Users Online: 179
Home Print this page Email this page
Home About us Editorial board Search Browse articles Submit article Ahead of Print Instructions Subscribe Contacts Login 


 
Previous article Browse articles Next article 
ORIGINAL ARTICLE
Adv Biomed Res 2014,  3:135

Association of HOTAIR expression in gastric carcinoma with invasion and distant metastasis


1 Department of Biology, Faculty of Sciences, Razi University, Kermanshah, Iran
2 Department of Genetics and Molecular Biology, Faculty of Medicine, Pediatric Inherited Diseases Research Center, Child Growth and Development Research Center, Isfahan University of Medical Sciences, Isfahan, Iran
3 Department of Genetics, Faculty of Basic Sciences, Research Institute of Biotechnology, Shahrekord University, Shahrekord, Iran

Date of Submission13-Aug-2013
Date of Acceptance14-Sep-2013
Date of Web Publication28-May-2014

Correspondence Address:
Dr. Parvaneh Nikpour
Department of Genetics and Molecular Biology, Faculty of Medicine, Isfahan University of Medical Sciences, Isfahan
Iran
Login to access the Email id

Source of Support: The study was supported in part by a research grant from Isfahan University of Medical Sciences, Isfahan and Razi University, Kermanshah, Iran, Conflict of Interest: None


DOI: 10.4103/2277-9175.133278

Rights and Permissions
  Abstract 

Background: Gastric cancer is the second and fourth most common cancer in Iranian men and women, respectively, but it is the first leading cause of cancer deaths in Iran. Most Iranian patients with gastric cancer are diagnosed at an advanced stage of disease when the conventional treatments have no effect on improving the survival. So, early gastric cancer detection is of high priority in order to decrease its high mortality rate in Iran. HOTAIR is a long non-coding RNA which its overexpression has been documented in different types of human cancer and can be considered as a potential cancer biomarker. The aim of this study was to evaluate the clinicopathological relevance of the expression of HOTAIR gene in gastric carcinoma.
Materials and Methods: A total of 60 tumoral and non-tumoral gastric specimens were evaluated for HOTAIR gene expression using quantitative real-time PCR.
Results: The expression of HOTAIR was markedly increased in gastric cancer tissues compared with adjacent non-tumoral tissues. We further showed that there was a positive significant correlation between the HOTAIR gene expression, TNM staging, perineural invasion, and distant metastasis, but not with other clinicopathological features of gastric tumors.
Conclusions: These results suggest that HOTAIR expression is modulated during gastric cancer progression and therefore may participate in molecular processes relevant to malignant transformation and metastasis in gastric carcinoma.

Keywords: Gastric carcinoma, gene expression, HOTAIR, invasion, metastasis


How to cite this article:
Emadi-Andani E, Nikpour P, Emadi-Baygi M, Bidmeshkipour A. Association of HOTAIR expression in gastric carcinoma with invasion and distant metastasis. Adv Biomed Res 2014;3:135

How to cite this URL:
Emadi-Andani E, Nikpour P, Emadi-Baygi M, Bidmeshkipour A. Association of HOTAIR expression in gastric carcinoma with invasion and distant metastasis. Adv Biomed Res [serial online] 2014 [cited 2019 Oct 14];3:135. Available from: http://www.advbiores.net/text.asp?2014/3/1/135/133278

§Elaheh Emadi Andani, Parvaneh Nikpour
§These two authors contributed equally to this work.



  Introduction Top


Gastric cancer is the second most common cancer worldwide and the second leading cause of cancer mortality. [1] Gastric cancer is the second and fourth most common cancer in Iranian men and women, respectively, but it is the first leading cause of cancer deaths in Iran. [2] The main environmental factors for the high incidence of gastric cancer in Iran are H. pylori infection, high intake of salt, and smoking. Most Iranian patients with gastric cancer are diagnosed at an advanced stage of disease when the conventional treatments have no effect on improving the survival. So, early gastric cancer detection is of high priority in order to decrease its high mortality rate in Iran. [3]

A large part of the genome is transcribed for non-coding RNAs (ncRNAs) with various biological functions. [4] Long non-coding RNAs (lncRNAs) have a length of >200 nucleotides, with direct effect on the transcription or employing histone modification complexes regulating expression of different genes. [5],[6] Hox transcript antisense intergenic RNA (HOTAIR) is a lncRNA with 2158 nucleotides in length which is expressed from HOXC locus on 12 chromosome. [7] It interacts with Polycomb Repressive Complex 2 (PRC2) and causes targeting it to the HOXD locus. [7],[8] Several studies display an active role for HOTAIR in cancers of the breast, [9],[10] colorectal, [11] hepatocellular, [12],[13],[14] pancreatic, [15] gastrointestinal stromal tumors, [16] nasopharyngeal carcinoma (NPC), [17] laryngeal squamous cell carcinoma (LSCC), [18] and sarcoma. [19] In all studies, increased expression of HOTAIR is associated with malignant progression and poor survival. Hence, HOTAIR may be considered as a potential target for diagnosis and treatment of various cancer types. [9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19]

Based on these findings, we tested if HOTAIR also shows a similar pattern in gastric cancer. To this aim, we evaluated HOTAIR expression in tumoral and non-tumoral gastric tissue samples by using quantitative real-time RT-PCR. Our results demonstrated that the expression of HOTAIR was markedly increased in gastric cancer tissues compared with adjacent normal tissues. We further showed that there was a positive correlation between the HOTAIR gene expression, TNM (T, N, and M stand for tumor, lymph node, and metastasis, respectively) staging, perineural invasion, and distant metastasis, but not with other clinicopathological features of gastric tumors.


  Materials and Methods Top


Tumor and non-tumor tissues

All experimental procedures were approved by the Ethics Committee of Isfahan University of Medical Sciences. A total of 60 specimens of gastric cancer tissues and adjacent benign tissues (paired) were obtained from the Iran Tumoral Bank (Tehran, Iran) as described previously. [20],[21],[22] All patients provided written informed consent to the Iran Tumoral Bank prior to the participation.

Total RNA isolation and cDNA synthesis

Total RNA was extracted from gastric cancer tissues using Qiazol reagent (Qiagen, Hilden, Germany) according to the manufacturer's protocol. The integrity of RNA was verified by electrophoresis on a 1% agarose gel stained with ethidium bromide. The quality and quantity of RNA were determined by ultraviolet spectroscopy. cDNA was synthesized using random hexamer primers and an M-MLV reverse transcriptase (Fermentas, Vilnius, Lithuania) as described elsewhere. [20],[21],[22]

Quantitative real-time PCR

The expression level of HOTAIR gene was determined by quantitative real-time RT-PCR with TBP (TATA box binding protein) as a reference gene. [23] The primers for the target gene were as follows: 5΄-AGACGGCGGCGAGAGGAA-3΄ and 5 ΄-CTGAAATGGAGGACCGGCG-3΄ with an amplicon size of 126 bp. PCR was performed using Maxima™ SYBR Green/ROX qPCR Master MIX (Fermentas, Vilnius, Lithuania) and an Applied Biosystems StepOnePlus™ instrument. The PCR amplification conditions consisted of an initial denaturation at 95°C for 10 minutes, 40 cycles of denaturation at 95°C for 15 seconds, annealing at 55°C and 58°C for TBP and HOTAIR genes, respectively, then extension for 15 seconds at 72°C. All samples were measured in triplicate. The 2 -ΔΔCt method was used to quantify the relative levels of gene expression.

Statistical analysis

All data are expressed as means ± standard error of mean (SEM) from at least three separate experiments. Statistical analyses were performed using SPSS version 16.0. Differences between groups were analyzed using a paired t-test or one-way ANOVA with post hoc multiple comparisons. Statistical significance was defined as P ≤ 0.05.


  Results Top


Optimization of PCR amplification

In order to obtain a specific amplicon for HOTAIR, both conventional and real-time PCR was done with a temperature gradient. As it was shown in a previous study that HOTAIR is expressed in MCF-7 breast cancer cell line, [9] we used the cDNA of this cell line for optimization procedures. Gel electrophoresis of amplified product of HOTAIR with the designed primers showed a specific band with expected size (126 bp) in 58°C [Figure 1]. Analysis of melting curves of real-time PCR also showed a unique melting curve for this amplicon without primer dimmers (data not shown).
Figure 1: Optimization of PCR conditions for HOTAIR gene expression. RT-PCR products were separated on agarose gel electrophoresis as follows: lane 1: DNA size marker, lane 2: Non-template control (adding no cDNA), and lane 3: adding cDNA of MCF-7 cell line

Click here to view


HOTAIR gene expression in tumoral and non-tumoral gastric specimens

To examine the expression of HOTAIR in human gastric tissues, cDNA was synthesized for all samples and real-time PCR was performed using specific primers for both HOTAIR and TBP genes. The relative expression of HOTAIR showed statistically significant overexpression in pooled tumoral specimens compared to the paired non-tumoral samples [[Figure 2], P = 0.028].
Figure 2: The relative expression levels of HOTAIR in tumoral vs non-tumoral gastric samples. Error bars represent standard error of mean (SEM) and the asterisk represents a statistically significant difference (p ≤ 0.05)

Click here to view


Correlation of HOTAIR expression with clinicopathological features in gastric carcinoma

In order to examine the clinical importance of the HOTAIR overexpression, the correlation between clinicopathological status of gastric tumor samples and level of HOTAIR expression was investigated. Analyses showed a significant and positive association between the expression levels of HOTAIR, TNM staging, perineural invasion, and distant metastasis. A trend was also evident toward the same pattern for lymph node metastasis (N classification) and invasion depth although not reaching statistical significance. No significant correlation was found for other clinicopathological features of gastric tumors [Table 1].
Table 1: Relationship between HOTAIR expression levels and clinicopathological parameters of tumoral gastric samples

Click here to view



  Discussion Top


Our study showed for the first time that HOTAIR expression is significantly correlated with perineural invasion and distant metastasis in gastric cancer. An increased HOTAIR expression in gastric carcinomas compared to their non-tumoral adjacent tissues was also documented.

Until now, altered expression of HOTAIR gene has been documented in different types of human cancer. Gupta et al.[9] showed increased expression of HOTAIR in primary breast tumors as well as metastases. They showed that high expression of HOTAIR is an independent prognostic factor for metastasis and death in breast cancer patients. In another study by Milhem et al., [19] increased expression of HOTAIR was detected in most of the primary and metastatic sarcoma patient tumor samples in such a way that its expression was correlated with the likelihood of metastasis in primary sarcoma tumors. In 2011, Geng et al. measured HOTAIR gene expression in hepatocellular carcinoma (HCC) tissues and showed that the expression of HOTAIR is significantly higher in tumoral vs. non-tumoral HCC tissue samples. Furthermore, they reported a positive correlation between the HOTAIR gene expression and lymph node metastasis. However, they did not observe any significant correlation between HOTAIR expression levels and other clinicopathological features of patients like age, gender, tumor size, tumor number, and portal invasion. [13] Kogo et al. also showed HOTAIR overexpression in colorectal cancerous tissues compared to the noncancerous ones. They divided their patients into two groups, one with high and one with the low HOTAIR expression. They found a strong correlation between HOTAIR expression and histological grade, depth of tumor and liver metastasis but not with age, gender, lymph node metastasis, lymphatic or venous invasion. The group with higher HOTAIR expression had also poorer prognosis. [11] In another study of HCC patients, HOTAIR expression level was shown to be higher in tumor tissues than their adjacent non-tumoral ones. Furthermore, the higher level of HOTAIR was linked to shorter survival and more probability of recurrence after liver transplantation. [12] In contrast to the other previous reports, a study by Lu et al. in 2012 demonstrated that high levels of HOTAIR are correlated with the lower chance of recurrence and mortality in 348 examined tissues from patients with breast cancer. They also found no significant correlation between HOTAIR levels and various pathological and clinical features of breast cancer samples like tumor stage, grade, histological type, tumor size, and nodal status. [24] In 2012, a study by Chisholm et al.[10] was performed to analyze HOTAIR gene expression in formalin-fixed paraffin-embedded breast cancer tissues. They showed a positive correlation between HOTAIR levels and ER/PR (estrogen receptor/progesterone receptor) positivity and also with worse survival rates. In 2013, overexpression of HOTAIR was also shown in LSCC tissue samples compared to their adjacent non-tumoral tissues. In that study, a positive association between HOTAIR gene expression levels and T classification, neck nodal metastasis, and clinical stage was reported. [18] Nie et al. examined HOTAIR gene expression using in situ hybridization and real-time PCR in NPC samples. Similar to other studies, they also showed increased expression of HOTAIR in cancerous samples in comparison to non-cancerous tissues. They also reported a positive association of HOTAIR gene expression with tumor size, clinical stage, lymph node tumor burden, and distant metastasis. [17]

Nearly all studies that have examined the HOTAIR expression levels in tumoral and non-tumoral samples of different cancer types have reported HOTAIR elevated levels in cancerous specimens. [9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19] Taken together our data are in accord with other studies [9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19] that showed HOTAIR expression increased significantly in cancerous tissues. We also observed a positive significant correlation between HOTAIR expression, staging, invasion, and metastasis; in a same way to the other studies. [9],[10],[11],[13],[17],[18],[19] Moreover, a trend was also evident toward the same pattern for lymph node metastasis (N classification) and invasion depth although not reaching statistical significance. This is consistent with findings of previous studies. [11],[13],[17],[18] However, we did not observe a significant association between the target gene expression and other clinicopathological parameters, like age, gender, tumor size, grades, histological types, and lymphatic invasion consistent with other studies. [11],[12],[13],[17],[18],[24] Finally, during processing of the manuscript, two relevant studies appeared in the Pubmed in which they also showed that HOTAIR is overexpressed in gastric cancer and is associated with TNM staging, lymph node metastasis, and poor overall survival. [25],[26]

In summary, this is the first study showing a positive and significant correlation between HOTAIR gene expression profile, perineural invasion, and distant metastasis in gastric tumor samples. These results suggest that HOTAIR expression is modulated during gastric cancer progression and therefore may participate in molecular processes relevant to malignant transformation and metastasis in gastric carcinoma.

 
  References Top

1.Gomceli I, Demiriz B, Tez M. Gastric carcinogenesis. World J Gastroenterol 2012;18:5164-70.  Back to cited text no. 1
    
2.Mousavi SM, Gouya MM, Ramazani R, Davanlou M, Hajsadeghi N, Seddighi Z. Cancer incidence and mortality in Iran. Ann Oncol 2009;20:556-63.  Back to cited text no. 2
    
3.Malekzadeh R, Derakhshan MH, Malekzadeh Z. Gastric cancer in Iran: Epidemiology and risk factors. Arch Iran Med 2009;12:576-83.  Back to cited text no. 3
    
4.Pan YF, Feng L, Zhang XQ, Song LJ, Liang HX, Li ZQ, et al. Role of long non-coding RNAs in gene regulation and oncogenesis. Chin Med J (Engl) 2011;124:2378-83.  Back to cited text no. 4
    
5.Kurokawa R. Long noncoding RNA as a regulator for transcription. Prog Mol Subcell Biol 2011;51:29-41.  Back to cited text no. 5
[PUBMED]    
6.De Lucia F, Dean C. Long non-coding RNAs and chromatin regulation. Curr Opin Plant Biol 2011;14:168-73.  Back to cited text no. 6
    
7.Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, et al. Functional demarcation of active and silent chromatin domains in human HOX Loci by Noncoding RNAs. Cell 2007;129:1311-23.  Back to cited text no. 7
    
8.Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, et al. Long noncoding RNA as modular scaffold of histone modification complexes. Science 2010;329:689-93.  Back to cited text no. 8
    
9.Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 2010;464:1071-6.  Back to cited text no. 9
    
10.Chisholm KM, Wan Y, Li R, Montgomery KD, Chang HY, West RB. Detection of long non-coding RNA in archival tissue: Correlation with polycomb protein expression in primary and metastatic breast carcinoma. PLoS One 2012;7:e47998.  Back to cited text no. 10
    
11.Kogo R, Shimamura T, Mimori K, Kawahara K, Imoto S, Sudo T, et al. Long Noncoding RNA HOTAIR Regulates Polycomb-Dependent Chromatin Modification and Is Associated with Poor Prognosis in Colorectal Cancers. Cancer Res 2011;71:6320-6.  Back to cited text no. 11
    
12.Yang Z, Zhou L, Wu LM, Lai MC, Xie HY, Zhang F, et al. Overexpression of long non-coding RNA HOTAIR predicts tumor recurrence in hepatocellular carcinoma patients following liver transplantation. Ann Surg Oncol 2011;18:1243-50.  Back to cited text no. 12
    
13.Geng YJ, Xie SL, Li Q, Ma J, Wang GY. Large intervening non-coding RNA HOTAIR is associated with hepatocellular carcinoma progression. J Int Med Res 2011;39:2119-28.  Back to cited text no. 13
    
14.Ishibashi M, Kogo R, Shibata K, Sawada G, Takahashi Y, Kurashige J, et al. Clinical significance of the expression of long non-coding RNA HOTAIR in primary hepatocellular carcinoma. Oncol Rep 2013;29:946-50.  Back to cited text no. 14
    
15.Kim K, Jutooru I, Chadalapaka G, Johnson G, Frank J, Burghardt R, et al. HOTAIR is a negative prognostic factor and exhibits pro-oncogenic activity in pancreatic cancer. Oncogene 2013;32:1616-25.  Back to cited text no. 15
    
16.Niinuma T, Suzuki H, Nojima M, Nosho K, Yamamoto H, Takamaru H, et al. Upregulation of miR-196a and HOTAIR drive malignant character in gastrointestinal stromal tumors. Cancer Res 2012;72:1126-36.  Back to cited text no. 16
    
17.Nie Y, Liu X, Qu S, Song E, Zou H, Gong C. Long non-coding RNA HOTAIR is an independent prognostic marker for nasopharyngeal carcinoma progression and survival. Cancer Sci 2013;104:458-6.  Back to cited text no. 17
    
18.Li D, Feng J, Wu T, Wang Y, Sun Y, Ren J, et al. Long Intergenic Noncoding RNA HOTAIR Is Overexpressed and Regulates PTEN Methylation in Laryngeal Squamous Cell Carcinoma. Am J Pathol 2013;182:64-70.  Back to cited text no. 18
    
19.Milhem MM, Knutson T, Yang S, Zhu D, Wang X, Leslie KK, et al. Correlation of MTDH/AEG-1 and HOTAIR Expression with Metastasis and Response to Treatment in Sarcoma Patients. J Cancer Sci Ther 2012;S5.Pii:004.  Back to cited text no. 19
    
20.Nikpour P, Emadi-Baygi M, Mohhamad-Hashem F, Maracy MR, Haghjooy-Javanmard S. MSI1 overexpression in diffuse type of gastric cancer. Pathol Res Pract 2013;209:10-3.  Back to cited text no. 20
    
21.Nikpour P, Emadi-Baygi M, Mohammad-Hashem F, Maracy MR, Haghjooy-Javanmard S. Differential expression of ZFX gene in gastric cancer. J Biosci 2012;37:85-90.  Back to cited text no. 21
    
22.Baygi ME, Nikpour P. Deregulation of MTDH gene expression in gastric cancer. Asian Pac J Cancer Prev 2012;13:2833-6.  Back to cited text no. 22
    
23.Nikpour P, Baygi ME, Steinhoff C, Hader C, Luca AC, Mowla SJ, et al. The RNA binding protein Musashi1 regulates apoptosis, gene expression and stress granule formation in urothelial carcinoma cells. J Cell Mol Med 2011;15:1210-24.  Back to cited text no. 23
    
24.Lu L, Zhu G, Zhang C, Deng Q, Katsaros D, Mayne ST, et al. Association of large noncoding RNA HOTAIR expression and its downstream intergenic CpG island methylation with survival in breast cancer. Breast Cancer Res Treat 2012;136:875-83.  Back to cited text no. 24
    
25.Hajjari M, Behmanesh M, Sadeghizadeh M, Zeinoddini M. Up-regulation of HOTAIR long non-coding RNA in human gastric adenocarcinoma tissues. Med Oncol 2013;30:670.  Back to cited text no. 25
    
26.Xu ZY, Yu QM, Du YA, Yang LT, Dong RZ, Huang L, et al. Knockdown of Long Non-coding RNA HOTAIR Suppresses Tumor Invasion and Reverses Epithelial-mesenchymal Transition in Gastric Cancer. Int J Biol Sci 2013;9:587-97.  Back to cited text no. 26
    


    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

  [Table 1]


This article has been cited by
1 HOX transcript antisense RNA is elevated in gastric carcinogenesis and regulated by the NF-?B pathway
Zhun Zhang,Bingbing Fan,Fengyan Liu,Ning Song,Yanping Peng,Wenzheng Ma,Rongtao Ma,Tianyi Dong,Shili Liu
Journal of Cellular Biochemistry. 2019;
[Pubmed] | [DOI]
2 In Situ Hybridization Analysis of Long Non-coding RNAs MALAT1 and HOTAIR in Gastroenteropancreatic Neuroendocrine Neoplasms
Ying-Hsia Chu,Heather Hardin,Jens Eickhoff,Ricardo V. Lloyd
Endocrine Pathology. 2019;
[Pubmed] | [DOI]
3 LncRNAs as potential diagnostic and prognostic biomarkers in gastric cancer: A novel approach to personalized medicine
Sadegh Fattahi,Mohadeseh Kosari-Monfared,Monireh Golpour,Zakieh Emami,Mohammad Ghasemiyan,Maryam Nouri,Haleh Akhavan-Niaki
Journal of Cellular Physiology. 2019;
[Pubmed] | [DOI]
4 Plasma long non-coding RNA HOTAIR as a potential biomarker for gastric cancer
Eman T. Elsayed,Perihan E. Salem,Azaa M. Darwish,Haytham M. Fayed
The International Journal of Biological Markers. 2018; 33(4): 528
[Pubmed] | [DOI]
5 HOTAIR induces the ubiquitination of Runx3 by interacting with Mex3b and enhances the invasion of gastric cancer cells
Meng Xue,Lu-yi Chen,Wei-jia Wang,Ting-ting Su,Liu-hong Shi,Lan Wang,Wen Zhang,Jian-min Si,Liang-jing Wang,Shu-jie Chen
Gastric Cancer. 2018;
[Pubmed] | [DOI]
6 The prognostic value of HOTAIR for predicting long-term prognosis of patients with gastrointestinal cancers
Yi Zhang,Li-juan Wang,Wei-feng Li,Xu Zhang,Xian-jin Yang
Medicine. 2018; 97(26): e11139
[Pubmed] | [DOI]
7 The contrary functions of lncRNA HOTAIR/miR-17-5p/PTEN axis and Shenqifuzheng injection on chemosensitivity of gastric cancer cells
Jianguang Jia,Dankai Zhan,Jing Li,Zhixiang Li,Hongbo Li,Jun Qian
Journal of Cellular and Molecular Medicine. 2018;
[Pubmed] | [DOI]
8 Aberrant expression of PlncRNA-1 and TUG1: potential biomarkers for gastric cancer diagnosis and clinically monitoring cancer progression
Zohreh Baratieh,Zahra Khalaj,Mohammad Amin Honardoost,Modjtaba Emadi-Baygi,Hossein Khanahmad,Mansoor Salehi,Parvaneh Nikpour
Biomarkers in Medicine. 2017;
[Pubmed] | [DOI]
9 No association of single nucleotide polymorphisms within H19 and HOX transcript antisense RNA (HOTAIR) with genetic susceptibility to systemic lupus erythematosus, rheumatoid arthritis, and primary Sjögren’s syndrome in a Chinese Han population
An-Fang Huang,Lin-Chong Su,Hong Jia,Yi Liu,Wang-Dong Xu
Clinical Rheumatology. 2017;
[Pubmed] | [DOI]
10 Analysis of the association of HOTAIR single nucleotide polymorphism (rs920778) and risk of cervical cancer
Haifeng Qiu,Qiuli Liu,Juan Li,Xiujuan Wang,Yuan Wang,Zhongfu Yuan,Jing Li,Dong-Sheng Pei
APMIS. 2016;
[Pubmed] | [DOI]
11 Emerging roles of non-coding RNAs in gastric cancer: Pathogenesis and clinical implications
Shan-Shan Xie
World Journal of Gastroenterology. 2016; 22(3): 1213
[Pubmed] | [DOI]
12 Identification of differentially expressed signatures of long non-coding RNAs associated with different metastatic potentials in gastric cancer
Wu Song,Yu-yi Liu,Jian-jun Peng,Han-hui Liang,Hua-yun Chen,Jian-hui Chen,Wei-ling He,Jian-bo Xu,Shi-rong Cai,Yu-long He
Journal of Gastroenterology. 2016; 51(2): 119
[Pubmed] | [DOI]
13 Long noncoding RNAs in gastric cancer carcinogenesis and metastasis
Mojdeh Nasrollahzadeh-Khakiani,Modjtaba Emadi-Baygi,Wolfgang Arthur Schulz,Parvaneh Nikpour
Briefings in Functional Genomics. 2016; : elw011
[Pubmed] | [DOI]
14 LINC00978 predicts poor prognosis in breast cancer patients
Lin-lin Deng,Ya-yun Chi,Lei Liu,Nai-si Huang,Lin Wang,Jiong Wu
Scientific Reports. 2016; 6: 37936
[Pubmed] | [DOI]
15 Long Noncoding RNAs in Digestive System Malignancies: A Novel Class of Cancer Biomarkers and Therapeutic Targets?
Athina Kladi-Skandali,Kleita Michaelidou,Andreas Scorilas,Konstantinos Mavridis
Gastroenterology Research and Practice. 2015; 2015: 1
[Pubmed] | [DOI]
16 Recent advances in the molecular diagnostics of gastric cancer
Mitsuro Kanda
World Journal of Gastroenterology. 2015; 21(34): 9838
[Pubmed] | [DOI]



 

Top
Previous article  Next article
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

 
  In this article
Abstract
Introduction
Materials and Me...
Results
Discussion
References
Article Figures
Article Tables

 Article Access Statistics
    Viewed1561    
    Printed27    
    Emailed0    
    PDF Downloaded374    
    Comments [Add]    
    Cited by others 16    

Recommend this journal