Mechanical Regulation of Mitochondrial Dynamics and Function in a 3D-Engineered Liver Tumor Microenvironment
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
37001010
PubMed Central
PMC10170482
DOI
10.1021/acsbiomaterials.2c01518
Knihovny.cz E-zdroje
- Klíčová slova
- cancer, cell plasticity, cytoskeleton, engineered cell microenvironments, extracellular matrix, mechanical forces, mitochondria,
- MeSH
- kolagen MeSH
- lidé MeSH
- mitochondriální dynamika MeSH
- nádorové mikroprostředí * MeSH
- nádory jater * MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- kolagen MeSH
It has become evident that physical stimuli of the cellular microenvironment transmit mechanical cues regulating key cellular functions, such as proliferation, migration, and malignant transformation. Accumulating evidence suggests that tumor cells face variable mechanical stimuli that may induce metabolic rewiring of tumor cells. However, the knowledge of how tumor cells adapt metabolism to external mechanical cues is still limited. We therefore designed soft 3D collagen scaffolds mimicking a pathological mechanical environment to decipher how liver tumor cells would adapt their metabolic activity to physical stimuli of the cellular microenvironment. Here, we report that the soft 3D microenvironment upregulates the glycolysis of HepG2 and Alexander cells. Both cell lines adapt their mitochondrial activity and function under growth in the soft 3D microenvironment. Cells grown in the soft 3D microenvironment exhibit marked mitochondrial depolarization, downregulation of mitochondrially encoded cytochrome c oxidase I, and slow proliferation rate in comparison with stiff monolayer cultures. Our data reveal the coupling of liver tumor glycolysis to mechanical cues. It is proposed here that soft 3D collagen scaffolds can serve as a useful model for future studies of mechanically regulated cellular functions of various liver (potentially other tissues as well) tumor cells.
Zobrazit více v PubMed
Duval K.; Grover H.; Han L. H.; Mou Y.; Pegoraro A. F.; Fredberg J.; Chen Z. Modeling Physiological Events in 2d Vs. 3d Cell Culture. Physiology 2017, 32, 266–277. 10.1152/physiol.00036.2016. PubMed DOI PMC
Rossi G.; Manfrin A.; Lutolf M. P. Progress and Potential in Organoid Research. Nat. Rev. Genet. 2018, 19, 671–687. 10.1038/s41576-018-0051-9. PubMed DOI
Hussey G. S.; Dziki J. L.; Badylak S. F. Extracellular Matrix-Based Materials for Regenerative Medicine. Nat. Rev. Mater. 2018, 3, 159–173. 10.1038/s41578-018-0023-x. DOI
Ma X.; Yu C.; Wang P.; Xu W.; Wan X.; Lai C. S. E.; Liu J.; Koroleva-Maharajh A.; Chen S. Rapid 3d Bioprinting of Decellularized Extracellular Matrix with Regionally Varied Mechanical Properties and Biomimetic Microarchitecture. Biomaterials 2018, 185, 310–321. 10.1016/j.biomaterials.2018.09.026. PubMed DOI PMC
Yao B.; Niu Y.; Li Y.; Chen T.; Wei X.; Liu Q. High-Matrix-Stiffness Induces Promotion of Hepatocellular Carcinoma Proliferation and Suppression of Apoptosis Via Mir-3682-3p-Phlda1-Fas Pathway. J. Cancer 2020, 11, 6188–6203. 10.7150/jca.45998. PubMed DOI PMC
Zhang R.; Ma M.; Dong G.; Yao R. R.; Li J. H.; Zheng Q. D.; Dong Y. Y.; Ma H.; Gao D. M.; Cui J. F.; Ren Z. G.; Chen R. X. Increased Matrix Stiffness Promotes Tumor Progression of Residual Hepatocellular Carcinoma after Insufficient Heat Treatment. Cancer Sci. 2017, 108, 1778–1786. 10.1111/cas.13322. PubMed DOI PMC
Kang N. Mechanotransduction in Liver Diseases. Semin. Liver Dis. 2020, 40, 84–90. 10.1055/s-0039-3399502. PubMed DOI PMC
Arriazu E.; de Galarreta M. R.; Cubero F. J.; Varela-Rey M.; de Obanos M. P. P.; Leung T. M.; Lopategi A.; Benedicto A.; Abraham-Enachescu I.; Nieto N. Extracellular Matrix and Liver Disease. Antioxid. Redox Signaling 2014, 21, 1078–1097. 10.1089/ars.2013.5697. PubMed DOI PMC
Frankova S.; Lunova M.; Gottfriedova H.; Senkerikova R.; Neroldova M.; Kovac J.; Kieslichova E.; Lanska V.; Urbanek P.; Spicak J.; Jirsa M.; Sperl J. Liver Stiffness Measured by Two-Dimensional Shear-Wave Elastography Predicts Hepatic Vein Pressure Gradient at High Values in Liver Transplant Candidates with Advanced Liver Cirrhosis. PLoS One 2021, 16, e024493410.1371/journal.pone.0244934. PubMed DOI PMC
Masuzaki R.; Tateishi R.; Yoshida H.; Sato T.; Ohki T.; Goto T.; Yoshida H.; Sato S.; Sugioka Y.; Ikeda H.; Shiina S.; Kawabe T.; Omata M. Assessing Liver Tumor Stiffness by Transient Elastography. Hepatol. Int. 2007, 1, 394–397. 10.1007/s12072-007-9012-7. PubMed DOI PMC
Masuzaki R.; Tateishi R.; Yoshida H.; Goto E.; Sato T.; Ohki T.; Imamura J.; Goto T.; Kanai F.; Kato N.; Ikeda H.; Shiina S.; Kawabe T.; Omata M. Prospective Risk Assessment for Hepatocellular Carcinoma Development in Patients with Chronic Hepatitis C by Transient Elastography. Hepatology 2009, 49, 1954–1961. 10.1002/hep.22870. PubMed DOI
Castera L.; Forns X.; Alberti A. Non-Invasive Evaluation of Liver Fibrosis Using Transient Elastography. J. Hepatol. 2008, 48, 835–847. 10.1016/j.jhep.2008.02.008. PubMed DOI
Roulot D.; Czernichow S.; Le Clesiau H.; Costes J. L.; Vergnaud A. C.; Beaugrand M. Liver Stiffness Values in Apparently Healthy Subjects: Influence of Gender and Metabolic Syndrome. J. Hepatol. 2008, 48, 606–613. 10.1016/j.jhep.2007.11.020. PubMed DOI
Castera L. Liver Stiffness and Hepatocellular Carcinoma: Liaisons Dangereuses?. Hepatology 2009, 49, 1793–1794. 10.1002/hep.22981. PubMed DOI
Choong K. L.; Wong Y. H.; Yeong C. H.; Gnanasuntharam G. K.; Goh K. L.; Yoong B. K.; Pongnapang N.; Abdullah B. J. J. Elasticity Characterization of Liver Cancers Using Shear Wave Ultrasound Elastography: Comparison between Hepatocellular Carcinoma and Liver Metastasis. J. Diagn. Med. Sonogr. 2017, 33, 481–488. 10.1177/8756479317733713. DOI
Liu Q. P.; Luo Q.; Deng B.; Ju Y.; Song G. B. Stiffer Matrix Accelerates Migration of Hepatocellular Carcinoma Cells through Enhanced Aerobic Glycolysis Via the Mapk-Yap Signaling. Cancers 2020, 12, 490.10.3390/cancers12020490. PubMed DOI PMC
Schrader J.; Gordon-Walker T. T.; Aucott R. L.; van Deemter M.; Quaas A.; Walsh S.; Benten D.; Forbes S. J.; Wells R. G.; Iredale J. P. Matrix Stiffness Modulates Proliferation, Chemotherapeutic Response, and Dormancy in Hepatocellular Carcinoma Cells. Hepatology 2011, 53, 1192–1205. 10.1002/hep.24108. PubMed DOI PMC
Dong Y.; Zheng Q.; Wang Z.; Lin X.; You Y.; Wu S.; Wang Y.; Hu C.; Xie X.; Chen J.; Gao D.; Zhao Y.; Wu W.; Liu Y.; Ren Z.; Chen R.; Cui J. Higher Matrix Stiffness as an Independent Initiator Triggers Epithelial-Mesenchymal Transition and Facilitates Hcc Metastasis. J. Hematol. Oncol. 2019, 12, 112.10.1186/s13045-019-0795-5. PubMed DOI PMC
Deville S. S.; Cordes N. The Extracellular, Cellular, and Nuclear Stiffness, a Trinity in the Cancer Resistome-a Review. Front. Oncol. 2019, 9, 1376.10.3389/fonc.2019.01376. PubMed DOI PMC
Liu X. Q.; Chen X. T.; Liu Z. Z.; Gu S. S.; He L. J.; Wang K. P.; Tang R. Z. Biomimetic Matrix Stiffness Modulates Hepatocellular Carcinoma Malignant Phenotypes and Macrophage Polarization through Multiple Modes of Mechanical Feedbacks. ACS Biomater. Sci. Eng. 2020, 6, 3994–4004. 10.1021/acsbiomaterials.0c00669. PubMed DOI
Craig A. J.; von Felden J.; Garcia-Lezana T.; Sarcognato S.; Villanueva A. Tumour Evolution in Hepatocellular Carcinoma. Nat. Rev. Gastroenterol. Hepatol. 2020, 17, 139–152. 10.1038/s41575-019-0229-4. PubMed DOI
Xu S.-L.; Liu S.; Cui W.; Shi Y.; Liu Q.; Duan J.-J.; Yu S.-C.; Zhang X.; Cui Y.-H.; Kung H.-F.; Bian X.-W. Aldehyde Dehydrogenase 1a1 Circumscribes High Invasive Glioma Cells and Predicts Poor Prognosis. Am. J. Cancer Res. 2015, 5, 1471–1483. PubMed PMC
Plodinec M.; Loparic M.; Monnier C. A.; Obermann E. C.; Zanetti-Dallenbach R.; Oertle P.; Hyotyla J. T.; Aebi U.; Bentires-Alj M.; Lim R. Y. H.; Schoenenberger C. A. The Nanomechanical Signature of Breast Cancer. Nat. Nanotechnol. 2012, 7, 757–765. 10.1038/nnano.2012.167. PubMed DOI
Anlaş A. A.; Nelson C. M. Soft Microenvironments Induce Chemoresistance by Increasing Autophagy Downstream of Integrin-Linked Kinase. Cancer Res. 2020, 80, 4103–4113. 10.1158/0008-5472.CAN-19-4021. PubMed DOI PMC
Sosa M. S.; Bragado P.; Aguirre-Ghiso J. A. Mechanisms of Disseminated Cancer Cell Dormancy: An Awakening Field. Nat. Rev. Cancer 2014, 14, 611–622. 10.1038/nrc3793. PubMed DOI PMC
Giancotti F. G. Mechanisms Governing Metastatic Dormancy and Reactivation. Cell 2013, 155, 750–764. 10.1016/j.cell.2013.10.029. PubMed DOI PMC
Di Martino J. S.; Nobre A. R.; Mondal C.; Taha I.; Farias E. F.; Fertig E. J.; Naba A.; Aguirre-Ghiso J. A.; Bravo-Cordero J. J. A Tumor-Derived Type Iii Collagen-Rich Ecm Niche Regulates Tumor Cell Dormancy. Nat. Cancer 2022, 3, 90–107. 10.1038/s43018-021-00291-9. PubMed DOI PMC
Riedl A.; Schlederer M.; Pudelko K.; Stadler M.; Walter S.; Unterleuthner D.; Unger C.; Kramer N.; Hengstschlager M.; Kenner L.; Pfeiffer D.; Krupitza G.; Dolznig H. Comparison of Cancer Cells in 2d Vs 3d Culture Reveals Differences in Akt-Mtor-S6k Signaling and Drug Responses. J. Cell Sci. 2017, 130, 203–218. 10.1242/jcs.188102. PubMed DOI
Kim M. J.; Chi B. H.; Yoo J. J.; Ju Y. M.; Whang Y. M.; Chang I. H. Structure Establishment of Three-Dimensional (3d) Cell Culture Printing Model for Bladder Cancer. PLoS One 2019, 14, e022368910.1371/journal.pone.0223689. PubMed DOI PMC
Lagies S.; Schlimpert M.; Neumann S.; Wäldin A.; Kammerer B.; Borner C.; Peintner L. Cells Grown in Three-Dimensional Spheroids Mirror in Vivo Metabolic Response of Epithelial Cells. Commun. Biol. 2020, 3, 246.10.1038/s42003-020-0973-6. PubMed DOI PMC
Zhou Y.; Chen H.; Li H.; Wu Y. 3d Culture Increases Pluripotent Gene Expression in Mesenchymal Stem Cells through Relaxation of Cytoskeleton Tension. J. Cell. Mol. Med. 2017, 21, 1073–1084. 10.1111/jcmm.12946. PubMed DOI PMC
Baker B. M.; Chen C. S. Deconstructing the Third Dimension - How 3d Culture Microenvironments Alter Cellular Cues. J. Cell Sci. 2012, 125, 3015–3024. 10.1242/jcs.079509. PubMed DOI PMC
Frtús A.; Smolková B.; Uzhytchak M.; Lunova M.; Jirsa M.; Hof M.; Jurkiewicz P.; Lozinsky V. I.; Wolfová L.; Petrenko Y.; Kubinová S.; Dejneka A.; Lunov O. Hepatic Tumor Cell Morphology Plasticity under Physical Constraints in 3d Cultures Driven by Yap-Mtor Axis. Pharmaceuticals 2020, 13, 430.10.3390/ph13120430. PubMed DOI PMC
Park J. S.; Burckhardt C. J.; Lazcano R.; Solis L. M.; Isogai T.; Li L.; Chen C. S.; Gao B. N.; Minna J. D.; Bachoo R.; DeBerardinis R. J.; Danuser G. Mechanical Regulation of Glycolysis Via Cytoskeleton Architecture. Nature 2020, 578, 621–626. 10.1038/s41586-020-1998-1. PubMed DOI PMC
de Chaumont F.; Dallongeville S.; Chenouard N.; Hervé N.; Pop S.; Provoost T.; Meas-Yedid V.; Pankajakshan P.; Lecomte T.; Le Montagner Y.; Lagache T.; Dufour A.; Olivo-Marin J. C. Icy: An Open Bioimage Informatics Platform for Extended Reproducible Research. Nat. Methods 2012, 9, 690–696. 10.1038/nmeth.2075. PubMed DOI
Koopman T.; Buikema H. J.; Hollema H.; de Bock G. H.; van der Vegt B. Digital Image Analysis of Ki67 Proliferation Index in Breast Cancer Using Virtual Dual Staining on Whole Tissue Sections: Clinical Validation and Inter-Platform Agreement. Breast Cancer Res. Treat. 2018, 169, 33–42. 10.1007/s10549-018-4669-2. PubMed DOI PMC
Uzhytchak M.; Smolková B.; Lunova M.; Jirsa M.; Frtús A.; Kubinová S.; Dejneka A.; Lunov O. Iron Oxide Nanoparticle-Induced Autophagic Flux Is Regulated by Interplay between P53-Mtor Axis and Bcl-2 Signaling in Hepatic Cells. Cells 2020, 9, 1015.10.3390/cells9041015. PubMed DOI PMC
Smolková B.; Lunova M.; Lynnyk A.; Uzhytchak M.; Churpita O.; Jirsa M.; Kubinová Š.; Lunov O.; Dejneka A. Non-Thermal Plasma, as a New Physicochemical Source, to Induce Redox Imbalance and Subsequent Cell Death in Liver Cancer Cell Lines. Cell. Physiol. Biochem. 2019, 52, 119–140. 10.33594/000000009. PubMed DOI
Lunov O.; Zablotskii V.; Churpita O.; Lunova M.; Jirsa M.; Dejneka A.; Kubinova Š. Chemically Different Non-Thermal Plasmas Target Distinct Cell Death Pathways. Sci. Rep. 2017, 7, 600.10.1038/s41598-017-00689-5. PubMed DOI PMC
Lunova M.; Prokhorov A.; Jirsa M.; Hof M.; Ozl̇yńska A.; Jurkiewicz P.; Kubinová Š.; Lunov O.; Dejneka A. Nanoparticle Core Stability and Surface Functionalization Drive the Mtor Signaling Pathway in Hepatocellular Cell Lines. Sci. Rep. 2017, 7, 16049.10.1038/s41598-017-16447-6. PubMed DOI PMC
Lunova M.; Kubovciak J.; Smolkova B.; Uzhytchak M.; Michalova K.; Dejneka A.; Strnad P.; Lunov O.; Jirsa M. Expression of Interferons Lambda 3 and 4 Induces Identical Response in Human Liver Cell Lines Depending Exclusively on Canonical Signaling. Int. J. Mol. Sci. 2021, 22, 2560.10.3390/ijms22052560. PubMed DOI PMC
Schmittgen T. D.; Livak K. J. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 2008, 3, 1101–1108. 10.1038/nprot.2008.73. PubMed DOI
Lynnyk A.; Lunova M.; Jirsa M.; Egorova D.; Kulikov A.; Kubinová S.; Lunov O.; Dejneka A. Manipulating the Mitochondria Activity in Human Hepatic Cell Line Huh7 by Low-Power Laser Irradiation. Biomed. Opt. Express 2018, 9, 1283–1300. 10.1364/BOE.9.001283. PubMed DOI PMC
Lunova M.; Smolková B.; Uzhytchak M.; Janosǔková K. Ž.; Jirsa M.; Egorova D.; Kulikov A.; Kubinová Š.; Dejneka A.; Lunov O. Light-Induced Modulation of the Mitochondrial Respiratory Chain Activity: Possibilities and Limitations. Cell. Mol. Life Sci. 2020, 77, 2815–2838. 10.1007/s00018-019-03321-z. PubMed DOI PMC
Levada K.; Pshenichnikov S.; Omelyanchik A.; Rodionova V.; Nikitin A.; Savchenko A.; Schetinin I.; Zhukov D.; Abakumov M.; Majouga A.; Lunova M.; Jirsa M.; Smolková B.; Uzhytchak M.; Dejneka A.; Lunov O. Progressive Lysosomal Membrane Permeabilization Induced by Iron Oxide Nanoparticles Drives Hepatic Cell Autophagy and Apoptosis. Nano Converg. 2020, 7, 17.10.1186/s40580-020-00228-5. PubMed DOI PMC
Smolková B.; MacCulloch T.; Rockwood T. F.; Liu M. H.; Henry S. J. W.; Frtús A.; Uzhytchak M.; Lunova M.; Hof M.; Jurkiewicz P.; Dejneka A.; Stephanopoulos N.; Lunov O. Protein Corona Inhibits Endosomal Escape of Functionalized DNA Nanostructures in Living Cells. ACS Appl. Mater. Inter. 2021, 13, 46375–46390. 10.1021/acsami.1c14401. PubMed DOI PMC
Smiley S. T.; Reers M.; Mottolahartshorn C.; Lin M.; Chen A.; Smith T. W.; Steele G. D. Jr.; Chen L. B. Intracellular Heterogeneity in Mitochondrial-Membrane Potentials Revealed by a J-Aggregate-Forming Lipophilic Cation Jc-1. Proc. Natl. Acad. Sci. U. S. A. 1991, 88, 3671–3675. 10.1073/pnas.88.9.3671. PubMed DOI PMC
Zuliani T.; Duval R.; Jayat C.; Schnébert S.; André P.; Dumas M.; Ratinaud M. H. Sensitive and Reliable Jc-1 and Toto-3 Double Staining to Assess Mitochondrial Transmembrane Potential and Plasma Membrane Integrity: Interest for Cell Death Investigations. Cytom. Part A 2003, 54a, 100–108. 10.1002/cyto.a.10059. PubMed DOI
Kuznetsov A. V.; Kehrer I.; Kozlov A. V.; Haller M.; Redl H.; Hermann M.; Grimm M.; Troppmair J. Mitochondrial Ros Production under Cellular Stress: Comparison of Different Detection Methods. Anal. Bioanal. Chem. 2011, 400, 2383–2390. 10.1007/s00216-011-4764-2. PubMed DOI
Esposti M. D.; Hatzinisiriou I.; McLennan H.; Ralph S. Bcl-2 and Mitochondrial Oxygen Radicals - New Approaches with Reactive Oxygen Species-Sensitive Probes. J. Biol. Chem. 1999, 274, 29831–29837. 10.1074/jbc.274.42.29831. PubMed DOI
Reczek C. R.; Chandel N. S. The Two Faces of Reactive Oxygen Species in Cancer. Annu. Rev. Cancer Biol. 2017, 1, 79–98. 10.1146/annurev-cancerbio-041916-065808. DOI
Arganda-Carreras I.; Fernandez-Gonzalez R.; Munoz-Barrutia A.; Ortiz-De-Solorzano C. 3d Reconstruction of Histological Sections: Application to Mammary Gland Tissue. Microsc. Res. Tech. 2010, 73, 1019–1029. 10.1002/jemt.20829. PubMed DOI
Michael M.; Meiring J. C. M.; Acharya B. R.; Matthews D. R.; Verma S.; Han S. P.; Hill M. M.; Parton R. G.; Gomez G. A.; Yap A. S. Coronin 1b Reorganizes the Architecture of F-Actin Networks for Contractility at Steady-State and Apoptotic Adherens Junctions. Dev. Cell 2016, 37, 58–71. 10.1016/j.devcel.2016.03.008. PubMed DOI
Papadopoulos N. G.; Dedoussis G. V. Z.; Spanakos G.; Gritzapis A. D.; Baxevanis C. N.; Papamichail M. An Improved Fluorescence Assay for the Determination of Lymphocyte-Mediated Cytotoxicity Using Flow-Cytometry. J. Immunol. Methods 1994, 177, 101–111. 10.1016/0022-1759(94)90147-3. PubMed DOI
Yamamori T.; Ike S.; Bo T.; Sasagawa T.; Sakai Y.; Suzuki M.; Yamamoto K.; Nagane M.; Yasui H.; Inanami O. Inhibition of the Mitochondrial Fission Protein Dynamin-Related Protein 1 (Drp1) Impairs Mitochondrial Fission and Mitotic Catastrophe after X-Irradiation. Mol. Biol. Cell 2015, 26, 4607–4617. 10.1091/mbc.E15-03-0181. PubMed DOI PMC
Rambold A. S.; Kostelecky B.; Elia N.; Lippincott-Schwartz J. Tubular Network Formation Protects Mitochondria from Autophagosomal Degradation During Nutrient Starvation. Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 10190–10195. 10.1073/pnas.1107402108. PubMed DOI PMC
Anand R.; Wai T.; Baker M. J.; Kladt N.; Schauss A. C.; Rugarli E.; Langer T. The I-Aaa Protease Yme1l and Oma1 Cleave Opa1 to Balance Mitochondrial Fusion and Fission. J. Cell Biol. 2014, 204, 919–929. 10.1083/jcb.201308006. PubMed DOI PMC
Stancikova J.; Krausova M.; Kolar M.; Fafilek B.; Svec J.; Sedlacek R.; Neroldova M.; Dobes J.; Horazna M.; Janeckova L.; Vojtechova M.; Oliverius M.; Jirsa M.; Korinek V. Nkd1 Marks Intestinal and Liver Tumors Linked to Aberrant Wnt Signaling. Cell Signal. 2015, 27, 245–256. 10.1016/j.cellsig.2014.11.008. PubMed DOI
Jonkman J.; Brown C. M.; Wright G. D.; Anderson K. I.; North A. J. Tutorial: Guidance for Quantitative Confocal Microscopy. Nat. Protoc. 2020, 15, 1585–1611. 10.1038/s41596-020-0313-9. PubMed DOI
Lee J. Y.; Kitaoka M. A Beginner’s Guide to Rigor and Reproducibility in Fluorescence Imaging Experiments. Mol. Biol. Cell 2018, 29, 1519–1525. 10.1091/mbc.E17-05-0276. PubMed DOI PMC
Dell R. B.; Holleran S.; Ramakrishnan R. Sample Size Determination. ILAR J. 2002, 43, 207–213. 10.1093/ilar.43.4.207. PubMed DOI PMC
Martinez-Hernandez A.; Amenta P. S. The hepatic extracellular matrix. Virchows Arch. A: Pathol. Anat. Histopathol. 1993, 423, 77–84. 10.1007/BF01606580. PubMed DOI
Martinez-Hernandez A.; Amenta P. S. The hepatic extracellular matrix. Virchows Arch. A: Pathol. Anat. Histopathol. 1993, 423, 1–11. 10.1007/BF01606425. PubMed DOI
Lee J. T. Y.; Chow K. L. Sem Sample Preparation for Cells on 3d Scaffolds by Freeze-Drying and Hmds. Scanning 2012, 34, 12–25. 10.1002/sca.20271. PubMed DOI
Barnes C. P.; Sell S. A.; Boland E. D.; Simpson D. G.; Bowlin G. L. Nanofiber Technology: Designing the Next Generation of Tissue Engineering Scaffolds. Adv. Drug Delivery Rev. 2007, 59, 1413–1433. 10.1016/j.addr.2007.04.022. PubMed DOI
Ruoß M.; Rebholz S.; Weimer M.; Grom-Baumgarten C.; Athanasopulu K.; Kemkemer R.; Kass H.; Ehnert S.; Nussler A. K. Development of Scaffolds with Adjusted Stiffness for Mimicking Disease-Related Alterations of Liver Rigidity. J. Funct. Biomater. 2020, 11, 17.10.3390/jfb11010017. PubMed DOI PMC
Arjmand A.; Tsipouras M. G.; Tzallas A. T.; Forlano R.; Manousou P.; Giannakeas N. Quantification of Liver Fibrosis - a Comparative Study. Appl. Sci. 2020, 10, 447.10.3390/app10020447. DOI
Lee J. S.; Shin J.; Park H. M.; Kim Y. G.; Kim B. G.; Oh J. W.; Cho S. W. Liver Extracellular Matrix Providing Dual Functions of Two-Dimensional Substrate Coating and Three-Dimensional Injectable Hydrogel Platform for Liver Tissue Engineering. Biomacromolecules 2014, 15, 206–218. 10.1021/bm4015039. PubMed DOI
Ruoß M.; Vosough M.; Königsrainer A.; Nadalin S.; Wagner S.; Sajadian S.; Huber D.; Heydari Z.; Ehnert S.; Hengstler J. G.; Nussler A. K. Towards Improved Hepatocyte Cultures: Progress and Limitations. Food Chem. Toxicol. 2020, 138, 11118810.1016/j.fct.2020.111188. PubMed DOI
Ladoux B.; Mège R.-M. Mechanobiology of Collective Cell Behaviours. Nat. Rev. Mol. Cell Biol. 2017, 18, 743–757. 10.1038/nrm.2017.98. PubMed DOI
You Y.; Zheng Q.; Dong Y.; Wang Y.; Zhang L.; Xue T.; Xie X.; Hu C.; Wang Z.; Chen R.; Wang Y.; Cui J.; Ren Z. Higher Matrix Stiffness Upregulates Osteopontin Expression in Hepatocellular Carcinoma Cells Mediated by Integrin β1/GSK3β/β-Catenin Signaling Pathway. PLoS One 2015, 10, e013424310.1371/journal.pone.0134243. PubMed DOI PMC
Lunova M.; Zablotskii V.; Dempsey N. M.; Devillers T.; Jirsa M.; Syková E.; Kubinová S.; Lunov O.; Dejneka A. Modulation of Collective Cell Behaviour by Geometrical Constraints. Integr. Biol. 2016, 8, 1099–1110. 10.1039/C6IB00125D. PubMed DOI
Payne K. K.; Keim R. C.; Graham L.; Idowu M. O.; Wan W.; Wang X.-Y.; Toor A. A.; Bear H. D.; Manjili M. H. Tumor-Reactive Immune Cells Protect against Metastatic Tumor and Induce Immunoediting of Indolent but Not Quiescent Tumor Cells. J. Leukocyte Biol. 2016, 100, 625–635. 10.1189/jlb.5A1215-580R. PubMed DOI PMC
Aqbi H. F.; Coleman C.; Zarei M.; Manjili S. H.; Graham L.; Koblinski J.; Guo C.; Xie Y.; Guruli G.; Bear H. D.; Idowu M. O.; Habibi M.; Wang X.-Y.; Manjili M. H. Local and Distant Tumor Dormancy During Early Stage Breast Cancer Are Associated with the Predominance of Infiltrating T Effector Subsets. Breast Cancer Res. 2020, 22, 116.10.1186/s13058-020-01357-9. PubMed DOI PMC
Romani P.; Valcarcel-Jimenez L.; Frezza C.; Dupont S. Crosstalk between Mechanotransduction and Metabolism. Nat. Rev. Mol. Cell Biol. 2021, 22, 22–38. 10.1038/s41580-020-00306-w. PubMed DOI
Ofek G.; Wiltz D. C.; Athanasiou K. A. Contribution of the Cytoskeleton to the Compressive Properties and Recovery Behavior of Single Cells. Biophys. J. 2009, 97, 1873–1882. 10.1016/j.bpj.2009.07.050. PubMed DOI PMC
Doss B. L.; Pan M.; Gupta M.; Grenci G.; Mège R.-M.; Lim C. T.; Sheetz M. P.; Voituriez R.; Ladoux B. Cell Response to Substrate Rigidity Is Regulated by Active and Passive Cytoskeletal Stress. Proc. Natl. Acad. Sci. U. S. A. 2020, 117, 12817–12825. 10.1073/pnas.1917555117. PubMed DOI PMC
Kubitschke H.; Schnauss J.; Nnetu K. D.; Warmt E.; Stange R.; Kaes J. Actin and Microtubule Networks Contribute Differently to Cell Response for Small and Large Strains. New J. Phys. 2017, 19, 09300310.1088/1367-2630/aa7658. DOI
Discher D. E.; Janmey P.; Wang Y. L. Tissue Cells Feel and Respond to the Stiffness of Their Substrate. Science 2005, 310, 1139–1143. 10.1126/science.1116995. PubMed DOI
Burridge K. Focal Adhesions: A Personal Perspective on a Half Century of Progress. FEBS J. 2017, 284, 3355–3361. 10.1111/febs.14195. PubMed DOI PMC
Moore A. S.; Holzbaur E. L. F. Mitochondrial-Cytoskeletal Interactions: Dynamic Associations That Facilitate Network Function and Remodeling. Curr. Opin. Physiol. 2018, 3, 94–100. 10.1016/j.cophys.2018.03.003. PubMed DOI PMC
Moore A. S.; Wong Y. C.; Simpson C. L.; Holzbaur E. L. F. Dynamic Actin Cycling through Mitochondrial Subpopulations Locally Regulates the Fission-Fusion Balance within Mitochondrial Networks. Nat. Commun. 2016, 7, 12886.10.1038/ncomms12886. PubMed DOI PMC
Manor U.; Bartholomew S.; Golani G.; Christenson E.; Kozlov M.; Higgs H.; Spudich J.; Lippincott-Schwartz J. A Mitochondria-Anchored Isoform of the Actin-Nucleating Spire Protein Regulates Mitochondrial Division. eLife 2015, 4, e0882810.7554/eLife.08828. PubMed DOI PMC
Helle S. C. J.; Feng Q.; Aebersold M. J.; Hirt L.; Gruter R. R.; Vahid A.; Sirianni A.; Mostowy S.; Snedeker J. G.; Šarić A.; Idema T.; Zambelli T.; Kornmann B. Mechanical Force Induces Mitochondrial Fission. eLife 2017, 6, e3029210.7554/eLife.30292. PubMed DOI PMC
Zorov D. B.; Juhaszova M.; Sollott S. J. Mitochondrial Reactive Oxygen Species (Ros) and Ros-Induced Ros Release. Physiol. Rev. 2014, 94, 909–950. 10.1152/physrev.00026.2013. PubMed DOI PMC
Chen H.; Chomyn A.; Chan D. C. Disruption of Fusion Results in Mitochondrial Heterogeneity and Dysfunction. J. Biol. Chem. 2005, 280, 26185–26192. 10.1074/jbc.M503062200. PubMed DOI
Frank S. Dysregulation of Mitochondrial Fusion and Fission: An Emerging Concept in Neurodegeneration. Acta. Neuropathol. 2006, 111, 93–100. 10.1007/s00401-005-0002-3. PubMed DOI
Wu S.; Zhou F.; Wei Y.; Chen W. R.; Chen Q.; Xing D. Cancer Phototherapy Via Selective Photoinactivation of Respiratory Chain Oxidase to Trigger a Fatal Superoxide Anion Burst. Antioxid. Redox Signaling 2014, 20, 733–746. 10.1089/ars.2013.5229. PubMed DOI PMC
Hollville E.; Carroll R. G.; Cullen S. P.; Martin S. J. Bcl-2 Family Proteins Participate in Mitochondrial Quality Control by Regulating Parkin/Pink1-Dependent Mitophagy. Mol. Cell 2014, 55, 451–466. 10.1016/j.molcel.2014.06.001. PubMed DOI
Czabotar P. E.; Lessene G.; Strasser A.; Adams J. M. Control of Apoptosis by the Bcl-2 Protein Family: Implications for Physiology and Therapy. Nat. Rev. Mol. Cell Biol. 2014, 15, 49–63. 10.1038/nrm3722. PubMed DOI
Ni Z.; Wang B.; Dai X.; Ding W.; Yang T.; Li X.; Lewin S.; Xu L.; Lian J.; He F. Hcc Cells with High Levels of Bcl-2 Are Resistant to Abt-737 Via Activation of the Ros-Jnk-Autophagy Pathway. Free Radical Biol. Med. 2014, 70, 194–203. 10.1016/j.freeradbiomed.2014.02.012. PubMed DOI
Yang Y.; Zhang G.; Guo F.; Li Q.; Luo H.; Shu Y.; Shen Y.; Gan J.; Xu L.; Yang H. Mitochondrial Uqcc3 Modulates Hypoxia Adaptation by Orchestrating Oxphos and Glycolysis in Hepatocellular Carcinoma. Cell Rep. 2020, 33, 10834010.1016/j.celrep.2020.108340. PubMed DOI
Shen Y. C.; Ou D. L.; Hsu C.; Lin K. L.; Chang C. Y.; Lin C. Y.; Liu S. H.; Cheng A. L. Activating Oxidative Phosphorylation by a Pyruvate Dehydrogenase Kinase Inhibitor Overcomes Sorafenib Resistance of Hepatocellular Carcinoma. Brit. J. Cancer 2013, 108, 72–81. 10.1038/bjc.2012.559. PubMed DOI PMC
Jovel J.; Lin Z.; O’keefe S.; Willows S.; Wang W. W.; Zhang G. Z.; Patterson J.; Moctezuma-Velázquez C.; Kelvin D. J.; Wong G. K.-S.; Mason A. L. A Survey of Molecular Heterogeneity in Hepatocellular Carcinoma. Hepatol. Commun. 2018, 2, 945–959. 10.1002/hep4.1197. PubMed DOI PMC
Kim B.; Lee J. H.; Kim J. K.; Kim H. J.; Kim Y. B.; Lee D. The Capsule Appearance of Hepatocellular Carcinoma in Gadoxetic Acid-Enhanced Mr Imaging Correlation with Pathology and Dynamic Ct. Medicine 2018, 97, e1114210.1097/MD.0000000000011142. PubMed DOI PMC
Park S.; Jung W.-H.; Pittman M.; Chen J.; Chen Y. The Effects of Stiffness, Fluid Viscosity, and Geometry of Microenvironment in Homeostasis, Aging, and Diseases: A Brief Review. J. Biomech. Eng. 2020, 142, 100804.10.1115/1.4048110. PubMed DOI PMC
Yamada K. M.; Doyle A. D.; Lu J. Cell-3d Matrix Interactions: Recent Advances and Opportunities. Trends Cell Biol. 2022, 32, 883–895. 10.1016/j.tcb.2022.03.002. PubMed DOI PMC
Luo J.; Walker M.; Xiao Y.; Donnelly H.; Dalby M. J.; Salmeron-Sanchez M. The Influence of Nanotopography on Cell Behaviour through Interactions with the Extracellular Matrix - a Review. Bioact. Mater. 2022, 15, 145–159. 10.1016/j.bioactmat.2021.11.024. PubMed DOI PMC
Wang K.; Bruce A.; Mezan R.; Kadiyala A.; Wang L.; Dawson J.; Rojanasakul Y.; Yang Y. Nanotopographical Modulation of Cell Function through Nuclear Deformation. ACS Appl. Mater. Interfaces 2016, 8, 5082–5092. 10.1021/acsami.5b10531. PubMed DOI PMC
Park J.; Kim D. H.; Kim H. N.; Wang C. J.; Kwak M. K.; Hur E.; Suh K. Y.; An S. S.; Levchenko A. Directed Migration of Cancer Cells Guided by the Graded Texture of the Underlying Matrix. Nat. Mater. 2016, 15, 792–801. 10.1038/nmat4586. PubMed DOI PMC
Paul C. D.; Mistriotis P.; Konstantopoulos K. Cancer Cell Motility: Lessons from Migration in Confined Spaces. Nat. Rev. Cancer 2017, 17, 131–140. 10.1038/nrc.2016.123. PubMed DOI PMC
Tozluoğlu M.; Tournier A. L.; Jenkins R. P.; Hooper S.; Bates P. A.; Sahai E. Matrix Geometry Determines Optimal Cancer Cell Migration Strategy and Modulates Response to Interventions. Nat. Cell Biol. 2013, 15, 751–762. 10.1038/ncb2775. PubMed DOI
Marshall W. F. Differential Geometry Meets the Cell. Cell 2013, 154, 265–266. 10.1016/j.cell.2013.06.032. PubMed DOI
Charras G.; Sahai E. Physical Influences of the Extracellular Environment on Cell Migration. Nat. Rev. Mol. Cell Biol. 2014, 15, 813–824. 10.1038/nrm3897. PubMed DOI
Versaevel M.; Grevesse T.; Gabriele S. Spatial Coordination between Cell and Nuclear Shape within Micropatterned Endothelial Cells. Nat. Commun. 2012, 3, 671.10.1038/ncomms1668. PubMed DOI
Jain N.; Iyer K. V.; Kumar A.; Shivashankar G. V. Cell Geometric Constraints Induce Modular Gene-Expression Patterns Via Redistribution of Hdac3 Regulated by Actomyosin Contractility. Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 11349–11354. 10.1073/pnas.1300801110. PubMed DOI PMC
Bose S.; Zhang C.; Le A. Glucose Metabolism in Cancer: The Warburg Effect and Beyond. Adv. Exp. Med. Biol. 2021, 1311, 3–15. 10.1007/978-3-030-65768-0_1. PubMed DOI PMC
Kim J.; DeBerardinis R. J. Mechanisms and Implications of Metabolic Heterogeneity in Cancer. Cell Metab. 2019, 30, 434–446. 10.1016/j.cmet.2019.08.013. PubMed DOI PMC
Lee J.-H.; Liu R.; Li J.; Zhang C.; Wang Y.; Cai Q.; Qian X.; Xia Y.; Zheng Y.; Piao Y.; Chen Q.; de Groot J. F.; Jiang T.; Lu Z. Stabilization of Phosphofructokinase 1 Platelet Isoform by Akt Promotes Tumorigenesis. Nat. Commun. 2017, 8, 949.10.1038/s41467-017-00906-9. PubMed DOI PMC
Gailhouste L.; Le Grand Y.; Odin C.; Guyader D.; Turlin B.; Ezan F.; Désille Y.; Guilbert T.; Bessard A.; Frémin C.; Theret N.; Baffet G. Fibrillar Collagen Scoring by Second Harmonic Microscopy: A New Tool in the Assessment of Liver Fibrosis. J. Hepatol. 2010, 52, 398–406. 10.1016/j.jhep.2009.12.009. PubMed DOI
Bedossa P.; Paradis V. Liver Extracellular Matrix in Health and Disease. J. Pathol. 2003, 200, 504–515. 10.1002/path.1397. PubMed DOI
Geometrically constrained cytoskeletal reorganisation modulates DNA nanostructures uptake
Peptide-coated DNA nanostructures as a platform for control of lysosomal function in cells
Impact of mechanical cues on key cell functions and cell-nanoparticle interactions