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Atractylenolide I alleviates the experimental allergic response in mice by suppressing TLR4/NF-kB/NLRP3 signalling

  • Weiran Cai , Zhijun Zhang , Chenyan Shi , Ru Sun , Han Ju , Xuelin Dong and Lei Teng ORCID logo EMAIL logo
Published/Copyright: August 8, 2025
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Open Life Sciences
From the journal Open Life Sciences Volume 20 Issue 1

Abstract

Allergic rhinitis (AR) is a frequent respiratory condition characterized by elevated immunoglobulin E (IgE) levels and nasal mucosal inflammation. Atractylenolide I (ATL-I), a bioactive ingredient in medicinal plants, is known for its ability to alleviate tissue damage by inhibiting inflammatory and oxidative stress responses. In this study, we aimed to investigate the protective roles of ATL-I in AR and reveal the potential mechanism involved. The AR model was developed in mice by intraperitoneal sensitization followed by intranasal exposure to ovalbumin. The effects of ATL-I on allergic responses were evaluated by recording sneezing and rubbing frequencies and measuring the serum concentrations of Th1 and Th2 cytokines following the intragastric administration of ATL-I. The activation of the Toll-like receptor 4/nuclear factor κB (TLR4/NF-κB) pathway and the NOD-like receptor 3 (NLRP3) inflammasome was assessed via Western blotting and immunohistochemistry. The results showed that ATL-I administration alleviated allergic responses in AR mice, as evidenced by significant decreases in the frequencies of sneezing and rubbing and in the serum concentrations of histamine and IgE. Compared with control mice, AR mice presented downregulated Th1 cytokines and upregulated Th2 cytokines, whereas the Th1/Th2 imbalance was improved by ATL-I. ATL-I reduced the mucosal layer thickness and alleviated goblet cell hyperplasia in AR mice. Furthermore, ATL-I inhibited TLR4/NF-κB pathway activation in mucosal tissues, which resulted in the inactivation of the downstream NLRP3 inflammasome. In summary, our results indicate that ATL-I alleviates allergic responses by inhibiting the TLR4/NF-κB/NLRP3 pathway, providing a promising therapeutic strategy for AR.

Graphical abstract

Keywords: allergic rhinitis; atractylenolide I; TLR4; NF-κB; NLRP3; Th1/Th2 imbalance

1 Introduction

Allergic rhinitis (AR) is a long-term allergic respiratory condition caused by exposure to specific allergens and is regulated by specific immunoglobulin E (IgE) [1]. The condition is frequently diagnosed in rhinology, affecting nearly 20–30% of the population worldwide [2]. AR causes no threat to life but results in nasal itching, sneezing, and rhinophobia, resulting in a reduction in individuals’ quality of life [3]. Currently, the primary medications for AR therapy include H1-antihistamines, corticosteroids, and allergen immunotherapy [4]. Although current treatment methods have made significant progress, no method that can fundamentally cure patients with AR exists. The identification of effective anti-AR drugs and the development of corresponding medical devices are indispensable.

Emerging evidence has shown that plant-derived compounds such as curcumin [5], shenqi [6], and luteolin [7] exert potent protective effects against AR, suggesting that these natural active ingredients might be potential therapeutic strategies for AR. Atractylenolide (ATL) is a member of a class of sesquiterpene lactones that is primarily derived primarily from Atractylodes macrocephala [8]. This class encompasses ATL-I, ATL-II, and ATL-III, all of which have demonstrated therapeutic potential. For example, ATL-III has been utilized to treat nonalcoholic fatty liver disorders, spinal cord injuries, and osteoarthritis [9,10,11]. ATL-II has shown efficacy in inhibiting lung cancer cell metastasis and in mitigating radiation damage [12,13]. ATL-I, the principal biologically active component of ATL, is associated with a variety of pharmacological activities. It has been found to protect against breast cancer tumorigenesis via the Toll-like receptor 4 (TLR4)/nuclear factor kappa B (NF-κB) pathways [14] and to suppress colorectal cancer by inducing apoptosis and inhibiting glycolysis [15]. Furthermore, ATL-I has shown promise as a therapeutic agent for managing Parkinson’s disease [16]. However, the role of ATL-I in AR remains to be elucidated.

A T helper 1 (Th1)/Th2 cell imbalance is closely correlated with the onset of allergic disorders, particularly AR [17]. Exposure to an allergen triggers an immune response, leading to Th2 cell proliferation. Activated Th2 cells release cytokines such as IL-4, IL-5, and IL-13, which prompt IgE antibody generation. When re-exposed to the allergen, mast cells and basophils that bind IgE produce inflammatory substances such as histamine, culminating in AR [18]. Conversely, Th1 cells produce interferon gamma (IFN-γ), which inhibits the production of Th2 cytokines [19]. Thus, addressing the Th1/Th2 imbalance may represent a promising approach for the treatment of AR. Excessive activation of the TLR4/NF-κB pathway has a pivotal effect on the Th1/Th2 imbalance. TLR4 activates NF-κB signalling, which subsequently accelerates the expression of proinflammatory cytokines and chemokines [20]. Notably, a recent study revealed that luteolin ameliorates the Th1/Th2 imbalance by inhibiting the activation of the TLR4/NF-κB pathway in AR rats [7], suggesting that TLR4/NF-κB signalling is a potential target for reversing the Th1/Th2 imbalance. Furthermore, NF-κB is a key initiator for activating the NOD-like receptor 3 (NLRP3) inflammasome by increasing NLRP3 expression and triggering caspase 1 activation [20,21]. Activated caspase-1 processes pro-IL-1β and pro-IL-18 into their biologically active forms (IL-1β and IL-18), driving inflammation. It also cleaves gasdermin D (GSDMD), initiating pyroptosis, a distinct form of programmed cell death [22]. The NLRP3 inflammasome plays a vital role in mediating allergic responses [23]. Given the effects of ATL-I on alleviating NLRP3 inflammasome activation in many types of diseases [24,25,26], we aimed to investigate whether ATL-I alleviates allergic responses by inhibiting TLR4/NF-kB/NLRP3 activation in an experimental AR model.

2 Materials and methods

2.1 Reagents

Ovalbumin (OVA, Cat# HY-W250978), aluminium hydroxide (Cat# HY-B1521), ATL-I (Cat# HY-N0201), and dexamethasone (Dex, Cat# HY-14648) were obtained from MCE (NJ, USA). Enzyme-linked immunosorbent assay (ELISA) kits for mouse histamine (ab213975), IL-2 (ab100706), IL-5 (ab100711), and IL-13 (ab100700), anti-rabbit secondary antibodies (HRP, ab6721), and DAB reagents (ab64238) were obtained from Abcam (MA, USA). ELISA kits for mouse IFN-γ (P1508) and IL-4 (PI612), TRIzol reagent (R0016), RIPA lysis buffer (Cat# P0013B), the BCA kit (Cat# P0012), BeyoECL Plus (Cat# P0018S), the haematoxylin and eosin (H&E) kit (C0105S), and the periodic acid–Schiff (PAS) kit (C0142S) were obtained from Beyotime (Shanghai, China). An IgE ELISA kit (Cat# CSB-E08914) was obtained from Cusabio (Wuhan, China). The cDNA reverse transcription reagent (Cat# 4368814), TLR4 polyclonal antibody (Cat# 48-2300), NLRP3 antibody (Cat# MA5-23919), cleaved caspase-1 antibody (Cat# PA5-99390), GSDMD antibody (Cat# PA5-116815), and phosphorylated p65 (p-p65) polyclonal antibody (Cat# 44-711G) were obtained from Thermo Fisher (MA, USA). The SYBR green mixture was obtained from TaKaRa (Tokyo, Japan).

2.2 Animal experiments

The work was conducted with approval from the Animal Ethics Committee of Shanghai University of Traditional Chinese Medicine (approval number: PZSHUTCM211227022) in accordance with the ARRIVE guidelines to minimize animal suffering and numbers. Female C57BL/6 mice (weighing 23–28 g; aged over 8 weeks) were obtained from Shanghai Vital River (Shanghai, China) and maintained in a temperature- and humidity-controlled environment. The AR model was developed by intraperitoneal sensitization with 50 μg of OVA and 5 mg of aluminium hydroxide on Days 1, 7, and 14, followed by intranasal exposure to OVA (20 μL, 40 mg/mL) from the 22nd to 29th days, as previously described [23,27,28]. In accordance with a previous study [24] and our preliminary experiment, AR mice were treated by intragastric delivery of ATL-I (0, 25, or 50 mg/kg) from the 22nd to 31st days. A positive control, Dex (3 mg/kg), was administered via intraperitoneal injection according to the manufacturer’s instructions. Similarly, TLR4 antagonist TAK-242 (MCE, 3 mg/kg) was also administered via intraperitoneal injection. All the animals were categorized into five separate groups (n = 6): (i) the Ctrl group, (ii) the AR group (AR mice treated with 0 mg/kg ATL-I), (iii) the ATL-25 group (AR mice treated with 25 mg/kg ATL-I), (iv) the ATL-50 group (AR mice treated with 50 mg/kg ATL-I), and (v) the Dex group. The frequencies of sneezing and rubbing were recorded over a period of 20 min on the 33rd day by two blinded observers to evaluate the severity of nasal symptoms. Nasal mucosal tissues were subsequently collected from all the mice after euthanasia by pentobarbital overdose and cervical dislocation.

  1. Ethical approval: The research related to animal use has been complied with all the relevant national regulations and institutional policies for the care and use of animals and has been approved by the Animal Ethics Committee of Shanghai University of Traditional Chinese Medicine (No. PZSHUTCM211227022).

2.3 ELISA

The concentrations of histamine, IFN-γ, IL-2, IL-4, IL-5, IL-13, and OVE-specific IgE were measured with commercial kits according to the manufacturers’ instructions.

2.4 Quantitative real-time PCR (qRT-PCR)

RNA was extracted from nasal mucosal tissues using TRIzol reagent and reverse transcribed into cDNA with a reverse transcription. qRT-PCR was conducted on a LightCycler 480® PCR system (Roche, Switzerland) in a 10 µL reaction mixture including cDNA, SYBR Green mix, and primers (Table S1). The mRNA level was determined with the 2−ΔΔCT formula after normalization to β-actin [29].

2.5 Western blot

Protein extraction was performed using RIPA buffer, the protein concentrations were quantified by the BCA method, and proteins were separated on 12% sodium dodecyl sulfate-polyacrylamide gel electrophoresis gels and subsequently transferred to polyvinylidene fluoride membranes. Afterwards, the membranes were incubated with primary antibodies for 1 h at room temperature, followed by a 60 min incubation with the secondary antibodies. The immunoblots were visualized using ECL reagents and quantified with ImageJ (NIH, MA, USA).

2.6 Immunohistochemistry (IHC)

Nasal tissues fixed with 4% paraformaldehyde were embedded in paraffin and sectioned into 4 μm thick slices. After deparaffinization, rehydration, antigen retrieval, and treatment with hydrogen peroxide, the slices were subjected to incubation with primary antibodies for 60 min, followed by a 60 min incubation with the secondary antibodies. After being visualized with DAB reagent and restained with haematoxylin, the slices were imaged with a fluorescence microscope (Olympus, Tokyo, Japan).

2.7 H&E and PAS staining

Nasal tissues embedded in paraffin were cut into 4 μm thick slices. Following deparaffinization and rehydration, the slices were stained via H&E and PAS kits according to the manufacturers’ instructions. The slices were photographed using a DM500 optical microscope (Leica, Wetzlar, Germany).

2.8 Statistics

The data, derived from three separate trials, are presented as the means ± standard deviation. One‐way analysis of variance (Dunnett’s post hoc test) was applied for multigroup comparisons with the aid of SPSS 20.0 (IBM, NY, USA). A p-value of less than 0.05 was considered statistically significant.

3 Results

3.1 ATL-I alleviated the clinical symptoms of AR mice

An AR model was developed in mice by intraperitoneal sensitization followed by intranasal exposure to OVA to investigate the protective effect of ATL-I (Figure 1a) on AR. Nasal symptoms were measured after the intragastric administration of ATL-I (0, 25, or 50 mg/kg) or a positive control, Dex (3 mg/kg) (Figure 1b). Compared with those of control mice, the frequencies of sneezing and rubbing were significantly increased in AR mice, whereas these increases were significantly reversed by 50 mg/kg ATL-I (Figure 2a and b). In addition, the serum histamine concentration was increased in AR mice compared to control mice, whereas this change was significantly blocked by 50 mg/kg ATL-I (Figure 2c). ATL-I also decreased the serum concentrations of IgE in AR mice (Figure 2d).

Figure 1 Schematic diagram of the experimental protocol. (a) Chemical structure of ATL-I. (b) Schematic diagram of AR mouse model construction and ATL-I treatment (n = 6 mice per group). The AR model was developed in mice by intraperitoneal sensitization with OVA (50 μg) and aluminium hydroxide (1 mg), followed by intranasal exposure to OVA (40 mg/mL) at the time points indicated by the red arrows. The control animals were administered saline. AR mice were treated by the intragastric delivery of ATL-I (0, 25, or 50 mg/kg) or a positive control, Dex (3 mg/kg), at the time points indicated by the green arrows.
Figure 1

Schematic diagram of the experimental protocol. (a) Chemical structure of ATL-I. (b) Schematic diagram of AR mouse model construction and ATL-I treatment (n = 6 mice per group). The AR model was developed in mice by intraperitoneal sensitization with OVA (50 μg) and aluminium hydroxide (1 mg), followed by intranasal exposure to OVA (40 mg/mL) at the time points indicated by the red arrows. The control animals were administered saline. AR mice were treated by the intragastric delivery of ATL-I (0, 25, or 50 mg/kg) or a positive control, Dex (3 mg/kg), at the time points indicated by the green arrows.

Figure 2 ATL-I alleviated clinical symptoms in AR mice. Sneezing (a) and rubbing (b) frequencies were counted for 20 min in control mice (Ctrl group) and AR mice treated with 0 mg/kg ATL-I (ATL-0 group), 25 mg/kg ATL-I (ATL-25 group), 50 mg/kg ATL-I (ATL-50 group), or 3 mg/kg Dex (Dex group). The serum concentrations of histamine (c) and OVA-specific IgE (d) were measured by ELISAs in the Ctrl group, the ATL-0 group, the ATL-25 group, the ATL-50 group, and the Dex group. Control mice and AR model mice were treated with 0 mg/kg ATL-I (ATL-0), 25 mg/kg ATL-I (ATL-25), 50 mg/kg ATL-I (ATL-50), or Dex (3 mg/kg). *p < 0.05, **p < 0.01, ***p < 0.001, ns, not significant.
Figure 2

ATL-I alleviated clinical symptoms in AR mice. Sneezing (a) and rubbing (b) frequencies were counted for 20 min in control mice (Ctrl group) and AR mice treated with 0 mg/kg ATL-I (ATL-0 group), 25 mg/kg ATL-I (ATL-25 group), 50 mg/kg ATL-I (ATL-50 group), or 3 mg/kg Dex (Dex group). The serum concentrations of histamine (c) and OVA-specific IgE (d) were measured by ELISAs in the Ctrl group, the ATL-0 group, the ATL-25 group, the ATL-50 group, and the Dex group. Control mice and AR model mice were treated with 0 mg/kg ATL-I (ATL-0), 25 mg/kg ATL-I (ATL-25), 50 mg/kg ATL-I (ATL-50), or Dex (3 mg/kg). *p < 0.05, **p < 0.01, ***p < 0.001, ns, not significant.

3.2 ATL-I improved the Th1/Th2 imbalance in AR mice

The ability of ATL-I to improve the Th1/Th2 imbalance was next investigated by measuring the serum concentrations of Th1 and Th2 cytokines. Figure 3a and b shows that the serum IFN-γ and IL-2 levels were markedly lower in AR mice than in control mice, whereas these decreases were prevented by ATL-I. Conversely, the serum concentrations of IL-4, IL-5, and IL-13 were markedly increased in AR mice, whereas these changes were blocked by ATL-I (Figure 3c–e). Compared with that in normal mice, the IFN-γ-to-IL-4 ratio in AR mice was significantly lower, whereas this decrease was counteracted by ATL-I (Figure 3f).

Figure 3 ATL-I improved the Th1/Th2 imbalance in AR mice. The serum concentrations of IFN-γ (a), IL-2 (b), IL-4 (c), IL-5 (d), and IL-13 (e) in the Ctrl, ATL-0, ATL-25, ATL-50, and Dex groups were measured via ELISAs. (f) The ratio of IFN-γ to IL-4 was calculated according to their concentrations. *p < 0.05, **p < 0.01, ***p < 0.001, ns, not significant.
Figure 3

ATL-I improved the Th1/Th2 imbalance in AR mice. The serum concentrations of IFN-γ (a), IL-2 (b), IL-4 (c), IL-5 (d), and IL-13 (e) in the Ctrl, ATL-0, ATL-25, ATL-50, and Dex groups were measured via ELISAs. (f) The ratio of IFN-γ to IL-4 was calculated according to their concentrations. *p < 0.05, **p < 0.01, ***p < 0.001, ns, not significant.

The impact of ATL-I on histological changes in the nasal mucosa was subsequently assessed. H&E staining revealed an orderly arrangement of epithelial cells and ciliated tissues in the normal nasal mucosa (Figure 4a). Conversely, the mucosal tissues from AR mice often displayed epithelial exfoliation and dilation of blood vessels in the lamina propria. These changes, however, were mitigated by ATL-I (Figure 4a). The epithelial thickness was significantly increased in AR mice, which was effectively prevented by ATL-I (Figure 4a and c). Compared with that of normal mice, the nasal mucosa of AR mice exhibited a marked increase in goblet cell hyperplasia, which was subsequently mitigated by ATL-I (Figure 4b and d).

Figure 4 The roles of ATL-I in histological alterations. H&E (a) and PAS (b) staining of nasal tissues from the Ctrl group, the ATL-0 group, the ATL-25 group, the ATL-50 group, and the Dex group. Epithelial thickness (c) and goblet cell hyperplasia (d) were assessed in nasal tissues from the Ctrl group, the ATL-0 group, the ATL-25 group, the ATL-50 group, and the Dex group. **p < 0.01, ***p < 0.001, ns, not significant.
Figure 4

The roles of ATL-I in histological alterations. H&E (a) and PAS (b) staining of nasal tissues from the Ctrl group, the ATL-0 group, the ATL-25 group, the ATL-50 group, and the Dex group. Epithelial thickness (c) and goblet cell hyperplasia (d) were assessed in nasal tissues from the Ctrl group, the ATL-0 group, the ATL-25 group, the ATL-50 group, and the Dex group. **p < 0.01, ***p < 0.001, ns, not significant.

3.3 ATL-I suppressed TLR4/NF-κB activation

Accumulating evidence has verified that the TLR4/NF-κB pathway is commonly activated in the nasal mucosa of AR mice and that the inhibition of this signalling pathway is crucial for ameliorating allergic responses [7,30,31,32,33,34]. As shown in Figure 5a–c, significant increases in TLR4 mRNA and protein expression were observed in AR mice, which were effectively blocked by ATL-I. Furthermore, p-p65 levels were markedly increased in the nasal mucosa of AR mice, whereas these increases were prevented by ATL-I (Figure 5b and c). IHC analysis revealed that ATL-I prominently decreased p-p65 levels in the nasal mucosa of AR mice (Figure 5d and e). Consistent with previous reports [31,35], the TLR4 antagonist TAK-242 markedly inhibited NF-κB signalling activation (Figure S1a and b) and improved the Th1/Th2 imbalance in AR mice (Figure S1c–g). These data indicate that ATL-I inhibits the activation of TLR4/NF-κB signalling in AR mice, which ameliorates Th1/Th2 imbalance.

Figure 5 ATL-I suppressed the TLR4/NF-κB signalling pathway. (a) qRT-PCR analysis of TLR4 mRNA expression in nasal mucosal tissues from the Ctrl group, the ATL-0 group, the ATL-25 group, the ATL-50 group, and the Dex group. Western blot (b) and quantitative (c) analyses of TLR4 and p-p65 protein levels in nasal mucosal tissues from the Ctrl group, the ATL-0 group, the ATL-25 group, the ATL-50 group, and the Dex group. IHC (d) and quantitative (e) analysis of p-p65 protein levels in nasal mucosal tissues from the Ctrl group, the ATL-0 group, the ATL-25 group, the ATL-50 group, and the Dex group. *p < 0.05, **p < 0.01, ***p < 0.001, ns, not significant.
Figure 5

ATL-I suppressed the TLR4/NF-κB signalling pathway. (a) qRT-PCR analysis of TLR4 mRNA expression in nasal mucosal tissues from the Ctrl group, the ATL-0 group, the ATL-25 group, the ATL-50 group, and the Dex group. Western blot (b) and quantitative (c) analyses of TLR4 and p-p65 protein levels in nasal mucosal tissues from the Ctrl group, the ATL-0 group, the ATL-25 group, the ATL-50 group, and the Dex group. IHC (d) and quantitative (e) analysis of p-p65 protein levels in nasal mucosal tissues from the Ctrl group, the ATL-0 group, the ATL-25 group, the ATL-50 group, and the Dex group. *p < 0.05, **p < 0.01, ***p < 0.001, ns, not significant.

3.4 ATL-I suppressed NLRP3 inflammasome activation

The effects of ATL-I on alleviating NLRP3 inflammasome activation in the nasal mucosa were subsequently investigated. As shown in Figure 6a and b, NLRP3 and cleaved caspase-1 protein levels were markedly increased in AR mice compared with control mice, and ATL-I treatment reversed this process. More importantly, ATL-I decreased GSDMD cleavage in AR mice (Figure 6a and c). Compared with those of control mice, the nasal tissues of AR mice presented increased IL-18 and IL-1β levels. However, these increases were blocked by ATL-I (Figure 6d). ATL-I treatment also resulted in decreased release of IL-18 and IL-1β in the nasal lavage fluid of AR mice (Figure 6e and f).

Figure 6 ATL-I suppressed the activation of the NLRP3 inflammasome. Western blot (a) and quantitative (b) and (c) analyses of the levels of the NLRP3, cleaved caspase-1, and GSDMD proteins in nasal mucosal tissues from the Ctrl group, the ATL-0 group, the ATL-25 group, the ATL-50 group, and the Dex group. (d) qRT-PCR analysis of IL-18 and IL-1β mRNA expression in nasal mucosal tissues from the Ctrl group, the ATL-0 group, the ATL-25 group, the ATL-50 group, and the Dex group. IL-18 (e) and IL-1β (f) levels in the nasal lavage fluid from the Ctrl, ATL-0, ATL-25, ATL-50, and Dex groups were measured by ELISAs. *p < 0.05, **p < 0.01, ***p < 0.001, ns, not significant.
Figure 6

ATL-I suppressed the activation of the NLRP3 inflammasome. Western blot (a) and quantitative (b) and (c) analyses of the levels of the NLRP3, cleaved caspase-1, and GSDMD proteins in nasal mucosal tissues from the Ctrl group, the ATL-0 group, the ATL-25 group, the ATL-50 group, and the Dex group. (d) qRT-PCR analysis of IL-18 and IL-1β mRNA expression in nasal mucosal tissues from the Ctrl group, the ATL-0 group, the ATL-25 group, the ATL-50 group, and the Dex group. IL-18 (e) and IL-1β (f) levels in the nasal lavage fluid from the Ctrl, ATL-0, ATL-25, ATL-50, and Dex groups were measured by ELISAs. *p < 0.05, **p < 0.01, ***p < 0.001, ns, not significant.

4 Discussion

AR is a common allergic disease that affects approximately 30% of the world’s population [36]. An increasing number of reports have highlighted the effects of plant-derived compounds on the treatment of AR. For example, the extract of Osterici Radix has antiallergic properties [37], whereas Nigella sativa has been found to alleviate symptoms such as nasal mucosal congestion, nasal itching, runny nose, and sneezing [38]. Furthermore, methylwarifteine has been reported to reduce eosinophilia, the number of inflammatory cells, and NF-кB activation in granulocytes and lymphocytes [39]. ATL-I, a compound used to treat various diseases, has been studied for its potential role in AR, although its efficacy remains unconfirmed [14,15,16]. Several studies have indicated that ATL-I functions by regulating TLR4 and related signalling pathways. For example, ATL-I mitigates liver damage by inhibiting TLR4/mitogen-activated protein kinase (MAPK)/NF-κB signalling [40], increasing the chemosensitivity of cancer cells to paclitaxel through the regulation of TLR4/MyD88 signalling [41], and decreasing breast cancer progression via the inhibition of TLR4/NF-κB signalling [14]. Given the crucial role of TLR4/NF-κB signalling in allergic inflammation, this study aimed to explore whether ATL-I has a protective effect on AR. The results revealed that (i) ATL-I mitigated the clinical symptoms of AR mice; (ii) ATL-I ameliorated the Th1/Th2 imbalance in AR mice; (iii) ATL-I decreased TLR4/NF-κB signalling activation; and (iv) ATL-I suppressed NLRP3 inflammasome activation.

The Th1/Th2 imbalance is crucial in the development of AR. Plant-derived compounds exhibit therapeutic potential in treating AR by addressing the Th1/Th2 imbalance. For example, Ke et al. showed that quercetin partially mitigates AR symptoms by inhibiting the Th1/Th2 imbalance [42]. Similarly, bergapten modulates the Th1/Th2 ratio by regulating the levels of cytokines associated with these T-helper cells in an AR mouse model [43]. Nguyen et al. proposed Artemisia gmelinii extracts as potential therapeutic agents for AR because of their role in maintaining Th1/Th2 homeostasis [44]. While a few studies have revealed the role of ALT in improving the Th1/Th2 imbalance [45], the function of ATL-I in AR has yet to be defined. Here, we discovered that ATL-I plays a regulatory role in the Th1/Th2 imbalance by increasing the levels of Th1-related cytokines (IL-2 and IFN-γ) and decreasing the levels of Th2-related cytokines (IL-4, IL-5, and IL-13) in AR mice. Moreover, ATL-I improved the Th1/Th2 imbalance by inactivating the TLR4/NF-κB/NLRP3 pathway. This finding aligns with emerging studies that highlight the regulatory role of ATL-I in the TLR4/NF-κB pathway [14,40]. This study is the first to reveal the role of ATL-I in addressing Th1/Th2 imbalance by decreasing TLR4/NF-κB activation.

ATL-I alleviates AR symptoms by ameliorating the Th1/Th2 imbalance through the inhibition of TLR4/NF-κB/NLRP3 activation, suggesting that ATL-I is a potential therapeutic agent for AR. Nevertheless, this study has several limitations: (i) Given the significant roles of other signalling pathways, including Janus kinase (JAK)/signal transducer and activator of transcription (STAT), MAPK, and activator protein 1 (AP-1), in AR, investigating the regulatory effects of ATL-I on these pathways is essential. Xu et al. reported that chlorogenic acid treatment effectively mitigates allergic responses by regulating the TLR4/MAPK/NF-κB pathway [46]. Psoralen exerts anti-inflammatory effects in AR through inactivating the AP-1 signalling pathway [47]. ATL-I has been shown to decrease the levels of phosphorylated JAK2 and phosphorylated STAT3 [48]. Therefore, further investigation into the roles of ATL-I in these signalling pathways is warranted to fully elucidate its therapeutic potential in AR. (ii) It is necessary to further investigate the optimal administration route and dosage of ATL-I. Intranasal administration may be a suitable route, allowing targeted delivery to nasal tissues while minimizing systemic exposure. Compared to conventional antihistamines and corticosteroids, ATL-I may offer advantages such as fewer adverse effects or enhanced modulation of inflammatory pathways. However, further studies are needed to evaluate its long-term safety, optimal dosing strategies, and potential formulation challenges.

5 Conclusions

These results show that ATL-I alleviates allergic responses by inhibiting the TLR4/NF-κB/NLRP3 pathway, providing a promising therapeutic strategy for AR.

# Co-first authors: Weiran Cai, Zhijun Zhang and Chenyan Shi contributed equally.

tel: +86-21-20256233

Acknowledgments

The authors are grateful for the reviewer’s valuable comments that improved the manuscript.

  1. Funding information: This study was funded by the General Project of the National Natural Science Foundation of China (82174447) and the Youth Project of the National Natural Science Foundation of China (82104940).

  2. Author contributions: All authors jointly conducted the experiments and carried out the data collection. TL and CW carried out statistical analysis, drafted the manuscript, and provided critical revisions. ZZ and SC handled data acquisition, analysis, and interpretation. SR, J H, and DX contributed significantly to the study’s design and manuscript preparation, with input from all co-authors. All authors reviewed and approved the final version.

  3. Conflict of interest: Authors state no conflict of interest.

  4. Data availability statement: The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

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Received: 2025-02-08
Revised: 2025-05-21
Accepted: 2025-06-05
Published Online: 2025-08-08

© 2025 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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https://doi.org/10.1515/biol-2025-1143
Keywords for this article
allergic rhinitis; atractylenolide I; TLR4; NF-κB; NLRP3; Th1/Th2 imbalance
Creative Commons
BY 4.0

Articles in the same Issue

  1. Biomedical Sciences
  2. Mechanism of triptolide regulating proliferation and apoptosis of hepatoma cells by inhibiting JAK/STAT pathway
  3. Maslinic acid improves mitochondrial function and inhibits oxidative stress and autophagy in human gastric smooth muscle cells
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  11. Neurodegenerative diseases and neuroinflammation-induced apoptosis
  12. Impact of fracture fixation surgery on cognitive function and the gut microbiota in mice with a history of stroke
  13. COLEC10: A potential tumor suppressor and prognostic biomarker in hepatocellular carcinoma through modulation of EMT and PI3K-AKT pathways
  14. High-temperature requirement serine protease A2 inhibitor UCF-101 ameliorates damaged neurons in traumatic brain-injured rats by the AMPK/NF-κB pathway
  15. SIK1 inhibits IL-1β-stimulated cartilage apoptosis and inflammation in vitro through the CRTC2/CREB1 signaling
  16. Rutin–chitooligosaccharide complex: Comprehensive evaluation of its anti-inflammatory and analgesic properties in vitro and in vivo
  17. Knockdown of Aurora kinase B alleviates high glucose-triggered trophoblast cells damage and inflammation during gestational diabetes
  18. Calcium-sensing receptors promoted Homer1 expression and osteogenic differentiation in bone marrow mesenchymal stem cells
  19. ABI3BP can inhibit the proliferation, invasion, and epithelial–mesenchymal transition of non-small-cell lung cancer cells
  20. Changes in blood glucose and metabolism in hyperuricemia mice
  21. Rapid detection of the GJB2 c.235delC mutation based on CRISPR-Cas13a combined with lateral flow dipstick
  22. IL-11 promotes Ang II-induced autophagy inhibition and mitochondrial dysfunction in atrial fibroblasts
  23. Short-chain fatty acid attenuates intestinal inflammation by regulation of gut microbial composition in antibiotic-associated diarrhea
  24. Application of metagenomic next-generation sequencing in the diagnosis of pathogens in patients with diabetes complicated by community-acquired pneumonia
  25. NAT10 promotes radiotherapy resistance in non-small cell lung cancer by regulating KPNB1-mediated PD-L1 nuclear translocation
  26. Phytol-mixed micelles alleviate dexamethasone-induced osteoporosis in zebrafish: Activation of the MMP3–OPN–MAPK pathway-mediating bone remodeling
  27. Association between TGF-β1 and β-catenin expression in the vaginal wall of patients with pelvic organ prolapse
  28. Primary pleomorphic liposarcoma involving bilateral ovaries: Case report and literature review
  29. Effects of de novo donor-specific Class I and II antibodies on graft outcomes after liver transplantation: A pilot cohort study
  30. Sleep architecture in Alzheimer’s disease continuum: The deep sleep question
  31. Ephedra fragilis plant extract: A groundbreaking corrosion inhibitor for mild steel in acidic environments – electrochemical, EDX, DFT, and Monte Carlo studies
  32. Langerhans cell histiocytosis in an adult patient with upper jaw and pulmonary involvement: A case report
  33. Inhibition of mast cell activation by Jaranol-targeted Pirin ameliorates allergic responses in mouse allergic rhinitis
  34. Aeromonas veronii-induced septic arthritis of the hip in a child with acute lymphoblastic leukemia
  35. Clusterin activates the heat shock response via the PI3K/Akt pathway to protect cardiomyocytes from high-temperature-induced apoptosis
  36. Research progress on fecal microbiota transplantation in tumor prevention and treatment
  37. Low-pressure exposure influences the development of HAPE
  38. Stigmasterol alleviates endplate chondrocyte degeneration through inducing mitophagy by enhancing PINK1 mRNA acetylation via the ESR1/NAT10 axis
  39. AKAP12, mediated by transcription factor 21, inhibits cell proliferation, metastasis, and glycolysis in lung squamous cell carcinoma
  40. Association between PAX9 or MSX1 gene polymorphism and tooth agenesis risk: A meta-analysis
  41. A case of bloodstream infection caused by Neisseria gonorrhoeae
  42. Case of nasopharyngeal tuberculosis complicated with cervical lymph node and pulmonary tuberculosis
  43. p-Cymene inhibits pro-fibrotic and inflammatory mediators to prevent hepatic dysfunction
  44. GFPT2 promotes paclitaxel resistance in epithelial ovarian cancer cells via activating NF-κB signaling pathway
  45. Transfer RNA-derived fragment tRF-36 modulates varicose vein progression via human vascular smooth muscle cell Notch signaling
  46. RTA-408 attenuates the hepatic ischemia reperfusion injury in mice possibly by activating the Nrf2/HO-1 signaling pathway
  47. Decreased serum TIMP4 levels in patients with rheumatoid arthritis
  48. Sirt1 protects lupus nephritis by inhibiting the NLRP3 signaling pathway in human glomerular mesangial cells
  49. Sodium butyrate aids brain injury repair in neonatal rats
  50. Interaction of MTHFR polymorphism with PAX1 methylation in cervical cancer
  51. Convallatoxin inhibits proliferation and angiogenesis of glioma cells via regulating JAK/STAT3 pathway
  52. The effect of the PKR inhibitor, 2-aminopurine, on the replication of influenza A virus, and segment 8 mRNA splicing
  53. Effects of Ire1 gene on virulence and pathogenicity of Candida albicans
  54. Small cell lung cancer with small intestinal metastasis: Case report and literature review
  55. GRB14: A prognostic biomarker driving tumor progression in gastric cancer through the PI3K/AKT signaling pathway by interacting with COBLL1
  56. 15-Lipoxygenase-2 deficiency induces foam cell formation that can be restored by salidroside through the inhibition of arachidonic acid effects
  57. FTO alleviated the diabetic nephropathy progression by regulating the N6-methyladenosine levels of DACT1
  58. Clinical relevance of inflammatory markers in the evaluation of severity of ulcerative colitis: A retrospective study
  59. Zinc valproic acid complex promotes osteoblast differentiation and exhibits anti-osteoporotic potential
  60. Primary pulmonary synovial sarcoma in the bronchial cavity: A case report
  61. Metagenomic next-generation sequencing of alveolar lavage fluid improves the detection of pulmonary infection
  62. Uterine tumor resembling ovarian sex cord tumor with extensive rhabdoid differentiation: A case report
  63. Genomic analysis of a novel ST11(PR34365) Clostridioides difficile strain isolated from the human fecal of a CDI patient in Guizhou, China
  64. Effects of tiered cardiac rehabilitation on CRP, TNF-α, and physical endurance in older adults with coronary heart disease
  65. Changes in T-lymphocyte subpopulations in patients with colorectal cancer before and after acupoint catgut embedding acupuncture observation
  66. Modulating the tumor microenvironment: The role of traditional Chinese medicine in improving lung cancer treatment
  67. Alterations of metabolites related to microbiota–gut–brain axis in plasma of colon cancer, esophageal cancer, stomach cancer, and lung cancer patients
  68. Research on individualized drug sensitivity detection technology based on bio-3D printing technology for precision treatment of gastrointestinal stromal tumors
  69. CEBPB promotes ulcerative colitis-associated colorectal cancer by stimulating tumor growth and activating the NF-κB/STAT3 signaling pathway
  70. Oncolytic bacteria: A revolutionary approach to cancer therapy
  71. A de novo meningioma with rapid growth: A possible malignancy imposter?
  72. Diagnosis of secondary tuberculosis infection in an asymptomatic elderly with cancer using next-generation sequencing: Case report
  73. Hesperidin and its zinc(ii) complex enhance osteoblast differentiation and bone formation: In vitro and in vivo evaluations
  74. Research progress on the regulation of autophagy in cardiovascular diseases by chemokines
  75. Anti-arthritic, immunomodulatory, and inflammatory regulation by the benzimidazole derivative BMZ-AD: Insights from an FCA-induced rat model
  76. Immunoassay for pyruvate kinase M1/2 as an Alzheimer’s biomarker in CSF
  77. The role of HDAC11 in age-related hearing loss: Mechanisms and therapeutic implications
  78. Evaluation and application analysis of animal models of PIPNP based on data mining
  79. Therapeutic approaches for liver fibrosis/cirrhosis by targeting pyroptosis
  80. Fabrication of zinc oxide nanoparticles using Ruellia tuberosa leaf extract induces apoptosis through P53 and STAT3 signalling pathways in prostate cancer cells
  81. Haplo-hematopoietic stem cell transplantation and immunoradiotherapy for severe aplastic anemia complicated with nasopharyngeal carcinoma: A case report
  82. Modulation of the KEAP1-NRF2 pathway by Erianin: A novel approach to reduce psoriasiform inflammation and inflammatory signaling
  83. The expression of epidermal growth factor receptor 2 and its relationship with tumor-infiltrating lymphocytes and clinical pathological features in breast cancer patients
  84. Innovations in MALDI-TOF Mass Spectrometry: Bridging modern diagnostics and historical insights
  85. BAP1 complexes with YY1 and RBBP7 and its downstream targets in ccRCC cells
  86. Hypereosinophilic syndrome with elevated IgG4 and T-cell clonality: A report of two cases
  87. Electroacupuncture alleviates sciatic nerve injury in sciatica rats by regulating BDNF and NGF levels, myelin sheath degradation, and autophagy
  88. Polydatin prevents cholesterol gallstone formation by regulating cholesterol metabolism via PPAR-γ signaling
  89. RNF144A and RNF144B: Important molecules for health
  90. Analysis of the detection rate and related factors of thyroid nodules in the healthy population
  91. Artesunate inhibits hepatocellular carcinoma cell migration and invasion through OGA-mediated O-GlcNAcylation of ZEB1
  92. Endovascular management of post-pancreatectomy hemorrhage caused by a hepatic artery pseudoaneurysm: Case report and review of the literature
  93. Efficacy and safety of anti-PD-1/PD-L1 antibodies in patients with relapsed refractory diffuse large B-cell lymphoma: A meta-analysis
  94. SATB2 promotes humeral fracture healing in rats by activating the PI3K/AKT pathway
  95. Overexpression of the ferroptosis-related gene, NFS1, corresponds to gastric cancer growth and tumor immune infiltration
  96. Understanding risk factors and prognosis in diabetic foot ulcers
  97. Atractylenolide I alleviates the experimental allergic response in mice by suppressing TLR4/NF-kB/NLRP3 signalling
  98. FBXO31 inhibits the stemness characteristics of CD147 (+) melanoma stem cells
  99. Immune molecule diagnostics in colorectal cancer: CCL2 and CXCL11
  100. Inhibiting CXCR6 promotes senescence of activated hepatic stellate cells with limited proinflammatory SASP to attenuate hepatic fibrosis
  101. Cadmium toxicity, health risk and its remediation using low-cost biochar adsorbents
  102. Pulmonary cryptococcosis with headache as the first presentation: A case report
  103. Solitary pulmonary metastasis with cystic airspaces in colon cancer: A rare case report
  104. RUNX1 promotes denervation-induced muscle atrophy by activating the JUNB/NF-κB pathway and driving M1 macrophage polarization
  105. Morphometric analysis and immunobiological investigation of Indigofera oblongifolia on the infected lung with Plasmodium chabaudi
  106. The NuA4/TIP60 histone-modifying complex and Hr78 modulate the Lobe2 mutant eye phenotype
  107. Experimental study on salmon demineralized bone matrix loaded with recombinant human bone morphogenetic protein-2: In vitro and in vivo study
  108. A case of IgA nephropathy treated with a combination of telitacicept and half-dose glucocorticoids
  109. Analgesic and toxicological evaluation of cannabidiol-rich Moroccan Cannabis sativa L. (Khardala variety) extract: Evidence from an in vivo and in silico study
  110. Wound healing and signaling pathways
  111. Combination of immunotherapy and whole-brain radiotherapy on prognosis of patients with multiple brain metastases: A retrospective cohort study
  112. To explore the relationship between endometrial hyperemia and polycystic ovary syndrome
  113. Research progress on the impact of curcumin on immune responses in breast cancer
  114. Biogenic Cu/Ni nanotherapeutics from Descurainia sophia (L.) Webb ex Prantl seeds for the treatment of lung cancer
  115. Dapagliflozin attenuates atrial fibrosis via the HMGB1/RAGE pathway in atrial fibrillation rats
  116. Glycitein alleviates inflammation and apoptosis in keratinocytes via ROS-associated PI3K–Akt signalling pathway
  117. ADH5 inhibits proliferation but promotes EMT in non-small cell lung cancer cell through activating Smad2/Smad3
  118. Apoptotic efficacies of AgNPs formulated by Syzygium aromaticum leaf extract on 32D-FLT3-ITD human leukemia cell line with PI3K/AKT/mTOR signaling pathway
  119. Novel cuproptosis-related genes C1QBP and PFKP identified as prognostic and therapeutic targets in lung adenocarcinoma
  120. Ecology and Environmental Science
  121. Optimization and comparative study of Bacillus consortia for cellulolytic potential and cellulase enzyme activity
  122. The complete mitochondrial genome analysis of Haemaphysalis hystricis Supino, 1897 (Ixodida: Ixodidae) and its phylogenetic implications
  123. Epidemiological characteristics and risk factors analysis of multidrug-resistant tuberculosis among tuberculosis population in Huzhou City, Eastern China
  124. Indices of human impacts on landscapes: How do they reflect the proportions of natural habitats?
  125. Genetic analysis of the Siberian flying squirrel population in the northern Changbai Mountains, Northeast China: Insights into population status and conservation
  126. Diversity and environmental drivers of Suillus communities in Pinus sylvestris var. mongolica forests of Inner Mongolia
  127. Global assessment of the fate of nitrogen deposition in forest ecosystems: Insights from 15N tracer studies
  128. Fungal and bacterial pathogenic co-infections mainly lead to the assembly of microbial community in tobacco stems
  129. Agriculture
  130. Integrated analysis of transcriptome, sRNAome, and degradome involved in the drought-response of maize Zhengdan958
  131. Variation in flower frost tolerance among seven apple cultivars and transcriptome response patterns in two contrastingly frost-tolerant selected cultivars
  132. Heritability of durable resistance to stripe rust in bread wheat (Triticum aestivum L.)
  133. Animal Science
  134. Effect of sex ratio on the life history traits of an important invasive species, Spodoptera frugiperda
  135. Plant Sciences
  136. Hairpin in a haystack: In silico identification and characterization of plant-conserved microRNA in Rafflesiaceae
  137. Widely targeted metabolomics of different tissues in Rubus corchorifolius
  138. The complete chloroplast genome of Gerbera piloselloides (L.) Cass., 1820 (Carduoideae, Asteraceae) and its phylogenetic analysis
  139. Field trial to correlate mineral solubilization activity of Pseudomonas aeruginosa and biochemical content of groundnut plants
  140. Correlation analysis between semen routine parameters and sperm DNA fragmentation index in patients with semen non-liquefaction: A retrospective study
  141. Plasticity of the anatomical traits of Rhododendron L. (Ericaceae) leaves and its implications in adaptation to the plateau environment
  142. Effects of Piriformospora indica and arbuscular mycorrhizal fungus on growth and physiology of Moringa oleifera under low-temperature stress
  143. Effects of different sources of potassium fertiliser on yield, fruit quality and nutrient absorption in “Harward” kiwifruit (Actinidia deliciosa)
  144. Comparative efficiency and residue levels of spraying programs against powdery mildew in grape varieties
  145. The DREB7 transcription factor enhances salt tolerance in soybean plants under salt stress
  146. Food Science
  147. Phytochemical analysis of Stachys iva: Discovering the optimal extract conditions and its bioactive compounds
  148. Review on role of honey in disease prevention and treatment through modulation of biological activities
  149. Computational analysis of polymorphic residues in maltose and maltotriose transporters of a wild Saccharomyces cerevisiae strain
  150. Optimization of phenolic compound extraction from Tunisian squash by-products: A sustainable approach for antioxidant and antibacterial applications
  151. Liupao tea aqueous extract alleviates dextran sulfate sodium-induced ulcerative colitis in rats by modulating the gut microbiota
  152. Toxicological qualities and detoxification trends of fruit by-products for valorization: A review
  153. Polyphenolic spectrum of cornelian cherry fruits and their health-promoting effect
  154. Optimizing the encapsulation of the refined extract of squash peels for functional food applications: A sustainable approach to reduce food waste
  155. Advancements in curcuminoid formulations: An update on bioavailability enhancement strategies curcuminoid bioavailability and formulations
  156. Impact of saline sprouting on antioxidant properties and bioactive compounds in chia seeds
  157. The dilemma of food genetics and improvement
  158. Bioengineering and Biotechnology
  159. Impact of hyaluronic acid-modified hafnium metalorganic frameworks containing rhynchophylline on Alzheimer’s disease
  160. Emerging patterns in nanoparticle-based therapeutic approaches for rheumatoid arthritis: A comprehensive bibliometric and visual analysis spanning two decades
  161. Application of CRISPR/Cas gene editing for infectious disease control in poultry
  162. Preparation of hafnium nitride-coated titanium implants by magnetron sputtering technology and evaluation of their antibacterial properties and biocompatibility
  163. Preparation and characterization of lemongrass oil nanoemulsion: Antimicrobial, antibiofilm, antioxidant, and anticancer activities
  164. Corrigendum
  165. Corrigendum to “Utilization of convolutional neural networks to analyze microscopic images for high-throughput screening of mesenchymal stem cells”
  166. Corrigendum to “Effects of Ire1 gene on virulence and pathogenicity of Candida albicans”
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