Lipidomics Revealed Aberrant Lipid Metabolism Caused by Inflammation in Cardiac Tissue in the Early Stage of Systemic Lupus Erythematosus in a Murine Model
Cardiac involvement, displayed as premature cardiovascular disease (CVD), is one of common clinical symptoms of patients with systemic lupus erythematosus (SLE), contributing to mortality of the disease. The precise underlying pathological mechanism(s) for the cardiac involvement in lupus remains po...
Main Authors: | , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
MDPI AG
2022-05-01
|
Series: | Metabolites |
Subjects: | |
Online Access: | https://www.mdpi.com/2218-1989/12/5/415 |
_version_ | 1797497957781602304 |
---|---|
author | Jida Zhang Lu Lu Xiaoyu Tian Kaili Wang Guanqun Xie Haichang Li Chengping Wen Changfeng Hu |
author_facet | Jida Zhang Lu Lu Xiaoyu Tian Kaili Wang Guanqun Xie Haichang Li Chengping Wen Changfeng Hu |
author_sort | Jida Zhang |
collection | DOAJ |
description | Cardiac involvement, displayed as premature cardiovascular disease (CVD), is one of common clinical symptoms of patients with systemic lupus erythematosus (SLE), contributing to mortality of the disease. The precise underlying pathological mechanism(s) for the cardiac involvement in lupus remains poorly understood. Lipids and their metabolites are directly involved in atherosclerosis development, oxidative stress, and inflammation, which are closely related to the development of CVD. In the study, shotgun lipidomics was exploited to quantitatively analyze cellular lipidomes in the cardiac tissue of MRL/lpr mice at two different time points (i.e., pre-lupus and lupus state) with/without treatment with glucocorticoids (GCs). Urine protein, spleen index, and renal histopathological evaluation of the mice were also performed for assessment of SLE onset and/or outcome. Lipidomics analysis revealed that the deposition of cholesterol and the aberrant metabolism of lipids caused by the increased energy metabolism and the enhanced activation of phospholipases, both of which were originally induced by inflammation, were already present in cardiac tissues from lupus-prone mice even at pre-lupus state. These lipid alterations could further induce inflammation and autoimmune responses, accelerating the process of CVD. In addition, the present study also demonstrated that GCs therapy could not only delay the progression of SLE, but also partially corrected these alterations of lipid species in cardiac tissue due to their anti-inflammatory effect. Thus, the medications with better anti-inflammatory effect might be a useful therapeutic method for premature CVD of SLE. |
first_indexed | 2024-03-10T03:26:33Z |
format | Article |
id | doaj.art-f78f92cec7da4dcba09b869435ad0d42 |
institution | Directory Open Access Journal |
issn | 2218-1989 |
language | English |
last_indexed | 2024-03-10T03:26:33Z |
publishDate | 2022-05-01 |
publisher | MDPI AG |
record_format | Article |
series | Metabolites |
spelling | doaj.art-f78f92cec7da4dcba09b869435ad0d422023-11-23T12:07:05ZengMDPI AGMetabolites2218-19892022-05-0112541510.3390/metabo12050415Lipidomics Revealed Aberrant Lipid Metabolism Caused by Inflammation in Cardiac Tissue in the Early Stage of Systemic Lupus Erythematosus in a Murine ModelJida Zhang0Lu Lu1Xiaoyu Tian2Kaili Wang3Guanqun Xie4Haichang Li5Chengping Wen6Changfeng Hu7College of Basic Medical Sciences, Zhejiang Chinese Medical University, 548 Bingwen Road, Hangzhou 310053, ChinaThird Clinical Medical College, Zhejiang Chinese Medical University, 548 Bingwen Road, Hangzhou 310053, ChinaCollege of Basic Medical Sciences, Zhejiang Chinese Medical University, 548 Bingwen Road, Hangzhou 310053, ChinaCollege of Basic Medical Sciences, Zhejiang Chinese Medical University, 548 Bingwen Road, Hangzhou 310053, ChinaCollege of Basic Medical Sciences, Zhejiang Chinese Medical University, 548 Bingwen Road, Hangzhou 310053, ChinaCollege of Basic Medical Sciences, Zhejiang Chinese Medical University, 548 Bingwen Road, Hangzhou 310053, ChinaCollege of Basic Medical Sciences, Zhejiang Chinese Medical University, 548 Bingwen Road, Hangzhou 310053, ChinaCollege of Basic Medical Sciences, Zhejiang Chinese Medical University, 548 Bingwen Road, Hangzhou 310053, ChinaCardiac involvement, displayed as premature cardiovascular disease (CVD), is one of common clinical symptoms of patients with systemic lupus erythematosus (SLE), contributing to mortality of the disease. The precise underlying pathological mechanism(s) for the cardiac involvement in lupus remains poorly understood. Lipids and their metabolites are directly involved in atherosclerosis development, oxidative stress, and inflammation, which are closely related to the development of CVD. In the study, shotgun lipidomics was exploited to quantitatively analyze cellular lipidomes in the cardiac tissue of MRL/lpr mice at two different time points (i.e., pre-lupus and lupus state) with/without treatment with glucocorticoids (GCs). Urine protein, spleen index, and renal histopathological evaluation of the mice were also performed for assessment of SLE onset and/or outcome. Lipidomics analysis revealed that the deposition of cholesterol and the aberrant metabolism of lipids caused by the increased energy metabolism and the enhanced activation of phospholipases, both of which were originally induced by inflammation, were already present in cardiac tissues from lupus-prone mice even at pre-lupus state. These lipid alterations could further induce inflammation and autoimmune responses, accelerating the process of CVD. In addition, the present study also demonstrated that GCs therapy could not only delay the progression of SLE, but also partially corrected these alterations of lipid species in cardiac tissue due to their anti-inflammatory effect. Thus, the medications with better anti-inflammatory effect might be a useful therapeutic method for premature CVD of SLE.https://www.mdpi.com/2218-1989/12/5/415systemic lupus erythematosuslipidomicsinflammationpremature cardiovascular diseaseglucocorticoids |
spellingShingle | Jida Zhang Lu Lu Xiaoyu Tian Kaili Wang Guanqun Xie Haichang Li Chengping Wen Changfeng Hu Lipidomics Revealed Aberrant Lipid Metabolism Caused by Inflammation in Cardiac Tissue in the Early Stage of Systemic Lupus Erythematosus in a Murine Model Metabolites systemic lupus erythematosus lipidomics inflammation premature cardiovascular disease glucocorticoids |
title | Lipidomics Revealed Aberrant Lipid Metabolism Caused by Inflammation in Cardiac Tissue in the Early Stage of Systemic Lupus Erythematosus in a Murine Model |
title_full | Lipidomics Revealed Aberrant Lipid Metabolism Caused by Inflammation in Cardiac Tissue in the Early Stage of Systemic Lupus Erythematosus in a Murine Model |
title_fullStr | Lipidomics Revealed Aberrant Lipid Metabolism Caused by Inflammation in Cardiac Tissue in the Early Stage of Systemic Lupus Erythematosus in a Murine Model |
title_full_unstemmed | Lipidomics Revealed Aberrant Lipid Metabolism Caused by Inflammation in Cardiac Tissue in the Early Stage of Systemic Lupus Erythematosus in a Murine Model |
title_short | Lipidomics Revealed Aberrant Lipid Metabolism Caused by Inflammation in Cardiac Tissue in the Early Stage of Systemic Lupus Erythematosus in a Murine Model |
title_sort | lipidomics revealed aberrant lipid metabolism caused by inflammation in cardiac tissue in the early stage of systemic lupus erythematosus in a murine model |
topic | systemic lupus erythematosus lipidomics inflammation premature cardiovascular disease glucocorticoids |
url | https://www.mdpi.com/2218-1989/12/5/415 |
work_keys_str_mv | AT jidazhang lipidomicsrevealedaberrantlipidmetabolismcausedbyinflammationincardiactissueintheearlystageofsystemiclupuserythematosusinamurinemodel AT lulu lipidomicsrevealedaberrantlipidmetabolismcausedbyinflammationincardiactissueintheearlystageofsystemiclupuserythematosusinamurinemodel AT xiaoyutian lipidomicsrevealedaberrantlipidmetabolismcausedbyinflammationincardiactissueintheearlystageofsystemiclupuserythematosusinamurinemodel AT kailiwang lipidomicsrevealedaberrantlipidmetabolismcausedbyinflammationincardiactissueintheearlystageofsystemiclupuserythematosusinamurinemodel AT guanqunxie lipidomicsrevealedaberrantlipidmetabolismcausedbyinflammationincardiactissueintheearlystageofsystemiclupuserythematosusinamurinemodel AT haichangli lipidomicsrevealedaberrantlipidmetabolismcausedbyinflammationincardiactissueintheearlystageofsystemiclupuserythematosusinamurinemodel AT chengpingwen lipidomicsrevealedaberrantlipidmetabolismcausedbyinflammationincardiactissueintheearlystageofsystemiclupuserythematosusinamurinemodel AT changfenghu lipidomicsrevealedaberrantlipidmetabolismcausedbyinflammationincardiactissueintheearlystageofsystemiclupuserythematosusinamurinemodel |