ORP5 and ORP8 orchestrate lipid droplet biogenesis and maintenance at ER-mitochondria contact sites

Lipid droplets (LDs) are the primary organelles of lipid storage, buffering energy fluctuations of the cell. They store neutral lipids in their core that is surrounded by a protein-decorated phospholipid monolayer. LDs arise from the endoplasmic reticulum (ER). The ER protein seipin, localizing at E...

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Published in:	The Journal of cell biology Vol. 221; no. 9; p. 1
Main Authors:	Guyard, Valentin, Monteiro-Cardoso, Vera Filipa, Omrane, Mohyeddine, Sauvanet, Cécile, Houcine, Audrey, Boulogne, Claire, Ben Mbarek, Kalthoum, Vitale, Nicolas, Faklaris, Orestis, El Khallouki, Naima, Thiam, Abdou Rachid, Giordano, Francesca
Format:	Journal Article
Language:	English
Published:	United States Rockefeller University Press 05-09-2022
Subjects:	Biochemistry Biosynthesis Crosstalk Droplets Endoplasmic reticulum Endoplasmic Reticulum - metabolism Energy storage Life Sciences Lipid Droplets - metabolism Lipid Metabolism Lipid transfer proteins Lipids Membranes Mitochondria Mitochondria - metabolism Nucleation Organelles Phosphatidic acid Phospholipids Phospholipids - metabolism Proteins Receptors, Steroid - metabolism Biochemistry, Organelles
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Abstract	Lipid droplets (LDs) are the primary organelles of lipid storage, buffering energy fluctuations of the cell. They store neutral lipids in their core that is surrounded by a protein-decorated phospholipid monolayer. LDs arise from the endoplasmic reticulum (ER). The ER protein seipin, localizing at ER-LD junctions, controls LD nucleation and growth. However, how LD biogenesis is spatially and temporally coordinated remains elusive. Here, we show that the lipid transfer proteins ORP5 and ORP8 control LD biogenesis at mitochondria-associated ER membrane (MAM) subdomains, enriched in phosphatidic acid. We found that ORP5/8 regulates seipin recruitment to these MAM-LD contacts, and their loss impairs LD biogenesis. Importantly, the integrity of ER-mitochondria contact sites is crucial for ORP5/8 function in regulating seipin-mediated LD biogenesis. Our study uncovers an unprecedented ORP5/8 role in orchestrating LD biogenesis and maturation at MAMs and brings novel insights into the metabolic crosstalk between mitochondria, ER, and LDs at the membrane contact sites.
AbstractList	Lipid droplets (LDs) are the primary organelles of lipid storage, buffering energy fluctuations of the cell. They store neutral lipids in their core that is surrounded by a protein-decorated phospholipid monolayer. LDs arise from the endoplasmic reticulum (ER). The ER protein seipin, localizing at ER-LD junctions, controls LD nucleation and growth. However, how LD biogenesis is spatially and temporally coordinated remains elusive. Here, we show that the lipid transfer proteins ORP5 and ORP8 control LD biogenesis at mitochondria-associated ER membrane (MAM) subdomains, enriched in phosphatidic acid. We found that ORP5/8 regulates seipin recruitment to these MAM–LD contacts, and their loss impairs LD biogenesis. Importantly, the integrity of ER–mitochondria contact sites is crucial for ORP5/8 function in regulating seipin-mediated LD biogenesis. Our study uncovers an unprecedented ORP5/8 role in orchestrating LD biogenesis and maturation at MAMs and brings novel insights into the metabolic crosstalk between mitochondria, ER, and LDs at the membrane contact sites. We reveal that the lipid droplets can emerge from ER subdomains in contact with mitochondria. The lipid transfer proteins ORP5 and ORP8 localize at these sites where they regulate the recruitment of seipin and ensure proper LD biogenesis. Lipid droplets (LDs) are the primary organelles of lipid storage, buffering energy fluctuations of the cell. They store neutral lipids in their core that is surrounded by a protein-decorated phospholipid monolayer. LDs arise from the endoplasmic reticulum (ER). The ER protein seipin, localizing at ER-LD junctions, controls LD nucleation and growth. However, how LD biogenesis is spatially and temporally coordinated remains elusive. Here, we show that the lipid transfer proteins ORP5 and ORP8 control LD biogenesis at mitochondria-associated ER membrane (MAM) subdomains, enriched in phosphatidic acid. We found that ORP5/8 regulates seipin recruitment to these MAM–LD contacts, and their loss impairs LD biogenesis. Importantly, the integrity of ER–mitochondria contact sites is crucial for ORP5/8 function in regulating seipin-mediated LD biogenesis. Our study uncovers an unprecedented ORP5/8 role in orchestrating LD biogenesis and maturation at MAMs and brings novel insights into the metabolic crosstalk between mitochondria, ER, and LDs at the membrane contact sites. Lipid droplets (LDs) are the primary organelles of lipid storage, buffering energy fluctuations of the cell. They store neutral lipids in their core that is surrounded by a protein-decorated phospholipid monolayer. LDs arise from the endoplasmic reticulum (ER). The ER protein seipin, localizing at ER-LD junctions, controls LD nucleation and growth. However, how LD biogenesis is spatially and temporally coordinated remains elusive. Here, we show that the lipid transfer proteins ORP5 and ORP8 control LD biogenesis at mitochondria-associated ER membrane (MAM) subdomains, enriched in phosphatidic acid. We found that ORP5/8 regulates seipin recruitment to these MAM-LD contacts, and their loss impairs LD biogenesis. Importantly, the integrity of ER-mitochondria contact sites is crucial for ORP5/8 function in regulating seipin-mediated LD biogenesis. Our study uncovers an unprecedented ORP5/8 role in orchestrating LD biogenesis and maturation at MAMs and brings novel insights into the metabolic crosstalk between mitochondria, ER, and LDs at the membrane contact sites.Lipid droplets (LDs) are the primary organelles of lipid storage, buffering energy fluctuations of the cell. They store neutral lipids in their core that is surrounded by a protein-decorated phospholipid monolayer. LDs arise from the endoplasmic reticulum (ER). The ER protein seipin, localizing at ER-LD junctions, controls LD nucleation and growth. However, how LD biogenesis is spatially and temporally coordinated remains elusive. Here, we show that the lipid transfer proteins ORP5 and ORP8 control LD biogenesis at mitochondria-associated ER membrane (MAM) subdomains, enriched in phosphatidic acid. We found that ORP5/8 regulates seipin recruitment to these MAM-LD contacts, and their loss impairs LD biogenesis. Importantly, the integrity of ER-mitochondria contact sites is crucial for ORP5/8 function in regulating seipin-mediated LD biogenesis. Our study uncovers an unprecedented ORP5/8 role in orchestrating LD biogenesis and maturation at MAMs and brings novel insights into the metabolic crosstalk between mitochondria, ER, and LDs at the membrane contact sites.
Author	Omrane, Mohyeddine Boulogne, Claire Houcine, Audrey Monteiro-Cardoso, Vera Filipa Sauvanet, Cécile Ben Mbarek, Kalthoum Vitale, Nicolas Thiam, Abdou Rachid El Khallouki, Naima Giordano, Francesca Guyard, Valentin Faklaris, Orestis
AuthorAffiliation	7 MRI, BioCampus Montpellier, CRBM, Univ. Montpellier, CNRS, Montpellier, France 5 Imagerie-Gif, Electron Microscopy Facility, Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ. Paris-Sud, Université Paris-Saclay, Gif-sur-Yvette, France 3 Laboratoire de Physique de l’École Normale Supérieure, ENS, Université PSL, CNRS, Sorbonne Université, Université Paris Cité, Paris, France 6 Centre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives, UPR-321267000 Strasbourg, France 4 Institut Jacques Monod, CNRS, UMR7592, Université Paris Diderot, Sorbonne Paris Cité, Paris, France 1 Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Saclay, Gif-sur-Yvette, France 2 Inserm U1280, Gif-sur-Yvette, France
AuthorAffiliation_xml	– name: 6 Centre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives, UPR-321267000 Strasbourg, France – name: 7 MRI, BioCampus Montpellier, CRBM, Univ. Montpellier, CNRS, Montpellier, France – name: 4 Institut Jacques Monod, CNRS, UMR7592, Université Paris Diderot, Sorbonne Paris Cité, Paris, France – name: 1 Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Saclay, Gif-sur-Yvette, France – name: 5 Imagerie-Gif, Electron Microscopy Facility, Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ. Paris-Sud, Université Paris-Saclay, Gif-sur-Yvette, France – name: 3 Laboratoire de Physique de l’École Normale Supérieure, ENS, Université PSL, CNRS, Sorbonne Université, Université Paris Cité, Paris, France – name: 2 Inserm U1280, Gif-sur-Yvette, France
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 V. Guyard, V.F. Monteiro-Cardoso, and M. Omrane contributed equally to this paper. A.R. Thiam and F. Giordano share equal senior authorship.
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Snippet	Lipid droplets (LDs) are the primary organelles of lipid storage, buffering energy fluctuations of the cell. They store neutral lipids in their core that is... We reveal that the lipid droplets can emerge from ER subdomains in contact with mitochondria. The lipid transfer proteins ORP5 and ORP8 localize at these sites...
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SubjectTerms	Biochemistry Biosynthesis Crosstalk Droplets Endoplasmic reticulum Endoplasmic Reticulum - metabolism Energy storage Life Sciences Lipid Droplets - metabolism Lipid Metabolism Lipid transfer proteins Lipids Membranes Mitochondria Mitochondria - metabolism Nucleation Organelles Phosphatidic acid Phospholipids Phospholipids - metabolism Proteins Receptors, Steroid - metabolism
Title	ORP5 and ORP8 orchestrate lipid droplet biogenesis and maintenance at ER-mitochondria contact sites
URI	https://www.ncbi.nlm.nih.gov/pubmed/35969857 https://www.proquest.com/docview/2709764148 https://www.proquest.com/docview/2702976744 https://hal.science/hal-04234751 https://pubmed.ncbi.nlm.nih.gov/PMC9375143
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