Impact of 4 Lactobacillus plantarum capsular polysaccharide clusters on surface glycan composition and host cell signaling

Microbial Cell Factories

Volumn 11, Issue , 2012, Pages

  Remus, Daniela M ^a,b,c   van Kranenburg, Richard ^d   van Swam, Iris I ^a,b   Taverne, Nico ^a,c   Bongers, Roger S ^a,b   Wels, Michiel ^a,b   Wells, Jerry M ^a,c   Bron, Peter A ^a,b,e   Kleerebezem, Michiel ^a,b,c  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b NIZO FOOD RESEARCH   (Netherlands)

^c WAGENINGEN UNIVERSITY   (Netherlands)

^d Purac ^*  (Netherlands)

^e KLUYVER CENTRE FOR GENOMICS OF INDUSTRIAL FERMENTATION   (Netherlands)

Author keywords

Host cell signaling; Lactobacillus plantarum; Probiotic; Surface polysaccharides; TLR2 activation

Indexed keywords

ABC TRANSPORTER; ADHESIN; ASPARAGINE; ASPARTIC ACID; CYSTEINE; GLUTAMIC ACID; GLYCAN; GLYCOSYLTRANSFERASE; I KAPPA B; ISOMERASE; METHIONINE; POLYSACCHARIDE; PROBIOTIC AGENT; PROTEIN TYROSINE KINASE; RHAMNOSE; SERINE; TOLL LIKE RECEPTOR 2; TRANSCRIPTOME; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE N ACETYLGLUCOSAMINE 4 EPIMERASE;

AMINO ACID METABOLISM; ARTICLE; BACTERIAL GENETICS; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BIOSYNTHESIS; CHEMICAL COMPOSITION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; GENE CLUSTER; GENE DELETION; GLYCOSYLATION; HOST CELL; INTRACELLULAR SIGNALING; LACTOBACILLUS PLANTARUM; LACTOBACILLUS RHAMNOSUS; MUTATION; NONHUMAN; UPREGULATION;

BACTERIAL PROTEINS; GENE DELETION; GENE EXPRESSION PROFILING; GLYCOSYLTRANSFERASES; HEK293 CELLS; HUMANS; LACTOBACILLUS PLANTARUM; MULTIGENE FAMILY; MUTATION; NF-KAPPA B; POLYSACCHARIDES, BACTERIAL; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2;

BACTERIA (MICROORGANISMS); LACTOBACILLUS PLANTARUM;

EID: 84869232480     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/1475-2859-11-149     Document Type: Article

References (50)

1. Silhavy TJ, Kahne D, Walker S. The bacterial cell envelope. Cold Spring Harb Perspect Biol 2010, 2:a000414. 10.1101/cshperspect.a000414, 2857177, 20452953.
2. Kleerebezem M, Hols P, Bernard E, Rolain T, Zhou MM, Siezen RJ, Bron PA. The extracellular biology of the lactobacilli. FEMS Microbiol Rev 2010, 34:199-230. 10.1111/j.1574-6976.2009.00208.x, 20088967.
3. Smit G, Smit BA, Engels WJ. Flavour formation by lactic acid bacteria and biochemical flavour profiling of cheese products. FEMS Microbiol Rev 2005, 29:591-610. 10.1016/j.fmrre.2005.04.002, 15935512.
4. FAO/WHO Guidelines for the evaluation of probiotics in food 2002, London, Ontario: Report at the Joint FAO/WHO Working Group on Drafting Guidelines for the Evaluation of Probiotics in Food, FAO/WHO.
5. Van Den Berg DJC, Smits A, Pot B, Ledeboer AM, Kersters K, Verbake JMA, Verrips CT. Isolation, screening and identification of lactic acid bacteria from traditional food fermentation processes and culture collections. Food Biotechnol 1993, 7:189-205.
6. Ruas-Madiedo P, Hugenholtz J, Zoon P. An overview of the functionality of exopolysaccharides produced by lactic acid bacteria. Int Dairy J 2002, 12:163-171.
7. De Vuyst L, De Vin F, Vaningelgem F, Degeest B. Recent developments in the biosynthesis and applications of heteropolysaccharides from lactic acid bacteria. Int Dairy J 2001, 11:687-707.
8. Ismail B, Nampoothiri KM. Production, purification and structural characterization of an exopolysaccharide produced by a probiotic Lactobacillus plantarum MTCC 9510. Arch Microbiol 2010, 192:1049-1057. 10.1007/s00203-010-0636-y, 20957348.
9. De Vuyst L, Degeest B. Heteropolysaccharides from lactic acid bacteria. FEMS Microbiol Rev 1999, 23:153-177.
10. Delcour J, Ferain T, Deghorain M, Palumbo E, Hols P. The biosynthesis and functionality of the cell-wall of lactic acid bacteria. Antonie van Leeuwenhoek 1999, 76:159-184. 10.1023/A:1002089722581, 10532377.
11. van Kranenburg R, Marugg JD, Van Swam II, Willem NJ, de Vos WM. Molecular characterization of the plasmid-encoded eps gene cluster essential for exopolysaccharide biosynthesis in Lactococcus lactis. Mol Microbiol 1997, 24:387-397. 10.1046/j.1365-2958.1997.3521720.x, 9159524.
12. Péant B, LaPointe G, Gilbert C, Atlan D, Ward P, Roy D. Comparative analysis of the exopolysaccharide biosynthesis gene clusters from four strains of Lactobacillus rhamnosus. Microbiology 2005, 151:1839-1851. 10.1099/mic.0.27852-0, 15941992.
13. Bentley SD, Aanensen DM, Mavroidi A, Saunders D, Rabbinowitsch E, Collins M, Donohoe K, Harris D, Murphy L, Quail MA, et al. Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS Genet 2006, 2:e31. 10.1371/journal.pgen.0020031, 1391919, 16532061.
14. Yother J. Capsules of Streptococcus pneumoniae and other bacteria: paradigms for polysaccharide biosynthesis and regulation. Annu Rev Microbiol 2011, 65:563-581. 10.1146/annurev.micro.62.081307.162944, 21721938.
15. Petry S, Furlan S, Waghorne E, Saulnier L, Cd J, Maguin E. Comparison of the thickening properties of four Lactobacillus delbrueckii subsp. bulgaricus strains and physicochemical characterization of their exopolysaccharides. FEMS Microbiol Lett 2003, 221:285-291. 10.1016/S0378-1097(03)00214-3, 12725940.
16. Laws AP, Marshall VM. The relevance of exopolysaccharides to the rheological properties in milk fermented with ropy strains of lactic acid bacteria. Int Dairy J 2001, 11:709-722.
17. van Kranenburg R, Boels IC, Kleerebezem M, de Vos WM. Genetics and engineering of microbial exopolysaccharides for food: approaches for the production of existing and novel polysaccharides. Curr Opin Biotechnol 1999, 10:498-504. 10.1016/S0958-1669(99)00017-8, 10508628.
18. Di Cagno R, De Angelis M, Limitone A, Minervini F, Carnevali P, Corsetti A, Gaenzle M, Ciati R, Gobbetti M. Glucan and fructan production by sourdough Weissella cibaria and Lactobacillus plantarum. J Agric Food Chem 2006, 54:9873-9881. 10.1021/jf061393+, 17177514.
19. García E, Llull D, Muñoz R, Mollerach M, López R. Current trends in capsular polysaccharide biosynthesis of Streptococcus pneumoniae. Res Microbiol 2000, 151:429-435. 10.1016/S0923-2508(00)00173-X, 10961455.
20. Henrichsen J. Six newly recognized types of Streptococcus pneumoniae. J Clin Microbiol 1995, 33:2759-2762. 228570, 8567920.
21. Lebeer S, Verhoeven TLA, Francius G, Schoofs G, Lambrichts I, Dufrene Y, Vanderleyden J, De Keersmaecker SCJ. Identification of a gene cluster for the biosynthesis of a long, galactose-rich exopolysaccharide in Lactobacillus rhamnosus GG and functional analysis of the priming glycosyltransferase. Appl Environ Microbiol 2009, 75:3554-3563. 10.1128/AEM.02919-08, 2687306, 19346339.
22. Lebeer S, Claes IJJ, Verhoeven TLA, Vanderleyden J, De Keersmaecker SCJ. Exopolysaccharides of Lactobacillus rhamnosus GG form a protective shield against innate immune factors in the intestine. Microb Biotechnol 2011, 4:368-374. 10.1111/j.1751-7915.2010.00199.x, 21375696.
23. Yasuda E, Serata M, Sako T. Suppressive Effect on Activation of Macrophages by Lactobacillus casei Strain Shirota Genes Determining the Synthesis of Cell Wall-Associated Polysaccharides. Appl Environ Microbiol 2008, 74:4746-4755. 10.1128/AEM.00412-08, 2519339, 18552190.
24. Marco ML, de Vries MC, Wels M, Molenaar D, Mangell P, Ahrne S, de Vos WM, Vaughan EE, Kleerebezem M. Convergence in probiotic Lactobacillus gut-adaptive responses in humans and mice. ISME J 2010, 4:1481-1484. 10.1038/ismej.2010.61, 20505752.
25. Remus DM, Kleerebezem M, Bron PA. An intimate tête-à-tête - How probiotic lactobacilli communicate with the host. Eur J Pharmacol 2011, 668:S33-42.
26. Siezen R, van Hylckama Vlieg JE. Genomic diversity and versatility of Lactobacillus plantarum, a natural metabolic engineer. Microb Cell Fact 2011, 10:S3. 10.1186/1475-2859-10-S1-S3, 3271238, 21995294.
27. Wels M, Kleerebezem M, Siezen RJ. Unraveling the regulatory network of Lactobacillus plantarum WCFS1 2008, Wageningen, The Netherlands: Wageningen UR (University & Research centre).
28. McDougald D, Rice SA, Barraud N, Steinberg PD, Kjelleberg S. Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal. Nat Rev Microbiol 2011, 10:39-50.
29. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. Microbial biofilms. Annu Rev Microbiol 1995, 49:711-745. 10.1146/annurev.mi.49.100195.003431, 8561477.
30. Davey ME, Duncan MJ. Enhanced biofilm formation and loss of capsule synthesis: deletion of a putative glycosyltransferase in Porphyromonas gingivalisi. J Bacteriol 2006, 188:5510-5523. 10.1128/JB.01685-05, 1540017, 16855241.
31. Medvedev AE, Vogel SN. Overexpression of CD14, TLR4, and MD-2 in HEK 293T cells does not prevent induction of in vitro endotoxin tolerance. J Endotoxin Res 2003, 9:60-64.
32. Latz E, Visintin A, Lien E, Fitzgerald KA, Monks BG, Kurt-Jones EA, Golenbock DT, Espevik T. Lipopolysaccharide rapidly traffics to and from the Golgi apparatus with the toll-like receptor 4-MD-2-CD14 complex in a process that is distinct from the initiation of signal transduction. J Biol Chem 2002, 277:47834-47843. 10.1074/jbc.M207873200, 12324469.
33. Kleerebezem M, Boekhorst J, van Kranenburg R, Molenaar D, Kuipers OP, Leer R, Tarchini R, Peters SA, Sandbrink HM, Fiers M, et al. Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci U S A 2003, 100:1990-1995. 10.1073/pnas.0337704100, 149946, 12566566.
34. Siezen RJ, Francke C, Renckens B, Boekhorst J, Wels M, Kleerebezem M, van Hijum SA. Complete resequencing and reannotation of the Lactobacillus plantarum WCFS1 genome. J Bacteriol 2012, 194:195-196. 10.1128/JB.06275-11, 3256602, 22156394.
35. Teusink B, van Enckevort FHJ, Francke C, Wiersma A, Wegkamp A, Smid EJ, Siezen RJ. In silico reconstruction of the metabolic pathways of Lactobacillus plantarum: Comparing predictions of nutrient requirements with those from growth experiments. Appl Environ Microbiol 2005, 71:7253-7262. 10.1128/AEM.71.11.7253-7262.2005, 1287688, 16269766.
36. Ferain T, Garmyn D, Bernard N, Hols P, Delcour J. Lactobacillus plantarum ldhL gene: overexpression and deletion. J Bacteriol 1994, 176:596-601. 205095, 8300514.
37. Josson K, Scheirlinck T, Michiels F, Platteeuw C, Stanssens P, Joos H, Dhaese P, Zabeau M, Mahillon J. Characterization of a gram-positive broad-host-range plasmid isolated from Lactobacillus hilgardiii. Plasmid 1989, 21:9-20. 10.1016/0147-619X(89)90082-6, 2727147.
38. Lambert JM, Bongers RS, Kleerebezem M. Cre-lox-based system for multiple gene deletions and selectable-marker removal in Lactobacillus plantarum. Appl Environ Microbiol 2007, 73:1126-1135. 10.1128/AEM.01473-06, 1828656, 17142375.
39. Andre G, Deghorain M, Bron PA, van Swam II, Kleerebezem M, Hols P, Dufrene YF. Fluorescence and atomic force microscopy imaging of wall teichoic acids in Lactobacillus plantarum. ACS Chem Biol 2011, 6:366-376. 10.1021/cb1003509, 21218855.
40. Saulnier DAA, Molenaar D, de Vos WA, Gibson GR, Kolida S. Identification of prebiotic fructooligosaccharide metabolism in Lactobacillus plantarum WCFS1 through microarrays. Appl Environ Microbiol 2007, 73:1753-1765. 10.1128/AEM.01151-06, 1828832, 17261521.
41. Marco ML, Peters THF, Bongers RS, Molenaar D, van Hemert S, Sonnenburg JL, Gordon JI, Kleerebezem M. Lifestyle of Lactobacillus plantarum in the mouse caecum. Environ Microbiol 2009, 11:2747-2757. 10.1111/j.1462-2920.2009.02001.x, 2978903, 19638173.
42. Pieterse B, Jellema RH, van der Werf MJ. Quenching of microbial samples for increased reliability of microarray data. J Microbiol Methods 2006, 64:207-216. 10.1016/j.mimet.2005.04.035, 15982764.
43. Meijerink M, van Hemert S, Taverne N, Wels M, de Vos P, Bron PA, Savelkoul HF, van Bilsen J, Kleerebezem M, Wells JM. Identification of Genetic Loci in Lactobacillus plantarum That Modulate the Immune Response of Dendritic Cells Using Comparative Genome Hybridization. PLoS One 2010, 5:e10632. 10.1371/journal.pone.0010632, 2869364, 20498715.
44. Barrett T, Edgar R. Gene expression omnibus: Microarray data storage, submission, retrieval, and analysis. DNA Microarrays, Part B: Databases and Statistics 2006, 352-369. Volume 411, Methods in Enzymology.
45. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002, 30:207-210. 10.1093/nar/30.1.207, 99122, 11752295.
46. van Hijum SA, Garcia De La Nava J, Trelles O, Kok J, Kuipers OP. MicroPreP: a cDNA microarray data pre-processing framework. Appl Bioinformatics 2003, 2:241-244.
47. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 1995, 57:289-300.
48. Looijesteijn PJ, Hugenholtz J. Uncoupling of growth and exopolysaccharide production by Lactococcus lactis subsp. cremoris NIZO B40 and optimization of its synthesis. J Biosci Bioeng 1999, 88:178-182. 10.1016/S1389-1723(99)80198-4, 16232594.
49. Looijesteijn PJ, Boels IC, Kleerebezem M, Hugenholtz J. Regulation of exopolysaccharide production by Lactococcus lactis subsp. cremoris by the sugar source. Appl Environ Microbiol 1999, 65:5003-5008. 91673, 10543815.
50. Karczewski J, Troost FJ, Konings I, Dekker J, Kleerebezem M, Brummer RJM, Wells JM. Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. Am J Physiol Gastrointest Liver Physiol 2010, 298:G851-859. 10.1152/ajpgi.00327.2009, 20224007.