Abstract:
Many species of Lactobacillus sp. possess Surface(s) layer proteins in their envelope. Among other important characteristics S-layer from Lactobacillus acidophilus binds to the cellular receptor DC-SIGN (Dendritic Cell-Specific Intercellular adhesion molecule-3-Grabbing Non-integrin; CD209), which is involved in adhesion and infection of several families of bacteria. In this report we investigate the activity of new S-layer proteins from the Lactobacillus family (Lactobacillus acidophilus, Lactobacillus brevis, Lactobacillus helveticus and Lactobacillus kefiri) over the infection of representative microorganisms important to human health. After the treatment of DC-SIGN expressing cells with these proteins, we were able to diminish bacterial infection by up to 79% in both gram negative and mycobacterial models. We discovered that pre-treatment of the bacteria with S-layers from Lactobacillus acidophilus and Lactobacillus brevis reduced bacteria viability but also prevent infection by the pathogenic bacteria. We also proved the importance of the glycosylation of the S-layer from Lactobacillus kefiri in the binding to the receptor and thus inhibition of infection. This novel characteristic of the S-layers proteins may contribute to the already reported pathogen exclusion activity for these Lactobacillus probiotic strains; and might be also considered as a novel enzymatic antimicrobial agents to inhibit bacterial infection and entry to host cells. © 2016 Elsevier B.V.
Registro:
Documento: |
Artículo
|
Título: | S-layer proteins from Lactobacillus sp. inhibit bacterial infection by blockage of DC-SIGN cell receptor |
Autor: | Prado Acosta, M.; Ruzal, S.M.; Cordo, S.M. |
Filiación: | Laboratorio de Bacterias Gram Positivas, Departamento de Química Biológica-IQUIBICEN, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires-CONICET, Argentina Laboratorio de Virología, Departamento de Química Biológica-IQUIBICEN, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires-CONICET, Argentina
|
Palabras clave: | DC-SIGN; Lactobacillus; S-layer; bacterial protein; CD209 antigen; s layer protein; unclassified drug; antiinfective agent; cell adhesion molecule; cell surface receptor; DC-specific ICAM-3 grabbing nonintegrin; lectin; membrane protein; S-layer proteins; Article; bacterial strain; bacterial viability; bacterium adherence; controlled study; enzyme inhibition; human; human cell; in vivo study; Lactobacillus; Lactobacillus acidophilus; Lactobacillus brevis; Lactobacillus helveticus; Lactobacillus kefiri; nonhuman; protein function; protein glycosylation; protein protein interaction; 3T3 cell line; animal; Bacterial Infections; chemistry; drug effects; glycosylation; metabolism; mouse; 3T3 Cells; Animals; Anti-Bacterial Agents; Bacterial Adhesion; Bacterial Infections; Cell Adhesion Molecules; Glycosylation; Humans; Lactobacillus; Lectins, C-Type; Membrane Glycoproteins; Mice; Receptors, Cell Surface |
Año: | 2016
|
Volumen: | 92
|
Página de inicio: | 998
|
Página de fin: | 1005
|
DOI: |
http://dx.doi.org/10.1016/j.ijbiomac.2016.07.096 |
Título revista: | International Journal of Biological Macromolecules
|
Título revista abreviado: | Int. J. Biol. Macromol.
|
ISSN: | 01418130
|
CODEN: | IJBMD
|
CAS: | Anti-Bacterial Agents; Cell Adhesion Molecules; DC-specific ICAM-3 grabbing nonintegrin; Lectins, C-Type; Membrane Glycoproteins; Receptors, Cell Surface; S-layer proteins
|
Registro: | https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_01418130_v92_n_p998_PradoAcosta |
Referencias:
- Hynönen, U., Palva, A., Lactobacillus surface layer proteins: structure, function and applications (2013) Appl. Microbiol. Biotechnol., 97, pp. 5225-5243
- Engelhardt, H., Are S-layers exoskeletons? The basic function of protein surface layers revisited (2007) J. Struct. Biol., 160, pp. 115-1124
- Poppinga, L., Janesch, B., Fünfhaus, A., Sekot, G., Garcia-Gonzalez, E., Hertlein, G., Identification and functional analysis of the S-layer protein SplA of Paenibacillus larvae, the causative agent of American Foulbrood of honey bees (2012) PLoS Pathog., 8
- Sekot, G., Posch, G., Messner, P., Matejka, M., Rausch-Fan, X., Andrukhov, O., Potential of the Tannerella forsythia S-layer to delay the immune response (2011) J. Dent. Res., 90, pp. 109-114
- Settem, R.P., Honma, K., Nakajima, T., Phansopa, C., Sheffield, S., (2014), 6, pp. 415-426. , Europe PMC Funders Group Europe PMC Funders Author Manuscripts A bacterial glycan core linked to surface (S) −layer proteins modulates host immunity through Th17 suppression; Liu, Z., Shen, T., Chen, H., Zhou, Y., Zhang, P., Ma, Y., Functional characterization of MIMP for its adhesion to the intestinal epithelium (2011) Front. Biosci. (Landmark Ed.), 16, pp. 2106-2127
- Liu, Z., Shen, T., Moyer, M.P., Qin, H., Identification of the Lactobacillus SLP domain that binds gastric mucin (2011) Front. Biosci. (Landmark Ed.), 16, pp. 2128-2143
- Mastromarino, P., Cacciotti, F., Masci, A., Mosca, L., Antiviral activity of Lactobacillus brevis towards herpes simplex virus type 2: Role of cell wall associated components (2011) Anaerobe, 17, pp. 334-336
- Liu, Z., Shen, T., Zhang, P., Ma, Y., Qin, H., Lactobacillus plantarum surface layer adhesive protein protects intestinal epithelial cells against tight junction injury induced by enteropathogenic Escherichia coli (2011) Mol. Biol. Rep., 38, pp. 3471-3480
- Martinez, M.G., Prado Acosta, M., Candurra, N.A., Ruzal, S.M., S-layer proteins of Lactobacillus acidophilus inhibits JUNV infection (2012) Biochem. Biophys. Res. Commun., 422, pp. 590-595
- Alvarez, C.P., Lasala, F., Carrillo, J., Muñiz, O., Corbí, A.L., Delgado, R., C-type lectins DC-SIGN and L-SIGN mediate cellular entry by Ebola virus in cis and in trans (2002) J. Virol., 76, pp. 6841-6844
- Geijtenbeek, T.B., Kwon, D.S., Torensma, R., van Vliet, S.J., van Duijnhoven, G.C., Middel, J., DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells (2000) Cell, 100, pp. 587-597
- Martinez, M.G., Bialecki, M.A., Belouzard, S., Cordo, S.M., Candurra, N.A., Whittaker, G.R., Utilization of human DC-SIGN and L-SIGN for entry and infection of host cells by the New World arenavirus, Junín virus (2013) Biochem. Biophys. Res. Commun., 3, pp. 612-617
- Navarro-Sanchez, E., Altmeyer, R., Amara, A., Schwartz, O., Fieschi, F., Virelizier, J.L., Dendritic-cell-specific ICAM3-grabbing non-integrin is essential for the productive infection of human dendritic cells by mosquito-cell-derived dengue viruses (2003) EMBO Rep., 4, pp. 723-728
- Koppel, E.A., van Gisbergen, K.P.J.M., Geijtenbeek, T.B.H., van Kooyk, Y., Distinct functions of DC-SIGN and its homologues L-SIGN (DC-SIGNR) and mSIGNR1 in pathogen recognition and immune regulation (2005) Cell. Microbiol., 7, pp. 157-165
- Konieczna, P., Groeger, D., Ziegler, M., Frei, R., Ferstl, R., Shanahan, F., Bifidobacterium infantis 35624 administration induces Foxp3 T regulatory cells in human peripheral blood: potential role for myeloid and plasmacytoid dendritic cells (2012) Gut, 61, pp. 354-366
- Konieczna, P., Akdis, C.A., Quigley, E.M.M., Shanahan, F., O'Mahony, L., Portrait of an immunoregulatory Bifidobacterium (2012) Gut Microbes, 3, pp. 261-266
- Soilleux, E.J., DC-SIGN (dendritic cell-specific ICAM-grabbing non-integrin) and DC-SIGN-related (DC-SIGNR): friend or foe? (2003) Clin. Sci. (Lond.), 104, pp. 437-446
- Zhang, P., Snyder, S., Feng, P., Azadi, P., Zhang, S., Bulgheresi, S., Role of N-acetylglucosamine within core lipopolysaccharide of several species of gram-negative bacteria in targeting the DC-SIGN (CD209) (2006) J. Immunol., 177, pp. 4002-4011
- Klena, J., Zhang, P., Schwartz, O., Hull, S., Chen, T., The core lipopolysaccharide of Escherichia coli is a ligand for the dendritic-cell-specific intercellular adhesion molecule nonintegrin CD209 receptor (2005) J. Bacteriol., 187, pp. 1710-1715
- Iyori, M., Ohtani, M., Hasebe, A., Totsuka, Y., ichiro Shibata, K., A role of the Ca2+ binding site of DC-SIGN in the phagocytosis of E. coli (2008) Biochem. Biophys. Res. Commun., 377, pp. 367-372
- Evrard, B., Balestrino, D., Dosgilbert, A., Bouya-Gachancard, J.L.J., Charbonnel, N., Forestier, C., Roles of capsule and lipopolysaccharide O antigen in interactions of human monocyte-derived dendritic cells and Klebsiella pneumoniae (2010) Infect. Immun., 78, pp. 210-219
- Tailleux, L., Pham-Thi, N., Bergeron-Lafaurie, A., Herrmann, J.L., Charles, P., Schwartz, O., DC-SIGN induction in alveolar macrophages defines privileged target host cells for mycobacteria in patients with tuberculosis (2005) PLoS Med., 2, pp. 1269-1279
- Geijtenbeek, T.B.H., van Vliet, S.J., Koppel, E.A., Sanchez-Hernandez, M., Vandenbroucke-Grauls, C.M.J.E., Appelmelk, B., Mycobacteria target DC-SIGN to suppress dendritic cell function (2002) J. Exp. Med., 197, pp. 7-17
- Tailleux, L., Schwartz, O., Herrmann, J.L., Pivert, E., Jackson, M., Amara, A., DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells (2003) J. Exp. Med., 197, pp. 121-127
- Zhang, F., Ren, S., Zuo, Y., DC-SIGN, DC-SIGNR and LSECtin: C-Type lectins for infection (2014) Int. Rev. Immunol., 33, pp. 54-66
- Konstantinov, S.R., Smidt, H., De Vos, W.M., Bruijns, S.C.M., Kaur, S., Valence, F., S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions (2008) Proc. Natl. Acad. Sci. U. S. A., 105, pp. 19474-19479
- Winter, S.E., Winter, M.G., Poon, V., Keestra, A.M., Sterzenbach, T., Faber, F., Salmonella enterica serovar typhi conceals the invasion-associated type three secretion system from the innate immune system by gene regulation (2014) PLoS Pathog., 10
- Kakikawa, M., Yokoi, K.J., Kimoto, H., Nakano, M., Kawasaki, K., Taketo, A., Molecular analysis of the lysis protein Lys encoded by Lactobacillus plantarum phage phig1e (2002) Gene, 299, pp. 227-234
- Valence, F., Lortal, S., Zymogram and preliminary characterization of Lactobacillus helveticus autolysins (1995) Appl. Environ. Microbiol., 61, pp. 3391-3399
- Acosta, M.P., Palomino, M.M., Allievi, M.C., Rivas, C.S., Ruzal, S.M., Murein hydrolase activity in the surface layer of Lactobacillus acidophilus ATCC 4356 (2008) Appl. Environ. Microbiol., 74, pp. 7824-7827
- Tallarida R, J.L., (1979), The Dose—Response Relation in Pharmacology; Mobili, P., de los Ángeles Serradell, M., Trejo, S.A., Avilés Puigvert, F.X., Abraham, A.G., De Antoni, G.L., Heterogeneity of S-layer proteins from aggregating and non-aggregating Lactobacillus kefir strains, Antonie van Leeuwenhoek (2009) Int. J. Gen. Mol. Microbiol., 95, pp. 363-372
- Beveridge, T.J., Pouwels, P.H., Sara, M., Kotiranta, A., Lounatmaa, K., Kari, K., Functions of S-layers (1997) FEMS Microbiol. Rev., 20, pp. 99-149
- Boot, H.J., Kolen, C.P.A.M., Pouwels, P.H., Identification, cloning, and nucleotide sequence of a silent S-layer protein gene of Lactobacillus acidophilus ATCC 4356 which has extensive similarity with the S-layer protein gene of this species (1995) J. Bacteriol., 177, pp. 7222-7230
- Boot, H.J., Kolen, C.P., Interchange of the active and silent S-layer protein genes of Lactobacillus acidophilus by inversion of the chromosomal slp segment (1996) Mol. Microbiol., 21, pp. 799-809
- Ashida, N., Yanagihara, S., Shinoda, T., Characterization of adhesive molecule with affinity to Caco-2 cells in Lactobacillus acidophilus by proteome analysis (2011) J. Biosci. Bioeng., 112, pp. 333-337
- Okuda, K.I., Yanagihara, S., Sugayama, T., Zendo, T., Nakayama, J., Sonomoto, K., Functional significance of the E loop, a novel motif conserved in the lantibiotic immunity ATP-binding cassette transport systems (2010) J. Bacteriol., 192, pp. 2801-2808
- Yanagihara, S., Kato, S., Ashida, N., Lactobacillus acidophilus CP23 with weak immunomodulatory activity lacks anchoring structure for surface layer protein (2015) J. Biosci. Bioeng., 119, pp. 521-525
- Carasi, P., Racedo, S.M., Jacquot, C., Romanin, D.E., Serradell, M.A., Urdaci, M.C., Impact of kefir derived lactobacillus kefiri on the mucosal immune response and gut microbiota (2015) J. Immunol. Res., 2015
Citas:
---------- APA ----------
Prado Acosta, M., Ruzal, S.M. & Cordo, S.M.
(2016)
. S-layer proteins from Lactobacillus sp. inhibit bacterial infection by blockage of DC-SIGN cell receptor. International Journal of Biological Macromolecules, 92, 998-1005.
http://dx.doi.org/10.1016/j.ijbiomac.2016.07.096---------- CHICAGO ----------
Prado Acosta, M., Ruzal, S.M., Cordo, S.M.
"S-layer proteins from Lactobacillus sp. inhibit bacterial infection by blockage of DC-SIGN cell receptor"
. International Journal of Biological Macromolecules 92
(2016) : 998-1005.
http://dx.doi.org/10.1016/j.ijbiomac.2016.07.096---------- MLA ----------
Prado Acosta, M., Ruzal, S.M., Cordo, S.M.
"S-layer proteins from Lactobacillus sp. inhibit bacterial infection by blockage of DC-SIGN cell receptor"
. International Journal of Biological Macromolecules, vol. 92, 2016, pp. 998-1005.
http://dx.doi.org/10.1016/j.ijbiomac.2016.07.096---------- VANCOUVER ----------
Prado Acosta, M., Ruzal, S.M., Cordo, S.M. S-layer proteins from Lactobacillus sp. inhibit bacterial infection by blockage of DC-SIGN cell receptor. Int. J. Biol. Macromol. 2016;92:998-1005.
http://dx.doi.org/10.1016/j.ijbiomac.2016.07.096