High expression of special AT‑rich sequence binding protein‑1 predicts esophageal squamous cell carcinoma relapse and poor prognosis

  • Authors:
    • Songhui Zhai
    • Jianxin Xue
    • Zheng Wang
    • Lijuan Hu
  • View Affiliations

  • Published online on: September 27, 2017     https://doi.org/10.3892/ol.2017.7081
  • Pages:7455-7460
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Abstract

Previous studies of the roles of special AT‑rich sequence binding protein‑1 (SATB1) in the development and progression of cancer have suggested that SATB1 promotes cancer cell metastasis. The aim of the present study is to evaluate the role of SATB1 in the progression and prognosis of esophageal squamous cell carcinoma (ESCC). ESCC tissues were collected from 102 patients and SATB1 mRNA expression was measured by reverse transcription‑quantitative polymerase chain reaction. The association between expression of SATB1 mRNA with clinicopathological features and prognosis was assessed, and the prognosis of ESCC was evaluated using Kaplan‑Meier survival curves. In the 102 ESCC tissues, SATB1 mRNA expression correlated with the clinical tumor node metastasis stage (P<0.05), but not with any other clinicopathological features (including age, gender, tumor differentiation grade, adjuvant radio/chemotherapy, or the consumption of alcohol and use of cigarettes) (P>0.05). The disease‑free survival (DFS) and overall survival (OS) of patients with high SATB1 expression was decreased compared with those with low SATB1 expression. The present study indicated that SATB1 mRNA expression was associated with the postoperative recurrent and poor prognosis in ESCC. SATB1 may be a novel marker for predicting the recurrent and worse prognosis of ESCC.

Introduction

Esophageal cancer cases are distributed worldwide; its mortality rate ranks sixth among all types of cancer and it is the fourth most commonly occurring cancer in China (1,2). China is among the highest risk areas of esophageal cancer, where ~90% of cases are squamous cell carcinoma (SCC) (3). The 5-year survival rate and quality of life remain low (3). However, the molecular mechanisms underlying the initiation and progression of esophageal SCC (ESCC) remain unclear.

Special AT-rich sequence binding protein-1 (SATB1), a tissue-specific nuclear matrix binding protein, was identified in 1992 (4). SATB1 is primarily expressed in thymocytes, and also the expression of SATB1 in the basal layer of the epidermis is regulated by p63 (5,6). SATB1 can regulate gene expression by folding chromatin into loop domains and tethering DNA domains to the SATB1 network structure (7,8). Under normal conditions, SATB1 is expressed at low levels in cells and tissues, but is overexpressed in a variety of malignant tumors, including laryngeal squamous cell carcinoma, endometrial cancer, hepatocellular carcinoma, rectal cancer, cutaneous malignant melanoma, gastric cancer, prostate cancer, lung cancer and cutaneous T-cell lymphoma (7,920). The expression of SATB1 has been examined in esophageal adenocarcinoma and is an independent prognostic factor (20). In several types of cancer, including laryngeal squamous cell carcinoma, endometrial cancer, hepatocellular cancer and lung cancer, high expression of SATB1 promotes tumor growth and metastasis, and is a negative prognostic factor (7,920). SATB1 can regulate the expression of >1,000 genes involved in the processes of DNA organization, proliferation and apoptosis (8,9). SATB1 has been demonstrated to serve roles in malignancies, in addition to malignant transformation (7,20).

The present study aimed to explore the role of SATB1 in ESCC by investigating the association between SATB1 mRNA expression and prognosis, and recurrence in 102 patients with ESCC following surgery.

Materials and methods

Tissue samples, patient data and follow-up

A total of 102 tissue samples of ESCC were obtained from patients (78 male, 24 female) undergoing surgery at the Department of Thoracic Oncology, West China Hospital, Sichuan University (Chengdu, China) between March 2010 and July 2014. Patient median age was 60.5 years old (range, 39–81 years old). All specimens were immediately frozen in liquid nitrogen and stored at −80°C until RNA extraction. All human ESCC tissue samples were obtained and handled in accordance with an approved Institutional Review Board application (Ethics Committee of Sichuan University). Written informed consent was obtained from all patients.

All patients were diagnosed with primary ESCC based on pathological assessment and had undergone a complete surgical resection (R0). Patients who underwent non-curative resection (R1), succumbed to postoperative complications, missed valid follow-up conditions or lacked clinical data were all excluded from the present study. No patients received chemotherapy or radiotherapy prior to surgery. The clinical stage and histologic grade of the tumor was defined according to the 7th edition of the Tumor Node Metastasis (TNM) classification of the International Union Against Cancer (21). Follow-up began on the date of surgery and ended in July 2014. The median follow-up was 35.5 months (range, 6–70 months). Regular history and physical examinations were performed in all patients every 3 months during the first 2 years after surgery and then every 6 months thereafter.

RNA extraction and reverse transcription-quantitative polymerase chain reaction (RT-qPCR)

Total RNA was extracted from cancerous specimens using TRIzol reagent (Invitrogen; Thermo Fisher Scientific, Inc., Waltham, MA, USA). A total of 5 µg of each RNA sample was reverse transcribed into complementary DNA using the Prime-Script™ one step RT-PCR kit (Takara Bio, Inc., Otsu, Japan). SATB1 expression level was determined by RT-qPCR using the following primer sequences: forward, 5′-GTGGAAGCCTTGGGAATCC-3′ and reverse, 5′-CTGACAGCTCTTCTTCTAGTT-3′. β-actin was used as an internal control, using the following primer sequences: forward, 5′-CTGGCACCACACCTTCTACAATG-3′ and reverse, 5′-CCTCGTAGATGGGCACAGTGTG-3′. The RT-qPCR reaction was performed with an initial 95°C denaturation step for 10 min, followed by 40 cycles of 95°C for 30 sec 60°C for 30 sec and 72°C for 30 sec at for 40 cycles using the ABI7500 system (Applied Biosystems; Thermo Fisher Scientific, Inc.) and the SYBRGreen PCR Master Mix (Takara Bio, Inc.). SATB1 mRNA levels were normalized to β-actin by the 2−ΔΔCq method (22).

Statistical analysis

All statistical analyses were performed using SPSS software, version 17.0 (SPSS, Inc., Chicago, IL, USA). Spearman's rank correlation coefficient test was used to analyze the correlation between SATB1 expression in different groups of patients. Comparison of continuous data was performed with an independent t-test between two groups, whereas the correlation among categorical variables was analyzed using a χ2 test. Disease-free survival (DFS) and overall survival (OS) analyses were performed with the Kaplan-Meier estimator and log-rank tests. Multiple factor analyses were performed using Cox regression models to evaluate prognostic factor for patients with ESCC. P<0.05 was considered to indicate a statistically significant difference.

Results

Patient clinicopathological characteristics

A total of 102 patients with ESCC were included in the current study (78 male, 24 female). Their median age was 60.5 years old (range, 39–81 years old). A total of 35 patients (34.3%) had lymph node metastases and none had distant nodal metastases (Table I).

Table I.

Association between SATB1 expression and clinicopathologic parameters in 102 patients with ESCC.

Table I.

Association between SATB1 expression and clinicopathologic parameters in 102 patients with ESCC.

FactorSATB1 low expression (n=53) N (%)SATB1 high expression (n=49) N (%)P-value
Age (mean ± standard deviation)a61.5±7.859.5±10.80.310b
Age group 0.666c
  ≤61 yrs25 (47.2)21 (42.0)
  >61 yrs28 (52.8)28 (56.0)
Gender 0.475c
  Male39 (73.6)39 (79.6)
  Female14 (26.4)10 (20.4)
Smoking/drinking alcohol 0.701c
  Never17 (32.1)14 (28.6)
  Ever and current36 (67.9)35 (71.4)
Family history of ESCC 0.963c
  No37 (69.8)34 (69.4)
  Yes16 (30.2)15 (30.6)
Barium meal examination 0.760c
  Mushroom type10 (18.9)6 (12.0)
  Medullary type16 (30.2)16 (32.0)
  Ulcer25 (47.2)24 (46.0)
  Mass01 (2.0)
  Coarctation2 (3.8)2 (4.0)
Tumor location 0.908c
  Upper2 (3.8)1 (2.0)
  Middle38 (71.7)35 (71.4)
  Low13 (24.5)13 (26.5)
Histological type 0.552c
  High22 (41.5)23 (46.9)
  Middle28 (50.9)24 (49)
  Low3 (5.7)2 (4.1)
pT status 0.074c
  pT11 (1.9)5 (10.2)
  pT2-452 (98.1)44 (89.8)
Lymph node metastasis 0.361c
  Yes16 (30.2)19 (38.8)
  No37 (69.8)30 (61.2)
pTNM stage 0.003c
  I15 (28.3)16 (32.7)
  II25 (47.2)10 (20.4)
  III13 (24.5)16 (32.7)
  IV0 (0)7 (14.3)
pTNM stage group 0.023c
  I–II40 (75.5)26 (53.1)
  III–IV13 (24.5)23 (46.9)
Relapse 0.029c
  No33 (62.3)19 (38.8)
  Yes20 (37.7)30 (61.2)

a Age data are presented as the mean ± standard deviation.

b Independent t-test.

c Two-sided 2χ-test. pT, pathological tumor stage; pN, pathological node stage; pTNM, pathological tumor node metastasis stage.

Association between SATB1 expression and clinicopathological characteristics

According to the average expression (the median value=1.39) of SATB1 mRNA, the 102 patients with ESCC were split into two groups. A high expression group with SATB1 mRNA expression above 1.39 and a low expression group with SATB1 mRNA expression below 1.39. A total of 49 (48.0%) specimens exhibited high expression and 53 (54.0%) specimens exhibited low expression of SATB1 mRNA. No significant associations were identified between the expression level of SATB1 and patient age, gender, tumor differentiation grade, adjuvant radio/chemotherapy or the use of alcohol and cigarettes (P>0.05). However, the expression level was correlated with clinical TNM stage (P<0.05) (Table I).

High expression of SATB1 mRNA is associated with poor prognosis for patients with ESCC

To reveal whether pathological TNM (pTNM) stage and SATB1 mRNA expression affected postoperative outcome, univariate analyses were performed. The results indicated that SATB1 expression and pTNM stage were associated with postoperative outcome (Table II). Patients with high SATB1 mRNA expression had a shorter OS (median, 34.9 months) compared with those with low SATB1 mRNA expression (median, 40.3 months) (P=0.035; Table III and Fig. 1A). Multivariate analysis suggested that SATB1 expression was an independent factor associated with OS (RR=2.02; 95% CI: 1.10–3.68, P<0.05).

Table II.

Univariate analyses of prognostic factors in ESCC with respect to OS.

Table II.

Univariate analyses of prognostic factors in ESCC with respect to OS.

FactorRR95% CIP-value
pT status (T1/T2-4)1.3580.472–3.9080.571
pN status (N0/1-3)0.5170.203–1.3170.167
pTNM stage (I–II/III–IV)7.251.62–32.4580.021a
Adjuvant therapy1.1340.668–1.9240.642
SATB1 expression: low/high1.9281.128–3.2970.016a

a P<0.05. ESCC, esophageal squamous cell carcinoma; OS, overall survival; pT, pathological tumor stage; pN, pathological node stage; pTNM, pathological tumor node metastasis stage.

Table III.

Cumulative proportion of OS at different time points.

Table III.

Cumulative proportion of OS at different time points.

Cumulative proportion of OS

GroupNo. of patients that succumbed12 months (%)36 months (%)60 months (%)
SATB1 low expression (n=53)1888.663.754.3
SATB1 high expression (n=49)2683.656.031.5

[i] OS, overall survival; SATB1, special AT-rich sequence-binding protein 1.

SATB1 mRNA expression is associated with the relapse of ESCC

The duration of DFS of patients with ESCC with high SATB1 mRNA expression (31.53±16.34 months) was significantly shorter compared with that of patients with low SATB1 mRNA expression (37.70±16.28 months, P=0.029) (Table IV and Fig. 1B).

Table IV.

The cumulative proportion of DFS at different time points.

Table IV.

The cumulative proportion of DFS at different time points.

Cumulative proportion of DFS

GroupN of relapse12 months (%)36 months (%)60 months (%)
SATB1 low expression (n=53)2086.676.151.2
SATB1 high expression (n=49)3085.449.014.8

[i] DFS, disease-free survival; SATB1, special AT-rich sequence-binding protein 1.

Discussion

Previous studies have indicated that SATB1 is associated with prognosis in resected upper gastrointestinal tract adenocarcinoma and other tumor forms (20,23,24). Data from the present study revealed that patients with higher SATB1 mRNA expression had a higher rate of relapse. SATB1 expression was detected in ESCC tumor tissues by measuring mRNA expression; high SATB1 mRNA expression was associated with poor DFS and OS, as determined by univariate analysis. Multivariate analysis revealed that high SATB1 expression may be an independent factor for poor prognosis in patients with ESCC following surgery. These results were consistent with another previous report, in which SATB1 expression groups were divided using a semi-quantitative scoring system for staining intensity and the percentage of positive malignant cells (25). These results verified the importance of the SATB1 gene in ESCC. The current study defined the expression state according to the median value of all ESCC tissues, which may exclude subjective bias. However, it is challenging to obtain a ‘clean’ tumor sample without inflammatory and stromal cells. Cong et al (25) reported that SATB1 expression measured by immunohistochemistry could classify SATB1 expression in tumor cells from inflammatory cells and stromal cells, whereas the results obtained using semi-quantitative systems were not precise. Furthermore, SATB1 expression was identified in inflammatory cells but not in stromal cells (26). SATB1 integrates global epigenetic and transcriptional programs that determine cellular phenotypes, differentiation, and the activity of leukocyte subsets (27). In future studies, more patients at respective pTNM stages will be recruited to define the median level of SATB1 mRNA expression at different stages, explore the expression of SATB1 expression between tumor tissues and inflammatory cells, and investigate the role of SATB1 in the development and prognosis of ESCC.

The incidence of ESCC was different in different regions of the world and the variation has changed over time (2). This suggests that multiple risk factors (genetic and environmental) contribute to the development of ESCC (2830). Morita et al (30) reported that cigarette smoking and alcohol consumption exhibit synergistic effects on the development of ESCC. Kasagi et al (31) reviewed the clinicopathological characteristics of ESCC in patients <50 years old and revealed that the incidence of ESCC was associated with heavy exposure to smoking and/or drinking. Wu et al (32) recruited 718 patients with ESCC in Taiwan and demonstrated that the habitual drinking of alcohol was the strongest predictor for ESCC survival, followed by areca chewing and smoking. In the current study, smoking and drinking was associated with the prognosis of ESCC, but had not with SATB1 mRNA expression, suggesting that other mechanisms participate in ESCC development.

In conclusion, the present study identified that high expression of SATB1 in ESCC was associated with a clinically unfavorable prognosis independent of the patient's disease stage, therefore SATB1 expression may be an independent factor of poor prognosis in ESCC. Further studies are required to elucidate the molecular mechanisms underlying the roles of SATB1 in the progression of ESCC.

Acknowledgements

The present study was financially supported by grants from the National Natural Science Foundation of China (grant no. 81472808). The authors would like to thank Dr Nan Li (Sichuan University, Chengdu, China) for language editing and proofreading.

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APA
Zhai, S., Xue, J., Wang, Z., & Hu, L. (2017). High expression of special AT‑rich sequence binding protein‑1 predicts esophageal squamous cell carcinoma relapse and poor prognosis. Oncology Letters, 14, 7455-7460. https://doi.org/10.3892/ol.2017.7081
MLA
Zhai, S., Xue, J., Wang, Z., Hu, L."High expression of special AT‑rich sequence binding protein‑1 predicts esophageal squamous cell carcinoma relapse and poor prognosis". Oncology Letters 14.6 (2017): 7455-7460.
Chicago
Zhai, S., Xue, J., Wang, Z., Hu, L."High expression of special AT‑rich sequence binding protein‑1 predicts esophageal squamous cell carcinoma relapse and poor prognosis". Oncology Letters 14, no. 6 (2017): 7455-7460. https://doi.org/10.3892/ol.2017.7081