Surface cholesterol-enriched domains specifically promote invasion of breast cancer cell lines by controlling invadopodia and extracellular matrix degradation.


Journal

Cellular and molecular life sciences : CMLS
ISSN: 1420-9071
Titre abrégé: Cell Mol Life Sci
Pays: Switzerland
ID NLM: 9705402

Informations de publication

Date de publication:
12 Jul 2022
Historique:
received: 16 03 2022
accepted: 13 06 2022
revised: 07 06 2022
entrez: 12 7 2022
pubmed: 13 7 2022
medline: 15 7 2022
Statut: epublish

Résumé

Tumor cells exhibit altered cholesterol content. However, cholesterol structural subcellular distribution and implication in cancer cell invasion are poorly understood mainly due to difficulties to investigate cholesterol both quantitatively and qualitatively and to compare isogenic cell models. Here, using the MCF10A cell line series (non-tumorigenic MCF10A, pre-malignant MCF10AT and malignant MCF10CAIa cells) as a model of breast cancer progression and the highly invasive MDA-MB-231 cell line which exhibits the common TP53 mutation, we investigated if cholesterol contributes to cancer cell invasion, whether the effects are specific to cancer cells and the underlying mechanism. We found that partial membrane cholesterol depletion specifically and reversibly decreased invasion of the malignant cell lines. Those cells exhibited dorsal surface cholesterol-enriched submicrometric domains and narrow ER-plasma membrane and ER-intracellular organelles contact sites. Dorsal cholesterol-enriched domains can be endocytosed and reach the cell ventral face where they were involved in invadopodia formation and extracellular matrix degradation. In contrast, non-malignant cells showed low cell invasion, low surface cholesterol exposure and cholesterol-dependent focal adhesions. The differential cholesterol distribution and role in breast cancer cell invasion provide new clues for the understanding of the molecular events underlying cellular mechanisms in breast cancer.

Identifiants

pubmed: 35819726
doi: 10.1007/s00018-022-04426-8
pii: 10.1007/s00018-022-04426-8
pmc: PMC9276565
doi:

Substances chimiques

Cholesterol 97C5T2UQ7J

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

417

Informations de copyright

© 2022. The Author(s).

Références

ACS Cent Sci. 2019 May 22;5(5):768-780
pubmed: 31139713
Dev Cell. 2013 Nov 11;27(3):249-62
pubmed: 24209575
Cell Commun Signal. 2019 Feb 20;17(1):15
pubmed: 30786890
Front Cell Dev Biol. 2021 Jan 12;8:622215
pubmed: 33511135
Cancer Cell Int. 2018 Feb 20;18:23
pubmed: 29467593
Cells. 2021 Apr 13;10(4):
pubmed: 33924659
Cell Mol Life Sci. 2015 Dec;72(23):4633-51
pubmed: 26077601
Eur Biophys J. 1999;28(4):312-6
pubmed: 10394623
Front Oncol. 2021 May 24;11:682911
pubmed: 34109128
Int J Mol Sci. 2018 Dec 04;19(12):
pubmed: 30518103
Nat Nanotechnol. 2017 Feb;12(2):177-183
pubmed: 27798607
Sci Adv. 2020 Dec 16;6(51):
pubmed: 33328230
Cancer Lett. 2018 Aug 10;429:66-77
pubmed: 29746928
J Cell Mol Med. 2009 Aug;13(8B):1728-1740
pubmed: 19175685
Hum Mutat. 2002 Jun;19(6):607-14
pubmed: 12007217
Biophys J. 2015 Nov 3;109(9):1925-36
pubmed: 26536269
Adv Sci (Weinh). 2020 Oct 08;7(22):2002643
pubmed: 33240781
Biochemistry. 2016 Jun 28;55(25):3504-3513
pubmed: 27267274
J Cell Biol. 2020 Jun 1;219(6):
pubmed: 32320462
Cancer Res. 2010 Oct 15;70(20):8117-26
pubmed: 20876798
Oncogene. 2019 Mar;38(12):2076-2091
pubmed: 30442980
Histochem Cell Biol. 2008 Nov;130(5):819-32
pubmed: 18820942
J Cell Biol. 2020 Aug 3;219(8):
pubmed: 32479595
Arch Biochem Biophys. 2012 Feb 15;518(2):151-6
pubmed: 22209753
Biophys J. 2005 May;88(5):3689-98
pubmed: 15722433
Elife. 2014 Jun 11;3:
pubmed: 24920391
Mol Cancer Res. 2009 Jun;7(6):809-20
pubmed: 19509114
J Bioenerg Biomembr. 2020 Oct;52(5):321-342
pubmed: 32715369
Cell Physiol Biochem. 2018;51(4):1544-1565
pubmed: 30497064
Methods Cell Biol. 2012;108:367-93
pubmed: 22325611
Matrix Biol. 2015 May-Jul;44-46:207-23
pubmed: 25794647
Biochem Biophys Res Commun. 2018 Jul 7;502(1):69-75
pubmed: 29782853
Cancer Res. 2011 May 1;71(9):3236-45
pubmed: 21415164
J Cell Sci. 2013 Jul 15;126(Pt 14):2979-89
pubmed: 23843616
Handb Exp Pharmacol. 2013;(215):211-38
pubmed: 23579458
Prog Lipid Res. 2016 Apr;62:1-24
pubmed: 26738447
J Cell Sci. 2009 Sep 1;122(Pt 17):3015-24
pubmed: 19692588
Nat Rev Mol Cell Biol. 2012 Sep;13(9):566-78
pubmed: 22850819
FASEB J. 2018 Mar;32(3):1281-1295
pubmed: 29092904
Cancer Res. 2006 Mar 15;66(6):3034-43
pubmed: 16540652
Arch Biochem Biophys. 2007 Mar 1;459(1):98-106
pubmed: 17222386
Cancer Cell Int. 2009 Mar 16;9:7
pubmed: 19291318
Proc Natl Acad Sci U S A. 1989 May;86(9):3184-8
pubmed: 2717615
Adv Drug Deliv Rev. 2013 Nov;65(13-14):1686-98
pubmed: 24055719
Traffic. 2008 Nov;9(11):1839-49
pubmed: 18647169
MethodsX. 2014 Jul 07;1:56-9
pubmed: 26150935
Ann Thorac Surg. 2002 May;73(5):1567-71
pubmed: 12022551
Bionanoscience. 2016;6:65-80
pubmed: 27014560
Int J Mol Sci. 2016 Nov 28;17(12):
pubmed: 27916803
Cell Rep. 2019 Jun 25;27(13):3927-3938.e6
pubmed: 31242424
Elife. 2019 Nov 14;8:
pubmed: 31724953
Biomolecules. 2020 Jul 29;10(8):
pubmed: 32751168
J Cell Biol. 2014 Jun 23;205(6):759-69
pubmed: 24958771
Cancer Res. 2002 Apr 15;62(8):2227-31
pubmed: 11956073
J Vis Exp. 2012 Aug 27;(66):e4119
pubmed: 22952016
Science. 2018 Aug 3;361(6401):
pubmed: 30072511
BMC Biophys. 2016 Jun 24;9:6
pubmed: 27347397
Curr Opin Cell Biol. 2018 Aug;53:37-43
pubmed: 29783105
Oncotarget. 2016 Mar 29;7(13):16227-47
pubmed: 26919102
Front Oncol. 2019 Jun 07;9:480
pubmed: 31231612
PLoS Biol. 2018 May 21;16(5):e2003864
pubmed: 29782498
Mol Cell. 2019 Feb 7;73(3):458-473.e7
pubmed: 30581148
Rapid Commun Mass Spectrom. 2016 Feb 28;30(4):533-42
pubmed: 26777684
Cancer Res. 2009 Nov 15;69(22):8594-602
pubmed: 19887621
Biochim Biophys Acta. 2016 Jul;1863(7 Pt A):1472-89
pubmed: 27066976
Cell. 2018 Oct 4;175(2):514-529.e20
pubmed: 30220461

Auteurs

Mauriane Maja (M)

CELL Unit and PICT Imaging Platform, de Duve Institute, UCLouvain, B1.75.05, avenue Hippocrate, 75, 1200, Brussels, Belgium.

Danahe Mohammed (D)

Louvain Institute of Biomolecular Science and Technology (LIBST), UCLouvain, Ottignies-Louvain-la-Neuve, Belgium.

Andra C Dumitru (AC)

Louvain Institute of Biomolecular Science and Technology (LIBST), UCLouvain, Ottignies-Louvain-la-Neuve, Belgium.

Sandrine Verstraeten (S)

Cellular and Molecular Pharmacology Unit (FACM), Louvain Drug Research Institute, UCLouvain, Brussels, Belgium.

Maxime Lingurski (M)

CELL Unit and PICT Imaging Platform, de Duve Institute, UCLouvain, B1.75.05, avenue Hippocrate, 75, 1200, Brussels, Belgium.

Marie-Paule Mingeot-Leclercq (MP)

Cellular and Molecular Pharmacology Unit (FACM), Louvain Drug Research Institute, UCLouvain, Brussels, Belgium.

David Alsteens (D)

Louvain Institute of Biomolecular Science and Technology (LIBST), UCLouvain, Ottignies-Louvain-la-Neuve, Belgium.

Donatienne Tyteca (D)

CELL Unit and PICT Imaging Platform, de Duve Institute, UCLouvain, B1.75.05, avenue Hippocrate, 75, 1200, Brussels, Belgium. donatienne.tyteca@uclouvain.be.

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