A Functional Genomic Approach Identifies FAL1 as an Oncogenic Long Noncoding RNA that Associates with BMI1 and Represses p21 Expression in Cancer

In a genome-wide survey on somatic copy-number alterations (SCNAs) of long noncoding RNA (lncRNA) in 2,394 tumor specimens from 12 cancer types, we found that about 21.8% of lncRNA genes were located in regions with focal SCNAs. By integrating bioinformatics analyses of lncRNA SCNAs and expression w...

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Published inCancer cell Vol. 26; no. 3; pp. 344 - 357
Main Authors Hu, Xiaowen, Feng, Yi, Zhang, Dongmei, Zhao, Sihai D., Hu, Zhongyi, Greshock, Joel, Zhang, Youyou, Yang, Lu, Zhong, Xiaomin, Wang, Li-Ping, Jean, Stephanie, Li, Chunsheng, Huang, Qihong, Katsaros, Dionyssios, Montone, Kathleen T., Tanyi, Janos L., Lu, Yiling, Boyd, Jeff, Nathanson, Katherine L., Li, Hongzhe, Mills, Gordon B., Zhang, Lin
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 08.09.2014
Subjects
Animals
Cell Line, Tumor
Cellular Senescence
Cyclin-Dependent Kinase Inhibitor p21 - genetics
Cyclin-Dependent Kinase Inhibitor p21 - metabolism
Female
Gene Expression
Gene Expression Regulation, Neoplastic
Genomics
Humans
Kaplan-Meier Estimate
Mice
Mice, Nude
Neoplasm Transplantation
Neoplasms, Glandular and Epithelial - genetics
Neoplasms, Glandular and Epithelial - metabolism
Neoplasms, Glandular and Epithelial - mortality
Neoplasms, Glandular and Epithelial - pathology
Oncogenes
Ovarian Neoplasms - genetics
Ovarian Neoplasms - metabolism
Ovarian Neoplasms - mortality
Ovarian Neoplasms - pathology
Polycomb Repressive Complex 1 - metabolism
Polymorphism, Single Nucleotide
Protein Stability
RNA Interference
RNA, Long Noncoding - physiology
Transcriptome
Tumor Burden
Online AccessGet full text

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Abstract In a genome-wide survey on somatic copy-number alterations (SCNAs) of long noncoding RNA (lncRNA) in 2,394 tumor specimens from 12 cancer types, we found that about 21.8% of lncRNA genes were located in regions with focal SCNAs. By integrating bioinformatics analyses of lncRNA SCNAs and expression with functional screening assays, we identified an oncogene, focally amplified lncRNA on chromosome 1 (FAL1), whose copy number and expression are correlated with outcomes in ovarian cancer. FAL1 associates with the epigenetic repressor BMI1 and regulates its stability in order to modulate the transcription of a number of genes including CDKN1A. The oncogenic activity of FAL1 is partially attributable to its repression of p21. FAL1-specific siRNAs significantly inhibit tumor growth in vivo. [Display omitted] •Copy number of lncRNA genes is altered in human cancer with high frequency•FAL1 amplification and high expression correlate with poor outcome in cancer•FAL1 stabilizes BMI1 by RNA-protein interaction and represses p21 transcription•Repressing FAL1 expression by siRNA inhibits tumor growth in vivo Large-scale screening by Hu et al. reveals frequent SCNAs of lncRNAs in many cancers. One of these lncRNAs, FAL1, associates with poor outcomes in ovarian cancer patients and stabilizes BMI1 to promote tumor growth.
AbstractList In a genome-wide survey on somatic copy-number alterations (SCNAs) of long noncoding RNA (lncRNA) in 2,394 tumor specimens from 12 cancer types, we found that about 21.8% of lncRNA genes were located in regions with focal SCNAs. By integrating bioinformatics analyses of lncRNA SCNAs and expression with functional screening assays, we identified an oncogene, focally amplified lncRNA on chromosome 1 (FAL1), whose copy number and expression are correlated with outcomes in ovarian cancer. FAL1 associates with the epigenetic repressor BMI1 and regulates its stability in order to modulate the transcription of a number of genes including CDKN1A. The oncogenic activity of FAL1 is partially attributable to its repression of p21. FAL1-specific siRNAs significantly inhibit tumor growth in vivo.
In a genome-wide survey on somatic copy-number alterations (SCNAs) of long noncoding RNA (lncRNA) in 2,394 tumor specimens from 12 cancer types, we found that about 21.8% of lncRNA genes were located in regions with focal SCNAs. By integrating bioinformatics analyses of lncRNA SCNAs and expression with functional screening assays, we identified an oncogene, focally amplified lncRNA on chromosome 1 (FAL1), whose copy number and expression are correlated with outcomes in ovarian cancer. FAL1 associates with the epigenetic repressor BMI1 and regulates its stability in order to modulate the transcription of a number of genes including CDKN1A. The oncogenic activity of FAL1 is partially attributable to its repression of p21. FAL1-specific siRNAs significantly inhibit tumor growth in vivo.In a genome-wide survey on somatic copy-number alterations (SCNAs) of long noncoding RNA (lncRNA) in 2,394 tumor specimens from 12 cancer types, we found that about 21.8% of lncRNA genes were located in regions with focal SCNAs. By integrating bioinformatics analyses of lncRNA SCNAs and expression with functional screening assays, we identified an oncogene, focally amplified lncRNA on chromosome 1 (FAL1), whose copy number and expression are correlated with outcomes in ovarian cancer. FAL1 associates with the epigenetic repressor BMI1 and regulates its stability in order to modulate the transcription of a number of genes including CDKN1A. The oncogenic activity of FAL1 is partially attributable to its repression of p21. FAL1-specific siRNAs significantly inhibit tumor growth in vivo.
In a genome-wide survey on somatic copy-number alterations (SCNAs) of long noncoding RNA (lncRNA) in 2,394 tumor specimens from 12 cancer types, we found that about 21.8% of lncRNA genes were located in regions with focal SCNAs. By integrating bioinformatics analyses of lncRNA SCNAs and expression with functional screening assays, we identified an oncogene, focally amplified lncRNA on chromosome 1 (FAL1), whose copy number and expression are correlated with outcomes in ovarian cancer. FAL1 associates with the epigenetic repressor BMI1 and regulates its stability in order to modulate the transcription of a number of genes including CDKN1A. The oncogenic activity of FAL1 is partially attributable to its repression of p21. FAL1-specific siRNAs significantly inhibit tumor growth in vivo. [Display omitted] •Copy number of lncRNA genes is altered in human cancer with high frequency•FAL1 amplification and high expression correlate with poor outcome in cancer•FAL1 stabilizes BMI1 by RNA-protein interaction and represses p21 transcription•Repressing FAL1 expression by siRNA inhibits tumor growth in vivo Large-scale screening by Hu et al. reveals frequent SCNAs of lncRNAs in many cancers. One of these lncRNAs, FAL1, associates with poor outcomes in ovarian cancer patients and stabilizes BMI1 to promote tumor growth.
Author Feng, Yi
Zhang, Dongmei
Yang, Lu
Hu, Xiaowen
Zhang, Youyou
Zhao, Sihai D.
Lu, Yiling
Li, Chunsheng
Huang, Qihong
Zhang, Lin
Hu, Zhongyi
Tanyi, Janos L.
Li, Hongzhe
Jean, Stephanie
Mills, Gordon B.
Nathanson, Katherine L.
Greshock, Joel
Boyd, Jeff
Zhong, Xiaomin
Montone, Kathleen T.
Wang, Li-Ping
Katsaros, Dionyssios
Author_xml – sequence: 1
  givenname: Xiaowen
  surname: Hu
  fullname: Hu, Xiaowen
  organization: Ovarian Cancer Research Center, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
– sequence: 2
  givenname: Yi
  surname: Feng
  fullname: Feng, Yi
  organization: Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
– sequence: 3
  givenname: Dongmei
  surname: Zhang
  fullname: Zhang, Dongmei
  organization: Ovarian Cancer Research Center, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
– sequence: 4
  givenname: Sihai D.
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  fullname: Zhao, Sihai D.
  organization: Department of Statistics, University of Illinois at Urbana-Champaign, Champaign, IL 61820, USA
– sequence: 5
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  surname: Hu
  fullname: Hu, Zhongyi
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– sequence: 6
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  surname: Greshock
  fullname: Greshock, Joel
  organization: Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
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  surname: Zhang
  fullname: Zhang, Youyou
  organization: Ovarian Cancer Research Center, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
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  surname: Yang
  fullname: Yang, Lu
  organization: Ovarian Cancer Research Center, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
– sequence: 9
  givenname: Xiaomin
  surname: Zhong
  fullname: Zhong, Xiaomin
  organization: Ovarian Cancer Research Center, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
– sequence: 10
  givenname: Li-Ping
  surname: Wang
  fullname: Wang, Li-Ping
  organization: Department of Pathology and Laboratory Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
– sequence: 11
  givenname: Stephanie
  surname: Jean
  fullname: Jean, Stephanie
  organization: Department of Obstetrics and Gynecology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
– sequence: 12
  givenname: Chunsheng
  surname: Li
  fullname: Li, Chunsheng
  organization: Ovarian Cancer Research Center, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
– sequence: 13
  givenname: Qihong
  surname: Huang
  fullname: Huang, Qihong
  organization: Wistar Institute, Philadelphia, PA 19104, USA
– sequence: 14
  givenname: Dionyssios
  surname: Katsaros
  fullname: Katsaros, Dionyssios
  organization: Department of Obstetrics and Gynecology, University of Turin, Turin 10124, Italy
– sequence: 15
  givenname: Kathleen T.
  surname: Montone
  fullname: Montone, Kathleen T.
  organization: Department of Pathology and Laboratory Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
– sequence: 16
  givenname: Janos L.
  surname: Tanyi
  fullname: Tanyi, Janos L.
  organization: Department of Obstetrics and Gynecology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
– sequence: 17
  givenname: Yiling
  surname: Lu
  fullname: Lu, Yiling
  organization: Department of Systems Biology, MD Anderson Cancer Center, Houston, TX 7705, USA
– sequence: 18
  givenname: Jeff
  surname: Boyd
  fullname: Boyd, Jeff
  organization: Cancer Genome Institute, Fox Chase Cancer Center, Philadelphia, PA 19111, USA
– sequence: 19
  givenname: Katherine L.
  surname: Nathanson
  fullname: Nathanson, Katherine L.
  organization: Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
– sequence: 20
  givenname: Hongzhe
  surname: Li
  fullname: Li, Hongzhe
  organization: Department of Biostatistics and Epidemiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
– sequence: 21
  givenname: Gordon B.
  surname: Mills
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  surname: Zhang
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  email: linzhang@mail.med.upenn.edu
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/25203321$$D View this record in MEDLINE/PubMed
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Snippet In a genome-wide survey on somatic copy-number alterations (SCNAs) of long noncoding RNA (lncRNA) in 2,394 tumor specimens from 12 cancer types, we found that...
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SubjectTerms Animals
Cell Line, Tumor
Cellular Senescence
Cyclin-Dependent Kinase Inhibitor p21 - genetics
Cyclin-Dependent Kinase Inhibitor p21 - metabolism
Female
Gene Expression
Gene Expression Regulation, Neoplastic
Genomics
Humans
Kaplan-Meier Estimate
Mice
Mice, Nude
Neoplasm Transplantation
Neoplasms, Glandular and Epithelial - genetics
Neoplasms, Glandular and Epithelial - metabolism
Neoplasms, Glandular and Epithelial - mortality
Neoplasms, Glandular and Epithelial - pathology
Oncogenes
Ovarian Neoplasms - genetics
Ovarian Neoplasms - metabolism
Ovarian Neoplasms - mortality
Ovarian Neoplasms - pathology
Polycomb Repressive Complex 1 - metabolism
Polymorphism, Single Nucleotide
Protein Stability
RNA Interference
RNA, Long Noncoding - physiology
Transcriptome
Tumor Burden
Title A Functional Genomic Approach Identifies FAL1 as an Oncogenic Long Noncoding RNA that Associates with BMI1 and Represses p21 Expression in Cancer
URI https://dx.doi.org/10.1016/j.ccr.2014.07.009
https://www.ncbi.nlm.nih.gov/pubmed/25203321
https://www.proquest.com/docview/1561470179
https://www.proquest.com/docview/1642619908
Volume 26
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