Cell Reports (Jan 2023)
Spatial and single-cell transcriptomics decipher the cellular environment containing HLA-G+ cancer cells and SPP1+ macrophages in colorectal cancer
- Yuki Ozato,
- Yasuhiro Kojima,
- Yuta Kobayashi,
- Yuuichi Hisamatsu,
- Takeo Toshima,
- Yusuke Yonemura,
- Takaaki Masuda,
- Kouichi Kagawa,
- Yasuhiro Goto,
- Mitsuaki Utou,
- Mituko Fukunaga,
- Ayako Gamachi,
- Kiyomi Imamura,
- Yuta Kuze,
- Junko Zenkoh,
- Ayako Suzuki,
- Atsushi Niida,
- Haruka Hirose,
- Shuto Hayashi,
- Jun Koseki,
- Eiji Oki,
- Satoshi Fukuchi,
- Kazunari Murakami,
- Taro Tobo,
- Satoshi Nagayama,
- Mamoru Uemura,
- Takeharu Sakamoto,
- Masanobu Oshima,
- Yuichiro Doki,
- Hidetoshi Eguchi,
- Masaki Mori,
- Takeshi Iwasaki,
- Yoshinao Oda,
- Tatsuhiro Shibata,
- Yutaka Suzuki,
- Teppei Shimamura,
- Koshi Mimori
Affiliations
- Yuki Ozato
- Department of Surgery, Kyushu University Beppu Hospital, Beppu 874-0838, Japan; Department of Gastroenterological Surgery, Osaka University Graduate School of Medicine, Suita 565-0871, Japan
- Yasuhiro Kojima
- Division of Systems Biology, Nagoya University Graduate School of Medicine, Nagoya 466-8550, Japan
- Yuta Kobayashi
- Department of Surgery, Kyushu University Beppu Hospital, Beppu 874-0838, Japan; Department of Gastroenterological Surgery, Osaka University Graduate School of Medicine, Suita 565-0871, Japan
- Yuuichi Hisamatsu
- Department of Surgery, Kyushu University Beppu Hospital, Beppu 874-0838, Japan
- Takeo Toshima
- Department of Surgery, Kyushu University Beppu Hospital, Beppu 874-0838, Japan
- Yusuke Yonemura
- Department of Surgery, Kyushu University Beppu Hospital, Beppu 874-0838, Japan
- Takaaki Masuda
- Department of Surgery, Kyushu University Beppu Hospital, Beppu 874-0838, Japan
- Kouichi Kagawa
- Department of Gastroenterology, Shinbeppu Hospital, Beppu 874-8538, Japan
- Yasuhiro Goto
- Department of Gastroenterology, Shinbeppu Hospital, Beppu 874-8538, Japan
- Mitsuaki Utou
- Department of Pathology, Kyushu University Beppu Hospital, Beppu 874-0838, Japan
- Mituko Fukunaga
- Department of Surgery, Kyushu University Beppu Hospital, Beppu 874-0838, Japan
- Ayako Gamachi
- Department of Pathology, Almeida Memorial Hospital, Oita 870-1195, Japan
- Kiyomi Imamura
- Laboratory of Systems Genomics, Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, the University of Tokyo, Kashiwa 277-8561, Japan
- Yuta Kuze
- Laboratory of Systems Genomics, Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, the University of Tokyo, Kashiwa 277-8561, Japan
- Junko Zenkoh
- Laboratory of Systems Genomics, Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, the University of Tokyo, Kashiwa 277-8561, Japan
- Ayako Suzuki
- Laboratory of Systems Genomics, Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, the University of Tokyo, Kashiwa 277-8561, Japan
- Atsushi Niida
- Laboratory of Molecular Medicine, the Institute of Medical Science, the University of Tokyo, Tokyo 108-8639, Japan
- Haruka Hirose
- Division of Systems Biology, Nagoya University Graduate School of Medicine, Nagoya 466-8550, Japan
- Shuto Hayashi
- Division of Systems Biology, Nagoya University Graduate School of Medicine, Nagoya 466-8550, Japan
- Jun Koseki
- Division of Systems Biology, Nagoya University Graduate School of Medicine, Nagoya 466-8550, Japan
- Eiji Oki
- Department of Surgery and Science, Graduate School of Medical Science, Kyushu University, Fukuoka 812-8582, Japan
- Satoshi Fukuchi
- Department of Gastroenterological Medicine, Almeida Memorial Hospital, Oita 870-1195, Japan
- Kazunari Murakami
- Department of Gastroenterology, Oita University Hospital, Yufu 879-5593, Japan
- Taro Tobo
- Department of Pathology, Almeida Memorial Hospital, Oita 870-1195, Japan
- Satoshi Nagayama
- Gastroenterological Center, Department of Gastroenterological Surgery, Cancer Institute Hospital, Japanese Foundation for Cancer Research, Tokyo 135-8550, Japan
- Mamoru Uemura
- Department of Gastroenterological Surgery, Osaka University Graduate School of Medicine, Suita 565-0871, Japan
- Takeharu Sakamoto
- Department of Cancer Biology, Institute of Biomedical Science, Kansai Medical University, Hirakata 573-1010, Japan
- Masanobu Oshima
- Division of Genetics, Cancer Research Institute, Kanazawa University, Kanazawa 920-1192, Japan
- Yuichiro Doki
- Department of Gastroenterological Surgery, Osaka University Graduate School of Medicine, Suita 565-0871, Japan
- Hidetoshi Eguchi
- Department of Gastroenterological Surgery, Osaka University Graduate School of Medicine, Suita 565-0871, Japan
- Masaki Mori
- Tokai University School of Medicine, Isehara 259-1193, Japan
- Takeshi Iwasaki
- Department of Pathology, Kyushu University Hospital, Fukuoka 812-8582, Japan
- Yoshinao Oda
- Department of Pathology, Kyushu University Hospital, Fukuoka 812-8582, Japan
- Tatsuhiro Shibata
- Laboratory of Molecular Medicine, the Institute of Medical Science, the University of Tokyo, Tokyo 108-8639, Japan
- Yutaka Suzuki
- Laboratory of Systems Genomics, Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, the University of Tokyo, Kashiwa 277-8561, Japan
- Teppei Shimamura
- Division of Systems Biology, Nagoya University Graduate School of Medicine, Nagoya 466-8550, Japan; Corresponding author
- Koshi Mimori
- Department of Surgery, Kyushu University Beppu Hospital, Beppu 874-0838, Japan; Corresponding author
- Journal volume & issue
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Vol. 42,
no. 1
p. 111929
Abstract
Summary: The cellular interactions in the tumor microenvironment of colorectal cancer (CRC) are poorly understood, hindering patient treatment. In the current study, we investigate whether events occurring at the invasion front are of particular importance for CRC treatment strategies. To this end, we analyze CRC tissues by combining spatial transcriptomics from patients with a public single-cell transcriptomic atlas to determine cell-cell interactions at the invasion front. We show that CRC cells are localized specifically at the invasion front. These cells induce human leukocyte antigen G (HLA-G) to produce secreted phosphoprotein 1 (SPP1)+ macrophages while conferring CRC cells with anti-tumor immunity, as well as proliferative and invasive properties. Taken together, these findings highlight the signaling between CRC cell populations and stromal cell populations at the cellular level.
