Skin CD4+ memory T cells play an essential role in acquired anti-tick immunity through interleukin-3-mediated basophil recruitment to tick-feeding sites

Takuya Ohta, Soichiro Yoshikawa, Yuya Tabakawa, Kayoko Yamaji, Kenji Ishiwata, Hiroshi Shitara, Choji Taya, Masatsugu Oh-Hora, Yohei Kawano, Kensuke Miyake, Yoshinori Yamanishi, Hiromichi Yonekawa, Naohiro Watanabe, Hirotaka Kanuka, Hajime Karasuyama

Research output: Contribution to journalArticle

7 Citations (Scopus)

Abstract

Ticks, blood-sucking arthropods, serve as vectors for transmission of infectious diseases including Lyme borreliosis. After tick infestation, several animal species can develop resistance to subsequent infestations, reducing the risk of transmission. In a mouse model, basophils reportedly infiltrate tick-feeding sites during the second but not first infestation and play a crucial role in the expression of acquired tick resistance. However, the mechanism underlying basophil recruitment to the second tick-feeding site remains ill-defined. Here, we investigated cells and their products responsible for the basophil recruitment. Little or no basophil infiltration was detected in T-cell-deficient mice, and adoptive transfer of CD4+ but not CD8+ T cells reconstituted it. Il3 gene expression was highly upregulated at the second tick-feeding site, and adoptive transfer of interleukin-3 (IL-3)-sufficient but not IL-3-deficient CD4+ T cells conferred the basophil infiltration on T-cell-deficient mice, indicating that the CD4+ T-cell-derived IL-3 is essential for the basophil recruitment. Notably, IL-3+ resident CD4+ memory T cells were detected even before the second infestation in previously uninfested skin distant from the first tick-feeding site. Taken together, IL-3 produced locally by skin CD4+ memory T cells appears to play a crucial role in basophil recruitment to the second tick-feeding site.

Original languageEnglish
Article number1348
JournalFrontiers in immunology
Volume8
Issue numberOCT
DOIs
Publication statusPublished - Oct 16 2017
Externally publishedYes

Fingerprint

Basophils
Interleukin-3
Ticks
Immunity
T-Lymphocytes
Skin
Adoptive Transfer
Tick Infestations
Infectious Disease Transmission
Lyme Disease
Arthropods
Gene Expression

Keywords

  • Basophils
  • CD4 memory T cells
  • IL-3
  • Protective immunity
  • Tick infestation

ASJC Scopus subject areas

  • Immunology and Allergy
  • Immunology

Cite this

Skin CD4+ memory T cells play an essential role in acquired anti-tick immunity through interleukin-3-mediated basophil recruitment to tick-feeding sites. / Ohta, Takuya; Yoshikawa, Soichiro; Tabakawa, Yuya; Yamaji, Kayoko; Ishiwata, Kenji; Shitara, Hiroshi; Taya, Choji; Oh-Hora, Masatsugu; Kawano, Yohei; Miyake, Kensuke; Yamanishi, Yoshinori; Yonekawa, Hiromichi; Watanabe, Naohiro; Kanuka, Hirotaka; Karasuyama, Hajime.

In: Frontiers in immunology, Vol. 8, No. OCT, 1348, 16.10.2017.

Research output: Contribution to journalArticle

Ohta, T, Yoshikawa, S, Tabakawa, Y, Yamaji, K, Ishiwata, K, Shitara, H, Taya, C, Oh-Hora, M, Kawano, Y, Miyake, K, Yamanishi, Y, Yonekawa, H, Watanabe, N, Kanuka, H & Karasuyama, H 2017, 'Skin CD4+ memory T cells play an essential role in acquired anti-tick immunity through interleukin-3-mediated basophil recruitment to tick-feeding sites', Frontiers in immunology, vol. 8, no. OCT, 1348. https://doi.org/10.3389/fimmu.2017.01348
Ohta, Takuya ; Yoshikawa, Soichiro ; Tabakawa, Yuya ; Yamaji, Kayoko ; Ishiwata, Kenji ; Shitara, Hiroshi ; Taya, Choji ; Oh-Hora, Masatsugu ; Kawano, Yohei ; Miyake, Kensuke ; Yamanishi, Yoshinori ; Yonekawa, Hiromichi ; Watanabe, Naohiro ; Kanuka, Hirotaka ; Karasuyama, Hajime. / Skin CD4+ memory T cells play an essential role in acquired anti-tick immunity through interleukin-3-mediated basophil recruitment to tick-feeding sites. In: Frontiers in immunology. 2017 ; Vol. 8, No. OCT.
@article{ab68954c77864cd7801c6266de6df8e8,
title = "Skin CD4+ memory T cells play an essential role in acquired anti-tick immunity through interleukin-3-mediated basophil recruitment to tick-feeding sites",
abstract = "Ticks, blood-sucking arthropods, serve as vectors for transmission of infectious diseases including Lyme borreliosis. After tick infestation, several animal species can develop resistance to subsequent infestations, reducing the risk of transmission. In a mouse model, basophils reportedly infiltrate tick-feeding sites during the second but not first infestation and play a crucial role in the expression of acquired tick resistance. However, the mechanism underlying basophil recruitment to the second tick-feeding site remains ill-defined. Here, we investigated cells and their products responsible for the basophil recruitment. Little or no basophil infiltration was detected in T-cell-deficient mice, and adoptive transfer of CD4+ but not CD8+ T cells reconstituted it. Il3 gene expression was highly upregulated at the second tick-feeding site, and adoptive transfer of interleukin-3 (IL-3)-sufficient but not IL-3-deficient CD4+ T cells conferred the basophil infiltration on T-cell-deficient mice, indicating that the CD4+ T-cell-derived IL-3 is essential for the basophil recruitment. Notably, IL-3+ resident CD4+ memory T cells were detected even before the second infestation in previously uninfested skin distant from the first tick-feeding site. Taken together, IL-3 produced locally by skin CD4+ memory T cells appears to play a crucial role in basophil recruitment to the second tick-feeding site.",
keywords = "Basophils, CD4 memory T cells, IL-3, Protective immunity, Tick infestation",
author = "Takuya Ohta and Soichiro Yoshikawa and Yuya Tabakawa and Kayoko Yamaji and Kenji Ishiwata and Hiroshi Shitara and Choji Taya and Masatsugu Oh-Hora and Yohei Kawano and Kensuke Miyake and Yoshinori Yamanishi and Hiromichi Yonekawa and Naohiro Watanabe and Hirotaka Kanuka and Hajime Karasuyama",
year = "2017",
month = "10",
day = "16",
doi = "10.3389/fimmu.2017.01348",
language = "English",
volume = "8",
journal = "Frontiers in Immunology",
issn = "1664-3224",
publisher = "Frontiers Media S. A.",
number = "OCT",

}

TY - JOUR

T1 - Skin CD4+ memory T cells play an essential role in acquired anti-tick immunity through interleukin-3-mediated basophil recruitment to tick-feeding sites

AU - Ohta, Takuya

AU - Yoshikawa, Soichiro

AU - Tabakawa, Yuya

AU - Yamaji, Kayoko

AU - Ishiwata, Kenji

AU - Shitara, Hiroshi

AU - Taya, Choji

AU - Oh-Hora, Masatsugu

AU - Kawano, Yohei

AU - Miyake, Kensuke

AU - Yamanishi, Yoshinori

AU - Yonekawa, Hiromichi

AU - Watanabe, Naohiro

AU - Kanuka, Hirotaka

AU - Karasuyama, Hajime

PY - 2017/10/16

Y1 - 2017/10/16

N2 - Ticks, blood-sucking arthropods, serve as vectors for transmission of infectious diseases including Lyme borreliosis. After tick infestation, several animal species can develop resistance to subsequent infestations, reducing the risk of transmission. In a mouse model, basophils reportedly infiltrate tick-feeding sites during the second but not first infestation and play a crucial role in the expression of acquired tick resistance. However, the mechanism underlying basophil recruitment to the second tick-feeding site remains ill-defined. Here, we investigated cells and their products responsible for the basophil recruitment. Little or no basophil infiltration was detected in T-cell-deficient mice, and adoptive transfer of CD4+ but not CD8+ T cells reconstituted it. Il3 gene expression was highly upregulated at the second tick-feeding site, and adoptive transfer of interleukin-3 (IL-3)-sufficient but not IL-3-deficient CD4+ T cells conferred the basophil infiltration on T-cell-deficient mice, indicating that the CD4+ T-cell-derived IL-3 is essential for the basophil recruitment. Notably, IL-3+ resident CD4+ memory T cells were detected even before the second infestation in previously uninfested skin distant from the first tick-feeding site. Taken together, IL-3 produced locally by skin CD4+ memory T cells appears to play a crucial role in basophil recruitment to the second tick-feeding site.

AB - Ticks, blood-sucking arthropods, serve as vectors for transmission of infectious diseases including Lyme borreliosis. After tick infestation, several animal species can develop resistance to subsequent infestations, reducing the risk of transmission. In a mouse model, basophils reportedly infiltrate tick-feeding sites during the second but not first infestation and play a crucial role in the expression of acquired tick resistance. However, the mechanism underlying basophil recruitment to the second tick-feeding site remains ill-defined. Here, we investigated cells and their products responsible for the basophil recruitment. Little or no basophil infiltration was detected in T-cell-deficient mice, and adoptive transfer of CD4+ but not CD8+ T cells reconstituted it. Il3 gene expression was highly upregulated at the second tick-feeding site, and adoptive transfer of interleukin-3 (IL-3)-sufficient but not IL-3-deficient CD4+ T cells conferred the basophil infiltration on T-cell-deficient mice, indicating that the CD4+ T-cell-derived IL-3 is essential for the basophil recruitment. Notably, IL-3+ resident CD4+ memory T cells were detected even before the second infestation in previously uninfested skin distant from the first tick-feeding site. Taken together, IL-3 produced locally by skin CD4+ memory T cells appears to play a crucial role in basophil recruitment to the second tick-feeding site.

KW - Basophils

KW - CD4 memory T cells

KW - IL-3

KW - Protective immunity

KW - Tick infestation

UR - http://www.scopus.com/inward/record.url?scp=85031777636&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85031777636&partnerID=8YFLogxK

U2 - 10.3389/fimmu.2017.01348

DO - 10.3389/fimmu.2017.01348

M3 - Article

AN - SCOPUS:85031777636

VL - 8

JO - Frontiers in Immunology

JF - Frontiers in Immunology

SN - 1664-3224

IS - OCT

M1 - 1348

ER -