CSF-1 receptor-mediated differentiation of a new type of monocytic cell with B cell-stimulating activity

Its selective dependence on IL-34

Fumihiro Yamane, Yumiko Nishikawa, Kazue Matsui, Miki Asakura, Eriko Iwasaki, Koji Watanabe, Hikaru Tanimoto, Hiroki Sano, Yuki Fujiwara, E. Richard Stanley, Naoki Kanayama, Neil A. Mabbott, Masaki Magari, Hitoshi Ohmori

Research output: Contribution to journalArticle

23 Citations (Scopus)

Abstract

With the use of a mouse FDC line, FL-Y, we have been analyzing roles for FDCs in controlling B cell fate in GCs. Beside these regulatory functions, we fortuitously found that FL-Y cells induced a new type of CD11b+ monocytic cells (F4/80+, Gr-1-, Ly6C-, I-A/E-/lo, CD11c-, CD115+, CXCR4+, CCR2+, CX3CR1-) when cultured with a Lin-c-kit+ population from mouse spleen cells. The developed CD11b+ cells shared a similar gene-expression profile to mononuclear phagocytes and were designated as FDMCs. Here, we describe characteristic immunological functions and the induction mechanism of FDMCs. Proliferation of anti-CD40 antibody-stimulated B cells was markedly accelerated in the presence of FDMCs. In addition, the FDMC-activated B cells efficiently acquired GC B cell-associated markers (Fas and GL-7). We observed an increase of FDMC-like cells in mice after immunization. On the other hand, FL-Y cells were found to produce CSF-1 as well as IL-34, both of which are known to induce development of macrophages and monocytes by binding to the common receptor, CSF-1R, expressed on the progenitors. However, we show that FL-Y-derived IL-34, but not CSF-1, was selectively responsible for FDMC generation using neutralizing antibodies and RNAi. We also confirmed that FDMC generation was strictly dependent on CSF-1R. To our knowledge, a CSF-1R-mediated differentiation process that is intrinsically specific for IL-34 has not been reported. Our results provide new insights into understanding the diversity of IL-34 and CSF-1 signaling pathways through CSF-1R.

Original languageEnglish (US)
Pages (from-to)19-31
Number of pages13
JournalJournal of Leukocyte Biology
Volume95
Issue number1
DOIs
StatePublished - 2014

Fingerprint

Macrophage Colony-Stimulating Factor Receptors
B-Lymphocytes
Macrophage Colony-Stimulating Factor
Colony-Stimulating Factor Receptors
Phagocytes
RNA Interference
Neutralizing Antibodies
Transcriptome
Monocytes
Anti-Idiotypic Antibodies
Immunization
Spleen
Macrophages
Population

Keywords

  • CD11b
  • Follicular dendritic cells
  • Mouse spleen

ASJC Scopus subject areas

  • Cell Biology
  • Immunology

Cite this

CSF-1 receptor-mediated differentiation of a new type of monocytic cell with B cell-stimulating activity : Its selective dependence on IL-34. / Yamane, Fumihiro; Nishikawa, Yumiko; Matsui, Kazue; Asakura, Miki; Iwasaki, Eriko; Watanabe, Koji; Tanimoto, Hikaru; Sano, Hiroki; Fujiwara, Yuki; Richard Stanley, E.; Kanayama, Naoki; Mabbott, Neil A.; Magari, Masaki; Ohmori, Hitoshi.

In: Journal of Leukocyte Biology, Vol. 95, No. 1, 2014, p. 19-31.

Research output: Contribution to journalArticle

Yamane, F, Nishikawa, Y, Matsui, K, Asakura, M, Iwasaki, E, Watanabe, K, Tanimoto, H, Sano, H, Fujiwara, Y, Richard Stanley, E, Kanayama, N, Mabbott, NA, Magari, M & Ohmori, H 2014, 'CSF-1 receptor-mediated differentiation of a new type of monocytic cell with B cell-stimulating activity: Its selective dependence on IL-34', Journal of Leukocyte Biology, vol. 95, no. 1, pp. 19-31. https://doi.org/10.1189/jlb.0613311
Yamane, Fumihiro ; Nishikawa, Yumiko ; Matsui, Kazue ; Asakura, Miki ; Iwasaki, Eriko ; Watanabe, Koji ; Tanimoto, Hikaru ; Sano, Hiroki ; Fujiwara, Yuki ; Richard Stanley, E. ; Kanayama, Naoki ; Mabbott, Neil A. ; Magari, Masaki ; Ohmori, Hitoshi. / CSF-1 receptor-mediated differentiation of a new type of monocytic cell with B cell-stimulating activity : Its selective dependence on IL-34. In: Journal of Leukocyte Biology. 2014 ; Vol. 95, No. 1. pp. 19-31.
@article{14c679faea534fd299727c45780f7665,
title = "CSF-1 receptor-mediated differentiation of a new type of monocytic cell with B cell-stimulating activity: Its selective dependence on IL-34",
abstract = "With the use of a mouse FDC line, FL-Y, we have been analyzing roles for FDCs in controlling B cell fate in GCs. Beside these regulatory functions, we fortuitously found that FL-Y cells induced a new type of CD11b+ monocytic cells (F4/80+, Gr-1-, Ly6C-, I-A/E-/lo, CD11c-, CD115+, CXCR4+, CCR2+, CX3CR1-) when cultured with a Lin-c-kit+ population from mouse spleen cells. The developed CD11b+ cells shared a similar gene-expression profile to mononuclear phagocytes and were designated as FDMCs. Here, we describe characteristic immunological functions and the induction mechanism of FDMCs. Proliferation of anti-CD40 antibody-stimulated B cells was markedly accelerated in the presence of FDMCs. In addition, the FDMC-activated B cells efficiently acquired GC B cell-associated markers (Fas and GL-7). We observed an increase of FDMC-like cells in mice after immunization. On the other hand, FL-Y cells were found to produce CSF-1 as well as IL-34, both of which are known to induce development of macrophages and monocytes by binding to the common receptor, CSF-1R, expressed on the progenitors. However, we show that FL-Y-derived IL-34, but not CSF-1, was selectively responsible for FDMC generation using neutralizing antibodies and RNAi. We also confirmed that FDMC generation was strictly dependent on CSF-1R. To our knowledge, a CSF-1R-mediated differentiation process that is intrinsically specific for IL-34 has not been reported. Our results provide new insights into understanding the diversity of IL-34 and CSF-1 signaling pathways through CSF-1R.",
keywords = "CD11b, Follicular dendritic cells, Mouse spleen",
author = "Fumihiro Yamane and Yumiko Nishikawa and Kazue Matsui and Miki Asakura and Eriko Iwasaki and Koji Watanabe and Hikaru Tanimoto and Hiroki Sano and Yuki Fujiwara and {Richard Stanley}, E. and Naoki Kanayama and Mabbott, {Neil A.} and Masaki Magari and Hitoshi Ohmori",
year = "2014",
doi = "10.1189/jlb.0613311",
language = "English (US)",
volume = "95",
pages = "19--31",
journal = "Journal of Leukocyte Biology",
issn = "0741-5400",
publisher = "FASEB",
number = "1",

}

TY - JOUR

T1 - CSF-1 receptor-mediated differentiation of a new type of monocytic cell with B cell-stimulating activity

T2 - Its selective dependence on IL-34

AU - Yamane, Fumihiro

AU - Nishikawa, Yumiko

AU - Matsui, Kazue

AU - Asakura, Miki

AU - Iwasaki, Eriko

AU - Watanabe, Koji

AU - Tanimoto, Hikaru

AU - Sano, Hiroki

AU - Fujiwara, Yuki

AU - Richard Stanley, E.

AU - Kanayama, Naoki

AU - Mabbott, Neil A.

AU - Magari, Masaki

AU - Ohmori, Hitoshi

PY - 2014

Y1 - 2014

N2 - With the use of a mouse FDC line, FL-Y, we have been analyzing roles for FDCs in controlling B cell fate in GCs. Beside these regulatory functions, we fortuitously found that FL-Y cells induced a new type of CD11b+ monocytic cells (F4/80+, Gr-1-, Ly6C-, I-A/E-/lo, CD11c-, CD115+, CXCR4+, CCR2+, CX3CR1-) when cultured with a Lin-c-kit+ population from mouse spleen cells. The developed CD11b+ cells shared a similar gene-expression profile to mononuclear phagocytes and were designated as FDMCs. Here, we describe characteristic immunological functions and the induction mechanism of FDMCs. Proliferation of anti-CD40 antibody-stimulated B cells was markedly accelerated in the presence of FDMCs. In addition, the FDMC-activated B cells efficiently acquired GC B cell-associated markers (Fas and GL-7). We observed an increase of FDMC-like cells in mice after immunization. On the other hand, FL-Y cells were found to produce CSF-1 as well as IL-34, both of which are known to induce development of macrophages and monocytes by binding to the common receptor, CSF-1R, expressed on the progenitors. However, we show that FL-Y-derived IL-34, but not CSF-1, was selectively responsible for FDMC generation using neutralizing antibodies and RNAi. We also confirmed that FDMC generation was strictly dependent on CSF-1R. To our knowledge, a CSF-1R-mediated differentiation process that is intrinsically specific for IL-34 has not been reported. Our results provide new insights into understanding the diversity of IL-34 and CSF-1 signaling pathways through CSF-1R.

AB - With the use of a mouse FDC line, FL-Y, we have been analyzing roles for FDCs in controlling B cell fate in GCs. Beside these regulatory functions, we fortuitously found that FL-Y cells induced a new type of CD11b+ monocytic cells (F4/80+, Gr-1-, Ly6C-, I-A/E-/lo, CD11c-, CD115+, CXCR4+, CCR2+, CX3CR1-) when cultured with a Lin-c-kit+ population from mouse spleen cells. The developed CD11b+ cells shared a similar gene-expression profile to mononuclear phagocytes and were designated as FDMCs. Here, we describe characteristic immunological functions and the induction mechanism of FDMCs. Proliferation of anti-CD40 antibody-stimulated B cells was markedly accelerated in the presence of FDMCs. In addition, the FDMC-activated B cells efficiently acquired GC B cell-associated markers (Fas and GL-7). We observed an increase of FDMC-like cells in mice after immunization. On the other hand, FL-Y cells were found to produce CSF-1 as well as IL-34, both of which are known to induce development of macrophages and monocytes by binding to the common receptor, CSF-1R, expressed on the progenitors. However, we show that FL-Y-derived IL-34, but not CSF-1, was selectively responsible for FDMC generation using neutralizing antibodies and RNAi. We also confirmed that FDMC generation was strictly dependent on CSF-1R. To our knowledge, a CSF-1R-mediated differentiation process that is intrinsically specific for IL-34 has not been reported. Our results provide new insights into understanding the diversity of IL-34 and CSF-1 signaling pathways through CSF-1R.

KW - CD11b

KW - Follicular dendritic cells

KW - Mouse spleen

UR - http://www.scopus.com/inward/record.url?scp=84897018686&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84897018686&partnerID=8YFLogxK

U2 - 10.1189/jlb.0613311

DO - 10.1189/jlb.0613311

M3 - Article

VL - 95

SP - 19

EP - 31

JO - Journal of Leukocyte Biology

JF - Journal of Leukocyte Biology

SN - 0741-5400

IS - 1

ER -