An Immunocompetent Mouse Model for MLL/AF9 Leukemia Reveals the Potential of Spontaneous Cytotoxic T-Cell Response to an Antigen Expressed in Leukemia Cells.

Leukemia differs substantially with respect to stromal milieu from tumors that progress locally as solid masses, and the physiological importance of immunosurveillance in leukemia remains unclear. However, currently available mouse leukemia models have critical limitations in the context of analyzin...

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Main Authors: Kana Hasegawa, Satomi Tanaka, Fumihiro Fujiki, Soyoko Morimoto, Hiroko Nakajima, Naoya Tatsumi, Jun Nakata, Satoshi Takashima, Sumiyuki Nishida, Akihiro Tsuboi, Yoshihiro Oka, Yusuke Oji, Atsushi Kumanogoh, Haruo Sugiyama, Naoki Hosen
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0144594&type=printable
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author Kana Hasegawa
Satomi Tanaka
Fumihiro Fujiki
Soyoko Morimoto
Hiroko Nakajima
Naoya Tatsumi
Jun Nakata
Satoshi Takashima
Sumiyuki Nishida
Akihiro Tsuboi
Yoshihiro Oka
Yusuke Oji
Atsushi Kumanogoh
Haruo Sugiyama
Naoki Hosen
author_facet Kana Hasegawa
Satomi Tanaka
Fumihiro Fujiki
Soyoko Morimoto
Hiroko Nakajima
Naoya Tatsumi
Jun Nakata
Satoshi Takashima
Sumiyuki Nishida
Akihiro Tsuboi
Yoshihiro Oka
Yusuke Oji
Atsushi Kumanogoh
Haruo Sugiyama
Naoki Hosen
author_sort Kana Hasegawa
collection DOAJ
description Leukemia differs substantially with respect to stromal milieu from tumors that progress locally as solid masses, and the physiological importance of immunosurveillance in leukemia remains unclear. However, currently available mouse leukemia models have critical limitations in the context of analyzing immunological regulation of leukemia development. In this study, we transferred mouse MLL/AF9 leukemia-initiating cells into immunocompetent recipient mice without any pre-conditioning such as irradiation, and then analyzed the spontaneous T cell response to an immunogenic antigen expressed in leukemia cells. When the minimum numbers of leukemia-initiating cells for engraftment were transferred, leukemia cells were eradicated by the adaptive immune response in most, if not all, wild-type mice, but not in Rag2-/- recipient mice, which lack adaptive immunity. By contrast, mice transplanted with larger numbers of leukemia cells always developed leukemia. In mice with advanced leukemia, antigen-specific CTLs were also expanded, but were unresponsive to antigen stimulation and expressed high levels of PD-1 and LAG-3. These results provide the first clear demonstration that the spontaneous CTL response to a tumor-cell antigen has the potential to eradicate leukemia, whereas antigen-specific CTLs are exhausted in animals with advanced leukemia. This immunocompetent mouse leukemia model provides a useful platform for developing effective immunotherapies against leukemia.
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spelling doaj-art-ff5de50689044014ac06fc076c337c5a2025-08-20T03:11:11ZengPublic Library of Science (PLoS)PLoS ONE1932-62032015-01-011012e014459410.1371/journal.pone.0144594An Immunocompetent Mouse Model for MLL/AF9 Leukemia Reveals the Potential of Spontaneous Cytotoxic T-Cell Response to an Antigen Expressed in Leukemia Cells.Kana HasegawaSatomi TanakaFumihiro FujikiSoyoko MorimotoHiroko NakajimaNaoya TatsumiJun NakataSatoshi TakashimaSumiyuki NishidaAkihiro TsuboiYoshihiro OkaYusuke OjiAtsushi KumanogohHaruo SugiyamaNaoki HosenLeukemia differs substantially with respect to stromal milieu from tumors that progress locally as solid masses, and the physiological importance of immunosurveillance in leukemia remains unclear. However, currently available mouse leukemia models have critical limitations in the context of analyzing immunological regulation of leukemia development. In this study, we transferred mouse MLL/AF9 leukemia-initiating cells into immunocompetent recipient mice without any pre-conditioning such as irradiation, and then analyzed the spontaneous T cell response to an immunogenic antigen expressed in leukemia cells. When the minimum numbers of leukemia-initiating cells for engraftment were transferred, leukemia cells were eradicated by the adaptive immune response in most, if not all, wild-type mice, but not in Rag2-/- recipient mice, which lack adaptive immunity. By contrast, mice transplanted with larger numbers of leukemia cells always developed leukemia. In mice with advanced leukemia, antigen-specific CTLs were also expanded, but were unresponsive to antigen stimulation and expressed high levels of PD-1 and LAG-3. These results provide the first clear demonstration that the spontaneous CTL response to a tumor-cell antigen has the potential to eradicate leukemia, whereas antigen-specific CTLs are exhausted in animals with advanced leukemia. This immunocompetent mouse leukemia model provides a useful platform for developing effective immunotherapies against leukemia.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0144594&type=printable
spellingShingle Kana Hasegawa
Satomi Tanaka
Fumihiro Fujiki
Soyoko Morimoto
Hiroko Nakajima
Naoya Tatsumi
Jun Nakata
Satoshi Takashima
Sumiyuki Nishida
Akihiro Tsuboi
Yoshihiro Oka
Yusuke Oji
Atsushi Kumanogoh
Haruo Sugiyama
Naoki Hosen
An Immunocompetent Mouse Model for MLL/AF9 Leukemia Reveals the Potential of Spontaneous Cytotoxic T-Cell Response to an Antigen Expressed in Leukemia Cells.
PLoS ONE
title An Immunocompetent Mouse Model for MLL/AF9 Leukemia Reveals the Potential of Spontaneous Cytotoxic T-Cell Response to an Antigen Expressed in Leukemia Cells.
title_full An Immunocompetent Mouse Model for MLL/AF9 Leukemia Reveals the Potential of Spontaneous Cytotoxic T-Cell Response to an Antigen Expressed in Leukemia Cells.
title_fullStr An Immunocompetent Mouse Model for MLL/AF9 Leukemia Reveals the Potential of Spontaneous Cytotoxic T-Cell Response to an Antigen Expressed in Leukemia Cells.
title_full_unstemmed An Immunocompetent Mouse Model for MLL/AF9 Leukemia Reveals the Potential of Spontaneous Cytotoxic T-Cell Response to an Antigen Expressed in Leukemia Cells.
title_short An Immunocompetent Mouse Model for MLL/AF9 Leukemia Reveals the Potential of Spontaneous Cytotoxic T-Cell Response to an Antigen Expressed in Leukemia Cells.
title_sort immunocompetent mouse model for mll af9 leukemia reveals the potential of spontaneous cytotoxic t cell response to an antigen expressed in leukemia cells
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0144594&type=printable
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