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RRS1 Gene Expression Involved in the Progression of Papillary Thyroid

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RRS1 Gene Expression Involved in the Progression of Papillary Thyroid Chen et al. Cancer Cell Int (2018) 18:20 https://doi.org/10.1186/s12935-018-0519-x Cancer Cell International PRIMARY RESEARCH Open Access RRS1 gene expression involved in the progression of papillary thyroid carcinoma Feng Chen1,2, Yaqiong Jin1,3, Lin Feng4, Jie Zhang2, Jun Tai2, Jin Shi1,2, Yongbo Yu1,3, Jie Lu1,3, Shengcai Wang2, Xin Li5, Ping Chu1,3, Shujing Han1,3, Shujun Cheng4, Yongli Guo1,3 and Xin Ni1,2,3* Abstract Background: Papillary thyroid carcinoma (PTC) is one of the most frequent malignancies of the endocrine system, whose mechanisms of pathogenesis, progression and prognosis are still far from being clearly elucidated. Despite an increasing body of evidences highlights ribosome biogenesis regulator homolog (RRS1) as a ribosome biogenesis protein in yeast and plants, little is known about human RRS1 function. Methods: Proliferation, cell cycle and apoptosis of PTC cells were assessed following the knockdown of RRS1 expression though MTT, colony formation assay, and fow cytometry. Then, transcriptome profling was conducted to explore pathway changes after RRS1 silencing in PTC cells. Receiver operating characteristic curve and Youden’s index were performed in twenty-four thyroid carcinoma samples to assess their potential clinical diagnostic value. Results: Firstly, we found that silencing RRS1 signifcantly reduced cell proliferation, inhibited cell cycle, and pro- moted apoptosis in PTC cell line. The result also showed that knock-down of RRS1 could up-regulate genes involving apoptosis and metabolism, while, down-regulate genes relative to cell proliferation and blood vessel development. Notably, the present study confrmed the diagnostic value of RRS1 for thyroid carcinoma in both children and adults. Conclusions: In conclusion, these data aford a comprehensive view of a novel function of human RRS1 by promot- ing cell proliferation and could be a potential indicator for papillary thyroid carcinoma. Keywords: Papillary thyroid carcinoma, RRS1, Cancer progression Background such as follicular thyroid cancer, medullary thyroid can- Tyroid cancer is the most common endocrine cancer cer, and anaplastic thyroid carcinoma, are rare in young [1]. Te incidence of thyroid cancer is increasing faster patients [6]. Although eforts have been done in tumo- than any other cancer in China, with expected 90,000 rigenesis, little is known about PTC. Tis type of tumor patients to be diagnosed in 2015 [2]. Tyroid cancer occurs mostly in women; sex hormones may play a role mainly comprises diferentiated thyroid cancer (DTC) in the pathogenesis [7]. In children, especially in those and medullary thyroid cancer (MTC). Terein, a large under 5 years old, the major risk factor for developing proportion (78–90%) of DTC is papillary thyroid carci- PTC is radiation exposure [6, 8]. Although PTC has a noma (PTC) in adults [3, 4]. Similar with adults cases, favorable prognosis, certain cases exhibit aggressive PTC accounts for 90% or more of thyroid cancer cases clinical characteristics, such as lymph node and distance in childhood [5]. However, other types of thyroid cancer, metastasis, and poorer prognosis. Once regional nodal metastases or aerodigestive invasion is discovered, radi- oiodine may be employed [3]. Radioiodine treatment *Correspondence: [email protected] 2 Department of Otolaryngology, Head and Neck Surgery, Beijing can signifcantly increase event-free survival of PTC Children’s Hospital, Capital Medical University, National Center patients. Lower dose of radioiodine applied in therapy for Children’s Health, No.56 Nanlishi Rd., Beijing 100045, China do not afect patients’ daily life. However, patients with Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Chen et al. Cancer Cell Int (2018) 18:20 Page 2 of 12 distance metastases, under radioactive iodine treatment and thyroid carcinoma progression. Our results support a (≥ 150 mCi), are at risk for poor life quality due to physi- novel function of RRS1 by promoting thyroid carcinoma cal pain, lower vitality, bad mental health, and physi- cells proliferation, which could be a potential indicator of cal/emotional problems [9]. Terefore, development PTC in both children and adults. of prognostic factors is important to early diagnosis of PTC, following establishment of therapeutic strategies. Methods and patients Many laboratory and clinical studies have been carried Cell lines and culture out for investigation of new markers to predict prognos- Human papillary thyroid carcinoma cell line TPC-1 was tic of PTC. For instance, clinical markers, such as extra obtain from American Type Culture Collection. Cells thyroidal extension and lymph node metastasis (LNM), were seeded in DMEM (Gibico) with 10% fetal bovine have been widely used to characterize persistent/recur- serum (Life Technologies, Inc., Gaithersburg, MD), rent PTC at initial diagnosis. 100 mg/ml streptomycin and 100 units/ml penicillin [20]. Beside clinical indicators, molecular markers are also Cells were grown at 37 °C under 5% CO2. Te TPC-1 cells very important in prognosis of PTC. In this regard, the had been tested within 3 months before the conduction expression of galectin-3, thyroid peroxidase and keratin of this study for morphologic features of thyroid carci- 19 are all widely used in diagnosis of PTC for adults [10]. noma cells by GENECHEM co. (Shanghai, China). However, these indicators are lack of evaluation in pedi- atric PTC samples. Several studies had showed diferent Real-time PCR molecular mechanism of PTC tumorigenesis in children Total RNA was isolated with Trizol reagent (Invitro- and adults. For instance, 2015 American Tyroid Asso- gen) according to the manufacturer’s protocol for total ciation (ATA) Management guidelines for children points RNA isolation. And then the RNA (2 μg) was subjected out that BRAF mutations are the most common abnor- to reverse transcription by using M-MuLV reverse tran- mality in adult PTC (36–83%) [6], but rare in children scriptase (Fermentas). Real-time PCR amplifcation PTC. In contrast, RET/PTC rearrangements are more was performed using primers pairs for RRS1: (sense) common in PTC from children than that in adults (45% 5′-CCCTACCGGACACCAGAGTAA-3′, (anti-sense) vs. 35%) [6, 11, 12]. Nonetheless, the clinical applications 5′-CCGAAAAGGGGTTGAAACTTCC-3′; GAPDH: of these molecular markers are still limited due to low (sense) 5′-TGACTTCAACAGCGACACCCA-3′, (anti- sensitivity and specifcity [13]. Terefore, hypersensitive sense) 5′-CACCCTGTTGCTGTAGCCAAA-3′. And and specifc diagnostic test for both children and adults real-time PCR was performed using a SYBR Green/Flu- are needed to be developed. orescein PCR master mix (Applied Biosystems) with a RRS1 was found as a regulatory protein for ribosome thermal profle of 95 °C for 5 min followed by 40 cycles of biogenesis in yeast [14]. So far, the function of human 94 °C for 20 s, 60 °C for 1 min. PCR reactions in triplicate RRS1 is far from fully understood. Gambe et al. found were carried out by using an ABI ViiA7™ Real-time PCR that RRS1 protein contributed to chromosome con- system (Life Technology). gression in HeLa cells [15]. Moreover, Carnemolla et al. reported that RRS1 involved in ER stress which was the Western blotting early event of Huntington disease [16]. However, the role Equal amounts (30 μg) of the total protein of the cells of human RRS1 in cancer is still unknown. Rapid cell pro- were subjected to 10% SDS-PAGE, blotted onto nitro- liferation is a biological feature of cancer, which accom- cellulose membranes (Pall Life Sciences). Membranes panies with enlarged nucleolus. Te available evidences were then blocked at room temperature for 1 h and indicate that the nucleolar changes in morphology or probed with specifc antibodies (1:1000 to 1:10,000) for function are the consequence of increased demand for RRS1 (ab117846, abcam) and GAPDH (sc-32233, Santa- ribosome biogenesis. PTC has several signifcant altera- Cruz) at 4 °C for overnight. Te membranes were further tions which are observed both in the fne structure and probed with the secondary antibody, HRP-labeled goat in the number of nucleoli [17, 18]. Tese studies raise anti-rabbit IgG (sc-2004, Santa-Cruz) or goat anti-mouse the possibility of the interference of a ribosome biogen- IgG (sc-2005, Santa-Cruz). After the ECL chemilumines- esis thus inducing PTC pathogenesis. Consistent with its cence kit (Amersham Biosciences), bands were visualized function in yeast, human RRS1 ortholog was identifed by ChemiDoc XRS + (Bio-Rad). in a proteome analysis of nucleolar extracts [15, 19]. We thus assumed that RRS1 may play essential role in PTC Short hairpin RNA constructs and antibodies proliferation. For RRS1 short hairpin RNA (shRNA), second-genera- Here we presumed that dysregulation of RRS1 in thy- tion lentiviruses expressing shRNA-RRS1 and shRNA- roid cancer played an important role in cell proliferation Negative control (shRNA-NC) were used. Briefy, 293T Chen et al. Cancer Cell Int (2018) 18:20 Page 3 of 12 cells were transfected with pLSLPw, TRIPZ, and GIPZ bufer was added. Cells were analyzed by fow cytometry constructs along with packaging plasmids, pVSVG, and within 30 min of staining. pLV-CMV-delta 8.2 by using lipofectamine. Virus-con- taining supernatants were collected at 48 and 72 h, and Colony formation assay thyroid carcinoma cells were transduced in the presence Te efect of RRS1 knockdown on colony formation abil- of 8 mg/ml polybrene (Sigma). ity of the TPC1 cells was detect by plate colony forma- tion assay.
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