Transcription Factor P300 Regulated MiR-451b Weakens the Cigarette Smoke Extract-Induced Cellular Stress by Targeting RhoA/ROCK2 Signaling

Overview

Journal Oxid Med Cell Longev

Publisher Wiley

Specialties Cell Biology
Endocrinology

Date 2022 Oct 24

PMID 36275894

Authors

Wen Shen

Shukun Wang

Ruili Wang

Yang Zhang

Hong Tian

Xi Wang

Xin Wu

Xiaolei Yang

Wei Wei

Affiliations

Soon will be listed here.

Abstract

Background: A previous study identified miR-451b as a potential biomarker in smoker with or without chronic obstructive pulmonary disease (COPD). However, the function and molecular mechanisms of miR-451b in the pathogenesis of COPD remain elusive.

Methods: Macrophages and lung fibroblasts were exposed to 10% cigarette smoke extract (CSE) solution for 24 h. Expression miR-451b and its potential transcription factor p300 were detected. The association between p300 and miR-451b, miR-451b and RhoA was validated by luciferase reporter assay. The release of IL-12 and TNF-by macrophages was measured by ELISA assay, and Transwell assay was performed to analyze its migration and invasion. Collagen protein of fibroblasts was detected by Western blotting.

Results: Results showed that p300 and miR-451b was downregulated, while RhoA was upregulated in CSE-induced macrophages and lung fibroblasts. The stimulation of CSE promoted the degradation of p300 by ubiquitination, and RhoA was confirmed as the target gene of miR-451b. MiR-451b overexpression significantly decreased the release of IL-12 and TNF-, downregulated the expression of RhoA, ROCK2, and p65, and suppressed cell migration and invasion in CES-induced macrophages. In addition, miR-451b overexpression decreased the expression of RhoA, ROCK2, COL1A1, and COL2A1 in lung fibroblasts.

Conclusions: Our data suggest that p300/miR-451b protects against CSE-induced cell stress possibly through downregulating RhoA/ROCK2 pathway.

Citing Articles

Evaluation of nanoparticle albumin-bound paclitaxel loaded macrophages for glioblastoma treatment based on a microfluidic chip.

Xie Z, Ye J, Gao X, Chen H, Chen M, Lian J Front Bioeng Biotechnol. 2024; 12:1361682.

PMID: 38562665 PMC: 10982336. DOI: 10.3389/fbioe.2024.1361682.

Activation of RhoA/ROCK2 signaling by hypoxia-inducible factor 1α in promoting tumor growth and metastasis in human colon cancer.

Du K, Wang P, Liu J, Ren J, Zheng G, Li S J Gastrointest Oncol. 2024; 15(1):237-249.

PMID: 38482232 PMC: 10932655. DOI: 10.21037/jgo-23-844.

References

Martey C, Pollock S, Turner C, OReilly K, Baglole C, Phipps R . Cigarette smoke induces cyclooxygenase-2 and microsomal prostaglandin E2 synthase in human lung fibroblasts: implications for lung inflammation and cancer. Am J Physiol Lung Cell Mol Physiol. 2004; 287(5):L981-91. DOI: 10.1152/ajplung.00239.2003. View

Conickx G, Avila Cobos F, van den Berge M, Faiz A, Timens W, Hiemstra P . microRNA profiling in lung tissue and bronchoalveolar lavage of cigarette smoke-exposed mice and in COPD patients: a translational approach. Sci Rep. 2017; 7(1):12871. PMC: 5634489. DOI: 10.1038/s41598-017-13265-8. View

Shigemura M, Lecuona E, Angulo M, Homma T, Rodriguez D, Gonzalez-Gonzalez F . Hypercapnia increases airway smooth muscle contractility via caspase-7-mediated miR-133a-RhoA signaling. Sci Transl Med. 2018; 10(457). PMC: 6889079. DOI: 10.1126/scitranslmed.aat1662. View

Rolle K, Piwecka M, Belter A, Wawrzyniak D, Jeleniewicz J, Barciszewska M . The Sequence and Structure Determine the Function of Mature Human miRNAs. PLoS One. 2016; 11(3):e0151246. PMC: 4816427. DOI: 10.1371/journal.pone.0151246. View

Etienne-Manneville S, Hall A . Rho GTPases in cell biology. Nature. 2002; 420(6916):629-35. DOI: 10.1038/nature01148. View

Carnevali S, Petruzzelli S, Longoni B, Vanacore R, Barale R, Cipollini M . Cigarette smoke extract induces oxidative stress and apoptosis in human lung fibroblasts. Am J Physiol Lung Cell Mol Physiol. 2003; 284(6):L955-63. DOI: 10.1152/ajplung.00466.2001. View

Sato T, Liu X, Nelson A, Nakanishi M, Kanaji N, Wang X . Reduced miR-146a increases prostaglandin E₂in chronic obstructive pulmonary disease fibroblasts. Am J Respir Crit Care Med. 2010; 182(8):1020-9. PMC: 2970844. DOI: 10.1164/rccm.201001-0055OC. View

Long Y, Liu X, Chen S, Zong D, Chen Y, Chen P . miR-34a is involved in CSE-induced apoptosis of human pulmonary microvascular endothelial cells by targeting Notch-1 receptor protein. Respir Res. 2018; 19(1):21. PMC: 5787261. DOI: 10.1186/s12931-018-0722-2. View

Paul S, Ruiz-Manriquez L, Ambriz-Gonzalez H, Medina-Gomez D, Valenzuela-Coronado E, Moreno-Gomez P . Impact of smoking-induced dysregulated human miRNAs in chronic disease development and their potential use in prognostic and therapeutic purposes. J Biochem Mol Toxicol. 2022; 36(9):e23134. DOI: 10.1002/jbt.23134. View

10.

Zhang C, Qin S, Qin L, Liu L, Sun W, Li X . Cigarette smoke extract-induced p120-mediated NF-κB activation in human epithelial cells is dependent on the RhoA/ROCK pathway. Sci Rep. 2016; 6:23131. PMC: 5009380. DOI: 10.1038/srep23131. View

11.

Barnes P . New anti-inflammatory targets for chronic obstructive pulmonary disease. Nat Rev Drug Discov. 2013; 12(7):543-59. DOI: 10.1038/nrd4025. View

12.

Shen W, Liu J, Zhao G, Fan M, Song G, Zhang Y . Repression of Toll-like receptor-4 by microRNA-149-3p is associated with smoking-related COPD. Int J Chron Obstruct Pulmon Dis. 2017; 12:705-715. PMC: 5327902. DOI: 10.2147/COPD.S128031. View

13.

Bei Y, Duong-Quy S, Hua-Huy T, Dao P, Le-Dong N, Dinh-Xuan A . Activation of RhoA/Rho-kinase pathway accounts for pulmonary endothelial dysfunction in patients with chronic obstructive pulmonary disease. Physiol Rep. 2013; 1(5):e00105. PMC: 3841041. DOI: 10.1002/phy2.105. View

14.

Zhang L, Huang C, Guo Y, Gou X, Hinsdale M, Lloyd P . MicroRNA-26b Modulates the NF-κB Pathway in Alveolar Macrophages by Regulating PTEN. J Immunol. 2015; 195(11):5404-14. PMC: 4655123. DOI: 10.4049/jimmunol.1402933. View

15.

Kara M, Kirkil G, Kalemci S . Differential Expression of MicroRNAs in Chronic Obstructive Pulmonary Disease. Adv Clin Exp Med. 2016; 25(1):21-6. DOI: 10.17219/acem/28343. View

16.

Xu J, Tao B, Guo X, Zhou S, Li Y, Zhang Y . Macrophage-Restricted Shp2 Tyrosine Phosphatase Acts as a Rheostat for MMP12 through TGF-β Activation in the Prevention of Age-Related Emphysema in Mice. J Immunol. 2017; 199(7):2323-2332. DOI: 10.4049/jimmunol.1601696. View

17.

Khatiwala C, Kim P, Peyton S, Putnam A . ECM compliance regulates osteogenesis by influencing MAPK signaling downstream of RhoA and ROCK. J Bone Miner Res. 2008; 24(5):886-98. PMC: 2672206. DOI: 10.1359/jbmr.081240. View

18.

. Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990-2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet. 2016; 388(10053):1545-1602. PMC: 5055577. DOI: 10.1016/S0140-6736(16)31678-6. View

19.

Tang K, Zhao J, Xie J, Wang J . Decreased miR-29b expression is associated with airway inflammation in chronic obstructive pulmonary disease. Am J Physiol Lung Cell Mol Physiol. 2019; 316(4):L621-L629. DOI: 10.1152/ajplung.00436.2018. View

20.

Yang S, Chida A, Bauter M, Shafiq N, Seweryniak K, Maggirwar S . Cigarette smoke induces proinflammatory cytokine release by activation of NF-kappaB and posttranslational modifications of histone deacetylase in macrophages. Am J Physiol Lung Cell Mol Physiol. 2006; 291(1):L46-57. DOI: 10.1152/ajplung.00241.2005. View