Startseite Knockdown of SHMT2 enhances the sensitivity of gastric cancer cells to radiotherapy through the Wnt/β-catenin pathway
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Knockdown of SHMT2 enhances the sensitivity of gastric cancer cells to radiotherapy through the Wnt/β-catenin pathway

  • Yu Mao und Tiyong Zhang EMAIL logo
Veröffentlicht/Copyright: 19. September 2022
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Open Life Sciences
Aus der Zeitschrift Open Life Sciences Band 17 Heft 1

Abstract

Gastric cancer (GC) is one of the most common malignant tumors. The mechanism of GC radioresistance and new radiosensitizers must be revealed and developed to treat GC. Serine hydroxymethyltransferase 2 (SHMT2) is responsible for encoding the mitochondrial form of the pyridoxal phosphate-dependent enzyme. SHMT2 plays a critical role in several types of cancers, while its possible effect on the radiological resistance in GC is still unclear. In this study, we investigated the role of SHMT2 in the radiological resistance of GC. Our data confirmed that SHMT2 was highly expressed in radiation-resistant GC cells. SHMT2 reduced the radiosensitivity of GC cells. In addition, SHMT2 is involved in radiation-induced GC cell apoptosis. Further, SHMT2 regulated the Wnt/β-catenin pathway, therefore reducing the radiosensitivity of GC cells in vivo. In conclusion, we revealed that depletion of SHMT2 enhanced the sensitivity of GC cells to interventional radiotherapy through the Wnt/β-catenin pathway.

Keywords: gastric cancer; SHMT2; apoptosis; radiosensitivity; Wnt/β-catenin pathway

1 Introduction

Gastric cancer (GC) is one of the most common malignant tumors [1,2]. Radiotherapy is the main treatment method for advanced GC patients. However, GC patients have limited benefits from radiation therapy, and most patients develop a tolerance to radiation therapy [3]. Although multiple genes are involved in mediating radiosensitivity in different cancers, the precise mechanisms of radioresistance in GC remain unknown.

Serine hydroxymethyltransferase 2 (SHMT2) is responsible for encoding the mitochondrial form of the pyridoxal phosphate-dependent enzyme [4]. SHMT2 is mainly involved in catalyzing the conversion of serine to glycine and the transfer of β-carbon from serine to hydrolyzed tetrahydrofluoric (THF) acid to form 5, 10-methylene tetrahydrofolate (Me THF) [5]. SHMT2 plays a regulatory role in cell proliferation [4]. High expression of SHMT2 has also been shown to predict the poor prognosis of GC and promote its progression [6]. SHMT2 levels are associated with elevated levels of β-catenin and CRC progression and can predict poor patient survival. Low expression of SHMT2 enhances sensitivity to 5-fluorouracil in colorectal cancer [7]. Higher SHTM2 expression was also observed in lapatinib-resistant breast cancer cells, and activation of SHMT2 enhanced breast cancer cell resistance to lapatinib [8].

Wnt signaling has been shown to play important roles in different cellular processes, including the regulation of cell proliferation, differentiation, migration, survival, and stem cell self-renewal [9]. Wnt inhibits β-catenin degradation, stabilizes β-catenin, and leads to β-catenin accumulation in the nucleus, ultimately controlling the expression of downstream target genes [10]. Studies have shown that the dysregulation of the Wnt/β-catenin signaling pathway is closely related to the occurrence of various human cancers [11]. In addition, the Wnt/β-catenin signaling pathway was found to mediate cancer radioresistance by participating in DNA damage repair. Together, these data support that activation of Wnt/β-catenin signaling plays a key role in tumorigenesis and radiological resistance.

In this study, we investigated the role of SHMT2 in the radioresistance of GC cells. Our data confirmed that SHMT2 affected the sensitivity of GC cells to interventional radiotherapy via the Wnt/β-catenin axis. Therefore, we confirmed that SHMT2 could serve as a target for the radioresistance of GC.

2 Materials and methods

2.1 Cell culture

The human GC cell lines, AGS and MKN45, were obtained from the ATCC (USA). To establish the radioresistant (RR) GC cell line, cells were exposed to a sublethal dose of irradiation for 6 months via the Small Animal Radiation Research Platform (Xstrahl, USA, 2018). The total exposure dose was 60 Gy. AGS and MKN45 were incubated with RPMI-1640 (HyClone, USA) supplied with 10% fetal bovine serum (Gibco, USA), as well as 1% penicillin–streptomycin. The resistant AGS and MKN45 cells were marked as AGS-R and MKN45-R, respectively.

2.2 Cell transfection

For the knockdown of SHMT2, a lentivirus-mediated delivery system, pLKD-CMV-G&PR-U6-shRNA (SHMT2) (4912, OBiO Technology, Shanghai, China), was used. Lentiviral shRNA targeting SHMT2 in this study was listed: 5′-CCGGAGAGTTGTGGACTTT-3′. Cell selection was performed with 2 μg/mL puromycin for 2 weeks.

2.3 Colony formation assay

Cells after indicated irradiation dose were seeded in 6-well plates (600/well). Ten days after irradiation, cells were fixed with 4% paraformaldehyde and cultured with 0.5% crystal violet. The colony numbers were counted manually.

2.4 Western blotting

Cell lysates were collected using RIPA buffer. Proteins were subjected to 10% sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) and transferred onto polyvinylidene difluoride membranes. Then, membranes were incubated with 5% BSA followed by primary antibodies targeting SHMT2 (1:1,000, CST), Bcl-2 (1:1,000, Abcam, Cambridge, UK), Bax (1:1,000, Abcam, Cambridge, UK), β-catenin (1:1,000, CST), Axin (1:1,000, CST), c-myc (1:1,000, Abcam), and GAPDH (1:10,000; Abcam). Membranes were incubated with horse radish peroxide-conjugated secondary antibodies (The catalog number was: mice [cat. no. 7076] and rabbit [cat. no. 7074; both from Cell Signaling Technology, Inc.]) at a 1:5,000 for 2 h after rinsing in TBST for 15 min. The signals were detected with an ECL detection kit.

2.5 Flow cytometry

Cells were placed into a 24-well plate. After indicated treatment, 106 cells were fixed and stained with fluorescein isothiocynate (FITC) and propidium iodide for 30 min in dark. Then, stained cells were washed by centrifugation and resuspend and analyzed on a BD FACS Canto II (BD Biosciences).

2.6 Statistical analysis

Data were represented by mean ± SD. Statistical analysis was performed using GraphPad. P < 0.05 was considered statistically significant. In the cell viability, colony formation, FCM, and Immunoblot assays, AGS-R vs AGS, * P < 0.05 ** P < 0.01, ***P < 0.001; ^ P < 0.05, ^^ P < 0.01, ^^^ P < 0.001 MKN45-R vs MKN45.

3 Results

3.1 Construction of RR GC cell line

For the construction of the RR GC cell line, AGS and MKN45 cells were exposed to fractioned irradiation at a total dose of 60 Gy for 6 months and validated to be RR. Colony number was significantly higher in the RR cells when compared with parental at varying doses of irradiation (Figure 1a and b). The quantification of survival fraction was also higher in RR cells (Figure 1c and d). Moreover, SHMT2 was upregulated in the RR of GC cells (Figure 1e). These results suggested that SHMT2 was upregulated in RR cells.

Figure 1 Construction of radioresistant (RR) GC cell line. (a) Colony formation assay in AGS and AGS-R cells treated with varying irradiations. The colony numbers were calculated. (b) Colony formation assay in MKN45 and MKN45-R cells treated with varying irradiations. The colony numbers were calculated. (c and d) The survival fraction as quantified from (a) and (b). (e) The expression of SHMT2 in AGS, AGS-R, MKN45, and MKN45-R cells. Data were represented by mean ± SD. ** P < 0.01, ***P < 0.001 AGS-R vs AGS, and ^ P < 0.05 MKN45-R vs MKN45.
Figure 1

Construction of radioresistant (RR) GC cell line. (a) Colony formation assay in AGS and AGS-R cells treated with varying irradiations. The colony numbers were calculated. (b) Colony formation assay in MKN45 and MKN45-R cells treated with varying irradiations. The colony numbers were calculated. (c and d) The survival fraction as quantified from (a) and (b). (e) The expression of SHMT2 in AGS, AGS-R, MKN45, and MKN45-R cells. Data were represented by mean ± SD. ** P < 0.01, ***P < 0.001 AGS-R vs AGS, and ^ P < 0.05 MKN45-R vs MKN45.

3.2 SHMT2 ablation sensitizes RR GC to irradiation

To reveal the role of SHMT2 in GC sensitivity to irradiation, we knocked down SHMT2 in GC cells and the knockdown efficiency was confirmed (Figure 2a). The role of SHMT2 in irradiation sensitivity was determined by colony formation assay. Interestingly, downregulation of SHMT2 decreased cell colony formation in response to an increased dose of irradiation compared with RR GC cells (Figure 2b and c). The decreased survival fraction in SHMT2 knockdown cells also confirmed the increased sensitivity to irradiation in RR cells (Figure 2d and e).

Figure 2 SHMT2 ablation sensitizes RR GC to irradiation. (a) The immunoblot confirmed the silencing efficiency in AGS-R and MKN45-R cells. (b) Colony formation assay in AGS-R cells treated with sh-NC and sh-SHMT2 and varying irradiations. (c) Colony formation assay in MKN45-R cells treated with sh-NC and sh-SHMT2 and varying irradiations. (d and e) The survival fraction as quantified from A, B. Data was represented by mean ± SD. ** P < 0.01, ***P < 0.001.
Figure 2

SHMT2 ablation sensitizes RR GC to irradiation. (a) The immunoblot confirmed the silencing efficiency in AGS-R and MKN45-R cells. (b) Colony formation assay in AGS-R cells treated with sh-NC and sh-SHMT2 and varying irradiations. (c) Colony formation assay in MKN45-R cells treated with sh-NC and sh-SHMT2 and varying irradiations. (d and e) The survival fraction as quantified from A, B. Data was represented by mean ± SD. ** P < 0.01, ***P < 0.001.

3.3 SHMT2 knockdown promoted radiation-induced GC cell apoptosis

To detect the effect of SHMT2 on cell apoptosis, flow cytometry was performed in RR GC cells. Flow cytometry analysis showed that SHMT2 knockdown led to enhanced cell apoptosis in 4 Gy irradiation conditions (Figure 3a). Moreover, the level of Bax was increased and Bcl-2 was repressed in SHMT2 knockdown RR cells with and without irradiation (Figure 3b). Overexpression of SHMT2 promoted viability and suppressed the apoptosis of RR GC cells (Figure S1a–c). Taken together, SHMT2 knockdown induces cell apoptosis of GC stimulated with radiation.

Figure 3 SHMT2 promoted radiation-induced GC cell apoptosis. (a) Cell apoptosis in AGS-R and MKN45-R cells treated with sh-NC and sh-SHMT2 and irradiations. (b) The level of bax and bcl-2 in AGS-R and MKN45-R cells treated with sh-NC and sh-SHMT2 and irradiations. The sh-NC was used as the statistical control group in the whole experiment. Data were represented by mean ± SD. ** P < 0.01, ***P < 0.001 AGS-R vs AGS, ^^ P < 0.01, and ^^^ P < 0.001 MKN45-R vs MKN45.
Figure 3

SHMT2 promoted radiation-induced GC cell apoptosis. (a) Cell apoptosis in AGS-R and MKN45-R cells treated with sh-NC and sh-SHMT2 and irradiations. (b) The level of bax and bcl-2 in AGS-R and MKN45-R cells treated with sh-NC and sh-SHMT2 and irradiations. The sh-NC was used as the statistical control group in the whole experiment. Data were represented by mean ± SD. ** P < 0.01, ***P < 0.001 AGS-R vs AGS, ^^ P < 0.01, and ^^^ P < 0.001 MKN45-R vs MKN45.

3.4 SHMT2 affected the sensitivity of GC cells to interventional radiotherapy via the Wnt/β-catenin pathway

We noticed a reduced level of β-catenin and c-myc, and an enhanced level of axin in SHMT2 knockdown RR cells with or without irradiation (Figure 4a). We further performed rescue assays through CCK-8 and FCM assays in MKN45-R cells. Our results revealed that the knockdown of SHMT2 suppressed the viability and stimulated apoptosis (Figure 4b and c), whereas overexpression of β-catenin reversed these effects in MKN45-R cells (Figure 4b and c). Altogether, knockdown of SHMT2 enhanced the sensitivity of GC cells to interventional radiotherapy through the Wnt/β-catenin pathway.

Figure 4 SHMT2 affected the sensitivity of GC cells to interventional radiotherapy via the Wnt/β-catenin pathway. (a) The expression of β-catenin, axin, and c-myc in AGS-R and MKN45-R cells treated with sh-NC and sh-SHMT2 and irradiations. (b) CCK-8 assays showed the viability of MKN45-R cells upon the indicated transfection. (c) FCM assays showed the apoptosis levels of MKN45-R cells upon the indicated transfection. The sh-NC was used as the statistical control group in the whole experiment. Data were represented by mean ± SD. ** P < 0.01, ***P < 0.001 AGS-R vs AGS, ^ P < 0.05, and ^^^ P < 0.001 MKN45-R vs MKN45.
Figure 4

SHMT2 affected the sensitivity of GC cells to interventional radiotherapy via the Wnt/β-catenin pathway. (a) The expression of β-catenin, axin, and c-myc in AGS-R and MKN45-R cells treated with sh-NC and sh-SHMT2 and irradiations. (b) CCK-8 assays showed the viability of MKN45-R cells upon the indicated transfection. (c) FCM assays showed the apoptosis levels of MKN45-R cells upon the indicated transfection. The sh-NC was used as the statistical control group in the whole experiment. Data were represented by mean ± SD. ** P < 0.01, ***P < 0.001 AGS-R vs AGS, ^ P < 0.05, and ^^^ P < 0.001 MKN45-R vs MKN45.

4 Discussion

GC is a malignant tumor with high morbidity and mortality, which is difficult to eradicate except for surgical resection after early detection [12]. Existing treatment methods, such as surgery, radiotherapy, and chemotherapy, are limited for GC treatment [13]. In the past, radiotherapy was not suitable for the treatment of GC either alone or in combination [14]. The main reasons include the following: GC is mostly adenocarcinoma, and adenocarcinoma is not sensitive to radiation [15]. Here, we noticed downregulation of SHMT2 enhanced the sensitivity of GC cells to interventional radiotherapy.

We constructed a radiotherapy-resistance GC cell line and performed a series of in vitro assays such as Immunoblot, CCK-8, and FCM, and the results revealed that SHMT2 was highly expressed in radiotherapy-resistance GC cells and reduced the radiosensitivity of GC cells, and stimulate cell apoptosis. In fact, proliferation, and apoptosis could be affected by radiotherapy in cancer cells. In RR cancer cells, radiotherapy had no obvious effects on the proliferation and apoptosis of cancer cells. The effects of SHMT2 on cancer progression and metastasis have been widely revealed. For example, SHMT2 knockdown disrupted the TCF3 transcriptional survival program in lymphoma [16]. Overexpression of SHMT2 was correlated with a poor prognosis and promoted tumor growth in bladder cancer and thyroid cancer [17,18]. In addition, loss of SHMT2 could mediate 5-fluorouracil chemoresistance in colorectal cancer via promoting autophagy [19]. Similarly, we revealed its effects on the radiotherapy sensitivity of GC cells. The depletion of SHMT2 could suppress the progression of tongue squamous cell carcinoma by mediating the cell cycle [20]. We should further detect the effects of SHMT2 on the cell cycle of RR cancer cells. Another study indicated that higher SHTM2 expression was also observed in lapatinib-resistant breast cancer cells, and activation of SHMT2 enhanced breast cancer cell resistance to lapatinib [21]. All these studies confirmed that SHMT2 could serve as a promising target for cancer treatment.

Notably, SHMT2 could drive the progression and metastasis of colorectal cancer via suppressing β-catenin degradation. Similarly, here, we also showed that SHMT2 affected the sensitivity of GC cells to interventional radiotherapy via this pathway. This pathway has been revealed to affect the proliferation and motility of tumors and affect the EMT progression of several types of cancers, including GC [9]. Multiple proteins or drugs affected GC progression via this pathway. Importantly, this pathway was involved in the radiotherapy resistance of GC cells. For example, DOCK6 contributed to chemo- and radioresistance of GC cells via this pathway [10]. LincRNA-p21 promoted the sensitivity of radiotherapy for GC via this pathway [22]. These studies confirmed that Wnt/β-catenin was a critical target to improve the radiotherapy-resistance of GC cells.

In summary, we constructed a RR GC cell line and investigated the role of SHMT2 in this cell line. Our data confirmed that SHMT2 was highly expressed in RR GC cells and affected the sensitivity of GC cells to radiotherapy via the Wnt/β-catenin pathway. We therefore confirmed that SHMT2 could serve as a target for the radioresistance of GC.

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  1. Funding information: Authors state no funding is involved.

  2. Author contributions: Yu Mao designed the study and carried it out; Tioyong Zhang supervised the data collection, analyzed the data, and interpreted the data; Yu Mao and Tioyong Zhang prepared the manuscript for publication and reviewed the draft of the manuscript. All authors have read and approved the manuscript.

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

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

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Received: 2022-02-25
Revised: 2022-05-20
Accepted: 2022-07-18
Published Online: 2022-09-19

© 2022 Yu Mao and Tiyong Zhang, published by De Gruyter

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

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  80. Application of metagenomic next-generation sequencing technique for diagnosing a specific case of necrotizing meningoencephalitis caused by human herpesvirus 2
  81. Case report: Quadruple primary malignant neoplasms including esophageal, ureteral, and lung in an elderly male
  82. Long non-coding RNA NEAT1 promotes angiogenesis in hepatoma carcinoma via the miR-125a-5p/VEGF pathway
  83. Osteogenic differentiation of periodontal membrane stem cells in inflammatory environments
  84. Knockdown of SHMT2 enhances the sensitivity of gastric cancer cells to radiotherapy through the Wnt/β-catenin pathway
  85. Continuous renal replacement therapy combined with double filtration plasmapheresis in the treatment of severe lupus complicated by serious bacterial infections in children: A case report
  86. Simultaneous triple primary malignancies, including bladder cancer, lymphoma, and lung cancer, in an elderly male: A case report
  87. Preclinical immunogenicity assessment of a cell-based inactivated whole-virion H5N1 influenza vaccine
  88. One case of iodine-125 therapy – A new minimally invasive treatment of intrahepatic cholangiocarcinoma
  89. S1P promotes corneal trigeminal neuron differentiation and corneal nerve repair via upregulating nerve growth factor expression in a mouse model
  90. Early cancer detection by a targeted methylation assay of circulating tumor DNA in plasma
  91. Calcifying nanoparticles initiate the calcification process of mesenchymal stem cells in vitro through the activation of the TGF-β1/Smad signaling pathway and promote the decay of echinococcosis
  92. Evaluation of prognostic markers in patients infected with SARS-CoV-2
  93. N6-Methyladenosine-related alternative splicing events play a role in bladder cancer
  94. Characterization of the structural, oxidative, and immunological features of testis tissue from Zucker diabetic fatty rats
  95. Effects of glucose and osmotic pressure on the proliferation and cell cycle of human chorionic trophoblast cells
  96. Investigation of genotype diversity of 7,804 norovirus sequences in humans and animals of China
  97. Characteristics and karyotype analysis of a patient with turner syndrome complicated with multiple-site tumors: A case report
  98. Aggravated renal fibrosis is positively associated with the activation of HMGB1-TLR2/4 signaling in STZ-induced diabetic mice
  99. Distribution characteristics of SARS-CoV-2 IgM/IgG in false-positive results detected by chemiluminescent immunoassay
  100. SRPX2 attenuated oxygen–glucose deprivation and reperfusion-induced injury in cardiomyocytes via alleviating endoplasmic reticulum stress-induced apoptosis through targeting PI3K/Akt/mTOR axis
  101. Aquaporin-8 overexpression is involved in vascular structure and function changes in placentas of gestational diabetes mellitus patients
  102. Relationship between CRP gene polymorphisms and ischemic stroke risk: A systematic review and meta-analysis
  103. Effects of growth hormone on lipid metabolism and sexual development in pubertal obese male rats
  104. Cloning and identification of the CTLA-4IgV gene and functional application of vaccine in Xinjiang sheep
  105. Antitumor activity of RUNX3: Upregulation of E-cadherin and downregulation of the epithelial–mesenchymal transition in clear-cell renal cell carcinoma
  106. PHF8 promotes osteogenic differentiation of BMSCs in old rat with osteoporosis by regulating Wnt/β-catenin pathway
  107. A review of the current state of the computer-aided diagnosis (CAD) systems for breast cancer diagnosis
  108. Bilateral dacryoadenitis in adult-onset Still’s disease: A case report
  109. A novel association between Bmi-1 protein expression and the SUVmax obtained by 18F-FDG PET/CT in patients with gastric adenocarcinoma
  110. The role of erythrocytes and erythroid progenitor cells in tumors
  111. Relationship between platelet activation markers and spontaneous abortion: A meta-analysis
  112. Abnormal methylation caused by folic acid deficiency in neural tube defects
  113. Silencing TLR4 using an ultrasound-targeted microbubble destruction-based shRNA system reduces ischemia-induced seizures in hyperglycemic rats
  114. Plant Sciences
  115. Seasonal succession of bacterial communities in cultured Caulerpa lentillifera detected by high-throughput sequencing
  116. Cloning and prokaryotic expression of WRKY48 from Caragana intermedia
  117. Novel Brassica hybrids with different resistance to Leptosphaeria maculans reveal unbalanced rDNA signal patterns
  118. Application of exogenous auxin and gibberellin regulates the bolting of lettuce (Lactuca sativa L.)
  119. Phytoremediation of pollutants from wastewater: A concise review
  120. Genome-wide identification and characterization of NBS-encoding genes in the sweet potato wild ancestor Ipomoea trifida (H.B.K.)
  121. Alleviative effects of magnetic Fe3O4 nanoparticles on the physiological toxicity of 3-nitrophenol to rice (Oryza sativa L.) seedlings
  122. Selection and functional identification of Dof genes expressed in response to nitrogen in Populus simonii × Populus nigra
  123. Study on pecan seed germination influenced by seed endocarp
  124. Identification of active compounds in Ophiopogonis Radix from different geographical origins by UPLC-Q/TOF-MS combined with GC-MS approaches
  125. The entire chloroplast genome sequence of Asparagus cochinchinensis and genetic comparison to Asparagus species
  126. Genome-wide identification of MAPK family genes and their response to abiotic stresses in tea plant (Camellia sinensis)
  127. Selection and validation of reference genes for RT-qPCR analysis of different organs at various development stages in Caragana intermedia
  128. Cloning and expression analysis of SERK1 gene in Diospyros lotus
  129. Integrated metabolomic and transcriptomic profiling revealed coping mechanisms of the edible and medicinal homologous plant Plantago asiatica L. cadmium resistance
  130. A missense variant in NCF1 is associated with susceptibility to unexplained recurrent spontaneous abortion
  131. Assessment of drought tolerance indices in faba bean genotypes under different irrigation regimes
  132. The entire chloroplast genome sequence of Asparagus setaceus (Kunth) Jessop: Genome structure, gene composition, and phylogenetic analysis in Asparagaceae
  133. Food Science
  134. Dietary food additive monosodium glutamate with or without high-lipid diet induces spleen anomaly: A mechanistic approach on rat model
  135. Binge eating disorder during COVID-19
  136. Potential of honey against the onset of autoimmune diabetes and its associated nephropathy, pancreatitis, and retinopathy in type 1 diabetic animal model
  137. FTO gene expression in diet-induced obesity is downregulated by Solanum fruit supplementation
  138. Physical activity enhances fecal lactobacilli in rats chronically drinking sweetened cola beverage
  139. Supercritical CO2 extraction, chemical composition, and antioxidant effects of Coreopsis tinctoria Nutt. oleoresin
  140. Functional constituents of plant-based foods boost immunity against acute and chronic disorders
  141. Effect of selenium and methods of protein extraction on the proteomic profile of Saccharomyces yeast
  142. Microbial diversity of milk ghee in southern Gansu and its effect on the formation of ghee flavor compounds
  143. Ecology and Environmental Sciences
  144. Effects of heavy metals on bacterial community surrounding Bijiashan mining area located in northwest China
  145. Microorganism community composition analysis coupling with 15N tracer experiments reveals the nitrification rate and N2O emissions in low pH soils in Southern China
  146. Genetic diversity and population structure of Cinnamomum balansae Lecomte inferred by microsatellites
  147. Preliminary screening of microplastic contamination in different marine fish species of Taif market, Saudi Arabia
  148. Plant volatile organic compounds attractive to Lygus pratensis
  149. Effects of organic materials on soil bacterial community structure in long-term continuous cropping of tomato in greenhouse
  150. Effects of soil treated fungicide fluopimomide on tomato (Solanum lycopersicum L.) disease control and plant growth
  151. Prevalence of Yersinia pestis among rodents captured in a semi-arid tropical ecosystem of south-western Zimbabwe
  152. Effects of irrigation and nitrogen fertilization on mitigating salt-induced Na+ toxicity and sustaining sea rice growth
  153. Bioengineering and Biotechnology
  154. Poly-l-lysine-caused cell adhesion induces pyroptosis in THP-1 monocytes
  155. Development of alkaline phosphatase-scFv and its use for one-step enzyme-linked immunosorbent assay for His-tagged protein detection
  156. Development and validation of a predictive model for immune-related genes in patients with tongue squamous cell carcinoma
  157. Agriculture
  158. Effects of chemical-based fertilizer replacement with biochar-based fertilizer on albic soil nutrient content and maize yield
  159. Genome-wide identification and expression analysis of CPP-like gene family in Triticum aestivum L. under different hormone and stress conditions
  160. Agronomic and economic performance of mung bean (Vigna radiata L.) varieties in response to rates of blended NPS fertilizer in Kindo Koysha district, Southern Ethiopia
  161. Influence of furrow irrigation regime on the yield and water consumption indicators of winter wheat based on a multi-level fuzzy comprehensive evaluation
  162. Discovery of exercise-related genes and pathway analysis based on comparative genomes of Mongolian originated Abaga and Wushen horse
  163. Lessons from integrated seasonal forecast-crop modelling in Africa: A systematic review
  164. Evolution trend of soil fertility in tobacco-planting area of Chenzhou, Hunan Province, China
  165. Animal Sciences
  166. Morphological and molecular characterization of Tatera indica Hardwicke 1807 (Rodentia: Muridae) from Pothwar, Pakistan
  167. Research on meat quality of Qianhua Mutton Merino sheep and Small-tail Han sheep
  168. SI: A Scientific Memoir
  169. Suggestions on leading an academic research laboratory group
  170. My scientific genealogy and the Toronto ACDC Laboratory, 1988–2022
  171. Erratum
  172. Erratum to “Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study”
  173. Erratum to “A two-microRNA signature predicts the progression of male thyroid cancer”
  174. Retraction
  175. Retraction of “Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis”
https://doi.org/10.1515/biol-2022-0480
Schlagwörter für diesen Artikel
gastric cancer; SHMT2; apoptosis; radiosensitivity; Wnt/β-catenin pathway
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Artikel in diesem Heft

  1. Biomedical Sciences
  2. Effects of direct oral anticoagulants dabigatran and rivaroxaban on the blood coagulation function in rabbits
  3. The mother of all battles: Viruses vs humans. Can humans avoid extinction in 50–100 years?
  4. Knockdown of G1P3 inhibits cell proliferation and enhances the cytotoxicity of dexamethasone in acute lymphoblastic leukemia
  5. LINC00665 regulates hepatocellular carcinoma by modulating mRNA via the m6A enzyme
  6. Association study of CLDN14 variations in patients with kidney stones
  7. Concanavalin A-induced autoimmune hepatitis model in mice: Mechanisms and future outlook
  8. Regulation of miR-30b in cancer development, apoptosis, and drug resistance
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  11. Characterization of intestinal microbiota and serum metabolites in patients with mild hepatic encephalopathy
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  13. Application of the FLP/LoxP-FRT recombination system to switch the eGFP expression in a model prokaryote
  14. Biomedical evaluation of antioxidant properties of lamb meat enriched with iodine and selenium
  15. Intravenous infusion of the exosomes derived from human umbilical cord mesenchymal stem cells enhance neurological recovery after traumatic brain injury via suppressing the NF-κB pathway
  16. Effect of dietary pattern on pregnant women with gestational diabetes mellitus and its clinical significance
  17. Potential regulatory mechanism of TNF-α/TNFR1/ANXA1 in glioma cells and its role in glioma cell proliferation
  18. Effect of the genetic mutant G71R in uridine diphosphate-glucuronosyltransferase 1A1 on the conjugation of bilirubin
  19. Quercetin inhibits cytotoxicity of PC12 cells induced by amyloid-beta 25–35 via stimulating estrogen receptor α, activating ERK1/2, and inhibiting apoptosis
  20. Nutrition intervention in the management of novel coronavirus pneumonia patients
  21. circ-CFH promotes the development of HCC by regulating cell proliferation, apoptosis, migration, invasion, and glycolysis through the miR-377-3p/RNF38 axis
  22. Bmi-1 directly upregulates glucose transporter 1 in human gastric adenocarcinoma
  23. Lacunar infarction aggravates the cognitive deficit in the elderly with white matter lesion
  24. Hydroxysafflor yellow A improved retinopathy via Nrf2/HO-1 pathway in rats
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  26. Elevated IL-35 level and iTr35 subset increase the bacterial burden and lung lesions in Mycobacterium tuberculosis-infected mice
  27. A case report of CAT gene and HNF1β gene variations in a patient with early-onset diabetes
  28. Study on the mechanism of inhibiting patulin production by fengycin
  29. SOX4 promotes high-glucose-induced inflammation and angiogenesis of retinal endothelial cells by activating NF-κB signaling pathway
  30. Relationship between blood clots and COVID-19 vaccines: A literature review
  31. Analysis of genetic characteristics of 436 children with dysplasia and detailed analysis of rare karyotype
  32. Bioinformatics network analyses of growth differentiation factor 11
  33. NR4A1 inhibits the epithelial–mesenchymal transition of hepatic stellate cells: Involvement of TGF-β–Smad2/3/4–ZEB signaling
  34. Expression of Zeb1 in the differentiation of mouse embryonic stem cell
  35. Study on the genetic damage caused by cadmium sulfide quantum dots in human lymphocytes
  36. Association between single-nucleotide polymorphisms of NKX2.5 and congenital heart disease in Chinese population: A meta-analysis
  37. Assessment of the anesthetic effect of modified pentothal sodium solution on Sprague-Dawley rats
  38. Genetic susceptibility to high myopia in Han Chinese population
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  40. Silencing circular RNA-friend leukemia virus integration 1 restrained malignancy of CC cells and oxaliplatin resistance by disturbing dyskeratosis congenita 1
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  42. The significance of PAK4 in signaling and clinicopathology: A review
  43. Sorafenib inhibits ovarian cancer cell proliferation and mobility and induces radiosensitivity by targeting the tumor cell epithelial–mesenchymal transition
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  45. Active legumain promotes invasion and migration of neuroblastoma by regulating epithelial-mesenchymal transition
  46. Effect of cell receptors in the pathogenesis of osteoarthritis: Current insights
  47. MT-12 inhibits the proliferation of bladder cells in vitro and in vivo by enhancing autophagy through mitochondrial dysfunction
  48. Study of hsa_circRNA_000121 and hsa_circRNA_004183 in papillary thyroid microcarcinoma
  49. BuyangHuanwu Decoction attenuates cerebral vasospasm caused by subarachnoid hemorrhage in rats via PI3K/AKT/eNOS axis
  50. Effects of the interaction of Notch and TLR4 pathways on inflammation and heart function in septic heart
  51. Monosodium iodoacetate-induced subchondral bone microstructure and inflammatory changes in an animal model of osteoarthritis
  52. A rare presentation of type II Abernethy malformation and nephrotic syndrome: Case report and review
  53. Rapid death due to pulmonary epithelioid haemangioendothelioma in several weeks: A case report
  54. Hepatoprotective role of peroxisome proliferator-activated receptor-α in non-cancerous hepatic tissues following transcatheter arterial embolization
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  57. β-Hydroxybutyrate upregulates FGF21 expression through inhibition of histone deacetylases in hepatocytes
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  59. BTBD10 inhibits glioma tumorigenesis by downregulating cyclin D1 and p-Akt
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  61. Metagenomic next-generation sequencing in diagnosing Pneumocystis jirovecii pneumonia: A case report
  62. Long non-coding RNA HOXB-AS1 is a prognostic marker and promotes hepatocellular carcinoma cells’ proliferation and invasion
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  77. Geometric basis of action potential of skeletal muscle cells and neurons
  78. Babesia microti-induced fulminant sepsis in an immunocompromised host: A case report and the case-specific literature review
  79. Role of cerebellar cortex in associative learning and memory in guinea pigs
  80. Application of metagenomic next-generation sequencing technique for diagnosing a specific case of necrotizing meningoencephalitis caused by human herpesvirus 2
  81. Case report: Quadruple primary malignant neoplasms including esophageal, ureteral, and lung in an elderly male
  82. Long non-coding RNA NEAT1 promotes angiogenesis in hepatoma carcinoma via the miR-125a-5p/VEGF pathway
  83. Osteogenic differentiation of periodontal membrane stem cells in inflammatory environments
  84. Knockdown of SHMT2 enhances the sensitivity of gastric cancer cells to radiotherapy through the Wnt/β-catenin pathway
  85. Continuous renal replacement therapy combined with double filtration plasmapheresis in the treatment of severe lupus complicated by serious bacterial infections in children: A case report
  86. Simultaneous triple primary malignancies, including bladder cancer, lymphoma, and lung cancer, in an elderly male: A case report
  87. Preclinical immunogenicity assessment of a cell-based inactivated whole-virion H5N1 influenza vaccine
  88. One case of iodine-125 therapy – A new minimally invasive treatment of intrahepatic cholangiocarcinoma
  89. S1P promotes corneal trigeminal neuron differentiation and corneal nerve repair via upregulating nerve growth factor expression in a mouse model
  90. Early cancer detection by a targeted methylation assay of circulating tumor DNA in plasma
  91. Calcifying nanoparticles initiate the calcification process of mesenchymal stem cells in vitro through the activation of the TGF-β1/Smad signaling pathway and promote the decay of echinococcosis
  92. Evaluation of prognostic markers in patients infected with SARS-CoV-2
  93. N6-Methyladenosine-related alternative splicing events play a role in bladder cancer
  94. Characterization of the structural, oxidative, and immunological features of testis tissue from Zucker diabetic fatty rats
  95. Effects of glucose and osmotic pressure on the proliferation and cell cycle of human chorionic trophoblast cells
  96. Investigation of genotype diversity of 7,804 norovirus sequences in humans and animals of China
  97. Characteristics and karyotype analysis of a patient with turner syndrome complicated with multiple-site tumors: A case report
  98. Aggravated renal fibrosis is positively associated with the activation of HMGB1-TLR2/4 signaling in STZ-induced diabetic mice
  99. Distribution characteristics of SARS-CoV-2 IgM/IgG in false-positive results detected by chemiluminescent immunoassay
  100. SRPX2 attenuated oxygen–glucose deprivation and reperfusion-induced injury in cardiomyocytes via alleviating endoplasmic reticulum stress-induced apoptosis through targeting PI3K/Akt/mTOR axis
  101. Aquaporin-8 overexpression is involved in vascular structure and function changes in placentas of gestational diabetes mellitus patients
  102. Relationship between CRP gene polymorphisms and ischemic stroke risk: A systematic review and meta-analysis
  103. Effects of growth hormone on lipid metabolism and sexual development in pubertal obese male rats
  104. Cloning and identification of the CTLA-4IgV gene and functional application of vaccine in Xinjiang sheep
  105. Antitumor activity of RUNX3: Upregulation of E-cadherin and downregulation of the epithelial–mesenchymal transition in clear-cell renal cell carcinoma
  106. PHF8 promotes osteogenic differentiation of BMSCs in old rat with osteoporosis by regulating Wnt/β-catenin pathway
  107. A review of the current state of the computer-aided diagnosis (CAD) systems for breast cancer diagnosis
  108. Bilateral dacryoadenitis in adult-onset Still’s disease: A case report
  109. A novel association between Bmi-1 protein expression and the SUVmax obtained by 18F-FDG PET/CT in patients with gastric adenocarcinoma
  110. The role of erythrocytes and erythroid progenitor cells in tumors
  111. Relationship between platelet activation markers and spontaneous abortion: A meta-analysis
  112. Abnormal methylation caused by folic acid deficiency in neural tube defects
  113. Silencing TLR4 using an ultrasound-targeted microbubble destruction-based shRNA system reduces ischemia-induced seizures in hyperglycemic rats
  114. Plant Sciences
  115. Seasonal succession of bacterial communities in cultured Caulerpa lentillifera detected by high-throughput sequencing
  116. Cloning and prokaryotic expression of WRKY48 from Caragana intermedia
  117. Novel Brassica hybrids with different resistance to Leptosphaeria maculans reveal unbalanced rDNA signal patterns
  118. Application of exogenous auxin and gibberellin regulates the bolting of lettuce (Lactuca sativa L.)
  119. Phytoremediation of pollutants from wastewater: A concise review
  120. Genome-wide identification and characterization of NBS-encoding genes in the sweet potato wild ancestor Ipomoea trifida (H.B.K.)
  121. Alleviative effects of magnetic Fe3O4 nanoparticles on the physiological toxicity of 3-nitrophenol to rice (Oryza sativa L.) seedlings
  122. Selection and functional identification of Dof genes expressed in response to nitrogen in Populus simonii × Populus nigra
  123. Study on pecan seed germination influenced by seed endocarp
  124. Identification of active compounds in Ophiopogonis Radix from different geographical origins by UPLC-Q/TOF-MS combined with GC-MS approaches
  125. The entire chloroplast genome sequence of Asparagus cochinchinensis and genetic comparison to Asparagus species
  126. Genome-wide identification of MAPK family genes and their response to abiotic stresses in tea plant (Camellia sinensis)
  127. Selection and validation of reference genes for RT-qPCR analysis of different organs at various development stages in Caragana intermedia
  128. Cloning and expression analysis of SERK1 gene in Diospyros lotus
  129. Integrated metabolomic and transcriptomic profiling revealed coping mechanisms of the edible and medicinal homologous plant Plantago asiatica L. cadmium resistance
  130. A missense variant in NCF1 is associated with susceptibility to unexplained recurrent spontaneous abortion
  131. Assessment of drought tolerance indices in faba bean genotypes under different irrigation regimes
  132. The entire chloroplast genome sequence of Asparagus setaceus (Kunth) Jessop: Genome structure, gene composition, and phylogenetic analysis in Asparagaceae
  133. Food Science
  134. Dietary food additive monosodium glutamate with or without high-lipid diet induces spleen anomaly: A mechanistic approach on rat model
  135. Binge eating disorder during COVID-19
  136. Potential of honey against the onset of autoimmune diabetes and its associated nephropathy, pancreatitis, and retinopathy in type 1 diabetic animal model
  137. FTO gene expression in diet-induced obesity is downregulated by Solanum fruit supplementation
  138. Physical activity enhances fecal lactobacilli in rats chronically drinking sweetened cola beverage
  139. Supercritical CO2 extraction, chemical composition, and antioxidant effects of Coreopsis tinctoria Nutt. oleoresin
  140. Functional constituents of plant-based foods boost immunity against acute and chronic disorders
  141. Effect of selenium and methods of protein extraction on the proteomic profile of Saccharomyces yeast
  142. Microbial diversity of milk ghee in southern Gansu and its effect on the formation of ghee flavor compounds
  143. Ecology and Environmental Sciences
  144. Effects of heavy metals on bacterial community surrounding Bijiashan mining area located in northwest China
  145. Microorganism community composition analysis coupling with 15N tracer experiments reveals the nitrification rate and N2O emissions in low pH soils in Southern China
  146. Genetic diversity and population structure of Cinnamomum balansae Lecomte inferred by microsatellites
  147. Preliminary screening of microplastic contamination in different marine fish species of Taif market, Saudi Arabia
  148. Plant volatile organic compounds attractive to Lygus pratensis
  149. Effects of organic materials on soil bacterial community structure in long-term continuous cropping of tomato in greenhouse
  150. Effects of soil treated fungicide fluopimomide on tomato (Solanum lycopersicum L.) disease control and plant growth
  151. Prevalence of Yersinia pestis among rodents captured in a semi-arid tropical ecosystem of south-western Zimbabwe
  152. Effects of irrigation and nitrogen fertilization on mitigating salt-induced Na+ toxicity and sustaining sea rice growth
  153. Bioengineering and Biotechnology
  154. Poly-l-lysine-caused cell adhesion induces pyroptosis in THP-1 monocytes
  155. Development of alkaline phosphatase-scFv and its use for one-step enzyme-linked immunosorbent assay for His-tagged protein detection
  156. Development and validation of a predictive model for immune-related genes in patients with tongue squamous cell carcinoma
  157. Agriculture
  158. Effects of chemical-based fertilizer replacement with biochar-based fertilizer on albic soil nutrient content and maize yield
  159. Genome-wide identification and expression analysis of CPP-like gene family in Triticum aestivum L. under different hormone and stress conditions
  160. Agronomic and economic performance of mung bean (Vigna radiata L.) varieties in response to rates of blended NPS fertilizer in Kindo Koysha district, Southern Ethiopia
  161. Influence of furrow irrigation regime on the yield and water consumption indicators of winter wheat based on a multi-level fuzzy comprehensive evaluation
  162. Discovery of exercise-related genes and pathway analysis based on comparative genomes of Mongolian originated Abaga and Wushen horse
  163. Lessons from integrated seasonal forecast-crop modelling in Africa: A systematic review
  164. Evolution trend of soil fertility in tobacco-planting area of Chenzhou, Hunan Province, China
  165. Animal Sciences
  166. Morphological and molecular characterization of Tatera indica Hardwicke 1807 (Rodentia: Muridae) from Pothwar, Pakistan
  167. Research on meat quality of Qianhua Mutton Merino sheep and Small-tail Han sheep
  168. SI: A Scientific Memoir
  169. Suggestions on leading an academic research laboratory group
  170. My scientific genealogy and the Toronto ACDC Laboratory, 1988–2022
  171. Erratum
  172. Erratum to “Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study”
  173. Erratum to “A two-microRNA signature predicts the progression of male thyroid cancer”
  174. Retraction
  175. Retraction of “Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis”
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Heruntergeladen am 3.10.2025 von https://www.degruyterbrill.com/document/doi/10.1515/biol-2022-0480/html
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