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Abstract

BACKGROUND:

Esophageal cancer is a common tumor with high mortality worldwide. In the present study, we aimed to investigate the prognostic significance and regulatory effects of miR-105 on cellular functions of esophageal cancer cells.

METHODS:

The expression level of miR-105 was analyzed in esophageal cancer tissues and cell lines by qRT-PCR. Survival analysis was carried out using the Kaplan-Meier and the prognostic significance of miR-105 was analyzed with Cox regression analysis. The effects of miR-105 on cell proliferation, migration, and invasion abilities were detected with cellular experiments.

RESULTS:

We found that miR-105 was significantly upregulated in esophageal cancer tissues and cell lines, compared with the control group, respectively. Moreover, overexpression of miR-105 was significantly associated with positive lymph node metastasis, advanced TNM stage, and poor overall survival. In addition, overexpression of miR-105 promoted cell proliferation, migration, and invasion in esophageal cancer cells, while downregulation of miR-105 suppressed these cellular behaviors.

CONCLUSION:

Our findings indicate that a higher level of miR-105 predicts poorer prognosis in esophageal cancer patients, and miR-105 can promote esophageal cancer cell proliferation, migration, and invasion.

Keywords

MicroRNA-105 esophageal cancer prognosis proliferation migration invasion

1. Introduction

Esophageal cancer is one of the most common types of cancer in the digestive system worldwide [1]. In China, it is the sixth most common malignant tumor and the fourth leading cause of cancer-related death nationwide [2]. What’s more, more than half of the global incidence of esophageal cancer is in China [3]. Despite diagnostic and therapeutic advancements in the past years, including surgery, chemotherapy, and radiotherapy, the prognosis of esophageal cancer patients has shown little improvement with the 5-year survival rate of approximately 20–40% [4, 5]. Esophageal cancer patients at early stages usually have no obvious symptoms, and a large proportion of patients are initially diagnosed at advanced stages with a 5-year survival rate of less than 20%, which seriously affected the quality of life of patients [6]. Therefore, identifying more effective therapeutic methods and novel prognostic molecular biomarkers are necessary for improving the patients’ survival rate [7].

MicroRNAs (miRNAs or miRs) are a group of small non-coding RNA molecules (approximately 22 nucleotides), and can negatively regulate gene expression at the post-transcriptional level by binding to 3’-UTRs of target genes [8, 9]. In recent years, numerous microRNAs have been demonstrated aberrantly expressed or mutated in human cancers that they acted as oncogenes or tumor suppressor genes by regulating multiple cellular processes, including cell proliferation, migration, and invasion [10, 11, 12]. In addition, many miRNAs also can be used as a novel molecular diagnostic/prognostic biomarkers and therapeutic targets for cancer therapies [13, 14, 15]. A number of studies have indicated that miRNAs may be involved in esophageal cancer progression and associated with prognosis [16, 17, 18]. MicroRNA-105 (miR-105), located on human chromosome Xq28, has been reported to play diverse oncogenic and tumor suppressor roles in many cancers [19]. In esophageal cancer, a study identified differentially expressed miRNAs using TCGA data, in which miR-105 was one of the upregulated miRNAs [20]. However, the role of miR-105 in esophageal cancer has not been clarified.

In the present study, we explored the expression levels of miR-105 in esophageal cancer tissues and cell lines. In addition, its clinical prognostic significance and functional role were also evaluated.

2. Materials and methods

2.1 Patients and tissue specimens

In all, 115 esophageal cancer patients who had undergone routine surgery at Dongying People’s Hospital of Shandong Province from June 2011 to December 2013 were enrolled in the present study. Paired esophageal cancer tissue specimens and adjacent normal tissue specimens were collected from the 115 esophageal cancer patients. All tissue specimens were confirmed by experienced pathologists and immediately snap-frozen in liquid nitrogen and then stored at $-$ 80 ${}^{\circ}$ C until RNA extraction. None of the patients had received any therapies prior to surgery. The clinicopathological characteristics of the patients were collected and presented in Table 1. 5-year follow-up information was also obtained and recorded by phone interview. Written informed consent was signed by all patients participated in the present study. And this study was approved by the Ethics Committee of Dongying People’s Hospital of Shandong Province.

Table 1
Comparison of clinical characteristics between patients with low or high miR-105 expression

Clinical characteristics	Cases	miR-105 expression		$P$ values
	$n=$ 115	Low	High
		( $n=$ 57)	( $n=$ 58)
Gender
Male	64	30	34	0.518
Female	51	27	24
Age
$<$ 60	52	24	28
$\geqslant$ 60	63	33	30
Tumor size (cm)
$<$ 4	68	36	32	0.384
$\geqslant$ 4	47	21	26
Differentiation
Well-moderate	66	29	37	0.161
Poor	49	28	21
Lymph node metastasis
Negative	69	40	29	0.027
Positive	46	17	29
TNM stage
I–II	61	37	24	0.011
III–IV	54	20	34

2.2 Cell culture and transfection

Three esophageal cancer cell lines (Eca-109, TE-1, and KYSE-150) and human normal esophageal endothelial cell line Het-1A were purchased from the Cell Bank of the Chinese Academy of Sciences (Shanghai, China). All esophageal cancer cells were cultured in RPMI-1640 medium (Gibco, Carlsbad, CA, USA) supplemented with 10% FBS (Gibco). The Het-1A cells were cultured in DMEM (Gibco) supplemented with 10% FBS (Gibco). All cells were incubated in a humidified 37 ${}^{\circ}$ C incubator with 5% CO ${}_{2}$ .

MiR-105 mimic, miR-105 inhibitor, and miRNA negative controls (NCs) (mimic NC and inhibitor NC) were purchased from GenePharma (Shanghai, China). Esophageal cancer cells were seeded in 6-well plates at a density of 3 $\times$ 10 ${}^{5}$ cells/well in RPMI-1640 medium. When cell confluence reached 50–70%, cell transfection was performed using Lipofectamine 3000 transfection reagent (Invitrogen; Thermo Fisher Scientific, Waltham, MA, USA) according to manufacturer’s instructions. Following a 48 h transfection, the cells were harvested for the subsequent experiments.

Figure 1.

The relative expression levels of miR-105 were determined by qRT-PCR in esophageal cancer tissues and cell lines. A. The relative expression levels of miR-105 were upregulated in tumor than that in matched adjacent normal tissue specimens. B. The relative expression levels of miR-105 were higher in esophageal cancer cells than that in normal Het-1A. ${}^{***}P<$ 0.001.

2.3 RNA extraction and quantitative reverse transcription-polymerase chain reaction (qRT-PCR)

Total RNAs were extracted by TRIzol reagent (Thermo Fisher Scientific, Waltham, MA, USA) from esophageal cancer tissues and cell lines. RNAs were reverse transcribed to cDNA by PrimeScript II 1 ${}^{\text{st}}$ Strand cDNA Synthesis kit (Takara, Dalian, China) according to the manufacturer’s protocol. Following cDNA synthesis, qRT-PCR was subsequently performed using SYBR Green Master Mixes (Thermo Fisher Scientific, Waltham, MA, USA) on the ABI 7500 real-time PCR System. The relative expression of miR-105 was quantified using the 2 ${}^{-\Delta\Delta\text{ct}}$ method and normalized to U6.

2.4 Cell proliferation assay

Cell proliferation ability was detected with cell counting kit-8 (CCK-8; Dojindo, Kumamoto, Japan) following instructions. Transfected cells were seeded into 96-well plates and cultured at 37 ${}^{\circ}$ C. 10 $\mu$ l CCK-8 kit was added to each well at 0, 24, 48, and 72 h, then plates were incubated at 37 ${}^{\circ}$ C for 2 h, and the absorbance at 450 nm was measured.

2.5 Cell migration and invasion assays

Cell migration and invasion abilities were measured using 24-well transwell chambers with 8 $\mu$ m pores (Corning, NY, USA), and chambers were non-Matrigel(BD, Franklin Lakes, CA, USA)-coated or Matrigel-coated, respectively. 100 $\mu$ l transfected cells (5 $\times$ 10 ${}^{4}$ /well) in serum-free RPMI-1640 medium were seeded into the upper chambers, and 600 $\mu$ l RPMI-1640 medium with 10% FBS was added into the lower chambers. Then, the cells were incubated for 24 h at 37 ${}^{\circ}$ C. The cells remaining in the upper chambers were removed by cotton swabs, and the migrated or invaded cells were fixed and stained. Then, the cells were counted in 5 random fields by a microscope (Olympus, Tokyo, Japan).

2.6 Statistical analysis

Data are presented as the mean $\pm$ standard deviation (SD). Each experiment was repeated at least three times. All statistical analyses were performed using SPSS version 20.0 (SPSS Inc., Chicago, IL, USA) and GraphPad Prism version 5.0 (GraphPad Software, Inc., La Jolla, CA, USA). Statistical significance in different groups was analyzed using the $\chi^{2}$ test, Student’s $t$ -test or one way ANOVA. Kaplan-Meier method and Cox regression proportional hazards model were used to analyze overall survival and prognostic factors. It was considered statistically significant when $P$ less than 0.05.

3. Results

3.1 miR-105 was upregulated in esophageal cancer tissues and cell lines

The expression of miR-105 was detected using qRT-PCR assay. As shown in Fig. 1A, the miR-105 expression level was significantly upregulated in esophageal cancer tissue specimens compared with matched adjacent normal tissues ( $P<$ 0.001). Similarly, the expression level of miR-105 was significantly increased in esophageal cancer cell lines Eca-109, TE-1, and KYSE-150, compared with normal esophageal endothelial cell line Het-1A ( $P<$ 0.001, Fig. 1B).

According to the median expression level of miR-105 in esophageal cancer tissue specimens, the patients were divided into low miR-105 expression group ( $n=$ 57) and high miR-105 expression group ( $n=$ 58) for subsequent analyses.

3.2 The relationship between miR-105 expression and clinical characteristics in patients with esophageal cancer

The relationships between miR-105 expression levels and clinicopathological characteristics of eso- phageal cancer patients were analyzed using the $\chi^{2}$ test and summarized in Table 1. We observed that the expression level of miR-105 was significantly correlated with the lymph node metastasis ( $P=$ 0.027) and TNM stage ( $P=$ 0.011). However, there is no significant association of miR-105 expression levels with patients’ gender, age, tumor size, and differentiation (all $P>$ 0.05).

3.3 The prognostic significance of miR-105 in esophageal cancer

To explore the prognostic significance of miR-105 in esophageal cancer, survival curves were conducted by the Kaplan-Meier method and compared by the log-rank test. Esophageal cancer patients with low miR-105 expression levels exhibited longer overall survival than those with high miR-105 expression levels (log-rank test, $P=$ 0.017, Fig. 2). Then multivariate Cox regression analysis was used to evaluate independent risk factors for poor prognosis using the level of miR-105 expression and clinical characteristics of esophageal cancer patients. Results showed that miR-105 expression level (HR $=$ 1.817, 95% CI: 1.033–3.195, $P=$ 0.038) and TNM stage (HR $=$ 1.748, 95% CI: 1.023–2.986, $P=$ 0.041) were independent factors in predicting the overall survival of esophageal cancer patients (Table 2).

Table 2
Multivariate Cox analysis of factors for the overall survival of esophageal cancer patients

Variables	Multivariate Cox analysis
	HR	95% CI	$P$ value
miR-105	1.817	1.033–3.195	0.038
Gender	1.248	0.758–2.055	0.384
Age	0.747	0.452–1.236	0.256
Tumor size	1.563	0.927–2.637	0.094
Differentiation	0.630	0.375–1.061	0.082
Lymph node metastasis	1.562	0.929–2.628	0.093
TNM stage	1.748	1.023–2.986	0.041

Figure 2.

Esophageal cancer patients with high miR-105 expression levels had shorter overall survival than those with low miR-105 expression levels (log-rank test, $P=$ 0.017).

Figure 3.

miR-105 overexpression and inhibitor affect the proliferation ability of human esophageal cancer Eca-109 and KYSE-150 cells. A. The expression levels of miR-105 were analyzed following transfection with miR-105 mimic, inhibitor, and negative controls. B. The Eca-109 and KYSE-150 cell proliferation were analyzed by CCK-8 assay. ${}^{*}P<$ 0.05, ${}^{**}P<$ 0.01, ${}^{***}P<$ 0.001.

Figure 4.

miR-105 promotes the migration and invasion of esophageal cancer Eca-109 and KYSE-150 cells. A. Transwell migration assays using Eca-109 and KYSE-150 cells transfected with miR-105 mimic, inhibitor, or negative controls. B. Transwell invasion assays using Eca-109 and KYSE-150 cells transfected with miR-105 mimic, inhibitor, or negative controls. ${}^{***}P<$ 0.001.

3.4 miR-105 promotes esophageal cancer cell proliferation, migration, and invasion

According to the above-mentioned results in cells, the expression of miR-105 in Eca-109 and KYSE-150 exhibited relatively higher in three esophageal cancer cells, thus both the cell lines were selected for the following experiments. We overexpressed/downregulated miR-105 in Eca-109 and KYSE-150 cell lines and examined the effects of miR-105 on proliferation, migration, and invasion. As shown in Fig. 3A, using qRT-PCR, we confirmed miR-105 mimic significantly increased miR-105 expression, while miR-105 inhibitor significantly decreased miR-105 expression in both Eca-109 and KYSE-150 cell lines, compared with that in untreated cells ( $P<$ 0.01). CCK-8 assays demonstrated that the cell proliferation ability was significantly increased by miR-105 mimic transfection, while the cell proliferation ability was significantly suppressed via miR-105 inhibitor transfection, compared with untreated cells ( $P<$ 0.05, Fig. 3B). In addition, considering the migration and invasion ability of cancer cells is an important factor related to tumor metastasis, we used Transwell assay to observe the effects of miR-105 on cell migration and invasion of esophageal cancer cells. As shown in Fig. 4A and B, the results indicated that overexpression of miR-105 promoted cell migration and invasion, while downregulation of miR-105 suppressed cell migration and invasion abilities of esophageal cancer cells, compared with untreated cells ( $P<$ 0.001).

4. Discussion

In the present study, we indicated that miR-105 was significantly upregulated in esophageal cancer tissues and cell lines compared with that in adjacent normal tissues and normal Het-1A cells, respectively. In addition, we observed that high miR-105 expression was independently associated with positive lymph node metastasis, advanced TNM stages, and unfavorable overall survival. These findings suggest that miR-105 might be an independent prognostic biomarker and be an oncogene gene in esophageal cancer. What’s more, we explored the effects of miR-105 on cell proliferation, migration, and invasion in esophageal cancer cells and found that miR-105 overexpression significantly promoted these cellular activities, while downregulation of miR-105 significantly subdued these cellular activities.

Numerous miRNAs have been identified to play important roles in tumor progression in a variety of tissues and to serve as diagnostic/prognostic biomarkers [21, 22, 23]. For instance, lower levels of miR-4262 predict poorer prognosis in gastric cancer patients and inhibit cell proliferation and invasion in gastric cancer by targeting proto-oncogene CD163 [24]. In esophageal cancer, tissue and serum miR-1290 levels were both increased in esophageal cancer, and its expression level could reflect the progress of esophageal cancer, suggesting miR-1290 might be a useful diagnostic and prognostic biomarker of esophageal cancer [25]. Another study indicated that miR-145 expression is significantly decreased in esophageal squamous cell carcinoma (ESCC) tissues and miR-145 may be a prognostic marker for predicting the overall survival of patients with ESCC [3]. These studies suggested that identifying functional miRNAs in tumor progression is important for the improvement of cancer treatment.

In this study, we used qRT-PCR analysis to detect the expression of miR-105 in esophageal cancer tissues and cell lines. Our findings showed the expression of miR-105 was significantly increased in both esophageal cancer tissues and cell lines compared to respective controls. The expression pattern of miR-105 in esophageal cancer was consistent with that in many other cancers, such as colorectal cancer [26] and triple-negative breast cancer [27]. The further clinical-based analysis showed that miR-106 expression was significantly associated with lymph node metastasis and TNM stage. The above results suggested miR-105 expression may be associated with the development of esophageal cancer. Considering metastasis and TNM stage are usually associated with overall survival, we speculate miR-105 expression may correlate with clinical outcomes of esophageal cancer patients. Kaplan-Meier curve method and Cox regression analysis results showed a high expression of miR-105 correlated with poor clinical outcomes and maybe an independent prognostic biomarker for esophageal cancer. The results are consistent with those from previous studies on various types of tumors [27, 28]. For instance, a previous study also indicated that miR-105 was associated with overall survival and disease-free survival in non-small cell lung cancer [28].

A number of studies have demonstrated that miR-105 functions as an oncogene or a tumor suppressor depending on tumor contexts [19]. miR-105 was downregulated in gastric carcinoma tissues and cells and inhibited cell progression of gastric cancer by targeting SOX9 [29]. High expression of miR-105 positively correlates with the clinical prognosis of hepatocellular carcinoma by targeting NCOA1 [30]. In non-small cell lung cancer (NSCLC), overexpression of miR-105 significantly promotes cell viability and migration of A549 and Calu-3 cells and promotes the epithelial-mesenchymal transition (EMT) of NSCLC cells through upregulation of Mcl-1 [31]. By these findings, we speculate that the functional role of miR-105 may be tumor-specific. In this study, overexpression of miR-105 promoted cell proliferation, migration, and invasion of Eca-109 and KYSE-150 cells, while suppression expression of miR-105 inhibited these cellular behaviors, suggesting miR-105 may play an oncogene role in esophageal cancer. In colorectal cancer, overexpression of miR-105 functions as an oncogene role and promotes cell migration and EMT by directly targeting RAP2C [26]. We hypothesized miR-105 may also function as an oncogene in esophageal cancer to promote the progression of esophageal cancer by targeting RAP2C or other genes. Further studies will be carried out to figure out the detailed molecular mechanism of miR-105 in esophageal cancer progression.

In conclusion, we found that miR-105 is significantly upregulated in esophageal cancer tissues and cell lines. Overexpression of miR-105 promotes esophageal cancer proliferation, migration, and invasion of esophageal cancer cells. The findings provide evidence that miR-105 may serve as a prognostic biomarker and therapeutic target for esophageal cancer and be involved in the progression of esophageal cancer.

Footnotes

Conflict of interest

The authors declare that they have no conflict of interest.

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MicroRNA-105 plays an independent prognostic role in esophageal cancer and acts as an oncogene

Abstract

BACKGROUND:

METHODS:

RESULTS:

CONCLUSION:

Keywords

1. Introduction

2. Materials and methods

2.1 Patients and tissue specimens

Table 1 Comparison of clinical characteristics between patients with low or high miR-105 expression

2.4 Cell proliferation assay

2.5 Cell migration and invasion assays

2.6 Statistical analysis

3. Results

3.1 miR-105 was upregulated in esophageal cancer tissues and cell lines

3.2 The relationship between miR-105 expression and clinical characteristics in patients with esophageal cancer

3.3 The prognostic significance of miR-105 in esophageal cancer

Table 2 Multivariate Cox analysis of factors for the overall survival of esophageal cancer patients

4. Discussion

Footnotes

Conflict of interest

References

Table 1
Comparison of clinical characteristics between patients with low or high miR-105 expression

Table 2
Multivariate Cox analysis of factors for the overall survival of esophageal cancer patients