Bifidobacterium breve and Lactobacillus rhamnosus treatment is as effective as budesonide at reducing inflammation in a murine model for chronic asthma

Respiratory Research

Volumn 15, Issue 1, 2014, Pages

  Sagar, Seil ^a,b   Morgan, Mary E ^a   Chen, Si ^a   Vos, Arjan P ^b   Garssen, Johan ^a,b   van Bergenhenegouwen, Jeroen ^b   Boon, Louis ^c   Georgiou, Niki A ^b   Kraneveld, Aletta D ^a   Folkerts, Gert ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b DANONE RESEARCH   (Netherlands)

^c BIOCEROS   (Netherlands)

Author keywords

Allergic asthma; Beneficial bacteria; Glucocorticoids; Regulatory T cell

Indexed keywords

ALLERGEN; BUDESONIDE; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CASPASE RECRUITMENT DOMAIN PROTEIN 4; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 23; INTERLEUKIN 4; INTERLEUKIN 6; METHACHOLINE; MONOCYTE CHEMOTACTIC PROTEIN 1; PATTERN RECOGNITION RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 9; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR T BET; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; ANTIINFLAMMATORY AGENT;

AIRWAY REMODELING; AIRWAY SMOOTH MUSCLE CELL; ALLERGIC ASTHMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; BIFIDOBACTERIUM BREVE; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL PROLIFERATION; CONNECTIVE TISSUE CELL; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE; GENE EXPRESSION; GOBLET CELL; IMMUNE RESPONSE; LACTOBACILLUS RHAMNOSUS; LONG TERM CARE; LUNG LAVAGE; LUNG RESISTANCE; MALE; MAST CELL DEGRANULATION; MOUSE; NONHUMAN; OROPHARYNGEAL DRUG ADMINISTRATION; REGULATORY T LYMPHOCYTE; RESPIRATORY TRACT INFLAMMATION; SMOOTH MUSCLE FIBER; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH2 CELL; UPREGULATION; ANIMAL; ASTHMA; BAGG ALBINO MOUSE; BIFIDOBACTERIUM; CHRONIC DISEASE; DISEASE MODEL; MICROBIOLOGY; PATHOLOGY; PNEUMONIA; TREATMENT OUTCOME;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ASTHMA; BIFIDOBACTERIUM; BUDESONIDE; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; LACTOBACILLUS RHAMNOSUS; MALE; MICE; MICE, INBRED BALB C; PNEUMONIA; TREATMENT OUTCOME;

EID: 84901404597     PISSN: 14659921     EISSN: 1465993X     Source Type: Journal    
DOI: 10.1186/1465-9921-15-46     Document Type: Article

References (62)

1. Navarro S, Cossalter G, Chiavaroli C, Kanda A, Fleury S, Lazzari A, Cazareth J, Sparwasser T, Dombrowicz D, Glaichenhaus N, Julia V. The oral administration of bacterial extracts prevents asthma via the recruitment of regulatory T cells to the airways. Mucosal Immunol 2011, 4(1):53-65. 10.1038/mi.2010.51, 20811345.
2. McMillan SJ, Lloyd CM. Prolonged allergen challenge in mice leads to persistent airway remodelling. Clin Exp Allergy 2004, 34(3):497-507. 10.1111/j.1365-2222.2004.01895.x, 3428844, 15005746.
3. Shifren A, Witt C, Christie C, Castro M. Mechanisms of remodeling in asthmatic airways. J Allergy (Cairo) 2012, 2012:316049. Article ID 316049, 12 pages, 3270414, 22315625.
4. Cho JY. Recent advances in mechanisms and treatments of airway remodeling in asthma: message from the bench side to the clinic. Korean J Intern Med 2011, 26(4):367-383. 10.3904/kjim.2011.26.4.367, 3245385, 22205837.
5. Bai TR, Knight DA. Structural changes in the airways in asthma: observations and consequences. Clin Sci (Lond) 2005, 108(6):463-477. 10.1042/CS20040342, 15896192.
6. Amin K, Janson C, Boman G, Venge P. The extracellular deposition of mast cell products is increased in hypertrophic airways smooth muscles in allergic asthma but not in nonallergic asthma. Allergy 2005, 60(10):1241-1247. 10.1111/j.1398-9995.2005.00823.x, 16134989.
7. Brightling CE, Bradding P, Symon FA, Holgate ST, Wardlaw AJ, Pavord ID. Mast-cell infiltration of airway smooth muscle in asthma. N Engl J Med 2002, 346(22):1699-1705. 10.1056/NEJMoa012705, 12037149.
8. Romagnani S. Coming back to a missing immune deviation as the main explanatory mechanism for the hygiene hypothesis. J Allergy Clin Immunol 2007, 119(6):1511-1513. 10.1016/j.jaci.2007.04.005, 17556059.
9. Dimov VV, Casale TB. Immunomodulators for asthma. Allergy Asthma Immunol Res 2010, 2(4):228-234. 10.4168/aair.2010.2.4.228, 2946700, 20885907.
10. Pejler G, Ronnberg E, Waern I, Wernersson S. Mast cell proteases: multifaceted regulators of inflammatory disease. Blood 2010, 115(24):4981-4990. 10.1182/blood-2010-01-257287, 20233968.
11. Sugimoto K, Kudo M, Sundaram A, Ren X, Huang K, Bernstein X, Wang Y, Raymond WW, Erle DJ, Abrink, Caughey GH, Huang X, Sheppard D. The alphavbeta6 integrin modulates airway hyperresponsiveness in mice by regulating intraepithelial mast cells. J Clin Invest 2012, 122(2):748-758. 10.1172/JCI58815, 3266785, 22232213.
12. Barnes PJ. Severe asthma: advances in current management and future therapy. J Allergy Clin Immunol 2012, 129(1):48-59. 10.1016/j.jaci.2011.11.006, 22196524.
13. Southam DS, Ellis R, Wattie J, Young S, Inman MD. Budesonide prevents but does not reverse sustained airway hyperresponsiveness in mice. Eur Respir J 2008, 32(4):970-978. 10.1183/09031936.00125307, 18508821.
14. Abe A, Ohtomo T, Koyama S, Kitamura N, Kaminuma O, Mori A. Comparative analysis of steroid sensitivity of T helper cells in vitro and in vivo. Int Arch Allergy Immunol 2011, 155(Suppl 1):110-116.
15. Noverr MC, Huffnagle GB. Does the microbiota regulate immune responses outside the gut?. Trends Microbiol 2004, 12(12):562-568. 10.1016/j.tim.2004.10.008, 15539116.
16. Kranich J, Maslowski KM, Mackay CR. Commensal flora and the regulation of inflammatory and autoimmune responses. Semin Immunol 2011, 23(2):139-145. 10.1016/j.smim.2011.01.011, 21292499.
17. Georgiou NA, Garssen J, Witkamp RF. Pharma-nutrition interface: the gap is narrowing. Eur J Pharmacol 2011, 651(1-3):1-8. 10.1016/j.ejphar.2010.11.007, 21114994.
18. Vouloumanou EK, Makris GC, Karageorgopoulos DE, Falagas ME. Probiotics for the prevention of respiratory tract infections: a systematic review. Int J Antimicrob Agents 2009, 34(3):e191-e210.
19. Johannsen H, Prescott SL. Practical prebiotics, probiotics and synbiotics for allergists: how useful are they?. Clin Exp Allergy 2009, 39(12):1801-1814. 10.1111/j.1365-2222.2009.03368.x, 20085596.
20. Guarner F, Schaafsma GJ. Probiotics. Int J Food Microbiol 1998, 39(3):237-238. 10.1016/S0168-1605(97)00136-0, 9553803.
21. Gourbeyre P, Denery S, Bodinier M. Probiotics, prebiotics, and synbiotics: impact on the gut immune system and allergic reactions. J Leukoc Biol 2011, 89(5):685-695. 10.1189/jlb.1109753, 21233408.
22. Ezendam J, de Klerk A, Gremmer ER, van Loveren H. Effects of Bifidobacterium animalis administered during lactation on allergic and autoimmune responses in rodents. Clin Exp Immunol 2008, 154(3):424-431. 10.1111/j.1365-2249.2008.03788.x, 2633237, 19037925.
23. Hougee S, Vriesema AJ, Wijering SC, Knippels LM, Folkerts G, Nijkamp FP, Knol J, Garssen J. Oral treatment with probiotics reduces allergic symptoms in ovalbumin-sensitized mice: a bacterial strain comparative study. Int Arch Allergy Immunol 2010, 151(2):107-117. 10.1159/000236000, 19752564.
24. Forsythe P, Inman MD, Bienenstock J. Oral treatment with live Lactobacillus reuteri inhibits the allergic airway response in mice. Am J Respir Crit Care Med 2007, 175(6):561-569. 10.1164/rccm.200606-821OC, 17204726.
25. Eder W, Klimecki W, Yu L, von Mutius E, Riedler J, Braun-Fahrlander C, Nowak D, Holst O, Martinez FD. Association between exposure to farming, allergies and genetic variation in CARD4/NOD1. Allergy 2006, 61(9):1117-1124. 10.1111/j.1398-9995.2006.01128.x, 16918516.
26. Nonaka Y, Izumo T, Izumi F, Maekawa T, Shibata H, Nakano A, Kishi A, Akatani K, Kiso Y. Antiallergic effects of Lactobacillus pentosus strain S-PT84 mediated by modulation of Th1/Th2 immunobalance and induction of IL-10 production. Int Arch Allergy Immunol 2008, 145(3):249-257. 10.1159/000109294, 17914277.
27. Kalliomaki M, Antoine JM, Herz U, Rijkers GT, Wells JM, Mercenier A. Guidance for substantiating the evidence for beneficial effects of probiotics: prevention and management of allergic diseases by probiotics. J Nutr 2010, 140(3):713S-721S. 10.3945/jn.109.113761, 20130079.
28. Chen K, Xiang Y, Yao X, Liu Y, Gong W, Yoshimura T, Wang JM. The active contribution of Toll-like receptors to allergic airway inflammation. Int Immunopharmacol 2011, 11(10):1391-1398. 10.1016/j.intimp.2011.05.003, 21624504.
29. Uehara A, Fujimoto Y, Fukase K, Takada H. Various human epithelial cells express functional Toll-like receptors, NOD1 and NOD2 to produce anti-microbial peptides, but not proinflammatory cytokines. Mol Immunol 2007, 44(12):3100-3111. 10.1016/j.molimm.2007.02.007, 17403538.
30. Barnes PJ. The cytokine network in chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 2009, 41(6):631-638. 10.1165/rcmb.2009-0220TR, 19717810.
31. Boyce JA, Bochner B, Finkelman FD, Rothenberg ME. Advances in mechanisms of asthma, allergy, and immunology in 2011. J Allergy Clin Immunol 2011, 129(2):335-341.
32. Heine H. TLRs, NLRs and RLRs: innate sensors and their impact on allergic diseases--a current view. Immunol Lett 2011, 139(1-2):14-24. 10.1016/j.imlet.2011.04.010, 21554901.
33. Eder W, Klimecki W, Yu L, von Mutius E, Riedler J, Braun-Fahrlander C, Nowak D, Martinez FD. Toll-like receptor 2 as a major gene for asthma in children of European farmers. J Allergy Clin Immunol 2004, 113(3):482-488. 10.1016/j.jaci.2003.12.374, 15007351.
34. Reijmerink NE, Bottema RW, Kerkhof M, Gerritsen J, Stelma FF, Thijs C, van Schayck CP, Smit HA, Brunekreef B, Koppelman GH, Postma DS. TLR-related pathway analysis: novel gene-gene interactions in the development of asthma and atopy. Allergy 2010, 65(2):199-207. 10.1111/j.1398-9995.2009.02111.x, 19968634.
35. Clarke TB, Davis KM, Lysenko ES, Zhou AY, Yu Y, Weiser JN. Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat Med 2010, 16(2):228-231. 10.1038/nm.2087, 20081863.
36. Kabesch M, Peters W, Carr D, Leupold W, Weiland SK, von Mutius E. Association between polymorphisms in caspase recruitment domain containing protein 15 and allergy in two German populations. J Allergy Clin Immunol 2003, 111(4):813-817. 10.1067/mai.2003.1336, 12704363.
37. Reece P, Thanendran A, Crawford L, Tulic MK, Thabane L, Prescott SL, Sehmi R, Denburg JA. Maternal allergy modulates cord blood hematopoietic progenitor Toll-like receptor expression and function. J Allergy Clin Immunol 2011, 127(2):447-453. 10.1016/j.jaci.2010.11.006, 21167570.
38. Gupta GK, Agrawal DK. CpG oligodeoxynucleotides as TLR9 agonists: therapeutic application in allergy and asthma. BioDrugs 2010, 24(4):225-235. 10.2165/11536140-000000000-00000, 20623989.
39. Lachheb J, Dhifallah IB, Chelbi H, Hamzaoui K, Hamzaoui A. Toll-like receptors and CD14 genes polymorphisms and susceptibility to asthma in Tunisian children. Tissue Antigens 2008, 71(5):417-425. 10.1111/j.1399-0039.2008.01011.x, 18312481.
40. Stowell NC, Seideman J, Raymond HA, Smalley KA, Lamb RJ, Egenolf DD, Bugelski PJ, Murray LA, Marsters PA, Bunting RA, Flavell RA, Alexopoulou L, San Mateo LR, Griswold DE, Sarisky RT, Mbow ML, Das AM. Long-term activation of TLR3 by poly(I:C) induces inflammation and impairs lung function in mice. Respir Res 2009, 10:43. 10.1186/1465-9921-10-43, 2694181, 19486528.
41. Mizel SB, Honko AN, Moors MA, Smith PS, West AP. Induction of macrophage nitric oxide production by Gram-negative flagellin involves signaling via heteromeric Toll-like receptor 5/Toll-like receptor 4 complexes. J Immunol 2003, 170(12):6217-6223. 10.4049/jimmunol.170.12.6217, 12794153.
42. Lloyd CM, Hawrylowicz CM. Regulatory T cells in asthma. Immunity 2009, 31(3):438-449. 10.1016/j.immuni.2009.08.007, 3385348, 19766086.
43. Shi YH, Shi GC, Wan HY, Jiang LH, Ai XY, Zhu HX, Tang W, Ma JY, Jin XY, Zhang BY. Coexistence of Th1/Th2 and Th17/Treg imbalances in patients with allergic asthma. Chin Med J (Engl) 2011, 124(13):1951-1956.
44. Robinson DS. The role of the T cell in asthma. J Allergy Clin Immunol 2010, 126(6):1081-1091. quiz 1092-1083, 10.1016/j.jaci.2010.06.025, 20709383.
45. Provoost S, Maes T, van Durme YM, Gevaert P, Bachert C, Schmidt-Weber CB, Brusselle GG, Joos GF, Tournoy KG. Decreased FOXP3 protein expression in patients with asthma. Allergy 2009, 64(10):1539-1546. 10.1111/j.1398-9995.2009.02056.x, 19392991.
46. Vale-Pereira S, Todo-Bom A, Geraldes L, Schmidt-Weber C, Akdis CA, Mota-Pinto A. FoxP3, GATA-3 and T-bet expression in elderly asthma. Clin Exp Allergy 2011, 41(4):490-496. 10.1111/j.1365-2222.2010.03640.x, 21114556.
47. Braber S, Overbeek SA, Koelink PJ, Henricks PA, Zaman GJ, Garssen J, Kraneveld AD, Folkerts G. CXCR2 antagonists block the N-Ac-PGP-induced neutrophil influx in the airways of mice, but not the production of the chemokine CXCL1. Eur J Pharmacol 2011, 668(3):443-449. 10.1016/j.ejphar.2011.03.025, 21458445.
48. Fernandez-Rodriguez S, Ford WR, Broadley KJ, Kidd EJ. Establishing the phenotype in novel acute and chronic murine models of allergic asthma. Int Immunopharmacol 2008, 8(5):756-763. 10.1016/j.intimp.2008.01.025, 18387519.
49. Nials AT, Uddin S. Mouse models of allergic asthma: acute and chronic allergen challenge. Dis Model Mech 2008, 1(4-5):213-220. 2590830, 19093027.
50. Janssen-Heininger YM, Irvin CG, Scheller EV, Brown AL, Kolls JK, Alcorn JF. Airway Hyperresponsiveness and Inflammation: causation, correlation, or no relation?. J Allergy Ther 2012, 2012(Suppl 1).
51. Li CY, Lin HC, Hsueh KC, Wu SF, Fang SH. Oral administration of Lactobacillus salivarius inhibits the allergic airway response in mice. Can J Microbiol 2010, 56(5):373-379. 10.1139/W10-024, 20555399.
52. Yu J, Jang SO, Kim BJ, Song YH, Kwon JW, Kang MJ, Choi WA, Jung HD, Hong SJ. The effects of Lactobacillus rhamnosus on the prevention of asthma in a Murine model. Allergy Asthma Immunol Res 2010, 2(3):199-205. 10.4168/aair.2010.2.3.199, 2892053, 20592920.
53. Jang SO, Kim HJ, Kim YJ, Kang MJ, Kwon JW, Seo JH, Kim HY, Kim BJ, Yu J, Hong SJ. Asthma prevention by Lactobacillus Rhamnosus in a mouse model is associated with CD4(+)CD25(+)Foxp3(+) T Cells. Allergy Asthma Immunol Res 2012, 4(3):150-156. 10.4168/aair.2012.4.3.150, 3328732, 22548208.
54. Lun SW, Wong CK, Ko FW, Hui DS, Lam CW. Expression and functional analysis of toll-like receptors of peripheral blood cells in asthmatic patients: implication for immunopathological mechanism in asthma. J Clin Immunol 2009, 29(3):330-342. 10.1007/s10875-008-9269-1, 19067129.
55. Karagiannidis C, Akdis M, Holopainen P, Woolley NJ, Hense G, Ruckert B, Mantel PY, Menz G, Akdis CA, Blaser K, Schmidt-Weber CB. Glucocorticoids upregulate FOXP3 expression and regulatory T cells in asthma. J Allergy Clin Immunol 2004, 114(6):1425-1433. 10.1016/j.jaci.2004.07.014, 15577848.
56. Chauhan SK, Saban DR, Lee HK, Dana R. Levels of Foxp3 in regulatory T cells reflect their functional status in transplantation. J Immunol 2009, 182(1):148-153. 10.4049/jimmunol.182.1.148, 2610348, 19109145.
57. Sutmuller RP, den Brok MH, Kramer M, Bennink EJ, Toonen LW, Kullberg BJ, Joosten LA, Akira S, Netea MG, Adema GJ. Toll-like receptor 2 controls expansion and function of regulatory T cells. J Clin Invest 2006, 116(2):485-494. 10.1172/JCI25439, 1332026, 16424940.
58. Montuschi P, Barnes PJ. New perspectives in pharmacological treatment of mild persistent asthma. Drug Discov Today 2011, 16(23-24):1084-1091. 10.1016/j.drudis.2011.09.005, 21930234.
59. Kraneveld AD, van der Kleij HP, Kool M, van Houwelingen AH, Weitenberg AC, Redegeld FA, Nijkamp FP. Key role for mast cells in nonatopic asthma. J Immunol 2002, 169(4):2044-2053. 10.4049/jimmunol.169.4.2044, 12165531.
60. de Kivit S, Saeland E, Kraneveld AD, van de Kant HJ, Schouten B, van Esch BC, Knol J, Sprikkelman AB, van der Aa LB, Knippels LM, Garssen J, van Kooyk Y, Willemsen LE. Galectin-9 induced by dietary synbiotics is involved in suppression of allergic symptoms in mice and humans. Allergy 2012, 67(3):343-352. 10.1111/j.1398-9995.2011.02771.x, 22229637.
61. Park SK, Beaven MA. Mechanism of upregulation of the inhibitory regulator, src-like adaptor protein (SLAP), by glucocorticoids in mast cells. Mol Immunol 2009, 46(3):492-497. 10.1016/j.molimm.2008.10.011, 2656921, 19036452.
62. Kumar RK, Webb DC, Herbert C, Foster PS. Interferon-gamma as a possible target in chronic asthma. Inflamm Allergy Drug Targets 2006, 5(4):253-256. 10.2174/187152806779010909, 17168796.