Bidirectional crosstalk between neutrophils and adipocytes promotes adipose tissue inflammation

Yasuharu Watanabe, Yoshinori Nagai, Hiroe Honda, Naoki Okamoto, Tsutomu Yanagibashi, Masaru Ogasawara, Seiji Yamamoto, Ryu Imamura, Ichiro Takasaki, Hiromitsu Hara, Masakiyo Sasahara, Makoto Arita, Shigeaki Hida, Shun'ichiro Taniguchi, Takashi Suda, Kiyoshi Takatsu

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Chronic activation of the IL-1β system in adipose tissue on metabolic disorders is well demonstrated. However, a mechanism for its expression and activation in the tissue has remained unexplored. Here, we demonstrate that IL-1β transcript was enriched in neutrophils of white adipose tissue (WAT) from lean mice. Mechanistically, the interaction of neutrophils with adipocytes induced IL-1β expression via NF-κB pathway. Lipolysis of adipocytes accumulated neutrophils prior to macrophages in WAT and produced high levels of IL-1β via an inflammasome pathway. Leukotriene B4 (LTB4) production in WAT also contributed to neutrophil accumulation. Furthermore, an LTB4-inflammasome axis contributed to the expression of chemotactic molecules involved in high-fat diet-induced macrophage infiltration into WAT. We have identified previously unappreciated roles for neutrophils in the development of adipose tissue inflammation: robust IL-1β production and infiltration of macrophages to initiate chronic inflammation.-Watanabe, Y., Nagai, Y., Honda, H., Okamoto, N., Yanagibashi, T., Ogasawara, M., Yamamoto, S., Imamura, R., Takasaki, I., Hara, H., Sasahara, M., Arita, M., Hida, S., Taniguchi, S., Suda, T., Takatsu, K. Bidirectional crosstalk between neutrophils and adipocytes promotes adipose tissue inflammation.

Original languageEnglish
Pages (from-to)11821-11835
Number of pages15
JournalFASEB journal : official publication of the Federation of American Societies for Experimental Biology
Volume33
Issue number11
DOIs
Publication statusPublished - 2019 Nov 1

Fingerprint

Crosstalk
Adipocytes
Adipose Tissue
White Adipose Tissue
Interleukin-1
Neutrophils
Tissue
Inflammation
Inflammasomes
Macrophages
Leukotriene B4
Infiltration
Lipolysis
Chemical activation
High Fat Diet
Nutrition
Fats
Molecules

Keywords

  • fatty acid
  • IL-1β inflammasome
  • metabolic disorder

ASJC Scopus subject areas

  • Biotechnology
  • Biochemistry
  • Molecular Biology
  • Genetics

Cite this

Bidirectional crosstalk between neutrophils and adipocytes promotes adipose tissue inflammation. / Watanabe, Yasuharu; Nagai, Yoshinori; Honda, Hiroe; Okamoto, Naoki; Yanagibashi, Tsutomu; Ogasawara, Masaru; Yamamoto, Seiji; Imamura, Ryu; Takasaki, Ichiro; Hara, Hiromitsu; Sasahara, Masakiyo; Arita, Makoto; Hida, Shigeaki; Taniguchi, Shun'ichiro; Suda, Takashi; Takatsu, Kiyoshi.

In: FASEB journal : official publication of the Federation of American Societies for Experimental Biology, Vol. 33, No. 11, 01.11.2019, p. 11821-11835.

Research output: Contribution to journalArticle

Watanabe, Y, Nagai, Y, Honda, H, Okamoto, N, Yanagibashi, T, Ogasawara, M, Yamamoto, S, Imamura, R, Takasaki, I, Hara, H, Sasahara, M, Arita, M, Hida, S, Taniguchi, S, Suda, T & Takatsu, K 2019, 'Bidirectional crosstalk between neutrophils and adipocytes promotes adipose tissue inflammation', FASEB journal : official publication of the Federation of American Societies for Experimental Biology, vol. 33, no. 11, pp. 11821-11835. https://doi.org/10.1096/fj.201900477RR
Watanabe, Yasuharu ; Nagai, Yoshinori ; Honda, Hiroe ; Okamoto, Naoki ; Yanagibashi, Tsutomu ; Ogasawara, Masaru ; Yamamoto, Seiji ; Imamura, Ryu ; Takasaki, Ichiro ; Hara, Hiromitsu ; Sasahara, Masakiyo ; Arita, Makoto ; Hida, Shigeaki ; Taniguchi, Shun'ichiro ; Suda, Takashi ; Takatsu, Kiyoshi. / Bidirectional crosstalk between neutrophils and adipocytes promotes adipose tissue inflammation. In: FASEB journal : official publication of the Federation of American Societies for Experimental Biology. 2019 ; Vol. 33, No. 11. pp. 11821-11835.
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AU - Ogasawara, Masaru

AU - Yamamoto, Seiji

AU - Imamura, Ryu

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AU - Hara, Hiromitsu

AU - Sasahara, Masakiyo

AU - Arita, Makoto

AU - Hida, Shigeaki

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AU - Suda, Takashi

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N2 - Chronic activation of the IL-1β system in adipose tissue on metabolic disorders is well demonstrated. However, a mechanism for its expression and activation in the tissue has remained unexplored. Here, we demonstrate that IL-1β transcript was enriched in neutrophils of white adipose tissue (WAT) from lean mice. Mechanistically, the interaction of neutrophils with adipocytes induced IL-1β expression via NF-κB pathway. Lipolysis of adipocytes accumulated neutrophils prior to macrophages in WAT and produced high levels of IL-1β via an inflammasome pathway. Leukotriene B4 (LTB4) production in WAT also contributed to neutrophil accumulation. Furthermore, an LTB4-inflammasome axis contributed to the expression of chemotactic molecules involved in high-fat diet-induced macrophage infiltration into WAT. We have identified previously unappreciated roles for neutrophils in the development of adipose tissue inflammation: robust IL-1β production and infiltration of macrophages to initiate chronic inflammation.-Watanabe, Y., Nagai, Y., Honda, H., Okamoto, N., Yanagibashi, T., Ogasawara, M., Yamamoto, S., Imamura, R., Takasaki, I., Hara, H., Sasahara, M., Arita, M., Hida, S., Taniguchi, S., Suda, T., Takatsu, K. Bidirectional crosstalk between neutrophils and adipocytes promotes adipose tissue inflammation.

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