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Exosomal HBV-DNA for diagnosis and treatment monitoring of chronic hepatitis B

  • Xu Xu , Li Zhang , Jiamin Liu , Xiangxin Kong , Yu Yin , Zhiwei Jia , Xiaoqin Zhang , Bin Peng , Min Ji and Wanlong Pan 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

This study examined exosomal hepatitis B virus (HBV)-DNA levels in chronic HBV infection (CHB). Patients were grouped according to the European Association for the Study of the Liver classification (1: HBV-DNA-positive CHB, normal alanine aminotransferase [ALT]; 2: HBV-DNA-positive CHB, elevated ALT; 3: HBV-DNA-negative HBeAb-positive CHB, normal ALT; 4: HBV-DNA-positive HBeAg-negative HBeAb-positive CHB, elevated ALT; 5: HBV-DNA-negative, HBcAb-positive; 6: HBV-negative, normal ALT). Exosomes were isolated, comparative analysis of exosomes and serum HBV-DNA. The HBV-DNA content was lower in exosomes than in serum for groups 1, 2, and 4 (all P < 0.05). In the groups negative for serum HBV-DNA (groups 3 and 5), the exosomal HBV-DNA levels were higher than the serum HBV-DNA levels (all P < 0.05). The exosomal and serum HBV-DNA levels were correlated in groups 2 (R 2 = 0.84) and 4 (R 2 = 0.98). The exosomal HBV-DNA levels were correlated with total bilirubin (R 2 = 0.94), direct bilirubin (R 2 = 0.82), and indirect bilirubin (R 2 = 0.81) in group 5 (all P < 0.05). In patients with CHB and negative for serum HBV-DNA, exosomal HBV-DNA was detectable and could be used to monitor the treatment effects. Exosomal HBV-DNA could be used in patients with a high suspicion of HBV infection but negative for serum HBV-DNA.

Keywords: exosomes; serum; hepatitis B; virus; DNA

1 Introduction

About 292 million people are infected with the hepatitis B virus (HBV) in the world, with the highest infection rates being observed in Africa and the Western Pacific region, where the virus-carrying rates are >6% [1]. China is a hard-hit country, and HBV carriers account for about 6% of the total Chinese population [1].

Presently, diagnosing hepatitis B is mainly based on the HBV-DNA nucleic acid test, HBV serum marker test, liver function test, and other auxiliary tests [2]. The latest version of the European HBV treatment guidelines [3] stipulates that the treatment criteria are met only when both HBV-DNA and liver function indicators (like alanine aminotransferase [ALT]) are elevated. The detection of low levels of HBV-DNA replication depends on liver biopsy [2,3], which is invasive, difficult for the patients to accept and cannot be used repeatedly for treatment effect monitoring.

Exosomes are small (40–200 nm) vesicles containing complex RNA, DNA, and proteins and are formed by the fusion and exocytosis of intracellular vesicles and plasma membrane through multiple vesicle bodies [4,5,6], first detected in humans by Caby et al. [7]. Exosomes mainly promote cell interactions through receptor-mediated endocytosis by the target cells [8,9]. Exosomes cannot be degraded by the enzymes found in body fluids due to the structure of their bimolecular lipid layer [10]. Therefore, the proteins, viruses, nucleic acids, and other substances carried by exosomes will not be found in the body fluids [10]. These features contribute to easy isolation and detection at all stages or even early stages of the disease [11,12,13]. Therefore, exosomes can be a medium for virus replication, transmission, and regulation [9,14]. Exosomes are potentially more sensitive indicators than serum markers to reflect the occurrence, development, and outcome of diseases and might provide treatment reference indicators with more clinical significance [9,14].

Based on this assumption, this study aimed to examine the sensitivity of exosomal HBV-DNA levels and their correlation with serum biochemical indicators of HBV infection.

2 Materials and methods

2.1 Patients and samples

Serum HBV-DNA (HBV-DNA nucleic acid detection kit, Shanghai Kehua), immune indicators (HBsAg, HBsAb, HBeAg, HBeAb, and HBcAb, Hepatitis B surface antigen Assay Detection Kit, Roche), and liver biochemical indicators (total bilirubin [TBIL], direct bilirubin [DBIL], indirect bilirubin [IBIL], and ALT) were determined in the serum samples of 39 patients at the Affiliated Hospital of North Sichuan Medical College. The study involved human participants and was reviewed and approved by North Sichuan Medical College-2020 NSMC, number 10. Written informed consent was obtained from all patients or their legal guardians when <18 years of age.

The patients were grouped according to the European Association for the Study of the Liver 2017 Clinical Practice Guidelines on managing HBV infection [3] (Table S1). Table S2 shows the numbers of patients in the HBV-DNA (++) chronic HBV-DNA infection group (group 1), HBV-DNA (++) chronic hepatitis group (group 2), HBV-DNA (–) chronic HBV infection (CHB) group (group 3), HBV-DNA (+) chronic hepatitis group (group 4), HBV-DNA (–) group (group 5), and normal group (group 6).

  1. Informed consent: Informed consent has been obtained from all individuals included in this study.

  2. Ethical approval: The research related to human use has been complied with all the relevant national regulations, institutional policies and in accordance with the tenets of the Helsinki Declaration, and has been approved by the North Sichuan Medical College-2020 NSMC, number 10.

2.2 Exosomes isolation

The exosomes were isolated from the serum samples using the ExoQuick-TC exosome extraction kit [15]. For identification, the exosomes were resuspended in 1× phosphate-buffered saline and examined by electron microscopy. The expression of ALIX, CD9, and CD63 was detected by western blot (#FD006, Biyuntian Bio) [16].

2.3 Nanoparticle tracking analysis (NTA)

A particle size analyzer (Particle Metrix GmbH, Ammersee, Germany) was used for NTA to determine the size and number of serum exosomes.

2.4 Cell culture

HepG2 cells (Saibo Kang Biotechnology Co., Shanghai, China) were cultured in DMEM with 10% fetal bovine serum without exosomes. The exosomes were fixed using 1 ml of 4% paraformaldehyde and stained with DIO (Dioc18(3) (# 40725ES10, YEASEN) at 2 mM in DMSO and diluted before use to 2 µM) for 20 min at 37°C. The exosomes were centrifuged at 1,000 rpm for 5 min, and the supernatant was removed. The exosomes were resuspended in DMEM and transferred to the HepG2 cells. After 24 h, the cell morphology was observed under fluorescence microscopy.

2.5 Extraction of HBV-DNA

First, 400 μl of HBV core particle DNA extract was added to the exosomes and incubated for 15 min at 37°C. The mixture was centrifuged for 3 min at 15,000×g. Next, 4 μl of MgCl2 and RNase and 5 μl of DNase I was added and incubated for 3–4 h at 37°C. Then, 200 μl of PEG8000 was added, mixed well, and incubated on ice for 40 min, followed by centrifugation at 12,000×g, 4°C for 7 min. The supernatant was discarded. Then, 400 μl of digestion solution was added, mixed, and added with 15 μl of proteinase K. After overnight digestion at 45°C, 400 μl of phenol chloroform isoamyl alcohol mixture (25:24:1) was added. The mixture was centrifuged at 14,000×g for 3 min. An equal volume of isopropanol was mixed with the supernatant, mixed, and centrifuged for 11 min at 16,500×g and 4°C. The supernatant was discarded, the pellet was washed with 70% ethanol, and resuspended in ddH2O after drying.

2.6 Quantitative polymerase chain reaction (qPCR)

An SYBR kit (# CW0957m, CWBIO) was used for the fluorescence quantification of the exosomes. The primers for HBV-DNA were forward 5′-ACC GAC CTT GAG GCA TAC TT-3′ and reverse 5′-GCC TAC AGC CTC CTA GTA CA-3′. The reaction system included 12.5 μl of 2× UltraSYBR Mixture, 1 μl of each HBV-DNA primer 10 μM, 8.5 μl of ddH2O, and 2 μl of 1/100 diluted template DNA. The thermal cycling conditions were (1) 95°C for 10 min as an initial denaturation step and (2) 39 cycles of 95°C for 15 s and 60°C for 1 min. The absolute quantification of HBV-DNA was generated based on the Ct value with the set dissociation curve.

2.7 Statistical analysis

SPSS 23.0 (IBM) was used for statistical analysis. Continuous variables were presented as means ± standard error (serum and exosomal HBV-DNA levels) or means ± standard deviation (other continuous variables) and compared with one-way analysis of variance; as the variances of the groups were not uniform, the Games-Howell method was used for pair-wise comparison among the six groups. In each group, exosomal HBV-DNA levels were compared with the serum HBV-DNA values using a non-parametric test. The correlations between exosomal HBV-DNA and the other clinical indexes were analyzed using Spearman’s correlation. Two-sided P-values <0.05 were considered statistically significant.

3 Results

3.1 Clinical characteristics of the study population

Patient grouping and characteristics are shown in Table S2. The groups are presented in Table S1.

3.2 Identification of serum exosomes

Under electron microscopy, the serum exosomes showed an obvious saucer-like structure (Figure 1a). The diameter of the exosomes was 30–95 nm (Figure 1b). After 24 h of co-culture of the exosomes with HepG2 cells for 24 h, the cell morphology was observed using DIO staining and fluorescence microscopy, and green fluorescent exosomes were seen in the cytoplasm (Figure 1c), indicating the capacity of the exosomes to be internalized by the HepG2 cells. According to the NTA, the exosome diameter peaked at 100–125 nm (Figure 1d). The expression of Alix, CD9, and CD63 was detected using western blotting (Figure 1e and f). Therefore, the isolated particles were considered exosomes since they possessed the morphological and protein characteristics of exosomes and could be internalized by cells.

Figure 1 Identification of the exosomes in the serum. (a and b) Under electron microscopy, the exosomes in the serum showed a vesicular saucer-like structure with a size of about 30–95 nm. (c) After transfection of the serum exosomes into HepG2 cells for 24 h, granular fluorescence was observed in the cytoplasm. (d) Nanoparticle tracking analysis (NTA) of the nanoparticles. (e) The expression of exosome surface protein was detected by western blotting. β-Actin was used as the loading control. (f) Relative intensity of protein marker expression on the surface of exosomes in three patients.
Figure 1

Identification of the exosomes in the serum. (a and b) Under electron microscopy, the exosomes in the serum showed a vesicular saucer-like structure with a size of about 30–95 nm. (c) After transfection of the serum exosomes into HepG2 cells for 24 h, granular fluorescence was observed in the cytoplasm. (d) Nanoparticle tracking analysis (NTA) of the nanoparticles. (e) The expression of exosome surface protein was detected by western blotting. β-Actin was used as the loading control. (f) Relative intensity of protein marker expression on the surface of exosomes in three patients.

3.3 Expression of HBV-DNA in exosomes among the six groups

The HBV-DNA copy numbers were (4.11 ± 1.17) × 106 IU/ml in group 1, (3.13 ± 0.998) × 106 IU/ml in group 2, (1.02 ± 0.149) × 105 IU/ml in group 3, (5.08 ± 2.65) × 105 IU/ml in group 4, (3.10 ± 0.478) × 103 IU/ml in group 5, and 0 IU/ml in group 6. There were significant differences between each pair of groups (all P < 0.05), except for group 1 vs. group 2 and group 3 vs. group 4. The HBV-DNA content was lower in the exosomes than in the serum for groups 1, 2, and 4 but higher in the exosomes in groups 3 and 5 (all P < 0.05) (Figure 2). Therefore, HBV-DNA can be detected in serum exosomes, and the HBV-DNA levels vary among the different groups of patients.

Figure 2 The expression of HBV-DNA in the exosomes of the six groups of serum samples. The absolute copy number of HBV-DNA in the exosomes in the six groups of serum samples detected by qPCR. *P < 0.05.
Figure 2

The expression of HBV-DNA in the exosomes of the six groups of serum samples. The absolute copy number of HBV-DNA in the exosomes in the six groups of serum samples detected by qPCR. *P < 0.05.

3.4 Exosomal HBV-DNA in groups with negative serum HBV-DNA

Since exosomal HBV-DNA has a potential diagnostic value, the exosomal HBV-DNA levels were examined in patients with negative serum HBV-DNA, i.e., groups 3 (HBV-DNA-negative HBeAb-positive, normal ALT) and 5 (HBV-DNA-negative, HBcAb-positive). In groups 3 and 5, the exosomal HBV-DNA levels were higher than the serum HBV-DNA levels (all P < 0.05) (Figure 3). Figure S1 presents the comparisons in each patient. In group 3, the exosomal HBV-DNA levels were from 6.06 × 104 to 1.56 + 05 IU/ml, while the serum HBV-DNA levels were below the detection threshold of 5.00 × 102 IU/ml. In group 5, exosomal HBV-DNA levels were from 1.57 × 103 to 5.57U + 03 IU/ml, while serum HBV-DNA levels were also below the detection threshold of 5.00 × 102 IU/ml. In groups 3 and 5, the average copy numbers of HBV-DNA in exosomes were 1.02 × 105 IU/ml (i.e., about 200 times the lowest serum HBV-DNA detection limit (500 IU/ml)) and 3.10 × 103 IU/ml (i.e., about 6 times the lowest serum HBV-DNA detection limit (500 IU/ml)), respectively, showing that the former was exosomes and the latter was serum (Figure 3). These results indicate that exosomal HBV-DNA could be used to monitor treatment effects in CHB patients with negative serum HBV-DNA.

Figure 3 Comparison of HBV-DNA between serum and exosomes in patients with negative serum HBV-DNA. (a) The copies of HBV-DNA in serum and exosomes in group 3 patients. (b) The copies of HBV-DNA in serum and exosomes in group 5 patients. *P < 0.05.
Figure 3

Comparison of HBV-DNA between serum and exosomes in patients with negative serum HBV-DNA. (a) The copies of HBV-DNA in serum and exosomes in group 3 patients. (b) The copies of HBV-DNA in serum and exosomes in group 5 patients. *P < 0.05.

3.5 Exosomal HBV-DNA in groups with positive serum HBV-DNA

In the HBV-DNA (+) group, only the exosomal HBV-DNA in groups 2 and 4 were correlated with the serum HBV-DNA, while there were no correlations in group 1 (because the ALT/AST levels are normal, indicating less cell damage; the release of exosomes was smaller, and the detected HBV in the serum exosomes was not related to HBV in serum). Figure 4 shows the comparison of exosomal and serum HBV-DNA in patients with positive serum HBV-DNA (groups 1, 2, and 4). The serum HBV-DNA levels were higher than the exosomal HBV-DNA levels (all P < 0.05). Figure S1 presents the comparisons in each patient. All patients had higher serum HBV-DNA levels than the exosomal HBV-DNA. Still, some patients presented high exosomal HBV-DNA levels (patients 13, 14, 20, 21, and 25). ALT and AST levels indicate the degree of liver damage. Exosomes are derived from cells. Damaged and ruptured cells can release more exosomes. If the liver cells are not damaged, the release of exosomes should be limited, resulting in that HBV in the liver would not be related to the serum levels. The exosomal and serum HBV-DNA levels were correlated in groups 2 (R 2 = 0.84) and 4 (R 2 = 0.98). The results indicate that as serum HBV-DNA, exosomal HBV-DNA can represent the disease activity in patients with positive serum HBV-DNA. When the serum HBV-DNA is high (groups 1 and 2; HBV-DNA > 2 × 105 IU/ml), the serum has a larger volume to accommodate HBV-DNA than exosomes, and thus, more HBV-DNA is detected in the serum. Serum HBV-DNA in group 1 was 4.35–27.45 times that of exosomal HBV-DNA, while serum HBV-DNA in group 2 was 1.84–41.17 times that of exosomal HBV-DNA. When serum HBV-DNA levels were moderate, such as in group 4 (HBV-DNA > 2 × 103 IU/ml), the serum HBV-DNA levels were still higher than that of exosomes, and the difference was 1.73–40.80 times (P < 0.05). When serum HBV-DNA was negative, such as in groups 3 and 5 (HBV-DNA < 5 × 102 IU/ml), there was still virus replication even if the HBV-DNA in serum was undetectable, but exosomal HBV-DNA was detectable because of their key function in replication.

Figure 4 Comparison and correlation (Pearson’s) of HBV-DNA between serum and exosomes in patients with positive serum HBV-DNA. (a) Group 1. (b) Group 2. (c) Group 4. *P < 0.05.
Figure 4

Comparison and correlation (Pearson’s) of HBV-DNA between serum and exosomes in patients with positive serum HBV-DNA. (a) Group 1. (b) Group 2. (c) Group 4. *P < 0.05.

3.6 Correlations of exosomal HBV-DNA with liver function markers

Since exosomal HBV-DNA could be clinically used in serum HBV-DNA-negative patients, the exosomal HBV-DNA levels were examined for correlation with liver function markers. The exosomal HBV-DNA levels were correlated with TBIL (R 2 = 0.94) (Figure 5a), DBIL (R 2 = 0.82) (Figure 5b), and IBIL (R 2 = 0.81) (Figure 5c) in group 5 (all P < 0.05). In the other groups, there were no correlations between exosomal HBV-DNA and liver function markers (Tables S3–S6; all P > 0.05). Therefore, the results support the clinical usefulness of exosomal HBV-DNA levels for monitoring CHB patients with negative serum HBV-DNA.

Figure 5 Correlations of exosomal HBV-DNA with liver function markers. (a) Total bilirubin (TBIL). (b) Direct bilirubin (DBIL). (c) Indirect bilirubin (IBIL).
Figure 5

Correlations of exosomal HBV-DNA with liver function markers. (a) Total bilirubin (TBIL). (b) Direct bilirubin (DBIL). (c) Indirect bilirubin (IBIL).

4 Discussion

Serum HBV-DNA and ALT are routinely used as key clinical indicators to diagnose and evaluate patients with CHB [17,18]. The best opportunity for antiviral therapy is the presence of serum HBV-DNA and ALT elevation [3,19]. Still, some patients have low-elevated HBV-DNA and normal ALT, and it is difficult to determine the treatment timing for such patients [19,20]. These indicators might not completely reflect the severity of the liver lesions, and treatment indication then depends on liver biopsy [21,22,23].

Exosomes play crucial roles in communication among cells and might be diagnostic and prognostic indicators for various diseases [23,24,25,26]. This study indicates that the exosome copy numbers of HBV-DNA (1.02 × 105 and 3.10 × 103 IU/ml) were far higher than the detection limit of serum HBV-DNA (5 × 102 IU/ml) in groups 3 and 5, suggesting that exosomal HBV-DNA might be more sensitive than serum HBV-DNA. Exosomal HBV-DNA is more sensitive than serum HBV-DNA when serum HBV-DNA is negative. Interestingly, for patients whose serum HBV-DNA levels indicated a moderate-high replication level (>2 × 103 IU/ml) (group 4), the copy numbers of exosomal HBV-DNA (1.02 × 105 IU/ml) (group 3) were comparable to the exosomal HBV-DNA levels (5.08 × 105 IU/ml) (group 4) from the HBV-DNA-positive patients (P > 0.05). It suggests that the serum HBV-DNA levels might not reflect the true status of HBV replication in disease progression.

When serum HBV-DNA levels were high, there was no correlation between exosomal HBV-DNA and liver function-related indicators in group 1, while there were correlations in groups 2 and 4, which can be due to liver damage. On the other hand, when serum HBV-DNA is low, exosomal HBV-DNA has a certain correlation with liver function-related indicators, such as in the HBV-DNA-negative group (group 5). This study showed that exosomal HBV-DNA was positively correlated with TBIL, DBIL, and IBIL, indicating that the exosomal HBV-DNA levels could reflect liver injury to a certain extent. It should also be noted that ALT, an important biochemical indicator of liver injury, showed no correlation to the HBV-DNA levels in serum and exosomes.

Combined with clinical diagnosis and treatment standards, when HBV-DNA is >2 × 105 IU/ml and ALT is normal, there is a controversy about the use of antiviral treatment [3]. Comprehensive judgment is needed to fully consider patients’ age, liver histological examination, and liver compensation since such patients lack simple indicators to reflect the timing of treatment accurately. For example, in group 1, serum HBV-DNA was high, while ALT was normal, and such patients could not be treated according to clinical treatment guidelines. Still, this study showed that the exosomal HBV-DNA copy number in group 1 was 4.11 × 106 IU/ml, i.e., 1.3 times higher than the exosomal HBV-DNA copy number in group 2. On the other hand, eight patients (HBeAg (+), serum HBV-DNA >2 × 103 IU/ml, and ALT > ULN) in group 2 absolutely met the guideline criteria for antiviral treatment, but their exosomal HBV-DNA levels were only 1.10 × 106 IU/ml, far lower than that of group 1. Based on this inference, antiviral therapy may be given to patients in group 1 when exosomal HBV-DNA is >3.13 × 105 IU/ml. Meanwhile, the patients in groups 3 and 5 did not meet the indications for clinical antiviral therapy. The average copy numbers of HBV-DNA in the exosomes and serum were 1.02 × 105 and 3.10 × 103 IU/ml, respectively, about 6–200 times higher in exosomes than in serum. Therefore, the lower limit of exosomal HBV-DNA could be >1.56 × 105 IU/ml for antiviral therapy. Exosomes could be used as a simple and non-invasive detection indicator for monitoring CHB [27,28,29].

Recent studies showed that exosomes could regulate the immune response during HBV infection. Immune escape by down-regulating IL-12 to inhibit the activity of NK cells is one of the important reasons for persistent virus infection [30,31]. The insidious repeated activities of the virus can cause severe liver disease. During the disease, there is a certain risk in determining the timing of treatment based on the serum HBV-DNA, ALT, and other indicators specified in the guidelines. For example, in patients with negative HBV-DNA, relying on the existing indicators (serum HBV-DNA, ALT, BIL, etc.) is not enough to determine the timing of treatment correctly. At this time, more sensitive, accurate, and stable indicators are needed to reflect the levels of HBV-DNA to determine treatment. This study also reveals that exosomes can play an important role in monitoring CHB. The possible reason is that HBV-DNA enters exosomes through a ceramide-dependent pathway [32]. The exosomes act as an important vector to transport HBV-DNA into the liver cells to promote the massive replication of HBV in the body [33,34]. Exosomes are not easily diluted by the body’s blood and remain stable in body fluids. Therefore, monitoring the level of HBV-DNA in exosomes can timely and accurately reflect the occurrence and progress of the disease and determine the treatment to prevent the disease from turning into liver cirrhosis and cancer.

5 Conclusion

This study suggests that when a patient’s serum HBV-DNA is negative, exosomal HBV-DNA can accurately reflect the level of HBV replication in vivo. In serum HBV-DNA-negative patients, exosomal HBV-DNA were strongly and positively correlated with TBIL, DBIL, and IBIL.

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Acknowledgments

We thank the Innovation Platform for Basic Medical Research of North Sichuan Medical College for supporting this research.

  1. Funding information: This research was funded by the 2019 National Pre-Research Project of NSMC, grant no. 7500820086, and Science and Technology Strategic Cooperation Project between Nanchong City and NSMC, grant no. 22SXQT0318.

  2. Author contributions: Xu Xu: extract exosomes; statistical analysis data; drafting the manuscript. Li Zhang: collect serum; data analysis. Jiamin Liu: culture HepG2 cell; data analysis. Yu Yin: study supervision; data analysis. Zhiwei Jia: some preparation work for WB. Xiaoqin Zhang: some preparation work for the electron microscope. Bin Peng: electron microscope operation. Min Ji: design primer. Wanlong Pan: study concept and design; study supervision; critical manuscript revision.

  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: 2022-07-07
Revised: 2023-01-19
Accepted: 2023-02-17
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-2022-0585
Keywords for this article
exosomes; serum; hepatitis B; virus; DNA
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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  43. PI3K/AKT/mTOR pathway and its related molecules participate in PROK1 silence-induced anti-tumor effects on pancreatic cancer
  44. The altered expression of cytoskeletal and synaptic remodeling proteins during epilepsy
  45. Effects of pegylated recombinant human granulocyte colony-stimulating factor on lymphocytes and white blood cells of patients with malignant tumor
  46. Prostatitis as initial manifestation of Chlamydia psittaci pneumonia diagnosed by metagenome next-generation sequencing: A case report
  47. NUDT21 relieves sevoflurane-induced neurological damage in rats by down-regulating LIMK2
  48. Association of interleukin-10 rs1800896, rs1800872, and interleukin-6 rs1800795 polymorphisms with squamous cell carcinoma risk: A meta-analysis
  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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