Fibroblast-derived matrix models desmoplastic properties and forms a prognostic signature in cancer progression.


Journal

Frontiers in immunology
ISSN: 1664-3224
Titre abrégé: Front Immunol
Pays: Switzerland
ID NLM: 101560960

Informations de publication

Date de publication:
2023
Historique:
received: 30 01 2023
accepted: 30 05 2023
medline: 7 8 2023
pubmed: 4 8 2023
entrez: 4 8 2023
Statut: epublish

Résumé

The desmoplastic reaction observed in many cancers is a hallmark of disease progression and prognosis, particularly in breast and pancreatic cancer. Stromal-derived extracellular matrix (ECM) is significantly altered in desmoplasia, and as such plays a critical role in driving cancer progression. Using fibroblast-derived matrices (FDMs), we show that cancer cells have increased growth on cancer associated FDMs, when compared to FDMs derived from non-malignant tissue (normal) fibroblasts. We assess the changes in ECM characteristics from normal to cancer-associated stroma at the primary tumor site. Compositional, structural, and mechanical analyses reveal significant differences, with an increase in abundance of core ECM proteins, coupled with an increase in stiffness and density in cancer-associated FDMs. From compositional changes of FDM, we derived a 36-ECM protein signature, which we show matches in large part with the changes in pancreatic ductal adenocarcinoma (PDAC) tumor and metastases progression. Additionally, this signature also matches at the transcriptomic level in multiple cancer types in patients, prognostic of their survival. Together, our results show relevance of FDMs for cancer modelling and identification of desmoplastic ECM components for further mechanistic studies.

Identifiants

pubmed: 37539058
doi: 10.3389/fimmu.2023.1154528
pmc: PMC10395327
doi:

Substances chimiques

Extracellular Matrix Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1154528

Informations de copyright

Copyright © 2023 Rafaeva, Jensen, Horton, Zornhagen, Strøbech, Fleischhauer, Mayorca-Guiliani, Nielsen, Grønseth, Kuś, Schoof, Arnes, Koch, Clausen-Schaumann, Izzi, Reuten and Erler.

Déclaration de conflit d'intérêts

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Références

Cell. 2009 Nov 25;139(5):891-906
pubmed: 19931152
Mol Cell Proteomics. 2012 Apr;11(4):M111.014647
pubmed: 22159717
PLoS Comput Biol. 2019 Oct 28;15(10):e1007251
pubmed: 31658254
Cancer Cell. 2005 May;7(5):469-83
pubmed: 15894267
Cancers (Basel). 2021 Jul 02;13(13):
pubmed: 34283050
Nat Med. 2017 Jul;23(7):890-898
pubmed: 28604702
Curr Protoc Pharmacol. 2016 Jun 01;73:14.39.1-14.39.20
pubmed: 27248578
Nat Commun. 2021 Jan 4;12(1):22
pubmed: 33397959
Proteomics. 2018 Mar;18(5-6):e1700167
pubmed: 29280568
BMC Med. 2008 Apr 28;6:11
pubmed: 18442412
World J Gastroenterol. 2016 Nov 28;22(44):9694-9705
pubmed: 27956793
Cancers (Basel). 2020 May 21;12(5):
pubmed: 32455670
Pathobiology. 2015 Sep;82(3-4):142-52
pubmed: 26330355
BMC Bioinformatics. 2018 Nov 6;19(1):404
pubmed: 30400809
J Cell Biol. 2017 Nov 6;216(11):3799-3816
pubmed: 29021221
Signal Transduct Target Ther. 2021 Jun 10;6(1):218
pubmed: 34108441
J Hematol Oncol. 2017 Mar 28;10(1):76
pubmed: 28351381
Heliyon. 2021 Feb 13;7(2):e06252
pubmed: 33659755
Methods Cell Biol. 2020;156:109-160
pubmed: 32222216
Cancer Res. 2013 Mar 15;73(6):1721-32
pubmed: 23345161
Surgery. 2002 Feb;131(2):129-34
pubmed: 11854689
J Biol Chem. 2019 Jan 4;294(1):281-289
pubmed: 30409905
Biochim Biophys Acta Rev Cancer. 2020 Apr;1873(2):188356
pubmed: 32147542
Oncotarget. 2012 Mar;3(3):267-85
pubmed: 22408128
Nat Methods. 2014 Mar;11(3):319-24
pubmed: 24487582
BMC Cancer. 2011 Jun 13;11:245
pubmed: 21668992
Nat Med. 2016 May;22(5):497-505
pubmed: 27089513
Nat Commun. 2022 Aug 6;13(1):4587
pubmed: 35933466
Methods Cell Biol. 2020;156:185-203
pubmed: 32222219
Nat Protoc. 2017 Nov;12(11):2376-2390
pubmed: 29048422
Cell. 2015 Jan 15;160(1-2):324-38
pubmed: 25557080
Dis Model Mech. 2011 Mar;4(2):165-78
pubmed: 21324931
PLoS One. 2014 Dec 09;9(12):e114983
pubmed: 25490719
FEBS J. 2020 Apr;287(8):1454-1477
pubmed: 31972068
Nat Rev Cancer. 2018 Sep;18(9):533-548
pubmed: 30002479
J Transl Med. 2019 Sep 14;17(1):309
pubmed: 31521169
Nat Cell Biol. 2013 Jun;15(6):637-46
pubmed: 23708000
Dev Cell. 2020 Aug 10;54(3):302-316.e7
pubmed: 32574556
Curr Opin Cell Biol. 2010 Oct;22(5):697-706
pubmed: 20822891
Am J Pathol. 2005 Aug;167(2):475-88
pubmed: 16049333
Curr Protoc Cell Biol. 2016 Jun 01;71:10.9.1-10.9.34
pubmed: 27245425
Nat Commun. 2020 Oct 9;11(1):5120
pubmed: 33037194
Cancers (Basel). 2018 Sep 06;10(9):
pubmed: 30200666
Nat Commun. 2016 Aug 04;7:12237
pubmed: 27488962
Nature. 2002 Dec 19-26;420(6917):860-7
pubmed: 12490959
Am J Pathol. 2011 Mar;178(3):1221-32
pubmed: 21356373
Nat Cell Biol. 2016 May;18(5):549-60
pubmed: 27088855
Br J Cancer. 2021 Apr;124(9):1491-1502
pubmed: 33731858
Matrix Biol. 2016 Jan;49:10-24
pubmed: 26163349
J Transl Med. 2020 May 20;18(1):207
pubmed: 32434573
J Exp Clin Cancer Res. 2018 Jul 28;37(1):175
pubmed: 30055645
Nucleic Acids Res. 2020 Nov 4;48(19):e113
pubmed: 32997146
Clin Gastroenterol Hepatol. 2009 Nov;7(11 Suppl):S44-7
pubmed: 19896098
Nat Commun. 2019 Apr 23;10(1):1848
pubmed: 31015465
Proc Natl Acad Sci U S A. 2019 Sep 24;116(39):19609-19618
pubmed: 31484774
Nat Protoc. 2019 Dec;14(12):3395-3425
pubmed: 31705125
Oncotarget. 2016 Nov 15;7(46):76197-76213
pubmed: 27776346
Nat Rev Cancer. 2021 Apr;21(4):217-238
pubmed: 33589810

Auteurs

Maria Rafaeva (M)

Biotech Research and Innovation Centre, University of Copenhagen, Copenhagen, Denmark.

Adina R D Jensen (ARD)

Biotech Research and Innovation Centre, University of Copenhagen, Copenhagen, Denmark.

Edward R Horton (ER)

Biotech Research and Innovation Centre, University of Copenhagen, Copenhagen, Denmark.

Kamilla W Zornhagen (KW)

Biotech Research and Innovation Centre, University of Copenhagen, Copenhagen, Denmark.

Jan E Strøbech (JE)

Biotech Research and Innovation Centre, University of Copenhagen, Copenhagen, Denmark.

Lutz Fleischhauer (L)

Center for Applied Tissue Engineering and Regenerative Medicine-CANTER, Munich University of Applied Sciences, Munich, Germany.
Center for NanoScience - CsNS, Ludwig-Maximilians-University Munich, Munich, Germany.

Alejandro E Mayorca-Guiliani (AE)

Biotech Research and Innovation Centre, University of Copenhagen, Copenhagen, Denmark.

Sebastian R Nielsen (SR)

Biotech Research and Innovation Centre, University of Copenhagen, Copenhagen, Denmark.

Dina S Grønseth (DS)

Biotech Research and Innovation Centre, University of Copenhagen, Copenhagen, Denmark.

Filip Kuś (F)

Biotech Research and Innovation Centre, University of Copenhagen, Copenhagen, Denmark.

Erwin M Schoof (EM)

Biotech Research and Innovation Centre, University of Copenhagen, Copenhagen, Denmark.
Department of Biotechnology and Biomedicine, Technical University of Denmark, Lyngby, Denmark.
The Finsen Laboratory, Rigshospitalet, Faculty of Health Sciences, University of Copenhagen, Copenhagen, Denmark.
Novo Nordisk Foundation Centre for Stem Cell Biology, DanStem, Faculty of Health Sciences, University of Copenhagen, Copenhagen, Denmark.

Luis Arnes (L)

Biotech Research and Innovation Centre, University of Copenhagen, Copenhagen, Denmark.

Manuel Koch (M)

Center for Biochemistry, Center for Molecular Medicine Cologne (CMMC), Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
Institute for Dental Research and Oral Musculoskeletal Biology, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.

Hauke Clausen-Schaumann (H)

Center for Applied Tissue Engineering and Regenerative Medicine-CANTER, Munich University of Applied Sciences, Munich, Germany.
Center for NanoScience - CsNS, Ludwig-Maximilians-University Munich, Munich, Germany.

Valerio Izzi (V)

Faculty of Biochemistry and Molecular Medicine, University of Oulu, Oulu, Finland.
Faculty of Medicine, University of Oulu, Oulu, Finland.
Foundation for the Finnish Cancer Institute, Helsinki, Finland.

Raphael Reuten (R)

Biotech Research and Innovation Centre, University of Copenhagen, Copenhagen, Denmark.
Institute of Experimental and Clinical Pharmacology and Toxicology, Medical Faculty, University of Freiburg, Freiburg, Germany.
Department of Obstetrics and Gynecology, Medical Center, University of Freiburg, Freiburg, Germany.

Janine T Erler (JT)

Biotech Research and Innovation Centre, University of Copenhagen, Copenhagen, Denmark.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH