High Mobility Group Protein B1 (HMGB1) Interacts with Receptor for Advanced Glycation End Products (RAGE) to Promote Airway Smooth Muscle Cell Proliferation Through ERK and NF-B Pathways

Overview

Journal Int J Clin Exp Pathol

Specialty Pathology

Date 2020 Jan 15

PMID 31934170

Citations 7

Authors

Dongming Qu

Zhougui Ling

Xiaoyu Tan

Yan Chen

Qinghua Huang

Mengze Li

Tangjuan Liu

Changchun Hou

Yiqiang Chen

Affiliations

Soon will be listed here.

Abstract

Background: High-mobility graoup box protein 1 (HMGB1) has been shown to mediate a wide range of pathologic responses by interacting with RAGE (receptor for advanced glycation endproducts) and TLRs (Toll-like receptors). Our previous study showed that HMGB1 has been involved in pathogenesis of airway remodeling in an allergen-induced chronic mice asthma model. Increased airway smooth muscle (ASM) mass is a vital feature of airway remodeling.

Objective: To evaluate the effect of HMGB1 on proliferation of ASMs and the underlying mechanisms.

Methods: Rat airway smooth muscle cells (RASMs) were obtained by primary explant techniques. We investigated the effect of HMGB1 on the proliferation of RASMs. To identify which receptors and signaling pathways be involved in proliferation of RASMs, we performed western blot and CCK-8 assay by specific receptor blockade and inhibition of MAPK (p38, JNK and ERK) and NF-B signaling pathways.

Results: HMGB1 stimulated RASMs proliferation in a dose- and time-dependent manner and also increased proliferating cell nuclear antigen (PCNA) and RAGE expression of RASMs. The inhibitor of RAGE, but not TLR2 and TLR4, reversed HMGB1-induced RASM proliferation and PCNA expression. Incubation of RASMs with HMGB1 caused a rapid increase in P65 and ERK phosphorylation. RASM proliferation and PCNA expression toward HMGB1 were significantly inhibited by the inhibitors of ERK and NF-B.

Conclusion: HMGB1 induces proliferation of RASMs through a RAGE-dependent activation of ERK and NF-B signaling pathways.

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References

de Martin R, Hoeth M, Hofer-Warbinek R, Schmid J . The transcription factor NF-kappa B and the regulation of vascular cell function. Arterioscler Thromb Vasc Biol. 2000; 20(11):E83-8. DOI: 10.1161/01.atv.20.11.e83. View

Xu Y, Wang Y, Yin L, Peng L, Park G, Yang Y . S100A8 inhibits PDGF-induced proliferation of airway smooth muscle cells dependent on the receptor for advanced glycation end-products. Biol Res. 2017; 50(1):23. PMC: 5479006. DOI: 10.1186/s40659-017-0128-5. View

Degryse B, Bonaldi T, Scaffidi P, Muller S, Resnati M, Sanvito F . The high mobility group (HMG) boxes of the nuclear protein HMG1 induce chemotaxis and cytoskeleton reorganization in rat smooth muscle cells. J Cell Biol. 2001; 152(6):1197-206. PMC: 2199202. DOI: 10.1083/jcb.152.6.1197. View

Ediger T, Schulte N, Murphy T, Toews M . Transcription factor activation and mitogenic synergism in airway smooth muscle cells. Eur Respir J. 2003; 21(5):759-69. DOI: 10.1183/09031936.03.00075702. View

Park J, Svetkauskaite D, He Q, Kim J, Strassheim D, Ishizaka A . Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J Biol Chem. 2003; 279(9):7370-7. DOI: 10.1074/jbc.M306793200. View

Park J, Arcaroli J, Yum H, Yang H, Wang H, Yang K . Activation of gene expression in human neutrophils by high mobility group box 1 protein. Am J Physiol Cell Physiol. 2003; 284(4):C870-9. DOI: 10.1152/ajpcell.00322.2002. View

Hou C, Zhao H, Liu L, Li W, Zhou X, Lv Y . High mobility group protein B1 (HMGB1) in Asthma: comparison of patients with chronic obstructive pulmonary disease and healthy controls. Mol Med. 2011; 17(7-8):807-15. PMC: 3146613. DOI: 10.2119/molmed.2010.00173. View

Lotze M, Tracey K . High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol. 2005; 5(4):331-42. DOI: 10.1038/nri1594. View

Yang H, Rivera Z, Jube S, Nasu M, Bertino P, Goparaju C . Programmed necrosis induced by asbestos in human mesothelial cells causes high-mobility group box 1 protein release and resultant inflammation. Proc Natl Acad Sci U S A. 2010; 107(28):12611-6. PMC: 2906549. DOI: 10.1073/pnas.1006542107. View

10.

Porto A, Palumbo R, Pieroni M, Aprigliano G, Chiesa R, Sanvito F . Smooth muscle cells in human atherosclerotic plaques secrete and proliferate in response to high mobility group box 1 protein. FASEB J. 2006; 20(14):2565-6. DOI: 10.1096/fj.06-5867fje. View

11.

Guttridge D, Albanese C, Reuther J, Pestell R, Baldwin Jr A . NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol Cell Biol. 1999; 19(8):5785-99. PMC: 84428. DOI: 10.1128/MCB.19.8.5785. View

12.

Cheng W, Yan K, Chen Y, Zhang W, Ji Z, Dang C . ABCA1 inhibits PDGF-induced proliferation and migration of rat airway smooth muscle cell through blocking TLR2/NF-κB/NFATc1 signaling. J Cell Biochem. 2018; 119(9):7388-7396. DOI: 10.1002/jcb.27046. View

13.

Zabini D, Crnkovic S, Xu H, Tscherner M, Ghanim B, Klepetko W . High-mobility group box-1 induces vascular remodelling processes via c-Jun activation. J Cell Mol Med. 2015; 19(5):1151-61. PMC: 4420616. DOI: 10.1111/jcmm.12519. View

14.

Ott C, Jacobs K, Haucke E, Navarrete Santos A, Grune T, Simm A . Role of advanced glycation end products in cellular signaling. Redox Biol. 2014; 2:411-29. PMC: 3949097. DOI: 10.1016/j.redox.2013.12.016. View

15.

Bianchi M, Crippa M, Manfredi A, Mezzapelle R, Querini P, Venereau E . High-mobility group box 1 protein orchestrates responses to tissue damage via inflammation, innate and adaptive immunity, and tissue repair. Immunol Rev. 2017; 280(1):74-82. DOI: 10.1111/imr.12601. View

16.

Chen J, Zhang J, Xu L, Xu C, Chen S, Yang J . Inhibition of neointimal hyperplasia in the rat carotid artery injury model by a HMGB1 inhibitor. Atherosclerosis. 2012; 224(2):332-9. DOI: 10.1016/j.atherosclerosis.2012.07.020. View

17.

Zhou Z, Wang K, Penn M, Marso S, Lauer M, Forudi F . Receptor for AGE (RAGE) mediates neointimal formation in response to arterial injury. Circulation. 2003; 107(17):2238-43. DOI: 10.1161/01.CIR.0000063577.32819.23. View

18.

Jube S, Rivera Z, Bianchi M, Powers A, Wang E, Pagano I . Cancer cell secretion of the DAMP protein HMGB1 supports progression in malignant mesothelioma. Cancer Res. 2012; 72(13):3290-301. PMC: 3389268. DOI: 10.1158/0008-5472.CAN-11-3481. View

19.

Saglani S, Lloyd C . Novel concepts in airway inflammation and remodelling in asthma. Eur Respir J. 2015; 46(6):1796-804. DOI: 10.1183/13993003.01196-2014. View

20.

Xie S, Sukkar M, Issa R, Khorasani N, Chung K . Mechanisms of induction of airway smooth muscle hyperplasia by transforming growth factor-beta. Am J Physiol Lung Cell Mol Physiol. 2007; 293(1):L245-53. PMC: 1934553. DOI: 10.1152/ajplung.00068.2007. View