Abstract
Lactobacillus plantarum can exert additional probiotic effects via regulation of human immune system. However, the direct interaction between probiotics and the receptors of immune cells still needs to be further studied. To identify the receptor of dendritic cells during the interaction with L. plantarum. Dendritic cells were pretreated with L. plantarum and the antibody to dendritic cells specific intercellular adhesion molecule-grabbing nonintegrin (DC-SIGN), toll like receptor (TLR)-2 and TLR-4. The maturation of immature dendritic cells, cytokine production, and modulation of T cells were studied by flow cytometry. Adherence between L. plantarum and dendritic cells were studied by ELISA, flow cytometry, and Western blot. L. plantarum could mature dendritic cells by up-regulating MHC-II and CD80 and CD86. Anti-inflammatory interlectin (IL)-10 and IL-6 was up-regulated and pro-inflammatory IL-12p70 was retro-regulated by L. plantarum. L. plantarum may interact with DC-SIGN and modulate of T to differentiate into IL-4 producing T cells. The interaction of L. plantarum and DC-SIGN and the biological effects could be blocked by EDTA and antibody to DC-SIGN. Effects of L. plantarum were concentration-dependent. L. plantarum could bind to DC-SIGN to improve DC maturation at different ratios, regulate the secretion of anti-inflammatory and pro-inflammatory cytokines, and induce the polarization of interlectin-4-producing T cells.
Similar content being viewed by others
References
Adawi D, Kasravi FB, Molin G, Jeppsson B (1997) Effect of Lactobacillus supplementation with and without arginine on liver damage and bacterial translocation in an acute liver injury model in the rat. Hepatology 25:642–647
Alverdy JC, Laughlin RS, Wu L (2003) Influence of the critically ill state on host-pathogen interactions within the intestine: gut-derived sepsis redefined. Crit Care Med 31:598–607
Bergman MP, Engering A, Smits HH, van Vliet SJ, van Bodegraven AA, Wirth HP, Kapsenberg ML, Vandenbroucke-Grauls CM, van Kooyk Y, Appelmelk BJ (2004) Helicobacter pylori modulates the T helper cell 1/T helper cell 2 balance through phase-variable interaction between lipopolysaccharide and DC-SIGN. J Exp Med 200:979–990
Cahyanto MN, Kawasaki H, Fujiyama K, Seki T (2006) Cloning of Lactobacillus plantarum IAM 12477 lysine biosynthetic genes encoding functional aspartate semialdehyde dehydrogenase, dihydrodipicolinate synthase, and dihydrodipicolinate reductase. World J Microbiol Biotechnol 22:409–416
Colmenares M, Corbi AL, Turco SJ, Rivas L (2004) The dendritic cell receptor DC-SIGN discriminates among species and life cycle forms of Leishmania. J Immunol 172:1186–1190
Ewaschuk J, Endersby R, Thiel D, Diaz H, Backer J, Ma M, Churchill T, Madsen K (2007) Probiotic bacteria prevent hepatic damage and maintain colonic barrier function in a mouse model of sepsis. Hepatology 46:841–850
Fiocchi C (2005) One commensal bacterial molecule—all we need for health? N Engl J Med 353:2078–2080
Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, Middel J, Cornelissen IL, Nottet HS, KewalRamani VN, Littman DR, Figdor CG, van Kooyk Y (2000) DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100:587–597
Geijtenbeek TB, Van Vliet SJ, Koppel EA, Sanchez-Hernandez M, Vandenbroucke-Grauls CM, Appelmelk B, Van Kooyk Y (2003) Mycobacteria target DC-SIGN to suppress dendritic cell function. J Exp Med 197:7–17
Grimbaldeston MA, Nakae S, Kalesnikoff J, Tsai M, Galli SJ (2007) Mast cell-derived interleukin 10 limits skin pathology in contact dermatitis and chronic irradiation with ultraviolet B. Nat Immunol 8:1095–1104
Gringhuis SI, den Dunnen J, Litjens M, van Het Hof B, van Kooyk Y, Geijtenbeek TB (2007) C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-kappaB. Immunity 26:605–616
Hart AL, Lammers K, Brigidi P, Vitali B, Rizzello F, Gionchetti P, Campieri M, Kamm MA, Knight SC, Stagg AJ (2004) Modulation of human dendritic cell phenotype and function by probiotic bacteria. Gut 53:1602–1609
Kabelitz D, Medzhitov R (2007) Innate immunity—cross-talk with adaptive immunity through pattern recognition receptors and cytokines. Curr Opin Immunol 19:1–3
Kelsall BL, Strober W (1996) Distinct populations of dendritic cells are present in the subepithelial dome and T cell regions of the murine Peyer’s patch. J Exp Med 183:237–247
Konstantinov SR, Smidt H, de Vos WM, Bruijns SC, Singh SK, Valence F, Molle D, Lortal S, Altermann E, Klaenhammer TR, van Kooyk Y (2008) S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proc Natl Acad Sci USA 105:19474–19479
Kraehenbuhl JP, Corbett M (2004) Immunology. Keeping the gut microflora at bay. Science 303:1624–1625
Liu CT, Hsu IT, Chou CC, Lo PR, Yu RC (2009) Exopolysaccharide production of Lactobacillus salivarius BCRC 14759 and Bifidobacterium bifidum BCRC 14615. World J Microbiol Biotechnol 25:883–890
Macpherson AJ, Uhr T (2004) Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303:1662–1665
Madsen K, Cornish A, Soper P, McKaigney C, Jijon H, Yachimec C, Doyle J, Jewell L, De Simone C (2001) Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 121:580–591
Maeda N, Nigou J, Herrmann JL, Jackson M, Amara A, Lagrange PH, Puzo G, Gicquel B, Neyrolles O (2003) The cell surface receptor DC-SIGN discriminates between Mycobacterium species through selective recognition of the mannose caps on lipoarabinomannan. J Biol Chem 278:5513–5516
Matsuzaki T, Takagi A, Ikemura H, Matsuguchi T, Yokokura T (2007) Intestinal microflora: probiotics and autoimmunity. J Nutr 137:798S–802S
Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL (2005) An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122:107–118
Mohamadzadeh M, Olson S, Kalina WV, Ruthel G, Demmin GL, Warfield KL, Bavari S, Klaenhammer TR (2005) Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization. Proc Natl Acad Sci USA 102:2880–2885
Mohamadzadeh M, Duong T, Sandwick SJ, Hoover T, Klaenhammer TR (2009) Dendritic cell targeting of Bacillus anthracis protective antigen expressed by Lactobacillus acidophilus protects mice from lethal challenge. Proc Natl Acad Sci USA 106:4331–4336
Niess JH, Brand S, Gu X, Landsman L, Jung S, McCormick BA, Vyas JM, Boes M, Ploegh HL, Fox JG, Littman DR, Reinecker HC (2005) CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307:254–258
Nuding S, Fellermann K, Wehkamp J, Stange EF (2007) Reduced mucosal antimicrobial activity in Crohn’s disease of the colon. Gut 56:1240–1247
Pamer EG (2007) Immune responses to commensal and environmental microbes. Nat Immunol 8:1173–1178
Petrof EO, Claud EC, Sun J, Abramova T, Guo Y, Waypa TS, He SM, Nakagawa Y, Chang EB (2009) Bacteria-free solution derived from Lactobacillus plantarum inhibits multiple NF-kappaB pathways and inhibits proteasome function. Inflamm Bowel Dis 15:1537–1547
Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R (2004) Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118:229–241
Reid G, Jass J, Sebulsky MT, McCormick JK (2003) Potential uses of probiotics in clinical practice. Clin Microbiol Rev 16:658–672
Rescigno M, Matteoli G (2008) Lamina propria dendritic cells: for whom the bell TOLLs? Eur J Immunol 38:1483–1486
Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R, Granucci F, Kraehenbuhl JP, Ricciardi-Castagnoli P (2001) Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2:361–367
Rhodes JM (2007) The role of Escherichia coli in inflammatory bowel disease. Gut 56:610–612
Robinson K, Chamberlain LM, Lopez MC, Rush CM, Marcotte H, Le Page RW, Wells JM (2004) Mucosal and cellular immune responses elicited by recombinant Lactococcus lactis strains expressing tetanus toxin fragment C. Infect Immun 72:2753–2761
Sallusto F, Lanzavecchia A (1994) Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med 179:1109–1118
Santosa S, Farnworth E, Jones PJ (2006) Probiotics and their potential health claims. Nutr Rev 64:265–274
Sartor RB (2004) Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology 126:1620–1633
Smits HH, Engering A, van der Kleij D, de Jong EC, Schipper K, van Capel TM, Zaat BA, Yazdanbakhsh M, Wierenga EA, van Kooyk Y, Kapsenberg ML (2005) Selective probiotic bacteria induce IL-10-producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin. J Allergy Clin Immunol 115:1260–1267
Underhill DM, Ozinsky A (2002) Toll-like receptors: key mediators of microbe detection. Curr Opin Immunol 14:103–110
van Gisbergen KP, Sanchez-Hernandez M, Geijtenbeek TB, van Kooyk Y (2005) Neutrophils mediate immune modulation of dendritic cells through glycosylation-dependent interactions between Mac-1 and DC-SIGN. J Exp Med 201:1281–1292
van Vliet SJ, den Dunnen J, Gringhuis SI, Geijtenbeek TB, van Kooyk Y (2007) Innate signaling and regulation of dendritic cell immunity. Curr Opin Immunol 19:435–440
Weis WI, Taylor ME, Drickamer K (1998) The C-type lectin superfamily in the immune system. Immunol Rev 163:19–34
Yasukawa H, Ohishi M, Mori H, Murakami M, Chinen T, Aki D, Hanada T, Takeda K, Akira S, Hoshijima M, Hirano T, Chien KR, Yoshimura A (2003) IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat Immunol 4:551–556
Zhang T, Li L, Wang XF, Zeng ZH, Hu YG, Cui ZJ (2009) Effects of Lactobacillus buchneri and Lactobacillus plantarum on fermentation, aerobic stability, bacteria diversity and ruminal degradability of alfalfa silage. World J Microbiol Biotechnol 25:965–971
Acknowledgments
The authors thank Dr. Hang Xiaomin (Institute of Science Life of Only, Shanghai Jiao Tong University, Shanghai, China) for generous provision of L. plantarum CGMCC 1258. The authors thank Shanghai Jiao Tong University Affiliated Sixth People’s Hospital for technical assistance during this study. This work was financially supported by National Natural Science Foundation of China (No. 30672044), and the National Basic Research Program of China (No. 2008CB517403).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Liu, Z., Ma, Y., Shen, T. et al. Identification of DC-SIGN as the receptor during the interaction of Lactobacillus plantarum CGMCC 1258 and dendritic cells. World J Microbiol Biotechnol 27, 603–611 (2011). https://doi.org/10.1007/s11274-010-0495-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11274-010-0495-3