Scalable Generation of Pre-Vascularized and Functional Human Beige Adipose Organoids.

adipose-derived stroma/stem cells (ASC) beige and brown adipocytes guided-assembly hydrogels microtissues organoid morphogenesis stromal vascular fraction

Journal

Advanced science (Weinheim, Baden-Wurttemberg, Germany)
ISSN: 2198-3844
Titre abrégé: Adv Sci (Weinh)
Pays: Germany
ID NLM: 101664569

Informations de publication

Date de publication:
11 2023
Historique:
revised: 07 08 2023
received: 07 03 2023
medline: 6 11 2023
pubmed: 21 9 2023
entrez: 21 9 2023
Statut: ppublish

Résumé

Obesity and type 2 diabetes are becoming a global sociobiomedical burden. Beige adipocytes are emerging as key inducible actors and putative relevant therapeutic targets for improving metabolic health. However, in vitro models of human beige adipose tissue are currently lacking and hinder research into this cell type and biotherapy development. Unlike traditional bottom-up engineering approaches that aim to generate building blocks, here a scalable system is proposed to generate pre-vascularized and functional human beige adipose tissue organoids using the human stromal vascular fraction of white adipose tissue as a source of adipose and endothelial progenitors. This engineered method uses a defined biomechanical and chemical environment using tumor growth factor β (TGFβ) pathway inhibition and specific gelatin methacryloyl (GelMA) embedding parameters to promote the self-organization of spheroids in GelMA hydrogel, facilitating beige adipogenesis and vascularization. The resulting vascularized organoids display key features of native beige adipose tissue including inducible Uncoupling Protein-1 (UCP1) expression, increased uncoupled mitochondrial respiration, and batokines secretion. The controlled assembly of spheroids allows to translate organoid morphogenesis to a macroscopic scale, generating vascularized centimeter-scale beige adipose micro-tissues. This approach represents a significant advancement in developing in vitro human beige adipose tissue models and facilitates broad applications ranging from basic research to biotherapies.

Identifiants

pubmed: 37731092
doi: 10.1002/advs.202301499
pmc: PMC10625054
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2301499

Subventions

Organisme : Agence Nationale de la Recherche
ID : ANR-18-CE18-0006
Organisme : Agence Nationale de la Recherche
ID : ANR21 CE1941
Organisme : Agence Nationale de la Recherche
ID : 18-EURE-0003
Organisme : LAAS-CNRS micro and nanotechnologies platform
Organisme : MultiFAB project
ID : 16007407/MP0011594
Organisme : HoliFAB project
ID : 760927
Organisme : HoliFAB project
ID : PID2020-114112RB-I00
Organisme : MCIN/AEI/10.13039/501100011033, Spain and the European Regional Development Fund
ID : PID2020-114112RB-I00

Informations de copyright

© 2023 The Authors. Advanced Science published by Wiley-VCH GmbH.

Références

J Physiol. 2022 Feb;600(4):869-883
pubmed: 34387376
Nature. 2012 Jan 11;481(7382):463-8
pubmed: 22237023
Gene. 2021 Feb 5;768:145269
pubmed: 33148459
Cells. 2022 Apr 20;11(9):
pubmed: 35563700
Cell Discov. 2017 Oct 10;3:17036
pubmed: 29021914
J Biol Chem. 2003 Jan 3;278(1):263-9
pubmed: 12414803
Cell Tissue Res. 1991 Oct;266(1):149-61
pubmed: 1747909
Sci Rep. 2016 Aug 31;6:32490
pubmed: 27577850
Tissue Eng Part A. 2017 Apr;23(7-8):253-262
pubmed: 28073315
Front Bioeng Biotechnol. 2022 Jul 01;10:906395
pubmed: 35845420
ACS Biomater Sci Eng. 2021 Nov 8;7(11):5175-5188
pubmed: 34597013
Nat Neurosci. 2015 Oct;18(10):1518-29
pubmed: 26368944
Trends Endocrinol Metab. 2017 Dec;28(12):855-867
pubmed: 29113711
Sci Rep. 2016 Aug 09;6:31036
pubmed: 27503340
PLoS One. 2014 Jan 06;9(1):e83363
pubmed: 24400072
Cell Stem Cell. 2019 Jun 6;24(6):860-876
pubmed: 31173716
Rev Endocr Metab Disord. 2022 Feb;23(1):103-110
pubmed: 33751363
Cell Stem Cell. 2022 May 5;29(5):667-677
pubmed: 35523137
Nat Neurosci. 2011 Aug 30;14(11):1481-8
pubmed: 21878933
Cell. 2014 Jun 5;157(6):1279-1291
pubmed: 24906147
Macromol Biosci. 2019 Jun;19(6):e1900098
pubmed: 31026127
Biomaterials. 2015 Dec;73:254-71
pubmed: 26414409
Cell. 2022 Feb 3;185(3):419-446
pubmed: 35120662
Pharmaceuticals (Basel). 2022 Jan 29;15(2):
pubmed: 35215284
FEBS Lett. 1984 Feb 13;167(1):10-4
pubmed: 6698197
Stem Cells. 2020 Jun;38(6):782-796
pubmed: 32083764
Cell Metab. 2018 Mar 6;27(3):602-615.e4
pubmed: 29514068
Stem Cell Res Ther. 2022 Jun 28;13(1):276
pubmed: 35765015
Sci Rep. 2017 Jun 7;7(1):2954
pubmed: 28592806
Adv Sci (Weinh). 2021 Aug;8(16):e2100106
pubmed: 34165908
Biomaterials. 2017 Jun;129:188-198
pubmed: 28343005
Diabetes. 2017 Jun;66(6):1479-1490
pubmed: 28254844
Nat Rev Endocrinol. 2022 Dec;18(12):744-759
pubmed: 36071283
Nat Commun. 2021 Nov 26;12(1):6931
pubmed: 34836963
Nat Rev Mater. 2021;6(5):402-420
pubmed: 33623712
Sci Rep. 2017 Jan 13;7:40445
pubmed: 28084425
Physiol Rev. 2004 Jan;84(1):277-359
pubmed: 14715917
Biomaterials. 2021 Feb;269:120611
pubmed: 33385685
Dev Cell. 2011 Jun 14;20(6):815-26
pubmed: 21664579
Cell Stem Cell. 2008 Sep 11;3(3):301-13
pubmed: 18786417
Cell Metab. 2017 Feb 7;25(2):481
pubmed: 28178569
Tissue Eng Part B Rev. 2018 Aug;24(4):289-299
pubmed: 28316259
Am J Physiol Cell Physiol. 2012 Jan 15;302(2):C463-72
pubmed: 22075692
Sci Rep. 2018 Jan 11;8(1):523
pubmed: 29323267
J Biomed Mater Res A. 2022 May;110(5):1147-1165
pubmed: 35102687
Acta Biomater. 2018 Apr 15;71:486-495
pubmed: 29555462
J Pathol. 2003 Oct;201(2):296-302
pubmed: 14517847
Cell Metab. 2018 Nov 6;28(5):750-763.e6
pubmed: 30122557
Sci Rep. 2019 May 10;9(1):7250
pubmed: 31076601
Front Endocrinol (Lausanne). 2018 Aug 07;9:447
pubmed: 30131768
Mol Aspects Med. 2019 Aug;68:74-81
pubmed: 31228478
FEBS Lett. 1997 Jul 7;411(1):83-6
pubmed: 9247147
Biomaterials. 2009 Dec;30(35):6702-7
pubmed: 19783300
Trends Mol Med. 2021 May;27(5):416-418
pubmed: 33865720
FASEB J. 2017 May;31(5):1775-1786
pubmed: 28119398
Cell Stem Cell. 2022 May 5;29(5):722-743
pubmed: 35523138
Obesity (Silver Spring). 2019 Oct;27(10):1606-1616
pubmed: 31411815
Cell. 2020 Jul 23;182(2):372-387.e14
pubmed: 32610084
Nat Commun. 2020 Jun 2;11(1):2758
pubmed: 32488069
J Cell Mol Med. 2012 Dec;16(12):2851-60
pubmed: 22882758
FEBS J. 2021 Jun;288(12):3647-3662
pubmed: 34028971
J Biol Chem. 1995 Mar 10;270(10):5666-73
pubmed: 7890689
Adv Sci (Weinh). 2022 Jun;9(18):e2104451
pubmed: 35466539
Cells. 2022 Sep 07;11(18):
pubmed: 36139371
Am J Physiol Endocrinol Metab. 2013 Dec;305(12):E1427-35
pubmed: 24105412
Adv Sci (Weinh). 2023 Nov;10(31):e2301499
pubmed: 37731092
Cell Metab. 2017 Oct 3;26(4):672-685.e4
pubmed: 28918936
Methods. 2013 Jan;59(1):80-8
pubmed: 23021995
Cell Metab. 2012 Feb 8;15(2):222-9
pubmed: 22326223
Front Cell Dev Biol. 2022 Aug 01;10:955612
pubmed: 35979379
PLoS One. 2020 May 26;15(5):e0233152
pubmed: 32453755
J Cell Sci. 1992 Dec;103 ( Pt 4):931-42
pubmed: 1362571
BMC Cell Biol. 2017 Jan 23;18(1):10
pubmed: 28114883
Methods Mol Biol. 2015;1235:105-20
pubmed: 25388390

Auteurs

Mélanie Escudero (M)

RESTORE Research Center, Université de Toulouse, INSERM 1301, CNRS 5070, EFS, ENVT, Toulouse, 31100, France.
LAAS-CNRS, Université de Toulouse, CNRS, INSA, Toulouse, 31400, France.

Laurence Vaysse (L)

RESTORE Research Center, Université de Toulouse, INSERM 1301, CNRS 5070, EFS, ENVT, Toulouse, 31100, France.

Gozde Eke (G)

LAAS-CNRS, Université de Toulouse, CNRS, INSA, Toulouse, 31400, France.

Marion Peyrou (M)

CIBER "Fisiopatologia de la Obesidad y Nutrición", Department of Biochemistry and Molecular Biomedicine, University of Barcelona, Madrid, 28029, Spain.

Francesc Villarroya (F)

CIBER "Fisiopatologia de la Obesidad y Nutrición", Department of Biochemistry and Molecular Biomedicine, University of Barcelona, Madrid, 28029, Spain.

Sophie Bonnel (S)

RESTORE Research Center, Université de Toulouse, INSERM 1301, CNRS 5070, EFS, ENVT, Toulouse, 31100, France.

Yannick Jeanson (Y)

RESTORE Research Center, Université de Toulouse, INSERM 1301, CNRS 5070, EFS, ENVT, Toulouse, 31100, France.

Louisa Boyer (L)

LAAS-CNRS, Université de Toulouse, CNRS, INSA, Toulouse, 31400, France.

Christophe Vieu (C)

LAAS-CNRS, Université de Toulouse, CNRS, INSA, Toulouse, 31400, France.

Benoit Chaput (B)

Service de Chirurgie plastique, reconstructrice et esthétique, Centre Hospitalier Universitaire Rangueil, Toulouse, 31400, France.

Xi Yao (X)

Faculté de Médecine, Université Côte d'Azur, INSERM, CNRS, iBV, Nice, 06103, France.

Frédéric Deschaseaux (F)

RESTORE Research Center, Université de Toulouse, INSERM 1301, CNRS 5070, EFS, ENVT, Toulouse, 31100, France.

Mélissa Parny (M)

RESTORE Research Center, Université de Toulouse, INSERM 1301, CNRS 5070, EFS, ENVT, Toulouse, 31100, France.
LabHPEC, Histology and Pathology Department, Université de Toulouse, ENVT, Toulouse, 31076, France.

Isabelle Raymond-Letron (I)

RESTORE Research Center, Université de Toulouse, INSERM 1301, CNRS 5070, EFS, ENVT, Toulouse, 31100, France.
LabHPEC, Histology and Pathology Department, Université de Toulouse, ENVT, Toulouse, 31076, France.

Christian Dani (C)

Faculté de Médecine, Université Côte d'Azur, INSERM, CNRS, iBV, Nice, 06103, France.

Audrey Carrière (A)

RESTORE Research Center, Université de Toulouse, INSERM 1301, CNRS 5070, EFS, ENVT, Toulouse, 31100, France.

Laurent Malaquin (L)

LAAS-CNRS, Université de Toulouse, CNRS, INSA, Toulouse, 31400, France.

Louis Casteilla (L)

RESTORE Research Center, Université de Toulouse, INSERM 1301, CNRS 5070, EFS, ENVT, Toulouse, 31100, France.

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