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Screening for Lactic Acid Bacterial Strains as Probiotics Exhibiting Anti-inflammatory and Antioxidative Characteristic Via Immune Modulation in HaCaT Cell

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Abstract

In this study, the basic probiotic characteristics and functional properties of lactic acid bacteria (LAB) were investigated using two in vitro models of inflammation induced by lipopolysaccharide (LPS) and H2O2. Fifteen strains were prescreened out of 60 LAB candidates based on their radical scavenging activity to determine the antioxidant capacity of the strains. The top 15 candidates were further investigated to evaluate their survival rate under low pH and bile salt conditions that mimic the intestinal environment. Three strains, Levilactobacillus brevis D70 (Levilact), Lactiplantibacillus pentosus S16 (Lactipla), and Limosilactobacillus fermentum MF10 (Limosilact), were capable of scavenging free radicals and survived under artificial intestinal conditions. Therefore, Levilact. brevis D70, Lactipla. pentosus S16, and Limosilact. fermentum MF10 were selected for further antioxidant, anti-inflammation, and mitochondrial activity examinations via cell models of inflammation and oxidative stress. Among the three strains, Limosilact. fermentum MF10 showed the highest anti-inflammatory activities by significantly downregulating the relative mRNA expression levels of inflammatory biomarkers such as interleukin 8 (IL-8) and interferon-gamma (IFN-γ) induced by LPS (P < 0.05). Moreover, Limosilact. fermentum MF10 was also capable of upregulating the gene expression levels of antioxidative mediator glutathione peroxidase 4 (GPX4) induced by reactive oxygen species (ROS) in both human HT-29 epithelial cells and human HaCaT keratinocytes. Limosilact. fermentum MF10 was also capable of regulating mitochondrial membrane potential (MMP), which plays a key role in the mitochondrial activity of HaCaT cells. As a result, Limosilact. fermentum MF10 showed the highest potential for probiotic properties and impacts the immune-related gut-skin axis by altering proinflammatory cytokines, antioxidative biomarkers, and MMP.

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Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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References

  1. Teneva D, Denkova R, Goranov B, Denkova Z, Kostov G (2017) Antimicrobial activity of Lactobacillus plantarum strains against Salmonella pathogens. Ukr Food J 6:125–133. https://doi.org/10.24263/2304-974X-2017-6-1-14

  2. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME (2014) 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 11:506–514. https://doi.org/10.1038/nrgastro.2014.66

    Article  PubMed  Google Scholar 

  3. Lee CS, Tan PL, Eor JY, Choi DH, Park M, Seo SK, Yoon S, Yang S, Kim SH (2019) Prophylactic use of probiotic chocolate modulates intestinal physiological functions in constipated rats. J Sci Food Agric 99:3045–3056. https://doi.org/10.1002/jsfa.9518

    Article  CAS  PubMed  Google Scholar 

  4. Lee CS, Park MH, Kim BK, Kim SH (2021) Antiobesity effect of novel probiotic strains in a mouse model of high-fat diet-induced obesity. Probiotics Antimicrob Proteins 13:1054–1067. https://doi.org/10.1007/s12602-021-09752-0

    Article  CAS  PubMed  Google Scholar 

  5. Lee CS, Kim JY, Kim BK, Lee IO, Park NH, Kim SH (2021) Lactobacillus-fermented milk products attenuate bone loss in an experimental rat model of ovariectomy-induced post-menopausal primary osteoporosis. J Appl Microbiol 130:2041–2062. https://doi.org/10.1111/jam.14852

    Article  CAS  PubMed  Google Scholar 

  6. Nam B, Kim SA, Park SD, Kim HJ, Kim JS, Bae CH, Kim JY, Nam W, Lee JL, Sim JH (2020) Regulatory effects of Lactobacillus plantarum HY7714 on skin health by improving intestinal condition. Plos One 15:e0231268. https://doi.org/10.1371/journal.pone.0231268

  7. Zheng J, Wittouck S, Salvetti E, Franz CMAP, Harris HMB, Mattarelli P, O’Toole PW, Pot B, Vandamme P, Walter J, Watanabe K, Wuyts S, Felis GE, Gänzle MG, Lebeer S (2020) A taxonomic note on the genus Lactobacillus: description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int J Syst Evol Microbiol 70:2782–2858. https://doi.org/10.1099/ijsem.0.004107

    Article  CAS  PubMed  Google Scholar 

  8. Bron PA, van Baarlen P, Kleerebezem M (2011) Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nat Rev Microbiol 10:66–78. https://doi.org/10.1038/nrmicro2690

    Article  CAS  PubMed  Google Scholar 

  9. Lee CS, Kim SH (2020) Anti-inflammatory and anti-osteoporotic potential of Lactobacillus plantarum A41 and L. fermentum SRK414 as probiotics. Probiotics Antimicrob Proteins 12:623–634. https://doi.org/10.1007/s12602-019-09577-y

    Article  CAS  PubMed  Google Scholar 

  10. O’Neill CA, Monteleone G, McLaughlin JT, Paus R (2016) The gut-skin axis in health and disease: a paradigm with therapeutic implications. BioEssays 38:1167–1176. https://doi.org/10.1002/bies.201600008

    Article  PubMed  Google Scholar 

  11. Byrd AL, Belkaid Y, Segre JA (2018) The human skin microbiome. Nat Rev Microbiol 16:143–155. https://doi.org/10.1038/nrmicro.2017.157

    Article  CAS  PubMed  Google Scholar 

  12. Jeong JH, Lee CY, Chung DK (2016) Probiotic lactic acid bacteria and skin health. Crit Rev Food Sci Nutr 56:2331–2337. https://doi.org/10.1080/10408398.2013.834874

    Article  CAS  PubMed  Google Scholar 

  13. Nestle FO, Di Meglio P, Qin JZ, Nickoloff BJ (2009) Skin immune sentinels in health and disease. Nat Rev Immunol 9:679–691. https://doi.org/10.1038/nri2622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Zhang Y, Shi S, Wang Y, Huang K (2011) Target-guided isolation and purification of antioxidants from Selaginella sinensis by offline coupling of DPPH-HPLC and HSCCC experiments. J Chromatogr B Analyt Technol Biomed Life Sci 879:191–196. https://doi.org/10.1016/j.jchromb.2010.12.004

    Article  CAS  PubMed  Google Scholar 

  15. Jacobsen CN, Rosenfeldt Nielsen V, Hayford AE, Møller PL, Michaelsen KF, Paerregaard A, Sandström B, Tvede M, Jakobsen M (1999) Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans. Appl Environ Microbiol 65:4949–4956. https://doi.org/10.1128/AEM.65.11.4949-4956.1999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Lee CS, Park MH, Kim SH (2022) Selection and characterization of probiotic bacteria exhibiting antiadipogenic potential in 3T3-L1 preadipocytes. Probiotics Antimicrob Proteins 14:72–86. https://doi.org/10.1007/s12602-021-09793-5

    Article  CAS  PubMed  Google Scholar 

  17. Jang S, Javadov S (2018) Elucidating the contribution of ETC complexes I and II to the respirasome formation in cardiac mitochondria. Sci Rep 8:17732. https://doi.org/10.1038/s41598-018-36040-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Di Caprio R, Lembo S, Di Costanzo L, Balato A, Monfrecola G (2015) Anti-inflammatory properties of low and high doxycycline doses: an in vitro study. Mediators Inflamm 2015:329418. https://doi.org/10.1155/2015/329418

  19. Kim Y, Koh JH, Ahn YJ, Oh S, Kim SH (2015) The synergic anti-inflammatory impact of Gleditsia sinensis Lam. and Lactobacillus brevis KY21 on intestinal epithelial cells in a DSS-induced colitis model. Korean J Food Sci Anim Resour 35:604–610. https://doi.org/10.5851/kosfa.2015.35.5.604

    Article  PubMed  PubMed Central  Google Scholar 

  20. Li Y, Xie H, Deng Z, Wang B, Tang Y, Zhao Z, Yuan X, Zuo Z, Xu S, Zhang Y (2019) Tranexamic acid ameliorates rosacea symptoms through regulating immune response and angiogenesis. Int Immunopharmacol 67:326–334. https://doi.org/10.1016/j.intimp.2018.12.031

    Article  CAS  PubMed  Google Scholar 

  21. Hardy OT, Perugini RA, Nicoloro SM, Gallagher-Dorval K, Puri V, Straubhaar J, Czech MP (2011) Body mass index-independent inflammation in omental adipose tissue associated with insulin resistance in morbid obesity. Surg Obes Relat Dis 7(1):60–67. https://doi.org/10.1016/j.soard.2010.05.013

    Article  PubMed  Google Scholar 

  22. Giles AJ, Hutchinson M-KN, Sonnemann HM, Jung J, Fecci PE, Ratnam NM, Zhang W, Song H, Bailey R, Davis D (2018) Dexamethasone-induced immunosuppression: mechanisms and implications for immunotherapy. J Immunother Cancer 6(1):1–13. https://doi.org/10.1186/s40425-018-0371-5

    Article  Google Scholar 

  23. Li Y, Cheng T, Wan C, Cang Y (2020) circRNA_0084043 contributes to the progression of diabetic retinopathy via sponging miR-140–3p and inducing TGFA gene expression in retinal pigment epithelial cells. Gene 747:144653. https://doi.org/10.1016/j.gene.2020.144653

  24. Hassani S, Ghaffari P, Chahardouli B, Alimoghaddam K, Ghavamzadeh A, Alizadeh S, Ghaffari SH (2018) Disulfiram/copper causes ROS levels alteration, cell cycle inhibition, and apoptosis in acute myeloid leukaemia cell lines with modulation in the expression of related genes. Biomed Pharmacother 99:561–569. https://doi.org/10.1016/j.biopha.2018.01.109

    Article  CAS  PubMed  Google Scholar 

  25. Wang Z, Cai B, Cao C, Lv H, Dai Y, Zheng M, Zhao G, Peng Y, Gou W, Wang J (2021) Downregulation of CD151 induces oxidative stress and apoptosis in trophoblast cells via inhibiting ERK/Nrf2 signaling pathway in preeclampsia. Free Radic Biol Med 164:249–257. https://doi.org/10.1016/j.freeradbiomed.2020.12.441

    Article  CAS  PubMed  Google Scholar 

  26. Liu Y, Wang Y, Liu J, Kang R, Tang D (2021) Interplay between MTOR and GPX4 signaling modulates autophagy-dependent ferroptotic cancer cell death. Cancer Gene Ther 28(1):55–63. https://doi.org/10.1038/s41417-020-0182-y

    Article  CAS  PubMed  Google Scholar 

  27. Zhao R, Ying M, Gu S, Yin W, Li Y, Yuan H, Fang S, Li M (2019) Cysteinyl leukotriene receptor 2 is involved in inflammation and neuronal damage by mediating microglia M1/M2 polarization through NF-κB pathway. Neuroscience 422:99–118. https://doi.org/10.1016/j.neuroscience.2019.10.048

    Article  CAS  PubMed  Google Scholar 

  28. Wang Y, Wu Y, Wang Y, Xu H, Mei X, Yu D, Wang Y, Li W (2017) Antioxidant properties of probiotic bacteria. Nutrients 9:521. https://doi.org/10.3390/nu9050521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Nowak A, Paliwoda A, Błasiak J (2019) Anti-proliferative, pro-apoptotic and anti-oxidative activity of Lactobacillus and Bifidobacterium strains: a review of mechanisms and therapeutic perspectives. Crit Rev Food Sci Nutr 59(21):3456–3467. https://doi.org/10.1080/10408398.2018.1494539

    Article  CAS  PubMed  Google Scholar 

  30. Ramirez-Chavarin M, Wacher C, Eslava-Campos C, Perez-Chabela M (2013) Probiotic potential of thermotolerant lactic acid bacteria strains isolated from cooked meat products. Int Food Res J 20:991–1000

    CAS  Google Scholar 

  31. Denkova R, Dimbareva D, Denkova Z, Dobrev I (2012) Probiotic properties of Lactobacillus acidophilus A2 of human origin. In: Modern Technol Food Ind 334–339

  32. Argyri AA, Zoumpopoulou G, Karatzas KA, Tsakalidou E, Nychas GJ, Panagou EZ, Tassou CC (2013) Selection of potential probiotic lactic acid bacteria from fermented olives by in vitro tests. Food Microbiol 33:282–291. https://doi.org/10.1016/j.fm.2012.10.005

    Article  CAS  PubMed  Google Scholar 

  33. Bao Y, Zhang Y, Zhang Y, Liu Y, Wang S, Dong X, Wang Y, Zhang H (2010) Screening of potential probiotic properties of Lactobacillus fermentum isolated from traditional dairy products. Food Control 21:695–701. https://doi.org/10.1016/j.foodcont.2009.10.010

    Article  CAS  Google Scholar 

  34. Tannock GW, Dashkevicz MP, Feighner SD (1989) Lactobacilli and bile salt hydrolase in the murine intestinal tract. Appl Environ Microbiol 55:1848–1851. https://doi.org/10.1128/aem.55.7.1848-1851.1989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Guo C-F, Zhang S, Yuan Y-H, Yue T-L, Li J-Y (2015) Comparison of Lactobacilli isolated from Chinese suan-tsai and koumiss for their probiotic and functional properties. J Funct Foods 12:294–302. https://doi.org/10.1016/j.jff.2014.11.029

    Article  CAS  Google Scholar 

  36. Salar U, Nizamani A, Arshad F, Khan KM, Fakhri MI, Perveen S, Ahmed N, Choudhary MI (2019) Bis-coumarins; non-cytotoxic selective urease inhibitors and antiglycation agents. Bioorg Chem 91:103170. https://doi.org/10.1016/j.bioorg.2019.103170

  37. Khan DM, Manzoor MAP, Rao IV, Moosabba MS (2019) Evaluation of biofilm formation, cell surface hydrophobicity and gelatinase activity in Acinetobacter baumannii strains isolated from patients of diabetic and non-diabetic foot ulcer infections. Biocatal Agric Biotechnol 18:101007. https://doi.org/10.1016/j.bcab.2019.01.045

  38. Duchen MR (2000) Mitochondria and calcium: from cell signalling to cell death. J Physiol 529:57–68. https://doi.org/10.1111/j.1469-7793.2000.00057.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Sanz A, Pamplona R, Barja G (2006) Is the mitochondrial free radical theory of aging intact? Antioxid Redox Signal 8:582–599. https://doi.org/10.1089/ars.2006.8.582

    Article  CAS  PubMed  Google Scholar 

  40. Schapira AHV (2006) Mitochondrial disease. Lancet 368:70–82. https://doi.org/10.1016/S0140-6736(06)68970-8

    Article  CAS  PubMed  Google Scholar 

  41. Suski JM, Lebiedzinska M, Bonora M, Pinton P, Duszynski J, Wieckowski MR (2012) Relation between mitochondrial membrane potential and ROS formation. Methods Mol Biol 810:183–205. https://doi.org/10.1007/978-1-61779-382-0_12

    Article  CAS  PubMed  Google Scholar 

  42. Lim HY, Jeong D, Park SH, Shin KK, Hong YH, Kim E, Yu YG, Kim TR, Kim H, Lee J, Cho JY (2020) Antiwrinkle and antimelanogenesis effects of tyndallized Lactobacillus acidophilus KCCM12625P. Int J Mol Sci 21:1620. https://doi.org/10.3390/ijms21051620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Philippe D, Favre L, Foata F, Adolfsson O, Perruisseau-Carrier G, Vidal K, Reuteler G, Dayer-Schneider J, Mueller C, Blum S (2011) Bifidobacterium lactis attenuates onset of inflammation in a murine model of colitis. World J Gastroenterol 17:459–469. https://doi.org/10.3748/wjg.v17.i4.459

    Article  PubMed  PubMed Central  Google Scholar 

  44. Atabati H, Esmaeili SA, Saburi E, Akhlaghi M, Raoofi A, Rezaei N, Momtazi-Borojeni AA (2020) Probiotics with ameliorating effects on the severity of skin inflammation in psoriasis: evidence from experimental and clinical studies. J Cell Physiol 235(12):8925–8937. https://doi.org/10.1002/jcp.29737

    Article  CAS  PubMed  Google Scholar 

  45. Matsumoto S, Hara T, Hori T, Mitsuyama K, Nagaoka M, Tomiyasu N, Suzuki A, Sata M (2005) Probiotic Lactobacillus-induced improvement in murine chronic inflammatory bowel disease is associated with the down-regulation of pro-inflammatory cytokines in lamina propria mononuclear cells. Clin Exp Immunol 140:417–426. https://doi.org/10.1111/j.1365-2249.2005.02790.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Lim H-W, Lee Y, Huang Y-H, Yoon J-Y, Lee SH, Kim K, Lim C-J (2017) Enhancement of skin antioxidant and anti-inflammatory potentials of Agastache rugosa leaf extract by probiotic bacterial fermentation in human epidermal keratinocytes. Microbiol Biotechnol Lett 45:35–42. https://doi.org/10.4014/mbl.1701.01002

    Article  CAS  Google Scholar 

  47. Ansary TM, Hossain MR, Kamiya K, Komine M, Ohtsuki M (2021) Inflammatory molecules associated with ultraviolet radiation-mediated skin aging. Int J Mol Sci 22:3974. https://doi.org/10.3390/ijms22083974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Kim HS, Jeong SG, Ham JS, Chae HS, Lee JM, Ahn CN (2006) Antioxidative and probiotic properties of Lactobacillus gasseri NLRI-312 isolated from Korean infant feces. Asian-Australas J Anim Sci 19:1335–1341. https://doi.org/10.5713/ajas.2006.1335

    Article  CAS  Google Scholar 

  49. Mishra V, Shah C, Mokashe N, Chavan R, Yadav H, Prajapati J (2015) Probiotics as potential antioxidants: a systematic review. J Agric Food Chem 63:3615–3626. https://doi.org/10.1021/jf506326t

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was financially supported by grants funded by the Ministry of Education of the Republic of Korea and the National Research Foundation of Korea (2021R1A6A3A01086566) and Korea University Grant.

Funding

This work was financially supported by grants funded by the by the Ministry of Education of the Republic of Korea and the National Research Foundation of Korea (2021R1A6A3A01086566) and Korea University Grant.

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  1. Min Jae Shin and Chul Sang Lee have equally contributed to the work. They were both listed as first authors.

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  1. College of Life Sciences and Biotechnology, Korea University, Seoul, 02841, Republic of Korea

    Min Jae Shin, Chul Sang Lee & Sae Hun Kim

  2. Institute of Life Science and Natural Resources, Korea University, Seoul, 02841, Republic of Korea

    Chul Sang Lee & Sae Hun Kim

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Min Jae Shin and Chul Sang Lee wrote the main manuscript text. Min Jae Shin and Chul Sang Lee has the equal contribution as co first authors. Chul Sang Lee and Sae Hun Kim has the equal contribution as co corresponding authors.

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Correspondence to Chul Sang Lee or Sae Hun Kim.

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Shin, M.J., Lee, C.S. & Kim, S.H. Screening for Lactic Acid Bacterial Strains as Probiotics Exhibiting Anti-inflammatory and Antioxidative Characteristic Via Immune Modulation in HaCaT Cell. Probiotics & Antimicro. Prot. 15, 1665–1680 (2023). https://doi.org/10.1007/s12602-023-10048-8

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