Time-Course Lipidomics of Ornithine-Induced Severe Acute Pancreatitis Model Reveals the Free Fatty Acids Centered Lipids Dysregulation Characteristics

The relationship between the type and intensities of lipids of blood and pancreas and the pathological changes in the pancreas during severe acute pancreatitis (SAP) remains unclear. In our study, we employed a rat model of SAP induced through intraperitoneal ornithine injections. We collected serum...

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Main Authors: Jinxi Yang, Manjiangcuo Wang, Qi Qiu, Yan Huang, Yiqin Wang, Qianlun Pu, Na Jiang, Rui Wang, Li Wen, Xiaoying Zhang, Chenxia Han, Dan Du
Format: Article
Language:English
Published: MDPI AG 2023-09-01
Series:Metabolites
Subjects:
Online Access:https://www.mdpi.com/2218-1989/13/9/993
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author Jinxi Yang
Manjiangcuo Wang
Qi Qiu
Yan Huang
Yiqin Wang
Qianlun Pu
Na Jiang
Rui Wang
Li Wen
Xiaoying Zhang
Chenxia Han
Dan Du
author_facet Jinxi Yang
Manjiangcuo Wang
Qi Qiu
Yan Huang
Yiqin Wang
Qianlun Pu
Na Jiang
Rui Wang
Li Wen
Xiaoying Zhang
Chenxia Han
Dan Du
author_sort Jinxi Yang
collection DOAJ
description The relationship between the type and intensities of lipids of blood and pancreas and the pathological changes in the pancreas during severe acute pancreatitis (SAP) remains unclear. In our study, we employed a rat model of SAP induced through intraperitoneal ornithine injections. We collected serum and pancreas samples at various time points (0–144 h) for histopathological and biochemical assessments, followed by lipidomic analyses using LC-MS/MS or in situ mass spectrometry imaging (MSI) To discern changes over time or at specific points, we employed time-course and univariate analyses for lipid screening, respectively. Our findings indicated that the peak inflammation in the Orn-SAP model occurred within the 24–30 h timeframe, with evident necrosis emerging from 24 h onwards, followed by regeneration starting at 48 h. Time-course analysis revealed an overall decrease in glycerophospholipids (PEs, PCs, LPEs, LPCs), while CEs exhibited an increase within the pancreas. Univariate analysis unveiled a significant reduction in serum TAGs containing 46–51 carbon atoms at 24 h, and CERs in the pancreas significantly increased at 30 h, compared with 0 h. Moreover, a substantial rise in TAGs containing 56–58 carbon atoms was observed at 144 h, both in serum and pancreas. MSI demonstrated the CERs containing saturated mono-acyl chains of 16 and 18 carbon atoms influenced pancreatic regeneration. Tracing the origin of FFAs hydrolyzed from pancreatic glycerophospholipids and serum TAGs during the early stages of inflammation, as well as FFAs utilized for CEs and CERs synthesis during the repair phase, may yield valuable strategies for diagnosing and managing SAP.
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spelling doaj.art-a84386b8ce9546fa89f6d3e061d4505e2023-11-19T11:55:16ZengMDPI AGMetabolites2218-19892023-09-0113999310.3390/metabo13090993Time-Course Lipidomics of Ornithine-Induced Severe Acute Pancreatitis Model Reveals the Free Fatty Acids Centered Lipids Dysregulation CharacteristicsJinxi Yang0Manjiangcuo Wang1Qi Qiu2Yan Huang3Yiqin Wang4Qianlun Pu5Na Jiang6Rui Wang7Li Wen8Xiaoying Zhang9Chenxia Han10Dan Du11West China Centre of Excellence for Pancreatitis, Institute of Integrated Traditional Chinese and Western Medicine, West China Hospital/West China Medical School, Sichuan University, Chengdu 610041, ChinaAdvanced Mass Spectrometry Center, Research Core Facility, Frontiers Science Center for Disease-Related Molecular Network, West China Hospital, Sichuan University, Chengdu 610041, ChinaWest China Centre of Excellence for Pancreatitis, Institute of Integrated Traditional Chinese and Western Medicine, West China Hospital/West China Medical School, Sichuan University, Chengdu 610041, ChinaWest China Centre of Excellence for Pancreatitis, Institute of Integrated Traditional Chinese and Western Medicine, West China Hospital/West China Medical School, Sichuan University, Chengdu 610041, ChinaWest China Centre of Excellence for Pancreatitis, Institute of Integrated Traditional Chinese and Western Medicine, West China Hospital/West China Medical School, Sichuan University, Chengdu 610041, ChinaAdvanced Mass Spectrometry Center, Research Core Facility, Frontiers Science Center for Disease-Related Molecular Network, West China Hospital, Sichuan University, Chengdu 610041, ChinaAdvanced Mass Spectrometry Center, Research Core Facility, Frontiers Science Center for Disease-Related Molecular Network, West China Hospital, Sichuan University, Chengdu 610041, ChinaAdvanced Mass Spectrometry Center, Research Core Facility, Frontiers Science Center for Disease-Related Molecular Network, West China Hospital, Sichuan University, Chengdu 610041, ChinaPeking Union Medical College Hospital, Chinese Academy of Medical Science & Peking Union Medical College, Beijing 100730, ChinaWest China Centre of Excellence for Pancreatitis, Institute of Integrated Traditional Chinese and Western Medicine, West China Hospital/West China Medical School, Sichuan University, Chengdu 610041, ChinaWest China Centre of Excellence for Pancreatitis, Institute of Integrated Traditional Chinese and Western Medicine, West China Hospital/West China Medical School, Sichuan University, Chengdu 610041, ChinaWest China Centre of Excellence for Pancreatitis, Institute of Integrated Traditional Chinese and Western Medicine, West China Hospital/West China Medical School, Sichuan University, Chengdu 610041, ChinaThe relationship between the type and intensities of lipids of blood and pancreas and the pathological changes in the pancreas during severe acute pancreatitis (SAP) remains unclear. In our study, we employed a rat model of SAP induced through intraperitoneal ornithine injections. We collected serum and pancreas samples at various time points (0–144 h) for histopathological and biochemical assessments, followed by lipidomic analyses using LC-MS/MS or in situ mass spectrometry imaging (MSI) To discern changes over time or at specific points, we employed time-course and univariate analyses for lipid screening, respectively. Our findings indicated that the peak inflammation in the Orn-SAP model occurred within the 24–30 h timeframe, with evident necrosis emerging from 24 h onwards, followed by regeneration starting at 48 h. Time-course analysis revealed an overall decrease in glycerophospholipids (PEs, PCs, LPEs, LPCs), while CEs exhibited an increase within the pancreas. Univariate analysis unveiled a significant reduction in serum TAGs containing 46–51 carbon atoms at 24 h, and CERs in the pancreas significantly increased at 30 h, compared with 0 h. Moreover, a substantial rise in TAGs containing 56–58 carbon atoms was observed at 144 h, both in serum and pancreas. MSI demonstrated the CERs containing saturated mono-acyl chains of 16 and 18 carbon atoms influenced pancreatic regeneration. Tracing the origin of FFAs hydrolyzed from pancreatic glycerophospholipids and serum TAGs during the early stages of inflammation, as well as FFAs utilized for CEs and CERs synthesis during the repair phase, may yield valuable strategies for diagnosing and managing SAP.https://www.mdpi.com/2218-1989/13/9/993lipidomicssevere acute pancreatitisfree fatty acidstriglyceridesceramides
spellingShingle Jinxi Yang
Manjiangcuo Wang
Qi Qiu
Yan Huang
Yiqin Wang
Qianlun Pu
Na Jiang
Rui Wang
Li Wen
Xiaoying Zhang
Chenxia Han
Dan Du
Time-Course Lipidomics of Ornithine-Induced Severe Acute Pancreatitis Model Reveals the Free Fatty Acids Centered Lipids Dysregulation Characteristics
Metabolites
lipidomics
severe acute pancreatitis
free fatty acids
triglycerides
ceramides
title Time-Course Lipidomics of Ornithine-Induced Severe Acute Pancreatitis Model Reveals the Free Fatty Acids Centered Lipids Dysregulation Characteristics
title_full Time-Course Lipidomics of Ornithine-Induced Severe Acute Pancreatitis Model Reveals the Free Fatty Acids Centered Lipids Dysregulation Characteristics
title_fullStr Time-Course Lipidomics of Ornithine-Induced Severe Acute Pancreatitis Model Reveals the Free Fatty Acids Centered Lipids Dysregulation Characteristics
title_full_unstemmed Time-Course Lipidomics of Ornithine-Induced Severe Acute Pancreatitis Model Reveals the Free Fatty Acids Centered Lipids Dysregulation Characteristics
title_short Time-Course Lipidomics of Ornithine-Induced Severe Acute Pancreatitis Model Reveals the Free Fatty Acids Centered Lipids Dysregulation Characteristics
title_sort time course lipidomics of ornithine induced severe acute pancreatitis model reveals the free fatty acids centered lipids dysregulation characteristics
topic lipidomics
severe acute pancreatitis
free fatty acids
triglycerides
ceramides
url https://www.mdpi.com/2218-1989/13/9/993
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