Recent advances in systemic lupus erythematosus and microbiota: from bench to bedside

doi:10.1007/s11684-022-0957-7

Front. Med.

2022, Vol. 16

Issue (5) : 686-700 https://doi.org/10.1007/s11684-022-0957-7

REVIEW

Recent advances in systemic lupus erythematosus and microbiota: from bench to bedside

Yijing Zhan¹, Qianmei Liu¹, Bo Zhang¹, Xin Huang²(

), Qianjin Lu¹(

)

¹. Key Laboratory of Basic and Translational Research on Immune-Mediated Skin Diseases, Chinese Academy of Medical Sciences, Jiangsu Key Laboratory of Molecular Biology for Skin Diseases and STIs, Institute of Dermatology, Chinese Academy of Medical Sciences and Peking Union Medical College, Nanjing 210042, China
². Department of Dermatology, The Second Xiangya Hospital of Central South University, Institute of Dermatology and Venereology of Central South University, Hunan Clinical Medicine Research Center for Major Skin Diseases and Skin Health, Changsha 410011, China

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Abstract

Systemic lupus erythematosus (SLE) is a complicated autoimmune disease affecting multiple systems and organs. It is highly heterogeneous, and it preferentially affects women at childbearing age, causing worldwide social burden. The pathogenesis of SLE mostly involves genetic predisposition, epigenetic dysregulation, overactivation of the immune system, and environment factors. Human microbiome, which is mostly composed of microbiota colonized in the gut, skin, and oral cavity, provides a natural microbiome barrier against environmental risks. The past decade of research has demonstrated a strong association between microbiota and metabolic diseases or gastrointestinal diseases. However, the role of microbiota in autoimmunity remains largely unknown until recently, when the technological and methodological progress facilitates further microbiota research in SLE. In this review, the latest research about the role and mechanisms of microbiota in SLE and the advances in the development of diagnostic and therapeutic strategies based on microbiota for SLE were summarized.

Keywords systemic lupus erythematosus microbiota biotherapy

Corresponding Author(s): Xin Huang,Qianjin Lu

Just Accepted Date: 23 September 2022 Online First Date: 27 October 2022 Issue Date: 18 November 2022

Cite this article:

Yijing Zhan,Qianmei Liu,Bo Zhang, et al. Recent advances in systemic lupus erythematosus and microbiota: from bench to bedside[J]. Front. Med., 2022, 16(5): 686-700.

URL:

https://academic.hep.com.cn/fmd/EN/10.1007/s11684-022-0957-7
https://academic.hep.com.cn/fmd/EN/Y2022/V16/I5/686

Human subjects (n)	Region	Colonization site	Bacteria in SLE	Reference
SLE (20) vs. HC (20)	Spain	Gut	Phyla: Firmicutes/Bacteroidetes ratio ↓; Firmicutes ↓	[25]
SLE (20) vs. HC (20)	Spain	Gut	Phyla: Firmicutes/Bacteroidetes ratio, Synergistetes ↓	[29]
SLE (16) vs. HC (14)	China	Gut	Phyla: Proteobacteria ↑Family: Enterobacterlaceae ↑; Ruminococcaceae, Prevotellaceae, Clostridiales ↓	[30]
SLE (45) vs. HC (48)	China	Gut	Phyla: Bacteroidetes, Actinobacteria, Proteobacteria ↑; Firmicutes/Bacteroidetes ratio, Firmicutes ↓Genus: Rhodococcus, Eggerthella, Klebsiella, Prevotella, Eubacterium, Flavonifractor↑; Dialister, Pseudobutyrivibrio↓	[31]
SLE (20) vs. HC (20)	Egypt	Gut	Phyla: Firmicutes/Bacteroidetes ↓Genus: Lactobacillus↓	[32]
SLE (32) vs. HC (26)	China	Gut	Phyla: Bifidobacterium, Firmicutes/Bacteroidetes ratio↓; Enterobacteriaceae ↑Family: Sartiphaea,Plavococcus ↓; Veillonella, Enterococci ↑Genus: Sartiphaea, Plavococcus↓; Enterococcus, Veillonella↑	[33]
SLE (14) vs. HC (17)	USA	Gut	Gram-negative bacteria ↑Phyla: Firmicutes/Bacteroidetes ratio was not different; Rikenellaceae, Proteobacteria ↑Genus: Odoribacter↓, Blautia↑	[34]
SLE (61) vs. HC (17)	USA	Gut	Species: Ruminococcus gnavus↑	[35]
SLE (40) vs. HC (22)	China	Gut	Genus: Streptococcus, Campylobacter, Veillonella↑; Bifidobacterium ↓Species: Streptococcus anginosus , Veillonella dispar↑	[36]
SLE-G (17) vs. SLE + G (20) + HC (20)	China	Gut	Phyla: Bacteroidetes↓; Firmicutes/Bacteroidetes ratio ↑	[40]
SLE (33) vs. HC (28)	China	Gut	Phyla: Proteobacteria↑Family: Ruminococcaceae, Christensenellaceae, Akkermansiaceae, Ruminococcaceae↓; Enterobacteriaceae↑ Genus: Gammaproteobacteria, Bacilli, Escherichia, Shigella, Lachnoclostridium, Kluyvera↑; Agathobacter, Ruminococcus, Coprococcus, Dialister, Faecalibacterium, and Subdoligranulum↓Species: Ruminococcus gnavus↑; Eubacterium coprostanoligenes↓	[41]
SLE (21) vs. HC (25)	Spain	Gut	Phyla: Firmicutes/Bacteroidetes ratio ↓	[44]
SLE (21) vs. HC (21)	Spain	Gut	Phyla: The serum malondialdehyde was inverse correlations with Cyanobacteria and Firmicutes and positive with Actinobacteria; the C reactive protein was positive association with Lentisphaerae, Proteobacteria, and Verrucomicrobia	[45]
SLE (27) vs. HC (27)	Australia	Gut	Family: Coriobacteriaceae, Enterobacteriaceae ↑Genus: Bifidobacterium, Ruminiclostridium, Streptococcus, Collinsella↑; Lachnoclostridium, Lachnospira, and Sutterella↓	[47]
SLE (47) vs. HC (203)	Japan	Gut	Species: Streptococcus intermedius, Streptococcus anginosus↑	[48]
SLE (117) vs. HC (115)	China	Gut	Genus: Desulfovibrio↓; Blautia↑Species: Clostridium species ATCC BAA-442, Atopobium rimae, Shuttleworthia satelles, Actinomyces massiliensis, Bacteroides fragilis, Clostridium leptum↑	[49]
SLE (30) vs. HC (965)	Netherlands	Gut	Phyla: Firmicutes/Bacteroidetes ratio ↓; Bacteroidetes, Proteobacteria ↑Genus: Bacteroides, Alistipes↑Species: Bacteroides vulgatus, Bacteroides uniformis, Bacteroides ovatus, Bacteroides thetaiotaomicron↑	[57]
SLE (35) vs. HC (35)	China	Gut	Family: Ruminococcaceae ↓Genus: Lactobacillus, Prevotella, Blautia, Ruminococcus↑; Bifidobacterium↓Species: Lactobacillus iners↑; Bifidobacterium adolescentis, Bifidobacterium longum↓	[64]
SLE (16) vs. HC (11)	USA	Gut	Phyla: Firmicutes/Bacteroidetes ratio ↓	[71]
SLE (12) vs. HC (22)	USA	Gut	Species: Lactobacillus spp. ↑	[72]
SLE (92) vs. HC (217)	China	Gut	Phyla: Bacteroidetes, Proteobacteria, and Actinobacteria ↑; Firmicutes ↓Family: Bacteroidaceae, Streptococcaceae ↑; Ruminococcaceae, Veillonellaceae, Lachnospiraceae ↓Genus: Ruminococcus, Klebsiella, Erysipelotrichaceae↑; Faecalibacterium↓	[73]
SLE (69) vs. HC (49)	China	Skin	Phyla: Firmicutes, Acidobacteria, Gemmatimonadetes, and Tenericutes ↑Genus: Corynebacterium, Staphylococcus, Rothia, Actinomyces, Deinococcus↑; Prevotella, Cutibacterium, Rhodococcus, Klebsiella↓Species: Staphylococcus aureus, Staphylococcus epidermidis, Staphylococcus hominis↑; Klebsiella pneumoniae, Rhodococcus erythropolis, Erwinia mallotivora↓	[12]
SLE (20) vs. HC (20)	China	Skin	Phyla: Firmicutes, Bacteroidetes, Spirochaetae, Verrucomicrobia, Tenericutes↑; Actinobacteria and Armatimonadetes ↓Class: Alphaproteobacteria ↓Order: Sphingomonadales ↓Family: Acetobacteraceae, Sphingomonadaceae, Phyllobacteriaceae ↓; Christensenellaceae, Erysipelotrichaceae, Methylocystaceae, Burkholderiaceae, and Verrucomicrobiaceae↑Genus: Nevskia, Stenotrophomonas, Phyllobacterium, Novosphingobium↓; Barnesiella, Acinetobacter↑Species: Chryseobacterium taiwanense, Nevskia aquatilis↓; Corynebacterium matruchotii, Ruminococcus sp. 5_1_39BFAA ↑Compared with non-rash region of SLE, genus in the rash region: Halomonas↑; Pelagibacterium, Novosphingobium, Curvibacter↓	[56]
SLE (117) vs. HC (115)	China	Oral	Species: Clostridium species ATCC BAA-442, Atopobium rimae, Shuttleworthia satelles, Actinomyces massiliensis, Bacteroides fragilis, Clostridium leptum↑	[49]
SLE (30) vs. HC (965)	Netherlands	Oral	Genus: Actinomyces↓; Lactobacillu↑	[57]
Anti-Ro⁺ mothers of neonatal lupus children (25) vs. HC (7)	USA	Oral	Phyla: Proteobacteria ↓; Actinobacteria, Firmicutes, Bacteroidetes ↑Class: Coriobacteriia, Bacilli, Negativicutes↑; Betaproteobacteria ↓Order: Neisseriale ↓Family: Neisseriaceae ↓Genus: Streptococcus, Veillonella↑; Neisseria↓	[59]
SLE (52) vs. HC (52)	Brazil	Oral	Genus: Fretibacterium, Selenomonas↑Species: Prevotella nigrescens↑	[60]
SLE-A (31) vs. SLE-I (29) + HC (31)	USA	Oral	Species in SLE-A: Treponema denticola, Tannerella forsythia↑; Capnocytophaga gingivalis, Streptococcus gordonii, Prevotella nigrescens, Capnocytophaga ochracea, Fusobacterium nucleatum, Streptococcus sanguinis↓	[61]
SLE (35) vs. HC (35)	China	Oral	Genus: Streptococcus↓; Prevotella, Selenomonas, Veillonella↑Species: Streptococcus anginosus↓	[64]

Tab.1 Microbiota alternation in patients with SLE

Fig.1 Role of skin–gut axis in SLE. The host skin and gut microbiota are linked via metabolic pathways. Genetic, environment, and hormonal factors affect the composition of skin and gut microbiota through the innate and adaptive immune responses. The activation of TLR7/8 was induced by specific gut bacteria, such as Enterococcus gallisepticum. The translocation of E. gallisepticum resulted in the activation of the aryl hydrocarbon receptor (AhR) system, which enhanced the activation and differentiation of Th17 and follicular helper T (Tfh) cells and autoantibody production. In the lamina propria of the small intestine, E. gallisepticum could also induce an increase in pDCs that produce IFN-α. In addition, reduction in Paenibacillus genus may lead to elevated lipopolysaccharide and increased expression of TLR4 in the vasculature, leading to increased NADPH oxidase-dependent superoxide production, inflammation, and endothelial dysfunction. Along with the activation of the innate immune response, bacteria such as Odoribacter splanchnicus could activate the adaptive immune response by increasing the secretion of IFN-γ and IL-17A. The proportion of Ruminococcus and Lactobacillus was positively correlated with the absolute count of Treg lymphocytes. When T and B cells are overactivated, autoantibodies such as ANA and dsDNA are produced, and high-avidity IgA (sIgA) is secreted. The immune complex deposited on skin, intestine, and other organs and inflammatory cytokines, such as IL-17, IFN-γ, and IL-6, were released, resulting in organ damage. The relationship between skin microbiota and SLE remains to be elusive, even though studies have shown that certain bacteria strains, such as Staphylococcus and Corynebacterium, increased in the skin of patients with SLE. Some research showed that superficial colonization of Staphylococcus epidermidis may induce the elevation of IL17A producing CD8⁺ T cell. SLE, systemic lupus erythematosus; TLR7/8, Toll-like receptor 7/8; Th17, T helper 17; IFN-α, interferon-α; pDC, plasmacytoid dendritic cells; IFN-γ, interferon-γ; IL-17A, interleukin-17A; IL-6, interleukin-6.

Microecological agents	Intervention	Models	Mode of administration	Effects	Reference
Probiotics	Lactobacillus oris (F0423), Lactobacillus rhamnosus (LMS201), Lactobacillu reuteri (CF48-3A), Lactobacillu johnsonii (135-1-CHN), and Lactobacillu gasseri (JV-V03)	MRL/lpr	Oral gavage, 3 W to dissection	“leaky gut,” IL-6, IgG2a ↓; IL-10 ↑	[61]
	Lactobacillus fermentum CECT5716	NZB/W F1	Oral gavage, 15 W	B and T cell, lymphocytes, IL-17α, IFN-γ, TNF-α, IL-21 ↓	[84]
	Lactobacillus fermentum CECT5716 and/or Bifidobacterium breve CECT7263	Imiquimod-induced lupus model	Oral gavage, 8–16 W	SLE activity and vascular inflammation ↓	[85]
	Lactobacillus paracasei GMNL-32, Lactobacillus reuteri GMNL-89, and Lactobacillus reuteri GMNL-263	NZB/W F1	Oral gavage, 8–20 W	IL-1β, IL-6, and TNF-α ↓	[86]
	Lactobacillus reuteri GMNL-263	NZB/W F1	Oral gavage, 16–28 W	TUNEL-positive cells, Fas death receptor-related components, apoptosis ↓	[87]
	Lactobacillus delbrueckii PTCC 1743 and Lactobacillus rhamnosus ATCC 9595	Pristane-induced lupus model	Oral gavage, 2–6 M	Th17, Th1, CTL, IFN-γ, IL-17 ↓	[90]
	Lactobacillus delbrueckii and Lactobacillus rhamnosus	Pristane-induced lupus model	Oral gavage, 0–6 M	Tregs, Foxp3 ↑; lipogranuloma, ANA, anti-dsDNA, IL-6 ↓	[91]
Dietary deviations	Resistant starch	TLR7.1 Tg, TLR7 KO, and C57BL/6 mice	Oral gavage, 7 W	Lactobacillus reuteri, pDCs, interferon pathways, organ involvement, mortality ↓	[72]
	Regular diet	Patients with SLE (20) vs. HC (20)	Diet	Orange intake was directly associated with Lactobacillus and apple intake was associated with Bifidobacterium in SLE, whilst red wine was the best contributor to Faecalibacterium variation	[92]
	Autoclaved neutral pH (7.0–7.2) water vs. acidic pH (3.0–3.2) water	(SWR×NZB) F1	Oral gavage, to dissection	Simple dietary deviations, such as pH of drinking water, influenced lupus incidence and affected the composition of gut microbiome	[93]
	Low fiber vs. normal fiber	NZB/W F1 mice	Oral gavage, 4 W to dissection	Low fiber diet is related with overall survival ↓; CD44, IFN-γ, IL-10, Treg, effector Treg, Tfh ↑	[95]
Microbiota transplant	Fecal microbiota transplantation	C57BL/6J, TC (SLE mice)	Fecal gavage, once every other day for 10 days	ds-DNA antibody in germ free mice after FMT from SLE mice ↑	[100]
Microbiota transplant	Fecal microbiota transplantation	MRL/lpr	Oral gavage, 2 W antibiotics, 4W fecal suspensions	Lupus severity and progression ↓	[101]

Tab.2 Application of microecological agents in the treatment of SLE in vivo

Fig.2 Current microbial interventions and therapies in SLE. The dysbiosis of the gut, skin, and oral microbiota plays an important role in the occurrence and development of SLE. Biological therapies of SLE, including probiotics, dietary deviations, and fecal microbiota transplant (FMT) alleviated SLE through the regulation of microbiota. The currently reported probiotics mainly include Lactobacillus and Bifidobacterium, and the dietary deviations mainly include the intake of fiber, wine, and fruit. FMT and miniFMT that selects specific intestinal bacterial strains for colonization appeared to be a promising therapy for lupus.

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