Maturation of the medaka immune system depends on reciprocal interactions between the microbiota and the intestinal tract

被引:2
作者
Sakaguchi, Hiyori [1 ]
Sato, Yuna [1 ]
Matsumoto, Ryo [1 ]
Gomikawa, Joe [1 ]
Yoshida, Namie [1 ]
Suzuki, Tomohiro [1 ]
Matsuda, Masaru [1 ]
Iwanami, Norimasa [1 ]
机构
[1] Utsunomiya Univ, Ctr Biosci Res & Educ, Utsunomiya, Japan
来源
FRONTIERS IN IMMUNOLOGY | 2023年 / 14卷
关键词
medaka; microbiota; immune system; germ-free; SCID; INNATE IMMUNITY; GUT MICROBIOTA; ZEBRAFISH; EXPRESSION; EVOLUTION; SEQUENCE; MUTATION; CELLS; MODEL; C1Q;
D O I
10.3389/fimmu.2023.1259519
中图分类号
R392 [医学免疫学]; Q939.91 [免疫学];
学科分类号
100102 ;
摘要
The interactions between the host immune system and intestinal microorganisms have been studied in many animals, including fish. However, a detailed analysis has not been performed in medaka, an established fish model for biological studies. Here, we investigated the effect of immunodeficiency on the microbiota composition and the effect of gut bacteria on intestinal epithelial development and immune responses in medaka. Chronological analysis of the intestinal microbiota of interleukin 2 receptor subunit gamma (il2rg) mutant medaka showed a gradual decrease in the evenness of operational taxonomic units, mainly caused by the increased abundance of the Aeromonadaceae family. Exposure of wild-type medaka to high doses of an intestine-derived opportunistic bacterium of the Aeromonadaceae family induced an inflammatory response, suggesting a harmful effect on adult il2rg mutants. In addition, we established germ-free conditions in larval medaka and observed large absorptive vacuoles in intestinal epithelial cells, indicating a block in epithelial maturation. Transcriptome analysis revealed a decrease in the expression of genes involved in the defense response, including the antimicrobial peptide gene hepcidin, whose expression is induced by lipopolysaccharide stimulation in normal larvae. These results show that reciprocal interactions between the microbiome and the intestinal tract are required for the maturation of the medaka immune system.
引用
收藏
页数:14
相关论文
共 58 条
[31]   Noninvasive intravital imaging of thymocyte dynamics in medaka [J].
Li, Jie ;
Iwanami, Norimasa ;
Hoa, Vu Quynh ;
Furutani-Seiki, Makoto ;
Takahama, Yousuke .
JOURNAL OF IMMUNOLOGY, 2007, 179 (03) :1605-1615
[32]   Best practices for germ-free derivation and gnotobiotic zebrafish husbandry [J].
Melancon, E. ;
Canny, S. Gomez De La Torre ;
Sichel, S. ;
Kelly, M. ;
Wiles, T. J. ;
Rawls, J. F. ;
Eisen, J. S. ;
Guillemin, K. .
ZEBRAFISH: DISEASE MODELS AND CHEMICAL SCREENS, 2017, 138 :61-100
[33]   T-CELL INDEPENDENT ANTIGENS [J].
MOND, JJ ;
VOS, Q ;
LEES, A ;
SNAPPER, CM .
CURRENT OPINION IN IMMUNOLOGY, 1995, 7 (03) :349-354
[34]   ASC-deficiency impairs host defense against Aeromonas hydrophila infection in Japanese medaka, Oryzias latipes [J].
Morimoto, Natsuki ;
Okamura, Yo ;
Maekawa, Shun ;
Wang, Han-Ching ;
Aoki, Takashi ;
Kono, Tomoya ;
Sakai, Masahiro ;
Hikima, Jun-ichi .
FISH & SHELLFISH IMMUNOLOGY, 2020, 105 :427-437
[35]   Commensal Microbiota Regulate Vertebrate Innate Immunity-Insights From the Zebrafish [J].
Murdoch, Caitlin C. ;
Rawls, John F. .
FRONTIERS IN IMMUNOLOGY, 2019, 10
[36]   INTERLEUKIN-2 RECEPTOR GAMMA CHAIN MUTATION RESULTS IN X-LINKED SEVERE COMBINED IMMUNODEFICIENCY IN HUMANS [J].
NOGUCHI, M ;
YI, HF ;
ROSENBLATT, HM ;
FILIPOVICH, AH ;
ADELSTEIN, S ;
MODI, WS ;
MCBRIDE, OW ;
LEONARD, WJ .
CELL, 1993, 73 (01) :147-157
[37]   Deficiency of interleukin-17 receptor A1 induces microbiota disruption the intestine of Japanese medaka, Oryzias latipes [J].
Okamura, Yo ;
Kinoshita, Masato ;
Kono, Tomoya ;
Sakai, Masahiro ;
Hikima, Jun-ichi .
COMPARATIVE BIOCHEMISTRY AND PHYSIOLOGY D-GENOMICS & PROTEOMICS, 2021, 40
[38]   Interleukin-17A/F1 Deficiency Reduces Antimicrobial Gene Expression and Contributes to Microbiome Alterations in Intestines of Japanese medaka (Oryzias latipes) [J].
Okamura, Yo ;
Morimoto, Natsuki ;
Ikeda, Daisuke ;
Mizusawa, Nanami ;
Watabe, Shugo ;
Miyanishi, Hiroshi ;
Saeki, Yuichi ;
Takeyama, Haruko ;
Aoki, Takashi ;
Kinoshita, Masato ;
Kono, Tomoya ;
Sakai, Masahiro ;
Hikima, Jun-ichi .
FRONTIERS IN IMMUNOLOGY, 2020, 11
[39]   Macrophage Polarization: Different Gene Signatures in M1(LPS+) vs. Classically and M2(LPS-) vs. Alternatively Activated Macrophages [J].
Orecchioni, Marco ;
Ghosheh, Yanal ;
Pramod, Akula Bala ;
Ley, Klaus .
FRONTIERS IN IMMUNOLOGY, 2019, 10
[40]   Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown [J].
Pertea, Mihaela ;
Kim, Daehwan ;
Pertea, Geo M. ;
Leek, Jeffrey T. ;
Salzberg, Steven L. .
NATURE PROTOCOLS, 2016, 11 (09) :1650-1667