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      LncRNA FENDRR-mediated tumor suppression and tumor-immune microenvironment changes in non-small cell lung cancer

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          Abstract

          Background

          Long noncoding RNAs (lncRNAs) play a key role in the development and progression of many cancer types, including lung cancer. The objective of this study is to examine the function and molecular mechanism of lncRNAs involved in non-small cell lung cancer (NSCLC).

          Methods

          First, 7 lung cancer-related differentially expressed LncRNAs were screened from 2 genomic profiling datasets. Of these lncRNAs, FOXF1 adjacent noncoding developmental regulatory RNA (FENDRR) was found to be the only one that was both significantly down-regulated in the patients with advanced pathology and negatively correlated with prognosis. Thus, lncRNA FENDRR was further studied in this project. Clinical correlation analysis was further conducted in the GSE30219 dataset and 73 paired lung cancer and noncancerous tissues stored in our lab; Subsequently, we evaluated FENDRR coding potential with the Phylogenetic Codon Substitution Frequencies (PhyloCSF), Coding-Potential Assessment Tool (CPAT), and Coding Potential Calculator (CPC) online analytical tool. The cell growth ability was measured by CCK8 assay and clonogenicity assay, the metastatic capacities were evaluated using Transwell migration and invasion assays. Mechanistically, we analyzed the correlation of FENDRR function in NSCLC with immune response by utilizing The Cancer Genome Atlas (TCGA) data.

          Results

          Results indicated a negative clinical correlation of FENDRR. Coding potential analysis showed FENDRR as a noncoding RNA. Elevated expression of FENDRR led to cell growth arrest, inhibition of proliferative ability, declined migration and invasion potential of NSCLC cells in vitro. Mechanistically, we discovered that FENDRR expression might be involved in aberrant immune response regulation.

          Conclusions

          Taken together, our results provide a greater understanding of lncRNA FENDRR as a tumor suppressor with respect to tumor-immune interactions in NSCLC.

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          Most cited references45

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          Hallmarks of Cancer: The Next Generation

          Douglas Hanahan, Robert A. Weinberg (2011)
          The hallmarks of cancer comprise six biological capabilities acquired during the multistep development of human tumors. The hallmarks constitute an organizing principle for rationalizing the complexities of neoplastic disease. They include sustaining proliferative signaling, evading growth suppressors, resisting cell death, enabling replicative immortality, inducing angiogenesis, and activating invasion and metastasis. Underlying these hallmarks are genome instability, which generates the genetic diversity that expedites their acquisition, and inflammation, which fosters multiple hallmark functions. Conceptual progress in the last decade has added two emerging hallmarks of potential generality to this list-reprogramming of energy metabolism and evading immune destruction. In addition to cancer cells, tumors exhibit another dimension of complexity: they contain a repertoire of recruited, ostensibly normal cells that contribute to the acquisition of hallmark traits by creating the "tumor microenvironment." Recognition of the widespread applicability of these concepts will increasingly affect the development of new means to treat human cancer. Copyright © 2011 Elsevier Inc. All rights reserved.
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            A coding-independent function of gene and pseudogene mRNAs regulates tumour biology

            Laura Poliseno, Leonardo Salmena, JiangWen Zhang … (2010)
            The canonical role of messenger RNA (mRNA) is to deliver protein-coding information to sites of protein synthesis. However, given that microRNAs bind to RNAs, we hypothesized that RNAs possess a biological role in cancer cells that relies upon their ability to compete for microRNA binding and is independent of their protein-coding function. As a paradigm for the protein-coding-independent role of RNAs, we describe the functional relationship between the mRNAs produced by the PTEN tumour suppressor gene and its pseudogene (PTENP1) and the critical consequences of this interaction. We find that PTENP1 is biologically active as determined by its ability to regulate cellular levels of PTEN, and that it can exert a growth-suppressive role. We also show that PTENP1 locus is selectively lost in human cancer. We extend our analysis to other cancer-related genes that possess pseudogenes, such as oncogenic KRAS. Further, we demonstrate that the transcripts of protein coding genes such as PTEN are also biologically active. Together, these findings attribute a novel biological role to expressed pseudogenes, as they can regulate coding gene expression, and reveal a non-coding function for mRNAs.
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              The GENCODE v7 catalog of human long noncoding RNAs: Analysis of their gene structure, evolution, and expression

              Thomas Derrien, Rory Johnson, Giovanni Bussotti … (2012)
              The human genome contains many thousands of long noncoding RNAs (lncRNAs). While several studies have demonstrated compelling biological and disease roles for individual examples, analytical and experimental approaches to investigate these genes have been hampered by the lack of comprehensive lncRNA annotation. Here, we present and analyze the most complete human lncRNA annotation to date, produced by the GENCODE consortium within the framework of the ENCODE project and comprising 9277 manually annotated genes producing 14,880 transcripts. Our analyses indicate that lncRNAs are generated through pathways similar to that of protein-coding genes, with similar histone-modification profiles, splicing signals, and exon/intron lengths. In contrast to protein-coding genes, however, lncRNAs display a striking bias toward two-exon transcripts, they are predominantly localized in the chromatin and nucleus, and a fraction appear to be preferentially processed into small RNAs. They are under stronger selective pressure than neutrally evolving sequences—particularly in their promoter regions, which display levels of selection comparable to protein-coding genes. Importantly, about one-third seem to have arisen within the primate lineage. Comprehensive analysis of their expression in multiple human organs and brain regions shows that lncRNAs are generally lower expressed than protein-coding genes, and display more tissue-specific expression patterns, with a large fraction of tissue-specific lncRNAs expressed in the brain. Expression correlation analysis indicates that lncRNAs show particularly striking positive correlation with the expression of antisense coding genes. This GENCODE annotation represents a valuable resource for future studies of lncRNAs.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Transl Cancer Res
                Journal ID (iso-abbrev): Transl Cancer Res
                Journal ID (publisher-id): TCR
                Title: Translational Cancer Research
                Publisher: AME Publishing Company
                ISSN (Print): 2218-676X
                ISSN (Electronic): 2219-6803
                Publication date (Print and electronic): June 2020
                Publication date (Print): June 2020
                Volume: 9
                Issue: 6
                Pages: 3946-3959
                Affiliations
                [1]deptFudan University Shanghai Cancer Center, Shanghai Medical College , Fudan University , Shanghai, China
                Author notes

                Contributions: (I) Conception and design: H Pan, T Yu, X Liu, M Yan; (II) Administrative support: M Yan; (III) Provision of study materials or patients: H Pan, T Yu, L Sun, W Chai; (IV) Collection and assembly of data: H Pan, T Yu, L Sun, W Chai; (V) Data analysis and interpretation: H Pan, T Yu; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

                [#]

                These authors contributed equally to this work.

                Correspondence to: Mingxia Yan; Xiaoli Liu. Fudan University Shanghai Cancer Center, Shanghai Medical College, Fudan University, No. 688, Hongqu Road, Shanghai 200032, China. Email: mingxia_yan@ 123456126.com ; liuxiaoli79@ 123456163.com .
                Article
                Publisher ID: tcr-09-06-3946
                DOI: 10.21037/tcr-20-2147
                PMC ID: 8797579
                PubMed ID: 35117761
                SO-VID: a1f5534d-7bda-4579-8df6-95e7ada372ba
                Copyright © 2020 Translational Cancer Research. All rights reserved.
                License:

                Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

                History
                Date received : 23 May 2020
                Date accepted : 15 June 2020
                Funding
                Funded by: the National Natural Science Foundation of China
                Award ID: grant No. 81702846
                Award ID: grant No. 81972173
                Funded by: Shanghai Science and Technology Committee Foundation
                Award ID: grant No. 19140900800
                Award ID: grant No. 18140903700
                Funded by: the Shanghai Health and Family Planning Commission Research Fund
                Award ID: grant No. 20174Y0183
                Categories
                Subject: Original Article

                Keywords: long noncoding rna (lncrna),foxf1 adjacent noncoding developmental regulatory rna (fendrr),tumor progression,immune regulation,non-small cell lung cancer (nsclc)
                Data availability:
                Keywords: long noncoding rna (lncrna), foxf1 adjacent noncoding developmental regulatory rna (fendrr), tumor progression, immune regulation, non-small cell lung cancer (nsclc)

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