Administration of Lactobacillus reuteri Combined with Clostridium butyricum Attenuates Cisplatin-Induced Renal Damage by Gut Microbiota Reconstitution, Increasing Butyric Acid Production, and Suppressing Renal Inflammation

Hsiao, Yu-Ping; Chen, Hsiao-Ling; Tsai, Jen-Ning; Lin, Meei-Yn; Liao, Jiunn-Wang; Wei, Meng-Syuan; Ko, Jiunn-Liang; Ou, Chu-Chyn

doi:10.3390/nu13082792

Open AccessArticle

Administration of Lactobacillus reuteri Combined with Clostridium butyricum Attenuates Cisplatin-Induced Renal Damage by Gut Microbiota Reconstitution, Increasing Butyric Acid Production, and Suppressing Renal Inflammation

by

Yu-Ping Hsiao

^1,2,

Hsiao-Ling Chen

³,

Jen-Ning Tsai

^4,5

,

Meei-Yn Lin

⁶,

Jiunn-Wang Liao

⁷

,

Meng-Syuan Wei

⁶,

Jiunn-Liang Ko

^1,8,*,†

and

Chu-Chyn Ou

^9,10,*,†

¹

Institute of Medicine, Chung Shan Medical University, Taichung 40201, Taiwan

²

Department of Dermatology, Chung Shan Medical University Hospital, Taichung 40201, Taiwan

³

Department of Food, Nutrition and Health Biotechnology, Asia University, Taichung 41354, Taiwan

⁴

Department of Medical Laboratory and Biotechnology, Chung Shan Medical University, Taichung 40201, Taiwan

⁵

Clinical Laboratory, Chung Shan Medical University Hospital, Taichung 40201, Taiwan

⁶

Department of Food Science and Biotechnology, National Chung Hsing University, Taichung 40227, Taiwan

⁷

Graduate Institute of Veterinary Pathobiology, National Chung Hsing University, Taichung 40227, Taiwan

⁸

Department of Medical Oncology and Chest Medicine, Chung Shan Medical University Hospital, Taichung 40201, Taiwan

⁹

Department of Nutrition, Chung Shan Medical University Hospital, Taichung 40201, Taiwan

¹⁰

Department of Nutrition, Chung Shan Medical University, Taichung 40201, Taiwan

^*

Authors to whom correspondence should be addressed.

^†

These authors contributed equally to this work.

Nutrients 2021, 13(8), 2792; https://doi.org/10.3390/nu13082792

Submission received: 9 July 2021 / Revised: 28 July 2021 / Accepted: 9 August 2021 / Published: 15 August 2021

(This article belongs to the Topic Probiotics, Prebiotics and Postbiotics in Human Health)

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Abstract

Cisplatin-induced nephrotoxicity is associated with gut microbiota disturbance. The present study aimed to investigate whether supplementation of Lactobacillus reuteri and Clostridium butyricum (LCs) had a protective effect on cisplatin-induced nephrotoxicity through reconstruction of gut microbiota. Wistar rats were given different treatments: control, cisplatin (Cis), cisplatin + C. butyricum and L. reuteri (Cis+LCs), and C. butyricum and L. reuteri (LCs). We observed that cisplatin-treated rats supplemented with LCs exhibited significantly decreased renal inflammation (KIM-1, F4/80, and MPO), oxidative stress, fibrosis (collagen IV, fibronectin, and a-SMA), apoptosis, concentration of blood endotoxin and indoxyl sulfate, and increased fecal butyric acid production compared with those without supplementation. In addition, LCs improved the cisplatin-induced microbiome dysbiosis by maintaining a healthy gut microbiota structure and diversity; depleting Escherichia-Shigella and the Enterobacteriaceae family; and enriching probiotic Bifidobacterium, Ruminococcaceae, Ruminiclostridium_9, and Oscillibacter. Moreover, the LCs intervention alleviated the cisplatin-induced intestinal epithelial barrier impairment. This study indicated LCs probiotic serves as a mediator of the gut–kidney axis in cisplatin-induced nephrotoxicity to restore the intestinal microbiota composition, thereby suppressing uremic toxin production and enhancing butyrate production. Furthermore, the renoprotective effect of LCs is partially mediated by increasing the anti-inflammatory effects and maintaining the integrity of the intestinal barrier.

Keywords: cisplatin; nephrotoxicity; Clostridium butyricum; Lactobacillus reuteri; Escherichia-Shigella

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MDPI and ACS Style

Hsiao, Y.-P.; Chen, H.-L.; Tsai, J.-N.; Lin, M.-Y.; Liao, J.-W.; Wei, M.-S.; Ko, J.-L.; Ou, C.-C. Administration of Lactobacillus reuteri Combined with Clostridium butyricum Attenuates Cisplatin-Induced Renal Damage by Gut Microbiota Reconstitution, Increasing Butyric Acid Production, and Suppressing Renal Inflammation. Nutrients 2021, 13, 2792. https://doi.org/10.3390/nu13082792

AMA Style

Hsiao Y-P, Chen H-L, Tsai J-N, Lin M-Y, Liao J-W, Wei M-S, Ko J-L, Ou C-C. Administration of Lactobacillus reuteri Combined with Clostridium butyricum Attenuates Cisplatin-Induced Renal Damage by Gut Microbiota Reconstitution, Increasing Butyric Acid Production, and Suppressing Renal Inflammation. Nutrients. 2021; 13(8):2792. https://doi.org/10.3390/nu13082792

Chicago/Turabian Style

Hsiao, Yu-Ping, Hsiao-Ling Chen, Jen-Ning Tsai, Meei-Yn Lin, Jiunn-Wang Liao, Meng-Syuan Wei, Jiunn-Liang Ko, and Chu-Chyn Ou. 2021. "Administration of Lactobacillus reuteri Combined with Clostridium butyricum Attenuates Cisplatin-Induced Renal Damage by Gut Microbiota Reconstitution, Increasing Butyric Acid Production, and Suppressing Renal Inflammation" Nutrients 13, no. 8: 2792. https://doi.org/10.3390/nu13082792

APA Style

Hsiao, Y.-P., Chen, H.-L., Tsai, J.-N., Lin, M.-Y., Liao, J.-W., Wei, M.-S., Ko, J.-L., & Ou, C.-C. (2021). Administration of Lactobacillus reuteri Combined with Clostridium butyricum Attenuates Cisplatin-Induced Renal Damage by Gut Microbiota Reconstitution, Increasing Butyric Acid Production, and Suppressing Renal Inflammation. Nutrients, 13(8), 2792. https://doi.org/10.3390/nu13082792

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Administration of Lactobacillus reuteri Combined with Clostridium butyricum Attenuates Cisplatin-Induced Renal Damage by Gut Microbiota Reconstitution, Increasing Butyric Acid Production, and Suppressing Renal Inflammation

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