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      A novel long noncoding RNA HOXC-AS3 mediates tumorigenesis of gastric cancer by binding to YBX1

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          Abstract

          Background

          Recently, increasing evidence shows that long noncoding RNAs (lncRNAs) play a significant role in human tumorigenesis. However, the function of lncRNAs in human gastric cancer remains largely unknown.

          Results

          By using publicly available expression profiling data from gastric cancer and integrating bioinformatics analyses, we screen and identify a novel lncRNA, HOXC-AS3. HOXC-AS3 is significantly increased in gastric cancer tissues and is correlated with clinical outcomes of gastric cancer. In addition, HOXC-AS3 regulates cell proliferation and migration both in vitro and in vivo. RNA-seq analysis reveals that HOXC-AS3 knockdown preferentially affects genes that are linked to proliferation and migration. Mechanistically, we find that HOXC-AS3 is obviously activated by gain of H3K4me3 and H3K27ac, both in cells and in tissues. RNA pull-down mass spectrometry analysis identifies that YBX1 interacts with HOXC-AS3, and RNA-seq analysis finds a marked overlap in genes differentially expressed after YBX1 knockdown and those transcriptionally regulated by HOXC-AS3, suggesting that YBX1 participates in HOXC-AS3-mediated gene transcriptional regulation in the tumorigenesis of gastric cancer.

          Conclusions

          Together, our data demonstrate that abnormal histone modification-activated HOXC-AS3 may play important roles in gastric cancer oncogenesis and may serve as a target for gastric cancer diagnosis and therapy.

          Electronic supplementary material

          The online version of this article (10.1186/s13059-018-1523-0) contains supplementary material, which is available to authorized users.

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          The Hox genes and their roles in oncogenesis.

          Nilay Shah, Saraswati Sukumar (2010)
          Hox genes, a highly conserved subgroup of the homeobox superfamily, have crucial roles in development, regulating numerous processes including apoptosis, receptor signalling, differentiation, motility and angiogenesis. Aberrations in Hox gene expression have been reported in abnormal development and malignancy, indicating that altered expression of Hox genes could be important for both oncogenesis and tumour suppression, depending on context. Therefore, Hox gene expression could be important in diagnosis and therapy.
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            Modulating Hox gene functions during animal body patterning.

            Joseph Pearson, Derek Lemons, William McGinnis (2005)
            With their power to shape animal morphology, few genes have captured the imagination of biologists as the evolutionarily conserved members of the Hox clusters have done. Recent research has provided new insight into how Hox proteins cause morphological diversity at the organismal and evolutionary levels. Furthermore, an expanding collection of sequences that are directly regulated by Hox proteins provides information on the specificity of target-gene activation, which might allow the successful prediction of novel Hox-response genes. Finally, the recent discovery of microRNA genes within the Hox gene clusters indicates yet another level of control by Hox genes in development and evolution.
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              LncRNA HOXA11-AS Promotes Proliferation and Invasion of Gastric Cancer by Scaffolding the Chromatin Modification Factors PRC2, LSD1, and DNMT1.

              Ming Sun, Fengqi Nie, Yunfei Wang … (2016)
              Long noncoding RNAs (lncRNA) have been implicated in human cancer but their mechanisms of action are mainly undocumented. In this study, we investigated lncRNA alterations that contribute to gastric cancer through an analysis of The Cancer Genome Atlas RNA sequencing data and other publicly available microarray data. Here we report the gastric cancer-associated lncRNA HOXA11-AS as a key regulator of gastric cancer development and progression. Patients with high HOXA11-AS expression had a shorter survival and poorer prognosis. In vitro and in vivo assays of HOXA11-AS alterations revealed a complex integrated phenotype affecting cell growth, migration, invasion, and apoptosis. Strikingly, high-throughput sequencing analysis after HOXA11-AS silencing highlighted alterations in cell proliferation and cell-cell adhesion pathways. Mechanistically, EZH2 along with the histone demethylase LSD1 or DNMT1 were recruited by HOXA11-AS, which functioned as a scaffold. HOXA11-AS also functioned as a molecular sponge for miR-1297, antagonizing its ability to repress EZH2 protein translation. In addition, we found that E2F1 was involved in HOXA11-AS activation in gastric cancer cells. Taken together, our findings support a model in which the EZH2/HOXA11-AS/LSD1 complex and HOXA11-AS/miR-1297/EZH2 cross-talk serve as critical effectors in gastric cancer tumorigenesis and progression, suggesting new therapeutic directions in gastric cancer. Cancer Res; 76(21); 6299-310. ©2016 AACR.
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                Author and article information

                Contributors
                Erbao Zhang: erbaozhang@njmu.edu.cn
                Dandan Yin: +86-025-83626321 , jsnydandan@sina.com
                Liang Han: hanliang_njmu@sina.com
                Wei De: +86-025-8686 2728 , dewei_njmu@sina.com
                Journal
                Journal ID (nlm-ta): Genome Biol
                Journal ID (iso-abbrev): Genome Biol
                Title: Genome Biology
                Publisher: BioMed Central (London )
                ISSN (Print): 1474-7596
                ISSN (Electronic): 1474-760X
                Publication date (Electronic): 4 October 2018
                Publication date PMC-release: 4 October 2018
                Publication date Collection: 2018
                Volume: 19
                Electronic Location Identifier: 154
                Affiliations
                [1 ]ISNI 0000 0000 9255 8984, GRID grid.89957.3a, Department of Epidemiology and Biostatistics, , Jiangsu Key Lab of Cancer Biomarkers, Prevention and Treatment, Collaborative Innovation Center for Cancer Personalized Medicine, School of Public Health, Nanjing Medical University, ; Nanjing, Jiangsu People’s Republic of China
                [2 ]ISNI 0000 0000 9255 8984, GRID grid.89957.3a, Department of Biochemistry and Molecular Biology, , Nanjing Medical University, ; Nanjing, Jiangsu People’s Republic of China
                [3 ]GRID grid.452511.6, Department of Oncology, , Second Affiliated Hospital of Nanjing Medical University, ; Nanjing, Jiangsu People’s Republic of China
                [4 ]GRID grid.452817.d, Department of Oncology, , The Affiliated Jiangyin Hospital of Southeast University Medical College, ; Jiangyin, Jiangsu People’s Republic of China
                [5 ]ISNI 0000 0004 1799 0784, GRID grid.412676.0, Department of Oncology, , First Affiliated Hospital of Nanjing Medical University, ; Nanjing, Jiangsu People’s Republic of China
                [6 ]ISNI 0000 0004 1800 0658, GRID grid.443480.f, Huaihai Institute of Technology, ; Lianyungang, Jiangsu People’s Republic of China
                [7 ]Department of Oncology, Nanjing First Hospital, Nanjing Medical University, Nanjing, Jiangsu People’s Republic of China
                [8 ]GRID grid.452675.7, Cancer Research and Biotherapy Center, , Nanjing Second Hospital, the Second Affiliated Hospital of Southeast University, ; Nanjing, Jiangsu People’s Republic of China
                [9 ]ISNI 0000 0004 1758 0558, GRID grid.452207.6, Department of Oncology, , Xuzhou Central Hospital, Affiliated Xuzhou Hospital, College of Medicine, Southeast University, ; Xuzhou, Jiangsu People’s Republic of China
                [10 ]ISNI 0000 0000 9927 0537, GRID grid.417303.2, Xuzhou Clinical School of Xuzhou Medical University, ; Xuzhou, Jiangsu People’s Republic of China
                Article
                Publisher ID: 1523
                DOI: 10.1186/s13059-018-1523-0
                PMC ID: 6172843
                PubMed ID: 30286788
                SO-VID: afd5b6d9-797d-424f-aa81-297ce7cdefdd
                Copyright © © The Author(s). 2018
                License:

                Open AccessThis 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.

                History
                Date received : 30 January 2018
                Date accepted : 3 September 2018
                Categories
                Subject: Research
                Custom metadata
                issue-copyright-statement © The Author(s) 2018

                ScienceOpen disciplines: Genetics
                Keywords: histone modification,hoxc-as3,ybx1,gc
                Data availability:
                ScienceOpen disciplines: Genetics
                Keywords: histone modification, hoxc-as3, ybx1, gc

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