VprBP/DCAF1 Regulates the Degradation and Nonproteolytic Activation of the Cell Cycle Transcription Factor FoxM1
The oncogenic transcription factor FoxM1 plays a vital role in cell cycle progression, is activated in numerous human malignancies, and is linked to chromosome instability. We characterize here a cullin 4-based E3 ubiquitin ligase and its substrate receptor, VprBP/DCAF1 (CRL4 VprBP ), which we show...
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| Published in | Molecular and cellular biology Vol. 37; no. 13 |
|---|---|
| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Taylor & Francis
01.07.2017
American Society for Microbiology |
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| Abstract | The oncogenic transcription factor FoxM1 plays a vital role in cell cycle progression, is activated in numerous human malignancies, and is linked to chromosome instability. We characterize here a cullin 4-based E3 ubiquitin ligase and its substrate receptor, VprBP/DCAF1 (CRL4
VprBP
), which we show regulate FoxM1 ubiquitylation and degradation. Paradoxically, we also found that the substrate receptor VprBP is a potent FoxM1 activator. VprBP depletion reduces expression of FoxM1 target genes and impairs mitotic entry, whereas ectopic VprBP expression strongly activates a FoxM1 transcriptional reporter. VprBP binding to CRL4 is reduced during mitosis, and our data suggest that VprBP activation of FoxM1 is ligase independent. This implies a nonproteolytic activation mechanism that is reminiscent of, yet distinct from, the ubiquitin-dependent transactivation of the oncoprotein Myc by other E3s. Significantly, VprBP protein levels were upregulated in high-grade serous ovarian patient tumors, where the FoxM1 signature is amplified. These data suggest that FoxM1 abundance and activity are controlled by VprBP and highlight the functional repurposing of E3 ligase substrate receptors independent of the ubiquitin system. |
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| AbstractList | The oncogenic transcription factor FoxM1 plays a vital role in cell cycle progression, is activated in numerous human malignancies, and is linked to chromosome instability. We characterize here a cullin 4-based E3 ubiquitin ligase and its substrate receptor, VprBP/DCAF1 (CRL4
), which we show regulate FoxM1 ubiquitylation and degradation. Paradoxically, we also found that the substrate receptor VprBP is a potent FoxM1 activator. VprBP depletion reduces expression of FoxM1 target genes and impairs mitotic entry, whereas ectopic VprBP expression strongly activates a FoxM1 transcriptional reporter. VprBP binding to CRL4 is reduced during mitosis, and our data suggest that VprBP activation of FoxM1 is ligase independent. This implies a nonproteolytic activation mechanism that is reminiscent of, yet distinct from, the ubiquitin-dependent transactivation of the oncoprotein Myc by other E3s. Significantly, VprBP protein levels were upregulated in high-grade serous ovarian patient tumors, where the FoxM1 signature is amplified. These data suggest that FoxM1 abundance and activity are controlled by VprBP and highlight the functional repurposing of E3 ligase substrate receptors independent of the ubiquitin system. The oncogenic transcription factor FoxM1 plays a vital role in cell cycle progression, is activated in numerous human malignancies, and is linked to chromosome instability. We characterize here a cullin 4-based E3 ubiquitin ligase and its substrate receptor, VprBP/DCAF1 (CRL4 VprBP ), which we show regulate FoxM1 ubiquitylation and degradation. Paradoxically, we also found that the substrate receptor VprBP is a potent FoxM1 activator. VprBP depletion reduces expression of FoxM1 target genes and impairs mitotic entry, whereas ectopic VprBP expression strongly activates a FoxM1 transcriptional reporter. VprBP binding to CRL4 is reduced during mitosis, and our data suggest that VprBP activation of FoxM1 is ligase independent. This implies a nonproteolytic activation mechanism that is reminiscent of, yet distinct from, the ubiquitin-dependent transactivation of the oncoprotein Myc by other E3s. Significantly, VprBP protein levels were upregulated in high-grade serous ovarian patient tumors, where the FoxM1 signature is amplified. These data suggest that FoxM1 abundance and activity are controlled by VprBP and highlight the functional repurposing of E3 ligase substrate receptors independent of the ubiquitin system. |
| Author | Bird, Kelly Choudhury, Rajarshi Zhou, Chunxiao Bowers, Albert Kernan, Jennifer L. Bae-Jump, Victoria Emanuele, Michael J. Mills, Christine A. Arceci, Anthony Wang, Xianxi |
| Author_xml | – sequence: 1 givenname: Xianxi surname: Wang fullname: Wang, Xianxi organization: Lineberger Comprehensive Cancer Center, The University of North Carolina at Chapel Hill – sequence: 2 givenname: Anthony surname: Arceci fullname: Arceci, Anthony organization: Curriculum in Genetics and Molecular Biology, The University of North Carolina at Chapel Hill – sequence: 3 givenname: Kelly surname: Bird fullname: Bird, Kelly organization: Eshelman School of Pharmacy, Division of Chemical Biology and Medicinal Chemistry, The University of North Carolina at Chapel Hill – sequence: 4 givenname: Christine A. surname: Mills fullname: Mills, Christine A. organization: Department of Pharmacology, The University of North Carolina at Chapel Hill – sequence: 5 givenname: Rajarshi surname: Choudhury fullname: Choudhury, Rajarshi organization: Lineberger Comprehensive Cancer Center, The University of North Carolina at Chapel Hill – sequence: 6 givenname: Jennifer L. surname: Kernan fullname: Kernan, Jennifer L. organization: Department of Pharmacology, The University of North Carolina at Chapel Hill – sequence: 7 givenname: Chunxiao surname: Zhou fullname: Zhou, Chunxiao organization: Division of Gynecologic Oncology, The University of North Carolina at Chapel Hill – sequence: 8 givenname: Victoria surname: Bae-Jump fullname: Bae-Jump, Victoria organization: Division of Gynecologic Oncology, The University of North Carolina at Chapel Hill – sequence: 9 givenname: Albert surname: Bowers fullname: Bowers, Albert organization: Eshelman School of Pharmacy, Division of Chemical Biology and Medicinal Chemistry, The University of North Carolina at Chapel Hill – sequence: 10 givenname: Michael J. surname: Emanuele fullname: Emanuele, Michael J. email: emanuele@email.unc.edu organization: Department of Pharmacology, The University of North Carolina at Chapel Hill |
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| Keywords | cullin ring ligase cell cycle ubiquitination FoxM1 transcriptional regulation |
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| SubjectTerms | Carrier Proteins - genetics Carrier Proteins - metabolism Cell Cycle Chromosomal Instability cullin ring ligase Cystadenocarcinoma, Serous - genetics Cystadenocarcinoma, Serous - metabolism Cystadenocarcinoma, Serous - pathology Female Forkhead Box Protein M1 - genetics Forkhead Box Protein M1 - metabolism FoxM1 Gene Expression Regulation, Neoplastic Humans Ovarian Neoplasms - genetics Ovarian Neoplasms - metabolism Ovarian Neoplasms - pathology Protein Serine-Threonine Kinases Proteolysis transcriptional regulation Tumor Cells, Cultured Ubiquitin-Protein Ligases - genetics Ubiquitin-Protein Ligases - metabolism Ubiquitination |
| Title | VprBP/DCAF1 Regulates the Degradation and Nonproteolytic Activation of the Cell Cycle Transcription Factor FoxM1 |
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