Startseite Untargeted metabolomics reveals sour jujube kernel benefiting the nutritional value and flavor of Morchella esculenta
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Untargeted metabolomics reveals sour jujube kernel benefiting the nutritional value and flavor of Morchella esculenta

  • Fenfang Wu , Zhiyuan Li , Xiaoni Chen , Xinlei Si und Shan Lin EMAIL logo
Veröffentlicht/Copyright: 31. August 2023
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Open Life Sciences
Aus der Zeitschrift Open Life Sciences Band 18 Heft 1

Abstract

Nucleosides, organic acids, and amino acids separated from Morchella esculenta are well known for their nutritional value and flavor. However, how to increase their content in a better way has been a challenge. In this study, the effect of adding jujube kernel on the active components of M. esculenta was investigated by untargeted metabolomics using UPLC-MS/MS. A total of 1,243 metabolites were identified, of which 262 metabolites (21.078%) were organic acids and derivatives, 245 metabolites (19.71%) were lipids and lipid-like molecules, and 26 metabolites (2.092%) were nucleosides, nucleotides, and analogues. Subsequently, differential metabolites between groups were screened by the orthogonal partial least squares-discriminant analysis model, which showed that 256 metabolites were identified as significantly different for the positive ion model and 149 for the negative ion model. Moreover, significant differential metabolites (VIP > 1, P < 0.05) in annotation of kyoto encyclopedia of genes and genomes pathway were investigated, which showed that ABC transporters were the most commonly observed transporters, followed by pyrimidine metabolism and purine metabolism. The results indicated that the main components of jujube kernel might be conducive to the accumulation of nucleoside organic acids and amino acid metabolites in M. esculenta. These results provide important information for the understanding of more suitable way for cultivation of M. esculenta.

Graphical abstract

Keywords: Morchella esculenta ; metabolomics; nutritional value; biological activity

1 Introduction

Morchella esculenta (also known as “Yellow morel”) is a widely distributed fungus all over the world, especially in France, Germany, USA, India, and China, which is generally found at low altitude plains to high altitudes of about 3,200 m, mostly growing in the humus layer of broad-leaved forests or coniferous and mixed broad-leaved forests [1]. M. esculenta is generally divided into 28 species and belongs to the species of Morchella, genus of Morchellaceae, family of Oncobacteria, subdivision of Ascomycetes, which has been valued for its high nutritional, medicinal, and physiological functions [2]. Recently, the biological activity of M. esculenta derived compounds has attracted attention, which has many functional properties including antibacterial [3], anticancer [4,5], and anti-inflammatory [6]. Moreover, current research demonstrated a wide range of biological functions including antioxidant activities [7,8], immunomodulatory activities [9], hepatoprotective effects [10], and anti-melanogenesis effects [11]. Due to health benefits and flavor, morels are not only provided as dishes but also used in skin care products. Recently, it has been cultivated and matured in our country and can be sold in large quantities [12].

Suanzao kernel is the dried seed of Jujube genus in the rhamnus family [13]. It has the functions of calming the heart, nourishing the liver, collecting sweat, and generating fluid [14]. Generally, more than 100 kinds of chemical components have been isolated and identified from sour jujube kernel, among which saponins are the main components [15]. Jujube saponins can be divided into tetracyclic triterpenes and pentacyclic triterpenes according to the structure of aglycones. At present, over 30 saponins have been identified from jujube kernel [16]. Current pharmacological studies showed that saponins are the main active components of jujube kernel [17,18]. Furthermore, the fermentation medium of Kombucha SCOBY with jujube kernel enhanced its sedative and hypnotic effect, which provided a new approach to process Chinese medicine with better functional effects and acceptable flavor [19]. Moreover, the addition of jujube kernel to the liquid fermentation medium of Schizophyllum commune Fr showed that the effective biomass, as well as the crude polysaccharide and total saponin content were significantly increased. Therefore, adding jujube kernel and saponins in jujube kernel into culture medium of M. esculenta may have positive effects on the metabolites and nutrient composition.

On the basis of genome, transcriptome, proteome, and other omics, metabolome is considered as a new “histology” [20]. At present, metabolomics has been widely used in many fields. Metabolomics was used to compare the metabolic amount between the experimental group and the control group to find out the differential metabolites, which can help in the screening of biomarkers, or to study the biological processes involved in the differential metabolites, to reveal the mechanisms of their involvement in life activities, and to completely study the regulatory pathways [21]. According to the detection mode, the metabolome can be divided into two categories: untargeted and targeted [22]. Non-targeted detection technologies are mostly based on high-resolution mass spectrometry, which can realize unbiased, large-scale and systematic detection of various metabolites in samples, providing an “aerial” view to reflect the maximum perturbation of metabolic levels in organisms, and therefore suitable for pre-project basic research [23]. It is suitable for metabolite detection of specific interest and validation of non-target metabolomes.

In order to find out a better way of cultivation, this article studied the various cultivation ways of Morchella. Subsequently, high-resolution non-targeted metabolomics technology was applied to detect metabolites in samples using ultra-high performance liquid chromatography-tandem time-of-flight mass spectrometry (UHPLC-Q-TOF MS), and the differential metabolite analysis may provide important information for the understanding of more suitable way to cultivate M. esculenta.

2 Materials and methods

2.1 Reagents and samples

Fresh morel mushrooms from two different cultivation methods were collected during their fruiting period. This matrix was first prepared by wheat (40%), mixed wood chips (30%), rice husk (20%), and humus (10%). Then, an extra lime (1%), gypsum (2%), potassium dihydrogen phosphate (0.1%), and sour jujube kernel (5%) were added. In addition, the matrix of control group has the same components except that no sour jujube kernel is added. Formic acid and ammonium acetate were commercially available from Sigma-Aldrich (Madrid, Spain). Methanol and acetonitrile were obtained from ANPEL (Shanghai, China). A Milli-Q water purification unit (Millipore, Millipore, MA, USA) was used throughout the study. The chemical reagents and solvents used in this product have been subjected to high performance liquid chromatography or analysis.

2.2 Sample preparations

Production conditions of morel mushrooms are described as follows: soil moisture of 60–70%, temperature of 10–20°C, sunlight transmission of 30%, soil pH requirements between 6.5 and 7.5, and the need for sufficient oxygen. After morel mushrooms were harvested, they were dried and crushed into powder form for untargeted metabolomics analysis. All frozen samples were ground to a fine powder and passed through a 425 µm sieve. Fine powder of 1.0 g was determined by UPLC-Q-TOF-MS and extracted by ultrasonic wave for 30 min. Next, the extract was centrifuged at 12,000 rpm for 20 min at 4°C. Next, the supernatant of each tube (100 µL) was filtered through a 0.22 µm micro-sieve and transferred to an LC vial. The content of the sample was determined by UPLC-Q-TOF-MS method, and the sample was stored at 4°C. In addition, all samples were equally divided into several parts, fully stirred by vortex method, and then measured by liquid chromatography to obtain quality control samples.

The sample was slowly dissolved at 4°C, the supernatant was dried in vacuo, and 100 μL of acetonitrile aqueous solution (acetonitrile:water = 1:1, volume ratio) was added for mass spectrometry. After centrifuging the supernatant at 14,000g for 15 min at 4°C, the supernatant was harvested for analysis.

2.3 Data acquisition of UPLC-Q-TOF-MS

The sample with hydrophilic interaction liquid chromatography (HILIC) was separated by Agilent 1290 InfinitLC (UHPLC) system at a column temperature of 25°C. The flow rate was set at 0.5 mL/min, and the injection volume was set to 2 μL, where A was water + ammonium acetate + ammonia water 25 mmol, B was acetonitrile, and gradient elution was carried out according to the following steps: 0–0.5 min, 95% B. Within 0.5–7 min, the B value changes linearly from 95 to 65%; within 7–8 min, the B value changes linearly from 65 to 40%; within 8–9 min, the B value remains at 40%; from 9 to 9.1 min, the B value changes linearly from 40 to 95%; from 9.1 to 12 min, the B value remains at 95%. During the measurement, the sample was placed at 4°C. During testing, the sample was placed in the autosampler. In order to eliminate the fluctuation of the measurement signal, the sample was analyzed in irregular continuous. On this basis, the QC samples were added to the sample library, and the experimental results were monitored and evaluated in real time.

Primary and secondary spectra were obtained using an AB TripleTOF6600 mass spectrometer. After HILIC chromatography, the ESI source conditions are Gas1 (Gas1) = 60, Gas2 (Gas2) = 60, CUR (CUR) = 30, source temperature 600°C, and IonSapary Voltage Floating ±5,500 V (positive, negative); the m/z scan (m/z) range of TOF MS is set at 60–1,000 Da, the m/z scan (m/z) range of product ions is set at 25–1,000 Da, the cumulative scan time of TOF MS is set at 0.20 s/s/s, and the cumulative scanning (m/z) time of product ions is set at 0.05 s/s. This project intends to adopt a highly sensitive and high-precision information association acquisition method, on this basis, to study the declustering potential: ±60 V (both positive and negative), collision energy (35 ± 15 eV), excluding isotopes below 4 Da, observing ten candidates per cycle.

2.4 Data processing and multivariate analysis

The samples in Wiff format were converted into mzXML files by ProteoWizard, and then XCMS software was used to correct the peak position of the sample, and the peak position correction and peak position extraction were performed on the sample. This project will identify the structure of the metabolites obtained by XCMS and preprocess them, then evaluate the quality of the test results, and conduct statistical analysis on the results. The specific contents of data analysis include univariate statistical analysis, multidimensional statistical analysis, screening of differential metabolites, correlation analysis of differential metabolites, and kyoto encyclopedia of genes and genomes (KEGG) path analysis (http://www.genome.jp/kegg/pathway.html).

3 Results

3.1 Quality evaluation of experimental data

The stability of the instrument, the repeatability of the experiment, and the reliability of the experiment were comprehensively evaluated. The test system designed in this article has satisfied the performance, and the test results are stable and reliable. The metabolite profile obtained from the experiment can reflect the biological characteristics of the sample itself.

The total ion current curve of the QC samples was compared with the overlaid spectral curves shown in Figure S1a and b. Through the analysis of the two methods, it is concluded that the response intensities and retention times of the peaks basically overlapped, indicating that the variation caused by the instrumental error was small during the whole experiment.

Population sample principal component analysis (PCA) was performed on the peaks extracted from the total test sample and the QC sample, as shown in Figure 1a and b. The results indicated that the proton exchange membrane showed obvious cluster structure in the positive and negative ion models, which suggested that the method had good reproducibility.

Figure 1 PCA analysis of QC samples: (a) PCA analysis of the overall sample in positive ion mode and (b) PCA analysis of the overall sample of negative ion patterns.
Figure 1

PCA analysis of QC samples: (a) PCA analysis of the overall sample in positive ion mode and (b) PCA analysis of the overall sample of negative ion patterns.

3.2 Identification of metabolites

In this study, the structures of match metabolites were determined in biological samples to retention times. Furthermore, the number of identified metabolites was calculated, and it was found that there were 1,243 metabolites identified by the combination of positive and negative ions, as shown in Table 1. In addition, the metabolites were chemically classified. The chemical taxonomic analysis of all metabolites (including metabolites separated by positive and negative ions) was carried out, and the distribution of various types of metabolites is shown in Figure 2.

Table 1

Statistics of identification of metabolites by positive and negative ion patterns

Detection mode Number of metabolites identified
Positive ion mode (Pos) 886
Negative ion mode (Neg) 423
Figure 2 Number share of identified metabolites in each chemical classification.
Figure 2

Number share of identified metabolites in each chemical classification.

3.3 Identification of the differential metabolites

In this study, we analyzed the differences between the two samples by multiplier change analysis (FC analysis) and t-test/non-parametric test. On this basis, the differences of different types of metabolites, including unknown metabolites, in positive and negative ion modes were compared. As shown in Figure S2, the differential metabolites with FC > 1.5 or FC < 0.67, P value <0.05 were visualized by a volcano plot. In order to visualize the classification attribution of the differential metabolites, different colors were used to make the distinction, and the results are shown in Figure 3. By studying the metabolic pathways involved in differential metabolites and retrospectively identifying regulatory enzymes and genes, it can help to reveal the mechanisms of life activities that they are involved in.

Figure 3 Volcano map of differential metabolite taxonomic attribution: (a) positive ion mode volcano map and (b) negative ion mode volcano map.
Figure 3

Volcano map of differential metabolite taxonomic attribution: (a) positive ion mode volcano map and (b) negative ion mode volcano map.

3.4 Multidimensional statistical analysis

In this study, we used PCA to understand the overall distribution trend of the data and the differences between the various groups of the data. Furthermore, PCA analysis was performed for each group, and the PCA score plot of the sample vs group is shown in Figure S3. After seven cross-checks, the obtained PCA results are consistent with Table 2. Therefore, the PCA of metabolites can better reflect the differences within the group and between the groups.

Table 2

PCA model parameters

Ionic mode Sample group A R 2 X (cum)
Positive ion mode (Pos) SZR_vs_CON 2 0.764
Negative ion mode (Neg) SZR_vs_CON 2 0.703

Note: A represents the main component score and R 2 X represents the model explanation rate of the X variable.

Orthogonal partial least squares-discriminant analysis (OPLS-DA) can enhance the resolution and accuracy of the model. In Figure S4, the OPLS-DA model scores for an exemplary control group are shown, and indicate that the OPLS-DA model is able to distinguish between the two sample groups.

The model evaluation parameters (R 2 Y, Q 2) obtained by seven cross-tests are shown in Table 3. The results suggested that the model has good stability and reliability with Q 2 > 0.5. The substitution test plot for the OPLS-DA model is shown in Figure 4, which indicates that the R 2 and Q 2 of the stochastic model gradually decrease as the substitution retention rate decreases, implying that there is no overfitting in the original model and that the model is robust.

Table 3

Evaluation index of OPLS-DA

Ionic mode Sample group A R 2 X (cum) R 2 Y (cum) Q 2 (cum)
Positive ion mode (Pos) SZR_vs_CON 2 0.739 1 0.993
Negative ion mode (Neg) SZR_vs_CON 2 0.7 1 0.998

Note: R 2 Y represents the model explanation rate of a Y variable and Q 2 represents the prediction of the model function.

Figure 4 OPLS-DA displacement test results: (a) positive ion mode OPLS-DA displacement test and (b) negative ion mode OPLS-DA displacement test.
Figure 4

OPLS-DA displacement test results: (a) positive ion mode OPLS-DA displacement test and (b) negative ion mode OPLS-DA displacement test.

3.5 Screening for differential metabolites

On this basis, we applied the OPLS-DA model to calculate the importance of each metabolite, evaluate the taxonomic differences of each metabolite in different categories, and discover the different lipid molecules with biological significances. This study was based on the two indicators of OPLS-DA VIP > 1 and P < 0.05 for screening metabolites with significant differences, and metabolites with VIP > 1 played an important role in the interpretation of the model. As can be seen from Figure S5, the change in the number of metabolic differences that are significantly different for ploidy recognition is represented in the bar graph.

3.6 Bioinformatic analysis of differential metabolites

The screened out metabolites with significant differences are subjected to subsequent original signal analysis, including correlation analysis, path analysis, and cluster analysis.

Each sample group is classified by a hierarchical method, and a cluster tree that can reflect the similarity between sample groups is obtained, and a result as shown in Figure S6 is obtained. In the same cluster, the similarity between samples is high. Obviously different metabolites (VIP > 1, P-value <0.05) are shown in Figure S7. Clustered metabolites, which exhibit similar expression profiles at the gene level, may have similar effects, and may also have the same metabolic pathways.

3.7 Correlation analysis

According to the correlation analysis method, the correlation analysis was carried out on the metabolites with significant differences, and the results of the correlation analysis were displayed as a correlation heat map, which is shown in Figure S8. In order to make the mutual regulation among various metabolites clear, this article transforms the correlation matrix into the chord curve and network curve as shown in Figure 5 and Figure S9. The chord diagram as well as the network diagram both show that the molecular pairing of metabolites has a certain correlation, namely: r > 0.8, P < 0.05 [24], which is an indicator that can be adjusted appropriately. Among them, the chord diagram better reflects the correlation between metabolites, while diagram of the network better reflects the correlation among metabolites [25], and they have their own strengths. Therefore, correlation analysis will reveal the degree of similarity between metabolites (VIP > 1, P < 0.05), and provide basis for in-depth comprehending the regulatory mechanism of metabolites when physiological states change.

Figure 5 Chord diagram between metabolites: (a) positive ion mode chord diagram and (b) negative ion mode chord diagram.
Figure 5

Chord diagram between metabolites: (a) positive ion mode chord diagram and (b) negative ion mode chord diagram.

3.8 KEGG pathway annotation and analysis

In this study, the differential metabolites were marked (VIP > 1, P < 0.05) using the KEGG pathway map function in the KEGG pathway. Furthermore, more than five KEGG metabolic pathways were screened out, different metabolites were marked on the KEGG metabolic pathways, and the change curves of different metabolites on the KEGG metabolic pathways were drawn as a heat map, and is shown in Figure S10.

In addition, the results of the metabolic pathway enrichment analysis are presented as bubble and bar graphs, and the results are shown in Figure 6. Therefore, KEGG pathway adopts Fisher’s precise test method, takes KEGG pathway and its related metabolic pathways as a whole, and calculates the significance of metabolite accumulation in each pathway, so as to find out the metabolism that is significantly affected by substances and signaling pathways.

Figure 6 KEGG enrichment pathway diagram (bubble diagram).
Figure 6

KEGG enrichment pathway diagram (bubble diagram).

4 Discussion

As a traditional fungus for both medicine and food, M. esculenta is widely distributed in South Korea, China, Japan, Europe, and other countries [1]. M. esculenta is rich in sugars, proteins, vitamins, minerals, and other ingredients. In addition, M. esculenta is rich in all kinds of essential amino acids, of which glutamic acid is the most, followed by aspartate and leucine [26]. Recently, M. esculenta is deeply favored by consumers because of its unique flavor, rich nutrition, and high medicinal value. Different medium components have different effects on the nutritional composition of M. esculenta [27]. In order to understand the effect of adding sour jujube kernel to the medium on the metabolism of M. esculenta, we developed a non-targeted metabolomics-based approach. Studies have found that adding sour jujube kernel during the cultivation process can increase the contents of organic acids, lipids, and nucleosides in M. esculenta thus improving the nutritional value and taste of M. esculenta.

Recently, UPLC-Q-TOF/MS-based method combined with multivariate statistical analysis was applied to distinguish small molecule metabolites with molecular weights <1,500 Da in a variety of organisms [28,29]. Typical food quality substances such as nucleosides, organic acids, and amino acids in M. esculenta can be effectively screened by non-targeted metabolomics method [30]. In this study, the metabolic profile changes of the samples were separately analyzed by metabolomics method based on UHPLC-Q-TOF MS. Quality control tests indicated that the instrument performed well and the test results were stable and reliable. The metabolite profiles obtained from the experiments could reflect the biological properties of the samples themselves.

The aroma of M. esculenta is mainly due to its high content of small molecules such as soluble sugars, polyols, amino acids, organic acids, etc. [31]. In M. esculenta, amino acids, such as alanine and glutamic acid, are important taste activators [32], which have floral aroma properties, and serine and tyrosine have wine-like properties. In general, the amino acid composition, content, and metabolites in protein have a great influence on the quality of protein. Meanwhile, organic acid is still an important substance in organisms, which plays a very important role in keeping the quality as well as nutritional value of food [31]. Furthermore, many kinds of organic acids, such as succinic acid, protect M. esculenta from various diseases because of their antioxidant capacity, and it also has positive effects on preservation [33]. In consequence, the results showed that amino acids as well as organic acids were the main factors in M. esculenta affecting its quality and flavor. In this study, both organic acids and amino acid differential metabolites showed a significant up-regulation trend in M. esculenta, whose medium was supplemented with sour jujube kernel, resulting in a typical M. esculenta flavor. Interestingly, the organic acid is dominated by a ternary or Krebs cycle, and the nutrients provided by sour jujube kernel may increase the metabolic rate and thus reduce the organic acid content.

Pyrimidine metabolism is an important form of nucleotide metabolism, which plays an important role in the bioenergetic processes and transport forms of carbohydrates such as sucrose, cellulose, cell wall matrix polysaccharides, and sugar synthesis [34]. In this study, we have systematically annotated several compounds involved in the pyrimidine metabolic pathway. Among them, the content of pyrimidine by the addition of sour jujube kernel was significantly up-regulated compared to the control group. In addition, a close link exists between organic nitrogen sources and amino acid metabolism [35]. Organic nitrogen sources may need to be supplied from external nutrient bags during the growth of hexagonal grass [36]. In this study, we conducted a systematic annotation analysis of metabolites with significantly different growth, and found significant metabolic differences involved in amino acid metabolism associated with the nitrogen source, which may be related to the added date palm enriched nitrogen source and delicately balanced during asexual growth of M. esculenta.

5 Conclusion

Regulatory differences between cultures, differential metabolites, including lipids, organic acids, and amino acids, have been shown to be viable biomarkers for differentiating regions and understanding metabolic profiles. Nevertheless, the results of this study are limited in their strength. Additional studies under controlled conditions are necessary to analyze the effects of environmental factors, intrinsic factors (including phylogeny and life cycle), and physicochemical changes in M. esculenta during culture/processing, particularly with regard to adenosine, organic acids, amino acids, lipids, and their detailed composition. The impact on potential applications is then assessed. Furthermore, this metabolomic analysis approach provided clear trends among different sources, which demonstrated the validity of the method. Further studies, such as absolute quantitative methods and GC/MS-based platform studies, are needed to gain insight into the effects of provenance on the nutritional value and flavor of M. esculenta.

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  1. Funding information: This work was supported by the National Natural Science Foundation of China (82172107), Basic and Applied Basic Research Foundation of Guangdong Province (2021A1515011927, 2021A1515010918), Shenzhen Municipal Science and Technology Innovation Committee (JCYJ20210324135014040, JCYJ20210324135600002, JCYJ20220818103407016), and Longgang District Special Fund for Economic and Technological Development (LGKCYLWS2022007, LGKCYLWS2020068).

  2. Author contributions: All authors contributed to the concept and design of the study. S.L. and F.F.W. performed the experiment, generated the data, and wrote the original draft. S.L. and X.N.C. conceived and designed the experiments. F.F.W. has reduced repetition and improved the syntax. X.L.S. and Z.Y.L. assisted with the experiments and analysis of the data. All authors contributed to the study and approved the manuscript.

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

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

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Received: 2023-03-16
Revised: 2023-05-08
Accepted: 2023-08-02
Published Online: 2023-08-31

© 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-2022-0708
Schlagwörter für diesen Artikel
Morchella esculenta; metabolomics; nutritional value; biological activity
Creative Commons
BY 4.0

Artikel in diesem Heft

  1. Biomedical Sciences
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  19. Long noncoding RNA ACART knockdown decreases 3T3-L1 preadipocyte proliferation and differentiation
  20. Surgery, adjuvant immunotherapy plus chemotherapy and radiotherapy for primary malignant melanoma of the parotid gland (PGMM): A case report
  21. Dosimetry comparison with helical tomotherapy, volumetric modulated arc therapy, and intensity-modulated radiotherapy for grade II gliomas: A single‑institution case series
  22. Soy isoflavone reduces LPS-induced acute lung injury via increasing aquaporin 1 and aquaporin 5 in rats
  23. Refractory hypokalemia with sexual dysplasia and infertility caused by 17α-hydroxylase deficiency and triple X syndrome: A case report
  24. Meta-analysis of cancer risk among end stage renal disease undergoing maintenance dialysis
  25. 6-Phosphogluconate dehydrogenase inhibition arrests growth and induces apoptosis in gastric cancer via AMPK activation and oxidative stress
  26. Experimental study on the optimization of ANM33 release in foam cells
  27. Primary retroperitoneal angiosarcoma: A case report
  28. Metabolomic analysis-identified 2-hydroxybutyric acid might be a key metabolite of severe preeclampsia
  29. Malignant pleural effusion diagnosis and therapy
  30. Effect of spaceflight on the phenotype and proteome of Escherichia coli
  31. Comparison of immunotherapy combined with stereotactic radiotherapy and targeted therapy for patients with brain metastases: A systemic review and meta-analysis
  32. Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation
  33. Association between the VEGFR-2 -604T/C polymorphism (rs2071559) and type 2 diabetic retinopathy
  34. The role of IL-31 and IL-34 in the diagnosis and treatment of chronic periodontitis
  35. Triple-negative mouse breast cancer initiating cells show high expression of beta1 integrin and increased malignant features
  36. mNGS facilitates the accurate diagnosis and antibiotic treatment of suspicious critical CNS infection in real practice: A retrospective study
  37. The apatinib and pemetrexed combination has antitumor and antiangiogenic effects against NSCLC
  38. Radiotherapy for primary thyroid adenoid cystic carcinoma
  39. Design and functional preliminary investigation of recombinant antigen EgG1Y162–EgG1Y162 against Echinococcus granulosus
  40. Effects of losartan in patients with NAFLD: A meta-analysis of randomized controlled trial
  41. Bibliometric analysis of METTL3: Current perspectives, highlights, and trending topics
  42. Performance comparison of three scaling algorithms in NMR-based metabolomics analysis
  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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Heruntergeladen am 6.9.2025 von https://www.degruyterbrill.com/document/doi/10.1515/biol-2022-0708/html?lang=de
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