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Implications of TP53 allelic state for genome stability, clinical presentation and outcomes in myelodysplastic syndromes
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Abstract
Tumor protein p53 (TP53) is the most frequently mutated gene in cancer 1,2. In patients with myelodysplastic syndromes (MDS), TP53 mutations are associated with high-risk disease 3,4, rapid transformation to acute myeloid leukemia (AML)5, resistance to conventional therapies 6-8 and dismal outcomes 9. Consistent with the tumor-suppressive role of TP53, patients harbor both mono- and biallelic mutations 10. However, the biological and clinical implications of TP53 allelic state have not been fully investigated in MDS or any other cancer type. We analyzed 3,324 patients with MDS for TP53 mutations and allelic imbalances and delineated two subsets of patients with distinct phenotypes and outcomes. One-third of TP53-mutated patients had monoallelic mutations whereas two-thirds had multiple hits (multi-hit) consistent with biallelic targeting. Established associations with complex karyotype, few co-occurring mutations, high-risk presentation and poor outcomes were specific to multi-hit patients only. TP53 multi-hit state predicted risk of death and leukemic transformation independently of the Revised International Prognostic Scoring System (IPSS-R)11. Surprisingly, monoallelic patients did not differ from TP53 wild-type patients in outcomes and response to therapy. This study shows that consideration of TP53 allelic state is critical for diagnostic and prognostic precision in MDS as well as in future correlative studies of treatment response.
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“Treatment outcomes for patients with TP53 mutations are poor with available therapies.8-12”
From Eprenetapopt (APR-246) and Azacitidine in TP53 -Mutant Myelodysplastic Syndromes (2021) · cites this paper as [9]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“The TP53 mutation burden (ie, high variant allele frequency [VAF], concurrent complex karyotype, and/or multihit state) is integrally linked to inferior survival with median OS of 6-8 months.8-10,12”
From Eprenetapopt (APR-246) and Azacitidine in TP53 -Mutant Myelodysplastic Syndromes (2021) · cites this paper as [9]
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“However, remissions in TP53-mutant patients are brief with a median overall survival (OS) ranging from 5 to 12 months,8,9,12,13,15-17”
From Eprenetapopt (APR-246) and Azacitidine in TP53 -Mutant Myelodysplastic Syndromes (2021) · cites this paper as [9]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“TP53 gene mutations (mTP53) represent a distinct molecular cohort with poor outcomes.”
From Long‐term follow‐up and combined Phase 2 results of eprenetapopt and azacitidine in patients with TP53 mutant MDS/AML (2025) · cites this paper as [3]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“TP53 gene mutations (mTP53) are found in up to 20% of myelodysplastic syndromes/neoplasms (MDS) or acute myeloid leukemia (AML) pts and 30%–40% of therapy‐related (TR) MDS/AML cases”
From Long‐term follow‐up and combined Phase 2 results of eprenetapopt and azacitidine in patients with TP53 mutant MDS/AML (2025) · cites this paper as [3]
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“Specifically, mTP53 patients with a high variant allele frequency (VAF; i.e., >20%–23%), biallelic state, and/or complex karyotype (CK) have particularly poor risk.”
From Long‐term follow‐up and combined Phase 2 results of eprenetapopt and azacitidine in patients with TP53 mutant MDS/AML (2025) · cites this paper as [3]
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“Despite the known dominant negative and/or gain of function effect of certain TP53 mutations28,42, loss of the TP53-WT allele, a genetic event associated with a particularly dismal prognosis2, confers an additional fitness advantage to TP53-sAML LSCs.”
From Single-cell multi-omics identifies chronic inflammation as a driver of TP53-mutant leukemic evolution (2023) · cites this paper as [2]
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Metadata
- Authors
- Bernard, E., Nannya, Y., Hasserjian, R. P., Devlin, S. M., Tuechler, H., Medina-Martinez, J. S., Yoshizato, T., Shiozawa, Y., Saiki, R., Malcovati, L., Levine, M. F., Arango, J. E., Zhou, Y., Solé, F., Cargo, C. A., Haase, D., Creignou, M., Germing, U., Zhang, Y., Gundem, G., Sarian, A., van de Loosdrecht, A. A., Jädersten, M., Tobiasson, M., Kosmider, O., Follo, M. Y., Thol, F., Pinheiro, R. F., Santini, V., Kotsianidis, I., Boultwood, J., Santos, F. P. S., Schanz, J., Kasahara, S., Ishikawa, T., Tsurumi, H., Takaori-Kondo, A., Kiguchi, T., Polprasert, C., Bennett, J. M., Klimek, V. M., Savona, M. R., Belickova, M., Ganster, C., Palomo, L., Sanz, G., Ades, L., Della Porta, M. G., Elias, H. K., Smith, A. G., Werner, Y., Patel, M., Viale, A., Vanness, K., Neuberg, D. S., Stevenson, K. E., Menghrajani, K., Bolton, K. L., Fenaux, P., Pellagatti, A., Platzbecker, U., Heuser, M., Valent, P., Chiba, S., Miyazaki, Y., Finelli, C., Voso, M. T., Shih, L.-Y., Fontenay, M., Jansen, J. H., Cervera, J., Atsuta, Y., Gattermann, N., Ebert, B. L., Bejar, R., Greenberg, P. L., Cazzola, M., Hellström-Lindberg, E., Ogawa, S., & Papaemmanuil, E.
- Affiliations
- Memorial Sloan Kettering Cancer Center (US)
- Kyoto University (JP)
- Massachusetts General Hospital (US)
- University of Pavia (IT)
- Josep Carreras Leukaemia Research Institute (ES)
- St James's University Hospital (GB)
- Universitätsmedizin Göttingen (DE)
- Karolinska University Hospital (SE)
- Heinrich Heine University Düsseldorf (DE)
- Université Paris Cité (FR)
- University of Bologna (IT)
- Medizinische Hochschule Hannover (DE)
- Universidade Federal do Ceará (BR)
- Azienda Ospedaliero-Universitaria Careggi (IT)
- University of Oxford (GB)
- Gifu Municipal Hospital (JP)
- Kobe City Medical Center General Hospital (JP)
- Gifu University (JP)
- Chugoku Central Hospital (JP)
- Chulalongkorn University (TH)
- University of Rochester Medicine (US)
- Vanderbilt University (US)
- Instituto de Salud Carlos III (ES)
- University of York (GB)
- Dana-Farber Cancer Institute (US)
- Hôpital Saint-Louis (FR)
- Leipzig University (DE)
- Ludwig Boltzmann Institute for Hematology and Oncology (AT)
- University of Tsukuba (JP)
- Nagasaki University (JP)
- IRCCS Azienda Ospedliero-Universitaria di Bologna Policlinico di Sant'Orsola (IT)
- University of Rome Tor Vergata (IT)
- Chang Gung University (TW)
- Radboud University Medical Center (NL)
- Hospital Universitari i Politècnic La Fe (ES)
- The Japanese Data Center for Hematopoietic Cell Transplantation (JP)
- Howard Hughes Medical Institute (US)
- Moores Cancer Center (US)
- Stanford Cancer Institute (US)
- Corresponding author
- Papaemmanuil, Elli
- ORCID
- Bernard, Elsa
- Nannya, Yasuhito
- Hasserjian, Robert P.
- Devlin, Sean M.
- Tuechler, Heinz
- Medina-Martinez, Juan S.
- Yoshizato, Tetsuichi
- Saiki, Ryunosuke
- Malcovati, Luca
- Levine, Max F.
- Solé, Francesc
- Cargo, Catherine A.
- Creignou, Maria
- Germing, Ulrich
- Zhang, Yanming
- Gundem, Gunes
- Jädersten, Martin
- Tobiasson, Magnus
- Kosmider, Olivier
- Follo, Matilde Y.
- Thol, Felicitas
- Pinheiro, Ronald F.
- Santini, Valeria
- Boultwood, Jacqueline
- Schanz, Julie
- Kasahara, Senji
- Ishikawa, Takayuki
- Tsurumi, Hisashi
- Takaori-Kondo, Akifumi
- Kiguchi, Toru
- Polprasert, Chantana
- Bennett, John M.
- Savona, Michael R.
- Belickova, Monika
- Ganster, Christina
- Palomo, Laura
- Sanz, Guillermo
- Elias, Harold K.
- Smith, Alexandra G.
- Werner, Yesenia
- Neuberg, Donna S.
- Stevenson, Kristen E.
- Menghrajani, Kamal
- Bolton, Kelly L.
- Fenaux, Pierre
- Pellagatti, Andrea
- Platzbecker, Uwe
- Heuser, Michael
- Valent, Peter
- Miyazaki, Yasushi
- Finelli, Carlo
- Voso, Maria Teresa
- Shih, Lee-Yung
- Fontenay, Michaela
- Jansen, Joop H.
- Cervera, José
- Atsuta, Yoshiko
- Ebert, Benjamin L.
- Bejar, Rafael
- Greenberg, Peter L.
- Cazzola, Mario
- Ogawa, Seishi
- Papaemmanuil, Elli
- Venue
- Nature Medicine
- Published
- 2020-08-03
- Volume
- 26
- Issue
- 10
- Pages
- 1549-1556
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- PMC
- PMC8381722
- OpenAlex
- W3046671820
- Cited by
- 648
- References
- 58
- Citations by year
- 2026: 73 · 2025: 91 · 2024: 106 · 2023: 136 · 2022: 130 · 2021: 87 · 2020: 22
- FWCI
- 59.16
- Type
- journal article
- Language
- en
- Update notices
- Open access
- green
- doi.org
- Licence
- Locations
- Nature Medicine (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion, other-oa)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
- White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (acceptedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Florence Research (University of Florence) (submittedVersion, other-oa)
- Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion)
- Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion, other-oa)
- eScholarship (California Digital Library) (submittedVersion)
- GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
- Radboud Repository (Radboud University) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- Amgen
- Pfizer
- Sanofi
- Alexion Pharmaceuticals
- Celgene (21267)
- Helsinn
- European Hematology Association
- Japan Agency for Medical Research and Development (JP18ck0106353, 19ck0106250h0003, JP19cm0106501)
- Taiho Pharmaceutical
- TG Therapeutics
- Astex Pharmaceuticals
- Sunesis
- Incyte
- Nippon Shinyaku
- Celltrion
- Geoffrey Beene Foundation
- Cancer Research UK (29685)
- Agence Nationale de la Recherche (ANR-18-IBHU-0003)
- Ministry of Education, Culture, Sports, Science and Technology (hp160219)
- Austrian Science Fund (#F4704-B20)
- Ministero dell’Istruzione, dell’Università e della Ricerca (21267)
- Astellas Pharma
- Associazione Italiana per la Ricerca sul Cancro (21267, 5×1000, 20125, 13042, project #21267, IG #20125)
- Genesis Pharma
- Otsuka Pharmaceutical
- Ono Pharmaceutical
- Blood Cancer UK (13042)
- Chugai Pharmaceutical
- Pharmacyclics
- Sanofi K.K.
- Japan Society for the Promotion of Science (19H03684, 13042, 18H02836, 26221308, hp160219, 19H05656, 15H05909)
- National Cancer Institute (P30CA008748, K12CA184746, P50CA254838)
- Daiichi Sankyo Europe
- Cilag
- Topics
- Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
- Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinoids in leukemia and cellular processes
- Keywords
- TP53 mutation, myelodysplastic syndrome, allelic state, monoallelic variants, biallelic variants, genome stability, leukemic transformation, acute myeloid leukemia, complex karyotype, prognosis, treatment response, wild-type p53
- MeSH terms
- Alleles, DNA Mutational Analysis, Female, Gene Frequency, Humans, Male, Mutation, Myelodysplastic Syndromes, Phenotype, Prognosis, Cohort Studies, Survival Analysis, Tumor Suppressor Protein p53, Treatment Outcome, Loss of Heterozygosity, Genomic Instability, DNA Copy Number Variations
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