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The role of rapamycin in the PINK1/Parkin signaling pathway in mitophagy in podocytes

  • Shengyou Yu , Weixue Zhu and Li Yu EMAIL logo
Published/Copyright: September 9, 2024
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Open Life Sciences
From the journal Open Life Sciences Volume 19 Issue 1

Abstract

This study aimed to clarify the role of rapamycin in the PINK1/Parkin signaling pathway in mitophagy in podocytes and the role of voltage-dependent anion channel 1 (VDAC1) in the PINK1/Parkin signaling pathway in mouse glomerular podocytes. For this purpose, podocytes were cultured with rapamycin and observed using microscopy. The apoptosis rate of podocytes was detected by flow cytometry. Changes in the mitochondrial membrane potential were measured. The autophagy-related proteins VDAC1, PINK1, Parkin, and LC3 were detected, and mitochondrial autophagosomes were observed via transmission electron microscopy. In the present study, we demonstrated that the number of podocytes treated with rapamycin was significantly reduced. Compared with those in the control group, the apoptosis rate of podocytes and the degree of mitochondrial membrane potential depolarization were significantly higher. We also found the expression levels of VDAC1, PINK1, Parkin, and LC3 were significantly increased. In the rapamycin-treated group, the numbers of swollen mitochondria and mitochondrial autophagosomes were significantly higher. Finally, we showed that rapamycin can upregulate the expression of VDAC1, PINK1, Parkin, and LC3 in glomerular podocytes, which is correlated with mitophagy. VDAC1 is involved in mitophagy and is related to the PINK1/Parkin signaling pathway, serving as an indicator of mitophagy in podocytes.

Keywords: podocyte; rapamycin; VDAC1; mitophagy; signaling pathway

1 Introduction

Inhibitors of the mammalian target of rapamycin (MTOR) belong to a family of drugs with potent immunosuppressive, antiangiogenic, and antiproliferative properties. Rapamycin was originally proposed as an immunosuppressant to prevent rejection of solid organ transplants. Despite its potential advantages in the transplant setting, evidence that sirolimus causes de novo or worsening proteinuria is unequivocal. In one study, disruption of the autophagic pathway may play a role in the pathogenesis of proteinuria in patients treated with MTOR inhibitors, but the mechanism by which this occurs is unknown [1]. The mTOR inhibitor rapamycin can reduce gene transcription and translation, leading to the activation of apoptosis signaling pathways. As a specific mTOR signaling pathway inhibitor, it can activate autophagy and mitophagy in damaged cells and mitochondria [2,3]. Mitophagy, the selective degradation of damaged and dysfunctional mitochondria via autophagy, is an important mechanism of mitochondrial quality control [4]. Mitophagy is the main pathway for the degradation of mitochondria [5,6]. It has been established that the specific mechanisms of mitophagy are primarily regulated by PINK1 (PTEN Induced Putative Kinase 1) and Parkin signaling pathway, and PINK1/Parkin-mediated mitophagy is one of the classical mitophagy pathways [7]. The PINK1/Parkin-mediated pathway involves protein phosphorylation and ubiquitination. VDAC1 is a mitochondrial outer membrane protein that forms a hydrophilic voltage-gated channel on the mitochondrial outer membrane that regulates the exchange of ions and small metabolites in and out of the mitochondria, forming a common pathway for exchanging metabolites between mitochondria and the cytoplasm. The common pathway plays a crucial role in the regulation of mitochondrial substances and energy functions [8]. VDAC1 is mainly involved in the ubiquitination process of the PINK1/Parkin signaling pathway and plays an integral role in mitophagy [9]. Therefore, rapamycin is essential for elucidating mTOR-dependent signaling events and their role in metabolism and disease; the use of this immunosuppressing drug for inhibiting the PINK1/Parkin signaling pathway pathway may serve as a new basis for the treatment of podocyte injury in renal disease. However, the effect of rapamycin on mitophagy in podocytes and VDAC1 is still unclear. In this study, we investigated the effect of rapamycin on normal podocytes, the effects of rapamycin on mitophagy in podocytes, and the effect of VDAC1 on the PINK1/Parkin signaling pathway in podocytes.

2 Materials and methods

2.1 Podocyte culture

In vitro immortalized mouse podocyte cell lines (MPC5) were authorized by the US Mundel Professor, Professor of Pediatrics, Peking University First Hospital, Ding Jie donation. Before the experiment, podocytes were recovered, collected, and cultured in RPMI 1640 medium (Gibco; Thermo Fisher Scientific, Inc.) containing antibiotics (1% penicillin and streptomycin) and 10% FBS (Gibco; Thermo Fisher Scientific, Inc.) at 33°C in a humidified 5% CO2/95% air atmosphere. Recombinant mouse γ-interferon (10 U/ml, BINDER GmbH) was used to induce podocyte proliferation. After podocyte confluence reached 80–90%, 0.25% trypsin/0.02% EDTA (Gibco; Thermo Fisher Scientific, Inc.) was added. Subsequently, the podocytes were moved to a 37°C environment for differentiation and maturation for 10–14 days. The differentiated and matured podocytes were then seeded into six-well plates (Corning), and after the cells reached 60–70% confluence, RPMI 1640 alone was used to starve the podocytes for 12 h to synchronize the proliferation of the cells, before the experimental grouping was performed.

Podocytes were treated with RPMI 1640 (Gibco, USA) supplemented with rapamycin (Med Chem Express, USA). Microscopy was used to observe the morphological changes in podocytes treated with different concentrations of rapamycin. The control group and the rapamycin group were designed as follows: control group: cells were treated with RPMI 1640 (Gibco, USA) nutrient solution containing 0.02% DMSO (Sigma, USA); rapamycin group: cells were treated with RPMI 1640 (Gibco, USA) nutrient solution containing 100 nmol/l rapamycin and 0.02% DMSO (Sigma, USA).

2.2 Flow cytometry analysis

The percentage of apoptotic podocytes was determined by Annexin V-FITC/propidium iodide (PI; Key GEN Biotech) dual staining. Changes in the mitochondrial membrane potential were detected with a JC-1 mitochondrial membrane potential detection kit (Key GEN Biotech). When the mitochondrial membrane potential is relatively normal, JC-1 gathers in the matrix of the mitochondria to form red-fluorescencent aggregates. When the mitochondrial membrane potential is decreased, JC-1 cannot accumulate in the matrix of the mitochondria and exists as green-fluorescencent monomer. JC-1 staining working solution was prepared according to the instructions. After 24 h, the culture medium was replaced by 1 mL fresh culture medium and 1 mL JC-1 staining working solution. The podocytes were further incubated at 37°C and JC-1 staining buffer was prepared according to the instructions during the incubation period. The JC-1 staining working solution was discarded, and the podocytes were washed twice with JC-1 staining buffer. After washing with phosphate-buffered saline (PBS) twice, the red fluorescent signals were excited to 530 nm and detected at 630 nm; the green fluorescence was excited to 488 nm and detected at 530 nm. Image J software was used to quantify the red and green fluorescence, and the ratios of red/green were calculated. Three independent experiments were carried out for validation.

2.3 RT-qPCR analysis

Total RNA was extracted according to the instructions of the RNA gents® Total RNA Isolation System (Promega Corporation). Then, the purity and integrity of the total RNA was detected. Briefly, the purity of the RNA was detected by measuring the OD 260/OD 280 ratio with a nucleic acid protein analyzer (Bio Photometer Plus; Shanghai Musen Biotechnology Co., Ltd.). The integrity of the total RNA was assessed by 1% agarose gel electrophoresis, which was performed at 80 V for 20 min, and the total RNA bands were observed with a gel imaging system (Zhuhai Hema Medical Instrument Co., Ltd.). Thereafter, the extracted RNA was transcribed into cDNA using PrimeScript™ RT Master Mix Kit (Takara Bio, Inc.) according to the manufacturer’s protocol. SYBR Premix Ex Taq™ II (Takara Bio, Inc.) was used for qPCR, and reactions were performed using a LightCycler480 Real-Time PCR System (Roche Diagnostics) with the following protocol:predenaturation at 95°C for 5 min and denaturation at 95°C for 10 s and annealing at 60°C for 20 s for a total of 40 cycles. The VDACs1, PINK1, Parkin, and LC3 genes were quantitatively amplified with primers as described previously using the SYBR Green qPCR method [10,11,12,13]. The quantization of mRNA was calculated according to the attached software (Bio-Rad, USA) and normalized to the quality of β-actin.

2.4 Western blot analysis

The podocytes in each group were rinsed twice with PBS. RIPA cell lysate (Thermo, USA) was used for splitting decomposition. A BCA protein assay kit (Thermo, USA) was used to measure the total protein concentration of the podocytes. SDS–PAGE was performed in our laboratory according to previously described methods [14]. Afterward, the membranes were blocked with 5% (v/v) BSA for 1 h at room temperature. The primary antibodies for VDAC1, PINK1, Parkin, and LC3-B (Abcam, UK) were incubated at 4°C overnight. A Tanon 5200 (Tianneng Group) chemiluminescence imaging system was used for band exposure. The images were analyzed using ImageJ image analysis software.

2.5 Transmission electronic microscopy

Podocytes from each group were collected, fixed with glutaraldehyde and 1% osmium tetroxide for 15–30 min at 4°C, and dehydrated at room temperature with gradient concentrations of acetone. The dehydrated samples were embedded in pure acetone‑EPON812 embedding medium for 2 h at room temperature, baked to solidify, sectioned (1 µm), stained dropwise with sodium acetate for 30 min at room temperature, and washed with PBS. Samples were imaged using a transmission electron microscope (Libra 120 microscope; Carl Zeiss AG) to observe autophagosomes.

2.6 Statistical analysis

All the data were statistically analyzed with SPSS 20.0 statistical software (IBM Corp., Armonk, NY, USA). Count data are expressed as rates (%), and the x 2 test was used; measurement data are expressed as x ¯ ± S, and comparisons between groups were made using one-way analysis of variance. p < 0.05 indicated that the differences were statistically significant.

3 Results

3.1 Morphological changes of podocytes

Figure 1 shows that there was no obvious abnormality in the morphology of the podocytes treated with 50 nmol/l rapamycin compared with those in the control group. Podocytes treated with 100 and 150 nmol/l rapamycin showed a significant reduction in size, and the podocyte process retracted or disappeared. The connections among cells were loose. Consistent with other studies [11], the rapamycin group in the following experiment was constructed with a concentration of 100 nmol/l (Figure 1).

Figure 1 Changes in podocyte morphology in the control group and groups treated with different concentrations of rapamycin (inverted microscope ×200). The red arrows indicate the morphology of the podocytes.
Figure 1

Changes in podocyte morphology in the control group and groups treated with different concentrations of rapamycin (inverted microscope ×200). The red arrows indicate the morphology of the podocytes.

3.2 Changes in podocyte apoptosis rate

In the control group, the apoptosis rate of podocytes at 12 and 24 h was low, and while the apoptosis rate slightly increased at 48 h, it was not significantly different (p > 0.05). After 12, 24, and 48 h of rapamycin treatment, the apoptosis rate of podocytes was significantly increased at 12 h compared to the control group (Figure 2).

Figure 2 (a) The apoptosis rates of podocytes detected by flow cytometry in the control group and rapamycin group at different time points. Propidium iodide (PI) and an Annexin V apoptosis kit with double staining were used to detect the apoptosis rate, which was analyzed by flow cytometry, in which the x-axis was Annexin V(+) and the y-axis was PI (+), Q1 was PI (+), Annexin (–V), Q2 was PI (+), Annexin (+V), late apoptotic or dead cells, Q3 was PI (–), Annexin V (+), early apoptotic cells, Q4 was Annexin V (−), PI (–), and normal living cells. (b) Bar chart of the podocyte apoptosis rate detected by flow cytometry in the control group and rapamycin group. *p < 0.05 versus the control group.
Figure 2

(a) The apoptosis rates of podocytes detected by flow cytometry in the control group and rapamycin group at different time points. Propidium iodide (PI) and an Annexin V apoptosis kit with double staining were used to detect the apoptosis rate, which was analyzed by flow cytometry, in which the x-axis was Annexin V(+) and the y-axis was PI (+), Q1 was PI (+), Annexin (–V), Q2 was PI (+), Annexin (+V), late apoptotic or dead cells, Q3 was PI (–), Annexin V (+), early apoptotic cells, Q4 was Annexin V (−), PI (–), and normal living cells. (b) Bar chart of the podocyte apoptosis rate detected by flow cytometry in the control group and rapamycin group. *p < 0.05 versus the control group.

3.3 Changes in podocyte mitochondrial membrane potential

In the control group, there were fewer mitochondrial JC-1 monomers at 12 h, and the number of monomers gradually increased with time, but the difference was not significant (p > 0.05). Compared with that in the control group, the monomer concentration in the rapamycin group increased at each time point, as shown in Figure 3. The number of monomers increased, indicating a greater degree of mitochondrial depolarization (p < 0.05; Figure 3).

Figure 3 (a) Changes in mitochondrial membrane potential detected by flow cytometry in the control group and rapamycin group. (b) Bar chart of mitochondrial membrane potential detected by flow cytometry in the control group and rapamycin group. *p < 0.05 versus the control group.
Figure 3

(a) Changes in mitochondrial membrane potential detected by flow cytometry in the control group and rapamycin group. (b) Bar chart of mitochondrial membrane potential detected by flow cytometry in the control group and rapamycin group. *p < 0.05 versus the control group.

3.4 mRNA expression levels of VDAC1, PINK1, Parkin, and LC3 in podocytes

In the control group, the mRNA expression of the mitophagy-associated genes VDAC1, PINK1, and Parkin and the autophagy-associated gene LC3 at 12 h was low, and the expression level did not change significantly with time (p > 0.05). Compared with those in the control group, the mRNA expression of VDAC1, PINK1, Parkin, and LC3-B in the rapamycin group significantly increased at each time point, and the expression gradually increased with time (p < 0.05; Figure 4).

Figure 4 Changes in the mRNA expression of VDAC1, PINK1, Parkin, and LC3-B in the control group and rapamycin group. (a) VDAC1 mRNA expression, (b) the mRNA expression of PINK1, (c) the mRNA expression of Parkin, and (d) the mRNA expression of LC3-B. *p < 0.05 versus the control group.
Figure 4

Changes in the mRNA expression of VDAC1, PINK1, Parkin, and LC3-B in the control group and rapamycin group. (a) VDAC1 mRNA expression, (b) the mRNA expression of PINK1, (c) the mRNA expression of Parkin, and (d) the mRNA expression of LC3-B. *p < 0.05 versus the control group.

3.5 Protein expression levels of VDAC1, PINK1, Parkin and LC3B in podocytes

In the control group, the expression of the mitophagy-related proteins VDAC1, PINK1, and Parkin and the autophagy-related protein LC3-B at 12 h was low, and their expression gradually increased with time, but there was no significant difference (p > 0.05). Compared with those in the control group, the expression levels of the proteins PINK1, Parkin, VDAC1, and LC3-B increased at each time point, and showed significant differences (p < 0.05; Figure 5).

Figure 5 (a) Western blot bands of VDAC1, Pink1, Parkin, and LC3-B in the control group and rapamycin group at different time points. 1, 2, and 3 indicate the control group at 12, 24, and 48 h, respectively. 4, 5, and 6 indicate the rapamycin groups at 12, 24, and 48 h, respectively. Bar chart of the protein expression of VDAC1, PINK1, Parkin, and LC3-B in the control group and rapamycin group. (b) VDAC1 protein expression, (c) expression of the PINK1 protein, (d) Parkin protein expression, and (e) expression of the LC3-B protein. *p < 0.05 versus the control group.
Figure 5

(a) Western blot bands of VDAC1, Pink1, Parkin, and LC3-B in the control group and rapamycin group at different time points. 1, 2, and 3 indicate the control group at 12, 24, and 48 h, respectively. 4, 5, and 6 indicate the rapamycin groups at 12, 24, and 48 h, respectively. Bar chart of the protein expression of VDAC1, PINK1, Parkin, and LC3-B in the control group and rapamycin group. (b) VDAC1 protein expression, (c) expression of the PINK1 protein, (d) Parkin protein expression, and (e) expression of the LC3-B protein. *p < 0.05 versus the control group.

3.6 Mitochondrial morphology and autophagosomes

In the control group, most of the mitochondria had clear structures with complete mitochondrial cristae. Several swollen mitochondria could be occasionally observed. No isolated bilayer-encapsulated mitochondrial autophagosomes were observed in multiple visual fields. At 48 h, the density of the podocytes was reduced, the volume was slightly reduced, and more lysosomal structures and swollen mitochondria were observed in the cytoplasm. In the rapamycin group, more swollen mitochondria were observed at various time points than in the control group, and as time progressed, the number of swollen mitochondria increased, some of them became vacuolated, and there were more lysosomes and lysosome-encapsulated autophagosomes (Figure 6).

Figure 6 Changes in mitochondrial autophagosomes and mitochondria in the different groups were observed by transmission electron microscopy. (a)–(c) (×13,500), (d)–(f) (×26,500): the control group at 12, 24, and 48 h, respectively. (g) (×13,500), (j) (×26,500): rapamycin group at 12 h. (h)–(i) (X13500), (k)–(l) (×26,500): rapamycin group at 24 h. (m)–(n) (×13,500), (o)–(p) (×26,500): rapamycin group at 48 h. The blue arrows indicate swollen mitochondria, and the red arrows indicate autophagosomes.
Figure 6

Changes in mitochondrial autophagosomes and mitochondria in the different groups were observed by transmission electron microscopy. (a)–(c) (×13,500), (d)–(f) (×26,500): the control group at 12, 24, and 48 h, respectively. (g) (×13,500), (j) (×26,500): rapamycin group at 12 h. (h)–(i) (X13500), (k)–(l) (×26,500): rapamycin group at 24 h. (m)–(n) (×13,500), (o)–(p) (×26,500): rapamycin group at 48 h. The blue arrows indicate swollen mitochondria, and the red arrows indicate autophagosomes.

4 Discussion

Mitochondria play a critical role in maintaining podocytic metabolic homeostasis. It has been demonstrated that Mitophagy is an important protective mechanism for eliminating damaged mitochondria and maintaining a healthy mitochondrial pool. Accumulating evidence has demonstrated that mitochondrial fragmentation is a prerequisite for the activation of mitophagy, which allows for the segregation of damaged mitochondria via the fission process and subsequent being engulfed by autophagosomes [15]. Mitophagy is a highly selective form of autophagy that eliminates dysfunctional or over-expressed mitochondria through the autophagosome-lysosomal system; this process is essentially giant autophagy [16].

At present, the most studied pathway for mediating mitochondrial autophagy is the PINK1/Parkin pathway, which is also the most recognized signaling pathway in mitophagy. Mitochondrial depolarization prevents the import of PINK1 to the inner membrane, leading to the accumulation of full-length PINK1 on the mitochondrial surface which recruits Parkin from the cytosol to damaged mitochondria. Following the recruitment to mitochondria, Parkin ubiquitinates various substrates to induce and promote the autophagic removal of mitochondria [17]. Under conditions of gene mutation, oxidative stress, or other factors, the mitochondrial permeability transition pore opens, and membrane potential (Δψm) depolarization occurs [18]. PINK1 transport is blocked, and parkin is induced to move to the damaged mitochondrial outer membrane so that Parkin is phosphorylated and activated; subsequently, VDAC1 and other related proteins on the mitochondrial outer membrane are ubiquitinated, leading to the accumulation of the autophagy receptor p62. Then, damaged mitochondria are formed into autophagosomes through LC3 binding and enter lysosomes for degradation, eventually allowing the damaged mitochondria to be cleared by autophagy [19,20]. The link between PINK1, Parkin, and mitophagy has been studied in degenerative diseases, cardiovascular diseases, and tumors [21,22,23].

Voltage-dependent anion channels (VDACs) are also known as mitochondrial outer membrane proteins and play a crucial role in the regulation of mitochondrial substances and energy functions [24]. VDAC1 interacts with the bcl-xl family of antiapoptotic proteins, inhibits the release of apoptotic proteins, and participates in mitochondria-mediated apoptosis. Changes in the expression of VDAC1 affect cell material, energy metabolism, and cell survival; silencing VDAC1 expression by siRNA can reduce intracellular ATP levels and cell growth [25], while VDAC1 overexpression can induce cell death [26]. In addition, VDAC1 plays an integral role in PINK1/Parkin-mediated mitophagy [27,28,29]. It is a mitochondrial target of polyubiquitination and mitophagy mediated by Parkin, and VDAC1 is the target of lysine polyubiquitination mediated by Parkin during depolarization of mitochondria. Silencing the VDAC1 gene can significantly reduce Parkin migration from the cytoplasm to damaged mitochondria and significantly inhibit the elimination of mitochondria.

mTOR as a major negative regulator of mitophagy has been paid increasing attention. RAP is a macrolide immunosuppressive drug that can specifically bind to the mammalian target of rapamycin (mTOR) in the P13K/AKT/mTOR signaling pathway, inhibiting the protein kinase activity of mTOR, regulating cell metabolism, and inducing autophagy to regulate various cellular responses [30]. Under physiological conditions, the dynamic equilibrium of podocytes usually also relies on increased autophagy activity and very low mTOR activity. When the balance between mTOR activity and autophagy activity is disrupted, podocytes are damaged [31,32,33]. Additionally, rapamycin can cause the accumulation of PINK1 and the recruitment of Parkin to impaired mitochondria, followed by ubiquitination of the mitochondrial outer membrane protein VDAC1, activation of mitochondrial autophagy, and elimination of dysfunctional mitochondria [34]. Studies have shown that after cells are treated with rapamycin, the expression of cytochrome c and the activity of caspase-3 are greatly increased, so rapamycin can inhibit the PI3K/Akt signaling pathway and induce mitochondria-mediated apoptosis. In addition, abnormal mTOR activation in podocytes involved a variety of molecular reactions, including the mislocalization of slit diaphragm proteins in podocytes [35,36,37]. This was consistent with our study that the abnormal activation of mTOR played a key role in podocyte injury and proteinuria.

In the present study, we found that rapamycin can cause depolarization of the mitochondrial membrane potential of podocytes. The expression of VDAC1 increased, and the rate of apoptosis increased, which may be related to the fact that rapamycin can decrease the mitochondrial membrane potential. This led to the opening of mitochondrial permeability transition pores, promoted enhanced expression of cytochrome C, increased caspase-3 activity, and induced apoptosis of podocytes. In addition, rapamycin, an mTOR inhibitor, can significantly inhibit PI3K/Akt/mTOR signaling and activate caspase activity and cytochrome C release, further accelerating cell apoptosis [16,29]. In addition, we also found that rapamycin can increase the expression of mitophagy-associated proteins such as PINK1, Parkin, and VDAC1. Moreover, many swollen mitochondria, mitochondrial autophagosomes, and autolysosomes can be observed via transmission electron microscopy. We speculated that rapamycin caused podocyte mitochondrial dysfunction, increased Parkin migration from the cytoplasm to damaged mitochondria, enhanced VDAC1 expression, and promoted mitophagy in podocytes. Therefore, VDAC1 can participate in the process of podocyte mitophagy through the PINK1/Parkin signaling pathway. There is low mitophagy in normal cells. When rapamycin acts on podocytes, it can disrupt the original autophagy balance and lead to enhanced mitophagy, which leads to podocyte dysfunction and structural damage. When external stimuli are weak, mitophagy is activated to eliminate a small part of the damaged mitochondria, which protects cells, and excessive autophagy may cause the leakage of cathepsins or other proteolytic enzymes from lysosomes or autolysosomes, leading to cell apoptosis or necrosis.

5 Conclusion

Our findings indicate that enhancing autophagy and mitophagy can eliminate damaged organelles to a certain extent to maintain cell homeostasis, and overactivation may be detrimental to healthy organelles and disrupt cell homeostasis. Rapamycin can increase the protein expression of PINK1, Parkin, and VDAC1 by affecting the mitochondrial membrane potential, which promotes mitophagy mediated by the PINK1/Parkin signaling pathway. An imbalance in mitophagy in podocytes can result in increased cell apoptosis. VDAC1 is involved in mitophagy mediated by the PINK1/Parkin signaling pathway and can be used as an indicator to detect mitophagy in podocytes.

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  1. Funding information: The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article. This study was supported by the fund from Guangzhou Planned Project of Science and Technology (No. 2024A03J1018); The National Key Research and Development Program of China (No. 2022YFC2705100; No. 2022YFC2705103;2022YFC2705104); Guangdong Science and Research Project of Traditional Chinese Medicine Bureau (No. 20222158); GuangDong Medical Science and Research Foundation (No. A2023160).

  2. Author contributions: Y.S.Y. contributed to the study conception and design. Z.W.X. performed cell culture and Western blots. Y.L. analyzed and interpreted the data. All authors contributed to the manuscript revision and approved the submitted version.

  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: 2024-05-18
Revised: 2024-08-05
Accepted: 2024-08-09
Published Online: 2024-09-09

© 2024 the author(s), published by De Gruyter

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

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  208. Retraction
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https://doi.org/10.1515/biol-2022-0958
Keywords for this article
podocyte; rapamycin; VDAC1; mitophagy; signaling pathway
Creative Commons
BY 4.0

Articles in the same Issue

  1. Biomedical Sciences
  2. Constitutive and evoked release of ATP in adult mouse olfactory epithelium
  3. LARP1 knockdown inhibits cultured gastric carcinoma cell cycle progression and metastatic behavior
  4. PEGylated porcine–human recombinant uricase: A novel fusion protein with improved efficacy and safety for the treatment of hyperuricemia and renal complications
  5. Research progress on ocular complications caused by type 2 diabetes mellitus and the function of tears and blepharons
  6. The role and mechanism of esketamine in preventing and treating remifentanil-induced hyperalgesia based on the NMDA receptor–CaMKII pathway
  7. Brucella infection combined with Nocardia infection: A case report and literature review
  8. Detection of serum interleukin-18 level and neutrophil/lymphocyte ratio in patients with antineutrophil cytoplasmic antibody-associated vasculitis and its clinical significance
  9. Ang-1, Ang-2, and Tie2 are diagnostic biomarkers for Henoch-Schönlein purpura and pediatric-onset systemic lupus erythematous
  10. PTTG1 induces pancreatic cancer cell proliferation and promotes aerobic glycolysis by regulating c-myc
  11. Role of serum B-cell-activating factor and interleukin-17 as biomarkers in the classification of interstitial pneumonia with autoimmune features
  12. Effectiveness and safety of a mumps containing vaccine in preventing laboratory-confirmed mumps cases from 2002 to 2017: A meta-analysis
  13. Low levels of sex hormone-binding globulin predict an increased breast cancer risk and its underlying molecular mechanisms
  14. A case of Trousseau syndrome: Screening, detection and complication
  15. Application of the integrated airway humidification device enhances the humidification effect of the rabbit tracheotomy model
  16. Preparation of Cu2+/TA/HAP composite coating with anti-bacterial and osteogenic potential on 3D-printed porous Ti alloy scaffolds for orthopedic applications
  17. Aquaporin-8 promotes human dermal fibroblasts to counteract hydrogen peroxide-induced oxidative damage: A novel target for management of skin aging
  18. Current research and evidence gaps on placental development in iron deficiency anemia
  19. Single-nucleotide polymorphism rs2910829 in PDE4D is related to stroke susceptibility in Chinese populations: The results of a meta-analysis
  20. Pheochromocytoma-induced myocardial infarction: A case report
  21. Kaempferol regulates apoptosis and migration of neural stem cells to attenuate cerebral infarction by O‐GlcNAcylation of β-catenin
  22. Sirtuin 5 regulates acute myeloid leukemia cell viability and apoptosis by succinylation modification of glycine decarboxylase
  23. Apigenin 7-glucoside impedes hypoxia-induced malignant phenotypes of cervical cancer cells in a p16-dependent manner
  24. KAT2A changes the function of endometrial stromal cells via regulating the succinylation of ENO1
  25. Current state of research on copper complexes in the treatment of breast cancer
  26. Exploring antioxidant strategies in the pathogenesis of ALS
  27. Helicobacter pylori causes gastric dysbacteriosis in chronic gastritis patients
  28. IL-33/soluble ST2 axis is associated with radiation-induced cardiac injury
  29. The predictive value of serum NLR, SII, and OPNI for lymph node metastasis in breast cancer patients with internal mammary lymph nodes after thoracoscopic surgery
  30. Carrying SNP rs17506395 (T > G) in TP63 gene and CCR5Δ32 mutation associated with the occurrence of breast cancer in Burkina Faso
  31. P2X7 receptor: A receptor closely linked with sepsis-associated encephalopathy
  32. Probiotics for inflammatory bowel disease: Is there sufficient evidence?
  33. Identification of KDM4C as a gene conferring drug resistance in multiple myeloma
  34. Microbial perspective on the skin–gut axis and atopic dermatitis
  35. Thymosin α1 combined with XELOX improves immune function and reduces serum tumor markers in colorectal cancer patients after radical surgery
  36. Highly specific vaginal microbiome signature for gynecological cancers
  37. Sample size estimation for AQP4-IgG seropositive optic neuritis: Retinal damage detection by optical coherence tomography
  38. The effects of SDF-1 combined application with VEGF on femoral distraction osteogenesis in rats
  39. Fabrication and characterization of gold nanoparticles using alginate: In vitro and in vivo assessment of its administration effects with swimming exercise on diabetic rats
  40. Mitigating digestive disorders: Action mechanisms of Mediterranean herbal active compounds
  41. Distribution of CYP2D6 and CYP2C19 gene polymorphisms in Han and Uygur populations with breast cancer in Xinjiang, China
  42. VSP-2 attenuates secretion of inflammatory cytokines induced by LPS in BV2 cells by mediating the PPARγ/NF-κB signaling pathway
  43. Factors influencing spontaneous hypothermia after emergency trauma and the construction of a predictive model
  44. Long-term administration of morphine specifically alters the level of protein expression in different brain regions and affects the redox state
  45. Application of metagenomic next-generation sequencing technology in the etiological diagnosis of peritoneal dialysis-associated peritonitis
  46. Clinical diagnosis, prevention, and treatment of neurodyspepsia syndrome using intelligent medicine
  47. Case report: Successful bronchoscopic interventional treatment of endobronchial leiomyomas
  48. Preliminary investigation into the genetic etiology of short stature in children through whole exon sequencing of the core family
  49. Cystic adenomyoma of the uterus: Case report and literature review
  50. Mesoporous silica nanoparticles as a drug delivery mechanism
  51. Dynamic changes in autophagy activity in different degrees of pulmonary fibrosis in mice
  52. Vitamin D deficiency and inflammatory markers in type 2 diabetes: Big data insights
  53. Lactate-induced IGF1R protein lactylation promotes proliferation and metabolic reprogramming of lung cancer cells
  54. Meta-analysis on the efficacy of allogeneic hematopoietic stem cell transplantation to treat malignant lymphoma
  55. Mitochondrial DNA drives neuroinflammation through the cGAS-IFN signaling pathway in the spinal cord of neuropathic pain mice
  56. Application value of artificial intelligence algorithm-based magnetic resonance multi-sequence imaging in staging diagnosis of cervical cancer
  57. Embedded monitoring system and teaching of artificial intelligence online drug component recognition
  58. Investigation into the association of FNDC1 and ADAMTS12 gene expression with plumage coloration in Muscovy ducks
  59. Yak meat content in feed and its impact on the growth of rats
  60. A rare case of Richter transformation with breast involvement: A case report and literature review
  61. First report of Nocardia wallacei infection in an immunocompetent patient in Zhejiang province
  62. Rhodococcus equi and Brucella pulmonary mass in immunocompetent: A case report and literature review
  63. Downregulation of RIP3 ameliorates the left ventricular mechanics and function after myocardial infarction via modulating NF-κB/NLRP3 pathway
  64. Evaluation of the role of some non-enzymatic antioxidants among Iraqi patients with non-alcoholic fatty liver disease
  65. The role of Phafin proteins in cell signaling pathways and diseases
  66. Ten-year anemia as initial manifestation of Castleman disease in the abdominal cavity: A case report
  67. Coexistence of hereditary spherocytosis with SPTB P.Trp1150 gene variant and Gilbert syndrome: A case report and literature review
  68. Utilization of convolutional neural networks to analyze microscopic images for high-throughput screening of mesenchymal stem cells
  69. Exploratory evaluation supported by experimental and modeling approaches of Inula viscosa root extract as a potent corrosion inhibitor for mild steel in a 1 M HCl solution
  70. Imaging manifestations of ductal adenoma of the breast: A case report
  71. Gut microbiota and sleep: Interaction mechanisms and therapeutic prospects
  72. Isomangiferin promotes the migration and osteogenic differentiation of rat bone marrow mesenchymal stem cells
  73. Prognostic value and microenvironmental crosstalk of exosome-related signatures in human epidermal growth factor receptor 2 positive breast cancer
  74. Circular RNAs as potential biomarkers for male severe sepsis
  75. Knockdown of Stanniocalcin-1 inhibits growth and glycolysis in oral squamous cell carcinoma cells
  76. The expression and biological role of complement C1s in esophageal squamous cell carcinoma
  77. A novel GNAS mutation in pseudohypoparathyroidism type 1a with articular flexion deformity: A case report
  78. Predictive value of serum magnesium levels for prognosis in patients with non-small cell lung cancer undergoing EGFR-TKI therapy
  79. HSPB1 alleviates acute-on-chronic liver failure via the P53/Bax pathway
  80. IgG4-related disease complicated by PLA2R-associated membranous nephropathy: A case report
  81. Baculovirus-mediated endostatin and angiostatin activation of autophagy through the AMPK/AKT/mTOR pathway inhibits angiogenesis in hepatocellular carcinoma
  82. Metformin mitigates osteoarthritis progression by modulating the PI3K/AKT/mTOR signaling pathway and enhancing chondrocyte autophagy
  83. Evaluation of the activity of antimicrobial peptides against bacterial vaginosis
  84. Atypical presentation of γ/δ mycosis fungoides with an unusual phenotype and SOCS1 mutation
  85. Analysis of the microecological mechanism of diabetic kidney disease based on the theory of “gut–kidney axis”: A systematic review
  86. Omega-3 fatty acids prevent gestational diabetes mellitus via modulation of lipid metabolism
  87. Refractory hypertension complicated with Turner syndrome: A case report
  88. Interaction of ncRNAs and the PI3K/AKT/mTOR pathway: Implications for osteosarcoma
  89. Association of low attenuation area scores with pulmonary function and clinical prognosis in patients with chronic obstructive pulmonary disease
  90. Long non-coding RNAs in bone formation: Key regulators and therapeutic prospects
  91. The deubiquitinating enzyme USP35 regulates the stability of NRF2 protein
  92. Neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio as potential diagnostic markers for rebleeding in patients with esophagogastric variceal bleeding
  93. G protein-coupled receptor 1 participating in the mechanism of mediating gestational diabetes mellitus by phosphorylating the AKT pathway
  94. LL37-mtDNA regulates viability, apoptosis, inflammation, and autophagy in lipopolysaccharide-treated RLE-6TN cells by targeting Hsp90aa1
  95. The analgesic effect of paeoniflorin: A focused review
  96. Chemical composition’s effect on Solanum nigrum Linn.’s antioxidant capacity and erythrocyte protection: Bioactive components and molecular docking analysis
  97. Knockdown of HCK promotes HREC cell viability and inner blood–retinal barrier integrity by regulating the AMPK signaling pathway
  98. The role of rapamycin in the PINK1/Parkin signaling pathway in mitophagy in podocytes
  99. Laryngeal non-Hodgkin lymphoma: Report of four cases and review of the literature
  100. Clinical value of macrogenome next-generation sequencing on infections
  101. Overview of dendritic cells and related pathways in autoimmune uveitis
  102. TAK-242 alleviates diabetic cardiomyopathy via inhibiting pyroptosis and TLR4/CaMKII/NLRP3 pathway
  103. Hypomethylation in promoters of PGC-1α involved in exercise-driven skeletal muscular alterations in old age
  104. Profile and antimicrobial susceptibility patterns of bacteria isolated from effluents of Kolladiba and Debark hospitals
  105. The expression and clinical significance of syncytin-1 in serum exosomes of hepatocellular carcinoma patients
  106. A histomorphometric study to evaluate the therapeutic effects of biosynthesized silver nanoparticles on the kidneys infected with Plasmodium chabaudi
  107. PGRMC1 and PAQR4 are promising molecular targets for a rare subtype of ovarian cancer
  108. Analysis of MDA, SOD, TAOC, MNCV, SNCV, and TSS scores in patients with diabetes peripheral neuropathy
  109. SLIT3 deficiency promotes non-small cell lung cancer progression by modulating UBE2C/WNT signaling
  110. The relationship between TMCO1 and CALR in the pathological characteristics of prostate cancer and its effect on the metastasis of prostate cancer cells
  111. Heterogeneous nuclear ribonucleoprotein K is a potential target for enhancing the chemosensitivity of nasopharyngeal carcinoma
  112. PHB2 alleviates retinal pigment epithelium cell fibrosis by suppressing the AGE–RAGE pathway
  113. Anti-γ-aminobutyric acid-B receptor autoimmune encephalitis with syncope as the initial symptom: Case report and literature review
  114. Comparative analysis of chloroplast genome of Lonicera japonica cv. Damaohua
  115. Human umbilical cord mesenchymal stem cells regulate glutathione metabolism depending on the ERK–Nrf2–HO-1 signal pathway to repair phosphoramide mustard-induced ovarian cancer cells
  116. Electroacupuncture on GB acupoints improves osteoporosis via the estradiol–PI3K–Akt signaling pathway
  117. Renalase protects against podocyte injury by inhibiting oxidative stress and apoptosis in diabetic nephropathy
  118. Review: Dicranostigma leptopodum: A peculiar plant of Papaveraceae
  119. Combination effect of flavonoids attenuates lung cancer cell proliferation by inhibiting the STAT3 and FAK signaling pathway
  120. Renal microangiopathy and immune complex glomerulonephritis induced by anti-tumour agents: A case report
  121. Correlation analysis of AVPR1a and AVPR2 with abnormal water and sodium and potassium metabolism in rats
  122. Gastrointestinal health anti-diarrheal mixture relieves spleen deficiency-induced diarrhea through regulating gut microbiota
  123. Myriad factors and pathways influencing tumor radiotherapy resistance
  124. Exploring the effects of culture conditions on Yapsin (YPS) gene expression in Nakaseomyces glabratus
  125. Screening of prognostic core genes based on cell–cell interaction in the peripheral blood of patients with sepsis
  126. Coagulation factor II thrombin receptor as a promising biomarker in breast cancer management
  127. Ileocecal mucinous carcinoma misdiagnosed as incarcerated hernia: A case report
  128. Methyltransferase like 13 promotes malignant behaviors of bladder cancer cells through targeting PI3K/ATK signaling pathway
  129. The debate between electricity and heat, efficacy and safety of irreversible electroporation and radiofrequency ablation in the treatment of liver cancer: A meta-analysis
  130. ZAG promotes colorectal cancer cell proliferation and epithelial–mesenchymal transition by promoting lipid synthesis
  131. Baicalein inhibits NLRP3 inflammasome activation and mitigates placental inflammation and oxidative stress in gestational diabetes mellitus
  132. Impact of SWCNT-conjugated senna leaf extract on breast cancer cells: A potential apoptotic therapeutic strategy
  133. MFAP5 inhibits the malignant progression of endometrial cancer cells in vitro
  134. Major ozonated autohemotherapy promoted functional recovery following spinal cord injury in adult rats via the inhibition of oxidative stress and inflammation
  135. Axodendritic targeting of TAU and MAP2 and microtubule polarization in iPSC-derived versus SH-SY5Y-derived human neurons
  136. Differential expression of phosphoinositide 3-kinase/protein kinase B and Toll-like receptor/nuclear factor kappa B signaling pathways in experimental obesity Wistar rat model
  137. The therapeutic potential of targeting Oncostatin M and the interleukin-6 family in retinal diseases: A comprehensive review
  138. BA inhibits LPS-stimulated inflammatory response and apoptosis in human middle ear epithelial cells by regulating the Nf-Kb/Iκbα axis
  139. Role of circRMRP and circRPL27 in chronic obstructive pulmonary disease
  140. Investigating the role of hyperexpressed HCN1 in inducing myocardial infarction through activation of the NF-κB signaling pathway
  141. Characterization of phenolic compounds and evaluation of anti-diabetic potential in Cannabis sativa L. seeds: In vivo, in vitro, and in silico studies
  142. Quantitative immunohistochemistry analysis of breast Ki67 based on artificial intelligence
  143. Ecology and Environmental Science
  144. Screening of different growth conditions of Bacillus subtilis isolated from membrane-less microbial fuel cell toward antimicrobial activity profiling
  145. Degradation of a mixture of 13 polycyclic aromatic hydrocarbons by commercial effective microorganisms
  146. Evaluation of the impact of two citrus plants on the variation of Panonychus citri (Acari: Tetranychidae) and beneficial phytoseiid mites
  147. Prediction of present and future distribution areas of Juniperus drupacea Labill and determination of ethnobotany properties in Antalya Province, Türkiye
  148. Population genetics of Todarodes pacificus (Cephalopoda: Ommastrephidae) in the northwest Pacific Ocean via GBS sequencing
  149. A comparative analysis of dendrometric, macromorphological, and micromorphological characteristics of Pistacia atlantica subsp. atlantica and Pistacia terebinthus in the middle Atlas region of Morocco
  150. Macrofungal sporocarp community in the lichen Scots pine forests
  151. Assessing the proximate compositions of indigenous forage species in Yemen’s pastoral rangelands
  152. Food Science
  153. Gut microbiota changes associated with low-carbohydrate diet intervention for obesity
  154. Reexamination of Aspergillus cristatus phylogeny in dark tea: Characteristics of the mitochondrial genome
  155. Differences in the flavonoid composition of the leaves, fruits, and branches of mulberry are distinguished based on a plant metabolomics approach
  156. Investigating the impact of wet rendering (solventless method) on PUFA-rich oil from catfish (Clarias magur) viscera
  157. Non-linear associations between cardiovascular metabolic indices and metabolic-associated fatty liver disease: A cross-sectional study in the US population (2017–2020)
  158. Knockdown of USP7 alleviates atherosclerosis in ApoE-deficient mice by regulating EZH2 expression
  159. Utility of dairy microbiome as a tool for authentication and traceability
  160. Agriculture
  161. Enhancing faba bean (Vicia faba L.) productivity through establishing the area-specific fertilizer rate recommendation in southwest Ethiopia
  162. Impact of novel herbicide based on synthetic auxins and ALS inhibitor on weed control
  163. Perspectives of pteridophytes microbiome for bioremediation in agricultural applications
  164. Fertilizer application parameters for drip-irrigated peanut based on the fertilizer effect function established from a “3414” field trial
  165. Improving the productivity and profitability of maize (Zea mays L.) using optimum blended inorganic fertilization
  166. Application of leaf multispectral analyzer in comparison to hyperspectral device to assess the diversity of spectral reflectance indices in wheat genotypes
  167. Animal Sciences
  168. Knockdown of ANP32E inhibits colorectal cancer cell growth and glycolysis by regulating the AKT/mTOR pathway
  169. Development of a detection chip for major pathogenic drug-resistant genes and drug targets in bovine respiratory system diseases
  170. Exploration of the genetic influence of MYOT and MB genes on the plumage coloration of Muscovy ducks
  171. Transcriptome analysis of adipose tissue in grazing cattle: Identifying key regulators of fat metabolism
  172. Comparison of nutritional value of the wild and cultivated spiny loaches at three growth stages
  173. Transcriptomic analysis of liver immune response in Chinese spiny frog (Quasipaa spinosa) infected with Proteus mirabilis
  174. Disruption of BCAA degradation is a critical characteristic of diabetic cardiomyopathy revealed by integrated transcriptome and metabolome analysis
  175. Plant Sciences
  176. Effect of long-term in-row branch covering on soil microorganisms in pear orchards
  177. Photosynthetic physiological characteristics, growth performance, and element concentrations reveal the calcicole–calcifuge behaviors of three Camellia species
  178. Transcriptome analysis reveals the mechanism of NaHCO3 promoting tobacco leaf maturation
  179. Bioinformatics, expression analysis, and functional verification of allene oxide synthase gene HvnAOS1 and HvnAOS2 in qingke
  180. Water, nitrogen, and phosphorus coupling improves gray jujube fruit quality and yield
  181. Improving grape fruit quality through soil conditioner: Insights from RNA-seq analysis of Cabernet Sauvignon roots
  182. Role of Embinin in the reabsorption of nucleus pulposus in lumbar disc herniation: Promotion of nucleus pulposus neovascularization and apoptosis of nucleus pulposus cells
  183. Revealing the effects of amino acid, organic acid, and phytohormones on the germination of tomato seeds under salinity stress
  184. Combined effects of nitrogen fertilizer and biochar on the growth, yield, and quality of pepper
  185. Comprehensive phytochemical and toxicological analysis of Chenopodium ambrosioides (L.) fractions
  186. Impact of “3414” fertilization on the yield and quality of greenhouse tomatoes
  187. Exploring the coupling mode of water and fertilizer for improving growth, fruit quality, and yield of the pear in the arid region
  188. Metagenomic analysis of endophytic bacteria in seed potato (Solanum tuberosum)
  189. Antibacterial, antifungal, and phytochemical properties of Salsola kali ethanolic extract
  190. Exploring the hepatoprotective properties of citronellol: In vitro and in silico studies on ethanol-induced damage in HepG2 cells
  191. Enhanced osmotic dehydration of watermelon rind using honey–sucrose solutions: A study on pre-treatment efficacy and mass transfer kinetics
  192. Effects of exogenous 2,4-epibrassinolide on photosynthetic traits of 53 cowpea varieties under NaCl stress
  193. Comparative transcriptome analysis of maize (Zea mays L.) seedlings in response to copper stress
  194. An optimization method for measuring the stomata in cassava (Manihot esculenta Crantz) under multiple abiotic stresses
  195. Fosinopril inhibits Ang II-induced VSMC proliferation, phenotype transformation, migration, and oxidative stress through the TGF-β1/Smad signaling pathway
  196. Antioxidant and antimicrobial activities of Salsola imbricata methanolic extract and its phytochemical characterization
  197. Bioengineering and Biotechnology
  198. Absorbable calcium and phosphorus bioactive membranes promote bone marrow mesenchymal stem cells osteogenic differentiation for bone regeneration
  199. New advances in protein engineering for industrial applications: Key takeaways
  200. An overview of the production and use of Bacillus thuringiensis toxin
  201. Research progress of nanoparticles in diagnosis and treatment of hepatocellular carcinoma
  202. Bioelectrochemical biosensors for water quality assessment and wastewater monitoring
  203. PEI/MMNs@LNA-542 nanoparticles alleviate ICU-acquired weakness through targeted autophagy inhibition and mitochondrial protection
  204. Unleashing of cytotoxic effects of thymoquinone-bovine serum albumin nanoparticles on A549 lung cancer cells
  205. Erratum
  206. Erratum to “Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM”
  207. Erratum to “Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation”
  208. Retraction
  209. Retraction to “MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB”
  210. Retraction to “A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis”
  211. Special Issue on Advances in Neurodegenerative Disease Research and Treatment
  212. Transplantation of human neural stem cell prevents symptomatic motor behavior disability in a rat model of Parkinson’s disease
  213. Special Issue on Multi-omics
  214. Inflammasome complex genes with clinical relevance suggest potential as therapeutic targets for anti-tumor drugs in clear cell renal cell carcinoma
  215. Gastroesophageal varices in primary biliary cholangitis with anti-centromere antibody positivity: Early onset?
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