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Effect of spaceflight on the phenotype and proteome of Escherichia coli

  • Yu Liu , Chong Xu , Guangxian Zhao , Yanji Wang , Yuanbing Zhu , Yishu Yin , Jiaping Wang EMAIL logo and Yongzhi Li EMAIL logo
Published/Copyright: February 28, 2023
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Open Life Sciences
From the journal Open Life Sciences Volume 18 Issue 1

Abstract

Microbial safety has become a research hotspot with the development of manned space technology. Escherichia coli is a conditional pathogen that can cause infectious diseases. Therefore, it is necessary to study the influence of the space environment on E. coli. Phenotypic experiments including growth curves, morphology, and environmental resistance experiment were used to study the phenotypic changes of E. coli after exposure to the space environment for 12 days carried by the “SJ-10” satellite. Tandem mass tag was used to assess the proteome change of E. coli. We found that the survival rate of E. coli in the spaceflight group was decreased when cultivated in acidic and high-salt environments. Proteomic analysis identified 72 downregulated proteins involved in chemotaxis, intracellular pH elevation, glycolate catabolic process, and glutamate metabolic process in the spaceflight group. Meanwhile, only one protein mtr that was involved in the uptake of tryptophan in E. coli was upregulated in the spaceflight group. Our research showed that proteomics results can explain phenotypic results, which demonstrated the successful application of proteomics in mechanism research. Our data provide a comprehensive resource for understanding the effect of the space environment on E. coli.

Keywords: spaceflight; proteomics; Escherichia coli

1 Introduction

Escherichia coli is a common Gram-negative bacterium that mainly exists in the intestines of humans and animals. It is an opportunistic pathogen, which can cause gastrointestinal infections in humans under certain conditions. In recent years, with the development of manned space technology, astronauts have been working longer and longer in space. Usually, bacteria will accompany humans into space [1]. Due to the existence of weightlessness, radiation, vacuum, and extreme temperature environments in space, the phenotype of bacteria including the growth rate, antibiotic resistance, anti-oxidation, biofilm formation, and virulence can be changed after being exposed to the space environment [1,2,3]. Conversely, the astronaut’s immune system is dysregulated [4,5]. Therefore, the existence of conditional pathogens may threaten the health of astronauts in the space environment. It is important to understand the phenotype and molecular changes of bacteria to ensure the health of astronauts during long-term space activities.

Proteins are the executor of most biological functions. With the development of proteomic technology, high-throughput protein identification became available for understanding global gene regulation. Tandem mass tag (TMT) technology is one of the most commonly used isobaric labeling technologies in mass spectrometry (MS) for the quantification of proteins present in different samples. The advantages of this method are high quantitative accuracy and high throughput, which enable the measurement of up to 16 samples simultaneously in a single run [6]. In this study, E. coli was carried by the SJ-10 returnable scientific experiment satellite in orbit for 12 days. The matched controls were cultured on the ground. The phenotypic changes of E. coli were explored, and the 6-plex TMT was used to compare the proteome of E. coli after exposure to the space environment. We found that proteomics results can explain phenotypic changes in the spaceflight group. This study should provide an important reference for understanding the effects of spaceflight on E. coli, which will contribute to keeping astronauts healthy during space flight.

2 Materials and methods

2.1 Strains and growth conditions

E. coli K12 strain (CGMCC 1.2389) was purchased from China General Microbiological Culture Collection Center (CGMCC). After cultivating E. coli to the exponential phase (OD600 = 1), 20 µL of bacteria was inoculated into an lysogeny broth (LB) agar slant culture medium. After being incubated at 37°C for 16 h, samples were cultured in space for 12 days, carried by the “SJ-10” satellite. The orbital height of the satellite is 252 km, the orbital inclination is 42°, and the average daily radiation equivalent dose is 160 µSv. Strains were stored at −20°C after returning.

2.2 Growth curves of E. coli

E. coli carried by the satellite and the ground control group were recovered on the LB solid medium at 37°C overnight. A single colony of each group of E. coli was inoculated in 10 mL of LB liquid medium and incubated at 150 rpm at 37°C. Growth curves were obtained by measuring OD600 every hour after inoculation for a total of 13 h.

2.3 Morphology of E. coli

As described in the previous study [7], the effect of spaceflight on the morphology of E. coli was studied. Briefly, the preserved strains of E. coli were inoculated into the LB solid medium and incubated at 37°C for 5 days to observe the colony wrinkles. To determine the biofilm formation, preserved strains of E. coli were recovered with 2 mL LB liquid medium in a 15 mL glass test tube at 37°C and 200 rpm until the exponential phase. OD600 of E. coli was measured after incubation. The culture medium in the test tube was discarded, and the test tube was washed twice with deionized water. The test tube was placed at 60°C for 1 h and stained with 5 mL 0.1% crystal violet solution for 15 min. The test tube was washed twice with sterile deionized water after discarding the crystal violet solution. Then 5 mL dimethyl sulfoxide was added into the test tube and OD570 was measured after 1 h. Relative biofilm production was calculated as 100 × OD570/OD600. Recovered samples were sent to the China Academy of Chinese Medical Sciences for scanning electron microscope (SEM) analysis with Hitachi S-3400N.

2.4 Environmental resistance assay

The environmental resistance assay was done according to the protocol described earlier [7]. Briefly, E. coli samples were recovered with the LB liquid medium at 37°C and 200 rpm until the exponential phase. Then samples were added into five mixed LB liquid media (1:100) containing ammonia (pH 9.0), 1% ethanol, 0.0003% hydrogen peroxide, HCl (pH 3.5), or 450 mmol/L NaCl. While the normal LB liquid medium was used as a background. After incubation for 1 h at 37°C and 200 rpm, the number of colonies was counted with the spread plate method. The survival rate was calculated as the number of colonies from the mixed LB medium divided by the number of colonies from the normal LB medium.

2.5 Protein extraction for quantitative proteomics

Protein extraction was performed using the protocol described previously with a few modifications [7]. In brief, the preserved strains of E. coli were recovered on LB solid medium at 37°C overnight. Single colonies from three technical replicates were inoculated in the LB liquid medium and incubated at 200 rpm at 37°C until the exponential phase (OD600 = 1). Samples were harvested by centrifugation at 4,000 rpm for 5 min at 4°C and washed with phosphate buffered saline three times. Then the samples were sonicated on ice for 3 min in lysis buffer containing 8 M urea, 2 mM ethylene diamine tetraacetic acid, 10 mM dithiothreitol (DTT), and 1% protease inhibitor cocktail. After centrifugation at 12,000g for 10 min, the supernatant was collected, and the protein concentration was determined by the bicinchoninic acid assay.

2.6 TMT labeling

TMT labeling was performed according to the manufacturer’s instructions (Thermo Fisher Scientific, USA) with some modifications [7]. Proteins (100 µg) in each group were reduced with reducing buffer (8 M urea, 10 mM DTT, 100 mM triethylammonium bicarbonate (TEAB), pH 8.0) in Amicon® Ultra-0.5 Centrifugal Filter (10 kDa) at 60°C for 1 h. Then samples were alkylated with iodoacetamide (final concentration of 50 mM) at room temperature in the dark for 40 min. After centrifugation at 12,000 rpm for 20 min, samples were washed three times with 300 mM TEAB and digested with trypsin (Promega, Madison, WI, USA) (enzyme to protein ratio 1:50) in TEAB buffer at 37°C overnight. Peptides from the spaceflight group were labeled with TMT tags 126, 127, and 128. Peptides from control samples were labeled with TMT tags 129, 130, and 131. Aqueous hydroxylamine solution (5% (w/v)) was added to quench the labeling reaction. The six samples were mixed and dried and then resuspended in buffer A (2% acetonitrile and 98% water with ammonia at pH 10) and fractionated to 15 fractions with 1100 HPLC System (Agilent Technologies, USA) coupling with Agilent Zorbax Extend RP column (5 µm, 150 mm × 2.1 mm). Samples were dried and stored at −20℃ until use.

2.7 LC-MS/MS analysis

All analyses were performed by a Q-Exactive mass spectrometer (Thermo Fisher Scientific, USA) coupled with a Nanospray Flex source (Thermo Fisher Scientific, USA) as described earlier [7]. Samples were redissolved with 0.1% formic acid and separated by a C18 column (15 cm × 75 µm) on an EASY-nLCTM 1200 system (Thermo Fisher Scientific, USA). The flow rate was 300 nL/min, and the linear gradient was 90 min. Full MS scans were acquired in the mass range of 300–1,600 m/z with a mass resolution of 70,000, and the automatic gain control (AGC) target value was set at 1e6. The ten most intense peaks in MS were fragmented with higher energy collisional dissociation with positive polarity in the data-dependent mode. MS/MS spectra were obtained with a resolution of 17,500 with an AGC target of 2e5 and a max injection time of 80 ms. Fragmentation was performed with normalized collision energy of 32 and dynamic exclusion of 30 s.

2.8 MS data analysis

The MS raw data were analyzed with Maxquant software (version 1.5.2.8) [8] using the Andromeda search engine to search against the UniProt E. coli K12 database. The following parameters were applied: isobaric type was selected as 6plex TMT; instrument type was selected as orbitrap with default parameters; the dynamic modifications were oxidation (M) and acetyl (protein N-term); the fixed modification was carbamidomethyl (C); I = L box was checked; a maximum of two missed cleavages was allowed. Peptides with a minimal length of seven amino acids were considered for protein identification and quantification. A false discovery rate of 0.01 was required for peptides and proteins.

2.9 Statistical analysis

Proteins quantified in all samples were considered for further analysis. The log 2 transformed intensity values were normalized with quantile using R (v3.5.3) package limma. Perseus software [9] was used to calculate the differentially expressed proteins with Student’s t-test. Permutation-based false discovery rate (FDR) with 250 randomizations was used for multiple hypothesis testing. Proteins with a fold change greater than 1.2 or lower than 5/6 with FDR <5% were significantly changed. The compare groups of growth curves permutation test [10] was used to compare the growth curves of E. coli in the spaceflight group and the control group. For other results, the SPSS software package (version 16.0) was used for statistical analysis with an unpaired Student’s t-test. The data are presented as means ± SD. All statistic tests were two sided, and statistical significance was set at P < 0.05.

3 Results

3.1 Effect of the space environment on the phenotype of E. coli

After being cultured in space for 12 days, the effect of the space environment on E. coli was investigated. We first studied the influence of the space environment on the morphology of E. coli. The result of the SEM showed that the morphology of E. coli in the spaceflight group has not changed significantly (Figure A1). There is no difference in the formation of wrinkles in the two groups of E. coli colonies (Figure A2a). No difference was observed in the relative biofilm formation between the spaceflight group and the control group (Figure A2b). Next, we studied the influence of the space environment on the growth rate of E. coli. As shown in Figure 1a, the growth rate of E. coli in the spaceflight group was slightly faster than that in the control group. However, there is no significant difference (P = 0.1) between the growth curves of the two E. coli groups. Finally, we studied the influence of the space environment on the environmental resistance of E. coli. The survival rate of E. coli in the spaceflight group was lower than that in the control group when cultured in LB medium containing HCl (pH 3.5) or 450 mM/L NaCl (Figure 1b and c). But there is no difference in the survival rate of E. coli between the spaceflight group and the control group in resisting hydrogen peroxide, alcohol, and alkaline environments (Figure A3).

Figure 1 The effect of space environment on the phenotype of E. coli. (a) The growth curves of E. coli under spaceflight environment compared with control. The survival rate of E. coli exposed to (b) HCl (pH 3.5) or (c) 450 mM/L NaCl in the spaceflight group and the control group. *P < 0.05.
Figure 1

The effect of space environment on the phenotype of E. coli. (a) The growth curves of E. coli under spaceflight environment compared with control. The survival rate of E. coli exposed to (b) HCl (pH 3.5) or (c) 450 mM/L NaCl in the spaceflight group and the control group. *P < 0.05.

3.2 TMT-based quantification proteomics for the analysis of E. coli

Three single colonies of E. coli from the spaceflight group and control group were cultured until the exponential phase. Equal amounts of proteins from each sample were digested and labeled with 6-plex TMT. In total, spectral searching identified 1982 protein groups and quantified 1981 protein groups (Figure 2a) with protein and peptide FDR at 0.01. Among them, 1969 protein groups that were quantified in all samples were used for further analysis. The reporter intensity of proteins in each sample was used as the relative quantitative value after log 2 transformed. The distribution of protein abundance in three replicates of the spaceflight sample and three replicates of the control sample showed good consistency of the TMT result (Figure 2b). Student’s t-test with permutation-based FDR correction was applied to identify the differentially expressed proteins between spaceflight groups and control groups after quantile normalization. We identified 73 differentially expressed proteins with FDR < 0.05 and ratio > 1.2 (Table S1) or ratio < 0.833 (Table S2). Among them, 72 proteins (98.6%) were downregulated in the spaceflight group compared to the control group (Figure 3a). Hierarchical cluster analysis was performed in Perseus with differentially expressed proteins for all the samples. As shown in Figure 3b, three replicates of the spaceflight sample and three replicates of the control sample were separated clearly as expected. These results demonstrated that the space environment influences the protein expression of E. coli. Furthermore, these results support the high reproducibility of our experiments, suggesting that TMT is a reliable quantitative proteomics method.

Figure 2 Quantitative analysis of E. coli proteome. (a) Venn diagram of protein quantified in controls (blue) and spaceflight group (red). (b) Box plot of protein abundance in each sample.
Figure 2

Quantitative analysis of E. coli proteome. (a) Venn diagram of protein quantified in controls (blue) and spaceflight group (red). (b) Box plot of protein abundance in each sample.

Figure 3 Differentially expressed proteins of E. coli. (a) Volcano plot of differentially expressed proteins. The red points represented proteins upregulated in the spaceflight group (FDR < 0.05; fold change ≥1.2). The blue points represented proteins downregulated in the spaceflight group (FDR < 0.05; fold change ≤0.833). (b) Hierarchical clustering of the differentially expressed proteins. The heat map represented the Z scores of protein levels across all samples.
Figure 3

Differentially expressed proteins of E. coli. (a) Volcano plot of differentially expressed proteins. The red points represented proteins upregulated in the spaceflight group (FDR < 0.05; fold change ≥1.2). The blue points represented proteins downregulated in the spaceflight group (FDR < 0.05; fold change ≤0.833). (b) Hierarchical clustering of the differentially expressed proteins. The heat map represented the Z scores of protein levels across all samples.

3.3 Effect of the space environment on the biological function of E. coli

Functional enrichment analysis was performed to identify the influence of the space environment on the biological function of E. coli. On the one hand, gene set enrichment analysis (GSEA) was performed with WebGestalt [11] to enrich the KEGG pathway. Pathways with permutation-based FDR < 0.05 were considered to be enriched in GSEA. As shown in Figure 4a, the bacterial motility proteins pathway was the only enriched KEGG pathway (FDR = 0.001), which was negatively regulated by the space environment (NES = −1.99). On the other hand, overrepresentation analysis (ORA) for the gene ontology (GO) biological process was performed with the differentially expressed proteins by DAVID [12]. Four biological processes including chemotaxis, intracellular pH elevation, glycolate catabolic process, and glutamate metabolic process were significantly enriched with the 72 downregulated proteins in the spaceflight group (Figure 4b). The pathway of intracellular pH elevation helps to maintain a near-neutral intracellular pH when cells are exposed to extremely acidic conditions. The downregulation of this pathway explains the decreased survival rate of E. coli in the spaceflight group.

Figure 4 Functional enrichment analysis of E. coli proteome. (a) GSEA was performed with the KEGG pathway. (b) Enriched GO biological process with the downregulated proteins in the spaceflight group. The x-axis shows the enrichment significance presented with –log 10 (p-value).
Figure 4

Functional enrichment analysis of E. coli proteome. (a) GSEA was performed with the KEGG pathway. (b) Enriched GO biological process with the downregulated proteins in the spaceflight group. The x-axis shows the enrichment significance presented with –log 10 (p-value).

4 Discussion

E. coli is an opportunistic pathogen, which can cause disease in the small bowels, large bowels, urinary tract, bladder, kidney, and central nervous system under certain conditions [13]. Studies [4] have shown that space flight can cause a decline in the immune function of astronauts. Besides, the space environment may cause changes in microbial pathogenicity. So it is important to understand the phenotype and molecular changes of E. coli under space environment. In the present study, we explored the phenotype and profiled the proteomes of E. coli after being cultured in space for 12 days. In total, 1982 protein groups were identified, and this is the largest proteomic dataset of E. coli under spaceflight conditions to our knowledge.

First, we analyzed the phenotypic of E. coli. No difference in growth curves and morphology between the spaceflight group and control group was observed, which was consistent with the previous report [5,14]. At the same time, there was no difference in the survival rate of E. coli against the hydrogen peroxide, alcohol, and alkaline environments between the two groups. The associated proteins were also not significantly different between the two groups. For example, OxyR protein, which is responsible for hydrogen peroxide resistance in E. coli [15], was not differentially expressed between the two groups. However, we found that the survival rate of E. coli in the spaceflight group was lower than that in the control group under acidic condition and hyperosmotic stress. To explore the mechanism of this phenotype, we analyzed the proteome result and found that five proteins involved in acid resistance and two proteins involved in osmotic pressure adjustment were downregulated in the spaceflight group. Among the five acid-resistance proteins, gadA and gadB are two types of glutamate decarboxylase that convert glutamate into gamma-aminobutyrate (GABA) [16]. gadC is involved in the transport of glutamate and GABA under acidic conditions [17]. The gad system, which protects cells from acidic conditions, was downregulated in the spaceflight group. In addition, the levels of hdeB and ydeP, which are important for the survival of E. coli in the acidic environment, were also decreased in the spaceflight group. Both proteomics results and phenotypic analysis showed that the acid resistance of E. coli in the spaceflight group was decreased. Yim et al. [18] found that microgravity decreased the acid resistance of E. coli Nissle 1917, which was consistent with our results. However, Zea et al. [19] observed an upregulation of acid resistance-related genes in E. coli ATCC 4157 after being cultured in a medium containing Gentamicin Sulfate in the International Space Station. The difference in these results may be caused by different experimental conditions such as strain, medium composition, spaceflight time, and environment. Consistent with the decline in the survival rate of E. coli in the spaceflight group under high salt conditions, the level of osmY that involved in the adaptation to hyperosmotic stress [20] was downregulated. Interestingly, low conductance mechanosensitive channel YnaI (ynaI) that protects cells against hypoosmotic stress [21] was also decreased in the spaceflight group. These results indicate that E. coli in the spaceflight group has a reduced ability to survive under extremely osmotic stress.

Next, we analyzed the biological function changes of E. coli under space environment. GO biological process enrichment analysis showed that proteins in chemotaxis, intracellular pH elevation, glycolate catabolic process, and glutamate metabolic process were significantly downregulated in the spaceflight group. Proteins enriched in the glutamate metabolic process, and intracellular pH elevation belongs to the gad system, which is related to acid resistance [16], indicating that the biological function changes of E. coli after exposure to the space environment are consistent with the phenotype result. Chemotaxis was the most significant biological process of enrichment analysis. Six proteins including fliG, fliM, cheA, cheB, tar, and tsr related to chemotaxis were downregulated in the spaceflight group. In addition, the bacterial motility protein pathway was enriched in GSEA, which is also related to chemotaxis. Our results indicate that the chemotaxis of E. coli in the spaceflight group was suppressed. However, different conclusions have been found in other similar studies. Tucker et al. [22] cultured E. coli MG1655 in minimal (3-(N-morpholino)propanesulfonic acid (MOPS) + glucose) medium and LB medium under a low-shear modeled microgravity (LSMMG) environment produced by a high-aspect rotating vessel. They found that genes involved in the E. coli acid tolerance response (gadE, hdeB), cell motility (flg and fli genes), and chemotaxis (cheZ, tar) were upregulated in LSMMG compared to the control under minimal MOPS medium. But no changes of these genes were observed in LSMMG compared to normal gravity controls under the LB medium. Only 14 downregulated genes were identified in LSMMG compared to the control under the LB medium. Those results and many other studies [18,19,23,24,25] demonstrated that the different space vehicles, bacterial strains, culture medium, and other factors can affect the response of E. coli to microgravity or spaceflight.

Tryptophan-specific transport protein (mtr) was the only upregulated protein in E. coli of the spaceflight group. This protein is involved in transporting tryptophan into the cell [26]. Our results showed that tryptophan is extremely important for E. coli in responding to the space environment. Interestingly, we found that other proteins with an upregulation trend (FDR < 0.05, 1 < ratio < 1.2) in the spaceflight group were all related to pyrimidine biosynthesis. In this pathway, carA (ratio = 1.15) and carB (ratio = 1.07) synthesize carbamoylphosphate from glutamine [27]. Then aspartate carbamoyltransferase catalyzes the conversion of carbamoylphosphate and aspartate to carbamoylaspartate [27]. PyrB (ratio = 1.13) is the catalytic subunit of aspartate carbamoyltransferase, and pyrI (ratio = 1.19) is the regulatory subunit of aspartate carbamoyltransferase. However, other enzymes of pyrimidine biosynthesis did not show an upregulation trend in the spaceflight group. The role of cumulative carbamoylaspartate in the spaceflight group of E. coli needs further study.

5 Conclusions

Our research explored the changes in the phenotype and proteome of E. coli after exposure to the space environment. The results of the phenotypic experiment showed that the survival rate of E. coli in the spaceflight group decreased in acidic and high-salt environments. Proteomics analysis revealed 73 differentially expressed proteins in the spaceflight group compared to the control group. Functional enrichment analysis showed that proteins in chemotaxis, intracellular pH elevation, glycolate catabolic process, and glutamate metabolic process were significantly downregulated in the spaceflight group. These results indicate that proteomics data can explain phenotypic changes, and our research will provide a theoretical basis for microbial safety in the space environment.

Acknowledgements

We thank Shanghai LuMing Biological Technology Co. Ltd. for proteome detection and data analysis.

  1. Funding information: This work was supported by the National Significant Science Foundation (2015ZX09J15102) and Pre Research of Manned Space Flight (020104).

  2. Author contributions: Y.L.: data analysis and manuscript preparation; C.X., G.Z., Y.W., Y.Z., and Y.Y.: methodology and software; J.W. and Y.L.: design, review, and editing the manuscript. All authors read and approved the final manuscript.

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

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available in the ProteomeXchange Consortium (http://proteomecentral.proteomexchange.org) via the iProX partner repository [13] with the dataset identifier PXD023158 (https://www.iprox.cn/page/ProjectFileList.html?projectId=IPX0002665000).

Appendix

Figure A1 Cell morphology of E. coli under control and spaceflight environment.
Figure A1

Cell morphology of E. coli under control and spaceflight environment.

Figure A2 The influence of space environment on E. coli biofilm. (a) Colony wrinkles of E. coli after being exposed to spaceflight (left) compared with control (right). (b) The relative biofilm formation of E. coli.
Figure A2

The influence of space environment on E. coli biofilm. (a) Colony wrinkles of E. coli after being exposed to spaceflight (left) compared with control (right). (b) The relative biofilm formation of E. coli.

Figure A3 Survival rate of E. coli under spaceflight environment compared with control. (a) E. coli cultured in LB liquid media with 0.0003% hydrogen peroxide, (b) ammonia (pH 9.0), or (c) 1% ethanol.
Figure A3

Survival rate of E. coli under spaceflight environment compared with control. (a) E. coli cultured in LB liquid media with 0.0003% hydrogen peroxide, (b) ammonia (pH 9.0), or (c) 1% ethanol.

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Received: 2022-12-03
Revised: 2023-01-14
Accepted: 2023-01-22
Published Online: 2023-02-28

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

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

Articles in the same Issue

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  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-2022-0576
Keywords for this article
spaceflight; proteomics; Escherichia coli
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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  17. Single-cell transcription analysis reveals the tumor origin and heterogeneity of human bilateral renal clear cell carcinoma
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  35. Triple-negative mouse breast cancer initiating cells show high expression of beta1 integrin and increased malignant features
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  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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