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NUDT21 relieves sevoflurane-induced neurological damage in rats by down-regulating LIMK2

  • Yuanping Zhong , Pengcheng Zhao , Chao Zhang , Zhenyu Wu , Xu Fang and Zhaoqiong Zhu EMAIL logo
Published/Copyright: April 15, 2023
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Open Life Sciences
From the journal Open Life Sciences Volume 18 Issue 1

Abstract

Postoperative cognitive dysfunction (POCD) is a common complication of cognitive decline after surgery and anesthesia. Sevoflurane, as a commonly used anesthetic, was found to cause POCD. Nudix Hydrolase 21 (NUDT21), a conserved splicing factor, has been reported to exert important functions in multiple diseases’ progression. In this study, the effect of NUDT21 on sevoflurane-induced POCD was elucidated. Results showed that NUDT21 was down-regulated in the hippocampal tissue of sevoflurane-induced rats. Morris water maze test results revealed that overexpression of NUDT21 improved sevoflurane-induced cognitive impairment. In addition, TUNEL assay results indicated that enhanced NUDT21 alleviated sevoflurane-induced apoptosis of hippocampal neurons. Furthermore, overexpression of NUDT21 suppressed the sevoflurane-induced LIMK2 expression. Taken together, NUDT21 alleviates sevoflurane-induced neurological damage in rats by down-regulating LIMK2, providing a novel target for the prevention of sevoflurane-induced POCD.

Keywords: NUDT21; POCD; cognitive impairment; apoptosis; LIMK2

1 Introduction

Postoperative cognitive dysfunction (POCD) is a common complication with long-term consequences after surgery and anesthesia, characterized by cognitive decline [1,2,3]. Elderly patients are susceptible to suffering from POCD after surgery and anesthesia [4]. The incidence of POCD in elderly patients was 28.5% at 1 week after operation, and patients with POCD need a prolonged length of hospital stay and higher hospital costs [5]. POCD is proved to be associated with neurodegenerative diseases, such as Alzheimer’s disease in elderly patients [4,6]. Besides, patients with POCD showed significantly higher mortality than patients without POCD [7]. Therefore, POCD is a significant threat to public health, especially the health of elderly patients. Sevoflurane is a commonly used anesthetic in the clinic, and emerging evidence revealed that sevoflurane could induce POCD [8]. Hence, it is essential to investigate the mechanism of sevoflurane-induced neurotoxicity to prevent POCD.

Nudix Hydrolase 21 (NUDT21) is a member of the Nudix family of hydrolases and encodes Cleavage Factor Im 25 (CFIm25) [9]. It acts as a conserved splicing factor and is involved in eukaryotic pre-mRNA assembly due to possessing the cleavage factor Im (CFIm) complex [9,10]. Accumulating evidence revealed that NUDT21 participated in regulating many diseases [11,12,13]. For example, Weng et al. found that knockdown of NUDT21 amplified dermal fibrosis via alternative polyadenylation [11]. Zheng et al. reported that inhibition of NUDT21 suppressed proliferation and promoted apoptosis of pancreatic ductal adenocarcinoma via EIF2 signaling [12]. Sommerkamp et al. demonstrated that NUDT21 is involved in glutaminase isoform switching [13]. In addition, recent research revealed that NUDT21 participated in cognitive regulation [14]. Alcott et al. demonstrated that partial loss of NUDT21 caused learning deficits and aberrant neuronal alternative polyadenylation [14]. Furthermore, NUDT21 was proved to modulate the expression of LIMK2, a protein involved in neuronal growth and morphology, synaptic function, pain response, learning, and memory [9,15]. Therefore, we inferred that NUDT21 might be involved in sevoflurane-induced POCD.

In this study, the sevoflurane-induced rat model was constructed to investigate the effect of NUDT21 on neurological damage and to explore the potential mechanism. The findings revealed that NUDT21 improved sevoflurane-induced neurological damage via modulating LIMK2, providing a novel target for POCD prevention.

2 Materials and methods

2.1 Animals

Sprague-Dawley rats aged 15 months were acquired from Experimental Animal Center of Chongqing Medical University (Chongqing, China). All rats were allocated in the control, SEV, SEV + AAV-scramble, and SEV + AAV-NUDT21groups. There were nine rats in each group. The control group rats were exposed to mixed gas (1 L/min O2 + 1 L/min air), while the rats in the SEV group were exposed to 3.2% sevoflurane with a total flow of 1 L/min O2 and 1 L/min air for 2 h. The rats in the SEV + AAV-scramble group and the SEV + AAV-NUDT21group were first injected with 3.5 × 1010 drp AAV-scramble or AAV-NUDT21 (Hanbio, Shanghai, China) to one hippocampus (stratum lacunosum moleculare). These rats were exposed to 3.2% sevoflurane with a total flow of 1 L/min O2 and 1 L/min air 1 month later.

  1. Ethical approval: The research related to animal use has been complied with all the relevant national regulations and institutional policies for the care and use of animals and has been aproved by the Ethics Committee of AffiliatedHospital of Zunyi Medical University (Approval No. KLL-2021-342).

2.2 Quantitative real-time polymerase chain reaction (qRT-PCR)

RNA sample isolation was conducted utilizing the PureLink™ RNA Mini Kit, and cDNA was generated using the DyNAmo cDNA Synthesis Kit (Thermo Fisher Scientific, Waltham, MA, USA). For NUDT21 mRNA detection, DyNAmo Flash SYBR Green qPCR Kit (Thermo Fisher Scientific, Waltham, MA, USA) was applied to qRT-PCRs on Light Cycler 480 II Real-Time PCR System (Roche Diagnostics, Basel, Switzerland) using GAPDH as the control. The primer sequences of NUDT21 [16] are presented in Table 1. The relative expression was calculated using the 2−ΔΔCT method.

Table 1

The primer sequences used in qRT-PCR

Gene name Forward Reverse
NUDT21 5′-GTCAACCAGTTCGGCAACAAG-3′ 5′-AGCTGTCCTTCTCATAGAGGG-3′

2.3 Western blot

Tissues were homogenized by radio-immunoprecipitation (RIPA) assay lysis buffer, and concentration determination was determined using the bicinchoninic acid (BCA) method. Tissue lysate was size-fractionated on sodium dodecyl sulfate polyacrylamide gel electrophoresis (SDS-PAGE) gels and transferred to PVDF membranes. The membranes were incubated with primary antibodies including NUDT21 (1:500), Bax (1:1,000), Bcl-2 (1:1,000), and GAPDH (1:2,500) antibodies (Abcam, Cambridge, MA, UK) overnight at 4°C after impeding non-specific binding, followed by treating with secondary antibody IgG H&L (HRP) (Abcam, Cambridge, MA, UK) at 37°C. After that, the blots were visualized utilizing the ECL detection system (Bio-Rad, Hercules, CA, USA).

2.4 Morris water maze test

Morris water maze test was used to evaluate the cognitive ability of rats [17]. The water maze consisted of a circular pool with 120 cm in diameter and filled with opaque water of 22°C. The maze was designated as four quadrants, and an escape platform was put in a quadrant at about 2 cm underwater. The rats were trained for 4 days with 4 trials each day, followed by a probe trial on the fifth day. During the training, rats were allowed to swim in the pool for the 120 s, and the time reached the platform was recorded. If the rats found the platform, the rat stayed on the platform for 10 s. If the rats did not find the platform, they were guided to the platform. During the probe trial, the rat was placed in the pool and swam for 60 s. The time crossing the platform and the time in the target quadrant were recorded. Besides, the swim routes of the rats were tracked automatically.

2.5 Terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL)

For hippocampal tissue neurons apoptosis determination, TUNEL assay was conducted utilizing Click-iT Plus TUNEL Assay Kit (Invitrogen) in line with the supplier’s protocols. In short, tissue slides were fixed in 4% paraformaldehyde and permeabilized in proteinase K solution for 15 min, respectively. Then, the TdT reaction buffer was added to the slides for 10 min at 37°C, followed by incubating with the Click-iT™ Plus TUNEL reaction cocktail for 30 min at 37°C protected from light. Afterward, the cell nucleus was dyed with DAPI. The fluorescence microscope observed the staining results. The apoptosis proportion is the ratio of TUNEL-positive cells to the total cells.

2.6 Immunofluorescence

For immunofluorescence, tissues were immersed in 4% paraformaldehyde for fixation. After unmasking the epitope using 0.2% Triton X-100 and blocking nonspecific binding using 3% BSA, the tissues were probed with anti-LIMK2 antibody (1:200; Cell Signaling Technology) overnight at −4°C. Then, tissues were incubated with secondary antibody IgG H&L (HRP) (Alexa Fluor® 594) (Abcam, Cambridge, MA, UK) for 1 h at room temperature. The cell nucleus was dyed with DAPI. The staining images were obtained under a confocal laser scanning microscopy.

2.7 Statistical analysis

Data were represented as mean ± standard deviation and statistically analyzed with SPSS 20.0 (IBM, SPSS, Chicago, IL, USA). Student’s t-test and one-way analysis of variance were typically used to test group difference. P < 0.05 was assumed to be statistically significant.

3 Results

3.1 NUDT21 was down-regulated in the hippocampal tissue of sevoflurane-induced rat

To investigate the action of NUDT21 on sevoflurane-induced COPD, the expression of NUDT21 in rats treated with 3% sevoflurane for 6 h was detected. NUDT21 mRNA was found to be decreased in hippocampal tissue of sevoflurane-induced rats (P < 0.01, Figure 1a). Similarly, Western blot results showed that the protein level of NUDT21 was reduced in hippocampal tissue of sevoflurane-induced rats (P < 0.01, Figure 1b). Therefore, NUDT21 was down-regulated in the hippocampal tissue of sevoflurane-induced rats.

Figure 1 NUDT21 was down-regulated in the hippocampal tissue of sevoflurane-induced rats. (a) The NUDT21 mRNA in hippocampal tissue of sevoflurane-induced rats was determined using qRT-PCR. (b) The protein level of NUDT21 in hippocampal tissue of sevoflurane-induced rats was detected using western blot. **P < 0.01.
Figure 1

NUDT21 was down-regulated in the hippocampal tissue of sevoflurane-induced rats. (a) The NUDT21 mRNA in hippocampal tissue of sevoflurane-induced rats was determined using qRT-PCR. (b) The protein level of NUDT21 in hippocampal tissue of sevoflurane-induced rats was detected using western blot. **P < 0.01.

3.2 NUDT21 improved sevoflurane-induced cognitive impairment in rats

To gain insight into the effect of NUDT21 on sevoflurane-induced neurological damage, the cognitive impairment of sevoflurane-induced rats was assessed after transfected with AAV-NUDT21. AAV-NUDT21 significantly enhanced the NUDT21 level (P < 0.01, Figure 2a). Morris water maze test was then conducted to evaluate the cognitive impairment of rats. The movement route of rats during the Morris water maze test is presented in Figure 2b. Results showed that the escape latency and swimming distance were increased in sevoflurane-induced rats, and enforced NUDT21 reversed the phenomenon (P < 0.01, Figure 2c). In addition, overexpressed NUDT21 increased the times of crossing target and time in the target quadrant of sevoflurane-induced rats (P < 0.01, Figure 2c). Taken together, NUDT21 improved sevoflurane-induced cognitive impairment in rats.

Figure 2 NUDT21 improved sevoflurane-induced cognitive impairment in rats. (a) The protein level of NUDT21 in hippocampal tissue of sevoflurane-induced rats after transfected with AAV-NUDT21 was detected by western blot. (b) The movement route of sevoflurane-induced rats after transfected with AAV-NUDT21 was recorded during the Morris water maze test. (c) The escape latency, swimming distance, times of crossing target, and time in the target quadrant of sevoflurane-induced rats after transfected with AAV-NUDT21 were measured during the Morris water maze test. **P < 0.01. # P < 0.05. ## P < 0.01.
Figure 2

NUDT21 improved sevoflurane-induced cognitive impairment in rats. (a) The protein level of NUDT21 in hippocampal tissue of sevoflurane-induced rats after transfected with AAV-NUDT21 was detected by western blot. (b) The movement route of sevoflurane-induced rats after transfected with AAV-NUDT21 was recorded during the Morris water maze test. (c) The escape latency, swimming distance, times of crossing target, and time in the target quadrant of sevoflurane-induced rats after transfected with AAV-NUDT21 were measured during the Morris water maze test. **P < 0.01. # P < 0.05. ## P < 0.01.

3.3 NUDT21 improved sevoflurane-induced apoptosis of hippocampal neurons

Next, the role of NUDT21 in hippocampal neurons apoptosis of sevoflurane-induced rats was explored. TUNEL staining results showed that overexpression of NUDT21 suppressed sevoflurane-induced apoptosis of hippocampal neurons (P < 0.01, Figure 3a and b). The apoptosis-related protein Bax was increased, and Bcl-2 was decreased in hippocampal of sevoflurane-induced rats, which were reversed by overexpression of NUDT21 (P < 0.01, Figure 3c). Thus, the findings indicated that NUDT21 improved sevoflurane-induced apoptosis of hippocampal neurons.

Figure 3 NUDT21 ameliorated sevoflurane-induced neurons apoptosis in hippocampal tissue. (a) Hippocampal neurons apoptosis of sevoflurane-induced rats after transfected with AAV-NUDT21 was evaluated using TUNEL assay. (b) Quantitative results of apoptosis rate in hippocampal neurons of sevoflurane-induced rats after transfected with AAV-NUDT21. (c) The protein levels of Bax and Bcl-2 in hippocampal neurons of sevoflurane-induced rats after transfected with AAV-NUDT21 were detected using Western blot. **P < 0.01. ## P < 0.01.
Figure 3

NUDT21 ameliorated sevoflurane-induced neurons apoptosis in hippocampal tissue. (a) Hippocampal neurons apoptosis of sevoflurane-induced rats after transfected with AAV-NUDT21 was evaluated using TUNEL assay. (b) Quantitative results of apoptosis rate in hippocampal neurons of sevoflurane-induced rats after transfected with AAV-NUDT21. (c) The protein levels of Bax and Bcl-2 in hippocampal neurons of sevoflurane-induced rats after transfected with AAV-NUDT21 were detected using Western blot. **P < 0.01. ## P < 0.01.

3.4 NUDT21 down-regulated the expression of LIMK2

To clarify the possible mechanism of NUDT21 on sevoflurane-induced POCD, the expression of LIMK2 in the sevoflurane-induced rat after transfected with AAV-NUDT21 was assessed. Immunofluorescence staining results showed that sevoflurane treatment increased the expression of LIMK2 in hippocampal tissue of rats and it was inhibited by enforced NUDT21 (Figure 4a). Similarly, Western blot results also proved that overexpression of NUDT21 suppressed sevoflurane-induced LIMK2 level in hippocampal tissue of rats (P < 0.01, Figure 4b). Hence, NUDT21 decreased the expression of LIMK2 in sevoflurane-induced rats.

Figure 4 NUDT21 down-regulates LIMK2 expression. (a) The LIMK2 expression in hippocampal tissue of sevoflurane-induced rat after transfected with AAV-NUDT21 was assessed using Immunofluorescence. (b) The LIMK2 expression in hippocampal tissue of sevoflurane-induced rat after transfected with AAV-NUDT21 was assessed by Western blot. **P < 0.01. ## P < 0.01.
Figure 4

NUDT21 down-regulates LIMK2 expression. (a) The LIMK2 expression in hippocampal tissue of sevoflurane-induced rat after transfected with AAV-NUDT21 was assessed using Immunofluorescence. (b) The LIMK2 expression in hippocampal tissue of sevoflurane-induced rat after transfected with AAV-NUDT21 was assessed by Western blot. **P < 0.01. ## P < 0.01.

4 Discussion

In recent years, there is a growing concern that anesthetic can have toxic effects on neurons and cause persistent cognitive damage [18]. As a commonly used anesthetic, sevoflurane was found to cause POCD [19]. However, the exact mechanism of sevoflurane caused POCD remained to be further elucidated. NUDT21, a conserved splicing factor, was revealed to play important roles in multiple diseases’ progression, while its influence on sevoflurane-induced POCD remains unclear.

Therefore, this study investigated the action of NUDT21 on sevoflurane-induced neurological damage. The expression of NUDT21 in sevoflurane-induced rats was determined. The results revealed that NUDT21 was down-regulated in the hippocampal tissue of sevoflurane-induced rats. The decreased expression of NUDT21 was also found in cancers, such as hepatocellular carcinoma, breast cancer, and bladder cancer [9,10,20]. However, up to now, the current study is the first to report the aberrant expression of NUDT21 in the hippocampal tissue of sevoflurane-induced rats. Previous study reported that NUDT21 was a highly constrained gene and it was closely related to health as its 125 missense and 13 loss-of-function variants would be expected in NUDT21 if loss-of-function variants were not pathogenic, but instead there were only 15 missense and 0 loss-of-function variants [21]. Hence, the aberrant expression of NUDT21 in the hippocampal tissue of sevoflurane-induced rats suggested that it might participate in the POCD development.

POCD is mainly manifested as the decline in cognitive function after surgery and anesthesia [22]. The previous study revealed that the cognitive function of sevoflurane anesthesia patients after operation was significantly worse than pre-operation [23]. Therefore, to clarify the role of abnormally expressed NUDT21 in sevoflurane-induced neurological damage, the cognitive impairment was detected using the Morris water maze test. The Morris water maze test is a well-established test for assessing spatial learning and memory [24]. The advantage of the test is that it can be carried out quickly without the restriction of water and food [25]. Furthermore, the factors affecting spatial learning and memory ability can be overcome by adjusting the test method [25]. According to the results of Morris water maze test, we found that sevoflurane exposure inhibited the spatial learning ability, as reflected by the index of escape latencies and spatial memory reflected by the time spent in the target quadrant. In other words, sevoflurane treatment suppressed the cognitive function of rats, which was consistent with the previous studies [26,27]. However, the cognitive impairment induced by sevoflurane was alleviated by overexpressed NUDT21, suggesting that NUDT21 protected against sevoflurane-caused cognitive impairment. Similarly, Alcott et al. reported that partial loss of NUDT21 caused learning deficits and cortical hyperexcitability via regulating alternative polyadenylation and protein levels in hundreds of genes [14].

Increasing studies found that neuronal apoptosis was a critical cause of POCD development [28]. For example, inhibition of α-Synuclein accumulation alleviated neuronal apoptosis and improved POCD in aged mice [29]. Besides, sevoflurane was demonstrated to induce apoptosis of the nervous system, which was closely associated with the POCD occurrence [30]. Ling et al. also found that sevoflurane induced neuronal apoptosis via enhancing DNMT3L expression and promoting methylation of PSD95 promoter in POCD [31]. Thus, the current study investigated neuronal apoptosis using TUNEL assay to explain the role of NUDT21 in sevoflurane-induced POCD. As expected, sevoflurane treatment induced apoptosis of hippocampal neurons. Nevertheless, enhanced NUDT21 suppressed sevoflurane-induced hippocampal neuronal apoptosis. In the study performed by Brumbaugh et al., NUDT21 was considered a novel cell fate regulator by connecting alternative polyadenylation [16]. Zheng et al. revealed that knockdown of NUDT21 promoted apoptosis of pancreatic ductal adenocarcinoma [12]. To our knowledge, the present study is the first to reveal the apoptosis inhibitory function of NUDT21 on sevoflurane-induced POCD. Based on the above evidence, we inferred that sevoflurane treatment suppressed the expression of NUDT21 to promote the hippocampal neuronal apoptosis, thereby inducing POCD. Therefore, restoring the expression level of NUDT1 may be an effective way to prevent sevoflurane-induced POCD.

LIMK2 was a member of the LIM kinase (LIMK) family of serine/threonine kinases [32]. Recent studies validated that LIMK2 regulated neuronal growth and morphology, synaptic function, pain response, neuronal apoptosis, learning, and memory [15,33]. In this study, the expression of LIMK2 was explored to explore the precise regulatory mechanism of NUDT21 on sevoflurane-induced POCD. The results indicated that sevoflurane stimulation increased the LIMK2 expression, which was inhibited by NUDT21. These findings were consistent with the study performed by Xiong et al. [9]. They found that LIMK2 was downregulated in NUDT21 overexpressed cells but was upregulated in NUDT21-knockdown cells [9]. As a conserved splicing factor, NUDT21 encoded CFIm25 which binds UGUA sequences in pre-mRNA and the CFIm complex recruits the enzymes essential for cleavage and polyadenylation [21]. Since the UGUA binding sites are usually enriched at the distal polyadenylation sites, proximal cleavage sites were more frequently used after NUDT21 expression was reduced [21]. Therefore, downregulation of NUDT21 caused 3′UTR shortening in hundreds of genes, thereby increasing protein levels of a subset of those genes [21]. In this study, the expression of LIMK2 was negatively regulated by NUDT21. This finding indicated that NUDT21 might modulate LIMK2 expression via alternative polyadenylation. Together, NUDT21 might attenuate sevoflurane-induced neurological damage in rats by down-regulating LIMK2.

In conclusion, NUDT21 was down-regulated in hippocampal tissue of sevoflurane-induced rats. Overexpression of NUDT21 alleviated sevoflurane-induced neurological damage by down-regulating LIMK2. These findings provided a novel target for the prevention of sevoflurane-induced POCD.

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Acknowledgments

We thank (1) Translational Neurology Laboratory, Affiliated Hospital of ZunYi Medical University and (2) WANG TINGHUA Translation lnstitute, Affiliated Hospital of ZunYi Medical University.

  1. Funding information: This work was supported by the Science and Technology Planning Project of Zunyi (Grant No. HZ(2021)71), The Science and Technology Planning Progect of Zunyi (Grant No. HZ(2021)83), Collaborative Innovation Center of Chinese Ministry of Education (2020-39) and The National Natural Science Foundation of China [No. 81960214].

  2. Author contributions: Yuanping Zhong, Pengcheng Zhao, and Chao Zhang designed the experiments and Zhenyu Wu carried them out. Xu Fang analyzed and interpreted the data and Zhaoqiong Zhu prepared the article with contributions from all co-authors.

  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: 2022-03-14
Revised: 2022-05-22
Accepted: 2022-07-28
Published Online: 2023-04-15

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

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

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  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
https://doi.org/10.1515/biol-2022-0486
Keywords for this article
NUDT21; POCD; cognitive impairment; apoptosis; LIMK2
Creative Commons
BY 4.0

Articles in the same Issue

  1. Biomedical Sciences
  2. Systemic investigation of inetetamab in combination with small molecules to treat HER2-overexpressing breast and gastric cancers
  3. Immunosuppressive treatment for idiopathic membranous nephropathy: An updated network meta-analysis
  4. Identifying two pathogenic variants in a patient with pigmented paravenous retinochoroidal atrophy
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  6. A case of pulmonary embolism with bad warfarin anticoagulant effects caused by E. coli infection
  7. Neutrophilia with subclinical Cushing’s disease: A case report and literature review
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  9. Immunoregulation of synovial macrophages for the treatment of osteoarthritis
  10. Novel CPLANE1 c.8948dupT (p.P2984Tfs*7) variant in a child patient with Joubert syndrome
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  13. High glucose and high lipid induced mitochondrial dysfunction in JEG-3 cells through oxidative stress
  14. Pharmacological inhibition of the ubiquitin-specific protease 8 effectively suppresses glioblastoma cell growth
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  17. Single-cell transcription analysis reveals the tumor origin and heterogeneity of human bilateral renal clear cell carcinoma
  18. Identification of iron metabolism-related genes as diagnostic signatures in sepsis by blood transcriptomic analysis
  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
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  26. Experimental study on the optimization of ANM33 release in foam cells
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  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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  49. Exosomal HBV-DNA for diagnosis and treatment monitoring of chronic hepatitis B
  50. Shear stress leads to the dysfunction of endothelial cells through the Cav-1-mediated KLF2/eNOS/ERK signaling pathway under physiological conditions
  51. Interaction between the PI3K/AKT pathway and mitochondrial autophagy in macrophages and the leukocyte count in rats with LPS-induced pulmonary infection
  52. Meta-analysis of the rs231775 locus polymorphism in the CTLA-4 gene and the susceptibility to Graves’ disease in children
  53. Cloning, subcellular localization and expression of phosphate transporter gene HvPT6 of hulless barley
  54. Coptisine mitigates diabetic nephropathy via repressing the NRLP3 inflammasome
  55. Significant elevated CXCL14 and decreased IL-39 levels in patients with tuberculosis
  56. Whole-exome sequencing applications in prenatal diagnosis of fetal bowel dilatation
  57. Gemella morbillorum infective endocarditis: A case report and literature review
  58. An unusual ectopic thymoma clonal evolution analysis: A case report
  59. Severe cumulative skin toxicity during toripalimab combined with vemurafenib following toripalimab alone
  60. Detection of V. vulnificus septic shock with ARDS using mNGS
  61. Novel rare genetic variants of familial and sporadic pulmonary atresia identified by whole-exome sequencing
  62. The influence and mechanistic action of sperm DNA fragmentation index on the outcomes of assisted reproduction technology
  63. Novel compound heterozygous mutations in TELO2 in an infant with You-Hoover-Fong syndrome: A case report and literature review
  64. ctDNA as a prognostic biomarker in resectable CLM: Systematic review and meta-analysis
  65. Diagnosis of primary amoebic meningoencephalitis by metagenomic next-generation sequencing: A case report
  66. Phylogenetic analysis of promoter regions of human Dolichol kinase (DOLK) and orthologous genes using bioinformatics tools
  67. Collagen changes in rabbit conjunctiva after conjunctival crosslinking
  68. Effects of NM23 transfection of human gastric carcinoma cells in mice
  69. Oral nifedipine and phytosterol, intravenous nicardipine, and oral nifedipine only: Three-arm, retrospective, cohort study for management of severe preeclampsia
  70. Case report of hepatic retiform hemangioendothelioma: A rare tumor treated with ultrasound-guided microwave ablation
  71. Curcumin induces apoptosis in human hepatocellular carcinoma cells by decreasing the expression of STAT3/VEGF/HIF-1α signaling
  72. Rare presentation of double-clonal Waldenström macroglobulinemia with pulmonary embolism: A case report
  73. Giant duplication of the transverse colon in an adult: A case report and literature review
  74. Ectopic thyroid tissue in the breast: A case report
  75. SDR16C5 promotes proliferation and migration and inhibits apoptosis in pancreatic cancer
  76. Vaginal metastasis from breast cancer: A case report
  77. Screening of the best time window for MSC transplantation to treat acute myocardial infarction with SDF-1α antibody-loaded targeted ultrasonic microbubbles: An in vivo study in miniswine
  78. Inhibition of TAZ impairs the migration ability of melanoma cells
  79. Molecular complexity analysis of the diagnosis of Gitelman syndrome in China
  80. Effects of maternal calcium and protein intake on the development and bone metabolism of offspring mice
  81. Identification of winter wheat pests and diseases based on improved convolutional neural network
  82. Ultra-multiplex PCR technique to guide treatment of Aspergillus-infected aortic valve prostheses
  83. Virtual high-throughput screening: Potential inhibitors targeting aminopeptidase N (CD13) and PIKfyve for SARS-CoV-2
  84. Immune checkpoint inhibitors in cancer patients with COVID-19
  85. Utility of methylene blue mixed with autologous blood in preoperative localization of pulmonary nodules and masses
  86. Integrated analysis of the microbiome and transcriptome in stomach adenocarcinoma
  87. Berberine suppressed sarcopenia insulin resistance through SIRT1-mediated mitophagy
  88. DUSP2 inhibits the progression of lupus nephritis in mice by regulating the STAT3 pathway
  89. Lung abscess by Fusobacterium nucleatum and Streptococcus spp. co-infection by mNGS: A case series
  90. Genetic alterations of KRAS and TP53 in intrahepatic cholangiocarcinoma associated with poor prognosis
  91. Granulomatous polyangiitis involving the fourth ventricle: Report of a rare case and a literature review
  92. Studying infant mortality: A demographic analysis based on data mining models
  93. Metaplastic breast carcinoma with osseous differentiation: A report of a rare case and literature review
  94. Protein Z modulates the metastasis of lung adenocarcinoma cells
  95. Inhibition of pyroptosis and apoptosis by capsaicin protects against LPS-induced acute kidney injury through TRPV1/UCP2 axis in vitro
  96. TAK-242, a toll-like receptor 4 antagonist, against brain injury by alleviates autophagy and inflammation in rats
  97. Primary mediastinum Ewing’s sarcoma with pleural effusion: A case report and literature review
  98. Association of ADRB2 gene polymorphisms and intestinal microbiota in Chinese Han adolescents
  99. Tanshinone IIA alleviates chondrocyte apoptosis and extracellular matrix degeneration by inhibiting ferroptosis
  100. Study on the cytokines related to SARS-Cov-2 in testicular cells and the interaction network between cells based on scRNA-seq data
  101. Effect of periostin on bone metabolic and autophagy factors during tooth eruption in mice
  102. HP1 induces ferroptosis of renal tubular epithelial cells through NRF2 pathway in diabetic nephropathy
  103. Intravaginal estrogen management in postmenopausal patients with vaginal squamous intraepithelial lesions along with CO2 laser ablation: A retrospective study
  104. Hepatocellular carcinoma cell differentiation trajectory predicts immunotherapy, potential therapeutic drugs, and prognosis of patients
  105. Effects of physical exercise on biomarkers of oxidative stress in healthy subjects: A meta-analysis of randomized controlled trials
  106. Identification of lysosome-related genes in connection with prognosis and immune cell infiltration for drug candidates in head and neck cancer
  107. Development of an instrument-free and low-cost ELISA dot-blot test to detect antibodies against SARS-CoV-2
  108. Research progress on gas signal molecular therapy for Parkinson’s disease
  109. Adiponectin inhibits TGF-β1-induced skin fibroblast proliferation and phenotype transformation via the p38 MAPK signaling pathway
  110. The G protein-coupled receptor-related gene signatures for predicting prognosis and immunotherapy response in bladder urothelial carcinoma
  111. α-Fetoprotein contributes to the malignant biological properties of AFP-producing gastric cancer
  112. CXCL12/CXCR4/CXCR7 axis in placenta tissues of patients with placenta previa
  113. Association between thyroid stimulating hormone levels and papillary thyroid cancer risk: A meta-analysis
  114. Significance of sTREM-1 and sST2 combined diagnosis for sepsis detection and prognosis prediction
  115. Diagnostic value of serum neuroactive substances in the acute exacerbation of chronic obstructive pulmonary disease complicated with depression
  116. Research progress of AMP-activated protein kinase and cardiac aging
  117. TRIM29 knockdown prevented the colon cancer progression through decreasing the ubiquitination levels of KRT5
  118. Cross-talk between gut microbiota and liver steatosis: Complications and therapeutic target
  119. Metastasis from small cell lung cancer to ovary: A case report
  120. The early diagnosis and pathogenic mechanisms of sepsis-related acute kidney injury
  121. The effect of NK cell therapy on sepsis secondary to lung cancer: A case report
  122. Erianin alleviates collagen-induced arthritis in mice by inhibiting Th17 cell differentiation
  123. Loss of ACOX1 in clear cell renal cell carcinoma and its correlation with clinical features
  124. Signalling pathways in the osteogenic differentiation of periodontal ligament stem cells
  125. Crosstalk between lactic acid and immune regulation and its value in the diagnosis and treatment of liver failure
  126. Clinicopathological features and differential diagnosis of gastric pleomorphic giant cell carcinoma
  127. Traumatic brain injury and rTMS-ERPs: Case report and literature review
  128. Extracellular fibrin promotes non-small cell lung cancer progression through integrin β1/PTEN/AKT signaling
  129. Knockdown of DLK4 inhibits non-small cell lung cancer tumor growth by downregulating CKS2
  130. The co-expression pattern of VEGFR-2 with indicators related to proliferation, apoptosis, and differentiation of anagen hair follicles
  131. Inflammation-related signaling pathways in tendinopathy
  132. CD4+ T cell count in HIV/TB co-infection and co-occurrence with HL: Case report and literature review
  133. Clinical analysis of severe Chlamydia psittaci pneumonia: Case series study
  134. Bioinformatics analysis to identify potential biomarkers for the pulmonary artery hypertension associated with the basement membrane
  135. Influence of MTHFR polymorphism, alone or in combination with smoking and alcohol consumption, on cancer susceptibility
  136. Catharanthus roseus (L.) G. Don counteracts the ampicillin resistance in multiple antibiotic-resistant Staphylococcus aureus by downregulation of PBP2a synthesis
  137. Combination of a bronchogenic cyst in the thoracic spinal canal with chronic myelocytic leukemia
  138. Bacterial lipoprotein plays an important role in the macrophage autophagy and apoptosis induced by Salmonella typhimurium and Staphylococcus aureus
  139. TCL1A+ B cells predict prognosis in triple-negative breast cancer through integrative analysis of single-cell and bulk transcriptomic data
  140. Ezrin promotes esophageal squamous cell carcinoma progression via the Hippo signaling pathway
  141. Ferroptosis: A potential target of macrophages in plaque vulnerability
  142. Predicting pediatric Crohn's disease based on six mRNA-constructed risk signature using comprehensive bioinformatic approaches
  143. Applications of genetic code expansion and photosensitive UAAs in studying membrane proteins
  144. HK2 contributes to the proliferation, migration, and invasion of diffuse large B-cell lymphoma cells by enhancing the ERK1/2 signaling pathway
  145. IL-17 in osteoarthritis: A narrative review
  146. Circadian cycle and neuroinflammation
  147. Probiotic management and inflammatory factors as a novel treatment in cirrhosis: A systematic review and meta-analysis
  148. Hemorrhagic meningioma with pulmonary metastasis: Case report and literature review
  149. SPOP regulates the expression profiles and alternative splicing events in human hepatocytes
  150. Knockdown of SETD5 inhibited glycolysis and tumor growth in gastric cancer cells by down-regulating Akt signaling pathway
  151. PTX3 promotes IVIG resistance-induced endothelial injury in Kawasaki disease by regulating the NF-κB pathway
  152. Pancreatic ectopic thyroid tissue: A case report and analysis of literature
  153. The prognostic impact of body mass index on female breast cancer patients in underdeveloped regions of northern China differs by menopause status and tumor molecular subtype
  154. Report on a case of liver-originating malignant melanoma of unknown primary
  155. Case report: Herbal treatment of neutropenic enterocolitis after chemotherapy for breast cancer
  156. The fibroblast growth factor–Klotho axis at molecular level
  157. Characterization of amiodarone action on currents in hERG-T618 gain-of-function mutations
  158. A case report of diagnosis and dynamic monitoring of Listeria monocytogenes meningitis with NGS
  159. Effect of autologous platelet-rich plasma on new bone formation and viability of a Marburg bone graft
  160. Small breast epithelial mucin as a useful prognostic marker for breast cancer patients
  161. Continuous non-adherent culture promotes transdifferentiation of human adipose-derived stem cells into retinal lineage
  162. Nrf3 alleviates oxidative stress and promotes the survival of colon cancer cells by activating AKT/BCL-2 signal pathway
  163. Favorable response to surufatinib in a patient with necrolytic migratory erythema: A case report
  164. Case report of atypical undernutrition of hypoproteinemia type
  165. Down-regulation of COL1A1 inhibits tumor-associated fibroblast activation and mediates matrix remodeling in the tumor microenvironment of breast cancer
  166. Sarcoma protein kinase inhibition alleviates liver fibrosis by promoting hepatic stellate cells ferroptosis
  167. Research progress of serum eosinophil in chronic obstructive pulmonary disease and asthma
  168. Clinicopathological characteristics of co-existing or mixed colorectal cancer and neuroendocrine tumor: Report of five cases
  169. Role of menopausal hormone therapy in the prevention of postmenopausal osteoporosis
  170. Precisional detection of lymph node metastasis using tFCM in colorectal cancer
  171. Advances in diagnosis and treatment of perimenopausal syndrome
  172. A study of forensic genetics: ITO index distribution and kinship judgment between two individuals
  173. Acute lupus pneumonitis resembling miliary tuberculosis: A case-based review
  174. Plasma levels of CD36 and glutathione as biomarkers for ruptured intracranial aneurysm
  175. Fractalkine modulates pulmonary angiogenesis and tube formation by modulating CX3CR1 and growth factors in PVECs
  176. Novel risk prediction models for deep vein thrombosis after thoracotomy and thoracoscopic lung cancer resections, involving coagulation and immune function
  177. Exploring the diagnostic markers of essential tremor: A study based on machine learning algorithms
  178. Evaluation of effects of small-incision approach treatment on proximal tibia fracture by deep learning algorithm-based magnetic resonance imaging
  179. An online diagnosis method for cancer lesions based on intelligent imaging analysis
  180. Medical imaging in rheumatoid arthritis: A review on deep learning approach
  181. Predictive analytics in smart healthcare for child mortality prediction using a machine learning approach
  182. Utility of neutrophil–lymphocyte ratio and platelet–lymphocyte ratio in predicting acute-on-chronic liver failure survival
  183. A biomedical decision support system for meta-analysis of bilateral upper-limb training in stroke patients with hemiplegia
  184. TNF-α and IL-8 levels are positively correlated with hypobaric hypoxic pulmonary hypertension and pulmonary vascular remodeling in rats
  185. Stochastic gradient descent optimisation for convolutional neural network for medical image segmentation
  186. Comparison of the prognostic value of four different critical illness scores in patients with sepsis-induced coagulopathy
  187. Application and teaching of computer molecular simulation embedded technology and artificial intelligence in drug research and development
  188. Hepatobiliary surgery based on intelligent image segmentation technology
  189. Value of brain injury-related indicators based on neural network in the diagnosis of neonatal hypoxic-ischemic encephalopathy
  190. Analysis of early diagnosis methods for asymmetric dementia in brain MR images based on genetic medical technology
  191. Early diagnosis for the onset of peri-implantitis based on artificial neural network
  192. Clinical significance of the detection of serum IgG4 and IgG4/IgG ratio in patients with thyroid-associated ophthalmopathy
  193. Forecast of pain degree of lumbar disc herniation based on back propagation neural network
  194. SPA-UNet: A liver tumor segmentation network based on fused multi-scale features
  195. Systematic evaluation of clinical efficacy of CYP1B1 gene polymorphism in EGFR mutant non-small cell lung cancer observed by medical image
  196. Rehabilitation effect of intelligent rehabilitation training system on hemiplegic limb spasms after stroke
  197. A novel approach for minimising anti-aliasing effects in EEG data acquisition
  198. ErbB4 promotes M2 activation of macrophages in idiopathic pulmonary fibrosis
  199. Clinical role of CYP1B1 gene polymorphism in prediction of postoperative chemotherapy efficacy in NSCLC based on individualized health model
  200. Lung nodule segmentation via semi-residual multi-resolution neural networks
  201. Evaluation of brain nerve function in ICU patients with Delirium by deep learning algorithm-based resting state MRI
  202. A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis
  203. Markov model combined with MR diffusion tensor imaging for predicting the onset of Alzheimer’s disease
  204. Effectiveness of the treatment of depression associated with cancer and neuroimaging changes in depression-related brain regions in patients treated with the mediator-deuterium acupuncture method
  205. Molecular mechanism of colorectal cancer and screening of molecular markers based on bioinformatics analysis
  206. Monitoring and evaluation of anesthesia depth status data based on neuroscience
  207. Exploring the conformational dynamics and thermodynamics of EGFR S768I and G719X + S768I mutations in non-small cell lung cancer: An in silico approaches
  208. Optimised feature selection-driven convolutional neural network using gray level co-occurrence matrix for detection of cervical cancer
  209. Incidence of different pressure patterns of spinal cerebellar ataxia and analysis of imaging and genetic diagnosis
  210. Pathogenic bacteria and treatment resistance in older cardiovascular disease patients with lung infection and risk prediction model
  211. Adoption value of support vector machine algorithm-based computed tomography imaging in the diagnosis of secondary pulmonary fungal infections in patients with malignant hematological disorders
  212. From slides to insights: Harnessing deep learning for prognostic survival prediction in human colorectal cancer histology
  213. Ecology and Environmental Science
  214. Monitoring of hourly carbon dioxide concentration under different land use types in arid ecosystem
  215. Comparing the differences of prokaryotic microbial community between pit walls and bottom from Chinese liquor revealed by 16S rRNA gene sequencing
  216. Effects of cadmium stress on fruits germination and growth of two herbage species
  217. Bamboo charcoal affects soil properties and bacterial community in tea plantations
  218. Optimization of biogas potential using kinetic models, response surface methodology, and instrumental evidence for biodegradation of tannery fleshings during anaerobic digestion
  219. Understory vegetation diversity patterns of Platycladus orientalis and Pinus elliottii communities in Central and Southern China
  220. Studies on macrofungi diversity and discovery of new species of Abortiporus from Baotianman World Biosphere Reserve
  221. Food Science
  222. Effect of berrycactus fruit (Myrtillocactus geometrizans) on glutamate, glutamine, and GABA levels in the frontal cortex of rats fed with a high-fat diet
  223. Guesstimate of thymoquinone diversity in Nigella sativa L. genotypes and elite varieties collected from Indian states using HPTLC technique
  224. Analysis of bacterial community structure of Fuzhuan tea with different processing techniques
  225. Untargeted metabolomics reveals sour jujube kernel benefiting the nutritional value and flavor of Morchella esculenta
  226. Mycobiota in Slovak wine grapes: A case study from the small Carpathians wine region
  227. Elemental analysis of Fadogia ancylantha leaves used as a nutraceutical in Mashonaland West Province, Zimbabwe
  228. Microbiological transglutaminase: Biotechnological application in the food industry
  229. Influence of solvent-free extraction of fish oil from catfish (Clarias magur) heads using a Taguchi orthogonal array design: A qualitative and quantitative approach
  230. Chromatographic analysis of the chemical composition and anticancer activities of Curcuma longa extract cultivated in Palestine
  231. The potential for the use of leghemoglobin and plant ferritin as sources of iron
  232. Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM
  233. Bioengineering and Biotechnology
  234. Biocompatibility and osteointegration capability of β-TCP manufactured by stereolithography 3D printing: In vitro study
  235. Clinical characteristics and the prognosis of diabetic foot in Tibet: A single center, retrospective study
  236. Agriculture
  237. Biofertilizer and NPSB fertilizer application effects on nodulation and productivity of common bean (Phaseolus vulgaris L.) at Sodo Zuria, Southern Ethiopia
  238. On correlation between canopy vegetation and growth indexes of maize varieties with different nitrogen efficiencies
  239. Exopolysaccharides from Pseudomonas tolaasii inhibit the growth of Pleurotus ostreatus mycelia
  240. A transcriptomic evaluation of the mechanism of programmed cell death of the replaceable bud in Chinese chestnut
  241. Melatonin enhances salt tolerance in sorghum by modulating photosynthetic performance, osmoregulation, antioxidant defense, and ion homeostasis
  242. Effects of plant density on alfalfa (Medicago sativa L.) seed yield in western Heilongjiang areas
  243. Identification of rice leaf diseases and deficiency disorders using a novel DeepBatch technique
  244. Artificial intelligence and internet of things oriented sustainable precision farming: Towards modern agriculture
  245. Animal Sciences
  246. Effect of ketogenic diet on exercise tolerance and transcriptome of gastrocnemius in mice
  247. Combined analysis of mRNA–miRNA from testis tissue in Tibetan sheep with different FecB genotypes
  248. Isolation, identification, and drug resistance of a partially isolated bacterium from the gill of Siniperca chuatsi
  249. Tracking behavioral changes of confined sows from the first mating to the third parity
  250. The sequencing of the key genes and end products in the TLR4 signaling pathway from the kidney of Rana dybowskii exposed to Aeromonas hydrophila
  251. Development of a new candidate vaccine against piglet diarrhea caused by Escherichia coli
  252. Plant Sciences
  253. Crown and diameter structure of pure Pinus massoniana Lamb. forest in Hunan province, China
  254. Genetic evaluation and germplasm identification analysis on ITS2, trnL-F, and psbA-trnH of alfalfa varieties germplasm resources
  255. Tissue culture and rapid propagation technology for Gentiana rhodantha
  256. Effects of cadmium on the synthesis of active ingredients in Salvia miltiorrhiza
  257. Cloning and expression analysis of VrNAC13 gene in mung bean
  258. Chlorate-induced molecular floral transition revealed by transcriptomes
  259. Effects of warming and drought on growth and development of soybean in Hailun region
  260. Effects of different light conditions on transient expression and biomass in Nicotiana benthamiana leaves
  261. Comparative analysis of the rhizosphere microbiome and medicinally active ingredients of Atractylodes lancea from different geographical origins
  262. Distinguish Dianthus species or varieties based on chloroplast genomes
  263. Comparative transcriptomes reveal molecular mechanisms of apple blossoms of different tolerance genotypes to chilling injury
  264. Study on fresh processing key technology and quality influence of Cut Ophiopogonis Radix based on multi-index evaluation
  265. An advanced approach for fig leaf disease detection and classification: Leveraging image processing and enhanced support vector machine methodology
  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
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