Broad spectrum antibiotic enrofloxacin modulates contact sensitivity through gut microbiota in a murine model

Strzępa, Anna; Majewska‐Szczepanik, Monika; Lobo, Francis; Li, Wen; Szczepanik, Marian

doi:10.1016/j.jaci.2016.11.052

Cited by 46 publications

(43 citation statements)

References 48 publications

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“…In line with the results from the current study, oral administration of broad-spectrum antibiotic cocktails is often reported to increase the relative abundance of CD4 + Treg cells in small intestine (Ivanov et al, 2008;Ochoa-Repáraz et al, 2009;Ichinohe et al, 2011;Janelsins et al, 2014;Benakis et al, 2016;Nakamura et al, 2016;Strzępa et al, 2017), and to reduce relative abundance of Th1 (Ochoa-Repáraz et al, 2009;Hill et al, 2010) and/or Th17 effector cells (Ivanov et al, 2008;Ochoa-Repáraz et al, 2009;Hill et al, 2010;Janelsins et al, 2014;Benakis et al, 2016). This shift in the balance between Tregs and effector T cells has been shown to reduce severity of multiple autoimmune (Ochoa-Repáraz et al, 2009;Benakis et al, 2016;Nakamura et al, 2016) and allergic diseases (Strzępa et al, 2017). On the other hand, the antibiotic-induced Treg promotion has been shown to prevent the development of proper immune responses to oral vaccination (Hall et al, 2008) and enteric infections (Sekirov and Finlay, 2009;Thackray et al, 2018).…”

Section: Discussionsupporting

confidence: 91%

Short-Term Amoxicillin-Induced Perturbation of the Gut Microbiota Promotes Acute Intestinal Immune Regulation in Brown Norway Rats

et al. 2020

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The intestinal gut microbiota is essential for maintaining host health. Concerns have been raised about the possible connection between antibiotic use, causing microbiota disturbances, and the increase in allergic and autoimmune diseases observed during the last decades. To elucidate the putative connection between antibiotic use and immune regulation, we have assessed the effects of the antibiotic amoxicillin on immune regulation, protein uptake, and bacterial community structure in a Brown Norway rat model. Daily intra-gastric administration of amoxicillin resulted in an immediate and dramatic shift in fecal microbiota, characterized by a reduction of within sample (α) diversity, reduced variation between animals (β diversity), increased relative abundance of Bacteroidetes and Gammaproteobacteria, with concurrent reduction of Firmicutes, compared to a water control group. In the small intestine, amoxicillin also affected microbiota composition significantly, but in a different way than observed in feces. The small intestine of control animals was vastly dominated by Lactobacillus, but this genus was much less abundant in the amoxicillin group. Instead, multiple different genera expanded after amoxicillin administration, with high variation between individual animals, thus the small intestinal α and β diversity were higher in the amoxicillin group compared to controls. After 1 week of daily amoxicillin administration, total fecal IgA level, relative abundance of small intestinal regulatory T cells and goblet cell numbers were higher in the amoxicillin group compared to controls. Several bacterial genera, including Escherichia/Shigella, Klebsiella (Gammaproteobacteria), and Bifidobacterium, for which the relative abundance was higher in the small intestine in the amoxicillin group than in controls, were positively correlated with the fraction of small intestinal regulatory T cells. Despite of epidemiologic studies showing an association between early life antibiotic consumption and later prevalence of inflammatory bowel diseases and food allergies, our findings surprisingly indicated that amoxicillin-induced perturbation of the gut microbiota promotes acute immune regulation. We speculate that the observed increase in relative abundance of small intestinal regulatory T cells is partly mediated by immunomodulatory lipopolysaccharides derived from outgrowth of Gammaproteobacteria.

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Section: Discussionsupporting

confidence: 91%

Short-Term Amoxicillin-Induced Perturbation of the Gut Microbiota Promotes Acute Intestinal Immune Regulation in Brown Norway Rats

et al. 2020

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“…Oral administration of enrofloxacin induced suppression of CHS and altered the gut microbiota composition in mice. Antibiotic treatment resulted in increased levels of Bacteroidetes, Bifidobacterium and Clostridium, while levels of segmented filamentous bacteria were decreased [25]. In our previous study, ciprofloxacin and metronidazole treatments blocked the suppressive activity of dietary SIs on CHS, whereas vancomycin treatment had little effect on their inhibitory activity against CHS [26].…”

Section: Discussionmentioning

confidence: 70%

Dietary soyasaponin attenuates 2,4-dinitrofluorobenzene-induced contact hypersensitivity via gut microbiota in mice

Nagano

Katase

Tsumura

2018

Clinical and Experimental Immunology

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Soyasaponins (SSs) are abundant in soybeans and display inhibitory activity against contact hypersensitivity (CHS), which is often used as a mouse model for allergic contact dermatitis (ACD); however, their therapeutic mechanisms remain unknown. Here, we attempted to clarify the role of gut microbiota in the inhibition of CHS by dietary soyasaponins. For antibiotic treatment, mice were administered a mixture of ciprofloxacin and metronidazole or vancomycin. These antibiotics and SSs were given to mice via drinking water 3-weeks prior to CHS induction with 2,4-dinitrofluorobenzene, and the mice were analysed for ear swelling, tissue oedema, infiltration of Gr-1-positive immune cells, the composition of faecal microbiota and regulatory T (T ) cells. The soyasaponin diets attenuated ear swelling and tissue oedema, and reduced the number of Gr-1-positive cells infiltrating ear tissues. CHS caused changes in the structure of the gut microbiota, but dietary SSs blocked the changes in the microbiota composition. Ciprofloxacin and metronidazole treatments significantly enhanced the severity of CHS symptoms, whereas vancomycin treatment blocked the suppressive effect of dietary SSs on CHS. These antibiotic treatments differed in their effects on the gut microbiota composition. T cells in auricular lymph node and spleen increased under SS-enriched diets, but this increase was blocked by vancomycin treatment. These results suggest that dietary SSs exert their inhibitory activity on CHS via the gut microbiota in mice, suggesting that dietary supplementation with SSs may have beneficial effects on ACD patients, but that the gut microbiota is a critical determinant of the therapeutic value of dietary SSs.

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“…It can be used to treat specific infections and against a broad spectrum of Gram-negative and Gram-positive bacteria in both stationary and growth phases of bacterial replication (Scheer, 1987). Its wide in vivo distribution, unique antimicrobial effect, high bioavailability, less toxicity, and side effects, make it one of the most commonly used antibiotics for treatment of various animal infectious diseases, and a desirable antibiotic choice for difficult-to-treat infections, particularly those that need long-term antibiotic treatment (Divers et al, 2008;Ebert et al, 2011;Reyes-Herrera et al, 2011;Jerjomiceva et al, 2014;Lin et al, 2014;Rico et al, 2014;Andrieu et al, 2015;Nguyen Dang Giang et al, 2015;Phillips et al, 2015;Piras et al, 2015;Carrascosa et al, 2017;Foster et al, 2017;Roth et al, 2017;Strze R pa et al, 2017;Zhu et al, 2017;Rico et al, 2018). The bactericidal activity of enrofloxacin is concentration-dependent, with susceptible bacterial cell death occurring within 20-30 minutes of exposure.…”

Section: Introductionmentioning

confidence: 99%

Formation of inclusion complex of enrofloxacin with 2-hydroxypropyl- β -cyclodextrin

Ding

Pang

Prasad³

et al. 2020

Drug Delivery

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Enrofloxacin, a third-generation fluoroquinolone, is a broad-spectrum antimicrobial drug against a lot of veterinary bacterial diseases. However, bactericidal activity of enrofloxacin is concentration-dependent and its poor aqueous solubility and bitter taste limit its development and application. Meanwhile, 2-hydroxypropyl-b-cyclodextrin (HP-b-CD), a widely used cyclodextrin analog, is a safe and an effective drug carrier. It forms inclusion complexes with its drug substrates and improves their physiochemical and pharmacokinetic properties. Enrofloxacin was also found to form a stable inclusion complex with HP-b-CD and different research groups have shown improved solubility for enrofloxacin by 32.5%, 9.25 and 165-fold. Our own efforts in this direction resulted in manifold improvement (916-fold) in its solubility compared to the previous studies. It was further shown that pharmaceutical properties, absorption and bioavailability, of enrofloxacin have also been significantly improved by complexation with HP-b-CD.

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Broad spectrum antibiotic enrofloxacin modulates contact sensitivity through gut microbiota in a murine model

Abstract: Oral treatment with a broad spectrum antibiotic modifies gut microbiota composition and promotes anti-inflammatory response, suggesting that manipulation of gut microbiota can be a powerful tool to modulate the course of CS.

Cited by 46 publications

References 48 publications

Short-Term Amoxicillin-Induced Perturbation of the Gut Microbiota Promotes Acute Intestinal Immune Regulation in Brown Norway Rats

Short-Term Amoxicillin-Induced Perturbation of the Gut Microbiota Promotes Acute Intestinal Immune Regulation in Brown Norway Rats

Dietary soyasaponin attenuates 2,4-dinitrofluorobenzene-induced contact hypersensitivity via gut microbiota in mice

Formation of inclusion complex of enrofloxacin with 2-hydroxypropyl- β -cyclodextrin

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