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Biofouling
The Journal of Bioadhesion and Biofilm Research
Volume 35, 2019 - Issue 8
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Original Articles

Characterization of the immunomodulatory and anti-Helicobacter pylori properties of the human gastric isolate Lactobacillus rhamnosus UCO-25A

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Pages 922-937 | Received 02 May 2019, Accepted 27 Sep 2019, Published online: 24 Oct 2019

References

  • Ansari SA, Devi S, Tenguria S, Kumar A, Ahmed N. 2014. Helicobacter pylori protein HP0986 (TieA) interacts with mouse TNFR1 and triggers proinflammatory and proapoptotic signaling pathways in cultured macrophage cells (RAW 264.7). Cytokine. 68:110–117. doi:10.1016/j.cyto.2014.03.006
  • Atherton JC. 2006. The pathogenesis of Helicobacter pylori induced gastro-duodenal diseases. Annu Rev Pathol Mech Dis. 1:63–96. doi:10.1146/annurev.pathol.1.110304.100125
  • Backert S, Neddermann M, Maubach G, Naumann M. 2016. Pathogenesis of Helicobacter pylori infection. Helicobacter. 21:19–25. doi:10.1111/hel.12335
  • Bauer B, Meyer TF. 2011. The human gastric pathogen Helicobacter pylori and its association with gastric cancer and ulcer disease. Ulcers. 2011:1–23. doi:10.1155/2011/340157
  • Brandt S, Kwok T, Hartig R, Konig W, Backert S. 2005. NF- B activation and potentiation of proinflammatory responses by the Helicobacter pylori CagA protein. Proc Natl Acad Sci USA. 102:9300–9305. doi:10.1073/pnas.0409873102
  • Brawner KM, Kumar R, Serrano CA, Ptacek T, Lefkowitz E, Morrow CD, Zhi D, Kyanam-Kabir-Baig KR, Smythies LE, Harris PR, et al. 2017. Helicobacter pylori infection is associated with an altered gastric microbiota in children. Mucosal Immunol. 10:1169–1177. doi:10.1038/mi.2016.131
  • Chen J, Domingue JC, Sears CL. 2017. Microbiota dysbiosis in select human cancers: evidence of association and causality. Semin Immunol. 32:25–34. doi:10.1016/j.smim.2017.08.001
  • Cizginer S, Ordulu Z, Kadayifci A. 2014. Approach to Helicobacter pylori infection in geriatric population. World J Gastrointest Pharmacol Therapeut. 5:139–147. doi:10.4292/wjgpt.v5.i3.139
  • Coker OO, Dai Z, Nie Y, Zhao G, Cao L, Nakatsu G, Wu WK, Wong SH, Chen Z, Sung JJY, et al. 2017. Mucosal microbiome dysbiosis in gastric carcinogenesis. Gut. 67:1024–1032.
  • Da Costa DM, Dos Santos Pereira E, Rabenhorst S. 2015. What exists beyond cagA and vacA? Helicobacter pylori genes in gastric diseases. World J Gastroenterol. 21:10563–10572. doi:10.3748/wjg.v21.i37.10563
  • Delgado S, Leite AMO, Ruas-Madiedo P, Mayo B. 2015. Probiotic and technological properties of Lactobacillus spp. strains from the human stomach in the search for potential candidates against gastric microbial dysbiosis. Front Microbiol. 5:1–8.
  • Eftang LL, Esbensen Y, Tannaes TM, Bukholm IRK, Bukholm G. 2012. Interleukin-8 is the single most up-regulated gene in whole genome profiling of H. pylori exposed gastric epithelial cells. BMC Microbiol. 12:9. doi:10.1186/1471-2180-12-9
  • Fehlings M, Drobbe L, Moos V, Viveros PR, Hagen J, Beigier-Bompadre M, Pang E, Belogolova E, Churin Y, Schneider T, et al. 2012. Comparative analysis of the interaction of Helicobacter pylori with human dendritic cells, macrophages, and monocytes. Infect Immun. 80:2724–2734. doi:10.1128/IAI.00381-12
  • Forman D, Bray F, Brewster DH, Gombe Mbalawa C, Kohler B, Piñeros M, Steliarova-Foucher E, Swaminathan R, and Ferlay J. 2017. International Agency for Research on Cancer. Cancer incidence in five continents. [Internet]. [cited 2018 Feb 5]. http://ci5.iarc.fr.
  • García A, Sáez K, Delgado C, González CL. 2012. Low co-existence rates of Lactobacillus spp. and Helicobacter pylori detected in gastric biopsies from patients with gastrointestinal symptoms. Rev Esp Enferm Dig. 104:473–478. doi:10.4321/S1130-01082012000900005
  • Garcia CA, Henriquez AP, Retamal RC, Pineda CS, Delgado Sch C, Gonzalez CC. 2009. Probiotic properties of Lactobacillus spp isolated from gastric biopsies of Helicobacter pylori infected and non-infected individuals. Rev Med Chil. 137:369–376.
  • García-Castillo V, Sanhueza E, McNerney E, Onate SA, García A. 2016. Review microbiota dysbiosis: a new piece in the understanding of the carcinogenesis puzzle. J Med Microbiol. 65:1347–1362. doi:10.1099/jmm.0.000371
  • Goderska K, Agudo Pena S, Alarcon T. 2017. Helicobacter pylori treatment: antibiotics or probiotics. Appl Microbiol Biotechnol. 102:1–7.
  • Herbert RA. 1990. Methods for enumerating microorganisms and determining biomass in natural environments. In: Grigorova R, Norris JR, editors. Methods in microbiology. Vol. 22, Academic Press, Elsevier Ltd. p. 1–39.
  • Homan M, Orel R. 2015. Are probiotics useful in Helicobacter pylori eradication? World J Gastroenterol. 21:10644–10653. doi:10.3748/wjg.v21.i37.10644
  • Kameoka S, Kameyama T, Hayashi T, Sato S, Ohnishi N, Hayashi T, Murata-Kamiya N, Higashi H, Hatakeyama M, Takaoka A. 2016. Helicobacter pylori induces IL-1β protein through the inflammasome activation in differentiated macrophagic cells. Biomed Res. 37:21–27. doi:10.2220/biomedres.37.21
  • Kaur B, Balgir PP, Kumar B, Garg N. 2010. Helicobacter pylori infection: efficacy of probiotics and role of genome wide association studies. Arch Clin Microbiol. 1–12.
  • Kinoshita H, Hirata Y, Nakagawa H, Sakamoto K, Hayakawa Y, Takahashi R, Nakata W, Sakitani K, Serizawa T, Hikiba Y, et al. 2013. Interleukin-6 mediates epithelial-stromal interactions and promotes gastric tumorigenesis. PLoS One. 8:e60914. doi:10.1371/journal.pone.0060914
  • Klymiuk I, Bilgilier C, Stadlmann A, Thannesberger J, Kastner MT, Högenauer C, Püspök A, Biowski-Frotz S, Schrutka-Kölbl C, Thallinger GG, et al. 2017. The human gastric microbiome is predicated upon infection with Helicobacter pylori. Front Microbiol. 8:2508. doi:10.3389/fmicb.2017.02508
  • Kumar S, Hanning CR, Rieman DJ, Lee JC, Lotze MT, Brigham-Burke MR, Lehr R, Khandekar S, Kirkpatrick RB, Scott GF, et al. 2002. Interleukin-1F7b (IL-1H4/IL-1F7) is processed by caspase-1 and mature IL-1F7b binds to the IL-18 receptor but does not induce IFN-γ production. Cytokine. 18:61–71. doi:10.1006/cyto.2002.0873
  • Lebeer S, Verhoeven TLA, Vélez MP, Vanderleyden J, De Keersmaecker S. 2007. Impact of environmental and genetic factors on biofilm formation by the probiotic strain Lactobacillus rhamnosus GG. Appl Environ Microbiol. 73:6768–6775. doi:10.1128/AEM.01393-07
  • Leccese Terraf MC, Juárez Tomás MS, Rault L, Le Loir Y, Even S, Nader-Macías M. 2016. Biofilms of vaginal Lactobacillus reuteri CRL 1324 and Lactobacillus rhamnosus CRL 1332: kinetics of formation and matrix characterization. Arch Microbiol. 198:689–700. doi:10.1007/s00203-016-1225-5
  • Lofgren JL, Whary MT, Ge Z, Muthupalani S, Taylor NS, Mobley M, Potter A, Varro A, Eibach D, Suerbaum S, et al. 2011. Lack of commensal flora in Helicobacter pylori -infected INS-GAS mice reduces gastritis and delays intraepithelial neoplasia. Gastroenterology. 140:210–220. doi:10.1053/j.gastro.2010.09.048
  • Losurdo G, Cubisino R, Barone M, Principi M, Leandro G, Ierardi E, Leo AD. 2018. Probiotic monotherapy and Helicobacter pylori eradication: a systematic review with pooled-data analysis. World J Gastroenterol. 24:139–149. doi:10.3748/wjg.v24.i1.139
  • Lu H, Wu JY, Kudo T, Ohno T, Graham DY, Yamaoka Y. 2005. Regulation of interleukin-6 promoter activation in gastric epithelial cells infected with Helicobacter pylori. Mol Biol Cell. 16:4954–4966. doi:10.1091/mbc.e05-05-0426
  • Maldonado C, De Moreno De Leblanc A, Vinderola G, Bibas Bonet ME, Perdigón G. 2007. Proposed model: mechanisms of immunomodulation induced by probiotic bacteria. Clin Vaccine Immunol. 14:485–492.
  • Maldonado-Contreras A, Goldfarb KC, Godoy-Vitorino F, Karaoz U, Contreras M, Blaser MJ, Brodie EL, Dominguez-Bello MG. 2011. Structure of the human gastric bacterial community in relation to Helicobacter pylori status. isme J. 5:574–579. doi:10.1038/ismej.2010.149
  • Malfertheiner P, Megraud F, O’Morain CA, Gisbert JP, Kuipers EJ, Axon AT, Bazzoli F, Gasbarrini A, Atherton J, Graham DY, et al. 2017. European Helicobacter and microbiota study group and consensus panel. Management of Helicobacter pylori infection the Maastricht V/Florence Consensus Report. Gut. 66:6–30. doi:10.1136/gutjnl-2016-312288
  • Marcus EA, Vagin O, Tokhtaeva E, Sachs G, Scott DR. 2013. Helicobacter pylori impedes acid-induced tightening of gastric epithelial junctions. AJP Gastrointest Liver Physiol. 305:G731–G739. doi:10.1152/ajpgi.00209.2013
  • McNamee EN, Masterson JC, Jedlicka P, McManus M, Grenz A, Collins CB, Nold MF, Nold-Petry C, Bufler P, Dinarello CA, Rivera-Nieves J. 2011. Interleukin 37 expression protects mice from colitis. Proc Natl Acad Sci USA. 108:16711–16716. doi:10.1073/pnas.1111982108
  • Nair MRB, Chouhan D, Gupta S, Sen, Chattopadhyay S. 2016. Fermented foods: are they tasty medicines for Helicobacter pylori associated peptic ulcer and gastric cancer?. Front Microbiol. 7:1148.
  • Naito Y, Yoshikawa T. 2002. Molecular and cellular mechanisms involved in Helicobacter pylori–induced inflammation and oxidative stress. Free Radic Biol Med. 33:323–336. doi:10.1016/S0891-5849(02)00868-7
  • Olson JK, Navarro JB, Allen JM, McCulloh CJ, Mashburn-Warren L, Wang Y, Varaljay VA, Bailey MT, Goodman SD, Besner GE. 2018. An enhanced Lactobacillus reuteri biofilm formulation that increases protection against experimental necrotizing enterocolitis. Am J Physiol Liver Physiol. 315:G408–G419.
  • Olson JK, Rager TM, Navarro JB, Mashburn-Warren L, Goodman SD, Besner GE. 2016. Harvesting the benefits of biofilms: a novel probiotic delivery system for the prevention of necrotizing enterocolitis. J Pediatr Surg. 51:936–941. doi:10.1016/j.jpedsurg.2016.02.062
  • 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. doi:10.1016/j.jmii.2013.03.010
  • Peek RM, Fiske C, Wilson KT. 2010. Role of innate immunity in Helicobacter pylori-induced gastric malignancy. Physiol Rev. 90:831–858. doi:10.1152/physrev.00039.2009
  • Peña JA, Versalovic J. 2003. Lactobacillus rhamnosus GG decreases TNF-a production in lipopolysaccharide-activated murine macrophages by a contact-independent mechanism. Cell Microbiol. 5:277–285. doi:10.1046/j.1462-5822.2003.t01-1-00275.x
  • Posselt G, Backert S, Wessler S. 2013. The functional interplay of Helicobacter pylori factors with gastric epithelial cells induces a multi-step process in pathogenesis. Cell Commun Signal. 11:77. doi:10.1186/1478-811X-11-77
  • Rad R, Dossumbekova A, Neu B, Lang R, Bauer S, Saur D, Gerhard M, Prinz C. 2004. Cytokine gene polymorphisms influence mucosal cytokine expression, gastric inflammation, and host specific colonisation during Helicobacter pylori infection. Gut. 53:1082–1089. doi:10.1136/gut.2003.029736
  • Rolig AS, Cech C, Ahler E, Carter JE, Ottemann KM. 2013. The degree of Helicobacter pylori-triggered inflammation is manipulated by preinfection host microbiota. Infect Immun. 81:1382–1389. doi:10.1128/IAI.00044-13
  • Roos S, Engstrand L, Jonsson H. 2005. Lactobacillus gastricus sp. nov., Lactobacillus antri sp. nov., Lactobacillus kalixensis sp. nov., and Lactobacillus ultunensis sp. nov., isolated from human stomach mucosa. Int J Syst Evol Microbiol. 55:77–82. doi:10.1099/ijs.0.63083-0
  • Sakamoto I, Igarashi M, Kimura K, Takagi A, Miwa T, Koga Y. 2001. Suppressive effect of Lactobacillus gasseri OLL 2716 (LG21) on Helicobacter pylori infection in humans. J Antimicrob Chemother. 47:709–710. doi:10.1093/jac/47.5.709
  • Salas-Jara MJ, Sanhueza EA, Retamal-Díaz A, González C, Urrutia H, García A. 2016. Probiotic Lactobacillus fermentum UCO-979C biofilm formation on AGS and Caco-2 cells and Helicobacter pylori inhibition. Biofouling. 32:1245–1257. doi:10.1080/08927014.2016.1249367
  • Salva S, Villena J, Alvarez S. 2010. Immunomodulatory activity of Lactobacillus rhamnosus strains isolated from goat milk: impact on intestinal and respiratory infections. Int J Food Microbiol. 141:82–89. doi:10.1016/j.ijfoodmicro.2010.03.013
  • Sato M, Miura K, Kageyama C, Sakae H, Obayashi Y, Kawahara Y, Matsushita O, Yokota K, Okada H. 2019. Association of host immunity with Helicobacter pylori infection in recurrent gastric cancer. Infect Agents Cancer. 14:4. doi:10.1186/s13027-019-0221-1
  • Schwab C, Tveit AT, Schleper C, Urich T. 2014. Gene expression of lactobacilli in murine forestomach biofilms. Microb Biotechnol. 7:347–359. doi:10.1111/1751-7915.12126
  • Sgouras D, Maragkoudakis P, Petraki K, Eriotou E, Michopoulos S, 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. doi:10.1128/AEM.70.1.518-526.2004
  • Shah MA. 2015. Update on metastatic gastric and esophageal cancers. J Clin Oncol. 33:1760–1769. doi:10.1200/JCO.2014.60.1799
  • Shan Y, Lu X, Han Y, Li X, Wang X, Shao C, Wang L, Liu Z, Tang W, Sun Y, et al. 2015. Helicobacter pylori outer membrane protein 18 (Hp1125) is involved in persistent colonization by evading interferon-γ signaling. Biomed Res Int. 2015:1. doi:10.1155/2015/571280
  • Stepanović S, Vuković D, Hola V, Di Bonaventura G, Djukić S, Ćirković I, Ruzicka F. 2007. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS. 115:891–899. doi:10.1111/j.1600-0463.2007.apm_630.x
  • Sunanliganon C, Thong-Ngam D, Tumwasorn S, Klaikeaw N. 2012. Lactobacillus plantarum B7 inhibits Helicobacter pylori growth and attenuates gastric inflammation. World J Gastroenterol. 18:2472–2480. doi:10.3748/wjg.v18.i20.2472
  • Walker MM, Talley NJ. 2014. Review article: bacteria and pathogenesis of disease in the upper gastrointestinal tract—beyond the era of Helicobacter pylori. Aliment Pharmacol Ther. 39:767–779. doi:10.1111/apt.12666
  • Wang F, Mao Z, Liu D, Yu J, Wang Y, Ye W, Lin D, Zhou N, Xie Y. 2017. Overexpression of Tim-3 reduces Helicobacter pylori–associated inflammation through TLR4/NFκB signaling in vitro. Mol Med Rep. 15:3252–3258. doi:10.3892/mmr.2017.6346
  • Wang YH, Wu JJ, Lei HY. 2009. When Helicobacter pylori invades and replicates in the cells. Autophagy. 5:540–542. doi:10.4161/auto.5.4.8167
  • White JR, Winter JA, Robinson K. 2015. Differential inflammatory response to Helicobacter pylori infection: etiology and clinical outcomes. J Inflamm Res. 8:137–147.
  • Xuan J, Deguchi R, Yanagi H, Ozawa H, Urano T, Ogawa Y, Fukuda R, Kojima S, Nishina M, Sudo H, et al. 2005. Relationship between gastric mucosal IL-8 levels and histological gastritis in patients with Helicobacter pylori infection. Tokai J Exp Clin Med. 30:83–88.
  • Yamada S, Kato S, Matsuhisa T, Makonkawkeyoon L, Yoshida M, Chakrabandhu T, Lertprasertsuk N, Suttharat P, Chakrabandhu B, Nishiumi S, et al. 2013. Predominant mucosal IL-8 mRNA expression in non-cagA Thais is risk for gastric cancer. World J Gastroenterol. 19:2941–2949. doi:10.3748/wjg.v19.i19.2941
  • Yamaoka Y, Kudo T, Lu H, Casola A, Brasier AR, Graham DY. 2004. Role of Interferon-stimulated responsive element-like element in interleukin-8 promoter in Helicobacter pylori Infection. Gastroenterology. 126:1030–1043. doi:10.1053/j.gastro.2003.12.048
  • Yao Z, Fenoglio S, Gao DC, Camiolo M, Stiles B, Lindsted T, Schlederer M, Johns C, Altorki N, Mittal V, et al. 2010. TGF-beta IL-6 axis mediates selective and adaptive mechanisms of resistance to molecular targeted therapy in lung cancer. Proc Natl Acad Sci USA. 107:15535–15540. doi:10.1073/pnas.1009472107

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