Cited by 88Cancer-related Molecular PathwaysUbiquitin and proteasome pathwaysAutophagy in Disease and Therapy

USP15-dependent lysosomal pathway controls p53-R175H turnover in ovarian cancer cells

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Padmanabhan, Achuth, Candelaria, Nicholes, Wong, Kwong-Kwok, Nikolai, Bryan C., Lonard, David M., O’Malley, Bert W., Richards, JoAnne S.·2018·Nature Communications

Abstract

Gain-of-function p53 mutants such as p53-R175H form stable aggregates that accumulate in cells and play important roles in cancer progression. Selective degradation of gain-of-function p53 mutants has emerged as a highly attractive therapeutic strategy to target cancer cells harboring specific p53 mutations. We identified a small molecule called MCB-613 to cause rapid ubiquitination, nuclear export, and degradation of p53-R175H through a lysosome-mediated pathway, leading to catastrophic cancer cell death. In contrast to its effect on the p53-R175H mutant, MCB-613 causes slight stabilization of p53-WT and has weaker effects on other p53 gain-of-function mutants. Using state-of-the-art genetic and chemical approaches, we identified the deubiquitinase USP15 as the mediator of MCB-613’s effect on p53-R175H, and established USP15 as a selective upstream regulator of p53-R175H in ovarian cancer cells. These results confirm that distinct pathways regulate the turnover of p53-WT and the different p53 mutants and open new opportunities to selectively target them.

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  • USP15 shows dual effects in tumorigenesis; USP15 copy number is increased in glioblastoma, breast cancer, and ovarian cancer, but decreased in pancreatic cancer.

    “Due to the conflicting functions of substrates, USP15 shows dual effects in tumorigenesis. For instance, USP15 copy number is increased in glioblastoma, breast cancer, and ovarian cancer, but decreased in pancreatic cancer40,52,55–58.”

    From Proteostatic reactivation of the developmental transcription factor TBX3 drives BRAF/MAPK-mediated tumorigenesis (2024) · cites this paper as [55]

    The Results section (page unavailable) states that USP15 is amplified in ovarian cancer, glioblastoma, and breast cancer, supporting the increased-copy-number portion of the claim. The passages found do not report decreased USP15 copy number in pancreatic cancer or establish that conflicting substrate functions give USP15 dual effects in tumorigenesis. (LLM, conf=0.88)

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Research works printed but not linked: 36

  1. [1]Freed-Pastor WA Prives C Mutantp53: one name, many proteins Genes Dev. 2012 26 1268 1286 10.1101/gad.190678.112 22713868 PMC3387655 · DOI
  2. [2]Shaw PH The role of p53 in cell cycle regulation Pathol. Res. Pract. 1996 192 669 675 10.1016/S0344-0338(96)80088-4 8880867 · DOI
  3. [3]Vousden KH Lu X Live or let die: the cell’s response to p53 Nat. Rev. Cancer 2002 2 594 604 10.1038/nrc864 12154352 · DOI
  4. [6]Donehower LA Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours Nature 1992 356 215 221 10.1038/356215a0 1552940 · DOI · Paper page
  5. [7]Drosten M Loss of p53 induces cell proliferation via Ras-independent activation of the Raf/Mek/Erk signaling pathway Proc. Natl Acad. Sci. USA 2014 111 15155 15160 10.1073/pnas.1417549111 25288756 PMC4210339 · DOI · Paper page
  6. [8]Yeo CQ p53 maintains genomic stability by preventing interference between transcription and replication Cell Rep. 2016 15 132 146 10.1016/j.celrep.2016.03.011 27052176 · DOI
  7. [9]Vogelstein B Lane D Levine AJ Surfing the p53 network Nature 2000 408 307 310 10.1038/35042675 11099028 · DOI · Paper page
  8. [10]Cole AJ Assessing mutant p53 in primary high-grade serous ovarian cancer using immunohistochemistry and massively parallel sequencing Sci. Rep. 2016 6 26191 10.1038/srep26191 27189670 PMC4870633 · DOI
  9. [11]Bertheau P p53 in breast cancer subtypes and new insights into response to chemotherapy Breast 2013 22 S27 S29 10.1016/j.breast.2013.07.005 24074787 · DOI
  10. [12]Agrawal N Exome sequencing of head and neck squamous cell carcinoma reveals inactivating mutations in NOTCH1 Science 2011 333 1154 1157 10.1126/science.1206923 21798897 PMC3162986 · DOI
  11. [14]Rivlin N Brosh R Oren M Rotter V Mutations in the p53 tumor suppressor gene: important milestones at the various steps of tumorigenesis Genes Cancer 2011 2 466 474 10.1177/1947601911408889 21779514 PMC3135636 · DOI · Paper page
  12. [15]Campbell C Quinn AG Ro YS Angus B Rees JL p53 mutations are common and early events that precede tumor invasion in squamous cell neoplasia of the skin J. Invest. Dermatol. 1993 100 746 748 10.1111/1523-1747.ep12475717 8496613 · DOI
  13. [16]Wang X Sun Q TP53 mutations, expression and interaction networks in human cancers Oncotarget 2017 8 624 643 27880943 PMC5352183
  14. [17]Brachova P Thiel KW Leslie KK The consequence of oncomorphic TP53 mutations in ovarian cancer Int. J. Mol. Sci. 2013 14 19257 19275 10.3390/ijms140919257 24065105 PMC3794832 · DOI
  15. [18]Frum RA Grossman SR Mechanisms of mutant p53 stabilization in cancer Sub-Cell. Biochem. 2014 85 187 197 10.1007/978-94-017-9211-0_10 25201195 · DOI
  16. [19]Chen L The isolation of an RNA aptamer targeting to p53 protein with single amino acid mutation Proc. Natl Acad. Sci. USA 2015 112 10002 10007 10.1073/pnas.1502159112 26216949 PMC4538674 · DOI
  17. [21]Wang L Characterization of a steroid receptor coactivator small molecule stimulator that overstimulates cancer cells and leads to cell stress and death Cancer Cell 2015 28 240 252 10.1016/j.ccell.2015.07.005 26267537 PMC4536575 · DOI
  18. [22]Lukashchuk N Vousden KH Ubiquitination and degradation of mutant p53 Mol. Cell. Biol. 2007 27 8284 8295 10.1128/MCB.00050-07 17908790 PMC2169174 · DOI · Paper page
  19. [23]Crane EK Nutlin-3a: a potential therapeutic opportunity for TP53 wild-type ovarian carcinomas PLOS One 2015 10 e0135101 10.1371/journal.pone.0135101 26248031 PMC4527847 · DOI
  20. [24]Nicholson B Characterization of ubiquitin and ubiquitin-like-protein isopeptidase activities Protein Sci. 2008 17 1035 1043 10.1110/ps.083450408 18424514 PMC2386736 · DOI
  21. [25]Yi P SRC-3 coactivator regulates cell resistance to cytotoxic stress via TRAF4-mediated p53 destabilization Genes Dev. 2013 27 274 287 10.1101/gad.203760.112 23388826 PMC3576513 · DOI
  22. [26]Zou Q USP15 stabilizes MDM2 to mediate cancer-cell survival and inhibit antitumor T cell responses Nat. Immunol. 2014 15 562 570 10.1038/ni.2885 24777531 PMC4032322 · DOI
  23. [27]Altun M Activity-based chemical proteomics accelerates inhibitor development for deubiquitylating enzymes Chem. Biol. 2011 18 1401 1412 10.1016/j.chembiol.2011.08.018 22118674 · DOI
  24. [28]Mullany LK Specific TP53 mutants overrepresented in ovarian cancer impact CNV, TP53 activity, responses to Nutlin-3a, and cell survival Neoplasia 2015 17 789 803 10.1016/j.neo.2015.10.003 26585234 PMC4656807 · DOI
  25. [29]Eichhorn PJ USP15 stabilizes TGF-beta receptor I and promotes oncogenesis through the activation of TGF-beta signaling in glioblastoma Nat. Med. 2012 18 429 435 10.1038/nm.2619 22344298 · DOI · Paper page
  26. [31]Parrales A DNAJA1 controls the fate of misfolded mutant p53 through the mevalonate pathway Nat. Cell Biol. 2016 18 1233 1243 10.1038/ncb3427 27775703 PMC5340314 · DOI
  27. [32]Brooks CL Gu W p53 ubiquitination: Mdm2 and beyond Mol. Cell 2006 21 307 315 10.1016/j.molcel.2006.01.020 16455486 PMC3737769 · DOI · Paper page
  28. [33]Duffy MJ Synnott NC Crown J Mutant p53 as a target for cancer treatment Eur. J. Cancer 2017 83 258 265 10.1016/j.ejca.2017.06.023 28756138 · DOI
  29. [34]Chan WM Ubiquitination of p53 at multiple sites in the DNA-binding domain Mol. Cancer Res. 2006 4 15 25 10.1158/1541-7786.MCR-05-0097 16446403 · DOI
  30. [35]Padmanabhan A Vuong SA Hochstrasser M Assembly of an evolutionarily conserved alternative proteasome isoform in human cells Cell Rep. 2016 14 2962 2974 10.1016/j.celrep.2016.02.068 26997268 PMC4828729 · DOI
  31. [36]Padmanabhan A Li X Bieberich CJ Protein kinase A regulates MYC protein through transcriptional and post-translational mechanisms in a catalytic subunit isoform-specific manner J. Biol. Chem. 2013 288 14158 14169 10.1074/jbc.M112.432377 23504319 PMC3656272 · DOI
  32. [37]Padmanabhan A Gosc EB Bieberich CJ Stabilization of the prostate-specific tumor suppressor NKX3.1 by the oncogenic protein kinase Pim-1 in prostate cancer cells J. Cell. Biochem. 2013 114 1050 1057 10.1002/jcb.24444 23129228 · DOI
  33. [38]Robinson MD McCarthy DJ Smyth GK edgeR: a bioconductor package for differential expression analysis of digital gene expression data Bioinformatics 2010 26 139 140 10.1093/bioinformatics/btp616 19910308 PMC2796818 · DOI · Paper page
  34. [39]Zhai Y Gene expression analysis of preinvasive and invasive cervical squamous cell carcinomas identifies HOXC10 as a key mediator of invasion Cancer Res. 2007 67 10163 10172 10.1158/0008-5472.CAN-07-2056 17974957 · DOI
  35. [41]Zhao H Different gene expression patterns in invasive lobular and ductal carcinomas of the breast Mol. Biol. Cell. 2004 15 2523 2536 10.1091/mbc.E03-11-0786 15034139 PMC420079 · DOI
  36. [42]Rhodes DR ONCOMINE: a cancer microarray database and integrated data-mining platform Neoplasia 2004 6 1 6 10.1016/S1476-5586(04)80047-2 15068665 PMC1635162 · DOI

Cited by

Sorted by citations

Authors
Padmanabhan, A., Candelaria, N., Wong, K.-K., Nikolai, B. C., Lonard, D. M., O’Malley, B. W., & Richards, J. S.
Affiliations
  • Baylor College of Medicine (US)
  • The University of Texas MD Anderson Cancer Center (US)
Corresponding author
Padmanabhan, Achuth
Venue
Nature Communications
Published
2018-03-28
Volume
9
Issue
1
Pages
1270-1270
ISSN
2041-1723 (ISSN-L)
OpenAlex
W2795066098
Cited by
88
References
6
Citations by year
2026: 4 · 2025: 6 · 2024: 15 · 2023: 19 · 2022: 10 · 2021: 8 · 2020: 14 · 2019: 4 · 2018: 8
FWCI
3.19
Type
journal article
Language
en
Open access
Locations
  • Nature Communications (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Cancer Prevention and Research Institute of Texas (DK56338, RP150578, CA125123)
  • John S. Dunn Gulf Coast Consortium for Chemical Genomics
  • National Institutes of Health (RP150578, DK56338, CA125123)
  • National Cancer Institute (R01CA181808, P30CA125123)
  • National Institute of Diabetes and Digestive and Kidney Diseases (P30DK056338)
Topics
  • Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
  • Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
Keywords
USP15, p53 R175H, lysosomal degradation, deubiquitinase, ovarian cancer, ubiquitination, nuclear export, small molecule drugs
MeSH terms
Cycloheximide, Female, Humans, Lysosomes, Mutation, Ovarian Neoplasms, Plasmids, Receptors, Steroid, Gene Expression Regulation, Neoplastic, Tumor Suppressor Protein p53, Cell Line, Tumor, HEK293 Cells, MCF-7 Cells, Ubiquitin-Specific Proteases

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