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Knockdown of Stanniocalcin-1 inhibits growth and glycolysis in oral squamous cell carcinoma cells

  • Chanyuan Wang , Jianpei Hu EMAIL logo and Lijian Wang
Published/Copyright: July 24, 2024
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Open Life Sciences
From the journal Open Life Sciences Volume 19 Issue 1

Abstract

Oral squamous cell carcinoma (OSCC) is the most common malignancy among head and neck squamous cell carcinomas. Targeted therapy plays a crucial role in the treatment of OSCC. However, new and more targets are still needed to develop. Stanniocalcin-1 (STC-1) is a glycoprotein hormone that affects the progression of cancers. However, the potential role of STC-1 in OSCC progression remains to be explored. Here, we aimed to elucidate the role of STC-1 in OSCC. We revealed that STC-1 was highly expressed in OSCC tissues and is correlated with poor patient prognosis. Knockdown of STC-1 significantly suppressed the growth of OSCC cells and restrained glycolysis by reducing glucose consumption, ATP production, and lactate levels. Mechanistically, STC-1 ablation inhibited the PI3K/Akt pathway, reducing the phosphorylation levels of PI3K and Akt. In conclusion, STC-1 depletion restrained OSCC cell growth and glycolysis via PI3K/Akt pathway and has the potential to serve as a therapeutic target for OSCC.

Keywords: oral squamous cell carcinoma; Stanniocalcin-1; growth; glycolysis; PI3K/Akt pathway

1 Introduction

Oral squamous cell carcinoma (OSCC) is the most common type of malignancy in head and neck squamous cell cancer [1]. Despite extensive research efforts to identify pathogenic factors and develop new treatments, the overall prognosis remains poor [2]. The occurrence of metastasis is a major factor contributing to poor survival in patients with OSCC and has become a prominent research focus in studies investigating possible potential treatments for OSCC [3]. Targeted therapy plays a crucial role in the treatment of OSCC by targeting specific molecular markers or signaling pathways to inhibit tumor growth and spread. For example, targeted drugs against the EGFR, such as Erlotinib and Cetuximab, have been used in the treatment of OSCC and have shown some efficacy [4,5]. However, new and more targets are still needed to develop.

Tumor cells primarily rely on oxidative phosphorylation for energy, but their growth is predominantly fueled by glycolysis, a process known as aerobic glycolysis, which is a fundamental biochemical characteristic of cancer cells [6,7]. Targeting cancer cell glycolysis is considered a promising approach for therapeutic interventions [6,7]. The PI3K/Akt pathway is vital in various cellular functions such as movement, autophagy, and cancer progression, and it is also critical in regulating metabolic adaptations that support cell growth [8]. Akt is considered a significant driver of the glycolytic phenotype in tumor cells, making them dependent on glycolysis for survival [9]. Akt enhances glucose uptake and glycolysis by increasing the expression of GLUT1, activating glycolytic enzymes, and regulating the expression, activity, as well as the interaction of HK with mitochondria [9].

Stanniocalcin-1 (STC-1) is a glycoprotein hormone implicated in the progression of various cancers [10]. STC-1 expression has been found during many developmental and pathophysiological processes in mammals [11,12]. Recent studies have shown that STC-1 promotes tumor angiogenesis, glycolysis, and metastasis in several malignancies, including breast, lung, and gastric cancers. Knockdown of STC-1 inhibits glycolysis in prostate cancer [13,14]. STC-1 promotes tumor angiogenesis by upregulating VEGF in gastric cancer cells [15]. Knockdown of STC-1 inhibits glycolysis in prostate cancer [16]. STC-1 enhances the stem-like characteristics of glioblastoma cells by binding to and activating NOTCH1 [17]. However, the potential role of STC-1 in OSCC progression remains to be explored.

In this study, we aimed to elucidate the role of STC-1 in OSCC and explore the therapeutic potential of targeting STC-1 in OSCC treatment. We found that STC1 is highly expressed in oral squamous cell cancer cells, and STC1 knockdown can inhibit OSCC cell growth and glycolysis, which is related to the regulation of the PI3K/Akt pathway.

2 Materials and methods

2.1 Bioinformatics

Transcriptome data for STC-1 in OSCC were obtained from The Cancer Genome Atlas (TCGA) database using the Genomic Data Commons Data Portal. Differential expression analysis was conducted between normal oral tissues (n = 40) and OSCC tissues (n = 520) using DESeq2 software. Statistical significance was evaluated using an adjusted p-value threshold of <0.05. Survival analysis was performed using data from the UALCAN database (https://ualcan.path.uab.edu/), where patients were categorized into high and low STC-1 expression groups based on median STC-1 expression levels. Kaplan–Meier survival curves were generated, and the log-rank test was used to determine significance (p < 0.05).

2.2 Cell culture and transfection

Human OSCC cell lines, including HSC-3 and CAL-27, and normal oral keratinocyte cell line HOK were purchased from ATCC. HOK, HSC-3, and CAL-27 cells were cultured with the DMEM (Gibco, USA) containing 10% FBS (Gbico, USA).

For STC-1 knockdown, two types of STC-1 shRNAs (sh-STC-1#1 and sh-STC-1#2) were constructed by our lab and cloned into a plasmid vector obtained from Addgene (USA). HSC-3 and CAL-27 cells were transfected with shRNA constructs using Lipofectamine 2000 (Invitrogen, USA) according to the manufacturer’s instructions. Control cells were transfected with a scrambled shRNA (sh-NC).

2.3 Immunoblotting

Samples were separated by sodiumdodecyl sulphate-polyacrylamide gel electrophoresis and transferred to polyvinylidene fluoride membranes. The membranes were blocked with 5% milk for 2 h, and then, the primary antibodies were added. Primary antibodies including anti-STC-1 (Abcam, ab2910; 1:1,000), HK2 (Abcam, ab209847; 1:1,000), LDHA (Abcam, ab52488; 1:500), Akt (Abcam, ab8805; 1:1,000), p-Akt (Abcam, ab38449; 1:500), PI3K (Abcam, ab302958; 1:1,000), p-PI3K (Abcam, ab278545; 1:500), and β-actin (Abcam, ab8226; 1:3,000, Cambridge, UK) antibodies and incubated with membranes for overnight at 4°C. Then, the membranes were incubated with secondary antibodies 1 h at room temperature. Protein expression was quantified using ImageJ software.

2.4 Cell counting kit-8 (CCK-8) assay

HSC-3 and CAL-27 cells were plated and maintained for 24, 48, and 72 h. Cells were subsequently incubated with CCK-8 (C0038, Beyotime, China). Then, the OD450 value was detected.

2.5 Edu assay

HSC-3 and CAL-27 cells were incubated with Edu agent (Abcam) for 2 h and removed the agent, then photographed by a microscope (Zeiss, German). Edu-positive cells were photographed using a fluorescence microscope (Zeiss, Germany) and quantified as a percentage of total cells.

2.6 Glucose intake, lactate, and ATP production test

The glycolysis levels of cells were detected using the kits including glucose intake (ab136955), lactate production (ab65330), and cellular ATP levels (ab83355; Abcam, Cambridge, UK).

2.7 Statistics

GraphPad 8.0 software was used and performed. Data were represented as mean ± standard deviation. p < 0.05 was thought as significant. Statistical significance was evaluated using Student’s t-test or analysis of variance, and p < 0.05 was considered statistically significant.

3 Results

3.1 STC-1 was highly expressed in human OSCC tissues and cells

To detect the role of STC-1 in OSCC, we first detected its expression in OSCC tissues. Interestingly, we noticed the low transcripts per million (TPM) value of STC-1 in OSCC tissues (Figure 1a). Further through the Ualcan database, we noticed that the expression of STC-1 was correlated with the poor prognosis (survival) of patients with OSCC (p = 0.02, Figure 1b). Subsequently, we detected the expression of STC-1 in OSCC cell lines, including HSC-3 and CAL-27 cells, and normal oral keratinocyte cell line HOK cells. Through quantitative polymerase chain reaction (qPCR) assays, we revealed the high mRNA levels of STC-1 in OSCC cell lines (Figure 1c). Similarly, immunoblot assays confirmed that STC-1 was upregulated in HSC-3 and CAL-27 cells compared to HOK cells (Figure 1d). Therefore, STC-1 was highly expressed in OSCC tissues and cells.

Figure 1 STC-1 was highly expressed in human OSCC tissues and cells. (a) TCGA database showed the TPM of STC-1 in 40 normal tissues and 520 OSCC tissues. (b) Ualcan database showed the correlation between STC-1 expression and the survival of OSCC patients (p = 0.02). (c) qPCR assays showed the mRNA levels of STC-1 in HOK, HSC-3, and CAL-27 cell lines. (d) Immunoblot assays showed the expression of STC-1 in HOK, HSC-3, and CAL-27 cell lines. **p < 0.01, ***p < 0.001, HSC3/CAL-27 vs HOK.
Figure 1

STC-1 was highly expressed in human OSCC tissues and cells. (a) TCGA database showed the TPM of STC-1 in 40 normal tissues and 520 OSCC tissues. (b) Ualcan database showed the correlation between STC-1 expression and the survival of OSCC patients (p = 0.02). (c) qPCR assays showed the mRNA levels of STC-1 in HOK, HSC-3, and CAL-27 cell lines. (d) Immunoblot assays showed the expression of STC-1 in HOK, HSC-3, and CAL-27 cell lines. **p < 0.01, ***p < 0.001, HSC3/CAL-27 vs HOK.

3.2 The depletion of STC-1 suppressed the growth of OSCC cells

We next used shRNAs to confirm the role of STC-1 in OSCC cells including HSC-3 and CAL-27 cells and the growth of OSCC cells. STC-1 was downregulated in these cells by the transfection of STC-1 shRNAs, including sh-STC-1#1 and sh-STC-1#2. Through Immunoblot assays, we noticed that the expression of STC-1 was significantly decreased upon the transfection of these shRNAs (Figure 2a). Interestingly, CCK-8 assays confirmed that the downregulation of STC-1 restrained the growth of HSC-3 and CAL-27 cells, with the decreased OD450 value at 1, 2, and 3 days (Figure 2b). Consistently, Edu assays showed that the percentage of Edu-positive cells was decreased upon the knockdown of STC-1 in HSC-3 and CAL-27 cells, suggesting the suppression of cell growth (Figure 2c). Collectively, STC-1 knockdown suppressed the growth of OSCC cells.

Figure 2 The depletion of STC-1 suppressed the growth of OSCC cells. (a) Immunoblot assays showed the expression of STC-1 in HSC3 (up) and CAL27 (down) cells upon the transfection of sh-NC, sh-STC-1#1, and sh-STC-1#2 for 24 h. The relative STC-1 expression was quantified. (b) CCK-8 assays showed the growth of HSC-3, and CAL-27 cells upon the transfection of sh-NC, sh-STC-1#1, and sh-STC-1#2 for 24, 48, and 72 h. OD450 value was measured. (c) Edu assays showed the growth degree of HSC-3, and CAL-27 cells upon the transfection of sh-NC, sh-STC-1#1, and sh-STC-1#2 for 24 h. The percentage of Edu-positive cells was quantified. Scale bar, 100 μm. Red panel indicates Edu. *p < 0.05, **p < 0.01, ***p < 0.001, sh-STC-1 vs sh-NC. NC, negative control.
Figure 2

The depletion of STC-1 suppressed the growth of OSCC cells. (a) Immunoblot assays showed the expression of STC-1 in HSC3 (up) and CAL27 (down) cells upon the transfection of sh-NC, sh-STC-1#1, and sh-STC-1#2 for 24 h. The relative STC-1 expression was quantified. (b) CCK-8 assays showed the growth of HSC-3, and CAL-27 cells upon the transfection of sh-NC, sh-STC-1#1, and sh-STC-1#2 for 24, 48, and 72 h. OD450 value was measured. (c) Edu assays showed the growth degree of HSC-3, and CAL-27 cells upon the transfection of sh-NC, sh-STC-1#1, and sh-STC-1#2 for 24 h. The percentage of Edu-positive cells was quantified. Scale bar, 100 μm. Red panel indicates Edu. *p < 0.05, **p < 0.01, ***p < 0.001, sh-STC-1 vs sh-NC. NC, negative control.

3.3 STC-1 ablation restrained the glycolysis of OSCC cells

Then, we detected the effects of STC-1 in HSC-3 and CAL-27 cells on the cell glycolysis. By the use of the glucose consumption kits, we noticed that knockdown of STC-1 suppressed the glucose consumption in HSC-3 and CAL-27 cells (Figure 3a). Furthermore, we noticed that STC-1 knockdown suppressed the production of ATP levels in these OSCC cells (Figure 3b). Our results further confirmed that the lactate production was suppressed upon STC-1 knockdown in HSC-3 and CAL-27 cells (Figure 3c). Consistently, we performed the Immunoblot assays, and the data confirmed that STC-1 knockdown restrained the expression of HK2 and LDHA, two markers of glycolysis, in OSCC cells (Figure 3d). Therefore, STC-1 knockdown restrained the glycolysis of OSCC cells.

Figure 3 STC-1 ablation restrained the glycolysis of OSCC cells. (a) The relative glucose consumption of HSC-3, and CAL-27 cells upon the transfection of sh-NC, sh-STC-1#1, and sh-STC-1#2 for 24 h was measured. (b) The ATP levels of HSC-3, and CAL-27 cells upon the transfection of sh-NC, sh-STC-1#1, and sh-STC-1#2 for 24 h was measured by the ATP detection kit. (c) The relative Lactate production of HSC-3, and CAL-27 cells upon the transfection of sh-NC, sh-STC-1#1, and sh-STC-1#2 for 24 h was measured by the kit. (d) Immunoblot showed the expression of HK2 and LDHA in HSC-3 and CAL-27 cells upon the transfection of sh-NC, sh-STC-1#1, and sh-STC-1#2 for 24 h. *p < 0.05, **p < 0.01, ***p < 0.001, sh-STC-1 vs sh-NC. NC, negative control.
Figure 3

STC-1 ablation restrained the glycolysis of OSCC cells. (a) The relative glucose consumption of HSC-3, and CAL-27 cells upon the transfection of sh-NC, sh-STC-1#1, and sh-STC-1#2 for 24 h was measured. (b) The ATP levels of HSC-3, and CAL-27 cells upon the transfection of sh-NC, sh-STC-1#1, and sh-STC-1#2 for 24 h was measured by the ATP detection kit. (c) The relative Lactate production of HSC-3, and CAL-27 cells upon the transfection of sh-NC, sh-STC-1#1, and sh-STC-1#2 for 24 h was measured by the kit. (d) Immunoblot showed the expression of HK2 and LDHA in HSC-3 and CAL-27 cells upon the transfection of sh-NC, sh-STC-1#1, and sh-STC-1#2 for 24 h. *p < 0.05, **p < 0.01, ***p < 0.001, sh-STC-1 vs sh-NC. NC, negative control.

3.4 STC-1 knockdown suppressed the PI3K/Akt pathway in OSCC cells

Finally, the possible mechanism underlying STC-1 knockdown suppressing OSCC progression was investigated. Through Immunoblot, we detected the phosphorylation levels of PI3K and Akt in both HSC-3 and CAL-27 cells. Interestingly, we noticed that STC-1 ablation suppressed the phosphorylation of both PI3K and Akt in HSC-3 and CAL-27 cells, suggesting the suppression of the PI3K/Akt pathway (Figure 4). Therefore, we believe that STC-1 knockdown suppressed the PI3K/Akt pathway in OSCC cells.

Figure 4 STC-1 knockdown suppressed the PI3K/Akt pathway in OSCC cells. Immunoblot showed the expression and phosphorylation levels of PI3K and Akt in HSC-3, and CAL-27 cells upon the transfection of sh-NC, sh-STC-1#1, and sh-STC-1#2 for 24 h was measured by the kit. The relative phosphorylation levels were quantified. *p < 0.05, **p < 0.01, ***p < 0.001, sh-STC-1 vs sh-NC. NC, negative control.
Figure 4

STC-1 knockdown suppressed the PI3K/Akt pathway in OSCC cells. Immunoblot showed the expression and phosphorylation levels of PI3K and Akt in HSC-3, and CAL-27 cells upon the transfection of sh-NC, sh-STC-1#1, and sh-STC-1#2 for 24 h was measured by the kit. The relative phosphorylation levels were quantified. *p < 0.05, **p < 0.01, ***p < 0.001, sh-STC-1 vs sh-NC. NC, negative control.

4 Discussion

OSCC remains a significant global health challenge due to its high incidence and mortality rates [4]. Current treatments for OSCC include surgery, radiotherapy, and chemotherapy, but the outcomes are often not satisfactory, with a high rate of recurrence and metastasis [1]. There is an urgent need for the development of targeted therapies for OSCC, which require the identification and validation of specific molecular targets [2]. The selection of these targets is crucial for improving therapeutic efficacy, reducing side effects, and improving the overall survival and quality of life of OSCC patients [5]. Key areas of focus include EGFR inhibitors like cetuximab and erlotinib, immunotherapies targeting PD-1/PD-L1 pathways such as pembrolizumab and nivolumab, and exploration of other molecular targets like VEGF, HER2, and the PI3K/AKT/mTOR pathway [18]. Efforts are also underway to personalize treatment based on individual tumor profiles [18]. However, the integration of targeted therapies into standard OSCC treatment protocols is still in the developmental stages and requires further research. Interestingly, we here indicated that STC-1 is highly expressed in OSCC cells, and knocking down STC-1 can inhibit OSCC cell growth and glycolysis. Therefore, we believed that STC-1 has the potential to serve as a promising target of OSCC.

STC-1 is a glycoprotein hormone involved in calcium and phosphate homeostasis, cellular protection against stress, angiogenesis, and inflammation [10,19]. The relationship between STC-1 and cancer has become a focus of research, with elevated expression of STC-1 observed in various cancers, including breast cancer, lung cancer, and ovarian cancer [14,20,21]. Studies have shown that STC-1 may promote tumor growth by activating signaling pathways such as PI3K/Akt and MAPK, facilitate tumor metastasis by affecting the degradation of the extracellular matrix, regulate the tumor microenvironment by promoting angiogenesis, and inhibit tumor cell apoptosis leading to chemotherapy resistance [22,23]. These findings underscore the multifunctional role of STC-1 in tumor biology and highlight the therapeutic potential of targeting STC-1 across various cancers. Strategies targeting STC-1 may help inhibit tumor growth and metastasis and improve chemotherapy efficacy. However, the specific mechanisms of STC-1 in cancer still require further investigation. Herein, our results confirmed that STC-1 ablation inhibited OSCC cell growth and glycolysis. However, the precise mechanism needs further study.

OSCC is closely associated with altered glucose metabolism, particularly an increase in glycolysis, a phenomenon known as the Warburg effect. This metabolic reprogramming is a hallmark of cancer cells, including those in OSCC, and is characterized by a preference for glycolysis over oxidative phosphorylation for energy production, even in the presence of oxygen [24,25]. Interestingly, we confirmed that STC-1 could serve as a key regulator in mediating glycolysis in OSCC cells. We believed that STC-1 may affect OSCC progression via mediating glycolysis.

The PI3K/Akt pathway is a critical regulator of cancer metabolism, and our data confirmed that STC-1 ablation suppresses this pathway in OSCC cells. Previous studies have demonstrated that inhibiting the PI3K/Akt pathway can significantly reduce glycolysis and tumor progression in colorectal cancer and nasopharyngeal carcinoma [26,27]. Activation of this pathway enhances glucose uptake by increasing the translocation of glucose transporters like GLUT1, upregulates key glycolytic enzymes such as hexokinase, phosphofructokinase, and pyruvate kinase, and inhibits apoptosis, allowing for sustained cancer cell proliferation [26]. In addition, Akt regulates HIF-1α, which further enhances glycolysis under hypoxic conditions, and alters the localization of metabolic enzymes like hexokinase to the mitochondria, increasing glycolytic flux [28]. Therefore, targeting the PI3K/Akt pathway is a potential therapeutic strategy to disrupt the altered energy metabolism in cancer cells. Notably, this pathway plays a crucial role in the development of OSCC by influencing cell proliferation, survival, angiogenesis, and metastasis [29]. Its activation is associated with resistance to conventional therapies, making it a potential target for therapeutic intervention. Our findings confirmed that STC-1 ablation inhibits the PI3K/Akt pathway, thereby inhibiting OSCC cell growth and glycolysis.

Overall, our findings, combined with those from other studies, highlight the potential of STC-1 as a promising therapeutic target in OSCC and other cancers. Future studies will focus on developing specific inhibitors targeting STC-1 and evaluating their efficacy in clinical settings.

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  1. Funding information: Authors state no funding involved.

  2. Author contributions: Chanyuan Wang and Jianpei Hu – designed the study and carried them out; B Chanyuan Wang, Jianpei Hu, and Lijian Wang – supervised the data collection, analyzed the data, and interpreted the data; and Chanyuan Wang and Jianpei Hu – prepared the manuscript for publication and reviewed the draft of the manuscript. All authors have read and approved the manuscript.

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

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

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Received: 2024-02-26
Revised: 2024-05-13
Accepted: 2024-06-03
Published Online: 2024-07-24

© 2024 the author(s), published by De Gruyter

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

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  27. Helicobacter pylori causes gastric dysbacteriosis in chronic gastritis patients
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  116. Electroacupuncture on GB acupoints improves osteoporosis via the estradiol–PI3K–Akt signaling pathway
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  120. Renal microangiopathy and immune complex glomerulonephritis induced by anti-tumour agents: A case report
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  158. Knockdown of USP7 alleviates atherosclerosis in ApoE-deficient mice by regulating EZH2 expression
  159. Utility of dairy microbiome as a tool for authentication and traceability
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  168. Knockdown of ANP32E inhibits colorectal cancer cell growth and glycolysis by regulating the AKT/mTOR pathway
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  176. Effect of long-term in-row branch covering on soil microorganisms in pear orchards
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  178. Transcriptome analysis reveals the mechanism of NaHCO3 promoting tobacco leaf maturation
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  205. Erratum
  206. Erratum to “Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM”
  207. Erratum to “Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation”
  208. Retraction
  209. Retraction to “MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB”
  210. Retraction to “A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis”
  211. Special Issue on Advances in Neurodegenerative Disease Research and Treatment
  212. Transplantation of human neural stem cell prevents symptomatic motor behavior disability in a rat model of Parkinson’s disease
  213. Special Issue on Multi-omics
  214. Inflammasome complex genes with clinical relevance suggest potential as therapeutic targets for anti-tumor drugs in clear cell renal cell carcinoma
  215. Gastroesophageal varices in primary biliary cholangitis with anti-centromere antibody positivity: Early onset?
https://doi.org/10.1515/biol-2022-0907
Keywords for this article
oral squamous cell carcinoma; Stanniocalcin-1; growth; glycolysis; PI3K/Akt pathway
Creative Commons
BY 4.0

Articles in the same Issue

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  4. PEGylated porcine–human recombinant uricase: A novel fusion protein with improved efficacy and safety for the treatment of hyperuricemia and renal complications
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  18. Current research and evidence gaps on placental development in iron deficiency anemia
  19. Single-nucleotide polymorphism rs2910829 in PDE4D is related to stroke susceptibility in Chinese populations: The results of a meta-analysis
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  23. Apigenin 7-glucoside impedes hypoxia-induced malignant phenotypes of cervical cancer cells in a p16-dependent manner
  24. KAT2A changes the function of endometrial stromal cells via regulating the succinylation of ENO1
  25. Current state of research on copper complexes in the treatment of breast cancer
  26. Exploring antioxidant strategies in the pathogenesis of ALS
  27. Helicobacter pylori causes gastric dysbacteriosis in chronic gastritis patients
  28. IL-33/soluble ST2 axis is associated with radiation-induced cardiac injury
  29. The predictive value of serum NLR, SII, and OPNI for lymph node metastasis in breast cancer patients with internal mammary lymph nodes after thoracoscopic surgery
  30. Carrying SNP rs17506395 (T > G) in TP63 gene and CCR5Δ32 mutation associated with the occurrence of breast cancer in Burkina Faso
  31. P2X7 receptor: A receptor closely linked with sepsis-associated encephalopathy
  32. Probiotics for inflammatory bowel disease: Is there sufficient evidence?
  33. Identification of KDM4C as a gene conferring drug resistance in multiple myeloma
  34. Microbial perspective on the skin–gut axis and atopic dermatitis
  35. Thymosin α1 combined with XELOX improves immune function and reduces serum tumor markers in colorectal cancer patients after radical surgery
  36. Highly specific vaginal microbiome signature for gynecological cancers
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  38. The effects of SDF-1 combined application with VEGF on femoral distraction osteogenesis in rats
  39. Fabrication and characterization of gold nanoparticles using alginate: In vitro and in vivo assessment of its administration effects with swimming exercise on diabetic rats
  40. Mitigating digestive disorders: Action mechanisms of Mediterranean herbal active compounds
  41. Distribution of CYP2D6 and CYP2C19 gene polymorphisms in Han and Uygur populations with breast cancer in Xinjiang, China
  42. VSP-2 attenuates secretion of inflammatory cytokines induced by LPS in BV2 cells by mediating the PPARγ/NF-κB signaling pathway
  43. Factors influencing spontaneous hypothermia after emergency trauma and the construction of a predictive model
  44. Long-term administration of morphine specifically alters the level of protein expression in different brain regions and affects the redox state
  45. Application of metagenomic next-generation sequencing technology in the etiological diagnosis of peritoneal dialysis-associated peritonitis
  46. Clinical diagnosis, prevention, and treatment of neurodyspepsia syndrome using intelligent medicine
  47. Case report: Successful bronchoscopic interventional treatment of endobronchial leiomyomas
  48. Preliminary investigation into the genetic etiology of short stature in children through whole exon sequencing of the core family
  49. Cystic adenomyoma of the uterus: Case report and literature review
  50. Mesoporous silica nanoparticles as a drug delivery mechanism
  51. Dynamic changes in autophagy activity in different degrees of pulmonary fibrosis in mice
  52. Vitamin D deficiency and inflammatory markers in type 2 diabetes: Big data insights
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  54. Meta-analysis on the efficacy of allogeneic hematopoietic stem cell transplantation to treat malignant lymphoma
  55. Mitochondrial DNA drives neuroinflammation through the cGAS-IFN signaling pathway in the spinal cord of neuropathic pain mice
  56. Application value of artificial intelligence algorithm-based magnetic resonance multi-sequence imaging in staging diagnosis of cervical cancer
  57. Embedded monitoring system and teaching of artificial intelligence online drug component recognition
  58. Investigation into the association of FNDC1 and ADAMTS12 gene expression with plumage coloration in Muscovy ducks
  59. Yak meat content in feed and its impact on the growth of rats
  60. A rare case of Richter transformation with breast involvement: A case report and literature review
  61. First report of Nocardia wallacei infection in an immunocompetent patient in Zhejiang province
  62. Rhodococcus equi and Brucella pulmonary mass in immunocompetent: A case report and literature review
  63. Downregulation of RIP3 ameliorates the left ventricular mechanics and function after myocardial infarction via modulating NF-κB/NLRP3 pathway
  64. Evaluation of the role of some non-enzymatic antioxidants among Iraqi patients with non-alcoholic fatty liver disease
  65. The role of Phafin proteins in cell signaling pathways and diseases
  66. Ten-year anemia as initial manifestation of Castleman disease in the abdominal cavity: A case report
  67. Coexistence of hereditary spherocytosis with SPTB P.Trp1150 gene variant and Gilbert syndrome: A case report and literature review
  68. Utilization of convolutional neural networks to analyze microscopic images for high-throughput screening of mesenchymal stem cells
  69. Exploratory evaluation supported by experimental and modeling approaches of Inula viscosa root extract as a potent corrosion inhibitor for mild steel in a 1 M HCl solution
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  71. Gut microbiota and sleep: Interaction mechanisms and therapeutic prospects
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  73. Prognostic value and microenvironmental crosstalk of exosome-related signatures in human epidermal growth factor receptor 2 positive breast cancer
  74. Circular RNAs as potential biomarkers for male severe sepsis
  75. Knockdown of Stanniocalcin-1 inhibits growth and glycolysis in oral squamous cell carcinoma cells
  76. The expression and biological role of complement C1s in esophageal squamous cell carcinoma
  77. A novel GNAS mutation in pseudohypoparathyroidism type 1a with articular flexion deformity: A case report
  78. Predictive value of serum magnesium levels for prognosis in patients with non-small cell lung cancer undergoing EGFR-TKI therapy
  79. HSPB1 alleviates acute-on-chronic liver failure via the P53/Bax pathway
  80. IgG4-related disease complicated by PLA2R-associated membranous nephropathy: A case report
  81. Baculovirus-mediated endostatin and angiostatin activation of autophagy through the AMPK/AKT/mTOR pathway inhibits angiogenesis in hepatocellular carcinoma
  82. Metformin mitigates osteoarthritis progression by modulating the PI3K/AKT/mTOR signaling pathway and enhancing chondrocyte autophagy
  83. Evaluation of the activity of antimicrobial peptides against bacterial vaginosis
  84. Atypical presentation of γ/δ mycosis fungoides with an unusual phenotype and SOCS1 mutation
  85. Analysis of the microecological mechanism of diabetic kidney disease based on the theory of “gut–kidney axis”: A systematic review
  86. Omega-3 fatty acids prevent gestational diabetes mellitus via modulation of lipid metabolism
  87. Refractory hypertension complicated with Turner syndrome: A case report
  88. Interaction of ncRNAs and the PI3K/AKT/mTOR pathway: Implications for osteosarcoma
  89. Association of low attenuation area scores with pulmonary function and clinical prognosis in patients with chronic obstructive pulmonary disease
  90. Long non-coding RNAs in bone formation: Key regulators and therapeutic prospects
  91. The deubiquitinating enzyme USP35 regulates the stability of NRF2 protein
  92. Neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio as potential diagnostic markers for rebleeding in patients with esophagogastric variceal bleeding
  93. G protein-coupled receptor 1 participating in the mechanism of mediating gestational diabetes mellitus by phosphorylating the AKT pathway
  94. LL37-mtDNA regulates viability, apoptosis, inflammation, and autophagy in lipopolysaccharide-treated RLE-6TN cells by targeting Hsp90aa1
  95. The analgesic effect of paeoniflorin: A focused review
  96. Chemical composition’s effect on Solanum nigrum Linn.’s antioxidant capacity and erythrocyte protection: Bioactive components and molecular docking analysis
  97. Knockdown of HCK promotes HREC cell viability and inner blood–retinal barrier integrity by regulating the AMPK signaling pathway
  98. The role of rapamycin in the PINK1/Parkin signaling pathway in mitophagy in podocytes
  99. Laryngeal non-Hodgkin lymphoma: Report of four cases and review of the literature
  100. Clinical value of macrogenome next-generation sequencing on infections
  101. Overview of dendritic cells and related pathways in autoimmune uveitis
  102. TAK-242 alleviates diabetic cardiomyopathy via inhibiting pyroptosis and TLR4/CaMKII/NLRP3 pathway
  103. Hypomethylation in promoters of PGC-1α involved in exercise-driven skeletal muscular alterations in old age
  104. Profile and antimicrobial susceptibility patterns of bacteria isolated from effluents of Kolladiba and Debark hospitals
  105. The expression and clinical significance of syncytin-1 in serum exosomes of hepatocellular carcinoma patients
  106. A histomorphometric study to evaluate the therapeutic effects of biosynthesized silver nanoparticles on the kidneys infected with Plasmodium chabaudi
  107. PGRMC1 and PAQR4 are promising molecular targets for a rare subtype of ovarian cancer
  108. Analysis of MDA, SOD, TAOC, MNCV, SNCV, and TSS scores in patients with diabetes peripheral neuropathy
  109. SLIT3 deficiency promotes non-small cell lung cancer progression by modulating UBE2C/WNT signaling
  110. The relationship between TMCO1 and CALR in the pathological characteristics of prostate cancer and its effect on the metastasis of prostate cancer cells
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  112. PHB2 alleviates retinal pigment epithelium cell fibrosis by suppressing the AGE–RAGE pathway
  113. Anti-γ-aminobutyric acid-B receptor autoimmune encephalitis with syncope as the initial symptom: Case report and literature review
  114. Comparative analysis of chloroplast genome of Lonicera japonica cv. Damaohua
  115. Human umbilical cord mesenchymal stem cells regulate glutathione metabolism depending on the ERK–Nrf2–HO-1 signal pathway to repair phosphoramide mustard-induced ovarian cancer cells
  116. Electroacupuncture on GB acupoints improves osteoporosis via the estradiol–PI3K–Akt signaling pathway
  117. Renalase protects against podocyte injury by inhibiting oxidative stress and apoptosis in diabetic nephropathy
  118. Review: Dicranostigma leptopodum: A peculiar plant of Papaveraceae
  119. Combination effect of flavonoids attenuates lung cancer cell proliferation by inhibiting the STAT3 and FAK signaling pathway
  120. Renal microangiopathy and immune complex glomerulonephritis induced by anti-tumour agents: A case report
  121. Correlation analysis of AVPR1a and AVPR2 with abnormal water and sodium and potassium metabolism in rats
  122. Gastrointestinal health anti-diarrheal mixture relieves spleen deficiency-induced diarrhea through regulating gut microbiota
  123. Myriad factors and pathways influencing tumor radiotherapy resistance
  124. Exploring the effects of culture conditions on Yapsin (YPS) gene expression in Nakaseomyces glabratus
  125. Screening of prognostic core genes based on cell–cell interaction in the peripheral blood of patients with sepsis
  126. Coagulation factor II thrombin receptor as a promising biomarker in breast cancer management
  127. Ileocecal mucinous carcinoma misdiagnosed as incarcerated hernia: A case report
  128. Methyltransferase like 13 promotes malignant behaviors of bladder cancer cells through targeting PI3K/ATK signaling pathway
  129. The debate between electricity and heat, efficacy and safety of irreversible electroporation and radiofrequency ablation in the treatment of liver cancer: A meta-analysis
  130. ZAG promotes colorectal cancer cell proliferation and epithelial–mesenchymal transition by promoting lipid synthesis
  131. Baicalein inhibits NLRP3 inflammasome activation and mitigates placental inflammation and oxidative stress in gestational diabetes mellitus
  132. Impact of SWCNT-conjugated senna leaf extract on breast cancer cells: A potential apoptotic therapeutic strategy
  133. MFAP5 inhibits the malignant progression of endometrial cancer cells in vitro
  134. Major ozonated autohemotherapy promoted functional recovery following spinal cord injury in adult rats via the inhibition of oxidative stress and inflammation
  135. Axodendritic targeting of TAU and MAP2 and microtubule polarization in iPSC-derived versus SH-SY5Y-derived human neurons
  136. Differential expression of phosphoinositide 3-kinase/protein kinase B and Toll-like receptor/nuclear factor kappa B signaling pathways in experimental obesity Wistar rat model
  137. The therapeutic potential of targeting Oncostatin M and the interleukin-6 family in retinal diseases: A comprehensive review
  138. BA inhibits LPS-stimulated inflammatory response and apoptosis in human middle ear epithelial cells by regulating the Nf-Kb/Iκbα axis
  139. Role of circRMRP and circRPL27 in chronic obstructive pulmonary disease
  140. Investigating the role of hyperexpressed HCN1 in inducing myocardial infarction through activation of the NF-κB signaling pathway
  141. Characterization of phenolic compounds and evaluation of anti-diabetic potential in Cannabis sativa L. seeds: In vivo, in vitro, and in silico studies
  142. Quantitative immunohistochemistry analysis of breast Ki67 based on artificial intelligence
  143. Ecology and Environmental Science
  144. Screening of different growth conditions of Bacillus subtilis isolated from membrane-less microbial fuel cell toward antimicrobial activity profiling
  145. Degradation of a mixture of 13 polycyclic aromatic hydrocarbons by commercial effective microorganisms
  146. Evaluation of the impact of two citrus plants on the variation of Panonychus citri (Acari: Tetranychidae) and beneficial phytoseiid mites
  147. Prediction of present and future distribution areas of Juniperus drupacea Labill and determination of ethnobotany properties in Antalya Province, Türkiye
  148. Population genetics of Todarodes pacificus (Cephalopoda: Ommastrephidae) in the northwest Pacific Ocean via GBS sequencing
  149. A comparative analysis of dendrometric, macromorphological, and micromorphological characteristics of Pistacia atlantica subsp. atlantica and Pistacia terebinthus in the middle Atlas region of Morocco
  150. Macrofungal sporocarp community in the lichen Scots pine forests
  151. Assessing the proximate compositions of indigenous forage species in Yemen’s pastoral rangelands
  152. Food Science
  153. Gut microbiota changes associated with low-carbohydrate diet intervention for obesity
  154. Reexamination of Aspergillus cristatus phylogeny in dark tea: Characteristics of the mitochondrial genome
  155. Differences in the flavonoid composition of the leaves, fruits, and branches of mulberry are distinguished based on a plant metabolomics approach
  156. Investigating the impact of wet rendering (solventless method) on PUFA-rich oil from catfish (Clarias magur) viscera
  157. Non-linear associations between cardiovascular metabolic indices and metabolic-associated fatty liver disease: A cross-sectional study in the US population (2017–2020)
  158. Knockdown of USP7 alleviates atherosclerosis in ApoE-deficient mice by regulating EZH2 expression
  159. Utility of dairy microbiome as a tool for authentication and traceability
  160. Agriculture
  161. Enhancing faba bean (Vicia faba L.) productivity through establishing the area-specific fertilizer rate recommendation in southwest Ethiopia
  162. Impact of novel herbicide based on synthetic auxins and ALS inhibitor on weed control
  163. Perspectives of pteridophytes microbiome for bioremediation in agricultural applications
  164. Fertilizer application parameters for drip-irrigated peanut based on the fertilizer effect function established from a “3414” field trial
  165. Improving the productivity and profitability of maize (Zea mays L.) using optimum blended inorganic fertilization
  166. Application of leaf multispectral analyzer in comparison to hyperspectral device to assess the diversity of spectral reflectance indices in wheat genotypes
  167. Animal Sciences
  168. Knockdown of ANP32E inhibits colorectal cancer cell growth and glycolysis by regulating the AKT/mTOR pathway
  169. Development of a detection chip for major pathogenic drug-resistant genes and drug targets in bovine respiratory system diseases
  170. Exploration of the genetic influence of MYOT and MB genes on the plumage coloration of Muscovy ducks
  171. Transcriptome analysis of adipose tissue in grazing cattle: Identifying key regulators of fat metabolism
  172. Comparison of nutritional value of the wild and cultivated spiny loaches at three growth stages
  173. Transcriptomic analysis of liver immune response in Chinese spiny frog (Quasipaa spinosa) infected with Proteus mirabilis
  174. Disruption of BCAA degradation is a critical characteristic of diabetic cardiomyopathy revealed by integrated transcriptome and metabolome analysis
  175. Plant Sciences
  176. Effect of long-term in-row branch covering on soil microorganisms in pear orchards
  177. Photosynthetic physiological characteristics, growth performance, and element concentrations reveal the calcicole–calcifuge behaviors of three Camellia species
  178. Transcriptome analysis reveals the mechanism of NaHCO3 promoting tobacco leaf maturation
  179. Bioinformatics, expression analysis, and functional verification of allene oxide synthase gene HvnAOS1 and HvnAOS2 in qingke
  180. Water, nitrogen, and phosphorus coupling improves gray jujube fruit quality and yield
  181. Improving grape fruit quality through soil conditioner: Insights from RNA-seq analysis of Cabernet Sauvignon roots
  182. Role of Embinin in the reabsorption of nucleus pulposus in lumbar disc herniation: Promotion of nucleus pulposus neovascularization and apoptosis of nucleus pulposus cells
  183. Revealing the effects of amino acid, organic acid, and phytohormones on the germination of tomato seeds under salinity stress
  184. Combined effects of nitrogen fertilizer and biochar on the growth, yield, and quality of pepper
  185. Comprehensive phytochemical and toxicological analysis of Chenopodium ambrosioides (L.) fractions
  186. Impact of “3414” fertilization on the yield and quality of greenhouse tomatoes
  187. Exploring the coupling mode of water and fertilizer for improving growth, fruit quality, and yield of the pear in the arid region
  188. Metagenomic analysis of endophytic bacteria in seed potato (Solanum tuberosum)
  189. Antibacterial, antifungal, and phytochemical properties of Salsola kali ethanolic extract
  190. Exploring the hepatoprotective properties of citronellol: In vitro and in silico studies on ethanol-induced damage in HepG2 cells
  191. Enhanced osmotic dehydration of watermelon rind using honey–sucrose solutions: A study on pre-treatment efficacy and mass transfer kinetics
  192. Effects of exogenous 2,4-epibrassinolide on photosynthetic traits of 53 cowpea varieties under NaCl stress
  193. Comparative transcriptome analysis of maize (Zea mays L.) seedlings in response to copper stress
  194. An optimization method for measuring the stomata in cassava (Manihot esculenta Crantz) under multiple abiotic stresses
  195. Fosinopril inhibits Ang II-induced VSMC proliferation, phenotype transformation, migration, and oxidative stress through the TGF-β1/Smad signaling pathway
  196. Antioxidant and antimicrobial activities of Salsola imbricata methanolic extract and its phytochemical characterization
  197. Bioengineering and Biotechnology
  198. Absorbable calcium and phosphorus bioactive membranes promote bone marrow mesenchymal stem cells osteogenic differentiation for bone regeneration
  199. New advances in protein engineering for industrial applications: Key takeaways
  200. An overview of the production and use of Bacillus thuringiensis toxin
  201. Research progress of nanoparticles in diagnosis and treatment of hepatocellular carcinoma
  202. Bioelectrochemical biosensors for water quality assessment and wastewater monitoring
  203. PEI/MMNs@LNA-542 nanoparticles alleviate ICU-acquired weakness through targeted autophagy inhibition and mitochondrial protection
  204. Unleashing of cytotoxic effects of thymoquinone-bovine serum albumin nanoparticles on A549 lung cancer cells
  205. Erratum
  206. Erratum to “Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM”
  207. Erratum to “Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation”
  208. Retraction
  209. Retraction to “MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB”
  210. Retraction to “A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis”
  211. Special Issue on Advances in Neurodegenerative Disease Research and Treatment
  212. Transplantation of human neural stem cell prevents symptomatic motor behavior disability in a rat model of Parkinson’s disease
  213. Special Issue on Multi-omics
  214. Inflammasome complex genes with clinical relevance suggest potential as therapeutic targets for anti-tumor drugs in clear cell renal cell carcinoma
  215. Gastroesophageal varices in primary biliary cholangitis with anti-centromere antibody positivity: Early onset?
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