Segmented filamentous bacteria‐induced immune responses: a balancing act between host protection and autoimmunity

Flannigan, Kyle L.; Denning, Timothy L.

doi:10.1111/imm.12950

Cited by 69 publications

(57 citation statements)

References 80 publications

(153 reference statements)

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“…However, these variations are overridden by the strong and consistent effect of age, validated through the present study which controlled for these factors. We found that “ Candidatus Savagella” appeared earlier and in higher abundance in BMD and T-Pbx treatment groups, similar to what has been previously found in turkeys (4), and our finding highlights the possible importance of segmented filamentous bacteria such as “ Candidatus Savagella” at priming the immune system and promoting diversification of the healthy microbiome in the gut (21). In the cecum, there is a trend from facultative anaerobes toward a diverse anaerobic bacterial composition, likely reflecting physical changes occurring in the gut during the first weeks of age.…”

Section: Discussionsupporting

confidence: 89%

Antibiotics and Host-Tailored Probiotics Similarly Modulate Effects on the Developing Avian Microbiome, Mycobiome, and Host Gene Expression

Ward

Weber

Mendoza

et al. 2019

mBio

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The microbiome is important to all animals, including poultry, playing a critical role in health and performance. Low-dose antibiotics have historically been used to modulate food production animals and their microbiome. Identifying alternatives to antibiotics conferring similar modulatory properties has been elusive. The purpose of this study was to determine if a host-tailored probiotic could recapitulate effects of a low-dose antibiotic on host response and the developing microbiome. Over 13 days of life, turkey poults were supplemented continuously with a low-dose antibiotic or oral supplementation of a prebiotic with or without two different probiotics (8 cage units, n = 80 per group). Gastrointestinal bacterial and fungal communities of poults were characterized by 16S rRNA gene and ITS2 amplicon sequencing. Localized and systemic host gene expression was assessed using transcriptome sequencing (RNA-Seq), kinase activity was assessed by avian-specific kinome peptide arrays, and performance parameters were assessed. We found that development of the early-life microbiome of turkey poults was tightly ordered in a tissue- and time-specific manner. Low-dose antibiotic and turkey-tailored probiotic supplementation, but not nontailored probiotic supplementation, elicited similar shifts in overall microbiome composition during development compared to controls. Treatment-induced bacterial changes were accompanied by parallel shifts in the fungal community and host gene expression and enhanced performance metrics. These results were validated in pen trials that identified further additive effects of the turkey-tailored probiotic combined with different prebiotics. Alternative approaches to low-dose antibiotic use in poultry are feasible and can be optimized utilizing the indigenous poultry microbiome. Similar approaches may also be beneficial for humans. IMPORTANCE Alternative approaches are greatly needed to reduce the need for antibiotic use in food animal production. This study utilized a pipeline for the development of a host-tailored probiotic to enhance performance in commercial turkeys and modulate their microbiota, similar to the effects of low-dose antibiotic administration. We determined that a host-tailored probiotic, developed in the context of the commercial turkey gut microbiome, was more effective at modulating these parameters than a nontailored probiotic cocktail. Furthermore, the host-tailored probiotic mimicked many of the effects of a low-dose antibiotic growth promoter. Surprisingly, the effects of the antibiotic growth promoter and host-tailored probiotic were observed across kingdoms, illustrating the coordinated interkingdom effects of these approaches. This work suggests that tailored approaches to probiotic development hold promise for modulating the avian host and its microbiota.

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Section: Discussionsupporting

confidence: 89%

Antibiotics and Host-Tailored Probiotics Similarly Modulate Effects on the Developing Avian Microbiome, Mycobiome, and Host Gene Expression

Ward

Weber

Mendoza

et al. 2019

mBio

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“…Recent investigations point to the IL-23/Th17 axis as playing a major role in psoriasis pathogenesis 19 . The adhesion of specific members of gut microbiome to intestinal epithelial cells is found to be essential for the induction of Th17 cells 20 – 22 . Mice exposed to antibiotics showed inhibition of psoriasis induction by a dysregulation of gut and skin microbiota 23 – 25 .…”

Section: Introductionmentioning

confidence: 99%

Metagenomic analysis of gut microbiota in non-treated plaque psoriasis patients stratified by disease severity: development of a new Psoriasis-Microbiome Index

Dei-Cas

Giliberto

Luce

et al. 2020

Sci Rep

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psoriasis is an immune-mediated skin disorder. imbalance of gut microbial populations has been implicated in many diseases. We aimed to investigate whether there were differences in gut microbiota in psoriasis patients vs non-psoriasis controls and between psoriasis severity groups. 55 psoriasis patients and 27 controls were included. V3-V4 regions of the 16S rRNA gene of fecal samples were analyzed using Illumina MiSeq. Bioinformatic analysis was performed. We found changes in gut microbiome composition depending on their psoriasis status as determined by weighted unifrac (p < 0.05), in particular an increase in Firmicutes and depletion of Bacteroidetes in psoriasis patients. Additionally, the Faecalibacterium and Blautia genus were higher in psoriasis patients while Bacteroides and Paraprevotella in non-psoriasis controls (p < 0.05, LDA score > 2). Moderate-to-severe psoriasis patients had lower biodiversity than mild psoriatic patients (p = 0.049). No differences for beta-diversity were found. We developed a Psoriasis-Microbiota Index (PMI), which discriminated among psoriasis patients and controls with sensitivity: 0.78 and specificity: 0.79. Furthermore, we performed a meta-analysis with published data to validate this index. We demonstrated gut dysbiosis in psoriasis patients, suggesting a role in psoriasis pathophysiology. Furthermore, we developed a PMI with the potential to discriminate between psoriasis patients and controls across different populations, which could be used as a biomarker in the clinical practice. Psoriasis is a chronic, immune-mediated inflammatory skin disease. It ranges in severity from a few scattered red, scaly plaques to involvement of almost the entire body surface 1. Psoriasis is estimated to affect about 2-4% of the population in western countries, causes considerable psychosocial disability and has a major impact on patients' quality of life 2,3. Skin lesions are characterized by angiogenesis, an inflammatory reaction with recruitment of T cells into the skin, hyperproliferation of keratinocytes and altered epidermal differentiation 4. Genetic and environmental factors are implicated in psoriasis, although, the exact etiology of the disease is not fully understood 5,6 .

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“…Segmented filamentous bacteria (SFB) are commensal bacteria widely studied for their immune-modulating properties. Flannigan et al demonstrated that SFB colonization has a potent effect in inducing Th17 differentiation, through the stimulation of IL-23 production in dendritic cells, which in turn can activate type 3 innate lymphoid cells (ILC3) to secrete IL-22 [101] (see Innate Lymphoid Cells May Link Microbiota Changes with T Cell Activation). The activation of IL-23/IL-22/IL-17 axis has been recently recognized as a key moment in the acquisition of the inflammatory activity of autoantibodies: in preclinical RA, this axis modulates the glycosylation pattern [102] (see Secretory Immunoglobulins and Aberrant Glycosylation).…”

Section: Humoral Immunity Abnormalities In At-risk Subjectsmentioning

confidence: 99%

Mucosa–Environment Interactions in the Pathogenesis of Rheumatoid Arthritis

Lucchino

Spinelli

Iannuccelli

et al. 2019

Cells

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Mucosal surfaces play a central role in the pathogenesis of rheumatoid arthritis (RA). Several risk factors, such as cigarette smoking, environmental pollution, and periodontitis interact with the host at the mucosal level, triggering immune system activation. Moreover, the alteration of microbiota homeostasis is gaining increased attention for its involvement in the disease pathogenesis, modulating the immune cell response at a local and subsequently at a systemic level. Currently, the onset of the clinical manifest arthritis is thought to be the last step of a series of pathogenic events lasting years. The positivity for anti-citrullinated protein antibodies (ACPAs) and rheumatoid factor (RF), in absence of symptoms, characterizes a preclinical phase of RA—namely systemic autoimmune phase- which is at high risk for disease progression. Several immune abnormalities, such as local ACPA production, increased T cell polarization towards a pro-inflammatory phenotype, and innate immune cell activation can be documented in at-risk subjects. Many of these abnormalities are direct consequences of the interaction between the environment and the host, which takes place at the mucosal level. The purpose of this review is to describe the humoral and cellular immune abnormalities detected in subjects at risk of RA, highlighting their origin from the mucosa–environment interaction.

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Segmented filamentous bacteria‐induced immune responses: a balancing act between host protection and autoimmunity

Cited by 69 publications

References 80 publications

Antibiotics and Host-Tailored Probiotics Similarly Modulate Effects on the Developing Avian Microbiome, Mycobiome, and Host Gene Expression

Antibiotics and Host-Tailored Probiotics Similarly Modulate Effects on the Developing Avian Microbiome, Mycobiome, and Host Gene Expression

Metagenomic analysis of gut microbiota in non-treated plaque psoriasis patients stratified by disease severity: development of a new Psoriasis-Microbiome Index

Mucosa–Environment Interactions in the Pathogenesis of Rheumatoid Arthritis

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