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miR-212-3p attenuates neuroinflammation of rats with Alzheimer's disease via regulating the SP1/BACE1/NLRP3/Caspase-1 signaling pathway

Nong, Wei, Bao, Chuanhong, Chen, Yixin, Wei, Zhiquan·2022·Bosnian Journal of Basic Medical Sciences
DOI 10.17305/bjbms.2021.6723PMC PMC9392983
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Abstract

Alzheimer's disease (AD) ranks as the leading cause of dementia. MicroRNA (miR)-212-3p has been identified to exert neuroprotective effects on brain disorders. The current study analyzed the protective role of miR-212-3p in AD rats via regulating the nucleotide-binding oligomerization domain-like receptor family pyrin domain containing 3 (NLRP3)/Caspase-1 signaling pathway. The AD rat model was established via injection of amyloid-β 1-42 (Aβ1-42), followed by the Morris water maze test. The morphology and functions of neurons were observed. Furthermore, miR-212-3p, NLRP3, cleaved Caspase-1, gasdermin D N-terminus, interleukin (IL)-1β and IL-18 expressions were measured. H19-7 cells were treated with Aβ1-42 to establish the AD cell model, followed by an assessment of cell viability and pyroptosis. Downstream targets of miR-212-3p and specificity protein 1 (SP1), as well as beta-site amyloid precursor protein cleaving enzyme 1 (BACE1) were predicted by databases and testified using dual-luciferase and chromatin immunoprecipitation assays. miR-212-3p was weakly expressed in AD rats. miR-212-3p overexpression was linked to improved learning and memory capacities of AD rats and reduced neuronal pyroptosis linked to neuroinflammation attenuation. In vitro, miR-212-3p improved viability and suppressed pyroptosis of neurons via inhibiting NLRP3/Caspase-1. Overall, miR-212-3p inhibited SP1 expression to block BACE1-induced activation of NLRP3/Caspase-1, thereby attenuating neuroinflammation of AD rats.

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FIGURE 1 miR-212-3p was weakly expressed in AD rats and miR-212-3p overexpression improved neurological functions of AD rats. The AD rat model was established through injection of Aβ1-42, followed by the treatment of miR-212-3p agomir. (A) miR-212-3p expression in the hippocampus was detected through RT-qPCR; (B-D) animal’s learning and memory capacities were assessed through MWMT; (E and F) morphology and functions of neurons were observed through H&E staining (E) and Nissl’s staining (F). N=6. Data were formalized as mean ± SD. Data in Figures A and C-F were analyzed using one-way ANOVA, and data in Figure B were analyzed using two-way ANOVA, followed by Tukey’s multiple comparison test.
FIGURE 1 miR-212-3p was weakly expressed in AD rats and miR-212-3p overexpression improved neurological functions of AD rats. The AD rat model was established through injection of Aβ1-42, followed by the treatment of miR-212-3p agomir. (A) miR-212-3p expression in the hippocampus was detected through RT-qPCR; (B-D) animal’s learning and memory capacities were assessed through MWMT; (E and F) morphology and functions of neurons were observed through H&E staining (E) and Nissl’s staining (F). N=6. Data were formalized as mean ± SD. Data in Figures A and C-F were analyzed using one-way ANOVA, and data in Figure B were analyzed using two-way ANOVA, followed by Tukey’s multiple comparison test.CC BY · PubMed Central
FIGURE 2 miR-212-3p overexpression suppressed NLRP3/Caspase-1-activated neuronal pyroptosis to attenuate neuroinflammation of AD rats. (A) NLRP3, cleaved Caspase-1, and GSDMD-N expressions were determined through Western blot analysis; IL-1β and IL-18 levels were measured through Western blot analysis (B) and ELISA (C). N=6. Data were formalized as mean ± SD. Data were analyzed using two-way ANOVA, followed by Tukey’s multiple comparison test.
FIGURE 2 miR-212-3p overexpression suppressed NLRP3/Caspase-1-activated neuronal pyroptosis to attenuate neuroinflammation of AD rats. (A) NLRP3, cleaved Caspase-1, and GSDMD-N expressions were determined through Western blot analysis; IL-1β and IL-18 levels were measured through Western blot analysis (B) and ELISA (C). N=6. Data were formalized as mean ± SD. Data were analyzed using two-way ANOVA, followed by Tukey’s multiple comparison test.CC BY · PubMed Central
FIGURE 3 miR-212-3p overexpression inhibited NLRP3/Caspase-1-activated neuronal pyroptosis in vitro post-Aβ1-42 treatment. (A) miR-212-3p expression was detected through RT-qPCR after the AD cell model was established using Aβ1-42 treatment with H19-7 cells; (B) miR-212-3p expression was detected through RT-qPCR after transfection of mimic NC and miR-212-3p mimic; (C) cell viability was assessed through the MTT method; (D) NLRP3, cleaved Caspase-1, and GSDMD-N expressions were determined through Western blot analysis; (E and F) IL-1β and IL-18 levels were measured through Western blot analysis (E) and ELISA (F); cell experiments were conducted 3 times. Data were formalized as mean ± SD. Data in Figures A and B were analyzed using T test, data in Figure C were analyzed using one-way ANOVA, and data in Figures D-F were analyzed using two-way ANOVA, followed by Tukey’s multiple comparison test.
FIGURE 3 miR-212-3p overexpression inhibited NLRP3/Caspase-1-activated neuronal pyroptosis in vitro post-Aβ1-42 treatment. (A) miR-212-3p expression was detected through RT-qPCR after the AD cell model was established using Aβ1-42 treatment with H19-7 cells; (B) miR-212-3p expression was detected through RT-qPCR after transfection of mimic NC and miR-212-3p mimic; (C) cell viability was assessed through the MTT method; (D) NLRP3, cleaved Caspase-1, and GSDMD-N expressions were determined through Western blot analysis; (E and F) IL-1β and IL-18 levels were measured through Western blot analysis (E) and ELISA (F); cell experiments were conducted 3 times. Data were formalized as mean ± SD. Data in Figures A and B were analyzed using T test, data in Figure C were analyzed using one-way ANOVA, and data in Figures D-F were analyzed using two-way ANOVA, followed by Tukey’s multiple comparison test.CC BY · PubMed Central
FIGURE 4 miR-212-3p negatively regulated SP1 expression. (A) The binding of miR-212-3p and SP1 was predicted by the Jefferson website (https://cm.jefferson.edu/rna22/Interactive/RNA22Controller); (B) the binding relationship of miR-212-3p and SP1 was testified dual-luciferase reporter assay; (C and D) SP1 expression in the hippocampus was detected through RT-qPCR (C) and Western blot analysis (D); (E and F) SP1 expression in H19-7 cells was detected through RT-qPCR (E) and Western blot analysis (F). N=6. Cell experiments were repeated 3 times. Data were formalized as mean ± SD. Data in Figure B were analyzed using two-way ANOVA and data in Figures C-F were analyzed using one-way ANOVA, followed by Tukey’s multiple comparison test.
FIGURE 4 miR-212-3p negatively regulated SP1 expression. (A) The binding of miR-212-3p and SP1 was predicted by the Jefferson website (https://cm.jefferson.edu/rna22/Interactive/RNA22Controller); (B) the binding relationship of miR-212-3p and SP1 was testified dual-luciferase reporter assay; (C and D) SP1 expression in the hippocampus was detected through RT-qPCR (C) and Western blot analysis (D); (E and F) SP1 expression in H19-7 cells was detected through RT-qPCR (E) and Western blot analysis (F). N=6. Cell experiments were repeated 3 times. Data were formalized as mean ± SD. Data in Figure B were analyzed using two-way ANOVA and data in Figures C-F were analyzed using one-way ANOVA, followed by Tukey’s multiple comparison test.CC BY · PubMed Central
FIGURE 5 SP1 promoted BACE1 transcription. (A) The binding of SP1 and BACE1 promoter region was predicted through the JASPAR website (http://jaspar.genereg.net/analysis); (B-C) the binding of SP1 and BACE1 promoter region was testified through ChIP (B) and dual-luciferase reporter assay (C); (D) BACE1 expression in the hippocampus was detected through RT-qPCR; (E and F) SP1 expression in cells was determined through RT-qPCR (E) and Western blot analysis (F) on H19-7 cells which were transfected oe-NC and oe-SP1; (G) BACE1 expression in H19-7 cells was determined through RT-qPCR on Aβ1-42-treated H19-7 cells which were transfected with miR-212-3p mimic and oe-SP1. N=6. Cell experiments were conducted 3 times. Data were formalized as mean ± SD. Data in Figures B and D-F were analyzed using T test and data in Figures C and G were analyzed using two-way ANOVA, followed by Tukey’s multiple comparison test.
FIGURE 5 SP1 promoted BACE1 transcription. (A) The binding of SP1 and BACE1 promoter region was predicted through the JASPAR website (http://jaspar.genereg.net/analysis); (B-C) the binding of SP1 and BACE1 promoter region was testified through ChIP (B) and dual-luciferase reporter assay (C); (D) BACE1 expression in the hippocampus was detected through RT-qPCR; (E and F) SP1 expression in cells was determined through RT-qPCR (E) and Western blot analysis (F) on H19-7 cells which were transfected oe-NC and oe-SP1; (G) BACE1 expression in H19-7 cells was determined through RT-qPCR on Aβ1-42-treated H19-7 cells which were transfected with miR-212-3p mimic and oe-SP1. N=6. Cell experiments were conducted 3 times. Data were formalized as mean ± SD. Data in Figures B and D-F were analyzed using T test and data in Figures C and G were analyzed using two-way ANOVA, followed by Tukey’s multiple comparison test.CC BY · PubMed Central
FIGURE 6 BACE1 upregulation activated NLRP3/Caspase-1 signaling pathway to reverse the inhibitory role of miR-212-3p overexpression in neuronal pyroptosis. (A) BACE1 was detected through RT-qPCR after H19-7 cells were transfected with oe-NC and oe-BACE1; (B) cell viability was assessed through the MTT method after Aβ1-42-treated H19-7 cells were transfected miR-212-3p mimic and oe-BACE1; (C) NLRP3, cleaved Caspase-1, and GSDMD-N expressions were determined through Western blot analysis; (D-E) IL-1β and IL-18 levels were measured through Western blot analysis (D) and ELISA (E). Cell experiments were conducted 3 times. Data were formalized as mean ± SD. Data in Figures A were analyzed using T test, data in Figure B were analyzed using one-way ANOVA, and data in Figures C-E were analyzed using two-way ANOVA, followed by Tukey’s multiple comparison test.
FIGURE 6 BACE1 upregulation activated NLRP3/Caspase-1 signaling pathway to reverse the inhibitory role of miR-212-3p overexpression in neuronal pyroptosis. (A) BACE1 was detected through RT-qPCR after H19-7 cells were transfected with oe-NC and oe-BACE1; (B) cell viability was assessed through the MTT method after Aβ1-42-treated H19-7 cells were transfected miR-212-3p mimic and oe-BACE1; (C) NLRP3, cleaved Caspase-1, and GSDMD-N expressions were determined through Western blot analysis; (D-E) IL-1β and IL-18 levels were measured through Western blot analysis (D) and ELISA (E). Cell experiments were conducted 3 times. Data were formalized as mean ± SD. Data in Figures A were analyzed using T test, data in Figure B were analyzed using one-way ANOVA, and data in Figures C-E were analyzed using two-way ANOVA, followed by Tukey’s multiple comparison test.CC BY · PubMed Central
FIGURE 7 Molecular mechanism of miR-212-3p in AD-induced neuroinflammation. SP1 bounds to the BACE1 promoter region to activate BACE1 expression. miR-212-3p inhibited SP1 and then BACE1 to block the activation of the NLRP3/Caspase-1 signaling pathway, thus attenuating neuroinflammation in AD rats.
FIGURE 7 Molecular mechanism of miR-212-3p in AD-induced neuroinflammation. SP1 bounds to the BACE1 promoter region to activate BACE1 expression. miR-212-3p inhibited SP1 and then BACE1 to block the activation of the NLRP3/Caspase-1 signaling pathway, thus attenuating neuroinflammation in AD rats.CC BY · PubMed Central

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Metadata

Authors
Nong, W., Bao, C., Chen, Y., & Wei, Z.
ORCID
Wei, Zhiquan
Venue
Bosnian Journal of Basic Medical Sciences
Publisher
Association of Basic Medical Sciences of FBIH
Published
2022-02-12
ISSN
  • 1840-4812
  • 1512-8601
DOI
10.17305/bjbms.2021.6723
PMC
PMC9392983
Cited by
14
References
5
Licence
creativecommons.org/licenses/by/4.0 (unspecified)

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