Oral administration of Lactobacillus salivarius inhibits the allergic airway response in mice

Canadian Journal of Microbiology

Volumn 56, Issue 5, 2010, Pages 373-379

  Li, Chia Yang ^a   Lin, Hung Chih ^b   Hsueh, Kai Chung ^b   Wu, Shu Fen ^b   Fang, Shih Hua ^c  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^b CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY OF SPORT   (Taiwan)

Author keywords

Bronchoalveolar lavage fluid; Cytokines; Lactobacillus salivarius; Probiotics

Indexed keywords

ASTHMA MODELS; BALB/C MICE; BRONCHOALVEOLAR LAVAGE FLUID; CYTOKINES; INFLAMMATORY CELLS; INFLAMMATORY DISEASE; METHACHOLINE; ORAL ADMINISTRATION; OVALBUMINS; PROBIOTICS; SPLENOCYTES; THERAPEUTIC POTENTIALS;

ANIMALS; ANTIGENS; BODY FLUIDS; FLUIDS;

DISEASES;

EOTAXIN; GAMMA INTERFERON; IMMUNOGLOBULIN E; METHACHOLINE; OVALBUMIN; PROBIOTIC AGENT; IMMUNOGLOBULIN G;

ASTHMA; BACTERIUM; DISEASE TREATMENT; INHIBITION; PROBIOTICS; PROTEIN; RODENT; SERUM;

ALLERGIC REACTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRONCHUS REACTIVITY; CONTROLLED STUDY; DRUG MECHANISM; EOSINOPHIL; FEMALE; INFLAMMATORY CELL; LACTOBACILLUS SALIVARIUS; LACTOBACILLUS SALIVARIUS PM A0006; LUNG LAVAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; TREATMENT OUTCOME; ANIMAL; ASTHMA; BAGG ALBINO MOUSE; BLOOD; BRONCHUS HYPERREACTIVITY; CHEMICALLY INDUCED; CHEMISTRY; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOLOGY; LACTOBACILLUS; MICROBIOLOGY; ORAL DRUG ADMINISTRATION;

ADMINISTRATION, ORAL; ANIMALS; ASTHMA; BRONCHIAL HYPERREACTIVITY; BRONCHOALVEOLAR LAVAGE FLUID; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; LACTOBACILLUS; MICE; MICE, INBRED BALB C; OVALBUMIN; PROBIOTICS;

ANIMALIA; LACTOBACILLUS SALIVARIUS; MUS;

EID: 77953465445     PISSN: 00084166     EISSN: None     Source Type: Journal    
DOI: 10.1139/W10-024     Document Type: Article

References (49)

1. Blümer, N., Sel, S., Virna, S., Patrascan, C.C., Zimmermann, S., Herz, U., et al. 2007. Perinatal maternal application of Lactobacillus rhamnosus GG suppresses allergic airway inflammation in mouse offspring. Clin. Exp. Allergy, 37(3): 348-357. doi:10.1111/j.1365-2222.2007.02671.x. PMID:17359385.
2. Borchers, A.T., Selmi, C., Meyers, F.J., Keen, C.L., and Gershwin, M.E. 2009. Probiotics and immunity. J. Gastroenterol. 44(1): 26-46. doi:10.1007/s00535-008-2296-0. PMID:19159071.
3. Boyle, R.J., and Tang, M.L. 2006. The role of probiotics in the management of allergic disease. Clin. Exp. Allergy, 36(5): 568-576. doi:10.1111/j.1365-2222.2006.02472.x. PMID:16650040.
4. Brusselle, G., Kips, J., Joos, G., Bluethmann, H., and Pauwels, R. 1995. Allergen-induced airway inflammation and bronchial responsiveness in wild-type and interleukin-4-deficient mice. Am. J. Respir. Cell Mol. Biol. 12(3): 254-259. PMID:7873190.
5. Cohn, L., Elias, J.A., and Chupp, G.L. 2004. Asthma: mechanisms of disease persistence and progression. Annu. Rev. Immunol. 22(1): 789-815. doi:10.1146/annurev.immunol.22.012703. 104716. PMID:15032597.
6. Del Prete, G.F., De Carli, M., D'Elios, M.M., Maestrelli, P., Ricci, M., Fabbri, L., and Romagnani, S. 1993. Allergen exposure induces the activation of allergen-specific Th2 cells in the airway mucosa of patients with allergic respiratory disorders. Eur. J. Immunol. 23(7): 1445-1449. doi:10.1002/eji. 1830230707. PMID:8100770.
7. Djukanović, R. 2000. Asthma: a disease of inflammation and repair. J. Allergy Clin. Immunol. 105(2 Pt. 2): S522-S526. doi:10.1016/S0091-6749(00) 90055-1. PMID:10669536.
8. Drago, L., Nicola, L., Iemoli, E., Banfi, G., and De Vecchi, E. 2010. Strain-dependent release of cytokines modulated by Lactobacillus salivarius human isolates in an in vitro model. BMC Res Notes, 3(1): 44. doi:10.1186/1756-0500-3-44. PMID: 20184725.
9. Feleszko, W., Jaworska, J., and Hamelmann, E. 2006. Toll-like receptors - novel targets in allergic airway disease (probiotics, friends and relatives). Eur. J. Pharmacol. 533(1-3): 308-318. doi:10.1016/j.ejphar.2005.12.062. PMID:16436277.
10. Feleszko, W., Jaworska, J., Rha, R.D., Steinhausen, S., Avagyan, A., Jaudszus, A., et al. 2007. Probiotic-induced suppression of allergic sensitization and airway inflammation is associated with an increase of T regulatory-dependent mechanisms in a murine model of asthma. Clin. Exp. Allergy, 37(4): 498-505. doi:10.1111/j.1365-2222.2006.02629.x. PMID:17430345.
11. Forsythe, P., Inman, M.D., and Bienenstock, J. 2007. Oral treatment with live Lactobacillus reuteri inhibits the allergic airway response in mice. Am. J. Respir. Crit. Care Med. 175(6): 561-569. doi:10.1164/rccm.200606-821OC. PMID:17204726.
12. Foster, P.S., Hogan, S.P., Ramsay, A.J., Matthaei, K.I., and Young, I.G. 1996. Interleukin 5 deficiency abolishes eosinophilia, airways hyperreactivity, and lung damage in a mouse asthma model. J. Exp. Med. 183(1): 195-201. doi:10.1084/jem.183.1.195. PMID:8551223.
13. Fujiwara, D., Inoue, S., Wakabayashi, H., and Fujii, T. 2004. 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. 135(3): 205-215. doi:10.1159/000081305. PMID:15467373.
14. Fuller, R. 1989. Probiotics in man and animals. J. Appl. Bacteriol. 66(5): 365-378. PMID:2666378.
15. Gionchetti, P., Rizzello, F., Helwig, U., Venturi, A., Lammers, K.M., Brigidi, P., et al. 2003. Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trial. Gastroenterology, 124(5): 1202-1209. doi:10.1016/S0016-5085(03)00171-9. PMID:12730861.
16. Grünig, G., Warnock, M., Wakil, A.E., Venkayya, R., Brombacher, F., Rennick, D.M., et al. 1998. Requirement for IL-13 independently of IL-4 in experimental asthma. Science (Washington, D.C.), 282(5397): 2261-2263. doi:10.1126/science.282.5397.2261. PMID:9856950.
17. Guarner, F., and Schaafsma, G.J. 1998. Probiotics. Int. J. Food Microbiol. 39(3): 237-238. doi:10.1016/S0168-1605(97)00136-0. PMID:9553803.
18. Hamelmann, E., Schwarze, J., Takeda, K., Oshiba, A., Larsen, G.L., Irvin, C.G., and Gelfand, E.W. 1997. Noninvasive measurement of airway responsiveness in allergic mice using barometric plethysmography. Am. J. Respir. Crit. Care Med. 156(3 Pt. 1): 766-775. PMID:9309991.
19. Hansen, G., McIntire, J.J., Yeung, V.P., Berry, G., Thorbecke, G.J., Chen, L., et al. 2000. CD4(+) T helper cells engineered to produce latent TGF-b1 reverse allergen-induced airway hyperreactivity and inflammation. J. Clin. Invest. 105(1): 61-70. doi:10. 1172/JCI7589. PMID:10619862.
20. Hatakka, K., Savilahti, E., Pönkä, A., Meurman, J.H., Poussa, T., Näse, L., et al. 2001. Effect of long term consumption of probiotic milk on infections in children attending day care centres: double blind, randomised trial. BMJ, 322(7298): 1327. doi:10.1136/bmj.322.7298.1327. PMID:11387176.
21. Hori, T., Kiyoshima, J., Shida, K., and Yasui, H. 2002. Augmentation of cellular immunity and reduction of influenza virus titer in aged mice fed Lactobacillus casei strain Shirota. Clin. Diagn. Lab. Immunol. 9(1): 105-108. PMID:11777838.
22. Hougee, S., Vriesema, A.J., Wijering, S.C., Knippels, L.M., Folkerts, G., Nijkamp, F.P., et al. 2010. Oral treatment with probiotics reduces allergic symptoms in ovalbumin-sensitized mice: a bacterial strain comparative study. Int. Arch. Allergy Immunol. 151(2): 107-117. doi:10.1159/000236000. PMID:19752564.
23. Ishida, Y., Nakamura, F., Kanzato, H., Sawada, D., Hirata, H., Nishimura, A., et al. 2005. Clinical effects of Lactobacillus acidophilus strain L-92 on perennial allergic rhinitis: a double-blind, placebo-controlled study. J. Dairy Sci. 88(2): 527-533. doi:10.3168/jds.S0022-0302(05)72714-4. PMID:15653517.
24. Isolauri, E., Salminen, S., and Ouwehand, A.C. 2004. Microbial-gut interactions in health and disease: Probiotics. Best Pract. Res. Clin. Gastroenterol. 18(2): 299-313. doi:10.1016/j.bpg.2003.10.006. PMID:15123071.
25. Kalliomäki, M., and Isolauri, E. 2003. Role of intestinal flora in the development of allergy. Curr. Opin. Allergy Clin. Immunol. 3(1): 15-20. doi:10.1097/00130832-200302000-00003. PMID: 12582309.
26. Karimi, K., Inman, M.D., Bienenstock, J., and Forsythe, P. 2009. Lactobacillus reuteri-induced regulatory T cells protect against an allergic airway response in mice. Am. J. Respir. Crit. Care Med. 179(3): 186-193. doi:10.1164/rccm.200806-951OC. PMID:19029003.
27. Kim, H., Kwack, K., Kim, D.Y., and Ji, G.E. 2005. Oral probiotic bacterial administration suppressed allergic responses in an ovalbumin- induced allergy mouse model. FEMS Immunol. Med. Microbiol. 45(2): 259-267. doi:10.1016/j.femsim.2005.05.005. PMID:15963706.
28. Kips, J.C., Brusselle, G.G., Joos, G.F., Peleman, R.A., Devos, R.R., Tavernier, J.H., and Pauwels, R.A. 1995. Importance of interleukin- 4 and interleukin-12 in allergen-induced airway changes in mice. Int. Arch. Allergy Immunol. 107(1-3): 115-118. doi:10. 1159/000236947. PMID:7613115.
29. Kruisselbrink, A., Heijne Den Bak-Glashouwer, M.J., Havenith, C.E., Thole, J.E., and Janssen, R. 2001. Recombinant Lactobacillus plantarum inhibits house dust mite-specific T-cell responses. Clin. Exp. Immunol. 126(1): 2-8. doi:10.1046/j.1365-2249.2001.01642.x. PMID:11678893.
30. Larché, M., Robinson, D.S., and Kay, A.B. 2003. The role of T lymphocytes in the pathogenesis of asthma. J. Allergy Clin. Immunol. 111(3): 450-463, quiz 464. doi:10.1067/mai.2003.169. PMID:12642820.
31. Lyons, A., O'Mahony, D., O'Brien, F., Macsharry, J., Sheil, B., Ceddia, M., et al. 2010. Bacterial strain-specific induction of Foxp3(+) T regulatory cells is protective in murine allergy models. Clin. Exp. Allergy. In press. doi:10.1111/j.1365-2222.2009. 03437.x. PMID:20067483.
32. Martinez, F.D., and Holt, P.G. 1999. Role of microbial burden in aetiology of allergy and asthma. Lancet, 354(Suppl. 2): SII12-SII15. doi:10.1016/S0140-6736(99)90437-3. PMID:10507253.
33. Meydani, S.N., and Ha, W.K. 2000. Immunologic effects of yogurt. Am. J. Clin. Nutr. 71(4): 861-872. PMID:10731490.
34. National Research Council. 1996. Guide for the care and use of laboratory animals. National Academy Press, Washington, D.C.
35. Noverr, M.C., and Huffnagle, G.B. 2004. Does the microbiota regulate immune responses outside the gut? Trends Microbiol. 12(12): 562-568. doi:10.1016/j.tim.2004.10.008. PMID: 15539116.
36. O'Mahony, L., McCarthy, J., Kelly, P., Hurley, G., Luo, F., Chen, K., et al. 2005. Lactobacillus and Bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. Gastroenterology, 128(3): 541-551. doi:10.1053/j.gastro.2004.11.050. PMID:15765388.
37. Prescott, S.L., Dunstan, J.A., Hale, J., Breckler, L., Lehmann, H., Weston, S., and Richmond, P. 2005. Clinical effects of probiotics are associated with increased interferon-g responses in very young children with atopic dermatitis. Clin. Exp. Allergy, 35(12): 1557-1564. PMID:16393321.
38. Robinson, D.S., Hamid, Q., Ying, S., Tsicopoulos, A., Barkans, J., Bentley, A.M., et al. 1992. Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N. Engl. J. Med. 326(5): 298-304. PMID:1530827.
39. Saha, S.K., Berry, M.A., Parker, D., Siddiqui, S., Morgan, A., May, R., et al. 2008. Increased sputum and bronchial biopsy IL-13 expression in severe asthma. J. Allergy Clin. Immunol. 121(3): 685-691. doi:10.1016/j.jaci.2008.01. 005. PMID:18328894.
40. Shi, H., Qin, S., Huang, G., Chen, Y., Xiao, C., Xu, H., et al. 1997. Infiltration of eosinophils into the asthmatic airways caused by interleukin 5. Am. J. Respir. Cell Mol. Biol. 16(3): 220-224. PMID:9070605.
41. Shida, K., Makino, K., Morishita, A., Takamizawa, K., Hachimura, S., Ametani, A., et al. 1998. Lactobacillus casei inhibits antigen-induced IgE secretion through regulation of cytokine production in murine splenocyte cultures. Int. Arch. Allergy Immunol. 115(4): 278-287. doi:10.1159/000069458. PMID:9566350.
42. Strickland, D.H., Stumbles, P.A., Zosky, G.R., Subrata, L.S., Thomas, J.A., Turner, D.J., et al. 2006. Reversal of airway hyperresponsiveness by induction of airway mucosal CD4+CD25+ regulatory T cells. J. Exp. Med. 203(12): 2649-2660. doi:10.1084/jem.20060155. PMID:17088431.
43. Suzuki, N., Kudo, K., Sano, Y., and Ito, K. 2001. Can Mycobacterium tuberculosis infection prevent asthma and other allergic disorders? Int. Arch. Allergy Immunol. 124(1-3): 113-116. doi:10.1159/000053686. PMID:11306944.
44. Vaarala, O. 2003. Immunological effects of probiotics with special reference to lactobacilli. Clin. Exp. Allergy, 33(12): 1634-1640. doi:10.1111/j.1365-2222.2003.01835.x. PMID:14656348.
45. Vanderhoof, J.A., and Young, R.J. 2004. Current and potential uses of probiotics. Ann. Allergy Asthma Immunol. 93(5 Suppl. 3): S33-S37. doi:10.1016/S1081-1206(10)61730-9. PMID:15562872.
46. Walker, C., Bode, E., Boer, L., Hansel, T.T., Blaser, K., and Virchow, J.C., Jr. 1992. Allergic and nonallergic asthmatics have distinct patterns of T-cell activation and cytokine production in peripheral blood and bronchoalveolar lavage. Am. Rev. Respir. Dis. 146(1): 109-115. PMID:1626792.
47. Wills-Karp, M. 1999. Immunologic basis of antigen-induced airway hyperresponsiveness. Annu. Rev. Immunol. 17(1): 255-281. doi:10.1146/annurev. immunol.17.1.255. PMID:10358759.
48. Wills-Karp, M., Luyimbazi, J., Xu, X., Schofield, B., Neben, T.Y., Karp, C.L., and Donaldson, D.D. 1998. Interleukin-13: central mediator of allergic asthma. Science (Washington, D.C.), 282(5397): 2258-2261. doi:10.1126/science. 282.5397.2258. PMID:9856949.
49. Wohlleben, G., and Erb, K.J. 2002. Inflammation versus immunoregulation: What is the key to the development of an effective antiallergy vaccine? Pathobiology, 70(5): 270-276. doi:10.1159/000070741. PMID:12771508.