罗伊氏黏液乳杆菌通过抑制ROS依赖性NLRP3炎性通路缓解大鼠肠缺血/再灌注损伤

doi:10.11843/j.issn.0366-6964.2024.09.042

Abstract

Abstract:

The aim of this study is to explore the mechanism of Limosilactobacillus reuteri (LR) improving intestinal ischemia-reperfusion injury (IR) using ROS/NLRP3 inflammasome as a starting point. The IR cell model was constructed using hypoxia/reoxygenation methods, and the rat IR model was constructed using microarterial clamping/perfusion methods. The cell experiment was divided into four groups: control group, IR group, LR pre-treatment group (LR+IR group), and LR group. The animal experiment was divided into three groups (10 rats in each group): sham surgery group (S group), IR group, and LR gavage treatment group (LR+IR group). The level of ROS, the expression of NLRP3 inflammasome related proteins (NLRP3, ASC, Caspase p10, and GSDMD), the levels of inflammation-related indicators, and the content of oxidative stress related indicators in each group were detected. Histopathological evaluation was also performed. The results showed that: 1) LR attenuates IR induced oxidative stress and NLRP3 inflammasome activation. 2) LR alleviates NLRP3 inflammasome activation by attenuating ROS expression. 3) LR could alleviate intestinal injury and the expression of inflammatory factors induced by IR. In summary, LR can alleviate intestinal IR and oxidative stress in rats, and its mechanism of action is related to the inhibition of ROS dependent NLRP3 inflammasome, providing experimental basis for the veterinary clinical treatment of LR in intestinal related diseases.

Key words: Limosilactobacillus reuteri, intestinal ischemia-reperfusion injury, reactive oxygen species, NLRP3 inflammasome

CLC Number:

S854.1615

Ya 'nan LI, Tianwen MA, Xiaoyu YANG, Jiaxin WU, Xiaoping LÜ, Hao REN, Hongri RUAN, Ying LIU, Jiantao ZHANG, Chengwei WEI. Limosilactobacillus reuteri Alleviates Intestinal Ischemia/Reperfusion Injury in Rats by Inhibiting the ROS Dependent NLRP3 Inflammatory Pathway[J]. Acta Veterinaria et Zootechnica Sinica, 2024, 55(9): 4186-4195.

Figures/Tables 7

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References 32

1	HOU M , CHEN F , HE Y , et al. Dexmedetomidine against intestinal ischemia/reperfusion injury: a systematic review and meta-analysis of preclinical studies[J]. Eur J Pharmacol, 2023, 959, 176090. doi: 10.1016/j.ejphar.2023.176090
2	ZHOU P , ZHANG S , WANG M H , et al. The induction mechanism of ferroptosis, necroptosis, and pyroptosis in inflammatory bowel disease, colorectal cancer, and intestinal injury[J]. Biomolecules, 2023, 13 (5): 820. doi: 10.3390/biom13050820
3	ACOSTA S . Epidemiology of mesenteric vascular disease: clinical implications[J]. Semin Vasc Surg, 2010, 23 (1): 4- 8. doi: 10.1053/j.semvascsurg.2009.12.001
4	WEN J , XU B , SUN Y C , et al. Paeoniflorin protects against intestinal ischemia/reperfusion by activating LKB1/AMPK and promoting autophagy[J]. Pharmacol Res, 2019, 146, 104308. doi: 10.1016/j.phrs.2019.104308
5	SENDA A , KOJIMA M , WATANABE A , et al. Profiles of lipid, protein and microRNA expression in exosomes derived from intestinal epithelial cells after ischemia-reperfusion injury in a cellular hypoxia model[J]. PLoS One, 2023, 18 (3): e0283702. doi: 10.1371/journal.pone.0283702
6	GUTIÉRREZ-SÁNCHEZ G , GARCÍA-ALONSO I , DE SANTA MARÍA J G , et al. Antioxidant-based therapy reduces early-stage intestinal ischemia-reperfusion injury in rats[J]. Antioxidants (Basel), 2021, 10 (6): 853. doi: 10.3390/antiox10060853
7	CHEN J Y , WANG Y , SHI Y X , et al. Association of gut microbiota with intestinal ischemia/reperfusion injury[J]. Front Cell Infect Microbiol, 2022, 12, 962782. doi: 10.3389/fcimb.2022.962782
8	BÄCKHED F , LEY R E , SONNENBURG J L , et al. Host-bacterial mutualism in the human intestine[J]. Science, 2005, 307 (5717): 1915- 1920. doi: 10.1126/science.1104816
9	周敏, 汪凯歌, 张濂, 等. 微生物-肠-肌轴调节骨骼肌代谢和功能的研究进展[J]. 畜牧兽医学报, 2022, 53 (9): 2845- 2857.
	ZHOU M , WANG K G , ZHANG L , et al. Advances in microbiota-gut-muscle axis regulating skeletal muscle metabolism and function[J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53 (9): 2845- 2857.
10	WANG F , LI Q R , WANG C Y , et al. Dynamic alteration of the colonic microbiota in intestinal ischemia-reperfusion injury[J]. PLoS One, 2012, 7 (7): e42027. doi: 10.1371/journal.pone.0042027
11	WANG X , LIU H L , LI Y F , et al. Altered gut bacterial and metabolic signatures and their interaction in gestational diabetes mellitus[J]. Gut Microbes, 2020, 12 (1): 1840765. doi: 10.1080/19490976.2020.1840765
12	SAVIGAMIN C , SAMUTHPONGTORN C , MAHAKIT N , et al. Probiotic as a potential gut microbiome modifier for stroke treatment: a systematic scoping review of in vitro and in vivo studies[J]. Nutrients, 2022, 14 (17): 3661. doi: 10.3390/nu14173661
13	MÁRQUEZ C M , ÁLVAREZ P F , DELGADO T V , et al. Randomized, double-blind, placebo-controlled clinical trial on the usefulness of probiotic Lactobacillus reuteri in bismuth-containing quadruple eradication therapy for infection with helicobacter pylori[J]. Rev Esp Enferm Dig, 2022, 114 (2): 89- 95.
14	CHEN F Y , LEE M T , HUANG H W . Sigmoidal concentration dependence of antimicrobial peptide activities: a case study on alamethicin[J]. Biophys J, 2002, 82 (2): 908- 914. doi: 10.1016/S0006-3495(02)75452-0
15	PENG Y J , MA Y Z , LUO Z C , et al. Lactobacillus reuteri in digestive system diseases: focus on clinical trials and mechanisms[J]. Front Cell Infect Microbiol, 2023, 13, 1254198. doi: 10.3389/fcimb.2023.1254198
16	LYU H P , NI H Z , HUANG J Y , et al. VX-765 prevents intestinal ischemia-reperfusion injury by inhibiting NLRP3 inflammasome[J]. Tissue Cell, 2022, 75, 101718. doi: 10.1016/j.tice.2021.101718
17	ROSA C P , BELO T C A , DE MELO SANTOS N C , et al. Reactive oxygen species trigger inflammasome activation after intracellular microbial interaction[J]. Life Sci, 2023, 331, 122076. doi: 10.1016/j.lfs.2023.122076
18	XUE J C , YUAN S , HOU X T , et al. Natural products modulate NLRP3 in ulcerative colitis[J]. Front Pharmacol, 2023, 14, 1265825. doi: 10.3389/fphar.2023.1265825
19	李婷, 汤继浪, 盛宣博, 等. 猪源罗伊氏乳杆菌GL001的分离与益生特性研究[J]. 畜牧与兽医, 2022, 54 (7): 47- 53.
	LI T , TANG J L , SHENG X B , et al. Isolation and characterization of Lactobacillus reuteri from pigs[J]. Animal Husbandry & Veterinary Medicine, 2022, 54 (7): 47- 53.
20	LI Y , FENG D C , WANG Z Y , et al. Ischemia-induced ACSL4 activation contributes to ferroptosis-mediated tissue injury in intestinal ischemia/reperfusion[J]. Cell Death Differ, 2019, 26 (11): 2284- 2299. doi: 10.1038/s41418-019-0299-4
21	CHIU C J , MCARDLE A H , BROWN R , et al. Intestinal mucosal lesion in low-flow states. I. A morphological, hemodynamic, and metabolic reappraisal[J]. Arch Surg, 1970, 101 (4): 478- 483. doi: 10.1001/archsurg.1970.01340280030009
22	YU Z H , CHEN J H , LIU Y X , et al. The role of potential probiotic strains Lactobacillus reuteri in various intestinal diseases: new roles for an old player[J]. Front Microbiol, 2023, 14, 1095555. doi: 10.3389/fmicb.2023.1095555
23	GUARNER F , CASELLAS F , BORRUEL N , et al. Role of microecology in chronic inflammatory bowel diseases[J]. Eur J Clin Nutr, 2002, 56 (Suppl 4): S34- S38.
24	WANG G , HUANG S , CAI S , et al. Lactobacillus reuteri ameliorates intestinal inflammation and modulates gut microbiota and metabolic disorders in dextran sulfate sodium-induced colitis in mice[J]. Nutrients, 2020, 12 (8): 2298. doi: 10.3390/nu12082298
25	XIE W C , SONG L Y , WANG X Y , et al. A bovine lactoferricin-lactoferrampin-encoding Lactobacillus reuteri CO21 regulates the intestinal mucosal immunity and enhances the protection of piglets against enterotoxigenic Escherichia coli K88 challenge[J]. Gut Microbes, 2021, 13 (1): 1956281. doi: 10.1080/19490976.2021.1956281
26	LIU Y Y , FATHEREE N Y , DINGLE B M , et al. Lactobacillus reuteri DSM 17938 changes the frequency of Foxp3+ regulatory T cells in the intestine and mesenteric lymph node in experimental necrotizing enterocolitis[J]. PLoS One, 2013, 8 (2): e56547. doi: 10.1371/journal.pone.0056547
27	PAGLIARO P , PENNA C . Inhibitors of NLRP3 inflammasome in ischemic heart disease: focus on functional and redox aspects[J]. Antioxidants (Basel), 2023, 12 (7): 1396. doi: 10.3390/antiox12071396
28	MINUTOLI L , PUZZOLO D , RINALDI M , et al. ROS-mediated NLRP3 inflammasome activation in brain, heart, kidney, and testis ischemia/reperfusion injury[J]. Oxid Med Cell Longev, 2016, 2016, 2183026. doi: 10.1155/2016/2183026
29	华锋, 刘金辉. TNF-α在抗感染中的作用[J]. 南昌大学学报: 医学版, 2012, 52 (5): 96- 99. doi: 10.3969/j.issn.1000-2294.2012.05.028
	HUA F , LIU J H . Role of TNF-α in anti-infection[J]. Journal of Nanchang University: Medical Science, 2012, 52 (5): 96- 99. doi: 10.3969/j.issn.1000-2294.2012.05.028
30	GHAFOURI-FARD S , SHOOREI H , POORNAJAF Y , et al. NLRP3:role in ischemia/reperfusion injuries[J]. Front Immunol, 2022, 13, 926895. doi: 10.3389/fimmu.2022.926895
31	DING J J , WANG K , LIU W , et al. Pore-forming activity and structural autoinhibition of the gasdermin family[J]. Nature, 2016, 535 (7610): 111- 116. doi: 10.1038/nature18590
32	曹雪芬, 冷玉芳, 韩晓霞, 等. 川芎嗪通过抑制NLRP3减轻肠缺血再灌注损伤的细胞焦亡[J]. 中国临床药理学与治疗学, 2023, 28 (11): 1201- 1208.
	CAO X F , LENG Y F , HAN X X , et al. Tetramethylpyrazine protected against intestinal ischemia-reperfusion injury induced pyroptosis by inhibiting NLRP3 inflammasome activation[J]. Chinese Journal of Clinical Pharmacology and Therapeutics, 2023, 28 (11): 1201- 1208.

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Limosilactobacillus reuteri Alleviates Intestinal Ischemia/Reperfusion Injury in Rats by Inhibiting the ROS Dependent NLRP3 Inflammatory Pathway

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