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WHOLE-GENOME CRISPR LIBRARY SCREENS IDENTIFY CD48 AS AN ESSENTIAL MOLECULE IN ADULT T-CELL LEUKEMIA/LYMPHOMA FOR DEFINING SUSCEPTIBILITY TO NATURAL KILLER CELL-MEDIATED CYTOTOXICITY
Author(s): ,
Masahiro Chiba
Affiliations:
Department of Hematology,Hokkaido University Graduate School of Medicine,Sapporo,Japan
,
Joji Shimono
Affiliations:
Department of Hematology,Hokkaido University Graduate School of Medicine,Sapporo,Japan
,
Takashi Ishio
Affiliations:
Department of Hematology,Hokkaido University Graduate School of Medicine,Sapporo,Japan
,
Hideki Goto
Affiliations:
Department of Hematology,Hokkaido University Graduate School of Medicine,Sapporo,Japan
,
Satoshi Hashino
Affiliations:
Health Care Center,Hokkaido University,Sapporo,Japan
,
Takanori Teshima
Affiliations:
Department of Hematology,Hokkaido University Graduate School of Medicine,Sapporo,Japan
Masao Nakagawa
Affiliations:
Department of Hematology,Hokkaido University Graduate School of Medicine,Sapporo,Japan
EHA Library. Chiba M. 06/09/21; 325610; EP852
Masahiro Chiba
Masahiro Chiba
Contributions
Abstract
Presentation during EHA2021: All e-poster presentations will be made available as of Friday, June 11, 2021 (09:00 CEST) and will be accessible for on-demand viewing until August 15, 2021 on the Virtual Congress platform.

Abstract: EP852

Type: E-Poster Presentation

Session title: Lymphoma Biology & Translational Research

Background
Adult T-cell lymphoma/leukemia (ATLL) is a mature T-cell neoplasm and its prognosis is poor. Human T-cell leukemia virus type 1 (HTLV-1) is the causative retrovirus of ATL and it infects infants’ CD4 positive T cell through breast feeding. A fraction of the HTLV-1 infected individuals develops ATLL after more than 50 years. During the long latency period genetic alterations and aberrant gene expression accumulate extensively in ATLL cells. In particular, ATLL has high frequency of somatic mutations, genomic losses and epigenetic silencing in human leukocyte antigen (HLA)-A, HLA-B and β2 microglobulin, highlighting immune escape from T-cells as a hallmark of ATLL. In theory this 'missing self' increases susceptibility to natural killer (NK) cell-mediated killing but it remains unknown how ATLL cells evade NK cell-mediated immunosurveillance. In fact, activation of NK cells is controlled by signal integration from multiple stimulatory and inhibitory receptors on their cell surface so that functional elucidation for the key mechanism by which ATLL cells evade NK-mediated immune surveillance remains challenging. 

Aims
The aim of this study was to identify ATLL cell-intrinsic molecules which play essential roles for immune evasion from NK cell-mediated cytotoxicity against ATLL.

Methods
Two Cas9-expressing ATLL cell lines were lentivirally transduced with the human clustered regularly interspaced short palindromic repeat (CRISPR) Brunello pooled library (Addgene #73178) of 76,441 single-guide RNAs targeting 19,114 protein-coding genes, selected by puromycin, cultivated for 2 weeks enough to have genes fully inactivated by sgRNAs. The cells were co-cultured with human YT1 NK cells at 1:2 of effector:target ratio for 24-48 hours. Mogamulizumab, anti-human CCR4 monoclonal antibody, was added to the effector/target cell mixture, which enabled us to evaluate the responsible genes for both direct NK cytotoxicity and mogamulizumab-mediated antibody dependent cellular cytotoxicity (ADCC). Resistance genes were those for which the corresponding sgRNAs were enriched in the screening cell pool relative to the cell pool without screening. MAGeCK algorithm was used to rank target genes enriched in the screening.

Results
Twenty genes were overlapped between top-ranked 500 genes in two ATLL cell lines. As a proof of concept, CCR4 was identified as the best overlapped gene, confirming the reliability of our screening. One of the other overlapped genes was CD48, which is a signaling lymphocyte activation molecule (SLAM) family cell surface receptor and is an activating NK cell receptor by ligating 2B4 receptor on NK cells. Through further analysis, the ability of CD48 knockout ATLL cells for evading NK cell-mediated direct cytotoxicity was confirmed by using not only a NK cell line but also human primary NK cells with reduced interferon gamma induction and degranulation. Notably, we found that primary ATLL cells reduced their CD48 mRNA expression along with aggressiveness of clinical subtypes.

Conclusion
Our findings indicated that CD48 is an essential molecule in ATLL for defining susceptibility to NK cell-mediated cytotoxicity. Thus this study improved our current understanding of the mechanisms for immune evasion in ATLL and provides a rationale for evaluation of CD48 as a biomarker for NK cell-based immunotherapies in the future.

Keyword(s):

Presentation during EHA2021: All e-poster presentations will be made available as of Friday, June 11, 2021 (09:00 CEST) and will be accessible for on-demand viewing until August 15, 2021 on the Virtual Congress platform.

Abstract: EP852

Type: E-Poster Presentation

Session title: Lymphoma Biology & Translational Research

Background
Adult T-cell lymphoma/leukemia (ATLL) is a mature T-cell neoplasm and its prognosis is poor. Human T-cell leukemia virus type 1 (HTLV-1) is the causative retrovirus of ATL and it infects infants’ CD4 positive T cell through breast feeding. A fraction of the HTLV-1 infected individuals develops ATLL after more than 50 years. During the long latency period genetic alterations and aberrant gene expression accumulate extensively in ATLL cells. In particular, ATLL has high frequency of somatic mutations, genomic losses and epigenetic silencing in human leukocyte antigen (HLA)-A, HLA-B and β2 microglobulin, highlighting immune escape from T-cells as a hallmark of ATLL. In theory this 'missing self' increases susceptibility to natural killer (NK) cell-mediated killing but it remains unknown how ATLL cells evade NK cell-mediated immunosurveillance. In fact, activation of NK cells is controlled by signal integration from multiple stimulatory and inhibitory receptors on their cell surface so that functional elucidation for the key mechanism by which ATLL cells evade NK-mediated immune surveillance remains challenging. 

Aims
The aim of this study was to identify ATLL cell-intrinsic molecules which play essential roles for immune evasion from NK cell-mediated cytotoxicity against ATLL.

Methods
Two Cas9-expressing ATLL cell lines were lentivirally transduced with the human clustered regularly interspaced short palindromic repeat (CRISPR) Brunello pooled library (Addgene #73178) of 76,441 single-guide RNAs targeting 19,114 protein-coding genes, selected by puromycin, cultivated for 2 weeks enough to have genes fully inactivated by sgRNAs. The cells were co-cultured with human YT1 NK cells at 1:2 of effector:target ratio for 24-48 hours. Mogamulizumab, anti-human CCR4 monoclonal antibody, was added to the effector/target cell mixture, which enabled us to evaluate the responsible genes for both direct NK cytotoxicity and mogamulizumab-mediated antibody dependent cellular cytotoxicity (ADCC). Resistance genes were those for which the corresponding sgRNAs were enriched in the screening cell pool relative to the cell pool without screening. MAGeCK algorithm was used to rank target genes enriched in the screening.

Results
Twenty genes were overlapped between top-ranked 500 genes in two ATLL cell lines. As a proof of concept, CCR4 was identified as the best overlapped gene, confirming the reliability of our screening. One of the other overlapped genes was CD48, which is a signaling lymphocyte activation molecule (SLAM) family cell surface receptor and is an activating NK cell receptor by ligating 2B4 receptor on NK cells. Through further analysis, the ability of CD48 knockout ATLL cells for evading NK cell-mediated direct cytotoxicity was confirmed by using not only a NK cell line but also human primary NK cells with reduced interferon gamma induction and degranulation. Notably, we found that primary ATLL cells reduced their CD48 mRNA expression along with aggressiveness of clinical subtypes.

Conclusion
Our findings indicated that CD48 is an essential molecule in ATLL for defining susceptibility to NK cell-mediated cytotoxicity. Thus this study improved our current understanding of the mechanisms for immune evasion in ATLL and provides a rationale for evaluation of CD48 as a biomarker for NK cell-based immunotherapies in the future.

Keyword(s):

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