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ZAG promotes colorectal cancer cell proliferation and epithelial–mesenchymal transition by promoting lipid synthesis

  • Maotao Xu , Xingzheng Jin and Zhouli Shen EMAIL logo
Published/Copyright: December 18, 2024
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Open Life Sciences
From the journal Open Life Sciences Volume 19 Issue 1

Abstract

Colorectal cancer (CRC) is a common malignant tumor characterized by a high degree of invasiveness, and since zinc-α2 glycoprotein (ZAG) has been implicated in the progression of several malignancies, this study was designed to investigate the role of ZAG in CRC. Its expression was assessed using the GEPIA database, and short hairpin RNA (shRNA) interference was conducted to create ZAG knockdown in CRC cell lines. We also conducted lipid synthesis, cell proliferation, apoptosis, and epithelial–mesenchymal transition (EMT) experiments to elucidate the effects of ZAG expression on CRC, as well as explored the potential underlying mechanistic pathways. Our findings reveal that ZAG is overexpressed in CRC. In vitro, ZAG knockdown resulted in the suppression of lipid production, cell division, and EMT while concurrently promoting apoptosis. The phosphoinositide 3-kinase (PI3K)/protein kinase B (AKT)/mechanistic target of rapamycin (mTOR) signaling pathway was found to mediate the effects of ZAG on CRC cells. In conclusion, the downregulation of ZAG can inhibit CRC cell survival, EMT, and lipid production via the PI3K/AKT/mTOR signaling pathway.

Graphical Abstract

Keywords: colorectal cancer; ZAG; epithelial-mesenchymal transition; lipid production; PI3K/AKT/mTOR

1 Introduction

Colorectal cancer (CRC) is one of the most prevalent cancers globally, accounting for approximately 8% of new cancer cases each year, with over 130,000 cases reported annually, ranking second in incidence among men and third among women [1,2]. The development of CRC is influenced by a combination of genetic, epigenetic, and environmental factors, and its pathogenesis involves anomalies in signaling pathways, lipid metabolic disorders, genetic alterations, and epigenetic modifications [3,4]. As various genetic and epigenetic changes, including histone modifications, DNA methylation, and non-coding RNAs, gradually accumulate in normal colonic epithelium, colorectal adenomas and invasive adenocarcinomas emerge. An increasing number of studies have highlighted the potential of targeting epigenetic alterations for therapeutic intervention, which may form the basis for individualized precision medicine strategies in the future [5,6]. In addition, dietary factors have been extensively studied as significant environmental risk factors associated with colon cancer, contributing to approximately 80% of cases. Moreover, factors such as Western diets, obesity, and high-fat intake have been shown to increase the risk of developing colon cancer and its recurrence [7,8]. Therefore, regulating lipid metabolism could be essential for controlling the progression of CRC.

Zinc-α2 glycoprotein (ZAG) is a 43 kDa polypeptide and has been classified as a novel adipokine due to its role in lipid mobilization [9]. ZAG has both lipolytic and lipogenic effects, and it promotes fat metabolism by interacting with β3 adrenergic receptors [10]. Recent research has demonstrated that ZAG treatment may enhance lipolysis in isolated adipocytes in both in vivo and in vitro studies involving humans and animals. In addition, ZAG can also regulate the metabolism of excess free fatty acids (FFA) produced by adipocytes during increased lipolysis [11,12]. Moreover, ZAG is recognized as a tumor marker, as it is overexpressed in various cancer types and is associated with weight loss when its levels are elevated. In both humans and rodents, ZAG expression in obesity is inversely correlated with body weight and fat mass [13]. For example, ZAG degradation promotes cholangiocarcinoma growth by inhibiting apoptosis through the tripartite motif-containing protein (TRIM) 25 [14]. Additionally, in triple-negative breast cancer, the release of ZAG promotes fibrosis within the tumor microenvironment [15]. ZAG is responsive to androgens and participates in AR-induced proliferation and metastasis of prostate cancer cells [16]. ZAG is a tumor suppressor in pancreatic cancer that induces mesenchymal–epithelial cell transdifferentiation by inhibiting TGF-β-mediated ERK signaling [17]. However, the role of ZAG in colorectal tumors has been inadequately explored, and the underlying mechanisms remain unclear.

This investigation aims to investigate the function of ZAG in CRC by knocking down the ZAG gene in CRC cells to assess its functional relevance and determine how such knockdown affects associated signaling pathways. Overall, our findings suggest that ZAG plays a significant role in the progression of CRC.

2 Methods

2.1 Cell lines and cell culture

Human CRC cell lines SW480, HCT116, and the intestinal epithelial cell line NCM460 were purchased from the Chinese Academy of Sciences Cell Bank and cultured in Dulbecco’s modified Eagle’s medium (DMEM) (Cytiva, Marlborough, USA) supplemented with 10% fetal calf serum (Gibco, Invitrogen, USA) and 1% penicillin/streptomycin (Gibco, Invitrogen, USA). All cells were maintained at 37°C in a 5% CO2 atmosphere.

2.2 Cell transfection

To facilitate gene knockdown, a ZAG plasmid was constructed, and a control shRNA plasmid was used as the negative control. The design, synthesis, and collection of all plasmids were performed by Suzhou Jima Pharmaceutical Co., Ltd. Lipofectamine 2000 (lot number: 2398587; Invitrogen) was utilized for transient transfections according to the manufacturer’s recommendations. A negative control (shNC) was used for experiments, and Western blotting was performed to verify the efficiency of ZAG knockdown.

2.3 Cell proliferation assay and colony formation assay

Cell growth was assessed using the counting kit-8 (CCK-8; Beyotime, China). Briefly, a total of 1,000 cells per well were seeded in a 96-well plate. After 72 h of incubation, the culture media was discarded, and the CCK-8 reagent was added to each well. After 1 h of incubation, cell proliferation was measured using a microplate reader (Bio-Tek).

For the colony formation assay, 500 cells per well were seeded in a 6-cm plate and cultured for 14 days in a medium containing 10% fetal bovine serum. After removing the growth media, the cells were fixed with methanol for 10 min, stained with crystal violet, washed with water, dried, and counted.

2.4 Apoptosis assay

The apoptotic rate of the cells was determined using the Annexin V-fluorescein isothiocyanate/propidium iodide kit (Beckman Coulter, Brea, CA). After staining, apoptosis rates were assessed and quantified by flow cytometry.

2.5 Oil red O staining

Coverslip-grown CRC cells were fixed for 15 min in 4% paraformaldehyde and subsequently stained for 30 min with a 3 mg/mL Oil Red O solution (Shanghai Yuanye Biological Co., Ltd.). Lipid droplets were visualized using a microscope (Olympus, DP73, Tokyo, Japan) and analyzed using ImageJ software after counterstaining with hematoxylin.

2.6 Western blot

The proteins were lysed on ice for 30 min using IP cell lysis buffer (Beyotime). The concentration of the extracted proteins was quantified using the Bicinchoninic Acid (BCA) protein assay kit (Thermo Fisher Scientific, Inc.). Then, the proteins were separated by electrophoresis on a 12% sodium dodecyl sulfate–polyacrylamide gel and transferred to a 0.45 µm polyvinylidene fluoride membrane. The membrane was blocked for 2 h using 1% bovine serum albumin to prevent non-specific binding. After blocking, the membrane was incubated overnight at 4°C on a shaker with diluted primary antibodies. Following this, the membrane was washed and incubated for 1 h with goat anti-rabbit IgG (1:2,000, ab7090; Abcam). The membrane was washed again before detection using the enhanced chemiluminescence substrate solution from Lulong Biotech.

The primary antibodies used were as follows: ZAG (1:1,000, ab180574, Abcam, UK), epithelial (E)-cadherin (1:1,000, ab40772, Abcam, UK), neural (N)-cadherin (1:1,000, ab76011, Abcam, UK), alpha-smooth muscle actin (α-SMA, 1:1,000, ab314895, Abcam, UK), acetyl-CoA carboxylase 1 (ACC1, 1:1,000, ab109368, Abcam, UK), ACC2 (1:1,000, ab287160, Abcam, UK), fatty acid synthase (FAS, 1:1,000, ab133619, Abcam, UK), phosphoinositide 3-kinase (PI3K, 1:1,000, ab267787, Abcam, UK), protein kinase B (AKT, 1:1,000, ab283852, Abcam, UK), phosphorylated AKT (p-AKT, 1:1,000, ab8805, Abcam, UK), mechanistic target of rapamycin (mTOR, 1:1,000, ab134903, Abcam, UK), phosphorylated mTOR (p-mTOR, 1:1,000, ab137133, Abcam, UK), and glyceraldehyde 3-phosphate dehydrogenase (1:1,000, ab8245, Abcam, UK).

2.7 Statistical analysis

The data were analyzed using GraphPad Prism 8 (GraphPad Software Inc., San Diego, CA) and are presented as mean ± standard deviation (SD). Statistical comparisons were performed using Student’s t-test or one-way analysis of variance, as appropriate, and p < 0.05 was considered statistically significant.

3 Results

3.1 ZAG is highly expressed in CRC

The expression of ZAG was first investigated in rectal adenocarcinoma tissues and normal intestinal tissues using the GEPIA database, and we observed that rectal tumor tissues exhibited significantly higher levels of ZAG expression than normal intestinal tissues (Figure 1a). Next, Western blot analysis was performed on the intestinal epithelial cell line NCM460 and CRC cell lines SW480 and HCT116 (Figure 1b), and the results demonstrated a significantly elevated expression level of ZAG protein in CRC cells compared to the intestinal epithelial cell line. Collectively, these results suggest that ZAG expression is upregulated in CRC.

Figure 1 ZAG is highly expressed in CRC. (a) Analysis of ZAG mRNA expression in human rectal adenocarcinoma tissues compared to normal tissues using the GEPIA database. (b) Western blot analysis was performed to detect ZAG protein expression in the intestinal epithelial cell line NCM460 and CRC cell lines SW480 and HCT116. Values are presented as mean ± SD. **p < 0.01, ***p < 0.001 versus NCM460 group. n = 3.
Figure 1

ZAG is highly expressed in CRC. (a) Analysis of ZAG mRNA expression in human rectal adenocarcinoma tissues compared to normal tissues using the GEPIA database. (b) Western blot analysis was performed to detect ZAG protein expression in the intestinal epithelial cell line NCM460 and CRC cell lines SW480 and HCT116. Values are presented as mean ± SD. **p < 0.01, ***p < 0.001 versus NCM460 group. n = 3.

3.2 Knockdown of ZAG inhibits the growth of CRC cells

To assess the role of ZAG, CRC cells were transfected with the ZAG shRNA plasmid to induce ZAG knockdown. Western blotting confirmed that ZAG shRNA significantly reduced ZAG expression in CRC cells, validating the successful creation of the shRNA plasmid (Figure 2a). The CCK-8 assay results demonstrated that ZAG knockdown inhibited the growth of CRC cells (Figure 2b). Furthermore, ZAG depletion was found to reduce colony formation in CRC cells (Figure 2c), and flow cytometry analysis revealed that ZAG knockdown significantly increased the apoptosis rate of CRC cells (Figure 2d). Overall, ZAG inhibition resulted in decreased survival of CRC cells.

Figure 2 The knockdown of ZAG inhibits CRC cell growth. (a) Western blot analysis of ZAG expression in CRC cells following ZAG knockdown. (b) CCK-8 assay was conducted to measure cell viability. (c) Crystal violet staining was used to assess colony formation. (d) Flow cytometry was performed to determine the apoptosis rate of CRC cells. Values are presented as mean ± SD. ***p < 0.001 versus shNC group. n = 3.
Figure 2

The knockdown of ZAG inhibits CRC cell growth. (a) Western blot analysis of ZAG expression in CRC cells following ZAG knockdown. (b) CCK-8 assay was conducted to measure cell viability. (c) Crystal violet staining was used to assess colony formation. (d) Flow cytometry was performed to determine the apoptosis rate of CRC cells. Values are presented as mean ± SD. ***p < 0.001 versus shNC group. n = 3.

3.3 Knockdown of ZAG inhibits EMT of CRC cells

Western blot analysis was performed to evaluate the impact of ZAG on the epithelial–mesenchymal transition (EMT) in CRC cells, and we found that shZAG reduced the levels of EMT-associated proteins, including N-cadherin and α-SMA. Conversely, shZAG increased the expression of E-cadherin in CRC cells (Figure 3). Therefore, lowering ZAG levels can effectively inhibit EMT in CRC cells.

Figure 3 Knockdown of ZAG inhibits EMT of CRC cells. Western blot analysis was performed to detect the expression of E-cadherin, N-cadherin, and α-SMA proteins. Values are presented as mean ± SD. **p < 0.01, ***p < 0.001 versus shNC group. n = 3.
Figure 3

Knockdown of ZAG inhibits EMT of CRC cells. Western blot analysis was performed to detect the expression of E-cadherin, N-cadherin, and α-SMA proteins. Values are presented as mean ± SD. **p < 0.01, ***p < 0.001 versus shNC group. n = 3.

3.4 Knockdown of ZAG inhibits lipid synthesis in CRC cells

To explore the relationship between ZAG and lipid production in CRC, we utilized protein immunoblotting and Oil Red O staining. Western blot analysis revealed a significant reduction in the levels of lipogenesis-related proteins FAS, ACC2, and ACC1 following ZAG knockdown (Figure 4a). Notably, ZAG is known to regulate adipogenesis. The results of Oil Red O staining indicated that the downregulation of ZAG was accompanied by a reduction in lipid droplet formation (Figure 4b). Thus, these findings suggest that ZAG inhibition can decrease lipid synthesis in CRC cells.

Figure 4 Knockdown of ZAG inhibits lipid synthesis in CRC cells. (a) Western blot analysis was conducted to detect the expression of ACC1, ACC2, p-ACC, and FAS proteins. (b) Oil Red O staining was used to quantify lipid droplet area. Values are presented as mean ± SD. **p < 0.01, ***p < 0.001 versus shNC group. n = 3.
Figure 4

Knockdown of ZAG inhibits lipid synthesis in CRC cells. (a) Western blot analysis was conducted to detect the expression of ACC1, ACC2, p-ACC, and FAS proteins. (b) Oil Red O staining was used to quantify lipid droplet area. Values are presented as mean ± SD. **p < 0.01, ***p < 0.001 versus shNC group. n = 3.

3.5 Knockdown of ZAG inhibits PI3K/AKT/mTOR signaling pathway

To further understand the molecular mechanisms underlying ZAG’s effects, we investigated its role in activating the PI3K/AKT/mTOR signaling pathway. Western blotting demonstrated that ZAG knockdown resulted in decreased expression levels of p-PI3K, p-AKT, and p-mTOR in CRC cells (Figure 5). This indicates that ZAG may promote cancer progression through the PI3K/AKT/mTOR signaling pathway.

Figure 5 Knockdown of ZAG inhibits PI3K/AKT/mTOR signaling pathway. Western blot analysis was performed to detect the expression of PI3K, p-PI3K, AKT, p-AKT, mTOR, and p-mTOR proteins. Values are presented as mean ± SD. *p < 0.05, **p < 0.01, ***p < 0.001 versus shNC group. n = 3.
Figure 5

Knockdown of ZAG inhibits PI3K/AKT/mTOR signaling pathway. Western blot analysis was performed to detect the expression of PI3K, p-PI3K, AKT, p-AKT, mTOR, and p-mTOR proteins. Values are presented as mean ± SD. *p < 0.05, **p < 0.01, ***p < 0.001 versus shNC group. n = 3.

4 Discussion

The formation of cancer is a complex process influenced by multiple factors, including genetics, nutrition, lifestyle choices, and genetic alterations [18], and identifying the genes that promote the onset and progression of CRC could significantly enhance its diagnosis and management. ZAG is predominantly secreted by mature adipocytes in healthy individuals, where it stimulates lipid mobilization in an autocrine or paracrine manner. Previous research has also indicated that malignant tumor cells express ZAG [19]. However, the specific impact of ZAG on CRC remains unclear. In this study, we demonstrated that ZAG is overexpressed in CRC tissues. Conversely, low ZAG expression was found to promote apoptosis and inhibit CRC cell proliferation. Additionally, ZAG inhibition suppressed the PI3K/AKT/mTOR signaling pathway, lipid production, and EMT. Our findings suggest that ZAG plays a crucial role in regulating lipid accumulation and colorectal carcinogenesis, indicating that targeting this protein could represent a viable therapeutic approach for CRC.

EMT is considered essential for tumor cells to acquire invasive and motile characteristics, facilitating metastasis and recurrence in various malignancies [20]. Cancer stem cells (CSCs) possess numerous protective mechanisms that enable them to withstand chemotherapy, making them a central focus in the study of aggressive cancers that currently lack effective treatments. In addition, numerous studies have shown that EMT is important for the enrichment of CSCs and their associated resistance to therapy [21,22]. Therefore, there is an emerging emphasis on understanding the biochemical components of CSCs and EMT in cancer therapy. E-cadherin, N-cadherin, and α-SMA are established markers of EMT [23]. In this study, our analysis indicates that low levels of ZAG expression effectively inhibit EMT.

Aberrant lipid metabolism is one of the earliest anomalies observed in tumor cells. Lipid synthesis not only produces a significant quantity of membrane phospholipids essential for tumor cell division and proliferation but also generates various lipid signaling molecules that promote cancer development [24]. Rapidly growing tumor cells have an increased demand for macromolecules, particularly lipids. When circulating lipids are insufficient to meet this demand, cancer cells compensate by enhancing de novo lipogenesis [25]. Given that CRC is reliant on lipid production, targeting lipid anabolism presents a potentially effective therapeutic strategy, and effective anti-CRC therapies likely depend on the inhibition of key molecules involved in lipid production [26]. Our results demonstrate that low ZAG expression inhibits lipid synthesis and accumulation, further supporting its potential as a therapeutic target in CRC.

Recent studies increasingly highlight the role of the PI3K/AKT/mTOR pathway in regulating various cellular processes, including adhesion, migration, survival, and proliferation [27]. The activation of AKT signaling promotes cell growth and tumor progression by regulating downstream cell cycle components [28]. In this pathway, phosphatidylinositol 4,5-bisphosphate (PIP2) is converted into phosphatidylinositol 3,4,5-trisphosphate (PIP3) by the lipid kinase PI3K. mTOR, a key protein in the PI3K/AKT/mTOR pathway, requires PIP3 as a second messenger for AKT translocation to the plasma membrane [29]. Furthermore, this pathway is crucial for lipid production and EMT [30].

The PI3K/AKT/mTOR pathway regulates the absorption and release of various amino acids and glucose in colon epithelial cells, influencing their responses to complex extracellular signals. This signaling pathway also plays a significant role in multiple cellular processes, transforming external stimuli into intracellular signals that affect metabolism and nutrient absorption. Thus, it has a profound impact on the onset, progression, metastasis, and prognosis of CRC [31,32]. The PI3K/AKT/mTOR pathway can also be activated by numerous growth factors, including vascular endothelial growth factor (VEGF), insulin-like growth factor 1 (IGF1), hormones, nutrients, and oxygen [33]. Herein, our study confirmed that the knockdown of ZAG can inhibit the expression of the PI3K/AKT/mTOR pathway in CRC cells.

5 Conclusion

In conclusion, the deletion of ZAG can effectively block the PI3K/AKT/mTOR signaling pathway, thereby preventing tumor cell proliferation, EMT, and lipid production in CRC. Our findings indicate that ZAG is an oncogene in CRC and a viable therapeutic target, particularly for patients with aberrant activity in the PI3K/AKT/mTOR pathway. However, due to the absence of in vivo and clinical investigations, further investigations are required to confirm these conclusions.

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  1. Funding information: Authors state no funding involved.

  2. Author contributions: All authors contributed to the study conception and design. Material preparation and the experiments were performed by Maotao Xu. Data collection and analysis were performed by Xingzheng Jin. The first draft of the manuscript was written by Zhouli Shen and all authors commented on previous versions of the manuscript. All authors read and approved the final 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 upon reasonable request.

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Received: 2024-08-23
Revised: 2024-10-21
Accepted: 2024-10-23
Published Online: 2024-12-18

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

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

Articles in the same Issue

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  2. Constitutive and evoked release of ATP in adult mouse olfactory epithelium
  3. LARP1 knockdown inhibits cultured gastric carcinoma cell cycle progression and metastatic behavior
  4. PEGylated porcine–human recombinant uricase: A novel fusion protein with improved efficacy and safety for the treatment of hyperuricemia and renal complications
  5. Research progress on ocular complications caused by type 2 diabetes mellitus and the function of tears and blepharons
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  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”
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https://doi.org/10.1515/biol-2022-1007
Keywords for this article
colorectal cancer; ZAG; epithelial-mesenchymal transition; lipid production; PI3K/AKT/mTOR
Creative Commons
BY 4.0

Articles in the same Issue

  1. Biomedical Sciences
  2. Constitutive and evoked release of ATP in adult mouse olfactory epithelium
  3. LARP1 knockdown inhibits cultured gastric carcinoma cell cycle progression and metastatic behavior
  4. PEGylated porcine–human recombinant uricase: A novel fusion protein with improved efficacy and safety for the treatment of hyperuricemia and renal complications
  5. Research progress on ocular complications caused by type 2 diabetes mellitus and the function of tears and blepharons
  6. The role and mechanism of esketamine in preventing and treating remifentanil-induced hyperalgesia based on the NMDA receptor–CaMKII pathway
  7. Brucella infection combined with Nocardia infection: A case report and literature review
  8. Detection of serum interleukin-18 level and neutrophil/lymphocyte ratio in patients with antineutrophil cytoplasmic antibody-associated vasculitis and its clinical significance
  9. Ang-1, Ang-2, and Tie2 are diagnostic biomarkers for Henoch-Schönlein purpura and pediatric-onset systemic lupus erythematous
  10. PTTG1 induces pancreatic cancer cell proliferation and promotes aerobic glycolysis by regulating c-myc
  11. Role of serum B-cell-activating factor and interleukin-17 as biomarkers in the classification of interstitial pneumonia with autoimmune features
  12. Effectiveness and safety of a mumps containing vaccine in preventing laboratory-confirmed mumps cases from 2002 to 2017: A meta-analysis
  13. Low levels of sex hormone-binding globulin predict an increased breast cancer risk and its underlying molecular mechanisms
  14. A case of Trousseau syndrome: Screening, detection and complication
  15. Application of the integrated airway humidification device enhances the humidification effect of the rabbit tracheotomy model
  16. Preparation of Cu2+/TA/HAP composite coating with anti-bacterial and osteogenic potential on 3D-printed porous Ti alloy scaffolds for orthopedic applications
  17. Aquaporin-8 promotes human dermal fibroblasts to counteract hydrogen peroxide-induced oxidative damage: A novel target for management of skin aging
  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
  20. Pheochromocytoma-induced myocardial infarction: A case report
  21. Kaempferol regulates apoptosis and migration of neural stem cells to attenuate cerebral infarction by O‐GlcNAcylation of β-catenin
  22. Sirtuin 5 regulates acute myeloid leukemia cell viability and apoptosis by succinylation modification of glycine decarboxylase
  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
  37. Sample size estimation for AQP4-IgG seropositive optic neuritis: Retinal damage detection by optical coherence tomography
  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
  53. Lactate-induced IGF1R protein lactylation promotes proliferation and metabolic reprogramming of lung cancer cells
  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
  70. Imaging manifestations of ductal adenoma of the breast: A case report
  71. Gut microbiota and sleep: Interaction mechanisms and therapeutic prospects
  72. Isomangiferin promotes the migration and osteogenic differentiation of rat bone marrow mesenchymal stem cells
  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
  111. Heterogeneous nuclear ribonucleoprotein K is a potential target for enhancing the chemosensitivity of nasopharyngeal carcinoma
  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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