Enhanced probiotic potential of Lactobacillus reuteri when delivered as a biofilm on dextranomer microspheres that contain beneficial cargo

Frontiers in Microbiology

Volumn 8, Issue MAR, 2017, Pages

  Navarro, Jason B ^a   Mashburn Warren, Lauren ^a   Bakaletz, Lauren O ^a   Bailey, Michael T ^a,b   Goodman, Steven D ^a  

^a THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^b THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

Dextranomer; Glucosyltransferase; Lactobacillus reuteri; Maltose; Microsphere; Reuterin

Indexed keywords

DEXTRANOMER; GLYCEROL; HISTAMINE; HISTIDINE; MALTOSE; MICROSPHERE; PROBIOTIC AGENT; SUCROSE;

ANTIINFLAMMATORY ACTIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL SURVIVAL; BACTERIUM ADHERENCE; BIOFILM; COLORIMETRY; CONFOCAL LASER SCANNING MICROSCOPY; CONTROLLED STUDY; ENZYMATIC ASSAY; HUMAN; HUMAN CELL; INCIDENCE; INTESTINE EPITHELIUM CELL; LACTOBACILLUS; LACTOBACILLUS REUTERI; LUCIFERASE ASSAY; NECROTIZING ENTEROCOLITIS; NONHUMAN; POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; SPECTROPHOTOMETRY; STOMACH PH;

EID: 85016548155     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.00489     Document Type: Article

References (74)

1. Agerholm-Larsen, L., Bell, M. L., Grunwald, G. K., and Astrup, A. (2000). The effect of a probiotic milk product on plasma cholesterol: a meta-analysis of short-term intervention studies. Eur. J. Clin. Nutr. 54, 856-860. doi: 10.1038/sj.ejcn.1601104
2. Araya, M., Morelli, L., Reid, G., Sanders, M. E., and Stanton, C. (2006). Probiotics in Food: Health and Nutritional Properties and Guidelines for Evaluation. Rome: Food and Agriculture Organization of the United Nations, World Health Organization
3. Arques, J. L., Fernandez, J., Gaya, P., Nunez, M., Rodriguez, E., and Medina, M. (2004). Antimicrobial activity of reuterin in combination with nisin against food-borne pathogens. Int. J. Food Microbiol. 95, 225-229. doi: 10.1016/j.ijfoodmicro.2004.03.009
4. Asmerom, M., Crowe, L., and Marin, T. (2015). Understanding the biologic therapies of probiotics, prebiotics, and synbiotics: exploring current evidence for use in premature infants for the prevention of necrotizing enterocolitis. J. Perinat. Neonatal Nurs. 29, 240-247. doi: 10.1097/JPN.0000000000000120
5. Bai, Y., van der Kaaij, R. M., Leemhuis, H., Pijning, T., van Leeuwen, S. S., Jin, Z., et al. (2015). Biochemical characterization of the Lactobacillus reuteri glycoside hydrolase family 70 GTFB type of 4,6-alpha-glucanotransferase enzymes that synthesize soluble dietary starch fibers. Appl. Environ. Microbiol. 81, 7223-7232. doi: 10.1128/AEM.01860-15
6. Cadieux, P., Wind, A., Sommer, P., Schaefer, L., Crowley, K., Britton, R. A., et al. (2008). Evaluation of reuterin production in urogenital probiotic Lactobacillus reuteri RC-14. Appl. Environ. Microbiol. 74, 4645-4649. doi: 10.1128/AEM.00139-08
7. Chang, J. C., LaSarre, B., Jimenez, J. C., Aggarwal, C., and Federle, M. J. (2011). Two group A streptococcal peptide pheromones act through opposing Rgg regulators to control biofilm development. PLoS Pathog. 7:e1002190. doi: 10.1371/journal.ppat.1002190
8. Cleusix, V., Lacroix, C., Vollenweider, S., Duboux, M., and Le Blay, G. (2007). Inhibitory activity spectrum of reuterin produced by Lactobacillus reuteri against intestinal bacteria. BMC Microbiol. 7:101. doi: 10.1186/1471-2180-7-101
9. Collins, M. D., and Gibson, G. R. (1999). Probiotics, prebiotics, and synbiotics: approaches for modulating the microbial ecology of the gut. Am. J. Clin. Nutr. 69, 1052S-1057S
10. Cook, M. T., Tzortzis, G., Charalampopoulos, D., and Khutoryanskiy, V. V. (2012). Microencapsulation of probiotics for gastrointestinal delivery. J. Control. Release 162, 56-67. doi: 10.1016/j.jconrel.2012.06.003
11. Cotter, P. D., Gahan, C. G., and Hill, C. (2001). A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid. Mol. Microbiol. 40, 465-475. doi: 10.1046/j.1365-2958.2001.02398.x
12. Danhier, F., Ansorena, E., Silva, J. M., Coco, R., Le Breton, A., and Preat, V. (2012). PLGA-based nanoparticles: an overview of biomedical applications. J. Control. Release 161, 505-522. doi: 10.1016/j.jconrel.2012.01.043
13. de Chaumont, F., Dallongeville, S., Chenouard, N., Herve, N., Pop, S., Provoost, T., et al. (2012). Icy: an open bioimage informatics platform for extended reproducible research. Nat. Methods 9, 690-696. doi: 10.1038/nmeth.2075
14. De Man, J. C., Rogosa, M., and Sharpe, M. E. (1960). A medium for the cultivation of Lactobacilli. J. Appl. Bact. 23:6. doi: 10.1111/j.1365-2672.1960.tb00188.x
15. Devaraj, A., Justice, S. S., Bakaletz, L. O., and Goodman, S. D. (2015). DNABII proteins play a central role in UPEC biofilm structure. Mol. Microbiol. 96, 1119-1135. doi: 10.1111/mmi.12994
16. de Vos, W. M. (2015). Microbial biofilms and the human intestinal microbiome. Npj Biofilms Microbio. 1:15005. doi: 10.1038/npjbiofilms.2015.5
17. de Vrese, M., and Schrezenmeir, J. (2008). Probiotics, prebiotics, and synbiotics. Adv. Biochem. Eng. Biotechnol. 111, 1-66. doi: 10.1007/10_2008_097
18. De Weirdt, R., Crabbé, A., Roos, S., Vollenweider, S., Lacroix, C., van Pijkeren, J. P., et al. (2012). Glycerol supplementation enhances L. reuteri's protective effect against S. Typhimurium colonization in a 3-D model of colonic epithelium. PLoS ONE 7:e37116. doi: 10.1371/journal.pone.0037116
19. Ding, W. K., and Shah, N. P. (2007). Acid, bile, and heat tolerance of free and microencapsulated probiotic bacteria. J. Food Sci. 72, M446-M450. doi: 10.1111/j.1750-3841.2007.00565.x
20. Dressman, J. B., Berardi, R. R., Dermentzoglou, L. C., Russell, T. L., Schmaltz, S. P., Barnett, J. L., et al. (1990). Upper gastrointestinal (GI) pH in young, healthy men and women. Pharm. Res. 7, 756-761. doi: 10.1023/A:1015827908309
21. el-Ziney, M. G., and Debevere, J. M. (1998). The effect of Reuterin on Listeria monocytogenes and Escherichia coli O157:H7 in milk and cottage cheese. J. Food Prot. 61, 1275-1280. doi: 10.4315/0362-028X-61.10.1275
22. Engels, C., Schwab, C., Zhang, J., Stevens, M. J., Bieri, C., Ebert, M. O., et al. (2016). Acrolein contributes strongly to antimicrobial and heterocyclic amine transformation activities of reuterin. Sci. Rep. 6:36246. doi: 10.1038/srep36246
23. Freire, M. O., Devaraj, A., Young, A., Navarro, J. B., Downey, J. S., Chen, C., et al. (2017). A bacterial biofilm induced oral osteolytic infection can be successfully treated by immuno-targeting an extracellular nucleoid associated protein. Mol. Oral Microbiol. 32, 74-88. doi: 10.1111/omi.12155
24. Freire, M. O., Sedghizadeh, P. P., Schaudinn, C., Gorur, A., Downey, J. S., Choi, J. H., et al. (2011). Development of an animal model for Aggregatibacter actinomycetemcomitans biofilm-mediated oral osteolytic infection: a preliminary study. J. Periodontol. 82, 778-789. doi: 10.1902/jop.2010.100263
25. Frese, S. A., Benson, A. K., Tannock, G. W., Loach, D. M., Kim, J., Zhang, M., et al. (2011). The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri. PLoS Genet. 7:e1001314. doi: 10.1371/journal.pgen.1001314
26. Ganzle, M. G., and Follador, R. (2012). Metabolism of oligosaccharides and starch in lactobacilli: a review. Front. Microbiol. 3:340. doi: 10.3389/fmicb.2012.00340
27. Gao, C., Major, A., Rendon, D., Lugo, M., Jackson, V., Shi, Z., et al. (2015). Histamine H2 receptor-mediated suppression of intestinal inflammation by probiotic Lactobacillus reuteri. MBio 6, e01358-e01315. doi: 10.1128/mBio.01358-15
28. Geier, M. S., Butler, R. N., and Howarth, G. S. (2007). Inflammatory bowel disease: current insights into pathogenesis and new therapeutic options; probiotics, prebiotics and synbiotics. Int. J. Food Microbiol. 115, 1-11. doi: 10.1016/j.ijfoodmicro.2006.10.006
29. Ghouri, Y. A., Richards, D. M., Rahimi, E. F., Krill, J. T., Jelinek, K. A., and DuPont, A. W. (2014). Systematic review of randomized controlled trials of probiotics, prebiotics, and synbiotics in inflammatory bowel disease. Clin. Exp. Gastroenterol. 7, 473-487. doi: 10.2147/CEG.S27530
30. Gomes, R., Meek, M. E., and Eggleton, M. (2002). Acrolein. Geneva: World Health Organization
31. Hall-Stoodley, L., Costerton, J. W., and Stoodley, P. (2004). Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2, 95-108. doi: 10.1038/nrmicro821
32. Heydorn, A., Nielsen, A. T., Hentzer, M., Sternberg, C., Givskov, M., Ersboll, B. K., et al. (2000). Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146, 2395-2407. doi: 10.1099/00221287-146-10-2395
33. Hoy, S. M. (2012). Dextranomer in stabilized sodium hyaluronate (Solesta(R)): in adults with faecal incontinence. Drugs 72, 1671-1678. doi: 10.2165/11209030-000000000-00000
34. Jacobsson, S., Jonsson, L., Rank, F., and Rothman, U. (1976). Studies on healing of Debrisan-treated wounds. Scand. J. Plast. Reconstr. Surg. 10, 97-101. doi: 10.3109/02844317609105196
35. Johnston, B. C., Ma, S. S. Y., Goldenberg, J. Z., Thorlund, K., Vandvik, P. O., Loeb, M., et al. (2012). Probiotics for the prevention of clostridium difficile-associated diarrhea a systematic review and meta-analysis. Ann. Intern. Med. 157, 878-U225. doi: 10.7326/0003-4819-157-12-201212180-00563
36. Jones, S. E., and Versalovic, J. (2009). Probiotic Lactobacillus reuteri biofilms produce antimicrobial and anti-inflammatory factors. BMC Microbiol. 9:35. doi: 10.1186/1471-2180-9-35
37. Kailasapathy, K. (2014). "Microencapsulation for gastrointestinal delivery of probiotic bacteria," in Nano Microencapsulation Foods, ed H.-S. Kwak (Wiley-Blackwell), 167-197. doi: 10.1002/9781118292327.ch7
38. Kralj, S., van Geel-Schutten, G. H., Dondorff, M. M. G., Kirsanovs, S., van der Maarel, M. J. E. C., and Dijkhuizen, L. (2004). Glucan synthesis in the genus Lactobacillus: isolation and characterization of glucansucrase genes, enzymes and glucan products from six different strains. Microbiology 150, 3681-3690. doi: 10.1099/mic.0.27321-0
39. Kralj, S., van Geel-Schutten, G. H., Rahaoui, H., Leer, R. J., Faber, E. J., van der Maarel, M. J., et al. (2002). Molecular characterization of a novel glucosyltransferase from Lactobacillus reuteri strain 121 synthesizing a unique, highly branched glucan with alpha-(1→4) and alpha-(1→6) glucosidic bonds. Appl. Environ. Microbiol. 68, 4283-4291. doi: 10.1128/AEM.68.9.4283-4291.2002
40. Leemhuis, H., Dijkman, W. P., Dobruchowska, J. M., Pijning, T., Grijpstra, P., Kralj, S., et al. (2013). 4,6-alpha-Glucanotransferase activity occurs more widespread in Lactobacillus strains and constitutes a separate GH70 subfamily. Appl. Microbiol. Biotechnol. 97, 181-193. doi: 10.1007/s00253-012-3943-1
41. Lukic, J., Strahinic, I., Jovcic, B., Filipic, B., Topisirovic, L., Kojic, M., et al. (2012). Different roles for lactococcal aggregation factor and mucin binding protein in adhesion to gastrointestinal mucosa. Appl. Environ. Microbiol. 78, 7993-8000. doi: 10.1128/AEM.02141-12
42. Macfarlane, S., and Dillon, J. F. (2007). Microbial biofilms in the human gastrointestinal tract. J. Appl. Microbiol. 102, 1187-1196. doi: 10.1111/j.1365-2672.2007.03287.x
43. Macfarlane, S., Woodmansey, E. J., and Macfarlane, G. T. (2005). Colonization of mucin by human intestinal bacteria and establishment of biofilm communities in a two-stage continuous culture system. Appl. Environ. Microbiol. 71, 7483-7492. doi: 10.1128/AEM.71.11.7483-7492.2005
44. Mackos, A. R., Galley, J. D., Eubank, T. D., Easterling, R. S., Parry, N. M., Fox, J. G., et al. (2016). Social stress-enhanced severity of Citrobacter rodentium-induced colitis is CCL2-dependent and attenuated by probiotic Lactobacillus reuteri. Mucosal Immunol. 9, 515-526. doi: 10.1038/mi.2015.81
45. Maintz, L., and Novak, N. (2007). Histamine and histamine intolerance. Am. J. Clin. Nutr. 85, 1185-1196
46. Mashburn-Warren, L., Morrison, D. A., and Federle, M. J. (2012). The cryptic competence pathway in Streptococcus pyogenes is controlled by a peptide pheromone. J. Bacteriol. 194, 4589-4600. doi: 10.1128/JB.00830-12
47. McFarland, L. V. (2006). Meta-analysis of probiotics for the prevention of antibiotic associated diarrhea and the treatment of Clostridium difficile disease. Am. J. Gastroenterol. 101, 812-822. doi: 10.1111/j.1572-0241.2006.00465.x
48. Merritt, J., Senpuku, H., and Kreth, J. (2016). Let there be bioluminescence: development of a biophotonic imaging platform for in situ analyses of oral biofilms in animal models. Environ. Microbiol. 18, 174-190. doi: 10.1111/1462-2920.12953
49. Miyoshi, Y., Okada, S., Uchimura, T., and Satoh, E. (2006). A mucus adhesion promoting protein, MapA, mediates the adhesion of Lactobacillus reuteri to Caco-2 human intestinal epithelial cells. Biosci. Biotechnol. Biochem. 70, 1622-1628. doi: 10.1271/bbb.50688
50. Monchois, V., Willemot, R. M., and Monsan, P. (1999). Glucansucrases: mechanism of action and structure-function relationships. FEMS Microbiol. Rev. 23, 131-151. doi: 10.1111/j.1574-6976.1999.tb00394.x
51. Mooser, G., Shur, D., Lyou, M., and Watanabe, C. (1985). Kinetic-studies on dextransucrase from the cariogenic oral bacterium streptococcus-mutans. J. Biol. Chem. 260, 6907-6915
52. Neu, J., and Walker, W. A. (2011). Necrotizing enterocolitis. N. Engl. J. Med. 364, 255-264. doi: 10.1056/NEJMra1005408
53. Nguyen, T. D. T., Kang, J. H., and Lee, M. S. (2007). Characterization of Lactobacillus plantarum PH04, a potential probiotic bacterium with cholesterol-lowering effects. Int. J. Food Microbiol. 113, 358-361. doi: 10.1016/j.ijfoodmicro.2006.08.015
54. Olson, J. K., Rager, T. M., Navarro, J. B., Mashburn-Warren, L., Goodman, S. D., and Besner, G. E. (2016). Harvesting the benefits of biofilms: a novel probiotic delivery system for the prevention of necrotizing enterocolitis. J. Pediatr. Surg. 51, 936-941. doi: 10.1016/j.jpedsurg.2016.02.062
55. Porath, J., and Flodin, P. (1959). Gel filtration: a method for desalting and group separation. Nature 183, 1657-1659. doi: 10.1038/1831657a0
56. Savino, F., Cordisco, L., Tarasco, V., Palumeri, E., Calabrese, R., Oggero, R., et al. (2010). Lactobacillus reuteri DSM 17938 in infantile colic: a randomized, double-blind, placebo-controlled trial. Pediatrics 126, e526-e533. doi: 10.1542/peds.2010-0433
57. Schaefer, L., Auchtung, T. A., Hermans, K. E., Whitehead, D., Borhan, B., and Britton, R. A. (2010). The antimicrobial compound reuterin (3-hydroxypropionaldehyde) induces oxidative stress via interaction with thiol groups. Microbiology 156(Pt 6), 1589-1599. doi: 10.1099/mic.0.035642-0
58. Schwab, C., Walter, J., Tannock, G. W., Vogel, R. F., and Ganzle, M. G. (2007). Sucrose utilization and impact of sucrose on glycosyltransferase expression in Lactobacillus reuteri. Syst. Appl. Microbiol. 30, 433-443. doi: 10.1016/j.syapm.2007.03.007
59. Soh, S. E., Aw, M., Gerez, I., Chong, Y. S., Rauff, M., Ng, Y. P. M., et al. (2009). Probiotic supplementation in the first 6 months of life in at risk Asian infants-effects on eczema and atopic sensitization at the age of 1 year. Clin. Exp. Allergy 39, 571-578. doi: 10.1111/j.1365-2222.2008.03133.x
60. Spinler, J. K., Taweechotipatr, M., Rognerud, C. L., Ou, C. N., Tumwasorn, S., and Versalovic, J. (2008). Human-derived probiotic Lactobacillus reuteri demonstrate antimicrobial activities targeting diverse enteric bacterial pathogens. Anaerobe 14, 166-171. doi: 10.1016/j.anaerobe.2008.02.001
61. Stefka, A. T., Feehley, T., Tripathi, P., Qiu, J., McCoy, K., Mazmanian, S. K., et al. (2014). Commensal bacteria protect against food allergen sensitization. Proc. Natl. Acad. Sci. U.S.A. 111, 13145-13150. doi: 10.1073/pnas.1412008111
62. Stenberg, A., and Lackgren, G. (1995). A new bioimplant for the endoscopic treatment of vesicoureteral reflux-experimental and short-term clinical-results. J. Urol. 154, 800-803. doi: 10.1016/S0022-5347(01)67168-4
63. Su, M. S., and Ganzle, M. G. (2014). Novel two-component regulatory systems play a role in biofilm formation of Lactobacillus reuteri rodent isolate 100-23. Microbiology 160(Pt 4), 795-806. doi: 10.1099/mic.0.071399-0
64. Sung, V., Hiscock, H., Tang, M. L. K., Mensah, F. K., Nation, M. L., Satzke, C., et al. (2014). Treating infant colic with the probiotic Lactobacillus reuteri: double blind, placebo controlled randomised trial. Br. Med. J. 348:g2107. doi: 10.1136/bmj.g2107
65. Talarico, T. L., Casas, I. A., Chung, T. C., and Dobrogosz, W. J. (1988). Production and isolation of reuterin, a growth inhibitor produced by Lactobacillus reuteri. Antimicrob. Agents Chemother. 32, 1854-1858. doi: 10.1128/AAC.32.12.1854
66. Thomas, C. M., Hong, T., van Pijkeren, J. P., Hemarajata, P., Trinh, D. V., Hu, W., et al. (2012). Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PLoS ONE 7:e31951. doi: 10.1371/journal.pone.0031951
67. Tieking, M., Kaditzky, S., Valcheva, R., Korakli, M., Vogel, R. F., and Ganzle, M. G. (2005). Extracellular homopolysaccharides and oligosaccharides from intestinal lactobacilli. J. Appl. Microbiol. 99, 692-702. doi: 10.1111/j.1365-2672.2005.02638.x
68. Turner, J. R. (2009). Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 9, 799-809. doi: 10.1038/nri2653
69. Updegraff, D. M. (1969). Semimicro determination of cellulose in biological materials. Anal. Biochem. 32, 420-424. doi: 10.1016/S0003-2697(69)80009-6
70. Van den Abbeele, P., Grootaert, C., Possemiers, S., Verstraete, W., Verbeken, K., and Van de Wiele, T. (2009). In vitro model to study the modulation of the mucin-adhered bacterial community. Appl. Microbiol. Biotechnol. 83, 349-359. doi: 10.1007/s00253-009-1947-2
71. van Zanten, G. C., Krych, L., Roytio, H., Forssten, S., Lahtinen, S. J., Abu Al-Soud, W., et al. (2014). Synbiotic Lactobacillus acidophilus NCFM and cellobiose does not affect human gut bacterial diversity but increases abundance of lactobacilli, bifidobacteria and branched-chain fatty acids: a randomized, double-blinded cross-over trial. FEMS Microbiol. Ecol. 90, 225-236. doi: 10.1111/1574-6941.12397
72. Venugopalan, V., Shriner, K. A., and Wong-Beringer, A. (2010). Regulatory oversight and safety of probiotic use. Emerging Infect. Dis. 16, 1661-1665. doi: 10.3201/eid1611.100574
73. Walter, J., Loach, D. M., Alqumber, M., Rockel, C., Hermann, C., Pfitzenmaier, M., et al. (2007). D-alanyl ester depletion of teichoic acids in Lactobacillus reuteri 100-23 results in impaired colonization of the mouse gastrointestinal tract. Environ. Microbiol. 9, 1750-1760. doi: 10.1111/j.1462-2920.2007.01292.x
74. Walter, J., Schwab, C., Loach, D. M., Ganzle, M. G., and Tannock, G. W. (2008). Glucosyltransferase A (GtfA) and inulosucrase (Inu) of Lactobacillus reuteri TMW1.106 contribute to cell aggregation, in vitro biofilm formation, and colonization of the mouse gastrointestinal tract. Microbiology 154(Pt 1), 72-80. doi: 10.1099/mic.0.2007/010637-0