Characterization of mesenchymal stem cells in pre-B acute lymphoblastic leukemia

Components of the bone marrow microenvironment (BMM) have been shown to mediate the way in which leukemia develops, progresses and responds to treatment. Increasing evidence shows that leukemic cells hijack the BMM, altering its functioning and establishing leukemia-supportive interactions with stro...

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Published in:	Frontiers in cell and developmental biology Vol. 11; p. 1005494
Main Authors:	Hughes, Anastasia M, Kuek, Vincent, Oommen, Joyce, Chua, Grace-Alyssa, van Loenhout, Maria, Malinge, Sebastien, Kotecha, Rishi S, Cheung, Laurence C
Format:	Journal Article
Language:	English
Published:	Switzerland Frontiers Media S.A 20-01-2023
Subjects:	bone marrow bone marrow microenvironment Cell and Developmental Biology leukemia mesenchymal stem cell pre-B cell acute lymphoblastic leukemia leukemia mesenchymal stem cell bone marrow microenvironment bone marrow pre-B cell acute lymphoblastic leukemia
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Abstract	Components of the bone marrow microenvironment (BMM) have been shown to mediate the way in which leukemia develops, progresses and responds to treatment. Increasing evidence shows that leukemic cells hijack the BMM, altering its functioning and establishing leukemia-supportive interactions with stromal and immune cells. While previous work has highlighted functional defects in the mesenchymal stem cell (MSC) population from the BMM of acute leukemias, thorough characterization and molecular profiling of MSCs in pre-B cell acute lymphoblastic leukemia (B-ALL), the most common cancer in children, has not been conducted. Here, we investigated the cellular and transcriptome profiles of MSCs isolated from the BMM of an immunocompetent BCR-ABL1 model of B-ALL. Leukemia-associated MSCs exhibited reduced self-renewal capacity and significant changes in numerous molecular signatures, including upregulation of inflammatory signaling pathways. Additionally, we found downregulation of genes involved in extracellular matrix organization and osteoblastogenesis in leukemia-associated MSCs. This study provides cellular and molecular insights into the role of MSCs during B-ALL progression.
AbstractList	Components of the bone marrow microenvironment (BMM) have been shown to mediate the way in which leukemia develops, progresses and responds to treatment. Increasing evidence shows that leukemic cells hijack the BMM, altering its functioning and establishing leukemia-supportive interactions with stromal and immune cells. While previous work has highlighted functional defects in the mesenchymal stem cell (MSC) population from the BMM of acute leukemias, thorough characterization and molecular profiling of MSCs in pre-B cell acute lymphoblastic leukemia (B-ALL), the most common cancer in children, has not been conducted. Here, we investigated the cellular and transcriptome profiles of MSCs isolated from the BMM of an immunocompetent BCR-ABL1 + model of B-ALL. Leukemia-associated MSCs exhibited reduced self-renewal capacity in vitro and significant changes in numerous molecular signatures, including upregulation of inflammatory signaling pathways. Additionally, we found downregulation of genes involved in extracellular matrix organization and osteoblastogenesis in leukemia-associated MSCs. This study provides cellular and molecular insights into the role of MSCs during B-ALL progression. Components of the bone marrow microenvironment (BMM) have been shown to mediate the way in which leukemia develops, progresses and responds to treatment. Increasing evidence shows that leukemic cells hijack the BMM, altering its functioning and establishing leukemia-supportive interactions with stromal and immune cells. While previous work has highlighted functional defects in the mesenchymal stem cell (MSC) population from the BMM of acute leukemias, thorough characterization and molecular profiling of MSCs in pre-B cell acute lymphoblastic leukemia (B-ALL), the most common cancer in children, has not been conducted. Here, we investigated the cellular and transcriptome profiles of MSCs isolated from the BMM of an immunocompetent BCR-ABL1+ model of B-ALL. Leukemia-associated MSCs exhibited reduced self-renewal capacity in vitro and significant changes in numerous molecular signatures, including upregulation of inflammatory signaling pathways. Additionally, we found downregulation of genes involved in extracellular matrix organization and osteoblastogenesis in leukemia-associated MSCs. This study provides cellular and molecular insights into the role of MSCs during B-ALL progression. Components of the bone marrow microenvironment (BMM) have been shown to mediate the way in which leukemia develops, progresses and responds to treatment. Increasing evidence shows that leukemic cells hijack the BMM, altering its functioning and establishing leukemia-supportive interactions with stromal and immune cells. While previous work has highlighted functional defects in the mesenchymal stem cell (MSC) population from the BMM of acute leukemias, thorough characterization and molecular profiling of MSCs in pre-B cell acute lymphoblastic leukemia (B-ALL), the most common cancer in children, has not been conducted. Here, we investigated the cellular and transcriptome profiles of MSCs isolated from the BMM of an immunocompetent BCR-ABL1 model of B-ALL. Leukemia-associated MSCs exhibited reduced self-renewal capacity and significant changes in numerous molecular signatures, including upregulation of inflammatory signaling pathways. Additionally, we found downregulation of genes involved in extracellular matrix organization and osteoblastogenesis in leukemia-associated MSCs. This study provides cellular and molecular insights into the role of MSCs during B-ALL progression.
Author	Chua, Grace-Alyssa Kuek, Vincent van Loenhout, Maria Oommen, Joyce Malinge, Sebastien Cheung, Laurence C Kotecha, Rishi S Hughes, Anastasia M
AuthorAffiliation	2 Curtin Medical School , Curtin University , Perth , WA , Australia 4 Department of Clinical Haematology , Oncology, Blood and Marrow Transplantation , Perth Children’s Hospital , Perth , WA , Australia 5 Curtin Health Innovation Research Institute , Curtin University , Perth , WA , Australia 1 Leukaemia Translational Research Laboratory , Telethon Kids Cancer Centre , Telethon Kids Institute , Perth , WA , Australia 3 School of Medicine , University of Western Australia , Perth , WA , Australia
AuthorAffiliation_xml	– name: 5 Curtin Health Innovation Research Institute , Curtin University , Perth , WA , Australia – name: 3 School of Medicine , University of Western Australia , Perth , WA , Australia – name: 2 Curtin Medical School , Curtin University , Perth , WA , Australia – name: 1 Leukaemia Translational Research Laboratory , Telethon Kids Cancer Centre , Telethon Kids Institute , Perth , WA , Australia – name: 4 Department of Clinical Haematology , Oncology, Blood and Marrow Transplantation , Perth Children’s Hospital , Perth , WA , Australia
Author_xml	– sequence: 1 givenname: Anastasia M surname: Hughes fullname: Hughes, Anastasia M organization: Curtin Medical School, Curtin University, Perth, WA, Australia – sequence: 2 givenname: Vincent surname: Kuek fullname: Kuek, Vincent organization: School of Medicine, University of Western Australia, Perth, WA, Australia – sequence: 3 givenname: Joyce surname: Oommen fullname: Oommen, Joyce organization: Leukaemia Translational Research Laboratory, Telethon Kids Cancer Centre, Telethon Kids Institute, Perth, WA, Australia – sequence: 4 givenname: Grace-Alyssa surname: Chua fullname: Chua, Grace-Alyssa organization: Leukaemia Translational Research Laboratory, Telethon Kids Cancer Centre, Telethon Kids Institute, Perth, WA, Australia – sequence: 5 givenname: Maria surname: van Loenhout fullname: van Loenhout, Maria organization: Leukaemia Translational Research Laboratory, Telethon Kids Cancer Centre, Telethon Kids Institute, Perth, WA, Australia – sequence: 6 givenname: Sebastien surname: Malinge fullname: Malinge, Sebastien organization: School of Medicine, University of Western Australia, Perth, WA, Australia – sequence: 7 givenname: Rishi S surname: Kotecha fullname: Kotecha, Rishi S organization: Department of Clinical Haematology, Oncology, Blood and Marrow Transplantation, Perth Children's Hospital, Perth, WA, Australia – sequence: 8 givenname: Laurence C surname: Cheung fullname: Cheung, Laurence C organization: Curtin Health Innovation Research Institute, Curtin University, Perth, WA, Australia
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Copyright	Copyright © 2023 Hughes, Kuek, Oommen, Chua, van Loenhout, Malinge, Kotecha and Cheung. Copyright © 2023 Hughes, Kuek, Oommen, Chua, van Loenhout, Malinge, Kotecha and Cheung. 2023 Hughes, Kuek, Oommen, Chua, van Loenhout, Malinge, Kotecha and Cheung
Copyright_xml	– notice: Copyright © 2023 Hughes, Kuek, Oommen, Chua, van Loenhout, Malinge, Kotecha and Cheung. – notice: Copyright © 2023 Hughes, Kuek, Oommen, Chua, van Loenhout, Malinge, Kotecha and Cheung. 2023 Hughes, Kuek, Oommen, Chua, van Loenhout, Malinge, Kotecha and Cheung
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Keywords	leukemia mesenchymal stem cell bone marrow microenvironment bone marrow pre-B cell acute lymphoblastic leukemia
Language	English
License	Copyright © 2023 Hughes, Kuek, Oommen, Chua, van Loenhout, Malinge, Kotecha and Cheung. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Reviewed by: Matthew Witkowski, University of Colorado Anschutz Medical Campus, United States Kim Kampen, Maastricht University, Netherlands Edited by: Charles De Bock, Children’s Cancer Institute Australia, Australia This article was submitted to Stem Cell Research, a section of the journal Frontiers in Cell and Developmental Biology
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SubjectTerms	bone marrow bone marrow microenvironment Cell and Developmental Biology leukemia mesenchymal stem cell pre-B cell acute lymphoblastic leukemia
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Title	Characterization of mesenchymal stem cells in pre-B acute lymphoblastic leukemia
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