Abstract:Objective To investigate the age distribution characteristics of intestinal segmented filamentous bacteria (SFB) in children and their relationship with intestinal mucosal immunity. Methods The fresh feces of 177 children and the ileocecal fluid of 47 children during colonoscopy were collected. The SFB was determined by real-time PCR. The concentration of secretory immunoglobulin A (sIgA) was determined by enzyme-linked immunosorbent assay. The numbers of interleukin 17A (IL-17A) cells and intraepithelial lymphocytes in the terminal ileum mucosa and the expression of transcription factors associated with the differentiation of T helper (Th) cells, T-box transcription factor (T-bet), forkhead box P3 (FOXP3), and retinoid-related orphan receptor gamma t (ROR-γt), were determined by immunohistochemistry. Results The positive rate of intestinal SFB in these children was 19.2% (34/177). Trend analysis showed that the positive rate of SFB was correlated with age:the rates for children aged 0-, 1-, 2-, 3-, 4-, 5-, 6-, and 7-15 years were 40%, 47%, 32%, 15%, 12%, 13%, 15% and 4% respectively (P < 0.001). The concentration of sIgA in intestinal fluid was significantly higher in SFB-positive children (n=24) than in SFB-negative children (n=23) (P < 0.01). The number of intraepithelial lymphocytes in the terminal ileum mucosa and the expression of T-bet, FOXP3, and ROR-γt were not significantly different between the SFB-positive group (n=12) and the SFB-negative group (n=11), but the number of IL-17A cells in the terminal ileum mucosa was significantly lower in the SFB-positive group than in the SFB-negative group (P < 0.05). Conclusions Intestinal SFB colonization in children is age-related, and the colonization rate is relatively high in children under 3 years old. In SFB-positive children, the secretion of intestinal sIgA is increased, while the number of IL-17A cells in the terminal ileum is reduced.
LIU Wei-Rong,SHU Xiao-Li,GU Wei-Zhong et al. Age distribution characteristics of intestinal segmented filamentous bacteria and their relationship with intestinal mucosal immunity in children[J]. CJCP, 2019, 21(6): 534-540.
Human Microbiome Project Consortium. A framework for Human Microbiome Research[J]. Nature, 2012, 486(7402):215-221.
[2]
Chung H, Pamp SJ, Hill JA, et al. Gut immune maturation depends on colonization with a host-specific microbiota[J]. Cell, 2012, 149(7):1578-1593.
[3]
Flannigan KL, Denning TL. Segmented filamentous bacteria-induced immune responses:a balancing act between host protection and autoimmunity[J]. Immunology, 2018, 154:537-546.
[4]
Liao N, Yin Y, Sun G, et al. Colonization and distribution of segmented filamentous bacteria (SFB) in chicken gastrointestinal tract and their relationship with host immunity[J]. FEMS Microbiol Ecol, 2012, 81(2):395-406.
[5]
Ohashi Y, Hiraguchi M, Ushida K. The composition of intestinal bacteria affects the level of luminal IgA[J]. Biosci Biotechnol Biochem, 2006, 70(12):3031-3035.
[6]
Yin Y, Wang Y, Zhu L, et al. Comparative analysis of the distribution of segmented filamentous bacteria in humans, mice, and chickens[J]. ISME J, 2013, 7(3):615-621.
[7]
Caselli M, Tosini D, Gafa R, et al. Segmented filamentous bacteria-like organisms in histological slides of ileo-cecal valves in patients with ulcerative colitis[J]. Am J Gastroenterol, 2013, 108(5):860-861.
[8]
Ge Z, Feng Y, Woods SE, et al. Spatial and temporal colonization dynamics of segmented filamentous bacteria is influenced by gender, age and experimental infection with Helicobacter hepaticus in Swiss Webstar mice[J]. Microbes Infect, 2015, 17(1):16-22.
[9]
Finotti A, Gasparello J, Lampronti I, et al. PCR detection of segmented filamentous bacteria in the terminal ileum of patients with ulcerative colitis[J]. BMJ Open Gastroenterol, 2017, 4(1):e000172.
[10]
Ericsson AC, Hagan CE, Davis DJ, et al. Segmented filamentous bacteria:commensal microbes with potential effects on research[J]. Comp Med, 2014, 64(2):90-98.
[11]
Schnupf P, Gaboriau-Routhiau V, Gros M, et al. Growth and host interaction of mouse segmented filamentous bacteria in vitro[J]. Nature, 2015, 520(7545):99-103.
[12]
Turnbaugh PJ, Ridaura VK, Faith JJ, et al. The effect of diet on the human gut microbiome:a metagenomic analysis in humanized gnotobiotic mice[J]. Sci Transl Med, 2009, 1(6):6ra14.
[13]
Jin S, Zhao D, Cai C, et al. Low-dose penicillin exposure in early life decreases Th17 and the susceptibility to DSS colitis in mice through gut microbiota modification[J]. Sci Rep, 2017, 7:43662.
[14]
Prakash T, Oshima K, Morita H, et al. Complete genome sequences of rat and mouse segmented filamentous bacteria, a potent inducer of Th17 cell differentiation[J]. Cell Host Microbe, 2011, 10(3):273-284.
[15]
Sczesnak A, Segata N, Qin X, et al. The genome of Th17 cell-inducing segmented filamentous bacteria reveals extensive auxotrophy and adaptations to the intestinal environment[J]. Cell Host Microbe, 2011, 10(3):260-272.
[16]
Suzuki K, Meek B, Doi Y, et al. Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut[J]. Proc Natl Acad Sci U S A, 2004, 101(7):1981-1986.
[17]
Brandzaeg P. Mucosal immunity:induction, dissemination, and effector functions[J]. Scand J Immunol, 2009, 70(6):505-515.
[18]
Palm NW, de Zoete MR, Cullen TW, et al. Immunoglobulin A coating identifies colitogenic bacteria in inflammatory bowel disease[J]. Cell, 2014, 158(5):1000-1010.
[19]
Klaasen HL, Van der Heijden PJ, Stok W, et al. A pathogenic, intestinal, segmented, filamentous bacteria stimulate the mucosal immune system of mice[J]. Infect Immun, 1993, 61(1):303-306.
[20]
Talham GL, Jiang HQ, Bos NA, et al. Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the murine gut mucosal immune system[J]. Infect Immun, 1999, 67(4):1992-2000.
[21]
Lamm ME. Interaction of antigens and antibodies at mucosal surfaces[J]. Annu Rev Microbiol, 1997, 51:311-340.
[22]
Farkas AM, Panea C, Goto Y, et al. Induction of Th17 cells by segmented filamentous bacteria in the murine intestine[J]. J Immunol Methods, 2015, 421:104-111.
[23]
Atarashi K, Tanoue T, Ando M, et al. Th17 cell induction by adhesion of microbes to intestinal epithelial cells[J]. Cell, 2015, 163(2):367-380.
[24]
Furusawa Y, ObataY, Hase K. Commensal microbiota regulates T cell fate decision in the gut[J]. Semin Immunopathol, 2015, 37(1):17-25.
[25]
Teng F, Klinger CN, Felix KM, et al. Gut microbiota drive autoimmune arthritis by promoting differentiation and migration of Peyer's patch T follicular helper cells[J]. Immunity, 2016, 44(4):875-888.