THBS1-producing tumor-infiltrating monocyte-like cells contribute to immunosuppression and metastasis in colorectal cancer

Mesenchymal activation, characterized by dense stromal infiltration of immune and mesenchymal cells, fuels the aggressiveness of colorectal cancers (CRC), driving progression and metastasis. Targetable molecules in the tumor microenvironment (TME) need to be identified to improve the outcome in CRC...

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Published inNature communications Vol. 14; no. 1; pp. 5534 - 19
Main Authors Omatsu, Mayuki, Nakanishi, Yuki, Iwane, Kosuke, Aoyama, Naoki, Duran, Angeles, Muta, Yu, Martinez-Ordoñez, Anxo, Han, Qixiu, Agatsuma, Nobukazu, Mizukoshi, Kenta, Kawai, Munenori, Yamakawa, Go, Namikawa, Mio, Hamada, Kensuke, Fukunaga, Yuichi, Utsumi, Takahiro, Sono, Makoto, Masuda, Tomonori, Hata, Akitaka, Araki, Osamu, Nagao, Munemasa, Yoshikawa, Takaaki, Ogawa, Satoshi, Hiramatsu, Yukiko, Tsuda, Motoyuki, Maruno, Takahisa, Kogame, Toshiaki, Kasashima, Hiroaki, Kakiuchi, Nobuyuki, Nakagawa, Masahiro M., Kawada, Kenji, Yashiro, Masakazu, Maeda, Kiyoshi, Saito, Yasuyuki, Matozaki, Takashi, Fukuda, Akihisa, Kabashima, Kenji, Obama, Kazutaka, Ogawa, Seishi, Sheibani, Nader, Diaz-Meco, Maria T., Moscat, Jorge, Seno, Hiroshi
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 25.09.2023
Nature Publishing Group
Nature Portfolio
Subjects
13/105
13/109
13/2
13/31
13/51
14/1
38/35
38/39
38/5
38/88
38/90
38/91
631/250/251/1574
631/67/327
64/110
692/4020/1503/1504/1885
96/95
Animal models
Animals
Antitumor agents
Biomarkers
Bone marrow
Cancer
Colorectal cancer
Colorectal carcinoma
Colorectal Neoplasms
CXCL12 protein
Cytotoxicity
Humanities and Social Sciences
Humans
Immune Checkpoint Inhibitors
Immunosuppression
Immunosuppression Therapy
Immunosuppressive agents
Inflammation
Lymphocytes T
Male
Malignancy
Mesenchyme
Metastases
Metastasis
Mice
Monocytes
multidisciplinary
Phenotypes
Prognosis
Science
Science (multidisciplinary)
Thrombospondin
Tumor Microenvironment
Vascularization
Online AccessGet full text
ISSN2041-1723
2041-1723
DOI10.1038/s41467-023-41095-y

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Abstract Mesenchymal activation, characterized by dense stromal infiltration of immune and mesenchymal cells, fuels the aggressiveness of colorectal cancers (CRC), driving progression and metastasis. Targetable molecules in the tumor microenvironment (TME) need to be identified to improve the outcome in CRC patients with this aggressive phenotype. This study reports a positive link between high thrombospondin-1 (THBS1) expression and mesenchymal characteristics, immunosuppression, and unfavorable CRC prognosis. Bone marrow-derived monocyte-like cells recruited by CXCL12 are the primary source of THBS1, which contributes to the development of metastasis by inducing cytotoxic T-cell exhaustion and impairing vascularization. Furthermore, in orthotopically generated CRC models in male mice, THBS1 loss in the TME renders tumors partially sensitive to immune checkpoint inhibitors and anti-cancer drugs. Our study establishes THBS1 as a potential biomarker for identifying mesenchymal CRC and as a critical suppressor of antitumor immunity that contributes to the progression of this malignancy with a poor prognosis. Thrombospondin-1 (THBS1) is a matricellular protein highly expressed in inflammatory processes, including cancer. Here the authors show that bone-marrow derived monocyte-like cells are the primary source of THBS1 in colorectal cancer, associated with mesenchymal characteristics, immunosuppression and a poor prognosis.
AbstractList Mesenchymal activation, characterized by dense stromal infiltration of immune and mesenchymal cells, fuels the aggressiveness of colorectal cancers (CRC), driving progression and metastasis. Targetable molecules in the tumor microenvironment (TME) need to be identified to improve the outcome in CRC patients with this aggressive phenotype. This study reports a positive link between high thrombospondin-1 (THBS1) expression and mesenchymal characteristics, immunosuppression, and unfavorable CRC prognosis. Bone marrow-derived monocyte-like cells recruited by CXCL12 are the primary source of THBS1, which contributes to the development of metastasis by inducing cytotoxic T-cell exhaustion and impairing vascularization. Furthermore, in orthotopically generated CRC models in male mice, THBS1 loss in the TME renders tumors partially sensitive to immune checkpoint inhibitors and anti-cancer drugs. Our study establishes THBS1 as a potential biomarker for identifying mesenchymal CRC and as a critical suppressor of antitumor immunity that contributes to the progression of this malignancy with a poor prognosis.Mesenchymal activation, characterized by dense stromal infiltration of immune and mesenchymal cells, fuels the aggressiveness of colorectal cancers (CRC), driving progression and metastasis. Targetable molecules in the tumor microenvironment (TME) need to be identified to improve the outcome in CRC patients with this aggressive phenotype. This study reports a positive link between high thrombospondin-1 (THBS1) expression and mesenchymal characteristics, immunosuppression, and unfavorable CRC prognosis. Bone marrow-derived monocyte-like cells recruited by CXCL12 are the primary source of THBS1, which contributes to the development of metastasis by inducing cytotoxic T-cell exhaustion and impairing vascularization. Furthermore, in orthotopically generated CRC models in male mice, THBS1 loss in the TME renders tumors partially sensitive to immune checkpoint inhibitors and anti-cancer drugs. Our study establishes THBS1 as a potential biomarker for identifying mesenchymal CRC and as a critical suppressor of antitumor immunity that contributes to the progression of this malignancy with a poor prognosis.
Abstract Mesenchymal activation, characterized by dense stromal infiltration of immune and mesenchymal cells, fuels the aggressiveness of colorectal cancers (CRC), driving progression and metastasis. Targetable molecules in the tumor microenvironment (TME) need to be identified to improve the outcome in CRC patients with this aggressive phenotype. This study reports a positive link between high thrombospondin-1 (THBS1) expression and mesenchymal characteristics, immunosuppression, and unfavorable CRC prognosis. Bone marrow-derived monocyte-like cells recruited by CXCL12 are the primary source of THBS1, which contributes to the development of metastasis by inducing cytotoxic T-cell exhaustion and impairing vascularization. Furthermore, in orthotopically generated CRC models in male mice, THBS1 loss in the TME renders tumors partially sensitive to immune checkpoint inhibitors and anti-cancer drugs. Our study establishes THBS1 as a potential biomarker for identifying mesenchymal CRC and as a critical suppressor of antitumor immunity that contributes to the progression of this malignancy with a poor prognosis.
Mesenchymal activation, characterized by dense stromal infiltration of immune and mesenchymal cells, fuels the aggressiveness of colorectal cancers (CRC), driving progression and metastasis. Targetable molecules in the tumor microenvironment (TME) need to be identified to improve the outcome in CRC patients with this aggressive phenotype. This study reports a positive link between high thrombospondin-1 (THBS1) expression and mesenchymal characteristics, immunosuppression, and unfavorable CRC prognosis. Bone marrow-derived monocyte-like cells recruited by CXCL12 are the primary source of THBS1, which contributes to the development of metastasis by inducing cytotoxic T-cell exhaustion and impairing vascularization. Furthermore, in orthotopically generated CRC models in male mice, THBS1 loss in the TME renders tumors partially sensitive to immune checkpoint inhibitors and anti-cancer drugs. Our study establishes THBS1 as a potential biomarker for identifying mesenchymal CRC and as a critical suppressor of antitumor immunity that contributes to the progression of this malignancy with a poor prognosis. Thrombospondin-1 (THBS1) is a matricellular protein highly expressed in inflammatory processes, including cancer. Here the authors show that bone-marrow derived monocyte-like cells are the primary source of THBS1 in colorectal cancer, associated with mesenchymal characteristics, immunosuppression and a poor prognosis.
Mesenchymal activation, characterized by dense stromal infiltration of immune and mesenchymal cells, fuels the aggressiveness of colorectal cancers (CRC), driving progression and metastasis. Targetable molecules in the tumor microenvironment (TME) need to be identified to improve the outcome in CRC patients with this aggressive phenotype. This study reports a positive link between high thrombospondin-1 (THBS1) expression and mesenchymal characteristics, immunosuppression, and unfavorable CRC prognosis. Bone marrow-derived monocyte-like cells recruited by CXCL12 are the primary source of THBS1, which contributes to the development of metastasis by inducing cytotoxic T-cell exhaustion and impairing vascularization. Furthermore, in orthotopically generated CRC models in male mice, THBS1 loss in the TME renders tumors partially sensitive to immune checkpoint inhibitors and anti-cancer drugs. Our study establishes THBS1 as a potential biomarker for identifying mesenchymal CRC and as a critical suppressor of antitumor immunity that contributes to the progression of this malignancy with a poor prognosis.
Mesenchymal activation, characterized by dense stromal infiltration of immune and mesenchymal cells, fuels the aggressiveness of colorectal cancers (CRC), driving progression and metastasis. Targetable molecules in the tumor microenvironment (TME) need to be identified to improve the outcome in CRC patients with this aggressive phenotype. This study reports a positive link between high thrombospondin-1 (THBS1) expression and mesenchymal characteristics, immunosuppression, and unfavorable CRC prognosis. Bone marrow-derived monocyte-like cells recruited by CXCL12 are the primary source of THBS1, which contributes to the development of metastasis by inducing cytotoxic T-cell exhaustion and impairing vascularization. Furthermore, in orthotopically generated CRC models in male mice, THBS1 loss in the TME renders tumors partially sensitive to immune checkpoint inhibitors and anti-cancer drugs. Our study establishes THBS1 as a potential biomarker for identifying mesenchymal CRC and as a critical suppressor of antitumor immunity that contributes to the progression of this malignancy with a poor prognosis. Thrombospondin-1 (THBS1) is a matricellular protein highly expressed in inflammatory processes, including cancer. Here the authors show that bone-marrow derived monocyte-like cells are the primary source of THBS1 in colorectal cancer, associated with mesenchymal characteristics, immunosuppression and a poor prognosis.
ArticleNumber 5534
Author Fukunaga, Yuichi
Kawada, Kenji
Saito, Yasuyuki
Fukuda, Akihisa
Ogawa, Seishi
Duran, Angeles
Han, Qixiu
Maruno, Takahisa
Tsuda, Motoyuki
Obama, Kazutaka
Moscat, Jorge
Iwane, Kosuke
Mizukoshi, Kenta
Omatsu, Mayuki
Kakiuchi, Nobuyuki
Kabashima, Kenji
Nakanishi, Yuki
Nagao, Munemasa
Martinez-Ordoñez, Anxo
Sono, Makoto
Ogawa, Satoshi
Sheibani, Nader
Nakagawa, Masahiro M.
Diaz-Meco, Maria T.
Yoshikawa, Takaaki
Kasashima, Hiroaki
Yamakawa, Go
Utsumi, Takahiro
Hamada, Kensuke
Aoyama, Naoki
Seno, Hiroshi
Hiramatsu, Yukiko
Muta, Yu
Agatsuma, Nobukazu
Hata, Akitaka
Masuda, Tomonori
Kogame, Toshiaki
Kawai, Munenori
Araki, Osamu
Yashiro, Masakazu
Namikawa, Mio
Maeda, Kiyoshi
Matozaki, Takashi
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/37749092$$D View this record in MEDLINE/PubMed
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Snippet Mesenchymal activation, characterized by dense stromal infiltration of immune and mesenchymal cells, fuels the aggressiveness of colorectal cancers (CRC),...
Abstract Mesenchymal activation, characterized by dense stromal infiltration of immune and mesenchymal cells, fuels the aggressiveness of colorectal cancers...
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multidisciplinary
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Title THBS1-producing tumor-infiltrating monocyte-like cells contribute to immunosuppression and metastasis in colorectal cancer
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