Extrinsic induction of apoptosis and tumor suppression via the p53–Reprimo–Hippo–YAP/TAZ–p73 pathway

M Masahiro Takikawa (Laboratory of Fundamental Oncology, National Cancer Center Research Institute) A Airi Nakano (Laboratory of Fundamental Oncology, National Cancer Center Research Institute) J Jayaraman Krishnaraj (Laboratory of Fundamental Oncology, National Cancer Center Research Institute) Y Yuko Tabata (Laboratory of Fundamental Oncology, National Cancer Center Research Institute) Y Yuzo Watanabe (Proteomics Facility, Graduate School of Biostudies, Kyoto University) A Atsushi Okabe (Department of Molecular Oncology, Graduate School of Medicine, Chiba University) Y Yukiko Sakaguchi (Laboratory of Fundamental Oncology, National Cancer Center Research Institute) R Ryoji Fujiki A Ami Mochizuki (Laboratory of Fundamental Oncology, National Cancer Center Research Institute) T Tomoko Tajima (Laboratory of Fundamental Oncology, National Cancer Center Research Institute) A Akane Sada (Laboratory of Fundamental Oncology, National Cancer Center Research Institute) S Shu Matsushita (Laboratory of Fundamental Oncology, National Cancer Center Research Institute) Y Yuichi Wakabayashi (Cancer Genome Center, Division of Experimental Animal Research, Chiba Cancer Center Research Institute) K Kimi Araki (Division of Developmental Genetics, Institute of Resource Development and Analysis, Kumamoto University) A Atsushi Kaneda F Fuyuki Ishikawa (Department of Gene Mechanisms, Graduate School of Biostudies, Kyoto University) M Mahito Sadaie (Department of Applied Biological Science, Faculty of Science and Technology, Tokyo University of Science) R Rieko Ohki (Laboratory of Fundamental Oncology, National Cancer Center Research Institute)

Abstract

Tumor progression is suppressed by inherent cellular mechanisms such as apoptosis. The p53 tumor suppressor gene is the most commonly mutated gene in human cancer and plays a pivotal role in tumor suppression. RPRM is a target gene of p53 known to be involved in tumor suppression, but its molecular function has remained elusive. Here, we report that Reprimo (the protein product of RPRM ) is secreted and extrinsically induces apoptosis in recipient cells. We identified FAT1, FAT4, CELSR1, CELSR2, and CELSR3, members of the protocadherin family, as receptors for Reprimo. Subsequent analyses revealed that Reprimo acts upstream of the Hippo–YAP/TAZ–p73 axis and induces apoptosis by transactivating various proapoptotic genes. In vivo analyses further support the tumor-suppressive effects of secreted Reprimo. These findings identify the p53–Reprimo–Hippo–YAP/TAZ–p73 axis as an extrinsic apoptosis pathway that plays a crucial role in tumor suppression. Our finding of the innate tumor eliminator Reprimo and the downstream pathway offers a promising avenue for the pharmacological treatment of cancer.

Article Details

Volume / Issue Vol. 122, Issue 6
Published February 11, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (18)

M

Masahiro Takikawa

Laboratory of Fundamental Oncology, National Cancer Center Research Institute

A

Airi Nakano

Laboratory of Fundamental Oncology, National Cancer Center Research Institute

J

Jayaraman Krishnaraj

Laboratory of Fundamental Oncology, National Cancer Center Research Institute

Y

Yuko Tabata

Laboratory of Fundamental Oncology, National Cancer Center Research Institute

Y

Yuzo Watanabe

Proteomics Facility, Graduate School of Biostudies, Kyoto University

A

Atsushi Okabe

Department of Molecular Oncology, Graduate School of Medicine, Chiba University

Y

Yukiko Sakaguchi

Laboratory of Fundamental Oncology, National Cancer Center Research Institute

R

Ryoji Fujiki

A

Ami Mochizuki

Laboratory of Fundamental Oncology, National Cancer Center Research Institute

T

Tomoko Tajima

Laboratory of Fundamental Oncology, National Cancer Center Research Institute

A

Akane Sada

Laboratory of Fundamental Oncology, National Cancer Center Research Institute

S

Shu Matsushita

Laboratory of Fundamental Oncology, National Cancer Center Research Institute

Y

Yuichi Wakabayashi

Cancer Genome Center, Division of Experimental Animal Research, Chiba Cancer Center Research Institute

K

Kimi Araki

Division of Developmental Genetics, Institute of Resource Development and Analysis, Kumamoto University

A

Atsushi Kaneda

F

Fuyuki Ishikawa

Department of Gene Mechanisms, Graduate School of Biostudies, Kyoto University

M

Mahito Sadaie

Department of Applied Biological Science, Faculty of Science and Technology, Tokyo University of Science

R

Rieko Ohki

Laboratory of Fundamental Oncology, National Cancer Center Research Institute