Journal of Microbiology and Biotechnology

  • 제33권8호
  • /
  • Pages.1039-1049
  • /
  • 2023
  • /
  • 1017-7825(pISSN)
  • /
  • 1738-8872(eISSN)
한국미생물·생명공학회 (The Korean Society for Microbiology and Biotechnology)
권호 표지
DOI QR코드

DOI QR Code

Anti-Inflammatory Response in TNFα/IFNγ-Induced HaCaT Keratinocytes and Probiotic Properties of Lacticaseibacillus rhamnosus MG4644, Lacticaseibacillus paracasei MG4693, and Lactococcus lactis MG5474

  • 투고 : 2023.01.19
  • 심사 : 2023.04.26
  • 발행 : 2023.08.28
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Atopic dermatitis (AD) is a chronic inflammatory disease caused by immune dysregulation. Meanwhile, the supernatant of lactic acid bacteria (SL) was recently reported to have anti-inflammatory effects. In addition, HaCaT keratinocytes stimulated by tumor necrosis factor alpha (TNF-α) and interferon gamma (IFN-γ) are widely used for studying AD-like responses. In this study, we evaluated the anti-inflammatory effects of SL from lactic acid bacteria (LAB) on TNF-α/IFN-γ-induced HaCaT keratinocytes, and then we investigated the strains' probiotic properties. SL was noncytotoxic and regulated chemokines (macrophage-derived chemokine (MDC) and thymus and activation-regulated chemokine (TARC)) and cytokines (interleukin (IL)-4, IL-5, IL-25, and IL-33) in TNF-α/IFN-γ-induced HaCaT keratinocytes. SL from Lacticaseibacillus rhamnosus MG4644, Lacticaseibacillus paracasei MG4693, and Lactococcus lactis MG5474 decreased the phosphorylation of nuclear factor-κB (NF-κB) and mitogen-activated protein kinase (MAPK). Furthermore, the safety of the three strains was demonstrated via hemolysis, bile salt hydrolase (BSH) activity, and toxicity tests, and the stability was confirmed under simulated gastrointestinal conditions. Therefore, L. rhamnosus MG4644, L. paracasei MG4693, and Lc. lactis MG5474 have potential applications in functional food as they are stable and safe for intestinal epithelial cells and could improve atopic inflammation.

키워드

참고문헌

  1. Torres T, Ferreira E, Goncalo M, Mendes-Bastos P, Selores M, Filipe P. 2019. Update on atopic dermatitis. Acta Medica Port. 32: 606-613. https://doi.org/10.20344/amp.11963
  2. Yoo J, Koo HYR, Han K, Lee YB. 2022. Impairment of quality of life and mental health status in adult-onset atopic dermatitis. Ann. Dermatol. 34: 278-286. https://doi.org/10.5021/ad.21.282
  3. Ha J, Lee SW, Yon DK. 2020. Ten-year trends and prevalence of asthma, allergic rhinitis, and atopic dermatitis among the Korean population, 2008-2017. Clin. Exp. Pediatr. 63: 278-283. https://doi.org/10.3345/cep.2019.01291
  4. Manjelievskaia J, Boytsov N, Brouillette MA, Onyekwere U, Pierce E, Goldblum O, et al. 2021. The direct and indirect costs of adult atopic dermatitis. J. Manag. Care Spec. Pharm. 27: 1416-1425. https://doi.org/10.18553/jmcp.2021.27.10.1416
  5. Albader SS, Alharbi AA, Alenezi RF, Alsaif FM. 2019. Dupilumab side effect in a patient with atopic dermatitis: a case report study. Biologics 13: 79-82. https://doi.org/10.2147/BTT.S195512
  6. Lee JY, Kim Y, Kim J-I, Lee H-Y, Moon G-S, Kang C-H. 2022. Improvements in human keratinocytes and antimicrobial effect mediated by cell-free supernatants derived from probiotics. Fermentation 8: 332.
  7. Bitschar K, Wolz C, Krismer B, Peschel A, Schittek B. 2017. Keratinocytes as sensors and central players in the immune defense against Staphylococcus aureus in the skin. J. Dermatol. Sci. 87: 215-220. https://doi.org/10.1016/j.jdermsci.2017.06.003
  8. Albanesi C, Scarponi C, Giustizieri ML, Girolomoni G. 2005. Keratinocytes in inflammatory skin diseases. Curr. Drug Targets Inflamm. Allergy 4: 329-334. https://doi.org/10.2174/1568010054022033
  9. Cho SH, Kim HS, Lee W, Han EJ, Kim SY, Fernando IS, et al. 2020. Eckol from Ecklonia cava ameliorates TNF-α/IFN-γ-induced inflammatory responses via regulating MAPKs and NF-κB signaling pathway in HaCaT cells. Int. Immunopharmacol. 82: 106146.
  10. Chieosilapatham P, Kiatsurayanon C, Umehara Y, Trujillo-Paez J, Peng G, Yue H, et al. 2021. Keratinocytes: Innate immune cells in atopic dermatitis. Clin. Expe. Immunol. 204: 296-309. https://doi.org/10.1111/cei.13575
  11. Yan F, Li F, Liu J, Ye S, Zhang Y, Jia J, et al. 2020. The formulae and biologically active ingredients of Chinese herbal medicines for the treatment of atopic dermatitis. Biomed. Pharmacother. 127: 110142.
  12. Edalati E, Saneei B, Alizadeh M, Hosseini SS, Bialvaei AZ, Taheri K. 2019. Isolation of probiotic bacteria from raw camel's milk and their antagonistic effects on two bacteria causing food poisoning. New Microb. New Infect. 27: 64-68. https://doi.org/10.1016/j.nmni.2018.11.008
  13. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, et al. 2014. The international scientific association for robiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 11: 506-514. https://doi.org/10.1038/nrgastro.2014.66
  14. Lizardo MV, Tavaria FK. 2022. Probiotics and skin health, pp. 389-405. Probiotics, Ed. Elsevier.
  15. Rusu E, Enache G, Cursaru R, Alexescu A, Radu R, Onila O, et al. 2019. Prebiotics and probiotics in atopic dermatitis. Exp. Ther. Med. 18: 926-931. https://doi.org/10.3892/etm.2019.7678
  16. Lew LC, Liong MT. 2013. Bioactives from probiotics for dermal health: functions and benefits. J. Appl. Microbiol. 114: 1241-1253. https://doi.org/10.1111/jam.12137
  17. Lee JY, Kang JH, Jung YR, Kang CH. 2022. Lactobacillus gasseri MG4247 and Lacticaseibacillus paracasei MG4272 and MG4577 modulate allergic inflammatory response in RAW 264.7 and RBL-2H3 cells. Probiotics Antimicrob. Proteins 31: 1-10. https://doi.org/10.1007/s12602-022-09950-4
  18. Tolosa L, Donato MT, Gomez-Lechon MJ. 2015. General cytotoxicity assessment by means of the MTT assay, pp. 333-348. Protocols in in vitro hepatocyte research, Ed. Springer.
  19. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25: 402-408. https://doi.org/10.1006/meth.2001.1262
  20. Bass JJ, Wilkinson DJ, Rankin D, Phillips BE, Szewczyk NJ, Smith K, et al. 2017. An overview of technical considerations for Western blotting applications to physiological research. Scand. J. Med. Sci. Sports 27: 4-25. https://doi.org/10.1111/sms.12702
  21. Park JY, Lee JY, Kim Y, Kang CH. 2023. Latilactobacillus sakei Wikim0066 protects skin through MMP regulation on UVB-irradiated in vitro and in vivo model. Nutrients 15: 726.
  22. Syed Yaacob SN, Huyop F, Kamarulzaman Raja Ibrahim R, Wahab RA. 2018. Identification of Lactobacillus spp. and Fructobacillus spp. isolated from fresh Heterotrigona itama honey and their antagonistic activities against clinical pathogenic bacteria. J. Apic. Res. 57: 395-405. https://doi.org/10.1080/00218839.2018.1428047
  23. Kang CH, Kim Y, Han SH, Jeong Y, Park H, Paek NS. 2019. Probiotic properties of bifidobacteria isolated from feces of infants. J. Milk Sci. Biotechnol. 37: 40-48. https://doi.org/10.22424/jmsb.2019.37.1.40
  24. Yasmin I, Saeed M, Khan WA, Khaliq A, Chughtai MFJ, Iqbal R, et al. 2020. In vitro probiotic potential and safety evaluation (hemolytic, cytotoxic activity) of Bifidobacterium strains isolated from raw camel milk. Microorganisms 8: 354.
  25. Buxton R. 2005. Blood agar plates and hemolysis protocols. American Society for Microbiology. pp. 1-9.
  26. Shehata M, El Sohaimy S, El-Sahn MA, Youssef M. 2016. Screening of isolated potential probiotic lactic acid bacteria for cholesterol lowering property and bile salt hydrolase activity. Ann. Agric. Sci. 61: 65-75. https://doi.org/10.1016/j.aoas.2016.03.001
  27. Kim S, Lee JY, Jeong Y, Kang CH. 2022. Antioxidant activity and probiotic properties of lactic acid bacteria. Fermentation 8: 29.
  28. Fonseca HC, de Sousa Melo D, Ramos CL, Dias DR, Schwan RF. 2021. Probiotic properties of lactobacilli and their ability to inhibit the adhesion of enteropathogenic bacteria to Caco-2 and HT-29 cells. Probiotics Antimicrob. Proteins 13: 102-112. https://doi.org/10.1007/s12602-020-09659-2
  29. Cheng KW, Tseng CH, Chen IJ, Huang BC, Liu HJ, Ho KW, et al. 2022. Inhibition of gut microbial β-glucuronidase effectively prevents carcinogen-induced microbial dysbiosis and intestinal tumorigenesis. Pharmacol. Res. 177: 106115.
  30. De Pessemier B, Grine L, Debaere M, Maes A, Paetzold B, Callewaert C. 2021. Gut-skin axis: current knowledge of the interrelationship between microbial dysbiosis and skin conditions. Microorganisms 9: 353.
  31. Lee SY, Lee E, Park YM, Hong SJ. 2018. Microbiome in the gut-skin axis in atopic dermatitis. Allergy, Asthma Immunol. Res. 10: 354-362. https://doi.org/10.4168/aair.2018.10.4.354
  32. Lolou V, Panayiotidis MI. 2019. Functional role of probiotics and prebiotics on skin health and disease. Fermentation 5: 41.
  33. De Vuyst E, Salmon M, Evrard C, Lambert de Rouvroit C, Poumay Y. 2017. Atopic dermatitis studies through in vitro models. Front. Med. 4: 119.
  34. Song HK, Park SH, Kim HJ, Jang S, Kim T. 2022. Spatholobus suberectus dunn water extract ameliorates atopic dermatitis-like symptoms by suppressing proinflammatory chemokine production in vivo and in vitro. Front. Pharmacol. 13: 919230.
  35. Hwang DH, Koh PO, Kang C, Kim E. 2021. Rosa davurica Pall. improves DNCB-induced atopic dermatitis in mice and regulated TNF-alpha/IFN-gamma-induced skin inflammatory responses in HaCaT cells. Phytomedicine 91: 153708.
  36. Yang CC, Hung YL, Ko WC, Tsai YJ, Chang JF, Liang CW, et al. 2021. Effect of neferine on DNCB-induced atopic dermatitis in HaCaT cells and BALB/c mice. Int. J. Mol. Sci. 22: 8237.
  37. Sebastian K, Borowski A, Kuepper M, Friedrich K. 2008. Signal transduction around thymic stromal lymphopoietin (TSLP) in atopic asthma. Cell Commun. Signal. 6: 5.
  38. Divekar R, Kita H. 2015. Recent advances in epithelium-derived cytokines (IL-33, IL-25 and TSLP) and allergic inflammation. Curr. Opin. Allergy Clin. Immunol. 15: 98.
  39. Xiao X, Hu X, Yao J, Cao W, Zou Z, Wang L, et al. 2022. The role of short-chain fatty acids in inflammatory skin diseases. Front. Microbiol. 13: 1083432.
  40. Kang CH, Kim JS, Park HM, Kim S, Paek NS. 2021. Antioxidant activity and short-chain fatty acid production of lactic acid bacteria isolated from Korean individuals and fermented foods. 3 Biotech. 11: 217.
  41. Aryantini NPD, Yamasaki E, Kurazono H, Sujaya IN, Urashima T, Fukuda K. 2017. In vitro safety assessments and antimicrobial activities of Lactobacillus rhamnosus strains isolated from a fermented mare's milk. Anim. Sci. J. 88: 517-525. https://doi.org/10.1111/asj.12668
  42. Meerloo JV, Kaspers GJ, Cloos J. 2011. Cell sensitivity assays: the MTT assay, pp. 237-245. Cancer cell culture, Ed. Springer.
  43. Ranjan KG, Sankar GG, Raju D. 2020. In vitro evaluation of antibacterial, cytotoxic and adherence studies of selected commercial probiotics. J. Pure Appl. Microbiol. 14: 2085-2091. https://doi.org/10.22207/JPAM.14.3.49
  44. Khare A, Gaur S. 2020. Cholesterol-lowering effects of Lactobacillus species. Curr. Microbiol. 77: 638-644. https://doi.org/10.1007/s00284-020-01903-w
  45. Byakika S, Mukisa IM, Byaruhanga YB, Muyanja C. 2019. A review of criteria and methods for evaluating the probiotic potential of microorganisms. Food Rev. Int. 35: 427-466. https://doi.org/10.1080/87559129.2019.1584815
  46. Casarotti SN, Todorov SD, Penna ALB. 2015. Effect of different matrices on probiotic resistance to in vitro simulated gastrointestinal conditions. Int. J. Dairy Technol. 68: 595-601. https://doi.org/10.1111/1471-0307.12215
  47. Jovanovic JN, Nikolic B, Seatovic S, Zavisic G, Mitic-Culafic D, Vukovic-Gacic B, et al. 2015. Characterization of some potentially probiotic Lactobacillus strains of human origin. Food Sci. Biotechnol. 24: 1781-1788. https://doi.org/10.1007/s10068-015-0232-7
  48. Verhoeckx K, Cotter P, Lopez-Exposito I, Kleiveland C, Lea T, Mackie A, et al. 2015. The impact of food bioactives on health: in vitro and ex vivo models. Cham (CH): Springer; 2015.