Enhanced breast cancer progression by mutant p53 is inhibited by the circular RNA circ-Ccnb1
TP53 mutations occur in many different types of cancers that produce mutant p53 proteins. The mutant p53 proteins have lost wild-type p53 activity and gained new functions that contribute to malignant tumor progression. Different p53 mutations create distinct profiles in loss of wild-type p53 activi...
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Published in | Cell death and differentiation Vol. 25; no. 12; pp. 2195 - 2208 |
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Main Authors | , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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Nature Publishing Group UK
01.12.2018
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Abstract | TP53 mutations occur in many different types of cancers that produce mutant p53 proteins. The mutant p53 proteins have lost wild-type p53 activity and gained new functions that contribute to malignant tumor progression. Different p53 mutations create distinct profiles in loss of wild-type p53 activity and gain of functions. Targeting the consequences generated by the great number of p53 mutations would be extremely complex. Therefore, in this study we used a workaround and took advantage of the fact that mutant p53 cannot bind H2AX. Using this, we developed a new approach to repress the acquisition of mutant p53 functions. We show here that the delivery of a circular RNA circ-Ccnb1 inhibited the function of three p53 mutations. By microarray analysis and real-time PCR, we detected decreased circ-Ccnb1 expression levels in patients bearing breast carcinoma. Ectopic delivery of circ-Ccnb1 inhibited tumor growth and extended mouse viability. Using proteomics, we found that circ-Ccnb1 precipitated p53 in p53 wild-type cells, but instead precipitated Bclaf1 in p53 mutant cells. Further experiments showed that H2AX serves as a bridge, linking the interaction of circ-Ccnb1 and wild-type p53, thus allowing Bclaf1 to bind Bcl2 resulting in cell survival. In the p53 mutant cells, circ-Ccnb1 formed a complex with H2AX and Bclaf1, resulting in the induction of cell death. We found that this occurred in three p53 mutations. These results shed light on the possible development of new approaches to inhibit the malignancy of p53 mutations. |
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AbstractList | TP53 mutations occur in many different types of cancers that produce mutant p53 proteins. The mutant p53 proteins have lost wild-type p53 activity and gained new functions that contribute to malignant tumor progression. Different p53 mutations create distinct profiles in loss of wild-type p53 activity and gain of functions. Targeting the consequences generated by the great number of p53 mutations would be extremely complex. Therefore, in this study we used a workaround and took advantage of the fact that mutant p53 cannot bind H2AX. Using this, we developed a new approach to repress the acquisition of mutant p53 functions. We show here that the delivery of a circular RNA circ-Ccnb1 inhibited the function of three p53 mutations. By microarray analysis and real-time PCR, we detected decreased circ-Ccnb1 expression levels in patients bearing breast carcinoma. Ectopic delivery of circ-Ccnb1 inhibited tumor growth and extended mouse viability. Using proteomics, we found that circ-Ccnb1 precipitated p53 in p53 wild-type cells, but instead precipitated Bclaf1 in p53 mutant cells. Further experiments showed that H2AX serves as a bridge, linking the interaction of circ-Ccnb1 and wild-type p53, thus allowing Bclaf1 to bind Bcl2 resulting in cell survival. In the p53 mutant cells, circ-Ccnb1 formed a complex with H2AX and Bclaf1, resulting in the induction of cell death. We found that this occurred in three p53 mutations. These results shed light on the possible development of new approaches to inhibit the malignancy of p53 mutations. TP53 mutations occur in many different types of cancers that produce mutant p53 proteins. The mutant p53 proteins have lost wild-type p53 activity and gained new functions that contribute to malignant tumor progression. Different p53 mutations create distinct profiles in loss of wild-type p53 activity and gain of functions. Targeting the consequences generated by the great number of p53 mutations would be extremely complex. Therefore, in this study we used a workaround and took advantage of the fact that mutant p53 cannot bind H2AX. Using this, we developed a new approach to repress the acquisition of mutant p53 functions. We show here that the delivery of a circular RNA circ-Ccnb1 inhibited the function of three p53 mutations. By microarray analysis and real-time PCR, we detected decreased circ-Ccnb1 expression levels in patients bearing breast carcinoma. Ectopic delivery of circ-Ccnb1 inhibited tumor growth and extended mouse viability. Using proteomics, we found that circ-Ccnb1 precipitated p53 in p53 wild-type cells, but instead precipitated Bclaf1 in p53 mutant cells. Further experiments showed that H2AX serves as a bridge, linking the interaction of circ-Ccnb1 and wild-type p53, thus allowing Bclaf1 to bind Bcl2 resulting in cell survival. In the p53 mutant cells, circ-Ccnb1 formed a complex with H2AX and Bclaf1, resulting in the induction of cell death. We found that this occurred in three p53 mutations. These results shed light on the possible development of new approaches to inhibit the malignancy of p53 mutations. |
Author | Li, Feiya MacKay, Helen J. Ma, Jian He, Alina Kwok, Yat Sze Sheila Wu, Nan Lyu, Juanjuan Yang, Burton B. Peng, Chun Yang, Bing L. Yee, Albert J. Yang, Weining He, Chengyan Awan, Faryal Mehwish Zhang, Chao Dong, Jun Fang, Ling Du, William W. |
Author_xml | – sequence: 1 givenname: Ling surname: Fang fullname: Fang, Ling organization: Sunnybrook Research Institute, and Department of Laboratory Medicine and Pathobiology, University of Toronto, China-Japan Union Hospital of Jilin University – sequence: 2 givenname: William W. surname: Du fullname: Du, William W. organization: Sunnybrook Research Institute, and Department of Laboratory Medicine and Pathobiology, University of Toronto – sequence: 3 givenname: Juanjuan surname: Lyu fullname: Lyu, Juanjuan organization: Sunnybrook Research Institute, and Department of Laboratory Medicine and Pathobiology, University of Toronto – sequence: 4 givenname: Jun surname: Dong fullname: Dong, Jun organization: Sunnybrook Research Institute, and Department of Laboratory Medicine and Pathobiology, University of Toronto – sequence: 5 givenname: Chao surname: Zhang fullname: Zhang, Chao organization: Sunnybrook Research Institute, and Department of Laboratory Medicine and Pathobiology, University of Toronto – sequence: 6 givenname: Weining surname: Yang fullname: Yang, Weining organization: Sunnybrook Research Institute – sequence: 7 givenname: Alina surname: He fullname: He, Alina organization: Sunnybrook Research Institute, and Department of Laboratory Medicine and Pathobiology, University of Toronto – sequence: 8 givenname: Yat Sze Sheila surname: Kwok fullname: Kwok, Yat Sze Sheila organization: Sunnybrook Research Institute, and Department of Laboratory Medicine and Pathobiology, University of Toronto – sequence: 9 givenname: Jian surname: Ma fullname: Ma, Jian organization: Sunnybrook Research Institute, and Department of Laboratory Medicine and Pathobiology, University of Toronto – sequence: 10 givenname: Nan surname: Wu fullname: Wu, Nan organization: Sunnybrook Research Institute, and Department of Laboratory Medicine and Pathobiology, University of Toronto – sequence: 11 givenname: Feiya surname: Li fullname: Li, Feiya organization: Sunnybrook Research Institute, and Department of Laboratory Medicine and Pathobiology, University of Toronto – sequence: 12 givenname: Faryal Mehwish surname: Awan fullname: Awan, Faryal Mehwish organization: Sunnybrook Research Institute, and Department of Laboratory Medicine and Pathobiology, University of Toronto – sequence: 13 givenname: Chengyan surname: He fullname: He, Chengyan organization: China-Japan Union Hospital of Jilin University – sequence: 14 givenname: Bing L. surname: Yang fullname: Yang, Bing L. organization: Sunnybrook Research Institute – sequence: 15 givenname: Chun surname: Peng fullname: Peng, Chun organization: Department of Biology, York University – sequence: 16 givenname: Helen J. surname: MacKay fullname: MacKay, Helen J. organization: Sunnybrook Research Institute – sequence: 17 givenname: Albert J. surname: Yee fullname: Yee, Albert J. organization: Sunnybrook Research Institute – sequence: 18 givenname: Burton B. surname: Yang fullname: Yang, Burton B. email: byang@sri.utoronto.ca organization: Sunnybrook Research Institute, and Department of Laboratory Medicine and Pathobiology, University of Toronto, Sunnybrook Research Institute |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29795334$$D View this record in MEDLINE/PubMed |
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Copyright | The Author(s) 2018 2018. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. ADMC Associazione Differenziamento e Morte Cellulare 2018 |
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Snippet | TP53 mutations occur in many different types of cancers that produce mutant p53 proteins. The mutant p53 proteins have lost wild-type p53 activity and gained... TP53 mutations occur in many different types of cancers that produce mutant p53 proteins. The mutant p53 proteins have lost wild-type p53 activity and gained... |
SourceID | pubmedcentral proquest crossref pubmed springer |
SourceType | Open Access Repository Aggregation Database Index Database Publisher |
StartPage | 2195 |
SubjectTerms | 14 14/19 38/39 45/90 631/337/475/2290 631/45/500 96/95 Apoptosis Biochemistry Biomedical and Life Sciences Breast cancer Breast carcinoma Cell Biology Cell Cycle Analysis Cell death Cell survival Circular RNA Life Sciences Malignancy Mutation p53 Protein Proteomics Ribonucleic acid RNA Stem Cells |
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Title | Enhanced breast cancer progression by mutant p53 is inhibited by the circular RNA circ-Ccnb1 |
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