Caveolae are specialized domains of the vertebrate cell surface with a well-defined morphology and crucial roles in cell migration and mechanoprotection. Unique compositions of proteins and lipids determine membrane architectures. The precise caveolar lipid profile and the roles of the major caveolar structural proteins, caveolins and cavins, in selectively sorting lipids have not been defined. Here, we used quantitative nanoscale lipid mapping together with molecular dynamic simulations to define the caveolar lipid profile. We show that caveolin-1 (CAV1) and cavin1 individually sort distinct plasma membrane lipids. Intact caveolar structures composed of both CAV1 and cavin1 further generate a unique lipid nano-environment. The caveolar lipid sorting capability includes selectivities for lipid headgroups and acyl chains. Because lipid headgroup metabolism and acyl chain remodeling are tightly regulated, this selective lipid sorting may allow caveolae to act as transit hubs to direct communications among lipid metabolism, vesicular trafficking, and signaling.
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1 March 2021
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January 26 2021
Caveolin-1 and cavin1 act synergistically to generate a unique lipid environment in caveolae
Yong Zhou
,
1
Department of Integrative Biology and Pharmacology, University of Texas Medical School, Houston, TX
Yong Zhou: Yong.Zhou@uth.tmc.edu
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Nicholas Ariotti
,
Nicholas Ariotti
2
University of New South Wales Sydney, Mark Wainwright Analytical Center, Sydney, New South Wales, Australia
3
University of New South Wales Sydney, Department of Pathology, School of Medical Sciences, Kensington, Sydney, New South Wales, Australia
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James Rae
,
James Rae
4
The University of Queensland, Institute for Molecular Bioscience, Brisbane, Queensland, Australia
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Hong Liang
,
Hong Liang
1
Department of Integrative Biology and Pharmacology, University of Texas Medical School, Houston, TX
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Vikas Tillu
,
Vikas Tillu
4
The University of Queensland, Institute for Molecular Bioscience, Brisbane, Queensland, Australia
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Shern Tee
,
Shern Tee
5
Australian Institute for Bioengineering and Nanotechnology, The University of Queensland, Brisbane, Queensland, Australia
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Michele Bastiani
,
Michele Bastiani
4
The University of Queensland, Institute for Molecular Bioscience, Brisbane, Queensland, Australia
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Adekunle T. Bademosi
,
Adekunle T. Bademosi
6
Queensland Brain Institute, The University of Queensland, Brisbane, Queensland, Australia
7
Clem Jones Centre for Ageing Dementia Research, The University of Queensland, Brisbane, Queensland, Australia
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Brett M. Collins
,
Brett M. Collins
3
University of New South Wales Sydney, Department of Pathology, School of Medical Sciences, Kensington, Sydney, New South Wales, Australia
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Frederic A. Meunier
,
Frederic A. Meunier
6
Queensland Brain Institute, The University of Queensland, Brisbane, Queensland, Australia
7
Clem Jones Centre for Ageing Dementia Research, The University of Queensland, Brisbane, Queensland, Australia
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John F. Hancock
,
John F. Hancock
1
Department of Integrative Biology and Pharmacology, University of Texas Medical School, Houston, TX
8
Program in Cell and Regulatory Biology, University of Texas Graduate School of Biomedical Sciences, Houston, TX
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Robert G. Parton
4
The University of Queensland, Institute for Molecular Bioscience, Brisbane, Queensland, Australia
9
The University of Queensland, Centre for Microscopy and Microanalysis, Brisbane, Queensland, Australia
Correspondence to Robert G. Parton: R.Parton@imb.uq.edu.au
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Yong Zhou
1
Department of Integrative Biology and Pharmacology, University of Texas Medical School, Houston, TX
Nicholas Ariotti
2
University of New South Wales Sydney, Mark Wainwright Analytical Center, Sydney, New South Wales, Australia
3
University of New South Wales Sydney, Department of Pathology, School of Medical Sciences, Kensington, Sydney, New South Wales, Australia
James Rae
4
The University of Queensland, Institute for Molecular Bioscience, Brisbane, Queensland, Australia
Hong Liang
1
Department of Integrative Biology and Pharmacology, University of Texas Medical School, Houston, TX
Vikas Tillu
4
The University of Queensland, Institute for Molecular Bioscience, Brisbane, Queensland, Australia
Shern Tee
5
Australian Institute for Bioengineering and Nanotechnology, The University of Queensland, Brisbane, Queensland, Australia
Michele Bastiani
4
The University of Queensland, Institute for Molecular Bioscience, Brisbane, Queensland, Australia
Adekunle T. Bademosi
6
Queensland Brain Institute, The University of Queensland, Brisbane, Queensland, Australia
7
Clem Jones Centre for Ageing Dementia Research, The University of Queensland, Brisbane, Queensland, Australia
Brett M. Collins
3
University of New South Wales Sydney, Department of Pathology, School of Medical Sciences, Kensington, Sydney, New South Wales, Australia
Frederic A. Meunier
6
Queensland Brain Institute, The University of Queensland, Brisbane, Queensland, Australia
7
Clem Jones Centre for Ageing Dementia Research, The University of Queensland, Brisbane, Queensland, Australia
John F. Hancock
1
Department of Integrative Biology and Pharmacology, University of Texas Medical School, Houston, TX
8
Program in Cell and Regulatory Biology, University of Texas Graduate School of Biomedical Sciences, Houston, TX
Robert G. Parton
4
The University of Queensland, Institute for Molecular Bioscience, Brisbane, Queensland, Australia
9
The University of Queensland, Centre for Microscopy and Microanalysis, Brisbane, Queensland, Australia
Correspondence to Robert G. Parton: R.Parton@imb.uq.edu.au
Yong Zhou: Yong.Zhou@uth.tmc.edu
Received:
May 19 2020
Revision Received:
November 20 2020
Accepted:
December 21 2020
Online Issn: 1540-8140
Print Issn: 0021-9525
Funding:
National Health and Medical Research Council
(APP1140064, APP1150083, APP1156489, GNT1120381, GNT1155794, APP1136021, APP1102730)
National Institutes of Health
(R01 GM124233)
University of Queensland
(NO AWARD)
© 2021 Zhou et al.
2021
This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
J Cell Biol (2021) 220 (3): e202005138.
Article history
Received:
May 19 2020
Revision Received:
November 20 2020
Accepted:
December 21 2020
Citation
Yong Zhou, Nicholas Ariotti, James Rae, Hong Liang, Vikas Tillu, Shern Tee, Michele Bastiani, Adekunle T. Bademosi, Brett M. Collins, Frederic A. Meunier, John F. Hancock, Robert G. Parton; Caveolin-1 and cavin1 act synergistically to generate a unique lipid environment in caveolae. J Cell Biol 1 March 2021; 220 (3): e202005138. doi: https://doi.org/10.1083/jcb.202005138
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