Protective Effects and Mechanism of a Novel Probiotic Strain <i>Ligilactobacillus salivarius</i> YL20 against <i>Cronobacter sakazakii</i>-Induced Necrotizing Enterocolitis In Vitro and In Vivo
Exposure to probiotics in early life contributes to host intestinal development and prevention of necrotizing enterocolitis (NEC). <i>Cronobacter sakazakii</i> (<i>C. sakazakii</i>), an opportunistic pathogen, can cause NEC, bacteremia, and meningitis in neonates, but the res...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2022-09-01
|
| Series: | Nutrients |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2072-6643/14/18/3827 |
| _version_ | 1797483932678094848 |
|---|---|
| author | Weiming Wang Meng Geng Caixia Zhu Lei Huang Yue Zhang Tengxun Zhang Chongjie Zhao Tongcun Zhang Xinjun Du Nan Wang |
| author_facet | Weiming Wang Meng Geng Caixia Zhu Lei Huang Yue Zhang Tengxun Zhang Chongjie Zhao Tongcun Zhang Xinjun Du Nan Wang |
| author_sort | Weiming Wang |
| collection | DOAJ |
| description | Exposure to probiotics in early life contributes to host intestinal development and prevention of necrotizing enterocolitis (NEC). <i>Cronobacter sakazakii</i> (<i>C. sakazakii</i>), an opportunistic pathogen, can cause NEC, bacteremia, and meningitis in neonates, but the research of probiotics against <i>C. sakazakii</i> is limited relative to other enteropathogens. Here, the protective effect and mechanism of a novel probiotic <i>Ligilactobacillus salivarius</i> (<i>L</i><i>. salivarius</i>) YL20 isolated from breast milk on <i>C. sakazakii</i>-induced intestinal injury were explored by using two in vitro models, including an <i>C. sakazakii</i>-infected intestinal organoid model and intestinal barrier model, as well as an in vivo experimental animal model. Our results revealed that <i>L</i><i>. salivarius</i> YL20 could promote epithelial cell proliferation in intestinal organoids, rescue budding-impaired organoids, prevent the decrease of mRNA levels of leucine-rich repeat containing G protein-coupled receptor 5 (<i>Lgr5</i>), zonula occludens-1 (<i>Zo-1</i>) and <i>Occludin</i>, and reverse <i>C. sakazakii</i>-induced low level of Mucin 2 (MUC2) in intestinal organoids. Additionally, YL20 could inhibit <i>C. sakazakii</i> invasion, increase the expression of ZO-1 and occludin in <i>C. sakazakii</i>-infected HT-29 cells, and reverse TEER decrease and corresponding permeability increase across <i>C. sakazakii</i>-infected Caco-2 monolayers. Furthermore, YL20 administration could alleviate NEC in <i>C. sakazakii</i>-infected neonatal mice by increasing the mice survival ratio, decreasing pathology scores, and downregulating pro-inflammatory cytokines. Meanwhile, YL20 could also enhance intestinal barrier function in vivo by increasing the number of goblet cells, the level of <i>MUC-2</i> and the expression of ZO-1. Our overall findings demonstrated for the first time the beneficial effects of <i>L</i><i>. salivarius</i> YL20 against <i>C. sakazakii</i>-induced NEC by improving intestinal stem cell function and enhancing intestinal barrier integrity. |
| first_indexed | 2024-03-09T22:55:06Z |
| format | Article |
| id | doaj.art-5f9b029dc031495cb139cc09a0d6230f |
| institution | Directory Open Access Journal |
| issn | 2072-6643 |
| language | English |
| last_indexed | 2024-03-09T22:55:06Z |
| publishDate | 2022-09-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Nutrients |
| spelling | doaj.art-5f9b029dc031495cb139cc09a0d6230f2023-11-23T18:12:45ZengMDPI AGNutrients2072-66432022-09-011418382710.3390/nu14183827Protective Effects and Mechanism of a Novel Probiotic Strain <i>Ligilactobacillus salivarius</i> YL20 against <i>Cronobacter sakazakii</i>-Induced Necrotizing Enterocolitis In Vitro and In VivoWeiming Wang0Meng Geng1Caixia Zhu2Lei Huang3Yue Zhang4Tengxun Zhang5Chongjie Zhao6Tongcun Zhang7Xinjun Du8Nan Wang9School of Traditional Chinese Medicine, Southern Medical University, Guangzhou 510515, ChinaKey Laboratory of Industrial Fermentation Microbiology, Ministry of Education and Tianjin, College of Biotechnology, Tianjin University of Science and Technology, Tianjin 300457, ChinaKey Laboratory of Industrial Fermentation Microbiology, Ministry of Education and Tianjin, College of Biotechnology, Tianjin University of Science and Technology, Tianjin 300457, ChinaKey Laboratory of Industrial Fermentation Microbiology, Ministry of Education and Tianjin, College of Biotechnology, Tianjin University of Science and Technology, Tianjin 300457, ChinaKey Laboratory of Industrial Fermentation Microbiology, Ministry of Education and Tianjin, College of Biotechnology, Tianjin University of Science and Technology, Tianjin 300457, ChinaKey Laboratory of Industrial Fermentation Microbiology, Ministry of Education and Tianjin, College of Biotechnology, Tianjin University of Science and Technology, Tianjin 300457, ChinaKey Laboratory of Industrial Fermentation Microbiology, Ministry of Education and Tianjin, College of Biotechnology, Tianjin University of Science and Technology, Tianjin 300457, ChinaKey Laboratory of Industrial Fermentation Microbiology, Ministry of Education and Tianjin, College of Biotechnology, Tianjin University of Science and Technology, Tianjin 300457, ChinaCollege of Biotechnology, Tianjin University of Science and Technology, Tianjin 300457, ChinaKey Laboratory of Industrial Fermentation Microbiology, Ministry of Education and Tianjin, College of Biotechnology, Tianjin University of Science and Technology, Tianjin 300457, ChinaExposure to probiotics in early life contributes to host intestinal development and prevention of necrotizing enterocolitis (NEC). <i>Cronobacter sakazakii</i> (<i>C. sakazakii</i>), an opportunistic pathogen, can cause NEC, bacteremia, and meningitis in neonates, but the research of probiotics against <i>C. sakazakii</i> is limited relative to other enteropathogens. Here, the protective effect and mechanism of a novel probiotic <i>Ligilactobacillus salivarius</i> (<i>L</i><i>. salivarius</i>) YL20 isolated from breast milk on <i>C. sakazakii</i>-induced intestinal injury were explored by using two in vitro models, including an <i>C. sakazakii</i>-infected intestinal organoid model and intestinal barrier model, as well as an in vivo experimental animal model. Our results revealed that <i>L</i><i>. salivarius</i> YL20 could promote epithelial cell proliferation in intestinal organoids, rescue budding-impaired organoids, prevent the decrease of mRNA levels of leucine-rich repeat containing G protein-coupled receptor 5 (<i>Lgr5</i>), zonula occludens-1 (<i>Zo-1</i>) and <i>Occludin</i>, and reverse <i>C. sakazakii</i>-induced low level of Mucin 2 (MUC2) in intestinal organoids. Additionally, YL20 could inhibit <i>C. sakazakii</i> invasion, increase the expression of ZO-1 and occludin in <i>C. sakazakii</i>-infected HT-29 cells, and reverse TEER decrease and corresponding permeability increase across <i>C. sakazakii</i>-infected Caco-2 monolayers. Furthermore, YL20 administration could alleviate NEC in <i>C. sakazakii</i>-infected neonatal mice by increasing the mice survival ratio, decreasing pathology scores, and downregulating pro-inflammatory cytokines. Meanwhile, YL20 could also enhance intestinal barrier function in vivo by increasing the number of goblet cells, the level of <i>MUC-2</i> and the expression of ZO-1. Our overall findings demonstrated for the first time the beneficial effects of <i>L</i><i>. salivarius</i> YL20 against <i>C. sakazakii</i>-induced NEC by improving intestinal stem cell function and enhancing intestinal barrier integrity.https://www.mdpi.com/2072-6643/14/18/3827<i>Cronobacter sakazakii</i>intestinal development<i>Ligilactobacillus salivarius</i>necrotizing enterocolitissuckling mouse |
| spellingShingle | Weiming Wang Meng Geng Caixia Zhu Lei Huang Yue Zhang Tengxun Zhang Chongjie Zhao Tongcun Zhang Xinjun Du Nan Wang Protective Effects and Mechanism of a Novel Probiotic Strain <i>Ligilactobacillus salivarius</i> YL20 against <i>Cronobacter sakazakii</i>-Induced Necrotizing Enterocolitis In Vitro and In Vivo Nutrients <i>Cronobacter sakazakii</i> intestinal development <i>Ligilactobacillus salivarius</i> necrotizing enterocolitis suckling mouse |
| title | Protective Effects and Mechanism of a Novel Probiotic Strain <i>Ligilactobacillus salivarius</i> YL20 against <i>Cronobacter sakazakii</i>-Induced Necrotizing Enterocolitis In Vitro and In Vivo |
| title_full | Protective Effects and Mechanism of a Novel Probiotic Strain <i>Ligilactobacillus salivarius</i> YL20 against <i>Cronobacter sakazakii</i>-Induced Necrotizing Enterocolitis In Vitro and In Vivo |
| title_fullStr | Protective Effects and Mechanism of a Novel Probiotic Strain <i>Ligilactobacillus salivarius</i> YL20 against <i>Cronobacter sakazakii</i>-Induced Necrotizing Enterocolitis In Vitro and In Vivo |
| title_full_unstemmed | Protective Effects and Mechanism of a Novel Probiotic Strain <i>Ligilactobacillus salivarius</i> YL20 against <i>Cronobacter sakazakii</i>-Induced Necrotizing Enterocolitis In Vitro and In Vivo |
| title_short | Protective Effects and Mechanism of a Novel Probiotic Strain <i>Ligilactobacillus salivarius</i> YL20 against <i>Cronobacter sakazakii</i>-Induced Necrotizing Enterocolitis In Vitro and In Vivo |
| title_sort | protective effects and mechanism of a novel probiotic strain i ligilactobacillus salivarius i yl20 against i cronobacter sakazakii i induced necrotizing enterocolitis in vitro and in vivo |
| topic | <i>Cronobacter sakazakii</i> intestinal development <i>Ligilactobacillus salivarius</i> necrotizing enterocolitis suckling mouse |
| url | https://www.mdpi.com/2072-6643/14/18/3827 |
| work_keys_str_mv | AT weimingwang protectiveeffectsandmechanismofanovelprobioticstrainiligilactobacillussalivariusiyl20againsticronobactersakazakiiiinducednecrotizingenterocolitisinvitroandinvivo AT menggeng protectiveeffectsandmechanismofanovelprobioticstrainiligilactobacillussalivariusiyl20againsticronobactersakazakiiiinducednecrotizingenterocolitisinvitroandinvivo AT caixiazhu protectiveeffectsandmechanismofanovelprobioticstrainiligilactobacillussalivariusiyl20againsticronobactersakazakiiiinducednecrotizingenterocolitisinvitroandinvivo AT leihuang protectiveeffectsandmechanismofanovelprobioticstrainiligilactobacillussalivariusiyl20againsticronobactersakazakiiiinducednecrotizingenterocolitisinvitroandinvivo AT yuezhang protectiveeffectsandmechanismofanovelprobioticstrainiligilactobacillussalivariusiyl20againsticronobactersakazakiiiinducednecrotizingenterocolitisinvitroandinvivo AT tengxunzhang protectiveeffectsandmechanismofanovelprobioticstrainiligilactobacillussalivariusiyl20againsticronobactersakazakiiiinducednecrotizingenterocolitisinvitroandinvivo AT chongjiezhao protectiveeffectsandmechanismofanovelprobioticstrainiligilactobacillussalivariusiyl20againsticronobactersakazakiiiinducednecrotizingenterocolitisinvitroandinvivo AT tongcunzhang protectiveeffectsandmechanismofanovelprobioticstrainiligilactobacillussalivariusiyl20againsticronobactersakazakiiiinducednecrotizingenterocolitisinvitroandinvivo AT xinjundu protectiveeffectsandmechanismofanovelprobioticstrainiligilactobacillussalivariusiyl20againsticronobactersakazakiiiinducednecrotizingenterocolitisinvitroandinvivo AT nanwang protectiveeffectsandmechanismofanovelprobioticstrainiligilactobacillussalivariusiyl20againsticronobactersakazakiiiinducednecrotizingenterocolitisinvitroandinvivo |