DOI QR코드

DOI QR Code

Probiotics as a Potential Immunomodulating Pharmabiotics in Allergic Diseases: Current Status and Future Prospects

  • Sharma, Garima (Academy of Immunology and Microbiology (AIM), Institute for Basic Science (IBS)) ;
  • Im, Sin-Hyeog (Academy of Immunology and Microbiology (AIM), Institute for Basic Science (IBS))
  • Received : 2018.03.19
  • Accepted : 2018.05.21
  • Published : 2018.11.01

Abstract

The prevalence of allergic disorders has dramatically increased over the past decade, particularly in developed countries. Apart from gastrointestinal disorders, neoplasia, genital and dermatological diseases etc., dysregulation of gut microbiota (dysbiosis) has also been found to be associated with increased risk of allergies. Probiotics are increasingly being employed to correct dysbiosis and, in turn, to modulate allergic diseases. However, several factors like strain variations and effector metabolites or component of them in a bacterial species can affect the efficacy of those as probiotics. On the other hand, host variations like geographical locations, food habits etc. could also affect the expected results from probiotic usage. Thus, there is a glaring deficiency in our approach to establish probiotics as an irrefutable treatment avenue for suitable disorders. In this review, we explicate on the reported probiotics and their effects on certain allergic diseases like atopic dermatitis, food allergy and asthma to establish their utility. We propose possible measures like elucidation of effector molecules and functional mechanisms of probiotics towards establishing probiotics for therapeutic use. Certain probiotics studies have led to very alarming outcomes which could have been precluded, had effective guidelines been in place. Thus, we also propose ways to secure the safety of probiotics. Overall, our efforts tend to propose necessary discovery and quality assurance guidelines for developing probiotics as potential immunomodulatory 'Pharmabiotics.'

Keywords

Acknowledgement

Supported by : Institute for Basic Science

References

  1. McCutcheon JP, Moran NA. Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 2011;10:13-26.
  2. Stein MM, Hrusch CL, Gozdz J, Igartua C, Pivniouk V, Murray SE, et al. Innate immunity and asthma risk in amish and hutterite farm children. N Engl J Med 2016;375:411-21. https://doi.org/10.1056/NEJMoa1508749
  3. Lee E, Kim BJ, Kang MJ, Choi KY, Cho HJ, Kim Y, et al. Dynamics of gut microbiota according to the delivery mode in healthy Korean infants. Allergy Asthma Immunol Res 2016;8:471-7. https://doi.org/10.4168/aair.2016.8.5.471
  4. Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, et al. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol 2017;14:491-502. https://doi.org/10.1038/nrgastro.2017.75
  5. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 2014;11:506-14. https://doi.org/10.1038/nrgastro.2014.66
  6. Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013;504:451-5. https://doi.org/10.1038/nature12726
  7. Hayashi A, Sato T, Kamada N, Mikami Y, Matsuoka K, Hisamatsu T, et al. A single strain of Clostridium butyricum induces intestinal IL-10-producing macrophages to suppress acute experimental colitis in mice. Cell Host Microbe 2013;13:711-22. https://doi.org/10.1016/j.chom.2013.05.013
  8. Sanders ME, Benson A, Lebeer S, Merenstein DJ, Klaenhammer TR. Shared mechanisms among probiotic taxa: implications for general probiotic claims. Curr Opin Biotechnol 2018;49:207-16. https://doi.org/10.1016/j.copbio.2017.09.007
  9. Walker WA, Iyengar RS. Breast milk, microbiota, and intestinal immune homeostasis. Pediatr Res 2015;77:220-8. https://doi.org/10.1038/pr.2014.160
  10. Olszak T, An D, Zeissig S, Vera MP, Richter J, Franke A, et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 2012;336:489-93. https://doi.org/10.1126/science.1219328
  11. Schuijs MJ, Willart MA, Vergote K, Gras D, Deswarte K, Ege MJ, et al. Farm dust and endotoxin protect against allergy through A20 induction in lung epithelial cells. Science 2015;349:1106-10. https://doi.org/10.1126/science.aac6623
  12. Johansson SG, Hourihane JO, Bousquet J, Bruijnzeel-Koomen C, Dreborg S, Haahtela T, et al. A revised nomenclature for allergy. An EAACI position statement from the EAACI nomenclature task force. Allergy 2001;56:813-24. https://doi.org/10.1034/j.1398-9995.2001.t01-1-00001.x
  13. Brunner PM, Guttman-Yassky E, Leung DY. The immunology of atopic dermatitis and its reversibility with broad-spectrum and targeted therapies. J Allergy Clin Immunol 2017;139:S65-76. https://doi.org/10.1016/j.jaci.2017.01.011
  14. Roesner LM, Floess S, Witte T, Olek S, Huehn J, Werfel T. Foxp3(+) regulatory T cells are expanded in severe atopic dermatitis patients. Allergy 2015;70:1656-60. https://doi.org/10.1111/all.12712
  15. Zhang YY, Wang AX, Xu L, Shen N, Zhu J, Tu CX. Characteristics of peripheral blood CD4+CD25+ regulatory T cells and related cytokines in severe atopic dermatitis. Eur J Dermatol 2016;26:240-6.
  16. Tauber M, Balica S, Hsu CY, Jean-Decoster C, Lauze C, Redoules D, et al. Staphylococcus aureus density on lesional and nonlesional skin is strongly associated with disease severity in atopic dermatitis. J Allergy Clin Immunol 2016;137:1272-1274.e3. https://doi.org/10.1016/j.jaci.2015.07.052
  17. Nylund L, Satokari R, Nikkila J, Rajilic-Stojanovic M, Kalliomaki M, Isolauri E, et al. Microarray analysis reveals marked intestinal microbiota aberrancy in infants having eczema compared to healthy children in at-risk for atopic disease. BMC Microbiol 2013;13:12. https://doi.org/10.1186/1471-2180-13-12
  18. Abrahamsson TR, Jakobsson HE, Andersson AF, Bjorksten B, Engstrand L, Jenmalm MC. Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol 2012;129:434-40, 440.e1-440.e2. https://doi.org/10.1016/j.jaci.2011.10.025
  19. West CE, Ryden P, Lundin D, Engstrand L, Tulic MK, Prescott SL. Gut microbiome and innate immune response patterns in IgE-associated eczema. Clin Exp Allergy 2015;45:1419-29. https://doi.org/10.1111/cea.12566
  20. Ewald DA, Noda S, Oliva M, Litman T, Nakajima S, Li X, et al. Major differences between human atopic dermatitis and murine models, as determined by using global transcriptomic profiling. J Allergy Clin Immunol 2017;139:562-71. https://doi.org/10.1016/j.jaci.2016.08.029
  21. Kim JE, Chae CS, Kim GC, Hwang W, Hwang JS, Hwang SM, et al. Lactobacillus helveticus suppresses experimental rheumatoid arthritis by reducing inflammatory T cell responses. J Funct Foods 2015;13:350-62. https://doi.org/10.1016/j.jff.2015.01.002
  22. Kwon HK, Lee CG, So JS, Chae CS, Hwang JS, Sahoo A, et al. Generation of regulatory dendritic cells and CD4+Foxp3+ T cells by probiotics administration suppresses immune disorders. Proc Natl Acad Sci U S A 2010;107:2159-64. https://doi.org/10.1073/pnas.0904055107
  23. Kim J, Choi SH, Kim YJ, Jeong HJ, Ryu JS, Lee HJ, et al. Clinical effect of IRT-5 probiotics on immune modulation of autoimmunity or alloimmunity in the eye. Nutrients 2017;9:E1166. https://doi.org/10.3390/nu9111166
  24. Kwon HK, Kim GC, Kim Y, Hwang W, Jash A, Sahoo A, et al. Amelioration of experimental autoimmune encephalomyelitis by probiotic mixture is mediated by a shift in T helper cell immune response. Clin Immunol 2013;146:217-27. https://doi.org/10.1016/j.clim.2013.01.001
  25. Chae CS, Kwon HK, Hwang JS, Kim JE, Im SH. Prophylactic effect of probiotics on the development of experimental autoimmune myasthenia gravis. PLoS One 2012;7:e52119. https://doi.org/10.1371/journal.pone.0052119
  26. Jeong JJ, Woo JY, Ahn YT, Shim JH, Huh CS, Im SH, et al. The probiotic mixture IRT5 ameliorates age-dependent colitis in rats. Int Immunopharmacol 2015;26:416-22. https://doi.org/10.1016/j.intimp.2015.04.021
  27. Lim SK, Kwon MS, Lee J, Oh YJ, Jang JY, Lee JH, et al. Weissella cibaria WIKIM28 ameliorates atopic dermatitis-like skin lesions by inducing tolerogenic dendritic cells and regulatory T cells in BALB/c mice. Sci Rep 2017;7:40040. https://doi.org/10.1038/srep40040
  28. Won TJ, Kim B, Lee Y, Bang JS, Oh ES, Yoo JS, et al. Therapeutic potential of Lactobacillus plantarum CJLP133 for house-dust mite-induced dermatitis in NC/Nga mice. Cell Immunol 2012;277:49-57. https://doi.org/10.1016/j.cellimm.2012.05.013
  29. Han Y, Kim B, Ban J, Lee J, Kim BJ, Choi BS, et al. A randomized trial of Lactobacillus plantarum CJLP133 for the treatment of atopic dermatitis. Pediatr Allergy Immunol 2012;23:667-73. https://doi.org/10.1111/pai.12010
  30. Wang IJ, Wang JY. Children with atopic dermatitis show clinical improvement after Lactobacillus exposure. Clin Exp Allergy 2015;45:779-87. https://doi.org/10.1111/cea.12489
  31. Navarro-Lopez V, Ramirez-Bosca A, Ramon-Vidal D, Ruzafa-Costas B, Genoves-Martinez S, Chenoll-Cuadros E, et al. Effect of oral administration of a mixture of probiotic strains on SCORAD index and use of topical steroids in young patients with moderate atopic dermatitis: a randomized clinical trial. JAMA Dermatol 2018;154:37-43. https://doi.org/10.1001/jamadermatol.2017.3647
  32. Kim SO, Ah YM, Yu YM, Choi KH, Shin WG, Lee JY. Effects of probiotics for the treatment of atopic dermatitis: a meta-analysis of randomized controlled trials. Ann Allergy Asthma Immunol 2014;113:217-26. https://doi.org/10.1016/j.anai.2014.05.021
  33. Huang R, Ning H, Shen M, Li J, Zhang J, Chen X. Probiotics for the treatment of atopic dermatitis in children: a systematic review and meta-analysis of randomized controlled trials. Front Cell Infect Microbiol 2017;7:392. https://doi.org/10.3389/fcimb.2017.00392
  34. Wickens K, Black P, Stanley TV, Mitchell E, Barthow C, Fitzharris P, et al. A protective effect of Lactobacillus rhamnosus HN001 against eczema in the first 2 years of life persists to age 4 years. Clin Exp Allergy 2012;42:1071-9. https://doi.org/10.1111/j.1365-2222.2012.03975.x
  35. Wickens K, Stanley TV, Mitchell EA, Barthow C, Fitzharris P, Purdie G, et al. Early supplementation with Lactobacillus rhamnosus HN001 reduces eczema prevalence to 6 years: does it also reduce atopic sensitization? Clin Exp Allergy 2013;43:1048-57. https://doi.org/10.1111/cea.12154
  36. Cao L, Wang L, Yang L, Tao S, Xia R, Fan W. Long-term effect of early-life supplementation with probiotics on preventing atopic dermatitis: a meta-analysis. J Dermatolog Treat 2015;26:537-40. https://doi.org/10.3109/09546634.2015.1027168
  37. Gollwitzer ES, Saglani S, Trompette A, Yadava K, Sherburn R, McCoy KD, et al. Lung microbiota promotes tolerance to allergens in neonates via PD-L1. Nat Med 2014;20:642-7. https://doi.org/10.1038/nm.3568
  38. Trompette A, Gollwitzer ES, Yadava K, Sichelstiel AK, Sprenger N, Ngom-Bru C, et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med 2014;20:159-66. https://doi.org/10.1038/nm.3444
  39. Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 2013;504:446-50. https://doi.org/10.1038/nature12721
  40. Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013;504:451-5. https://doi.org/10.1038/nature12726
  41. Chen YS, Lin YL, Jan RL, Chen HH, Wang JY. Randomized placebo-controlled trial of lactobacillus on asthmatic children with allergic rhinitis. Pediatr Pulmonol 2010;45:1111-20. https://doi.org/10.1002/ppul.21296
  42. Wu CT, Chen PJ, Lee YT, Ko JL, Lue KH. Effects of immunomodulatory supplementation with Lactobacillus rhamnosus on airway inflammation in a mouse asthma model. J Microbiol Immunol Infect 2016;49:625-35. https://doi.org/10.1016/j.jmii.2014.08.001
  43. Cuello-Garcia CA, Brozek JL, Fiocchi A, Pawankar R, Yepes-Nunez JJ, Terracciano L, et al. Probiotics for the prevention of allergy: a systematic review and meta-analysis of randomized controlled trials. J Allergy Clin Immunol 2015;136:952-61. https://doi.org/10.1016/j.jaci.2015.04.031
  44. Castellazzi AM, Valsecchi C, Caimmi S, Licari A, Marseglia A, Leoni MC, et al. Probiotics and food allergy. Ital J Pediatr 2013;39:47. https://doi.org/10.1186/1824-7288-39-47
  45. Hammad H, Lambrecht BN. Barrier epithelial cells and the control of type 2 immunity. Immunity 2015;43:29-40. https://doi.org/10.1016/j.immuni.2015.07.007
  46. Lack G. Update on risk factors for food allergy. J Allergy Clin Immunol 2012;129:1187-97. https://doi.org/10.1016/j.jaci.2012.02.036
  47. Berni Canani R, Di Costanzo M, Bedogni G, Amoroso A, Cosenza L, Di Scala C, et al. Extensively hydrolyzed casein formula containing Lactobacillus rhamnosus GG reduces the occurrence of other allergic manifestations in children with cow's milk allergy: 3-year randomized controlled trial. J Allergy Clin Immunol 2017;139:1906-1913.e4. https://doi.org/10.1016/j.jaci.2016.10.050
  48. Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 2013;500:232-6. https://doi.org/10.1038/nature12331
  49. Noval Rivas M, Burton OT, Wise P, Zhang YQ, Hobson SA, Garcia Lloret M, et al. A microbiota signature associated with experimental food allergy promotes allergic sensitization and anaphylaxis. J Allergy Clin Immunol 2013;131:201-12. https://doi.org/10.1016/j.jaci.2012.10.026
  50. Tang ML, Ponsonby AL, Orsini F, Tey D, Robinson M, Su EL, et al. Administration of a probiotic with peanut oral immunotherapy: a randomized trial. J Allergy Clin Immunol 2015;135:737-744.e8. https://doi.org/10.1016/j.jaci.2014.11.034
  51. West CE, Dzidic M, Prescott SL, Jenmalm MC. Bugging allergy; role of pre-, pro- and synbiotics in allergy prevention. Allergol Int 2017;66:529-38. https://doi.org/10.1016/j.alit.2017.08.001
  52. Fiocchi A, Pawankar R, Cuello-Garcia C, Ahn K, Al-Hammadi S, Agarwal A, et al. World Allergy Organization-McMaster University Guidelines for Allergic Disease Prevention (GLAD-P): Probiotics. World Allergy Organ J 2015;8:4. https://doi.org/10.1186/s40413-015-0055-2
  53. Doron S, Snydman DR. Risk and safety of probiotics. Clin Infect Dis 2015;60 Suppl 2:S129-34. https://doi.org/10.1093/cid/civ085
  54. Besselink MG, van Santvoort HC, Buskens E, Boermeester MA, van Goor H, Timmerman HM, et al. Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial. Lancet 2008;371:651-9. https://doi.org/10.1016/S0140-6736(08)60207-X
  55. Tan TG, Sefik E, Geva-Zatorsky N, Kua L, Naskar D, Teng F, et al. Identifying species of symbiont bacteria from the human gut that, alone, can induce intestinal Th17 cells in mice. Proc Natl Acad Sci U S A 2016;113:E8141-50. https://doi.org/10.1073/pnas.1617460113
  56. Trinchieri V, Laghi L, Vitali B, Parolin C, Giusti I, Capobianco D, et al. Efficacy and safety of a multistrain probiotic formulation depends from manufacturing. Front Immunol 2017;8:1474. https://doi.org/10.3389/fimmu.2017.01474
  57. Roessler A, Friedrich U, Vogelsang H, Bauer A, Kaatz M, Hipler UC, et al. The immune system in healthy adults and patients with atopic dermatitis seems to be affected differently by a probiotic intervention. Clin Exp Allergy 2008;38:93-102.
  58. Kim J, Lee BS, Kim B, Na I, Lee J, Lee JY, et al. Identification of atopic dermatitis phenotypes with good responses to probiotics (Lactobacillus plantarum CJLP133) in children. Benef Microbes 2017;8:755-61. https://doi.org/10.3920/BM2017.0034
  59. Choi CY, Kim YH, Oh S, Lee HJ, Kim JH, Park SH, et al. Anti-inflammatory potential of a heat-killed Lactobacillus strain isolated from Kimchi on house dust mite-induced atopic dermatitis in NC/Nga mice. J Appl Microbiol 2017;123:535-43. https://doi.org/10.1111/jam.13515
  60. Shin JH, Chung MJ, Seo JG. A multistrain probiotic formulation attenuates skin symptoms of atopic dermatitis in a mouse model through the generation of CD4+Foxp3+ T cells. Food Nutr Res 2016;60:32550. https://doi.org/10.3402/fnr.v60.32550
  61. Kim MS, Kim JE, Yoon YS, Seo JG, Chung MJ, Yum DY. A probiotic preparation alleviates atopic dermatitis-like skin lesions in murine models. Toxicol Res 2016;32:149-58. https://doi.org/10.5487/TR.2016.32.2.149
  62. Weise C, Zhu Y, Ernst D, Kuhl AA, Worm M. Oral administration of Escherichia coli Nissle 1917 prevents allergen-induced dermatitis in mice. Exp Dermatol 2011;20:805-9. https://doi.org/10.1111/j.1600-0625.2011.01326.x
  63. Niccoli AA, Artesi AL, Candio F, Ceccarelli S, Cozzali R, Ferraro L, et al. Preliminary results on clinical effects of probiotic Lactobacillus salivarius LS01 in children affected by atopic dermatitis. J Clin Gastroenterol 2014;48 Suppl 1:S34-6. https://doi.org/10.1097/MCG.0000000000000233
  64. Yang HJ, Min TK, Lee HW, Pyun BY. Efficacy of probiotic therapy on atopic dermatitis in children: a randomized, double-blind, placebo-controlled trial. Allergy Asthma Immunol Res 2014;6:208-15. https://doi.org/10.4168/aair.2014.6.3.208
  65. Inoue Y, Kambara T, Murata N, Komori-Yamaguchi J, Matsukura S, Takahashi Y, et al. Effects of oral administration of Lactobacillus acidophilus L-92 on the symptoms and serum cytokines of atopic dermatitis in Japanese adults: a double-blind, randomized, clinical trial. Int Arch Allergy Immunol 2014;165:247-54. https://doi.org/10.1159/000369806
  66. Yesilova Y, Calka O, Akdeniz N, Berktas M. Effect of probiotics on the treatment of children with atopic dermatitis. Ann Dermatol 2012;24:189-93. https://doi.org/10.5021/ad.2012.24.2.189
  67. Iemoli E, Trabattoni D, Parisotto S, Borgonovo L, Toscano M, Rizzardini G, et al. Probiotics reduce gut microbial translocation and improve adult atopic dermatitis. J Clin Gastroenterol 2012;46 Suppl:S33-40. https://doi.org/10.1097/MCG.0b013e31826a8468
  68. Gore C, Custovic A, Tannock GW, Munro K, Kerry G, Johnson K, et al. Treatment and secondary prevention effects of the probiotics Lactobacillus paracasei or Bifidobacterium lactis on early infant eczema: randomized controlled trial with follow-up until age 3 years. Clin Exp Allergy 2012;42:112-22. https://doi.org/10.1111/j.1365-2222.2011.03885.x
  69. Drago L, Iemoli E, Rodighiero V, Nicola L, De Vecchi E, Piconi S. Effects of Lactobacillus salivarius LS01 (DSM 22775) treatment on adult atopic dermatitis: a randomized placebo-controlled study. Int J Immunopathol Pharmacol 2011;24:1037-48. https://doi.org/10.1177/039463201102400421
  70. Woo SI, Kim JY, Lee YJ, Kim NS, Hahn YS. Effect of Lactobacillus sakei supplementation in children with atopic eczema-dermatitis syndrome. Ann Allergy Asthma Immunol 2010;104:343-8. https://doi.org/10.1016/j.anai.2010.01.020

Cited by

  1. A Novel Postbiotic From Lactobacillus rhamnosus GG With a Beneficial Effect on Intestinal Barrier Function vol.10, pp.None, 2018, https://doi.org/10.3389/fmicb.2019.00477
  2. Obesity and adiposity indicators in asthma and allergic rhinitis in children vol.19, pp.1, 2019, https://doi.org/10.1097/aci.0000000000000504
  3. Intestinal Microbiota and Allergy. Probiotics and Prebiotics in Prevention and Treatment of Allergic Diseases vol.16, pp.1, 2018, https://doi.org/10.15690/pf.v16i1.1999
  4. Oral Lactobacillus reuteri LR06 or Bifidobacterium BL5b supplement do not produce analgesic effects on neuropathic and inflammatory pain in rats vol.9, pp.4, 2018, https://doi.org/10.1002/brb3.1260
  5. Mechanisms and immunomodulatory properties of pre- and probiotics vol.10, pp.3, 2018, https://doi.org/10.3920/bm2018.0066
  6. Ginsenoside Rh2 Ameliorates Atopic Dermatitis in NC/Nga Mice by Suppressing NF-kappaB-Mediated Thymic Stromal Lymphopoietin Expression and T Helper Type 2 Differentiation vol.20, pp.24, 2018, https://doi.org/10.3390/ijms20246111
  7. 아토피 피부염에서 프로바이오틱스 치료 유효성에 관한 문헌적 고찰 vol.33, pp.1, 2018, https://doi.org/10.6114/jkood.2020.33.1.025
  8. Host–microbe cross-talk in the lung microenvironment: implications for understanding and treating chronic lung disease vol.56, pp.2, 2018, https://doi.org/10.1183/13993003.02320-2019
  9. A randomized trial of Lactobacillus rhamnosus IDCC 3201 tyndallizate (RHT3201) for treating atopic dermatitis vol.31, pp.7, 2018, https://doi.org/10.1111/pai.13269
  10. Characterization and Functional Test of Canine Probiotics vol.12, pp.None, 2018, https://doi.org/10.3389/fmicb.2021.625562
  11. Prevention and Management with Pro-, Pre and Synbiotics in Children with Asthma and Allergic Rhinitis: A Narrative Review vol.13, pp.3, 2018, https://doi.org/10.3390/nu13030934
  12. Gut microbiota restoration through fecal microbiota transplantation: a new atopic dermatitis therapy vol.53, pp.5, 2018, https://doi.org/10.1038/s12276-021-00627-6