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C14orf159 Suppresses Gastric Cancer Cells' Invasion and Proliferation By Journal name: Cancer Management and Research Article Designation: Original Research Year: 2019 Volume: 11 Cancer Management and Research Dovepress Running head verso: Zhu et al Running head recto: Zhu et al open access to scientific and medical research DOI: http://dx.doi.org/10.2147/CMAR.S176771 Open Access Full Text Article ORIGINAL RESEARCH C14orf159 suppresses gastric cancer cells’ invasion and proliferation by inactivating ERK signaling Yan-Mei Zhu1 Background: C14orf159, a new protein, has been identified recently. But its expression in Qiang Li1 tissues and clinicopathologic correlation is still unknown. Xiao-Zhuo Gao1 Patients and methods: We carried out immunohistochemistry staining in 144 gastric cancer Xiao Meng1 cases in this study. Then Western blot was used to detect the expression of protein. MTT and Li-Li Sun1 matrigel invasion assay were used to assess the biological effects. The immunohistochemical results indicated that the expression of C14orf159 in normal Yu Shi2 Results: gastric mucosa close to cancer tissue was remarkably higher than that in stomach carcinoma En-Tian Lu3 samples (63.9% and 34.7%, respectively, P<0.001). Negative C14orf159 expression was dramati- Yong Zhang1 cally related to high TNM stages (P=0.033) and positive lymph node metastasis (P=0.008). Once 1Department of Pathology, Cancer C14orf159 was overexpressed, the expression levels of phosphorylated ERK and its regulated Hospital of China Medical University, downstream molecules, such as Snail, phosphorylated P90RSK and Cyclin D1, were decreased, Liaoning Cancer Hospital and Institute, Shenyang, Liaoning 110042, while the expression level of E-cadherin was increased. Finally, the invasion and proliferation P.R. China; 2Department of Pathology, capacity of gastric cancer cells was inhibited. People’s Hospital of Dawa District, Panjin, Liaoning 124200, P.R. China; Conclusion: In other words, loss of C14orf159 is associated with the progression of gastric cancer. 3Department of Pathology, Central The role of C14orf159 in repression of proliferation and invasion may be due to resuming E-cadherin Hospital of Pulandian District, Dalian, and abolishing Snail and Cyclin D1 expression through inactivating ERK–P90RSK pathway. Liaoning 116200, P.R. China Keywords: C14orf159, gastric cancer, ERK, invasion, proliferation Introduction Gastric cancer is one of the most common malignant tumors in the world that ranks fourth among men and fifth among women. It is the main reason of carcinoma-related deaths globally.1 It is often found in the late clinical stages and the prognosis is not good.2 The molecular mechanisms indicating occurrence and development of gastric carcinoma have not been elaborated thoroughly so far. Therefore, it is very important to seek for new therapeutic targets for controlling gastric carcinoma progression. C14orf159 is a newly identified protein, which comprises 661 amino acids. C14orf159 is a D-glutamate cyclase that converts D-glutamate to 5-oxo-D-proline and relates to the chemical reactions and pathways involving glutamate, the anion of Correspondence: Yong Zhang 2-aminopentanedioic acid. It is localized in the matrix of mitochondria.3 At present, Department of Pathology, Cancer Hospital of China Medical University, there is no literature on the expression pattern and clinicopathologic relevance of Liaoning Cancer Hospital and Institute, C14orf159 in human tissues, particularly in malignant tumors. No. 44 Xiaoheyan Road, Dadong District, For the purpose of exploring the effect of C14orf159 on the progression of gastric Shenyang City 110042, Liaoning Province, P.R. China cancer, we explored the expression of C14orf159 in both gastric carcinoma samples Tel +86 133 5245 6072 and cell lines and analyzed their clinicopathologic correlation. In addition, we analyzed Email zhangyong@cancerhosp-ln-cmu. com the influences of C14orf159 on the proliferation and invasiveness of gastric cancer submit your manuscript | www.dovepress.com Cancer Management and Research 2019:11 1717–1723 1717 Dovepress © 2019 Zhu et al. This work is published and licensed by Dove Medical Press Limited. The full terms of this license are available at https://www.dovepress.com/terms. php and incorporate the Creative Commons Attribution – Non Commercial (unported, v3.0) License (http://creativecommons.org/licenses/by-nc/3.0/). By accessing the work http://dx.doi.org/10.2147/CMAR.S176771 you hereby accept the Terms. Non-commercial uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed. For permission for commercial use of this work, please see paragraphs 4.2 and 5 of our Terms (https://www.dovepress.com/terms.php). Zhu et al Dovepress cell lines after C14orf159 knock-in or knock-down. Our find- same quantity of protein (30 µg per lane) was separated by ings revealed that C14orf159 might become a new potential 10% SDS-PAGE. The proteins were incubated with primary therapeutic target of gastric cancer. antibodies overnight at 4°C against C14orf159 and GAPDH (1:200 and 1:3,000; Sigma-Aldrich Co.), p-ERK, ERK, Patients and methods p-P90RSK, P90RSK, p-P38, P38, p-P65, P65, p-AKT, AKT, Patients and clinical specimens Cyclin A2, Cyclin B1, Cyclin D1, Myc-tag, Vimentin, Snail, Gastric cancer specimens were obtained from 118 males Slug (1:1,000; BD Transduction Laboratories, Lexington, KY, and 26 females (totally 144 patients). The average age of USA), E-cadherin, N-cadherin, Zo-1 and Occludin (1:1,000; the patients was 60 years (from 32 to 78 years). They were Cell Signaling Technology, Danvers, MA, USA). After incu- diagnosed with gastric adenocarcinoma and underwent major bating with anti-mouse or anti-rabbit IgG (BD Transduction gastrectomy in the Cancer Hospital of China Medical Univer- Laboratories) at 37°C for 2 hours, the membranes were devel- sity from 2012 to 2017. None of them adopted other treatments oped with enhanced chemiluminescence reagent (Solarbio). such as chemotherapy or radiotherapy before surgery. H&E- stained sections were made, and each section was diagnosed Plasmid transfection and siRNA by two pathologists with extensive diagnostic experience in Plasmids pCMV6-ddk-myc-C14orf159 (RC223847) and line with the WHO classification of digestive system tumors. pCMV6-ddk-myc were bought from Origene (Rockville, Lymph node metastasis was found in 43 of the 144 patients. MD, USA). C14orf159-siRNA (sc-92378) and NC-siRNA The samples were divided into two groups, stage I (n=62) and (sc-37007) were purchased from Santa Cruz Biotechnology stage II–III (n=82), on the basis of the p-TNM staging system (Dallas, TX, USA). Lipofectamine 3000 reagent (Thermo of the International Anti-Cancer Alliance (eighth edition). We Fisher Scientific, Waltham, MA, USA) was used to transfect have obtained written informed consent for this study from as we described previously.7 patients and ethical approval in accordance with the Declara- tion of Helsinki from the local trials committee of the Cancer MTT assay Hospital of China Medical University. To perform the MTT assay, we plated cells of gastric cancer cell lines in 96-well plates. Cell number was about 4,000 Immunohistochemistry (IHC) cells per well. After 24 hours, transfection was carried out. Streptavidin-peroxidase method was manipulated as Cells were stained after 4 days to quantitate cell viability as described previously.4 The slices were incubated overnight we performed earlier.7 at 4°C with a monoclonal mouse anti-C14orf159 antibody (1:100; Sigma-Aldrich Co., St Louis, MO, USA). After Matrigel invasion assay that, they were incubated with the secondary antibody at Transwell chamber, 24-well, 8 µm pore membranes (Corning room temperature. To assess the sections, semi-quantitative Incorporated, Corning, NY, USA), was used to carry out cell scoring method was used by two pathologists with extensive invasion assays as we described previously.8 diagnostic experience, but they were blinded to the clinical information. Staining intensity and percentage of stained Statistical analysis cells were considered as described previously.5 A score ≥4 SPSS (v 20.0) was used for statistical analysis. P-value <0.05 was regarded as positive C14orf159 expression. was considered statistically significant. Cell culture Results The SGC-7901, BGC-823, MGC80-3 and HGC-27 cell lines The expression of C14orf159 in gastric were bought from the Chinese Academy of Sciences Cell cancer tissues and cell lines Bank (Beijing, P.R. China) and were maintained in recom- First, IHC was carried out in 144 cases of gastric carcinoma mended growth medium. and the corresponding normal tissues to access the expression and subcellular localization of C14orf159. The results indi- Western blotting cated that C14orf159 was strongly expressed in the cytoplasm Total protein was obtained by a RIPA buffer (Beyotime, of normal stomach tissue (Figure 1A); however, it was dimly Shanghai, P.R. China) and quantified with bicinchoninic expressed in the cytoplasm of gastric carcinoma specimens acid protein assay kit (Solarbio, Shanghai, P.R. China).6 The (Figure 1B). The positive expression rate of C14orf159 in 1718 submit your manuscript | www.dovepress.com Cancer Management and Research 2019:11 Dovepress Dovepress Zhu et al AB CD s NoncancerouStomach tissueMGC80-3 SGC-7901 BGC-823 HGC-27 C14orf159 GAPDH Figure 1 The expression of C14orf159 in both gastric cancer specimens and cell lines. Notes: C14orf159 revealed strong cytosolic expression in noncancerous stomach tissues (A, 200×); however, it showed dim expression in the cytoplasm of gastric carcinoma specimens (B, 200×). In some gastric cancer tissues, it was positively expressed (C, 200×). (D) C14orf159 was expressed in noncancerous stomach tissue and all four gastric cancer cells (MGC80-3, SGC-7901, BGC-823 and HGC-27), highly expressed in 7901 cells and less expressed in 803 cells. Data are mean ± SEM from three independent experiments. Abbreviation: SEM, standard error of the mean. gastric cancer samples was significantly lower than that in thelial–mesenchymal transition–related proteins and found noncancerous samples (34.7%, 50/144 vs 63.9%, 92/144; that Snail expression level was downregulated; at the same P<0.001).
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