Elevated expression of glycolytic genes as a prominent feature of early-onset preeclampsia: insights from integrative transcriptomic analysis

Introduction: Preeclampsia (PE), a notable pregnancy-related disorder, leads to 40,000+ maternal deaths yearly. Recent research shows PE divides into early-onset (EOPE) and late-onset (LOPE) subtypes, each with distinct clinical features and outcomes. However, the molecular characteristics of variou...

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Main Authors: Jie He, Huan Yang, Zheng Liu, Miaomiao Chen, Ying Ye, Yuelan Tao, Shuhong Li, Jie Fang, Jiacheng Xu, Xiafei Wu, Hongbo Qi
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-09-01
Series:Frontiers in Molecular Biosciences
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmolb.2023.1248771/full
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author Jie He
Jie He
Jie He
Huan Yang
Zheng Liu
Zheng Liu
Zheng Liu
Miaomiao Chen
Ying Ye
Yuelan Tao
Yuelan Tao
Yuelan Tao
Shuhong Li
Jie Fang
Jie Fang
Jie Fang
Jiacheng Xu
Jiacheng Xu
Jiacheng Xu
Xiafei Wu
Xiafei Wu
Xiafei Wu
Hongbo Qi
Hongbo Qi
Hongbo Qi
Hongbo Qi
author_facet Jie He
Jie He
Jie He
Huan Yang
Zheng Liu
Zheng Liu
Zheng Liu
Miaomiao Chen
Ying Ye
Yuelan Tao
Yuelan Tao
Yuelan Tao
Shuhong Li
Jie Fang
Jie Fang
Jie Fang
Jiacheng Xu
Jiacheng Xu
Jiacheng Xu
Xiafei Wu
Xiafei Wu
Xiafei Wu
Hongbo Qi
Hongbo Qi
Hongbo Qi
Hongbo Qi
author_sort Jie He
collection DOAJ
description Introduction: Preeclampsia (PE), a notable pregnancy-related disorder, leads to 40,000+ maternal deaths yearly. Recent research shows PE divides into early-onset (EOPE) and late-onset (LOPE) subtypes, each with distinct clinical features and outcomes. However, the molecular characteristics of various subtypes are currently subject to debate and are not consistent.Methods: We integrated transcriptomic expression data from a total of 372 placental samples across 8 publicly available databases via combat algorithm. Then, a variety of strategies including Random Forest Recursive Feature Elimination (RF-RFE), differential analysis, oposSOM, and Weighted Correlation Network Analysis were employed to identify the characteristic genes of the EOPE and LOPE subtypes. Finally, we conducted in vitro experiments on the key gene HK2 in HTR8/SVneo cells to explore its function.Results: Our results revealed a complex classification of PE placental samples, wherein EOPE manifests as a highly homogeneous sample group characterized by hypoxia and HIF1A activation. Among the core features is the upregulation of glycolysis-related genes, particularly HK2, in the placenta-an observation corroborated by independent validation data and single-cell data. Building on the pronounced correlation between HK2 and EOPE, we conducted in vitro experiments to assess the potential functional impact of HK2 on trophoblast cells. Additionally, the LOPE samples exhibit strong heterogeneity and lack distinct features, suggesting a complex molecular makeup for this subtype. Unsupervised clustering analysis indicates that LOPE likely comprises at least two distinct subtypes, linked to cell-environment interaction and cytokine and protein modification functionalities.Discussion: In summary, these findings elucidate potential mechanistic differences between the two PE subtypes, lend support to the hypothesis of classifying PE based on gestational weeks, and emphasize the potential significant role of glycolysis-related genes, especially HK2 in EOPE.
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spelling doaj.art-10a44a56edf843b3a70dfcffde21059f2023-09-26T06:41:59ZengFrontiers Media S.A.Frontiers in Molecular Biosciences2296-889X2023-09-011010.3389/fmolb.2023.12487711248771Elevated expression of glycolytic genes as a prominent feature of early-onset preeclampsia: insights from integrative transcriptomic analysisJie He0Jie He1Jie He2Huan Yang3Zheng Liu4Zheng Liu5Zheng Liu6Miaomiao Chen7Ying Ye8Yuelan Tao9Yuelan Tao10Yuelan Tao11Shuhong Li12Jie Fang13Jie Fang14Jie Fang15Jiacheng Xu16Jiacheng Xu17Jiacheng Xu18Xiafei Wu19Xiafei Wu20Xiafei Wu21Hongbo Qi22Hongbo Qi23Hongbo Qi24Hongbo Qi25Department of Obstetrics, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaChongqing Key Laboratory of Maternal and Fetal Medicine, Chongqing Medical University, Chongqing, ChinaJoint International Research Laboratory of Reproduction and Development of Chinese Ministry of Education, Chongqing Medical University, Chongqing, ChinaDepartment of Obstetrics, Chongqing University Three Gorges Hospital, Chongqing, ChinaDepartment of Obstetrics, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaChongqing Key Laboratory of Maternal and Fetal Medicine, Chongqing Medical University, Chongqing, ChinaJoint International Research Laboratory of Reproduction and Development of Chinese Ministry of Education, Chongqing Medical University, Chongqing, ChinaMaternal and Child Health Hospital of Hubei Province, Wuhan, ChinaDepartment of Cardiothoracic Surgery, The Second Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaDepartment of Obstetrics, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaChongqing Key Laboratory of Maternal and Fetal Medicine, Chongqing Medical University, Chongqing, ChinaJoint International Research Laboratory of Reproduction and Development of Chinese Ministry of Education, Chongqing Medical University, Chongqing, ChinaDepartment of Oncology, Chengdu Second People’s Hospital, Chengdu, ChinaDepartment of Obstetrics, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaChongqing Key Laboratory of Maternal and Fetal Medicine, Chongqing Medical University, Chongqing, ChinaJoint International Research Laboratory of Reproduction and Development of Chinese Ministry of Education, Chongqing Medical University, Chongqing, ChinaDepartment of Obstetrics, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaChongqing Key Laboratory of Maternal and Fetal Medicine, Chongqing Medical University, Chongqing, ChinaJoint International Research Laboratory of Reproduction and Development of Chinese Ministry of Education, Chongqing Medical University, Chongqing, ChinaDepartment of Obstetrics, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaChongqing Key Laboratory of Maternal and Fetal Medicine, Chongqing Medical University, Chongqing, ChinaJoint International Research Laboratory of Reproduction and Development of Chinese Ministry of Education, Chongqing Medical University, Chongqing, ChinaDepartment of Obstetrics, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaChongqing Key Laboratory of Maternal and Fetal Medicine, Chongqing Medical University, Chongqing, ChinaJoint International Research Laboratory of Reproduction and Development of Chinese Ministry of Education, Chongqing Medical University, Chongqing, ChinaDepartment of Obstetrics and Gynecology, Women and Children’s Hospital of Chongqing Medical University, Chongqing, ChinaIntroduction: Preeclampsia (PE), a notable pregnancy-related disorder, leads to 40,000+ maternal deaths yearly. Recent research shows PE divides into early-onset (EOPE) and late-onset (LOPE) subtypes, each with distinct clinical features and outcomes. However, the molecular characteristics of various subtypes are currently subject to debate and are not consistent.Methods: We integrated transcriptomic expression data from a total of 372 placental samples across 8 publicly available databases via combat algorithm. Then, a variety of strategies including Random Forest Recursive Feature Elimination (RF-RFE), differential analysis, oposSOM, and Weighted Correlation Network Analysis were employed to identify the characteristic genes of the EOPE and LOPE subtypes. Finally, we conducted in vitro experiments on the key gene HK2 in HTR8/SVneo cells to explore its function.Results: Our results revealed a complex classification of PE placental samples, wherein EOPE manifests as a highly homogeneous sample group characterized by hypoxia and HIF1A activation. Among the core features is the upregulation of glycolysis-related genes, particularly HK2, in the placenta-an observation corroborated by independent validation data and single-cell data. Building on the pronounced correlation between HK2 and EOPE, we conducted in vitro experiments to assess the potential functional impact of HK2 on trophoblast cells. Additionally, the LOPE samples exhibit strong heterogeneity and lack distinct features, suggesting a complex molecular makeup for this subtype. Unsupervised clustering analysis indicates that LOPE likely comprises at least two distinct subtypes, linked to cell-environment interaction and cytokine and protein modification functionalities.Discussion: In summary, these findings elucidate potential mechanistic differences between the two PE subtypes, lend support to the hypothesis of classifying PE based on gestational weeks, and emphasize the potential significant role of glycolysis-related genes, especially HK2 in EOPE.https://www.frontiersin.org/articles/10.3389/fmolb.2023.1248771/fullpreeclampsiaplacentagestational hypertensiontranscriptomicsmicroarraysingle-cell sequencing
spellingShingle Jie He
Jie He
Jie He
Huan Yang
Zheng Liu
Zheng Liu
Zheng Liu
Miaomiao Chen
Ying Ye
Yuelan Tao
Yuelan Tao
Yuelan Tao
Shuhong Li
Jie Fang
Jie Fang
Jie Fang
Jiacheng Xu
Jiacheng Xu
Jiacheng Xu
Xiafei Wu
Xiafei Wu
Xiafei Wu
Hongbo Qi
Hongbo Qi
Hongbo Qi
Hongbo Qi
Elevated expression of glycolytic genes as a prominent feature of early-onset preeclampsia: insights from integrative transcriptomic analysis
Frontiers in Molecular Biosciences
preeclampsia
placenta
gestational hypertension
transcriptomics
microarray
single-cell sequencing
title Elevated expression of glycolytic genes as a prominent feature of early-onset preeclampsia: insights from integrative transcriptomic analysis
title_full Elevated expression of glycolytic genes as a prominent feature of early-onset preeclampsia: insights from integrative transcriptomic analysis
title_fullStr Elevated expression of glycolytic genes as a prominent feature of early-onset preeclampsia: insights from integrative transcriptomic analysis
title_full_unstemmed Elevated expression of glycolytic genes as a prominent feature of early-onset preeclampsia: insights from integrative transcriptomic analysis
title_short Elevated expression of glycolytic genes as a prominent feature of early-onset preeclampsia: insights from integrative transcriptomic analysis
title_sort elevated expression of glycolytic genes as a prominent feature of early onset preeclampsia insights from integrative transcriptomic analysis
topic preeclampsia
placenta
gestational hypertension
transcriptomics
microarray
single-cell sequencing
url https://www.frontiersin.org/articles/10.3389/fmolb.2023.1248771/full
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