Mutations underlie all cancers, and their identification and study are the foundation of cancer biology. We describe what we believe to be a novel approach to mutagenesis and cancer studies based on the DNA polymerase ε (POLE) ultramutator phenotype recently described in human cancers, in which a single amino acid substitution (most commonly P286R) in the proofreading domain results in error-prone DNA replication. We engineered a conditional PoleP286R allele in mice. PoleP286R/+ embryonic fibroblasts exhibited a striking mutator phenotype and immortalized more efficiently. PoleP286R/+ mice were born at Mendelian ratios but rapidly developed lethal cancers of diverse lineages, yielding the most cancer-prone monoallelic model described to date, to our knowledge. Comprehensive whole-genome sequencing analyses showed that the cancers were driven by high base substitution rates in the range of human cancers, overcoming a major limitation of previous murine cancer models. These data establish polymerase-mediated ultramutagenesis as an efficient in vivo approach for the generation of diverse animal cancer models that recapitulate the high mutational loads inherent to human cancers.
Hao-Dong Li, Ileana Cuevas, Musi Zhang, Changzheng Lu, Md Maksudul Alam, Yang-Xin Fu, M. James You, Esra A. Akbay, He Zhang, Diego H. Castrillon
Title and authors | Publication | Year |
---|---|---|
DNA polymerase ε and δ variants drive mutagenesis in polypurine tracts in human tumors.
Ostroverkhova D, Tyryshkin K, Beach AK, Moore EA, Masoudi-Sobhanzadeh Y, Barbari SR, Rogozin IB, Shaitan KV, Panchenko AR, Shcherbakova PV |
Cell Reports | 2024 |
Proteogenomic insights into early-onset endometrioid endometrial carcinoma: predictors for fertility-sparing therapy response.
Hu Z, Wu Z, Liu W, Ning Y, Liu J, Ding W, Fan J, Cai S, Li Q, Li W, Yang X, Dou Y, Wang W, Peng W, Lu F, Zhuang X, Qin T, Kang X, Feng C, Xu Z, Lv Q, Wang Q, Wang C, Wang X, Wang Z, Wang J, Jiang J, Wang B, Mills GB, Ma D, Gao Q, Li K, Chen G, Chen X, Sun C |
Nature Genetics | 2024 |
Integration of CD4(+) T cells and molecular subtype predicts benefit from PD-L1 blockade in muscle-invasive bladder cancer.
Liu G, Jin K, Liu Z, Su X, Xu Z, Li B, Xu J, Liu H, Chang Y, Zhu Y, Xu L, Wang Z, Wang Y, Zhang W |
Cancer Science | 2024 |
Mutation rate heterogeneity at the sub-gene scale due to local DNA hypomethylation
Mas-Ponte D, Supek F |
Nucleic Acids Research | 2024 |
Melanoma-Derived DNA Polymerase Theta Variants Exhibit Altered DNA Polymerase Activity
Thomas C, Avalos-Irving L, Victorino J, Green S, Andrews M, Rodrigues N, Ebirim S, Mudd A, Towle-Weicksel JB |
Biochemistry | 2024 |
Human DNA polymerase ε is a source of C>T mutations at CpG dinucleotides.
Tomkova M, McClellan MJ, Crevel G, Shahid AM, Mozumdar N, Tomek J, Shepherd E, Cotterill S, Schuster-Böckler B, Kriaucionis S |
Nature genetics | 2024 |
Critical roles of Dpb3-Dpb4 sub-complex of DNA polymerase epsilon in DNA replication, genome stability, and pathogenesis of Candida albicans
Utkalaja BG, Patel SK, Sahu SR, Dutta A, Acharya N |
mBio | 2024 |
Altered dNTP pools accelerate tumor formation in mice.
Tran P, Mishra P, Williams LG, Moskalenko R, Sharma S, Nilsson AK, Watt DL, Andersson P, Bergh A, Pursell ZF, Chabes A |
Nucleic acids research | 2024 |
Immune Checkpoint Blockade Delays Cancer Development and Extends Survival in DNA Polymerase Mutator Syndromes
Sawant A, Shi F, Cararo Lopes E, Hu Z, Abdelfattah S, Baul J, Powers JR, Hinrichs CS, Rabinowitz JD, Chan CS, Lattime EC, Ganesan S, White EP |
Cancer Research | 2024 |
The hereditary N363K POLE exonuclease mutant extends PPAP tumor spectrum to glioblastomas by causing DNA damage and aneuploidy in addition to increased mismatch mutagenicity
Labrousse G, Vande Perre P, Parra G, Jaffrelot M, Leroy L, Chibon F, Escudie F, Selves J, Hoffmann JS, Guimbaud R, Lutzmann M |
2023 | |
β-catenin, Pax2, and Pten Panel Identifies Precancers Among Histologically Subdiagnostic Endometrial Lesions
Aguilar M, Chen H, Sahoo SS, Zheng W, Grubman J, SoRelle JA, Lucas E, Castrillon DH |
The American Journal of Surgical Pathology | 2023 |
Recommendations for the classification of germline variants in the exonuclease domain of POLE and POLD1
Mur P, Viana-Errasti J, García-Mulero S, Magraner-Pardo L, Muñoz IG, Pons T, Capellá G, Pineda M, Feliubadaló L, Valle L |
Genome Medicine | 2023 |
Loss of p53 and mutational heterogeneity drives immune resistance in an autochthonous mouse lung cancer model with high tumor mutational burden.
Zhu M, Kim J, Deng Q, Ricciuti B, Alessi JV, Eglenen-Polat B, Bender ME, Huang HC, Kowash RR, Cuevas I, Bennett ZT, Gao J, Minna JD, Castrillon DH, Awad MM, Xu L, Akbay EA |
Cancer Cell | 2023 |
Susceptibility Genes Associated with Multiple Primary Cancers
Lu M, Zhang X, Chu Q, Chen Y, Zhang P |
Cancers | 2023 |
Mouse model and human patient data reveal critical roles for Pten and p53 in suppressing POLE mutant tumor development
V Park, M Sun, W Frey, L Williams, K Hodel, J Strauss, S Wellens, J Jackson, Z Pursell |
NAR Cancer | 2022 |
Polymerase Epsilon-Associated Ultramutagenesis in Cancer
X Xing, N Jin, J Wang |
Cancers | 2022 |
Pembrolizumab and Trastuzumab in High Tumor Mutational Burden and POLE -Mutated HER2-Positive Refractory Breast Cancer
L Zhang, Y Chen, Y Lv, S Jiao, W Zhao |
The oncologist | 2022 |
DNA repair defects in cancer and therapeutic opportunities
J Hopkins, L Lan, L Zou |
Genes & development | 2022 |
PrimPol: A Breakthrough among DNA Replication Enzymes and a Potential New Target for Cancer Therapy
A Díaz-Talavera, C Montero-Conde, L Leandro-García, M Robledo |
Biomolecules | 2022 |
POLE/POLD1 mutation and tumor immunotherapy
Ma X, Dong L, Liu X, Ou K, Yang L |
Journal of experimental & clinical cancer research : CR | 2022 |
Enhanced polymerase activity permits efficient synthesis by cancer-associated DNA polymerase ϵ variants at low dNTP levels
Barbari SR, Beach AK, Markgren JG, Parkash V, Moore EA, Johansson E, Shcherbakova PV |
Nucleic Acids Research | 2022 |
Functional landscapes of POLE and POLD1 mutations in checkpoint blockade-dependent antitumor immunity.
Ma X, Riaz N, Samstein RM, Lee M, Makarov V, Valero C, Chowell D, Kuo F, Hoen D, Fitzgerald CWR, Jiang H, Alektiar J, Alban TJ, Juric I, Parthasarathy PB, Zhao Y, Sabio EY, Verma R, Srivastava RM, Vuong L, Yang W, Zhang X, Wang J, Chu LK, Wang SL, Kelly DW, Pei X, Chen J, Yaeger R, Zamarin D, Zehir A, Gönen M, Morris LGT, Chan TA |
Nature Genetics | 2022 |
The mismatch recognition protein MutSα promotes nascent strand degradation at stalled replication forks
Zhang J, Zhao X, Liu L, Li HD, Gu L, Castrillon DH, Li GM |
Proceedings of the National Academy of Sciences | 2022 |
Quantitative methods to study helicase, DNA polymerase, and exonuclease coupling during DNA replication
Singh A, Patel SS |
Methods in enzymology | 2022 |
Immunotherapy in colorectal cancer: current achievements and future perspective
A Fan, B Wang, X Wang, Y Nie, D Fan, X Zhao, Y Lu |
International journal of biological sciences | 2021 |
Mutagenic mechanisms of cancer-associated DNA polymerase ϵ alleles
M Herzog, E Alonso-Perez, I Salguero, J Warringer, DJ Adams, SP Jackson, F Puddu |
Nucleic Acids Research | 2021 |
Expression of the cancer-associated DNA polymerase ε P286R in fission yeast leads to translesion synthesis polymerase dependent hypermutation and defective DNA replication
I Soriano, E Vazquez, ND Leon, S Bertrand, E Heitzer, S Toumazou, Z Bo, C Palles, CC Pai, TC Humphrey, I Tomlinson, S Cotterill, SE Kearsey, JL Nitiss |
PLoS genetics | 2021 |
Rate volatility and asymmetric segregation diversify mutation burden in cells with mutator alleles
IT Dowsett, JL Sneeden, BJ Olson, J McKay-Fleisch, E McAuley, SR Kennedy, AJ Herr |
2021 | |
Increased somatic mutation burdens in normal human cells due to defective DNA polymerases
PS Robinson, TH Coorens, C Palles, E Mitchell, F Abascal, S Olafsson, BC Lee, AR Lawson, H Lee-Six, L Moore, MA Sanders, J Hewinson, L Martin, CM Pinna, S Galavotti, R Rahbari, PJ Campbell, I Martincorena, I Tomlinson, MR Stratton |
Nature Genetics | 2021 |
Unravelling roles of error-prone DNA polymerases in shaping cancer genomes
C Vaziri, IB Rogozin, Q Gu, D Wu, TA Day |
Oncogene | 2021 |
MIF is a 3’ flap nuclease that facilitates DNA replication and promotes tumor growth
Y Wang, Y Chen, C Wang, M Yang, Y Wang, L Bao, JE Wang, BW Kim, KY Chan, W Xu, E Capota, J Ortega, D Nijhawan, GM Li, W Luo, Y Wang |
Nature Communications | 2021 |
A PoleP286R mouse model of endometrial cancer recapitulates high mutational burden and immunotherapy response
Hao-Dong Li, Changzheng Lu, He Zhang, Qing Hu, Junqiu Zhang, Ileana C Cuevas, Subhransu S Sahoo, Mitzi Aguilar, Elizabeth Maurais, Shanrong Zhang, Xiaojing Wang, Esra A Akbay, Guo-Min Li, Bo Li, Prasad Koduru, Peter Ly, Yang-Xin Fu, Diego H. Castrillon |
JCI Insight | 2020 |
Cancers from Novel Pole -Mutant Mouse Models Provide Insights into Polymerase-Mediated Hypermutagenesis and Immune Checkpoint Blockade
MA Galati, KP Hodel, MS Gams, S Sudhaman, T Bridge, WJ Zahurancik, NA Ungerleider, VS Park, AB Ercan, L Joksimovic, I Siddiqui, R Siddaway, M Edwards, R de Borja, D Elshaer, J Chung, VJ Forster, NM Nunes, M Aronson, X Wang, J Ramdas, A Seeley, T Sarosiek, GP Dunn, JN Byrd, O Mordechai, C Durno, A Martin, A Shlien, E Bouffet, Z Suo, JG Jackson, CE Hawkins, CJ Guidos, ZF Pursell, U Tabori |
Cancer research | 2020 |
DNA Polymerases at the Eukaryotic Replication Fork Thirty Years after: Connection to Cancer
YI Pavlov, AS Zhuk, EI Stepchenkova |
Cancers | 2020 |
DNA polymerase δ proofreads errors made by DNA polymerase ε
CR Bulock, X Xing, PV Shcherbakova |
Proceedings of the National Academy of Sciences | 2020 |
Mismatch repair and DNA polymerase δ proofreading prevent catastrophic accumulation of leading strand errors in cells expressing a cancer-associated DNA polymerase ϵ variant
CR Bulock, X Xing, PV Shcherbakova |
Nucleic Acids Research | 2020 |
POLE Mutation Spectra Are Shaped by the Mutant Allele Identity, Its Abundance, and Mismatch Repair Status
KP Hodel, MJ Sun, N Ungerleider, VS Park, LG Williams, DL Bauer, VE Immethun, J Wang, Z Suo, H Lu, JB McLachlan, ZF Pursell |
Molecular Cell | 2020 |
Ultra‐mutated colorectal cancer patients with POLE driver mutations exhibit distinct clinical patterns
H Hu, W Cai, D Wu, W Hu, LD Wang, J Mao, S Zheng, W Ge |
Cancer Medicine | 2020 |
Spontaneous Polyploids and Antimutators Compete During the Evolution of Saccharomyces cerevisiae Mutator Cells
MA Tracy, MB Lee, BL Hearn, IT Dowsett, LC Thurber, J Loo, AM Loeb, K Preston, MI Tuncel, N Ghodsian, A Bode, TT Tang, AR Chia, AJ Herr |
Genetics | 2020 |
Excessive excision of correct nucleotides during DNA synthesis explained by replication hurdles
A Singh, M Pandey, D Nandakumar, KD Raney, YW Yin, SS Patel |
The EMBO Journal | 2020 |
POLE Proofreading Defects: Contributions to Mutagenesis and Cancer
VS Park, ZF Pursell |
DNA repair | 2019 |
Evaluation of POLE and POLD1 Mutations as Biomarkers for Immunotherapy Outcomes Across Multiple Cancer Types
F Wang, Q Zhao, YN Wang, Y Jin, MM He, ZX Liu, RH Xu |
JAMA Oncology | 2019 |
A recurrent cancer-associated substitution in DNA polymerase ε produces a hyperactive enzyme
X Xing, DP Kane, CR Bulock, EA Moore, S Sharma, A Chabes, PV Shcherbakova |
Nature Communications | 2019 |
Structural consequence of the most frequently recurring cancer-associated substitution in DNA polymerase ε
V Parkash, Y Kulkarni, J ter Beek, PV Shcherbakova, SC Kamerlin, E Johansson |
Nature Communications | 2019 |
Errors in translational decoding: tRNA wobbling or misincorporation?
X Ou, J Cao, A Cheng, MP Peppelenbosch, Q Pan, RB Gartenhaus |
PLoS genetics | 2019 |
Replication-Coupled DNA Repair
D Cortez |
Molecular Cell | 2019 |
Opportunities for new studies of nuclear DNA replication enzymology in budding yeast
MA Garbacz, SA Lujan, TA Kunkel |
Current Genetics | 2019 |
A simple but profound mutation in mouse DNA polymerase epsilon drives tumorigenesis
Thomas A Kunkel |
Journal of Clinical Investigation | 2018 |