TY - JOUR
T1 - Macrophages rely on extracellular serine to suppress aberrant cytokine production
AU - Kurita, Kento
AU - Ohta, Hiroya
AU - Shirakawa, Ibuki
AU - Tanaka, Miyako
AU - Kitaura, Yasuyuki
AU - Iwasaki, Yorihiro
AU - Matsuzaka, Takashi
AU - Shimano, Hitoshi
AU - Aoe, Seiichiro
AU - Arima, Hiroshi
AU - Ogawa, Yoshihiro
AU - Ito, Ayaka
AU - Suganami, Takayoshi
N1 - Funding Information:
We thank Dr. Norihiko Takeda (Jichi Medical University) and the members of the Suganami laboratory for their helpful discussions, and Center for Animal Research and Education (CARE), Nagoya University for support on animal experiments. This work was supported in part by Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (20H03447, 20H05503, and 20H04944 to T.S., 19K11765 and 19KK0249 to A.I.) and Japan Agency for Medical Research and Development (CREST) (20gm1210009s0102 to T.S.). This study was also supported by research grants from Smoking Research Foundation (T.S.), Astellas Foundation for Research on Metabolic Disorders, Kowa Life Science Foundation (A.I.), The Hori Sciences and Arts Foundation, and Takeda Science Foundation (T.S., A.I.).
Publisher Copyright:
© 2021, The Author(s).
PY - 2021/12
Y1 - 2021/12
N2 - A growing body of evidence indicates that cellular metabolism is involved in immune cell functions, including cytokine production. Serine is a nutritionally non-essential amino acid that can be generated by de novo synthesis and conversion from glycine. Serine contributes to various cellular responses, but the role in inflammatory responses remains poorly understood. Here, we show that macrophages rely on extracellular serine to suppress aberrant cytokine production. Depleting serine from the culture media reduced the cellular serine content in macrophages markedly, suggesting that macrophages depend largely on extracellular serine rather than cellular synthesis. Under serine deprivation, macrophages stimulated with lipopolysaccharide showed aberrant cytokine expression patterns, including a marked reduction of anti-inflammatory interleukin-10 expression and sustained expression of interleukine-6. Transcriptomic and metabolomics analyses revealed that serine deprivation causes mitochondrial dysfunction: reduction in the pyruvate content, the NADH/NAD+ ratio, the oxygen consumption rate, and the mitochondrial production of reactive oxygen species (ROS). We also found the role of mitochondrial ROS in appropriate cytokine production. Thus, our results indicate that cytokine production in macrophages is tightly regulated by the nutritional microenvironment.
AB - A growing body of evidence indicates that cellular metabolism is involved in immune cell functions, including cytokine production. Serine is a nutritionally non-essential amino acid that can be generated by de novo synthesis and conversion from glycine. Serine contributes to various cellular responses, but the role in inflammatory responses remains poorly understood. Here, we show that macrophages rely on extracellular serine to suppress aberrant cytokine production. Depleting serine from the culture media reduced the cellular serine content in macrophages markedly, suggesting that macrophages depend largely on extracellular serine rather than cellular synthesis. Under serine deprivation, macrophages stimulated with lipopolysaccharide showed aberrant cytokine expression patterns, including a marked reduction of anti-inflammatory interleukin-10 expression and sustained expression of interleukine-6. Transcriptomic and metabolomics analyses revealed that serine deprivation causes mitochondrial dysfunction: reduction in the pyruvate content, the NADH/NAD+ ratio, the oxygen consumption rate, and the mitochondrial production of reactive oxygen species (ROS). We also found the role of mitochondrial ROS in appropriate cytokine production. Thus, our results indicate that cytokine production in macrophages is tightly regulated by the nutritional microenvironment.
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U2 - 10.1038/s41598-021-90086-w
DO - 10.1038/s41598-021-90086-w
M3 - Article
C2 - 34045514
AN - SCOPUS:85106891368
SN - 2045-2322
VL - 11
JO - Scientific reports
JF - Scientific reports
IS - 1
M1 - 11137
ER -