Breast Cancer Cell Type and Biomechanical Properties of Decellularized Mouse Organs Drives Tumor Cell Colonization
Abstract
:1. Introduction
2. Materials and Methods
2.1. Laboratory Animals and Organ Harvesting
2.2. Decellularization of the Organ Samples
2.3. Total DNA Content Analysis
2.4. Cell Culture
2.5. Recellularization of the Matrices
2.6. 3D Tumor Growth Models in Collagen Hydrogel
2.7. Histomorphological Analysis
2.8. Scanning Electron Microscopy
2.9. Macroindentation
2.10. Atomic Force Microscopy (Nanoindentation)
2.11. Rheometry
3. Results
3.1. Obtaining DCL Matrices of Murine Organs
3.2. Histological Analysis of Decellularized Matrices
3.2.1. Liver
3.2.2. Lung
3.2.3. Spleen
3.2.4. Kidney
3.2.5. Ovary
3.3. SEM Analysis of Matrices
3.4. Mechanical Properties of the Decellularized Matrices
3.4.1. Macroindentation
3.4.2. Nanoindentation
3.5. Repopulation of the Decellularized Matrices
3.5.1. Liver
3.5.2. Lungs
3.5.3. Spleen
3.5.4. Kidney
3.5.5. Ovary
3.5.6. Collagen
3.6. Correlations between Matrix Properties and Cancer Cell Growth
4. Discussion
4.1. Decellularization Protocol for Murine Organs
4.2. Biomechanical and Structural Properties of DCL Matrices of Murine Organs
4.3. The Current Ideas about Stiffness-Dependent Behavior of Cells on 2D and 3D Substrates
4.4. Behavior of Breast Cancer Cells in DCL Matrices of Murine Organs with Different Biomechanical Characteristics
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Total DNA Content | |||
---|---|---|---|
Native Tissue, µg/g Wet Tissue Weight | DCL Tissue, µg/g Wet Tissue Weight | DCL Tissue, % from Native | |
Liver | 1032 ± 11 | 0.63 ± 0.28 | 0.06 |
Lung | 1955 ± 29 | 0.90 ± 0.12 | 0.05 |
Spleen | 2337 ± 30 | 2.12 ± 0.14 | 0.09 |
Kidney | 1286 ± 45 | 1.03 ± 0.32 | 0.08 |
Ovary | 1757 ± 63 | 1.22 ± 0.26 | 0.07 |
Liver | Lung | Spleen | Kidney | Ovary | Collagen Gel | ||
---|---|---|---|---|---|---|---|
Matrix fiber density | Medium | Low | High | Medium | High | High | |
Pore area, μm2 | 133 | 240 | 78 | 90 | 152,34 | N/A | |
Local matrix stiffness (nanoindentation), kPa | 6.15 | 2.85 | 3.6 | 5.6 | 6.4 | 0.36 | |
Total matrix stiffness (macroindentation), kPa | 18 | 13.4 | 37 | 25.4 | 15.7 | N/A | |
Degree of repopulation | MDA-MB-231 | Medium | High | Medium | Medium | High | Low |
SKBR-3 | Single | Low | Low | Low | Single | Low | |
Cell morphology | MDA-MB-231 | Mes a/Ep b | Mes | Mes | Mes | Mes | Mes |
SKBR-3 | Ep | Ep | Ep | Ep | Ep | Ep |
DCL Organ | Young’s Modulus | Method | Device and Measuring Conditions | Ref. |
---|---|---|---|---|
Porcine liver | 1.25 ± 0.07 kPa | Compression test | Zwick/Roell ProLine Z005 testing machine (Zwick/Roell, Ulm, Germany) equipped with a 10 N load cell. | [62] |
Ferret liver | 1.18 kPa | Compression test | ElectroForce TestBench mechanical testing system equipped with a 1000-g load cell (Bose ElectroForce, Eden Prairie, MN, USA). | [63] |
Rat liver | 145 ± 19.68 kPa | Tensile test | Uniaxial tensile testing machine (CMT8502, Shenzhen New Sans Test Technical Company, Nanshan, Shenzhen, China). The test was performed at loading speed of 1 mm/min until the final fracture of the specimen. | [64] |
Human liver | 18,490 ± 1400 kPa | Tensile test | Instron 3367 dual column universal testing system (Instron, Glenview, IL, USA) fitted with Instron biopulse submersible pneumatic side action grips (Instron, USA) and a 50 N load cell. A gauge length of 20 mm and an extension rate of 20 mm/min were used. | [65] |
Rat lung | ~80 kPa | Tensile test | Santam tensile testing machine STM-1 (SANTAM, Tehran, Iran). The uniaxial tensile test was carried out by a crosshead speed of 2 mm/min, elongation raised to 20–40 mm, and a load cell of 6 kg at a constant elongation speed until rupture of the specimen was observed. | [66] |
Rat lung | 74.91 ± 5.78 kPa | Tensile test | Material testing machine BZ2.5/TN1S (Zwick/Roell, Ulm, Germany). Preloading of 0.015 N was imposed and the sample length was reported, then a preload of 0.003 N was set. | [67] |
Rat lung | 0.38 ± 0.07 kPa | Tensile test | Displacement actuator 300C-LR (Aurora Scientific, Aurora, ON, Canada) with a force transducer 404A (Aurora Scientific, Canada). Uniaxial tensile measurements after preconditioning with triangular stretch at 0.1 mN force. | [68] |
Porcine kidney (cortex) | 6.4 ± 2.7 kPa | Compression test | Instron 3342 Single Column Universal Testing System (Instron, USA) and Instron Model 1321 (Instron, Glenview, IL, USA) were used to perform compression tests at a rate of 0.07 mm/sec until a compression force of 45 N was reached. | [69] |
Rat Kidney | 178.9 ± 50.2 kPa | Tensile test | Tensile mechanical testing machine (Instron, Glenview, IL, USA). Samples were preconditioned by cycles of loading and unloading. Strain rate was 0.01 s−1 throughout the test. | [70] |
Rat liver | 4242.2 ± 891.6 kPa | |||
Rat Lung | 233.6 ± 98.0 kPa |
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Pospelov, A.D.; Kutova, O.M.; Efremov, Y.M.; Nekrasova, A.A.; Trushina, D.B.; Gefter, S.D.; Cherkasova, E.I.; Timofeeva, L.B.; Timashev, P.S.; Zvyagin, A.V.; et al. Breast Cancer Cell Type and Biomechanical Properties of Decellularized Mouse Organs Drives Tumor Cell Colonization. Cells 2023, 12, 2030. https://doi.org/10.3390/cells12162030
Pospelov AD, Kutova OM, Efremov YM, Nekrasova AA, Trushina DB, Gefter SD, Cherkasova EI, Timofeeva LB, Timashev PS, Zvyagin AV, et al. Breast Cancer Cell Type and Biomechanical Properties of Decellularized Mouse Organs Drives Tumor Cell Colonization. Cells. 2023; 12(16):2030. https://doi.org/10.3390/cells12162030
Chicago/Turabian StylePospelov, Anton D., Olga M. Kutova, Yuri M. Efremov, Albina A. Nekrasova, Daria B. Trushina, Sofia D. Gefter, Elena I. Cherkasova, Lidia B. Timofeeva, Peter S. Timashev, Andrei V. Zvyagin, and et al. 2023. "Breast Cancer Cell Type and Biomechanical Properties of Decellularized Mouse Organs Drives Tumor Cell Colonization" Cells 12, no. 16: 2030. https://doi.org/10.3390/cells12162030