Oxylipin-PPARγ-initiated adipocyte senescence propagates secondary senescence in the bone marrow.

INK-family proteins PPARγ bone marrow adipocytes bone marrow adiposity cellular senescence glucocorticoids osteoporosis oxylipins prostaglandins senescence-associated secretory phenotype

Journal

Cell metabolism
ISSN: 1932-7420
Titre abrégé: Cell Metab
Pays: United States
ID NLM: 101233170

Informations de publication

Date de publication:
04 04 2023
Historique:
received: 09 06 2022
revised: 12 01 2023
accepted: 06 03 2023
pmc-release: 04 04 2024
medline: 7 4 2023
entrez: 5 4 2023
pubmed: 6 4 2023
Statut: ppublish

Résumé

The chronic use of glucocorticoids decreases bone mass and quality and increases bone-marrow adiposity, but the underlying mechanisms remain unclear. Here, we show that bone-marrow adipocyte (BMAd) lineage cells in adult mice undergo rapid cellular senescence upon glucocorticoid treatment. The senescent BMAds acquire a senescence-associated secretory phenotype, which spreads senescence in bone and bone marrow. Mechanistically, glucocorticoids increase the synthesis of oxylipins, such as 15d-PGJ2, for peroxisome proliferator-activated receptor gamma (PPARγ) activation. PPARγ stimulates the expression of key senescence genes and also promotes oxylipin synthesis in BMAds, forming a positive feedback loop. Transplanting senescent BMAds into the bone marrow of healthy mice is sufficient to induce the secondary spread of senescent cells and bone-loss phenotypes, whereas transplanting BMAds harboring a p16INK4a deletion did not show such effects. Thus, glucocorticoid treatment induces a lipid metabolic circuit that robustly triggers the senescence of BMAd lineage cells that, in turn, act as the mediators of glucocorticoid-induced bone deterioration.

Identifiants

pubmed: 37019080
pii: S1550-4131(23)00083-9
doi: 10.1016/j.cmet.2023.03.005
pmc: PMC10127143
mid: NIHMS1883407
pii:
doi:

Substances chimiques

PPAR gamma 0
Oxylipins 0
Glucocorticoids 0

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

667-684.e6

Subventions

Organisme : NIA NIH HHS
ID : P01 AG066603
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG068226
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG072090
Pays : United States

Commentaires et corrections

Type : CommentIn
Type : CommentIn

Informations de copyright

Copyright © 2023 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Références

J Clin Invest. 2021 Jan 19;131(2):
pubmed: 33206630
Mol Cell Endocrinol. 2002 Nov 29;197(1-2):35-44
pubmed: 12431793
Bone. 2010 Mar;46(3):564-70
pubmed: 19591965
Arthritis Rheum. 2008 Jun;58(6):1674-86
pubmed: 18512788
Stem Cells Transl Med. 2019 Mar;8(3):271-284
pubmed: 30394698
J Bone Miner Res. 2016 Nov;31(11):1920-1929
pubmed: 27341653
JCI Insight. 2022 Nov 8;7(21):
pubmed: 36048537
Cell Metab. 2022 Jan 4;34(1):75-89.e8
pubmed: 34813734
Exp Cell Res. 2007 Aug 15;313(14):3046-56
pubmed: 17560572
Cell. 2017 Jun 1;169(6):1000-1011
pubmed: 28575665
J Cereb Blood Flow Metab. 2006 Jun;26(6):811-20
pubmed: 16208315
Annu Rev Pathol. 2010;5:99-118
pubmed: 20078217
J Bone Miner Res. 2017 Jun;32(6):1153-1156
pubmed: 28370194
Physiol Rev. 2016 Apr;96(2):409-47
pubmed: 26842265
Nat Commun. 2021 Mar 23;12(1):1832
pubmed: 33758201
J Endocrinol. 2018 Jan;236(1):R69-R91
pubmed: 29051192
Adv Exp Med Biol. 2015;872:99-126
pubmed: 26215992
Elife. 2021 Oct 07;10:
pubmed: 34617510
Cell Rep. 2019 Apr 23;27(4):997-1007.e5
pubmed: 31018144
Cells. 2021 Nov 11;10(11):
pubmed: 34831349
Bone Res. 2022 Mar 2;10(1):24
pubmed: 35232979
Sci Adv. 2019 Jun 05;5(6):eaaw0254
pubmed: 31183403
Bone. 2015 Apr;73:60-8
pubmed: 25532480
Bone. 2018 May;110:134-140
pubmed: 29343445
J Vis Exp. 2018 Jan 6;(131):
pubmed: 29364278
Cell Metab. 2010 Jun 9;11(6):517-31
pubmed: 20519123
Bone. 2018 Sep;114:1-13
pubmed: 29800693
Nat Med. 2017 Sep;23(9):1072-1079
pubmed: 28825716
Elife. 2020 Apr 14;9:
pubmed: 32286228
Ageing Res Rev. 2021 Sep;70:101412
pubmed: 34302996
Nat Med. 2014 Nov;20(11):1270-8
pubmed: 25282358
Proc Natl Acad Sci U S A. 2019 Feb 12;116(7):2603-2611
pubmed: 30683717
J Clin Invest. 2006 Aug;116(8):2152-60
pubmed: 16878176
Horm Mol Biol Clin Investig. 2016 Oct 1;28(1):21-38
pubmed: 27149203
PLoS Biol. 2020 Jan 16;18(1):e3000599
pubmed: 31945054
Curr Osteoporos Rep. 2019 Dec;17(6):438-445
pubmed: 31749087
Trends Endocrinol Metab. 2014 Apr;25(4):197-211
pubmed: 24418120
Cell Metab. 2014 Aug 5;20(2):368-375
pubmed: 24998914
Nature. 2014 May 22;509(7501):439-46
pubmed: 24848057
J Clin Invest. 2020 Jul 1;130(7):3483-3498
pubmed: 32191640
Nat Rev Drug Discov. 2017 Oct;16(10):718-735
pubmed: 28729727
Cancer Sci. 2017 Apr;108(4):563-569
pubmed: 28165648
Metabolism. 2011 Nov;60(11):1500-10
pubmed: 21864867
J Cell Biol. 2013 May 13;201(4):613-29
pubmed: 23649808
Cell Stem Cell. 2017 Jun 1;20(6):771-784.e6
pubmed: 28330582
J Cell Sci. 2008 Jul 1;121(Pt 13):2235-45
pubmed: 18544633
Bone Res. 2018 Jul 18;6:22
pubmed: 30038821
Nucl Receptor Res. 2018;5:
pubmed: 30310815
Endocrinology. 2004 Apr;145(4):1835-41
pubmed: 14691012
Endocrinology. 2006 Dec;147(12):5592-9
pubmed: 16935844
J Endocrinol. 2019 Jul 1;:
pubmed: 31370004
Nat Metab. 2021 Oct;3(10):1290-1301
pubmed: 34663974
Nature. 2014 Mar 20;507(7492):323-328
pubmed: 24646994
Nat Med. 2016 Jan;22(1):78-83
pubmed: 26657143
PPAR Res. 2019 Aug 1;2019:7242030
pubmed: 31467514
Trends Cell Biol. 2017 Nov;27(11):820-832
pubmed: 28822679
J Clin Invest. 1998 Jul 15;102(2):274-82
pubmed: 9664068
Biomed Res. 2011 Feb;32(1):37-44
pubmed: 21383509
Arthritis Rheum. 2009 May;60(5):1427-37
pubmed: 19404943
Oncotarget. 2011 Nov;2(11):862-73
pubmed: 22113502
Ann N Y Acad Sci. 2011 Dec;1240:26-31
pubmed: 22172036
Adipocyte. 2016 Mar 22;5(3):251-69
pubmed: 27617171
Trends Endocrinol Metab. 2010 May;21(5):294-301
pubmed: 20079660
Front Cell Dev Biol. 2021 Mar 29;9:645593
pubmed: 33855023
N Engl J Med. 2011 Jul 7;365(1):62-70
pubmed: 21732837
BMC Cell Biol. 2015 Mar 13;16:9
pubmed: 25887471
Bone. 2020 Mar;132:115220
pubmed: 31904537
Cell Death Dis. 2013 Oct 03;4:e832
pubmed: 24091675
Best Pract Res Clin Endocrinol Metab. 2021 Jul;35(4):101518
pubmed: 33812853
Semin Arthritis Rheum. 2014 Aug;44(1):47-54
pubmed: 24680381
Endocrinology. 2016 Feb;157(2):508-21
pubmed: 26696121
Dev Cell. 2014 Dec 22;31(6):722-33
pubmed: 25499914
Front Biosci. 2008 Jan 01;13:1813-26
pubmed: 17981670
J Endocrinol. 2020 Apr;245(1):141-153
pubmed: 32045363
Annu Rev Physiol. 2020 Feb 10;82:461-484
pubmed: 31702948
Cell Metab. 2021 Jun 1;33(6):1124-1136.e5
pubmed: 33811820
Eur J Endocrinol. 2018 Oct 01;179(4):R165-R182
pubmed: 30299886
Adipocyte. 2017 Jul 3;6(3):193-204
pubmed: 28872979
Transl Res. 2019 Jul;209:14-21
pubmed: 30981698
Nature. 2014 Mar 20;507(7492):376-380
pubmed: 24647000
Nat Rev Mol Cell Biol. 2014 Jul;15(7):482-96
pubmed: 24954210
Nat Cell Biol. 2013 Aug;15(8):978-90
pubmed: 23770676
Clin Exp Rheumatol. 2015 Jul-Aug;33(4 Suppl 92):S37-9
pubmed: 26458014

Auteurs

Xiaonan Liu (X)

Department of Orthopaedic Surgery, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.

Yiru Gu (Y)

Department of Orthopaedic Surgery, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.

Surendra Kumar (S)

Department of Orthopaedic Surgery, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.

Sahran Amin (S)

Department of Orthopaedic Surgery, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.

Qiaoyue Guo (Q)

Department of Orthopaedic Surgery, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.

Jiekang Wang (J)

Department of Orthopaedic Surgery, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.

Ching-Lien Fang (CL)

Department of Orthopaedic Surgery, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.

Xu Cao (X)

Department of Orthopaedic Surgery, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.

Mei Wan (M)

Department of Orthopaedic Surgery, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA. Electronic address: mwan4@jhmi.edu.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH