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. 2022 Jan 29;74(2):309–317. doi: 10.1007/s10616-022-00521-7

Lotus root extract inhibits skin damage through suppression of collagenase production in vitro

Akira Iwamoto 1,✉, Ryoko Yamauchi 2, Shigeki Oogai 2, Yumi Tsuruta 1, Tsuge Keisuke 1, Yasuo Nagata 2,3, Teruyoshi Yanagita 2,4
PMCID: PMC8975922  PMID: 35464168

Abstract

Lotus root is a traditional food ingredient used primarily in Asia and is rich in polyphenols. To determine its potential use in antiphotoaging, polyphenols were extracted from lotus root with 50% ethanol, and the activity of matrix metalloproteinase (MMP) was measured in dermal cells treated with ultraviolet A (UVA). UVA exposure increased the gene expression of IL-1α, the mRNA levels of MMP-1, and hence, the levels of MMP-1 protein in HaCaT cells, whereas cells treated with lotus polyphenol (LP) normalized these values to the control. In the presence of LP at concentrations of 1 and 10 μg/mL, both the secretion of IL-1α and protein levels of MMP-1 in human keratinocyte cells significantly reduced. Similarly, in the LabCyte EPI-MODEL24, irradiation with UVA caused an increase in mRNA expression of IL-1α and MMP-1, which was prevented by adding LP to the cells. Our results with three different skin cells accordingly showed that LP may help maintain skin health through decreased levels of MMP-1 activity via its anti-inflammatory properties.

Keywords: Lotus root, Polyphenols, Matrix metalloproteinase, Degranulation, Photoaging

Introduction

Aging is becoming a worldwide health issue. With age, chronic diseases, such as diabetes, cardiovascular disease, and dementia develop, leading to poor quality of life and financial burden. Nutritional products, such as fish oils and vitamins/minerals, are often recommended to maintain a healthy life, in addition to exercise. Skin aging is another concern, as we get older. Skin aging occurs due to a broad range of factors, including intrinsic factors, such as age and hormonal changes, and extrinsic factors, such as sunlight, pollutants, and smoking (Farage et al. 2008). Aging due to prolonged exposure to ultraviolet radiation (UV) is called photoaging (Afaq and Mukhtar 2006). UVA is able to penetrate the dermis and may be responsible for chronic skin damage. As a result, photoaging triggers skin dryness, wrinkles, and hyperpigmentation (Oriba et al. 1996). It has been suggested that photoaging promotes the production of reactive oxygen species (ROS) in the skin, increases proinflammatory cytokines, and consequently induces matrix metalloproteinase (MMP) expression and collagen degradation, resulting in skin problems, such as wrinkles (Naylor et al. 2011). Hence, the search for natural materials that are able to inhibit the production of UV-induced aging factors has been progressed, and Sambucus nigra, Sorbaria kirilowii, and cherry blossom, for example, have been studied (Lin et al. 2019; Chen et al. 2021; Wang et al. 2019).

Polyphenols are secondary metabolites found in plants that protect them from ultraviolet radiation and pathogens. Accumulating evidence suggests that polyphenols have a wide range of physiological functions as well as anti-inflammatory, antimicrobial, and antiallergic properties (Santhakumar et al. 2018). UVB exposure is known to induce ROS production and trigger inflammation in skin cells (Afaq and Mukhtar 2006). In addition, ROS leads to the upregulation of MMP, resulting in the breakdown of collagen. Decreased collagen then causes the loss of firmness to skin and eventually induces wrinkles. It has been reported that flavonoids, a dietary polyphenol group, protect the skin from UV radiation mainly via their antioxidant activities (Nichols and Katiyar 2010). For example, a previous study showed that luteolin, a strong naturally occurring antioxidant, prevented UVB-induced skin inflammation (Wölfle et al. 2011). The photoprotective effects of green tea polyphenols have also been extensively examined at the molecular level (Yusuf et al. 2007).

The lotus (Nelumbo nucifera) root is a traditional food ingredient in Asian countries. The lotus root is composed of various nutrients and is rich in vitamin C. In southeastern Asia, lotus leaves and seeds containing polyphenols, such as quercetin, have been used in folk medicine because of their antibacterial, hepatoprotective, and antioxidant activities (Manach et al. 2005). However, only a few studies have reported the types and amounts of polyphenols present in lotus root, despite their use in traditional medicine. We have previously determined the type and level of polyphenols and found that lotus root contains proanthocyanidins, including catechin and gallocatechin (Tsuruta et al. 2011), and that polyphenols derived from lotus root exerted antilipidemic activity in db/db mice (Tsuruta et al. 2012).

Because UV irradiation promotes ROS production and augments collagen degradation via activated collagenolytic MMPs, leading to skin photoaging, polyphenol-rich lotus root may exert photoprotective effects through antioxidant activity. The aim of this study is to determine whether polyphenols derived from lotus root exhibit anti-photoaging in vitro and how they affect at the molecular level.

Materials and methods

Chemicals

Dulbecco’s Modified Eagle’s Medium (DMEM) and fetal bovine serum (FBS) were purchased from Thermo Fisher Scientific (Waltham, MA, USA). PrimeScript™ RT Master Mix and TB Green Premix Ex Taq™ II were obtained from Takara Bio (Shiga, Japan). 3-(4,5-Dimethyl-2-thiazolyl)-2,5-diphenyl-2H-tetrazolium bromide (MTT) was purchased from Dojindo Molecular Technologies, Inc. (Kumamoto, Japan). Anti-human MMP-1 mouse antibodies were obtained from Santa Cruz Biotechnology (Santa Cruz, CA, USA). Anti-mouse IgG antibodies conjugated with horseradish peroxidase (HRP) were purchased from Bethyl Laboratories (Montgomery, TX, USA). Anti-human IL-1α and biotin-conjugated anti-human IL-1α were purchased from Peprotech (Cranbury, NJ, USA). HRP-conjugated streptavidin and 3,3′,5,5′-tetramethylbenzidine (TMB) for ELISA were obtained from Thermo Fisher Scientific. Other reagents were of analytical grade and used without further purification.

Lotus polyphenol

The phenolic lotus root extract was prepared as previously described with some modifications (Tsuruta et al. 2011). In brief, lotus roots were harvested in the Saga Prefecture, Japan, and dried at 70 °C. The dried lotus roots were powdered and extracted with 50% EtOH for 5 h at room temperature. After filtration, the extract was purified with Diaion HP-20, a hydrophobic resin (Mitsubishi Chemical, Tokyo, Japan) and used as the lotus root polyphenol (LP). Approximately 9.95 g of LP was obtained from 300 g of lotus root powder and was dissolved in 50% EtOH. The putative structure of LP was previously presented as B-type proanthocyanidin, which is condensed with catechin and gallocatechin (Tsuruta et al. 2011).

Cell culture

Spontaneously immortalized human keratinocyte cell line (HaCaT) cells were obtained from Cell Line Service (Eppelheim, Germany). The cells were maintained in DMEM supplemented with 10% FBS.

Normal human epidermal keratinocytes (NHEK) were obtained from Kurabo Industries Ltd. (Okayama, Japan). NHEK cells were maintained in KGM-Gold™ BulletKit™ (Lonza, Walkersville, MD, USA).

HaCaT cells were cultured at 3.0 × 105 cells/well in a 24-well culture plate for 24 h and were washed twice with phosphate buffer saline (PBS) followed by exposure to UVA at 30 J/cm2. After UVA irradiation, cells were cultured in DMEM in the presence or absence of LP at concentrations of 0.4, 2, and 10 μg/mL. After cultivation for 48 h, cell viability was measured using the MTT assay. After incubation for 6 and 48 h, the mRNA expression levels of IL-1α and MMP-1 were measured by RT-qPCR. Western blot analysis was used to determine the effect of LP on the protein levels of MMP-1 in the medium cultured for 48 h.

Similar to HaCaT cells, NHEK cells were incubated in KGM-Gold™ BulletKit™, supplemented with or without LP for 48 h after exposure to UVA at 25 J/cm2. Cell viability and the levels of IL-1α and MMP-1 were determined.

The human epidermis model (LabCyte EPI-MODEL) was purchased from J-TEC (Nagoya, Japan). On receipt, the epidermis was transferred to the assay medium (J-Tec) and cultured for 18 h. After UVA irradiation at 30 J/cm2, the epidermis model was incubated in the presence or absence of LP (1 and 10 μg/mL) on the apical side for 6 h. LP was discarded by washing the epidermis model with PBS twice, after which the cells were incubated for an additional 18 h. On the following day, the epidermis model was re-loaded with LP or PBS to the apical side and incubated for another 6 h. LP or PBS were again removed by washing, and cells were incubated for an additional 18 h. After 48 h of exposure to UV irradiation, the cells were finally collected and used for the analysis of IL-1α and MMP-1 expression. Cell viability was measured using the MTT assay. All cells and the epidermis model were cultured under a humidified 5% CO2/95% air atmosphere at 37 °C.

UVA irradiation

UVA irradiation experiments were performed using a TOSHIBA SH1002MA lamp with an Asahi SPECTRA SH0385 + LU0325 filter that emits UVA (320–400 nm), and the emitted dose was measured with a UIT-250 luminometer equipped with a UVD-C365 probe. HaCaT and NHEK cells were exposed to UVA at doses of 30 and 25 J/cm2, respectively. The LabCyte EPI-MODEL was precultured in the assay media for 18 h and was exposed to 30 J/cm2 of UVA. Cells were then treated as described above. UVA- irradiation was used at an intensity that stably produced MMP-1 in each cell.

Measurement of IL-1α

The levels of IL-1α in the cell medium were measured using sandwich-ELISA. A 96-well microplate was coated with anti-human IL-1α. The antibody-coated wells were blocked with 1.0% BSA/PBS, and then each sample was added to the wells. After washing three times with 0.05% Tween 20 containing PBS (TPBS), biotin-conjugated anti-human IL-1α and HRP-conjugated streptavidin were added to the wells. After washing three times with TPBS, the TMB solution was added. After 15 min, 2 N H2SO4 was added, and the absorbance was measured at 415 nm using a microplate reader (Bio-Rad, Hercules, CA, USA).

Real-time qPCR

The mRNA expression of IL-1α and MMP-1 in HaCaT cells and in the LabCyte EPI-MODEL24 were quantified by RT-qPCR. The cells from both models were collected after cultivation for 48 h, and the total RNA from the cells was extracted using TRIzol reagent (Invitrogen, CA, USA) according to the manufacturer’s instructions. The total RNA was reverse-transcribed to synthesize cDNA using PrimeScript™ RT Master Mix (Takara Bio, Shiga, Japan). RT-qPCR was conducted using TB® Green Premix Ex Taq™ II (Takara Bio) and CFX96 Touch Real-Time System (Bio-Rad).

Western blotting

After 48 h of culturing, each supernatant was subjected to SDS-PAGE, and the proteins were transferred to a nitrocellulose membrane (Bio-Rad). The membrane was blocked with a PVDF blocking reagent for Can Get Signal™ acquisition (Toyobo, Co., Ltd, Osaka, Japan) at 4 °C overnight. After washing with 0.1% TPBS, the membrane was incubated with anti-human MMP-1 mouse antibodies in Can Get Signal™ solution 1 (Toyobo, Co., Ltd) at room temperature for 2 h. After washing with TPBS, the membrane was incubated with HRP-labeled anti-mouse IgG antibody in Can Get Signal™ solution 2 (Toyobo, Co., Ltd) at room temperature for 1 h. After washing again with TPBS, blots were developed using the TMB solution for western blotting (Nacalai Tesque, Kyoto, Japan). The band density was quantified using Image J system.

Statistics

All values are expressed as mean ± standard deviation (SD). Statistical analysis was performed using one-way ANOVA with Tukey–Kramer’s post hoc test. p-value < 0.05 was considered statistically significant (Statcel software (OMS Publishing Inc., Saitama, Japan).

Results and discussion

To evaluate the effects of LP on photoaging, mRNA expression of the pro-inflammatory cytokine IL-1α was measured in UVA-irradiated HaCaT cells in the presence of different doses of LP. We also analyzed the effects of LP on protein levels and gene expression of MMP-1. When the strength of irradiation was set at 30 J/cm2, the cell viability of HaCaT cells was not affected in the presence of LP, as shown in Fig. 1a. It has been reported that keratinocytes expressed IL-1α and IL-1β mRNA in vitro, and that IL-1α predominates in keratinocytes. IL-1α is constitutively synthesized as a biologically active precursor protein while IL-1β exists as an inactive precursor form in keratinocyte cultures (Magcwebeba et al. 2012; Mizutani et al. 1991). For this reason, IL-1α production is often used as skin inflammation marker and thus was measured in the present study. The mRNA expression of IL-1α was upregulated by exposure to UVA and counteracted by the presence of LP, which was not dose-dependent (Fig. 1b). UVA irradiation significantly increased the mRNA levels of MMP-1, whereas MMP-1 mRNA levels diminished dose-dependently in the cells treated with LP. This decreased expression was associated with lower MMP-1 protein levels (Fig. 1c), indicating that LP modified collagen-degrading enzyme activity at the cellular and molecular levels. These results suggest that lotus polyphenols may have the potential to reduce photoaging induced by UV irradiation by decreasing inflammation and subsequent expression of the collagen-degrading enzyme MMP-1. UV irradiation of the skin results in immunosuppression, photoaging, and photocarcinogenesis via ROS production, inflammation, and DNA breakdown (Afaq and Mukhtar 2006); UVB-induced ROS are known to cause skin damage through mitogen-activated protein kinases (MAPKs) and nuclear factor-kappa B (NF-κB) (Kim et al. 2012a, b). To further detail the underlying mechanism of the anti-photoaging activity of LP, the levels of ROS and ROS-induced alterations, such as MAPK and NF-κB, need to be evaluated.

Fig. 1.

Fig. 1

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Effect of LP on IL-1α and MMP-1 expression in HaCaT. Cells were cultured in DMEM in the presence or absence of LP for 6 or 48 h after UVA irradiation. a Cell viability was measured by MTT assay. b mRNA expression levels of IL-1α and MMP-1 was measured by RT-qPCR. c MMP-1 levels in the culture medium were detected using western blotting. The result showed the average value of four–five independent measurements. Data are expressed as the mean ± SD (n = 4). Statically significant differences were represented as *p < 0.05, **p < 0.01 vs. UVA (−) LP (−), †p < 0.05, ††p < 0.01 vs. UVA (+) LP (−)

Next, we used human keratinocytes (NHEK) to further determine how LP modulates UV-induced photoaging and measured inflammation and collagenase level, as shown in Fig. 2. Cell viability of normal keratinocytes was decreased by UV irradiation, but was not affected by LP at a concentration of 10 μg/mL. UV exposure to keratinocytes did not alter the levels of IL-1α in the cell medium, which was probably because IL-1α was determined 48 h after UV irradiation, and the effect of exposure on IL-1α might have been diluted. Magcwebeba et al. (2012) showed that the level of extracellular IL-1α in medium of UV-irradiated keratinocytes peaked out at 6 h post-irradiation and was thereafter equal to or lower than that of the control at 24 h, indicating that timing of measurement may account for apparent contradictory result on IL-1α. Since, in our study, extracellular IL-1α of keratinocytes was examined after 48 h of UV irradiation, IL-1α did thus not appear to be elevated. In contrast, the presence of LP markedly ameliorated the secretion of IL-1α into the cell medium without a dose-dependent effect. Western blot analysis clearly revealed that the level of MMP-1 protein was enhanced by UV irradiation, whereas it was dramatically decreased by more than 90% in cells treated with LP, indicating that our analysis is considered to be appropriate to show the effect of LP on UV irradiation. Thus, the intracellular and extracellular IL-1α-concentrations changed significantly depending on the time after UV irradiation, but LP decreased the release of IL-1α and MMP-1, implying that it may have a strong inhibitory activity.

Fig. 2.

Fig. 2

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Effect of LP on IL-1α and MMP-1 production in NHEK. NHEK were cultured in KGM-Gold™ BulletKit™ in the presence or absence of LP for 48 h after UVA irradiation. a Cell viability was measured by MTT assay. b IL-1α in the medium was measured by ELISA. c MMP-1 levels in the culture medium were detected by western blotting. The result showed the average value of four–five independent measurements. Data are expressed as the mean ± SD (n = 3). Statically significant differences were represented as *p < 0.05, **p < 0.01 vs. UVA (−) LP (−), †p < 0.05, ††p < 0.01 vs. UVA (+) LP (−)

Using LabCyte EPI-MODEL24, we investigated whether LP influences photoaging, as seen in HaCaT and NHEK. The cell viability of the epidermal model was decreased by UV irradiation, but was increased by the addition of LP (Fig. 3a). UV irradiation caused an increase in gene expression of IL-1α. These levels were dose-dependently downregulated by the addition of LP, as shown in Fig. 3b. LP lowered the mRNA levels of MMP-1 induced by UV irradiation, which was associated with lower levels of MMP-1 protein in the culture medium (Fig. 3b and c), indicating that as seen in HaCaT and NHEK, LP improved damage triggered by UV irradiation in the epidermal model. The functions of the skin are dependent on collagen integrity in the dermis, which is often manipulated by MMP-1 (collagenase), leading to wrinkled and stiffened skin (Naylor et al. 2011). Our results with three different skin cells showed that LP may help maintain skin health through decreased levels of MMP-1 activity via its anti-inflammatory properties. UVB alters the expression of AP-1 and NF-κB via ROS production, leading to the destruction of the extracellular matrix (ECM) (Zhi et al. 2020). Polyphenols are known to reduce ROS production. Accordingly, the mechanisms by which LP modifies skin physiology need to be further evaluated.

Fig. 3.

Fig. 3

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Effect of LP on IL-1α and MMP-1 production in the human epidermal model. The epidermal model was treated on the apical side with LP for 6 h a day for 2 days after UVA irradiation. a Cell viability was measured by MTT assay. b mRNA expression levels of IL-1α and MMP-1 were measured by RT-qPCR. c IL-1α in medium was measured by ELISA. d MMP-1 levels in the culture medium were detected by western blotting. The result showed the average value of four–five independent measurements. Data are expressed as the mean ± SD (n = 4–5). Statically significant differences were represented as *p < 0.05, **p < 0.01 vs. UVA (−) LP (−), †p < 0.05, ††p < 0.01 vs. UVA (+) LP (−)

Previous studies have shown that botanical products alleviate photoaging caused by UV exposure through a wide range of mechanisms in various cells (Afaq and Mukhtar 2006; Kim et al. 2012a, b; Apraj and Pandita 2016; Kim et al. 2017; Wölfle et al. 2011; Vayalil et al. 2004; Park et al. 2014; Huang et al. 2007). For example, kirenol in Siegesbeckia glabrescens suppressed UVB-induced photoaging such as mRNA expression of collagenase, catalase, and matrix metalloproteinase via the inhibition of MAPK and NF-κB pathways in fibroblasts (Kim et al. 2017). Bae et al. (2010) reported that ellagic acid in berries attenuated collagen degradation through decreased secretion of MMP, and blocked collagen degradation in UVB-treated HaCaT keratinocytes, thereby suppressing the production of pro-inflammatory cytokines such as IL-1β and IL-6. Park et al. (2014) reported that the extract of Kaempferia parviflora (black ginger) prevented UVB-induced photoaging via reduced expression of IL-1β in hairless mice. Green tea polyphenols, including epigallocatechin-3-gallate and epigallocatechin, inhibit the MAPK pathway and, as a result, attenuate inflammation via antioxidative activity (Huang et al. 2007). La et al. (2009) have reported that cranberry proanthocyanidins including catechin inhibit MMP production and activity in human monocytes stimulated with LPS. Proanthocyanidins derived from LP used in the present study are polymer of catechin and gallocatechin as stated in our previous report (Tsuruta et al. 2011). Taken together, our results indicate that polyphenols in lotus root extract are responsible for an anti-photoaging potential via attenuating inflammation. In addition to the antioxidant activity and the anti-obesity activity in our previous study (Tsuruta et al. 2012), the results of the present study expand the applicability of LP to nutraceuticals.

Author contributions

AI conceived and designed the experiment. AI and RY equally performed the experiment and wrote the paper. SO and YT partially analyzed data. TK, YN, and TY supervised and helped with the editing of the manuscript.

Funding

This research did not receive any specific grant from funding agencies in the commercial or not-for-profit sectors.

Data availability

The data that support the findings of this study are available from the corresponding author, AI, upon reasonable request.

Declarations

Conflict of interest

Authors declare no conflict of interest.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Akira Iwamoto, Email: iwamoto@saga-itc.jp.

Ryoko Yamauchi, Email: yamauchi0803ryoko@gmail.com.

Shigeki Oogai, Email: ogai-shigeki@mb.infosaga.or.jp.

Yumi Tsuruta, Email: tsuruta-yumi@pref.saga.lg.jp.

Tsuge Keisuke, Email: tsuge-keisuke@pref.saga.lg.jp.

Yasuo Nagata, Email: y-nagata@mb.infosaga.or.jp.

Teruyoshi Yanagita, Email: yanagitt@mb.infosaga.or.jp.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author, AI, upon reasonable request.

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