A novel protein encoded by the circular form of the SHPRH gene suppresses glioma tumorigenesis

Circular RNAs (circRNAs) are recognized as functional non-coding transcripts in eukaryotic cells. Recent evidence has indicated that even though circRNAs are generally expressed at low levels, they may be involved in many physiological or pathological processes, such as gene regulation, tissue devel...

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Veröffentlicht in:	Oncogene Jg. 37; H. 13; S. 1805 - 1814
Hauptverfasser:	Zhang, Maolei, Huang, Nunu, Yang, Xuesong, Luo, Jingyan, Yan, Sheng, Xiao, Feizhe, Chen, Wenping, Gao, Xinya, Zhao, Kun, Zhou, Huangkai, Li, Ziqiang, Ming, Liu, Xie, Bo, Zhang, Nu
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	London Nature Publishing Group UK 01.03.2018 Nature Publishing Group
Schlagworte:	631/337/384 631/67/1922 Apoptosis Brain cancer Brief Communication Carcinogenesis Cell Biology Cell proliferation DNA helicase Eukaryotes Gene regulation Glioblastoma Glioblastoma cells Glioma Human Genetics Internal Medicine Internal ribosome entry site Medicine Medicine & Public Health MicroRNAs miRNA Oncology Physiology Proliferating cell nuclear antigen Proteasomes Proteins Stop codon Tumor suppressor genes Tumorigenesis Tumorigenicity Tumors Ubiquitin Ubiquitin-protein ligase
ISSN:	0950-9232, 1476-5594, 1476-5594
Online-Zugang:	Volltext
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Abstract	Circular RNAs (circRNAs) are recognized as functional non-coding transcripts in eukaryotic cells. Recent evidence has indicated that even though circRNAs are generally expressed at low levels, they may be involved in many physiological or pathological processes, such as gene regulation, tissue development and carcinogenesis. Although the ‘microRNA sponge’ function is well characterized, most circRNAs do not contain perfect trapping sites for microRNAs, which suggests the possibility that circRNAs have functions that have not yet been defined. In this study, we show that a circRNA containing an open reading frame (ORF) driven by the internal ribosome entry site (IRES) can translate a functional protein. The circular form of the SNF2 histone linker PHD RING helicase (SHPRH) gene encodes a novel protein that we termed SHPRH-146aa. Circular SHPRH (circ-SHPRH) uses overlapping genetic codes to generate a ‘UGA’ stop codon, which results in the translation of the 17 kDa SHPRH-146aa. Both circ-SHPRH and SHPRH-146aa are abundantly expressed in normal human brains and are down-regulated in glioblastoma. The overexpression of SHPRH-146aa in U251 and U373 glioblastoma cells reduces their malignant behavior and tumorigenicity in vitro and in vivo. Mechanistically, SHPRH-146aa protects full-length SHPRH from degradation by the ubiquitin proteasome. Stabilized SHPRH sequentially ubiquitinates proliferating cell nuclear antigen (PCNA) as an E3 ligase, leading to inhibited cell proliferation and tumorigenicity. Our findings provide a novel perspective regarding circRNA function in physiological and pathological processes. Specifically, SHPRH-146aa generated from overlapping genetic codes of circ-SHPRH is a tumor suppressor in human glioblastoma.
AbstractList	Circular RNAs (circRNAs) are recognized as functional non-coding transcripts in eukaryotic cells. Recent evidence has indicated that even though circRNAs are generally expressed at low levels, they may be involved in many physiological or pathological processes, such as gene regulation, tissue development and carcinogenesis. Although the 'microRNA sponge' function is well characterized, most circRNAs do not contain perfect trapping sites for microRNAs, which suggests the possibility that circRNAs have functions that have not yet been defined. In this study, we show that a circRNA containing an open reading frame (ORF) driven by the internal ribosome entry site (IRES) can translate a functional protein. The circular form of the SNF2 histone linker PHD RING helicase (SHPRH) gene encodes a novel protein that we termed SHPRH-146aa. Circular SHPRH (circ-SHPRH) uses overlapping genetic codes to generate a 'UGA' stop codon, which results in the translation of the 17 kDa SHPRH-146aa. Both circ-SHPRH and SHPRH-146aa are abundantly expressed in normal human brains and are down-regulated in glioblastoma. The overexpression of SHPRH-146aa in U251 and U373 glioblastoma cells reduces their malignant behavior and tumorigenicity in vitro and in vivo. Mechanistically, SHPRH-146aa protects full-length SHPRH from degradation by the ubiquitin proteasome. Stabilized SHPRH sequentially ubiquitinates proliferating cell nuclear antigen (PCNA) as an E3 ligase, leading to inhibited cell proliferation and tumorigenicity. Our findings provide a novel perspective regarding circRNA function in physiological and pathological processes. Specifically, SHPRH-146aa generated from overlapping genetic codes of circ-SHPRH is a tumor suppressor in human glioblastoma.Circular RNAs (circRNAs) are recognized as functional non-coding transcripts in eukaryotic cells. Recent evidence has indicated that even though circRNAs are generally expressed at low levels, they may be involved in many physiological or pathological processes, such as gene regulation, tissue development and carcinogenesis. Although the 'microRNA sponge' function is well characterized, most circRNAs do not contain perfect trapping sites for microRNAs, which suggests the possibility that circRNAs have functions that have not yet been defined. In this study, we show that a circRNA containing an open reading frame (ORF) driven by the internal ribosome entry site (IRES) can translate a functional protein. The circular form of the SNF2 histone linker PHD RING helicase (SHPRH) gene encodes a novel protein that we termed SHPRH-146aa. Circular SHPRH (circ-SHPRH) uses overlapping genetic codes to generate a 'UGA' stop codon, which results in the translation of the 17 kDa SHPRH-146aa. Both circ-SHPRH and SHPRH-146aa are abundantly expressed in normal human brains and are down-regulated in glioblastoma. The overexpression of SHPRH-146aa in U251 and U373 glioblastoma cells reduces their malignant behavior and tumorigenicity in vitro and in vivo. Mechanistically, SHPRH-146aa protects full-length SHPRH from degradation by the ubiquitin proteasome. Stabilized SHPRH sequentially ubiquitinates proliferating cell nuclear antigen (PCNA) as an E3 ligase, leading to inhibited cell proliferation and tumorigenicity. Our findings provide a novel perspective regarding circRNA function in physiological and pathological processes. Specifically, SHPRH-146aa generated from overlapping genetic codes of circ-SHPRH is a tumor suppressor in human glioblastoma. Circular RNAs (circRNAs) are recognized as functional non-coding transcripts in eukaryotic cells. Recent evidence has indicated that even though circRNAs are generally expressed at low levels, they may be involved in many physiological or pathological processes, such as gene regulation, tissue development and carcinogenesis. Although the 'microRNA sponge' function is well characterized, most circRNAs do not contain perfect trapping sites for microRNAs, which suggests the possibility that circRNAs have functions that have not yet been defined. In this study, we show that a circRNA containing an open reading frame (ORF) driven by the internal ribosome entry site (IRES) can translate a functional protein. The circular form of the SNF2 histone linker PHD RING helicase (SHPRH) gene encodes a novel protein that we termed SHPRH-146aa. Circular SHPRH (circ-SHPRH) uses overlapping genetic codes to generate a 'UGA' stop codon, which results in the translation of the 17 kDa SHPRH-146aa. Both circ-SHPRH and SHPRH-146aa are abundantly expressed in normal human brains and are down-regulated in glioblastoma. The overexpression of SHPRH-146aa in U251 and U373 glioblastoma cells reduces their malignant behavior and tumorigenicity in vitro and in vivo. Mechanistically, SHPRH-146aa protects full-length SHPRH from degradation by the ubiquitin proteasome. Stabilized SHPRH sequentially ubiquitinates proliferating cell nuclear antigen (PCNA) as an E3 ligase, leading to inhibited cell proliferation and tumorigenicity. Our findings provide a novel perspective regarding circRNA function in physiological and pathological processes. Specifically, SHPRH-146aa generated from overlapping genetic codes of circ-SHPRH is a tumor suppressor in human glioblastoma.
Author	Xie, Bo Luo, Jingyan Yan, Sheng Xiao, Feizhe Yang, Xuesong Zhang, Maolei Chen, Wenping Zhou, Huangkai Ming, Liu Li, Ziqiang Gao, Xinya Zhang, Nu Huang, Nunu Zhao, Kun
Author_xml	– sequence: 1 givenname: Maolei surname: Zhang fullname: Zhang, Maolei organization: Department of Neurosurgery, The 1st Affiliated Hospital of Sun Yat-sen University, Guangdong Provincial Key Laboratory of Pituitary Tumors – sequence: 2 givenname: Nunu surname: Huang fullname: Huang, Nunu organization: Department of Neurosurgery, The 1st Affiliated Hospital of Sun Yat-sen University, Guangdong Provincial Key Laboratory of Pituitary Tumors – sequence: 3 givenname: Xuesong surname: Yang fullname: Yang, Xuesong organization: Department of Neurosurgery, The 1st Affiliated Hospital of Sun Yat-sen University, Guangdong Provincial Key Laboratory of Pituitary Tumors – sequence: 4 givenname: Jingyan surname: Luo fullname: Luo, Jingyan organization: Forevergen Biosciences Center – sequence: 5 givenname: Sheng surname: Yan fullname: Yan, Sheng organization: Department of Neurosurgery, The 1st Affiliated Hospital of Sun Yat-sen University, Guangdong Provincial Key Laboratory of Pituitary Tumors – sequence: 6 givenname: Feizhe surname: Xiao fullname: Xiao, Feizhe organization: Department of Scientific Research Section, The 1st Affiliated Hospital of Sun Yat-sen University – sequence: 7 givenname: Wenping surname: Chen fullname: Chen, Wenping organization: Department of Neurosurgery, The 1st Affiliated Hospital of Sun Yat-sen University, Guangdong Provincial Key Laboratory of Pituitary Tumors – sequence: 8 givenname: Xinya surname: Gao fullname: Gao, Xinya organization: Department of Neurosurgery, The 1st Affiliated Hospital of Sun Yat-sen University, Guangdong Provincial Key Laboratory of Pituitary Tumors – sequence: 9 givenname: Kun surname: Zhao fullname: Zhao, Kun organization: Department of Neurosurgery, The 1st Affiliated Hospital of Sun Yat-sen University, Guangdong Provincial Key Laboratory of Pituitary Tumors – sequence: 10 givenname: Huangkai surname: Zhou fullname: Zhou, Huangkai organization: Department of Neurosurgery, The 1st Affiliated Hospital of Sun Yat-sen University, Guangdong Provincial Key Laboratory of Pituitary Tumors – sequence: 11 givenname: Ziqiang surname: Li fullname: Li, Ziqiang organization: Guangzhou Geneseed Anti-Aging Research Institute – sequence: 12 givenname: Liu surname: Ming fullname: Ming, Liu organization: Guangzhou Geneseed Anti-Aging Research Institute – sequence: 13 givenname: Bo surname: Xie fullname: Xie, Bo organization: Department of Pharmacology, Zhongshan School of Medicine, Sun Yat-sen University – sequence: 14 givenname: Nu surname: Zhang fullname: Zhang, Nu email: zhangnu2@mail.sysu.edu.cn organization: Department of Neurosurgery, The 1st Affiliated Hospital of Sun Yat-sen University, Guangdong Provincial Key Laboratory of Pituitary Tumors
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/29343848$$D View this record in MEDLINE/PubMed
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Snippet	Circular RNAs (circRNAs) are recognized as functional non-coding transcripts in eukaryotic cells. Recent evidence has indicated that even though circRNAs are...
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SubjectTerms	631/337/384 631/67/1922 Apoptosis Brain cancer Brief Communication Carcinogenesis Cell Biology Cell proliferation DNA helicase Eukaryotes Gene regulation Glioblastoma Glioblastoma cells Glioma Human Genetics Internal Medicine Internal ribosome entry site Medicine Medicine & Public Health MicroRNAs miRNA Oncology Physiology Proliferating cell nuclear antigen Proteasomes Proteins Stop codon Tumor suppressor genes Tumorigenesis Tumorigenicity Tumors Ubiquitin Ubiquitin-protein ligase
Title	A novel protein encoded by the circular form of the SHPRH gene suppresses glioma tumorigenesis
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