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Tanshinone IIA alleviates chondrocyte apoptosis and extracellular matrix degeneration by inhibiting ferroptosis

  • Jin Xu , Xiaocheng Zhi , Yunhui Zhang and Ren Ding EMAIL logo
Published/Copyright: August 7, 2023
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Open Life Sciences
From the journal Open Life Sciences Volume 18 Issue 1

Abstract

Articular cartilage degeneration caused by chondrocyte damage is the primary pathological mechanism of osteoarthritis (OA). Oxidative stress is correlated with chondrocyte injury by potentiating ferroptosis, a newly identified form of cell death. Given the effects of Tanshinone IIA (Tan IIA) on alleviating oxidative stress, we further explored whether Tan IIA inhibited chondrocyte death and cartilage degeneration by decreasing ferroptosis. ATDC5 chondrocytes were treated with lipopolysaccharides (LPS) and Tan IIA, and cell viability was assessed using cell counting kit-8 (CCK-8) assays. Matrix metalloproteinase-13 (MMP13), a disintegrin and metalloproteinase with thrombospondin motif-5 (ADAMTS5), and type II collagen (Col II) levels were measured using quantitative real-time polymerase chain reaction (qRT‒PCR), western blotting, and immunofluorescence (IF) analysis. We demonstrated that Tan IIA treatment prominently increased ATDC5 cell viability and decreased cell apoptosis in the presence of LPS-induced stress. MMP13 and ADAMTS5 expression was increased, and Col II expression was decreased in ATDC5 cells after LPS stimulation, whereas these changes were reversed by Tan IIA. Mechanistically, Tan IIA inhibited LPS-induced ferroptosis in ATDC5 cells, as indicated by decreased levels of iron, reactive oxygen species, and malondialdehyde and increased GSH levels. Importantly, a ferroptosis agonist partially abrogated the effect of Tan IIA on alleviating chondrocyte damage and death. Taken together, these results suggest that Tan IIA ameliorates chondrocyte apoptosis and cartilage degeneration by inhibiting ferroptosis and may be a potential therapeutic agent for OA.

Graphical abstract

Keywords: osteoarthritis; chondrocytes; oxidative stress; ferroptosis; Tanshinone IIA

1 Introduction

Osteoarthritis (OA) is a frequent degenerative joint disorder worldwide that is characterized by intraarticular inflammation, cartilage degeneration, and architectural alterations in subchondral bone [1,2]. Ageing and obesity are the two major risk factors for OA in addition to genetic factors [3]. Chondrocytes, which originate from mesenchymal stem cells, are resident cells in articular cartilage that are responsible for extracellular matrix (ECM) generation [4,5,6]. Inflammatory factors, such as lipopolysaccharide (LPS) or IL-1β, accelerate chondrocyte apoptosis and subsequent cartilage degeneration by increasing the generation of proinflammatory factors and matrix metalloproteinases [7,8].

Medical intervention is necessary for OA patients because of the limited self-healing capacity of chondrocytes after injury [9]. Nonsteroidal anti-inflammatory agents and opioids are effective in alleviating inflammation and pain in OA patients, but their side effects limit their clinical application [10]. Several active components extracted from plants exert protective effects against chondrocyte injury because of their antioxidant and anti-inflammatory properties. Ellagic acid, a natural polyphenol in fruits or nuts, alleviates oxidative stress and chondrocyte injury by activating nuclear factor erythroid 2-related factor 2 (Nrf2) signalling [11]. Quercetin, a kaempferol isolated from lotus leaves, exerts a protective effect on joints and IL-1β-induced chondrocyte injury by regulating autophagy [12].

Tanshinone IIA (Tan IIA), a lipophilic component of Salvia miltiorrhiza, exerts protective effects against tissue inflammation and fibrosis [13]. Tan IIA mitigates LPS-induced brain injury by inhibiting oxidative stress and the inflammatory response [14]. Tan IIA ameliorates sepsis-induced lung damage by inhibiting NF-κB signalling activation in pulmonary epithelial cells [15]. Recent studies have also revealed the biological role of Tan IIA in regulating the inflammatory response and chondrocyte injury in OA. Tan IIA contributes to cartilage regeneration and exerts a protective effect against chondrocyte dedifferentiation [16]. Tan IIA treatment alleviates LPS-induced inflammation and chondrocyte apoptosis by inhibiting forkhead box O-3 (FOXO3) expression [17].

Ferroptosis is a recently identified form of cell death that is triggered by iron-dependent lipid peroxidation [18,19]. Lipid peroxidation caused by glutathione exhaustion or glutathione peroxidase 4 (GPX4) inactivation is a typical characteristic of cell ferroptosis [20]. Given the antioxidant effect of Tan IIA and that oxidative stress is associated with chondrocyte injury by potentiating ferroptosis [21], our aim was to investigate whether Tan IIA can alleviate chondrocyte injury by regulating ferroptosis.

2 Materials and methods

2.1 Cell culture and treatment

The mouse chondrocyte cell line ATDC5 was obtained from the Cell Bank of RIKEN BioResource Center (Tsukuba, Japan) and cultured in DMEM (Invitrogen, CA, USA) containing 10% FBS in a 5% CO2 incubator. Prior to functional experiments, 10 µg/mL recombinant insulin (Merck, MA, USA) was used to treat ATDC5 cells to induce chondrogenesis, as previously described [22]. ATDC5 cells were treated with LPS (5 µg/mL) and Tan IIA (0, 10, 20, 40, 100, or 200 µM) or erastin (10 µM) for 48 h, and then, cell viability, apoptosis, and cartilage degeneration were assessed.

2.2 CCK8 assay

ATDC5 cells were seeded in 96-well plates (2 × 103 cells/well) and treated with LPS and Tan IIA (or erastin) for 48 h. Subsequently, 10 µL of CCK-8 was added to each well for 1 h at 37°C. The absorbance was measured at 450 nm with a microplate reader (Molecular Device, CA, USA).

2.3 Terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL) assay

TUNEL staining was used to measure cell apoptosis. Briefly, after being treated with LPS and Tan IIA (or erastin) for 48 h, ATDC5 cells were fixed with 4% PFA (Solarbio, Shanghai, China) for 20 min and stained with TUNEL reagent (Solarbio) according to the manufacturer’s suggestions. The apoptotic cells were dyed with TUNEL and observed with a fluorescence microscope (Leica, Wetzlar, Germany).

2.4 qRT‒PCR

Total RNA was extracted from ATDC5 cells after treatment with LPS and Tan IIA (or erastin) using TRIzol reagent (Invitrogen), digested with RNA-free DNase I (TaKaRa, Tokyo, Japan), quantitated with a Bioanalyzer 2100 (Agilent, CA, USA), and used to synthesize cDNA with M-MLV and Oligo(dT)16 (TaKaRa). Subsequently, qRT‒PCR was performed in triplicate using a OneStep RT‒PCR kit (QIAGEN, Duesseldorf, Germany) on an Agilent Mx3005P qPCR system (Agilent) under the following conditions: 95°C for 10 min, 38 cycles of 95°C for 15 s and 59°C for 25 s. Gene expression was calculated with the 2−ΔΔCT method [23] after normalization to β-actin. All primers are listed in Table S1.

2.5 Western blotting

Total proteins were extracted from ATDC5 cells after treatment with LPS and Tan IIA (or erastin) with RIPA buffer (Merck), quantified by BCA assays (Abcam, CA, USA), and separated by 12% SDS‒PAGE. After being separated, the proteins were transferred onto PVDF membranes (Merck). Subsequently, the membranes were sealed with 3% BSA, washed three times with TBST, and incubated with primary antibodies against Bax (ab32503, Abcam), Bcl-2 (ab182858, Abcam), MMP13 (ab39012, Abcam), ADAMTS5 (AB41037, Abcam), Col II (ab34712, Abcam), and β-actin (ab8227, Abcam) for 2 h at room temperature. Then, the membranes were washed five times with TBST, incubated with HRP-labelled secondary antibodies against rabbit or mice (Abcam), and visualized with a Novex® ECL reagent (Merck).

2.6 IF Assay

ATDC5 cells were grown on glass slides, fixed with 4% PFA, permeabilized with 0.1% Triton X-100, and sealed with 10% goat serum. After being washed three times with PBS, the cells were treated with primary antibodies against Col II (ab34712) overnight at 4°C and then incubated with Goat Anti-Rabbit IgG H&L (Alexa Fluor® 488) (ab150077) for 1 h in the dark. Cell nuclei were dyed using DAPI (Merck). IF images were captured with a DMI4000B fluorescence microscope (Leica).

2.7 Reactive oxygen species (ROS) assay

ATDC5 Cells were cultured in 24-well plates (0.5 × 104 cells/well) and treated with 5 µg/mL LPS and 40 µM Tan IIA. Forty-eight hours later, the cells were incubated with DCFH-DA (10 μM, Thermo Fisher Scientific) in the dark for 30 min [24]. Images were observed with a DMI4000B fluorescence microscope.

2.8 Iron concentration

ATDC5 Cells were treated with 5 µg/mL LPS and 40 µM Tan IIA for 48 h, and then, the concentration of ferrous iron (Fe2+) was measured using a commercial assay kit (ab83366, Abcam) in accordance with the manufacturer’s suggestions.

2.9 Malondialdehyde (MDA) and glutathione (GSH) assay

ATDC5 Cells were treated with 5 µg/mL LPS and 40 µM Tan IIA for 48 h, and then, MDA and GSH levels were measured with a lipid peroxidation assay kit (ab118970) and a glutathione assay kit (ab65322), respectively, according to the manufacturer’s suggestions and previous studies [25].

2.10 Statistics

All data are presented as the mean ± SD from at least three replicates, and statistical analyses were performed with SPSS 20.0 (IBM, NY, USA) using one-way ANOVA followed by the Scheffé test. A p-value < 0.05 was considered a statistically significant difference.

3 Results

3.1 Tan IIA-alleviated LPS-induced chondrocyte apoptosis

To investigate the role of Tan IIA in regulating chondrocyte viability, its cytotoxic effect was first measured. ATDC5 cells were treated with Tan IIA for 48 h, and cell viability was assessed using the CCK8 assay. Figure 1a shows that no cytotoxic effects were observed in response to Tan IIA at concentrations less than 100 μM. Subsequently, 40 μM Tan IIA was used to treat ATDC5 cells. Tan IIA treatment prominently rescued ATDC5 cell viability, which was repressed by LPS-induced stress (Figure 1b). The TUNEL assay revealed that Tan IIA prominently decreased LPS-induced ATDC5 cell apoptosis (Figure 1c and d). Moreover, there was an obvious increase in Bax protein levels and a decrease in Bcl-2 protein levels in ATDC5 cells in response to LPS-induced stress compared with the control, whereas these effects were blocked by Tan IIA (Figure 1e).

Figure 1 Tan IIA-alleviated LPS-induced chondrocyte apoptosis: (a) ATDC5 cells were treated with different doses of Tan IIA for 48 h, and cell viability was measured using CCK8 assays. (b) ATDC5 cells were treated with LPS in the presence or absence of Tan IIA for 48 h, and cell viability was measured using CCK8 assays. (c and d) ATDC5 cells were treated with LPS in the presence or absence of Tan IIA for 48 h, and cell apoptosis was measured using TUNEL staining. (e) ATDC5 cells were treated with LPS and Tan IIA for 48 h, and Bax and Bcl-2 protein levels were assessed using western blotting.
Figure 1

Tan IIA-alleviated LPS-induced chondrocyte apoptosis: (a) ATDC5 cells were treated with different doses of Tan IIA for 48 h, and cell viability was measured using CCK8 assays. (b) ATDC5 cells were treated with LPS in the presence or absence of Tan IIA for 48 h, and cell viability was measured using CCK8 assays. (c and d) ATDC5 cells were treated with LPS in the presence or absence of Tan IIA for 48 h, and cell apoptosis was measured using TUNEL staining. (e) ATDC5 cells were treated with LPS and Tan IIA for 48 h, and Bax and Bcl-2 protein levels were assessed using western blotting.

3.2 Tan IIA relieved LPS-induced chondrocyte injury

To investigate the effect of Tan IIA on regulating LPS-induced chondrocyte injury, ATDC5 cells were treated with LPS in the presence or absence of Tan IIA, and then, the expression of cartilage-degrading enzymes (MMP13 and ADAMTS5) and Col II was assessed. The qRT‒PCR results revealed that MMP13 and ADAMTS5 mRNA levels were increased, and Col II mRNA levels were decreased in ATDC5 cells after treatment with LPS, whereas Tan IIA effectively suppressed these changes (Figure 2a). Furthermore, western blot analysis revealed similar effects of Tan IIA on regulating MMP13, ADAMTS5, and Col II protein expression in ATDC5 cells (Figure 2b and c). IF Staining also revealed that Col II levels were decreased in ATDC5 cells in response to LPS-induced stress, whereas Tan IIA inhibited these changes (Figure 2d).

Figure 2 Tan IIA alleviated LPS-induced chondrocyte injury: (a) ATDC5 cells were treated with LPS and Tan IIA for 48 h, and MMP13, ADAMTS5, and Col II mRNA levels were assessed by qRT‒PCR. (b and c) ATDC5 cells were treated with LPS and Tan IIA for 48 h, and MMP13, ADAMTS5, and Col II protein levels were assessed by western blotting. (d) IF analysis of Col II in ATDC5 cells after treatment with LPS in the presence or absence of Tan IIA for 48 h.
Figure 2

Tan IIA alleviated LPS-induced chondrocyte injury: (a) ATDC5 cells were treated with LPS and Tan IIA for 48 h, and MMP13, ADAMTS5, and Col II mRNA levels were assessed by qRT‒PCR. (b and c) ATDC5 cells were treated with LPS and Tan IIA for 48 h, and MMP13, ADAMTS5, and Col II protein levels were assessed by western blotting. (d) IF analysis of Col II in ATDC5 cells after treatment with LPS in the presence or absence of Tan IIA for 48 h.

3.3 Tan IIA-inhibited LPS-induced chondrocyte ferroptosis

Given that oxidative stress is correlated with chondrocyte injury by potentiating ferroptosis and that Tan IIA can alleviate oxidative stress, the role of Tan IIA in regulating chondrocyte ferroptosis was next investigated. Figure 3a and b shows that Tan IIA prominently repressed LPS-induced ROS generation in ATDC5 cells. To determine the effect of Tan IIA on ferroptosis, ATDC5 cells were treated with LPS and Tan IIA, and then, ferroptosis markers (iron concentration, MDA level, and GSH content) were measured. Figure 3c shows that MDA levels were increased in ATDC5 cells after LPS treatment, whereas this effect was reversed by Tan IIA. In contrast, Tan IIA increased GSH levels in LPS-treated ATDC5 cells (Figure 3d). More importantly, the iron concentration was elevated in ATDC5 cells after LPS treatment, whereas this change was reversed by Tan IIA (Figure 3e). Tan IIA also restored Gpx4 expression in LPS-treated ATDC5 cells (Figure 3f). These results demonstrate that Tan IIA effectively suppresses LPS-induced ferroptosis.

Figure 3 Tan IIA-inhibited LPS-induced chondrocyte ferroptosis. (a and b) Intracellular ROS levels were assessed in ATDC5 cells after treatment with LPS in the presence or absence of Tan IIA for 48 h. After treatment with LPS in the presence or absence of Tan IIA for 48 h, MDA levels (c), GSH levels (d), and iron concentration (e) were assessed in ATDC5 cells using commercial kits. (f) ATDC5 cells were treated with LPS and Tan IIA for 48 h, and Gpx4 mRNA levels were assessed using qRT‒PCR.
Figure 3

Tan IIA-inhibited LPS-induced chondrocyte ferroptosis. (a and b) Intracellular ROS levels were assessed in ATDC5 cells after treatment with LPS in the presence or absence of Tan IIA for 48 h. After treatment with LPS in the presence or absence of Tan IIA for 48 h, MDA levels (c), GSH levels (d), and iron concentration (e) were assessed in ATDC5 cells using commercial kits. (f) ATDC5 cells were treated with LPS and Tan IIA for 48 h, and Gpx4 mRNA levels were assessed using qRT‒PCR.

3.4 Tan IIA-alleviated chondrocyte injury by inhibiting ferroptosis

Finally, the mediating role of ferroptosis in Tan IIA-regulating chondrocyte viability and injury was investigated. As shown in Figure 4a, although Tan IIA increased ATDC5 cell viability compared with the control in the presence of LPS, erastin (a ferroptosis agonist) treatment significantly abrogated this effect. Moreover, erastin suppressed the Tan IIA-induced decrease in MMP13 and ADAMTS5 levels and increase in Col II levels (Figure 4b), indicating that Tan IIA alleviates chondrocyte injury by repressing ferroptosis.

Figure 4 Tan IIA alleviates chondrocyte injury by inhibiting ferroptosis: (a) ATDC5 cells were treated with Tan IIA and erastin for 48 h under LPS-induced stress, and then, cell viability was measured using CCK8 assays. (b) ATDC5 cells were treated with Tan IIA and erastin for 48 h under LPS-induced stress, and then, the mRNA levels of MMP13, ADAMTS5, and Col II were assessed using qRT‒PCR.
Figure 4

Tan IIA alleviates chondrocyte injury by inhibiting ferroptosis: (a) ATDC5 cells were treated with Tan IIA and erastin for 48 h under LPS-induced stress, and then, cell viability was measured using CCK8 assays. (b) ATDC5 cells were treated with Tan IIA and erastin for 48 h under LPS-induced stress, and then, the mRNA levels of MMP13, ADAMTS5, and Col II were assessed using qRT‒PCR.

4 Discussion

Articular cartilage degeneration caused by chondrocyte injury is a major characteristic of OA, and oxidative stress plays a critical role in chondrocyte injury. Given the biological effect of Tan IIA on alleviating oxidative stress and inflammation, the protective effects of Tan IIA against inflammation-induced oxidative stress and chondrocyte injury were investigated. In this study, we demonstrated that i) Tan IIA mitigated LPS-induced chondrocyte apoptosis; ii) Tan IIA mitigated LPS-induced ECM degeneration; iii) Tan IIA mitigated LPS-induced oxidative stress and ferroptosis in chondrocytes, and iv) Tan IIA mitigated chondrocyte injury by inhibiting ferroptosis. These findings suggest that Tan IIA may be a promising therapeutic agent for treating OA.

ROS are chemically reactive molecules that are constantly produced in mitochondria by the reduction‒oxidation response or electronic excitation [26,27]. ROS generation is crucial for maintaining normal cellular function. Low ROS levels are necessary to sustain redox equilibrium, cell survival, and proliferation [28]. Cell ageing, the immune response, and inflammation are also managed by ROS [29,30,31]. ROS produced during inflammation and ageing contribute to the resorption of articular cartilage [32]. ROS concentrations are finely controlled by antioxidants under physiological conditions [31]. An imbalance in ROS production will result in oxidative stress and have dual effects on cell survival or death [33]. Elevated production of ROS destroys redox homeostasis and subsequently increases pro-death elements (e.g., Bax and Bid) and decreases pro-survival factors (e.g., Bcl-2) [33]. Low antioxidant levels are a hazard factor for OA owing to the overproduction of ROS. Therefore, synthetic and natural antioxidants may alleviate chondrocyte injury by scavenging ROS [32,34,35]. As an anti-inflammatory and antioxidant natural component in crustaceans, algae, and yeast, astaxanthin alleviates chondrocyte injury and slows OA progression by decreasing ROS generation [36]. Echinacoside, a natural phenylethanoid glycoside, increases chondrocyte viability and relieves OA by restraining oxidative stress [37].

Tan IIA is a phenanthrenequinone derivative in Salvia miltiorrhiza Bunge and exerts protective effects against tissue inflammation and fibrosis [13]. Tan IIA alleviates inflammation-induced brain injury by inhibiting oxidant stress and proinflammatory cytokines production [14]. Tan IIA inhibits inflammation-induced chondrocyte apoptosis by inhibiting FOXO3 expression [17]. In the present study, the effects of Tan IIA on regulating chondrocyte survival were further investigated. Tan IIA treatment decreased LPS-induced chondrocyte apoptosis. Tan IIA also relieved LPS-induced ECM degeneration by decreasing ROS generation.

In addition to apoptotic cell death, ROS can trigger ferroptosis in different types of cells [38,39,40], and ferroptosis is correlated with OA progression [40,41]. For example, Deferoxamine mitigates OA by decreasing chondrocyte ferroptosis [21]. Herein, we revealed the role of Tan IIA in inhibiting chondrocyte ferroptosis. In chondrocytes that were treated with LPS, ROS levels, MDA levels, and iron concentration were increased, while GSH levels and Gpx4 expression were decreased, indicating that LPS triggered chondrocyte ferroptosis. More importantly, these changes were reversed by Tan IIA. Furthermore, erastin abrogated the effect of Tan IIA on alleviating LPS-induced chondrocyte injury. The major limitations of this study were that i) the underlying mechanism by which Tan IIA regulates chondrocyte ferroptosis remains unclear, and ii) it is essential to investigate whether Tan IIA regulates other forms of cell death besides ferroptosis.

5 Conclusion

Tan IIA alleviates chondrocyte apoptosis and ECM degeneration by inhibiting ferroptosis.

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  1. Funding information: The study is funded by Shanghai Baoshan District Science and Technology Innovation Special Fund Medical Health Project (No. 20-E-17).

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

  3. 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: 2023-01-31
Revised: 2023-05-08
Accepted: 2023-07-04
Published Online: 2023-08-07

© 2023 the author(s), published by De Gruyter

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

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  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
https://doi.org/10.1515/biol-2022-0666
Keywords for this article
osteoarthritis; chondrocytes; oxidative stress; ferroptosis; Tanshinone IIA
Creative Commons
BY 4.0

Articles in the same Issue

  1. Biomedical Sciences
  2. Systemic investigation of inetetamab in combination with small molecules to treat HER2-overexpressing breast and gastric cancers
  3. Immunosuppressive treatment for idiopathic membranous nephropathy: An updated network meta-analysis
  4. Identifying two pathogenic variants in a patient with pigmented paravenous retinochoroidal atrophy
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  6. A case of pulmonary embolism with bad warfarin anticoagulant effects caused by E. coli infection
  7. Neutrophilia with subclinical Cushing’s disease: A case report and literature review
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  9. Immunoregulation of synovial macrophages for the treatment of osteoarthritis
  10. Novel CPLANE1 c.8948dupT (p.P2984Tfs*7) variant in a child patient with Joubert syndrome
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  13. High glucose and high lipid induced mitochondrial dysfunction in JEG-3 cells through oxidative stress
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  44. The altered expression of cytoskeletal and synaptic remodeling proteins during epilepsy
  45. Effects of pegylated recombinant human granulocyte colony-stimulating factor on lymphocytes and white blood cells of patients with malignant tumor
  46. Prostatitis as initial manifestation of Chlamydia psittaci pneumonia diagnosed by metagenome next-generation sequencing: A case report
  47. NUDT21 relieves sevoflurane-induced neurological damage in rats by down-regulating LIMK2
  48. Association of interleukin-10 rs1800896, rs1800872, and interleukin-6 rs1800795 polymorphisms with squamous cell carcinoma risk: A meta-analysis
  49. Exosomal HBV-DNA for diagnosis and treatment monitoring of chronic hepatitis B
  50. Shear stress leads to the dysfunction of endothelial cells through the Cav-1-mediated KLF2/eNOS/ERK signaling pathway under physiological conditions
  51. Interaction between the PI3K/AKT pathway and mitochondrial autophagy in macrophages and the leukocyte count in rats with LPS-induced pulmonary infection
  52. Meta-analysis of the rs231775 locus polymorphism in the CTLA-4 gene and the susceptibility to Graves’ disease in children
  53. Cloning, subcellular localization and expression of phosphate transporter gene HvPT6 of hulless barley
  54. Coptisine mitigates diabetic nephropathy via repressing the NRLP3 inflammasome
  55. Significant elevated CXCL14 and decreased IL-39 levels in patients with tuberculosis
  56. Whole-exome sequencing applications in prenatal diagnosis of fetal bowel dilatation
  57. Gemella morbillorum infective endocarditis: A case report and literature review
  58. An unusual ectopic thymoma clonal evolution analysis: A case report
  59. Severe cumulative skin toxicity during toripalimab combined with vemurafenib following toripalimab alone
  60. Detection of V. vulnificus septic shock with ARDS using mNGS
  61. Novel rare genetic variants of familial and sporadic pulmonary atresia identified by whole-exome sequencing
  62. The influence and mechanistic action of sperm DNA fragmentation index on the outcomes of assisted reproduction technology
  63. Novel compound heterozygous mutations in TELO2 in an infant with You-Hoover-Fong syndrome: A case report and literature review
  64. ctDNA as a prognostic biomarker in resectable CLM: Systematic review and meta-analysis
  65. Diagnosis of primary amoebic meningoencephalitis by metagenomic next-generation sequencing: A case report
  66. Phylogenetic analysis of promoter regions of human Dolichol kinase (DOLK) and orthologous genes using bioinformatics tools
  67. Collagen changes in rabbit conjunctiva after conjunctival crosslinking
  68. Effects of NM23 transfection of human gastric carcinoma cells in mice
  69. Oral nifedipine and phytosterol, intravenous nicardipine, and oral nifedipine only: Three-arm, retrospective, cohort study for management of severe preeclampsia
  70. Case report of hepatic retiform hemangioendothelioma: A rare tumor treated with ultrasound-guided microwave ablation
  71. Curcumin induces apoptosis in human hepatocellular carcinoma cells by decreasing the expression of STAT3/VEGF/HIF-1α signaling
  72. Rare presentation of double-clonal Waldenström macroglobulinemia with pulmonary embolism: A case report
  73. Giant duplication of the transverse colon in an adult: A case report and literature review
  74. Ectopic thyroid tissue in the breast: A case report
  75. SDR16C5 promotes proliferation and migration and inhibits apoptosis in pancreatic cancer
  76. Vaginal metastasis from breast cancer: A case report
  77. Screening of the best time window for MSC transplantation to treat acute myocardial infarction with SDF-1α antibody-loaded targeted ultrasonic microbubbles: An in vivo study in miniswine
  78. Inhibition of TAZ impairs the migration ability of melanoma cells
  79. Molecular complexity analysis of the diagnosis of Gitelman syndrome in China
  80. Effects of maternal calcium and protein intake on the development and bone metabolism of offspring mice
  81. Identification of winter wheat pests and diseases based on improved convolutional neural network
  82. Ultra-multiplex PCR technique to guide treatment of Aspergillus-infected aortic valve prostheses
  83. Virtual high-throughput screening: Potential inhibitors targeting aminopeptidase N (CD13) and PIKfyve for SARS-CoV-2
  84. Immune checkpoint inhibitors in cancer patients with COVID-19
  85. Utility of methylene blue mixed with autologous blood in preoperative localization of pulmonary nodules and masses
  86. Integrated analysis of the microbiome and transcriptome in stomach adenocarcinoma
  87. Berberine suppressed sarcopenia insulin resistance through SIRT1-mediated mitophagy
  88. DUSP2 inhibits the progression of lupus nephritis in mice by regulating the STAT3 pathway
  89. Lung abscess by Fusobacterium nucleatum and Streptococcus spp. co-infection by mNGS: A case series
  90. Genetic alterations of KRAS and TP53 in intrahepatic cholangiocarcinoma associated with poor prognosis
  91. Granulomatous polyangiitis involving the fourth ventricle: Report of a rare case and a literature review
  92. Studying infant mortality: A demographic analysis based on data mining models
  93. Metaplastic breast carcinoma with osseous differentiation: A report of a rare case and literature review
  94. Protein Z modulates the metastasis of lung adenocarcinoma cells
  95. Inhibition of pyroptosis and apoptosis by capsaicin protects against LPS-induced acute kidney injury through TRPV1/UCP2 axis in vitro
  96. TAK-242, a toll-like receptor 4 antagonist, against brain injury by alleviates autophagy and inflammation in rats
  97. Primary mediastinum Ewing’s sarcoma with pleural effusion: A case report and literature review
  98. Association of ADRB2 gene polymorphisms and intestinal microbiota in Chinese Han adolescents
  99. Tanshinone IIA alleviates chondrocyte apoptosis and extracellular matrix degeneration by inhibiting ferroptosis
  100. Study on the cytokines related to SARS-Cov-2 in testicular cells and the interaction network between cells based on scRNA-seq data
  101. Effect of periostin on bone metabolic and autophagy factors during tooth eruption in mice
  102. HP1 induces ferroptosis of renal tubular epithelial cells through NRF2 pathway in diabetic nephropathy
  103. Intravaginal estrogen management in postmenopausal patients with vaginal squamous intraepithelial lesions along with CO2 laser ablation: A retrospective study
  104. Hepatocellular carcinoma cell differentiation trajectory predicts immunotherapy, potential therapeutic drugs, and prognosis of patients
  105. Effects of physical exercise on biomarkers of oxidative stress in healthy subjects: A meta-analysis of randomized controlled trials
  106. Identification of lysosome-related genes in connection with prognosis and immune cell infiltration for drug candidates in head and neck cancer
  107. Development of an instrument-free and low-cost ELISA dot-blot test to detect antibodies against SARS-CoV-2
  108. Research progress on gas signal molecular therapy for Parkinson’s disease
  109. Adiponectin inhibits TGF-β1-induced skin fibroblast proliferation and phenotype transformation via the p38 MAPK signaling pathway
  110. The G protein-coupled receptor-related gene signatures for predicting prognosis and immunotherapy response in bladder urothelial carcinoma
  111. α-Fetoprotein contributes to the malignant biological properties of AFP-producing gastric cancer
  112. CXCL12/CXCR4/CXCR7 axis in placenta tissues of patients with placenta previa
  113. Association between thyroid stimulating hormone levels and papillary thyroid cancer risk: A meta-analysis
  114. Significance of sTREM-1 and sST2 combined diagnosis for sepsis detection and prognosis prediction
  115. Diagnostic value of serum neuroactive substances in the acute exacerbation of chronic obstructive pulmonary disease complicated with depression
  116. Research progress of AMP-activated protein kinase and cardiac aging
  117. TRIM29 knockdown prevented the colon cancer progression through decreasing the ubiquitination levels of KRT5
  118. Cross-talk between gut microbiota and liver steatosis: Complications and therapeutic target
  119. Metastasis from small cell lung cancer to ovary: A case report
  120. The early diagnosis and pathogenic mechanisms of sepsis-related acute kidney injury
  121. The effect of NK cell therapy on sepsis secondary to lung cancer: A case report
  122. Erianin alleviates collagen-induced arthritis in mice by inhibiting Th17 cell differentiation
  123. Loss of ACOX1 in clear cell renal cell carcinoma and its correlation with clinical features
  124. Signalling pathways in the osteogenic differentiation of periodontal ligament stem cells
  125. Crosstalk between lactic acid and immune regulation and its value in the diagnosis and treatment of liver failure
  126. Clinicopathological features and differential diagnosis of gastric pleomorphic giant cell carcinoma
  127. Traumatic brain injury and rTMS-ERPs: Case report and literature review
  128. Extracellular fibrin promotes non-small cell lung cancer progression through integrin β1/PTEN/AKT signaling
  129. Knockdown of DLK4 inhibits non-small cell lung cancer tumor growth by downregulating CKS2
  130. The co-expression pattern of VEGFR-2 with indicators related to proliferation, apoptosis, and differentiation of anagen hair follicles
  131. Inflammation-related signaling pathways in tendinopathy
  132. CD4+ T cell count in HIV/TB co-infection and co-occurrence with HL: Case report and literature review
  133. Clinical analysis of severe Chlamydia psittaci pneumonia: Case series study
  134. Bioinformatics analysis to identify potential biomarkers for the pulmonary artery hypertension associated with the basement membrane
  135. Influence of MTHFR polymorphism, alone or in combination with smoking and alcohol consumption, on cancer susceptibility
  136. Catharanthus roseus (L.) G. Don counteracts the ampicillin resistance in multiple antibiotic-resistant Staphylococcus aureus by downregulation of PBP2a synthesis
  137. Combination of a bronchogenic cyst in the thoracic spinal canal with chronic myelocytic leukemia
  138. Bacterial lipoprotein plays an important role in the macrophage autophagy and apoptosis induced by Salmonella typhimurium and Staphylococcus aureus
  139. TCL1A+ B cells predict prognosis in triple-negative breast cancer through integrative analysis of single-cell and bulk transcriptomic data
  140. Ezrin promotes esophageal squamous cell carcinoma progression via the Hippo signaling pathway
  141. Ferroptosis: A potential target of macrophages in plaque vulnerability
  142. Predicting pediatric Crohn's disease based on six mRNA-constructed risk signature using comprehensive bioinformatic approaches
  143. Applications of genetic code expansion and photosensitive UAAs in studying membrane proteins
  144. HK2 contributes to the proliferation, migration, and invasion of diffuse large B-cell lymphoma cells by enhancing the ERK1/2 signaling pathway
  145. IL-17 in osteoarthritis: A narrative review
  146. Circadian cycle and neuroinflammation
  147. Probiotic management and inflammatory factors as a novel treatment in cirrhosis: A systematic review and meta-analysis
  148. Hemorrhagic meningioma with pulmonary metastasis: Case report and literature review
  149. SPOP regulates the expression profiles and alternative splicing events in human hepatocytes
  150. Knockdown of SETD5 inhibited glycolysis and tumor growth in gastric cancer cells by down-regulating Akt signaling pathway
  151. PTX3 promotes IVIG resistance-induced endothelial injury in Kawasaki disease by regulating the NF-κB pathway
  152. Pancreatic ectopic thyroid tissue: A case report and analysis of literature
  153. The prognostic impact of body mass index on female breast cancer patients in underdeveloped regions of northern China differs by menopause status and tumor molecular subtype
  154. Report on a case of liver-originating malignant melanoma of unknown primary
  155. Case report: Herbal treatment of neutropenic enterocolitis after chemotherapy for breast cancer
  156. The fibroblast growth factor–Klotho axis at molecular level
  157. Characterization of amiodarone action on currents in hERG-T618 gain-of-function mutations
  158. A case report of diagnosis and dynamic monitoring of Listeria monocytogenes meningitis with NGS
  159. Effect of autologous platelet-rich plasma on new bone formation and viability of a Marburg bone graft
  160. Small breast epithelial mucin as a useful prognostic marker for breast cancer patients
  161. Continuous non-adherent culture promotes transdifferentiation of human adipose-derived stem cells into retinal lineage
  162. Nrf3 alleviates oxidative stress and promotes the survival of colon cancer cells by activating AKT/BCL-2 signal pathway
  163. Favorable response to surufatinib in a patient with necrolytic migratory erythema: A case report
  164. Case report of atypical undernutrition of hypoproteinemia type
  165. Down-regulation of COL1A1 inhibits tumor-associated fibroblast activation and mediates matrix remodeling in the tumor microenvironment of breast cancer
  166. Sarcoma protein kinase inhibition alleviates liver fibrosis by promoting hepatic stellate cells ferroptosis
  167. Research progress of serum eosinophil in chronic obstructive pulmonary disease and asthma
  168. Clinicopathological characteristics of co-existing or mixed colorectal cancer and neuroendocrine tumor: Report of five cases
  169. Role of menopausal hormone therapy in the prevention of postmenopausal osteoporosis
  170. Precisional detection of lymph node metastasis using tFCM in colorectal cancer
  171. Advances in diagnosis and treatment of perimenopausal syndrome
  172. A study of forensic genetics: ITO index distribution and kinship judgment between two individuals
  173. Acute lupus pneumonitis resembling miliary tuberculosis: A case-based review
  174. Plasma levels of CD36 and glutathione as biomarkers for ruptured intracranial aneurysm
  175. Fractalkine modulates pulmonary angiogenesis and tube formation by modulating CX3CR1 and growth factors in PVECs
  176. Novel risk prediction models for deep vein thrombosis after thoracotomy and thoracoscopic lung cancer resections, involving coagulation and immune function
  177. Exploring the diagnostic markers of essential tremor: A study based on machine learning algorithms
  178. Evaluation of effects of small-incision approach treatment on proximal tibia fracture by deep learning algorithm-based magnetic resonance imaging
  179. An online diagnosis method for cancer lesions based on intelligent imaging analysis
  180. Medical imaging in rheumatoid arthritis: A review on deep learning approach
  181. Predictive analytics in smart healthcare for child mortality prediction using a machine learning approach
  182. Utility of neutrophil–lymphocyte ratio and platelet–lymphocyte ratio in predicting acute-on-chronic liver failure survival
  183. A biomedical decision support system for meta-analysis of bilateral upper-limb training in stroke patients with hemiplegia
  184. TNF-α and IL-8 levels are positively correlated with hypobaric hypoxic pulmonary hypertension and pulmonary vascular remodeling in rats
  185. Stochastic gradient descent optimisation for convolutional neural network for medical image segmentation
  186. Comparison of the prognostic value of four different critical illness scores in patients with sepsis-induced coagulopathy
  187. Application and teaching of computer molecular simulation embedded technology and artificial intelligence in drug research and development
  188. Hepatobiliary surgery based on intelligent image segmentation technology
  189. Value of brain injury-related indicators based on neural network in the diagnosis of neonatal hypoxic-ischemic encephalopathy
  190. Analysis of early diagnosis methods for asymmetric dementia in brain MR images based on genetic medical technology
  191. Early diagnosis for the onset of peri-implantitis based on artificial neural network
  192. Clinical significance of the detection of serum IgG4 and IgG4/IgG ratio in patients with thyroid-associated ophthalmopathy
  193. Forecast of pain degree of lumbar disc herniation based on back propagation neural network
  194. SPA-UNet: A liver tumor segmentation network based on fused multi-scale features
  195. Systematic evaluation of clinical efficacy of CYP1B1 gene polymorphism in EGFR mutant non-small cell lung cancer observed by medical image
  196. Rehabilitation effect of intelligent rehabilitation training system on hemiplegic limb spasms after stroke
  197. A novel approach for minimising anti-aliasing effects in EEG data acquisition
  198. ErbB4 promotes M2 activation of macrophages in idiopathic pulmonary fibrosis
  199. Clinical role of CYP1B1 gene polymorphism in prediction of postoperative chemotherapy efficacy in NSCLC based on individualized health model
  200. Lung nodule segmentation via semi-residual multi-resolution neural networks
  201. Evaluation of brain nerve function in ICU patients with Delirium by deep learning algorithm-based resting state MRI
  202. A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis
  203. Markov model combined with MR diffusion tensor imaging for predicting the onset of Alzheimer’s disease
  204. Effectiveness of the treatment of depression associated with cancer and neuroimaging changes in depression-related brain regions in patients treated with the mediator-deuterium acupuncture method
  205. Molecular mechanism of colorectal cancer and screening of molecular markers based on bioinformatics analysis
  206. Monitoring and evaluation of anesthesia depth status data based on neuroscience
  207. Exploring the conformational dynamics and thermodynamics of EGFR S768I and G719X + S768I mutations in non-small cell lung cancer: An in silico approaches
  208. Optimised feature selection-driven convolutional neural network using gray level co-occurrence matrix for detection of cervical cancer
  209. Incidence of different pressure patterns of spinal cerebellar ataxia and analysis of imaging and genetic diagnosis
  210. Pathogenic bacteria and treatment resistance in older cardiovascular disease patients with lung infection and risk prediction model
  211. Adoption value of support vector machine algorithm-based computed tomography imaging in the diagnosis of secondary pulmonary fungal infections in patients with malignant hematological disorders
  212. From slides to insights: Harnessing deep learning for prognostic survival prediction in human colorectal cancer histology
  213. Ecology and Environmental Science
  214. Monitoring of hourly carbon dioxide concentration under different land use types in arid ecosystem
  215. Comparing the differences of prokaryotic microbial community between pit walls and bottom from Chinese liquor revealed by 16S rRNA gene sequencing
  216. Effects of cadmium stress on fruits germination and growth of two herbage species
  217. Bamboo charcoal affects soil properties and bacterial community in tea plantations
  218. Optimization of biogas potential using kinetic models, response surface methodology, and instrumental evidence for biodegradation of tannery fleshings during anaerobic digestion
  219. Understory vegetation diversity patterns of Platycladus orientalis and Pinus elliottii communities in Central and Southern China
  220. Studies on macrofungi diversity and discovery of new species of Abortiporus from Baotianman World Biosphere Reserve
  221. Food Science
  222. Effect of berrycactus fruit (Myrtillocactus geometrizans) on glutamate, glutamine, and GABA levels in the frontal cortex of rats fed with a high-fat diet
  223. Guesstimate of thymoquinone diversity in Nigella sativa L. genotypes and elite varieties collected from Indian states using HPTLC technique
  224. Analysis of bacterial community structure of Fuzhuan tea with different processing techniques
  225. Untargeted metabolomics reveals sour jujube kernel benefiting the nutritional value and flavor of Morchella esculenta
  226. Mycobiota in Slovak wine grapes: A case study from the small Carpathians wine region
  227. Elemental analysis of Fadogia ancylantha leaves used as a nutraceutical in Mashonaland West Province, Zimbabwe
  228. Microbiological transglutaminase: Biotechnological application in the food industry
  229. Influence of solvent-free extraction of fish oil from catfish (Clarias magur) heads using a Taguchi orthogonal array design: A qualitative and quantitative approach
  230. Chromatographic analysis of the chemical composition and anticancer activities of Curcuma longa extract cultivated in Palestine
  231. The potential for the use of leghemoglobin and plant ferritin as sources of iron
  232. Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM
  233. Bioengineering and Biotechnology
  234. Biocompatibility and osteointegration capability of β-TCP manufactured by stereolithography 3D printing: In vitro study
  235. Clinical characteristics and the prognosis of diabetic foot in Tibet: A single center, retrospective study
  236. Agriculture
  237. Biofertilizer and NPSB fertilizer application effects on nodulation and productivity of common bean (Phaseolus vulgaris L.) at Sodo Zuria, Southern Ethiopia
  238. On correlation between canopy vegetation and growth indexes of maize varieties with different nitrogen efficiencies
  239. Exopolysaccharides from Pseudomonas tolaasii inhibit the growth of Pleurotus ostreatus mycelia
  240. A transcriptomic evaluation of the mechanism of programmed cell death of the replaceable bud in Chinese chestnut
  241. Melatonin enhances salt tolerance in sorghum by modulating photosynthetic performance, osmoregulation, antioxidant defense, and ion homeostasis
  242. Effects of plant density on alfalfa (Medicago sativa L.) seed yield in western Heilongjiang areas
  243. Identification of rice leaf diseases and deficiency disorders using a novel DeepBatch technique
  244. Artificial intelligence and internet of things oriented sustainable precision farming: Towards modern agriculture
  245. Animal Sciences
  246. Effect of ketogenic diet on exercise tolerance and transcriptome of gastrocnemius in mice
  247. Combined analysis of mRNA–miRNA from testis tissue in Tibetan sheep with different FecB genotypes
  248. Isolation, identification, and drug resistance of a partially isolated bacterium from the gill of Siniperca chuatsi
  249. Tracking behavioral changes of confined sows from the first mating to the third parity
  250. The sequencing of the key genes and end products in the TLR4 signaling pathway from the kidney of Rana dybowskii exposed to Aeromonas hydrophila
  251. Development of a new candidate vaccine against piglet diarrhea caused by Escherichia coli
  252. Plant Sciences
  253. Crown and diameter structure of pure Pinus massoniana Lamb. forest in Hunan province, China
  254. Genetic evaluation and germplasm identification analysis on ITS2, trnL-F, and psbA-trnH of alfalfa varieties germplasm resources
  255. Tissue culture and rapid propagation technology for Gentiana rhodantha
  256. Effects of cadmium on the synthesis of active ingredients in Salvia miltiorrhiza
  257. Cloning and expression analysis of VrNAC13 gene in mung bean
  258. Chlorate-induced molecular floral transition revealed by transcriptomes
  259. Effects of warming and drought on growth and development of soybean in Hailun region
  260. Effects of different light conditions on transient expression and biomass in Nicotiana benthamiana leaves
  261. Comparative analysis of the rhizosphere microbiome and medicinally active ingredients of Atractylodes lancea from different geographical origins
  262. Distinguish Dianthus species or varieties based on chloroplast genomes
  263. Comparative transcriptomes reveal molecular mechanisms of apple blossoms of different tolerance genotypes to chilling injury
  264. Study on fresh processing key technology and quality influence of Cut Ophiopogonis Radix based on multi-index evaluation
  265. An advanced approach for fig leaf disease detection and classification: Leveraging image processing and enhanced support vector machine methodology
  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
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