PD-L1/L2 protein levels rapidly increase on monocytes via trogocytosis from tumor cells in classical Hodgkin lymphoma

In classical Hodgkin lymphoma (cHL)—characterized by the presence of Hodgkin and Reed-Sternberg (HRS) cells—tumor-associated macrophages (TAMs) play a pivotal role in tumor formation. However, the significance of direct contact between HRS cells and TAMs has not been elucidated. HRS cells and TAMs a...

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Published inLeukemia Vol. 34; no. 9; pp. 2405 - 2417
Main Authors Kawashima, Masaharu, Carreras, Joaquim, Higuchi, Hiroshi, Kotaki, Ryutaro, Hoshina, Takahiro, Okuyama, Kazuki, Suzuki, Naoto, Kakizaki, Masatoshi, Miyatake, Yuji, Ando, Kiyoshi, Nakayama, Masafumi, Umezu, Shinjiro, Horie, Ryouichi, Higuchi, Yuriko, Katagiri, Koko, Goyama, Susumu, Kitamura, Toshio, Chamoto, Kenji, Yano, Shingo, Nakamura, Naoya, Kotani, Ai
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.09.2020
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Abstract In classical Hodgkin lymphoma (cHL)—characterized by the presence of Hodgkin and Reed-Sternberg (HRS) cells—tumor-associated macrophages (TAMs) play a pivotal role in tumor formation. However, the significance of direct contact between HRS cells and TAMs has not been elucidated. HRS cells and TAMs are known to express PD-L1, which leads to PD-1 + CD4 + T cell exhaustion in cHL. Here, we found that PD-L1/L2 expression was elevated in monocytes co-cultured with HRS cells within 1 h, but not in monocytes cultured with supernatants of HRS cells. Immunofluorescence analysis of PD-L1/L2 revealed that their upregulation resulted in membrane transfer called “trogocytosis” from HRS cells to monocytes. PD-L1/L2 upregulation was not observed in monocytes co-cultured with PD-L1/L2-deficient HRS cells, validating the hypothesis that there is a direct transfer of PD-L1/L2 from HRS cells to monocytes. In the patients, both ligands (PD-L1/L2) were upregulated in TAMs in contact with HRS cells, but not in TAMs distant from HRS cells, suggesting that trogocytosis occurs in cHL patients. Taken together, trogocytosis may be one of the mechanisms that induces rapid upregulation of PD-L1/L2 in monocytes to evade antitumor immunity through the suppression of T cells as mediated by MHC antigen presentation.
AbstractList In classical Hodgkin lymphoma (cHL)--characterized by the presence of Hodgkin and Reed-Sternberg (HRS) cells--tumor-associated macrophages (TAMs) play a pivotal role in tumor formation. However, the significance of direct contact between HRS cells and TAMs has not been elucidated. HRS cells and TAMs are known to express PD-L1, which leads to PD-1.sup.+ CD4.sup.+ T cell exhaustion in cHL. Here, we found that PD-L1/L2 expression was elevated in monocytes co-cultured with HRS cells within 1 h, but not in monocytes cultured with supernatants of HRS cells. Immunofluorescence analysis of PD-L1/L2 revealed that their upregulation resulted in membrane transfer called "trogocytosis" from HRS cells to monocytes. PD-L1/L2 upregulation was not observed in monocytes co-cultured with PD-L1/L2-deficient HRS cells, validating the hypothesis that there is a direct transfer of PD-L1/L2 from HRS cells to monocytes. In the patients, both ligands (PD-L1/L2) were upregulated in TAMs in contact with HRS cells, but not in TAMs distant from HRS cells, suggesting that trogocytosis occurs in cHL patients. Taken together, trogocytosis may be one of the mechanisms that induces rapid upregulation of PD-L1/L2 in monocytes to evade antitumor immunity through the suppression of T cells as mediated by MHC antigen presentation.
In classical Hodgkin lymphoma (cHL)—characterized by the presence of Hodgkin and Reed-Sternberg (HRS) cells—tumor-associated macrophages (TAMs) play a pivotal role in tumor formation. However, the significance of direct contact between HRS cells and TAMs has not been elucidated. HRS cells and TAMs are known to express PD-L1, which leads to PD-1 + CD4 + T cell exhaustion in cHL. Here, we found that PD-L1/L2 expression was elevated in monocytes co-cultured with HRS cells within 1 h, but not in monocytes cultured with supernatants of HRS cells. Immunofluorescence analysis of PD-L1/L2 revealed that their upregulation resulted in membrane transfer called “trogocytosis” from HRS cells to monocytes. PD-L1/L2 upregulation was not observed in monocytes co-cultured with PD-L1/L2-deficient HRS cells, validating the hypothesis that there is a direct transfer of PD-L1/L2 from HRS cells to monocytes. In the patients, both ligands (PD-L1/L2) were upregulated in TAMs in contact with HRS cells, but not in TAMs distant from HRS cells, suggesting that trogocytosis occurs in cHL patients. Taken together, trogocytosis may be one of the mechanisms that induces rapid upregulation of PD-L1/L2 in monocytes to evade antitumor immunity through the suppression of T cells as mediated by MHC antigen presentation.
In classical Hodgkin lymphoma (cHL)—characterized by the presence of Hodgkin and Reed-Sternberg (HRS) cells—tumor-associated macrophages (TAMs) play a pivotal role in tumor formation. However, the significance of direct contact between HRS cells and TAMs has not been elucidated. HRS cells and TAMs are known to express PD-L1, which leads to PD-1+ CD4+ T cell exhaustion in cHL. Here, we found that PD-L1/L2 expression was elevated in monocytes co-cultured with HRS cells within 1 h, but not in monocytes cultured with supernatants of HRS cells. Immunofluorescence analysis of PD-L1/L2 revealed that their upregulation resulted in membrane transfer called “trogocytosis” from HRS cells to monocytes. PD-L1/L2 upregulation was not observed in monocytes co-cultured with PD-L1/L2-deficient HRS cells, validating the hypothesis that there is a direct transfer of PD-L1/L2 from HRS cells to monocytes. In the patients, both ligands (PD-L1/L2) were upregulated in TAMs in contact with HRS cells, but not in TAMs distant from HRS cells, suggesting that trogocytosis occurs in cHL patients. Taken together, trogocytosis may be one of the mechanisms that induces rapid upregulation of PD-L1/L2 in monocytes to evade antitumor immunity through the suppression of T cells as mediated by MHC antigen presentation.
In classical Hodgkin lymphoma (cHL)-characterized by the presence of Hodgkin and Reed-Sternberg (HRS) cells-tumor-associated macrophages (TAMs) play a pivotal role in tumor formation. However, the significance of direct contact between HRS cells and TAMs has not been elucidated. HRS cells and TAMs are known to express PD-L1, which leads to PD-1 CD4 T cell exhaustion in cHL. Here, we found that PD-L1/L2 expression was elevated in monocytes co-cultured with HRS cells within 1 h, but not in monocytes cultured with supernatants of HRS cells. Immunofluorescence analysis of PD-L1/L2 revealed that their upregulation resulted in membrane transfer called "trogocytosis" from HRS cells to monocytes. PD-L1/L2 upregulation was not observed in monocytes co-cultured with PD-L1/L2-deficient HRS cells, validating the hypothesis that there is a direct transfer of PD-L1/L2 from HRS cells to monocytes. In the patients, both ligands (PD-L1/L2) were upregulated in TAMs in contact with HRS cells, but not in TAMs distant from HRS cells, suggesting that trogocytosis occurs in cHL patients. Taken together, trogocytosis may be one of the mechanisms that induces rapid upregulation of PD-L1/L2 in monocytes to evade antitumor immunity through the suppression of T cells as mediated by MHC antigen presentation.
Audience Academic
Author Hoshina, Takahiro
Carreras, Joaquim
Higuchi, Hiroshi
Kitamura, Toshio
Kakizaki, Masatoshi
Miyatake, Yuji
Nakamura, Naoya
Katagiri, Koko
Goyama, Susumu
Higuchi, Yuriko
Kotani, Ai
Yano, Shingo
Kawashima, Masaharu
Kotaki, Ryutaro
Chamoto, Kenji
Ando, Kiyoshi
Okuyama, Kazuki
Suzuki, Naoto
Nakayama, Masafumi
Umezu, Shinjiro
Horie, Ryouichi
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  organization: Frontier Research Institute for Interdisciplinary Sciences, Tohoku University
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  organization: Department of Modern Mechanical Engineering, Waseda University
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  organization: Division of Hematology, Department of Laboratory Sciences, School of Allied Health Sciences, Kitasato University
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  email: aikotani@k-lab.jp
  organization: Department of Hematological Malignancy, Institute of Medical Science, Tokai University, Precursory Research for Embryonic Science and Technology, Japan Science and Technology Agency, AMED-PRIME, Japan Agency for Medical Research and Development
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32089543$$D View this record in MEDLINE/PubMed
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Snippet In classical Hodgkin lymphoma (cHL)—characterized by the presence of Hodgkin and Reed-Sternberg (HRS) cells—tumor-associated macrophages (TAMs) play a pivotal...
In classical Hodgkin lymphoma (cHL)-characterized by the presence of Hodgkin and Reed-Sternberg (HRS) cells-tumor-associated macrophages (TAMs) play a pivotal...
In classical Hodgkin lymphoma (cHL)--characterized by the presence of Hodgkin and Reed-Sternberg (HRS) cells--tumor-associated macrophages (TAMs) play a...
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SubjectTerms 13/31
13/51
14/19
631/250/580
631/67/1990/291/1556
Analysis
Antigen presentation
Antigens
B cells
B7-H1 Antigen - metabolism
Cancer Research
CD4 antigen
Cell Line, Tumor
Cell Movement
Critical Care Medicine
Exhaustion
Hematology
Hodgkin Disease - immunology
Hodgkin Disease - metabolism
Hodgkin Disease - pathology
Hodgkin's lymphoma
Humans
Immunofluorescence
Intensive
Internal Medicine
Lymphocytes
Lymphocytes T
Lymphoma
Macrophages
Major histocompatibility complex
Major Histocompatibility Complex - immunology
Medicine
Medicine & Public Health
Monocytes
Monocytes - metabolism
Non-Hodgkin's lymphomas
Oncology
PD-1 protein
PD-L1 protein
Plasma membranes
Programmed Cell Death 1 Ligand 2 Protein - metabolism
T cells
Tumor cells
Tumor Microenvironment - immunology
Title PD-L1/L2 protein levels rapidly increase on monocytes via trogocytosis from tumor cells in classical Hodgkin lymphoma
URI https://link.springer.com/article/10.1038/s41375-020-0737-9
https://www.ncbi.nlm.nih.gov/pubmed/32089543
https://www.proquest.com/docview/2437278187
https://www.proquest.com/docview/2475018475
https://search.proquest.com/docview/2363070224
Volume 34
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