The Potential of Lactobacillus spp. Fermented Plant Extract in Modulating Collagen and MMPs in Photoaging Skin : A Review

Frisilia Tifanygrasiela; Bantari Wisynu Kusuma Wardhani; Donny Lukmanto; Meidi Utami Puteri

doi:10.35814/jifi.v24i2.2186

Penulis

Frisilia Tifanygrasiela Faculty of Pharmacy, Universitas Indonesia, Kota Depok 16424, Indonesia
Bantari Wisynu Kusuma Wardhani Research Center for Pharmaceutical Ingredients and Traditional Medicine, BRIN, South Tangerang 15314, Indonesia
Donny Lukmanto Laboratory of Regenerative Medicine & Stem Cell Biology, Institute of Medicine, University of Tsukuba, Ibaraki, Japan
Meidi Utami Puteri Laboratory of Pharmacology and Toxicology, Faculty of Pharmacy, Universitas Indonesia, Kota Depok 16424, Indonesia

DOI:

https://doi.org/10.35814/jifi.v24i2.2186

Kata Kunci:

Lactobacillus spp., fermented plant extract, collagen restoration, photoaging, matrix metalloproteinases

Abstrak

Photoaging poses a challenge to skin health, marked by collagen degradation and heightened matrix metalloproteinases (MMPs) activity. This review summarizes the role of Lactobacillus spp. fermented plant extracts in restoring collagen levels, modulating MMP activity in photoaging skin and presents current research explaining the processes by which Lactobacillus spp. fermentation contributes to rejuvenate the skin and explores possible uses in skincare products. Recent evidence suggests that these fermented extracts possess potent antioxidant properties, that counteract oxidative stress (a key factor in photoaging). The fermentation process can modify the structural characteristics of compounds, enhance the bioavailability of beneficial compounds, such as phenolics and flavonoids, which are known for their protective effects on the skin. These fermented extracts can help maintain skin structure and support collagen synthesis by activating the Nrf-2-Keap1 pathway through phenolic acids (for example, salidroside) and inhibiting the activation of MAPK and NF-kB by flavonoids and Dendrobium officinale polysaccharides, thereby reducing visible signs of aging. In summary, Lactobacillus spp. fermented plant extracts show potential in restoring collagen levels, particularly Type I and Type III collagen, modulating MMPs, including MMP-1, MMP-2, MMP-3, and MMP-9, in photoaging skin. Several clinical trials further support their efficacy and practical use in antiaging products. These findings underscore the promise of using natural fermented extracts as effective strategies for mitigating photoaging and promoting healthier skin. Future research should optimize formulations and concentrations, examine interactions with other bioactives, and establish long-term safety and mechanisms in developing targeted treatments for photoaging.

Referensi

[1] Y. Zhang et al., “Effects of Lactobacillus kefiri fermentation supernatant on skin aging caused by oxidative stress,” J. Funct. Foods, vol. 96, p. 105222, 2022, doi: 10.1016/j.jff.2022.105222.

[2] H.-R. Kim et al., “Fermentation of Blackberry with L. plantarum JBMI F5 Enhance the Protection Effect on UVB-Mediated Photoaging in Human Foreskin Fibroblast and Hairless Mice through Regulation of MAPK/NF-κB Signaling,” Nutrients, vol. 11, no. 10, p. 2429, 2019, doi: 10.3390/nu11102429.

[3] L. Marracino et al., “Fermentation of Vaccinium floribundum Berries with Lactiplantibacillus plantarum Reduces Oxidative Stress in Endothelial Cells and Modulates Macrophages Function,” Nutrients, vol. 14, no. 8, p. 1560, 2022, doi: 10.3390/nu14081560.

[4] T. Teame et al., “Paraprobiotics and Postbiotics of Probiotic Lactobacilli, Their Positive Effects on the Host and Action Mechanisms: A Review,” Front. Nutr., vol. 7, 2020, doi: 10.3389/fnut.2020.570344.

[5] J. S. Ong et al., “Lactobacillus plantarum USM8613 Aids in Wound Healing and Suppresses Staphylococcus aureus Infection at Wound Sites,” Probiotics Antimicrob. Proteins, vol. 12, no. 1, pp. 125–137, 2019, doi: 10.1007/s12602-018-9505-9.

[6] E. Alves, J. Gregório, P. Rijo, C. Rosado, and L. M. Rodrigues, “The Impact of Kefir on Epidermal Water Homeostasis in Healthy Human Skin,”. Life, vol. 12, no. 7, p. 1075, 2022, doi: 10.3390/life12071075.

[7] H. Kimoto-Nira, “New lactic acid bacteria for skin health via oral intake of heat-killed or live cells,” Animal Science Journal, vol. 89, no. 6, pp. 835–842, 2018, doi: 10.1111/asj.13017.

[8] D. Bouilly-Gauthier et al., “Clinical evidence of benefits of a dietary supplement containing probiotic and carotenoids on ultraviolet-induced skin damage,” British Journal of Dermatology, vol. 163, no. 3, pp. 536–543, 2010, doi: 10.1111/j.1365-2133.2010.09888.x.

[9] H. M. Kim et al., “Oral administration of Lactobacillus plantarum HY7714 protects hairless mouse against ultraviolet B-induced photoaging,” J. Microbiol. Biotechnol., vol. 24, no. 11, pp. 1583–1591, 2014, doi: 10.4014/jmb.1406.06038.

[10] N. Elazab, A. Mendy, J. Gasana, E. R. Vieira, A. Quizon, and E. Forno, “Probiotic Administration in Early Life, Atopy, and Asthma: A Meta-analysis of Clinical Trials,” Pediatrics, vol. 132, no. 3, pp. e666–e676, 2013, doi: 10.1542/peds.2013-0246.

[11] X. Hu, M. Chen, J. Nawaz, and X. Duan, “Regulatory Mechanisms of Natural Active Ingredients and Compounds on Keratinocytes and Fibroblasts in Mitigating Skin Photoaging,” Clin. Cosmet. Investig. Dermatol., vol. Volume 17, pp. 1943–1962, 2024, doi: 10.2147/ccid.s478666.

[12] A. Pourang et al., “Effects of visible light on mechanisms of skin photoaging,” Photodermatol. Photoimmunol. Photomed., vol. 38, no. 3, pp. 191–196, 2022, doi: 10.1111/phpp.12736.

[13] B. Yilmaz et al., “The Impacts of Lactiplantibacillus plantarum on the Functional Properties of Fermented Foods: A Review of Current Knowledge,” Microorganisms, vol. 10, no. 4, p. 826, 2022, doi: 10.3390/microorganisms10040826.

[14] P. Zhang et al., “Physicochemical properties, antioxidant and cardioprotective activities of polysaccharides from fermented Polygonatum kingianum with Lactobacillus species,” Ind. Crops Prod., vol. 216, p. 118699, 2024, doi: 10.1016/j.indcrop.2024.118699.

[15] N. D. K. Akpabli-Tsigbe et al., “Novel solid-state fermentation extraction of 5-O-caffeoylquinic acid from heilong48 soybean using Lactobacillus helviticus: Parametric screening and optimization,” LWT, vol. 149, p. 111809, 2021, doi: 10.1016/j.lwt.2021.111809.

[16] R. Modi and P. P. Sahota, “Bio-process optimization for developing a Turmeric (Curcuma longa Linn.) beverage fermented with functional lactic acid starter cultures,” Biocatal. Agric. Biotechnol., vol. 61, p. 103360, 2024, doi: 10.1016/j.bcab.2024.103360.

[17] A. S. Isas et al., “Fermented pomegranate juice enriched with pomegranate seed oil ameliorates metabolic disorders associated with a high-fat diet in C57BL/6 mice,” Food Chem., vol. 463, p. 141434, 2024, doi: 10.1016/j.foodchem.2024.141434.

[18] Y. Tan et al., “Functional components and antioxidant activity were improved in ginger fermented by Bifidobacterium adolescentis and Monascus purpureus,” Lebensmittel-Wissenschaft + Technologie/Food science & technology, vol. 197, p. 115931, 2024, doi: 10.1016/j.lwt.2024.115931.

[19] H.-B. Jiang et al., “The polyphenols profile of co-fermented quinoa and black barley with Lactobacillus kisonensis and its in vitro bioactivities,” Food Biosci., vol. 58, p. 103712, 2024, doi: 10.1016/j.fbio.2024.103712.

[20] L. Yuna, Y. Bo-Gyeong, C. Fengjia, B. Eui-Baek, and S. Ha-Yeon, “Fermented Codonopsis lanceolata root extract exhibits anti-viral effects against influenza A infection by inhibiting neuraminidase activity and inflammatory responses,” Food Biosci., vol. 61, p. 104617, 2024, doi: 10.1016/j.fbio.2024.104617.

[21] Y. Song et al., “Effect of Lacticaseibacillus rhamnosus L08 fermentation on xanthine oxidase inhibitory activity and flavour profile of honeysuckle (Lonicera japonica thunb.),” LWT, vol. 200, p. 116196, 2024, doi: 10.1016/j.lwt.2024.116196.

[22] R. Zhang et al., “Metabolite profiling, antioxidant and anti-glycemic activities of Tartary buckwheat processed by solid-state fermentation(SSF)with Ganoderma lucidum,” Food Chem. X, vol. 22, Jun. 2024, doi: 10.1016/j.fochx.2024.101376.

[23] S. Plessas, I. Mantzourani, A. Terpou, and A. Bekatorou, “Assessment of the Physicochemical, Antioxidant, Microbial, and Sensory Attributes of Yogurt-Style Products Enriched with Probiotic-Fermented Aronia melanocarpa Berry Juice,” Foods, vol. 13, no. 1, p. 111, 2024, doi: 10.3390/foods13010111.

[24] E. J. Brown, H. Khodr, C. R. Hider, and C. Rice-Evans, “Structural dependence of flavonoid interactions with Cu2+ ions: implications for their antioxidant properties,” Biochemical Journal, vol. 330, no. 3, pp. 1173–1178, 1998, doi: 10.1042/bj3301173.

[25] C. M. C. Andrés, J. M. Pérez de la Lastra, C. A. Juan, F. J. Plou, and E. Pérez-Lebeña, “Polyphenols as Antioxidant/Pro-Oxidant Compounds and Donors of Reducing Species: Relationship with Human Antioxidant Metabolism,” Processes, vol. 11, no. 9, p. 2771, 2023, doi: 10.3390/pr11092771.

[26] C. M. C. Andrés, J. M. Pérez de la Lastra, C. A. Juan, F. J. Plou, and E. Pérez-Lebeña, “Chemistry of Hydrogen Peroxide Formation and Elimination in Mammalian Cells, and Its Role in Various Pathologies,” Stresses, vol. 2, no. 3, pp. 256–274, 2022, doi: 10.3390/stresses2030019.

[27] A. Kaltsa, D. Papaliaga, E. Papaioannou, and P. Kotzekidou, “Characteristics of oleuropeinolytic strains of Lactobacillus plantarum group and influence on phenolic compounds in table olives elaborated under reduced salt conditions,” Food Microbiol., vol. 48, pp. 58–62, 2015, doi: 10.1016/j.fm.2014.10.016.

[28] L. G. Ruiz Rodríguez, V. M. Zamora Gasga, M. Pescuma, C. Van Nieuwenhove, F. Mozzi, and J. A. Sánchez Burgos, “Fruits and fruit by-products as sources of bioactive compounds. Benefits and trends of lactic acid fermentation in the development of novel fruit-based functional beverages,” Food Research International, vol. 140, p. 109854, 2021, doi: 10.1016/j.foodres.2020.109854.

[29] W. Fei, M. Noda, N. Danshiitsoodol, and M. Sugiyama, “Dendrobium officinale Extract Fermented with Lactobacillus plantarum GT-17F Enhances the Protection of UV-Mediated Photoaging,” Biol. Pharm. Bull., vol. 46, no. 10, pp. b23-00373, Oct. 2023, doi: 10.1248/bpb.b23-00373.

[30] Y. Mai, Z. Niu, W. He, X.-P. Lai, S. Huang, and X. Zheng, “The Reparative Effect of Dendrobium officinale Protocorms against Photodamage Caused by UV-Irradiation in Hairless Mice,” J-STAGE, vol. 42, no. 5, pp. 728–735, 2019, doi: 10.1248/bpb.b18-00901.

[31] M. Li et al., “Transformation of mulberry polyphenols by Lactobacillus plantarum SC-5: Increasing phenolic acids and enhancement of anti-aging effect,” Food Research International, vol. 192, p. 114778, 2024, doi: 10.1016/j.foodres.2024.114778.

[32] H. Fu et al., “Anti-Photoaging Effect of Rhodiola rosea Fermented by Lactobacillus plantarum on UVA-Damaged Fibroblasts,” Nutrients, vol. 14, no. 11, p. 2324, 2022, doi: 10.3390/nu14112324.

[33] L. Chan, Y. Tseng, C. Liu, and C. Liang, “Fermented pomegranate extracts protect against oxidative stress and aging of skin,” J. Cosmet. Dermatol., vol. 21, no. 5, pp. 2236–2245, 2021, doi: 10.1111/jocd.14379.

[34] M. N. Islam et al., “Superoxide dismutase: an updated review on its health benefits and industrial applications,” Crit. Rev. Food Sci. Nutr., vol. 62, no. 26, pp. 1–19, 2021, doi: 10.1080/10408398.2021.1913400.

[35] C. Glorieux and P. B. Calderon, “Catalase, a remarkable enzyme: targeting the oldest antioxidant enzyme to find a new cancer treatment approach,” Biol. Chem., vol. 398, no. 10, pp. 1095–1108, 2017, doi: 10.1515/hsz-2017-0131.

[36] T. Liu, L. Sun, Y. Zhang, Y. Wang, and J. Zheng, “Imbalanced GSH/ROS and sequential cell death,” J. Biochem. Mol. Toxicol., vol. 36, no. 1, 2021, doi: 10.1002/jbt.22942.

[37] R. Ji, F. Jia, X. Chen, Z. Wang, W. Jin, and J. Yang, “Salidroside alleviates oxidative stress and apoptosis via AMPK/Nrf2 pathway in DHT-induced human granulosa cell line KGN,” Arch. Biochem. Biophys., vol. 715, p. 109094, 2022, doi: 10.1016/j.abb.2021.109094.

[38] T. Suzuki and M. Yamamoto, “Molecular basis of the Keap1–Nrf2 system,” Free Radic. Biol. Med., vol. 88, pp. 93–100, 2015, doi: 10.1016/j.freeradbiomed.2015.06.006.

[39] T. Suzuki and M. Yamamoto, “Stress-sensing mechanisms and the physiological roles of the Keap1–Nrf2 system during cellular stress,” Journal of Biological Chemistry, vol. 292, no. 41, pp. 16817–16824, 2017, doi: 10.1074/jbc.r117.800169.

[40] P. Canning, F. J. Sorrell, and A. N. Bullock, “Structural basis of Keap1 interactions with Nrf2,” Free Radic. Biol. Med., vol. 88, pp. 101–107, 2015, doi: 10.1016/j.freeradbiomed.2015.05.034.

[41] Q. Luo et al., “Chemical properties and antioxidant activity of a water-soluble polysaccharide from Dendrobium officinale,” Int. J. Biol. Macromol., vol. 89, pp. 219–227, 2016, doi: 10.1016/j.ijbiomac.2016.04.067.

[42] S. Xing, X. Zhang, H. Ke, J. Lin, Y. Huang, and G. Wei, “Physicochemical properties of polysaccharides from Dendrobium officinale by fractional precipitation and their preliminary antioxidant and anti-HepG2 cells activities in vitro,” Chem. Cent. J., vol. 12, no. 1, 2018, doi: 10.1186/s13065-018-0468-4.

[43] L.-H. Pan et al., “Comparison of hypoglycemic and antioxidative effects of polysaccharides from four different Dendrobium species,” Int. J. Biol. Macromol., vol. 64, pp. 420–427, 2014, doi: 10.1016/j.ijbiomac.2013.12.024.

[44] H. Lim and H. Kim, “Inhibition of Mammalian Collagenase, Matrix Metalloproteinase-1, by Naturally-Occurring Flavonoids,” Planta Med., vol. 73, no. 12, pp. 1267–1274, 2007, doi: 10.1055/s-2007-990220.

[45] X. Wu and A. G. Schauss, “Mitigation of Inflammation with Foods,” J. Agric. Food Chem., vol. 60, no. 27, pp. 6703–6717, 2012, doi: 10.1021/jf3007008.

[46] R. Zhong et al., “Anti-inflammatory activity of flavonols via inhibiting MAPK and NF-κB signaling pathways in RAW264.7 macrophages,” Curr. Res. Food Sci., vol. 5, pp. 1176–1184, 2022, doi: 10.1016/j.crfs.2022.07.007.

[47] R. Gum, H. Wang, E. Lengyel, J. Juarez, and D. Boyd, “Regulation of 92 kDa type IV collagenase expression by the jun aminoterminal kinase- and the extracellular signal-regulated kinase-dependent signaling cascades,” Oncogene, vol. 14, no. 12, pp. 1481–1493, 1997, doi: 10.1038/sj.onc.1200973.

[48] L. Xiang et al., “Polysaccharides of Dendrobium officinale inhibit TNF-α-induced apoptosis in A-253 cell line,” Inflammation Research, vol. 62, no. 3, pp. 313–324, 2012, doi: 10.1007/s00011-012-0584-x.

[49] C. Sun, Z. Wang, Q. Zheng, and H. Zhang, “Salidroside inhibits migration and invasion of human fibrosarcoma HT1080 cells,” Phytomedicine, vol. 19, no. 3–4, pp. 355–363, 2012, doi: 10.1016/j.phymed.2011.09.070.

[50] J. Yang, H. Cho, M. Gil, and K. E. Kim, “Anti-Inflammation and Anti-Melanogenic Effects of Maca Root Extracts Fermented Using Lactobacillus Strains,” Antioxidants, vol. 12, no. 4, p. 798, Mar. 2023, doi: 10.3390/antiox12040798.

[51] X. Zhou et al., “Anti-aging effect of Lactobacillus plantarum HFY09-fermented soymilk on D-galactose-induced oxidative aging in mice through modulation of the Nrf2 signaling pathway,” J. Funct. Foods, vol. 78, p. 104386, 2021, doi: 10.1016/j.jff.2021.104386.

[52] P. Yang, Y. Chai, M. Wei, Y. Ge, and F. Xu, “Mechanism of salidroside in the treatment of endometrial cancer based on network pharmacology and molecular docking,” Sci. Rep., vol. 13, no. 1, p. 14114, 2023, doi: 10.1038/s41598-023-41157-7.

[53] R. L. Sun et al., “Screening of lactic acid bacteria against Phytophthora capsici in postharvest pepper and analysis of related characteristics,” Mod. Food Sci. Technol, vol. 38, no. 11, pp. 63–72, 2022, doi: https://doi.org/10.13982/j.mfst.1673-9078.2022.11.1433.

[54] Z. Li et al., “Lactobacillus-fermentation enhances nutritional value and improves the inhibition on pancreatic lipase and oral pathogens of edible red seaweed Bangia fusco-purpurea,” LWT, vol. 179, p. 114643, Apr. 2023, doi: 10.1016/j.lwt.2023.114643.

[55] E. Kwaw et al., “Effect of lactobacillus strains on phenolic profile, color attributes and antioxidant activities of lactic-acid-fermented mulberry juice,” Food Chem., vol. 250, pp. 148–154, Jun. 2018, doi: 10.1016/j.foodchem.2018.01.009.

[56] T. Li, T. Jiang, N. Liu, C. Wu, H. Xu, and H. Lei, “Biotransformation of phenolic profiles and improvement of antioxidant capacities in jujube juice by select lactic acid bacteria,” Food Chem., vol. 339, p. 127859, Mar. 2021, doi: 10.1016/j.foodchem.2020.127859.

[57] A. I. Martinez-Gonzalez et al., “In Vitro Inhibition of Pancreatic Lipase by Polyphenols: A Kinetic, Fluorescence Spectroscopy and Molecular Docking Study,” Food Technol. Biotechnol., vol. 55, no. 4, 2017, doi: 10.17113/ftb.55.04.17.5138.

[58] A. V. Rusu, M. Trif, and J. M. Rocha, “Microbial Secondary Metabolites via Fermentation Approaches for Dietary Supplementation Formulations,” Molecules, vol. 28, no. 16, p. 6020, 2023, doi: 10.3390/molecules28166020.

[59] C.-Y. Chen, C.-Y. Hu, Y.-H. Chen, Y.-T. Li, and Y.-C. Chung, “Submerged fermentation with Lactobacillus brevis significantly improved the physiological activities of Citrus aurantium flower extract,” Heliyon, vol. 8, no. 9, p. e10498, Sep. 2022, doi: 10.1016/j.heliyon.2022.e10498.

[60] Y.-A. Park et al., “Suppressive Effect of Fermented Angelica tenuissima Root Extract against Photoaging: Possible Involvement of Hemeoxygenase-1,” J. Microbiol. Biotechnol., vol. 28, no. 8, pp. 1391–1400, 2018, doi: 10.4014/jmb.1805.05065.

[61] W. Fei, M. Noda, N. Danshiitsoodol, and M. Sugiyama, “Skin Anti-Aging Efficacy of a Lactobacillus plantarum GT-17F Fermented Dendrobium officinale Ingredient: A Randomized, Double-Blind, Placebo-Controlled Clinical Study,” Cosmetics, vol. 11, no. 1, p. 26, 2024, doi: 10.3390/cosmetics11010026.