Sugar transporter Slc37a2 regulates bone metabolism in mice via a tubular lysosomal network in osteoclasts

Osteoclasts are giant bone-digesting cells that harbor specialized lysosome-related organelles termed secretory lysosomes (SLs). SLs store cathepsin K and serve as a membrane precursor to the ruffled border, the osteoclast’s ‘resorptive apparatus’. Yet, the molecular composition and spatiotemporal o...

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Published inNature communications Vol. 14; no. 1; p. 906
Main Authors Ng, Pei Ying, Ribet, Amy B. P., Guo, Qiang, Mullin, Benjamin H., Tan, Jamie W. Y., Landao-Bassonga, Euphemie, Stephens, Sébastien, Chen, Kai, Yuan, Jinbo, Abudulai, Laila, Bollen, Maike, Nguyen, Edward T. T. T., Kular, Jasreen, Papadimitriou, John M., Søe, Kent, Teasdale, Rohan D., Xu, Jiake, Parton, Robert G., Takayanagi, Hiroshi, Pavlos, Nathan J.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 21.02.2023
Nature Publishing Group
Nature Portfolio
Subjects
13/106
13/109
14
38
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45
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631/443/63
631/80/313/1624
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Animals
Biological Transport
Bone and Bones - metabolism
Bone diseases
Bone mass
Bone Resorption - metabolism
Bone turnover
Cathepsin K
Cell Membrane - metabolism
Chemical composition
Digestion
Humanities and Social Sciences
Lysosomes
Lysosomes - metabolism
Membranes
Metabolism
Mice
Monosaccharides
multidisciplinary
Organelles
Osteoclasts
Osteoclasts - metabolism
Proteomics
Science
Science (multidisciplinary)
Sugar
Therapeutic targets
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Abstract Osteoclasts are giant bone-digesting cells that harbor specialized lysosome-related organelles termed secretory lysosomes (SLs). SLs store cathepsin K and serve as a membrane precursor to the ruffled border, the osteoclast’s ‘resorptive apparatus’. Yet, the molecular composition and spatiotemporal organization of SLs remains incompletely understood. Here, using organelle-resolution proteomics, we identify member a2 of the solute carrier 37 family (Slc37a2) as a SL sugar transporter. We demonstrate in mice that Slc37a2 localizes to the SL limiting membrane and that these organelles adopt a hitherto unnoticed but dynamic tubular network in living osteoclasts that is required for bone digestion. Accordingly, mice lacking Slc37a2 accrue high bone mass owing to uncoupled bone metabolism and disturbances in SL export of monosaccharide sugars, a prerequisite for SL delivery to the bone-lining osteoclast plasma membrane. Thus, Slc37a2 is a physiological component of the osteoclast’s unique secretory organelle and a potential therapeutic target for metabolic bone diseases. Despite the importance of osteoclast secretory lysosomes in bone digestion, the proteins that regulate them remain ill defined. Here, the authors identify Slc37a2 as a secretory lysosome sugar transporter that is required for maintenance of skeletal bone mass.
AbstractList Osteoclasts are giant bone-digesting cells that harbor specialized lysosome-related organelles termed secretory lysosomes (SLs). SLs store cathepsin K and serve as a membrane precursor to the ruffled border, the osteoclast’s ‘resorptive apparatus’. Yet, the molecular composition and spatiotemporal organization of SLs remains incompletely understood. Here, using organelle-resolution proteomics, we identify member a2 of the solute carrier 37 family (Slc37a2) as a SL sugar transporter. We demonstrate in mice that Slc37a2 localizes to the SL limiting membrane and that these organelles adopt a hitherto unnoticed but dynamic tubular network in living osteoclasts that is required for bone digestion. Accordingly, mice lacking Slc37a2 accrue high bone mass owing to uncoupled bone metabolism and disturbances in SL export of monosaccharide sugars, a prerequisite for SL delivery to the bone-lining osteoclast plasma membrane. Thus, Slc37a2 is a physiological component of the osteoclast’s unique secretory organelle and a potential therapeutic target for metabolic bone diseases. Despite the importance of osteoclast secretory lysosomes in bone digestion, the proteins that regulate them remain ill defined. Here, the authors identify Slc37a2 as a secretory lysosome sugar transporter that is required for maintenance of skeletal bone mass.
Osteoclasts are giant bone-digesting cells that harbor specialized lysosome-related organelles termed secretory lysosomes (SLs). SLs store cathepsin K and serve as a membrane precursor to the ruffled border, the osteoclast’s ‘resorptive apparatus’. Yet, the molecular composition and spatiotemporal organization of SLs remains incompletely understood. Here, using organelle-resolution proteomics, we identify member a2 of the solute carrier 37 family (Slc37a2) as a SL sugar transporter. We demonstrate in mice that Slc37a2 localizes to the SL limiting membrane and that these organelles adopt a hitherto unnoticed but dynamic tubular network in living osteoclasts that is required for bone digestion. Accordingly, mice lacking Slc37a2 accrue high bone mass owing to uncoupled bone metabolism and disturbances in SL export of monosaccharide sugars, a prerequisite for SL delivery to the bone-lining osteoclast plasma membrane. Thus, Slc37a2 is a physiological component of the osteoclast’s unique secretory organelle and a potential therapeutic target for metabolic bone diseases.
Osteoclasts are giant bone-digesting cells that harbor specialized lysosome-related organelles termed secretory lysosomes (SLs). SLs store cathepsin K and serve as a membrane precursor to the ruffled border, the osteoclast’s ‘resorptive apparatus’. Yet, the molecular composition and spatiotemporal organization of SLs remains incompletely understood. Here, using organelle-resolution proteomics, we identify member a2 of the solute carrier 37 family (Slc37a2) as a SL sugar transporter. We demonstrate in mice that Slc37a2 localizes to the SL limiting membrane and that these organelles adopt a hitherto unnoticed but dynamic tubular network in living osteoclasts that is required for bone digestion. Accordingly, mice lacking Slc37a2 accrue high bone mass owing to uncoupled bone metabolism and disturbances in SL export of monosaccharide sugars, a prerequisite for SL delivery to the bone-lining osteoclast plasma membrane. Thus, Slc37a2 is a physiological component of the osteoclast’s unique secretory organelle and a potential therapeutic target for metabolic bone diseases.Despite the importance of osteoclast secretory lysosomes in bone digestion, the proteins that regulate them remain ill defined. Here, the authors identify Slc37a2 as a secretory lysosome sugar transporter that is required for maintenance of skeletal bone mass.
Despite the importance of osteoclast secretory lysosomes in bone digestion, the proteins that regulate them remain ill defined. Here, the authors identify Slc37a2 as a secretory lysosome sugar transporter that is required for maintenance of skeletal bone mass.
ArticleNumber 906
Author Ribet, Amy B. P.
Takayanagi, Hiroshi
Stephens, Sébastien
Nguyen, Edward T. T. T.
Parton, Robert G.
Xu, Jiake
Yuan, Jinbo
Papadimitriou, John M.
Søe, Kent
Teasdale, Rohan D.
Guo, Qiang
Chen, Kai
Pavlos, Nathan J.
Mullin, Benjamin H.
Landao-Bassonga, Euphemie
Bollen, Maike
Ng, Pei Ying
Abudulai, Laila
Kular, Jasreen
Tan, Jamie W. Y.
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springer_journals_10_1038_s41467_023_36484_2
PublicationCentury 2000
PublicationDate 2023-02-21
PublicationDateYYYYMMDD 2023-02-21
PublicationDate_xml – month: 02
  year: 2023
  text: 2023-02-21
  day: 21
PublicationDecade 2020
PublicationPlace London
PublicationPlace_xml – name: London
– name: England
PublicationTitle Nature communications
PublicationTitleAbbrev Nat Commun
PublicationTitleAlternate Nat Commun
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
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Snippet Osteoclasts are giant bone-digesting cells that harbor specialized lysosome-related organelles termed secretory lysosomes (SLs). SLs store cathepsin K and...
Despite the importance of osteoclast secretory lysosomes in bone digestion, the proteins that regulate them remain ill defined. Here, the authors identify...
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Animals
Biological Transport
Bone and Bones - metabolism
Bone diseases
Bone mass
Bone Resorption - metabolism
Bone turnover
Cathepsin K
Cell Membrane - metabolism
Chemical composition
Digestion
Humanities and Social Sciences
Lysosomes
Lysosomes - metabolism
Membranes
Metabolism
Mice
Monosaccharides
multidisciplinary
Organelles
Osteoclasts
Osteoclasts - metabolism
Proteomics
Science
Science (multidisciplinary)
Sugar
Therapeutic targets
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Title Sugar transporter Slc37a2 regulates bone metabolism in mice via a tubular lysosomal network in osteoclasts
URI https://link.springer.com/article/10.1038/s41467-023-36484-2
https://www.ncbi.nlm.nih.gov/pubmed/36810735
https://www.proquest.com/docview/2778492912
https://search.proquest.com/docview/2779346409
https://pubmed.ncbi.nlm.nih.gov/PMC9945426
https://doaj.org/article/cfbfda3751ad47868d62c17e221301bd
Volume 14
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