Therapeutic implications of altered cholesterol homeostasis mediated by loss of CYP46A1 in human glioblastoma

Abstract Dysregulated cholesterol metabolism is a hallmark of many cancers, including glioblastoma (GBM), but its role in disease progression is not well understood. Here, we identified cholesterol 24‐hydroxylase (CYP46A1), a brain‐specific enzyme responsible for the elimination of cholesterol throu...

Full description

Saved in:
Bibliographic Details
Main Authors: Mingzhi Han, Shuai Wang, Ning Yang, Xu Wang, Wenbo Zhao, Halala Sdik Saed, Thomas Daubon, Bin Huang, Anjing Chen, Gang Li, Hrvoje Miletic, Frits Thorsen, Rolf Bjerkvig, Xingang Li, Jian Wang
Format: Article
Language:English
Published: Springer Nature 2019-11-01
Series:EMBO Molecular Medicine
Subjects:
Online Access:https://doi.org/10.15252/emmm.201910924
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849761549558743040
author Mingzhi Han
Shuai Wang
Ning Yang
Xu Wang
Wenbo Zhao
Halala Sdik Saed
Thomas Daubon
Bin Huang
Anjing Chen
Gang Li
Hrvoje Miletic
Frits Thorsen
Rolf Bjerkvig
Xingang Li
Jian Wang
author_facet Mingzhi Han
Shuai Wang
Ning Yang
Xu Wang
Wenbo Zhao
Halala Sdik Saed
Thomas Daubon
Bin Huang
Anjing Chen
Gang Li
Hrvoje Miletic
Frits Thorsen
Rolf Bjerkvig
Xingang Li
Jian Wang
author_sort Mingzhi Han
collection DOAJ
description Abstract Dysregulated cholesterol metabolism is a hallmark of many cancers, including glioblastoma (GBM), but its role in disease progression is not well understood. Here, we identified cholesterol 24‐hydroxylase (CYP46A1), a brain‐specific enzyme responsible for the elimination of cholesterol through the conversion of cholesterol into 24(S)‐hydroxycholesterol (24OHC), as one of the most dramatically dysregulated cholesterol metabolism genes in GBM. CYP46A1 was significantly decreased in GBM samples compared with normal brain tissue. A reduction in CYP46A1 expression was associated with increasing tumour grade and poor prognosis in human gliomas. Ectopic expression of CYP46A1 suppressed cell proliferation and in vivo tumour growth by increasing 24OHC levels. RNA‐seq revealed that treatment of GBM cells with 24OHC suppressed tumour growth through regulation of LXR and SREBP signalling. Efavirenz, an activator of CYP46A1 that is known to penetrate the blood–brain barrier, inhibited GBM growth in vivo. Our findings demonstrate that CYP46A1 is a critical regulator of cellular cholesterol in GBM and that the CYP46A1/24OHC axis is a potential therapeutic target.
format Article
id doaj-art-9027dbabbdc145e0a2567a88a9cc744f
institution DOAJ
issn 1757-4676
1757-4684
language English
publishDate 2019-11-01
publisher Springer Nature
record_format Article
series EMBO Molecular Medicine
spelling doaj-art-9027dbabbdc145e0a2567a88a9cc744f2025-08-20T03:06:00ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842019-11-0112111810.15252/emmm.201910924Therapeutic implications of altered cholesterol homeostasis mediated by loss of CYP46A1 in human glioblastomaMingzhi Han0Shuai Wang1Ning Yang2Xu Wang3Wenbo Zhao4Halala Sdik Saed5Thomas Daubon6Bin Huang7Anjing Chen8Gang Li9Hrvoje Miletic10Frits Thorsen11Rolf Bjerkvig12Xingang Li13Jian Wang14Shandong Key Laboratory of Brain Function Remodeling, Department of Neurosurgery, Qilu Hospital of Shandong University and Institute of Brain and Brain‐Inspired Science, Shandong UniversityShandong Key Laboratory of Brain Function Remodeling, Department of Neurosurgery, Qilu Hospital of Shandong University and Institute of Brain and Brain‐Inspired Science, Shandong UniversityShandong Key Laboratory of Brain Function Remodeling, Department of Neurosurgery, Qilu Hospital of Shandong University and Institute of Brain and Brain‐Inspired Science, Shandong UniversityShandong Key Laboratory of Brain Function Remodeling, Department of Neurosurgery, Qilu Hospital of Shandong University and Institute of Brain and Brain‐Inspired Science, Shandong UniversityShandong Key Laboratory of Brain Function Remodeling, Department of Neurosurgery, Qilu Hospital of Shandong University and Institute of Brain and Brain‐Inspired Science, Shandong UniversityDepartment of Biomedicine, University of BergenINSERM U1029, Institut Nationale de la Santé et de la Recherche MédicaleShandong Key Laboratory of Brain Function Remodeling, Department of Neurosurgery, Qilu Hospital of Shandong University and Institute of Brain and Brain‐Inspired Science, Shandong UniversityShandong Key Laboratory of Brain Function Remodeling, Department of Neurosurgery, Qilu Hospital of Shandong University and Institute of Brain and Brain‐Inspired Science, Shandong UniversityShandong Key Laboratory of Brain Function Remodeling, Department of Neurosurgery, Qilu Hospital of Shandong University and Institute of Brain and Brain‐Inspired Science, Shandong UniversityDepartment of Biomedicine, University of BergenDepartment of Biomedicine, University of BergenDepartment of Biomedicine, University of BergenShandong Key Laboratory of Brain Function Remodeling, Department of Neurosurgery, Qilu Hospital of Shandong University and Institute of Brain and Brain‐Inspired Science, Shandong UniversityShandong Key Laboratory of Brain Function Remodeling, Department of Neurosurgery, Qilu Hospital of Shandong University and Institute of Brain and Brain‐Inspired Science, Shandong UniversityAbstract Dysregulated cholesterol metabolism is a hallmark of many cancers, including glioblastoma (GBM), but its role in disease progression is not well understood. Here, we identified cholesterol 24‐hydroxylase (CYP46A1), a brain‐specific enzyme responsible for the elimination of cholesterol through the conversion of cholesterol into 24(S)‐hydroxycholesterol (24OHC), as one of the most dramatically dysregulated cholesterol metabolism genes in GBM. CYP46A1 was significantly decreased in GBM samples compared with normal brain tissue. A reduction in CYP46A1 expression was associated with increasing tumour grade and poor prognosis in human gliomas. Ectopic expression of CYP46A1 suppressed cell proliferation and in vivo tumour growth by increasing 24OHC levels. RNA‐seq revealed that treatment of GBM cells with 24OHC suppressed tumour growth through regulation of LXR and SREBP signalling. Efavirenz, an activator of CYP46A1 that is known to penetrate the blood–brain barrier, inhibited GBM growth in vivo. Our findings demonstrate that CYP46A1 is a critical regulator of cellular cholesterol in GBM and that the CYP46A1/24OHC axis is a potential therapeutic target.https://doi.org/10.15252/emmm.20191092424OHCcholesterol homeostasisCYP46A1efavirenzglioblastoma
spellingShingle Mingzhi Han
Shuai Wang
Ning Yang
Xu Wang
Wenbo Zhao
Halala Sdik Saed
Thomas Daubon
Bin Huang
Anjing Chen
Gang Li
Hrvoje Miletic
Frits Thorsen
Rolf Bjerkvig
Xingang Li
Jian Wang
Therapeutic implications of altered cholesterol homeostasis mediated by loss of CYP46A1 in human glioblastoma
EMBO Molecular Medicine
24OHC
cholesterol homeostasis
CYP46A1
efavirenz
glioblastoma
title Therapeutic implications of altered cholesterol homeostasis mediated by loss of CYP46A1 in human glioblastoma
title_full Therapeutic implications of altered cholesterol homeostasis mediated by loss of CYP46A1 in human glioblastoma
title_fullStr Therapeutic implications of altered cholesterol homeostasis mediated by loss of CYP46A1 in human glioblastoma
title_full_unstemmed Therapeutic implications of altered cholesterol homeostasis mediated by loss of CYP46A1 in human glioblastoma
title_short Therapeutic implications of altered cholesterol homeostasis mediated by loss of CYP46A1 in human glioblastoma
title_sort therapeutic implications of altered cholesterol homeostasis mediated by loss of cyp46a1 in human glioblastoma
topic 24OHC
cholesterol homeostasis
CYP46A1
efavirenz
glioblastoma
url https://doi.org/10.15252/emmm.201910924
work_keys_str_mv AT mingzhihan therapeuticimplicationsofalteredcholesterolhomeostasismediatedbylossofcyp46a1inhumanglioblastoma
AT shuaiwang therapeuticimplicationsofalteredcholesterolhomeostasismediatedbylossofcyp46a1inhumanglioblastoma
AT ningyang therapeuticimplicationsofalteredcholesterolhomeostasismediatedbylossofcyp46a1inhumanglioblastoma
AT xuwang therapeuticimplicationsofalteredcholesterolhomeostasismediatedbylossofcyp46a1inhumanglioblastoma
AT wenbozhao therapeuticimplicationsofalteredcholesterolhomeostasismediatedbylossofcyp46a1inhumanglioblastoma
AT halalasdiksaed therapeuticimplicationsofalteredcholesterolhomeostasismediatedbylossofcyp46a1inhumanglioblastoma
AT thomasdaubon therapeuticimplicationsofalteredcholesterolhomeostasismediatedbylossofcyp46a1inhumanglioblastoma
AT binhuang therapeuticimplicationsofalteredcholesterolhomeostasismediatedbylossofcyp46a1inhumanglioblastoma
AT anjingchen therapeuticimplicationsofalteredcholesterolhomeostasismediatedbylossofcyp46a1inhumanglioblastoma
AT gangli therapeuticimplicationsofalteredcholesterolhomeostasismediatedbylossofcyp46a1inhumanglioblastoma
AT hrvojemiletic therapeuticimplicationsofalteredcholesterolhomeostasismediatedbylossofcyp46a1inhumanglioblastoma
AT fritsthorsen therapeuticimplicationsofalteredcholesterolhomeostasismediatedbylossofcyp46a1inhumanglioblastoma
AT rolfbjerkvig therapeuticimplicationsofalteredcholesterolhomeostasismediatedbylossofcyp46a1inhumanglioblastoma
AT xingangli therapeuticimplicationsofalteredcholesterolhomeostasismediatedbylossofcyp46a1inhumanglioblastoma
AT jianwang therapeuticimplicationsofalteredcholesterolhomeostasismediatedbylossofcyp46a1inhumanglioblastoma