Isolation of surface (S) layer protein carrying Lactobacillus species from porcine intestine and faeces and characterization of their adhesion properties to different host tissues
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Surface-layer proteins (Slps) of lactobacilli have been shown to confer tissue adherence. This study aimed to isolate and identify Slps carrying Lactobacillus species from the porcine intestine and faeces and to characterize these S-layer-expressing strains for their ability to adhere to the pig and human intestinal cells and to extracellular matrix (ECM) proteins. In total 99 strains, putatively belonging to the genus Lactobacillus, were isolated as pure cultures. SDS-PAGE and a gene probe specific for the Lactobacillus brevis ATCC 8287 S-layer protein gene (slpA) were used to screen the presence of strains possessing putative Slps. Eight of the 99 pure cultures exhibited Slps according to the SDS-PAGE analyses. In these strains the presence of genes encoding Slps was confirmed by PCR and partial sequencing. Only one isolate of the 99 strains gave a positive hybridisation signal with the L. brevis slpA probe but did not appear to produce S-layer protein. Their taxonomic identification, based on phenotyping and the 16S rRNA sequences, revealed that the eight S-layer protein-producing strains were closely related to Lactobacillus amylovorus, Lactobacillus sobrius and Lactobacillus crispatus. The strain with the slpA positive hybridisation result was identified as Lactobacillus mucosae. The SDS-extractable protein profile, the size of the putative S-layer protein and binding capability of the strains varied greatly, even among the isolates belonging to the same Lactobacillus cluster. Removal of the intact Slps from the bacterial surface by extraction with guanidine hydrochloride reduced the adhesion of some strains to fibronectin and laminin, whereas, the adhesiveness to laminin increased with some strains.
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Besides surface layer proteins, other surface structures such as lipoteichoic acids and pili, passive forces, electrostatic interactions, and hydrophobicity affect probiotics' adherence to the host.
“The literature acknowledges that besides surface layer proteins, other surface structures such as lipoteichoic acids and pili, passive forces, electrostatic interactions, and hydrophobicity affects the probiotics' adherence to the host [28,50].”
From The Biological Role of the S-Layer Produced by Lactobacillus helveticus 34.9 in Cell Protection and Its Probiotic Properties (2024) · cites this paper as [50]
Cites
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
Kos, B., Šušković, J., Vuković, S., Šimpraga, M., Frece, J., & Matošić, S. (2003) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2003.01915.x · Cited by 880 · see citing works
Functional Analysis of Putative Adhesion Factors in <i>Lactobacillus acidophilus</i> NCFM
Buck, B. L., Altermann, E., Svingerud, T., & Klaenhammer, T. R. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.12.8344-8351.2005 · Cited by 390 · see citing works
Roos, S., & Jonsson, H. (2002) · Microbiology · doi:10.1099/00221287-148-2-433 · Cited by 376 · see citing works
Post‐natal development of the porcine microbiota composition and activities
Konstantinov, S. R., Awati, A., Williams, B. A., Miller, B. G., Jones, P., Stokes, C., Akkermans, A. D. L., Smidt, H., & de Vos, W. M. (2006) · Environmental Microbiology · doi:10.1111/j.1462-2920.2006.01009.x · Cited by 350 · see citing works
Lactobacillus surface layers and their applications.
Åvall-Jääskeläinen, S., & Palva, A. (2005) · FEMS Microbiology Reviews · doi:10.1016/j.fmrre.2005.04.003 · Cited by 277 · see citing works
Self-citationJohnson-Henry, K. C., Hagen, K. E., Gordonpour, M., Tompkins, T. A., & Sherman, P. M. (2007) · Cellular Microbiology · doi:10.1111/j.1462-5822.2006.00791.x · Cited by 274 · see citing works
Lactobacillus surface layers and their applications
Åvall-Jääskeläinen, S., & Palva, A. (2005) · FEMS Microbiology Reviews · doi:10.1016/j.femsre.2005.04.003 · Cited by 262 · see citing works
Self-citationGranato, D., Perotti, F., Masserey‐Elmelegy, I., Rouvet, M., Golliard, M., Servin, A. L., & Brassart, D. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.3.1071-1077.1999 · Cited by 248 · see citing works
Lactobacilli as live vaccine delivery vectors: progress and prospects
Seegers, J. F. M. L. (2002) · Trends in biotechnology · doi:10.1016/s0167-7799(02)02075-9 · Cited by 226 · see citing works
Lactic Acid Bacteria As Live Vaccines
(2000) · Current Issues in Molecular Biology · doi:10.21775/cimb.002.017 · Cited by 193 · see citing works
Boekhorst, J., Helmer, Q., Kleerebezem, M., & Siezen, R. J. (2005) · Microbiology · doi:10.1099/mic.0.28415-0 · Cited by 191 · see citing works
Importance of S-layer proteins in probiotic activity of Lactobacillus acidophilus M92
Frece, J., Kos, B., Svetec, I., Zgaga, Z., Mrša, V., & Suskovic, J. (2005) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2004.02473.x · Cited by 179 · see citing works
Pryde, S. E., Richardson, A. J., Stewart, C. S., & Flint, H. J. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.12.5372-5377.1999 · Cited by 179 · see citing works
Antikainen, J., Anton, L., Sillanpää, J., & Korhonen, T. K. (2002) · Molecular Microbiology · doi:10.1046/j.1365-2958.2002.03180.x · Cited by 161 · see citing works
Characterization of the Collagen-Binding S-Layer Protein CbsA of Lactobacillus crispatus
Sillanpää, J., Martı́nez, B., Antikainen, J., Toba, T., Kalkkinen, N., Tankka, S., Lounatmaa, K., Keränen, J., Höök, M., Westerlund‐Wikström, B., et al. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.22.6440-6450.2000 · Cited by 157 · see citing works
MIYOSHI, Y., Okada, S., Uchimura, T., & Satoh, E. (2006) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.50688 · Cited by 139 · see citing works
Expression, secretion and antigenic variation of bacterial S‐layer proteins
Boot, H. J., & Pouwels, P. H. (1996) · Molecular Microbiology · doi:10.1046/j.1365-2958.1996.711442.x · Cited by 133 · see citing works
Boekhorst, J., Wels, M., Kleerebezem, M., & Siezen, R. J. (2006) · Microbiology · doi:10.1099/mic.0.29217-0 · Cited by 114 · see citing works
Hynönen, U., Westerlund‐Wikström, B., Palva, A., & Korhonen, T. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.12.3360-3367.2002 · Cited by 113 · see citing works
Self-citationJakava-Viljanen, M., Åvall-Jääskeläinen, S., Messner, P., Sleytr, U., & Palva, A. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.24.6786-6795.2002 · Cited by 105 · see citing works
Self-citationThe adherence of lactic acid bacteria to the columnar epithelial cells of pigs and calves
Mäyrä‐Mäukinen, A., Mnninen, M., & Gyllenberg, H. G. (1983) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1983.tb01321.x · Cited by 101 · see citing works
Åvall-Jääskeläinen, S., Lindholm, A., & Palva, A. (2003) · Applied and Environmental Microbiology · doi:10.1128/aem.69.4.2230-2236.2003 · Cited by 98 · see citing works
Self-citationSurface Display of Foreign Epitopes on the Lactobacillus brevis S-Layer
Åvall-Jääskeläinen, S., Kylä-Nikkilä, K., Kahala, M., Miikkulainen-Lahti, T., & Palva, A. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.12.5943-5951.2002 · Cited by 96 · see citing works
Self-citationEhrmann, M., Ludwig, W., & Schleifer, K. H. (1994) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1994.tb06756.x · Cited by 82 · see citing works
de Leeuw, E. D., Li, X., & Lu, W.-Y. (2006) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2006.00313.x · Cited by 73 · see citing works
Båth, K., Roos, S., Wall, T., & Jonsson, H. (2005) · FEMS Microbiology Letters · doi:10.1016/j.femsle.2005.09.042 · Cited by 62 · see citing works
Smit, E., Jager, D., Martı́nez, B., et al. (2002) · Journal of Molecular Biology · doi:10.1016/s0022-2836(02)01135-x · Cited by 52 · see citing works
Mulder, R. W. A. W., Havenaar, R., & Veld, J. H. J. H. I. (1997) · Springer eBooks · doi:10.1007/978-94-011-5860-2_8 · Cited by 50 · see citing works
Hagen, K. E., Guan, L. L., Tannock, G. W., Korver, D. R., & Allison, G. E. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.11.6633-6643.2005 · Cited by 40 · see citing works
Laitinen, R., Malinen, E., & Palva, A. M. (2002) · Systematic and Applied Microbiology · doi:10.1078/0723-2020-00118 · Cited by 28 · see citing works
Self-citationLAITINEN, R., Malinen, E., & Palva, A. M. (2002) · Systematic and Applied Microbiology · doi:10.1016/s0723-2020(04)70108-3 · Cited by 13 · see citing works
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Lactobacillus surface layer proteins: Structure, function and applications
Hynönen, U., & Palva, A. (2013) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-013-4962-2 · Cited by 283 · see citing works
Self-citationDu, Y., Li, H., Shao, J., Wu, T., Xu, W., Hu, X., & Chen, J. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.878874 · Cited by 45 · see citing works
“Several lactic acid bacteria have S-layer proteins on their surfaces, and some strains may have more than one S-layer protein on their surfaces (Sára and Sleytr, 2000), and the probiotic function of LAB S-layer protein has been reported recently, but it is not clear enough (Jakava-Viljanen and Palva, 2007).”
BackgroundUroić, K., Novak, J., Hynönen, U., Pietilä, T. E., Leboš Pavunc, A., Kant, R., Kos, B., Palva, A., & Šušković, J. (2016) · LWT - Food Science and Technology · doi:10.1016/j.lwt.2016.02.013 · Cited by 46 · see citing works
Self-citationBanić, M., Uroić, K., Leboš Pavunc, A., Novak, J., Zorić, K., Durgo, K., Petković, H., Jamnik, P., Kazazić, S., Kazazić, S., et al. (2018) · LWT · doi:10.1016/j.lwt.2018.03.054 · Cited by 35 · see citing works
Angelescu, I.-R., Zamfir, M., Ionetic, E.-C., & Grosu-Tudor, S.-S. (2024) · Fermentation · doi:10.3390/fermentation10030150 · Cited by 14 · see citing works
- Authors
- Jakava-Viljanen, M., & Palva, A.
- Affiliations
- University of Helsinki (FI)
- Corresponding author
- Jakava-Viljanen, Miia
- Venue
- Veterinary Microbiology
- Publisher
- Elsevier BV
- Published
- 2007-10
- Volume
- 124
- Issue
- 3-4
- Pages
- 264-273
- ISSN
- 0378-1135 (ISSN-L)
- OpenAlex
- W2085512170
- Cited by
- 82
- References
- 32
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 1 · 2023: 3 · 2022: 1 · 2021: 3 · 2020: 2 · 2019: 6 · 2018: 8 · 2017: 5 · 2016: 5 · 2015: 3 · 2014: 7 · 2013: 5 · 2012: 8
- FWCI
- 7.58
- Type
- journal article
- Language
- en
- Open access
- green
- hal.science
- Licence
- Locations
- Veterinary Microbiology (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- Trinity's Access to Research Output (TARA) (Trinity College Dublin) (submittedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Nutrition and Physiology
- Life Sciences › Immunology and Microbiology › Microbiology › Reproductive tract infections research
- Keywords
- surface layer protein, S-layer, Lactobacillus, porcine intestine, pig feces, bacterial adhesion, extracellular matrix proteins, fibronectin, laminin, Lactobacillus amylovorus, Lactobacillus crispatus, Lactobacillus mucosae, guanidine hydrochloride extraction, pigs
- MeSH terms
- Amino Acid Sequence, Animals, Bacterial Adhesion, Bacterial Proteins, DNA, Bacterial, DNA, Ribosomal, Electrophoresis, Polyacrylamide Gel, Feces, Humans, Intestines, Lactobacillus, Molecular Sequence Data, Phylogeny, RNA, Bacterial, RNA, Ribosomal, 16S, Swine, Polymerase Chain Reaction, Extracellular Matrix Proteins, Sequence Alignment
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