Home Knockdown of SETD5 inhibited glycolysis and tumor growth in gastric cancer cells by down-regulating Akt signaling pathway
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Knockdown of SETD5 inhibited glycolysis and tumor growth in gastric cancer cells by down-regulating Akt signaling pathway

  • Jing Shi EMAIL logo , Litao Yu , Changhong Zhu and Haiyan Zhong
Published/Copyright: October 24, 2023
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Open Life Sciences
From the journal Open Life Sciences Volume 18 Issue 1

Abstract

Gastric cancer (GC) is the 5th most common cancer and the 3rd leading cause of cancer-related death worldwide. It is of great significance to study the underlying molecular mechanism of GC, and targeting glycolysis is a good strategy to treat GC. SET domain containing 5 (SETD5) contains a catalytic methyltransferase SET domain, which is known as a lysine methyltransferase that affects the progression of multiple cancers. However, its possible role in GC was still unclear. Here, we revealed that SETD5 was highly expressed in GC and was associated with a poor prognosis. Further through the in vitro experiments, we revealed that the downregulation of SETD5 inhibited the proliferation and migration of GC cells. Knockdown of SETD5 inhibited glucose consumption and glycolysis. Further studies have shown that SETD5 knockdown restrained the Akt signaling pathway. Therefore, we thought that SETD5 could act as a GC target.

Keywords: gastric cancer; SET domain containing 5; proliferation; glucose consumption; glycolysis

1 Introduction

Gastric cancer (GC) is the 5th most common cancer and the 3rd leading cause of cancer-related death in the world [1]. Although great progress has been made in diagnostic methods and surgical procedures over the past few years, the high recurrence rate and the low 5-year survival rate of GC are still unsatisfactory [2,3]. Therefore, it is key to investigate the underlying molecular mechanism of the malignant progression of GC to improve the survival and reduce the recurrence rate of GC patients.

Metabolic reprogramming of tumor cells is usually caused by the Warburg effect [4]. Recent studies have found that rapidly proliferated cancer cells rely on glycolysis for energy needs, even when oxygen is available [5]. Although the efficiency of ATP produced by glycolysis is quite low, it can rapidly provide an energy supply for tumor cells and macromolecular substances synthesized by molecules, forming an acidic environment and promoting metastasis of tumor cells [6]. Therefore, targeting glycolysis is a good strategy for treating GC.

SET domain containing 5 (SETD5), which contains a catalytic methyltransferase SET domain, is known as a lysine methyltransferase [7]. SETD5 gene has been found to be mutated in patients with intellectual disabilities and autism spectrum disorders [8]. Loss of SETD5 in embryonic stem cells leads to impaired proliferation and differentiation, further altering gene expression [9]. The function of SETD5 in cancer is largely unexplored. SETD5 plays a critical role in multiple types of cancers [10,11,12,13]. SETD5 enhances the cytodryness of non-small-cell lung cancer (NSCLC) through the PI3K/Akt/mTOR pathway [13,14]. In addition, SETD5 mediates the glycolysis in breast cancer stem cell-like cells and promotes tumor growth [12]. However, its possible effects on GC are still unclear. TCGA data analysis found that SETD5 was highly expressed in GC and was associated with poor prognosis, but the function of SETD5 in GC was not clear. In this study, it was found that knockdown SETD5 inhibited the proliferation and motility of GC cells, as well as suppressed the glycolysis of GC cells. Further studies showed that the downregulation of SETD5 restrained the Akt pathway. Therefore, we thought that it could serve as a promising GC target.

2 Materials and methods

2.1 Bioinformatics

To be more objective about the genes under study, transcriptome data were obtained from The Cancer Genome Atlas databases. In addition, the expression level of SETD5 and its relation with the overall survival of GC patients were analyzed using GEPIA online platforms based on the TCGA database. Kaplan–Meier in the low- and high-risk groups was analyzed. The online platform GEPIA was used to analyze the expression of SETD5 and its relation with the overall survival of GC patients based on the TCGA database.

2.2 Cell culture and transfection

Human gastric cell lines GES-1 and GC cells (AGS, HS746T, MKN-45, and HGC-27) were all purchased from the Cell Bank of the Chinese Academy of Sciences. Gastric and GC cells were cultured with the complete medium (DMEM containing 10% FBS). Cells were seeded in 6-well plates with 1 × 105 cells in each well. After 12 h of culture, Lipofectamine®3000 reagent (Invitrogen, Carlsbad, CA, USA) was used to co-transfect the cells with sh-NC, sh-SETD5, pcDNA-SETD5, and pcDNA, respectively. 5 μL Lipofectamine®3000 reagent and 5 μg shRNA plasmids were used in each well in 100 μL serum-free medium. 100 μL of the mixture was slowly added to the six-well plate, and the cells were incubated for 6 h. Then, western blotting was used to detect protein expression in the cells, and the transfection effect was verified for subsequent experiments.

2.3 Quantitative PCR

TRIzol (Invitrogen, Waltham, MA, USA) reagent was used. Then RNA was reverse-transcribed into cDNA using Moloney Murine Leukemia Virus Reverse Transcriptase (Promega, Madison, WI, USA). Fast Start Universal SYBR Green Master kit (Roche, Basel, Switzerland) was used for quantitative mRNA detection on the ABI StepOne system (Applied BioSystems, Foster City, CA, USA). The levels of targeted genes were determined by using the 2–ΔΔCT method.

2.4 Western blotting

Total protein was extracted from cells using RIPA buffer, and then, the protein was quantitated by BCA reagent, separated by SDS-PAGE, and further transferred to the PVDF membrane. The proteins were blocked with TBST containing 5% milk for 1 h, and then, the corresponding primary antibodies were added and incubated at 4°C overnight. Primary antibodies included SETD5 (Abcam, ab204363; 1:1,000), SLC2A1 (Abcam, ab261869; 1:500), PFKFB3 (Abcam, ab181861; 1:1,000), HK2 (Abcam, ab273721; 1:1,000), LDHA (Abcam, ab52488; 1:1,000), and β-actin (Abcam, ab8226; 1:3,000), and then, secondary antibodies were incubated with membranes for 1 h and photographed after chemiluminescence. The reagents used in this were purchased from Wuhan Google Co., Ltd.

2.5 MTT assay

GC cells were plated into 96-well plates with 1,000 cell density and then maintained for 48 h. Cells were subsequently incubated with MTT for 4 h and then dissolved with 150 μL of DMSO. Then, the OD value was measured at 490 nm wave length by a microplate reader (BD).

2.6 Colony formation assay

Cells were plated into the six-well plates (500 cells per well) and maintained in media (10% FBS) for 10 days at 37°C. Then, cells were fixed with PFA for 15 min and then stained with 0.1% crystal violet for 20 min. Then, cells were photographed by an Olympus microscope.

2.7 Transwell assays

Cells were plated into the upper of Transwell chambers in a culture medium without serum. Subsequently, a medium containing 10% FBS was added to the bottom to stimulate motility. After 24 h, cells in the upper were removed, and the remaining cells were fixed and stained with crystal violet and photographed by an Olympus microscope.

2.8 Glucose intake test

The glycolysis levels of cells were detected according to the glucose intake kit (Abcam, ab136955) according to the relevant instructions.

2.9 Oxygen consumption rate (OCR) and extracellular acidification rate (ECAR) test

OCR and ECAR were detected on an XF24 Extracellular Flux Analyzer (Seahorse Bioscience, Billerica, MA) following the manufacturer’s guidelines. OCR and ECAR measurement was performed after the exchange of medium for 90 min. The inhibitors of the electron transport chain and oxidative phosphorylation were injected: oligomycin A (1 μM), CCCP (1.5 μM), rotenone (0.5 μM), and antimycin A (0.5 μM).

2.10 Statistics

GraphPad 5.0 software was used for the statistical analysis. Data were represented as mean ± SEM. Student’s t-test was used for the comparisons, and p < 0.05 was considered statistically significant.

3 Results

3.1 SETD5 was highly expressed in human GC tissues and cells and correlated with the prognosis

We first detected the expression of SETD5 in GC tissues. We analyzed the expression of SETD5 in GC tissues (n = 415) and normal tissues (34) according to the TCGA database. We found a high expression of SETD5 in the GC tissues of patients (Figure 1a). Further, through the clinical sample analysis, it was found that SETD5 expression was correlated with the prognosis of patients with GC (Figure 1b). Subsequently, we detected SETD5 protein levels in GC cells including AGS, HS746T, MKN-45, and HGC-27 cells, and normal gastric GES-1 cells. Through Immunoblot, we found high protein levels of SETD5 in GC cells compared to normal gastric cells (Figure 1c). The immunostaining assays also showed high protein levels of SETD5 in GC cells compared to normal gastric cells (Figure S1). Therefore, SETD5 was highly expressed in human GC tissues and cells and correlated with the prognosis.

Figure 1 SETD5 was highly expressed in human gastric cancer tissues and cells and correlated with the prognosis of gastric cancer. (a) TCGA database showed the expression of SETD5 in gastric cancer tissues and normal tissues. (b) TCGA database showed the correlation between SETD5 expression and the prognosis of patients with gastric cancer. (c) Immunoblot showed the protein levels of SETD5 in cell lines including gastric cells GES-1 and GC cell lines (AGS, HS746T, MKN-45, and HGC-27). *p < 0.05, ***p < 0.001.
Figure 1

SETD5 was highly expressed in human gastric cancer tissues and cells and correlated with the prognosis of gastric cancer. (a) TCGA database showed the expression of SETD5 in gastric cancer tissues and normal tissues. (b) TCGA database showed the correlation between SETD5 expression and the prognosis of patients with gastric cancer. (c) Immunoblot showed the protein levels of SETD5 in cell lines including gastric cells GES-1 and GC cell lines (AGS, HS746T, MKN-45, and HGC-27). *p < 0.05, ***p < 0.001.

3.2 SETD5 depletion suppressed viability as well as the motility of GC cells

Subsequently, we detected the effects of SETD5 on the viability and motility of GC cells. The plasmids and siRNAs of SETD5 were transfected into AGS and HGC-27 cells to alter the expression of SETD5 in GC cells. Through qPCR and Immunoblot, we revealed that the transfection of SETD5 plasmids obviously increased its expression in AGS and HGC-27 cells, whereas the transfection of SETD5 siRNAs significantly suppressed the expression of SETD5 in GC cells (Figure 2a and b).

Figure 2 SETD5 depletion suppressed viability as well as the motility of GC cells. (a) qPCR showed the mRNA levels of SETD5 in AGS and HGC-27 cells upon the indicated transfection. (b) Immunoblot showed the expression of SETD5 in AGS and HGC-27 cells upon the indicated transfection. (c) MTT assays showed the OD value at 490 nm wavelength of AGS and HGC-27 cells upon the indicated transfection at 48 h. (d) Colony formation assay showed the viability of AGS and HGC-27 cells upon the transfection of indicated plasmids or siRNAs. (e) Transwell assay showed the effects of SETD5 on the invasion of AGS and HGC-27 cells upon the indicated transfection. ## p < 0.01, ### p < 0.001, SETD5 vs control; ***p < 0.001. siSETD5 vs siControl.
Figure 2

SETD5 depletion suppressed viability as well as the motility of GC cells. (a) qPCR showed the mRNA levels of SETD5 in AGS and HGC-27 cells upon the indicated transfection. (b) Immunoblot showed the expression of SETD5 in AGS and HGC-27 cells upon the indicated transfection. (c) MTT assays showed the OD value at 490 nm wavelength of AGS and HGC-27 cells upon the indicated transfection at 48 h. (d) Colony formation assay showed the viability of AGS and HGC-27 cells upon the transfection of indicated plasmids or siRNAs. (e) Transwell assay showed the effects of SETD5 on the invasion of AGS and HGC-27 cells upon the indicated transfection. ## p < 0.01, ### p < 0.001, SETD5 vs control; ***p < 0.001. siSETD5 vs siControl.

Through MTT assays, we found that SETD5 overexpression promoted the viability of AGS and HGC-27 cells, and its knockdown suppressed the viability of cells, with decreased OD490 value (Figure 2c). Through colony formation assays, we found that SETD5 overexpression increased the colony formation number of AGS and HGC-27 cells, whereas its knockdown decreased the colony numbers of GC cells (Figure 2d). Subsequently, we performed transwell assays to detect the effects of GC on cell motility. We noticed that SETD5 overexpression increased invasive cell numbers, whereas its downregulation decreased invasive cell numbers in AGS and HGC-27 cells (Figure 2e). Therefore, SETD5 knockdown suppressed viability and the motility of GC cells.

3.3 SETD5 knockdown inhibited aerobic glycolysis of GC cells

Then, we detected the effects of SETD5 on the aerobic glycolysis of GC cells. Through GEPIA analysis, we found that the expression of SETD5 was correlated with four aerobic glycolysis markers, including GLUT1, HK2, and LDHA (Figure 3a). We detected the expression of markers of aerobic glycolysis, including GLUT1, HK2, and LDHA in AGS and HGC-27 cells by western blotting upon the overexpression and knockdown of SETD5. We found that SETD5 overexpression increased the expression of GLUT1, HK2, and LDHA, and downregulation of SETD5 suppressed the expression of these proteins in AGS and HGC-27 cells (Figure 3b).

Figure 3 The expression of SETD5 is correlated with glycolysis of GC cells. (a) GEPIA database showed the correlation between SETD5 expression and the expression of glycolysis markers including SLC2A1, GLUT1, HK2, as well as LDHA in gastric cancer. (b). Immunoblot showed the protein levels of SLC2A1, GLUT1, HK2, as well as LDHA in AGS and HGC-27 cells upon the indicated transfection. ### p < 0.001, SETD5 vs control; ***p < 0.001. siSETD5 vs siControl.
Figure 3

The expression of SETD5 is correlated with glycolysis of GC cells. (a) GEPIA database showed the correlation between SETD5 expression and the expression of glycolysis markers including SLC2A1, GLUT1, HK2, as well as LDHA in gastric cancer. (b). Immunoblot showed the protein levels of SLC2A1, GLUT1, HK2, as well as LDHA in AGS and HGC-27 cells upon the indicated transfection. ### p < 0.001, SETD5 vs control; ***p < 0.001. siSETD5 vs siControl.

We then performed OCR and ECAR assays and found that SETD5 overexpression enhanced OCR and suppressed ECAR in AGS and HGC-27 cells, whereas its knockdown suppressed the OCR and increased ECAR (Figure 4a). We subsequently performed glucose uptake assays, and the data confirmed that SETD5 overexpression promoted the glucose uptake in AGS and HGC-27 cells, whereas its knockdown suppressed the glucose uptake (Figure 4b). Therefore, SETD5 knockdown inhibited aerobic glycolysis of GC cells.

Figure 4 SETD5 ablation suppressed the glucose consumption in GC cells. (a) OCR and ECAR levels of AGS and HGC-27 cells upon the indicated transfection. (b) Glucose uptake assays showed the relative glucose uptake capacity of AGS and HGC-27 cells upon the indicated transfection. # p < 0.05, ## p < 0.01, ### p < 0.001, SETD5 vs control; *p < 0.05, **p < 0.01, ***p < 0.001. siSETD5 vs siControl.
Figure 4

SETD5 ablation suppressed the glucose consumption in GC cells. (a) OCR and ECAR levels of AGS and HGC-27 cells upon the indicated transfection. (b) Glucose uptake assays showed the relative glucose uptake capacity of AGS and HGC-27 cells upon the indicated transfection. # p < 0.05, ## p < 0.01, ### p < 0.001, SETD5 vs control; *p < 0.05, **p < 0.01, ***p < 0.001. siSETD5 vs siControl.

4 SETD5 knockdown suppressed the Akt pathway in GC cells

Subsequently, we investigated the possible mechanism underlying SETD5 promoting the progression of GC. Through Immunoblot, we noticed that the knockdown of SETD5 suppressed the phosphorylation of Akt, PI3K, and mTOR in AGS and HGC-27 cells (Figure 5). However, the overexpression of SETD5 significantly promoted the phosphorylation levels of Akt, PI3K, and mTOR in AGS and HGC-27 cells but did not affect the total protein expression (Figure 5). These data suggested that SETD5 activated the Akt pathway in GC cells.

Figure 5 SETD5 knockdown suppressed the Akt pathway in GC cells. Immunoblot showed the protein levels of Akt, PI3K, and mTOR and the phosphorylation levels of Akt, PI3K, and mTOR in AGS and HGC-27 cells upon the indicated transfection. ## p < 0.01, ### p < 0.001, SETD5 vs control; *p < 0.05, **p < 0.01. siSETD5 vs siControl.
Figure 5

SETD5 knockdown suppressed the Akt pathway in GC cells. Immunoblot showed the protein levels of Akt, PI3K, and mTOR and the phosphorylation levels of Akt, PI3K, and mTOR in AGS and HGC-27 cells upon the indicated transfection. ## p < 0.01, ### p < 0.001, SETD5 vs control; *p < 0.05, **p < 0.01. siSETD5 vs siControl.

4.1 SETD5 knockdown suppressed GC cell glycolysis and growth

To further confirm the possible mechanism, we used the inhibitor of the Akt pathway, LY294002, to detect its effects on the glycolysis and growth of AGS cells. Through Immunoblot assays, we found that SETD5 overexpression increased the phosphorylation levels of mTOR, Akt, and PI3K in AGS cells, and the treatment of LY294002 suppressed the phosphorylation levels of mTOR, Akt, and PI3K in AGS cells (Figure 6a). MTT and transwell assays confirmed that SETD5 overexpression increased the proliferation and invasion of AGS cells, whereas the treatment of LY294002 attenuated the promoted proliferation and invasion of AGS cells (Figure 6b and c). We further found that the treatment of LY294002 attenuated the promoted relative glucose uptake and lactate production capacity in AGS cells (Figure 6d). Therefore, SETD5 knockdown suppressed GC cell glycolysis and growth.

Figure 6 SETD5 knockdown suppressed GC cell glycolysis and growth. (a) Immunoblot showed the expression of AKT, p-AKT, PI3K, p-PI3K, mTOR, and p-mTOR in AGS cells upon the indicated treatment. (b) MTT assays showed the OD value at 490 nm wavelength of AGS cells upon the indicated treatment at 48 h. (c) Transwell assay showed the invasion capacity of AGS cells upon the indicated treatment. (d) Glucose uptake assays showed the relative glucose uptake and lactate production capacity of AGS cells upon the indicated treatment. **p < 0.01, ***p < 0.001. SETD5 vs Vector. ### p < 0.001, SETD5 + LY294002 vs SETD5.
Figure 6

SETD5 knockdown suppressed GC cell glycolysis and growth. (a) Immunoblot showed the expression of AKT, p-AKT, PI3K, p-PI3K, mTOR, and p-mTOR in AGS cells upon the indicated treatment. (b) MTT assays showed the OD value at 490 nm wavelength of AGS cells upon the indicated treatment at 48 h. (c) Transwell assay showed the invasion capacity of AGS cells upon the indicated treatment. (d) Glucose uptake assays showed the relative glucose uptake and lactate production capacity of AGS cells upon the indicated treatment. **p < 0.01, ***p < 0.001. SETD5 vs Vector. ### p < 0.001, SETD5 + LY294002 vs SETD5.

5 Discussion

GC is a common malignant tumor in the digestive system, with occult onset and no specific symptoms [15]. The incidence of GC ranks the first in China, and about 170,000 people die from GC every year, which is a serious threat to people’s health [15]. The survival rate of early GC is high, but once it reaches the advanced stage, even with comprehensive treatment, the survival rate is still less than 30% [16]. The occurrence of GC is caused by multiple types of factors, and to improve survival, it is still necessary to have a detailed and in-depth understanding of its pathogenesis [16]. In this study, TCGA data analysis showed that SETD5 was highly expressed in GC and was associated with a poor prognosis. We therefore thought that it could serve as a promising GC target.

SETD5 is an important methyltransferase that has been found to be abnormally expressed in multiple tumors, correlated with the patient prognosis, and involved in the regulation of tumor progression and metastasis [9,12,14,17]. Downregulation of SETD5 restrained the tumorigenicity of the hepatocellular carcinoma (HCC) cells [18]. SETD5 mediated the glycolysis in breast cancer stem-like cells and promoted tumor growth [12]. Similarly, here, we also found that SETD5 knockdown inhibited glucose consumption and glycolysis in GC cells. SETD5 contributed to tumor cell invasion and was associated with a poor prognosis in NSCLC patients [13]. Through MTT, colony formation, and transwell assays, we found that SETD5 knockdown inhibited GC cell proliferation and migration. Our data therefore showed the involvement of SETD5 in GC progression.

One of the most common metabolic changes in tumor cells relative to normal cells is aerobic glycolysis, also known as the Warburg effect [4]. This effect plays an important role in the development of GC. In contrast to well-differentiated normal cells, which rely on the oxidation of pyruvate to produce energy for physiological functions, rapidly proliferating tumor cells rely on glycolysis for energy needs, even when adequate oxygen is available [4]. Although the efficiency of ATP produced by glycolysis is low, it can rapidly provide an energy supply for tumor cells and macromolecular substances synthesized by molecules, forming an acidic environment and promoting tumor cell metastasis [4]. Therefore, identifying the key mediators of the glycolysis pathway will provide effective strategies for the diagnosis and treatment of GC. By analyzing ATP level, glucose consumption, lactic acid production, OCR, and ECAR, we found that SETD5 knockdown inhibited the glucose consumption of GC cells.

Through Immunoblot assays, we found that the downregulation of SETD5 inhibited the Akt pathway in GC cells. This pathway affected multiple cellular processes in tumor cells, such as proliferation, motility, drug resistant, autophagy, and glucose consumption [19,20]. Urolithin A suppressed tumor progression and induced autophagy in GC via the Akt pathway [21]. The Akt pathway was also involved in P2RY2 activation and stimulated the proliferation and metastasis of GC [22]. These studies confirmed that the Akt pathway could serve as a promising GC target.

In summary, we revealed that SETD5 was highly expressed in GC and was associated with a poor prognosis. Downregulation of SETD5 inhibited the proliferation and motility of GC cells, as well as the glycolysis. Further studies have found that SETD5 knockdown restrained the Akt signaling pathway. Therefore, we thought that SETD5 could act as a potential therapeutic target for the treatment of GC.

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  1. Funding information: Authors state no funding involved.

  2. Author contributions: Jing Shi and Litao Yu designed the study and carried them out. Jing Shi, Litao Yu, Changhong Zhu, and Haiyan Zhong supervised the data collection, analyzed the data, and interpreted the data. Jing Shi and Litao Yu prepared the article for publication and reviewed the draft of the article. All authors have read and approved the article.

  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: 2022-12-30
Revised: 2023-06-07
Accepted: 2023-07-30
Published Online: 2023-10-24

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

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

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  21. Dosimetry comparison with helical tomotherapy, volumetric modulated arc therapy, and intensity-modulated radiotherapy for grade II gliomas: A single‑institution case series
  22. Soy isoflavone reduces LPS-induced acute lung injury via increasing aquaporin 1 and aquaporin 5 in rats
  23. Refractory hypokalemia with sexual dysplasia and infertility caused by 17α-hydroxylase deficiency and triple X syndrome: A case report
  24. Meta-analysis of cancer risk among end stage renal disease undergoing maintenance dialysis
  25. 6-Phosphogluconate dehydrogenase inhibition arrests growth and induces apoptosis in gastric cancer via AMPK activation and oxidative stress
  26. Experimental study on the optimization of ANM33 release in foam cells
  27. Primary retroperitoneal angiosarcoma: A case report
  28. Metabolomic analysis-identified 2-hydroxybutyric acid might be a key metabolite of severe preeclampsia
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  30. Effect of spaceflight on the phenotype and proteome of Escherichia coli
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  32. Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation
  33. Association between the VEGFR-2 -604T/C polymorphism (rs2071559) and type 2 diabetic retinopathy
  34. The role of IL-31 and IL-34 in the diagnosis and treatment of chronic periodontitis
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  51. Interaction between the PI3K/AKT pathway and mitochondrial autophagy in macrophages and the leukocyte count in rats with LPS-induced pulmonary infection
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  54. Coptisine mitigates diabetic nephropathy via repressing the NRLP3 inflammasome
  55. Significant elevated CXCL14 and decreased IL-39 levels in patients with tuberculosis
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  65. Diagnosis of primary amoebic meningoencephalitis by metagenomic next-generation sequencing: A case report
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  68. Effects of NM23 transfection of human gastric carcinoma cells in mice
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  220. Studies on macrofungi diversity and discovery of new species of Abortiporus from Baotianman World Biosphere Reserve
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  242. Effects of plant density on alfalfa (Medicago sativa L.) seed yield in western Heilongjiang areas
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  245. Animal Sciences
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  250. The sequencing of the key genes and end products in the TLR4 signaling pathway from the kidney of Rana dybowskii exposed to Aeromonas hydrophila
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  252. Plant Sciences
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  254. Genetic evaluation and germplasm identification analysis on ITS2, trnL-F, and psbA-trnH of alfalfa varieties germplasm resources
  255. Tissue culture and rapid propagation technology for Gentiana rhodantha
  256. Effects of cadmium on the synthesis of active ingredients in Salvia miltiorrhiza
  257. Cloning and expression analysis of VrNAC13 gene in mung bean
  258. Chlorate-induced molecular floral transition revealed by transcriptomes
  259. Effects of warming and drought on growth and development of soybean in Hailun region
  260. Effects of different light conditions on transient expression and biomass in Nicotiana benthamiana leaves
  261. Comparative analysis of the rhizosphere microbiome and medicinally active ingredients of Atractylodes lancea from different geographical origins
  262. Distinguish Dianthus species or varieties based on chloroplast genomes
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  264. Study on fresh processing key technology and quality influence of Cut Ophiopogonis Radix based on multi-index evaluation
  265. An advanced approach for fig leaf disease detection and classification: Leveraging image processing and enhanced support vector machine methodology
  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
https://doi.org/10.1515/biol-2022-0697
Keywords for this article
gastric cancer; SET domain containing 5; proliferation; glucose consumption; glycolysis
Creative Commons
BY 4.0

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  3. Immunosuppressive treatment for idiopathic membranous nephropathy: An updated network meta-analysis
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  19. Long noncoding RNA ACART knockdown decreases 3T3-L1 preadipocyte proliferation and differentiation
  20. Surgery, adjuvant immunotherapy plus chemotherapy and radiotherapy for primary malignant melanoma of the parotid gland (PGMM): A case report
  21. Dosimetry comparison with helical tomotherapy, volumetric modulated arc therapy, and intensity-modulated radiotherapy for grade II gliomas: A single‑institution case series
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  23. Refractory hypokalemia with sexual dysplasia and infertility caused by 17α-hydroxylase deficiency and triple X syndrome: A case report
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  26. Experimental study on the optimization of ANM33 release in foam cells
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  30. Effect of spaceflight on the phenotype and proteome of Escherichia coli
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  34. The role of IL-31 and IL-34 in the diagnosis and treatment of chronic periodontitis
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  37. The apatinib and pemetrexed combination has antitumor and antiangiogenic effects against NSCLC
  38. Radiotherapy for primary thyroid adenoid cystic carcinoma
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  80. Effects of maternal calcium and protein intake on the development and bone metabolism of offspring mice
  81. Identification of winter wheat pests and diseases based on improved convolutional neural network
  82. Ultra-multiplex PCR technique to guide treatment of Aspergillus-infected aortic valve prostheses
  83. Virtual high-throughput screening: Potential inhibitors targeting aminopeptidase N (CD13) and PIKfyve for SARS-CoV-2
  84. Immune checkpoint inhibitors in cancer patients with COVID-19
  85. Utility of methylene blue mixed with autologous blood in preoperative localization of pulmonary nodules and masses
  86. Integrated analysis of the microbiome and transcriptome in stomach adenocarcinoma
  87. Berberine suppressed sarcopenia insulin resistance through SIRT1-mediated mitophagy
  88. DUSP2 inhibits the progression of lupus nephritis in mice by regulating the STAT3 pathway
  89. Lung abscess by Fusobacterium nucleatum and Streptococcus spp. co-infection by mNGS: A case series
  90. Genetic alterations of KRAS and TP53 in intrahepatic cholangiocarcinoma associated with poor prognosis
  91. Granulomatous polyangiitis involving the fourth ventricle: Report of a rare case and a literature review
  92. Studying infant mortality: A demographic analysis based on data mining models
  93. Metaplastic breast carcinoma with osseous differentiation: A report of a rare case and literature review
  94. Protein Z modulates the metastasis of lung adenocarcinoma cells
  95. Inhibition of pyroptosis and apoptosis by capsaicin protects against LPS-induced acute kidney injury through TRPV1/UCP2 axis in vitro
  96. TAK-242, a toll-like receptor 4 antagonist, against brain injury by alleviates autophagy and inflammation in rats
  97. Primary mediastinum Ewing’s sarcoma with pleural effusion: A case report and literature review
  98. Association of ADRB2 gene polymorphisms and intestinal microbiota in Chinese Han adolescents
  99. Tanshinone IIA alleviates chondrocyte apoptosis and extracellular matrix degeneration by inhibiting ferroptosis
  100. Study on the cytokines related to SARS-Cov-2 in testicular cells and the interaction network between cells based on scRNA-seq data
  101. Effect of periostin on bone metabolic and autophagy factors during tooth eruption in mice
  102. HP1 induces ferroptosis of renal tubular epithelial cells through NRF2 pathway in diabetic nephropathy
  103. Intravaginal estrogen management in postmenopausal patients with vaginal squamous intraepithelial lesions along with CO2 laser ablation: A retrospective study
  104. Hepatocellular carcinoma cell differentiation trajectory predicts immunotherapy, potential therapeutic drugs, and prognosis of patients
  105. Effects of physical exercise on biomarkers of oxidative stress in healthy subjects: A meta-analysis of randomized controlled trials
  106. Identification of lysosome-related genes in connection with prognosis and immune cell infiltration for drug candidates in head and neck cancer
  107. Development of an instrument-free and low-cost ELISA dot-blot test to detect antibodies against SARS-CoV-2
  108. Research progress on gas signal molecular therapy for Parkinson’s disease
  109. Adiponectin inhibits TGF-β1-induced skin fibroblast proliferation and phenotype transformation via the p38 MAPK signaling pathway
  110. The G protein-coupled receptor-related gene signatures for predicting prognosis and immunotherapy response in bladder urothelial carcinoma
  111. α-Fetoprotein contributes to the malignant biological properties of AFP-producing gastric cancer
  112. CXCL12/CXCR4/CXCR7 axis in placenta tissues of patients with placenta previa
  113. Association between thyroid stimulating hormone levels and papillary thyroid cancer risk: A meta-analysis
  114. Significance of sTREM-1 and sST2 combined diagnosis for sepsis detection and prognosis prediction
  115. Diagnostic value of serum neuroactive substances in the acute exacerbation of chronic obstructive pulmonary disease complicated with depression
  116. Research progress of AMP-activated protein kinase and cardiac aging
  117. TRIM29 knockdown prevented the colon cancer progression through decreasing the ubiquitination levels of KRT5
  118. Cross-talk between gut microbiota and liver steatosis: Complications and therapeutic target
  119. Metastasis from small cell lung cancer to ovary: A case report
  120. The early diagnosis and pathogenic mechanisms of sepsis-related acute kidney injury
  121. The effect of NK cell therapy on sepsis secondary to lung cancer: A case report
  122. Erianin alleviates collagen-induced arthritis in mice by inhibiting Th17 cell differentiation
  123. Loss of ACOX1 in clear cell renal cell carcinoma and its correlation with clinical features
  124. Signalling pathways in the osteogenic differentiation of periodontal ligament stem cells
  125. Crosstalk between lactic acid and immune regulation and its value in the diagnosis and treatment of liver failure
  126. Clinicopathological features and differential diagnosis of gastric pleomorphic giant cell carcinoma
  127. Traumatic brain injury and rTMS-ERPs: Case report and literature review
  128. Extracellular fibrin promotes non-small cell lung cancer progression through integrin β1/PTEN/AKT signaling
  129. Knockdown of DLK4 inhibits non-small cell lung cancer tumor growth by downregulating CKS2
  130. The co-expression pattern of VEGFR-2 with indicators related to proliferation, apoptosis, and differentiation of anagen hair follicles
  131. Inflammation-related signaling pathways in tendinopathy
  132. CD4+ T cell count in HIV/TB co-infection and co-occurrence with HL: Case report and literature review
  133. Clinical analysis of severe Chlamydia psittaci pneumonia: Case series study
  134. Bioinformatics analysis to identify potential biomarkers for the pulmonary artery hypertension associated with the basement membrane
  135. Influence of MTHFR polymorphism, alone or in combination with smoking and alcohol consumption, on cancer susceptibility
  136. Catharanthus roseus (L.) G. Don counteracts the ampicillin resistance in multiple antibiotic-resistant Staphylococcus aureus by downregulation of PBP2a synthesis
  137. Combination of a bronchogenic cyst in the thoracic spinal canal with chronic myelocytic leukemia
  138. Bacterial lipoprotein plays an important role in the macrophage autophagy and apoptosis induced by Salmonella typhimurium and Staphylococcus aureus
  139. TCL1A+ B cells predict prognosis in triple-negative breast cancer through integrative analysis of single-cell and bulk transcriptomic data
  140. Ezrin promotes esophageal squamous cell carcinoma progression via the Hippo signaling pathway
  141. Ferroptosis: A potential target of macrophages in plaque vulnerability
  142. Predicting pediatric Crohn's disease based on six mRNA-constructed risk signature using comprehensive bioinformatic approaches
  143. Applications of genetic code expansion and photosensitive UAAs in studying membrane proteins
  144. HK2 contributes to the proliferation, migration, and invasion of diffuse large B-cell lymphoma cells by enhancing the ERK1/2 signaling pathway
  145. IL-17 in osteoarthritis: A narrative review
  146. Circadian cycle and neuroinflammation
  147. Probiotic management and inflammatory factors as a novel treatment in cirrhosis: A systematic review and meta-analysis
  148. Hemorrhagic meningioma with pulmonary metastasis: Case report and literature review
  149. SPOP regulates the expression profiles and alternative splicing events in human hepatocytes
  150. Knockdown of SETD5 inhibited glycolysis and tumor growth in gastric cancer cells by down-regulating Akt signaling pathway
  151. PTX3 promotes IVIG resistance-induced endothelial injury in Kawasaki disease by regulating the NF-κB pathway
  152. Pancreatic ectopic thyroid tissue: A case report and analysis of literature
  153. The prognostic impact of body mass index on female breast cancer patients in underdeveloped regions of northern China differs by menopause status and tumor molecular subtype
  154. Report on a case of liver-originating malignant melanoma of unknown primary
  155. Case report: Herbal treatment of neutropenic enterocolitis after chemotherapy for breast cancer
  156. The fibroblast growth factor–Klotho axis at molecular level
  157. Characterization of amiodarone action on currents in hERG-T618 gain-of-function mutations
  158. A case report of diagnosis and dynamic monitoring of Listeria monocytogenes meningitis with NGS
  159. Effect of autologous platelet-rich plasma on new bone formation and viability of a Marburg bone graft
  160. Small breast epithelial mucin as a useful prognostic marker for breast cancer patients
  161. Continuous non-adherent culture promotes transdifferentiation of human adipose-derived stem cells into retinal lineage
  162. Nrf3 alleviates oxidative stress and promotes the survival of colon cancer cells by activating AKT/BCL-2 signal pathway
  163. Favorable response to surufatinib in a patient with necrolytic migratory erythema: A case report
  164. Case report of atypical undernutrition of hypoproteinemia type
  165. Down-regulation of COL1A1 inhibits tumor-associated fibroblast activation and mediates matrix remodeling in the tumor microenvironment of breast cancer
  166. Sarcoma protein kinase inhibition alleviates liver fibrosis by promoting hepatic stellate cells ferroptosis
  167. Research progress of serum eosinophil in chronic obstructive pulmonary disease and asthma
  168. Clinicopathological characteristics of co-existing or mixed colorectal cancer and neuroendocrine tumor: Report of five cases
  169. Role of menopausal hormone therapy in the prevention of postmenopausal osteoporosis
  170. Precisional detection of lymph node metastasis using tFCM in colorectal cancer
  171. Advances in diagnosis and treatment of perimenopausal syndrome
  172. A study of forensic genetics: ITO index distribution and kinship judgment between two individuals
  173. Acute lupus pneumonitis resembling miliary tuberculosis: A case-based review
  174. Plasma levels of CD36 and glutathione as biomarkers for ruptured intracranial aneurysm
  175. Fractalkine modulates pulmonary angiogenesis and tube formation by modulating CX3CR1 and growth factors in PVECs
  176. Novel risk prediction models for deep vein thrombosis after thoracotomy and thoracoscopic lung cancer resections, involving coagulation and immune function
  177. Exploring the diagnostic markers of essential tremor: A study based on machine learning algorithms
  178. Evaluation of effects of small-incision approach treatment on proximal tibia fracture by deep learning algorithm-based magnetic resonance imaging
  179. An online diagnosis method for cancer lesions based on intelligent imaging analysis
  180. Medical imaging in rheumatoid arthritis: A review on deep learning approach
  181. Predictive analytics in smart healthcare for child mortality prediction using a machine learning approach
  182. Utility of neutrophil–lymphocyte ratio and platelet–lymphocyte ratio in predicting acute-on-chronic liver failure survival
  183. A biomedical decision support system for meta-analysis of bilateral upper-limb training in stroke patients with hemiplegia
  184. TNF-α and IL-8 levels are positively correlated with hypobaric hypoxic pulmonary hypertension and pulmonary vascular remodeling in rats
  185. Stochastic gradient descent optimisation for convolutional neural network for medical image segmentation
  186. Comparison of the prognostic value of four different critical illness scores in patients with sepsis-induced coagulopathy
  187. Application and teaching of computer molecular simulation embedded technology and artificial intelligence in drug research and development
  188. Hepatobiliary surgery based on intelligent image segmentation technology
  189. Value of brain injury-related indicators based on neural network in the diagnosis of neonatal hypoxic-ischemic encephalopathy
  190. Analysis of early diagnosis methods for asymmetric dementia in brain MR images based on genetic medical technology
  191. Early diagnosis for the onset of peri-implantitis based on artificial neural network
  192. Clinical significance of the detection of serum IgG4 and IgG4/IgG ratio in patients with thyroid-associated ophthalmopathy
  193. Forecast of pain degree of lumbar disc herniation based on back propagation neural network
  194. SPA-UNet: A liver tumor segmentation network based on fused multi-scale features
  195. Systematic evaluation of clinical efficacy of CYP1B1 gene polymorphism in EGFR mutant non-small cell lung cancer observed by medical image
  196. Rehabilitation effect of intelligent rehabilitation training system on hemiplegic limb spasms after stroke
  197. A novel approach for minimising anti-aliasing effects in EEG data acquisition
  198. ErbB4 promotes M2 activation of macrophages in idiopathic pulmonary fibrosis
  199. Clinical role of CYP1B1 gene polymorphism in prediction of postoperative chemotherapy efficacy in NSCLC based on individualized health model
  200. Lung nodule segmentation via semi-residual multi-resolution neural networks
  201. Evaluation of brain nerve function in ICU patients with Delirium by deep learning algorithm-based resting state MRI
  202. A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis
  203. Markov model combined with MR diffusion tensor imaging for predicting the onset of Alzheimer’s disease
  204. Effectiveness of the treatment of depression associated with cancer and neuroimaging changes in depression-related brain regions in patients treated with the mediator-deuterium acupuncture method
  205. Molecular mechanism of colorectal cancer and screening of molecular markers based on bioinformatics analysis
  206. Monitoring and evaluation of anesthesia depth status data based on neuroscience
  207. Exploring the conformational dynamics and thermodynamics of EGFR S768I and G719X + S768I mutations in non-small cell lung cancer: An in silico approaches
  208. Optimised feature selection-driven convolutional neural network using gray level co-occurrence matrix for detection of cervical cancer
  209. Incidence of different pressure patterns of spinal cerebellar ataxia and analysis of imaging and genetic diagnosis
  210. Pathogenic bacteria and treatment resistance in older cardiovascular disease patients with lung infection and risk prediction model
  211. Adoption value of support vector machine algorithm-based computed tomography imaging in the diagnosis of secondary pulmonary fungal infections in patients with malignant hematological disorders
  212. From slides to insights: Harnessing deep learning for prognostic survival prediction in human colorectal cancer histology
  213. Ecology and Environmental Science
  214. Monitoring of hourly carbon dioxide concentration under different land use types in arid ecosystem
  215. Comparing the differences of prokaryotic microbial community between pit walls and bottom from Chinese liquor revealed by 16S rRNA gene sequencing
  216. Effects of cadmium stress on fruits germination and growth of two herbage species
  217. Bamboo charcoal affects soil properties and bacterial community in tea plantations
  218. Optimization of biogas potential using kinetic models, response surface methodology, and instrumental evidence for biodegradation of tannery fleshings during anaerobic digestion
  219. Understory vegetation diversity patterns of Platycladus orientalis and Pinus elliottii communities in Central and Southern China
  220. Studies on macrofungi diversity and discovery of new species of Abortiporus from Baotianman World Biosphere Reserve
  221. Food Science
  222. Effect of berrycactus fruit (Myrtillocactus geometrizans) on glutamate, glutamine, and GABA levels in the frontal cortex of rats fed with a high-fat diet
  223. Guesstimate of thymoquinone diversity in Nigella sativa L. genotypes and elite varieties collected from Indian states using HPTLC technique
  224. Analysis of bacterial community structure of Fuzhuan tea with different processing techniques
  225. Untargeted metabolomics reveals sour jujube kernel benefiting the nutritional value and flavor of Morchella esculenta
  226. Mycobiota in Slovak wine grapes: A case study from the small Carpathians wine region
  227. Elemental analysis of Fadogia ancylantha leaves used as a nutraceutical in Mashonaland West Province, Zimbabwe
  228. Microbiological transglutaminase: Biotechnological application in the food industry
  229. Influence of solvent-free extraction of fish oil from catfish (Clarias magur) heads using a Taguchi orthogonal array design: A qualitative and quantitative approach
  230. Chromatographic analysis of the chemical composition and anticancer activities of Curcuma longa extract cultivated in Palestine
  231. The potential for the use of leghemoglobin and plant ferritin as sources of iron
  232. Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM
  233. Bioengineering and Biotechnology
  234. Biocompatibility and osteointegration capability of β-TCP manufactured by stereolithography 3D printing: In vitro study
  235. Clinical characteristics and the prognosis of diabetic foot in Tibet: A single center, retrospective study
  236. Agriculture
  237. Biofertilizer and NPSB fertilizer application effects on nodulation and productivity of common bean (Phaseolus vulgaris L.) at Sodo Zuria, Southern Ethiopia
  238. On correlation between canopy vegetation and growth indexes of maize varieties with different nitrogen efficiencies
  239. Exopolysaccharides from Pseudomonas tolaasii inhibit the growth of Pleurotus ostreatus mycelia
  240. A transcriptomic evaluation of the mechanism of programmed cell death of the replaceable bud in Chinese chestnut
  241. Melatonin enhances salt tolerance in sorghum by modulating photosynthetic performance, osmoregulation, antioxidant defense, and ion homeostasis
  242. Effects of plant density on alfalfa (Medicago sativa L.) seed yield in western Heilongjiang areas
  243. Identification of rice leaf diseases and deficiency disorders using a novel DeepBatch technique
  244. Artificial intelligence and internet of things oriented sustainable precision farming: Towards modern agriculture
  245. Animal Sciences
  246. Effect of ketogenic diet on exercise tolerance and transcriptome of gastrocnemius in mice
  247. Combined analysis of mRNA–miRNA from testis tissue in Tibetan sheep with different FecB genotypes
  248. Isolation, identification, and drug resistance of a partially isolated bacterium from the gill of Siniperca chuatsi
  249. Tracking behavioral changes of confined sows from the first mating to the third parity
  250. The sequencing of the key genes and end products in the TLR4 signaling pathway from the kidney of Rana dybowskii exposed to Aeromonas hydrophila
  251. Development of a new candidate vaccine against piglet diarrhea caused by Escherichia coli
  252. Plant Sciences
  253. Crown and diameter structure of pure Pinus massoniana Lamb. forest in Hunan province, China
  254. Genetic evaluation and germplasm identification analysis on ITS2, trnL-F, and psbA-trnH of alfalfa varieties germplasm resources
  255. Tissue culture and rapid propagation technology for Gentiana rhodantha
  256. Effects of cadmium on the synthesis of active ingredients in Salvia miltiorrhiza
  257. Cloning and expression analysis of VrNAC13 gene in mung bean
  258. Chlorate-induced molecular floral transition revealed by transcriptomes
  259. Effects of warming and drought on growth and development of soybean in Hailun region
  260. Effects of different light conditions on transient expression and biomass in Nicotiana benthamiana leaves
  261. Comparative analysis of the rhizosphere microbiome and medicinally active ingredients of Atractylodes lancea from different geographical origins
  262. Distinguish Dianthus species or varieties based on chloroplast genomes
  263. Comparative transcriptomes reveal molecular mechanisms of apple blossoms of different tolerance genotypes to chilling injury
  264. Study on fresh processing key technology and quality influence of Cut Ophiopogonis Radix based on multi-index evaluation
  265. An advanced approach for fig leaf disease detection and classification: Leveraging image processing and enhanced support vector machine methodology
  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
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