Physicochemical properties of the vacuolar membrane and cellular factors determine formation of vacuolar invaginations
Vacuoles change their morphology in response to stress. In yeast exposed to chronically high temperatures, vacuolar membranes get deformed and invaginations are formed. We show that phase-separation of vacuolar membrane occurred after heat stress leading to the formation of the invagination. In addi...
Saved in:
| Published in: | Scientific reports Vol. 13; no. 1; p. 16187 |
|---|---|
| Main Authors: | , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
London
Nature Publishing Group UK
27-09-2023
Nature Publishing Group Nature Portfolio |
| Subjects: | |
| Online Access: | Get full text |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| Abstract | Vacuoles change their morphology in response to stress. In yeast exposed to chronically high temperatures, vacuolar membranes get deformed and invaginations are formed. We show that phase-separation of vacuolar membrane occurred after heat stress leading to the formation of the invagination. In addition, Hfl1, a vacuolar membrane-localized Atg8-binding protein, was found to suppress the excess vacuolar invaginations after heat stress. At that time, Hfl1 formed foci at the neck of the invaginations in wild-type cells, whereas it was efficiently degraded in the vacuole in the
atg8
Δ mutant. Genetic analysis showed that the endosomal sorting complex required for transport machinery was necessary to form the invaginations irrespective of Atg8 or Hfl1. In contrast, a combined mutation with the vacuole BAR domain protein Ivy1 led to vacuoles in
hfl1
Δ
ivy1
Δ and
atg8
Δ
ivy1
Δ mutants having constitutively invaginated structures; moreover, these mutants showed stress-sensitive phenotypes. Our findings suggest that vacuolar invaginations result from the combination of changes in the physiochemical properties of the vacuolar membrane and other cellular factors. |
|---|---|
| AbstractList | Vacuoles change their morphology in response to stress. In yeast exposed to chronically high temperatures, vacuolar membranes get deformed and invaginations are formed. We show that phase-separation of vacuolar membrane occurred after heat stress leading to the formation of the invagination. In addition, Hfl1, a vacuolar membrane-localized Atg8-binding protein, was found to suppress the excess vacuolar invaginations after heat stress. At that time, Hfl1 formed foci at the neck of the invaginations in wild-type cells, whereas it was efficiently degraded in the vacuole in the
atg8
Δ mutant. Genetic analysis showed that the endosomal sorting complex required for transport machinery was necessary to form the invaginations irrespective of Atg8 or Hfl1. In contrast, a combined mutation with the vacuole BAR domain protein Ivy1 led to vacuoles in
hfl1
Δ
ivy1
Δ and
atg8
Δ
ivy1
Δ mutants having constitutively invaginated structures; moreover, these mutants showed stress-sensitive phenotypes. Our findings suggest that vacuolar invaginations result from the combination of changes in the physiochemical properties of the vacuolar membrane and other cellular factors. Vacuoles change their morphology in response to stress. In yeast exposed to chronically high temperatures, vacuolar membranes get deformed and invaginations are formed. We show that phase-separation of vacuolar membrane occurred after heat stress leading to the formation of the invagination. In addition, Hfl1, a vacuolar membrane-localized Atg8-binding protein, was found to suppress the excess vacuolar invaginations after heat stress. At that time, Hfl1 formed foci at the neck of the invaginations in wild-type cells, whereas it was efficiently degraded in the vacuole in the atg8Δ mutant. Genetic analysis showed that the endosomal sorting complex required for transport machinery was necessary to form the invaginations irrespective of Atg8 or Hfl1. In contrast, a combined mutation with the vacuole BAR domain protein Ivy1 led to vacuoles in hfl1Δivy1Δ and atg8Δivy1Δ mutants having constitutively invaginated structures; moreover, these mutants showed stress-sensitive phenotypes. Our findings suggest that vacuolar invaginations result from the combination of changes in the physiochemical properties of the vacuolar membrane and other cellular factors. Abstract Vacuoles change their morphology in response to stress. In yeast exposed to chronically high temperatures, vacuolar membranes get deformed and invaginations are formed. We show that phase-separation of vacuolar membrane occurred after heat stress leading to the formation of the invagination. In addition, Hfl1, a vacuolar membrane-localized Atg8-binding protein, was found to suppress the excess vacuolar invaginations after heat stress. At that time, Hfl1 formed foci at the neck of the invaginations in wild-type cells, whereas it was efficiently degraded in the vacuole in the atg8Δ mutant. Genetic analysis showed that the endosomal sorting complex required for transport machinery was necessary to form the invaginations irrespective of Atg8 or Hfl1. In contrast, a combined mutation with the vacuole BAR domain protein Ivy1 led to vacuoles in hfl1Δivy1Δ and atg8Δivy1Δ mutants having constitutively invaginated structures; moreover, these mutants showed stress-sensitive phenotypes. Our findings suggest that vacuolar invaginations result from the combination of changes in the physiochemical properties of the vacuolar membrane and other cellular factors. |
| ArticleNumber | 16187 |
| Author | Higuchi, Miyuki Kimura, Masafumi Tsuji, Takuma Fujimoto, Toyoshi Watanabe, Yuki Kimura, Yoko Shimizu, Yosuke |
| Author_xml | – sequence: 1 givenname: Yoko surname: Kimura fullname: Kimura, Yoko email: kimura.yoko@shizuoka.ac.jp organization: Graduate School of Integrated Science and Technology, Shizuoka University, Department of Agriculture, Shizuoka University – sequence: 2 givenname: Takuma surname: Tsuji fullname: Tsuji, Takuma organization: Laboratory of Molecular Cell Biology, Research Institute for Diseases of Old Age, Juntendo University Graduate School of Medicine – sequence: 3 givenname: Yosuke surname: Shimizu fullname: Shimizu, Yosuke organization: Graduate School of Integrated Science and Technology, Shizuoka University – sequence: 4 givenname: Yuki surname: Watanabe fullname: Watanabe, Yuki organization: Graduate School of Integrated Science and Technology, Shizuoka University – sequence: 5 givenname: Masafumi surname: Kimura fullname: Kimura, Masafumi organization: Graduate School of Integrated Science and Technology, Shizuoka University – sequence: 6 givenname: Toyoshi surname: Fujimoto fullname: Fujimoto, Toyoshi organization: Laboratory of Molecular Cell Biology, Research Institute for Diseases of Old Age, Juntendo University Graduate School of Medicine – sequence: 7 givenname: Miyuki surname: Higuchi fullname: Higuchi, Miyuki organization: Department of Agriculture, Shizuoka University |
| BookMark | eNp9UstuFDEQtFAQCUt-gNNIXLgMePz2CaGIR6RIcICz5eeuVzP2Ys-slL_HsxsFwgFfbHdXlbpa9RJcpJw8AK8H-G6AWLyvZKBS9BDhnmCEUU-fgSsECe3bB1389b4E17XuYTsUSTLIF-ASc04l5OgKHL_v7mu02e78FK0eu0PJB1_m6GuXQzfvfHfUdsmjLt3kJ1N08p1OrrN-HJe1GrSdc6md87MvU2ztkMuk55jTqvDIjumotzGdGvUVeB70WP31w70BPz9_-nHztb_79uX25uNdbwmTc-8c45gLjwMPyFAhuRVD4Job7jgXIWAtrTNmIMwZgpkxTEhsTEBQCxsg3oDbs67Leq8OJU663KusozoVctkq3cza0ashOCmYZYIFTqClRhPNMQyMGR-IdE3rw1nrsJjJO-vTXPT4RPRpJ8Wd2uajGiDFmMh1mrcPCiX_Wnyd1RTrusi21LxUhQSHzcrqYQPe_APd56WktquGYpJAThltKHRG2ZJrLT48TjNAtcZEnWOiWkzUKSZqJeEzqTZw2vryR_o_rN_7R8PN |
| Cites_doi | 10.7554/eLife.26403 10.1016/j.ceb.2019.12.001 10.1083/jcb.128.5.779 10.1016/j.cell.2015.04.046 10.1242/jcs.070045 10.1074/jbc.M300568200 10.1042/BST20180120 10.1016/j.bbrc.2019.11.064 10.1016/j.tcb.2016.05.004 10.3389/fpls.2014.00476 10.1073/pnas.2116007119 10.1093/pcp/pcm085 10.1534/genetics.111.128033 10.1016/0005-2736(81)90082-1 10.1073/pnas.71.2.522 10.1103/PhysRevLett.100.148102 10.1083/jcb.201301039 10.1242/jcs.164905 10.1074/jbc.M000917200 10.1016/0092-8674(87)90711-2 10.1083/jcb.201404115 10.1146/annurev.ge.27.120193.002253 10.1091/mbc.E21-04-0179 10.1007/s00018-017-2478-0 10.7554/eLife.25960 10.7554/eLife.00459 10.1534/genetics.111.128264 10.1186/s12915-021-01048-7 10.7554/eLife.41237 10.1038/35044114 10.1083/jcb.201611029 10.1038/s41598-018-20781-8 10.1038/nature02013 10.1016/j.bpj.2017.09.029 10.1016/j.bbamcr.2008.08.003 10.1111/j.1365-2443.2009.01376.x 10.1038/s41598-019-51254-1 10.1016/j.bbamcr.2005.06.010 |
| ContentType | Journal Article |
| Copyright | The Author(s) 2023 The Author(s) 2023. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Springer Nature Limited 2023 |
| Copyright_xml | – notice: The Author(s) 2023 – notice: The Author(s) 2023. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: Springer Nature Limited 2023 |
| DBID | C6C AAYXX CITATION 3V. 7X7 7XB 88A 88E 88I 8FE 8FH 8FI 8FJ 8FK ABUWG AFKRA AZQEC BBNVY BENPR BHPHI CCPQU DWQXO FYUFA GHDGH GNUQQ HCIFZ K9. LK8 M0S M1P M2P M7P PIMPY PQEST PQQKQ PQUKI Q9U 7X8 5PM DOA |
| DOI | 10.1038/s41598-023-43232-5 |
| DatabaseName | Springer Open Access CrossRef ProQuest Central (Corporate) Health & Medical Collection ProQuest Central (purchase pre-March 2016) Biology Database (Alumni Edition) Medical Database (Alumni Edition) Science Database (Alumni Edition) ProQuest SciTech Collection ProQuest Natural Science Collection Hospital Premium Collection Hospital Premium Collection (Alumni Edition) ProQuest Central (Alumni) (purchase pre-March 2016) ProQuest Central (Alumni) ProQuest Central ProQuest Central Essentials Biological Science Collection AUTh Library subscriptions: ProQuest Central ProQuest Natural Science Collection ProQuest One Community College ProQuest Central Health Research Premium Collection Health Research Premium Collection (Alumni) ProQuest Central Student SciTech Premium Collection ProQuest Health & Medical Complete (Alumni) Biological Sciences Health & Medical Collection (Alumni Edition) PML(ProQuest Medical Library) Science Database Biological Science Database Publicly Available Content Database (Proquest) (PQ_SDU_P3) ProQuest One Academic Eastern Edition (DO NOT USE) ProQuest One Academic ProQuest One Academic UKI Edition ProQuest Central Basic MEDLINE - Academic PubMed Central (Full Participant titles) Directory of Open Access Journals |
| DatabaseTitle | CrossRef Publicly Available Content Database ProQuest Central Student ProQuest Central Essentials ProQuest Health & Medical Complete (Alumni) ProQuest Central (Alumni Edition) SciTech Premium Collection ProQuest One Community College ProQuest Natural Science Collection ProQuest Biology Journals (Alumni Edition) ProQuest Central Health Research Premium Collection Health and Medicine Complete (Alumni Edition) Natural Science Collection ProQuest Central Korea Biological Science Collection ProQuest Medical Library (Alumni) ProQuest Science Journals (Alumni Edition) ProQuest Biological Science Collection ProQuest Central Basic ProQuest Science Journals ProQuest One Academic Eastern Edition ProQuest Hospital Collection Health Research Premium Collection (Alumni) Biological Science Database ProQuest SciTech Collection ProQuest Hospital Collection (Alumni) ProQuest Health & Medical Complete ProQuest Medical Library ProQuest One Academic UKI Edition ProQuest One Academic ProQuest Central (Alumni) MEDLINE - Academic |
| DatabaseTitleList | Publicly Available Content Database MEDLINE - Academic CrossRef |
| Database_xml | – sequence: 1 dbid: DOA name: Directory of Open Access Journals url: http://www.doaj.org/ sourceTypes: Open Website |
| DeliveryMethod | fulltext_linktorsrc |
| Discipline | Biology |
| EISSN | 2045-2322 |
| EndPage | 16187 |
| ExternalDocumentID | oai_doaj_org_article_1fd986c686f740c5ba4a730f66bef49d 10_1038_s41598_023_43232_5 |
| GrantInformation_xml | – fundername: Takeda Science Foundation funderid: http://dx.doi.org/10.13039/100007449 – fundername: Grants-in-Aid for Scientific Research from the Ministry of Education, Cultures, Sports, Science and Technology grantid: 20K06620; 19K07265; 22K06818; 22H04654 – fundername: Ohsumi Frontier Science Foundation funderid: http://dx.doi.org/10.13039/501100018732 – fundername: JST CREST grantid: JPMJCR20E – fundername: ; – fundername: ; grantid: 20K06620; 19K07265; 22K06818; 22H04654 – fundername: ; grantid: JPMJCR20E |
| GroupedDBID | 0R~ 3V. 4.4 53G 5VS 7X7 88A 88E 88I 8FE 8FH 8FI 8FJ AAFWJ AAJSJ AAKDD ABDBF ABUWG ACGFS ACSMW ADBBV ADRAZ AENEX AFKRA AJTQC ALIPV ALMA_UNASSIGNED_HOLDINGS AOIJS AZQEC BAWUL BBNVY BCNDV BENPR BHPHI BPHCQ BVXVI C6C CCPQU DIK DWQXO EBD EBLON EBS ESX FYUFA GNUQQ GROUPED_DOAJ GX1 HCIFZ HH5 HMCUK HYE KQ8 LK8 M0L M1P M2P M48 M7P M~E NAO OK1 PIMPY PQQKQ PROAC PSQYO RIG RNT RNTTT RPM SNYQT UKHRP AAYXX CITATION 7XB 8FK K9. PQEST PQUKI Q9U 7X8 5PM AFPKN |
| ID | FETCH-LOGICAL-c469t-dd67378e3f7f2b5897c81f7a7b7d778ff3a9cdbb146db436bb6893bbf20a8cf03 |
| IEDL.DBID | RPM |
| ISSN | 2045-2322 |
| IngestDate | Tue Oct 22 14:44:31 EDT 2024 Tue Sep 17 21:29:24 EDT 2024 Fri Oct 25 02:06:33 EDT 2024 Sat Nov 09 03:01:52 EST 2024 Fri Nov 22 00:38:48 EST 2024 Fri Oct 11 20:47:53 EDT 2024 |
| IsDoiOpenAccess | true |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 1 |
| Language | English |
| License | Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c469t-dd67378e3f7f2b5897c81f7a7b7d778ff3a9cdbb146db436bb6893bbf20a8cf03 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
| OpenAccessLink | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10533490/ |
| PMID | 37759072 |
| PQID | 2869407565 |
| PQPubID | 2041939 |
| PageCount | 1 |
| ParticipantIDs | doaj_primary_oai_doaj_org_article_1fd986c686f740c5ba4a730f66bef49d pubmedcentral_primary_oai_pubmedcentral_nih_gov_10533490 proquest_miscellaneous_2870146689 proquest_journals_2869407565 crossref_primary_10_1038_s41598_023_43232_5 springer_journals_10_1038_s41598_023_43232_5 |
| PublicationCentury | 2000 |
| PublicationDate | 2023-09-27 |
| PublicationDateYYYYMMDD | 2023-09-27 |
| PublicationDate_xml | – month: 09 year: 2023 text: 2023-09-27 day: 27 |
| PublicationDecade | 2020 |
| PublicationPlace | London |
| PublicationPlace_xml | – name: London |
| PublicationTitle | Scientific reports |
| PublicationTitleAbbrev | Sci Rep |
| PublicationYear | 2023 |
| Publisher | Nature Publishing Group UK Nature Publishing Group Nature Portfolio |
| Publisher_xml | – name: Nature Publishing Group UK – name: Nature Publishing Group – name: Nature Portfolio |
| References | Ishii (CR12) 2019; 9 Mizushima (CR13) 2020; 63 Yanagisawa, Imai, Taniguchi (CR24) 2008; 100 Tsuji (CR28) 2017; 6 Levin (CR4) 2011; 189 Leveille, Cornell, Merz, Keller (CR33) 2022; 119 Tanaka (CR9) 2007; 48 Zhao, Macgurn, Liu, Emr (CR11) 2013; 2 Liu (CR19) 2018; 7 Lipowsky (CR32) 1992; 2 MacDiarmid, Milanick, Eide (CR31) 2003; 278 Veatch, Keller (CR23) 2005; 1746 Morano, Grant, Moye-Rowley (CR1) 2012; 190 Finley, Ozkaynak, Varshavsky (CR5) 1987; 48 Legesse-Miller, Sagiv, Glozman, Elazar (CR15) 2000; 275 Sinensky (CR34) 1974; 71 Protter, Parker (CR3) 2016; 26 Baumgart, Hess, Webb (CR22) 2003; 425 Tamura, Oku, Sakai (CR18) 2010; 123 Mikawa, Kanoh, Ishikawa (CR17) 2010; 15 Wang, Miao, Chang (CR20) 2014; 206 Oku (CR36) 2017; 216 Salzer, Kostan, Djinović-Carugo (CR39) 2017; 74 Maeda, Oku, Sakai (CR16) 2017; 161 Zhang, Hicks, Raikhel (CR8) 2014; 5 Parsell, Lindquist (CR2) 1993; 27 Toulmay, Prinz (CR26) 2013; 202 Zhu, Jorgensen, Li, Chuang, Emr (CR38) 2017; 6 Fan, Evans (CR35) 2015; 161 Liao, Garcia, Tan, Tsang, Pon (CR29) 2021; 32 Numrich (CR10) 2015; 128 Vida, Emr (CR40) 1995; 128 Tsuji, Fujimoto (CR27) 2018; 46 He (CR21) 2021; 19 Li, Kane (CR7) 2009; 1793 Ichimura (CR14) 2000; 408 Rayermann, Rayermann, Cornell, Merz, Keller (CR25) 2017; 113 Morshed, Sharmin, Ushimaru (CR37) 2020; 522 Ishii (CR6) 2018; 8 Moeller, Mudd, Thomson (CR30) 1981; 643 T Tsuji (43232_CR28) 2017; 6 N Mizushima (43232_CR13) 2020; 63 Y Maeda (43232_CR16) 2017; 161 A Legesse-Miller (43232_CR15) 2000; 275 SL Veatch (43232_CR23) 2005; 1746 TA Vida (43232_CR40) 1995; 128 DA Parsell (43232_CR2) 1993; 27 SP Rayermann (43232_CR25) 2017; 113 CH Moeller (43232_CR30) 1981; 643 W Fan (43232_CR35) 2015; 161 M Yanagisawa (43232_CR24) 2008; 100 A Ishii (43232_CR6) 2018; 8 A Ishii (43232_CR12) 2019; 9 U Salzer (43232_CR39) 2017; 74 X-M Liu (43232_CR19) 2018; 7 T Mikawa (43232_CR17) 2010; 15 DE Levin (43232_CR4) 2011; 189 C-W Wang (43232_CR20) 2014; 206 CW MacDiarmid (43232_CR31) 2003; 278 P-C Liao (43232_CR29) 2021; 32 DSW Protter (43232_CR3) 2016; 26 Y Ichimura (43232_CR14) 2000; 408 C-W He (43232_CR21) 2021; 19 A Toulmay (43232_CR26) 2013; 202 L Zhu (43232_CR38) 2017; 6 KA Morano (43232_CR1) 2012; 190 C Zhang (43232_CR8) 2014; 5 Y Zhao (43232_CR11) 2013; 2 Y Tanaka (43232_CR9) 2007; 48 SC Li (43232_CR7) 2009; 1793 T Baumgart (43232_CR22) 2003; 425 M Sinensky (43232_CR34) 1974; 71 N Tamura (43232_CR18) 2010; 123 T Tsuji (43232_CR27) 2018; 46 CL Leveille (43232_CR33) 2022; 119 M Oku (43232_CR36) 2017; 216 S Morshed (43232_CR37) 2020; 522 D Finley (43232_CR5) 1987; 48 J Numrich (43232_CR10) 2015; 128 R Lipowsky (43232_CR32) 1992; 2 |
| References_xml | – volume: 6 start-page: e26403 year: 2017 ident: CR38 article-title: ESCRTs function directly on the lysosome membrane to downregulate ubiquitinated lysosomal membrane proteins publication-title: Elife doi: 10.7554/eLife.26403 contributor: fullname: Emr – volume: 63 start-page: 1 year: 2020 end-page: 10 ident: CR13 article-title: The ATG conjugation systems in autophagy publication-title: Curr. Opin. Cell Biol. doi: 10.1016/j.ceb.2019.12.001 contributor: fullname: Mizushima – volume: 128 start-page: 779 year: 1995 end-page: 792 ident: CR40 article-title: A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast publication-title: J. Cell Biol. doi: 10.1083/jcb.128.5.779 contributor: fullname: Emr – volume: 161 start-page: 962 year: 2015 end-page: 963 ident: CR35 article-title: Turning up the heat on membrane fluidity publication-title: Cell doi: 10.1016/j.cell.2015.04.046 contributor: fullname: Evans – volume: 123 start-page: 4107 year: 2010 end-page: 4116 ident: CR18 article-title: Atg8 regulates vacuolar membrane dynamics in a lipidation-independent manner in Pichia pastoris publication-title: J. Cell Sci. doi: 10.1242/jcs.070045 contributor: fullname: Sakai – volume: 278 start-page: 15065 year: 2003 end-page: 15072 ident: CR31 article-title: Induction of the ZRC1 metal tolerance gene in zinc-limited yeast confers resistance to zinc shock publication-title: J. Biol. Chem. doi: 10.1074/jbc.M300568200 contributor: fullname: Eide – volume: 46 start-page: 1047 year: 2018 end-page: 1054 ident: CR27 article-title: Lipids and lipid domains of the yeast vacuole publication-title: Biochem. Soc. Trans. doi: 10.1042/BST20180120 contributor: fullname: Fujimoto – volume: 522 start-page: 88 year: 2020 end-page: 94 ident: CR37 article-title: TORC1 regulates ESCRT-0 complex formation on the vacuolar membrane and microautophagy induction in yeast publication-title: Biochem. Biophys. Res. Commun. doi: 10.1016/j.bbrc.2019.11.064 contributor: fullname: Ushimaru – volume: 26 start-page: 668 year: 2016 end-page: 679 ident: CR3 article-title: Principles and properties of stress granules publication-title: Trends Cell Biol. doi: 10.1016/j.tcb.2016.05.004 contributor: fullname: Parker – volume: 5 start-page: 476 year: 2014 ident: CR8 article-title: Plant vacuole morphology and vacuolar trafficking publication-title: Front. Plant Sci. doi: 10.3389/fpls.2014.00476 contributor: fullname: Raikhel – volume: 119 start-page: e2116007119 year: 2022 ident: CR33 article-title: Yeast cells actively tune their membranes to phase separate at temperatures that scale with growth temperatures publication-title: Proc. Natl. Acad. Sci. U.S.A. doi: 10.1073/pnas.2116007119 contributor: fullname: Keller – volume: 48 start-page: 1159 year: 2007 end-page: 1169 ident: CR9 article-title: Intra-vacuolar reserves of membranes during stomatal closure: The possible role of guard cell vacuoles estimated by 3-D reconstruction publication-title: Plant Cell Physiol. doi: 10.1093/pcp/pcm085 contributor: fullname: Tanaka – volume: 190 start-page: 1157 year: 2012 end-page: 1195 ident: CR1 article-title: The response to heat shock and oxidative stress in publication-title: Genetics doi: 10.1534/genetics.111.128033 contributor: fullname: Moye-Rowley – volume: 643 start-page: 376 year: 1981 end-page: 386 ident: CR30 article-title: Lipid phase separations and intramembranous particle movements in the yeast tonoplast publication-title: Biochim. Biophys. Acta doi: 10.1016/0005-2736(81)90082-1 contributor: fullname: Thomson – volume: 71 start-page: 522 year: 1974 end-page: 525 ident: CR34 article-title: Homeoviscous adaptation—A homeostatic process that regulates the viscosity of membrane lipids in publication-title: Proc. Natl. Acad. Sci. U.S.A. doi: 10.1073/pnas.71.2.522 contributor: fullname: Sinensky – volume: 100 start-page: 148102 year: 2008 ident: CR24 article-title: Shape deformation of ternary vesicles coupled with phase separation publication-title: Phys. Rev. Lett. doi: 10.1103/PhysRevLett.100.148102 contributor: fullname: Taniguchi – volume: 202 start-page: 35 year: 2013 end-page: 44 ident: CR26 article-title: Direct imaging reveals stable, micrometer-scale lipid domains that segregate proteins in live cells publication-title: J. Cell Biol. doi: 10.1083/jcb.201301039 contributor: fullname: Prinz – volume: 128 start-page: 2278 year: 2015 end-page: 2292 ident: CR10 article-title: The I-BAR protein Ivy1 is an effector of the Rab7 GTPase Ypt7 involved in vacuole membrane homeostasis publication-title: J. Cell Sci. doi: 10.1242/jcs.164905 contributor: fullname: Numrich – volume: 275 start-page: 32966 year: 2000 end-page: 32973 ident: CR15 article-title: Aut7p, a soluble autophagic factor, participates in multiple membrane trafficking processes publication-title: J. Biol. Chem. doi: 10.1074/jbc.M000917200 contributor: fullname: Elazar – volume: 48 start-page: 1035 year: 1987 end-page: 1046 ident: CR5 article-title: The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, and other stresses publication-title: Cell doi: 10.1016/0092-8674(87)90711-2 contributor: fullname: Varshavsky – volume: 206 start-page: 357 year: 2014 end-page: 366 ident: CR20 article-title: A sterol-enriched vacuolar microdomain mediates stationary phase lipophagy in budding yeast publication-title: J. Cell Biol. doi: 10.1083/jcb.201404115 contributor: fullname: Chang – volume: 27 start-page: 437 year: 1993 end-page: 496 ident: CR2 article-title: The function of heat-shock proteins in stress tolerance: Degradation and reactivation of damaged proteins publication-title: Annu. Rev. Genet. doi: 10.1146/annurev.ge.27.120193.002253 contributor: fullname: Lindquist – volume: 32 start-page: br12 year: 2021 ident: CR29 article-title: Roles for L microdomains and ESCRT in ER stress-induced lipid droplet microautophagy in budding yeast publication-title: Mol. Biol. Cell doi: 10.1091/mbc.E21-04-0179 contributor: fullname: Pon – volume: 74 start-page: 2413 year: 2017 end-page: 2438 ident: CR39 article-title: Deciphering the BAR code of membrane modulators publication-title: Cell. Mol. Life Sci. doi: 10.1007/s00018-017-2478-0 contributor: fullname: Djinović-Carugo – volume: 6 start-page: e25960 year: 2017 ident: CR28 article-title: Niemann-Pick type C proteins promote microautophagy by expanding raft-like membrane domains in the yeast vacuole publication-title: Elife doi: 10.7554/eLife.25960 contributor: fullname: Tsuji – volume: 2 start-page: e00459 year: 2013 ident: CR11 article-title: The ART-Rsp5 ubiquitin ligase network comprises a plasma membrane quality control system that protects yeast cells from proteotoxic stress publication-title: Elife doi: 10.7554/eLife.00459 contributor: fullname: Emr – volume: 189 start-page: 1145 year: 2011 end-page: 1175 ident: CR4 article-title: Regulation of cell wall biogenesis in : The cell wall integrity signaling pathway publication-title: Genetics doi: 10.1534/genetics.111.128264 contributor: fullname: Levin – volume: 19 start-page: 117 year: 2021 ident: CR21 article-title: Membrane recruitment of Atg8 by Hfl1 facilitates turnover of vacuolar membrane proteins in yeast cells approaching stationary phase publication-title: BMC Biol. doi: 10.1186/s12915-021-01048-7 contributor: fullname: He – volume: 7 start-page: e41237 year: 2018 ident: CR19 article-title: Lipidation-independent vacuolar functions of Atg8 rely on its noncanonical interaction with a vacuole membrane protein publication-title: Elife doi: 10.7554/eLife.41237 contributor: fullname: Liu – volume: 408 start-page: 488 year: 2000 end-page: 492 ident: CR14 article-title: A ubiquitin-like system mediates protein lipidation publication-title: Nature doi: 10.1038/35044114 contributor: fullname: Ichimura – volume: 216 start-page: 3263 year: 2017 end-page: 3274 ident: CR36 article-title: Evidence for ESCRT- and clathrin-dependent microautophagy publication-title: J. Cell Biol. doi: 10.1083/jcb.201611029 contributor: fullname: Oku – volume: 2 start-page: 1825 year: 1992 end-page: 1840 ident: CR32 article-title: Budding of membranes induced by intramembrane domains publication-title: J. Phys. II contributor: fullname: Lipowsky – volume: 8 start-page: 2644 year: 2018 ident: CR6 article-title: Accelerated invagination of vacuoles as a stress response in chronically heat-stressed yeasts publication-title: Sci. Rep. doi: 10.1038/s41598-018-20781-8 contributor: fullname: Ishii – volume: 425 start-page: 821 year: 2003 end-page: 824 ident: CR22 article-title: Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension publication-title: Nature doi: 10.1038/nature02013 contributor: fullname: Webb – volume: 113 start-page: 2425 year: 2017 end-page: 2432 ident: CR25 article-title: Hallmarks of reversible separation of living, unperturbed cell membranes into two liquid phases publication-title: Biophys. J. doi: 10.1016/j.bpj.2017.09.029 contributor: fullname: Keller – volume: 161 start-page: 339 year: 2017 end-page: 348 ident: CR16 article-title: Autophagy-independent function of Atg8 in lipid droplet dynamics in yeast publication-title: J. Biochem. contributor: fullname: Sakai – volume: 1793 start-page: 650 year: 2009 end-page: 663 ident: CR7 article-title: The yeast lysosome-like vacuole: Endpoint and crossroads publication-title: Biochim. Biophys. Acta doi: 10.1016/j.bbamcr.2008.08.003 contributor: fullname: Kane – volume: 15 start-page: 229 year: 2010 end-page: 242 ident: CR17 article-title: Fission yeast Vps1 and Atg8 contribute to oxidative stress resistance publication-title: Genes Cells doi: 10.1111/j.1365-2443.2009.01376.x contributor: fullname: Ishikawa – volume: 9 start-page: 14828 year: 2019 ident: CR12 article-title: Role of Atg8 in the regulation of vacuolar membrane invagination publication-title: Sci. Rep. doi: 10.1038/s41598-019-51254-1 contributor: fullname: Ishii – volume: 1746 start-page: 172 year: 2005 end-page: 185 ident: CR23 article-title: Seeing spots: Complex phase behavior in simple membranes publication-title: Biochim. Biophys. Acta doi: 10.1016/j.bbamcr.2005.06.010 contributor: fullname: Keller – volume: 71 start-page: 522 year: 1974 ident: 43232_CR34 publication-title: Proc. Natl. Acad. Sci. U.S.A. doi: 10.1073/pnas.71.2.522 contributor: fullname: M Sinensky – volume: 74 start-page: 2413 year: 2017 ident: 43232_CR39 publication-title: Cell. Mol. Life Sci. doi: 10.1007/s00018-017-2478-0 contributor: fullname: U Salzer – volume: 8 start-page: 2644 year: 2018 ident: 43232_CR6 publication-title: Sci. Rep. doi: 10.1038/s41598-018-20781-8 contributor: fullname: A Ishii – volume: 408 start-page: 488 year: 2000 ident: 43232_CR14 publication-title: Nature doi: 10.1038/35044114 contributor: fullname: Y Ichimura – volume: 6 start-page: e25960 year: 2017 ident: 43232_CR28 publication-title: Elife doi: 10.7554/eLife.25960 contributor: fullname: T Tsuji – volume: 522 start-page: 88 year: 2020 ident: 43232_CR37 publication-title: Biochem. Biophys. Res. Commun. doi: 10.1016/j.bbrc.2019.11.064 contributor: fullname: S Morshed – volume: 216 start-page: 3263 year: 2017 ident: 43232_CR36 publication-title: J. Cell Biol. doi: 10.1083/jcb.201611029 contributor: fullname: M Oku – volume: 48 start-page: 1035 year: 1987 ident: 43232_CR5 publication-title: Cell doi: 10.1016/0092-8674(87)90711-2 contributor: fullname: D Finley – volume: 206 start-page: 357 year: 2014 ident: 43232_CR20 publication-title: J. Cell Biol. doi: 10.1083/jcb.201404115 contributor: fullname: C-W Wang – volume: 63 start-page: 1 year: 2020 ident: 43232_CR13 publication-title: Curr. Opin. Cell Biol. doi: 10.1016/j.ceb.2019.12.001 contributor: fullname: N Mizushima – volume: 202 start-page: 35 year: 2013 ident: 43232_CR26 publication-title: J. Cell Biol. doi: 10.1083/jcb.201301039 contributor: fullname: A Toulmay – volume: 161 start-page: 962 year: 2015 ident: 43232_CR35 publication-title: Cell doi: 10.1016/j.cell.2015.04.046 contributor: fullname: W Fan – volume: 27 start-page: 437 year: 1993 ident: 43232_CR2 publication-title: Annu. Rev. Genet. doi: 10.1146/annurev.ge.27.120193.002253 contributor: fullname: DA Parsell – volume: 190 start-page: 1157 year: 2012 ident: 43232_CR1 publication-title: Genetics doi: 10.1534/genetics.111.128033 contributor: fullname: KA Morano – volume: 15 start-page: 229 year: 2010 ident: 43232_CR17 publication-title: Genes Cells doi: 10.1111/j.1365-2443.2009.01376.x contributor: fullname: T Mikawa – volume: 32 start-page: br12 year: 2021 ident: 43232_CR29 publication-title: Mol. Biol. Cell doi: 10.1091/mbc.E21-04-0179 contributor: fullname: P-C Liao – volume: 189 start-page: 1145 year: 2011 ident: 43232_CR4 publication-title: Genetics doi: 10.1534/genetics.111.128264 contributor: fullname: DE Levin – volume: 48 start-page: 1159 year: 2007 ident: 43232_CR9 publication-title: Plant Cell Physiol. doi: 10.1093/pcp/pcm085 contributor: fullname: Y Tanaka – volume: 161 start-page: 339 year: 2017 ident: 43232_CR16 publication-title: J. Biochem. contributor: fullname: Y Maeda – volume: 425 start-page: 821 year: 2003 ident: 43232_CR22 publication-title: Nature doi: 10.1038/nature02013 contributor: fullname: T Baumgart – volume: 2 start-page: 1825 year: 1992 ident: 43232_CR32 publication-title: J. Phys. II contributor: fullname: R Lipowsky – volume: 100 start-page: 148102 year: 2008 ident: 43232_CR24 publication-title: Phys. Rev. Lett. doi: 10.1103/PhysRevLett.100.148102 contributor: fullname: M Yanagisawa – volume: 5 start-page: 476 year: 2014 ident: 43232_CR8 publication-title: Front. Plant Sci. doi: 10.3389/fpls.2014.00476 contributor: fullname: C Zhang – volume: 643 start-page: 376 year: 1981 ident: 43232_CR30 publication-title: Biochim. Biophys. Acta doi: 10.1016/0005-2736(81)90082-1 contributor: fullname: CH Moeller – volume: 278 start-page: 15065 year: 2003 ident: 43232_CR31 publication-title: J. Biol. Chem. doi: 10.1074/jbc.M300568200 contributor: fullname: CW MacDiarmid – volume: 275 start-page: 32966 year: 2000 ident: 43232_CR15 publication-title: J. Biol. Chem. doi: 10.1074/jbc.M000917200 contributor: fullname: A Legesse-Miller – volume: 26 start-page: 668 year: 2016 ident: 43232_CR3 publication-title: Trends Cell Biol. doi: 10.1016/j.tcb.2016.05.004 contributor: fullname: DSW Protter – volume: 123 start-page: 4107 year: 2010 ident: 43232_CR18 publication-title: J. Cell Sci. doi: 10.1242/jcs.070045 contributor: fullname: N Tamura – volume: 1793 start-page: 650 year: 2009 ident: 43232_CR7 publication-title: Biochim. Biophys. Acta doi: 10.1016/j.bbamcr.2008.08.003 contributor: fullname: SC Li – volume: 19 start-page: 117 year: 2021 ident: 43232_CR21 publication-title: BMC Biol. doi: 10.1186/s12915-021-01048-7 contributor: fullname: C-W He – volume: 1746 start-page: 172 year: 2005 ident: 43232_CR23 publication-title: Biochim. Biophys. Acta doi: 10.1016/j.bbamcr.2005.06.010 contributor: fullname: SL Veatch – volume: 128 start-page: 779 year: 1995 ident: 43232_CR40 publication-title: J. Cell Biol. doi: 10.1083/jcb.128.5.779 contributor: fullname: TA Vida – volume: 9 start-page: 14828 year: 2019 ident: 43232_CR12 publication-title: Sci. Rep. doi: 10.1038/s41598-019-51254-1 contributor: fullname: A Ishii – volume: 7 start-page: e41237 year: 2018 ident: 43232_CR19 publication-title: Elife doi: 10.7554/eLife.41237 contributor: fullname: X-M Liu – volume: 128 start-page: 2278 year: 2015 ident: 43232_CR10 publication-title: J. Cell Sci. doi: 10.1242/jcs.164905 contributor: fullname: J Numrich – volume: 2 start-page: e00459 year: 2013 ident: 43232_CR11 publication-title: Elife doi: 10.7554/eLife.00459 contributor: fullname: Y Zhao – volume: 119 start-page: e2116007119 year: 2022 ident: 43232_CR33 publication-title: Proc. Natl. Acad. Sci. U.S.A. doi: 10.1073/pnas.2116007119 contributor: fullname: CL Leveille – volume: 6 start-page: e26403 year: 2017 ident: 43232_CR38 publication-title: Elife doi: 10.7554/eLife.26403 contributor: fullname: L Zhu – volume: 113 start-page: 2425 year: 2017 ident: 43232_CR25 publication-title: Biophys. J. doi: 10.1016/j.bpj.2017.09.029 contributor: fullname: SP Rayermann – volume: 46 start-page: 1047 year: 2018 ident: 43232_CR27 publication-title: Biochem. Soc. Trans. doi: 10.1042/BST20180120 contributor: fullname: T Tsuji |
| SSID | ssj0000529419 |
| Score | 2.4473605 |
| Snippet | Vacuoles change their morphology in response to stress. In yeast exposed to chronically high temperatures, vacuolar membranes get deformed and invaginations... Abstract Vacuoles change their morphology in response to stress. In yeast exposed to chronically high temperatures, vacuolar membranes get deformed and... |
| SourceID | doaj pubmedcentral proquest crossref springer |
| SourceType | Open Website Open Access Repository Aggregation Database Publisher |
| StartPage | 16187 |
| SubjectTerms | 631/208 631/326 631/80 Autophagy Genetic analysis Heat Heat tolerance High temperature Humanities and Social Sciences Invaginations Lipids Localization Membrane proteins Membranes Morphology multidisciplinary Mutants Oxidative stress Phenotypes Physicochemical properties Proteins Science Science (multidisciplinary) Temperature Temperature effects Vacuoles Yeasts |
| SummonAdditionalLinks | – databaseName: Directory of Open Access Journals dbid: DOA link: http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV3Nb9UwDLdgEhIXtPEhuo0pSNygWpu0-TjCPrQTF0DiFuVT7LC-aW_vSfz32GlfoZMQF65N2ia2k9ix_TPAu9xJGbmLtUyhqbsQTO0jOXm9Q3FOvWtK_ZSrL-rzd31-QTA5c6kvigkb4YFHwp22ORotg9Qyq64JvXedQ6nMUvqUOxPL7tvIP4ypEdWbm641U5ZMI_TpGk8qyibjou4EqhF1vziJCmD_Qst8GCP5wFFazp_LfXg2KY7s4zjgA3iUhufwZCwl-fMFbEsoZ6D6VwUAgN3SLfsdwaWyVWao5rGtCxsyZNlNukEbeUjMDZHRzT2ForKp8g6LU4BMYnNiI31hfvt62FJlo_Gm7yV8u7z4enZVTzUV6oCG8H0dIxWm0UlklbnvtVFBt1k55VVUSucsnAnRe9xAo--E9F6iRuN95o3TITfiFewNqyG9BoaGiEk6G9EG8l1yHcmrF1suU6udjhW839HX3o7QGba4vIW2IzcscsMWbti-gk_EgrknwV6XBygMdhIG-y9hqOB4x0A7rcW15VoaNFtRc63g7dyMq4gIjMRebaiPIhQdnGsFesH4xYCWLcP1j4LH3ZZ8ZtNU8GEnI7___vcZH_6PGR_BU04yTX4ydQx793eb9AYer-PmpKyIX2yxEtM priority: 102 providerName: Directory of Open Access Journals |
| Title | Physicochemical properties of the vacuolar membrane and cellular factors determine formation of vacuolar invaginations |
| URI | https://link.springer.com/article/10.1038/s41598-023-43232-5 https://www.proquest.com/docview/2869407565 https://search.proquest.com/docview/2870146689 https://pubmed.ncbi.nlm.nih.gov/PMC10533490 https://doaj.org/article/1fd986c686f740c5ba4a730f66bef49d |
| Volume | 13 |
| hasFullText | 1 |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| link | http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9QwELbYSkhcEE-R0lZG4gbpJnbix7GUVr2AkACJm-UnrMRmV7vdlfj3zDjJQipx4Ron8WPG9jy_IeR1aoQIzIZSRF-Vjfe6dAGdvM4CO8fWVrl-ys1n-fGben-FMDlizIXJQfveLc67n8vzbvEjx1aul34-xonNP324rHMCqa7mMzID4fAvHb1H9Ga6qfWQIVNxNd_CLYWZZIyXDQcRosR6NVzKFjRDNrmQMm7_RNi8Gyp5x1-ar6HrR-ThID_Si36cj8m92D0h9_uKkr-ekn2O6PRYBivjANA1Gts3iJpKV4mCtEf31u9Qn6XLuARVuYvUdoGiAR8jUulQgIeGIU4m0kN-I_7h8PWi22OBo97g94x8vb76cnlTDqUVSg_68G0ZAtanUZEnmZhrlZZe1Ula6WSQUqXErfbBOThHg2u4cE6AYONcYpVVPlX8OTnqVl18QSjoIzqqpHnt0YXJVEDnXqiZiLWyKhTkzbi-Zt0jaJjs-ebK9IQxQBiTCWPagrxDEhzeRPTr_GC1-W4GHjB1CloJL5RIsql862xj4aRKQriYGg1dnowENMOW3BqmhAbtFQTYgrw6NMNmwgWGxV7t8B2JYDow14KoCeEnA5q2AJdmWO6RKwvyduSRP73_e8bH_9_TS_KAIVOjk0yekKPbzS6ektk27M6ybeEsb4zfixsUBA |
| link.rule.ids | 230,315,729,782,786,866,887,2106,27933,27934,53800,53802 |
| linkProvider | National Library of Medicine |
| linkToHtml | http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9QwELZoEYILb0SggJG4QbqJk_hxhNJqEW2FRJG4WX7CSmx2tdtdiX_PjJMspBKXXmMnjj0z9oxn5htC3sSac8-Mz3lwRV47p3Lr0clrDbBzaEyR6qdMv4rz7_LjMcLk8CEXJgXtOzs7bH_ND9vZzxRbuZy7yRAnNvlydlSmBFJVTPbITRDYovjHSu8wvZmqS9XnyBSVnKzhnMJcMlbldQVKRI4VayohGrAN2ehISsj9I3XzarDkFY9pOohO7l13CvfJ3V71pO-79gfkRmgfkltdMcrfj8g2BYM6rKCVIAToEu_pVwi4SheRgqJIt8Zt0BSm8zAHK7sN1LSe4t0_BrPSvnYP9X2ITaC71Ej8wu7tWbvF2kjdXeFj8u3k-OJomvdVGXIHpvRl7j2WtpGhiiIy20glnCyjMMIKL4SMsTLKeWthC_a2rri1HHQiayMrjHSxqJ6Q_XbRhqeEgimjgoyqKh16P5n06Bf0JeOhlEb6jLwdCKOXHfiGTk7zSuqOohooqhNFdZORD0i7XU8Ezk4PFqsful97XUavJHdc8ijqwjXW1AY2uci5DbFWMOTBQHndS_NaM8kVGL6g-2bk9a4Z5BAXGBZ7scE-AnF4YK4ZkSOOGf3QuAW4IyF6D9yQkXcDc_0d_f8zfnb9kV6R29OLs1N9-un883Nyh6FkoK9NHJD9y9UmvCB7a795meTqDxWQKME |
| linkToPdf | http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1Lb9QwELZoEYgLb8RCASNxgzSJk_jBDdquioCqEiBxs_yEldjsare7Ev-eGSdZSCUucI2dOPbM2DOemW8IeRFrzj0zPuPBFVntnMqsRyevNcDOoTFFqp9y-kmcfZXHJwiT83rIhUlB-87ODtsf88N29j3FVi7nLh_ixPLzj0dlSiBVRb70Md8jV0FoC_aHpd7hejNVl6rPkykqma_hrMJ8MlZldQWKRIZVayohGrAP2ehYSuj9I5XzcsDkJa9pOoymt_5nGrfJzV4FpW-6PnfIldDeJde6opQ_75FtCgp1WEkrQQnQJd7XrxB4lS4iBYWRbo3boElM52EO1nYbqGk9RR8ABrXSvoYP9X2oTaC7FEn8wu7tWbvFGkndneF98mV68vnoNOurM2QOTOqLzHsscSNDFUVktpFKOFlGYYQVXggZY2WU89bCVuxtXXFrOehG1kZWGOliUT0g--2iDQ8JBZNGBRlVVTr0gjLp0T_oS8ZDKY30E_JyII5ediAcOjnPK6k7qmqgqk5U1c2EvEX67XoigHZ6sFh90_366zJ6JbnjkkdRF66xpjaw2UXObYi1giEPBurrXqrXmkmuwAAGHXhCnu-aQR5xgWGxFxvsIxCPB-Y6IXLENaMfGrcAhyRk74EjJuTVwGC_R__7jB_9-0jPyPXz46n-8O7s_WNyg6FwoMtNHJD9i9UmPCF7a795mkTrF1S4K0E |
| 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=Physicochemical+properties+of+the+vacuolar+membrane+and+cellular+factors+determine+formation+of+vacuolar+invaginations&rft.jtitle=Scientific+reports&rft.au=Kimura%2C+Yoko&rft.au=Tsuji%2C+Takuma&rft.au=Shimizu%2C+Yosuke&rft.au=Watanabe%2C+Yuki&rft.date=2023-09-27&rft.pub=Nature+Publishing+Group+UK&rft.eissn=2045-2322&rft.volume=13&rft.issue=1&rft_id=info:doi/10.1038%2Fs41598-023-43232-5&rft.externalDocID=10_1038_s41598_023_43232_5 |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=2045-2322&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=2045-2322&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=2045-2322&client=summon |