Genomic subtyping and therapeutic targeting of acute erythroleukemia

Acute erythroid leukemia (AEL) is a high-risk leukemia of poorly understood genetic basis, with controversy regarding diagnosis in the spectrum of myelodysplasia and myeloid leukemia. We compared genomic features of 159 childhood and adult AEL cases with non-AEL myeloid disorders and defined five ag...

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Vydáno v:Nature genetics Ročník 51; číslo 4; s. 694 - 704
Hlavní autoři: Iacobucci, Ilaria, Wen, Ji, Meggendorfer, Manja, Choi, John K., Shi, Lei, Pounds, Stanley B., Carmichael, Catherine L., Masih, Katherine E., Morris, Sarah M., Lindsley, R. Coleman, Janke, Laura J., Alexander, Thomas B., Song, Guangchun, Qu, Chunxu, Li, Yongjin, Payne-Turner, Debbie, Tomizawa, Daisuke, Kiyokawa, Nobutaka, Valentine, Marcus, Valentine, Virginia, Basso, Giuseppe, Locatelli, Franco, Enemark, Eric J., Kham, Shirley K. Y., Yeoh, Allen E. J., Ma, Xiaotu, Zhou, Xin, Sioson, Edgar, Rusch, Michael, Ries, Rhonda E., Stieglitz, Elliot, Hunger, Stephen P., Wei, Andrew H., To, L Bik, Lewis, Ian D., D’Andrea, Richard J., Kile, Benjamin T., Brown, Anna L., Scott, Hamish S., Hahn, Christopher N., Marlton, Paula, Pei, Deqing, Cheng, Cheng, Loh, Mignon L., Ebert, Benjamin L., Meshinchi, Soheil, Haferlach, Torsten, Mullighan, Charles G.
Médium: Journal Article
Jazyk:angličtina
Vydáno: New York Nature Publishing Group US 01.04.2019
Nature Publishing Group
Témata:
631/67/1990/283
631/67/1990/283/1897
Acute leukemia
Adolescent
Adult
Adults
Age
Agriculture
Animal Genetics and Genomics
Bioinformatics
Biomedical and Life Sciences
Biomedicine
Bone marrow
Cancer genetics
Cancer Research
Cancer therapies
Care and treatment
Cell cycle
Child
Child, Preschool
Children
Classification
Deoxyribonucleic acid
Diagnosis
DNA
DNA methylation
Epigenetics
Erythroleukemia
Female
fms-Like Tyrosine Kinase 3 - genetics
Gene Function
Genes
Genetic aspects
Genomes
Genomics
Genomics - methods
Homeodomain Proteins - genetics
Human Genetics
Humans
Infant
Infant, Newborn
Leukemia
Leukemia, Erythroblastic, Acute - genetics
Leukemogenesis
Male
Medical prognosis
Medical schools
Mutation
Mutation - genetics
Myelodysplastic syndrome
Myeloid leukemia
Myeloid-Lymphoid Leukemia Protein - genetics
Nuclear Proteins - genetics
Nucleophosmin
p53 Protein
Pediatrics
Prognosis
Risk
Subgroups
Therapeutic targets
Transcription
Tumor proteins
Tumor Suppressor Protein p53 - genetics
Tumors
Young Adult
ISSN:1061-4036, 1546-1718, 1546-1718
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Abstract Acute erythroid leukemia (AEL) is a high-risk leukemia of poorly understood genetic basis, with controversy regarding diagnosis in the spectrum of myelodysplasia and myeloid leukemia. We compared genomic features of 159 childhood and adult AEL cases with non-AEL myeloid disorders and defined five age-related subgroups with distinct transcriptional profiles: adult, TP53 mutated; NPM1 mutated; KMT2A mutated/rearranged; adult, DDX41 mutated; and pediatric, NUP98 rearranged. Genomic features influenced outcome, with NPM1 mutations and HOXB9 overexpression being associated with a favorable prognosis and TP53 , FLT3 or RB1 alterations associated with poor survival. Targetable signaling mutations were present in 45% of cases and included recurrent mutations of ALK and NTRK1 , the latter of which drives erythroid leukemogenesis sensitive to TRK inhibition. This genomic landscape of AEL provides the framework for accurate diagnosis and risk stratification of this disease, and the rationale for testing targeted therapies in this high-risk leukemia. Analysis of genomic and clinical features of acute erythroid leukemia in comparison to other myeloid disorders supports its distinct classification, defines subgroups and suggests therapeutic vulnerabilities.
AbstractList Acute erythroid leukemia (AEL) is a high risk leukemia of poorly understood genetic basis, with controversy regarding diagnosis in the spectrum of myelodysplasia and myeloid leukemia. We compared genomic features of 159 childhood and adult AEL cases to non-AEL myeloid disorders, and defined 5 age-related subgroups with distinct transcriptional profiles: adult, TP53-mutated; NPM1-mutated; KMT2A-mutated/rearranged; adult, DDX41-mutated; and pediatric, NUP98-rearranged. Genomic features influenced outcome, with NPM1 mutations and HOXB9 over-expression associated with favorable prognosis, and TP53, FLT3 or RB1 alterations associated with poor survival. Targetable signaling mutations were present in 45% of cases, and included recurrent mutations of ALK and NTRK1, the latter of which drive erythroid leukemogenesis sensitive to TRK inhibition. This genomic landscape of AEL provides the framework for accurate diagnosis and risk stratification of this disease, and the rationale for testing targeted therapies in this high-risk leukemia. Analysis of genomic and clinical features of acute erythroid leukemia in comparison to other myeloid disorders argues for its distinct classification, defines subgroups and suggests therapeutic vulnerabilities.
Acute erythroid leukemia (AEL) is a high-risk leukemia of poorly understood genetic basis, with controversy regarding diagnosis in the spectrum of myelodysplasia and myeloid leukemia. We compared genomic features of 159 childhood and adult AEL cases with non-AEL myeloid disorders and defined five age-related subgroups with distinct transcriptional profiles: adult, TP53 mutated; NPM1 mutated; KMT2A mutated/rearranged; adult, DDX41 mutated; and pediatric, NUP98 rearranged. Genomic features influenced outcome, with NPM1 mutations and HOXB9 overexpression being associated with a favorable prognosis and TP53, FLT3 or RB1 alterations associated with poor survival. Targetable signaling mutations were present in 45% of cases and included recurrent mutations of ALK and NTRK1, the latter of which drives erythroid leukemogenesis sensitive to TRK inhibition. This genomic landscape of AEL provides the framework for accurate diagnosis and risk stratification of this disease, and the rationale for testing targeted therapies in this high-risk leukemia.
Acute erythroid leukemia (AEL) is a high-risk leukemia of poorly understood genetic basis, with controversy regarding diagnosis in the spectrum of myelodysplasia and myeloid leukemia. We compared genomic features of 159 childhood and adult AEL cases with non-AEL myeloid disorders and defined five age-related subgroups with distinct transcriptional profiles: adult, TP53 mutated; NPM1 mutated; KMT2A mutated/rearranged; adult, DDX41 mutated; and pediatric, NUP98 rearranged. Genomic features influenced outcome, with NPM1 mutations and HOXB9 overexpression being associated with a favorable prognosis and TP53, FLT3 or RB1 alterations associated with poor survival. Targetable signaling mutations were present in 45% of cases and included recurrent mutations of ALK and NTRK1, the latter of which drives erythroid leukemogenesis sensitive to TRK inhibition. This genomic landscape of AEL provides the framework for accurate diagnosis and risk stratification of this disease, and the rationale for testing targeted therapies in this high-risk leukemia. Analysis of genomic and clinical features of acute erythroid leukemia in comparison to other myeloid disorders supports its distinct classification, defines subgroups and suggests therapeutic vulnerabilities.
Acute erythroid leukemia (AEL) is a high-risk leukemia of poorly understood genetic basis, with controversy regarding diagnosis in the spectrum of myelodysplasia and myeloid leukemia. We compared genomic features of 159 childhood and adult AEL cases with non-AEL myeloid disorders and defined five age-related subgroups with distinct transcriptional profiles: adult, TP53 mutated; NPM1 mutated; KMT2A mutated/rearranged; adult, DDX41 mutated; and pediatric, NUP98 rearranged. Genomic features influenced outcome, with NPM1 mutations and HOXB9 overexpression being associated with a favorable prognosis and TP53, FLT3 or RB1 alterations associated with poor survival. Targetable signaling mutations were present in 45% of cases and included recurrent mutations of ALK and NTRK1, the latter of which drives erythroid leukemogenesis sensitive to TRK inhibition. This genomic landscape of AEL provides the framework for accurate diagnosis and risk stratification of this disease, and the rationale for testing targeted therapies in this high-risk leukemia.Acute erythroid leukemia (AEL) is a high-risk leukemia of poorly understood genetic basis, with controversy regarding diagnosis in the spectrum of myelodysplasia and myeloid leukemia. We compared genomic features of 159 childhood and adult AEL cases with non-AEL myeloid disorders and defined five age-related subgroups with distinct transcriptional profiles: adult, TP53 mutated; NPM1 mutated; KMT2A mutated/rearranged; adult, DDX41 mutated; and pediatric, NUP98 rearranged. Genomic features influenced outcome, with NPM1 mutations and HOXB9 overexpression being associated with a favorable prognosis and TP53, FLT3 or RB1 alterations associated with poor survival. Targetable signaling mutations were present in 45% of cases and included recurrent mutations of ALK and NTRK1, the latter of which drives erythroid leukemogenesis sensitive to TRK inhibition. This genomic landscape of AEL provides the framework for accurate diagnosis and risk stratification of this disease, and the rationale for testing targeted therapies in this high-risk leukemia.
Acute erythroid leukemia (AEL) is a high-risk leukemia of poorly understood genetic basis, with controversy regarding diagnosis in the spectrum of myelodysplasia and myeloid leukemia. We compared genomic features of 159 childhood and adult AEL cases with non-AEL myeloid disorders and defined five age-related subgroups with distinct transcriptional profiles: adult, TP53 mutated; NPM1 mutated; KMT2A mutated/rearranged; adult, DDX41 mutated; and pediatric, NUP98 rearranged. Genomic features influenced outcome, with NPM1 mutations and HOXB9 overexpression being associated with a favorable prognosis and TP53 , FLT3 or RB1 alterations associated with poor survival. Targetable signaling mutations were present in 45% of cases and included recurrent mutations of ALK and NTRK1 , the latter of which drives erythroid leukemogenesis sensitive to TRK inhibition. This genomic landscape of AEL provides the framework for accurate diagnosis and risk stratification of this disease, and the rationale for testing targeted therapies in this high-risk leukemia. Analysis of genomic and clinical features of acute erythroid leukemia in comparison to other myeloid disorders supports its distinct classification, defines subgroups and suggests therapeutic vulnerabilities.
Audience Academic
Author Alexander, Thomas B.
Kham, Shirley K. Y.
Brown, Anna L.
Song, Guangchun
Locatelli, Franco
Wei, Andrew H.
Cheng, Cheng
Morris, Sarah M.
Hahn, Christopher N.
Ma, Xiaotu
Ries, Rhonda E.
Ebert, Benjamin L.
Carmichael, Catherine L.
Scott, Hamish S.
Kiyokawa, Nobutaka
Lewis, Ian D.
D’Andrea, Richard J.
Qu, Chunxu
Enemark, Eric J.
Meggendorfer, Manja
Kile, Benjamin T.
Pei, Deqing
Haferlach, Torsten
Iacobucci, Ilaria
Shi, Lei
Tomizawa, Daisuke
Janke, Laura J.
Loh, Mignon L.
Mullighan, Charles G.
Basso, Giuseppe
To, L Bik
Pounds, Stanley B.
Lindsley, R. Coleman
Rusch, Michael
Payne-Turner, Debbie
Meshinchi, Soheil
Wen, Ji
Stieglitz, Elliot
Marlton, Paula
Zhou, Xin
Masih, Katherine E.
Choi, John K.
Li, Yongjin
Yeoh, Allen E. J.
Hunger, Stephen P.
Valentine, Marcus
Sioson, Edgar
Valentine, Virginia
AuthorAffiliation 15 Department of Structural Biology, St. Jude Children’s Research Hospital, Memphis, TN
25 Centre for Cancer Biology, University of South Australia and SA Pathology, Adelaide, Australia
13 Department of Gynecology/Obstetrics and Pediatrics, Sapienza University of Rome, Rome, Italy
5 Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts, USA
1 Department of Pathology, St. Jude Children’s Research Hospital, Memphis, TN
19 Department of Pediatrics, Benioff Children’s Hospital, and the Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, CA
7 Department of Computational Biology, St. Jude Children’s Research Hospital, Memphis, TN
10 Cytogenetics Shared Resource, St. Jude Children’s Research Hospital, Memphis, TN
24 Faculty of Health Sciences, University of Adelaide, Adelaide, Australia
18 Fred Hutchinson Cancer Research Center, Seattle, WA
4 The Australian Centre for Blood Diseases, Monash University, Melbourne, Austral
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30926971$$D View this record in MEDLINE/PubMed
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K.E.M., S.M.M., T.B.A., D.P.T., M.V., V.V. performed experiments. G.S. analyzed copy number data. E.J.E. performed structure modeling. M.M, C.C, D.T., N.K., G.B., F.L., S.K.K.Y., A.Y.E.J., R.E.R., E.S., A.W., L.B.T., I.D.L., R.D.A., B.T.K., A.L.B., H.S., C.H., P.M., S.M., T.H. provided patient samples and clinical data. R.C.L., B.L.E. shared data for the MDS comparison cohort. Y.L., C.Q., X.M., X.Z., E.S., S.P.H, M.R. performed genomic sequencing, analysis, and support. L.S., S.P., D.P., C.C. performed statistical analyses. C.G.M. designed and oversaw the study, analyzed genomic data and wrote the manuscript. All the authors read and approved the final version of the manuscript.
AUTHOR CONTRIBUTIONS
I.I. led the collaboration, coordination and processing of patient samples, analyzed genomic data, performed experiments and wrote the manuscript. J.W. analyzed sequencing data. J.K.C. performed central review of immunophenotypic data. L.J.J. performed histopathology analyses
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SSID ssj0014408
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Snippet Acute erythroid leukemia (AEL) is a high-risk leukemia of poorly understood genetic basis, with controversy regarding diagnosis in the spectrum of...
Acute erythroid leukemia (AEL) is a high risk leukemia of poorly understood genetic basis, with controversy regarding diagnosis in the spectrum of...
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proquest
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pubmed
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springer
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StartPage 694
SubjectTerms 631/67/1990/283
631/67/1990/283/1897
Acute leukemia
Adolescent
Adult
Adults
Age
Agriculture
Animal Genetics and Genomics
Bioinformatics
Biomedical and Life Sciences
Biomedicine
Bone marrow
Cancer genetics
Cancer Research
Cancer therapies
Care and treatment
Cell cycle
Child
Child, Preschool
Children
Classification
Deoxyribonucleic acid
Diagnosis
DNA
DNA methylation
Epigenetics
Erythroleukemia
Female
fms-Like Tyrosine Kinase 3 - genetics
Gene Function
Genes
Genetic aspects
Genomes
Genomics
Genomics - methods
Homeodomain Proteins - genetics
Human Genetics
Humans
Infant
Infant, Newborn
Leukemia
Leukemia, Erythroblastic, Acute - genetics
Leukemogenesis
Male
Medical prognosis
Medical schools
Mutation
Mutation - genetics
Myelodysplastic syndrome
Myeloid leukemia
Myeloid-Lymphoid Leukemia Protein - genetics
Nuclear Proteins - genetics
Nucleophosmin
p53 Protein
Pediatrics
Prognosis
Risk
Subgroups
Therapeutic targets
Transcription
Tumor proteins
Tumor Suppressor Protein p53 - genetics
Tumors
Young Adult
Title Genomic subtyping and therapeutic targeting of acute erythroleukemia
URI https://link.springer.com/article/10.1038/s41588-019-0375-1
https://www.ncbi.nlm.nih.gov/pubmed/30926971
https://www.proquest.com/docview/2206006371
https://www.proquest.com/docview/2200781322
https://pubmed.ncbi.nlm.nih.gov/PMC6828160
Volume 51
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