The genomes of Lactobacillus casei/paracasei and Lactobacillus rhamnosus strains carry two genes encoding homologues of p40 and p75 from L. rhamnosus GG, two secreted proteins which display anti-apoptotic and cell protective effects on human intestinal epithelial cells. p40 and p75 carry cysteine, histidine-dependent aminohydrolase/peptidase (CHAP) and NLPC/P60 domains, respectively, which are characteristic of proteins with cell-wall hydrolase activity. In L. casei BL23 both proteins were secreted to the growth medium and were also located at the bacterial cell surface. The genes coding for both proteins were inactivated in this strain. Inactivation of LCABL_00230 (encoding p40) did not result in a significant difference in phenotype, whereas a mutation in LCABL_02770 (encoding p75) produced cells that formed very long chains. Purified glutathione-S-transferase (GST)-p40 and -p75 fusion proteins were able to hydrolyze the muropeptides from L. casei cell walls. Both fusions bound to mucin, collagen and to intestinal epithelial cells and, similar to L. rhamnosus GG p40, stimulated epidermal growth factor receptor phosphorylation in mouse intestine ex vivo. These results indicate that extracellular proteins belonging to the machinery of cell-wall metabolism in the closely related L. casei/paracasei-L. rhamnosus group are most likely involved in the probiotic effects described for these bacteria
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- Cell-wall hydrolases
- Acedo-Felix E, Perez-Martinez G: Significant differences between Lactobacillus casei subsp. casei ATCC 393T and a commonly used plasmid-cured derivative revealed by a polyphasic study. Int J Syst Evol Microbiol 2003;53:67–75.
- Anantharaman V, Aravind L: Evolutionary history, structural features and biochemical diversity of the NLPC/P60 superfamily of enzymes. Genome Biol 2003;4:R11.
- Atrih A, Bacher G, Allmaier G, Williamson MP, Foster SJ: Analysis of peptidoglycan structure from vegetative cells of Bacillus subtilis 168 and role of PBP 5 in peptidoglycan maturation. J Bacteriol 1999;181:3956–3966.
- Bateman A, Rawlings ND: The CHAP domain: a large family of amidases including GSP amidase and peptidoglycan hydrolases. Trends Biochem Sci 2003;28:234–237.
- Bergonzelli GE, Granato D, Pridmore RD, Marvin-Guy LF, Donnicola D, Corthesy-Theulaz IE: GroEL of Lactobacillus johnsonii La1 (NCC 533) is cell surface associated: potential role in interactions with the host and the gastric pathogen Helicobacter pylori. Infect Immun 2006;74:425–434.
- Corthesy B, Gaskins HR, Mercenier A: Cross-talk between probiotic bacteria and the host immune system. J Nutr 2007;137:781S–790S.
- Dougherty TJ: Analysis of Neisseria gonorrhoeae peptidoglycan by reverse-phase, high-pressure liquid chromatography. J Bacteriol 1985;163:69–74.
- Fadda S, Vignolo G, Holgado APR, Oliver G: Proteolytic activity of Lactobacillus strains isolated from dry fermented sausages on muscle sarcoplasmic proteins Meat Sci 1998;49:11–18.
- Foligne B, Nutten S, Grangette C, Dennin V, Goudercourt D, Poiret S, Dewulf J, Brassart D, Mercenier A, Pot B: Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World J Gastroenterol 2007;13:236–243.
- Gao LY, Pak M, Kish R, Kajihara K, Brown EJ: A mycobacterial operon essential for virulence in vivo and invasion and intracellular persistence in macrophages. Infect Immun 2006;74:1757–1767.
- Granato D, Bergonzelli GE, Pridmore RD, Marvin L, Rouvet M, Corthesy-Theulaz IE: Cell surface-associated elongation factor Tu mediates the attachment of Lactobacillus johnsonii NCC533 (La1) to human intestinal cells and mucins. Infect Immun 2004;72:2160–2169.
- Heilmann C, Hartleib J, Hussain MS, Peters G: The multifunctional Staphylococcus aureus autolysin Aaa mediates adherence to immobilized fibrinogen and fibronectin. Infect Immun 2005;73:4793–4802.
- Hörmannsperger G, Haller D: Molecular cross-talk of probiotic bacteria with the intestinal immune system: clinical relevance in the context of inflammatory bowel disease. Int J Med Microbiol 2010;300:63–73.
- Hurmalainen V, Edelman S, Antikainen J, Baumann M, Lahteenmaki K, Korhonen TK: Extracellular proteins of Lactobacillus crispatus enhance activation of human plasminogen. Microbiology 2007;153:1112–1122.
- Kinoshita H, Wakahara N, Watanabe M, Kawasaki T, Matsuo H, Kawai Y, Kitazawa H, Ohnuma S, Miura K, Horii A, Saito T: Cell surface glyceraldehyde-3-phosphate dehydrogenase (GAPdh) of Lactobacillus plantarum La 318 recognizes human A and B blood group antigens. Res Microbiol 2008;159:685–691.
- Konstantinov SR, Smidt H, de Vos WM, Bruijns SC, Singh SK, Valence F, Molle D, Lortal S, Altermann E, Klaenhammer TR, van Kooyk Y: S layer protein a of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T-cell functions. Proc Natl Acad Sci USA 2008;105:19474–19479.
- Layec S, Decaris B, Leblond-Bourget N: Diversity of firmicutes peptidoglycan hydrolases and specificities of those involved in daughter cell separation. Res Microbiol 2008;159:507–515.
- Lebeer S, Vanderleyden J, De Keersmaecker SC: Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 2008;72:728–764.
- Lebeer S, Vanderleyden J, De Keersmaecker SC: Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat Rev Microbiol 2010;8:171–184.
- Leloup L, Ehrlich SD, Zagorec M, Morel-Deville F: Single-crossover integration in the Lactobacillus sake chromosome and insertional inactivation of the ptsI and lacL genes. Appl Environ Microbiol 1997;63:2117–2123.
- Meyrand M, Boughammoura A, Courtin P, Mezange C, Guillot A, Chapot-Chartier MP: Peptidoglycan N-acetylglucosamine deacetylation decreases autolysis in Lactococcus lactis. Microbiology 2007;153:3275–3285.
- Milohanic E, Jonquieres R, Cossart P, Berche P, Gaillard JL: The autolysin Ami contributes to the adhesion of Listeria monocytogenes to eukaryotic cells via its cell wall anchor. Mol Microbiol 2001;39:1212–1224.
- Monedero V, Maze A, Boël G, Zuñiga M, Beaufils S, Hartke A, Deutscher J: The phosphotransferase system of Lactobacillus casei: regulation of carbon metabolism and connection to cold shock response. J Mol Microbiol Biotechnol 2007;12:20–32.
- Mozzi F, Savoy de Giori G, Oliver G, Font de Valdez G: Exopolysaccharide production by Lactobacillus casei under controlled pH. Biotechnol Lett 1996;18:435–439.
- Muñoz-Provencio D, Llopis M, Antolin M, de Torres I, Guarner F, Perez-Martinez G, Monedero V: Adhesion properties of Lactobacillus casei strains to resected intestinal fragments and components of the extracellular matrix. Arch Microbiol 2009;191:153–161.
- Muñoz-Provencio D, Perez-Martinez G, Monedero V: Characterization of a fibronectin-binding protein from Lactobacillus casei BL23. J Appl Microbiol 2010;108:1050–1059.
- Polk DB: Ontogenic regulation of phospholipase C-γ1 activity and expression in the rat small intestine. Gastroenterology 1994;107:109–116.
- Posno M, Leer RJ, van Luijk N, van Giezen MJ, Heuvelmans PT, Lokman BC, Pouwels PH: Incompatibility of Lactobacillus vectors with replicons derived from small cryptic Lactobacillus plasmids and segregational instability of the introduced vectors. Appl Environ Microbiol 1991;57:1822–1828.
- Ramiah K, van Reenen CA, Dicks LM: Surface-bound proteins of Lactobacillus plantarum 423 that contribute to adhesion of Caco-2 cells and their role in competitive exclusion and displacement of Clostridium sporogenes and Enterococcus faecalis. Res Microbiol 2008;159:470–475.
- Rochat T, Bermudez-Humaran L, Gratadoux JJ, Fourage C, Hoebler C, Corthier G, Langella P: Anti-inflammatory effects of Lactobacillus casei BL23 producing or not a manganese-dependant catalase on dextran sodium sulfate-induced colitis in mice. Microb Cell Fact 2007;6:22.
- Seth A, Yan F, Polk DB, Rao RK: Probiotics ameliorate the hydrogen peroxide-induced epithelial barrier disruption by a PKC- and MAP kinase-dependent mechanism. Am J Physiol 2008;294:G1060–G1069.
- Tao Y, Drabik KA, Waypa TS, Musch MW, Alverdy JC, Schneewind O, Chang EB, Petrof EO: Soluble factors from Lactobacillus GG activate MAPKs and induce cytoprotective heat-shock proteins in intestinal epithelial cells. Am J Physiol 2006;290:C1018–C1030.
- Teng F, Kawalec M, Weinstock GM, Hryniewicz W, Murray BE: An Enterococcus faecium secreted antigen, SagA, exhibits broad-spectrum binding to extracellular matrix proteins and appears essential for E. faecium growth. Infect Immun 2003;71:5033–5041.
- Vanderpool C, Yan F, Polk DB: Mechanisms of probiotic action: Implications for therapeutic applications in inflammatory bowel diseases. Inflamm Bowel Dis 2008;14:1585–1596.
- Wuenscher MD, Kohler S, Bubert A, Gerike U, Goebel W: The iap gene of Listeria monocytogenes is essential for cell viability, and its gene product, p60, has bacteriolytic activity. J Bacteriol 1993;175:3491–3501.
- Yamaguchi H, Furuhata K, Fukushima T, Yamamoto H, Sekiguchi J: Characterization of a new Bacillus subtilis peptidoglycan hydrolase gene, yvcE (named cwlO), and the enzymatic properties of its encoded protein. J Biosci Bioeng 2004;98:174–181.
- Yan F, Cao H, Cover TL, Chaturvedi MH, Washington K, Shi Y, Liu L, Wilson KT, Polk DB: Colon-specific delivery of a probiotic-derived soluble protein ameliorates intestinal inflammation in mice through an EGF receptor-dependent mechanism. 2010 (manuscript under revision).
- Yan F, Cao H, Cover TL, Whitehead R, Washington MK, Polk DB: Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 2007;132:562–575.
- Yan F, Polk DB: Probiotic bacterium prevents cytokine-induced apoptosis in intestinal epithelial cells. J Biol Chem 2002;277:50959–50965.
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Published online: December 17, 2010
Number of Print Pages : 11
Number of Figures : 8, Number of Tables : 1, Number of References : 39
Journal of Molecular Microbiology and Biotechnology
Vol. 19, No. 4, Year 2010 (Cover Date: January 2011)
Journal Editor: Saier Jr. M.H. (La Jolla, Calif.)
ISSN: 1464-1801 (Print), eISSN: 1660-2412 (Online)
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