Secretory GFP reconstitution labeling of neighboring cells interrogates cell–cell interactions in metastatic niches

Misa Minegishi, Takahiro Kuchimaru (), Kaori Nishikawa, Takayuki Isagawa, Satoshi Iwano, Kei Iida, Hiromasa Hara, Shizuka Miura, Marika Sato, Shigeaki Watanabe, Akifumi Shiomi, Yo Mabuchi, Hiroshi Hamana, Hiroyuki Kishi, Tatsuyuki Sato, Daigo Sawaki, Shigeru Sato, Yutaka Hanazono, Atsushi Suzuki, Takahide Kohro, Tetsuya Kadonosono, Tomomi Shimogori, Atsushi Miyawaki, Norihiko Takeda, Hirofumi Shintaku (), Shinae Kizaka-Kondoh and Satoshi Nishimura
Additional contact information
Misa Minegishi: Tokyo Institute of Technology
Takahiro Kuchimaru: RIKEN Cluster for Pioneering Research
Kaori Nishikawa: RIKEN Cluster for Pioneering Research
Takayuki Isagawa: Jichi Medical University
Satoshi Iwano: RIKEN Center for Brain Science
Kei Iida: Kindai University
Hiromasa Hara: Jichi Medical University
Shizuka Miura: Kyushu University
Marika Sato: MediGear International Corporation
Shigeaki Watanabe: MediGear International Corporation
Akifumi Shiomi: RIKEN Cluster for Pioneering Research
Yo Mabuchi: Juntendo University
Hiroshi Hamana: University of Toyama
Hiroyuki Kishi: University of Toyama
Tatsuyuki Sato: Jichi Medical University
Daigo Sawaki: Jichi Medical University
Shigeru Sato: Jichi Medical University
Yutaka Hanazono: Jichi Medical University
Atsushi Suzuki: Kyushu University
Takahide Kohro: Jichi Medical University
Tetsuya Kadonosono: Tokyo Institute of Technology
Tomomi Shimogori: RIKEN Center for Brain Science
Atsushi Miyawaki: RIKEN Center for Brain Science
Norihiko Takeda: Jichi Medical University
Hirofumi Shintaku: RIKEN Cluster for Pioneering Research
Shinae Kizaka-Kondoh: Tokyo Institute of Technology
Satoshi Nishimura: Jichi Medical University

Nature Communications, 2023, vol. 14, issue 1, 1-12

Abstract: Abstract Cancer cells inevitably interact with neighboring host tissue-resident cells during the process of metastatic colonization, establishing a metastatic niche to fuel their survival, growth, and invasion. However, the underlying mechanisms in the metastatic niche are yet to be fully elucidated owing to the lack of methodologies for comprehensively studying the mechanisms of cell–cell interactions in the niche. Here, we improve a split green fluorescent protein (GFP)-based genetically encoded system to develop secretory glycosylphosphatidylinositol-anchored reconstitution-activated proteins to highlight intercellular connections (sGRAPHIC) for efficient fluorescent labeling of tissue-resident cells that neighbor on and putatively interact with cancer cells in deep tissues. The sGRAPHIC system enables the isolation of metastatic niche-associated tissue-resident cells for their characterization using a single-cell RNA sequencing platform. We use this sGRAPHIC-leveraged transcriptomic platform to uncover gene expression patterns in metastatic niche-associated hepatocytes in a murine model of liver metastasis. Among the marker genes of metastatic niche-associated hepatocytes, we identify Lgals3, encoding galectin-3, as a potential pro-metastatic factor that accelerates metastatic growth and invasion.

Date: 2023
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DOI: 10.1038/s41467-023-43855-2

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