Skip to main content

Advertisement

Log in

Differential Suppression of Heat-Killed Lactobacilli Isolated from kimchi, a Korean Traditional Food, on Airway Hyper-responsiveness in Mice

  • Published:
Journal of Clinical Immunology Aims and scope Submit manuscript

Abstract

Rationale

Probiotics have been shown to be effective in reducing allergic symptoms. However, there are few studies to evaluate the therapeutic effects of lactobacilli on allergen-induced airway inflammation.

Objective

We investigated whether three heat-killed lactobacilli, Lactobacillus plantarum, Lactobacillus curvatus and Lactobacillus sakei subsp. sakei, isolated from kimchi, exerted inhibitory effects on airway hyper-responsiveness in a murine asthma model.

Methods

Heat-killed lactic acid bacteria were orally administered into BALB/c mice, followed by challenge with aerosolized ovalbumin, after which allergic symptoms were evaluated.

Results

Airway inflammation was suppressed in the L. plantarum- and L. curvatus-treated mice. Interleukin (IL)-4 and IL-5 levels were significantly lower in the L. plantarum- and L. curvatus-treated mice than in those treated with L. sakei subsp. sakei. Importantly, heat-killed L. plantarum administration induced Foxp3 expression in intestinal lamina propria cells, and heat-killed L. curvatus induced IL-10 as a way of inducing tolerance.

Conclusion

Specific strains of lactobacilli isolated from kimchi can effectively suppress airway hyper-responsiveness.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

Penh:

Enhanced pause

MeCh:

Methacholin

BALF:

Bronchoalveolar lavage fluid

OVA:

Ovalbumin

H&E:

Hematoxylin and eosin

Ig:

Immunoglobulin

CFU:

Colony-forming unit

Th:

T helper

References

  1. Kay AB. TH2-type cytokines in asthma. Ann NY Acad Sci. 1996;796:1–8.

    Article  CAS  PubMed  Google Scholar 

  2. Eder W, Ege MJ, von Mutius E. The asthma epidemic. N Engl J Med. 2006;355:2226–35.

    Article  CAS  PubMed  Google Scholar 

  3. Nowak D, Ulrik CS, von Mutius E. Asthma and atopy: has peak prevalence been reached? Eur Respir J. 2004;23:359–60.

    Article  CAS  PubMed  Google Scholar 

  4. Mogi J. Many asthma patients experience persistent symptoms despite appropriate clinical and guideline-based treatment with inhaled corticosteroids. J Am Acad Nurse Pract. 2007;19:459–70.

    Article  Google Scholar 

  5. Umetsu DT, McIntire JJ, Akbari O, Macaubas C, DeKruyff RH. Asthma: an epidemic of dysregulated immunity. Nat Immunol. 2002;3:715–20.

    Article  CAS  PubMed  Google Scholar 

  6. Herrick CA, Bottomly K. To respond or not to respond: T cells in allergic asthma. Nat Rev Immunol. 2003;3:405–12.

    Article  CAS  PubMed  Google Scholar 

  7. Strachan DP. Hay fever, hygiene, and household size. Brit Med J. 1989;299:1259–60.

    Article  CAS  PubMed  Google Scholar 

  8. Guarner F, Bourdet-Sicard R, Brandtzaeg P, Gill HS, McGuirk P, van Eden W, et al. Mechanisms of disease: the hygiene hypothesis revisited. Nat Clin Pract Gastroenterol Hepatol. 2006;3:275–84.

    Article  CAS  PubMed  Google Scholar 

  9. Kalliomäki 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;107:129–34.

    Article  PubMed  Google Scholar 

  10. Kaila M, Isolauri E, Soppi E, Virtanen E, Laine S, Arvilommi H. Enhancement of the circulating antibody secreting cell response in human diarrehea by human lactobacillus strain. Pediatr Res. 1992;32:141–4.

    CAS  PubMed  Google Scholar 

  11. Morita H, He F, Fuse T, Ouwehand AC, Hashimoto H, Hosoda M, et al. Adhesion of lactic acid bacteria to Caco-2 cells and their effect on cytokine secretion. Microbiol Immunol. 2002;46:293–7.

    CAS  PubMed  Google Scholar 

  12. Madsen KL, Doyle JS, Jewell LD, Tavernini MM, Fedorak RN. Lactobacillus species prevents colitis in interleukin-10 gene-deficient mice. Gastroenterol. 1999;116:1107.

    Article  CAS  Google Scholar 

  13. Schultz M, Veltkamp C, Dieleman LA, Grenther WB, Wyrick PB, Tonkonogy SL, et al. Lactobacillus plantarum 299V in the treatment and prevention of spontaneous colitis in interleukin-10-deficient mice. Inflamm Bowel Dis. 2002;8:71.

    Article  PubMed  Google Scholar 

  14. FAO/WHO. Guidelines for the Evaluation of Probiotics in Food. Joint FAO/WHO Working Group Report on Drafting Guidelines for the Evaluation of Probiotics in Food, 2002. ftp://ftp.fao.org/es/esn/food/wgreport2.pdf.

  15. Kaillomaki M, Salminen S, Poussa T, Arvilommi H, Isolauri E. Probiotics and prevention of atopic disease: 4-year follow-up of a randomized placebo-controlled trial. Lancet. 2003;361:1869–71.

    Article  Google Scholar 

  16. Majamaa H, Isoauri E. Probiotics: a novel approach in the management of food allergy. Allergy Clin Immunol. 1997;9:179–85.

    Article  Google Scholar 

  17. Peng GC, Hsu CH. The efficacy and safety of heat-killed Lactobacillus paracasei for treatment of perennial allergic rhinitis induced by house-dust mite. Pediatr Allergy Immunol. 2005;16:433–8.

    Article  PubMed  Google Scholar 

  18. Xiao JZ, Kondo S, Yanagisawa N, Takahashi N, Odamaki T, Iwabuchi N, et al. Effect of probiotic Bifidobacterium longum BB536 in relieving clinical symptoms and modulating plasma cytokine levels of Japanese cedar pollinosis during the pollen season. A randomized double-blind, placebo-controlled trial. J Investig Allergol Clin Immunol. 2006;16:86–93.

    CAS  PubMed  Google Scholar 

  19. Cho J, Lee D, Yang C, Jeon J, Kim J, Han H. Microbial population dynamics of kimchi, a fermented cabbage product. FEMS Microbiol Lett. 2006;257:262–7.

    Article  CAS  PubMed  Google Scholar 

  20. Lee J, Hwang KT, Heo MS, Lee JH, Park KY. Resistance of Lactobacillus plantarum KCTC 3099 from Kimchi to oxidative stress. J Med Food. 2005;8:299–304.

    Article  CAS  PubMed  Google Scholar 

  21. Cho YR, Chang JY, Chang HC. Production of gamma-aminobutyric acid (GABA) by Lactobacillus buchneri isolated from kimchi and its neuroprotective effect on neuronal cells. J Microbiol Biotechnol. 2007;17:104–9.

    CAS  PubMed  Google Scholar 

  22. Kim TS, Dekruyff RH, Rupper R, Maecher HT, Levy S, Umetsu DT. An ovalbumin-IL-12 fusion protein is more effective than ovalbumin plus free recombinant IL-12 in inducing T helper cell type 1-dominated immune response and inhibiting antigen-specific IgE production. J Immunol. 1997;158:4137–44.

    CAS  PubMed  Google Scholar 

  23. Quarcoo D, Weixler S, Groneberg D, Groneberg D, Joachim R, Ahrens B, et al. Inhibition of signal transducer and activatior of transcription 1 attenuates allergen-induced airway inflammation and hyperreactivity. J Allergy Clin Immunol. 2004;114:288–95.

    Article  CAS  PubMed  Google Scholar 

  24. Weigmann B, Tubbe I, Seidel D, Nicolaev A, Becker C, Neurath MF. Isolation and subsequent analysis of murine lamina propria mononuclear cells from colonic tissue. Nat Protoc. 2007;2:2307–11.

    Article  CAS  PubMed  Google Scholar 

  25. Kim E, Kim SH, Kim S, Cho D, Kim TS. AIMP1/p43 protein induces the maturation of bone marrow-derived dendritic cells with T helper type 1-polarizing ability. J Immunol. 2008;180:2894–902.

    CAS  PubMed  Google Scholar 

  26. Isolauri E. Probiotics in the prevention and treatment of allergic disease. Pediatr Allergy Immunol. 2001;12 Suppl 14:56–9.

    Article  PubMed  Google Scholar 

  27. Ogden NS, Bielory L. Probiotics: a novel approach in the treatment and prevention of pediatric atopic disease. Curr Opin Allergy Clin Immunol. 2005;5:179–84.

    Article  PubMed  Google Scholar 

  28. Maassen CB, Laman JD, den Bak-Glashouwer MJ, Tielen FJ, van Holten-Neelen JC, Hoogteijling L, et al. Instruments for oral disease-intervention strategies: recombinant Lactobacillus casei expressing tetanus toxin fragment C for vaccination or myelin proteins for oral tolerance induction in multiple sclerosis. Vaccine. 1999;17:2117–28.

    Article  CAS  PubMed  Google Scholar 

  29. von der WT, Bulliard C, Schiffrin EJ. Induction by a lactic acid bacterium of a population of CD4(+) T cells with low proliferative capacity that produce transforming growth factor beta and interleukin-10. Clin Diagn Lab Immunol. 2001;8:695–701.

    Google Scholar 

  30. Khoury SJ, Hancock WW, Weiner HL. Oral tolerance to myelin basic protein and natural recovery from experimental autoimmune encephalomyelitis are associated with downregulation of inflammatory cytokines and differential upregulation of transforming growth factor beta, interleukin 4, and prostaglandin E expression in the brain. J Exp Med. 1992;176:1355–64.

    Article  CAS  PubMed  Google Scholar 

  31. Feleszko W, Jaworska J, Rha RD, Steinhausen S, Avagyan A, Jaudszus A, et al. 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. 2007;37:498–505.

    Article  CAS  PubMed  Google Scholar 

  32. Hougee S, Vriesema AJM, Wigering SC, Knippels LMJ, Folkerts G, Nijkamp FP, et al. Oral treatment with probiotics reduces allergic symptoms in ovalbumin-sensitized mice: a bacterial strain comparative study. Int Arch Allergy Immunol. 2009;151(2):107–17.

    Article  PubMed  Google Scholar 

  33. Di Giacinto C, Marinaro M, Sanchez M, Strober W, Boirivant M. Probiotics ameliorate recurrent Th1-mediated murine colitis by inducing IL-10 and IL-10-dependent TGF-beta-bearing regulatory cells. J Immunol. 2005;174:3237–46.

    PubMed  Google Scholar 

  34. Taylor JJ, Mohrs M, Pearce EJ. Regulatory T cell responses develop in parallel to Th responses and control the magnitude and phenotype of th Th effector population. J Immunol. 2006;176:5839–47.

    CAS  PubMed  Google Scholar 

  35. Grindebacke H, Wing K, Andersson AC, Suri-Payer E, Rak S, Rudin A. Defective suppression of Th3 cytokines by CD4CD25 regulatory T cells in birch allergic during birch pollen season. Clin Exp Allergy. 2004;34:1364–72.

    Article  CAS  PubMed  Google Scholar 

  36. Martínez-Cañavate A, Sierra S, Lara-Villoslada F, Romero J, Maldonado J, Boza J, et al. A probiotic dairy product containing L. gasseri CECT5714 and L. coryniformis CECT5711 induces immunological changes in children suffering from allergy. Pediatr Allergy Immunol. 2009;20:592–600.

    Article  PubMed  Google Scholar 

  37. Brightbill HD, Libraty DH, Krutzik SR, Yang RB, Belislem JT, Bleharski JR, et al. Host defense mechanisms triggered by microbial lipoproteins through Toll-like receptors. Science. 1999;285:732–6.

    Article  CAS  PubMed  Google Scholar 

  38. Fuchs B, Braun A. Modulation of asthma and allergy by addressing toll-like receptor 2. J Occup Med Toxicol. 2008;3 Suppl 1:S5.

    Article  PubMed  Google Scholar 

  39. Eder W, Klimecki W, Yu L, von Mutrius E, Riedler J, Braun-Fahrlander C, et al. Toll like receptor 2 as a major gene for asthma in children of European farmers. J Allergy Clin Immunol. 2004;113:482–8.

    Article  CAS  PubMed  Google Scholar 

  40. Veckman V, Miettinen M, Matikainen S, Lande R, Giacomini E, Coccia EM, et al. Lactobacilli and streptococci induce inflammatory chemokine production in human macrophages that stimulates Th1 cell chemotaxis. J Leukoc Biol. 2003;74:395–402.

    Article  CAS  PubMed  Google Scholar 

  41. Osborn DA, Sinn JK. Probiotics in infants for prevention of allergic disease and food hypersensitivity. Cochrane Database Syst Rev. 2007;17:CD006475.

    Google Scholar 

  42. Boyle RJ, Bath-Hextall FJ, Leonardi-Bee J, Murrell DF, Tang ML. Probiotics for the treatment of eczema: a systematic review. Clin Exp Allergy. 2009;38:1117–27.

    Article  Google Scholar 

  43. Bibiloni R, Fedorak RN, Tannock GW, Madsen KL, Gionchetti P, Campieri M, et al. VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am J Gastroenterol. 2005;100:1539–46.

    Article  PubMed  Google Scholar 

  44. Mastrangeli G, Corinti S, Butteroni C, Afferni C, Bonura A, Boirivant M, et al. Effects of live and inactivated VSL#3 probiotic preparations in the modulation of in vitro and in vivo allergen-induced Th2 responses. Int Arch Allergy Immunol. 2009;150:133–43.

    Article  CAS  PubMed  Google Scholar 

  45. Kiyono H, Fukuyama S. NALT- versus Peyer’s-patch-mediated mucosal immunity. Nat Rev Immunol. 2004;4:699–710.

    Article  CAS  PubMed  Google Scholar 

  46. Challacombe SJ, Tomasi Jr TB. Systemic tolerance and secretory immumity after oral immunization. J Exp Med. 1980;152:1459–72.

    Article  CAS  PubMed  Google Scholar 

  47. Khoury SJ, Hancock WW, Weiner HL. Oral tolerance to myelin basic protein and natural recovery from experimental autoimmune encephalomyelitis are associated with downregulation of inflammatory cytokines and differential upregulation of transforming growth factor beta, interleukin 4, and prostaglandin E expression in the brain. J Exp Med. 1992;176:1355–64.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant of the Science Research Center Program, Ministry of Science & Technology, Republic of Korea (R11-2005-017).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tae Sung Kim.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hong, HJ., Kim, E., Cho, D. et al. Differential Suppression of Heat-Killed Lactobacilli Isolated from kimchi, a Korean Traditional Food, on Airway Hyper-responsiveness in Mice. J Clin Immunol 30, 449–458 (2010). https://doi.org/10.1007/s10875-010-9375-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10875-010-9375-8

Keywords

Navigation