Aggregating Phenotype in Lactobacillus crispatus Determines Intestinal Colonization and TLR2 and TLR4 Modulation in Murine Colonic Mucosa

Voltan, Sandra; Castagliuolo, Ignazio; Elli, Marina; Longo, Stefano; Brun, Paola; D'Incà, Renata; Porzionato, Andrea; Macchi, Veronica; Palù, Giorgio; Sturniolo, Giacomo C.; Morelli, Lorenzo; Martines, Diego

doi:10.1128/cvi.00079-07

Cited by 98Probiotics and Fermented FoodsGut microbiota and healthImmune Response and Inflammation

Aggregating Phenotype in Lactobacillus crispatus Determines Intestinal Colonization and TLR2 and TLR4 Modulation in Murine Colonic Mucosa

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Voltan, Sandra, Castagliuolo, Ignazio, Elli, Marina, Longo, Stefano, Brun, Paola, D'Incà, Renata, Porzionato, Andrea, Macchi, Veronica +4 more·2007·Clinical and Vaccine Immunology

DOI 10.1128/cvi.00079-07PMC PMC2043298

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Abstract

The colonic microbiota is a major modulator of the mucosal immune system; therefore, its manipulation through supplementation with probiotics may significantly affect the host's immune responses. Since different probiotics seem to exert various effects in vivo, we tested the relevance of the autoaggregation phenotype on the intestinal persistence of lactobacilli and their ability to modulate the host's innate immune responses. After 14 days of diet supplementation, the aggregating strain Lactobacillus crispatus M247 but not aggregation-deficient isogenic mutant MU5 was recovered from the feces and colonic mucosa of mice. This observation was confirmed by strain-specific PCR amplification and by Lactobacillus -specific denaturing gradient gel electrophoresis analysis. Indeed, L. crispatus M247 increased Toll-like receptor 2 (TLR2) mRNA levels, while it reduced TLR4 mRNA and protein levels in the colonic mucosa, whereas MU5 was ineffective. In colonic epithelial cells (CMT-93 cells) L. crispatus M247 but not MU5 induced time-dependent extracellular signal-regulated kinase-1 (ERK1) tyrosine phosphorylation and TLR modulation, which were abolished in the presence of PD98059 (an ERK1 inhibitor). To assess the functional relevance of probiotic-induced TLR modulation, we determined the consequences of L. crispatus preexposure on TLR4 (lipopolysaccharide [LPS]) and TLR2 [Pam 3 Cys-Ser-(Lys) 4 ] ligand-mediated effects in intestinal epithelial cells. Preexposure to L. crispatus M247 blunted LPS-induced interleukin-6 (IL-6) release and inhibition of CMT-93 migration over a wound edge, whereas it enhanced TLR2-mediated IL-10 up-regulation. In summary, the aggregation phenotype is required for L. crispatus persistence in the colon and for modulation of TLR2/TLR4 expression through an ERK-dependent pathway. We speculate that the aggregation phenotype in L. crispatus M247 is required to temper epithelial cell responsiveness to bacterial endotoxins, which thus affects the evolution of intestinal inflammatory processes.

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Attachment of probiotic bacteria to intestinal cells can have long-term health benefits, including pathogen exclusion, immunomodulation, and the synthesis of helpful bacterial compounds.
“Attachment of probiotic bacteria to intestinal cells can have long-term health benefits, including pathogen exclusion, immunomodulation, and the synthesis of helpful bacterial compounds [6].”
From EVALUATION OF ADHESIVE AND AGGREGATION PROPERTIES OF LACTIC ACID BACTERIA ISOLATED FROM DIFFERENT BIOTOPES (2025) · cites this paper as [6]
Auto-aggregation is associated with enhanced colonization, inhibition of pathogenic infections and immunomodulation of the intestinal mucosa.
“Auto-aggregation is a desired property for probiotics which is associated with enhanced colonization, inhibition of pathogenic infections and immunomodulation of the intestinal mucosa [12, 13, 28, 43, 44].”
From Bistable auto-aggregation phenotype in Lactiplantibacillus plantarum emerges after cultivation in in vitro colonic microbiota (2021) · cites this paper as [44]

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Immuno-Modulation Properties of Lactobacillus delbrueckii
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Lactobacilli stimulate the innate immune response and modulate the TLR expression of HT29 intestinal epithelial cells in vitro
Vizoso-Pinto, M. G., Gómez, M. R., Seifert, S., Watzl, B., Holzapfel, W. H., & Franz, C. M. A. P. (2009) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2009.05.013 · Cited by 152 · see citing works

Authors: Voltan, S., Castagliuolo, I., Elli, M., Longo, S., Brun, P., D'Incà, R., Porzionato, A., Macchi, V., Palù, G., Sturniolo, G. C., Morelli, L., & Martines, D.
Affiliations: University of Padua (IT)
Department of Histology, Microbiology, and Medical Biotechnologies
Corresponding author: Castagliuolo, Ignazio
ORCID: Castagliuolo, Ignazio
Elli, Marina
Brun, Paola
Porzionato, Andrea
Macchi, Veronica
Morelli, Lorenzo
Martines, Diego
Venue: Clinical and Vaccine Immunology
Publisher: American Society for Microbiology
Published: 2007-09
Volume: 14
Issue: 9
Pages: 1138-1148
ISSN: 1556-679X (ISSN-L)
1556-6811
DOI: 10.1128/cvi.00079-07
PMC: PMC2043298
OpenAlex: W2106765603
Cited by: 96
References: 61
Citations by year: 2025: 3 · 2024: 1 · 2023: 3 · 2022: 6 · 2021: 9 · 2019: 7 · 2018: 6 · 2017: 2 · 2016: 3 · 2015: 4 · 2014: 5 · 2013: 10 · 2012: 9
FWCI: 11.39
Type: journal article
Language: en
Open access: diamond
doi.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Clinical and Vaccine Immunology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Padua Research Archive (University of Padova) (submittedVersion, other-oa)
Funders: Ministero dell’Istruzione, dell’Università e della Ricerca
Università degli Studi di Padova
Topics: Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Keywords: Lactobacillus crispatus, self-aggregation, probiotics, intestinal colonization, colonic mucosa, TLR2, TLR4, innate immunity, interleukin-6, IL-10, lipopolysaccharide, intestinal inflammation, isogenic mutants
MeSH terms: Animals, Bacterial Adhesion, DNA, Bacterial, Feces, Intestinal Mucosa, Intestines, Lactobacillus, Mice, Inbred BALB C, Phenotype, RNA, Messenger, Cytokines, Th1 Cells, Th2 Cells, Probiotics, Extracellular Signal-Regulated MAP Kinases, Toll-Like Receptor 2, Toll-Like Receptor 4, Mice

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Aggregating Phenotype in Lactobacillus crispatus Determines Intestinal Colonization and TLR2 and TLR4 Modulation in Murine Colonic Mucosa

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