Physical confinement induces malignant transformation in mammary epithelial cells.

Acinar Cells / pathology Animals Capsules Carcinogenesis / pathology Cell Transformation, Neoplastic / pathology Epithelial Cells / pathology Extracellular Matrix / metabolism Female Humans Hydrogels / chemistry Insulin / metabolism Insulin-Like Growth Factor I / metabolism Mammary Glands, Human / pathology Mice, SCID Sequence Analysis, RNA Signal Transduction Xenograft Model Antitumor Assays
Breast cancer Hydrogel Physical confinement Tumorigenesis

Journal

Biomaterials
ISSN: 1878-5905
Titre abrégé: Biomaterials
Pays: Netherlands
ID NLM: 8100316

Informations de publication

Date de publication:
10 2019
Historique:
received: 13 03 2019
revised: 16 06 2019
accepted: 25 06 2019
pubmed: 5 7 2019
medline: 24 9 2020
entrez: 5 7 2019
Statut: ppublish

Résumé

The physical microenvironment of tumor cells plays an important role in cancer initiation and progression. Here, we present evidence that confinement - a new physical parameter that is apart from matrix stiffness - can also induce malignant transformation in mammary epithelial cells. We discovered that MCF10A cells, a benign mammary cell line that forms growth-arrested polarized acini in Matrigel, transforms into cancer-like cells within the same Matrigel material following confinement in alginate shell hydrogel microcapsules. The confined cells exhibited a range of tumor-like behaviors, including uncontrolled cellular proliferation and invasion. Additionally, 4-6 weeks after transplantation into the mammary fad pads of immunocompromised mice, the confined cells formed large palpable masses that exhibited histological features similar to that of carcinomas. Taken together, our findings suggest that physical confinement represents a previously unrecognized mechanism for malignancy induction in mammary epithelial cells and also provide a new, microcapsule-based, high throughput model system for testing new breast cancer therapeutics.

Identifiants

DOI: 10.1016/j.biomaterials.2019.119307 PMID: 31271857 PMC: PMC7336132
pubmed: 31271857
pii: S0142-9612(19)30406-5
doi: 10.1016/j.biomaterials.2019.119307
pmc: PMC7336132
mid: NIHMS1604269
pii:
doi:

Substances chimiques

Capsules 0
Hydrogels 0
Insulin 0
Insulin-Like Growth Factor I 67763-96-6

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

119307

Subventions

Organisme : NIBIB NIH HHS
ID : R03 EB020910
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA221346
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA182413
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA197160
Pays : United States
Organisme : NCRR NIH HHS
ID : S10 RR025502
Pays : United States
Organisme : NICHD NIH HHS
ID : P50 HD076210
Pays : United States

Informations de copyright

Copyright © 2019 Elsevier Ltd. All rights reserved.

Références

Genes Dev. 2009 Nov 15;23(22):2563-77
pubmed: 19933147
Cancer Lett. 1994 Oct 28;86(1):1-4
pubmed: 7954344
Breast Cancer Res. 2011;13(6):227
pubmed: 22078026
Biochim Biophys Acta. 2009 May;1793(5):893-902
pubmed: 19027042
FASEB J. 2012 Oct;26(10):4045-56
pubmed: 22707566
BMC Cancer. 2012 Oct 30;12:500
pubmed: 23110523
Cell. 2009 Nov 25;139(5):891-906
pubmed: 19931152
Breast Dis. 2010;32(1-2):35-48
pubmed: 21778573
J Struct Biol. 2009 Sep;167(3):216-9
pubmed: 19481153
J Vis Exp. 2015 Feb 08;(96):
pubmed: 25742185
Proc Natl Acad Sci U S A. 2011 Feb 1;108(5):1943-8
pubmed: 21245302
Cell. 2006 Dec 1;127(5):905-15
pubmed: 17129778
Sci Rep. 2016 Mar 21;6:23353
pubmed: 26996336
Genes Dev. 2013 Oct 15;27(20):2192-206
pubmed: 24142872
PLoS One. 2015 Jul 06;10(7):e0131285
pubmed: 26147507
Acta Biomater. 2018 Sep 1;77:85-95
pubmed: 30030173
Oncogenesis. 2017 Jul 3;6(7):e352
pubmed: 28671675
Cancer. 2007 May 1;109(9):1721-8
pubmed: 17387718
Trends Biochem Sci. 2016 Mar;41(3):211-218
pubmed: 26778478
Methods. 2003 Jul;30(3):256-68
pubmed: 12798140
Biophys J. 2014 Dec 2;107(11):2528-37
pubmed: 25468332
Mod Pathol. 2010 May;23 Suppl 2:S1-7
pubmed: 20436497
Breast Cancer Res Treat. 2001 Jan;65(2):101-10
pubmed: 11261825
J Clin Invest. 2007 Nov;117(11):3155-63
pubmed: 17975657
Int J Breast Cancer. 2013;2013:872743
pubmed: 23401782
Aust N Z J Surg. 1984 Feb;54(1):11-5
pubmed: 6586161
Nat Genet. 2000 May;25(1):25-9
pubmed: 10802651
Biophys J. 2011 Aug 3;101(3):643-50
pubmed: 21806932
CA Cancer J Clin. 2017 Nov;67(6):439-448
pubmed: 28972651
Cancer Res. 2014 May 15;74(10):2655-62
pubmed: 24778418
Cell Cycle. 2018;17(19-20):2360-2373
pubmed: 30304981
J Cell Physiol. 2006 Jul;208(1):141-8
pubmed: 16607610
Am J Pathol. 1996 Jan;148(1):313-9
pubmed: 8546221
Proc Natl Acad Sci U S A. 2013 Sep 10;110(37):14843-8
pubmed: 23980147
J Mater Chem B. 2015 Jan 21;3(3):353-360
pubmed: 32262039
Chem Rev. 2017 Oct 25;117(20):12764-12850
pubmed: 28991456
N Engl J Med. 2007 Jan 18;356(3):227-36
pubmed: 17229950
PLoS One. 2017 Sep 5;12(9):e0184285
pubmed: 28873464
Cancer. 1996 Jun 1;77(11):2267-74
pubmed: 8635094
Biophys J. 2013 Jul 2;105(1):11-20
pubmed: 23823219
Nat Mater. 2014 Oct;13(10):970-8
pubmed: 24930031
Cell. 2014 Apr 24;157(3):611-23
pubmed: 24726433
Proc Natl Acad Sci U S A. 2017 Oct 10;114(41):E8618-E8627
pubmed: 28973866
Matrix Biol. 2005 Oct;24(7):489-502
pubmed: 16153814
Proc Natl Acad Sci U S A. 2013 Jan 2;110(1):163-8
pubmed: 23248267
Cancer Cell. 2005 Sep;8(3):241-54
pubmed: 16169468
Methods Mol Biol. 2009;472:343-60
pubmed: 19107441
J Cell Commun Signal. 2019 Mar;13(1):129-143
pubmed: 30515709
Phys Med Biol. 2007 Mar 21;52(6):1565-76
pubmed: 17327649
J Clin Oncol. 2008 Jul 1;26(19):3153-8
pubmed: 18490649

Auteurs

Yen-Chun Lu (YC)

Department of Biological and Environmental Engineering, Cornell University, 111 Wing Drive, Ithaca, NY, 14853, USA. Electronic address: yl2347@cornell.edu.

Tinyi Chu (T)

Baker Institute for Animal Health, College of Veterinary Medicine, Cornell University, 235 Hungerford Hill Road, Ithaca, NY, 14853, USA.

Matthew S Hall (MS)

Department of Biological and Environmental Engineering, Cornell University, 111 Wing Drive, Ithaca, NY, 14853, USA.

Dah-Jiun Fu (DJ)

Department of Biomedical Science, College of Veterinary Medicine, Cornell University, 930 Campus Road, Ithaca, NY, 14853, USA.

Quanming Shi (Q)

Bioengineering, Stanford University, 443 Via Ortega Shriram Center, Stanford, CA, 94305, USA; BioX Institute, Stanford University, 318 Campus Drive, Stanford, CA, 94305, USA.

Alan Chiu (A)

Department of Biological and Environmental Engineering, Cornell University, 111 Wing Drive, Ithaca, NY, 14853, USA.

Duo An (D)

Department of Biological and Environmental Engineering, Cornell University, 111 Wing Drive, Ithaca, NY, 14853, USA.

Long-Hai Wang (LH)

Department of Biological and Environmental Engineering, Cornell University, 111 Wing Drive, Ithaca, NY, 14853, USA.

Yehudah Pardo (Y)

Nancy E. and Peter C. Meinig School of Biomedical Engineering, Cornell University, Ithaca, NY, 14853, USA.

Teresa Southard (T)

Department of Biomedical Science, College of Veterinary Medicine, Cornell University, 930 Campus Road, Ithaca, NY, 14853, USA.

Charles G Danko (CG)

Baker Institute for Animal Health, College of Veterinary Medicine, Cornell University, 235 Hungerford Hill Road, Ithaca, NY, 14853, USA; Department of Biomedical Science, College of Veterinary Medicine, Cornell University, 930 Campus Road, Ithaca, NY, 14853, USA.

Jan Liphardt (J)

Bioengineering, Stanford University, 443 Via Ortega Shriram Center, Stanford, CA, 94305, USA; BioX Institute, Stanford University, 318 Campus Drive, Stanford, CA, 94305, USA.

Alexander Yu Nikitin (AY)

Department of Biomedical Science, College of Veterinary Medicine, Cornell University, 930 Campus Road, Ithaca, NY, 14853, USA.

Mingming Wu (M)

Department of Biological and Environmental Engineering, Cornell University, 111 Wing Drive, Ithaca, NY, 14853, USA.

Claudia Fischbach (C)

Nancy E. and Peter C. Meinig School of Biomedical Engineering, Cornell University, Ithaca, NY, 14853, USA; Kavli Institute at Cornell for Nanoscale Science, Cornell University, Ithaca, NY, 14853, USA.

Scott Coonrod (S)

Baker Institute for Animal Health, College of Veterinary Medicine, Cornell University, 235 Hungerford Hill Road, Ithaca, NY, 14853, USA; Department of Biomedical Science, College of Veterinary Medicine, Cornell University, 930 Campus Road, Ithaca, NY, 14853, USA. Electronic address: sac269@cornell.edu.

Minglin Ma (M)

Department of Biological and Environmental Engineering, Cornell University, 111 Wing Drive, Ithaca, NY, 14853, USA. Electronic address: mm826@cornell.edu.

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

Evaluation of Low-Value Services Across Major Medicare Advantage Insurers and Traditional Medicare.

Ciara Duggan, Adam L Beckman, Ishani Ganguli et al.
1.00
Humans United States Aged Cross-Sectional Studies Medicare Part C

Effectiveness of Virtual Yoga for Chronic Low Back Pain: A Randomized Clinical Trial.

Hallie Tankha, Devyn Gaskins, Amanda Shallcross et al.
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH

questionsmedicales.fr › Cellules › Cellules acineuses › Physical confinement induces malignant...
questionsmedicales.fr › Eucaryotes › Animaux › Physical confinement induces malignant...
questionsmedicales.fr › Préparations pharmaceutiques › Capsules › Physical confinement induces malignant...
questionsmedicales.fr › États, signes et symptômes pathologiques › Processus pathologiques › Processus néoplasiques › Carcinogenèse › Physical confinement induces malignant...
questionsmedicales.fr › États, signes et symptômes pathologiques › Processus pathologiques › Processus néoplasiques › Carcinogenèse › Transformation cellulaire néoplasique › Physical confinement induces malignant...
questionsmedicales.fr › Cellules › Cellules épithéliales › Physical confinement induces malignant...
questionsmedicales.fr › Cellules › Structures cellulaires › Espace extracellulaire › Matrice extracellulaire › Physical confinement induces malignant...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Physical confinement induces malignant...
questionsmedicales.fr › Préparations pharmaceutiques › Colloïdes › Gels › Hydrogels › Physical confinement induces malignant...
questionsmedicales.fr › Acides aminés, peptides et protéines › Peptides › Hormones peptidiques › Hormones pancréatiques › Insulines › Insuline › Physical confinement induces malignant...
questionsmedicales.fr › Facteurs biologiques › Protéines et peptides de signalisation intercellulaire › Somatomédines › Facteur de croissance IGF-I › Physical confinement induces malignant...
questionsmedicales.fr › Tissus › Glandes exocrines › Glandes mammaires humaines › Physical confinement induces malignant...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Souches mutantes de souris › Souris SCID › Physical confinement induces malignant...
questionsmedicales.fr › Techniques d'investigation › Techniques génétiques › Analyse de séquence › Analyse de séquence d'ARN › Physical confinement induces malignant...
questionsmedicales.fr › Phénomènes physiologiques cellulaires › Transduction du signal › Physical confinement induces malignant...
questionsmedicales.fr › Techniques d'investigation › Transplantation tumorale › Tests d'activité antitumorale sur modèle de xénogreffe › Physical confinement induces malignant...