Fibrin Stiffness Regulates Phenotypic Plasticity of Metastatic Breast Cancer Cells

The extracellular matrix (ECM)‐regulated phenotypic plasticity is crucial for metastatic progression of triple negative breast cancer (TNBC). While ECM faithful cell‐based models are available for in situ and invasive tumors, such as cell aggregate cultures in reconstituted basement membrane and in...

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Published inAdvanced healthcare materials Vol. 12; no. 31; pp. e2301137 - n/a
Main Authors Heilala, Maria, Lehtonen, Arttu, Arasalo, Ossi, Peura, Aino, Pokki, Juho, Ikkala, Olli, Nonappa, Klefström, Juha, Munne, Pauliina M.
Format Journal Article
LanguageEnglish
Published Germany Wiley Subscription Services, Inc 01.12.2023
John Wiley and Sons Inc
Subjects
3D cell culture
Actin
Basements
Biological properties
Breast cancer
Cell culture
circulating tumor cells
Cytology
Cytotoxicity
Extracellular matrix
Fibrin
fibrin hydrogels
Gene expression
Hydrogels
Immune system
Membranes
Metastases
Metastasis
Phenotypes
Phenotypic plasticity
Plastic properties
Protective coatings
Shear stress
Stiffness
triple negative breast cancer
Tubulin
Tumor cells
Tumors
fibrin hydrogels
3D cell culture
phenotypic plasticity
triple negative breast cancer
circulating tumor cells
metastasis
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Abstract The extracellular matrix (ECM)‐regulated phenotypic plasticity is crucial for metastatic progression of triple negative breast cancer (TNBC). While ECM faithful cell‐based models are available for in situ and invasive tumors, such as cell aggregate cultures in reconstituted basement membrane and in collagenous gels, there are no ECM faithful models for metastatic circulating tumor cells (CTCs). Such models are essential to represent the stage of metastasis where clinical relevance and therapeutic opportunities are significant. Here, CTC‐like DU4475 TNBC cells are cultured in mechanically tunable 3D fibrin hydrogels. This is motivated, as in circulation fibrin aids CTC survival by forming a protective coating reducing shear stress and immune cell‐mediated cytotoxicity and promotes several stages of late metastatic processes at the interface between circulation and tissue. This work shows that fibrin hydrogels support DU4475 cell growth, resulting in spheroid formation. Furthermore, increasing fibrin stiffness from 57 to 175 Pa leads to highly motile, actin and tubulin containing cellular protrusions, which are associated with specific cell morphology and gene expression patterns that markedly differ from basement membrane or suspension cultures. Thus, mechanically tunable fibrin gels reveal specific matrix‐based regulation of TNBC cell phenotype and offer scaffolds for CTC‐like cells with better mechano‐biological properties than liquid. 3D fibrin gels are used to model the phenotypic plasticity of circulating tumor cells (CTCs) ‐like breast cancer cells. Compared with standard 3D culture conditions, cells in fibrin gels show unique gene expression signatures. The cell phenotype is subject to regulation by matrix mechanical properties, with stiff fibrin inducing dynamic cell protrusions that resemble prometastatic structures.
AbstractList The extracellular matrix (ECM)-regulated phenotypic plasticity is crucial for metastatic progression of triple negative breast cancer (TNBC). While ECM faithful cell-based models are available for in situ and invasive tumors, such as cell aggregate cultures in reconstituted basement membrane and in collagenous gels, there are no ECM faithful models for metastatic circulating tumor cells (CTCs). Such models are essential to represent the stage of metastasis where clinical relevance and therapeutic opportunities are significant. Here, CTC-like DU4475 TNBC cells are cultured in mechanically tunable 3D fibrin hydrogels. This is motivated, as in circulation fibrin aids CTC survival by forming a protective coating reducing shear stress and immune cell-mediated cytotoxicity and promotes several stages of late metastatic processes at the interface between circulation and tissue. This work shows that fibrin hydrogels support DU4475 cell growth, resulting in spheroid formation. Furthermore, increasing fibrin stiffness from 57 to 175 Pa leads to highly motile, actin and tubulin containing cellular protrusions, which are associated with specific cell morphology and gene expression patterns that markedly differ from basement membrane or suspension cultures. Thus, mechanically tunable fibrin gels reveal specific matrix-based regulation of TNBC cell phenotype and offer scaffolds for CTC-like cells with better mechano-biological properties than liquid.
The extracellular matrix (ECM)‐regulated phenotypic plasticity is crucial for metastatic progression of triple negative breast cancer (TNBC). While ECM faithful cell‐based models are available for in situ and invasive tumors, such as cell aggregate cultures in reconstituted basement membrane and in collagenous gels, there are no ECM faithful models for metastatic circulating tumor cells (CTCs). Such models are essential to represent the stage of metastasis where clinical relevance and therapeutic opportunities are significant. Here, CTC‐like DU4475 TNBC cells are cultured in mechanically tunable 3D fibrin hydrogels. This is motivated, as in circulation fibrin aids CTC survival by forming a protective coating reducing shear stress and immune cell‐mediated cytotoxicity and promotes several stages of late metastatic processes at the interface between circulation and tissue. This work shows that fibrin hydrogels support DU4475 cell growth, resulting in spheroid formation. Furthermore, increasing fibrin stiffness from 57 to 175 Pa leads to highly motile, actin and tubulin containing cellular protrusions, which are associated with specific cell morphology and gene expression patterns that markedly differ from basement membrane or suspension cultures. Thus, mechanically tunable fibrin gels reveal specific matrix‐based regulation of TNBC cell phenotype and offer scaffolds for CTC‐like cells with better mechano‐biological properties than liquid.
The extracellular matrix (ECM)‐regulated phenotypic plasticity is crucial for metastatic progression of triple negative breast cancer (TNBC). While ECM faithful cell‐based models are available for in situ and invasive tumors, such as cell aggregate cultures in reconstituted basement membrane and in collagenous gels, there are no ECM faithful models for metastatic circulating tumor cells (CTCs). Such models are essential to represent the stage of metastasis where clinical relevance and therapeutic opportunities are significant. Here, CTC‐like DU4475 TNBC cells are cultured in mechanically tunable 3D fibrin hydrogels. This is motivated, as in circulation fibrin aids CTC survival by forming a protective coating reducing shear stress and immune cell‐mediated cytotoxicity and promotes several stages of late metastatic processes at the interface between circulation and tissue. This work shows that fibrin hydrogels support DU4475 cell growth, resulting in spheroid formation. Furthermore, increasing fibrin stiffness from 57 to 175 Pa leads to highly motile, actin and tubulin containing cellular protrusions, which are associated with specific cell morphology and gene expression patterns that markedly differ from basement membrane or suspension cultures. Thus, mechanically tunable fibrin gels reveal specific matrix‐based regulation of TNBC cell phenotype and offer scaffolds for CTC‐like cells with better mechano‐biological properties than liquid. 3D fibrin gels are used to model the phenotypic plasticity of circulating tumor cells (CTCs) ‐like breast cancer cells. Compared with standard 3D culture conditions, cells in fibrin gels show unique gene expression signatures. The cell phenotype is subject to regulation by matrix mechanical properties, with stiff fibrin inducing dynamic cell protrusions that resemble prometastatic structures.
The extracellular matrix (ECM)-regulated phenotypic plasticity is crucial for metastatic progression of triple negative breast cancer (TNBC). While ECM faithful cell-based models are available for in situ and invasive tumors, such as cell aggregate cultures in reconstituted basement membrane and in collagenous gels, there are no ECM faithful models for metastatic circulating tumor cells (CTCs). Such models are essential to represent the stage of metastasis where clinical relevance and therapeutic opportunities are significant. Here, CTC-like DU4475 TNBC cells are cultured in mechanically tunable 3D fibrin hydrogels. This is motivated, as in circulation fibrin aids CTC survival by forming a protective coating reducing shear stress and immune cell-mediated cytotoxicity and promotes several stages of late metastatic processes at the interface between circulation and tissue. This work shows that fibrin hydrogels support DU4475 cell growth, resulting in spheroid formation. Furthermore, increasing fibrin stiffness from 57 to 175 Pa leads to highly motile, actin and tubulin containing cellular protrusions, which are associated with specific cell morphology and gene expression patterns that markedly differ from basement membrane or suspension cultures. Thus, mechanically tunable fibrin gels reveal specific matrix-based regulation of TNBC cell phenotype and offer scaffolds for CTC-like cells with better mechano-biological properties than liquid.The extracellular matrix (ECM)-regulated phenotypic plasticity is crucial for metastatic progression of triple negative breast cancer (TNBC). While ECM faithful cell-based models are available for in situ and invasive tumors, such as cell aggregate cultures in reconstituted basement membrane and in collagenous gels, there are no ECM faithful models for metastatic circulating tumor cells (CTCs). Such models are essential to represent the stage of metastasis where clinical relevance and therapeutic opportunities are significant. Here, CTC-like DU4475 TNBC cells are cultured in mechanically tunable 3D fibrin hydrogels. This is motivated, as in circulation fibrin aids CTC survival by forming a protective coating reducing shear stress and immune cell-mediated cytotoxicity and promotes several stages of late metastatic processes at the interface between circulation and tissue. This work shows that fibrin hydrogels support DU4475 cell growth, resulting in spheroid formation. Furthermore, increasing fibrin stiffness from 57 to 175 Pa leads to highly motile, actin and tubulin containing cellular protrusions, which are associated with specific cell morphology and gene expression patterns that markedly differ from basement membrane or suspension cultures. Thus, mechanically tunable fibrin gels reveal specific matrix-based regulation of TNBC cell phenotype and offer scaffolds for CTC-like cells with better mechano-biological properties than liquid.
Author Pokki, Juho
Ikkala, Olli
Nonappa
Heilala, Maria
Arasalo, Ossi
Peura, Aino
Klefström, Juha
Lehtonen, Arttu
Munne, Pauliina M.
AuthorAffiliation 1 Department of Applied Physics Aalto University P.O. Box 15100 Aalto Espoo FI‐00076 Finland
2 Department of Electrical Engineering and Automation Aalto University P.O. Box 12200 Aalto Espoo FI‐00076 Finland
4 Faculty of Engineering and Natural Sciences Tampere University P.O. Box 541 Tampere FI‐33720 Finland
3 Finnish Cancer Institute and FICAN South Helsinki University Hospital & Cancer Cell Circuitry Laboratory Translational Cancer Medicine Medical Faculty University of Helsinki P.O. Box 63 (Haartmaninkatu 8) Helsinki 00014 Finland
AuthorAffiliation_xml – name: 2 Department of Electrical Engineering and Automation Aalto University P.O. Box 12200 Aalto Espoo FI‐00076 Finland
– name: 1 Department of Applied Physics Aalto University P.O. Box 15100 Aalto Espoo FI‐00076 Finland
– name: 3 Finnish Cancer Institute and FICAN South Helsinki University Hospital & Cancer Cell Circuitry Laboratory Translational Cancer Medicine Medical Faculty University of Helsinki P.O. Box 63 (Haartmaninkatu 8) Helsinki 00014 Finland
– name: 4 Faculty of Engineering and Natural Sciences Tampere University P.O. Box 541 Tampere FI‐33720 Finland
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Keywords fibrin hydrogels
3D cell culture
phenotypic plasticity
triple negative breast cancer
circulating tumor cells
metastasis
Language English
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2016; 16
2011; 6
2016; 11
2011; 9
2012; 197
2021; 56
2021; 55
2020; 31
2020; 30
2013; 339
2022; 12
2020; 23
2020; 22
2005; 15
2009; 107
2012; 43
2011; 145
1998; 140
2018; 15
2018; 14
2006; 103
2022; 19
2017; 7
2004; 64
2015; 36
2021; 23
2012; 321
2021; 125
2008; 9
2007; 28
2020; 5
2014; 4
2023; 25
2014; 2
2017; 37
2015; 40
2013; 319
2018; 137
2000; 61
1983; 62
2003; 5
2020; 133
2014; 9
2021; 109
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2006; 12
2006; 16
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2014; 111
2009; 136
1991; 5
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2011; 105
2008; 181
2021; 16
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2013; 33
2017; 15
2013; 32
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1970; 45
2009; 9
2013; 493
2009; 6
2020; 232
2009; 4
2009; 425
2014; 102
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Snippet The extracellular matrix (ECM)‐regulated phenotypic plasticity is crucial for metastatic progression of triple negative breast cancer (TNBC). While ECM...
The extracellular matrix (ECM)-regulated phenotypic plasticity is crucial for metastatic progression of triple negative breast cancer (TNBC). While ECM...
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StartPage e2301137
SubjectTerms 3D cell culture
Actin
Basements
Biological properties
Breast cancer
Cell culture
circulating tumor cells
Cytology
Cytotoxicity
Extracellular matrix
Fibrin
fibrin hydrogels
Gene expression
Hydrogels
Immune system
Membranes
Metastases
Metastasis
Phenotypes
Phenotypic plasticity
Plastic properties
Protective coatings
Shear stress
Stiffness
triple negative breast cancer
Tubulin
Tumor cells
Tumors
Title Fibrin Stiffness Regulates Phenotypic Plasticity of Metastatic Breast Cancer Cells
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fadhm.202301137
https://www.ncbi.nlm.nih.gov/pubmed/37671812
https://www.proquest.com/docview/2901757221
https://www.proquest.com/docview/2861645224
https://pubmed.ncbi.nlm.nih.gov/PMC11469292
Volume 12
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