Natural Killer Cell Mechanosensing in Solid Tumors
Abstract
:1. Introduction
2. Natural Killer Cells
3. NK Cell Mechanosensors
3.1. Integrins
3.2. Mechanically Gated Ion Channels
3.3. NK Immunological Synapse (NKIS) Formation and Cytoskeletal Rearrangement
3.4. Mechanically Induced Nuclear Deformation
4. Physical Traits of Solid Tumors
4.1. Elevated Solid Stress
4.2. Elevated Fluid Stress
4.2.1. Interstitial Fluid Pressure (IFP)
4.2.2. Vascular Shear Stress
4.3. Increased Stiffness and Altered Mechanical Properties
4.3.1. Metastatic Cancer Cell Softening
4.3.2. Altered NK Cell Stiffness
4.4. Altered Tissue Microarchitecture
5. Advanced Engineering Approaches
5.1. Microfabrication Techniques
5.1.1. Microfluidics
5.1.2. Micropatterning
5.2. 3D Tissue Engineering
5.2.1. Hydrogels
5.2.2. Microspheres
5.3. Nanoscale Materials
5.3.1. Nanowires
5.3.2. Nanoparticles
5.3.3. Backpacks
6. Conclusions and Outlook
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Cancer Statistics, 2023—Siegel—2023—CA: A Cancer Journal for Clinicians—Wiley Online Library. Available online: https://acsjournals.onlinelibrary.wiley.com/doi/10.3322/caac.21763 (accessed on 15 February 2024).
- June, C.H.; O’Connor, R.S.; Kawalekar, O.U.; Ghassemi, S.; Milone, M.C. CAR T Cell Immunotherapy for Human Cancer. Science 2018, 359, 1361–1365. [Google Scholar] [CrossRef] [PubMed]
- Porter, D.L.; Levine, B.L.; Kalos, M.; Bagg, A.; June, C.H. Chimeric Antigen Receptor–Modified T Cells in Chronic Lymphoid Leukemia. N. Engl. J. Med. 2011, 365, 725–733. [Google Scholar] [CrossRef] [PubMed]
- Lee, D.W.; Santomasso, B.D.; Locke, F.L.; Ghobadi, A.; Turtle, C.J.; Brudno, J.N.; Maus, M.V.; Park, J.H.; Mead, E.; Pavletic, S.; et al. ASTCT Consensus Grading for Cytokine Release Syndrome and Neurologic Toxicity Associated with Immune Effector Cells. Biol. Blood Marrow Transplant. 2019, 25, 625–638. [Google Scholar] [CrossRef] [PubMed]
- Rafiq, S.; Hackett, C.S.; Brentjens, R.J. Engineering Strategies to Overcome the Current Roadblocks in CAR T Cell Therapy. Nat. Rev. Clin. Oncol. 2020, 17, 147–167. [Google Scholar] [CrossRef] [PubMed]
- Teachey, D.T.; Bishop, M.R.; Maloney, D.G.; Grupp, S.A. Toxicity Management after Chimeric Antigen Receptor T Cell Therapy: One Size Does Not Fit “ALL”. Nat. Rev. Clin. Oncol. 2018, 15, 218. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, R.; Wu, H.; Pounds, S.; Inaba, H.; Ribeiro, R.C.; Cullins, D.; Rooney, B.; Bell, T.; Lacayo, N.J.; Heym, K.; et al. A Phase II Clinical Trial of Adoptive Transfer of Haploidentical Natural Killer Cells for Consolidation Therapy of Pediatric Acute Myeloid Leukemia. J. Immunother. Cancer 2019, 7, 81. [Google Scholar] [CrossRef] [PubMed]
- Ciurea, S.O.; Schafer, J.R.; Bassett, R.; Denman, C.J.; Cao, K.; Willis, D.; Rondon, G.; Chen, J.; Soebbing, D.; Kaur, I.; et al. Phase 1 Clinical Trial Using mbIL21 Ex Vivo-Expanded Donor-Derived NK Cells after Haploidentical Transplantation. Blood 2017, 130, 1857–1868. [Google Scholar] [CrossRef] [PubMed]
- Williams, S.M.; Sumstad, D.; Kadidlo, D.; Curtsinger, J.; Luo, X.; Miller, J.S.; McKenna, D.H., Jr. Clinical-Scale Production of cGMP Compliant CD3/CD19 Cell-Depleted NK Cells in the Evolution of NK Cell Immunotherapy at a Single Institution. Transfusion 2018, 58, 1458–1467. [Google Scholar] [CrossRef] [PubMed]
- Tang, X.; Yang, L.; Li, Z.; Nalin, A.P.; Dai, H.; Xu, T.; Yin, J.; You, F.; Zhu, M.; Shen, W.; et al. First-in-Man Clinical Trial of CAR NK-92 Cells: Safety Test of CD33-CAR NK-92 Cells in Patients with Relapsed and Refractory Acute Myeloid Leukemia. Am. J. Cancer Res. 2018, 8, 1083–1089. [Google Scholar] [PubMed]
- Li, Y.; Sun, R. Tumor Immunotherapy: New Aspects of Natural Killer Cells. Chin. J. Cancer Res. 2018, 30, 173–196. [Google Scholar] [CrossRef] [PubMed]
- Tonn, T.; Schwabe, D.; Klingemann, H.G.; Becker, S.; Esser, R.; Koehl, U.; Suttorp, M.; Seifried, E.; Ottmann, O.G.; Bug, G. Treatment of Patients with Advanced Cancer with the Natural Killer Cell Line NK-92. Cytotherapy 2013, 15, 1563–1570. [Google Scholar] [CrossRef] [PubMed]
- Tong, A.A.; Hashem, H.; Eid, S.; Allen, F.; Kingsley, D.; Huang, A.Y. Adoptive Natural Killer Cell Therapy Is Effective in Reducing Pulmonary Metastasis of Ewing Sarcoma. Oncoimmunology 2017, 6, e1303586. [Google Scholar] [CrossRef] [PubMed]
- Menon, A.G.; Fleuren, G.J.; Alphenaar, E.A.; Jonges, L.E.; Janssen van Rhijn, C.M.; Ensink, N.G.; Putter, H.; Tollenaar, R.A.E.M.; van de Velde, C.J.H.; Kuppen, P.J.K. A Basal Membrane-like Structure Surrounding Tumour Nodules May Prevent Intraepithelial Leucocyte Infiltration in Colorectal Cancer. Cancer Immunol. Immunother. 2003, 52, 121–126. [Google Scholar] [CrossRef] [PubMed]
- Burke, S.; Lakshmikanth, T.; Colucci, F.; Carbone, E. New Views on Natural Killer Cell-Based Immunotherapy for Melanoma Treatment. Trends Immunol. 2010, 31, 339–345. [Google Scholar] [CrossRef] [PubMed]
- Villegas, F.R.; Coca, S.; Villarrubia, V.G.; Jiménez, R.; Chillón, M.J.; Jareño, J.; Zuil, M.; Callol, L. Prognostic Significance of Tumor Infiltrating Natural Killer Cells Subset CD57 in Patients with Squamous Cell Lung Cancer. Lung Cancer 2002, 35, 23–28. [Google Scholar] [CrossRef] [PubMed]
- His, W. Unsere Korperform Und Das Physiologische Problem Ihrer Entstehung; F.C.W. Vogel: Leipzig, Germany, 1874. [Google Scholar]
- Vivier, E.; Tomasello, E.; Baratin, M.; Walzer, T.; Ugolini, S. Functions of Natural Killer Cells. Nat. Immunol. 2008, 9, 503–510. [Google Scholar] [CrossRef] [PubMed]
- Cooper, M.A.; Fehniger, T.A.; Caligiuri, M.A. The Biology of Human Natural Killer-Cell Subsets. Trends Immunol. 2001, 22, 633–640. [Google Scholar] [CrossRef] [PubMed]
- Maki, G.; Klingemann, H.-G.; Martinson, J.A.; Tam, Y.K. Factors Regulating the Cytotoxic Activity of the Human Natural Killer Cell Line, NK-92. J. Hematotherapy Stem Cell Res. 2001, 10, 369–383. [Google Scholar] [CrossRef] [PubMed]
- Caligiuri, M.A. Human Natural Killer Cells. Blood 2008, 112, 461–469. [Google Scholar] [CrossRef] [PubMed]
- Paul, S.; Lal, G. The Molecular Mechanism of Natural Killer Cells Function and Its Importance in Cancer Immunotherapy. Front. Immunol. 2017, 8, 290728. [Google Scholar] [CrossRef] [PubMed]
- Vivier, E.; Ugolini, S.; Blaise, D.; Chabannon, C.; Brossay, L. Targeting Natural Killer Cells and Natural Killer T Cells in Cancer. Nat. Rev. Immunol. 2012, 12, 239–252. [Google Scholar] [CrossRef] [PubMed]
- Zhou, H.; Wang, M.; Zhang, Y.; Su, Q.; Xie, Z.; Chen, X.; Yan, R.; Li, P.; Li, T.; Qin, X.; et al. Functions and Clinical Significance of Mechanical Tumor Microenvironment: Cancer Cell Sensing, Mechanobiology and Metastasis. Cancer Commun. 2022, 42, 374–400. [Google Scholar] [CrossRef] [PubMed]
- Shannon, M.J.; Mace, E.M. Natural Killer Cell Integrins and Their Functions in Tissue Residency. Front. Immunol. 2021, 12, 647358. [Google Scholar] [CrossRef] [PubMed]
- Orsini, E.M.; Perelas, A.; Southern, B.D.; Grove, L.M.; Olman, M.A.; Scheraga, R.G. Stretching the Function of Innate Immune Cells. Front. Immunol. 2021, 12, 767319. [Google Scholar] [CrossRef] [PubMed]
- Santoni, G.; Amantini, C.; Santoni, M.; Maggi, F.; Morelli, M.B.; Santoni, A. Mechanosensation and Mechanotransduction in Natural Killer Cells. Front. Immunol. 2021, 12, 688918. [Google Scholar] [CrossRef] [PubMed]
- Wong, D.C.P.; Ding, J.L. The Mechanobiology of NK Cells—“Forcing NK to Sense” Target Cells. Biochim. Biophys. Acta Rev. Cancer 2023, 1878, 188860. [Google Scholar] [CrossRef] [PubMed]
- Pang, X.; He, X.; Qiu, Z.; Zhang, H.; Xie, R.; Liu, Z.; Gu, Y.; Zhao, N.; Xiang, Q.; Cui, Y. Targeting Integrin Pathways: Mechanisms and Advances in Therapy. Signal Transduct. Target. Ther. 2023, 8, 1. [Google Scholar] [CrossRef] [PubMed]
- Hynes, R.O. Integrins: Bidirectional, Allosteric Signaling Machines. Cell 2002, 110, 673–687. [Google Scholar] [CrossRef] [PubMed]
- Butcher, E.C. Leukocyte-Endothelial Cell Recognition: Three (or More) Steps to Specificity and Diversity. Cell 1991, 67, 1033–1036. [Google Scholar] [CrossRef] [PubMed]
- Springer, T.A. Traffic Signals for Lymphocyte Recirculation and Leukocyte Emigration: The Multistep Paradigm. Cell 1994, 76, 301–314. [Google Scholar] [CrossRef] [PubMed]
- Dustin, M.L. Integrins and Their Role in Immune Cell Adhesion. Cell 2019, 177, 499–501. [Google Scholar] [CrossRef] [PubMed]
- Kechagia, J.Z.; Ivaska, J.; Roca-Cusachs, P. Integrins as Biomechanical Sensors of the Microenvironment. Nat. Rev. Mol. Cell Biol. 2019, 20, 457–473. [Google Scholar] [CrossRef] [PubMed]
- Austen, K.; Ringer, P.; Mehlich, A.; Chrostek-Grashoff, A.; Kluger, C.; Klingner, C.; Sabass, B.; Zent, R.; Rief, M.; Grashoff, C. Extracellular Rigidity Sensing by Talin Isoform-Specific Mechanical Linkages. Nat. Cell Biol. 2015, 17, 1597–1606. [Google Scholar] [CrossRef] [PubMed]
- Hirata, H.; Sokabe, M.; Lim, C.T. Molecular Mechanisms Underlying the Force-Dependent Regulation of Actin-to-ECM Linkage at the Focal Adhesions. Prog. Mol. Biol. Transl. Sci. 2014, 126, 135–154. [Google Scholar] [CrossRef] [PubMed]
- Salas, A.; Shimaoka, M.; Chen, S.; Carman, C.V.; Springer, T. Transition From Rolling to Firm Adhesion Is Regulated by the Conformation of the I Domain of the Integrin Lymphocyte Function-Associated Antigen-1. J. Biol. Chem. 2002, 277, 50255–50262. [Google Scholar] [CrossRef] [PubMed]
- Alon, R.; Dustin, M.L. Force as a Facilitator of Integrin Conformational Changes during Leukocyte Arrest on Blood Vessels and Antigen-Presenting Cells. Immunity 2007, 26, 17–27. [Google Scholar] [CrossRef] [PubMed]
- Liu, F.; Wu, Q.; Dong, Z.; Liu, K. Integrins in Cancer: Emerging Mechanisms and Therapeutic Opportunities. Pharmacol. Ther. 2023, 247, 108458. [Google Scholar] [CrossRef] [PubMed]
- Mierke, C.T.; Frey, B.; Fellner, M.; Herrmann, M.; Fabry, B. Integrin A5β1 Facilitates Cancer Cell Invasion through Enhanced Contractile Forces. J. Cell Sci. 2011, 124, 369–383. [Google Scholar] [CrossRef] [PubMed]
- Roman, J.; Ritzenthaler, J.D.; Roser-Page, S.; Sun, X.; Han, S. A5β1-Integrin Expression Is Essential for Tumor Progression in Experimental Lung Cancer. Am. J. Respir. Cell Mol. Biol. 2010, 43, 684–691. [Google Scholar] [CrossRef] [PubMed]
- Renner, G.; Janouskova, H.; Noulet, F.; Koenig, V.; Guerin, E.; Bär, S.; Nuesch, J.; Rechenmacher, F.; Neubauer, S.; Kessler, H.; et al. Integrin A5β1 and P53 Convergent Pathways in the Control of Anti-Apoptotic Proteins PEA-15 and Survivin in High-Grade Glioma. Cell Death Differ. 2016, 23, 640–653. [Google Scholar] [CrossRef] [PubMed]
- Kuonen, F.; Surbeck, I.; Sarin, K.Y.; Dontenwill, M.; Rüegg, C.; Gilliet, M.; Oro, A.E.; Gaide, O. TGFβ, Fibronectin and Integrin A5β1 Promote Invasion in Basal Cell Carcinoma. J. Investig. Dermatol. 2018, 138, 2432–2442. [Google Scholar] [CrossRef] [PubMed]
- Krishn, S.R.; Singh, A.; Bowler, N.; Duffy, A.N.; Friedman, A.; Fedele, C.; Kurtoglu, S.; Tripathi, S.K.; Wang, K.; Hawkins, A.; et al. Prostate Cancer Sheds the Avβ3 Integrin in Vivo through Exosomes. Matrix Biol. 2019, 77, 41–57. [Google Scholar] [CrossRef] [PubMed]
- Luo, J.; Yao, J.-F.; Deng, X.-F.; Zheng, X.-D.; Jia, M.; Wang, Y.-Q.; Huang, Y.; Zhu, J.-H. 14, 15-EET Induces Breast Cancer Cell EMT and Cisplatin Resistance by up-Regulating Integrin Avβ3 and Activating FAK/PI3K/AKT Signaling. J. Exp. Clin. Cancer Res. 2018, 37, 23. [Google Scholar] [CrossRef] [PubMed]
- Vannini, A.; Leoni, V.; Barboni, C.; Sanapo, M.; Zaghini, A.; Malatesta, P.; Campadelli-Fiume, G.; Gianni, T. Avβ3-Integrin Regulates PD-L1 Expression and Is Involved in Cancer Immune Evasion. Proc. Natl. Acad. Sci. USA 2019, 116, 20141–20150. [Google Scholar] [CrossRef] [PubMed]
- Böger, C.; Kalthoff, H.; Goodman, S.L.; Behrens, H.-M.; Röcken, C. Integrins and Their Ligands Are Expressed in Non-Small Cell Lung Cancer but Not Correlated with Parameters of Disease Progression. Virchows Arch. 2014, 464, 69–78. [Google Scholar] [CrossRef]
- Grzesiak, J.J.; Bouvet, M. Determination of the Ligand-Binding Specificities of the A2β1 and A1β1 Integrins in a Novel 3-Dimensional In Vitro Model of Pancreatic Cancer. Pancreas 2007, 34, 220. [Google Scholar] [CrossRef] [PubMed]
- Zhu, Z.; Mesci, P.; Bernatchez, J.A.; Gimple, R.C.; Wang, X.; Schafer, S.T.; Wettersten, H.I.; Beck, S.; Clark, A.E.; Wu, Q.; et al. Zika Virus Targets Glioblastoma Stem Cells through a SOX2-Integrin Avβ5 Axis. Cell Stem Cell 2020, 26, 187–204. [Google Scholar] [CrossRef] [PubMed]
- Vicente-Manzanares, M.; Sánchez-Madrid, F. Targeting the Integrin Interactome in Human Disease. Curr. Opin. Cell Biol. 2018, 55, 17–23. [Google Scholar] [CrossRef] [PubMed]
- Gismondi, A.; Morrone, S.; Humphries, M.J.; Piccoli, M.; Frati, L.; Santoni, A. Human Natural Killer Cells Express VLA-4 and VLA-5, Which Mediate Their Adhesion to Fibronectin. J. Immunol. 1991, 146, 384–392. [Google Scholar] [CrossRef] [PubMed]
- Virtanen, I.; Ylänne, J.; Vartio, T.; Saksela, E. Human Natural Killer Cells Express Different Integrins and Spread on Fibronectin. Scand. J. Immunol. 1991, 33, 421–428. [Google Scholar] [CrossRef] [PubMed]
- Macías, C.; Ballester, J.M.; Hernández, P. Expression and Functional Activity of the Very Late Activation Antigen-4 Molecule on Human Natural Killer Cells in Different States of Activation. Immunology 2000, 100, 77–83. [Google Scholar] [CrossRef] [PubMed]
- Davis, D.M.; Chiu, I.; Fassett, M.; Cohen, G.B.; Mandelboim, O.; Strominger, J.L. The Human Natural Killer Cell Immune Synapse. Proc. Natl. Acad. Sci. USA 1999, 96, 15062–15067. [Google Scholar] [CrossRef] [PubMed]
- Paganin, C.; Matteucci, C.; Cenzuales, S.; Mantovani, A.; Allavena, P. IL-4 Inhibits Binding and Cytotoxicity of NK Cells to Vascular Endothelium. Cytokine 1994, 6, 135–140. [Google Scholar] [CrossRef] [PubMed]
- Fogler, W.E.; Volker, K.; McCormick, K.L.; Watanabe, M.; Ortaldo, J.R.; Wiltrout, R.H. NK Cell Infiltration into Lung, Liver, and Subcutaneous B16 Melanoma Is Mediated by VCAM-1/VLA-4 Interaction. J. Immunol. 1996, 156, 4707–4714. [Google Scholar] [CrossRef] [PubMed]
- Hornung, A.; Sbarrato, T.; Garcia-Seyda, N.; Aoun, L.; Luo, X.; Biarnes-Pelicot, M.; Theodoly, O.; Valignat, M.-P. A Bistable Mechanism Mediated by Integrins Controls Mechanotaxis of Leukocytes. Biophys. J. 2020, 118, 565–577. [Google Scholar] [CrossRef] [PubMed]
- Hickman, A.; Koetsier, J.; Kurtanich, T.; Nielsen, M.C.; Winn, G.; Wang, Y.; Bentebibel, S.-E.; Shi, L.; Punt, S.; Williams, L.; et al. LFA-1 Activation Enriches Tumor-Specific T Cells in a Cold Tumor Model and Synergizes with CTLA-4 Blockade. J. Clin. Investig. 2022, 132, e154152. [Google Scholar] [CrossRef] [PubMed]
- van der Flier, A.; Sonnenberg, A. Function and Interactions of Integrins. Cell Tissue Res. 2001, 305, 285–298. [Google Scholar] [CrossRef] [PubMed]
- Peng, H.; Jiang, X.; Chen, Y.; Sojka, D.K.; Wei, H.; Gao, X.; Sun, R.; Yokoyama, W.M.; Tian, Z. Liver-Resident NK Cells Confer Adaptive Immunity in Skin-Contact Inflammation. J. Clin. Investig. 2013, 123, 1444–1456. [Google Scholar] [CrossRef] [PubMed]
- Sojka, D.K.; Plougastel-Douglas, B.; Yang, L.; Pak-Wittel, M.A.; Artyomov, M.N.; Ivanova, Y.; Zhong, C.; Chase, J.M.; Rothman, P.B.; Yu, J.; et al. Tissue-Resident Natural Killer (NK) Cells Are Cell Lineages Distinct from Thymic and Conventional Splenic NK Cells. eLife 2014, 3, e01659. [Google Scholar] [CrossRef] [PubMed]
- Stotesbury, C.; Alves-Peixoto, P.; Montoya, B.; Ferez, M.; Nair, S.; Snyder, C.M.; Zhang, S.; Knudson, C.J.; Sigal, L.J. A2β1 Integrin Is Required for Optimal NK Cell Proliferation during Viral Infection but Not for Acquisition of Effector Functions or NK Cell-Mediated Virus Control. J. Immunol. 2020, 204, 1582–1591. [Google Scholar] [CrossRef] [PubMed]
- Hamza, A.; Amit, J.; Elizabeth, L.E.; Medha, M.P.; Michael, D.C.; Wendy, F.L. Ion Channel Mediated Mechanotransduction in Immune Cells. Curr. Opin. Solid State Mater. Sci. 2021, 25, 100951. [Google Scholar] [CrossRef] [PubMed]
- Brown, D.M.; Donaldson, K.; Stone, V. Role of Calcium in the Induction of TNFα Expression by Macrophages on Exposure to Ultrafine Particles. Ann. Occup. Hyg. 2002, 46, 219–222. [Google Scholar] [CrossRef]
- Immler, R.; Simon, S.I.; Sperandio, M. Calcium Signalling and Related Ion Channels in Neutrophil Recruitment and Function. Eur. J. Clin. Investig. 2018, 48, e12964. [Google Scholar] [CrossRef] [PubMed]
- Hope, J.M.; Dombroski, J.A.; Pereles, R.S.; Lopez-Cavestany, M.; Greenlee, J.D.; Schwager, S.C.; Reinhart-King, C.A.; King, M.R. Fluid Shear Stress Enhances T Cell Activation through Piezo1. BMC Biol. 2022, 20, 61. [Google Scholar] [CrossRef] [PubMed]
- Liu, C.S.C.; Raychaudhuri, D.; Paul, B.; Chakrabarty, Y.; Ghosh, A.R.; Rahaman, O.; Talukdar, A.; Ganguly, D. Cutting Edge: Piezo1 Mechanosensors Optimize Human T Cell Activation. J. Immunol. 2018, 200, 1255–1260. [Google Scholar] [CrossRef] [PubMed]
- Solis, A.G.; Bielecki, P.; Steach, H.R.; Sharma, L.; Harman, C.C.D.; Yun, S.; de Zoete, M.R.; Warnock, J.N.; To, S.D.F.; York, A.G.; et al. Mechanosensation of Cyclical Force by PIEZO1 Is Essential for Innate Immunity. Nature 2019, 573, 69–74. [Google Scholar] [CrossRef] [PubMed]
- Atcha, H.; Jairaman, A.; Holt, J.R.; Meli, V.S.; Nagalla, R.R.; Veerasubramanian, P.K.; Brumm, K.T.; Lim, H.E.; Othy, S.; Cahalan, M.D.; et al. Mechanically Activated Ion Channel Piezo1 Modulates Macrophage Polarization and Stiffness Sensing. Nat. Commun. 2021, 12, 3256. [Google Scholar] [CrossRef] [PubMed]
- Yanamandra, A.K.; Zhang, J.; Montalvo, G.; Biedenweg, D.; Hoth, M.; Lautenschläger, F.; Otto, O.; del Campo, A.; Qu, B. PIEZO1-Mediated Mechanosensing Governs NK Cell Killing Efficiency and Infiltration in Three-Dimensional Matrices. Eur. J. Immunol. 2024, 54, 2350693. [Google Scholar] [CrossRef] [PubMed]
- Maul-Pavicic, A.; Chiang, S.C.C.; Rensing-Ehl, A.; Jessen, B.; Fauriat, C.; Wood, S.M.; Sjöqvist, S.; Hufnagel, M.; Schulze, I.; Bass, T.; et al. ORAI1-Mediated Calcium Influx Is Required for Human Cytotoxic Lymphocyte Degranulation and Target Cell Lysis. Proc. Natl. Acad. Sci. USA 2011, 108, 3324–3329. [Google Scholar] [CrossRef] [PubMed]
- Zhou, X.; Friedmann, K.S.; Lyrmann, H.; Zhou, Y.; Schoppmeyer, R.; Knörck, A.; Mang, S.; Hoxha, C.; Angenendt, A.; Backes, C.S.; et al. A Calcium Optimum for Cytotoxic T Lymphocyte and Natural Killer Cell Cytotoxicity. J. Physiol. 2018, 596, 2681–2698. [Google Scholar] [CrossRef] [PubMed]
- Backes, C.S.; Friedmann, K.S.; Mang, S.; Knörck, A.; Hoth, M.; Kummerow, C. Natural Killer Cells Induce Distinct Modes of Cancer Cell Death: Discrimination, Quantification, and Modulation of Apoptosis, Necrosis, and Mixed Forms. J. Biol. Chem. 2018, 293, 16348–16363. [Google Scholar] [CrossRef] [PubMed]
- Lee, E.H.C.; Wong, D.C.P.; Ding, J.L. NK Cells in a Tug-of-War With Cancer: The Roles of Transcription Factors and Cytoskeleton. Front. Immunol. 2021, 12, 734551. [Google Scholar] [CrossRef] [PubMed]
- Ben-Shmuel, A.; Sabag, B.; Biber, G.; Barda-Saad, M. The Role of the Cytoskeleton in Regulating the Natural Killer Cell Immune Response in Health and Disease: From Signaling Dynamics to Function. Front. Cell Dev. Biol. 2021, 9, 609532. [Google Scholar] [CrossRef] [PubMed]
- Chen, X.; Trivedi, P.P.; Ge, B.; Krzewski, K.; Strominger, J.L. Many NK Cell Receptors Activate ERK2 and JNK1 to Trigger Microtubule Organizing Center and Granule Polarization and Cytotoxicity. Proc. Natl. Acad. Sci. USA 2007, 104, 6329–6334. [Google Scholar] [CrossRef] [PubMed]
- Li, C.; Ge, B.; Nicotra, M.; Stern, J.N.H.; Kopcow, H.D.; Chen, X.; Strominger, J.L. JNK MAP Kinase Activation Is Required for MTOC and Granule Polarization in NKG2D-Mediated NK Cell Cytotoxicity. Proc. Natl. Acad. Sci. USA 2008, 105, 3017–3022. [Google Scholar] [CrossRef] [PubMed]
- Prager, I.; Watzl, C. Mechanisms of Natural Killer Cell-Mediated Cellular Cytotoxicity. J. Leukoc. Biol. 2019, 105, 1319–1329. [Google Scholar] [CrossRef] [PubMed]
- Jankowska, K.I.; Williamson, E.K.; Roy, N.H.; Blumenthal, D.; Chandra, V.; Baumgart, T.; Burkhardt, J.K. Integrins Modulate T Cell Receptor Signaling by Constraining Actin Flow at the Immunological Synapse. Front. Immunol. 2018, 9, 311323. [Google Scholar] [CrossRef] [PubMed]
- Stebbins, C.C.; Watzl, C.; Billadeau, D.D.; Leibson, P.J.; Burshtyn, D.N.; Long, E.O. Vav1 Dephosphorylation by the Tyrosine Phosphatase SHP-1 as a Mechanism for Inhibition of Cellular Cytotoxicity. Mol. Cell. Biol. 2003, 23, 6291–6299. [Google Scholar] [CrossRef] [PubMed]
- Matalon, O.; Fried, S.; Ben-Shmuel, A.; Pauker, M.H.; Joseph, N.; Keizer, D.; Piterburg, M.; Barda-Saad, M. Dephosphorylation of the Adaptor LAT and Phospholipase C–γ by SHP-1 Inhibits Natural Killer Cell Cytotoxicity. Sci. Signal. 2016, 9, ra54. [Google Scholar] [CrossRef] [PubMed]
- Matalon, O.; Ben-Shmuel, A.; Kivelevitz, J.; Sabag, B.; Fried, S.; Joseph, N.; Noy, E.; Biber, G.; Barda-Saad, M. Actin Retrograde Flow Controls Natural Killer Cell Response by Regulating the Conformation State of SHP-1. EMBO J. 2018, 37, e96264. [Google Scholar] [CrossRef] [PubMed]
- Davis, D.M. Mechanisms and Functions for the Duration of Intercellular Contacts Made by Lymphocytes. Nat. Rev. Immunol. 2009, 9, 543–555. [Google Scholar] [CrossRef] [PubMed]
- Wolf, K.; Alexander, S.; Schacht, V.; Coussens, L.M.; von Andrian, U.H.; van Rheenen, J.; Deryugina, E.; Friedl, P. Collagen-Based Cell Migration Models in Vitro and in Vivo. Semin. Cell Dev. Biol. 2009, 20, 931–941. [Google Scholar] [CrossRef] [PubMed]
- Yamada, K.M.; Sixt, M. Mechanisms of 3D Cell Migration. Nat. Rev. Mol. Cell Biol. 2019, 20, 738–752. [Google Scholar] [CrossRef] [PubMed]
- Szczesny, S.E.; Mauck, R.L. The Nuclear Option: Evidence Implicating the Cell Nucleus in Mechanotransduction. J. Biomech. Eng. 2017, 139, 021006. [Google Scholar] [CrossRef] [PubMed]
- Long, J.T.; Lammerding, J. Nuclear Deformation Lets Cells Gauge Their Physical Confinement. Dev. Cell 2021, 56, 156–158. [Google Scholar] [CrossRef] [PubMed]
- Kalukula, Y.; Stephens, A.D.; Lammerding, J.; Gabriele, S. Mechanics and Functional Consequences of Nuclear Deformations. Nat. Rev. Mol. Cell Biol. 2022, 23, 583–602. [Google Scholar] [CrossRef] [PubMed]
- Gupta, S.; Marcel, N.; Sarin, A.; Shivashankar, G.V. Role of Actin Dependent Nuclear Deformation in Regulating Early Gene Expression. PLoS ONE 2012, 7, e53031. [Google Scholar] [CrossRef] [PubMed]
- Wong, D.C.P.; Lee, E.H.C.; Er, J.; Yow, I.; Koean, R.A.G.; Ang, O.; Xiao, J.; Low, B.C.; Ding, J.L. Lung Cancer Induces NK Cell Contractility and Cytotoxicity Through Transcription Factor Nuclear Localization. Front. Cell Dev. Biol. 2022, 10, 871326. [Google Scholar] [CrossRef] [PubMed]
- Seirin-Lee, S.; Osakada, F.; Takeda, J.; Tashiro, S.; Kobayashi, R.; Yamamoto, T.; Ochiai, H. Role of Dynamic Nuclear Deformation on Genomic Architecture Reorganization. PLoS Comput. Biol. 2019, 15, e1007289. [Google Scholar] [CrossRef] [PubMed]
- Krause, M.; Yang, F.W.; te Lindert, M.; Isermann, P.; Schepens, J.; Maas, R.J.A.; Venkataraman, C.; Lammerding, J.; Madzvamuse, A.; Hendriks, W.; et al. Cell Migration through Three-Dimensional Confining Pores: Speed Accelerations by Deformation and Recoil of the Nucleus. Philos. Trans. R. Soc. B Biol. Sci. 2019, 374, 20180225. [Google Scholar] [CrossRef]
- Thiam, H.-R.; Vargas, P.; Carpi, N.; Crespo, C.L.; Raab, M.; Terriac, E.; King, M.C.; Jacobelli, J.; Alberts, A.S.; Stradal, T.; et al. Perinuclear Arp2/3-Driven Actin Polymerization Enables Nuclear Deformation to Facilitate Cell Migration through Complex Environments. Nat. Commun. 2016, 7, 10997. [Google Scholar] [CrossRef] [PubMed]
- Mace, E.M.; Monkley, S.J.; Critchley, D.R.; Takei, F. A Dual Role for Talin in NK Cell Cytotoxicity: Activation of LFA-1-Mediated Cell Adhesion and Polarization of NK Cells. J. Immunol. 2009, 182, 948–956. [Google Scholar] [CrossRef] [PubMed]
- Hanahan, D.; Weinberg, R.A. Hallmarks of Cancer: The next Generation. Cell 2011, 144, 646–674. [Google Scholar] [CrossRef] [PubMed]
- Nia, H.T.; Munn, L.L.; Jain, R.K. Physical Traits of Cancer. Science 2020, 370, eaaz0868. [Google Scholar] [CrossRef] [PubMed]
- Jain, R.K. Antiangiogenesis strategies revisited: From starving tumors to alleviating hypoxia. Cancer Cell 2014, 26, 605–622. [Google Scholar] [CrossRef] [PubMed]
- Stylianopoulos, T.; Martin, J.D.; Chauhan, V.P.; Jain, S.R.; Diop-Frimpong, B.; Bardeesy, N.; Smith, B.L.; Ferrone, C.R.; Hornicek, F.J.; Boucher, Y.; et al. Causes, Consequences, and Remedies for Growth-Induced Solid Stress in Murine and Human Tumors. Proc. Natl. Acad. Sci. USA 2012, 109, 15101–15108. [Google Scholar] [CrossRef] [PubMed]
- Stylianopoulos, T.; Martin, J.D.; Snuderl, M.; Mpekris, F.; Jain, S.R.; Jain, R.K. Coevolution of Solid Stress and Interstitial Fluid Pressure in Tumors during Progression: Implications for Vascular Collapse. Cancer Res. 2013, 73, 3833–3841. [Google Scholar] [CrossRef] [PubMed]
- Voutouri, C.; Polydorou, C.; Papageorgis, P.; Gkretsi, V.; Stylianopoulos, T. Hyaluronan-Derived Swelling of Solid Tumors, the Contribution of Collagen and Cancer Cells, and Implications for Cancer Therapy. Neoplasia 2016, 18, 732–741. [Google Scholar] [CrossRef] [PubMed]
- Simon, D.D.; Horgan, C.O.; Humphrey, J.D. Mechanical Restrictions on Biological Responses by Adherent Cells within Collagen Gels. J. Mech. Behav. Biomed. Mater. 2012, 14, 216–226. [Google Scholar] [CrossRef] [PubMed]
- Nia, H.T.; Liu, H.; Seano, G.; Datta, M.; Jones, D.; Rahbari, N.; Incio, J.; Chauhan, V.P.; Jung, K.; Martin, J.D.; et al. Solid Stress and Elastic Energy as Measures of Tumour Mechanopathology. Nat. Biomed. Eng. 2016, 1, 4. [Google Scholar] [CrossRef] [PubMed]
- Huang, W.; Hu, H.; Zhang, Q.; Wu, X.; Wei, F.; Yang, F.; Gan, L.; Wang, N.; Yang, X.; Guo, A.-Y. Regulatory Networks in Mechanotransduction Reveal Key Genes in Promoting Cancer Cell Stemness and Proliferation. Oncogene 2019, 38, 6818–6834. [Google Scholar] [CrossRef] [PubMed]
- Halder, G.; Dupont, S.; Piccolo, S. Transduction of Mechanical and Cytoskeletal Cues by YAP and TAZ. Nat. Rev. Mol. Cell Biol. 2012, 13, 591–600. [Google Scholar] [CrossRef] [PubMed]
- Du, H.; Bartleson, J.M.; Butenko, S.; Alonso, V.; Liu, W.F.; Winer, D.A.; Butte, M.J. Tuning Immunity through Tissue Mechanotransduction. Nat. Rev. Immunol. 2023, 23, 174–188. [Google Scholar] [CrossRef] [PubMed]
- Cheng, D.; Jin, L.; Chen, Y.; Xi, X.; Guo, Y. YAP Promotes Epithelial Mesenchymal Transition by Upregulating Slug Expression in Human Colorectal Cancer Cells. Int. J. Clin. Exp. Pathol. 2020, 13, 701–710. [Google Scholar] [PubMed]
- Wong, D.C.P.; Xia, Z.; Shao, N.; Yow, I.; Thivakar, T.; Yeo, J.Y.; Salazar, A.M.; Liou, Y.-C.; Low, B.C.; Ding, J.L. Hiltonol, a dsRNA Mimic, Promotes NK Cell Anticancer Cytotoxicity Through TAZ Cytoplasmic Sequestration. Adv. Ther. 2023, 6, 2300016. [Google Scholar] [CrossRef]
- Klopotowska, M.; Bajor, M.; Graczyk-Jarzynka, A.; Kraft, A.; Pilch, Z.; Zhylko, A.; Firczuk, M.; Baranowska, I.; Lazniewski, M.; Plewczynski, D.; et al. PRDX-1 Supports the Survival and Antitumor Activity of Primary and CAR-Modified NK Cells under Oxidative Stress. Cancer Immunol. Res. 2022, 10, 228–244. [Google Scholar] [CrossRef] [PubMed]
- Chauhan, V.P.; Boucher, Y.; Ferrone, C.R.; Roberge, S.; Martin, J.D.; Stylianopoulos, T.; Bardeesy, N.; DePinho, R.A.; Padera, T.P.; Munn, L.L.; et al. Compression of Pancreatic Tumor Blood Vessels by Hyaluronan Is Caused by Solid Stress and Not Interstitial Fluid Pressure. Cancer Cell 2014, 26, 14–15. [Google Scholar] [CrossRef] [PubMed]
- Jain, R.K. Normalizing Tumor Microenvironment to Treat Cancer: Bench to Bedside to Biomarkers. J. Clin. Oncol. 2013, 31, 2205–2218. [Google Scholar] [CrossRef] [PubMed]
- Zhang, T.; Jia, Y.; Yu, Y.; Zhang, B.; Xu, F.; Guo, H. Targeting the Tumor Biophysical Microenvironment to Reduce Resistance to Immunotherapy. Adv. Drug Deliv. Rev. 2022, 186, 114319. [Google Scholar] [CrossRef] [PubMed]
- Jain, R.K. Normalization of Tumor Vasculature: An Emerging Concept in Antiangiogenic Therapy. Science 2005, 307, 58–62. [Google Scholar] [CrossRef] [PubMed]
- Hurwitz, H. Integrating the Anti–VEGF-A Humanized Monoclonal Antibody Bevacizumab with Chemotherapy in Advanced Colorectal Cancer. Clin. Color. Cancer 2004, 4, S62–S68. [Google Scholar] [CrossRef] [PubMed]
- Tilki, D.; Kilic, N.; Sevinc, S.; Zywietz, F.; Stief, C.G.; Ergun, S. Zone-Specific Remodeling of Tumor Blood Vessels Affects Tumor Growth. Cancer 2007, 110, 2347–2362. [Google Scholar] [CrossRef] [PubMed]
- Klein, D. The Tumor Vascular Endothelium as Decision Maker in Cancer Therapy. Front. Oncol. 2018, 8, 367. [Google Scholar] [CrossRef] [PubMed]
- Hu, B.; Xin, Y.; Hu, G.; Li, K.; Tan, Y. Fluid Shear Stress Enhances Natural Killer Cell’s Cytotoxicity toward Circulating Tumor Cells through NKG2D-Mediated Mechanosensing. APL Bioeng. 2023, 7, 036108. [Google Scholar] [CrossRef] [PubMed]
- Dirkx, A.E.M.; Oude Egbrink, M.G.A.; Kuijpers, M.J.E.; van der Niet, S.T.; Heijnen, V.V.T.; Bouma-ter Steege, J.C.A.; Wagstaff, J.; Griffioen, A.W. Tumor Angiogenesis Modulates Leukocyte-Vessel Wall Interactions in Vivo by Reducing Endothelial Adhesion Molecule Expression. Cancer Res 2003, 63, 2322–2329. [Google Scholar] [PubMed]
- Won Jun, H.; Kyung Lee, H.; Ho Na, I.; Jeong Lee, S.; Kim, K.; Park, G.; Sook Kim, H.; Ju Son, D.; Kim, Y.; Tae Hong, J.; et al. The Role of CCL2, CCL7, ICAM-1, and VCAM-1 in Interaction of Endothelial Cells and Natural Killer Cells. Int. Immunopharmacol. 2022, 113, 109332. [Google Scholar] [CrossRef] [PubMed]
- Wu, L.; Saxena, S.; Singh, R.K. Neutrophils in the Tumor Microenvironment. Adv. Exp. Med. Biol. 2020, 1224, 1–20. [Google Scholar] [CrossRef] [PubMed]
- Cochlin, D.L.; Ganatra, R.H.; Griffiths, D.F.R. Elastography in the Detection of Prostatic Cancer. Clin. Radiol. 2002, 57, 1014–1020. [Google Scholar] [CrossRef] [PubMed]
- Boyd, N.F.; Li, Q.; Melnichouk, O.; Huszti, E.; Martin, L.J.; Gunasekara, A.; Mawdsley, G.; Yaffe, M.J.; Minkin, S. Evidence That Breast Tissue Stiffness Is Associated with Risk of Breast Cancer. PLoS ONE 2014, 9, e100937. [Google Scholar] [CrossRef] [PubMed]
- Maskarinec, G.; Pagano, I.S.; Little, M.A.; Conroy, S.M.; Park, S.-Y.; Kolonel, L.N. Mammographic Density as a Predictor of Breast Cancer Survival: The Multiethnic Cohort. Breast Cancer Res. 2013, 15, R7. [Google Scholar] [CrossRef] [PubMed]
- Liu, C.; Pei, H.; Tan, F. Matrix Stiffness and Colorectal Cancer. OTT 2020, 13, 2747–2755. [Google Scholar] [CrossRef] [PubMed]
- Pickup, M.W.; Mouw, J.K.; Weaver, V.M. The Extracellular Matrix Modulates the Hallmarks of Cancer. EMBO Rep. 2014, 15, 1243–1253. [Google Scholar] [CrossRef]
- Paszek, M.J.; Zahir, N.; Johnson, K.R.; Lakins, J.N.; Rozenberg, G.I.; Gefen, A.; Reinhart-King, C.A.; Margulies, S.S.; Dembo, M.; Boettiger, D.; et al. Tensional Homeostasis and the Malignant Phenotype. Cancer Cell 2005, 8, 241–254. [Google Scholar] [CrossRef] [PubMed]
- Ulrich, T.A.; de Juan Pardo, E.M.; Kumar, S. The Mechanical Rigidity of the Extracellular Matrix Regulates the Structure, Motility, and Proliferation of Glioma Cells. Cancer Res. 2009, 69, 4167–4174. [Google Scholar] [CrossRef] [PubMed]
- Bordeleau, F.; Mason, B.N.; Lollis, E.M.; Mazzola, M.; Zanotelli, M.R.; Somasegar, S.; Califano, J.P.; Montague, C.; LaValley, D.J.; Huynh, J.; et al. Matrix Stiffening Promotes a Tumor Vasculature Phenotype. Proc. Natl. Acad. Sci. USA 2017, 114, 492–497. [Google Scholar] [CrossRef] [PubMed]
- Tung, J.C.; Barnes, J.M.; Desai, S.R.; Sistrunk, C.; Conklin, M.W.; Schedin, P.; Eliceiri, K.W.; Keely, P.J.; Seewaldt, V.L.; Weaver, V.M. Tumor Mechanics and Metabolic Dysfunction. Free Radic. Biol. Med. 2015, 79, 269–280. [Google Scholar] [CrossRef] [PubMed]
- Levental, K.R.; Yu, H.; Kass, L.; Lakins, J.N.; Egeblad, M.; Erler, J.T.; Fong, S.F.T.; Csiszar, K.; Giaccia, A.; Weninger, W.; et al. Matrix Crosslinking Forces Tumor Progression by Enhancing Integrin Signaling. Cell 2009, 139, 891–906. [Google Scholar] [CrossRef] [PubMed]
- Lang, N.R.; Skodzek, K.; Hurst, S.; Mainka, A.; Steinwachs, J.; Schneider, J.; Aifantis, K.E.; Fabry, B. Biphasic Response of Cell Invasion to Matrix Stiffness in Three-Dimensional Biopolymer Networks. Acta Biomater. 2015, 13, 61–67. [Google Scholar] [CrossRef] [PubMed]
- Wirtz, D.; Konstantopoulos, K.; Searson, P.C. The Physics of Cancer: The Role of Physical Interactions and Mechanical Forces in Metastasis. Nat. Rev. Cancer 2011, 11, 512–522. [Google Scholar] [CrossRef] [PubMed]
- Pathak, A.; Kumar, S. Independent Regulation of Tumor Cell Migration by Matrix Stiffness and Confinement. Proc. Natl. Acad. Sci. USA 2012, 109, 10334–10339. [Google Scholar] [CrossRef] [PubMed]
- Charras, G.; Sahai, E. Physical Influences of the Extracellular Environment on Cell Migration. Nat. Rev. Mol. Cell Biol. 2014, 15, 813–824. [Google Scholar] [CrossRef] [PubMed]
- Panzetta, V.; Musella, I.; Rapa, I.; Volante, M.; Netti, P.A.; Fusco, S. Mechanical Phenotyping of Cells and Extracellular Matrix as Grade and Stage Markers of Lung Tumor Tissues. Acta Biomater. 2017, 57, 334–341. [Google Scholar] [CrossRef] [PubMed]
- Najafi, M.; Farhood, B.; Mortezaee, K. Extracellular Matrix (ECM) Stiffness and Degradation as Cancer Drivers. J. Cell. Biochem. 2019, 120, 2782–2790. [Google Scholar] [CrossRef] [PubMed]
- Eble, J.A.; Niland, S. The Extracellular Matrix in Tumor Progression and Metastasis. Clin. Exp. Metastasis 2019, 36, 171–198. [Google Scholar] [CrossRef] [PubMed]
- Friedman, D.; Simmonds, P.; Hale, A.; Bere, L.; Hodson, N.W.; White, M.R.H.; Davis, D.M. Natural Killer Cell Immune Synapse Formation and Cytotoxicity Are Controlled by Tension of the Target Interface. J. Cell Sci. 2021, 134, jcs258570. [Google Scholar] [CrossRef] [PubMed]
- Rianna, C.; Radmacher, M.; Kumar, S. Direct Evidence That Tumor Cells Soften When Navigating Confined Spaces. Mol. Biol. Cell 2020, 31, 1726–1734. [Google Scholar] [CrossRef] [PubMed]
- Roberts, A.B.; Zhang, J.; Raj Singh, V.; Nikolić, M.; Moeendarbary, E.; Kamm, R.D.; So, P.T.C.; Scarcelli, G. Tumor Cell Nuclei Soften during Transendothelial Migration. J. Biomech. 2021, 121, 110400. [Google Scholar] [CrossRef]
- Chen, Y.; Lan, H.; Wu, Y.; Yang, W.; Chiou, A.; Yang, M. Epithelial-mesenchymal Transition Softens Head and Neck Cancer Cells to Facilitate Migration in 3D Environments. J. Cell. Mol. Med. 2018, 22, 3837–3846. [Google Scholar] [CrossRef] [PubMed]
- Melder, R.J.; Kristensen, C.A.; Munn, L.L.; Jain, R.K. Modulation of A-NK Cell Rigidity: In Vitro Characterization and in Vivo Implications for Cell Delivery. Biorheology 2001, 38, 151–159. [Google Scholar] [PubMed]
- Melder, R.J.; Jain, R.K. Reduction of Rigidity in Human Activated Natural Killer Cells by Thioglycollate Treatment. J. Immunol. Methods 1994, 175, 69–77. [Google Scholar] [CrossRef] [PubMed]
- Ishihara, S.; Yasuda, M.; Harada, I.; Mizutani, T.; Kawabata, K.; Haga, H. Substrate Stiffness Regulates Temporary NF-κB Activation via Actomyosin Contractions. Exp. Cell Res. 2013, 319, 2916–2927. [Google Scholar] [CrossRef] [PubMed]
- Simonetta, F.; Pradier, A.; Roosnek, E. T-Bet and Eomesodermin in NK Cell Development, Maturation, and Function. Front. Immunol. 2016, 7, 241. [Google Scholar] [CrossRef] [PubMed]
- Melder, R.J.; Jain, R.K. Kinetics of Interleukin-2 Induced Changes in Rigidity of Human Natural Killer Cells. Cell Biophys. 1992, 20, 161–176. [Google Scholar] [CrossRef] [PubMed]
- Frantz, C.; Stewart, K.M.; Weaver, V.M. The Extracellular Matrix at a Glance. J. Cell Sci. 2010, 123, 4195–4200. [Google Scholar] [CrossRef] [PubMed]
- Cukierman, E.; Bassi, D.E. Physico-Mechanical Aspects of Extracellular Matrix Influences on Tumorigenic Behaviors. Semin. Cancer Biol. 2010, 20, 139–145. [Google Scholar] [CrossRef] [PubMed]
- Provenzano, P.P.; Eliceiri, K.W.; Campbell, J.M.; Inman, D.R.; White, J.G.; Keely, P.J. Collagen Reorganization at the Tumor-Stromal Interface Facilitates Local Invasion. BMC Med. 2006, 4, 38. [Google Scholar] [CrossRef] [PubMed]
- Conklin, M.W.; Eickhoff, J.C.; Riching, K.M.; Pehlke, C.A.; Eliceiri, K.W.; Provenzano, P.P.; Friedl, A.; Keely, P.J. Aligned Collagen Is a Prognostic Signature for Survival in Human Breast Carcinoma. Am. J. Pathol. 2011, 178, 1221–1232. [Google Scholar] [CrossRef] [PubMed]
- Fraley, S.I.; Wu, P.; He, L.; Feng, Y.; Krisnamurthy, R.; Longmore, G.D.; Wirtz, D. Three-Dimensional Matrix Fiber Alignment Modulates Cell Migration and MT1-MMP Utility by Spatially and Temporally Directing Protrusions. Sci. Rep. 2015, 5, 14580. [Google Scholar] [CrossRef] [PubMed]
- Velez, D.O.; Tsui, B.; Goshia, T.; Chute, C.L.; Han, A.; Carter, H.; Fraley, S.I. 3D Collagen Architecture Induces a Conserved Migratory and Transcriptional Response Linked to Vasculogenic Mimicry. Nat. Commun. 2017, 8, 1651. [Google Scholar] [CrossRef] [PubMed]
- Hung, W.-C.; Yang, J.R.; Yankaskas, C.L.; Wong, B.S.; Wu, P.-H.; Pardo-Pastor, C.; Serra, S.A.; Chiang, M.-J.; Gu, Z.; Wirtz, D.; et al. Confinement Sensing and Signal Optimization via Piezo1/PKA and Myosin II Pathways. Cell Rep. 2016, 15, 1430–1441. [Google Scholar] [CrossRef] [PubMed]
- Henke, E.; Nandigama, R.; Ergün, S. Extracellular Matrix in the Tumor Microenvironment and Its Impact on Cancer Therapy. Front. Mol. Biosci. 2020, 6, 160. [Google Scholar] [CrossRef] [PubMed]
- Friedl, P.; Weigelin, B. Interstitial Leukocyte Migration and Immune Function. Nat. Immunol. 2008, 9, 960–969. [Google Scholar] [CrossRef] [PubMed]
- Raab, M.; Gentili, M.; de Belly, H.; Thiam, H.-R.; Vargas, P.; Jimenez, A.J.; Lautenschlaeger, F.; Voituriez, R.; Lennon-Duménil, A.-M.; Manel, N.; et al. ESCRT III Repairs Nuclear Envelope Ruptures during Cell Migration to Limit DNA Damage and Cell Death. Science 2016, 352, 359–362. [Google Scholar] [CrossRef] [PubMed]
- Irianto, J.; Xia, Y.; Pfeifer, C.R.; Athirasala, A.; Ji, J.; Alvey, C.; Tewari, M.; Bennett, R.R.; Harding, S.M.; Liu, A.J.; et al. DNA Damage Follows Repair Factor Depletion and Portends Genome Variation in Cancer Cells after Pore Migration. Curr. Biol. 2017, 27, 210–223. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Y.; Zhuo, Y.; Peng, R.; Zhang, Y.; Du, Y.; Zhang, Q.; Sun, Y.; Qiu, L. Functional Nucleic Acid-Based Cell Imaging and Manipulation. Sci. China Chem. 2021, 64, 1817–1825. [Google Scholar] [CrossRef]
- Wang, Y.-L.; Lin, Y.-C. Traction Force Microscopy by Deep Learning. Biophys. J. 2021, 120, 3079–3090. [Google Scholar] [CrossRef] [PubMed]
- Le Saux, G.; Schvartzman, M. Advanced Materials and Devices for the Regulation and Study of NK Cells. Int. J. Mol. Sci. 2019, 20, 646. [Google Scholar] [CrossRef] [PubMed]
- Ayuso, J.M.; Rehman, S.; Virumbrales-Munoz, M.; McMinn, P.H.; Geiger, P.; Fitzgerald, C.; Heaster, T.; Skala, M.C.; Beebe, D.J. Microfluidic Tumor-on-a-Chip Model to Evaluate the Role of Tumor Environmental Stress on NK Cell Exhaustion. Sci. Adv. 2021, 7, eabc2331. [Google Scholar] [CrossRef] [PubMed]
- Ayuso, J.M.; Truttschel, R.; Gong, M.M.; Humayun, M.; Virumbrales-Munoz, M.; Vitek, R.; Felder, M.; Gillies, S.D.; Sondel, P.; Wisinski, K.B.; et al. Evaluating Natural Killer Cell Cytotoxicity against Solid Tumors Using a Microfluidic Model. OncoImmunology 2019, 8, 1553477. [Google Scholar] [CrossRef] [PubMed]
- Boudreau, J.E.; Bonehill, A.; Thielemans, K.; Wan, Y. Engineering Dendritic Cells to Enhance Cancer Immunotherapy. Mol. Ther. 2011, 19, 841–853. [Google Scholar] [CrossRef] [PubMed]
- Hipolito, J.; Peretz-Soroka, H.; Zhang, M.; Yang, K.; Karimi-Abdolrezaee, S.; Lin, F.; Kung, S.K.P. A New Microfluidic Platform for Studying Natural Killer Cell and Dendritic Cell Interactions. Micromachines 2019, 10, 851. [Google Scholar] [CrossRef] [PubMed]
- Culley, F.J.; Johnson, M.; Evans, J.H.; Kumar, S.; Crilly, R.; Casasbuenas, J.; Schnyder, T.; Mehrabi, M.; Deonarain, M.P.; Ushakov, D.S.; et al. Natural Killer Cell Signal Integration Balances Synapse Symmetry and Migration. PLoS Biol. 2009, 7, e1000159. [Google Scholar] [CrossRef] [PubMed]
- Cho, Y.; Kim, J.; Park, J.; Doh, J. Surface Nanotopography and Cell Shape Modulate Tumor Cell Susceptibility to NK Cell Cytotoxicity. Mater. Horiz. 2023, 10, 4532–4540. [Google Scholar] [CrossRef] [PubMed]
- McWhorter, F.Y.; Wang, T.; Nguyen, P.; Chung, T.; Liu, W.F. Modulation of Macrophage Phenotype by Cell Shape. Proc. Natl. Acad. Sci. USA 2013, 110, 17253. [Google Scholar] [CrossRef] [PubMed]
- Doh, J.; Irvine, D.J. Immunological Synapse Arrays: Patterned Protein Surfaces That Modulate Immunological Synapse Structure Formation in T Cells. Proc. Natl. Acad. Sci. USA 2006, 103, 5700–5705. [Google Scholar] [CrossRef] [PubMed]
- Peppas, N.A.; Hilt, J.Z.; Khademhosseini, A.; Langer, R. Hydrogels in Biology and Medicine: From Molecular Principles to Bionanotechnology. Adv. Mater. 2006, 18, 1345–1360. [Google Scholar] [CrossRef]
- Tibbitt, M.W.; Anseth, K.S. Hydrogels as Extracellular Matrix Mimics for 3D Cell Culture. Biotechnol. Bioeng. 2009, 103, 655–663. [Google Scholar] [CrossRef] [PubMed]
- Drury, J.L.; Mooney, D.J. Hydrogels for Tissue Engineering: Scaffold Design Variables and Applications. Biomaterials 2003, 24, 4337–4351. [Google Scholar] [CrossRef] [PubMed]
- Temples, M.N.; Adjei, I.M.; Nimocks, P.M.; Djeu, J.; Sharma, B. Engineered Three-Dimensional Tumor Models to Study Natural Killer Cell Suppression. ACS Biomater. Sci. Eng. 2020, 6, 4179–4199. [Google Scholar] [CrossRef] [PubMed]
- Wu, D.; Yu, Y.; Zhao, C.; Shou, X.; Piao, Y.; Zhao, X.; Zhao, Y.; Wang, S. NK-Cell-Encapsulated Porous Microspheres via Microfluidic Electrospray for Tumor Immunotherapy. ACS Appl. Mater. Interfaces 2019, 11, 33716–33724. [Google Scholar] [CrossRef] [PubMed]
- Le Saux, G.; Bar-Hanin, N.; Edri, A.; Hadad, U.; Porgador, A.; Schvartzman, M. Nanoscale Mechanosensing of Natural Killer Cells Is Revealed by Antigen-Functionalized Nanowires. Adv. Mater. 2019, 31, 1805954. [Google Scholar] [CrossRef] [PubMed]
- Bhingardive, V.; Le Saux, G.; Edri, A.; Porgador, A.; Schvartzman, M. Nanowire Based Guidance of the Morphology and Cytotoxic Activity of Natural Killer Cells. Small 2021, 17, 2007347. [Google Scholar] [CrossRef] [PubMed]
- Shalek, A.K.; Gaublomme, J.T.; Wang, L.; Yosef, N.; Chevrier, N.; Andersen, M.S.; Robinson, J.T.; Pochet, N.; Neuberg, D.; Gertner, R.S.; et al. Nanowire-Mediated Delivery Enables Functional Interrogation of Primary Immune Cells: Application to the Analysis of Chronic Lymphocytic Leukemia. Nano Lett. 2012, 12, 6498–6504. [Google Scholar] [CrossRef] [PubMed]
- Jiao, P.; Otto, M.; Geng, Q.; Li, C.; Li, F.; Butch, E.R.; Snyder, S.E.; Zhou, H.; Yan, B. Enhancing Both CT Imaging and Natural Killer Cell-Mediated Cancer Cell Killing by a GD2-Targeting Nanoconstruct. J. Mater. Chem. B Mater. Biol. Med. 2016, 4, 513–520. [Google Scholar] [CrossRef] [PubMed]
- Wu, L.; Zhang, F.; Wei, Z.; Li, X.; Zhao, H.; Lv, H.; Ge, R.; Ma, H.; Zhang, H.; Yang, B.; et al. Magnetic Delivery of Fe3O4 @polydopamine Nanoparticle-Loaded Natural Killer Cells Suggest a Promising Anticancer Treatment. Biomater. Sci. 2018, 6, 2714–2725. [Google Scholar] [CrossRef]
- Sim, T.; Choi, B.; Kwon, S.W.; Kim, K.-S.; Choi, H.; Ross, A.; Kim, D.-H. Magneto-Activation and Magnetic Resonance Imaging of Natural Killer Cells Labeled with Magnetic Nanocomplexes for the Treatment of Solid Tumors. ACS Nano 2021, 15, 12780–12793. [Google Scholar] [CrossRef]
- Lim, Y.T.; Cho, M.Y.; Noh, Y.-W.; Chung, J.W.; Chung, B.H. Near-Infrared Emitting Fluorescent Nanocrystals-Labeled Natural Killer Cells as a Platform Technology for the Optical Imaging of Immunotherapeutic Cells-Based Cancer Therapy. Nanotechnology 2009, 20, 475102. [Google Scholar] [CrossRef] [PubMed]
- Adjei, I.M.; Jordan, J.; Tu, N.; Trinh, T.L.; Kandell, W.; Wei, S.; Sharma, B. Functional Recovery of Natural Killer Cell Activity by Nanoparticle-Mediated Delivery of Transforming Growth Factor Beta 2 Small Interfering RNA. J. Interdiscip. Nanomed. 2019, 4, 98–112. [Google Scholar] [CrossRef]
- Grady, M.E.; Parrish, E.; Caporizzo, M.A.; Seeger, S.C.; Composto, R.J.; Eckmann, D.M. Intracellular Nanoparticle Dynamics Affected by Cytoskeletal Integrity. Soft Matter 2017, 13, 1873–1880. [Google Scholar] [CrossRef] [PubMed]
- Královec, K.; Melounková, L.; Slováková, M.; Mannová, N.; Sedlák, M.; Bartáček, J.; Havelek, R. Disruption of Cell Adhesion and Cytoskeletal Networks by Thiol-Functionalized Silica-Coated Iron Oxide Nanoparticles. Int. J. Mol. Sci. 2020, 21, 9350. [Google Scholar] [CrossRef]
- Déciga-Alcaraz, A.; Delgado-Buenrostro, N.L.; Ispanixtlahuatl-Meráz, O.; Freyre-Fonseca, V.; Flores-Flores, J.O.; Ganem-Rondero, A.; Vaca-Paniagua, F.; del Pilar Ramos-Godinez, M.; Morales-Barcenas, R.; Sánchez-Pérez, Y.; et al. Irreversible Disruption of the Cytoskeleton as Induced by Non-Cytotoxic Exposure to Titanium Dioxide Nanoparticles in Lung Epithelial Cells. Chem.-Biol. Interact. 2020, 323, 109063. [Google Scholar] [CrossRef] [PubMed]
- Prakash, S.; Kumbhojkar, N.; Lu, A.; Kapate, N.; Suja, V.C.; Park, K.S.; Wang, L.L.-W.; Mitragotri, S. Polymer Micropatches as Natural Killer Cell Engagers for Tumor Therapy. ACS Nano 2023, 17, 15918–15930. [Google Scholar] [CrossRef] [PubMed]
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Lightsey, S.; Sharma, B. Natural Killer Cell Mechanosensing in Solid Tumors. Bioengineering 2024, 11, 328. https://doi.org/10.3390/bioengineering11040328
Lightsey S, Sharma B. Natural Killer Cell Mechanosensing in Solid Tumors. Bioengineering. 2024; 11(4):328. https://doi.org/10.3390/bioengineering11040328
Chicago/Turabian StyleLightsey, Suzanne, and Blanka Sharma. 2024. "Natural Killer Cell Mechanosensing in Solid Tumors" Bioengineering 11, no. 4: 328. https://doi.org/10.3390/bioengineering11040328
APA StyleLightsey, S., & Sharma, B. (2024). Natural Killer Cell Mechanosensing in Solid Tumors. Bioengineering, 11(4), 328. https://doi.org/10.3390/bioengineering11040328