Lactobacillus rhamnosus GG and Lactobacillus casei suppress Escherichia coli-induced chemokine expression in intestinal epithelial cells

International Archives of Allergy and Immunology

Volumn 148, Issue 1, 2008, Pages 45-58

  Toki, Shinji ^a,b   Kagaya, Shinji ^a   Shinohara, Miwa ^a,c   Wakiguchi, Hiroshi ^c   Matsumoto, Takashi ^b   Takahata, Yoshihisa ^b   Morimatsu, Fumiki ^b   Saito, Hirohisa ^a   Matsumoto, Kenji ^a  

^a NATIONAL RESEARCH INSTITUTE FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

^b NIPPON MEAT PACKERS INC   (Japan)

^c KOCHI MEDICAL SCHOOL   (Japan)

Author keywords

Chemokine; Intestinal epithelial cells; Intestinal microbiota; Lactobacillus

Indexed keywords

ATCC 53103; CASPASE RECRUITMENT DOMAIN PROTEIN 4; CHEMOKINE; FLAGELLIN; FRACTALKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN A1; HEAT SHOCK PROTEIN A6; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MESSENGER RNA; PEPTIDOGLYCAN; PROBIOTIC AGENT; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG;

ARTICLE; CELL ACTIVATION; CELL STRAIN CACO 2; COMMENSAL; CONCENTRATION (PARAMETERS); CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ESCHERICHIA COLI; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNE SYSTEM; IMMUNOREGULATION; INTESTINE EPITHELIUM CELL; LACTOBACILLUS CASEI; LACTOBACILLUS RHAMNOSUS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

BUTYRATES; CACO-2 CELLS; CHEMOKINES; EPITHELIAL CELLS; ESCHERICHIA COLI; HEAT-SHOCK PROTEINS; HUMANS; INTESTINAL MUCOSA; LACTOBACILLUS CASEI; LACTOBACILLUS RHAMNOSUS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 49849084574     PISSN: 10182438     EISSN: None     Source Type: Journal    
DOI: 10.1159/000151505     Document Type: Article

References (66)

1. Holgate ST: Genetic and environmental interaction in allergy and asthma. J Allergy Clin Immunol 1999;104:1139-1146.
2. Sengler C, Lau S, Wahn U, Nickel R: Interactions between genes and environmental factors in asthma and atopy: new developments. Respir Res 2002;3:7.
3. Strachan DP: Hay fever, hygiene, and household size. BMJ 1989;299:1259-1260.
4. von Mutius E: Infection: friend or foe in the development of atopy and asthma? The epidemiological evidence. Eur Respir J 2001;18:872-881.
5. Gehring U, Bolte G, Borte M, Bischof W, Fahlbusch B, Wichmann HE, Heinrich J: Exposure to endotoxin decreases the risk of atopic eczema in infancy: a cohort study. J Allergy Clin Immunol 2001;108:847-854.
6. Matricardi PM, Ronchetti R: Are infections protecting from atopy? Curr Opin Allergy Clin Immunol 2001;1:413-419.
7. Wold AE: The hygiene hypothesis revised:is the rising frequency of allergy due to changes in the intestinal flora? Allergy 1998;53:20-25.
8. Macpherson AJ, Harris NL: Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 2004;4:478-485.
9. Rhee KJ, Sethupathi P, Driks A, Lanning DK, Knight KL: Role of commensal bacteria in development of gut-associated lymphoid tissues and preimmune antibody repertoire. J Immunol 2004;172:1118-1124.
10. Moreau MC, Corthier G: Effect of the gastrointestinal microflora on induction and maintenance of oral tolerance to ovalbumin in C3H/HeJ mice. Infect Immun 1988;56:2766-2768.
11. Bjorksten B, Naaber P, Sepp E, Mikelsaar M: The intestinal microflora in allergic Estonian and Swedish 2-year-old children. Clin Exp Allergy 1999;29:342-346.
12. Bjorksten B, Sepp E, Julge K, Voor T, Mikelsaar M:Allergy development and the intestinal microflora during the first year of life. J Allergy Clin Immunol 2001;108:516-520.
13. Kalliomaki M, Kirjavainen P, Eerola E, Kero P, Salminen S, Isolauri E: Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J Allergy Clin Immunol 2001;107:129-134.
14. Gronlund MM, Lehtonen OP, Eerola E, Kero P: Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after cesarean delivery. J Pediatr Gastroenterol Nutr 1999;28:19-25.
15. Xu B, Pekkanen J, Hartikainen AL, Jarvelin MR:Caesarean section and risk of asthma and allergy in adulthood. J Allergy Clin Immunol 2001;107:732-733.
16. Kalliomaki M, Salminen S, Arvilommi H, Kero P, Koskinen P, Isolauri E: Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet 2001;357:1076-1079.
17. Kukkonen K, Savilahti E, Haahtela T, Juntunen-Backman K, Korpela R, Poussa T, Tuure T, Kuitunen M: Probiotics and prebiotic galacto-oligosaccharides in the prevention of allergic diseases: a randomized, double-blind, placebo-controlled trial. J Allergy Clin Immunol 2007;119:192-198.
18. Kirjavainen PV, Salminen SJ, Isolauri E: Probiotic bacteria in the management of atopic disease: underscoring the importance of viability. J Pediatr Gastroenterol Nutr 2003;36:223-227.
19. Rosenfeldt V, Benfeldt E, Nielsen SD, Michaelsen KF, Jeppesen DL, Valerius NH, Paerregaard A: Effect of probiotic Lactobacillus strains in children with atopic dermatitis. J Allergy Clin Immunol 2003;111:389-395.
20. Prescott SL, Dunstan JA, Hale J, Breckler L, Lehmann H, Weston S, Richmond P: Clinical effects of probiotics are associated with increased interferon-gamma responses in very young children with atopic dermatitis. Clin Exp Allergy 2005;35:1557-1564.
21. Taylor AL, Dunstan JA, Prescott SL: Probiotic supplementation for the first 6 months of life fails to reduce the risk of atopic dermatitis and increases the risk of allergen sensitization in high-risk children: a randomized controlled trial. J Allergy Clin Immunol 2007;119:184-191.
22. Brouwer ML, Wolt-Plompen SA, Dubois AE, van der Heide S, Jansen DF, Hoijer MA, Kauffman HF, Duiverman EJ: No effects of probiotics on atopic dermatitis in infancy: a randomized placebo-controlled trial. Clin Exp Allergy 2006;36:899-906.
23. Saavedra JM: Clinical applications of probiotic agents. Am J Clin Nutr 2001;73:1147S-1151S.
24. Pohjavuori E, Viljanen M, Korpela R, Kuitunen M, Tiittanen M, Vaarala O, Savilahti E: Lactobacillus GG effect in increasing IFN-gamma production in infants with cow's milk allergy. J Allergy Clin Immunol 2004;114:131-136.
25. Viljanen M, Kuitunen M, Haahtela T, Juntunen-Backman K, Korpela R, Savilahti E: Probiotic effects on faecal inflammatory markers and on faecal IgA in food allergic atopic eczema/dermatitis syndrome infants. Pediatr Allergy Immunol 2005;16:65-71.
26. Viljanen M, Savilahti E, Haahtela T, Juntunen-Backman K, Korpela R, Poussa T, Tuure T, Kuitunen M: Probiotics in the treatment of atopic eczema/dermatitis syndrome in infants: a double-blind placebo-controlled trial. Allergy 2005;60:494-500.
27. Weizman Z, Asli G, Alsheikh A: Effect of a probiotic infant formula on infections in child care centers: comparison of two probiotic agents. Pediatrics 2005;115:5-9.
28. Isolauri E, Arvola T, Sutas Y, Moilanen E, Salminen S: Probiotics in the management of atopic eczema. Clin Exp Allergy 2000;30:1604-1610.
29. Fujiwara D, Inoue S, Wakabayashi H, Fujii T: The anti-allergic effects of lactic acid bacteria are strain dependent and mediated by effects on both Th1/Th2 cytokine expression and balance. Int Arch Allergy Immunol 2004;135:205-215.
30. Rosenfeldt V, Benfeldt E, Valerius NH, Paerregaard A, Michaelsen KF: Effect of probiotics on gastrointestinal symptoms and small intestinal permeability in children with atopic dermatitis. J Pediatr 2004;145:612-616.
31. Helin T, Haahtela S, Haahtela T: No effect of oral treatment with an intestinal bacterial strain, Lactobacillus rhamnosus (ATCC 53103), on birch-pollen allergy: a placebo-controlled double-blind study. Allergy 2002;57:243-246.
32. Karlsson H, Larsson P, Wold AE, Rudin A: Pattern of cytokine responses to gram-positive and gram-negative commensal bacteria is profoundly changed when monocytes differentiate into dendritic cells. Infect Immun 2004;72:2671-2678.
33. Pochard P, Gosset P, Grangette C, Andre C, Tonnel AB, Pestel J, Mercenier A: Lactic acid bacteria inhibit TH2 cytokine production by mononuclear cells from allergic patients. J Allergy Clin Immunol 2002;110:617-623.
34. Niers LE, Timmerman HM, Rijkers GT, van Bleek GM, van Uden NO, Knol EF, Kapsenberg ML, Kimpen JL, Hoekstra MO: Identification of strong interleukin-10 inducing lactic acid bacteria which down-regulate T helper type 2 cytokines. Clin Exp Allergy 2005;35:1481-1489.
35. Hart AL, Lammers K, Brigidi P, Vitali B, Rizzello F, Gionchetti P, Campieri M, Kamm MA, Knight SC, Stagg AJ: Modulation of human dendritic cell phenotype and function by probiotic bacteria. Gut 2004;53:1602-1609.
36. Smith DW, Nagler-Anderson C: Preventing intolerance: the induction of nonresponsiveness to dietary and microbial antigens in the intestinal mucosa. J Immunol 2005;174:3851-3857.
37. Lan JG, Cruickshank SM, Singh JC, Farrar M, Lodge JP, Felsburg PJ, Carding SR: Different cytokine response of primary colonic epithelial cells to commensal bacteria. World J Gastroenterol 2005;11:3375-3384.
38. Sierro F, Dubois B, Coste A, Kaiserlian D, Kraehenbuhl JP, Sirard JC: Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells. Proc Natl Acad Sci USA 2001;98:13722-13727.
39. Kunkel EJ, Campbell DJ, Butcher EC: Chemokines in lymphocyte trafficking and intestinal immunity. Microcirculation 2003;10:313-323.
40. Kato A, Ogasawara T, Homma T, Batchelor J, Imai S, Wakiguchi H, Saito H, Matsumoto K: CpG oligodeoxynucleotides directly induce CXCR3 chemokines in human B cells. Biochem Biophys Res Commun 2004;320:1139-1147.
41. Kato A, Homma T, Batchelor J, Hashimoto N, Imai S, Wakiguchi H, Saito H, Matsumoto K: Interferon-alpha/beta receptor-mediated selective induction of a gene cluster by CpG oligodeoxynucleotide 2006. BMC Immunol 2003;4:8.
42. Furrie E, Macfarlane S, Thomson G, Macfarlane GT: Toll-like receptors-2, -3 and -4 expression patterns on human colon and their regulation by mucosal-associated bacteria. Immunology 2005;115:565-574.
43. Bambou JC, Giraud A, Menard S, Begue B, Rakotobe S, Heyman M, Taddei F, Cerf-Bensussan N, Gaboriau-Routhiau V: In vitro and ex vivo activation of the TLR5 signaling pathway in intestinal epithelial cells by a commensal Escherichia coli strain. J Biol Chem 2004;279:42984-42992.
44. Ono SJ, Nakamura T, Miyazaki D, Ohbayashi M, Dawson M, Toda M: Chemokines: roles in leukocyte development, trafficking, and effector function. J Allergy Clin Immunol 2003;111:1185-1199.
45. Lim HW, Lee J, Hillsamer P, Kim CH: Human Th17 cells share major trafficking receptors with both polarized effector T cells and FOXP3+ regulatory T cells. J Immunol 2008;180:122-129.
46. Hirota K, Yoshitomi H, Hashimoto M, Maeda S, Teradaira S, Sugimoto N, Yamaguchi T, Nomura T, Ito H, Nakamura T, Sakaguchi N, Sakaguchi S: Preferential recruitment of CCR6-expressing Th17 cells to inflamed joints via CCL20 in rheumatoid arthritis and its animal model. J Exp Med 2007;204:2803-2812.
47. Annunziato F, Cosmi L, Santarlasci V, Maggi L, Liotta F, Mazzinghi B, Parente E, Fili L, Ferri S, Frosali F, Giudici F, Romagnani P, Parronchi P, Tonelli F, Maggi E, Romagnani S: Phenotypic and functional features of human Th17 cells. J Exp Med 2007;204:1849-1861.
48. Suzuki S, Shimojo N, Tajiri Y, Kumemura M, Kohno Y: Differences in the composition of intestinal Bifidobacterium species and the development of allergic diseases in infants in rural Japan. Clin Exp Allergy 2007;37:506-511.
49. Fujimori S, Tatsuguchi A, Gudis K, Kishida T, Mitsui K, Ehara A, Kobayashi T, Sekita Y, Seo T, Sakamoto C: High dose probiotic and prebiotic cotherapy for remission induction of active Crohn's disease. J Gastroenterol Hepatol 2007;22:1199-1204.
50. Fajdiga S, Koninkx JF, Tooten PC, Marinsek-Logar R: Interference of Salmonella enteritidis and Lactobacillus spp. with IL-8 levels and transepithelial electrical resistance of enterocyte-like Caco-2 cells. Folia Microbiol (Praha) 2006;51:268-272.
51. Roselli M, Finamore A, Britti MS, Mengheri E:Probiotic bacteria Bifidobacterium animalis MB5 and Lactobacillus rhamnosus GG protect intestinal Caco-2 cells from the inflammation-associated response induced by enterotoxigenic Escherichia coli K88. Br J Nutr 2006;95:1177-1184.
52. Lee J, Mo JH, Katakura K, Alkalay I, Rucker AN, Liu YT, Lee HK, Shen C, Cojocaru G, Shenouda S, Kagnoff M, Eckmann L, Ben-Neriah Y, Raz E: Maintenance of colonic homeostasis by distinctive apical TLR9 signalling in intestinal epithelial cells. Nat Cell Biol 2006;8:1327-1336.
53. Kobayashi K, Inohara N, Hernandez LD, Galan JE, Nunez G, Janeway CA, Medzhitov R, Flavell RA: RICK/Rip2/CARDIAK mediates signalling for receptors of the innate and adaptive immune systems. Nature 2002;416:194-199.
54. Vidal K, Donnet-Hughes A, Granato D: Lipoteichoic acids from Lactobacillus johnsonii strain La1 and Lactobacillus acidophilus strain La10 antagonize the responsiveness of human intestinal epithelial HT29 cells to lipopolysaccharide and gram-negative bacteria. Infect Immun 2002;70:2057-2064.
55. Gusils C, Cuozzo S, Sesma F, Gonzalez S: Examination of adhesive determinants in three species of Lactobacillus isolated from chicken. Can J Microbiol 2002;48:34-42.
56. Velez MP, Verhoeven TL, Draing C, Von Aulock S, Pfitzenmaier M, Geyer A, Lambrichts I, Pot B, Vanderleyden J, De Keersmaecker SC: Functional analysis of D-alanylation of lipoteichoic acid in the probiotic strain Lactobacillus rhamnosus GG. Appl Environ Microbiol 2007;103:666-674.
57. Nemeth E, Fajdiga S, Malago J, Koninkx J, Tooten P, van Dijk J: Inhibition of Salmonella -induced IL-8 synthesis and expression of Hsp70 in enterocyte-like Caco-2 cells after exposure to non-starter lactobacilli. Int J Food Microbiol 2006;112:266-274.
58. Malago JJ, Koninkx JF, Tooten PC, van Liere EA, van Dijk JE: Anti-inflammatory properties of heat shock protein 70 and butyrate on Salmonella -induced interleukin-8 secretion in enterocyte-like Caco-2 cells. Clin Exp Immunol 2005;141:62-71.
59. Petrof EO, Kojima K, Ropeleski MJ, Musch MW, Tao Y, De Simone C, Chang EB: Probiotics inhibit nuclear factor-kappaB and induce heat shock proteins in colonic epithelial cells through proteasome inhibition. Gastroenterology 2004;127:1474-1487.
60. Duncan SH, Louis P, Flint HJ: Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl Environ Microbiol 2004;70:5810-5817.
61. Matsumoto M, Aranami A, Ishige A, Watanabe K, Benno Y: LKM512 yogurt consumption improves the intestinal environment and induces the T-helper type 1 cytokine in adult patients with intractable atopic dermatitis. Clin Exp Allergy 2007;37:358-370.
62. Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ: Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther 2008;27:104-119.
63. Zhang L, Li N, Caicedo R, Neu J: Alive and dead Lactobacillus rhamnosus GG decrease tumor necrosis factor-alpha-induced interleukin-8 production in Caco-2 cells. J Nutr 2005;135:1752-1756.
64. Tuomola EM, Salminen SJ: Adhesion of some probiotic and dairy Lactobacillus strains to Caco-2 cell cultures. Int J Food Microbiol 1998;41:45-51.
65. He F, Ouwehand AC, Isolauri E, Hashimoto H, Benno Y, Salminen S: Comparison of mucosal adhesion and species identification of bifidobacteria isolated from healthy and allergic infants. FEMS Immunol Med Microbiol 2001;30:43-47.
66. Prescott SL, Bjorksten B: Probiotics for the prevention or treatment of allergic diseases. J Allergy Clin Immunol 2007;120:255-262.