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Role of human noncoding RNAs in the control of tumorigenesis
Open accessAbstract
Related studies showed that the protein PSF represses proto-oncogene transcription, and VL30–1 RNA, a mouse noncoding retroelement RNA, binds and releases PSF from a proto-oncogene, activating transcription. Here we show that this mechanism regulates tumorigenesis in human cells, with human RNAs replacing VL30–1 RNA. A library of human RNA fragments was used to isolate, by affinity chromatography, 5 noncoding RNA fragments that bind to human PSF (hPSF), releasing hPSF from a proto-oncogene and activating transcription. Each of the 5 RNA fragments maps to a different human gene. The tumorigenic function of the hPSF-binding RNAs was tested in a human melanoma line and mouse fibroblast line, by determining the effect of the RNAs on formation of colonies in agar and tumors in mice. ( i ) Expressing in human melanoma cells the RNA fragments individually promoted tumorigenicity. ( ii ) Expressing in human melanoma cells a shRNA, which causes degradation of the endogenous RNA from which an RNA fragment was derived, suppressed tumorigenicity. ( iii ) Expressing in mouse NIH/3T3 cells the RNA fragments individually resulted in transformation to tumorigenic cells. ( iv ) A screen of 9 human tumor lines showed that each line expresses high levels of several hPSF-binding RNAs, relative to the levels in human fibroblast cells. We conclude that human hPSF-binding RNAs drive transformation and tumorigenesis by reversing PSF-mediated repression of proto-oncogene transcription and that dysfunctional regulation of human hPSF-binding RNA expression has a central role in the etiology of human cancer.
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“One of the non-coding RNA fragments that can bind PSF was shown to belong to a member of the HERVK11 group mapped as MER11C 18.”
From Are human endogenous retroviruses pathogenic? An approach to testing the hypothesis (2013) · cites this paper as [18]
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Liu, H., Wang, H., Wu, B., Yao, K., Liao, A., Miao, M., Li, Y., & Yang, W. (2017) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/1440-1681.12804 · Cited by 36
Multidimensional crosstalk between RNA-binding proteins and noncoding RNAs in cancer biology
Li, L., Miao, H., Chang, Y., Yao, H., Zhao, Y., Wu, F., & Song, X. (2021) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2021.03.007 · Cited by 34
Self-citationChen, J., Ouyang, H., An, X., & Liu, S. (2018) · PLoS ONE · doi:10.1371/journal.pone.0191325 · Cited by 34
RetractedLa, Y., He, X., Zhang, L., Di, R., Wang, X., Gan, S., Zhang, X., Zhang, J., Hu, W., & Chu, M. (2020) · Genes · doi:10.3390/genes11030301 · Cited by 33
Long noncoding RNA expression profile of infantile hemangioma identified by microarray analysis
Liu, X., Lv, R., Zhang, L., Xu, G., Bi, J., Gao, F., Zhang, J., Xue, F., Wang, F., Wu, Y.-L., et al. (2016) · Tumor Biology · doi:10.1007/s13277-016-5434-y · Cited by 32
Shen, W., Liang, X., Sun, H., Hoyos, C. L. D., & Crooke, S. T. (2017) · PLoS ONE · doi:10.1371/journal.pone.0173494 · Cited by 31
Long non-coding RNA CCAL/miR-149/FOXM1 axis promotes metastasis in gastric cancer
Luo, X., Wang, G., Bian, Z., Li, X., Zhu, B., Jin, C., & Ju, S. (2018) · Cell Death and Disease · doi:10.1038/s41419-018-0969-z · Cited by 31
Sattarifard, H., Hashemi, M. M., Hassanzarei, S., Narouie, B., & Bahari, G. (2017) · Molecular and Clinical Oncology · doi:10.3892/mco.2017.1462 · Cited by 30
Metadata
- Authors
- Li, L., Feng, T., Lian, Y., Zhang, G., Garen, A., & Song, X.
- Affiliations
- Sichuan University (CN)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2009-08-04
- Volume
- 106
- Issue
- 31
- Pages
- 12956-12961
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2722347
- OpenAlex
- W2037471476
- Cited by
- 185
- References
- 13
- Citations by year
- 2025: 3 · 2024: 5 · 2023: 7 · 2022: 5 · 2021: 11 · 2020: 19 · 2019: 16 · 2018: 12 · 2017: 23 · 2016: 12 · 2015: 14 · 2014: 15 · 2013: 17 · 2012: 13
- FWCI
- 2.91
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China (30700459, 90919005)
- Ministry of Education of the People's Republic of China
- Scientific Research Foundation for Returned Scholars of Ministry of Education (20071108)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- non-coding RNA, PSF, transcriptional repression, carcinogenesis, RNA fragments, melanoma, cancer transformation, shRNA knockdown, tumor suppressor function
- MeSH terms
- PTB-Associated Splicing Factor, Proto-Oncogene Mas, Animals, Cell Line, Cloning, Molecular, Humans, Neoplasms, Proto-Oncogenes, Transcription, Genetic, RNA-Binding Proteins, RNA, Untranslated, NIH 3T3 Cells, Mice
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