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Research Paper

Lactobacillus paracasei KBL382 administration attenuates atopic dermatitis by modulating immune response and gut microbiota

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Article: 1819156 | Received 06 Dec 2019, Accepted 21 Aug 2020, Published online: 04 Oct 2020

References

  • Nutten S. Atopic dermatitis: global epidemiology and risk factors. Ann Nutr Metab. 2015;1:8–16. doi:10.1159/000370220.
  • Furue M, Chiba T, Tsuji G, Ulzii D, Kido-Nakahara M, Nakahara T, Kadono T. Atopic dermatitis: immune deviation, barrier dysfunction, IgE autoreactivity and new therapies. Allergol Int. 2017;66(3):398–403. doi:10.1016/j.alit.2016.12.002.
  • Bieber T. Atopic dermatitis. N Engl J Med. 2008;22(2):125–137. doi:10.5021/ad.2010.22.2.125.
  • Kim JY, Park BK, Park HJ, Park YH, Kim BO, Pyo S. Atopic dermatitis-mitigating effects of new Lactobacillus strain, Lactobacillus sakei probio 65 isolated from Kimchi. J Appl Microbiol. 2013;115(2):517–526. doi:10.1111/jam.12229.
  • Karki R, Jung M-A, Kim K-J, Kim D-W. Inhibitory effect of Nelumbo nucifera (Gaertn.) on the development of atopic dermatitis-like skin lesions in NC/Nga mice. Evid Based Complement Alternat Med. 2012;2012:7. doi:10.1155/2012/153568.
  • Gandhi NA, Bennett BL, Graham NMH, Pirozzi G, Stahl N, Yancopoulos GD. Targeting key proximal drivers of type 2 inflammation in disease. Nat Rev Drug Discov. 2016;15(1):35–50. doi:10.1038/nrd4624.
  • Nakazato J, Kishida M, Kuroiwa R, Fujiwara J, Shimoda M, Shinomiya N. Serum levels of Th2 chemokines, CCL17, CCL22, and CCL27, were the important markers of severity in infantile atopic dermatitis. Pediatr Allergy Immunol. 2008;19(7):605–613. doi:10.1111/j.1399-3038.2007.00692.x.
  • Spergel JM, Mizoguchi E, Oettgen H, Bhan AK, Geha RS, Herz U, Bunikowski R, Renz H, Leung D, Leiferman K, et al. Roles of TH1 and TH2 cytokines in a murine model of allergic dermatitis. J Clin Invest. 1999;103(8):1103–1111. doi:10.1172/JCI5669.
  • Matsuda H, Watanabe N, Geba GP, Sperl J, Tsudzuki M, Hiroi J, Matsumoto M, Ushio H, Saito S, Askenase PW, et al. Development of atopic dermatitis-like skin lesion with IgE hyperproduction in NC/Nga mice. Int Immunol. 1997;9(3):461–466. doi:10.1093/intimm/9.3.461.
  • Takeuchi S, Yasukawa F, Furue M, Katz SI. Collared mice: A model to assess the effects of scratching. J Dermatol Sci. 2010;57(1):44. doi:10.1016/j.jdermsci.2009.09.008.
  • Zhao H, Li M, Wang L, Su Y, Fang H, Lin J, Mohabeer N, Li D. Angiotensin II induces TSLP via an AT1 receptor/NF-κB pathway, promoting Th17 differentiation. Cell Physiol Biochem. 2012;30(6):1383–1397. doi:10.1159/000343327.
  • Gittler JK, Shemer A, Suárez-Fariñas M, Fuentes-Duculan J, Gulewicz KJ, Wang CQF, Mitsui H, Cardinale I, De Guzman Strong C, Krueger JG, et al. Progressive activation of TH2/TH22 cytokines and selective epidermal proteins characterizes acute and chronic atopic dermatitis. J Allergy Clin Immunol. 2012;130(6):1344–1354. doi:10.1016/j.jaci.2012.07.012.
  • Koga C, Kabashima K, Shiraishi N, Kobayashi M, Tokura Y. Possible pathogenic role of Th17 cells for atopic dermatitis. J Invest Dermatol. 2008;128(11):2625–2630. doi:10.1038/jid.2008.111.
  • Boguniewicz M, Leung DYM. Atopic dermatitis: A disease of altered skin barrier and immune dysregulation. Immunol Rev. 2011;242(1):233–246. doi:10.1111/j.1600-065X.2011.01027.x.
  • Liu Y-J. Thymic stromal lymphopoietin: master switch for allergic inflammation. J Exp Med. 2006;203(2):269–273. doi:10.1084/jem.20051745.
  • Shimada Y, Takehara K, Sato S. Both Th2 and Th1 chemokines (TARC/CCL17, MDC/CCL22, and Mig/CXCL9) are elevated in sera from patients with atopic dermatitis. J Dermatol Sci. 2004;34(3):201–208. doi:10.1016/j.jdermsci.2004.01.001.
  • Olszak T, An D, Zeissig S, Vera MP, Richter J, Franke A, Glickman JN, Siebert R, Baron RM, Kasper DL, et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science. 2012;336(6080):489–493. doi:10.1126/science.1219328.
  • Levy M, Blacher E, Elinav E. Microbiome, metabolites and host immunity. Curr Opin Microbiol. 2017;35:8–15. doi:10.1016/j.mib.2016.10.003.
  • Pineiro M, Stanton C. Probiotic bacteria: legislative framework – requirements to evidence basis. J Nutr. 2007;137(3):850S–3S. doi:10.1093/jn/137.3.850S.
  • Yeom M, Sur BJ, Park J, Cho SG, Lee B, Kim ST, Kim KS, Lee H, Hahm DH. Oral administration of Lactobacillus casei variety rhamnosus partially alleviates TMA-induced atopic dermatitis in mice through improving intestinal microbiota. J Appl Microbiol. 2015;119(2):560–570. doi:10.1111/jam.12844.
  • Inoue R, Nishio A, Fukushima Y, Ushida K. Oral treatment with probiotic Lactobacillus johnsonii NCC533 (La1) for a specific part of the weaning period prevents the development of atopic dermatitis induced after maturation in model mice, NC/Nga. Br J Dermatol. 2007;156(3):499–509. doi:10.1111/j.1365-2133.2006.07695.x.
  • Sunada Y, Nakamura S, Kamei C. Effect of Lactobacillus acidophilus strain L-55 on the development of atopic dermatitis-like skin lesions in NC/Nga mice. Int Immunopharmacol. 2008;8(13–14):1761–1766. doi:10.1016/j.intimp.2008.08.011.
  • Won TJ, Kim B, Lim YT, Song DS, Park SY, Park ES, Lee DI, Hwang KW. Oral administration of Lactobacillus strains from Kimchi inhibits atopic dermatitis in NC/Nga mice. J Appl Microbiol. 2011;110(5):1195–1202. doi:10.1111/j.1365-2672.2011.04981.x.
  • Sawada J, Morita H, Tanaka A, Salminen S, He F, Matsuda H. Ingestion of heat-treated Lactobacillus rhamnosus GG prevents development of atopic dermatitis in NC/Nga mice. Clin Exp Allergy. 2007;37(2):296–303. doi:10.1111/j.1365-2222.2006.02645.x.
  • Tanaka A, Jung K, Benyacoub J, Prioult G, Okamoto N, Ohmori K, Blum S, Mercenier A, Matsuda H. Oral supplementation with Lactobacillus rhamnosus CGMCC 1.3724 prevents development of atopic dermatitis in NC/NgaTnd mice possibly by modulating local production of IFN-γ. Exp Dermatol. 2009;18(12):1022–1027. doi:10.1111/j.1600-0625.2009.00895.x.
  • 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. doi:10.3402/fnr.v60.32550.
  • Kim HJ, Kim YJ, Kang MJ, Seo JH, Kim HY, Jeong SK, Lee SH, Kim JM, Hong SJ. A novel mouse model of atopic dermatitis with epicutaneous allergen sensitization and the effect of Lactobacillus rhamnosus. Exp Dermatol. 2012;21(9):672–675. doi:10.1111/j.1600-0625.2012.01539.x.
  • Van Baarlen P, Wells JM, Kleerebezem M. Regulation of intestinal homeostasis and immunity with probiotic lactobacilli. Trends Immunol. 2013;34(5):208–215. doi:10.1016/j.it.2013.01.005.
  • Dupont AW, Dupont HL. The intestinal microbiota and chronic disorders of the gut. Nat Rev Gastroenterol Hepatol. 2011;8(9):523–531. doi:10.1038/nrgastro.2011.133.
  • Han S-C, Kang G-J, Ko Y-J, Kang H-K, Moon S-W, Ann Y-S, Yoo E-S. Fermented fish oil suppresses T helper 1/2 cell response in a mouse model of atopic dermatitis via generation of CD4+CD25+Foxp3+ T cells. BMC Immunol. 2012;13:44. doi:10.1186/1471-2172-13-44.
  • Kang H, Lee CH, Kim JR, Kwon JY, Seo SG, Han JG, Kim BG, Kim JE, Lee KW. Chlorella vulgaris attenuates Dermatophagoides farinae-induced atopic dermatitis-like symptoms in NC/Nga mice. Int J Mol Sci. 2015;16(9):21021–21034. doi:10.3390/ijms160921021.
  • Takaoka A, Arai I, Sugimoto M, Honma Y, Futaki N, Nakamura A, Nakaike S. Involvement of IL-31 on scratching behavior in NC/Nga mice with atopic-like dermatitis. Exp Dermatol. 2006;15(3):161–167. doi:10.1111/j.1600-0625.2006.00405.x.
  • Kim HJ, Kim HY, Lee SY, Seo JH, Lee E, Hong SJ. Clinical efficacy and mechanism of probiotics in allergic diseases. Korean J Pediatr. 2013;56(9):369–376. doi:10.3345/kjp.2013.56.9.369.
  • Lim SK, Kwon MS, Lee J, Oh YJ, Jang JY, Lee JH, Park HW, Nam YD, Seo MJ, Roh SW, 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. doi:10.1038/srep40040.
  • Kwon H-K, Lee C-G, So J-S, Chae C-S, Hwang J-S, Sahoo A, Nam JH, Rhee JH, Hwang K-C, Im S-H. Generation of regulatory dendritic cells and CD4+Foxp3+ T cells by probiotics administration suppresses immune disorders. Proc Natl Acad Sci. 2010;107(5):2159–2164. doi:10.1073/pnas.0904055107.
  • Sommer F, Bäckhed F. The gut microbiota-masters of host development and physiology. Nat Rev Microbiol. 2013;11(4):227–238. doi:10.1038/nrmicro2974.
  • Rooks MG, Veiga P, Wardwell-Scott LH, Tickle T, Segata N, Michaud M, Gallini CA, Beal C, van Hylckama-vlieg JE, Ballal SA, et al. Gut microbiome composition and function in experimental colitis during active disease and treatment-induced remission. ISME J. 2014;8(7):1403–1417. doi:10.1038/ismej.2014.3.
  • Berry D, Reinisch W. Intestinal microbiota: A source of novel biomarkers in inflammatory bowel diseases? Best Pract Res Clin Gastroenterol. 2013;27(1):47–58. doi:10.1016/j.bpg.2013.03.005.
  • Roopchand DE, Carmody RN, Kuhn P, Moskal K, Rojas-Silva P, Turnbaugh PJ, Raskin I. Dietary polyphenols promote growth of the gut bacterium Akkermansia muciniphila and attenuate high-fat diet-induced metabolic syndrome. Diabetes. 2015;64(8):2847–2858. doi:10.2337/db14-1916.
  • Ottman N, Reunanen J, Meijerink M, Pietila TE, Kainulainen V, Klievink J, Huuskonen L, Aalvink S, Skurnik M, Boeren S, et al. Pili-like proteins of Akkermansia muciniphila modulate host immune responses and gut barrier function. PLoS One. 2017;12(3):e0173004. doi:10.1371/journal.pone.0173004.
  • Louis P, Scott KP, Duncan SH, Flint HJ. Understanding the effects of diet on bacterial metabolism in the large intestine. J Appl Microbiol. 2007;102(5):1197–1208. doi:10.1111/j.1365-2672.2007.03322.x.
  • Rather IA, Bajpai VK, Kumar S, Lim J, Paek WK, Park Y-H. Probiotics and atopic dermatitis: an overview. Front Microbiol. 2016;7:507. doi:10.3389/fmicb.2016.00507.
  • Lee SH, Yoon JM, Kim YH, Jeong DG, Park S, Kang DJ. Therapeutic effect of tyndallized Lactobacillus rhamnosus IDCC 3201 on atopic dermatitis mediated by down-regulation of immunoglobulin E in NC/Nga mice. Microbiol Immunol. 2016;60(7):468–476. doi:10.1111/1348-0421.12390.
  • Grüber C, Wendt M, Sulser C, Lau S, Kulig M, Wahn U, Werfel T, Niggemann B. Randomized, placebo-controlled trial of Lactobacillus rhamnosus GG as treatment of atopic dermatitis in infancy. Allergy. 2007;62(11):1270–1276. doi:10.1111/j.1398-9995.2007.01543.x.
  • Jang YJ, Kim WK, Han DH, Lee K, Ko G. Lactobacillus fermentum species ameliorate dextran sulfate sodium-induced colitis by regulating the immune response and altering gut microbiota. Gut Microbes. 2019;10(6):696–711. doi:10.1080/19490976.2019.1589281.
  • Kim W-K, Jang YJ, Seo B, Han DH, Park S, Ko G. Administration of Lactobacillus paracasei strains improves immunomodulation and changes the composition of gut microbiota leading to improvement of colitis in mice. J Funct Foods. 2019;52:565–575. doi:10.1016/j.jff.2018.11.035.
  • Jimbo N, Kawada C, Nomura Y. Herb extracts and collagen hydrolysate improve skin damage resulting from ultraviolet-induced aging in hairless mice. Biosci Biotechnol Biochem. 2015;79(10):1624–1628. doi:10.1080/09168451.2015.1046362.
  • Andoh T, Haza S, Saito A, Kuraishi Y. Involvement of leukotriene B4 in spontaneous itch-related behaviour in NC mice with atopic dermatitis-like skin lesions. Exp Dermatol. 2011;20(11):894–898. doi:10.1111/j.1600-0625.2011.01346.x.
  • Kuraishi Y, Nagasawa T, Hayashi K, Satoh M. Scratching behavior induced by pruritogenic but not algesiogenic agents in mice. Eur J Pharmacol. 1995;275(3):229–233. doi:10.1016/0014-2999(94)00780-b.
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCᵀ method. Methods. 2001;25(4):402–408. doi:10.1006/meth.2001.1262.
  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pẽa AG, Goodrich JK, Gordon JI, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–336. doi:10.1038/nmeth.f.303.
  • Kim W, Jang YJ, Han DH, Seo B, Park S. Administration of Lactobacillus fermentum KBL375 causes taxonomic and functional changes in gut microbiota leading to improvement of atopic dermatitis. Front Mol Biosci. 2019;6:1–12. doi:10.3389/fmolb.2019.00092.
  • Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013;31:814–821. doi:10.1038/nbt.2676.
  • David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–563. doi:10.1038/nature12820.
  • Roucher VF, Desnots E, Naël C, Agnoux AM, Alexandre-Gouabau MC, Darmaun D, Boquien CY. Use of UPLC-ESI-MS/MS to quantitate free amino acid concentrations in micro-samples of mammalian milk. Springerplus. 2013;2:622. doi:10.1186/2193-1801-2-622.