The Anti-Helicobacter pylori effects of Limosilactobacillus reuteri strain 2892 isolated from Camel milk in C57BL/6 mice.
Anti-inflammatory
Antioxidant stress
Helicobacter pylori
Limosilactobacillus reuteri 2892
Probiotics
Journal
World journal of microbiology & biotechnology
ISSN: 1573-0972
Titre abrégé: World J Microbiol Biotechnol
Pays: Germany
ID NLM: 9012472
Informations de publication
Date de publication:
15 Mar 2023
15 Mar 2023
Historique:
received:
01
10
2022
accepted:
24
02
2023
entrez:
15
3
2023
pubmed:
16
3
2023
medline:
17
3
2023
Statut:
epublish
Résumé
Helicobacter pylori infection (H. pylori) is associated with chronic gastritis, peptic ulcers, and gastric cancer. The present study provides information on the protective effects of Limosilactobacillus reuteri strain 2892 (L. reuteri 2892) isolated from camel's milk against H. pylori-induced gastritis in the stomach tissue of animal models. Animal assays revealed that L. reuteri 2892 pretreatment significantly downregulated the virulence factor cagA gene expression. It upregulated the expression level of tight junction molecules [zona occludens (ZO-1), claudin-4] and suppressed metalloproteinase (MMP)-2 and MMP-9 expressions. L. reuteri 2892 exhibited immunomodulatory effects on cytokine profile, as it reduced the serum concentrations of pro-inflammatory cytokines interleukin (IL)-6, IL-1β, and INF-γ and increased the anti-inflammatory cytokine, IL-10. In addition, L. reuteri 2892 showed anti-oxidative stress activity by regulating the levels of oxidative stress-associated markers [superoxide dismutase (SOD) and malondialdehyde (MDA)]. Our findings suggest that L. reuteri 2892 attenuates H. pylori-induced gastritis.
Identifiants
pubmed: 36918449
doi: 10.1007/s11274-023-03555-x
pii: 10.1007/s11274-023-03555-x
doi:
Substances chimiques
Cytokines
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
119Subventions
Organisme : Islamic Azad University of Shiraz
ID : 162449566
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature B.V.
Références
Asgari B, Kermanian F, Hedayat Yaghoobi M, Vaezi A, Soleimanifar F, Yaslianifard S (2020) The anti-Helicobacter pylori effects of lactobacillus acidophilus, L. plantarum, and L. rhamnosus in stomach tissue of C57BL/6 mice. Visc Med 36:137–143. https://doi.org/10.1159/000500616
doi: 10.1159/000500616
pubmed: 32356850
Azad MAK, Sarker M, Wan D (2018) Immunomodulatory effects of probiotics on cytokine profiles. Biomed Res. Int 2018. https://doi.org/10.1155/2018/8063647
doi: 10.1155/2018/8063647
pubmed: 30426014
pmcid: 6218795
Bang CS, Baik GH (2014) Attempts to enhance the eradication rate of Helicobacter pylori infection. World J Gastroenterol 20:5252–5262. https://doi.org/10.3748/wjg.v20.i18.5252
doi: 10.3748/wjg.v20.i18.5252
pubmed: 24833855
pmcid: 4017040
Butcher LD, den Hartog G, Ernst PB, Crowe SE (2017) Oxidative stress resulting from Helicobacter pylori infection contributes to gastric carcinogenesis. Cell Mol Gastroenterol Hepatol 3:316–322. https://doi.org/10.1016/j.jcmgh.2017.02.002
doi: 10.1016/j.jcmgh.2017.02.002
pubmed: 28462373
pmcid: 5404027
Cabral-Pacheco GA, Garza-Veloz I, Castruita-De la Rosa C, Ramirez-Acuña JM, Perez-Romero BA, Guerrero-Rodriguez JF, Martinez-Avila N, Martinez-Fierro ML (2020) The roles of matrix metalloproteinases and their inhibitors in human diseases. Int J Mol Sci 21:9739
doi: 10.3390/ijms21249739
pubmed: 33419373
pmcid: 7767220
Caron TJ, Scott KE, Fox JG, Hagen SJ (2015) Tight junction disruption: Helicobacter pylori and dysregulation of the gastric mucosal barrier. World J Gastroenterol 21:11411–11427. https://doi.org/10.3748/wjg.v21.i40.11411
doi: 10.3748/wjg.v21.i40.11411
pubmed: 26523106
pmcid: 4616217
Chen M-J, Chen C-C, Huang Y-C, Tseng C-C, Hsu J-T, Lin Y-F, Fang Y-J, Wu M-S, Liou J-M, for the Taiwan Gastrointestinal Disease H C (2021) The efficacy of Lactobacillus acidophilus and rhamnosus in the reduction of bacterial load of Helicobacter pylori and modification of gut microbiota—a double-blind, placebo-controlled, randomized trial. Helicobacter 26:e12857. https://doi.org/10.1111/hel.12857
doi: 10.1111/hel.12857
pubmed: 34708471
Corcoran BM, Stanton C, Fitzgerald GF, Ross RP (2005) Survival of probiotic lactobacilli in acidic environments is enhanced in the presence of metabolizable sugars. Appl Environ Microbiol 71:3060–3067. https://doi.org/10.1128/aem.71.6.3060-3067.2005
doi: 10.1128/aem.71.6.3060-3067.2005
pubmed: 15933002
pmcid: 1151822
Crabtree JE, Lindley IJ (1994) Mucosal interleukin-8 and Helicobacter pylori-associated gastroduodenal disease. Eur J Gastroenterol Hepatol 6(Suppl 1):S33–S38
pubmed: 7735932
de Moreno de LeBlanc A, LeBlanc JG, Perdigón G, Miyoshi A, Langella P, Azevedo V, Sesma F (2008) Oral administration of a catalase-producing Lactococcus lactis can prevent a chemically induced colon cancer in mice. J Med Microbiol 57:100–105. https://doi.org/10.1099/jmm.0.47403-0
doi: 10.1099/jmm.0.47403-0
pubmed: 18065674
Díaz P, Valenzuela Valderrama M, Bravo J, Quest AFG (2018) Helicobacter pylori and gastric cancer: adaptive cellular mechanisms involved in disease progression. Front Microbiol. https://doi.org/10.3389/fmicb.2018.00005
doi: 10.3389/fmicb.2018.00005
pubmed: 30524403
pmcid: 6262351
Ding S-Z, Minohara Y, Fan XJ, Wang J, Reyes VE, Patel J, Dirden-Kramer B, Boldogh I, Ernst PB, Crowe SE (2007) Helicobacter pylori infection induces oxidative stress and programmed cell death in human gastric epithelial cells. Infect Immun 75:4030–4039. https://doi.org/10.1128/IAI.00172-07
doi: 10.1128/IAI.00172-07
pubmed: 17562777
pmcid: 1952011
Dixon B, Hossain R, Patel RV, Algood HMS (2019) Th17 cells in Helicobacter pylori infection: a dichotomy of help and harm. Infect Immun. https://doi.org/10.1128/iai.00363-19
doi: 10.1128/iai.00363-19
pubmed: 31427446
pmcid: 6803329
Edalati E, Saneei B, Alizadeh M, Hosseini SS, Zahedi Bialvaei A, Taheri K (2019) Isolation of probiotic bacteria from raw camel’s milk and their antagonistic effects on two bacteria causing food poisoning. New Microbes New Infect 27:64–68. https://doi.org/10.1016/j.nmni.2018.11.008
doi: 10.1016/j.nmni.2018.11.008
pubmed: 30622712
García A, Navarro K, Sanhueza E, Pineda S, Pastene E, Quezada M, Henríquez K, Karlyshev A, Villena J, González C (2017) Characterization of Lactobacillus fermentum UCO-979 C, a probiotic strain with a potent anti-helicobacter pylori activity. ELECTRON J BIOTECHN 25:75–83. https://doi.org/10.1016/j.ejbt.2016.11.008
doi: 10.1016/j.ejbt.2016.11.008
Gebremariam HG, Qazi KR, Somiah T, Pathak SK, Sjölinder H, Sverremark Ekström E, Jonsson A-B (2019) Lactobacillus gasseri suppresses the production of proinflammatory cytokines in helicobacter pylori-infected macrophages by inhibiting the expression of ADAM17. Front Immunol. https://doi.org/10.3389/fimmu.2019.02326
doi: 10.3389/fimmu.2019.02326
pubmed: 31636639
pmcid: 6788455
Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, Malfertheiner P, Graham DY, Wong VWS, Wu JCY, Chan FKL, Sung JJY, Kaplan GG, Ng SC (2017) Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. J Gastroenterol 153:420–429. https://doi.org/10.1053/j.gastro.2017.04.022
doi: 10.1053/j.gastro.2017.04.022
Huang JQ, Zheng GF, Sumanac K, Irvine EJ, Hunt RH (2003) Meta-analysis of the relationship between cagA seropositivity and gastric cancer. J Gastroenterol 125:1636–1644. https://doi.org/10.1053/j.gastro.2003.08.033
doi: 10.1053/j.gastro.2003.08.033
Ierardi E, Giorgio F, Losurdo G, Di Leo A, Principi M (2013) How antibiotic resistances could change Helicobacter pylori treatment: A matter of geography? World J Gastroenterol 19:8168–8180. https://doi.org/10.3748/wjg.v19.i45.8168
doi: 10.3748/wjg.v19.i45.8168
pubmed: 24363506
pmcid: 3857438
Ito F, Sono Y, Ito T (2019) Measurement and clinical significance of lipid peroxidation as a biomarker of oxidative stress: oxidative stress in diabetes, atherosclerosis, and chronic inflammation. Antioxidants 8:72
doi: 10.3390/antiox8030072
pubmed: 30934586
pmcid: 6466575
Ji J, Yang H (2020) Using probiotics as supplementation for Helicobacter pylori antibiotic therapy. Int J Mol Sci 21:1136
doi: 10.3390/ijms21031136
pubmed: 32046317
pmcid: 7037652
Ji J, Yang H (2021) In vitro effects of lactobacillus plantarum LN66 and antibiotics used alone or in combination on Helicobacter pylori mature biofilm. Microorganisms 9:424
doi: 10.3390/microorganisms9020424
pubmed: 33670726
pmcid: 7923053
Karamese M, Aydin H, Sengul E, Gelen V, Sevim C, Ustek D, Karakus E (2016) The Immunostimulatory Effect of Lactic acid Bacteria in a rat model. Iran J Immunol 13:220–228
pubmed: 27671513
Keikha M, Karbalaei M (2021) Probiotics as the live microscopic fighters against Helicobacter pylori gastric infections. BMC Gastroenterol 21:388. https://doi.org/10.1186/s12876-021-01977-1
doi: 10.1186/s12876-021-01977-1
pubmed: 34670526
pmcid: 8527827
Khaiboullina SF, Abdulkhakov S, Khalikova A, Safina D, Martynova EV, Davidyuk Y, Khuzin F, Faizullina R, Lombardi VC, Cherepnev GV, Rizvanov AA (2016) Serum cytokine signature that discriminates Helicobacter pylori positive and negative juvenile gastroduodenitis. Front Microbiol. https://doi.org/10.3389/fmicb.2016.01916
doi: 10.3389/fmicb.2016.01916
pubmed: 28018296
pmcid: 5156714
Koyama S (2004) Significance of cell-surface expression of matrix metalloproteinases and their inhibitors on gastric epithelium and infiltrating mucosal lymphocytes in progression of helicobacter pylori-associated gastritis. Scand J Gastroenterol 39:1046–1053. https://doi.org/10.1080/00365520410003245
doi: 10.1080/00365520410003245
pubmed: 15545160
Kusters JG, van Vliet AHM, Kuipers EJ (2006) Pathogenesis of Helicobacter pylori infection. Clin Microbiol reviews 19: 449 – 90. https://doi.org/10.1128/CMR.00054-05
doi: 10.1128/CMR.00054-05
Lamb A, Chen L-F (2013) Role of the Helicobacter pylori-Induced inflammatory response in the development of gastric cancer. J Cell Biochem 114:491–497. https://doi.org/10.1002/jcb.24389
doi: 10.1002/jcb.24389
pubmed: 22961880
pmcid: 3909030
LeBlanc JG, del Carmen S, Miyoshi A, Azevedo V, Sesma F, Langella P, Bermúdez-Humarán LG, Watterlot L, Perdigon G, de Moreno A (2011) Use of superoxide dismutase and catalase producing lactic acid bacteria in TNBS induced Crohn’s disease in mice. J Biotechnol 151:287–293. https://doi.org/10.1016/j.jbiotec.2010.11.008
doi: 10.1016/j.jbiotec.2010.11.008
pubmed: 21167883
Li SL, Zhao JR, Ren XY, Xie JP, Ma QZ, Rong QH (2013) Increased expression of matrix metalloproteinase-9 associated with gastric ulcer recurrence. World J Gastroenterol 19:4590–4595. https://doi.org/10.3748/wjg.v19.i28.4590
doi: 10.3748/wjg.v19.i28.4590
pubmed: 23901237
pmcid: 3725386
Lin C-C, Huang W-C, Su C-H, Lin W-D, Wu W-T, Yu B, Hsu Y-M (2020) Effects of multi-strain probiotics on immune responses and metabolic balance in Helicobacter pylori-Infected mice. Nutrients 12:2476
doi: 10.3390/nu12082476
pubmed: 32824501
pmcid: 7468736
Lin W-Y, Lin J-H, Kuo Y-W, Chiang P-FR, Ho H-H (2022) Probiotics and their metabolites reduce oxidative stress in middle-aged mice. Curr Microbiol 79:1–12
doi: 10.1007/s00284-022-02783-y
Macfarlane GT, Cummings JH (1999) Probiotics and prebiotics: can regulating the activities of intestinal bacteria benefit health? BMJ 318:999–1003. https://doi.org/10.1136/bmj.318.7189.999
doi: 10.1136/bmj.318.7189.999
pubmed: 10195977
pmcid: 1115424
Mishra V, Shah C, Mokashe N, Chavan R, Yadav H, Prajapati J (2015) Probiotics as potential antioxidants: a systematic review. J Agric Food Chem 63:3615–3626. https://doi.org/10.1021/jf506326t
doi: 10.1021/jf506326t
pubmed: 25808285
Panpetch W, Spinler JK, Versalovic J, Tumwasorn S (2016) Characterization of Lactobacillus salivarius strains B37 and B60 capable of inhibiting IL-8 production in Helicobacter pylori-stimulated gastric epithelial cells. BMC Microbiol 16:242. https://doi.org/10.1186/s12866-016-0861-x
doi: 10.1186/s12866-016-0861-x
pubmed: 27756217
pmcid: 5070129
Patel A, Shah N, Prajapati JB (2014) Clinical application of probiotics in the treatment of Helicobacter pylori infection—A brief review. J Microbiol Immunol Infect 47:429–437. https://doi.org/10.1016/j.jmii.2013.03.010
doi: 10.1016/j.jmii.2013.03.010
pubmed: 23757373
Peña JA, Rogers AB, Ge Z, Ng V, Li SY, Fox JG, Versalovic J (2005) Probiotic Lactobacillus spp. diminish Helicobacter hepaticus-induced inflammatory bowel disease in interleukin-10-deficient mice. Infect Immun 73:912–920. https://doi.org/10.1128/iai.73.2.912-920.2005
doi: 10.1128/iai.73.2.912-920.2005
pubmed: 15664933
pmcid: 547020
Piscione M, Mazzone M, Di Marcantonio MC, Muraro R, Mincione G (2021) Eradication of Helicobacter pylori and gastric Cancer: a controversial relationship. Front Microbiol 12:630852. https://doi.org/10.3389/fmicb.2021.630852
doi: 10.3389/fmicb.2021.630852
pubmed: 33613500
pmcid: 7889593
Ruggiero P (2014) Use of probiotics in the fight against Helicobacter pylori. World J Gastrointest Pathophysiol 5:384–391. https://doi.org/10.4291/wjgp.v5.i4.384
doi: 10.4291/wjgp.v5.i4.384
pubmed: 25400981
pmcid: 4231502
Ruiz RLG, Mohamed F, Bleckwedel J, Medina R, De Vuyst L, Hebert EM, Mozzi F (2019) Diversity and functional properties of lactic acid bacteria isolated from wild fruits and flowers present in Northern Argentina. Front Microbiol. https://doi.org/10.3389/fmicb.2019.01091
doi: 10.3389/fmicb.2019.01091
pubmed: 31849872
pmcid: 6895012
Sgouras D, Maragkoudakis P, Petraki K, Martinez-Gonzalez B, Eriotou E, Michopoulos S, Kalantzopoulos G, Tsakalidou E, Mentis A (2004) In vitro and in vivo inhibition of Helicobacter pylori by Lactobacillus casei strain Shirota. Appl Environ Microbiol 70:518–526. https://doi.org/10.1128/aem.70.1.518-526.2004
doi: 10.1128/aem.70.1.518-526.2004
pubmed: 14711683
pmcid: 321236
Sokolova O, Naumann M (2022) Matrix metalloproteinases in Helicobacter pylori–Associated gastritis and gastric cancer. Int J Mol Sci 23(3):1883
doi: 10.3390/ijms23031883
pubmed: 35163805
pmcid: 8836485
Sugimoto M, Yamaoka Y (2009) Virulence factor genotypes of Helicobacter pylori affect cure rates of eradication therapy. ARCH IMMUNOL THER EX 57:45–56. https://doi.org/10.1007/s00005-009-0007-z
doi: 10.1007/s00005-009-0007-z
Taverniti V, Guglielmetti S (2011) The immunomodulatory properties of probiotic microorganisms beyond their viability (ghost probiotics: proposal of paraprobiotic concept). Genes Nutr 6:261–274. https://doi.org/10.1007/s12263-011-0218-x
doi: 10.1007/s12263-011-0218-x
pubmed: 21499799
pmcid: 3145061
Thung I, Aramin H, Vavinskaya V, Gupta S, Park JY, Crowe SE, Valasek MA (2016) Review article: the global emergence of Helicobacter pylori antibiotic resistance. Aliment Pharmacol Ther 43:514–533. https://doi.org/10.1111/apt.13497
doi: 10.1111/apt.13497
pubmed: 26694080
Verma S, Kesh K, Ganguly N, Jana S, Swarnakar S (2014) Matrix metalloproteinases and gastrointestinal cancers: impacts of dietary antioxidants. World J Biol Chem 5:355–376. https://doi.org/10.4331/wjbc.v5.i3.355
doi: 10.4331/wjbc.v5.i3.355
pubmed: 25225603
pmcid: 4160529
Wang Y, Wu Y, Wang Y, Xu H, Mei X, Yu D, Wang Y, Li W (2017) Antioxidant Properties of probiotic Bacteria. Nutrients 9:521
doi: 10.3390/nu9050521
pubmed: 28534820
pmcid: 5452251
Westerik N, Reid G, Sybesma W, Kort R (2018) The probiotic lactobacillus rhamnosus for alleviation of Helicobacter pylori-associated gastric pathology in East Africa. Front Microbiol. https://doi.org/10.3389/fmicb.2018.01873
doi: 10.3389/fmicb.2018.01873
pubmed: 30154777
pmcid: 6102400
Zhou Q, Xue B, Gu R, Li P, Gu Q (2021) Lactobacillus plantarum ZJ316 attenuates Helicobacter pylori-Induced Gastritis in C57BL/6 mice. J Agric Food Chem 69:6510–6523. https://doi.org/10.1021/acs.jafc.1c01070
doi: 10.1021/acs.jafc.1c01070
pubmed: 34096709
WHO. Antimicrobial resistance global report on surveillance: 2014 summary (2014) (2014)
Wroblewski LE, Peek RM Jr, Wilson KT (2010) Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 23:713–739. https://doi.org/10.1128/cmr.00011-10
doi: 10.1128/cmr.00011-10
pubmed: 20930071
pmcid: 2952980
Wu Y, Zhu C, Chen Z, Chen Z, Zhang W, Ma X, Wang L, Yang X, Jiang Z (2016) Protective effects of Lactobacillus plantarum on epithelial barrier disruption caused by enterotoxigenic Escherichia coli in intestinal porcine epithelial cells. Vet Immunol Immunopathol 172:55–63. https://doi.org/10.1016/j.vetimm.2016.03.005
doi: 10.1016/j.vetimm.2016.03.005
pubmed: 27032504
Xia X, Zhang L, Wu H, Chen F, Liu X, Xu H, Cui Y, Zhu Q, Wang M, Hao H (2022) CagA+ Helicobacter pylori, not CagA–Helicobacter pylori, infection impairs endothelial function through exosomes-mediated ROS formation. Front Cardiovasc Med. https://doi.org/10.3389/fcvm.2022.881372
doi: 10.3389/fcvm.2022.881372
pubmed: 36756639
pmcid: 9815775
Yang Y-J, Chuang C-C, Yang H-B, Lu C-C, Sheu B-S (2012) Lactobacillus acidophilus ameliorates H. pylori-induced gastric inflammation by inactivating the Smad7 and NFκB pathways. BMC Microbiol 12:38. https://doi.org/10.1186/1471-2180-12-38
doi: 10.1186/1471-2180-12-38
pubmed: 22429929
pmcid: 3340303
Yang KM, Jiang ZY, Zheng CT, Wang L, Yang XF (2014) Effect of Lactobacillus plantarum on diarrhea and intestinal barrier function of young piglets challenged with enterotoxigenic Escherichia coli K88. J Anim Sci 92:1496–1503. https://doi.org/10.2527/jas.2013-6619
doi: 10.2527/jas.2013-6619
pubmed: 24492550
Yarmohammadi M, Yadegar A, Ebrahimi MT, Zali MR (2021) Effects of a potential probiotic strain Lactobacillus gasseri ATCC 33323 on Helicobacter pylori-Induced Inflammatory Response and Gene expression in coinfected gastric epithelial cells. Probiotics Antimicrob Proteins 13:751–764. https://doi.org/10.1007/s12602-020-09721-z
doi: 10.1007/s12602-020-09721-z
pubmed: 33206342
Zhang M (2015) High antibiotic resistance rate: a difficult issue for Helicobacter pylori eradication treatment. World J Gastroenterol 21:13432–13437. https://doi.org/10.3748/wjg.v21.i48.13432
doi: 10.3748/wjg.v21.i48.13432
pubmed: 26730153
pmcid: 4690171
Zhang W, Lu H, Graham DY (2014) An update on Helicobacter pylori as the cause of gastric cancer. Gastrointest Tumors 1:155–165
doi: 10.1159/000365310
pubmed: 26672968
pmcid: 4645582