Symbiotic polyamine metabolism regulates epithelial proliferation and macrophage differentiation in the colon

Atsuo Nakamura, Shin Kurihara, Daisuke Takahashi, Wakana Ohashi, Yutaka Nakamura, Shunsuke Kimura, Masayoshi Onuki, Aiko Kume, Yukiko Sasazawa, Yukihiro Furusawa, Yuuki Obata, Shinji Fukuda, Shinji Saiki, Mitsuharu Matsumoto () and Koji Hase ()
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Atsuo Nakamura: Keio University, Minato-ku
Shin Kurihara: Ishikawa Prefectural University
Daisuke Takahashi: Keio University, Minato-ku
Wakana Ohashi: Keio University, Minato-ku
Yutaka Nakamura: Keio University, Minato-ku
Shunsuke Kimura: Keio University, Minato-ku
Masayoshi Onuki: Keio University, Minato-ku
Aiko Kume: Kyodo Milk Industry Co., Ltd., Hinode-machi, Nishitama-gun
Yukiko Sasazawa: Juntendo University, Bunkyo-ku
Yukihiro Furusawa: Keio University, Minato-ku
Yuuki Obata: Keio University, Minato-ku
Shinji Fukuda: PRESTO, Japan Science and Technology Agency
Shinji Saiki: Juntendo University, Bunkyo-ku
Mitsuharu Matsumoto: Kyodo Milk Industry Co., Ltd., Hinode-machi, Nishitama-gun
Koji Hase: Keio University, Minato-ku

Nature Communications, 2021, vol. 12, issue 1, 1-14

Abstract: Abstract Intestinal microbiota-derived metabolites have biological importance for the host. Polyamines, such as putrescine and spermidine, are produced by the intestinal microbiota and regulate multiple biological processes. Increased colonic luminal polyamines promote longevity in mice. However, no direct evidence has shown that microbial polyamines are incorporated into host cells to regulate cellular responses. Here, we show that microbial polyamines reinforce colonic epithelial proliferation and regulate macrophage differentiation. Colonisation by wild-type, but not polyamine biosynthesis-deficient, Escherichia coli in germ-free mice raises intracellular polyamine levels in colonocytes, accelerating epithelial renewal. Commensal bacterium-derived putrescine increases the abundance of anti-inflammatory macrophages in the colon. The bacterial polyamines ameliorate symptoms of dextran sulfate sodium-induced colitis in mice. These effects mainly result from enhanced hypusination of eukaryotic initiation translation factor. We conclude that bacterial putrescine functions as a substrate for symbiotic metabolism and is further absorbed and metabolised by the host, thus helping maintain mucosal homoeostasis in the intestine.

Date: 2021
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DOI: 10.1038/s41467-021-22212-1

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