Proteogenomic characterization of highly enriched viable leukemic blasts in acute myeloid leukemia: A SWOG report

Abstract Introduction Acute myeloid leukemia (AML) remains one of the deadliest hematopoietic malignancies. A better understanding of the molecular biology governing AML may lead to improved risk stratification and facilitate the development of novel therapies. Proteins are responsible for much of t...

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Main Authors: Jasmine Naru, Megan Othus, ChenWei Lin, Melinda A. Biernacki, Marie Bleakley, Thomas R. Chauncey, Harry P. Erba, Min Fang, Matthew P. Fitzgibbon, Phillip R. Gafken, Richard G. Ivey, Jacob J. Kennedy, Travis D. Lorentzen, Soheil Meshinchi, Anna Moseley, Era L. Pogosova‐Agadjanyan, Vivian M. Liu, Jerald P. Radich, Uliana J. Voytovich, Pei Wang, Jeffrey R. Whiteaker, Cheryl L. Willman, Feinan Wu, Amanda G. Paulovich, Derek L. Stirewalt
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Language:English
Published: Wiley 2024-12-01
Series:eJHaem
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Online Access:https://doi.org/10.1002/jha2.1041
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author Jasmine Naru
Megan Othus
ChenWei Lin
Melinda A. Biernacki
Marie Bleakley
Thomas R. Chauncey
Harry P. Erba
Min Fang
Matthew P. Fitzgibbon
Phillip R. Gafken
Richard G. Ivey
Jacob J. Kennedy
Travis D. Lorentzen
Soheil Meshinchi
Anna Moseley
Era L. Pogosova‐Agadjanyan
Vivian M. Liu
Jerald P. Radich
Uliana J. Voytovich
Pei Wang
Jeffrey R. Whiteaker
Cheryl L. Willman
Feinan Wu
Amanda G. Paulovich
Derek L. Stirewalt
author_facet Jasmine Naru
Megan Othus
ChenWei Lin
Melinda A. Biernacki
Marie Bleakley
Thomas R. Chauncey
Harry P. Erba
Min Fang
Matthew P. Fitzgibbon
Phillip R. Gafken
Richard G. Ivey
Jacob J. Kennedy
Travis D. Lorentzen
Soheil Meshinchi
Anna Moseley
Era L. Pogosova‐Agadjanyan
Vivian M. Liu
Jerald P. Radich
Uliana J. Voytovich
Pei Wang
Jeffrey R. Whiteaker
Cheryl L. Willman
Feinan Wu
Amanda G. Paulovich
Derek L. Stirewalt
author_sort Jasmine Naru
collection DOAJ
description Abstract Introduction Acute myeloid leukemia (AML) remains one of the deadliest hematopoietic malignancies. A better understanding of the molecular biology governing AML may lead to improved risk stratification and facilitate the development of novel therapies. Proteins are responsible for much of the biology of cells. Several studies have examined the global proteome in bulk mononuclear cells (MNCs) from AML specimens, which are comprised a heterogenous population of cells at various stages of differentiation. Methods Given the potential impact of the nonleukemic cells on protein expression profiles, we applied an integrative proteogenomic approach utilizing next‐generation sequencing and mass spectrometry‐based proteomics to identify novel protein biomarkers in unsorted MNCs and viable leukemic blasts (VLBs) isolated from blood and bone marrow specimens obtained at the time of AML diagnosis. Results We identified significant differences in protein expression between VLBs and MNCs. Subsequent studies (N = 27) focused on proteomic profiling of VLBs that identified novel candidate biomarkers associated with mutational genotypes and clinical outcome, some of which were recapitulated in an independent cohort of patients. Using mass spectrometry, we also detected mutated protein products, some of which were predicted via in silico analyses to be potential neoantigens amenable to adoptive immunotherapy. As previously described, analyses comparing transcript and protein expression showed an overall modest correlation between mRNA and protein dataset, but enriching for genes associated with mutations significantly improved the protein–RNA correlation. Conclusion Together, the results provide insight into the biology of VLBs and demonstrate the gains derived from examining the proteome in addition to genome and transcriptome.
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spelling doaj-art-18d3b04e042e48a2a897b435a871a0b62024-12-16T12:47:38ZengWileyeJHaem2688-61462024-12-01561243125110.1002/jha2.1041Proteogenomic characterization of highly enriched viable leukemic blasts in acute myeloid leukemia: A SWOG reportJasmine Naru0Megan Othus1ChenWei Lin2Melinda A. Biernacki3Marie Bleakley4Thomas R. Chauncey5Harry P. Erba6Min Fang7Matthew P. Fitzgibbon8Phillip R. Gafken9Richard G. Ivey10Jacob J. Kennedy11Travis D. Lorentzen12Soheil Meshinchi13Anna Moseley14Era L. Pogosova‐Agadjanyan15Vivian M. Liu16Jerald P. Radich17Uliana J. Voytovich18Pei Wang19Jeffrey R. Whiteaker20Cheryl L. Willman21Feinan Wu22Amanda G. Paulovich23Derek L. Stirewalt24Translational Science and Therapeutics Division Fred Hutch Seattle Washington USATranslational Science and Therapeutics Division Fred Hutch Seattle Washington USATranslational Science and Therapeutics Division Fred Hutch Seattle Washington USATranslational Science and Therapeutics Division Fred Hutch Seattle Washington USATranslational Science and Therapeutics Division Fred Hutch Seattle Washington USATranslational Science and Therapeutics Division Fred Hutch Seattle Washington USADuke Cancer Institute Durham North Carolina USATranslational Science and Therapeutics Division Fred Hutch Seattle Washington USAGenomics and Bioinformatics Shared Resource Fred Hutch Seattle Washington USAProteomics and Metabolomics Shared Resource Fred Hutch Seattle Washington USATranslational Science and Therapeutics Division Fred Hutch Seattle Washington USATranslational Science and Therapeutics Division Fred Hutch Seattle Washington USATranslational Science and Therapeutics Division Fred Hutch Seattle Washington USATranslational Science and Therapeutics Division Fred Hutch Seattle Washington USATranslational Science and Therapeutics Division Fred Hutch Seattle Washington USATranslational Science and Therapeutics Division Fred Hutch Seattle Washington USATranslational Science and Therapeutics Division Fred Hutch Seattle Washington USATranslational Science and Therapeutics Division Fred Hutch Seattle Washington USATranslational Science and Therapeutics Division Fred Hutch Seattle Washington USADepartment of Genetics and Genomics Icahn School of Medicine at Mount Sinai New York New York USATranslational Science and Therapeutics Division Fred Hutch Seattle Washington USADepartment of Laboratory Medicine and Pathology Mayo Clinic Comprehensive Cancer Center Rochester Minnesota USAGenomics and Bioinformatics Shared Resource Fred Hutch Seattle Washington USATranslational Science and Therapeutics Division Fred Hutch Seattle Washington USATranslational Science and Therapeutics Division Fred Hutch Seattle Washington USAAbstract Introduction Acute myeloid leukemia (AML) remains one of the deadliest hematopoietic malignancies. A better understanding of the molecular biology governing AML may lead to improved risk stratification and facilitate the development of novel therapies. Proteins are responsible for much of the biology of cells. Several studies have examined the global proteome in bulk mononuclear cells (MNCs) from AML specimens, which are comprised a heterogenous population of cells at various stages of differentiation. Methods Given the potential impact of the nonleukemic cells on protein expression profiles, we applied an integrative proteogenomic approach utilizing next‐generation sequencing and mass spectrometry‐based proteomics to identify novel protein biomarkers in unsorted MNCs and viable leukemic blasts (VLBs) isolated from blood and bone marrow specimens obtained at the time of AML diagnosis. Results We identified significant differences in protein expression between VLBs and MNCs. Subsequent studies (N = 27) focused on proteomic profiling of VLBs that identified novel candidate biomarkers associated with mutational genotypes and clinical outcome, some of which were recapitulated in an independent cohort of patients. Using mass spectrometry, we also detected mutated protein products, some of which were predicted via in silico analyses to be potential neoantigens amenable to adoptive immunotherapy. As previously described, analyses comparing transcript and protein expression showed an overall modest correlation between mRNA and protein dataset, but enriching for genes associated with mutations significantly improved the protein–RNA correlation. Conclusion Together, the results provide insight into the biology of VLBs and demonstrate the gains derived from examining the proteome in addition to genome and transcriptome.https://doi.org/10.1002/jha2.1041AMLhematological malignancyneoantigensproteogenomicstranscriptomics
spellingShingle Jasmine Naru
Megan Othus
ChenWei Lin
Melinda A. Biernacki
Marie Bleakley
Thomas R. Chauncey
Harry P. Erba
Min Fang
Matthew P. Fitzgibbon
Phillip R. Gafken
Richard G. Ivey
Jacob J. Kennedy
Travis D. Lorentzen
Soheil Meshinchi
Anna Moseley
Era L. Pogosova‐Agadjanyan
Vivian M. Liu
Jerald P. Radich
Uliana J. Voytovich
Pei Wang
Jeffrey R. Whiteaker
Cheryl L. Willman
Feinan Wu
Amanda G. Paulovich
Derek L. Stirewalt
Proteogenomic characterization of highly enriched viable leukemic blasts in acute myeloid leukemia: A SWOG report
eJHaem
AML
hematological malignancy
neoantigens
proteogenomics
transcriptomics
title Proteogenomic characterization of highly enriched viable leukemic blasts in acute myeloid leukemia: A SWOG report
title_full Proteogenomic characterization of highly enriched viable leukemic blasts in acute myeloid leukemia: A SWOG report
title_fullStr Proteogenomic characterization of highly enriched viable leukemic blasts in acute myeloid leukemia: A SWOG report
title_full_unstemmed Proteogenomic characterization of highly enriched viable leukemic blasts in acute myeloid leukemia: A SWOG report
title_short Proteogenomic characterization of highly enriched viable leukemic blasts in acute myeloid leukemia: A SWOG report
title_sort proteogenomic characterization of highly enriched viable leukemic blasts in acute myeloid leukemia a swog report
topic AML
hematological malignancy
neoantigens
proteogenomics
transcriptomics
url https://doi.org/10.1002/jha2.1041
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