<i>Lactobacillus johnsonii</i> N5 from heat stress-resistant pigs improves gut mucosal immunity and barrier in dextran sodium sulfate-induced colitis

Lactobacillus johnsonii N5 from heat stress-resistant pigs improves gut mucosal immunity and barrier in dextran sodium sulfate-induced colitis

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Long Yuan^a, Chuyang Zhu^a, Fang Gu^a^,^b, Miaonan Zhu^a, Jiacheng Yao^a, Cuipeng Zhu^a, Shicheng Li^a, Kun Wang^c, Ping Hu^a, Yunzeng Zhang^c, Demin Cai^a^,^b^,^*, Hao-Yu Liu^a^,^b^,^*

Animal Nutrition | 2023, 15(1) : 210 - 224

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Animal Nutrition | 2023, 15(1): 210-224

• Original Research Article •

Lactobacillus johnsonii N5 from heat stress-resistant pigs improves gut mucosal immunity and barrier in dextran sodium sulfate-induced colitis

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Long Yuan^a, Chuyang Zhu^a, Fang Gu^a^,^b, Miaonan Zhu^a, Jiacheng Yao^a, Cuipeng Zhu^a, Shicheng Li^a, Kun Wang^c, Ping Hu^a, Yunzeng Zhang^c, Demin Cai^a^,^b^,^*, Hao-Yu Liu^a^,^b^,^*

Affiliations

^aCollege of Animal Science and Technology, Yangzhou University, Yangzhou 225009, China

^bJoint International Research Laboratory of Agricultural & Agri-Product Safety, The Ministry of Education of China, Yangzhou University, Yangzhou 225009, China

^cJiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou 225009, China

Published: 2023-12-10 doi: 10.1016/j.aninu.2023.04.012

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Abstract

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Developing effective strategies to prevent diarrhea and associated-gut disorders in mammals has gained great significance. Owing to the many health benefits provided by the commensal microbiota of the intestinal tract, such as against environmental perturbation, we explored the host phenotype-associated microbes and their probiotic potential. Based on the observations that the chronic heat stress-exposed weaned piglets present as heat stress-susceptible (HS-SUS) or heat stress-resistant (HS-RES) individuals, we confirmed the phenotypic difference between the two on growth performance (P < 0.05), diarrhea index (P < 0.001), intestinal heat shock protein 70 (HSP70) regulation (P < 0.01), and inflammatory responses (P < 0.01). By comparing the gut microbiome using 16S rRNA gene sequencing and KEGG functional analysis, we found that Lactobacillus johnsonii exhibited significantly higher relative abundance in the HS-RES piglets than in the HS-SUS ones (P < 0.05). Further experiments using a mouse model for chemical-induced inflammation and intestinal injury demonstrated that oral administration of a representative L. johnsonii N5 (isolated from the HS-RES piglets) ameliorated the clinical and histological signs of colitis while suppressing intestinal pro-inflammatory cytokines TNF-α and IL-6 production (P < 0.05). We found that N5 treatment enhanced tight junction proteins ZO-1 and occludin and cytoprotective HSP70 levels under physiological condition and restored their mucosal expressions in colitis (P < 0.05). In support of the high production of the anti-inflammatory cytokine IL-10, N5 promoted the intestinal Peyer's patches MHCII⁺ and CD103⁺ dendritic cell populations (P < 0.05), increased the regulatory T (Treg) cell numbers (P < 0.05), and decreased the Th17 population and its IL-17a production under physiological condition and during colitis (P < 0.01). Our results shed light on understanding the interaction between commensal Lactobacillus and the host health, and provide L. johnsonii N5 as an alternative to antibiotics for preventing diarrhea and intestinal diseases.

Key words

Lactobacillus johnsonii / Probiotic / Heat shock protein / Diarrhea / Heat stress / Treg/Th17

Cite this Article

Long Yuan, Chuyang Zhu, Fang Gu, Miaonan Zhu, Jiacheng Yao, Cuipeng Zhu, Shicheng Li, Kun Wang, Ping Hu, Yunzeng Zhang, Demin Cai, Hao-Yu Liu. Lactobacillus johnsonii N5 from heat stress-resistant pigs improves gut mucosal immunity and barrier in dextran sodium sulfate-induced colitis[J]. Animal Nutrition, 2023 , 15 (1) : 210 -224 . DOI: 10.1016/j.aninu.2023.04.012

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Year 2023 volume 15 Issue 1

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Article Info

doi: 10.1016/j.aninu.2023.04.012

Receive Date：2023-02-06
Online Date：2026-02-03
Published：2023-12-10

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History

Received：2023-02-06
Revised：2023-03-21
Accepted：2023-04-06

Affiliations

^aCollege of Animal Science and Technology, Yangzhou University, Yangzhou 225009, China

^bJoint International Research Laboratory of Agricultural & Agri-Product Safety, The Ministry of Education of China, Yangzhou University, Yangzhou 225009, China

^cJiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou 225009, China

Corresponding:

^* Corresponding authors. E-mail addresses: demincai@yzu.edu.cn (D. Cai)

Haoyu.liu@yzu.edu.cn (H.-Y. Liu).

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表12种不同金属材料的力学参数

科 Family	属数 Number of genus	种数 Number of species	占总种数比例 Percentage of total species (%)	属 Genus	种数 Number of species	占总种数比例 Percentage of total species (%)
鹅膏菌科Amanitaceae	2	11	5.26	鹅膏菌属 Amanita	10	4.78
小菇科 Mycenaceae	2	12	5.74	丝盖伞属 Inocybe	5	2.39
多孔菌科 Polyporaceae	8	14	6.70	蜡蘑属 Laccaria	5	2.39
红菇科 Russulaceae	3	23	11.00	小皮伞属 Marasmius	6	2.87
				小菇属 Mycena	11	5.26
				光柄菇属 Pluteus	5	2.39
				红菇属 Russula	17	8.13
				栓菌属 Trametes	5	2.39

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