Can Gut Microbiota Affect Dry Eye Syndrome?

Jayoon Moon, Chang Ho Yoon, Se Hyun Choi, Mee Kum Kim, Jayoon Moon, Chang Ho Yoon, Se Hyun Choi, Mee Kum Kim

Abstract

Using metagenomics, continuing evidence has elicited how intestinal microbiota trigger distant autoimmunity. Sjögren's syndrome (SS) is an autoimmune disease that affects the ocular surface, with frequently unmet therapeutic needs requiring new interventions for dry eye management. Current studies also suggest the possible relation of autoimmune dry eye with gut microbiota. Herein, we review the current knowledge of how the gut microbiota interact with the immune system in homeostasis as well as its influence on rheumatic and ocular autoimmune diseases, and compare their characteristics with SS. Both rodent and human studies regarding gut microbiota in SS and environmental dry eye are explored, and the effects of prebiotics and probiotics on dry eye are discussed. Recent clinical studies have commonly observed a correlation between gut dysbiosis and clinical manifestations of SS, while environmental dry eye portrays characteristics in between normal and autoimmune. Moreover, a decrease in both the Firmicutes/Bacteroidetes ratio and genus Faecalibacterium have most commonly been observed in SS subjects. The presumable pathways forming the "gut dysbiosis-ocular surface-lacrimal gland axis" are introduced. This review may provide perspectives into the link between the gut microbiome and dry eye, enhance our understanding of the pathogenesis in autoimmune dry eye, and be useful in the development of future interventions.

Keywords: Sjögren’s syndrome; dry eye; dysbiosis; gut microbiota; ocular surface.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
The major interplay pathways between gut microbiota and innate immune cells. (A) Epithelial interleukin (IL)-18 orchestrates to produce antimicrobial peptide and mucus. (B) CX3CR1+ dendritic cells prime natural killer (NK) cells fighting against enteric pathogens. (C) Group 3 innate lymphoid cells (ILC3s) produce IL-22 mediated by IL-1β and IL-23 from CD103+ or CX3CR1+ dendritic cells after sensing flagellin or segmented filamentous bacteria. IL-22 modulates epithelial cells to produce antimicrobial peptides and to stimulate surface fucosylation. (D) ILC2s produce IL-5, IL13, and amphiregulin to promote the growth of epithelial cells. (E) The microbiota affects the myelopoiesis in bone marrow, and the migration and phenotypes of circulating or tissue-resident myeloid cells. (Modified from the study by Thaiss et al. [27]).
Figure 2
Figure 2
The major interplay pathways between gut microbiota and adaptive immune cells. (A) Ig A-producing plasma cells are activated by T follicular helper (TFH) cell-dependent or TFH cell-independent pathways. Segmented filamentous bacteria (SFB), Mucispirillum, Clostridium scindens, and Akkermansia muciniphila can generate TFH cell-dependent- Ig A+ plasma cells. Microbiota-primed group 3 innate lymphoid cells (ILC-3s) interact with dendritic cells (DCs) through Lymphotoxin (LT)α and LTβ. The activated DCs promote TFH cell-independent Ig A production mediated by B-cell activating factor (BAFF) and a proliferation-inducing ligand (APRIL). (B) Regulatory T (Treg) cells can be elicited by short-chain fatty acids (SCFAs), which are produced from dietary fibers by clusters IV, XIVa and XVIII of Clostridia or by polysaccharides from certain Bacteroides (Phylum: Bacteroidetes), such as B. fragilis, B. theta and B. cacae, and Bifidobacterium bifidum (Phylum: Actinobacteria). Lactobacillus reuteri and L. murinus (Phylum: Firmicutes) can also induce Treg cells. ILC-3s through GM-CSF, and CD103+ DCs through transforming growth factor (TGF)-β and IL-10 may interact with Treg cell induction. (C) SFB can elicit physiologic TH17 cell induction whereas Citrobacter rodentium can induce pathogenic TH17 cell induction. ILC-3s and CXCR1+ dendritic cells facilitate induction of TH17 cells. Upon the abundance of IL-23 and IL-1β under the environment with higher concentrations of salt, long-chain fatty acids, and saturated fatty acids, pathogenic TH17 cells secrete interferon (IFN)-γ and granulocyte–macrophage colony-stimulating factor (GM-CSF). (Modified from the study by Honda and Littman [29]).
Figure 3
Figure 3
The hypothesis of Gut dysbiosis–Ocular surface–Lacrimal gland Axis. Gut dysbiosis may induce dry eye disease by the following five mechanisms. Myeloid cell migration theory; Gut dysbiosis-mediated CD103+ or CXCR1+ dendritic cells or monocyte/macrophages migrate to drainage lymph nodes, ocular surface and lacrimal glands in order to prime T cells or secrete pro-inflammatory cytokines. Effector lymphocyte imprint theory; Gut-derived helper T 1 (TH1) and 17 (TH17) cells migrate to the ocular surface and lacrimal gland, or gut-derived Treg cells are less circulated. Molecular mimicry theory; Microbial-derived antigens cross-prime autoreactive CD4+ T cells helping B cells to produce autoantibodies. Metabolite circulation theory; Microbial metabolites, such as short-chain fatty acids, decrease to enter systemic circulation reaching ocular surface and lacrimal gland. Neuropeptide circulation theory; Homeostatic circulation of gut-derived neuropeptides is distributed to reach lacrimal gland and influence tear secretion.

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