Inhibition of binding of Helicobacter pylori to the glycolipid receptors by probiotic Lactobacillus reuteri

Mukai, Takao; Asasaka, Tomoko; Sato, Eri; Mori, Kenichi; Matsumoto, Mitsuyo; Ohori, Hitoshi

doi:10.1111/j.1574-695x.2002.tb00541.x

Cited by 298Probiotics and Fermented FoodsHelicobacter pylori-related gastroenterology studiesBacterial biofilms and quorum sensing

Inhibition of binding of Helicobacter pylori to the glycolipid receptors by probiotic Lactobacillus reuteri

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Mukai, Takao, Asasaka, Tomoko, Sato, Eri, Mori, Kenichi, Matsumoto, Mitsuyo, Ohori, Hitoshi·2002·FEMS Immunology & Medical Microbiology

DOI 10.1111/j.1574-695x.2002.tb00541.x

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Abstract

We examined the competition of binding of Lactobacillus reuteri and Helicobacter pylori to gangliotetraosylceramide (asialo-GM1) and sulfatide which are putative glycolipid receptor molecules of H. pylori, and identified a possible sulfatide-binding protein of the L. reuteri strain. Among nine L. reuteri strains, two (JCM1081 and TM105) were shown to bind to asialo-GM1 and sulfatide, and to inhibit binding of H. pylori to both glycolipids by a thin layer chromatogram-overlay assay using biotin-labeled bacterial cells. The extract from the bacterial cells of strain TM105 with several detergents, including octyl beta-D-glucopyranoside, retained binding to both glycolipids and also inhibited H. pylori binding, suggesting that a binding inhibitor(s) is associated with the bacterial cell surface. When the cell extract was applied to the agarose gel immobilized galactose 3-sulfate corresponding to the structure of sugar moieties of sulfatide, an approximately 47-kDa protein was found to bind to the gel. This observation strongly suggested that inhibition by selected L. reuteri strains help to prevent infection in an early stage of colonization in H. pylori and proposed that L. reuteri strains sharing glycolipid specificity with H. pylori have a potential as probiotics.

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EF-Tu has been proved to be a vital mucin adhesion factor identified at the surface of several Lactobacillus species.
“One example is EF-Tu which has been proved to be a vital mucin adhesion factor identified at the surface of several Lactobacillus species (Mukai et al., 2002; Granato et al., 2004; Dhanani and Bagchi, 2013; Nishiyama et al., 2013).”
From Adhesion and Colonization of the Probiotic Lactobacillus plantarum HC-2 in the Intestine of Litopenaeus Vannamei Are Associated With Bacterial Surface Proteins (2022) · cites this paper as Mukai et al., 2002

Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4
LAEMMLI, U. K. (1970) · Nature · doi:10.1038/227680a0 · Cited by 249,961 · see citing works
Fluorometric Deoxyribonucleic Acid-Deoxyribonucleic Acid Hybridization in Microdilution Wells as an Alternative to Membrane Filter Hybridization in which Radioisotopes Are Used To Determine Genetic Relatedness among Bacterial Strains
EZAKI, T., HASHIMOTO, Y., & Yabuuchi, E. (1989) · International Journal of Systematic Bacteriology · doi:10.1099/00207713-39-3-224 · Cited by 3,249 · see citing works
Helicobacter pylori
Dunn, B. E., Cohen, H., & Blaser, M. J. (1997) · Clinical Microbiology Reviews · doi:10.1128/cmr.10.4.720 · Cited by 1,076 · see citing works
Overview of gut flora and probiotics
Holzapfel, W. H., Haberer, P., Snel, J., Schillinger, U., & Veld, J. H. J. H. I. (1998) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(98)00044-0 · Cited by 887 · see citing works
Lactobacillus acidophilus LA 1 binds to cultured human intestinal cell lines and inhibits cell attachment and cell invasion by enterovirulent bacteria.
Bernet‐Camard, M., Brassart, D., Neeser, J., & Servin, A. L. (1994) · Gut · doi:10.1136/gut.35.4.483 · Cited by 751 · see citing works
Many pulmonary pathogenic bacteria bind specifically to the carbohydrate sequence GalNAc beta 1-4Gal found in some glycolipids.
Krivan, H. C., Roberts, D. D., & Ginsburg, V. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.16.6157 · Cited by 389 · see citing works
Emergence of DiverseHelicobacterSpecies in the Pathogenesis of Gastric and Enterohepatic Diseases
Solnick, J. V., & Schauer, D. B. (2001) · Clinical Microbiology Reviews · doi:10.1128/cmr.14.1.59-97.2001 · Cited by 352 · see citing works
Bacteriotherapy with Lactobacillus reuteri in rotavirus gastroenteritis
Shornikova, A., Casas, I. A., Mykkänen, H. M., Salo, E., & Vesikari, T. (1997) · The Pediatric Infectious Disease Journal · doi:10.1097/00006454-199712000-00002 · Cited by 319 · see citing works
Antagonistic Activity against Helicobacter Infection In Vitro and In Vivo by the Human Lactobacillus acidophilus Strain LB
Coconnier, M. H., Moal, V. L.-L., Hemery, E., & Servin, A. L. (1998) · Applied and Environmental Microbiology · doi:10.1128/aem.64.11.4573-4580.1998 · Cited by 315 · see citing works
Prevention of Helicobacter pylori infection by lactobacilli in a gnotobiotic murine model.
Kabir, A. M., Aiba, Y., Takagi, A., Kamiya, S., Miwa, T., & Koga, Y. (1997) · Gut · doi:10.1136/gut.41.1.49 · Cited by 308 · see citing works
The human Lactobacillus acidophilus strain LA1 secretes a nonbacteriocin antibacterial substance(s) active in vitro and in vivo
Bernet‐Camard, M., Moal, V. L.-L., Brassart, D., Neeser, J., Servin, A. L., & Hudault, S. (1997) · Applied and Environmental Microbiology · doi:10.1128/aem.63.7.2747-2753.1997 · Cited by 306 · see citing works
Lactic acid bacteria in health and disease.
Salminen, S., Deighton, M., & Gorbach, S. L. (1993) · Medical Entomology and Zoology · Cited by 238 · see citing works
In vitro inhibition of Helicobacter pylori NCTC 11637 by organic acids and lactic acid bacteria
Midolo, P. D., Lambert, J. R., Hull, R., Luo, F., & Grayson, M. L. (1995) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1995.tb03164.x · Cited by 228 · see citing works
Safe as mother's milk: Carbohydrates as future anti-adhesion drugs for bacterial diseases
Sharon, N., & Ofek, I. (2000) · Glycoconjugate Journal · doi:10.1023/a:1011091029973 · Cited by 193 · see citing works
Meaning and therapeutic potential of microbial recognition of host glycoconjugates
Karlsson, K. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00854.x · Cited by 170 · see citing works
Lactobacillus johnsonii La1 shares carbohydrate-binding specificities with several enteropathogenic bacteria
Neeser, J., Granato, D., Rouvet, M., Servin, A. L., Teneberg, S., & Karlsson, K. ‐. (2000) · Glycobiology · doi:10.1093/glycob/10.11.1193 · Cited by 165 · see citing works
Principles of ex ovo competitive exclusion and in ovo administration of Lactobacillus reuteri
Edens, F. W., Parkhurst, C. R., Casas, I. A., et al. (1997) · Poultry Science · doi:10.1093/ps/76.1.179 · Cited by 148 · see citing works
Acidic pH changes receptor binding specificity of Helicobacter pylori: a binary adhesion model in which surface heat shock (stress) proteins mediate sulfatide recognition in gastric colonization
Huesca, M., Borgia, S., Hoffman, P. S., et al. (1996) · Infection and Immunity · doi:10.1128/iai.64.7.2643-2648.1996 · Cited by 146 · see citing works
Identification of glycolipid receptors for Helicobacter pylori by TLC‐immunostaining
Saitoh, T., Natomi, H., Zhao, W., et al. (1991) · FEBS Letters · doi:10.1016/0014-5793(91)80519-9 · Cited by 142 · see citing works
Proteinaceous factor(s) in culture supernatant fluids of bifidobacteria which prevents the binding of enterotoxigenic Escherichia coli to gangliotetraosylceramide
Fujiwara, S., Hashiba, H., Hirota, T., & Forstner, J. (1997) · Applied and Environmental Microbiology · doi:10.1128/aem.63.2.506-512.1997 · Cited by 119 · see citing works
A collagen binding protein from Lactobacillus reuteri is part of an ABC transporter system?
Roos, S., Aleljung, P., Robert, N., Lee, B. H., Wadström, T., Lindberg, M., & Jonsson, H. (1996) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1996.tb08505.x · Cited by 117 · see citing works
Inhibition of adhesion of food-borne pathogens to Caco-2 cells by Lactobacillus strains
Todoriki, K., Mukai, T., Satô, S., et al. (2001) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2001.01371.x · Cited by 115 · see citing works
Self-citation
Role of sulfatides in adhesion of Helicobacter pylori to gastric cancer cells
Kamisago, S., Iwamori, M., Tai, T., et al. (1996) · Infection and Immunity · doi:10.1128/iai.64.2.624-628.1996 · Cited by 105 · see citing works
Effect of Lactobacillus reuteri on Intestinal Resistance to Cryptosporidium parvum Infection in a Murine Model of Acquired Immunodeficiency Syndrome
Alak, J. I. B., Wolf, B. W., Mdurvwa, E. G., et al. (1997) · The Journal of Infectious Diseases · doi:10.1093/infdis/175.1.218 · Cited by 101 · see citing works
Purification of collagen-binding proteins ofLactobacillus reuteri NCIB 11951
Aleljung, P., Shen, W., Różalska, B., Hellman, U., Ljungh, Å., & Wadström, T. (1994) · Current Microbiology · doi:10.1007/bf01575966 · Cited by 75 · see citing works
LACTIC ACID BACTERIA
Doelle, H. W. (1969) · Elsevier eBooks · doi:10.1016/b978-1-4832-3135-8.50011-4 · Cited by 65 · see citing works
Identification and characterization of a basic cell surface-located protein from Lactobacillus fermentum BR11
Turner, M. S., Timms, P., Hafner, L. M., et al. (1997) · Journal of Bacteriology · doi:10.1128/jb.179.10.3310-3316.1997 · Cited by 64 · see citing works
Autoaggregation of Lactobacillus reuteri is mediated by a putative DEAD‐box helicase
Roos, S., Lindgren, S., & Jonsson, H. (1999) · Molecular Microbiology · doi:10.1046/j.1365-2958.1999.01363.x · Cited by 58 · see citing works
Binding Specificity ofLactobacillusto Glycolipids
Yamamoto, K., Miwa, T., Taniguchi, H., Nagano, T., SHIMAMURA, K., Tanaka, T., & Kumagai, H. (1996) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1996.1630 · Cited by 55 · see citing works
Purification and characterization of a novel protein produced byBifidobacterium longumSBT2928 that inhibits the binding of enterotoxigenicEscherichia coliPb176 (CFA/II) to gangliotetraosylceramide
Fujiwara, S., Hashiba, H., Hirota, T., & Forstner, J. (1999) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.1999.00705.x · Cited by 40 · see citing works
Haemagglutination and glycolipid‐binding activities of Lactobacillus reuteri
Mukai, T., Kaneko, S., & Ohori, H. (1998) · Letters in Applied Microbiology · doi:10.1046/j.1472-765x.1998.00418.x · Cited by 28 · see citing works
Self-citation
Immunohistochemical localization of heparan sulfate proteoglycan in human gastrointestinal tract
Oshiro, M., Ono, K., Suzuki, Y., et al. (2001) · Histochemistry and Cell Biology · doi:10.1007/s004180100271 · Cited by 27 · see citing works
Comparative Analysis of Colonization of Helicobacter pylori and Glycolipids Receptor Density in Mongolian Gerbils and Mice
Osawa, H., Sugano, K., Iwamori, M., et al. (2001) · Digestive Diseases and Sciences · doi:10.1023/a:1005657708342 · Cited by 11 · see citing works

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Authors: Mukai, T., Asasaka, T., Sato, E., Mori, K., Matsumoto, M., & Ohori, H.
Affiliations: Kitasato University (JP)
Corresponding author: Mukai, Takao
ORCID: Mori, Kenichi
Venue: FEMS Immunology & Medical Microbiology
Publisher: Oxford University Press (OUP)
Published: 2002-01
Volume: 32
Issue: 2
Pages: 105-110
ISSN: 0928-8244 (ISSN-L)
1574-695X
DOI: 10.1111/j.1574-695x.2002.tb00541.x
OpenAlex: W1964021200
Cited by: 298
References: 33
Citations by year: 2026: 7 · 2025: 13 · 2024: 10 · 2023: 19 · 2022: 21 · 2021: 18 · 2020: 14 · 2019: 17 · 2018: 11 · 2017: 13 · 2016: 14 · 2015: 16 · 2014: 11 · 2013: 8 · 2012: 17
FWCI: 17.53
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: FEMS Immunology & Medical Microbiology (publishedVersion)
PubMed (publishedVersion)
Funders: Kitasato University
Topics: Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Health Sciences › Medicine › Surgery › Helicobacter pylori-related gastroenterology studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
Keywords: Helicobacter pylori, Lactobacillus reuteri, probiotics, glycolipid receptors, asialo GM1, sulfatide, bacterial cell surface, competitive inhibition, bacterial adhesion
MeSH terms: Animals, Bacterial Adhesion, G(M1) Ganglioside, Gangliosides, Glycosphingolipids, Humans, Lactobacillus, Receptors, Cell Surface, Sulfoglycosphingolipids, Helicobacter pylori, Probiotics

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Inhibition of binding of Helicobacter pylori to the glycolipid receptors by probiotic Lactobacillus reuteri

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