Oral administration of Lactobacillus plantarum JC7 alleviates OVA-induced murine food allergy through immunoregulation and restoring disordered intestinal microbiota

被引:17
作者
Duan, Cuicui [1 ]
Ma, Lin [1 ]
Yu, Jie [1 ]
Sun, Yixue [1 ]
Liu, Lifan [2 ]
Ma, Fumin [1 ]
Li, Xiaolei [1 ]
Li, Dan [1 ]
机构
[1] Changchun Univ, Jilin Prov Dept Educ, Key Lab Agroprod Proc Technol, 6543 Weixing Rd, Changchun 130022, Jilin, Peoples R China
[2] Changchun Univ, Grad Sch, 6543 Weixing Rd, Changchun 130022, Jilin, Peoples R China
关键词
Food allergy; Th1; Th2; imbalance; Treg; Th17; Lactobacillus plantarum; Gut microbiota;
D O I
10.1007/s00394-022-03016-5
中图分类号
R15 [营养卫生、食品卫生]; TS201 [基础科学];
学科分类号
100403 ;
摘要
Purpose The incidence and prevalence of food allergy have sharply risen over the past several decades. Oral administration of probiotic stains has been proven as a safe and effective method to control food allergy. In this study, it aims to comprehensively investigate the anti-allergic effect of Lactobacillus plantarum JC7. Methods Balb/c mice were randomly divided into three groups and received OVA (20 mu g/mouse, intraperitoneal injection), L. plantarum JC7 (2 x 10(8) CFU/mouse, intragastric administration) + OVA (20 mu g/mouse, intraperitoneal injection) or 0.9% saline (intragastric administration) for 3 weeks. Body weight was monitored weekly, and allergic reactions were evaluated after challenge of OVA. Serum levels of OVA-specific immunoglobulins and various cytokines were tested using ELISA, and the cecum microbiota was analysed by 16S rRNA sequencing to explore the relationships between these indicators and OVA-induced food allergy. Western blotting was used to identify the expression levels of phosphorylated I kappa B alpha and nuclear factor kappa B p65. Results OVA-sensitised mice showed mitigation of respiratory manifestations, alleviation of lung inflammation and congestion, and the presence of an intact intestinal villus structure. Furthermore, OVA-specific immunoglobulin E (IgE), OVA-specific-IgG1, and plasma histamine levels were declined in mice treated with L. plantarum JC7 than in OVA-sensitised mice. In addition, interferon-gamma (IFN-gamma) and interleukin 10 (IL-10) levels were significantly increased, while IL-4 and IL-17A levels were clearly decreased in mice that had undergone oral administration of L. plantarum JC7, compared with OVA-sensitised mice. These findings indicated imbalances of T helper cell type 1 (Th1)/Th2 and regulatory T cells (Treg)/Th17, which were confirmed by quantitative polymerase chain reaction (PCR). Western blotting demonstrated that the expression levels of phosphorylated I kappa B alpha and nuclear factor kappa B p65 were significantly increased in OVA-sensitised mice, but these changes were partly reversed after treatment with L. plantarum JC7. Oral administration of L. plantarum JC7 increased the richness, diversity, and evenness of cecum microbiota, characterised by higher Bacteroidetes abundance and lower Firmicutes abundance. Additionally, the intestinal microbial community composition was significantly altered in the OVA-sensitised group, indicating a disordered intestinal microbiota that was restored by the oral administration of L. plantarum JC7. Conclusion Overall, L. plantarum JC7 can prevent food allergy by rectifying Th1/Th2 and Treg/Th17 imbalances, combined with modifications of disordered intestinal microbiota.
引用
收藏
页码:685 / 698
页数:14
相关论文
共 37 条
[1]   Gut Microbiota as a Target for Preventive and Therapeutic Intervention against Food Allergy [J].
Aitoro, Rosita ;
Paparo, Lorella ;
Amoroso, Antonio ;
Di Costanzo, Margherita ;
Cosenza, Linda ;
Granata, Viviana ;
Di Scala, Carmen ;
Nocerino, Rita ;
Trinchese, Giovanna ;
Montella, Mariangela ;
Ercolini, Danilo ;
Canani, Roberto Berni .
NUTRIENTS, 2017, 9 (07)
[2]   Allergen Immunization Induces Major Changes in Microbiota Composition and Short-Chain Fatty Acid Production in Different Gut Segments in a Mouse Model of Lupine Food Allergy [J].
Andreassen, Monica ;
Rudi, Knut ;
Angell, Inga Leena ;
Dirven, Hubert ;
Nygaard, Unni C. .
INTERNATIONAL ARCHIVES OF ALLERGY AND IMMUNOLOGY, 2018, 177 (04) :311-323
[3]   Allergy development and the intestinal microflora during the first year of life [J].
Björkstén, B ;
Sepp, E ;
Julge, K ;
Voor, T ;
Mikelsaar, M .
JOURNAL OF ALLERGY AND CLINICAL IMMUNOLOGY, 2001, 108 (04) :516-520
[4]   Microbiome and food allergy [J].
Blazquez, Ana B. ;
Berin, M. Cecilia .
TRANSLATIONAL RESEARCH, 2017, 179 :199-203
[5]   Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 [J].
Bolyen, Evan ;
Rideout, Jai Ram ;
Dillon, Matthew R. ;
Bokulich, NicholasA. ;
Abnet, Christian C. ;
Al-Ghalith, Gabriel A. ;
Alexander, Harriet ;
Alm, Eric J. ;
Arumugam, Manimozhiyan ;
Asnicar, Francesco ;
Bai, Yang ;
Bisanz, Jordan E. ;
Bittinger, Kyle ;
Brejnrod, Asker ;
Brislawn, Colin J. ;
Brown, C. Titus ;
Callahan, Benjamin J. ;
Caraballo-Rodriguez, Andres Mauricio ;
Chase, John ;
Cope, Emily K. ;
Da Silva, Ricardo ;
Diener, Christian ;
Dorrestein, Pieter C. ;
Douglas, Gavin M. ;
Durall, Daniel M. ;
Duvallet, Claire ;
Edwardson, Christian F. ;
Ernst, Madeleine ;
Estaki, Mehrbod ;
Fouquier, Jennifer ;
Gauglitz, Julia M. ;
Gibbons, Sean M. ;
Gibson, Deanna L. ;
Gonzalez, Antonio ;
Gorlick, Kestrel ;
Guo, Jiarong ;
Hillmann, Benjamin ;
Holmes, Susan ;
Holste, Hannes ;
Huttenhower, Curtis ;
Huttley, Gavin A. ;
Janssen, Stefan ;
Jarmusch, Alan K. ;
Jiang, Lingjing ;
Kaehler, Benjamin D. ;
Bin Kang, Kyo ;
Keefe, Christopher R. ;
Keim, Paul ;
Kelley, Scott T. ;
Knights, Dan .
NATURE BIOTECHNOLOGY, 2019, 37 (08) :852-857
[6]   Differences in DNA methylation profile of Th1 and Th2 cytokine genes are associated with tolerance acquisition in children with IgE-mediated cow's milk allergy [J].
Canani, Roberto Berni ;
Paparo, Lorella ;
Nocerino, Rita ;
Cosenza, Linda ;
Pezzella, Vincenza ;
Di Costanzo, Margherita ;
Capasso, Mario ;
Del Monaco, Valentina ;
D'Argenio, Valeria ;
Greco, Luigi ;
Salvatore, Francesco .
CLINICAL EPIGENETICS, 2015, 7 :1-9
[7]   Alterations in the gut microbiotas of children with food sensitization in early life [J].
Chen, Chien-Chang ;
Chen, Kun-Jei ;
Kong, Man-Shan ;
Chang, Hung-Ju ;
Huang, Jing-Long .
PEDIATRIC ALLERGY AND IMMUNOLOGY, 2016, 27 (03) :254-262
[8]   The Relationship between the Infant Gut Microbiota and Allergy. The Role of Bifidobacterium breve and Prebiotic Oligosaccharides in the Activation of Anti-Allergic Mechanisms in Early Life [J].
Cukrowska, Bozena ;
Bierla, Joanna B. ;
Zakrzewska, Magdalena ;
Klukowski, Mark ;
Maciorkowska, Elzbieta .
NUTRIENTS, 2020, 12 (04)
[9]  
Duan CC, 2021, FOOD FUNCT, V12, P5417, DOI [10.1039/d1fo00492a, 10.1039/D1FO00492A]
[10]   Effect of 3 lactobacilli on immunoregulation and intestinal microbiota in a β-lactoglobulin-induced allergic mouse model [J].
Fu, Guiming ;
Zhao, Kui ;
Chen, Hui ;
Wang, Yuanyuan ;
Nie, Lijuan ;
Wei, Hua ;
Wan, Cuixiang .
JOURNAL OF DAIRY SCIENCE, 2019, 102 (03) :1943-1958