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Transforming growth factor‑β1 functions as a competitive endogenous RNA that ameliorates intracranial hemorrhage injury by sponging microRNA‑93‑5p

Wang, Han, Cao, Xianming, Wen, Xiaoqing, Li, Dongling, Ouyang, Yetong, Bao, Bing, Zhong, Yuqin, Qin, Zhengfang, Yin, Min, Chen, Zhiying, Yin, Xiaoping·2021·Molecular Medicine Reports
DOI 10.3892/mmr.2021.12138PMC PMC8127068
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Abstract

Intracerebral hemorrhage (ICH) has the highest mortality rate of all stroke subtypes but an effective treatment has yet to be clinically implemented. Transforming growth factor‑β1 (TGF‑β1) has been reported to modulate microglia‑mediated neuroinflammation after ICH and promote functional recovery; however, the underlying mechanisms remain unclear. Non‑coding RNAs such as microRNAs (miRNAs) and competitive endogenous RNAs (ceRNAs) have surfaced as critical regulators in human disease. A known miR‑93 target, nuclear factor erythroid 2‑related factor 2 (Nrf2), has been shown to be neuroprotective after ICH. It was hypothesized that TGF‑β1 functions as a ceRNA that sponges miR‑93‑5p and thereby ameliorates ICH injury in the brain. Short interfering RNA (siRNA) was used to knock down TGF‑β1 and miR‑93 expression was also pharmacologically manipulated to elucidate the mechanistic association between miR‑93‑5p, Nrf2, and TGF‑β1 in an in vitro model of ICH (thrombin‑treated human microglial HMO6 cells). Bioinformatics predictive analyses showed that miR‑93‑5p could bind to both TGF‑β1 and Nrf2. It was found that neuronal miR‑93‑5p was dramatically decreased in these HMO6 cells, and similar changes were observed in fresh brain tissue from patients with ICH. Most importantly, luciferase reporter assays were used to demonstrate that miR‑93‑5p directly targeted Nrf2 to inhibit its expression and the addition of the TGF‑β1 untranslated region restored the levels of Nrf2. Moreover, an miR‑93‑5p inhibitor increased the expression of TGF‑β1 and Nrf2 and decreased apoptosis. Collectively, these results identified a novel function of TGF‑β1 as a ceRNA that sponges miR‑93‑5p to increase the expression of neuroprotective Nrf2 and decrease cell death after ICH. The present findings provided evidence to support miR‑93‑5p as a potential therapeutic target for the treatment of ICH.

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Figure 1. Bioinformatics analysis linking TGF-β1, Nrf2 and miR-93. (A) Association of human (homo sapiens; Hsa) TGF-β1 and Nrf2 sharing a common miR-93 binding site on their 3′-UTRs. Two programs (TargetScan and miRTarBase) predicted that both TGF-β1 and Nrf2 were potential targets of the miR-93-5p. The GenBank accession number and base-pair location of the 3′-UTR sequence of TGF-β1 and Nrf2 are included in parentheses. (B) Protein-protein interaction, co-expression network analyses using GeneMANIA. Genes are shown as nodes (gray circles) and color-coded lines indicate seven different types of interactions. The two gray circles on the left depict Nrf2 (also known as NFE2L2) and TGF-β1 (TGFB1) and the gray circles on the right depict the GeneMANIA-predicted genes. A larger gray circle indicates a higher correlation. Numbers represent the percentage of different types of interactions over the total. TGF, transforming growth factor; miR, microRNA; Nrf2, nuclear factor erythroid 2-related factor 2; UTR, untranslated region.
Figure 1. Bioinformatics analysis linking TGF-β1, Nrf2 and miR-93. (A) Association of human (homo sapiens; Hsa) TGF-β1 and Nrf2 sharing a common miR-93 binding site on their 3′-UTRs. Two programs (TargetScan and miRTarBase) predicted that both TGF-β1 and Nrf2 were potential targets of the miR-93-5p. The GenBank accession number and base-pair location of the 3′-UTR sequence of TGF-β1 and Nrf2 are included in parentheses. (B) Protein-protein interaction, co-expression network analyses using GeneMANIA. Genes are shown as nodes (gray circles) and color-coded lines indicate seven different types of interactions. The two gray circles on the left depict Nrf2 (also known as NFE2L2) and TGF-β1 (TGFB1) and the gray circles on the right depict the GeneMANIA-predicted genes. A larger gray circle indicates a higher correlation. Numbers represent the percentage of different types of interactions over the total. TGF, transforming growth factor; miR, microRNA; Nrf2, nuclear factor erythroid 2-related factor 2; UTR, untranslated region.CC BY-NC-ND · PubMed Central
Figure 2. Morphology and expression of HMO6 microglial cells after thrombin treatment. (A) TNF-α mRNA levels in thrombin-treated HMO6 cells are elevated significantly after 48 h, in a dose-dependent manner, compared with control cells (untreated). (B) Phase contrast microscopy showing the morphology of HMO6 cells that are untreated or treated with thrombin at concentrations of 20 or 40 U/ml. Scale bar, 50 µm. (C) Images of Iba1 (green) and CD68 (red) immunoreactivity in HMO6 cells, treated with 20 U/ml thrombin. DAPI (blue) labels the cell nuclei. Scale bar, 20 µm. (D) miR-93 expression in HMO6 cells with or without thrombin treatment. (E and F) The modulation of Nrf2 or TGF-β1 mRNA levels in thrombin-treated HMO6 cells after transfection with miR-93 mimic or the corresponding control (mimic NC) was assessed by reverse transcription-quantitative PCR. The red border represents the thrombin-treated groups. (G) TGF-β1 and miR-93 RNA expression levels in HMO6 cells were negatively correlated as assessed by Pearson correlation analysis (r=−0.967; P <0.05). (H) Western blotting images showing the protein levels of TGF-β1 and Nrf2 in HMO6 cells after thrombin (20 U/ml) treatment. β-actin was the loading control. (I) Quantification of the TGF-β1 and Nrf2 protein levels in untreated or thrombin-treated HMO6 cells. n=6 for each group. Data are presented as the means ± SD. *P<0.05, **P<0. 01. TNF, tumor necrosis factor; miR, microRNA; TGF, transforming growth factor; Nrf2, nuclear factor erythroid 2-related factor 2.
Figure 2. Morphology and expression of HMO6 microglial cells after thrombin treatment. (A) TNF-α mRNA levels in thrombin-treated HMO6 cells are elevated significantly after 48 h, in a dose-dependent manner, compared with control cells (untreated). (B) Phase contrast microscopy showing the morphology of HMO6 cells that are untreated or treated with thrombin at concentrations of 20 or 40 U/ml. Scale bar, 50 µm. (C) Images of Iba1 (green) and CD68 (red) immunoreactivity in HMO6 cells, treated with 20 U/ml thrombin. DAPI (blue) labels the cell nuclei. Scale bar, 20 µm. (D) miR-93 expression in HMO6 cells with or without thrombin treatment. (E and F) The modulation of Nrf2 or TGF-β1 mRNA levels in thrombin-treated HMO6 cells after transfection with miR-93 mimic or the corresponding control (mimic NC) was assessed by reverse transcription-quantitative PCR. The red border represents the thrombin-treated groups. (G) TGF-β1 and miR-93 RNA expression levels in HMO6 cells were negatively correlated as assessed by Pearson correlation analysis (r=−0.967; P <0.05). (H) Western blotting images showing the protein levels of TGF-β1 and Nrf2 in HMO6 cells after thrombin (20 U/ml) treatment. β-actin was the loading control. (I) Quantification of the TGF-β1 and Nrf2 protein levels in untreated or thrombin-treated HMO6 cells. n=6 for each group. Data are presented as the means ± SD. *P<0.05, **P<0. 01. TNF, tumor necrosis factor; miR, microRNA; TGF, transforming growth factor; Nrf2, nuclear factor erythroid 2-related factor 2.CC BY-NC-ND · PubMed Central
Figure 3. mRNA and protein expressions of miR93, TGF-s of TGF-β1 and Nrf2 in control and ICH patients. (A) mRNA expression of miRNAs known to be decreased by ICH, miR-181c measured by RT-qPCR in human brain tissue. (B-D) The relative RNA expression of miR-93, TGF-β1 and Nrf2 in patients without ICH (control patients) compared with patients with ICH was detected by RT-qPCR (n=6 for each group). Each individual data point is shown for both groups. The unpaired Student's t-test was used to compare differences. *P<0.05 vs. control patients. (E) TGF-β1 and miR-93 RNA expression levels in human brain tissue were negatively correlated as assessed by Pearson correlation analysis (r=−0.908; P<0.05). (F) A representative western blotting image showing Nrf2 and TGF-β1 protein expressions in human brain tissues. (G) The histogram on the right presents the quantification of the group data. Each experiment was independently repeated at least three times and the data are presented as the means ± SD. *P<0.05. miRNA/miR, microRNA; RT-qPCR, reverse transcription-quantitative PCR; TGF, transforming growth factor; Nrf2, nuclear factor erythroid 2-related factor 2; ICH, intracerebral hemorrhage.
Figure 3. mRNA and protein expressions of miR93, TGF-s of TGF-β1 and Nrf2 in control and ICH patients. (A) mRNA expression of miRNAs known to be decreased by ICH, miR-181c measured by RT-qPCR in human brain tissue. (B-D) The relative RNA expression of miR-93, TGF-β1 and Nrf2 in patients without ICH (control patients) compared with patients with ICH was detected by RT-qPCR (n=6 for each group). Each individual data point is shown for both groups. The unpaired Student's t-test was used to compare differences. *P<0.05 vs. control patients. (E) TGF-β1 and miR-93 RNA expression levels in human brain tissue were negatively correlated as assessed by Pearson correlation analysis (r=−0.908; P<0.05). (F) A representative western blotting image showing Nrf2 and TGF-β1 protein expressions in human brain tissues. (G) The histogram on the right presents the quantification of the group data. Each experiment was independently repeated at least three times and the data are presented as the means ± SD. *P<0.05. miRNA/miR, microRNA; RT-qPCR, reverse transcription-quantitative PCR; TGF, transforming growth factor; Nrf2, nuclear factor erythroid 2-related factor 2; ICH, intracerebral hemorrhage.CC BY-NC-ND · PubMed Central
Figure 4. TGF-β1 competes with Nrf2 mRNA for binding to miR-93. (A) Expression of miR-93 in HMO6 cells of each group after transfection. The expression of miR-93 was significantly elevated in miR-93 mimics group and declined in miR-93 inhibitor group, **P<0.05 vs. control group. (B) Expression of TGF-β1 in HMO6 cells of each group after transfection. The expression of TGF-β1 was significantly declined in the siTGF-β1 group. *P<0.05 vs. control group. (C) Mutated nucleotides in the TGF-β1 3′-UTR sequence (indicated by the dotted line and red font) were generated in the seed region of miR-93 to abolish binding. The mutated sequence is labeled TGF-β1−3′-UTR-MUT. (D and E) A dual luciferase reporter assay was used to test whether TGF-β1 and Nrf2 were targets of miR-93. 293T cells were co-transfected with (d) TGF-β1−3′-UTR or (e) Nrf2−3′-UTR and miR-93 mimic or mimic control. **P<0.01. (F) 293T cells were co-transfected with miR-93 mimic + TGF-β1−3′UTR-WT, miR-93 mimic + TGF-β1−3′-UTR-MUT, miR-93 mimic + TGF-β1-CDS, or miR-93 mimic + empty vector pcDNA 4.0. Under these different miR-93/TGF-β1 conditions, the expression of Nrf2 was assessed by measuring relative luciferase activity. Data are presented as the means ± SD of three independent experiments. *P<0.05 by Student's t-test. 3′UTR WT is the endogenous 3′-UTR sequence and 3′UTR MUT is the mutated 3′-UTR sequence. (G) The same experimental setup, measures and analyses were conducted as in (F), except with the miR-93 inhibitor. miR, microRNA; RT-qPCR, reverse transcription-quantitative PCR; TGF, transforming growth factor; Nrf2, nuclear factor erythroid 2-related factor 2; si, small interfering RNA; UTR, untranslated region; WT, wild type; MUT, mutant; NC, negative control; CDS, coding DNA sequence.
Figure 4. TGF-β1 competes with Nrf2 mRNA for binding to miR-93. (A) Expression of miR-93 in HMO6 cells of each group after transfection. The expression of miR-93 was significantly elevated in miR-93 mimics group and declined in miR-93 inhibitor group, **P<0.05 vs. control group. (B) Expression of TGF-β1 in HMO6 cells of each group after transfection. The expression of TGF-β1 was significantly declined in the siTGF-β1 group. *P<0.05 vs. control group. (C) Mutated nucleotides in the TGF-β1 3′-UTR sequence (indicated by the dotted line and red font) were generated in the seed region of miR-93 to abolish binding. The mutated sequence is labeled TGF-β1−3′-UTR-MUT. (D and E) A dual luciferase reporter assay was used to test whether TGF-β1 and Nrf2 were targets of miR-93. 293T cells were co-transfected with (d) TGF-β1−3′-UTR or (e) Nrf2−3′-UTR and miR-93 mimic or mimic control. **P<0.01. (F) 293T cells were co-transfected with miR-93 mimic + TGF-β1−3′UTR-WT, miR-93 mimic + TGF-β1−3′-UTR-MUT, miR-93 mimic + TGF-β1-CDS, or miR-93 mimic + empty vector pcDNA 4.0. Under these different miR-93/TGF-β1 conditions, the expression of Nrf2 was assessed by measuring relative luciferase activity. Data are presented as the means ± SD of three independent experiments. *P<0.05 by Student's t-test. 3′UTR WT is the endogenous 3′-UTR sequence and 3′UTR MUT is the mutated 3′-UTR sequence. (G) The same experimental setup, measures and analyses were conducted as in (F), except with the miR-93 inhibitor. miR, microRNA; RT-qPCR, reverse transcription-quantitative PCR; TGF, transforming growth factor; Nrf2, nuclear factor erythroid 2-related factor 2; si, small interfering RNA; UTR, untranslated region; WT, wild type; MUT, mutant; NC, negative control; CDS, coding DNA sequence.CC BY-NC-ND · PubMed Central
Figure 5. Schematic representation of TGF-β1 function as a ceRNA to regulate Nrf2 after ICH. The TGF-β1 3′-UTR acts as a ceRNA to compete with the Nrf2 3′-UTR for binding to the miR-93. Increased TGF-β1/miR-93 binding leaves Nrf2 mRNA free to be translated. Increased expression of the Nrf2 protein is neuroprotective after ICH. ceRNA, competitive endogenous RNA; ICH, intracerebral hemorrhage; TGF, transforming growth factor; Nrf2, nuclear factor erythroid 2-related factor 2; UTR, untranslated region; miRNA/miR, microRNA.
Figure 5. Schematic representation of TGF-β1 function as a ceRNA to regulate Nrf2 after ICH. The TGF-β1 3′-UTR acts as a ceRNA to compete with the Nrf2 3′-UTR for binding to the miR-93. Increased TGF-β1/miR-93 binding leaves Nrf2 mRNA free to be translated. Increased expression of the Nrf2 protein is neuroprotective after ICH. ceRNA, competitive endogenous RNA; ICH, intracerebral hemorrhage; TGF, transforming growth factor; Nrf2, nuclear factor erythroid 2-related factor 2; UTR, untranslated region; miRNA/miR, microRNA.CC BY-NC-ND · PubMed Central
Figure 6. Effects of manipulating miR-93 and TGF-β1 levels on Nrf2 expression and apoptosis. (A-C) Protein expression levels of TGF-β1 and Nrf2 in HMO6 cells transfected for 48 h with (A) miR-93 mimic, (B) miR-93 inhibitor or (C) siTGF-β1 were determined by western blotting. The negative controls in (A), (B), and (C) are mimic NC, inhibitor NC and scramble siRNA, respectively. Representative western blotting images and quantification of the group data are shown. (D) HMO6 cells were treated with 48 h of thrombin treatment (20 U/ml). Then, apoptotic cell death was measured by counting TUNEL-stained cells (red) after transfection with miR-93 mimic, miR-93 inhibitor or siTGF-β1. DAPI (blue) labels cell nuclei. Scale bar, 100 µm. (E) The bar graph quantifies the number of TUNEL-positive (TUNEL+) cells in the different groups as a percentage of total cells. The group data represent three separate experiments and are expressed as the means ± SD. *P<0.05 by Student's t-test. miR, microRNA; TGF, transforming growth factor; Nrf2, nuclear factor erythroid 2-related factor 2; si, small interfering RNA; NC, negative control.
Figure 6. Effects of manipulating miR-93 and TGF-β1 levels on Nrf2 expression and apoptosis. (A-C) Protein expression levels of TGF-β1 and Nrf2 in HMO6 cells transfected for 48 h with (A) miR-93 mimic, (B) miR-93 inhibitor or (C) siTGF-β1 were determined by western blotting. The negative controls in (A), (B), and (C) are mimic NC, inhibitor NC and scramble siRNA, respectively. Representative western blotting images and quantification of the group data are shown. (D) HMO6 cells were treated with 48 h of thrombin treatment (20 U/ml). Then, apoptotic cell death was measured by counting TUNEL-stained cells (red) after transfection with miR-93 mimic, miR-93 inhibitor or siTGF-β1. DAPI (blue) labels cell nuclei. Scale bar, 100 µm. (E) The bar graph quantifies the number of TUNEL-positive (TUNEL+) cells in the different groups as a percentage of total cells. The group data represent three separate experiments and are expressed as the means ± SD. *P<0.05 by Student's t-test. miR, microRNA; TGF, transforming growth factor; Nrf2, nuclear factor erythroid 2-related factor 2; si, small interfering RNA; NC, negative control.CC BY-NC-ND · PubMed Central

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Cited by

Metadata

Authors
Wang, H., Cao, X., Wen, X., Li, D., Ouyang, Y., Bao, B., Zhong, Y., Qin, Z., Yin, M., Chen, Z., & Yin, X.
Affiliations
  • Department of Neurology, The Affiliated Hospital of Jiujiang University, Jiujiang, Jiangxi 332000, P.R. China
  • Department of Neurology, Jiangxi Provincial People's Hospital, Nanchang, Jiangxi 330006, P.R. China
  • Department of Neurology, The Second Affiliated Hospital of Nanchang University, Nanchang, Jiangxi 330006, P.R. China
Venue
Molecular Medicine Reports
Publisher
Spandidos Publications
Published
2021-05-06
Volume
24
Issue
1
ISSN
  • 1791-2997
  • 1791-3004
DOI
10.3892/mmr.2021.12138
PMC
PMC8127068
Cited by
19
References
30

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