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Berberine suppressed sarcopenia insulin resistance through SIRT1-mediated mitophagy

  • Xiaojuan Su , Danqi Yang , Yu Hu , Ying Yuan EMAIL logo and Le Song EMAIL logo
Published/Copyright: July 17, 2023
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Open Life Sciences
From the journal Open Life Sciences Volume 18 Issue 1

Abstract

Abnormal mitochondrial function resulting in inadequate energy supply leads to sarcopenia and IR, suggesting that maintaining mitochondrial homeostasis by regulating mitophagy may be a promising strategy for sarcopenia IR therapy. Herein, we constructed sarcopenia mice model, which was treated with berberine and/or SIRT1/mitophagy inhibitors, and the activity of SIRT1/mitophagy signaling pathway was identified. Then, muscle tissue, blood biochemical index, inflammatory factors, GTT, and ITT were detected. We found that berberine treatment increased the body weight and alleviated d-galactose-induced weight loss in mice. SIRT1/mitophagy inhibitors suppressed the effects of berberine in the treatment of sarcopenia. The effect of berberine on the increase of muscle tissue, improving metabolic disorders, reducing the expression of inflammatory factors, and suppressing sarcopenia insulin resistance (IR) were reversed by SIRT1/mitophagy inhibitors. Our study establishes proof-of-concept to distinct the effect of berberine in sarcopenia IR, and provides strong evidence to support the hypothesis that berberine-induced SIRT1 triggers mitochondrial autophagy pathway and suppresses IR in sarcopenia.

Keywords: berberine; sarcopenia; insulin resistance; SIRT1-mediated mitophagy

1 Introduction

As an essential energy generator for tissue homeostasis, the quality and quantity of mitochondria were strictly controlled [1]. Mitophagy is an evolutionarily conserved cellular process which removes dysfunctional or excess mitochondria, thereby fine-tuning mitochondrial number and maintaining energy metabolism [2]. Mitophagy mediated by PINK1 and Parkin is a common mitochondrial quality control pathway. PINK1 and Parkin recruit damaged mitochondria and autophagosomes and then fuse with lysosomes to form autophagosomes and degrade mitochondria [3]. Therefore, the study of mitophagy regulated by which substances under pathological conditions is a key scientific questions that need to be answered urgently.

Sarcopenia is a syndrome caused by continuous loss of skeletal muscle mass, strength, and function [4]. Skeletal muscle is one of the mainly target of insulin and responsible for most glucose metabolism. Therefore, skeletal muscle loss may produce insulin resistance (IR), which leads to a large number of systemic inflammations and metabolic disorders [5]. In addition, reports showed that sarcopenia increases the incidence of type 2 diabetes [6]. Multiple studies have noted that sarcopenia and IR are related to mitochondria function abnormalities [7]. Abnormal mitochondrial function resulting in inadequate energy supply leads to sarcopenia and IR, suggesting that maintaining mitochondrial homeostasis by regulating mitophagy may be a promising strategy for sarcopenia IR therapy.

Berberine is the main bioactive component of Coptis which improves sensitivity of insulin and ameliorates metabolic disorders [8]. Berberine regulates IR of skeletal muscle and tissue inflammation by up-regulating expression level of GLUT4 and increasing skeletal muscle glucose uptake, accompanied by an increase in skeletal muscle fiber number [9]. Therefore, berberine plays an important role in skeletal muscle metabolism and insulin sensitivity. However, the relationship between mitophagy and berberine remains unclear.

2 Methods

2.1 Model construction of sarcopenia

The mice were divided into five groups (blank group, model group, treatment group, SIRT1 inhibition group, and mitochondrial autophagy inhibition group, n = 5). Model construction of sarcopenia was performed as described previously [10]. Except the blank group, the other four groups were given d-galactose (Med Chem Express, USA; 400 mg/kg, prepared with 0.9% normal saline) by intrabitoneal injection, once a day for 60 days.

  1. Ethical approval: The research related to animal use has been complied with all the relevant national regulations and institutional policies for the care and use of animals, and has been approved by the Ethics Committee of Zhongshan Hospital, Fudan University (KZ0020).

2.2 Drug administration and tissue sample collection

The treatment group was given berberine (50 mg/kg, Med Chem Express, USA), intragastric administration once a day for 30 days. In addition to berberine, SIRT1 inhibition group was also given selisistat (20 mg/kg, Med Chem Express, USA) and was administered by intrabitoneal injection once every 3 days for 30 days. In addition to berberine, the mitochondria autophagy inhibition group was additionally given U0126-EtOH (10 mg/kg, Med Chem Express, USA) by intrabitoneal injection once every 3 days for 30 days. The mice were sacrificed to collect blood, gastrocnemius muscle, subcutaneous fat, visceral fat, and brown fat for subsequent use.

2.3 Biochemical index detection of serum

The blood was let to stand for about 30 min, and the serum was completely collected by centrifugation at 3,000 rpm/min at 4℃ for 10 min. The contents of blood glucose, insulin, triglycerides, cholesterol, low density lipoprotein cholesterol, high density lipoprotein cholesterol, free fatty acids, and C-reactive protein were detected.

2.4 Glucose tolerance test (GTT)

All groups of mice were fasted 16 h before the experiment and water intake during the fasting period was kept normal. Each mouse was weighed and labeled. The tail end of mouse was cut off by 1–2 mm and gently squeezed. After the blood was enriched into a drop, it was evenly smeared on the blood glucose test paper and recorded as the blood glucose value of 0 min. After 30 min, the glucose solution prepared with 0.9% saline solution was given intragastrically at 1 g/kg. The blood glucose was measured at 15, 30, 60, 90, and 120 min, respectively.

2.5 Insulin tolerance test (ITT)

All groups of mice were fasted 4 h before the experiment and water intake during the fasting period was kept normal. Each mouse was weighed and labeled. The tail end of mouse was cut off by 1–2 mm, and the tail was gently squeezed. After the blood was enriched into a drop, it was evenly smeared on the blood glucose test paper and recorded as the blood glucose value of 0 min. After 30 min, the insulin was given as intraperitoneal injection at 0.75 U/kg. The blood glucose was measured at 15, 30, 60, 90, and 120 min, respectively.

2.6 ELISA

ELISA assay was performed using ELISA kit (Wellbio, China). The sample diluent, standard, and serum samples were added to the enzyme-labeled well, 50 µL per well. Coated and incubated at 37℃ for 40 min. Add 350 µL washing buffer to each well, shake for 2 min. Biotinylated antibody diluent was added to the blank well, and 100 µL biotinylated antibody working solution was added to the other wells. The mixture was coated and incubated at 37℃ for 30 min. Add 350 µL washing buffer to each well, shake for 2 min. Each well was added with SABC working solution and incubated at 37℃ for 20 min. Then added 350 µL washing liquid to each well and shaken for 2 min. Added TMB mixture to each well and incubated at 37℃ for 10 min. Added 100 µL termination solution to each well and absorbance was measured at 450 nm with enzyme micro-plate reader.

2.7 Quantitative real-time PCR

RNA was extracted from gastrocnemius muscle, subcutaneous fat, visceral fat, and brown adipose tissue. Quantitative real-time PCR was performed after reverse transcription. Primer design is as follows (Jinweizhi Biotechnology, China): 5′-GGATGATATGACGCTGTGGC-3′ (forward) and 5′-ACAGGAGACAGAAACCCCAG-3′ (reverse) for SIRT1; 5′-CGAGCATCTTCTAGCCCTGA-3′ (forward) and 5′-TCCAGGAAGAGAGGAGGAGG-3′ (reverse) for PINK1; 5′-TCAAGAAGACCACCAAGCCT-3′ (forward) and 5′-AACCAGTGATCTCCCATGCA-3′ (reverse) for Parkin; 5′-TCAAGATAATCAGACGGCGC-3′ (forward) and 5′-TTGCTGTCCCGAATGTCTCC-3′ (reverse) for LC3; 5′-TCAAGAAGACCACCAAGCCT-3′ (forward) and 5′-AACCAGTGATCTCCCATGCA-3′ (reverse) for Parkin; 5′-TCTCCTGCGACTTCAACA-3′ (forward) and 5′-TGTAGCCGTATTCATTGTCA-3′ (reverse) for GAPDH. The relative expression of target gene (RQ) was calculated by comparing 2−δδCt according to previous study [11].

2.8 Hematoxylin–eosin staining

Paraffin sections were baked at 60℃ for 1 h. Gradient dewaxing is followed by gradient rehydration. The tissue sections were immersed in hematoxylin solution and stained for 10 min. The sections were rinsed with water to remove unbound dyes. The sections were immersed in hydrochloric acid ethanol ultra-rapid differentiation solution for 3 s, and then soaked in PBS for 10 min, repeated three times. The sections were immersed in eosin solution for 5 min and rinsed with water to remove unbound dyes. The sections were dried at 60℃ and sealed with a drop of neutral gum.

2.9 Statistical analysis

All the results were analyzed by the software GraphPad Prism 7.0 and SPSS 16.0, and were presented as the mean  ±  SD. Beyond that, the comparisons among the four groups were performed by one-way ANOVA. P  <  0.05 was considered as statistically significant.

3 Results

3.1 Berberine alleviated sarcopenia through SIRT1/mitochondrial autophagy pathway

To investigate the effect of berberine on suppressing sarcopenia, we constructed sarcopenia model by giving d-galactose (Figure 1a). Long-term exposure to d-galactose decreased the weight of the mouse (Figure 1a). Results showed that berberine treatment increased the body weight and alleviated d-galactose-induced weight loss in mice. Pink1 and Parkin-mediated mitophagy was a common mitochondrial quality control pathway. During mitophagy, Pink1 and Parkin recruited damaged mitochondria and autophagosomes, and then fused with lysosomes to form autolysosomes to degrade mitochondria [12]. Therefore, mitophagy inhibitor was given to verify whether berberine regulated mitophagy to improve sarcopenia. Results showed that the effect of berberine on sarcopenia was inhibited after treatment with mitophagy inhibitor (Figure 1a). Previous studies showed that SIRT1 mediated the activation of mitophagy [13]. Activation of SIRT1/PGC-1 pathway triggered autophagy/mitochondria and attenuated oxidative damage in intestinal epithelial cells [14]. In our study, it was also observed that SIRT inhibitors also suppressed the effects of berberine in the treatment of sarcopenia (Figure 1a).

Figure 1 Identification of berberine as an inducer of SIRT1 mitochondrial autophagy-pathway in sarcopenia. (a) Anti-sarcopenia activity of berberine in sarcopenia model mice. Mice were treated with d-galactose (400 mg/kg orally) by intrabitoneal injection or control (0.9% normal saline) once a day for 60 days. Then, the mice were divided into five groups (blank group, model group, treatment group, SIRT1 inhibition group, and mitochondrial autophagy inhibition group, n  = 5). The treatment group was given berberine (50 mg/kg) by intragastric administration once a day for 30 days. In addition to berberine, SIRT1 inhibition group was also given selisistat (20 mg/kg) by intraperitoneal injection once every 3 days. In addition to berberine, the mitochondria autophagy inhibition group was additionally given U0126-EtOH (10 mg/kg) by intrabitoneal injection once every 3 days. The weight of mice in each group was determined once every 15 days. (b) Quantitative real-time PCR was performed to verify the role of SIRT1/mitophagy signaling pathway in berberine treating sarcopenia. The expression levels of SIRT1 and mitochondria autophagy related molecules (PINK1, Parkin, LC3II/I) in tissues were detected. Representative results were performed from independent experiments (n  = 5), error bars, SD. P values were indicated by a two-tailed unpaired Student’s t-test. **, P < 0.01; ***, P < 0.001; ##, P < 0.01; ###, P < 0.001.
Figure 1

Identification of berberine as an inducer of SIRT1 mitochondrial autophagy-pathway in sarcopenia. (a) Anti-sarcopenia activity of berberine in sarcopenia model mice. Mice were treated with d-galactose (400 mg/kg orally) by intrabitoneal injection or control (0.9% normal saline) once a day for 60 days. Then, the mice were divided into five groups (blank group, model group, treatment group, SIRT1 inhibition group, and mitochondrial autophagy inhibition group, n  = 5). The treatment group was given berberine (50 mg/kg) by intragastric administration once a day for 30 days. In addition to berberine, SIRT1 inhibition group was also given selisistat (20 mg/kg) by intraperitoneal injection once every 3 days. In addition to berberine, the mitochondria autophagy inhibition group was additionally given U0126-EtOH (10 mg/kg) by intrabitoneal injection once every 3 days. The weight of mice in each group was determined once every 15 days. (b) Quantitative real-time PCR was performed to verify the role of SIRT1/mitophagy signaling pathway in berberine treating sarcopenia. The expression levels of SIRT1 and mitochondria autophagy related molecules (PINK1, Parkin, LC3II/I) in tissues were detected. Representative results were performed from independent experiments (n  = 5), error bars, SD. P values were indicated by a two-tailed unpaired Student’s t-test. **, P < 0.01; ***, P < 0.001; ##, P < 0.01; ###, P < 0.001.

In addition, we further detected the SIRT1/mitophagy signaling pathway in gastrocnemius muscle, subcutaneous fat, visceral fat, and brown adipose tissue. The results showed that SIRT1/mitophagy signaling pathway was inhibited by d-galactose, which indicated that sarcopenia decreased the activity of SIRT1/mitophagy signaling pathway. However, after berberine treatment, SIRT1/mitophagy signaling pathway was activated (Figure 1b). These results suggested that berberine ameliorates sarcopenia through SIRT1/mitophagy pathway.

3.2 Berberine alleviated the loss of muscle tissue in sarcopenia mice

Loss of muscle tissue is the main character of sarcopenia [4], which was also found in d-galactose-treated mice in our study. Berberine significantly increased muscle tissue in d-galactose-treated mice. Mechanically, berberine alleviated muscle tissue loss in sarcopenia via SIRT1/mitophagy pathway. The effect of berberine on the increase of muscle tissue was reversed by SIRT1 and mitophagy inhibitor (Figure 2).

Figure 2 Muscle tissue significantly increased after treatment with berberine. Gastrocnemius tissue was observed by HE staining. Scale bar, 10 µm. Representative results were performed from independent experiments (n  = 5).
Figure 2

Muscle tissue significantly increased after treatment with berberine. Gastrocnemius tissue was observed by HE staining. Scale bar, 10 µm. Representative results were performed from independent experiments (n  = 5).

3.3 Berberine improved metabolic disorders associated with sarcopenia

As an important target of insulin, skeletal muscle was responsible for most glucose metabolism in the body. Loss of skeletal muscle may produce IR, which leads to a large number of systemic inflammation and metabolic disorders [15]. In our study, metabolism was altered in mice treated with d-galactose, among which blood glucose, insulin, triglycerides, triglycerides, cholesterol, LDL cholesterol, HDL cholesterol, free fatty acids, and C-reactive protein were significantly up-regulated. Notably, the metabolism of mice tended to be the same as the control group after treatment with berberine. To further investigate the mechanism of how berberine regulated metabolic disorders in sarcopenia, blood biochemical index was detected after treatment of SIRT1 and mitochondrial autophagy inhibitors, while the effect of berberine on regulating metabolic disorders was inhibited by SIRT1 and mitochondrial autophagy inhibitors (Figure 3). In conclusion, berberine regulated sarcopenia related metabolic disorders, and its implied mechanism was activation of SIRT1/mitochondrial autophagy pathway.

Figure 3 Effect of regulating metabolic disorders in sarcopenia of berberine was observed by blood biochemical index detection. Representative results were performed from independent experiments (n  = 5), error bars, SD. P values were indicated by a two-tailed unpaired Student’s t-test. ***, P < 0.001; ##, P < 0.01; ###, P < 0.001.
Figure 3

Effect of regulating metabolic disorders in sarcopenia of berberine was observed by blood biochemical index detection. Representative results were performed from independent experiments (n  = 5), error bars, SD. P values were indicated by a two-tailed unpaired Student’s t-test. ***, P < 0.001; ##, P < 0.01; ###, P < 0.001.

3.4 Berberine reduced the expression of inflammatory factors in sarcopenia mice

Our previous results revealed that the metabolic disorders of sarcopenia were decreased by berberine. However, whether berberine influenced the systemic inflammation of sarcopenia is unclear. Since berberine ameliorated tissue inflammation by up-regulating GLUT4 expression and increasing skeletal muscle glucose uptake, and was associated with an increase in skeletal muscle fiber number [16], we tested the possibility that berberine ameliorated tissue inflammation via SIRT1/mitochondrial autophagy pathway. The ELISA assay demonstrated that berberine down-regulated the expression of TNF-α and IL-6, as well as elevated the expression of IL-4 and IL-10. Moreover, treatment to SIRT1 and mitochondrial autophagy inhibitors rescued the effect of berberine reducing the expression of inflammatory factors (Figure 4). These results suggested that berberine suppressed systemic inflammation of sarcopenia through SIRT1/mitochondrial autophagy pathway.

Figure 4 Berberine reduced the expression of inflammatory factors in sarcopenia mice. The levels of inflammatory factors (TNF-α, IL-6, IL-4, and IL-10) in tissues were detected by ELISA kit. Representative results were performed from independent experiments (n  = 5), error bars, SD. P values were indicated by a two-tailed unpaired Student’s t-test. ***, P < 0.001; ##, P < 0.01; ###, P < 0.001.
Figure 4

Berberine reduced the expression of inflammatory factors in sarcopenia mice. The levels of inflammatory factors (TNF-α, IL-6, IL-4, and IL-10) in tissues were detected by ELISA kit. Representative results were performed from independent experiments (n  = 5), error bars, SD. P values were indicated by a two-tailed unpaired Student’s t-test. ***, P < 0.001; ##, P < 0.01; ###, P < 0.001.

3.5 Berberine exhibits significant effect on suppressing sarcopenia IR

Recent study revealed that sarcopenia increases the risk of type 2 diabetes [6]. In addition, many symptoms of metabolic syndrome such as obesity, hyperglycemia, and abnormal lipid metabolism are associated with sarcopenia [15]. We observed that d-galactose decreased the GTT and ITT of sarcopenia model mouse, while treatment with berberine increased the GTT and ITT of sarcopenia model mouse (Figure 5). To confirm this effect, the GTT and ITT of sarcopenia model mouse treated with berberine were determined after treatment to SIRT1 and mitochondrial autophagy inhibitors. Taken together, Berberine relieved IR in sarcopenia, and the relief of IR in sarcopenia by berberine depends on SIRT1/mitochondrial autophagy pathway.

Figure 5 Berberine exhibits significant effect on suppressing sarcopenia IR. The levels of GTT and the ITT were measured by a glucose analyzer at 4, 8, 16, and 20 weeks, respectively. Representative results were performed from independent experiments (n  = 5), error bars, SD. P values were indicated by a two-tailed unpaired Student’s t-test. ***, P < 0.001; ##, P < 0.01; ###, P < 0.001.
Figure 5

Berberine exhibits significant effect on suppressing sarcopenia IR. The levels of GTT and the ITT were measured by a glucose analyzer at 4, 8, 16, and 20 weeks, respectively. Representative results were performed from independent experiments (n  = 5), error bars, SD. P values were indicated by a two-tailed unpaired Student’s t-test. ***, P < 0.001; ##, P < 0.01; ###, P < 0.001.

4 Discussion

In this study, we identified berberine as a novel inducer of mitophagy, exhibiting a significant effect on sarcopenia IR. Berberine increases the SITRT1 activity and accelerates mitophagy by PINK1/Parkin pathway. We also show that berberine ameliorates sarcopenia IR mainly by inducing mitophagy. Thus, our results reveal the mechanism under the effect of berberine on sarcopenia IR via PINK1/Parkin-inducing mitophagy, which provides a new paradigm to develop promising therapeutic strategies for sarcopenia IR. It was revealed that berberine ameliorated IR in sarcopenia. The implied mechanism was through up-regulating the SIRT1/mitochondrial autophagy pathway.

Multiple studies have noted that sarcopenia increases the risk of type 2 diabetes [17]. Sarcopenia IR is harmful to the physical and mental health of patients, but the existing clinical prevention and treatment strategies are limited. In recent years, traditional Chinese medicine and its extracts have broad development and application value due to their advantages of low price, easy access to materials, and remarkable effects [18]. Berberine shows significant effect on improving insulin sensitivity and metabolic disorders [19]. Berberine also showed critical role in regulating abnormal bone metabolism [20]. Mechanically, berberine regulates skeletal muscle metabolism through various ways. For example, the metabolism of skeletal muscle cells is regulated through AMPK/SIRT1 and PCG-1α pathways [20]. Another study has shown that berberine suppresses skeletal muscle IR by down-regulating TLR4/IKKβ/NF-κB and PPARα signaling [21]. Therefore, berberine plays an important role in skeletal muscle metabolism and insulin sensitivity. It was also observed in our study that berberine alleviates the symptoms of IR in sarcopenia. However, the mechanism of berberine in ameliorating IR in sarcopenia is still unclear.

In view of this, this study identified a strategy for treating IR in sarcopenia through berberine. Preliminary experiment confirmed that the expression of SIRT1 was significantly up-regulated in skeletal muscle and adipose tissue of mice after the treatment of berberine. SIRT1 is a niacin amine adenine dinucleotide (NAD+) dependent histone deacetylase, which participates in physiological activities such as cell aging, apoptosis, and differentiation [22]. Previous studies have found that SIRT1 in vascular endothelial cells has antioxidant stress effects. Notably, berberine in adipose tissue inhibits tissue inflammation and insulin sensitivity by up-regulating SIRT1 signal [23,24]. In addition, berberine plays a protective role in brain trauma by regulating SIRT1 signal [25]. Interestingly, our results showed that berberine up-regulated the expression of SIRT, and SIRT inhibitors inhibited the effect of berberine, suggesting that berberine mainly inhibits sarcopenia by regulating SIRT1. According to the above information, the protective effect of berberine depends on SIRT1 signal. However, the downstream molecular mechanism of SIRT1 still needs to be further explored.

It was aware of that sarcopenia and insulin resistance were related to mitochondria function mitochondria [26]. Abnormal mitochondrial function results in insufficient energy supply and leads to sarcopenia and IR. Therefore, maintaining mitochondrial homeostasis represents a promising strategy for IR in sarcopenia. Mitophagy is an evolutionally conserved cellular process to clear dysfunctional or redundant mitochondria, thus fine-tuning mitochondrial number and maintaining energy metabolism [27,28]. Mitochondrial autophagy mediated by PINK1 and Parkin is a common mitochondrial quality control pathway [12,29]. Meanwhile, SIRT1 mediates the activation of mitochondrial autophagy [13]. SIRT1/PGC-1 pathway activates autophagy/mitochondria and weakens oxidative damage in intestinal epithelial cells [30]. MiR-34a/SIRT1 signaling protects cochlear hair cells from oxidative stress and delays age-related hearing loss by regulating mitochondrial autophagy and mitochondrial biogenesis [31]. At present, the role of mitochondrial autophagy in sarcopenia has been preliminarily confirmed [32]. There is also a certain correlation between mitochondrial autophagy and IR [33]. Results of our study also confirmed that after treatment of berberine in IR mice with sarcopenia, the expression level of mitochondrial autophagy related molecules (PINK1 and Parkin) was significantly up-regulated. Meanwhile, SIRT1-mediated mitochondrial autophagy activation in sarcopenia IR is the main mechanism by which berberine ameliorates IR in sarcopenia, and that mitochondrial autophagy may play an important role in IR in sarcopenia.

In summary, our study establishes proof-of-concept to distinct the effect of berberine in sarcopenia IR, and provides strong evidence to support the hypothesis that berberine-induced SIRT1 triggers mitochondrial autophagy pathway and suppresses IR in sarcopenia. Understanding the precise role of berberine in treating sarcopenia IR and the regulation of SIRT1/mitochondrial autophagy pathway will advance our knowledge of sarcopenia pathogenesis.

# Contributed equally.

tel: +86-021-64041990

  1. Funding information: Guiding project of Xiamen Science and Technology Bureau (KZXD202113/3502Z20214ZD1073).

  2. Author contributions: X.J.S. and F.Q.Y. designed the experiments. X.J.S., F.Q.Y., and Y.H. performed the experiments. Y.H., Y.Y., and L.S. collected and analyzed the data. Y.Y. and L.S. drafted 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 from the corresponding author on reasonable request.

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Received: 2023-02-15
Revised: 2023-05-04
Accepted: 2023-05-31
Published Online: 2023-07-17

© 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-2022-0648
Keywords for this article
berberine; sarcopenia; insulin resistance; SIRT1-mediated mitophagy
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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  7. Neutrophilia with subclinical Cushing’s disease: A case report and literature review
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  10. Novel CPLANE1 c.8948dupT (p.P2984Tfs*7) variant in a child patient with Joubert syndrome
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  13. High glucose and high lipid induced mitochondrial dysfunction in JEG-3 cells through oxidative stress
  14. Pharmacological inhibition of the ubiquitin-specific protease 8 effectively suppresses glioblastoma cell growth
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  19. Long noncoding RNA ACART knockdown decreases 3T3-L1 preadipocyte proliferation and differentiation
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  28. Metabolomic analysis-identified 2-hydroxybutyric acid might be a key metabolite of severe preeclampsia
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  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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