Mast cell maturation is driven via a group III phospholipase A 2-prostaglandin D2-DP1 receptor paracrine axis

Yoshitaka Taketomi, Noriko Ueno, Takumi Kojima, Hiroyasu Sato, Remi Murase, Kei Yamamoto, Satoshi Tanaka, Mariko Sakanaka, Masanori Nakamura, Yasumasa Nishito, Momoko Kawana, Naotomo Kambe, Kazutaka Ikeda, Ryo Taguchi, Satoshi Nakamizo, Kenji Kabashima, Michael H. Gelb, Makoto Arita, Takehiko Yokomizo, Motonao NakamuraKikuko Watanabe, Hiroyuki Hirai, Masataka Nakamura, Yoshimichi Okayama, Chisei Ra, Kosuke Aritake, Yoshihiro Urade, Kazushi Morimoto, Yukihiko Sugimoto, Takao Shimizu, Shuh Narumiya, Shuntaro Hara, Makoto Murakami

Research output: Contribution to journalArticle

70 Citations (Scopus)

Abstract

Microenvironment-based alterations in phenotypes of mast cells influence the susceptibility to anaphylaxis, yet the mechanisms underlying proper maturation of mast cells toward an anaphylaxis-sensitive phenotype are incompletely understood. Here we report that PLA2G3, a mammalian homolog of anaphylactic bee venom phospholipase A2, regulates this process. PLA2G3 secreted from mast cells is coupled with fibroblastic lipocalin-type PGD2 synthase (L-PGDS) to provide PGD2, which facilitates mast-cell maturation via PGD2 receptor DP1. Mice lacking PLA2G3, L-PGDS or DP1, mast cell-deficient mice reconstituted with PLA2G3-null or DP1-null mast cells, or mast cells cultured with L-PGDS-ablated fibroblasts exhibited impaired maturation and anaphylaxis of mast cells. Thus, we describe a lipid-driven PLA2G3-L-PGDS-DP1 loop that drives mast cell maturation.

Original languageEnglish
Pages (from-to)554-563
Number of pages10
JournalNature Immunology
Volume14
Issue number6
DOIs
Publication statusPublished - Jun 2013

Fingerprint

Phospholipases A
Mast Cells
prostaglandin R2 D-isomerase
Lipocalins
Anaphylaxis
Bee Venoms
Phenotype
prostaglandin D2 receptor
Prostaglandin D2
Null Lymphocytes
Phospholipases A2
Fibroblasts
Lipids

ASJC Scopus subject areas

  • Immunology

Cite this

Taketomi, Y., Ueno, N., Kojima, T., Sato, H., Murase, R., Yamamoto, K., ... Murakami, M. (2013). Mast cell maturation is driven via a group III phospholipase A 2-prostaglandin D2-DP1 receptor paracrine axis. Nature Immunology, 14(6), 554-563. https://doi.org/10.1038/ni.2586

Mast cell maturation is driven via a group III phospholipase A 2-prostaglandin D2-DP1 receptor paracrine axis. / Taketomi, Yoshitaka; Ueno, Noriko; Kojima, Takumi; Sato, Hiroyasu; Murase, Remi; Yamamoto, Kei; Tanaka, Satoshi; Sakanaka, Mariko; Nakamura, Masanori; Nishito, Yasumasa; Kawana, Momoko; Kambe, Naotomo; Ikeda, Kazutaka; Taguchi, Ryo; Nakamizo, Satoshi; Kabashima, Kenji; Gelb, Michael H.; Arita, Makoto; Yokomizo, Takehiko; Nakamura, Motonao; Watanabe, Kikuko; Hirai, Hiroyuki; Nakamura, Masataka; Okayama, Yoshimichi; Ra, Chisei; Aritake, Kosuke; Urade, Yoshihiro; Morimoto, Kazushi; Sugimoto, Yukihiko; Shimizu, Takao; Narumiya, Shuh; Hara, Shuntaro; Murakami, Makoto.

In: Nature Immunology, Vol. 14, No. 6, 06.2013, p. 554-563.

Research output: Contribution to journalArticle

Taketomi, Y, Ueno, N, Kojima, T, Sato, H, Murase, R, Yamamoto, K, Tanaka, S, Sakanaka, M, Nakamura, M, Nishito, Y, Kawana, M, Kambe, N, Ikeda, K, Taguchi, R, Nakamizo, S, Kabashima, K, Gelb, MH, Arita, M, Yokomizo, T, Nakamura, M, Watanabe, K, Hirai, H, Nakamura, M, Okayama, Y, Ra, C, Aritake, K, Urade, Y, Morimoto, K, Sugimoto, Y, Shimizu, T, Narumiya, S, Hara, S & Murakami, M 2013, 'Mast cell maturation is driven via a group III phospholipase A 2-prostaglandin D2-DP1 receptor paracrine axis', Nature Immunology, vol. 14, no. 6, pp. 554-563. https://doi.org/10.1038/ni.2586
Taketomi, Yoshitaka ; Ueno, Noriko ; Kojima, Takumi ; Sato, Hiroyasu ; Murase, Remi ; Yamamoto, Kei ; Tanaka, Satoshi ; Sakanaka, Mariko ; Nakamura, Masanori ; Nishito, Yasumasa ; Kawana, Momoko ; Kambe, Naotomo ; Ikeda, Kazutaka ; Taguchi, Ryo ; Nakamizo, Satoshi ; Kabashima, Kenji ; Gelb, Michael H. ; Arita, Makoto ; Yokomizo, Takehiko ; Nakamura, Motonao ; Watanabe, Kikuko ; Hirai, Hiroyuki ; Nakamura, Masataka ; Okayama, Yoshimichi ; Ra, Chisei ; Aritake, Kosuke ; Urade, Yoshihiro ; Morimoto, Kazushi ; Sugimoto, Yukihiko ; Shimizu, Takao ; Narumiya, Shuh ; Hara, Shuntaro ; Murakami, Makoto. / Mast cell maturation is driven via a group III phospholipase A 2-prostaglandin D2-DP1 receptor paracrine axis. In: Nature Immunology. 2013 ; Vol. 14, No. 6. pp. 554-563.
@article{c74c0fc5f1d6462c9c70d638fc351b4f,
title = "Mast cell maturation is driven via a group III phospholipase A 2-prostaglandin D2-DP1 receptor paracrine axis",
abstract = "Microenvironment-based alterations in phenotypes of mast cells influence the susceptibility to anaphylaxis, yet the mechanisms underlying proper maturation of mast cells toward an anaphylaxis-sensitive phenotype are incompletely understood. Here we report that PLA2G3, a mammalian homolog of anaphylactic bee venom phospholipase A2, regulates this process. PLA2G3 secreted from mast cells is coupled with fibroblastic lipocalin-type PGD2 synthase (L-PGDS) to provide PGD2, which facilitates mast-cell maturation via PGD2 receptor DP1. Mice lacking PLA2G3, L-PGDS or DP1, mast cell-deficient mice reconstituted with PLA2G3-null or DP1-null mast cells, or mast cells cultured with L-PGDS-ablated fibroblasts exhibited impaired maturation and anaphylaxis of mast cells. Thus, we describe a lipid-driven PLA2G3-L-PGDS-DP1 loop that drives mast cell maturation.",
author = "Yoshitaka Taketomi and Noriko Ueno and Takumi Kojima and Hiroyasu Sato and Remi Murase and Kei Yamamoto and Satoshi Tanaka and Mariko Sakanaka and Masanori Nakamura and Yasumasa Nishito and Momoko Kawana and Naotomo Kambe and Kazutaka Ikeda and Ryo Taguchi and Satoshi Nakamizo and Kenji Kabashima and Gelb, {Michael H.} and Makoto Arita and Takehiko Yokomizo and Motonao Nakamura and Kikuko Watanabe and Hiroyuki Hirai and Masataka Nakamura and Yoshimichi Okayama and Chisei Ra and Kosuke Aritake and Yoshihiro Urade and Kazushi Morimoto and Yukihiko Sugimoto and Takao Shimizu and Shuh Narumiya and Shuntaro Hara and Makoto Murakami",
year = "2013",
month = "6",
doi = "10.1038/ni.2586",
language = "English",
volume = "14",
pages = "554--563",
journal = "Nature Immunology",
issn = "1529-2908",
publisher = "Nature Publishing Group",
number = "6",

}

TY - JOUR

T1 - Mast cell maturation is driven via a group III phospholipase A 2-prostaglandin D2-DP1 receptor paracrine axis

AU - Taketomi, Yoshitaka

AU - Ueno, Noriko

AU - Kojima, Takumi

AU - Sato, Hiroyasu

AU - Murase, Remi

AU - Yamamoto, Kei

AU - Tanaka, Satoshi

AU - Sakanaka, Mariko

AU - Nakamura, Masanori

AU - Nishito, Yasumasa

AU - Kawana, Momoko

AU - Kambe, Naotomo

AU - Ikeda, Kazutaka

AU - Taguchi, Ryo

AU - Nakamizo, Satoshi

AU - Kabashima, Kenji

AU - Gelb, Michael H.

AU - Arita, Makoto

AU - Yokomizo, Takehiko

AU - Nakamura, Motonao

AU - Watanabe, Kikuko

AU - Hirai, Hiroyuki

AU - Nakamura, Masataka

AU - Okayama, Yoshimichi

AU - Ra, Chisei

AU - Aritake, Kosuke

AU - Urade, Yoshihiro

AU - Morimoto, Kazushi

AU - Sugimoto, Yukihiko

AU - Shimizu, Takao

AU - Narumiya, Shuh

AU - Hara, Shuntaro

AU - Murakami, Makoto

PY - 2013/6

Y1 - 2013/6

N2 - Microenvironment-based alterations in phenotypes of mast cells influence the susceptibility to anaphylaxis, yet the mechanisms underlying proper maturation of mast cells toward an anaphylaxis-sensitive phenotype are incompletely understood. Here we report that PLA2G3, a mammalian homolog of anaphylactic bee venom phospholipase A2, regulates this process. PLA2G3 secreted from mast cells is coupled with fibroblastic lipocalin-type PGD2 synthase (L-PGDS) to provide PGD2, which facilitates mast-cell maturation via PGD2 receptor DP1. Mice lacking PLA2G3, L-PGDS or DP1, mast cell-deficient mice reconstituted with PLA2G3-null or DP1-null mast cells, or mast cells cultured with L-PGDS-ablated fibroblasts exhibited impaired maturation and anaphylaxis of mast cells. Thus, we describe a lipid-driven PLA2G3-L-PGDS-DP1 loop that drives mast cell maturation.

AB - Microenvironment-based alterations in phenotypes of mast cells influence the susceptibility to anaphylaxis, yet the mechanisms underlying proper maturation of mast cells toward an anaphylaxis-sensitive phenotype are incompletely understood. Here we report that PLA2G3, a mammalian homolog of anaphylactic bee venom phospholipase A2, regulates this process. PLA2G3 secreted from mast cells is coupled with fibroblastic lipocalin-type PGD2 synthase (L-PGDS) to provide PGD2, which facilitates mast-cell maturation via PGD2 receptor DP1. Mice lacking PLA2G3, L-PGDS or DP1, mast cell-deficient mice reconstituted with PLA2G3-null or DP1-null mast cells, or mast cells cultured with L-PGDS-ablated fibroblasts exhibited impaired maturation and anaphylaxis of mast cells. Thus, we describe a lipid-driven PLA2G3-L-PGDS-DP1 loop that drives mast cell maturation.

UR - http://www.scopus.com/inward/record.url?scp=84878250182&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84878250182&partnerID=8YFLogxK

U2 - 10.1038/ni.2586

DO - 10.1038/ni.2586

M3 - Article

C2 - 23624557

AN - SCOPUS:84878250182

VL - 14

SP - 554

EP - 563

JO - Nature Immunology

JF - Nature Immunology

SN - 1529-2908

IS - 6

ER -