Basic Study
Copyright ©The Author(s) 2021. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Diabetes. Nov 15, 2021; 12(11): 1875-1893
Published online Nov 15, 2021. doi: 10.4239/wjd.v12.i11.1875
Profilin-1 is involved in macroangiopathy induced by advanced glycation end products via vascular remodeling and inflammation
Zhi-Lin Xiao, Li-Ping Ma, Da-Feng Yang, Mei Yang, Zhen-Yu Li, Mei-Fang Chen
Zhi-Lin Xiao, Mei Yang, Zhen-Yu Li, Mei-Fang Chen, Department of Geriatric Cardiology, National Clinical Research Center for Geriatric Disorders, Xiangya Hospital, Central South University, Changsha 410008, Hunan Province, China
Li-Ping Ma, Department of Cardiology, Shandong Provincial Qianfoshan Hospital, Shandong University, Jinan 250014, Shandong Province, China
Da-Feng Yang, Department of Cardiovascular Surgery, The Second Xiangya Hospital, Central South University, Changsha 410011, Hunan Province, China
Author contributions: Chen MF contributed to the conception and design of the study, and reviewed and edited the manuscript; Xiao ZL analyzed and interpreted the data, and wrote the original draft; Ma LP was responsible for animal experiments; Yang DF was responsible for clinical trials; Yang M was responsible for cell-based experiments; Li ZY had important intellectual contributions to the manuscript; all authors have read and approved the final manuscript.
Supported by the National Natural Science Foundation of China, No. 81000140, No. 81770358, and No. 82000339; Natural Science Foundation of Hunan Province, No. 2017JJ3486; and the Fund for Health Care in Hunan Province, No. B2017-01.
Institutional review board statement: The study was reviewed and approved by the Institutional Review Board of Xiangya Hospital, Central South University (Approval No. 202004051).
Institutional animal care and use committee statement: All procedures were performed in compliance with guidelines from the Ethics Committee for Animal Care and Research at Xiangya Hospital of Central South University (Changsha, Hunan Province, China).
Conflict-of-interest statement: The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Data sharing statement: The analyzed data sets generated during the present study are available from the corresponding author on reasonable request.
ARRIVE guidelines statement: The authors have read the ARRIVE Guidelines, and the manuscript was prepared and revised according to the ARRIVE Guidelines.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Mei-Fang Chen, MD, PhD, Associate Professor, Department of Geriatric Cardiology, National Clinical Research Center for Geriatric Disorders, Xiangya Hospital, Central South University, No. 87 Xiangya Road, Kaifu District, Changsha 410008, Hunan Province, China. meifang121@sohu.com
Received: May 26, 2021
Peer-review started: May 26, 2021
First decision: June 16, 2021
Revised: June 29, 2021
Accepted: August 20, 2021
Article in press: August 20, 2021
Published online: November 15, 2021
Processing time: 173 Days and 6.6 Hours
Abstract
BACKGROUND

The accumulation of advanced glycation end products (AGEs) have been implicated in the development and progression of diabetic vasculopathy. However, the role of profilin-1 as a multifunctional actin-binding protein in AGEs-induced atherosclerosis (AS) is largely unknown.

AIM

To explore the potential role of profilin-1 in the pathogenesis of AS induced by AGEs, particularly in relation to the Janus kinase 2 (JAK2) and signal transducer and activator of transcription 3 (STAT3) signaling pathway.

METHODS

Eighty-nine individuals undergoing coronary angiography were enrolled in the study. Plasma cytokine levels were detected using ELISA kits. Rat aortic vascular smooth muscle cells (RASMCs) were incubated with different compounds for different times. Cell proliferation was determined by performing the MTT assay and EdU staining. An AGEs-induced vascular remodeling model was established in rats and histological and immunohistochemical analyses were performed. The mRNA and protein levels were detected using real-time PCR and Western blot analysis, respectively. In vivo, shRNA transfection was performed to verify the role of profilin-1 in AGEs-induced proatherogenic mediator release and aortic remodeling. Statistical analyses were performed using SPSS 22.0 software.

RESULTS

Compared with the control group, plasma levels of profilin-1 and receptor for AGEs (RAGE) were significantly increased in patients with coronary artery disease, especially in those complicated with diabetes mellitus (P < 0.01). The levels of profilin-1 were positively correlated with the levels of RAGE (P < 0.01); additionally, the levels of both molecules were positively associated with the degree of coronary artery stenosis (P < 0.01). In vivo, tail vein injections of AGEs induced the release of proatherogenic mediators, such as asymmetric dimethylarginine, intercellular adhesion molecule-1, and the N-terminus of procollagen III peptide, concomitant with apparent aortic morphological changes and significantly upregulated expression of the profilin-1 mRNA and protein in the thoracic aorta (P < 0.05 or P < 0.01). Downregulation of profilin-1 expression with an shRNA significantly attenuated AGEs-induced proatherogenic mediator release (P < 0.05) and aortic remodeling. In vitro, incubation of vascular smooth muscle cells (VSMCs) with AGEs significantly promoted cell proliferation and upregulated the expression of the profilin-1 mRNA and protein (P < 0.05). AGEs (200 μg/mL, 24 h) significantly upregulated the expression of the STAT3 mRNA and protein and JAK2 protein, which was blocked by a JAK2 inhibitor (T3042-1) and/or STAT3 inhibitor (T6308-1) (P < 0.05). In addition, pretreatment with T3042-1 or T6308-1 significantly inhibited AGEs-induced RASMC proliferation (P < 0.05).

CONCLUSION

AGEs induce proatherogenic events such as VSMC proliferation, proatherogenic mediator release, and vascular remodeling, changes that can be attenuated by silencing profilin-1 expression. These results suggest a crucial role for profilin-1 in AGEs-induced vasculopathy.

Keywords: Advanced glycation end products; Profilin-1; Diabetic macroangiopathy; Atherosclerosis; Vascular remodeling; Janus kinase 2/signal transducer and activator of transcription 3 signaling pathway

Core Tip: The formation and accumulation of advanced glycation end products (AGEs) contribute to accelerated macrovascular complications in individuals with diabetes. Currently, few studies have examined the role of profilin-1 in vasculopathy induced by AGEs. The present study proved that AGEs induced proatherogenic events such as vascular smooth muscle cell proliferation, proatherogenic mediator expression, and vascular remodeling, changes that were attenuated by silencing profilin-1 gene expression. These data suggested for the first time that profilin-1 was involved in AGEs-induced aortic atheroma formation in rats, indicating that drugs targeting profilin-1 may become a potential therapeutic strategy for ameliorating atherosclerosis secondary to diabetes.