Protective effect of Bifidobacterium animalis CGMCC25262 on HaCaT keratinocytes.

Publisher: Springer Nature Country of Publication: Switzerland NLM ID: 9816585 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1618-1905 (Electronic) Linking ISSN: 11396709 NLM ISO Abbreviation: Int Microbiol Subsets: MEDLINE

Publication: 2018- : Switzerland AG : Springer Nature
Original Publication: Barcelona, Spain : Springer, c1998-

Keratinocytes*/metabolism ; Keratinocytes*/microbiology ; Filaggrin Proteins* ; HaCaT Cells* ; Bifidobacterium animalis*/physiology; Humans ; Cytokines/metabolism ; Probiotics/pharmacology ; Tumor Necrosis Factor-alpha/metabolism ; Hyaluronan Synthases/metabolism ; Hyaluronan Synthases/genetics ; Interferon-gamma/metabolism ; Cell Line ; Skin/microbiology ; Aquaporin 3/metabolism ; Aquaporin 3/genetics ; Intermediate Filament Proteins/metabolism ; Intermediate Filament Proteins/genetics

Bifidobacteria are the most prevalent members of the intestinal microbiota in mammals and other animals, and they play a significant role in promoting gut health through their probiotic effects. Recently, the potential applications of Bifidobacteria have been extended to skin health. However, the beneficial mechanism of Bifidobacteria on the skin barrier remains unclear. In this study, keratinocyte HaCaT cells were used as models to evaluate the protective effects of the cell-free supernatant (CFS), heat-inactivated bacteria, and bacterial lysate of Bifidobacterium animalis CGMCC25262 on the skin barrier and inflammatory cytokines. The results showed that all the tested samples were able to upregulate the transcription levels of biomarker genes associated with the skin barrier, such as hyaluronic acid synthetase (HAS) and aquaporins (AQPs). Notably, the transcription of the hyaluronic acid synthetase gene-2 (HAS-2) is upregulated by 3~4 times, and AQP3 increased by 2.5 times when the keratinocyte HaCaT cells were co-incubated with 0.8 to 1% CFS. In particular, the expression level of Filaggrin (FLG) in HaCaT cells increased by 1.7 to 2.7 times when incubated with Bifidobacterial samples, reaching its peak at a concentration of 0.8% CFS. Moreover, B. animalis CGMCC25262 also decreased the expression of the proinflammatory cytokine RANTES to one-tenth compared to the levels observed in HaCaT cells induced with tumor necrosis factor alpha (TNF-α) and interferon gamma (IFN-γ). These results demonstrate the potential of B. animalis CGMCC25262 in protecting the skin barrier and reducing inflammatory response.
(© 2024. The Author(s), under exclusive licence to Springer Nature Switzerland AG.)

Abir-Awan M, Kitchen P et al (2019) Inhibitors of mammalian aquapor in water channels. Int J Mol Sci 20(7):22. https://doi.org/10.3390/ijms20071589. (PMID: 10.3390/ijms20071589)
Amaretti A, di Nunzio M et al (2013) Antioxidant properties of potentially probiotic bacteria: in vitro and in vivo activities. Appl Microbiol Biotechnol 97(2). https://doi.org/10.1007/s00253-012-4241-7.
Andrew WB, Richard LG (2011) The coordinated response of the physical and antimicrobial peptide barriers of the skin. J Invest Dermatol 131(2). https://doi.org/10.1038/jid.2010.360.
Arck P, Handjiski B et al (2010) Is there a 'gut-brain-skin axis'? Exp Dermatol 19(5). https://doi.org/10.1111/j.1600-0625.2009.01060.x.
Bieber T (2022) Atopic dermatitis: an expanding therapeutic pipeline for a complex disease. Nat Rev Drug Discov 21(1):20. https://doi.org/10.1038/s41573-021-00266-6. (PMID: 10.1038/s41573-021-00266-6)
Boada A, Bielsa I et al (2010) Perniosis: clinical and histopathological analysis. Am J Dermatopathol 32(1). https://doi.org/10.1097/DAD.0b013e3181af1d24.
Boguniewicz M, Schmid-Grendelmeier P et al (2006) Atopic dermatitis. J Allergy Clin Immunol 118(1):4. https://doi.org/10.1016/j.jaci.2005.10.018. (PMID: 10.1016/j.jaci.2005.10.018)
Cushing CA, Phillips LG (2013) Evidence-based medicine: pressure sores. Plast Reconstr Surg 132(6). https://doi.org/10.1097/PRS.0b013e3182a808ba.
Dainichi T, Hanakawa S et al (2014) Classification of inflammatory skin diseases: a proposal based on the disorders of the three-layered defense systems, barrier, innate immunity and acquired immunity. J Dermatol Sci 76(2):81–89. https://doi.org/10.1016/j.jdermsci.2014.08.010. (PMID: 10.1016/j.jdermsci.2014.08.01025242498)
De Rodas BZ, Gilliland SE et al (1996) Hypocholesterolemic action of Lactobacillus acidophilus ATCC 43121 and calcium in swine with hypercholesterolemia induced by diet. J Dairy Sci 79(12). https://doi.org/10.3390/foods11091283.
Deguchi Y, Morishita T et al (1985) Comparative studies on synthesis of water-soluble vitamins among human species of Bifidobacteria. Agric Biol Chem 49(1):13–19. https://doi.org/10.1080/00021369.1985.10866683. (PMID: 10.1080/00021369.1985.10866683)
Duarte M, Oliveira AL et al (2022) Current postbiotics in the cosmetic market-an update and development opportunities. Appl Microbiol Biotechnol 106(18):5879–5891. https://doi.org/10.1007/s00253-022-12116-5. (PMID: 10.1007/s00253-022-12116-536008565)
Fijan S (2014) Microorganisms with claimed probiotic properties: an overview of recent literature. Int J Environ Res Public Health 11(5):4745–4767. https://doi.org/10.3390/ijerph110504745. (PMID: 10.3390/ijerph110504745248597494053917)
Gabriela O, Jesse CL et al (2014) The effects of heat on skin barrier function and in vivo dermal absorption. Int J Pharm 464(1-2). https://doi.org/10.1016/j.ijpharm.2014.01.012.
Gao H, Yang B et al (2020) Characteristics of bifidobacterial conjugated fatty acid and hydroxy fatty acid production and its potential application in fermented milk. LWT- Food Sci Technol 120. https://doi.org/10.1016/j.lwt.2019.108940.
Gewiss C, Augustin M (2023) Recent insights into comorbidities in atopic dermatitis. Expert Rev Clin Immunol 19(4):12. https://doi.org/10.1080/1744666X.2023.2181790. (PMID: 10.1080/1744666X.2023.2181790)
Goderska K (2019) The antioxidant and prebiotic properties of lactobionic acid. Appl Microbiol Biotechnol 103(9). https://doi.org/10.1007/s00253-019-09754-7.
Gomes C, Silva AC et al (2020) Biotechnology applied to cosmetics and aesthetic medicines. Cosmetics 7(2). https://doi.org/10.3390/cosmetics7020033.
Gueniche A, Bastien P et al (2010) Bifidobacterium longum lysate, a new ingredient for reactive skin. Exp Dermatol 19(8):E1–E8. https://doi.org/10.1111/j.1600-0625.2009.00932.x. (PMID: 10.1111/j.1600-0625.2009.00932.x19624730)
Gueniche A, Perin O et al (2022) Advances in microbiome-derived solutions and methodologies are founding a new era in skin health and care. Pathogens 11(2):121. https://doi.org/10.3390/pathogens11020121. (PMID: 10.3390/pathogens11020121352150658879973)
Hermo L, Smith CE (2011) Thirsty business: cell, region, and membrane specificity of aquaporins in the testis, efferent ducts, and epididymis and factors regulating their expression. J Androl 32(6):565–575. https://doi.org/10.2164/jandrol.110.012831. (PMID: 10.2164/jandrol.110.01283121441426)
Hong K, Jeong M et al (2015) Photoprotective effects of galacto-oligosaccharide and/or Bifidobacterium longum supplementation against skin damage induced by ultraviolet irradiation in hairless mice. Int J Food Sci Nutr 66(8):923–930. https://doi.org/10.3109/09637486.2015.1088823. (PMID: 10.3109/09637486.2015.108882326470918)
Hong YK, An S et al (2022) Potential anti-ageing effects of probiotic-derived conditioned media on human skin cells. Acta Pharm 72(3):359–374. https://doi.org/10.2478/acph-2022-0027. (PMID: 10.2478/acph-2022-002736651546)
Kakehi K, Kinoshita M et al (2003) Hyaluronic acid: separation and biological implications. J Chromatogr B Anal Technol Biomed Life Sci 797(1-2):347–355. https://doi.org/10.1016/S1570-0232(03)00479-3. (PMID: 10.1016/S1570-0232(03)00479-3)
Kalliomaki M, Salminen S et al (2003) Probiotics and prevention of atopic disease: 4-year follow-up of a randomised placebo-controlled trial. Lancet 361(9372):1869–1871. https://doi.org/10.1016/S0140-6736(03)13490-3. (PMID: 10.1016/S0140-6736(03)13490-312788576)
Karampoor M, Fouladpour A et al (2022) Probiotics as a promising treatment approach to burn wound healing. Burns 48(8). https://doi.org/10.1016/j.burns.2022.07.003.
Kemgang TS, Kapila S et al (2014) Cross-talk between probiotic lactobacilli and host immune system. J Appl Microbiol 117(2):303–319. https://doi.org/10.1093/jn/137.3.781S. (PMID: 10.1093/jn/137.3.781S24738909)
Kenji K, Shunsuke S et al (2020) Vulnerability of the skin barrier to mechanical rubbing. Int J Pharm 587. https://doi.org/10.1016/j.ijpharm.2020.119708.
Khmaladze I, Butler E et al (2019) Lactobacillus reuteri DSM 17938 - a comparative study on the effect of probiotics and lysates on human skin. Exp Dermatol 28(7):822–828. https://doi.org/10.1111/exd.13950. (PMID: 10.1111/exd.1395031021014)
Kim MY, Lim YY et al (2015) Synergistic inhibition of tumor necrosis factor-alpha-stimulated pro-inflammatory cytokine expression in HaCaT cells by a combination of rapamycin and mycophenolic acid. Ann Dermatol 27(1):32–39. https://doi.org/10.5021/ad.2015.27.1.32. (PMID: 10.5021/ad.2015.27.1.32256739294323600)
Kobayashi T, Chanmee T et al (2020) Hyaluronan: metabolism and function. Biomolecules 10(11). https://doi.org/10.3390/biom10111525.
Lee H, Kim M (2022) Skin barrier function and the microbiome. Int J Mol Sci 23(21). https://doi.org/10.3390/ijms232113071.
Lidbeck A, Nord CE (1991) Lactobacilli in relation to human-ecology and antimicrobial therapy. Int J Tissue React 13(2):115–122. (PMID: 1955293)
Ma X, Pan Y et al (2022) Bifidobacteriumi nfantis strain YLGB-1496 possesses excellent antioxidant and skinbarrier-enhancing efficacy in vitro. Exp Dermatol 31(7):6. https://doi.org/10.1111/exd.14583. (PMID: 10.1111/exd.14583)
Magdalena B, Ewa D et al (2016) Structural and biophysical characteristics of human skin in maintaining proper epidermal barrier function. Adv Dermatol Allergol 33(1). https://doi.org/10.5114/pdia.2015.48037.
Mohtashami M, Mohamadi M et al (2020) Lactobacillus bulgaricus and Lactobacillus plantarum improve diabetic wound healing through modulating inflammatory factors. Biotechnol Appl Biochem 68(6). https://doi.org/10.1002/bab.2064.
Moysidis M, Stavrou G et al (2022) The 3-D configuration of excisional skin wound healing after topical probiotic application. Injury 53(4). https://doi.org/10.1016/j.injury.2022.02.006.
O'Callaghan A, van Sinderen D (2016) Bifidobacteria and their role as members of the human gut microbiota. Front Microbiol 7. https://doi.org/10.3389/fmicb.2016.00925.
O'Neil DA (2003) Regulation of expression of beta-defensins: endogenous enteric peptide antibiotics. Mol Immunol 40(7):445–450. https://doi.org/10.1016/S0161-5890(03)00161-5. (PMID: 10.1016/S0161-5890(03)00161-514568390)
Pandey KR, Naik SR et al (2015) Probiotics, prebiotics and synbiotics- a review. J Food Sci Technol 52(12):7577–7587. https://doi.org/10.1007/s13197-015-1921-1. (PMID: 10.1007/s13197-015-1921-1266043354648921)
Park MS, Kim JI et al (2018) Towards the application of human defensins as antivirals. Biomol Ther 26(3):13. https://doi.org/10.4062/biomolther.2017.172. (PMID: 10.4062/biomolther.2017.172)
PueblaBarragan S, Reid G (2021) Probiotics in cosmetic and personal care products: trends and challenges. Molecules 26(5). https://doi.org/10.3390/molecules26051249.
Rawal S, Ali SA (2023) Probiotics and postbiotics play a role in maintaining dermal health. Food Funct 14(9):3966–3981. https://doi.org/10.1039/D3FO00152K. (PMID: 10.1039/D3FO00152K37051640)
Ren D, Li C et al (2015) Evaluation of immunomodulatory activity of two potential probiotic Lactobacillus strains by in vivo tests. Anaerobe 35:22–27. https://doi.org/10.1016/j.anaerobe.2015.06.008. (PMID: 10.1016/j.anaerobe.2015.06.00826143437)
Rossi M, Amaretti A et al (2011) Folate production by probiotic bacteria. Nutrients 3(1):118–134. https://doi.org/10.3390/nu3010118. (PMID: 10.3390/nu3010118222540783257725)
Sen A, Nishimura T et al (2023) Comprehensive analysis of metabolites produced by co-cultivation of Bifidobacterium breve MCC1274 with human iPS-derived intestinal epithelial cells. Front Microbiol 14. https://doi.org/10.3389/fmicb.2023.1155438.
Siiskonen H, Oikari S et al (2015) Hyaluronansynthase1: a mysterious enzyme with unexpected functions. Front Immunol 6:11. https://doi.org/10.3389/fimmu.2015.00043. (PMID: 10.3389/fimmu.2015.00043)
Skandalis SS, Karalis T et al (2020) Intracellular hyaluronan: importance for cellular functions. Semin Cancer Biol 62:20–30. https://doi.org/10.1016/j.semcancer.2019.07.002. (PMID: 10.1016/j.semcancer.2019.07.00231276783)
Solopova A, Bottacini F et al (2020) Riboflavin biosynthesis and overproduction by a derivative of the human gut commensal Bifidobacterium longum subsp. infantis ATCC 15697. Front Microbiol 11:573335. https://doi.org/10.3389/fmicb.2020.573335. (PMID: 10.3389/fmicb.2020.573335330420837522473)
Spicer AP, Nguyen TK (1999) Mammalian hyaluronan synthases: investigation of functional relationships in vivo. Biochem Soc Trans 27(2):7. https://doi.org/10.1042/bst0270109. (PMID: 10.1042/bst0270109)
Sroka-Tomaszewska J, Trzeciak M (2021) Molecular mechanisms of atopic dermatitis pathogenesis. Int J Mol Sci 22(8). https://doi.org/10.3390/ijms22084130.
Suez J, Zmora N et al (2019) The pros, cons, and many unknowns of probiotics. Nat Med 25(5):716–729. https://doi.org/10.1038/s41591-019-0439-x. (PMID: 10.1038/s41591-019-0439-x31061539)
Takata K, Matsuzaki T et al (2004) Aquaporins: water channel proteins of the cellmembrane. Prog Histochem Cytochem 39(1):83. https://doi.org/10.1016/j.proghi.2004.03.001. (PMID: 10.1016/j.proghi.2004.03.001)
Thorakkattu P, Khanashyam AC et al (2022) Postbiotics: current trends in food and pharmaceutical industry. Foods 11(19). https://doi.org/10.3390/foods11193094.
Tsai W, Chou C et al (2021) Regulatory effects of Lactobacillus plantarum-GMNL6 on human skin health by improving skin microbiome. Int J Med Sci 18(5). https://doi.org/10.7150/ijms.51545.
Vale ADS, de Melo Pereira GV et al (2023) Production, formulation, and application of postbiotics in the treatment of skin conditions. Fermentation 9(3). https://doi.org/10.3390/fermentation9030264.
Vasiliki L, Mihalis IP (2019) Functional role of probiotics and prebiotics on skin health and disease. Fermentation 5(2). https://doi.org/10.3390/fermentation5020041.
Wang F, Feng XC et al (2006) Aquaporins as potential drug targets. Acta Pharmacol Sin 27(4):395–401. https://doi.org/10.1111/j.1745-7254.2006.00318.x. (PMID: 10.1111/j.1745-7254.2006.00318.x16539837)
Wegh CAM, Geerlings SY et al (2019) Postbiotics and their potential applications in early life nutrition and beyond. Int J Mol Sci 20(19). https://doi.org/10.3390/ijms20194673.
Wei Q, Chen T et al (2007) Using of lactobacillus and Bifidobacterium to product the isoflavone aglycones in fermented soymilk. Int J Food Microbiol 117(1):120–124. https://doi.org/10.1016/j.ijfoodmicro.2007.02.024. (PMID: 10.1016/j.ijfoodmicro.2007.02.02417477997)
Weigel PH (2002) Functional characteristics and catalytic mechanisms of the bacterial hyaluronan synthases. IUBMB Life 54(4):201–211. https://doi.org/10.1080/15216540214931. (PMID: 10.1080/1521654021493112512859)
Yano C, Saeki H et al (2015) Mechanism of macrophage-derived chemokine/CCL22 production by HaCaT keratinocytes. Ann Dermatol 27(2):152–156. https://doi.org/10.5021/ad.2015.27.2.152. (PMID: 10.5021/ad.2015.27.2.152258343534377403)
Yu J, Ma X et al (2022) Application and mechanism of probiotics in skin care: a review. J Cosmet Dermatol 21(3). https://doi.org/10.1111/jocd.14734.
Zapaśnik A, Sokołowska B et al (2022) Role of lactic acid bacteria in food preservation and safety. Foods 11(9). https://doi.org/10.3390/foods11091283.
Zhang Y, Hou Y et al (2023) Bifidobacterium animalis A12, a probiotic strain that promotes glucose and lipid metabolism, improved the texture and aroma of the fermented sausage. Foods 12(2). https://doi.org/10.3390/foods12020336.
Zhao L, Wang S et al (2021) Identification, characterization, and antioxidant potential of Bifidobacterium longum subsp. longum strains isolated from feces of healthy infants. Front Microbiol 12. https://doi.org/10.3389/fmicb.2021.756519.

Keywords: Bifidobacterium animalis; Cosmetic material; Keratinocyte HaCaT; Probiotic role; Skin barrier

0 (Filaggrin Proteins)
0 (FLG protein, human)
0 (Cytokines)
0 (Tumor Necrosis Factor-alpha)
EC 2.4.1.212 (Hyaluronan Synthases)
82115-62-6 (Interferon-gamma)
158801-98-0 (Aquaporin 3)
0 (Intermediate Filament Proteins)
0 (AQP3 protein, human)

Date Created: 20240126 Date Completed: 20241004 Latest Revision: 20241004

20241004

10.1007/s10123-024-00485-y

38278974