Orthogonal lipid sensors identify transbilayer asymmetry of plasma membrane cholesterol

Orthogonal cholesterol sensors that are useful for imaging cholesterol in the plasma membrane leaflets reveal an asymmetry in which a high outer leaflet concentration is important for signaling processes and is potentially actively maintained. Controlled distribution of lipids across various cell me...

Full description

Saved in:
Bibliographic Details
Published inNature chemical biology Vol. 13; no. 3; pp. 268 - 274
Main Authors Liu, Shu-Lin, Sheng, Ren, Jung, Jae Hun, Wang, Li, Stec, Ewa, O'Connor, Matthew J, Song, Seohyoen, Bikkavilli, Rama Kamesh, Winn, Robert A, Lee, Daesung, Baek, Kwanghee, Ueda, Kazumitsu, Levitan, Irena, Kim, Kwang-Pyo, Cho, Wonhwa
Format Journal Article
LanguageEnglish
Published New York Nature Publishing Group US 01.03.2017
Nature Publishing Group
Subjects
631/80/86
631/92/287
631/92/314
631/92/96
Asymmetry
Biochemical Engineering
Biochemistry
Bioorganic Chemistry
Cell Biology
Cell Line
Cell Membrane - chemistry
Chemistry
Chemistry/Food Science
Cholesterol
Cholesterol - analysis
HEK293 Cells
Homeostasis
Humans
Hyperlipidemia
Lipids
Lipids - chemistry
Membranes
Sensors
United States > US
Illinois
Chicago Illinois
Online AccessGet full text

Cover

Abstract Orthogonal cholesterol sensors that are useful for imaging cholesterol in the plasma membrane leaflets reveal an asymmetry in which a high outer leaflet concentration is important for signaling processes and is potentially actively maintained. Controlled distribution of lipids across various cell membranes is crucial for cell homeostasis and regulation. We developed an imaging method that allows simultaneous in situ quantification of cholesterol in two leaflets of the plasma membrane (PM) using tunable orthogonal cholesterol sensors. Our imaging revealed marked transbilayer asymmetry of PM cholesterol (TAPMC) in various mammalian cells, with the concentration in the inner leaflet (IPM) being ∼12-fold lower than that in the outer leaflet (OPM). The asymmetry was maintained by active transport of cholesterol from IPM to OPM and its chemical retention at OPM. Furthermore, the increase in the IPM cholesterol level was triggered in a stimulus-specific manner, allowing cholesterol to serve as a signaling lipid. We found excellent correlation between the IPM cholesterol level and cellular Wnt signaling activity, suggesting that TAPMC and stimulus-induced PM cholesterol redistribution are crucial for tight regulation of cellular processes under physiological conditions.
AbstractList Controlled distribution of lipids across various cell membranes is crucial for cell homeostasis and regulation. We developed an imaging method that allows simultaneous in situ quantification of cholesterol in two leaflets of the plasma membrane (PM) using tunable orthogonal cholesterol sensors. Our imaging revealed marked transbilayer asymmetry of PM cholesterol (TAPMC) in various mammalian cells, with the concentration in the inner leaflet (IPM) being ∼12-fold lower than that in the outer leaflet (OPM). The asymmetry was maintained by active transport of cholesterol from IPM to OPM and its chemical retention at OPM. Furthermore, the increase in the IPM cholesterol level was triggered in a stimulus-specific manner, allowing cholesterol to serve as a signaling lipid. We found excellent correlation between the IPM cholesterol level and cellular Wnt signaling activity, suggesting that TAPMC and stimulus-induced PM cholesterol redistribution are crucial for tight regulation of cellular processes under physiological conditions.
Controlled distribution of lipids across various cell membranes is crucial for cell homeostasis and regulation. We developed an imaging method that allows simultaneous in situ quantification of cholesterol in two leaflets of the plasma membrane (PM) using tunable orthogonal cholesterol sensors. Our imaging revealed marked transbilayer asymmetry of PM cholesterol (TAPMC) in various mammalian cells, with the concentration in the inner leaflet (IPM) being 12-fold lower than that in the outer leaflet (OPM). The asymmetry was maintained by active transport of cholesterol from IPM to OPM and its chemical retention at OPM. Furthermore, the increase in the IPM cholesterol level was triggered in a stimulus-specific manner, allowing cholesterol to serve as a signaling lipid. We found excellent correlation between the IPM cholesterol level and cellular Wnt signaling activity, suggesting that TAPMC and stimulus-induced PM cholesterol redistribution are crucial for tight regulation of cellular processes under physiological conditions.
Orthogonal cholesterol sensors that are useful for imaging cholesterol in the plasma membrane leaflets reveal an asymmetry in which a high outer leaflet concentration is important for signaling processes and is potentially actively maintained. Controlled distribution of lipids across various cell membranes is crucial for cell homeostasis and regulation. We developed an imaging method that allows simultaneous in situ quantification of cholesterol in two leaflets of the plasma membrane (PM) using tunable orthogonal cholesterol sensors. Our imaging revealed marked transbilayer asymmetry of PM cholesterol (TAPMC) in various mammalian cells, with the concentration in the inner leaflet (IPM) being ∼12-fold lower than that in the outer leaflet (OPM). The asymmetry was maintained by active transport of cholesterol from IPM to OPM and its chemical retention at OPM. Furthermore, the increase in the IPM cholesterol level was triggered in a stimulus-specific manner, allowing cholesterol to serve as a signaling lipid. We found excellent correlation between the IPM cholesterol level and cellular Wnt signaling activity, suggesting that TAPMC and stimulus-induced PM cholesterol redistribution are crucial for tight regulation of cellular processes under physiological conditions.
Controlled distribution of lipids across various cell membranes is crucial for cell homeostasis and regulation. We developed an imaging method that allows simultaneous in situ quantification of cholesterol in two leaflets of the plasma membrane (PM) using tunable orthogonal cholesterol sensors. Our imaging revealed marked transbilayer asymmetry of PM cholesterol (TAPMC) in various mammalian cells, with the concentration in the inner leaflet (IPM) being ~12-fold lower than that in the outer leaflet (OPM). The asymmetry was maintained by active transport of cholesterol from IPM to OPM and its chemical retention at OPM. Furthermore, the increase in the IPM cholesterol level was triggered in a stimulus-specific manner, allowing cholesterol to serve as a signaling lipid. We found excellent correlation between the IPM cholesterol level and cellular Wnt signaling activity, suggesting that TAPMC and stimulus-induced PM cholesterol redistribution are crucial for tight regulation of cellular processes under physiological conditions.
Author Sheng, Ren
O'Connor, Matthew J
Song, Seohyoen
Bikkavilli, Rama Kamesh
Wang, Li
Stec, Ewa
Kim, Kwang-Pyo
Cho, Wonhwa
Jung, Jae Hun
Ueda, Kazumitsu
Lee, Daesung
Levitan, Irena
Winn, Robert A
Baek, Kwanghee
Liu, Shu-Lin
AuthorAffiliation 2 Department of Applied Chemistry, Kyung Hee University, Yongin, Korea
5 Institute for Integrated Cell-Material Sciences (WPI-iCeMS), and Division of Applied Life Sciences, Kyoto University, Kyoto, Japan
3 Department of Medicine, University of Illinois at Chicago, Chicago, Illinois, USA
1 Department of Chemistry, University of Illinois at Chicago, Chicago, Illinois, USA
4 Department of Genetic Engineering, Kyung Hee University, Yongin, Korea
AuthorAffiliation_xml – name: 1 Department of Chemistry, University of Illinois at Chicago, Chicago, Illinois, USA
– name: 4 Department of Genetic Engineering, Kyung Hee University, Yongin, Korea
– name: 2 Department of Applied Chemistry, Kyung Hee University, Yongin, Korea
– name: 5 Institute for Integrated Cell-Material Sciences (WPI-iCeMS), and Division of Applied Life Sciences, Kyoto University, Kyoto, Japan
– name: 3 Department of Medicine, University of Illinois at Chicago, Chicago, Illinois, USA
Author_xml – sequence: 1
  givenname: Shu-Lin
  surname: Liu
  fullname: Liu, Shu-Lin
  organization: Department of Chemistry, University of Illinois at Chicago
– sequence: 2
  givenname: Ren
  surname: Sheng
  fullname: Sheng, Ren
  organization: Department of Chemistry, University of Illinois at Chicago
– sequence: 3
  givenname: Jae Hun
  surname: Jung
  fullname: Jung, Jae Hun
  organization: Department of Applied Chemistry, Kyung Hee University
– sequence: 4
  givenname: Li
  surname: Wang
  fullname: Wang, Li
  organization: Department of Chemistry, University of Illinois at Chicago
– sequence: 5
  givenname: Ewa
  surname: Stec
  fullname: Stec, Ewa
  organization: Department of Chemistry, University of Illinois at Chicago
– sequence: 6
  givenname: Matthew J
  surname: O'Connor
  fullname: O'Connor, Matthew J
  organization: Department of Chemistry, University of Illinois at Chicago
– sequence: 7
  givenname: Seohyoen
  surname: Song
  fullname: Song, Seohyoen
  organization: Department of Chemistry, University of Illinois at Chicago
– sequence: 8
  givenname: Rama Kamesh
  surname: Bikkavilli
  fullname: Bikkavilli, Rama Kamesh
  organization: Department of Medicine, University of Illinois at Chicago
– sequence: 9
  givenname: Robert A
  surname: Winn
  fullname: Winn, Robert A
  organization: Department of Medicine, University of Illinois at Chicago
– sequence: 10
  givenname: Daesung
  surname: Lee
  fullname: Lee, Daesung
  organization: Department of Chemistry, University of Illinois at Chicago
– sequence: 11
  givenname: Kwanghee
  surname: Baek
  fullname: Baek, Kwanghee
  organization: Department of Genetic Engineering, Kyung Hee University
– sequence: 12
  givenname: Kazumitsu
  surname: Ueda
  fullname: Ueda, Kazumitsu
  organization: and Division of Applied Life Sciences, Institute for Integrated Cell-Material Sciences (WPI-iCeMS), Kyoto University
– sequence: 13
  givenname: Irena
  surname: Levitan
  fullname: Levitan, Irena
  organization: Department of Medicine, University of Illinois at Chicago
– sequence: 14
  givenname: Kwang-Pyo
  surname: Kim
  fullname: Kim, Kwang-Pyo
  organization: Department of Applied Chemistry, Kyung Hee University
– sequence: 15
  givenname: Wonhwa
  surname: Cho
  fullname: Cho, Wonhwa
  email: wcho@uic.edu
  organization: Department of Chemistry, University of Illinois at Chicago, Department of Genetic Engineering, Kyung Hee University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28024150$$D View this record in MEDLINE/PubMed
BookMark eNqNkTtrHDEURkVw8Csu0wZBGje70dVrpSYQjO0EDG4SUgqNRrMro5Em0mxg_n20-IGTKtUV3MPHufrO0FHKySP0HsgaCFOfktv5sQt5TalUb9ApCEFXnEt99PIW5ASd1fpACJMS1DE6oYpQDoKcop_3Zd7lbU424him0OPqU82l4tD7NIdhwXOxqXYh2sUXbOsyjn4uC84DnqKto8VjE2iMx26Xo6-zLzm-Q28HG6u_eJrn6MfN9ferr6u7-9tvV1_uVhPVcl6xTitPqXcCiOu1gq6nsHEge9mD9NoB8IGyvtO8kdwyJxx13cA7q6hlwM7R58fcad-NvnfNudhophJGWxaTbTB_b1LYmW3-bYQGqvSmBVw-BZT8a9_szRiq8zG2g_K-GlAbqkDBf6GCMSE5Zw39-A_6kPelffKBkpoCEUw16sNr-Rfr53oasH4EalulrS-vYog59G-e-zeH_tkf3h-mcw
Cites_doi 10.1016/j.cmet.2008.10.008
10.1126/science.1174621
10.1126/science.1107710
10.1097/00041433-200306000-00006
10.1146/annurev.bi.48.070179.000403
10.15252/embj.201591481
10.1074/jbc.M206885200
10.1038/nrm2336
10.1111/j.1742-4658.2011.08170.x
10.1161/CIRCRESAHA.110.228619
10.1242/jcs.164715
10.1016/j.cell.2005.12.022
10.1074/jbc.M403191200
10.1146/annurev.biochem.78.081307.112144
10.1016/j.cell.2015.02.019
10.1016/j.chemphyslip.2015.08.009
10.1146/annurev.cellbio.22.010305.104656
10.1073/pnas.1309273110
10.1038/nmeth.2368
10.1016/j.cell.2015.01.036
10.1038/ncomms2221
10.1038/nature04399
10.1083/jcb.201407122
10.1007/978-90-481-8622-8_1
10.1016/j.bbalip.2006.03.019
10.1002/iub.1182
10.1002/anie.201408153
10.1016/0304-4157(85)90011-5
10.1038/nbt0307-285
10.1016/j.devcel.2006.07.003
10.1046/j.1432-1033.2002.03338.x
10.1016/j.cub.2004.03.051
10.1091/mbc.e08-07-0785
10.1194/jlr.M500546-JLR200
10.1038/ncomms5393
10.1021/bi9921384
10.1146/annurev.biophys.33.110502.133337
10.1073/pnas.0911581107
10.1016/j.bbamem.2007.03.026
10.1007/978-90-481-8622-8_20
10.1016/j.coph.2012.10.004
10.1186/1471-2121-7-28
10.1126/science.1241908
10.1038/35080071
10.1038/nature14429
10.1038/nchem.1163
10.1101/cshperspect.a004671
10.1161/CIRCRESAHA.114.300738
ContentType Journal Article
Copyright Springer Nature America, Inc. 2016
Copyright Nature Publishing Group Mar 2017
Copyright_xml – notice: Springer Nature America, Inc. 2016
– notice: Copyright Nature Publishing Group Mar 2017
DBID CGR
CUY
CVF
ECM
EIF
NPM
3V.
7QL
7QP
7QR
7TK
7TM
7U9
7X7
7XB
88A
88E
88I
8AO
8FD
8FE
8FG
8FH
8FI
8FJ
8FK
ABJCF
ABUWG
AFKRA
AZQEC
BBNVY
BENPR
BGLVJ
BHPHI
BKSAR
C1K
CCPQU
D1I
DWQXO
FR3
FYUFA
GHDGH
GNUQQ
H94
HCIFZ
K9.
KB.
LK8
M0S
M1P
M2P
M7N
M7P
P64
PCBAR
PDBOC
PQEST
PQQKQ
PQUKI
Q9U
RC3
7X8
5PM
DOI 10.1038/nchembio.2268
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
ProQuest Central (Corporate)
Bacteriology Abstracts (Microbiology B)
Calcium & Calcified Tissue Abstracts
Chemoreception Abstracts
Neurosciences Abstracts
Nucleic Acids Abstracts
Virology and AIDS Abstracts
ProQuest Health & Medical Collection
ProQuest Central (purchase pre-March 2016)
Biology Database (Alumni Edition)
Medical Database (Alumni Edition)
Science Database (Alumni Edition)
ProQuest Pharma Collection
Technology Research Database
ProQuest SciTech Collection
ProQuest Technology Collection
ProQuest Natural Science Collection
Hospital Premium Collection
Hospital Premium Collection (Alumni Edition)
ProQuest Central (Alumni) (purchase pre-March 2016)
Materials Science & Engineering Collection
ProQuest Central (Alumni)
ProQuest Central
ProQuest Central Essentials
Biological Science Collection
ProQuest Central
Technology Collection
Natural Science Collection
Earth, Atmospheric & Aquatic Science Collection
Environmental Sciences and Pollution Management
ProQuest One Community College
ProQuest Materials Science Collection
ProQuest Central Korea
Engineering Research Database
Health Research Premium Collection
Health Research Premium Collection (Alumni)
ProQuest Central Student
AIDS and Cancer Research Abstracts
SciTech Premium Collection
ProQuest Health & Medical Complete (Alumni)
https://resources.nclive.org/materials
Biological Sciences
Health & Medical Collection (Alumni Edition)
Medical Database
Science Database
Algology Mycology and Protozoology Abstracts (Microbiology C)
Biological Science Database
Biotechnology and BioEngineering Abstracts
Earth, Atmospheric & Aquatic Science Database
Materials Science Collection
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Academic
ProQuest One Academic UKI Edition
ProQuest Central Basic
Genetics Abstracts
MEDLINE - Academic
PubMed Central (Full Participant titles)
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
ProQuest Central Student
ProQuest Central Essentials
Nucleic Acids Abstracts
SciTech Premium Collection
Environmental Sciences and Pollution Management
Health Research Premium Collection
Natural Science Collection
Biological Science Collection
Chemoreception Abstracts
ProQuest Medical Library (Alumni)
Virology and AIDS Abstracts
ProQuest Science Journals (Alumni Edition)
ProQuest Biological Science Collection
ProQuest One Academic Eastern Edition
Earth, Atmospheric & Aquatic Science Database
ProQuest Hospital Collection
ProQuest Technology Collection
Health Research Premium Collection (Alumni)
Biological Science Database
Neurosciences Abstracts
ProQuest Hospital Collection (Alumni)
Biotechnology and BioEngineering Abstracts
ProQuest Health & Medical Complete
ProQuest One Academic UKI Edition
Engineering Research Database
ProQuest One Academic
Calcium & Calcified Tissue Abstracts
Technology Collection
Technology Research Database
Materials Science Collection
ProQuest Health & Medical Complete (Alumni)
ProQuest Central (Alumni Edition)
ProQuest One Community College
ProQuest Natural Science Collection
ProQuest Pharma Collection
ProQuest Biology Journals (Alumni Edition)
ProQuest Central
Earth, Atmospheric & Aquatic Science Collection
Genetics Abstracts
Health and Medicine Complete (Alumni Edition)
ProQuest Central Korea
Bacteriology Abstracts (Microbiology B)
Algology Mycology and Protozoology Abstracts (Microbiology C)
AIDS and Cancer Research Abstracts
Materials Science Database
ProQuest Materials Science Collection
ProQuest Central Basic
ProQuest Science Journals
ProQuest SciTech Collection
ProQuest Medical Library
Materials Science & Engineering Collection
ProQuest Central (Alumni)
MEDLINE - Academic
DatabaseTitleList ProQuest Central Student
Nucleic Acids Abstracts
MEDLINE - Academic

MEDLINE
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
– sequence: 3
  dbid: 8FG
  name: ProQuest Technology Collection
  url: https://search.proquest.com/technologycollection1
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Anatomy & Physiology
Chemistry
EISSN 1552-4469
EndPage 274
ExternalDocumentID 4315112131
28024150
10_1038_nchembio_2268
Genre Research Support, Non-U.S. Gov't
Journal Article
Research Support, N.I.H., Extramural
GeographicLocations United States--US
Illinois
Chicago Illinois
GeographicLocations_xml – name: United States--US
– name: Illinois
– name: Chicago Illinois
GrantInformation_xml – fundername: NCI NIH HHS
  grantid: U54 CA202995
– fundername: NIGMS NIH HHS
  grantid: R01 GM110128
– fundername: NHLBI NIH HHS
  grantid: R01 HL073965
– fundername: NIGMS NIH HHS
  grantid: R35 GM122530
– fundername: NHLBI NIH HHS
  grantid: R01 HL083298
– fundername: NIGMS NIH HHS
  grantid: R01 GM068849
– fundername: NCI NIH HHS
  grantid: U54 CA202997
– fundername: NCI NIH HHS
  grantid: U54 CA203000
GroupedDBID ---
0R~
123
29M
39C
3V.
4.4
53G
5BI
70F
7X7
88A
88E
88I
8AO
8FE
8FG
8FH
8FI
8FJ
8R4
8R5
AAEEF
AARCD
AAZLF
ABAWZ
ABDBF
ABJCF
ABJNI
ABLJU
ABUWG
ABVXF
ACGFS
ACGOD
ACIWK
ACPRK
ADBBV
AENEX
AFBBN
AFKRA
AFRAH
AFSHS
AGAYW
AGEZK
AGHTU
AHBCP
AHMBA
AHOSX
AHSBF
AIBTJ
ALFFA
ALIPV
ALMA_UNASSIGNED_HOLDINGS
ARMCB
ASPBG
AVWKF
AXYYD
AZFZN
AZQEC
BBNVY
BENPR
BGLVJ
BHPHI
BKKNO
BKSAR
BPHCQ
BVXVI
CCPQU
CS3
CZ9
D1I
DB5
DU5
DWQXO
EBS
EE.
EJD
EMOBN
ESX
EXGXG
F5P
FEDTE
FQGFK
FSGXE
FYUFA
GNUQQ
HCIFZ
HMCUK
HVGLF
HZ~
KB.
KC.
LK5
LK8
M0L
M1P
M2P
M7P
M7R
NACWA
NNMJJ
O9-
ODYON
P2P
PCBAR
PDBOC
PQQKQ
PROAC
PSQYO
Q2X
RNT
RNTTT
SHXYY
SIXXV
SJN
SNYQT
SV3
TAOOD
TBHMF
TDRGL
TSG
TUS
UKHRP
~8M
AAYZH
CGR
CUY
CVF
ECM
EIF
NPM
7QL
7QP
7QR
7TK
7TM
7U9
7XB
8FD
8FK
ACBWK
C1K
FR3
H94
K9.
M7N
P64
PQEST
PQUKI
Q9U
RC3
7X8
5PM
ID FETCH-LOGICAL-p296t-3b98e22ec510cd981bd217c16d6d16e9c114f23db94b984a3c5c2cbf4ba82a313
IEDL.DBID 8FG
ISSN 1552-4450
IngestDate Tue Sep 17 21:26:33 EDT 2024
Wed Dec 04 14:37:45 EST 2024
Wed Dec 04 04:40:18 EST 2024
Tue Nov 19 05:07:09 EST 2024
Wed Oct 16 01:00:33 EDT 2024
Fri Oct 11 20:52:27 EDT 2024
IsPeerReviewed true
IsScholarly true
Issue 3
Language English
License Reprints and permissions information is available online at http://www.nature.com/reprints/index.html.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-p296t-3b98e22ec510cd981bd217c16d6d16e9c114f23db94b984a3c5c2cbf4ba82a313
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
These authors contributed equally to this work.
PMID 28024150
PQID 1869210538
PQPubID 29034
PageCount 7
ParticipantIDs pubmedcentral_primary_oai_pubmedcentral_nih_gov_5912897
proquest_miscellaneous_1872818197
proquest_miscellaneous_1853356443
proquest_journals_1869210538
pubmed_primary_28024150
springer_journals_10_1038_nchembio_2268
PublicationCentury 2000
PublicationDate 2017-03-01
PublicationDateYYYYMMDD 2017-03-01
PublicationDate_xml – month: 03
  year: 2017
  text: 2017-03-01
  day: 01
PublicationDecade 2010
PublicationPlace New York
PublicationPlace_xml – name: New York
– name: United States
– name: Cambridge
PublicationTitle Nature chemical biology
PublicationTitleAbbrev Nat Chem Biol
PublicationTitleAlternate Nat Chem Biol
PublicationYear 2017
Publisher Nature Publishing Group US
Nature Publishing Group
Publisher_xml – name: Nature Publishing Group US
– name: Nature Publishing Group
References Sumandea, Das, Sumandea, Cho (CR31) 1999; 38
Farrand, LaChapelle, Hotze, Johnson, Tweten (CR35) 2010; 107
Goldstein, Brown (CR7) 2015; 161
Brachet (CR17) 2015; 208
Irvine (CR26) 2004; 14
Frechin (CR18) 2015; 523
Maekawa, Fairn (CR24) 2015; 128
Yoon, Lee, Kurilova, Cho (CR27) 2011; 3
Chu (CR43) 2015; 161
Voelker (CR39) 2009; 78
Das, Goldstein, Anderson, Brown, Radhakrishnan (CR23) 2013; 110
Raiborg, Wenzel, Stenmark (CR41) 2015; 34
van Meer (CR2) 2011; 3
Radhakrishnan, Goldstein, McDonald, Brown (CR34) 2008; 8
Várnai, Balla (CR25) 2006; 1761
Hamilton (CR38) 2003; 14
Stahelin (CR51) 2004; 279
Goldstein, DeBose-Boyd, Brown (CR20) 2006; 124
Mondal, Mesmin, Mukherjee, Maxfield (CR22) 2009; 20
Wang, Weng, Anderson (CR16) 2005; 307
Chang, Chang, Ohgami, Yamauchi (CR40) 2006; 22
Luu, Sharpe, Gelissen, Brown (CR45) 2013; 65
Kobayashi (CR44) 2006; 47
Yamamoto, Komekado, Kikuchi (CR52) 2006; 11
Ramachandran, Heuck, Tweten, Johnson (CR28) 2002; 9
Amanchy (CR47) 2007; 25
Sheng (CR15) 2014; 5
Murate, Kobayashi (CR3) 2016; 194
CR10
Hulce, Cognetta, Niphakis, Tully, Cravatt (CR13) 2013; 10
Pagler (CR19) 2011; 108
Lange, Swaisgood, Ramos, Steck (CR8) 1989; 264
Shimada, Maruya, Iwashita, Ohno-Iwashita (CR29) 2002; 269
Sprong, van der Sluijs, van Meer (CR37) 2001; 2
Nagao, Tomioka, Ueda (CR46) 2011; 278
Gimpl (CR21) 2010; 51
Ray, Skipski, Barclay, Essner, Archibald (CR9) 1969; 244
Silvente-Poirot, Poirot (CR49) 2012; 12
Zidovetzki, Levitan (CR36) 2007; 1768
Nelson (CR50) 2013; 342
Blitzer, Nusse (CR53) 2006; 7
Maxfield, Tabas (CR5) 2005; 438
Fantini, Barrantes (CR11) 2013; 4
Westerterp (CR42) 2014; 114
Yeagle (CR4) 1985; 822
Heuck, Moe, Johnson (CR30) 2010; 51
Cho, Stahelin (CR32) 2005; 34
Ikonen (CR6) 2008; 9
Lingwood, Simons (CR12) 2010; 327
Sheng (CR14) 2012; 3
Op den Kamp (CR1) 1979; 48
Tanaka (CR48) 2003; 278
Liu (CR33) 2014; 53
23450735 - Front Physiol. 2013 Feb 28;4:31
2917977 - J Biol Chem. 1989 Mar 5;264(7):3786-93
24385509 - Circ Res. 2014 Jan 3;114(1):157-70
21436058 - Cold Spring Harb Perspect Biol. 2011 May 01;3(5):null
11433364 - Nat Rev Mol Cell Biol. 2001 Jul;2(7):504-13
15084300 - Curr Biol. 2004 Apr 20;14(8):R308-10
25753037 - J Cell Biol. 2015 Mar 16;208(6):791-806
16319881 - Nature. 2005 Dec 1;438(7068):612-21
15746430 - Science. 2005 Mar 4;307(5714):1472-6
15869386 - Annu Rev Biophys Biomol Struct. 2005;34:119-51
23396283 - Nat Methods. 2013 Mar;10(3):259-64
26009010 - Nature. 2015 Jul 2;523(7558):88-91
25815993 - Cell. 2015 Mar 26;161(1):161-72
25024088 - Nat Commun. 2014 Jul 15;5:4393
21554545 - FEBS J. 2011 Sep;278(18):3190-203
18216769 - Nat Rev Mol Cell Biol. 2008 Feb;9(2):125-38
4310600 - J Biol Chem. 1969 Oct 25;244(20):5528-36
16824228 - BMC Cell Biol. 2006 Jul 06;7:28
24288332 - Science. 2013 Nov 29;342(6162):1094-8
19489735 - Annu Rev Biochem. 2009;78:827-56
24920391 - Elife. 2014 Jun 11;3:null
21148432 - Circ Res. 2011 Jan 21;108(2):194-200
16702602 - J Lipid Res. 2006 Aug;47(8):1791-802
20213539 - Subcell Biochem. 2010;51:1-45
12840657 - Curr Opin Lipidol. 2003 Jun;14(3):263-71
10587453 - Biochemistry. 1999 Dec 7;38(49):16290-7
22024883 - Nat Chem. 2011 Oct 09;3(11):868-74
25860611 - Cell. 2015 Apr 9;161(2):291-306
16702024 - Biochim Biophys Acta. 2006 Aug;1761(8):957-67
19019985 - Mol Biol Cell. 2009 Jan;20(2):581-8
20044567 - Science. 2010 Jan 1;327(5961):46-50
26319805 - Chem Phys Lipids. 2016 Jan;194:58-71
12509412 - J Biol Chem. 2003 Mar 7;278(10):8815-9
23103112 - Curr Opin Pharmacol. 2012 Dec;12(6):673-6
3904832 - Biochim Biophys Acta. 1985 Dec 9;822(3-4):267-87
23847008 - IUBMB Life. 2013 Aug;65(8):675-84
26041457 - EMBO J. 2015 Jul 14;34(14):1848-58
20145114 - Proc Natl Acad Sci U S A. 2010 Mar 2;107(9):4341-6
17493580 - Biochim Biophys Acta. 2007 Jun;1768(6):1311-24
15105418 - J Biol Chem. 2004 Jul 9;279(28):29501-12
12368903 - Nat Struct Biol. 2002 Nov;9(11):823-7
17344875 - Nat Biotechnol. 2007 Mar;25(3):285-6
16753029 - Annu Rev Cell Dev Biol. 2006;22:129-57
23754385 - Proc Natl Acad Sci U S A. 2013 Jun 25;110(26):10580-5
16890161 - Dev Cell. 2006 Aug;11(2):213-23
12473115 - Eur J Biochem. 2002 Dec;269(24):6195-203
20213558 - Subcell Biochem. 2010;51:551-77
16413480 - Cell. 2006 Jan 13;124(1):35-46
25663704 - J Cell Sci. 2015 Apr 1;128(7):1422-33
382989 - Annu Rev Biochem. 1979;48:47-71
30422112 - Elife. 2018 Nov 13;7
25345859 - Angew Chem Int Ed Engl. 2014 Dec 22;53(52):14387-91
19041766 - Cell Metab. 2008 Dec;8(6):512-21
23212378 - Nat Commun. 2012;3:1249
References_xml – volume: 8
  start-page: 512
  year: 2008
  end-page: 521
  ident: CR34
  article-title: Switch-like control of SREBP-2 transport triggered by small changes in ER cholesterol: a delicate balance
  publication-title: Cell Metab.
  doi: 10.1016/j.cmet.2008.10.008
  contributor:
    fullname: Brown
– volume: 327
  start-page: 46
  year: 2010
  end-page: 50
  ident: CR12
  article-title: Lipid rafts as a membrane-organizing principle
  publication-title: Science
  doi: 10.1126/science.1174621
  contributor:
    fullname: Simons
– volume: 307
  start-page: 1472
  year: 2005
  end-page: 1476
  ident: CR16
  article-title: OSBP is a cholesterol-regulated scaffolding protein in control of ERK 1/2 activation
  publication-title: Science
  doi: 10.1126/science.1107710
  contributor:
    fullname: Anderson
– volume: 14
  start-page: 263
  year: 2003
  end-page: 271
  ident: CR38
  article-title: Fast flip-flop of cholesterol and fatty acids in membranes: implications for membrane transport proteins
  publication-title: Curr. Opin. Lipidol.
  doi: 10.1097/00041433-200306000-00006
  contributor:
    fullname: Hamilton
– volume: 48
  start-page: 47
  year: 1979
  end-page: 71
  ident: CR1
  article-title: Lipid asymmetry in membranes
  publication-title: Annu. Rev. Biochem.
  doi: 10.1146/annurev.bi.48.070179.000403
  contributor:
    fullname: Op den Kamp
– volume: 34
  start-page: 1848
  year: 2015
  end-page: 1858
  ident: CR41
  article-title: ER-endosome contact sites: molecular compositions and functions
  publication-title: EMBO J.
  doi: 10.15252/embj.201591481
  contributor:
    fullname: Stenmark
– volume: 278
  start-page: 8815
  year: 2003
  end-page: 8819
  ident: CR48
  article-title: Effects of mutations of ABCA1 in the first extracellular domain on subcellular trafficking and ATP binding/hydrolysis
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.M206885200
  contributor:
    fullname: Tanaka
– volume: 9
  start-page: 125
  year: 2008
  end-page: 138
  ident: CR6
  article-title: Cellular cholesterol trafficking and compartmentalization
  publication-title: Nat. Rev. Mol. Cell Biol.
  doi: 10.1038/nrm2336
  contributor:
    fullname: Ikonen
– volume: 244
  start-page: 5528
  year: 1969
  end-page: 5536
  ident: CR9
  article-title: Lipid composition of rat liver plasma membranes
  publication-title: J. Biol. Chem.
  contributor:
    fullname: Archibald
– volume: 278
  start-page: 3190
  year: 2011
  end-page: 3203
  ident: CR46
  article-title: Function and regulation of ABCA1--membrane meso-domain organization and reorganization
  publication-title: FEBS J.
  doi: 10.1111/j.1742-4658.2011.08170.x
  contributor:
    fullname: Ueda
– volume: 108
  start-page: 194
  year: 2011
  end-page: 200
  ident: CR19
  article-title: Deletion of ABCA1 and ABCG1 impairs macrophage migration because of increased Rac1 signaling
  publication-title: Circ. Res.
  doi: 10.1161/CIRCRESAHA.110.228619
  contributor:
    fullname: Pagler
– volume: 128
  start-page: 1422
  year: 2015
  end-page: 1433
  ident: CR24
  article-title: Complementary probes reveal that phosphatidylserine is required for the proper transbilayer distribution of cholesterol
  publication-title: J. Cell Sci.
  doi: 10.1242/jcs.164715
  contributor:
    fullname: Fairn
– volume: 124
  start-page: 35
  year: 2006
  end-page: 46
  ident: CR20
  article-title: Protein sensors for membrane sterols
  publication-title: Cell
  doi: 10.1016/j.cell.2005.12.022
  contributor:
    fullname: Brown
– volume: 279
  start-page: 29501
  year: 2004
  end-page: 29512
  ident: CR51
  article-title: Mechanism of diacylglycerol-induced membrane targeting and activation of protein kinase Cdelta
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.M403191200
  contributor:
    fullname: Stahelin
– volume: 78
  start-page: 827
  year: 2009
  end-page: 856
  ident: CR39
  article-title: Genetic and biochemical analysis of non-vesicular lipid traffic
  publication-title: Annu. Rev. Biochem.
  doi: 10.1146/annurev.biochem.78.081307.112144
  contributor:
    fullname: Voelker
– volume: 161
  start-page: 291
  year: 2015
  end-page: 306
  ident: CR43
  article-title: Cholesterol transport through lysosome-peroxisome membrane contacts
  publication-title: Cell
  doi: 10.1016/j.cell.2015.02.019
  contributor:
    fullname: Chu
– volume: 194
  start-page: 58
  year: 2016
  end-page: 71
  ident: CR3
  article-title: Revisiting transbilayer distribution of lipids in the plasma membrane
  publication-title: Chem. Phys. Lipids
  doi: 10.1016/j.chemphyslip.2015.08.009
  contributor:
    fullname: Kobayashi
– volume: 22
  start-page: 129
  year: 2006
  end-page: 157
  ident: CR40
  article-title: Cholesterol sensing, trafficking, and esterification
  publication-title: Annu. Rev. Cell Dev. Biol.
  doi: 10.1146/annurev.cellbio.22.010305.104656
  contributor:
    fullname: Yamauchi
– volume: 110
  start-page: 10580
  year: 2013
  end-page: 10585
  ident: CR23
  article-title: Use of mutant 125I-perfringolysin O to probe transport and organization of cholesterol in membranes of animal cells
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.1309273110
  contributor:
    fullname: Radhakrishnan
– volume: 4
  start-page: 31
  year: 2013
  ident: CR11
  article-title: How cholesterol interacts with membrane proteins: an exploration of cholesterol-binding sites including CRAC, CARC, and tilted domains
  publication-title: Front. Physiol.
  contributor:
    fullname: Barrantes
– volume: 10
  start-page: 259
  year: 2013
  end-page: 264
  ident: CR13
  article-title: Proteome-wide mapping of cholesterol-interacting proteins in mammalian cells
  publication-title: Nat. Methods
  doi: 10.1038/nmeth.2368
  contributor:
    fullname: Cravatt
– volume: 161
  start-page: 161
  year: 2015
  end-page: 172
  ident: CR7
  article-title: A century of cholesterol and coronaries: from plaques to genes to statins
  publication-title: Cell
  doi: 10.1016/j.cell.2015.01.036
  contributor:
    fullname: Brown
– volume: 264
  start-page: 3786
  year: 1989
  end-page: 3793
  ident: CR8
  article-title: Plasma membranes contain half the phospholipid and 90% of the cholesterol and sphingomyelin in cultured human fibroblasts
  publication-title: J. Biol. Chem.
  contributor:
    fullname: Steck
– volume: 3
  start-page: 1249
  year: 2012
  ident: CR14
  article-title: Cholesterol modulates cell signaling and protein networking by specifically interacting with PDZ domain-containing scaffold proteins
  publication-title: Nat. Commun.
  doi: 10.1038/ncomms2221
  contributor:
    fullname: Sheng
– volume: 9
  start-page: 823
  year: 2002
  end-page: 827
  ident: CR28
  article-title: Structural insights into the membrane-anchoring mechanism of a cholesterol-dependent cytolysin
  publication-title: Nat. Struct. Biol.
  contributor:
    fullname: Johnson
– volume: 438
  start-page: 612
  year: 2005
  end-page: 621
  ident: CR5
  article-title: Role of cholesterol and lipid organization in disease
  publication-title: Nature
  doi: 10.1038/nature04399
  contributor:
    fullname: Tabas
– volume: 208
  start-page: 791
  year: 2015
  end-page: 806
  ident: CR17
  article-title: LTP-triggered cholesterol redistribution activates Cdc42 and drives AMPA receptor synaptic delivery
  publication-title: J. Cell Biol.
  doi: 10.1083/jcb.201407122
  contributor:
    fullname: Brachet
– volume: 51
  start-page: 1
  year: 2010
  end-page: 45
  ident: CR21
  article-title: Cholesterol-protein interaction: methods and cholesterol reporter molecules
  publication-title: Subcell. Biochem.
  doi: 10.1007/978-90-481-8622-8_1
  contributor:
    fullname: Gimpl
– volume: 1761
  start-page: 957
  year: 2006
  end-page: 967
  ident: CR25
  article-title: Live cell imaging of phosphoinositide dynamics with fluorescent protein domains
  publication-title: Biochim. Biophys. Acta
  doi: 10.1016/j.bbalip.2006.03.019
  contributor:
    fullname: Balla
– volume: 65
  start-page: 675
  year: 2013
  end-page: 684
  ident: CR45
  article-title: The role of signalling in cellular cholesterol homeostasis
  publication-title: IUBMB Life
  doi: 10.1002/iub.1182
  contributor:
    fullname: Brown
– volume: 53
  start-page: 14387
  year: 2014
  end-page: 14391
  ident: CR33
  article-title: Simultaneous in situ quantification of two cellular lipid pools using orthogonal fluorescent sensors
  publication-title: Angew. Chem. Int. Edn Engl.
  doi: 10.1002/anie.201408153
  contributor:
    fullname: Liu
– volume: 822
  start-page: 267
  year: 1985
  end-page: 287
  ident: CR4
  article-title: Cholesterol and the cell membrane
  publication-title: Biochim. Biophys. Acta
  doi: 10.1016/0304-4157(85)90011-5
  contributor:
    fullname: Yeagle
– volume: 25
  start-page: 285
  year: 2007
  end-page: 286
  ident: CR47
  article-title: A curated compendium of phosphorylation motifs
  publication-title: Nat. Biotechnol.
  doi: 10.1038/nbt0307-285
  contributor:
    fullname: Amanchy
– ident: CR10
– volume: 11
  start-page: 213
  year: 2006
  end-page: 223
  ident: CR52
  article-title: Caveolin is necessary for Wnt-3a-dependent internalization of LRP6 and accumulation of beta-catenin
  publication-title: Dev. Cell
  doi: 10.1016/j.devcel.2006.07.003
  contributor:
    fullname: Kikuchi
– volume: 269
  start-page: 6195
  year: 2002
  end-page: 6203
  ident: CR29
  article-title: The C-terminal domain of perfringolysin O is an essential cholesterol-binding unit targeting to cholesterol-rich microdomains
  publication-title: Eur. J. Biochem.
  doi: 10.1046/j.1432-1033.2002.03338.x
  contributor:
    fullname: Ohno-Iwashita
– volume: 14
  start-page: R308
  year: 2004
  end-page: R310
  ident: CR26
  article-title: Inositol lipids: to PHix or not to PHix?
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2004.03.051
  contributor:
    fullname: Irvine
– volume: 20
  start-page: 581
  year: 2009
  end-page: 588
  ident: CR22
  article-title: Sterols are mainly in the cytoplasmic leaflet of the plasma membrane and the endocytic recycling compartment in CHO cells
  publication-title: Mol. Biol. Cell
  doi: 10.1091/mbc.e08-07-0785
  contributor:
    fullname: Maxfield
– volume: 47
  start-page: 1791
  year: 2006
  end-page: 1802
  ident: CR44
  article-title: Efflux of sphingomyelin, cholesterol, and phosphatidylcholine by ABCG1
  publication-title: J. Lipid Res.
  doi: 10.1194/jlr.M500546-JLR200
  contributor:
    fullname: Kobayashi
– volume: 5
  start-page: 4393
  year: 2014
  ident: CR15
  article-title: Cholesterol selectively activates canonical Wnt signalling over non-canonical Wnt signalling
  publication-title: Nat. Commun.
  doi: 10.1038/ncomms5393
  contributor:
    fullname: Sheng
– volume: 38
  start-page: 16290
  year: 1999
  end-page: 16297
  ident: CR31
  article-title: Roles of aromatic residues in high interfacial activity of Naja naja atra phospholipase A2
  publication-title: Biochemistry
  doi: 10.1021/bi9921384
  contributor:
    fullname: Cho
– volume: 34
  start-page: 119
  year: 2005
  end-page: 151
  ident: CR32
  article-title: Membrane-protein interactions in cell signaling and membrane trafficking
  publication-title: Annu. Rev. Biophys. Biomol. Struct.
  doi: 10.1146/annurev.biophys.33.110502.133337
  contributor:
    fullname: Stahelin
– volume: 107
  start-page: 4341
  year: 2010
  end-page: 4346
  ident: CR35
  article-title: Only two amino acids are essential for cytolytic toxin recognition of cholesterol at the membrane surface
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.0911581107
  contributor:
    fullname: Tweten
– volume: 1768
  start-page: 1311
  year: 2007
  end-page: 1324
  ident: CR36
  article-title: Use of cyclodextrins to manipulate plasma membrane cholesterol content: evidence, misconceptions and control strategies
  publication-title: Biochim. Biophys. Acta
  doi: 10.1016/j.bbamem.2007.03.026
  contributor:
    fullname: Levitan
– volume: 51
  start-page: 551
  year: 2010
  end-page: 577
  ident: CR30
  article-title: The cholesterol-dependent cytolysin family of gram-positive bacterial toxins
  publication-title: Subcell. Biochem.
  doi: 10.1007/978-90-481-8622-8_20
  contributor:
    fullname: Johnson
– volume: 12
  start-page: 673
  year: 2012
  end-page: 676
  ident: CR49
  article-title: Cholesterol metabolism and cancer: the good, the bad and the ugly
  publication-title: Curr. Opin. Pharmacol.
  doi: 10.1016/j.coph.2012.10.004
  contributor:
    fullname: Poirot
– volume: 7
  start-page: 28
  year: 2006
  ident: CR53
  article-title: A critical role for endocytosis in Wnt signaling
  publication-title: BMC Cell Biol.
  doi: 10.1186/1471-2121-7-28
  contributor:
    fullname: Nusse
– volume: 342
  start-page: 1094
  year: 2013
  end-page: 1098
  ident: CR50
  article-title: 27-Hydroxycholesterol links hypercholesterolemia and breast cancer pathophysiology
  publication-title: Science
  doi: 10.1126/science.1241908
  contributor:
    fullname: Nelson
– volume: 2
  start-page: 504
  year: 2001
  end-page: 513
  ident: CR37
  article-title: How proteins move lipids and lipids move proteins
  publication-title: Nat. Rev. Mol. Cell Biol.
  doi: 10.1038/35080071
  contributor:
    fullname: van Meer
– volume: 523
  start-page: 88
  year: 2015
  end-page: 91
  ident: CR18
  article-title: Cell-intrinsic adaptation of lipid composition to local crowding drives social behaviour
  publication-title: Nature
  doi: 10.1038/nature14429
  contributor:
    fullname: Frechin
– volume: 3
  start-page: 868
  year: 2011
  end-page: 874
  ident: CR27
  article-title: quantitative imaging of cellular lipids using molecular sensors
  publication-title: Nat. Chem.
  doi: 10.1038/nchem.1163
  contributor:
    fullname: Cho
– volume: 3
  start-page: a004671
  year: 2011
  ident: CR2
  article-title: Dynamic transbilayer lipid asymmetry
  publication-title: Cold Spring Harb. Perspect. Biol.
  doi: 10.1101/cshperspect.a004671
  contributor:
    fullname: van Meer
– volume: 114
  start-page: 157
  year: 2014
  end-page: 170
  ident: CR42
  article-title: ATP-binding cassette transporters, atherosclerosis, and inflammation
  publication-title: Circ. Res.
  doi: 10.1161/CIRCRESAHA.114.300738
  contributor:
    fullname: Westerterp
SSID ssj0036618
Score 2.6200333
Snippet Orthogonal cholesterol sensors that are useful for imaging cholesterol in the plasma membrane leaflets reveal an asymmetry in which a high outer leaflet...
Controlled distribution of lipids across various cell membranes is crucial for cell homeostasis and regulation. We developed an imaging method that allows...
SourceID pubmedcentral
proquest
pubmed
springer
SourceType Open Access Repository
Aggregation Database
Index Database
Publisher
StartPage 268
SubjectTerms 631/80/86
631/92/287
631/92/314
631/92/96
Asymmetry
Biochemical Engineering
Biochemistry
Bioorganic Chemistry
Cell Biology
Cell Line
Cell Membrane - chemistry
Chemistry
Chemistry/Food Science
Cholesterol
Cholesterol - analysis
HEK293 Cells
Homeostasis
Humans
Hyperlipidemia
Lipids
Lipids - chemistry
Membranes
Sensors
Title Orthogonal lipid sensors identify transbilayer asymmetry of plasma membrane cholesterol
URI https://link.springer.com/article/10.1038/nchembio.2268
https://www.ncbi.nlm.nih.gov/pubmed/28024150
https://www.proquest.com/docview/1869210538
https://search.proquest.com/docview/1853356443
https://search.proquest.com/docview/1872818197
https://pubmed.ncbi.nlm.nih.gov/PMC5912897
Volume 13
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1Lb9QwEB7R9gAXBC2PhbIyEoKTaWIndnJCpepSIVEQomJvUfyikTYPNulh_z1jb1IooJ49seIZe-Ybz3gG4JUSUkQutVRypmkS25yWknGqTSKlsWhUrH8o_OlcnF0kH5fpcrxw68e0ykknBkVtWu3vyI986yR0T_B8vut-Ut81ykdXxxYaO7AXMyl8Sl-2-DBpYo62JzyFS1NGkySNxhqbEc-OGmRJrar2LcKP7H_o8t8kyb8ipcEALR7A_RE5kuOtqB_CHdvsw8Fxg15zvSGvScjlDJfk-3D3ZOrjdgDfP6-Hy_aHR9xkVXWVIT26ru26J1V4pOs2ZPAGS1WrEvE3KftNXVv8lLSOdAiu65LUuAqkscQry1BboV09govF6beTMzq2U6Ady8VAucozy5jVeAy1yRGvGvRHdCyMMLGwuUbXyDFuVJ4gZVJynWqmlUtUmbGSx_wx7DZtY58CQV4jt5USlqNMRZmlLuLORcYmZeScncHhxNBiPBN98VuCM3h5PYzM8CEKXEJ75WkQfqaI0fhtNNKXsIpzOYMnWxkV3bY0R8GyyEOSaAbyhvSuCXw17ZsjTXUZqmqnOZpqP-ebSc5__LqP1POsmHZN4XfNs9sX-RzuMQ8BQr7aIewO6yv7AgHMoOawI5dyHvbqHPben55_-foLSYL3WA
link.rule.ids 230,314,780,784,885,12056,12765,21388,27924,27925,31719,31720,33373,33374,33744,33745,43310,43600,43805,73745,74035,74302
linkProvider ProQuest
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1Lb9QwELagHMoFQctjoYCREJxME7-SnFBVsSzQlksreov8bCNtHmzSw_57xt6kUEA9e2LFHnvmG88LobdaZjLxwpGMUUN46gqiMsqIsTzLrAOl4kKi8PGJXJzxr-fifHxw68ewykkmRkFtWxPeyPdD6yQwT-B-fux-ktA1KnhXxxYad9E9zkB1h0zx-edJEjPQPTEVTghKOBfJWGMzYfl-A1tS66r9APAj_x-6_DdI8i9PaVRA84fowYgc8cGG1Y_QHdfsoN2DBqzmeo3f4RjLGR_Jd9D24dTHbRf9-L4aLtuLgLjxsuoqi3swXdtVj6uYpOvXeAgKS1dLBfgbq35d1w4-xa3HHYDrWuEaVgE0DgdhGWsrtMvH6Gz-6fRwQcZ2CqSjhRwI00XuKHUGrqGxBeBVC_aISaWVNpWuMGAaecqsLjhQcsWMMNRoz7XKqWIpe4K2mrZxzxCmGbBYaC0dA55KlQufMO8T67hKvHcztDdtaDneib78zcEZenM9DJsRXBSwhPYq0AD8FIDR2G00WShhlRbZDD3d8KjsNqU5SponAZIkM5Td4N41QaimfXOkqS5jVW1RgKoOc76f-PzHrwdPPcvL6dSU4dQ8v32Rr9H24vT4qDz6cvLtBbpPAxyIsWt7aGtYXbmXAGYG_Sqe2F9dIfe5
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1Lb9QwEB7BVgIuqLQ8FlowEoKTaWLHcXJCbemqvJYKUdFbFL9opM2DTXrYf884m7QUUM-eWLFnPPONZzwD8ErFMg6csFRypmkU2pTmknGqTSSlsWhUrH8o_GUeH59GH8_E2ZD_1A5plaNO7BW1qbW_I9_zrZPQPcHzueeGtIiT97N3zS_qO0j5SOvQTuM2bKBVDNgENg6O5iffRr3M0RL1D-OEYDSKRDBU3Axwxgo3qFRF_RbBSPI_rPlvyuRfcdPeHM024f6AI8n-mvEP4JattmB7v0IfulyR16TP7OyvzLfg7uHY1W0bfnxdduf1T4-_yaJoCkNadGTrZUuK_smuW5HOmy9VLHJE4yRvV2Vp8VNSO9Ig1C5zUuIqkMYSrzr7Sgv14iGczo6-Hx7TobkCbVgad5SrNLGMWY2HUpsU0atB70SHsYlNGNtUo6PkGDcqjZAyyrkWmmnlIpUnLOchfwSTqq7sEyBMIsOFUrHlyOE4T4QLuHOBsVEeOGensDNuaDackDa74ucUXl4O42b4gAUuob7wNAhGBSI2fhON9AWtwlRO4fGaR1mzLtSRsSTwACWYgrzGvUsCX1v7-khVnPc1tkWKhtvP-Wbk8x-_7uP2PMlGqcm81Dy9eZEv4A6Ka_b5w_zTM7jHPDboE9l2YNItL-wuIptOPR9E9jfa2v1V
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Orthogonal+lipid+sensors+identify+transbilayer+asymmetry+of+plasma+membrane+cholesterol&rft.jtitle=Nature+chemical+biology&rft.au=Liu%2C+Shu-Lin&rft.au=Sheng%2C+Ren&rft.au=Jung%2C+Jae+Hun&rft.au=Wang%2C+Li&rft.date=2017-03-01&rft.pub=Nature+Publishing+Group+US&rft.issn=1552-4450&rft.eissn=1552-4469&rft.volume=13&rft.issue=3&rft.spage=268&rft.epage=274&rft_id=info:doi/10.1038%2Fnchembio.2268&rft.externalDocID=10_1038_nchembio_2268
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1552-4450&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1552-4450&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1552-4450&client=summon