Modulation effect of Lactobacillus acidophilus KLDS 1.0738 on gut microbiota and TLR4 expression in -lactoglobulin-induced allergic mice model
Main Article Content
Keywords
Lactobacillus acidophilus, β-lactoglobulin allergy, Gut microbiota, TLR4, 16S rRNA gene sequencing
Abstract
Objectives: -lactoglobulin (-Lg)-sensitized mice model was employed to investigate the correlation between Lactobacillus acidophilus KLDS 1.0738 (Lap KLDS 1.0738) modulating gut microbiota and inducting Toll-like receptors (TLRs) expression.
Methods: The alterations of mice fecal microbiota were analyzed by 16S rRNA gene sequencing. The serum cytokines production and TLR4/NF-B mRNA expression in the colon tissues were measured by ELISA kit and quantitative RT-PCR, respectively.
Results: The results showed that Lap KLDS 1.0738 pretreatment attenuated -Lg-induced hypersensitivity, accompanied with a diminished expression of TLR4/NF-B signaling. Moreover, oral administration of Lap KLDS 1.0738 improved the richness and diversity of fecal microbiota, which was characterized by fewer Proteobacteria phylum and Helicobacteraceae family, and higher Firmicutes phylum and Lachnospiraceae family than allergic group. Notably, TLR4/NF-B expression was positively correlated with the family of Helicobacteraceae in allergic group, but negatively correlated with the family of Lachnospiraceae, Ruminococcaceae and anti-inflammatory cytokines level. A significant positive correlation was observed between TLR4/NF-B expression and the production of histamine, total IgE and pro-inflammatory cytokines.
Conclusions: Intake of Lap KLDS 1.0738 can influence the gut bacterial composition, which might result in recognizing TLRs signaling so as to inhibit allergic response.
References
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2. Wood RA, Sicherer SH, Vickery BP, Jones SM, Liu AH, Fleischer DM, et al. The natural history of milk allergy in an observational cohort. J Allergy Clin Immunol. 2013;131:805-12.
3. Zimmermann P, Messina N, Mohn WW, Finlay BB, Curtis N. Association between the intestinal microbiota and allergic sensitization, eczema, and asthma: A systematic review. J Allergy Clin Immunol. 2019;143:467-85.
4. Kasselman LJ, Vernice NA, DeLeon J, Reiss AB. The gut microbiome and elevated cardiovascular risk in obesity and autoimmunity. Atherosclerosis. 2018;271:203-13.
5. Shukla R, Ghoshal U, Ranjan P, Ghoshal UC. Expression of toll-like receptors, pro-, and anti-inflammatory cytokines in relation to gut microbiota in Irritable Bowel syndrome: The evidence for its micro-organic basis. J Neurogastroenterol Motil. 2018;24:628-42.
6. Rogier R, Ederveen THA, Boekhorst J, Wopereis H, Scher JU, Manasson J, et al. Aberrant intestinal microbiota due to IL-1 receptor antagonist deficiency promotes IL-17- and TLR4- dependent arthritis. Microbiome. 2017;5:63.
7. Sharma G, Im SH. Probiotics as a potential immunomodulating pharmabiotics in allergic diseases: Current status and future prospects. Allergy Asthma Immunol Res. 2018;10:575-90.
8. Zhang J, Ma JY, Li QH, Su H, Sun X. Lactobacillus rhamnosus GG induced protective effect on allergic airway inflammation is associated with gut microbiota. Cell Immunol. 2018;332:77-84.
9. Durack J, Kimes NE, Lin DL, Rauch M, McKean M, McCauley K, et al. Delayed gut microbiota development in high-risk for asthma infants is temporarily modifiable by Lactobacillus supplementation. Nat Commun. 2018;9:707.
10. Jeffrey MP, Strap JL, Taggart HJ, Green-Johnson JM. Suppression of intestinal epithelial cell chemokine production by Lactobacillus rhamnosus R0011 and Lactobacillus helveticus R0389 is mediated by secreted bioactive molecules. Front Immunol. 2018;9:13.
11. Martens K, Pugin B, De Boeck I, Spacova I, Steelant B, Seys SF, et al. Probiotics for the airways: Potential to improve epithelial and immune homeostasis. Allergy. 2018;73:1954-63.
12. Kamaladevi A, Balamurugan K. Lactobacillus casei triggers a TLR mediated RACK-1 dependent p38 MAPK pathway in Caenorhabditis elegans to resist Klebsiella pneumoniae infection. Food Funct. 2016;7:3211-23.
13. Li HH, Zhang L, Chen LB, Zhu Q, Wang WJ, Qiao JY. Lactobacillus acidophilus alleviates the inflammatory response to enterotoxigenic Escherichia coli K88 via inhibition of the NF-kappa B and p38 mitogen-activated protein kinase signaling pathways in piglets. BMC Microbiol. 2016;16:8.
14. Li AL, Meng XC, Duan CC, Huo GC, Zheng QL, Li D. Suppressive effects of oral administration of heat-killed Lactobacillus acidophilus on T Helper-17 immune responses in a bovine beta-Lactoglobulin-sensitized mice model. Biol Pharm Bull. 2013;36:202-7.
15. Wang JJ, Li SH, Li AL, Zhang QM, Ni WW, Li MN, et al. Effect of Lactobacillus acidophilus KLDS 1.0738 on miRNA expression in vitro and in vivo models of beta-lactoglobulin allergy. Biosci Biotechnol Biochem. 2018;82:1955-63.
16. Zheng JP, Cheng G, Li QY, Jiao SM, Feng C, Zhao XM, et al. Chitin oligosaccharide modulates gut microbiota and attenuates high fat-diet-induced metabolic syndrome in mice. Mar Drugs. 2018;16.
17. Maldonado Galdeano C, Cazorla SI, Lemme Dumit JM, Velez E, Perdigon G. Beneficial effects of probiotic consumption on the immune system. Ann Nutr Metab. 2019;74:115-24.
18. Tsai YL, Lin TL, Chang CJ, Wu TR, Lai WF, Lu CC, et al. Probiotics, prebiotics and amelioration of diseases. J Biomed Sci. 2019;26.
19. Shin NR, Whon TW, Bae JW. Proteobacteria: Microbial signature of dysbiosis in gut microbiota. Trends Biotechnol. 2015;33:496-503.
20. Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012;13.
21. Zhang HS, Wang HF, Shepherd M, Wen K, Li GH, Yang XD, et al. Probiotics and virulent human rotavirus modulate the transplanted human gut microbiota in gnotobiotic pigs. Gut Pathog. 2014;6.
22. Papamichael K, Konstantopoulos P, Mantzaris GJ. Helicobacter pylori infection and inflammatory bowel disease: is there a link? World J Gastroenterol. 2014;20:6374-85.
23. Yu Q, Zhang S, Li L, Xiong L, Chao K, Zhong B, et al. Enterohepatic helicobacter species as a potential causative factor in inflammatory bowel disease: A meta-analysis. Medicine (Baltimore). 2015;94:e1773.
24. Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system. Science. 2012;336:1268-73.
25. Curtis MM, Hu Z, Klimko C, Narayanan S, Deberardinis R, Sperandio V. The gut commensal Bacteroides thetaiotaomicron exacerbates enteric infection through modification of the metabolic landscape. Cell Host Microbe. 2014;16:759-69.
26. Berni Canani R, De Filippis F, Nocerino R, Paparo L, Di Scala C, Cosenza L, et al. Gut microbiota composition and butyrate production in children affected by non-IgE-mediated cow’s milk allergy. Sci Rep. 2018;8:12500.
27. Meehan CJ, Beiko RG. A phylogenomic view of ecological specialization in the Lachnospiraceae, a family of digestive tract-associated bacteria. Genome Biol Evol. 2014;6:703-13.
28. Esquivel-Elizondo S, Ilhan ZE, Garcia-Pena EI, Krajmalnik-Brown R. Insights into butyrate production in a controlled fermentation system via gene predictions. Msystems. 2017;2.
29. Sossai P. Butyric acid: What is the future for this old substance? Swiss Med Wkly. 2012;142:w13596.
30. Wang YY, Guo YL, Chen H, Wei H, Wan CX. Potential of Lactobacillus plantarum ZDY2013 and Bifidobacterium bifidum WBIN03 in relieving colitis by gut microbiota, immune, and antioxidative stress. Can J Microbiol. 2018;64:327-37.
31. Sagheddu V, Patrone V, Miragoli F, Puglisi E, Morelli L. Infant early gut colonization by lachnospiraceae: High frequency of Ruminococcus gnavus. Front Pediatr. 2016;4:57.
32. Zhao L, Zhang Q, Ma WN, Tian F, Shen HY, Zhou MM. A combination of quercetin and resveratrol reduces obesity in high-fat diet-fed rats by modulation of gut microbiota. Food Funct. 2017;8:4644-56.
33. Qi C, Li Y, Yu RQ, Zhou SL, Wang XG, Le GW, et al. Composition and immuno-stimulatory properties of extracellular DNA from mouse gut flora. World J Gastroenterol. 2017;23:7830-9.
34. Chen CY, Kao CL, Liu CM. The cancer prevention, antiinflammatory and anti-oxidation of bioactive phytochemicals targeting the TLR4 signaling pathway. Int J Mol Sci. 2018;19.
35. Loganathan R, Nazeer M, Goda V, Devaraju P, Ali M, Karunakaran P, et al. Genetic variants of TLR4 and TLR9 are risk factors for chronic Helicobacter pylori infection in South Indian Tamils. Hum Immunol. 2017;78:216-20.
36. Kim JM, Oh YK, Kim YJ, Oh HB, Cho YJ. Polarized secretion of CXC chemokines by human intestinal epithelial cells in response to Bacteroides fragilis enterotoxin: NF-kappa B plays a major role in the regulation of IL-8 expression. Clin Exp Immunol. 2010;123:421-7.
37. Dong LN, Wang JP, Liu P, Yang YF, Feng J, Han Y. Faecal and mucosal microbiota in patients with functional gastrointestinal disorders: Correlation with toll-like receptor 2/toll-like receptor 4 expression. World J Gastroenterol. 2017;23:6665-73.
38. Chen L, Wilson JE, Koenigsknecht MJ, Chou WC, Montgomery SA, Truax AD, et al. NLRP12 attenuates colon inflammation by maintaining colonic microbial diversity and promoting protective commensal bacterial growth. Nat Immunol. 2017;18:541---51.
39. Lu CC, Kuo HC, Wang FS, Jou MH, Lee KC, Chuang JH. Upregulation of TLRs and IL-6 as a marker in human colorectal cancer.
Int J Mol Sci. 2015;16:159-77.
40. Takeda K, Akira S. TLR signaling pathways. Semin Immunol. 2004;16:3-9.
41. Li AL, Sun YQ, Du P, Meng XC, Guo L, Li S, et al. The effect of Lactobacillus actobacillus peptidoglycan on bovine betaLactoglobulin sensitized mice via TLR2/NF-kappa B pathway. Iran J Allergy Asthma Immunol. 2017;16:147-58.
42. Michels KR, Lukacs NW, Fonseca W. TLR activation and allergic disease: Early life microbiome and treatment. Curr Allergy Asthma Rep. 2018;18.
43. Vijaykrishnaraj M, Mohan Kumar BV, Muthukumar SP, Kurrey NK, Prabhasankar P. Antigen-specific gut inflammation and systemic immune responses induced by prolonging wheat gluten sensitization in BALB/c murine model. J Proteome Res. 2017;16, acs.jproteome.7b00199.
44. Saad MA, El-Sahhar AE, Arab HH, Al-Shorbagy MY. Nicorandil abates arthritic perturbations induced by complete Freund’s adjuvant in rats via conquering TLR4-MyD88-TRAF6 signaling pathway. Life Sci. 2019;218:284-91.
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Mar 15, 2020
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Ni, W.- w., Zhang, Q.- m., Zhang, X., Li, Y., Yu, S.- s., Wu, H.- y., Chen, Z., Li, A.- l., Du, P., & Li, C. (2020). Modulation effect of Lactobacillus acidophilus KLDS 1.0738 on gut microbiota and TLR4 expression in -lactoglobulin-induced allergic mice model. Allergologia Et Immunopathologia, 48(2), 149-157. https://all-imm.com/index.php/aei/article/view/226
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How to Cite
Ni, W.- w., Zhang, Q.- m., Zhang, X., Li, Y., Yu, S.- s., Wu, H.- y., Chen, Z., Li, A.- l., Du, P., & Li, C. (2020). Modulation effect of Lactobacillus acidophilus KLDS 1.0738 on gut microbiota and TLR4 expression in -lactoglobulin-induced allergic mice model. Allergologia Et Immunopathologia, 48(2), 149-157. https://all-imm.com/index.php/aei/article/view/226