Genomic trajectory in leukemogenesis of myeloproliferative neoplasms: a case report.

Case report Clonal evolution Essential thrombocythemia Leukemia Myeloproliferative neoplasms

Journal

BMC medical genomics
ISSN: 1755-8794
Titre abrégé: BMC Med Genomics
Pays: England
ID NLM: 101319628

Informations de publication

Date de publication:
22 05 2021
Historique:
received: 06 10 2020
accepted: 18 05 2021
entrez: 23 5 2021
pubmed: 24 5 2021
medline: 21 1 2022
Statut: epublish

Résumé

We report a patient with Essential Thrombocythemia (ET), subsequently diagnosed with concurrent myeloid and lymphoid leukemia. Generally, the molecular mechanisms underlying leukemic transformation of Philadelphia-negative myeloproliferative neoplasms (Ph-MPN) are poorly understood. Risk of transformation to acute myelogenous leukemia (AML) is low; transformation to both AML and acute lymphoblastic leukemia (ALL) is extremely low. Genetic defects, including allele burden, order of mutation acquisition, clonal heterogeneity and epigenetic mechanisms are important contributors to disease acceleration. A 78-year-old Caucasian female originally treated for stable ET, underwent disease acceleration and transition to myeloid sarcoma and B-cell ALL. Genomic reconstruction based on targeted sequencing revealed the presence of a large del(5q) in all three malignancies and somatic driver mutations: TET2, TP53, SF3B1, and ASXL1 at high allele frequency. We propose that the combination of genetic and molecular abnormalities led to hematopoietic stem cell (HSC) injury and disease progression through sub-clone branching. We hypothesize that ancestral reconstruction of genomic data is a useful tool to uncover subclonal events leading to transformation. The use of ancestral reconstruction of genomic data sheds light on the unique clinical scenario described in this case report. By determining the mutational profile of tumors at several timepoints and deducing the most parsimonious relationship between them, we propose a reconstruction of their origin. We propose that blast progression originated from subclonal events with malignant potential, which coexisted with but did not originate from JAK2 p.V617F-positive ET. We conclude that the application of genomic reconstruction enhances our understanding of leukemogenesis by identifying the timing of molecular events, potentially leading to better chemotherapy choices as well as the development of new targeted therapies.

Sections du résumé

BACKGROUND
We report a patient with Essential Thrombocythemia (ET), subsequently diagnosed with concurrent myeloid and lymphoid leukemia. Generally, the molecular mechanisms underlying leukemic transformation of Philadelphia-negative myeloproliferative neoplasms (Ph-MPN) are poorly understood. Risk of transformation to acute myelogenous leukemia (AML) is low; transformation to both AML and acute lymphoblastic leukemia (ALL) is extremely low. Genetic defects, including allele burden, order of mutation acquisition, clonal heterogeneity and epigenetic mechanisms are important contributors to disease acceleration.
CASE PRESENTATION
A 78-year-old Caucasian female originally treated for stable ET, underwent disease acceleration and transition to myeloid sarcoma and B-cell ALL. Genomic reconstruction based on targeted sequencing revealed the presence of a large del(5q) in all three malignancies and somatic driver mutations: TET2, TP53, SF3B1, and ASXL1 at high allele frequency. We propose that the combination of genetic and molecular abnormalities led to hematopoietic stem cell (HSC) injury and disease progression through sub-clone branching. We hypothesize that ancestral reconstruction of genomic data is a useful tool to uncover subclonal events leading to transformation.
CONCLUSIONS
The use of ancestral reconstruction of genomic data sheds light on the unique clinical scenario described in this case report. By determining the mutational profile of tumors at several timepoints and deducing the most parsimonious relationship between them, we propose a reconstruction of their origin. We propose that blast progression originated from subclonal events with malignant potential, which coexisted with but did not originate from JAK2 p.V617F-positive ET. We conclude that the application of genomic reconstruction enhances our understanding of leukemogenesis by identifying the timing of molecular events, potentially leading to better chemotherapy choices as well as the development of new targeted therapies.

Identifiants

pubmed: 34022887
doi: 10.1186/s12920-021-00986-z
pii: 10.1186/s12920-021-00986-z
pmc: PMC8141236
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

137

Subventions

Organisme : NIH HHS
ID : R01HL136333
Pays : United States
Organisme : NIH HHS
ID : R01HL134880
Pays : United States

Références

Proc Natl Acad Sci U S A. 2007 Jul 3;104(27):11406-11
pubmed: 17576924
N Engl J Med. 2016 Nov 24;375(21):2023-2036
pubmed: 27959731
Hum Pathol. 2015 Jan;46(1):65-73
pubmed: 25387813
Proc Natl Acad Sci U S A. 2014 Dec 16;111(50):E5401-10
pubmed: 25516983
Ann Hematol. 2014 Jan;93(1):1-11
pubmed: 24018623
Blood. 2019 Jul 11;134(2):186-198
pubmed: 31010849
Eur J Haematol. 2019 Mar;102(3):203-209
pubmed: 30578738
Blood. 1989 Jan;73(1):248-54
pubmed: 2562924
Clin Case Rep. 2017 Dec 06;6(1):155-161
pubmed: 29375856
Arterioscler Thromb Vasc Biol. 2019 Jul;39(7):1288-1300
pubmed: 31043076
Genes Chromosomes Cancer. 2016 Oct;55(10):777-85
pubmed: 27218649
Leukemia. 2016 Sep;30(9):1956-9
pubmed: 27133825
Leuk Lymphoma. 2019 Dec;60(12):2993-3001
pubmed: 31017498
Int J Mol Sci. 2019 Apr 13;20(8):
pubmed: 31013941

Auteurs

Yujie Chen (Y)

Department of Statistics and Bioengineering, Rice University, 6100 Main Street, Houston, TX, USA.

Rafee Talukder (R)

Department of Medicine, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX, USA.

Brian Y Merritt (BY)

The Dan L. Duncan Comprehensive Cancer Center at Baylor College of Medicine, 1 Baylor Plaza, Houston, TX, USA.
Department of Pathology and Immunology, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX, USA.
Department of Molecular and Human Genetics, Baylor Genetics and Baylor College of Medicine, 1 Baylor Plaza, Houston, TX, USA.

Katherine Y King (KY)

The Dan L. Duncan Comprehensive Cancer Center at Baylor College of Medicine, 1 Baylor Plaza, Houston, TX, USA.
Department of Pediatrics, Section of Infectious Disease, Baylor College of Medicine, 1102 Bates St. Suite 1150, Houston, TX, USA.

Marek Kimmel (M)

Department of Statistics and Bioengineering, Rice University, 6100 Main Street, Houston, TX, USA.

Gustavo Rivero (G)

Department of Medicine, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX, USA.
Fox Chase Cancer Center, 333 Cottman Ave, Philadelphia, PA, 19111, USA.
Section of Hematology and Oncology, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX, USA.

Romina Sosa (R)

The Dan L. Duncan Comprehensive Cancer Center at Baylor College of Medicine, 1 Baylor Plaza, Houston, TX, USA. iberia.sosa@fccc.edu.
Fox Chase Cancer Center, 333 Cottman Ave, Philadelphia, PA, 19111, USA. iberia.sosa@fccc.edu.
Section of Hematology and Oncology, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX, USA. iberia.sosa@fccc.edu.

Articles similaires

Humans Primary Myelofibrosis Thrombosis Myeloproliferative Disorders Neoplasms

Clonal hematopoiesis and hematological malignancy.

William G Dunn, Matthew A McLoughlin, George S Vassiliou
1.00
Humans Clonal Hematopoiesis Mutation Hematologic Neoplasms Leukemia, Myeloid, Acute
Humans Myeloproliferative Disorders Deep Learning Neural Networks, Computer Philadelphia Chromosome

Landscape of biallelic DNMT3A mutant myeloid neoplasms.

Naomi Kawashima, Yasuo Kubota, Carlos Bravo-Perez et al.
1.00
Humans DNA Methyltransferase 3A DNA (Cytosine-5-)-Methyltransferases Male Female

Classifications MeSH