu K">K Hu</name>
</author>
<author><name sortKey="Wu, M" uniqKey="Wu M">M Wu</name>
</author>
<author><name sortKey="Liang, Y" uniqKey="Liang Y">Y Liang</name>
</author>
<author><name sortKey="Liu, P" uniqKey="Liu P">P Liu</name>
</author>
<author><name sortKey="Tang, J" uniqKey="Tang J">J Tang</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Lv, Xb" uniqKey="Lv X">XB Lv</name>
</author>
<author><name sortKey="Jiao, Y" uniqKey="Jiao Y">Y Jiao</name>
</author>
<author><name sortKey="Qing, Y" uniqKey="Qing Y">Y Qing</name>
</author>
<author><name sortKey="Hu, H" uniqKey="Hu H">H Hu</name>
</author>
<author><name sortKey="Cui, X" uniqKey="Cui X">X Cui</name>
</author>
<author><name sortKey="Lin, T" uniqKey="Lin T">T Lin</name>
</author>
<author><name sortKey="Song, E" uniqKey="Song E">E Song</name>
</author>
<author><name sortKey="Yu, F" uniqKey="Yu F">F Yu</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Yan, Hj" uniqKey="Yan H">HJ Yan</name>
</author>
<author><name sortKey="Tan, Y" uniqKey="Tan Y">Y Tan</name>
</author>
<author><name sortKey="Gu, W" uniqKey="Gu W">W Gu</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Proshchina, Ae" uniqKey="Proshchina A">AE Proshchina</name>
</author>
<author><name sortKey="Krivova, Ys" uniqKey="Krivova Y">YS Krivova</name>
</author>
<author><name sortKey="Barabanov, Vm" uniqKey="Barabanov V">VM Barabanov</name>
</author>
<author><name sortKey="Saveliev, Sv" uniqKey="Saveliev S">SV Saveliev</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Tang, D" uniqKey="Tang D">D Tang</name>
</author>
<author><name sortKey="Wang, M" uniqKey="Wang M">M Wang</name>
</author>
<author><name sortKey="Sui, A" uniqKey="Sui A">A Sui</name>
</author>
<author><name sortKey="Wang, Y" uniqKey="Wang Y">Y Wang</name>
</author>
<author><name sortKey="Yang, R" uniqKey="Yang R">R Yang</name>
</author>
<author><name sortKey="Wang, Z" uniqKey="Wang Z">Z Wang</name>
</author>
<author><name sortKey="Zhao, Y" uniqKey="Zhao Y">Y Zhao</name>
</author>
<author><name sortKey="Jiao, W" uniqKey="Jiao W">W Jiao</name>
</author>
<author><name sortKey="Shen, Y" uniqKey="Shen Y">Y Shen</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Jang, Sm" uniqKey="Jang S">SM Jang</name>
</author>
<author><name sortKey="Kim, Jw" uniqKey="Kim J">JW Kim</name>
</author>
<author><name sortKey="Kim, Ch" uniqKey="Kim C">CH Kim</name>
</author>
<author><name sortKey="Kim, D" uniqKey="Kim D">D Kim</name>
</author>
<author><name sortKey="Rhee, S" uniqKey="Rhee S">S Rhee</name>
</author>
<author><name sortKey="Choi, Kh" uniqKey="Choi K">KH Choi</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Gronowitz, Js" uniqKey="Gronowitz J">JS Gronowitz</name>
</author>
<author><name sortKey="Bergstrom, R" uniqKey="Bergstrom R">R Bergström</name>
</author>
<author><name sortKey="Nou, E" uniqKey="Nou E">E Nôu</name>
</author>
<author><name sortKey="P Hlman, S" uniqKey="P Hlman S">S Påhlman</name>
</author>
<author><name sortKey="Brodin, O" uniqKey="Brodin O">O Brodin</name>
</author>
<author><name sortKey="Nilsson, S" uniqKey="Nilsson S">S Nilsson</name>
</author>
<author><name sortKey="K Llander, Cf" uniqKey="K Llander C">CF Källander</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Jett, Jr" uniqKey="Jett J">JR Jett</name>
</author>
<author><name sortKey="Schild, Se" uniqKey="Schild S">SE Schild</name>
</author>
<author><name sortKey="Kesler, Ka" uniqKey="Kesler K">KA Kesler</name>
</author>
<author><name sortKey="Kalemkerian, Gp" uniqKey="Kalemkerian G">GP Kalemkerian</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Hanahan, D" uniqKey="Hanahan D">D Hanahan</name>
</author>
<author><name sortKey="Weinberg, Ra" uniqKey="Weinberg R">RA Weinberg</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Lurje, G" uniqKey="Lurje G">G Lurje</name>
</author>
<author><name sortKey="Zhang, W" uniqKey="Zhang W">W Zhang</name>
</author>
<author><name sortKey="Schultheis, Am" uniqKey="Schultheis A">AM Schultheis</name>
</author>
<author><name sortKey="Yang, D" uniqKey="Yang D">D Yang</name>
</author>
<author><name sortKey="Groshen, S" uniqKey="Groshen S">S Groshen</name>
</author>
<author><name sortKey="Hendifar, Ae" uniqKey="Hendifar A">AE Hendifar</name>
</author>
<author><name sortKey="Husain, H" uniqKey="Husain H">H Husain</name>
</author>
<author><name sortKey="Gordon, Ma" uniqKey="Gordon M">MA Gordon</name>
</author>
<author><name sortKey="Nagashima, F" uniqKey="Nagashima F">F Nagashima</name>
</author>
<author><name sortKey="Chang, Hm" uniqKey="Chang H">HM Chang</name>
</author>
<author><name sortKey="Lenz, Hj" uniqKey="Lenz H">HJ Lenz</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Ustuner, Z" uniqKey="Ustuner Z">Z Ustuner</name>
</author>
<author><name sortKey="Saip, P" uniqKey="Saip P">P Saip</name>
</author>
<author><name sortKey="Yasasever, V" uniqKey="Yasasever V">V Yasasever</name>
</author>
<author><name sortKey="Vural, B" uniqKey="Vural B">B Vural</name>
</author>
<author><name sortKey="Yazar, A" uniqKey="Yazar A">A Yazar</name>
</author>
<author><name sortKey="Bal, C" uniqKey="Bal C">C Bal</name>
</author>
<author><name sortKey="Ozturk, B" uniqKey="Ozturk B">B Ozturk</name>
</author>
<author><name sortKey="Ozbek, U" uniqKey="Ozbek U">U Ozbek</name>
</author>
<author><name sortKey="Topuz, E" uniqKey="Topuz E">E Topuz</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Berx, G" uniqKey="Berx G">G Berx</name>
</author>
<author><name sortKey="Van Roy, F" uniqKey="Van Roy F">F van Roy</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Li, Li" uniqKey="Li L">LI Li</name>
</author>
<author><name sortKey="Lv, Y" uniqKey="Lv Y">Y Lv</name>
</author>
<author><name sortKey="Zhang, Y" uniqKey="Zhang Y">Y Zhang</name>
</author>
<author><name sortKey="He, L" uniqKey="He L">L He</name>
</author>
<author><name sortKey="Zhang, H" uniqKey="Zhang H">H Zhang</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Carotenuto, M" uniqKey="Carotenuto M">M Carotenuto</name>
</author>
<author><name sortKey="De Antonellis, P" uniqKey="De Antonellis P">P de Antonellis</name>
</author>
<author><name sortKey="Chiarolla, Cm" uniqKey="Chiarolla C">CM Chiarolla</name>
</author>
<author><name sortKey="Attanasio, C" uniqKey="Attanasio C">C Attanasio</name>
</author>
<author><name sortKey="Damiani, V" uniqKey="Damiani V">V Damiani</name>
</author>
<author><name sortKey="Boffa, I" uniqKey="Boffa I">I Boffa</name>
</author>
<author><name sortKey="Aiese, N" uniqKey="Aiese N">N Aiese</name>
</author>
<author><name sortKey="Pedone, E" uniqKey="Pedone E">E Pedone</name>
</author>
<author><name sortKey="Accordi, B" uniqKey="Accordi B">B Accordi</name>
</author>
<author><name sortKey="Basso, G" uniqKey="Basso G">G Basso</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Esposito, S" uniqKey="Esposito S">S Esposito</name>
</author>
<author><name sortKey="Russo, Mv" uniqKey="Russo M">MV Russo</name>
</author>
<author><name sortKey="Airoldi, I" uniqKey="Airoldi I">I Airoldi</name>
</author>
<author><name sortKey="Tupone, Mg" uniqKey="Tupone M">MG Tupone</name>
</author>
<author><name sortKey="Sorrentino, C" uniqKey="Sorrentino C">C Sorrentino</name>
</author>
<author><name sortKey="Barbarito, G" uniqKey="Barbarito G">G Barbarito</name>
</author>
<author><name sortKey="Di Meo, S" uniqKey="Di Meo S">S Di Meo</name>
</author>
<author><name sortKey="Di Carlo, E" uniqKey="Di Carlo E">E Di Carlo</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Huang, Cs" uniqKey="Huang C">CS Huang</name>
</author>
<author><name sortKey="Shih, Mk" uniqKey="Shih M">MK Shih</name>
</author>
<author><name sortKey="Chuang, Ch" uniqKey="Chuang C">CH Chuang</name>
</author>
<author><name sortKey="Hu, Ml" uniqKey="Hu M">ML Hu</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Kim, Yi" uniqKey="Kim Y">YI Kim</name>
</author>
<author><name sortKey="Park, S" uniqKey="Park S">S Park</name>
</author>
<author><name sortKey="Jeoung, Di" uniqKey="Jeoung D">DI Jeoung</name>
</author>
<author><name sortKey="Lee, H" uniqKey="Lee H">H Lee</name>
</author>
</analytic>
</biblStruct>
</listBibl>
</div1>
</back>
</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Oncol Lett</journal-id>
<journal-id journal-id-type="iso-abbrev">Oncol Lett</journal-id>
<journal-id journal-id-type="publisher-id">OL</journal-id>
<journal-title-group><journal-title>Oncology Letters</journal-title>
</journal-title-group>
<issn pub-type="ppub">1792-1074</issn>
<issn pub-type="epub">1792-1082</issn>
<publisher><publisher-name>D.A. Spandidos</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31611991</article-id>
<article-id pub-id-type="pmc">6781773</article-id>
<article-id pub-id-type="doi">10.3892/ol.2019.10797</article-id>
<article-id pub-id-type="publisher-id">OL-0-0-10797</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Articles</subject>
</subj-group>
</article-categories>
<title-group><article-title>Knockdown of neuron-specific enolase suppresses the proliferation and migration of NCI-H209 cells</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Liu</surname>
<given-names>Xia</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10797">1</xref>
<xref rid="fn1-ol-0-0-10797" ref-type="author-notes">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Liu</surname>
<given-names>Shousheng</given-names>
</name>
<xref ref-type="aff" rid="af2-ol-0-0-10797">2</xref>
<xref ref-type="aff" rid="af3-ol-0-0-10797">3</xref>
<xref rid="fn1-ol-0-0-10797" ref-type="author-notes">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fu</surname>
<given-names>Juan</given-names>
</name>
<xref ref-type="aff" rid="af2-ol-0-0-10797">2</xref>
<xref ref-type="aff" rid="af4-ol-0-0-10797">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Huang</surname>
<given-names>Jinsheng</given-names>
</name>
<xref ref-type="aff" rid="af2-ol-0-0-10797">2</xref>
<xref ref-type="aff" rid="af3-ol-0-0-10797">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Weng</surname>
<given-names>Chengyin</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10797">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fang</surname>
<given-names>Xisheng</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10797">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Guan</surname>
<given-names>Mingmei</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10797">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wu</surname>
<given-names>Yong</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10797">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Yang</surname>
<given-names>Lin</given-names>
</name>
<xref ref-type="aff" rid="af5-ol-0-0-10797">5</xref>
<xref rid="c2-ol-0-0-10797" ref-type="corresp"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Liu</surname>
<given-names>Guolong</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10797">1</xref>
<xref rid="c1-ol-0-0-10797" ref-type="corresp"></xref>
</contrib>
</contrib-group>
<aff id="af1-ol-0-0-10797"><label>1</label>
Department of Medical Oncology, Guangzhou First People's Hospital, School of Medicine, South China University of Technology, Guangzhou, Guangdong 510180, P.R. China</aff>
<aff id="af2-ol-0-0-10797"><label>2</label>
State Key Laboratory of Oncology in South China, Collaborative Innovation Centre for Cancer Medicine, Guangzhou, Guangdong 510060, P.R. China</aff>
<aff id="af3-ol-0-0-10797"><label>3</label>
Department of General Medicine, Sun Yat-Sen University Cancer Center, Guangzhou, Guangdong 510060, P.R. China</aff>
<aff id="af4-ol-0-0-10797"><label>4</label>
Department of Ultrasonography, Sun Yat-Sen University Cancer Center, Guangzhou, Guangdong 510060, P.R. China</aff>
<aff id="af5-ol-0-0-10797"><label>5</label>
Department of Radiation Oncology, Nanfang Hospital, Southern Medical University, Guangzhou, Guangdong 510515, P.R. China</aff>
<author-notes><corresp id="c1-ol-0-0-10797"><italic>Correspondence to</italic>
: Dr Guolong Liu, Department of Medical Oncology, Guangzhou First People's Hospital, School of Medicine, South China University of Technology, 1 Panfu Road, Guangzhou, Guangdong 510180, P.R. China, E-mail: <email>eyglliu@scut.edu.cn</email>
</corresp>
<corresp id="c2-ol-0-0-10797">Dr Lin Yang, Department of Radiation Oncology, Nanfang Hospital, Southern Medical University, 1838 Guangzhou Avenue North, Guangzhou, Guangdong 510515, P.R. China, E-mail: <email>yanglin1nfyy@smu.edu.cn</email>
</corresp>
<fn id="fn1-ol-0-0-10797"><label>*</label>
<p>Contributed equally</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><month>11</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="epub"><day>04</day>
<month>9</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>04</day>
<month>9</month>
<year>2019</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the . </pmc-comment>
<volume>18</volume>
<issue>5</issue>
<fpage>4809</fpage>
<lpage>4815</lpage>
<history><date date-type="received"><day>16</day>
<month>1</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>26</day>
<month>7</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>Copyright: © Liu et al.</copyright-statement>
<copyright-year>2019</copyright-year>
<license license-type="open-access"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by-nc-nd/4.0/">Creative Commons Attribution-NonCommercial-NoDerivs License</ext-link>
, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.</license-p>
</license>
</permissions>
<abstract><p>Neuron-specific enolase (NSE) is generally considered as a marker for diagnosis and evaluation of the response to therapy in small cell lung cancer (SCLC). However, the role of NSE in the progression of SCLC remains to be elucidated. In the present study, the functions of NSE in SCLC, in addition to the potential mechanisms, were investigated using a loss-of-function approach with NSE-targeting small interfering (si)RNA. The knockdown of NSE markedly decreased the proliferation of NCI-H209 cells, as indicated by MTT assay (P<0.05). Furthermore, the silencing of NSE resulted in the formation of smaller and fewer colonies compared with that in the control group (P<0.001). Flow cytometric analysis indicated that the silencing of NSE resulted in a decreased S-phase population among NCI-H209 cells (P<0.05). Transwell assay demonstrated that the silencing of NSE suppressed the migration of NCI-H209 cells (P<0.001). NCI-H209 cells transfected with NSE siRNA-1 or negative control were collected and the protein levels of metastasis-associated genes were detected using western blot analysis. The results indicated that the knockdown of NSE led to downregulation of the pro-metastatic gene vascular endothelial growth factor (VEGF; P<0.05) and the upregulation of metastasis suppressor genes NM23 and E-cadherin (P<0.05). Taken together, the results of the present study demonstrated that the silencing of NSE suppressed the migration, proliferation and colony formation ability of SCLC cells and decreased the S-phase population. In addition, the knockdown of NSE resulted in the upregulation of E-cadherin and NM23 and the downregulation of VEGF. Collectively, these results indicated that intracellular NSE may have an important role in the progression of SCLC.</p>
</abstract>
<kwd-group><kwd>small cell lung cancer</kwd>
<kwd>neuron-specific enolase</kwd>
<kwd>proliferation</kwd>
<kwd>migration</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="f1-ol-0-0-10797" orientation="portrait" position="float"><label>Figure 1.</label>
<caption><p>Silencing NSE represses cell proliferation and colony formation. (A) Evaluation of the expression of NSE in small cell lung cancer cell lines using western blot analysis compared with GAPDH. (B) Silencing efficiency of NSE by siRNAs was evaluated using western blotting. (C) Silencing of NSE suppressed the proliferation of NCI-H209 cells, as determined using an MTT assay. *P<0.05 vs. control at the corresponding time points. (D) Silencing of NSE reduced the colony formation of NCI-H209 cells. *P<0.05 and **P<0.001 vs. control. NSE, neuron-specific enolase; siRNA, small interfering RNA; NC, negative control; OD, optical density.</p>
</caption>
<graphic xlink:href="ol-18-05-4809-g00"></graphic>
</fig>
<fig id="f2-ol-0-0-10797" orientation="portrait" position="float"><label>Figure 2.</label>
<caption><p>Silencing of NSE reduces the S-phase population of NCI-H209 cells. NCI-H209 cells transfected with NSE siRNA-1 or NC for 48 h were collected and the cell cycle profile was analyzed using flow cytometry. *P<0.05 compared with the NC group. NSE, neuron-specific enolase; siRNA, small interfering RNA; NC, negative control.</p>
</caption>
<graphic xlink:href="ol-18-05-4809-g01"></graphic>
</fig>
<fig id="f3-ol-0-0-10797" orientation="portrait" position="float"><label>Figure 3.</label>
<caption><p>Silencing of NSE suppresses the migration of NCI-H209 cells. (A) NCI-H209 cells transfected with NSE siRNA-1 or NC for 48 h were collected and subjected to a Transwell assay under a microscope. Magnification, ×100. (B) NCI-H209 cells transfected with NSE siRNA-1 or NC for 48 h were collected and the protein levels were detected using western blot analysis. *P<0.05 and **P<0.001 compared with the NC group. NSE, neuron-specific enolase; siRNA, small interfering RNA; NC, negative control; E-cad, E-cadherin; VEGF, vascular endothelial growth factor.</p>
</caption>
<graphic xlink:href="ol-18-05-4809-g02"></graphic>
</fig>
</floats-group>
</pmc>
</record>
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