Home Knockdown of NUPR1 inhibits angiogenesis in lung cancer through IRE1/XBP1 and PERK/eIF2α/ATF4 signaling pathways
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Knockdown of NUPR1 inhibits angiogenesis in lung cancer through IRE1/XBP1 and PERK/eIF2α/ATF4 signaling pathways

  • Lihuai Wang , Jing Wen , Yinhui Sun , Xiao Yang , Yi Ma and Xuefei Tian EMAIL logo
Published/Copyright: October 16, 2023
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Open Medicine
From the journal Open Medicine Volume 18 Issue 1

Abstract

The stress response molecule nuclear protein‑1 (NUPR1) is essential for the growth of multiple types of human malignant tumor cells. However, the significance of NUPR1 in lung cancer is still not entirely elucidated. Therefore, this study is aimed to explore the function and underlying mechanisms of NUPR1 in lung cancer. NUPR1 mRNA and protein levels in lung cancer cell lines (A549 or H1299 cells) were silenced through siRNA transfection and western blot observed its successful infection efficiency. Then, using tube formation and wound healing experiments, the effects of si-NUPR1 on angiogenesis and migration of human umbilical vein endothelial cells (HUVEC) were examined, respectively, which indicated inhibitory effects on the angiogenesis and migration of HUVEC. Vascular endothelial growth factor A (VEGFA), a vital molecule in angiogenesis, was detected by PCR and western blot assays, manifesting NUPR1 knockdown represses VEGFA expression. Furthermore, the knockdown of NUPR1 may reduce angiogenesis by lowering VEGFA expression through inositol-requiring enzyme 1 (IRE1)/X box binding protein 1 (XBP1) and protein kinase RNA-like endoplasmic reticulum kinase (PERK)/eukaryotic translation initiation factor 2 A (eIF2α)/recombinant activating transcription factor 4 (ATF4) signaling pathways in A549 or H1299 cells. In conclusion, these findings demonstrated that NUPR1 knockdown inhibits angiogenesis in A549 and H1299 cells through IRE1/XBP1 and PERK/eIF2α/ATF4 signaling pathways, indicating that NUPR1 could represent a novel lung cancer therapeutic target.

Keywords: NUPR1; lung cancer; angiogenesis; signaling pathways

1 Introduction

Lung cancer is among the most prevalent and lethal forms of cancer, having a high mortality rate [1]. Lung cancer is usually characterized by early migration and invasion, with richly vascularized tumor tissues [1]. Non-small cell lung cancer (NSCLC), which comprises adenocarcinoma, large cell carcinoma, and squamous carcinoma, is the predominant subtype of lung cancer, comprising approximately 80% of lung malignancies [1,2]. Despite significant breakthroughs in lung cancer treatment, such as the development of new medications and treatment alternatives, patients with NSCLC continue to have a dismal 5-year survival rate [3]. Consequently, it is essential to investigate the molecular processes underlying the advancement of NSCLC.

Endoplasmic reticulum (ER) buildup of misfolded or unfolded proteins is a characteristic of all malignancies [4], including NSCLC [5]. Around 55.9–87.5% of NSCLC tissues are under ER stress [5]. Efficient reduction of such protein folding load is required to maintain ER homeostasis, and the reduction impact is predominantly through the unfolded protein response (UPR), an evolutionarily conserved signaling pathway in eukaryotic cells [5,6]. Interestingly, UPR activation is required for high proliferation and chemoresistance in NSCLC cells [5].

Angiogenesis, characterized by the germination, migration, and remodeling of existing blood vessels, is crucial to the development of NSCLC, and vascular endothelial growth factor A (VEGFA) involves in the progress of angiogenesis [7]. Furthermore, activated UPR has been found to result in the upregulation of many pro-angiogenic factors (such as VEGFA) through inducing transcription factors inositol-requiring enzyme 1 (XBP-1) and activating transcription factor 4 (ATF4) to contribute to stabilizing VEGFA mRNA and stimulating VEGFA transcription [8].

Nuclear protein 1 (NUPR1), a stress-induced protein, has been found to represent an intriguing link between cellular and ER stress, which plays an essential part in the development of a number of malignancies, including pancreatic, breast, and prostate cancers [9]. In addition, NUPR1 has been reported to contribute to the progression of lung cancer [10]. Our previous study also confirmed that the knockdown of NUPR1 inhibited UPR-related factors (including UPR, XBP1, and ATF4) [11]. It has been shown that NUPR1 enhances VEGFA-mediated angiogenesis in hepatocellular carcinoma [12]. Unfortunately, the involvement of NUPR1 in lung cancer angiogenesis and related mechanisms are unclear.

In this study, the effect of NUPR1 in lung cancer cell lines was estimated. It was found that NUPR1 silencing could inhibit angiogenesis in human umbilical vein endothelial cells (HUVEC) cells, and these inhibitory effects may exert through reducing VEGFA expression and modulating UPR-induced transcription factors (inositol-requiring enzyme 1 [IRE1]/XBP1 and protein kinase RNA-like endoplasmic reticulum kinase [PERK]/eukaryotic translation initiation factor 2 A [eIF2α]/ATF4).

2 Methods

2.1 Cell culture in hypoxic

American Type Culture Collection was the source for the A549 (CRM-CCL-185) and H1299 (CRL-5809) human lung cancer cell lines. They were cultivated in RPMI-1640 media (Sigma Aldrich, MFCD00217820) with 10% fetal bovine serum (FBS) (Gibco, 10099-141) under a hypoxic environment (5% CO2, 1% O2, and 94% N2).

2.2 Downregulation of NUPR1 gene by siRNA

The NUPR1 gene was knockdown using the siRNA transfection kit (Shanghai GeneChem Co., Ltd, China): NUPR1 siRNA #1 5ʹ-GGAUGAAUCUGACCUCUAUTT-3ʹ and NUPR1 siRNA #2 5ʹ-GGCAGCAACAAUAAAUAGATT-3ʹ. By adding Lipofectamine RNAiMAX complex (Invitrogen, Carlsbad, CA, USA) containing siRNA to the culture media, siRNA transfection of A549 and H1299 cells was initiated. A well contained Lipofectamine RNAiMAX and siRNA and the ratio was 1.5 μL:5 pmol per well. Silencer Select Negative Control #1 siRNA (Ambion) was employed as a negative control (NC) for the siRNA therapy.

2.3 Tube formation assay

Growth factor-reduced Matrigel Basement Membrane Matrix (BD Biosciences, USA) was thawed gently on ice. A 96-well plate was then added with 50 μL of polymerization solution. Lung cancer cells were cultivated under hypoxic environment (5% CO2, 1% O2, and 94% N2) and incubated for 24 h on a total of 1 × 104 HUVECs plated on the top of the Matrigel matrix. Finally, the capillary network was examined by counting all the tubes in ten different microscopic regions at random.

2.4 Wound healing

In six-well plates, the A549 and H1299 cells were cultivated till confluence. After treatments, confluent monolayers were scraped to form a linear wound by starving the cells for an overnight period in a medium containing 1% FBS (Gibco). The cells were washed and then cultivated for 24 h in complete media. The wounds were captured on camera using a phase contrast microscope.

2.5 Reverse transcription quantitative PCR

Using the 2−ΔΔCT method, the mRNA relative expression level was quantified. Total RNA was extracted and then its concentration and purity were determined through a spectrophotometer (Thermo Fisher Scientific, Inc., MA, USA). Subsequently, using the StepOne™ PCR amplifier (Applied Biosystems, USA) and SYBR Premix Ex Taq™ II PCR kit (Takara Biotechnology Co., Ltd) following the manufacturer’s instructions, appropriate primer-coated RNA was reverse transcribed into cDNA. The primer sequences of NUPR1 were 5ʹ-GGAAAGGTCGCACCAAGAGAG-3ʹ (forward) and 5ʹ-ACCAGTTTCCTCTCGTGCCC-3ʹ (reverse). The primer sequences of β-actin, as a control group, were 5ʹ-CATGTACGTTGCTATCCAGGC-3ʹ (forward) and 5ʹ-CTCCTTAATGTCACGCACGAT-3ʹ (reverse).

2.6 Western blot

By using western blot, NUPR1, VEGFA, PERK, p-eIF2α, eIF2α, ATF4, IRE1, XBP1, and β-actin expression in A549 and H1299 cells were assessed. The protein debris was removed by centrifuging (Thermo Fisher, 75004061) at 12,000 rpm for 10 min at 4°C, after extraction with RIPA buffer (Beyotime, Shanghai, China). Protein concentration was then quantified using a bicinchoninic acid kit (Beyotime, Shanghai, China). Equivalent quantities (10 μg) of denaturized proteins were electrophoretically separated based on the molecular weight before being transferred to polyvinylidene difluoride membranes (LMAI Bio, LM1136). The membranes were blocked with 5% nonfat dry milk at room temperature for 1 h. The membrane was then treated with primary antibodies at 4°C overnight, rinsed with tris-buffered saline with 0.1% Tween® 20 detergent, and incubated with corresponding secondary antibodies at 37°C for 1 h. The emitter coupled logic detection technique was then used to identify particular protein bands in membranes (GE Healthcare, Piscataway, NJ, USA).

Antibodies against NUPR1 (#ab234696, 1:1,000), VEGFA (#ab52917, 1:1,000), PERK (#ab229912, 1:1,000), eIF2α (#ab169528, 1:1,000), ATF4 (#ab270980, 1:1,000), IRE1 (#ab124945, 1:1,000), XBP1 (#ab220783, 1:1,000), and β-actin (#ab8226, 1:1,000) were purchased from Abcam. Anti-mouse (#4410, 1:10,000) and anti-rabbit (#4414, 1:10,000) peroxidase-conjugated secondary antibodies were acquired from Cell Signaling Technologies.

2.7 Statistical analysis

Using SPSS 22.0 (IBM, Armonk, NY, USA), all data were statistically evaluated. Student’s t-test was utilized to identify significant differences. The findings of three separate trials are shown as the mean ± standard deviation (SD). p  ≤  0.05 was considered to be statistically significant.

3 Results

3.1 NUPR1 knockdown inhibits angiogenesis in lung cancer cells

To better understand the significance of NUPR1 in the lung cancer cell lines, the siRNA against NUPR1 was used for gene silencing in the A549 and H1299 cells. The expression protein levels of NUPR1 were detected using western blot, the results of which revealed that NUPR1 protein expression has a significant reduction in the si-NUPR1#1 and i-NUPR1#2 groups compared to that in the NC group (Figure 1a).

Figure 1 NUPR1 knockdown inhibits angiogenesis in lung cancer cells: (a) expression of NUPR1 was detected by western blot and normalized with β-actin and (b) tube formation assays were performed to measure angiogenesis in HUVEC cells, which were cultured in si-NUPR1-transfected lung cancer cells medium. Data represent the mean ± SD. **p < 0.01, ***p < 0.001 vs the NC group.
Figure 1

NUPR1 knockdown inhibits angiogenesis in lung cancer cells: (a) expression of NUPR1 was detected by western blot and normalized with β-actin and (b) tube formation assays were performed to measure angiogenesis in HUVEC cells, which were cultured in si-NUPR1-transfected lung cancer cells medium. Data represent the mean ± SD. **p < 0.01, ***p < 0.001 vs the NC group.

Angiogenesis is critical for tumorigenesis, migration, and invasion and the hypoxic microenvironment of tumors may further induce angiogenesis [3]. Moreover, NUPR1 has been reported to have an angiogenic effect [12]. Then, in this study, the supernatants of si-NUPR1-transfected cells were obtained to analyze HUVEC cell tube development. The accumulated number of tubes in the si-NUPR1#1 and si-NUPR1#2 supernatant groups was much lower than in the sh-NC group (Figure 1b). Together, our findings suggested that inhibiting NUPR1 expression might reduce angiogenesis in lung cancer.

3.2 NUPR1 knockdown decreases cell migration of HUVEC cells

Some studies showed that HUVEC cell migration is essential for tumor angiogenesis, accelerating tumor progression [3]. Hence, a wound-healing experiment was conducted to determine the effect of NUPR1 on HUVEC cells. HUVEC cells were incubated with medium from A549 and H1299 cells, which were cultivated under hypoxic environments. The analysis confirmed that a medium with NUPR1 deletion could markedly reduce the number of migrative HUVEC cells (Figure 2). Collectively, the result suggested that NUPR1 knockdown could repress HUEVC cell migration.

Figure 2 NUPR1 knockdown decreases cell migration of HUVEC cells. Wound healing analysis was performed to measure cell migration. Scale bar, 100 μm. Data represent the mean ± SD. *p < 0.05, ***p < 0.001 vs the NC group.
Figure 2

NUPR1 knockdown decreases cell migration of HUVEC cells. Wound healing analysis was performed to measure cell migration. Scale bar, 100 μm. Data represent the mean ± SD. *p < 0.05, ***p < 0.001 vs the NC group.

3.3 NUPR1 knockdown suppresses VEGFA expression

VEGFA is pivotal in controlling angiogenesis, and the hypoxic status in tumor tissues could upregulate the secretion of the pro-angiogenic factor VEGFA [13]. Thus, the mRNA and protein expression levels of VEGFA were assessed by PCR and western blot, respectively. These findings showed the knockdown of NUPR1 in A549 and H1299 cells markedly decreased the expression levels of VEGFA (Figure 3a and b).

Figure 3 NUPR1 knockdown suppresses VEGFA expression: (a) RT-qPCR analysis of VEGFA mRNA levels and (b) western blot analysis of VEGFA protein expression levels. Data represent the mean ± SD. **p < 0.01, ***p < 0.001 vs the NC group.
Figure 3

NUPR1 knockdown suppresses VEGFA expression: (a) RT-qPCR analysis of VEGFA mRNA levels and (b) western blot analysis of VEGFA protein expression levels. Data represent the mean ± SD. **p < 0.01, ***p < 0.001 vs the NC group.

3.4 NUPR1 knockdown represses VEGFA expression through XBP1 and ATF4

Chipurupalli et al. found that PERK–eIF2α–ATF4 signaling pathway confers a survival advantage to tumor cells under hypoxic environment [14]. Additionally, hypoxic activates the expression levels of XBP1 mRNA and protein, and the deficiency of XBP1 inhibits tumor growth [14]. Then, to clarify whether the mechanism of NUPR1 affected the reduction of VEGFA, and whether the effects may exert through acting on XBP1 and ATF4, the expression of PERK, p-eIF2α, eIF2α, ATF4, IRE1, and XBP1 in A549 and H1299 cells were detected by western blot. Data suggest that these XBP1 and ATF4 pathway-related molecules (Figure 4a and b) and VEGFA (Figure 4c) were dramatically decreased in NUPR1 knockdown group than in the control group. Furthermore, to determine the relationship between NUPR1 and XBP1 and ATF4 transcription factors, si-NUPR1 transfected cells supplied with XBP1 or ATF4 have upregulated the expression of VEGFA compared to si-NUPR1 with vector group (Figure 4c), which demonstrated that si-NUPR1 may repress the secretion of VEGFA by deregulating XBP1 and ATF4.

Figure 4 NUPR1 knockdown represses VEGFA expression through XBP1 and ATF4: (a) western blot analysis of PERK, p-eIF2α, eIF2α, and ATF4, and normalized with β-actin, (b) western blot analysis of IRE1 and XBP1 and normalized with β-actin, and (c) RT-qPCR analysis of VEGFA mRNA levels in A549 and H1299 cells. **p < 0.01, ***p < 0.001 vs the NC group. ^^^p < 0.001 vs the vector with si-NUPR1 group.
Figure 4

NUPR1 knockdown represses VEGFA expression through XBP1 and ATF4: (a) western blot analysis of PERK, p-eIF2α, eIF2α, and ATF4, and normalized with β-actin, (b) western blot analysis of IRE1 and XBP1 and normalized with β-actin, and (c) RT-qPCR analysis of VEGFA mRNA levels in A549 and H1299 cells. **p < 0.01, ***p < 0.001 vs the NC group. ^^^p < 0.001 vs the vector with si-NUPR1 group.

3.5 NUPR1 knockdown decreases angiogenesis by reducing VEGFA expression

VEGFA, a key angiogenic regulator, involves in the formation of the vascular network [13]. Here, HUVEC cells were seeded in the plate and cultured in A549 or H1299 cell medium, and measured angiogenesis through tube formation assay. We then found that NUPR1 knockdown significantly decreased the tube number in HUVEC cells, while cells in si-NUPR1 medium added with VEGFA stimulated the activities of angiogenesis than cells in si-NUPR1 (Figure 5), which suggests that the deletion of NUPR1 may decrease angiogenesis by reducing VEGFA expression.

Figure 5 NUPR1 knockdown decreases angiogenesis by reducing VEGFA expression. Tube formation assays were performed to measure angiogenesis in HUVEC cells. ***p < 0.001 vs the NC group. ^^^p < 0.001 vs the vector with si-NUPR1 group.
Figure 5

NUPR1 knockdown decreases angiogenesis by reducing VEGFA expression. Tube formation assays were performed to measure angiogenesis in HUVEC cells. ***p < 0.001 vs the NC group. ^^^p < 0.001 vs the vector with si-NUPR1 group.

4 Discussion

In this study, the knockdown of NUPR1 could inhibit angiogenesis in A549 and H1299 cells through IRE1/XBP1 and PERK/eIF2α/ATF4 signaling pathways. These findings first provide novel evidence for NUPR1 as a therapeutic target and its specific mechanism on lung cancer.

NUPR1, as a stress-induced protein, appears to be involved in a variety of stress-related functions [11] and can promote tumor growth and aggressiveness [9]. Previous studies have shown that NUPR1 affects the biological functions of tumor cells by regulating cell apoptosis and proliferation, and angiogenesis [12]. For example, NUPR1 alleviates apoptosis by promoting UPR in NSCLC [11]. NUPR1 controls the expression of genes critical to angiogenesis and tumor cell migration and invasion, facilitating the development and metastasis of metastatic breast cancer [15].

It is well established that angiogenesis and angiogenic factors contribute to several processes, which are important to cancer development and progression [3,16]. For instance, VEGF/VEGFR acts as a therapeutic target to inhibit metastasis and angiogenesis of NSCLC [3]. VEGFA, as the major pro-angiogenetic molecule, is induced by thyroid hormone, thereby accelerating angiogenesis and metastasis of liver cancer [12]. Vitexin, a bioactive flavonoid compound, inhibits the angiogenesis of cervical cancer through the VEGFA/VEGFR2 pathway, contributing to inhibition of tumor progression [16]. Similarly, our previous study also confirmed that NUPR1 knockdown inhibited the angiogenic activity of NSCLC by suppressing UPR-related factors (including XBP1 and others) and VEGFA activity [11]. In this study, NUPR1 was successfully silenced in lung cancer cell lines (A549 and H1299 cells) using si-RNA technology to investigate the effect of NUPR1 silencing on cell biological functions such as angiogenesis and migration in lung cancer. It was found that HUVEC cells cultured with cultures of si-NUPR1-transfected cancer cells showed a significant reduction in tube formation activity and inhibition of VEGFA expression. Further studies revealed that HUVEC tube formation activity was significantly improved by exogenous supplementation of VEGFA. These results suggest that si-NUPR1 may affect tumor progression by inhibiting the secretion of VEGFA to reduce angiogenesis.

In addition, it was shown that NUPR1 actively participates in the activation of the UPR, which may be responsible for the secretion of many pro-angiogenic factors, including VEGFA, XBP1, and ATF4 [17]. In this study, si-NUPR1 transfected cells were exogenously supplied with XBP1 or ATF4, which are downstream of NUPR1. These findings demonstrated that si-NUPR1 can inhibit VEGFA secretion by downregulating the activity of IRE1/XBP1 and PERK/eIF2α/ATF4 signaling pathways to reduce angiogenesis.

In conclusion, this study shows that si-RNA-mediated knockdown of NUPR1 significantly inhibited tubule formation activity in lung cancer and suppressed the cell migration activity, thereby suppressing tumor progression. The effect may be through the inhibition of the secretion of VEGFA, a pro-angiogenic factor, by downregulating the activity of IRE1/XBP1 and PERK/eIF2α/ATF4 signaling pathways. Further studies on the functional role of NUPR1 may lead to an improved understanding of the molecular mechanisms of lung cancer drugs, and inhibition of NUPR1 action contributing to the reduction of angiogenesis may be an effective strategy for the treatment of lung cancer.

# These authors contributed equally to the work.

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Acknowledgements

Not applicable.

  1. Funding information: This work was supported by the Hunan Province Traditional Chinese Medicine Cancer Clinical Research Center Project (Grant no. 2021SK4023) and Hunan Province Clinical Medical Technology Innovation Guidance Project (Grant no. 2020SK51405).

  2. Author contributions: Conceptualization, methodology, and writing – original draft were performed by Lihuai Wang and Jing Wen; formal analysis, resources, and investigation were performed by Yinhui Sun; formal analysis, visualization, and data curation were performed by Xiao Yang; project administration, supervision, and validation were performed by Yi Ma; validation, supervision, and writing – review and editing were performed by Xuefei Tian. All authors read and approved the final manuscript.

  3. Conflict of interest: The authors state that there are no conflicts of interest to disclose.

  4. Data availability statement: All data generated or analyzed during this study are included in this published article. The datasets used and/or analyzed during the present study are available from the corresponding author on reasonable request.

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Received: 2023-04-06
Revised: 2023-07-17
Accepted: 2023-08-15
Published Online: 2023-10-16

© 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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  171. D-dimer trends predict COVID-19 patient’s prognosis: A retrospective chart review study
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  176. Prevalence and antibiogram of bacteria causing urinary tract infection among patients with chronic kidney disease
  177. Reactive oxygen species within the vaginal space: An additional promoter of cervical intraepithelial neoplasia and uterine cervical cancer development?
  178. Identification of disulfidptosis-related genes and immune infiltration in lower-grade glioma
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  193. Integrative bioinformatics analysis reveals STAT2 as a novel biomarker of inflammation-related cardiac dysfunction in atrial fibrillation
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  196. lncRNA LENGA sponges miR-378 to promote myocardial fibrosis in atrial fibrillation
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  216. Long-term administration of probiotics prevents gastrointestinal mucosal barrier dysfunction in septic mice partly by upregulating the 5-HT degradation pathway
  217. miR-192 inhibits the activation of hepatic stellate cells by targeting Rictor
  218. Diagnostic and prognostic value of MR-pro ADM, procalcitonin, and copeptin in sepsis
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  237. Liver abscess complicated with multiple organ invasive infection caused by hematogenous disseminated hypervirulent Klebsiella pneumoniae: A case report
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  242. Clinicopathological characteristics and diagnosis of hepatic sinusoidal obstruction syndrome caused by Tusanqi – Case report and literature review
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  245. Malignant hyperthermia: Report on a successful rescue of a case with the highest temperature of 44.2°C
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  247. Rapid Communication
  248. Impact of COVID-19 lockdown on glycemic levels during pregnancy: A retrospective analysis
  249. Erratum
  250. Erratum to “Inhibition of miR-21 improves pulmonary vascular responses in bronchopulmonary dysplasia by targeting the DDAH1/ADMA/NO pathway”
  251. Erratum to: “Fer exacerbates renal fibrosis and can be targeted by miR-29c-3p”
  252. Retraction
  253. Retraction of “Study to compare the effect of casirivimab and imdevimab, remdesivir, and favipiravir on progression and multi-organ function of hospitalized COVID-19 patients”
  254. Retraction of “circ_0062491 alleviates periodontitis via the miR-142-5p/IGF1 axis”
  255. Retraction of “miR-223-3p alleviates TGF-β-induced epithelial-mesenchymal transition and extracellular matrix deposition by targeting SP3 in endometrial epithelial cells”
  256. Retraction of “SLCO4A1-AS1 mediates pancreatic cancer development via miR-4673/KIF21B axis”
  257. Retraction of “circRNA_0001679/miR-338-3p/DUSP16 axis aggravates acute lung injury”
  258. Retraction of “lncRNA ACTA2-AS1 inhibits malignant phenotypes of gastric cancer cells”
  259. Special issue Linking Pathobiological Mechanisms to Clinical Application for cardiovascular diseases
  260. Effect of cardiac rehabilitation therapy on depressed patients with cardiac insufficiency after cardiac surgery
  261. Special issue The evolving saga of RNAs from bench to bedside - Part I
  262. FBLIM1 mRNA is a novel prognostic biomarker and is associated with immune infiltrates in glioma
  263. Special Issue Computational Intelligence Methodologies Meets Recurrent Cancers - Part III
  264. Development of a machine learning-based signature utilizing inflammatory response genes for predicting prognosis and immune microenvironment in ovarian cancer
https://doi.org/10.1515/med-2023-0796
Keywords for this article
NUPR1; lung cancer; angiogenesis; signaling pathways
Creative Commons
BY 4.0

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  78. Identification of key enzalutamide-resistance-related genes in castration-resistant prostate cancer and verification of RAD51 functions
  79. Falls during oxaliplatin-based chemotherapy for gastrointestinal malignancies – (lessons learned from) a prospective study
  80. Outcomes of low-risk birth care during the Covid-19 pandemic: A cohort study from a tertiary care center in Lithuania
  81. Vitamin D protects intestines from liver cirrhosis-induced inflammation and oxidative stress by inhibiting the TLR4/MyD88/NF-κB signaling pathway
  82. Integrated transcriptome analysis identifies APPL1/RPS6KB2/GALK1 as immune-related metastasis factors in breast cancer
  83. Genomic analysis of immunogenic cell death-related subtypes for predicting prognosis and immunotherapy outcomes in glioblastoma multiforme
  84. Circular RNA Circ_0038467 promotes the maturation of miRNA-203 to increase lipopolysaccharide-induced apoptosis of chondrocytes
  85. An economic evaluation of fine-needle cytology as the primary diagnostic tool in the diagnosis of lymphadenopathy
  86. Midazolam impedes lung carcinoma cell proliferation and migration via EGFR/MEK/ERK signaling pathway
  87. Network pharmacology combined with molecular docking and experimental validation to reveal the pharmacological mechanism of naringin against renal fibrosis
  88. PTPN12 down-regulated by miR-146b-3p gene affects the malignant progression of laryngeal squamous cell carcinoma
  89. miR-141-3p accelerates ovarian cancer progression and promotes M2-like macrophage polarization by targeting the Keap1-Nrf2 pathway
  90. lncRNA OIP5-AS1 attenuates the osteoarthritis progression in IL-1β-stimulated chondrocytes
  91. Overexpression of LINC00607 inhibits cell growth and aggressiveness by regulating the miR-1289/EFNA5 axis in non-small-cell lung cancer
  92. Subjective well-being in informal caregivers during the COVID-19 pandemic
  93. Nrf2 protects against myocardial ischemia-reperfusion injury in diabetic rats by inhibiting Drp1-mediated mitochondrial fission
  94. Unfolded protein response inhibits KAT2B/MLKL-mediated necroptosis of hepatocytes by promoting BMI1 level to ubiquitinate KAT2B
  95. Bladder cancer screening: The new selection and prediction model
  96. circNFATC3 facilitated the progression of oral squamous cell carcinoma via the miR-520h/LDHA axis
  97. Prone position effect in intensive care patients with SARS-COV-2 pneumonia
  98. Clinical observation on the efficacy of Tongdu Tuina manipulation in the treatment of primary enuresis in children
  99. Dihydroartemisinin ameliorates cerebral I/R injury in rats via regulating VWF and autophagy-mediated SIRT1/FOXO1 pathway
  100. Knockdown of circ_0113656 assuages oxidized low-density lipoprotein-induced vascular smooth muscle cell injury through the miR-188-3p/IGF2 pathway
  101. Low Ang-(1–7) and high des-Arg9 bradykinin serum levels are correlated with cardiovascular risk factors in patients with COVID-19
  102. Effect of maternal age and body mass index on induction of labor with oral misoprostol for premature rupture of membrane at term: A retrospective cross-sectional study
  103. Potential protective effects of Huanglian Jiedu Decoction against COVID-19-associated acute kidney injury: A network-based pharmacological and molecular docking study
  104. Clinical significance of serum MBD3 detection in girls with central precocious puberty
  105. Clinical features of varicella-zoster virus caused neurological diseases detected by metagenomic next-generation sequencing
  106. Collagen treatment of complex anorectal fistula: 3 years follow-up
  107. LncRNA CASC15 inhibition relieves renal fibrosis in diabetic nephropathy through down-regulating SP-A by sponging to miR-424
  108. Efficacy analysis of empirical bismuth quadruple therapy, high-dose dual therapy, and resistance gene-based triple therapy as a first-line Helicobacter pylori eradication regimen – An open-label, randomized trial
  109. SMOC2 plays a role in heart failure via regulating TGF-β1/Smad3 pathway-mediated autophagy
  110. A prospective cohort study of the impact of chronic disease on fall injuries in middle-aged and older adults
  111. circRNA THBS1 silencing inhibits the malignant biological behavior of cervical cancer cells via the regulation of miR-543/HMGB2 axis
  112. hsa_circ_0000285 sponging miR-582-3p promotes neuroblastoma progression by regulating the Wnt/β-catenin signaling pathway
  113. Long non-coding RNA GNAS-AS1 knockdown inhibits proliferation and epithelial–mesenchymal transition of lung adenocarcinoma cells via the microRNA-433-3p/Rab3A axis
  114. lncRNA UCA1 regulates miR-132/Lrrfip1 axis to promote vascular smooth muscle cell proliferation
  115. Twenty-four-color full spectrum flow cytometry panel for minimal residual disease detection in acute myeloid leukemia
  116. Hsa-miR-223-3p participates in the process of anthracycline-induced cardiomyocyte damage by regulating NFIA gene
  117. Anti-inflammatory effect of ApoE23 on Salmonella typhimurium-induced sepsis in mice
  118. Analysis of somatic mutations and key driving factors of cervical cancer progression
  119. Hsa_circ_0028007 regulates the progression of nasopharyngeal carcinoma through the miR-1179/SQLE axis
  120. Variations in sexual function after laparoendoscopic single-site hysterectomy in women with benign gynecologic diseases
  121. Effects of pharmacological delay with roxadustat on multi-territory perforator flap survival in rats
  122. Analysis of heroin effects on calcium channels in rat cardiomyocytes based on transcriptomics and metabolomics
  123. Risk factors of recurrent bacterial vaginosis among women of reproductive age: A cross-sectional study
  124. Alkbh5 plays indispensable roles in maintaining self-renewal of hematopoietic stem cells
  125. Study to compare the effect of casirivimab and imdevimab, remdesivir, and favipiravir on progression and multi-organ function of hospitalized COVID-19 patients
  126. Correlation between microvessel maturity and ISUP grades assessed using contrast-enhanced transrectal ultrasonography in prostate cancer
  127. The protective effect of caffeic acid phenethyl ester in the nephrotoxicity induced by α-cypermethrin
  128. Norepinephrine alleviates cyclosporin A-induced nephrotoxicity by enhancing the expression of SFRP1
  129. Effect of RUNX1/FOXP3 axis on apoptosis of T and B lymphocytes and immunosuppression in sepsis
  130. The function of Foxp1 represses β-adrenergic receptor transcription in the occurrence and development of bladder cancer through STAT3 activity
  131. Risk model and validation of carbapenem-resistant Klebsiella pneumoniae infection in patients with cerebrovascular disease in the ICU
  132. Calycosin protects against chronic prostatitis in rats via inhibition of the p38MAPK/NF-κB pathway
  133. Pan-cancer analysis of the PDE4DIP gene with potential prognostic and immunotherapeutic values in multiple cancers including acute myeloid leukemia
  134. The safety and immunogenicity to inactivated COVID-19 vaccine in patients with hyperlipemia
  135. Circ-UBR4 regulates the proliferation, migration, inflammation, and apoptosis in ox-LDL-induced vascular smooth muscle cells via miR-515-5p/IGF2 axis
  136. Clinical characteristics of current COVID-19 rehabilitation outpatients in China
  137. Luteolin alleviates ulcerative colitis in rats via regulating immune response, oxidative stress, and metabolic profiling
  138. miR-199a-5p inhibits aortic valve calcification by targeting ATF6 and GRP78 in valve interstitial cells
  139. The application of iliac fascia space block combined with esketamine intravenous general anesthesia in PFNA surgery of the elderly: A prospective, single-center, controlled trial
  140. Elevated blood acetoacetate levels reduce major adverse cardiac and cerebrovascular events risk in acute myocardial infarction
  141. The effects of progesterone on the healing of obstetric anal sphincter damage in female rats
  142. Identification of cuproptosis-related genes for predicting the development of prostate cancer
  143. Lumican silencing ameliorates β-glycerophosphate-mediated vascular smooth muscle cell calcification by attenuating the inhibition of APOB on KIF2C activity
  144. Targeting PTBP1 blocks glutamine metabolism to improve the cisplatin sensitivity of hepatocarcinoma cells through modulating the mRNA stability of glutaminase
  145. A single center prospective study: Influences of different hip flexion angles on the measurement of lumbar spine bone mineral density by dual energy X-ray absorptiometry
  146. Clinical analysis of AN69ST membrane continuous venous hemofiltration in the treatment of severe sepsis
  147. Antibiotics therapy combined with probiotics administered intravaginally for the treatment of bacterial vaginosis: A systematic review and meta-analysis
  148. Construction of a ceRNA network to reveal a vascular invasion associated prognostic model in hepatocellular carcinoma
  149. A pan-cancer analysis of STAT3 expression and genetic alterations in human tumors
  150. A prognostic signature based on seven T-cell-related cell clustering genes in bladder urothelial carcinoma
  151. Pepsin concentration in oral lavage fluid of rabbit reflux model constructed by dilating the lower esophageal sphincter
  152. The antihypertensive felodipine shows synergistic activity with immune checkpoint blockade and inhibits tumor growth via NFAT1 in LUSC
  153. Tanshinone IIA attenuates valvular interstitial cells’ calcification induced by oxidized low density lipoprotein via reducing endoplasmic reticulum stress
  154. AS-IV enhances the antitumor effects of propofol in NSCLC cells by inhibiting autophagy
  155. Establishment of two oxaliplatin-resistant gallbladder cancer cell lines and comprehensive analysis of dysregulated genes
  156. Trial protocol: Feasibility of neuromodulation with connectivity-guided intermittent theta-burst stimulation for improving cognition in multiple sclerosis
  157. LncRNA LINC00592 mediates the promoter methylation of WIF1 to promote the development of bladder cancer
  158. Factors associated with gastrointestinal dysmotility in critically ill patients
  159. Mechanisms by which spinal cord stimulation intervenes in atrial fibrillation: The involvement of the endothelin-1 and nerve growth factor/p75NTR pathways
  160. Analysis of two-gene signatures and related drugs in small-cell lung cancer by bioinformatics
  161. Silencing USP19 alleviates cigarette smoke extract-induced mitochondrial dysfunction in BEAS-2B cells by targeting FUNDC1
  162. Menstrual irregularities associated with COVID-19 vaccines among women in Saudi Arabia: A survey during 2022
  163. Ferroptosis involves in Schwann cell death in diabetic peripheral neuropathy
  164. The effect of AQP4 on tau protein aggregation in neurodegeneration and persistent neuroinflammation after cerebral microinfarcts
  165. Activation of UBEC2 by transcription factor MYBL2 affects DNA damage and promotes gastric cancer progression and cisplatin resistance
  166. Analysis of clinical characteristics in proximal and distal reflux monitoring among patients with gastroesophageal reflux disease
  167. Exosomal circ-0020887 and circ-0009590 as novel biomarkers for the diagnosis and prediction of short-term adverse cardiovascular outcomes in STEMI patients
  168. Upregulated microRNA-429 confers endometrial stromal cell dysfunction by targeting HIF1AN and regulating the HIF1A/VEGF pathway
  169. Bibliometrics and knowledge map analysis of ultrasound-guided regional anesthesia
  170. Knockdown of NUPR1 inhibits angiogenesis in lung cancer through IRE1/XBP1 and PERK/eIF2α/ATF4 signaling pathways
  171. D-dimer trends predict COVID-19 patient’s prognosis: A retrospective chart review study
  172. WTAP affects intracranial aneurysm progression by regulating m6A methylation modification
  173. Using of endoscopic polypectomy in patients with diagnosed malignant colorectal polyp – The cross-sectional clinical study
  174. Anti-S100A4 antibody administration alleviates bronchial epithelial–mesenchymal transition in asthmatic mice
  175. Prognostic evaluation of system immune-inflammatory index and prognostic nutritional index in double expressor diffuse large B-cell lymphoma
  176. Prevalence and antibiogram of bacteria causing urinary tract infection among patients with chronic kidney disease
  177. Reactive oxygen species within the vaginal space: An additional promoter of cervical intraepithelial neoplasia and uterine cervical cancer development?
  178. Identification of disulfidptosis-related genes and immune infiltration in lower-grade glioma
  179. A new technique for uterine-preserving pelvic organ prolapse surgery: Laparoscopic rectus abdominis hysteropexy for uterine prolapse by comparing with traditional techniques
  180. Self-isolation of an Italian long-term care facility during COVID-19 pandemic: A comparison study on care-related infectious episodes
  181. A comparative study on the overlapping effects of clinically applicable therapeutic interventions in patients with central nervous system damage
  182. Low intensity extracorporeal shockwave therapy for chronic pelvic pain syndrome: Long-term follow-up
  183. The diagnostic accuracy of touch imprint cytology for sentinel lymph node metastases of breast cancer: An up-to-date meta-analysis of 4,073 patients
  184. Mortality associated with Sjögren’s syndrome in the United States in the 1999–2020 period: A multiple cause-of-death study
  185. CircMMP11 as a prognostic biomarker mediates miR-361-3p/HMGB1 axis to accelerate malignant progression of hepatocellular carcinoma
  186. Analysis of the clinical characteristics and prognosis of adult de novo acute myeloid leukemia (none APL) with PTPN11 mutations
  187. KMT2A maintains stemness of gastric cancer cells through regulating Wnt/β-catenin signaling-activated transcriptional factor KLF11
  188. Evaluation of placental oxygenation by near-infrared spectroscopy in relation to ultrasound maturation grade in physiological term pregnancies
  189. The role of ultrasonographic findings for PIK3CA-mutated, hormone receptor-positive, human epidermal growth factor receptor-2-negative breast cancer
  190. Construction of immunogenic cell death-related molecular subtypes and prognostic signature in colorectal cancer
  191. Long-term prognostic value of high-sensitivity cardiac troponin-I in patients with idiopathic dilated cardiomyopathy
  192. Establishing a novel Fanconi anemia signaling pathway-associated prognostic model and tumor clustering for pediatric acute myeloid leukemia patients
  193. Integrative bioinformatics analysis reveals STAT2 as a novel biomarker of inflammation-related cardiac dysfunction in atrial fibrillation
  194. Adipose-derived stem cells repair radiation-induced chronic lung injury via inhibiting TGF-β1/Smad 3 signaling pathway
  195. Real-world practice of idiopathic pulmonary fibrosis: Results from a 2000–2016 cohort
  196. lncRNA LENGA sponges miR-378 to promote myocardial fibrosis in atrial fibrillation
  197. Diagnostic value of urinary Tamm-Horsfall protein and 24 h urine osmolality for recurrent calcium oxalate stones of the upper urinary tract: Cross-sectional study
  198. The value of color Doppler ultrasonography combined with serum tumor markers in differential diagnosis of gastric stromal tumor and gastric cancer
  199. The spike protein of SARS-CoV-2 induces inflammation and EMT of lung epithelial cells and fibroblasts through the upregulation of GADD45A
  200. Mycophenolate mofetil versus cyclophosphamide plus in patients with connective tissue disease-associated interstitial lung disease: Efficacy and safety analysis
  201. MiR-1278 targets CALD1 and suppresses the progression of gastric cancer via the MAPK pathway
  202. Metabolomic analysis of serum short-chain fatty acid concentrations in a mouse of MPTP-induced Parkinson’s disease after dietary supplementation with branched-chain amino acids
  203. Cimifugin inhibits adipogenesis and TNF-α-induced insulin resistance in 3T3-L1 cells
  204. Predictors of gastrointestinal complaints in patients on metformin therapy
  205. Prescribing patterns in patients with chronic obstructive pulmonary disease and atrial fibrillation
  206. A retrospective analysis of the effect of latent tuberculosis infection on clinical pregnancy outcomes of in vitro fertilization–fresh embryo transferred in infertile women
  207. Appropriateness and clinical outcomes of short sustained low-efficiency dialysis: A national experience
  208. miR-29 regulates metabolism by inhibiting JNK-1 expression in non-obese patients with type 2 diabetes mellitus and NAFLD
  209. Clinical features and management of lymphoepithelial cyst
  210. Serum VEGF, high-sensitivity CRP, and cystatin-C assist in the diagnosis of type 2 diabetic retinopathy complicated with hyperuricemia
  211. ENPP1 ameliorates vascular calcification via inhibiting the osteogenic transformation of VSMCs and generating PPi
  212. Significance of monitoring the levels of thyroid hormone antibodies and glucose and lipid metabolism antibodies in patients suffer from type 2 diabetes
  213. The causal relationship between immune cells and different kidney diseases: A Mendelian randomization study
  214. Interleukin 33, soluble suppression of tumorigenicity 2, interleukin 27, and galectin 3 as predictors for outcome in patients admitted to intensive care units
  215. Identification of diagnostic immune-related gene biomarkers for predicting heart failure after acute myocardial infarction
  216. Long-term administration of probiotics prevents gastrointestinal mucosal barrier dysfunction in septic mice partly by upregulating the 5-HT degradation pathway
  217. miR-192 inhibits the activation of hepatic stellate cells by targeting Rictor
  218. Diagnostic and prognostic value of MR-pro ADM, procalcitonin, and copeptin in sepsis
  219. Review Articles
  220. Prenatal diagnosis of fetal defects and its implications on the delivery mode
  221. Electromagnetic fields exposure on fetal and childhood abnormalities: Systematic review and meta-analysis
  222. Characteristics of antibiotic resistance mechanisms and genes of Klebsiella pneumoniae
  223. Saddle pulmonary embolism in the setting of COVID-19 infection: A systematic review of case reports and case series
  224. Vitamin C and epigenetics: A short physiological overview
  225. Ebselen: A promising therapy protecting cardiomyocytes from excess iron in iron-overloaded thalassemia patients
  226. Aspirin versus LMWH for VTE prophylaxis after orthopedic surgery
  227. Mechanism of rhubarb in the treatment of hyperlipidemia: A recent review
  228. Surgical management and outcomes of traumatic global brachial plexus injury: A concise review and our center approach
  229. The progress of autoimmune hepatitis research and future challenges
  230. METTL16 in human diseases: What should we do next?
  231. New insights into the prevention of ureteral stents encrustation
  232. VISTA as a prospective immune checkpoint in gynecological malignant tumors: A review of the literature
  233. Case Reports
  234. Mycobacterium xenopi infection of the kidney and lymph nodes: A case report
  235. Genetic mutation of SLC6A20 (c.1072T > C) in a family with nephrolithiasis: A case report
  236. Chronic hepatitis B complicated with secondary hemochromatosis was cured clinically: A case report
  237. Liver abscess complicated with multiple organ invasive infection caused by hematogenous disseminated hypervirulent Klebsiella pneumoniae: A case report
  238. Urokinase-based lock solutions for catheter salvage: A case of an upcoming kidney transplant recipient
  239. Two case reports of maturity-onset diabetes of the young type 3 caused by the hepatocyte nuclear factor 1α gene mutation
  240. Immune checkpoint inhibitor-related pancreatitis: What is known and what is not
  241. Does total hip arthroplasty result in intercostal nerve injury? A case report and literature review
  242. Clinicopathological characteristics and diagnosis of hepatic sinusoidal obstruction syndrome caused by Tusanqi – Case report and literature review
  243. Synchronous triple primary gastrointestinal malignant tumors treated with laparoscopic surgery: A case report
  244. CT-guided percutaneous microwave ablation combined with bone cement injection for the treatment of transverse metastases: A case report
  245. Malignant hyperthermia: Report on a successful rescue of a case with the highest temperature of 44.2°C
  246. Anesthetic management of fetal pulmonary valvuloplasty: A case report
  247. Rapid Communication
  248. Impact of COVID-19 lockdown on glycemic levels during pregnancy: A retrospective analysis
  249. Erratum
  250. Erratum to “Inhibition of miR-21 improves pulmonary vascular responses in bronchopulmonary dysplasia by targeting the DDAH1/ADMA/NO pathway”
  251. Erratum to: “Fer exacerbates renal fibrosis and can be targeted by miR-29c-3p”
  252. Retraction
  253. Retraction of “Study to compare the effect of casirivimab and imdevimab, remdesivir, and favipiravir on progression and multi-organ function of hospitalized COVID-19 patients”
  254. Retraction of “circ_0062491 alleviates periodontitis via the miR-142-5p/IGF1 axis”
  255. Retraction of “miR-223-3p alleviates TGF-β-induced epithelial-mesenchymal transition and extracellular matrix deposition by targeting SP3 in endometrial epithelial cells”
  256. Retraction of “SLCO4A1-AS1 mediates pancreatic cancer development via miR-4673/KIF21B axis”
  257. Retraction of “circRNA_0001679/miR-338-3p/DUSP16 axis aggravates acute lung injury”
  258. Retraction of “lncRNA ACTA2-AS1 inhibits malignant phenotypes of gastric cancer cells”
  259. Special issue Linking Pathobiological Mechanisms to Clinical Application for cardiovascular diseases
  260. Effect of cardiac rehabilitation therapy on depressed patients with cardiac insufficiency after cardiac surgery
  261. Special issue The evolving saga of RNAs from bench to bedside - Part I
  262. FBLIM1 mRNA is a novel prognostic biomarker and is associated with immune infiltrates in glioma
  263. Special Issue Computational Intelligence Methodologies Meets Recurrent Cancers - Part III
  264. Development of a machine learning-based signature utilizing inflammatory response genes for predicting prognosis and immune microenvironment in ovarian cancer
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