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Published in: Cancer and Metastasis Reviews 1-2/2009

Open Access 01-06-2009

Mechanics, malignancy, and metastasis: The force journey of a tumor cell

Authors: Sanjay Kumar, Valerie M. Weaver

Published in: Cancer and Metastasis Reviews | Issue 1-2/2009

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Abstract

A cell undergoes many genetic and epigenetic changes as it transitions to malignancy. Malignant transformation is also accompanied by a progressive loss of tissue homeostasis and perturbations in tissue architecture that ultimately culminates in tumor cell invasion into the parenchyma and metastasis to distant organ sites. Increasingly, cancer biologists have begun to recognize that a critical component of this transformation journey involves marked alterations in the mechanical phenotype of the cell and its surrounding microenvironment. These mechanical differences include modifications in cell and tissue structure, adaptive force-induced changes in the environment, altered processing of micromechanical cues encoded in the extracellular matrix (ECM), and cell-directed remodeling of the extracellular stroma. Here, we review critical steps in this “force journey,” including mechanical contributions to tissue dysplasia, invasion of the ECM, and metastasis. We discuss the biophysical basis of this force journey and present recent advances in the measurement of cellular mechanical properties in vitro and in vivo. We end by describing examples of molecular mechanisms through which tumor cells sense, process and respond to mechanical forces in their environment. While our understanding of the mechanical components of tumor growth, survival and motility remains in its infancy, considerable work has already yielded valuable insight into the molecular basis of force-dependent tumor pathophysiology, which offers new directions in cancer chemotherapeutics.
Literature
1.
go back to reference Lelievre, S. A., Weaver, V. M., Nickerson, J. A., Larabell, C. A., Bhaumik, A., Petersen, O. W., et al. (1998). Tissue phenotype depends on reciprocal interactions between the extracellular matrix and the structural organization of the nucleus. Proceedings of the National Academy of Sciences of the United States of America, 95(25), 14711–14716.PubMed Lelievre, S. A., Weaver, V. M., Nickerson, J. A., Larabell, C. A., Bhaumik, A., Petersen, O. W., et al. (1998). Tissue phenotype depends on reciprocal interactions between the extracellular matrix and the structural organization of the nucleus. Proceedings of the National Academy of Sciences of the United States of America, 95(25), 14711–14716.PubMed
2.
go back to reference Nelson, C. A., & Bissell, M. J. (2005). Modeling dynamic reciprocity: Engineering three-dimensional culture models of breast architecture, function, and neoplastic transformation. Seminars in Cancer Biology, 15(5), 342–352.PubMed Nelson, C. A., & Bissell, M. J. (2005). Modeling dynamic reciprocity: Engineering three-dimensional culture models of breast architecture, function, and neoplastic transformation. Seminars in Cancer Biology, 15(5), 342–352.PubMed
3.
go back to reference Paszek, M. J., & Weaver, V. M. (2004). The tension mounts: Mechanics meets morphogenesis and malignancy. Journal of Mammary Gland Biology and Neoplasia, 9(4), 325–342.PubMed Paszek, M. J., & Weaver, V. M. (2004). The tension mounts: Mechanics meets morphogenesis and malignancy. Journal of Mammary Gland Biology and Neoplasia, 9(4), 325–342.PubMed
4.
go back to reference Bershadsky, A. D., Balaban, N. Q., & Geiger, B. (2003). Adhesion-dependent cell mechanosensitivity. Annual Review of Cell and Developmental Biology, 19, 677–695.PubMed Bershadsky, A. D., Balaban, N. Q., & Geiger, B. (2003). Adhesion-dependent cell mechanosensitivity. Annual Review of Cell and Developmental Biology, 19, 677–695.PubMed
5.
go back to reference Giancotti, F. G., & Ruoslahti, E. (1999). Transduction — Integrin signaling. Science, 285(5430), 1028–1032.PubMed Giancotti, F. G., & Ruoslahti, E. (1999). Transduction — Integrin signaling. Science, 285(5430), 1028–1032.PubMed
6.
go back to reference Ingber, D. E. (2008). Tensegrity-based mechanosensing from macro to micro. Progress in Biophysics & Molecular Biology, 97(2–3), 163–179. Ingber, D. E. (2008). Tensegrity-based mechanosensing from macro to micro. Progress in Biophysics & Molecular Biology, 97(2–3), 163–179.
7.
go back to reference Janmey, P. A. (1998). The cytoskeleton and cell signaling: Component localization and mechanical coupling. Physiological Reviews, 78(3), 763–781.PubMed Janmey, P. A. (1998). The cytoskeleton and cell signaling: Component localization and mechanical coupling. Physiological Reviews, 78(3), 763–781.PubMed
8.
go back to reference Lele, T. P., & Kumar, S. (2007). Brushes, cables, and anchors: Recent insights into multiscale assembly and mechanics of cellular structural networks. Cell Biochemistry and Biophysics, 47(3), 348–360.PubMed Lele, T. P., & Kumar, S. (2007). Brushes, cables, and anchors: Recent insights into multiscale assembly and mechanics of cellular structural networks. Cell Biochemistry and Biophysics, 47(3), 348–360.PubMed
9.
go back to reference Paszek, M. J., Zahir, N., Johnson, K. R., Lakins, J. N., Rozenberg, G. I., Gefen, A., et al. (2005). Tensional homeostasis and the malignant phenotype. Cancer Cell, 8, 241–254.PubMed Paszek, M. J., Zahir, N., Johnson, K. R., Lakins, J. N., Rozenberg, G. I., Gefen, A., et al. (2005). Tensional homeostasis and the malignant phenotype. Cancer Cell, 8, 241–254.PubMed
10.
go back to reference Wang, N., Butler, J. P., & Ingber, D. E. (1993). Mechanotransduction across the cell surface and through the cytoskeleton. Science, 260(5111), 1124–1127.PubMed Wang, N., Butler, J. P., & Ingber, D. E. (1993). Mechanotransduction across the cell surface and through the cytoskeleton. Science, 260(5111), 1124–1127.PubMed
11.
go back to reference Ingber, D. E. (2003). Mechanobiology and diseases of mechanotransduction. Annals of Medicine, 35(8), 564–577.PubMed Ingber, D. E. (2003). Mechanobiology and diseases of mechanotransduction. Annals of Medicine, 35(8), 564–577.PubMed
12.
go back to reference Farge, E. (2003). Mechanical induction of Twist in the Drosophila foregut/stomodeal primordium. Current Biology, 13(16), 1365–1377.PubMed Farge, E. (2003). Mechanical induction of Twist in the Drosophila foregut/stomodeal primordium. Current Biology, 13(16), 1365–1377.PubMed
13.
go back to reference Supatto, W., Debarre, D., Moulia, B., Brouzes, E., Martin, J. L., Farge, E., et al. (2005). In vivo modulation of morphogenetic movements in Drosophila embryos with femtosecond laser pulses. Proceedings of the National Academy of Sciences of the United States of America, 102(4), 1047–1052.PubMed Supatto, W., Debarre, D., Moulia, B., Brouzes, E., Martin, J. L., Farge, E., et al. (2005). In vivo modulation of morphogenetic movements in Drosophila embryos with femtosecond laser pulses. Proceedings of the National Academy of Sciences of the United States of America, 102(4), 1047–1052.PubMed
14.
go back to reference Wei, L., Roberts, W., Wang, L., Yamada, M., Zhang, S., Zhao, Z., et al. (2001). Rho kinases play an obligatory role in vertebrate embryonic organogenesis. Development, 128(15), 2953–2962.PubMed Wei, L., Roberts, W., Wang, L., Yamada, M., Zhang, S., Zhao, Z., et al. (2001). Rho kinases play an obligatory role in vertebrate embryonic organogenesis. Development, 128(15), 2953–2962.PubMed
15.
go back to reference Ewald, A. J., Brenot, A., Duong, M., Chan, B. S., & Werb, Z. (2008). Collective epithelial migration and cell rearrangements drive mammary branching morphogenesis. Developmental Cell, 14(4), 570–581.PubMed Ewald, A. J., Brenot, A., Duong, M., Chan, B. S., & Werb, Z. (2008). Collective epithelial migration and cell rearrangements drive mammary branching morphogenesis. Developmental Cell, 14(4), 570–581.PubMed
16.
go back to reference Engler, A. J., Sen, S., Sweeney, H. L., & Discher, D. E. (2006). Matrix elasticity directs stem cell lineage specification. Cell, 126(4), 677–689.PubMed Engler, A. J., Sen, S., Sweeney, H. L., & Discher, D. E. (2006). Matrix elasticity directs stem cell lineage specification. Cell, 126(4), 677–689.PubMed
17.
go back to reference Winer, J. P., Janmey, P. A., McCormick, M. E., & Funaki, M. (2009). Bone Marrow-Derived Human Mesenchymal Stem Cells Become Quiescent on Soft Substrates but Remain Responsive to Chemical or Mechanical Stimuli. Tissue Engineering Part A, 15(1), 147–154. Winer, J. P., Janmey, P. A., McCormick, M. E., & Funaki, M. (2009). Bone Marrow-Derived Human Mesenchymal Stem Cells Become Quiescent on Soft Substrates but Remain Responsive to Chemical or Mechanical Stimuli. Tissue Engineering Part A, 15(1), 147–154.
18.
go back to reference Saha, K., Keung, A. J., Irwin, E. F., Li, Y., Little, L., Schaffer, D. V., et al. (2008). Substrate modulus directs neural stem cell behavior. Biophysical Journal, 95(9), 4426–4438. Saha, K., Keung, A. J., Irwin, E. F., Li, Y., Little, L., Schaffer, D. V., et al. (2008). Substrate modulus directs neural stem cell behavior. Biophysical Journal, 95(9), 4426–4438.
19.
go back to reference Kokkinos, M. I., Wafai, R., Wong, M. K., Newgreen, D. F., Thompson, E. W., & Waltham, M. (2007). Vimentin and epithelial-mesenchymal transition in human breast cancer—Observations in vitro and in vivo. Cells Tissues Organs, 185(1–3), 191–203.PubMed Kokkinos, M. I., Wafai, R., Wong, M. K., Newgreen, D. F., Thompson, E. W., & Waltham, M. (2007). Vimentin and epithelial-mesenchymal transition in human breast cancer—Observations in vitro and in vivo. Cells Tissues Organs, 185(1–3), 191–203.PubMed
20.
go back to reference Pagan, R., Martin, I., Alonso, A., Llobera, M., & Vilaro, S. (1996). Vimentin filaments follow the preexisting cytokeratin network during epithelial-mesenchymal transition of cultured neonatal rat hepatocytes. Experimental Cell Research, 222(2), 333–344.PubMed Pagan, R., Martin, I., Alonso, A., Llobera, M., & Vilaro, S. (1996). Vimentin filaments follow the preexisting cytokeratin network during epithelial-mesenchymal transition of cultured neonatal rat hepatocytes. Experimental Cell Research, 222(2), 333–344.PubMed
21.
go back to reference Willipinski-Stapelfeldt, B., Riethdorf, S., Assmann, V., Woelfle, U., Rau, T., Sauter, G., et al. (2005). Changes in cytoskeletal protein composition indicative of an epithelial-mesenchymal transition in human micrometastatic and primary breast carcinoma cells. Clinical Cancer Research, 11(22), 8006–8014.PubMed Willipinski-Stapelfeldt, B., Riethdorf, S., Assmann, V., Woelfle, U., Rau, T., Sauter, G., et al. (2005). Changes in cytoskeletal protein composition indicative of an epithelial-mesenchymal transition in human micrometastatic and primary breast carcinoma cells. Clinical Cancer Research, 11(22), 8006–8014.PubMed
22.
go back to reference Wang, H. B., Dembo, M., & Wang, Y. L. (2000). Substrate flexibility regulates growth and apoptosis of normal but not transformed cells. American Journal of Physiology — Cell Physiology, 279(5), C1345–1350.PubMed Wang, H. B., Dembo, M., & Wang, Y. L. (2000). Substrate flexibility regulates growth and apoptosis of normal but not transformed cells. American Journal of Physiology — Cell Physiology, 279(5), C1345–1350.PubMed
23.
go back to reference Wozniak, M. A., Desai, R., Solski, P. A., Der, C. J., & Keely, P. J. (2003). ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. Journal of Cell Biology, 163(3), 583–595.PubMed Wozniak, M. A., Desai, R., Solski, P. A., Der, C. J., & Keely, P. J. (2003). ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. Journal of Cell Biology, 163(3), 583–595.PubMed
24.
go back to reference Wolf, K., Friedl, P. (2008). Mapping proteolytic cancer cell-extracellular matrix interfaces. Clinical and Expermiental Metastasis, (in press). Wolf, K., Friedl, P. (2008). Mapping proteolytic cancer cell-extracellular matrix interfaces. Clinical and Expermiental Metastasis, (in press).
25.
go back to reference Yamaguchi, H., Wyckoff, J., & Condeelis, J. (2005). Cell migration in tumors. Current Opinion in Cell Biology, 17(5), 559–564.PubMed Yamaguchi, H., Wyckoff, J., & Condeelis, J. (2005). Cell migration in tumors. Current Opinion in Cell Biology, 17(5), 559–564.PubMed
26.
go back to reference Yamaguchi, H., Lorenz, M., Kempiak, S., Sarmiento, C., Coniglio, S., Symons, M., et al. (2005). Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. Journal of Cell Biology, 168(3), 441–452.PubMed Yamaguchi, H., Lorenz, M., Kempiak, S., Sarmiento, C., Coniglio, S., Symons, M., et al. (2005). Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. Journal of Cell Biology, 168(3), 441–452.PubMed
27.
go back to reference Wolf, K., Wu, Y. I., Liu, Y., Geiger, J., Tam, E., Overall, C., et al. (2007). Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nature Cell Biology, 9(8), 893–904.PubMed Wolf, K., Wu, Y. I., Liu, Y., Geiger, J., Tam, E., Overall, C., et al. (2007). Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nature Cell Biology, 9(8), 893–904.PubMed
28.
go back to reference Khaled, W., Reichling, S., Bruhns, O. T., Boese, H., Baumann, M., Monkman, G., et al. (2004). Palpation imaging using a haptic system for virtual reality applications in medicine. Studies in Health Technology and Informatics, 98, 147–153.PubMed Khaled, W., Reichling, S., Bruhns, O. T., Boese, H., Baumann, M., Monkman, G., et al. (2004). Palpation imaging using a haptic system for virtual reality applications in medicine. Studies in Health Technology and Informatics, 98, 147–153.PubMed
29.
go back to reference Khaled, W., Reichling, S., Bruhns, O. T., & Ermert, H. (2006). Ultrasonic strain imaging and reconstructive elastography for biological tissue. Ultrasonics, 44(Suppl 1), e199–202.PubMed Khaled, W., Reichling, S., Bruhns, O. T., & Ermert, H. (2006). Ultrasonic strain imaging and reconstructive elastography for biological tissue. Ultrasonics, 44(Suppl 1), e199–202.PubMed
30.
go back to reference Selbekk, T., Bang, J., & Unsgaard, G. (2005). Strain processing of intraoperative ultrasound images of brain tumours: initial results. Ultrasound in Medicine and Biology, 31(1), 45–51.PubMed Selbekk, T., Bang, J., & Unsgaard, G. (2005). Strain processing of intraoperative ultrasound images of brain tumours: initial results. Ultrasound in Medicine and Biology, 31(1), 45–51.PubMed
31.
go back to reference Unsgaard, G., Rygh, O. M., Selbekk, T., Muller, T. B., Kolstad, F., Lindseth, F., et al. (2006). Intra-operative 3D ultrasound in neurosurgery. Acta Neurochir (Wien), 148(3), 235–253 discussion 253. Unsgaard, G., Rygh, O. M., Selbekk, T., Muller, T. B., Kolstad, F., Lindseth, F., et al. (2006). Intra-operative 3D ultrasound in neurosurgery. Acta Neurochir (Wien), 148(3), 235–253 discussion 253.
32.
go back to reference Croft, D. R., Sahai, E., Mavria, G., Li, S., Tsai, J., Lee, W. M., et al. (2004). Conditional ROCK activation in vivo induces tumor cell dissemination and angiogenesis. Cancer Research, 64(24), 8994–9001.PubMed Croft, D. R., Sahai, E., Mavria, G., Li, S., Tsai, J., Lee, W. M., et al. (2004). Conditional ROCK activation in vivo induces tumor cell dissemination and angiogenesis. Cancer Research, 64(24), 8994–9001.PubMed
33.
go back to reference O’Brien, L. E., Jou, T. S., Pollack, A. L., Zhang, Q., Hansen, S. H., Yurchenco, P., et al. (2001). Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nature Cell Biology, 3(9), 831–838.PubMed O’Brien, L. E., Jou, T. S., Pollack, A. L., Zhang, Q., Hansen, S. H., Yurchenco, P., et al. (2001). Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nature Cell Biology, 3(9), 831–838.PubMed
34.
go back to reference Wang, F., Weaver, V. M., Petersen, O. W., Larabell, C. A., Dedhar, S., Briand, P., et al. (1998). Reciprocal interactions between beta1-integrin and epidermal growth factor receptor in three-dimensional basement membrane breast cultures: a different perspective in epithelial biology. Proceedings of the National Academy of Sciences of the United States of America, 95(25), 14821–14826.PubMed Wang, F., Weaver, V. M., Petersen, O. W., Larabell, C. A., Dedhar, S., Briand, P., et al. (1998). Reciprocal interactions between beta1-integrin and epidermal growth factor receptor in three-dimensional basement membrane breast cultures: a different perspective in epithelial biology. Proceedings of the National Academy of Sciences of the United States of America, 95(25), 14821–14826.PubMed
35.
go back to reference Ingman, W. V., Wyckoff, J., Gouon-Evans, V., Condeelis, J., & Pollard, J. W. (2006). Macrophages promote collagen fibrillogenesis around terminal end buds of the developing mammary gland. Developmental Dynamics, 235(12), 3222–3229.PubMed Ingman, W. V., Wyckoff, J., Gouon-Evans, V., Condeelis, J., & Pollard, J. W. (2006). Macrophages promote collagen fibrillogenesis around terminal end buds of the developing mammary gland. Developmental Dynamics, 235(12), 3222–3229.PubMed
36.
go back to reference Provenzano, P. P., Inman, D. R., Eliceiri, K. W., Knittel, J. G., Yan, L., Rueden, C. T., et al. (2008). Collagen density promotes mammary tumor initiation and progression. BMC Medicine, 6(1), 1–11. Provenzano, P. P., Inman, D. R., Eliceiri, K. W., Knittel, J. G., Yan, L., Rueden, C. T., et al. (2008). Collagen density promotes mammary tumor initiation and progression. BMC Medicine, 6(1), 1–11.
37.
go back to reference Wyckoff, J. B., Pinner, S. E., Gschmeissner, S., Condeelis, J. S., & Sahai, E. (2006). ROCK- and myosin-dependent matrix deformation enables protease-independent tumor-cell invasion in vivo. Current Biology, 16(15), 1515–1523.PubMed Wyckoff, J. B., Pinner, S. E., Gschmeissner, S., Condeelis, J. S., & Sahai, E. (2006). ROCK- and myosin-dependent matrix deformation enables protease-independent tumor-cell invasion in vivo. Current Biology, 16(15), 1515–1523.PubMed
38.
go back to reference Ingber, D. E., Madri, J. A., & Jamieson, J. D. (1981). Role of basal lamina in neoplastic disorganization of tissue architecture. Proceedings of the National Academy of Sciences of the United States of America, 78(6), 3901–3905.PubMed Ingber, D. E., Madri, J. A., & Jamieson, J. D. (1981). Role of basal lamina in neoplastic disorganization of tissue architecture. Proceedings of the National Academy of Sciences of the United States of America, 78(6), 3901–3905.PubMed
39.
go back to reference Black, P. (1998). Management of malignant glioma: role of surgery in relation to multimodality therapy. Journal of Neurovirology, 4(2), 227–236.PubMedCrossRef Black, P. (1998). Management of malignant glioma: role of surgery in relation to multimodality therapy. Journal of Neurovirology, 4(2), 227–236.PubMedCrossRef
40.
go back to reference Schankin, C. J., Ferrari, U., Reinisch, V. M., Birnbaum, T., Goldbrunner, R., & Straube, A. (2007). Characteristics of brain tumour-associated headache. Cephalalgia, 27(8), 904–911.PubMed Schankin, C. J., Ferrari, U., Reinisch, V. M., Birnbaum, T., Goldbrunner, R., & Straube, A. (2007). Characteristics of brain tumour-associated headache. Cephalalgia, 27(8), 904–911.PubMed
41.
go back to reference Watanapa, P., & Williamson, R. C. N. (1992). Surgical Palliation for Pancreatic-Cancer—Developments during the Past 2 Decades. British Journal of Surgery, 79(1), 8–20.PubMed Watanapa, P., & Williamson, R. C. N. (1992). Surgical Palliation for Pancreatic-Cancer—Developments during the Past 2 Decades. British Journal of Surgery, 79(1), 8–20.PubMed
42.
go back to reference Harris, A. L. (2002). Hypoxia—a key regulatory factor in tumour growth. Nature Reviews Cancer, 2(1), 38–47.PubMed Harris, A. L. (2002). Hypoxia—a key regulatory factor in tumour growth. Nature Reviews Cancer, 2(1), 38–47.PubMed
43.
go back to reference Roose, T., Netti, P. A., Munn, L. L., Boucher, Y., & Jain, R. K. (2003). Solid stress generated by spheroid growth estimated using a linear poroelasticity model small star, filled. Microvascular Research, 66(3), 204–212.PubMed Roose, T., Netti, P. A., Munn, L. L., Boucher, Y., & Jain, R. K. (2003). Solid stress generated by spheroid growth estimated using a linear poroelasticity model small star, filled. Microvascular Research, 66(3), 204–212.PubMed
44.
go back to reference Tschumperlin, D. J., Dai, G., Maly, I. V., Kikuchi, T., Laiho, L. H., McVittie, A. K., et al. (2004). Mechanotransduction through growth-factor shedding into the extracellular space. Nature, 429(6987), 83–86.PubMed Tschumperlin, D. J., Dai, G., Maly, I. V., Kikuchi, T., Laiho, L. H., McVittie, A. K., et al. (2004). Mechanotransduction through growth-factor shedding into the extracellular space. Nature, 429(6987), 83–86.PubMed
45.
go back to reference Minchinton, A. I., & Tannock, I. F. (2006). Drug penetration in solid tumours. Nature Reviews Cancer, 6(8), 583–592.PubMed Minchinton, A. I., & Tannock, I. F. (2006). Drug penetration in solid tumours. Nature Reviews Cancer, 6(8), 583–592.PubMed
46.
go back to reference Marshburn, P. B., & Hulka, J. F. (1990). A simple irrigator-aspirator cannula for laparoscopy: the Stewart system. Obstetrics and Gynecology, 75(3 Pt 1), 458–460.PubMed Marshburn, P. B., & Hulka, J. F. (1990). A simple irrigator-aspirator cannula for laparoscopy: the Stewart system. Obstetrics and Gynecology, 75(3 Pt 1), 458–460.PubMed
47.
go back to reference Davies, P. F., Spaan, J. A., & Krams, R. (2005). Shear stress biology of the endothelium. Annals of Biomedical Engineering, 33(12), 1714–1718.PubMed Davies, P. F., Spaan, J. A., & Krams, R. (2005). Shear stress biology of the endothelium. Annals of Biomedical Engineering, 33(12), 1714–1718.PubMed
48.
go back to reference Thamilselvan, V., Craig, D. H., & Basson, M. D. (2007). FAK association with multiple signal proteins mediates pressure-induced colon cancer cell adhesion via a Src-dependent PI3K/Akt pathway. FASEB Journal, 21(8), 1730–1741.PubMed Thamilselvan, V., Craig, D. H., & Basson, M. D. (2007). FAK association with multiple signal proteins mediates pressure-induced colon cancer cell adhesion via a Src-dependent PI3K/Akt pathway. FASEB Journal, 21(8), 1730–1741.PubMed
49.
go back to reference von Sengbusch, A., Gassmann, P., Fisch, K. M., Enns, A., Nicolson, G. L., & Haier, J. (2005). Focal adhesion kinase regulates metastatic adhesion of carcinoma cells within liver sinusoids. American Journal of Pathology, 166(2), 585–596. von Sengbusch, A., Gassmann, P., Fisch, K. M., Enns, A., Nicolson, G. L., & Haier, J. (2005). Focal adhesion kinase regulates metastatic adhesion of carcinoma cells within liver sinusoids. American Journal of Pathology, 166(2), 585–596.
50.
go back to reference Miles, F. L., Pruitt, F. L., van Golen, K. L., & Cooper, C. R. (2008). Stepping out of the flow: capillary extravasation in cancer metastasis. Clinical and Expermiental Metastasis, 25(4), 305–324. Miles, F. L., Pruitt, F. L., van Golen, K. L., & Cooper, C. R. (2008). Stepping out of the flow: capillary extravasation in cancer metastasis. Clinical and Expermiental Metastasis, 25(4), 305–324.
51.
go back to reference Stewart, D. A., Cooper, C. R., & Sikes, R. A. (2004). Changes in extracellular matrix (ECM) and ECM-associated proteins in the metastatic progression of prostate cancer. Reproductive Biology and Endocrinology, 2, 2.PubMed Stewart, D. A., Cooper, C. R., & Sikes, R. A. (2004). Changes in extracellular matrix (ECM) and ECM-associated proteins in the metastatic progression of prostate cancer. Reproductive Biology and Endocrinology, 2, 2.PubMed
52.
go back to reference Heino, J., & Massague, J. (1989). Transforming growth factor-beta switches the pattern of integrins expressed in MG-63 human osteosarcoma cells and causes a selective loss of cell adhesion to laminin. Journal of Biological Chemistry, 264(36), 21806–21811.PubMed Heino, J., & Massague, J. (1989). Transforming growth factor-beta switches the pattern of integrins expressed in MG-63 human osteosarcoma cells and causes a selective loss of cell adhesion to laminin. Journal of Biological Chemistry, 264(36), 21806–21811.PubMed
53.
go back to reference Mierke, C. T., Zitterbart, D. P., Kollmannsberger, P., Raupach, C., Schlotzer-Schrehardt, U., Goecke, T. W., et al. (2008). Breakdown of the endothelial barrier function in tumor cell transmigration. Biophysical Journal, 94(7), 2832–2846.PubMed Mierke, C. T., Zitterbart, D. P., Kollmannsberger, P., Raupach, C., Schlotzer-Schrehardt, U., Goecke, T. W., et al. (2008). Breakdown of the endothelial barrier function in tumor cell transmigration. Biophysical Journal, 94(7), 2832–2846.PubMed
54.
go back to reference Levental, I., Georges, P. C., & Janmey, P. A. (2007). Soft biological materials and their impact on cell function. Soft Matter, 3(3), 299–306. Levental, I., Georges, P. C., & Janmey, P. A. (2007). Soft biological materials and their impact on cell function. Soft Matter, 3(3), 299–306.
55.
go back to reference Janmey, P. A., Georges, P. C., & Hvidt, S. (2007). Basic rheology for biologists. Methods in Cell Biology, 83(1), 3–27.PubMed Janmey, P. A., Georges, P. C., & Hvidt, S. (2007). Basic rheology for biologists. Methods in Cell Biology, 83(1), 3–27.PubMed
56.
go back to reference Chown, M. G., & Kumar, S. (2007). Imaging and manipulating the structural machinery of living cells on the micro- and nanoscale. International Journal of Nanomedicine, 2(3), 333–344.PubMed Chown, M. G., & Kumar, S. (2007). Imaging and manipulating the structural machinery of living cells on the micro- and nanoscale. International Journal of Nanomedicine, 2(3), 333–344.PubMed
57.
go back to reference Dao, M., Lim, C. T., & Suresh, S. (2003). Mechanics of the human red blood cell deformed by optical tweezers. Journal of the Mechanics and Physics of Solids, 51(11–12), 2259–2280. Dao, M., Lim, C. T., & Suresh, S. (2003). Mechanics of the human red blood cell deformed by optical tweezers. Journal of the Mechanics and Physics of Solids, 51(11–12), 2259–2280.
58.
go back to reference Guck, J., Schinkinger, S., Lincoln, B., Wottawah, F., Ebert, S., Romeyke, M., et al. (2005). Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophysical Journal, 88(5), 3689–3698.PubMed Guck, J., Schinkinger, S., Lincoln, B., Wottawah, F., Ebert, S., Romeyke, M., et al. (2005). Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophysical Journal, 88(5), 3689–3698.PubMed
59.
go back to reference Lincoln, B., Wottawah, F., Schinkinger, S., Ebert, S., & Guck, J. (2007). High-throughput rheological measurements with an optical stretcher. Methods in Cell Biology, 83(1), 397–423.PubMed Lincoln, B., Wottawah, F., Schinkinger, S., Ebert, S., & Guck, J. (2007). High-throughput rheological measurements with an optical stretcher. Methods in Cell Biology, 83(1), 397–423.PubMed
60.
go back to reference Trepat, X., Grabulosa, M., Puig, F., Maksym, G. N., Navajas, D., & Farre, R. (2004). Viscoelasticity of human alveolar epithelial cells subjected to stretch. American Journal of Physiology-Lung Cellular and Molecular Physiology, 287(5), L1025–L1034.PubMed Trepat, X., Grabulosa, M., Puig, F., Maksym, G. N., Navajas, D., & Farre, R. (2004). Viscoelasticity of human alveolar epithelial cells subjected to stretch. American Journal of Physiology-Lung Cellular and Molecular Physiology, 287(5), L1025–L1034.PubMed
61.
go back to reference Drury, J. L., & Dembo, M. (2001). Aspiration of human neutrophils: Effects of shear thinning and cortical dissipation. Biophysical Journal, 81(6), 3166–3177.PubMed Drury, J. L., & Dembo, M. (2001). Aspiration of human neutrophils: Effects of shear thinning and cortical dissipation. Biophysical Journal, 81(6), 3166–3177.PubMed
62.
go back to reference Hochmuth, R. M. (2000). Micropipette aspiration of living cells. Journal of Biomechanics, 33(1), 15–22.PubMed Hochmuth, R. M. (2000). Micropipette aspiration of living cells. Journal of Biomechanics, 33(1), 15–22.PubMed
63.
go back to reference Jones, W. R., Ting-Beall, H. P., Lee, G. M., Kelley, S. S., Hochmuth, R. M., & Guilak, F. (1999). Alterations in the Young’s modulus and volumetric properties of chondrocytes isolated from normal and osteoarthritic human cartilage. Journal of Biomechanics, 32(2), 119–127.PubMed Jones, W. R., Ting-Beall, H. P., Lee, G. M., Kelley, S. S., Hochmuth, R. M., & Guilak, F. (1999). Alterations in the Young’s modulus and volumetric properties of chondrocytes isolated from normal and osteoarthritic human cartilage. Journal of Biomechanics, 32(2), 119–127.PubMed
64.
go back to reference Koay, E. J., Shieh, A. C., & Athanasiou, K. A. (2003). Creep indentation of single cells. Journal of Biomechanical Engineering-Transactions of the ASME, 125(3), 334–341. Koay, E. J., Shieh, A. C., & Athanasiou, K. A. (2003). Creep indentation of single cells. Journal of Biomechanical Engineering-Transactions of the ASME, 125(3), 334–341.
65.
go back to reference Trickey, W. R., Baaijens, F. P. T., Laursen, T. A., Alexopoulos, L. G., & Guilak, F. (2006). Determination of the Poisson’s ratio of the cell: recovery properties of chondrocytes after release from complete micropipette aspiration. Journal of Biomechanics, 39(1), 78–87.PubMed Trickey, W. R., Baaijens, F. P. T., Laursen, T. A., Alexopoulos, L. G., & Guilak, F. (2006). Determination of the Poisson’s ratio of the cell: recovery properties of chondrocytes after release from complete micropipette aspiration. Journal of Biomechanics, 39(1), 78–87.PubMed
66.
go back to reference Beningo, K. A., Dembo, M., Kaverina, I., Small, J. V., & Wang, Y. L. (2001). Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. Journal of Cell Biology, 153(4), 881–887.PubMed Beningo, K. A., Dembo, M., Kaverina, I., Small, J. V., & Wang, Y. L. (2001). Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. Journal of Cell Biology, 153(4), 881–887.PubMed
67.
go back to reference Butler, J. P., Tolic-Norrelykke, I. M., Fabry, B., & Fredberg, J. J. (2002). Traction fields, moments, and strain energy that cells exert on their surroundings. American Journal of Physiology-Cell Physiology, 282(3), C595–C605.PubMed Butler, J. P., Tolic-Norrelykke, I. M., Fabry, B., & Fredberg, J. J. (2002). Traction fields, moments, and strain energy that cells exert on their surroundings. American Journal of Physiology-Cell Physiology, 282(3), C595–C605.PubMed
68.
go back to reference Munevar, S., Wang, Y. L., & Dembo, M. (2001). Traction force microscopy of migrating normal and H-ras transformed 3T3 fibroblasts. Biophysical Journal, 80(4), 1744–1757.PubMed Munevar, S., Wang, Y. L., & Dembo, M. (2001). Traction force microscopy of migrating normal and H-ras transformed 3T3 fibroblasts. Biophysical Journal, 80(4), 1744–1757.PubMed
69.
go back to reference Pelham, R. J., & Wang, Y. L. (1999). High resolution detection of mechanical forces exerted by locomoting fibroblasts on the substrate. Molecular Biology of the Cell, 10(4), 935–945.PubMed Pelham, R. J., & Wang, Y. L. (1999). High resolution detection of mechanical forces exerted by locomoting fibroblasts on the substrate. Molecular Biology of the Cell, 10(4), 935–945.PubMed
70.
go back to reference Hansma, H. G., & Hoh, J. H. (1994). Biomolecular Imaging with the Atomic-Force Microscope. Annual Review of Biophysics and Biomolecular Structure, 23(1), 115–139.PubMed Hansma, H. G., & Hoh, J. H. (1994). Biomolecular Imaging with the Atomic-Force Microscope. Annual Review of Biophysics and Biomolecular Structure, 23(1), 115–139.PubMed
71.
go back to reference Kumar, S., & Hoh, J. H. (2001). Probing the machinery of intracellular trafficking with the atomic force microscope. Traffic, 2(11), 746–756.PubMed Kumar, S., & Hoh, J. H. (2001). Probing the machinery of intracellular trafficking with the atomic force microscope. Traffic, 2(11), 746–756.PubMed
72.
go back to reference Lal, R., & John, S. A. (1994). Biological Applications of Atomic-Force Microscopy. American Journal of Physiology, 266(1), C1–&.PubMed Lal, R., & John, S. A. (1994). Biological Applications of Atomic-Force Microscopy. American Journal of Physiology, 266(1), C1–&.PubMed
73.
go back to reference Radmacher, M. (2002). Measuring the elastic properties of living cells by the atomic force microscope. Methods in Cell Biology, 68(1), 67–90.PubMed Radmacher, M. (2002). Measuring the elastic properties of living cells by the atomic force microscope. Methods in Cell Biology, 68(1), 67–90.PubMed
74.
go back to reference An, S. S., Laudadio, R. E., Lai, J., Rogers, R. A., & Fredberg, J. J. (2002). Stiffness changes in cultured airway smooth muscle cells. American Journal of Physiology-Cell Physiology, 283(3), C792–C801.PubMed An, S. S., Laudadio, R. E., Lai, J., Rogers, R. A., & Fredberg, J. J. (2002). Stiffness changes in cultured airway smooth muscle cells. American Journal of Physiology-Cell Physiology, 283(3), C792–C801.PubMed
75.
go back to reference Ingber, D. E., Prusty, D., Sun, Z. Q., Betensky, H., & Wang, N. (1995). Cell shape, cytoskeletal mechanics, and cell cycle control in angiogenesis. Journal of Biomechanics, 28(12), 1471–1484.PubMed Ingber, D. E., Prusty, D., Sun, Z. Q., Betensky, H., & Wang, N. (1995). Cell shape, cytoskeletal mechanics, and cell cycle control in angiogenesis. Journal of Biomechanics, 28(12), 1471–1484.PubMed
76.
go back to reference Maksym, G. N., Fabry, B., Butler, J. P., Navajas, D., Tschumperlin, D. J., Laporte, J. D., et al. (2000). Mechanical properties of cultured human airway smooth muscle cells from 0.05 to 0.4 Hz. Journal of Applied Physiology, 89(4), 1619–1632.PubMed Maksym, G. N., Fabry, B., Butler, J. P., Navajas, D., Tschumperlin, D. J., Laporte, J. D., et al. (2000). Mechanical properties of cultured human airway smooth muscle cells from 0.05 to 0.4 Hz. Journal of Applied Physiology, 89(4), 1619–1632.PubMed
77.
go back to reference Wang, N., Tolic-Norrelykke, I. M., Chen, J. X., Mijailovich, S. M., Butler, J. P., Fredberg, J. J., et al. (2002). Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells. American Journal of Physiology-Cell Physiology, 282(3), C606–C616.PubMed Wang, N., Tolic-Norrelykke, I. M., Chen, J. X., Mijailovich, S. M., Butler, J. P., Fredberg, J. J., et al. (2002). Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells. American Journal of Physiology-Cell Physiology, 282(3), C606–C616.PubMed
78.
go back to reference Berns, M. W., Aist, J., Edwards, J., Strahs, K., Girton, J., McNeill, P., et al. (1981). Laser microsurgery in cell and developmental biology. Science, 213(4507), 505–13.PubMed Berns, M. W., Aist, J., Edwards, J., Strahs, K., Girton, J., McNeill, P., et al. (1981). Laser microsurgery in cell and developmental biology. Science, 213(4507), 505–13.PubMed
79.
go back to reference Heisterkamp, A., Maxwell, I. Z., Mazur, E., Underwood, J. M., Nickerson, J. A., Kumar, S., et al. (2005). Pulse energy dependence of subcellular dissection by femtosecond laser pulses. Optics Express, 13(10), 3690–3696.PubMed Heisterkamp, A., Maxwell, I. Z., Mazur, E., Underwood, J. M., Nickerson, J. A., Kumar, S., et al. (2005). Pulse energy dependence of subcellular dissection by femtosecond laser pulses. Optics Express, 13(10), 3690–3696.PubMed
80.
go back to reference Kumar, S., Maxwell, I. Z., Heisterkamp, A., Polte, T. R., Lele, T. P., Salanga, M., et al. (2006). Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics. Biophysical Journal, 90(10), 3762–3773.PubMed Kumar, S., Maxwell, I. Z., Heisterkamp, A., Polte, T. R., Lele, T. P., Salanga, M., et al. (2006). Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics. Biophysical Journal, 90(10), 3762–3773.PubMed
81.
go back to reference Lele, T. P., Pendse, J., Kumar, S., Salanga, M., Karavitis, J., & Ingber, D. E. (2006). Mechanical forces alter zyxin unbinding kinetics within focal adhesions of living cells. Journal of Cellular Physiology, 207(1), 187–194.PubMed Lele, T. P., Pendse, J., Kumar, S., Salanga, M., Karavitis, J., & Ingber, D. E. (2006). Mechanical forces alter zyxin unbinding kinetics within focal adhesions of living cells. Journal of Cellular Physiology, 207(1), 187–194.PubMed
82.
go back to reference Shen, N., Colvin, M., Genin, F., Huser, T., Cortopassi, G. A., Stearns, T., et al. (2004). Using femtosecond laser subcellular surgery to studycell biology. Biophysical Journal, 86(1), 520A–520A. Shen, N., Colvin, M., Genin, F., Huser, T., Cortopassi, G. A., Stearns, T., et al. (2004). Using femtosecond laser subcellular surgery to studycell biology. Biophysical Journal, 86(1), 520A–520A.
83.
go back to reference du Roure, O., Saez, A., Buguin, A., Austin, R. H., Chavrier, P., Siberzan, P., et al. (2005). Force mapping in epithelial cell migration. Proceedings of the National Academy of Sciences of the United States of America, 102(7), 2390–2395.PubMed du Roure, O., Saez, A., Buguin, A., Austin, R. H., Chavrier, P., Siberzan, P., et al. (2005). Force mapping in epithelial cell migration. Proceedings of the National Academy of Sciences of the United States of America, 102(7), 2390–2395.PubMed
84.
go back to reference Nelson, C. M., Jean, R. P., Tan, J. L., Liu, W. F., Sniadecki, N. J., Spector, A. A., et al. (2005). Emergent patterns of growth controlled by multicellular form and mechanics. Proceedings of the National Academy of Sciences of the United States of America, 102(33), 11594–11599.PubMed Nelson, C. M., Jean, R. P., Tan, J. L., Liu, W. F., Sniadecki, N. J., Spector, A. A., et al. (2005). Emergent patterns of growth controlled by multicellular form and mechanics. Proceedings of the National Academy of Sciences of the United States of America, 102(33), 11594–11599.PubMed
85.
go back to reference Poujade, M., Grasland-Mongrain, E., Hertzog, A., Jouanneau, J., Chavrier, P., Ladoux, B., et al. (2007). Collective migration of an epithelial monolayer in response to a model wound. Proceedings of the National Academy of Sciences of the United States of America, 104(41), 15988–15993.PubMed Poujade, M., Grasland-Mongrain, E., Hertzog, A., Jouanneau, J., Chavrier, P., Ladoux, B., et al. (2007). Collective migration of an epithelial monolayer in response to a model wound. Proceedings of the National Academy of Sciences of the United States of America, 104(41), 15988–15993.PubMed
86.
go back to reference Rabodzey, A., Alcaide, P., Luscinskas, F. W., & Ladoux, B. (2008). Mechanical forces induced by the transendothelial migration of human neutrophils. Biophysical Journal, 95(3), 1428–1438.PubMed Rabodzey, A., Alcaide, P., Luscinskas, F. W., & Ladoux, B. (2008). Mechanical forces induced by the transendothelial migration of human neutrophils. Biophysical Journal, 95(3), 1428–1438.PubMed
87.
go back to reference Sniadecki, N. J., Anguelouch, A., Yang, M. T., Lamb, C. M., Liu, Z., Kirschner, S. B., et al. (2007). Magnetic microposts as an approach to apply forces to living cells. Proceedings of the National Academy of Sciences of the United States of America, 104(37), 14553–14558.PubMed Sniadecki, N. J., Anguelouch, A., Yang, M. T., Lamb, C. M., Liu, Z., Kirschner, S. B., et al. (2007). Magnetic microposts as an approach to apply forces to living cells. Proceedings of the National Academy of Sciences of the United States of America, 104(37), 14553–14558.PubMed
88.
go back to reference Tan, J. L., Tien, J., Pirone, D. M., Gray, D. S., Bhadriraju, K., & Chen, C. S. (2003). Cells lying on a bed of microneedles: An approach to isolate mechanical force. Proceedings of the National Academy of Sciences of the United States of America, 100(4), 1484–1489.PubMed Tan, J. L., Tien, J., Pirone, D. M., Gray, D. S., Bhadriraju, K., & Chen, C. S. (2003). Cells lying on a bed of microneedles: An approach to isolate mechanical force. Proceedings of the National Academy of Sciences of the United States of America, 100(4), 1484–1489.PubMed
89.
go back to reference Bausch, A. R., Ziemann, F., Boulbitch, A. A., Jacobson, K., & Sackmann, E. (1998). Local measurements of viscoelastic parameters of adherent cell surfaces by magnetic bead microrheometry. Biophysical Journal, 75(4), 2038–2049.PubMed Bausch, A. R., Ziemann, F., Boulbitch, A. A., Jacobson, K., & Sackmann, E. (1998). Local measurements of viscoelastic parameters of adherent cell surfaces by magnetic bead microrheometry. Biophysical Journal, 75(4), 2038–2049.PubMed
90.
go back to reference Tseng, Y., Kole, T. P., & Wirtz, D. (2002). Micromechanical mapping of live cells by multiple-particle-tracking microrheology. Biophysical Journal, 83(6), 3162–3176.PubMed Tseng, Y., Kole, T. P., & Wirtz, D. (2002). Micromechanical mapping of live cells by multiple-particle-tracking microrheology. Biophysical Journal, 83(6), 3162–3176.PubMed
91.
go back to reference Valentine, M. T., Perlman, Z. E., Gardel, M. L., Shin, J. H., Matsudaira, P., Mitchison, T. J., et al. (2004). Colloid surface chemistry critically affects multiple particle tracking measurements of biomaterials. Biophysical Journal, 86(6), 4004–4014.PubMed Valentine, M. T., Perlman, Z. E., Gardel, M. L., Shin, J. H., Matsudaira, P., Mitchison, T. J., et al. (2004). Colloid surface chemistry critically affects multiple particle tracking measurements of biomaterials. Biophysical Journal, 86(6), 4004–4014.PubMed
92.
go back to reference Yamada, S., Wirtz, D., & Kuo, S. C. (2000). Mechanics of living cells measured by laser tracking microrheology. Biophysical Journal, 78(4), 1736–1747.PubMed Yamada, S., Wirtz, D., & Kuo, S. C. (2000). Mechanics of living cells measured by laser tracking microrheology. Biophysical Journal, 78(4), 1736–1747.PubMed
93.
go back to reference Yap, B., & Kamm, R. D. (2005). Mechanical deformation of neutrophils into narrow channels induces pseudopod projection and changes in biomechanical properties. Journal of Applied Physiology, 98(5), 1930–1939.PubMed Yap, B., & Kamm, R. D. (2005). Mechanical deformation of neutrophils into narrow channels induces pseudopod projection and changes in biomechanical properties. Journal of Applied Physiology, 98(5), 1930–1939.PubMed
94.
go back to reference Pesen, D., & Hoh, J. H. (2005). Modes of remodeling in the cortical cytoskeleton of vascular endothelial cells. FEBS Letters, 579(2), 473–476.PubMed Pesen, D., & Hoh, J. H. (2005). Modes of remodeling in the cortical cytoskeleton of vascular endothelial cells. FEBS Letters, 579(2), 473–476.PubMed
95.
go back to reference Pesen, D., & Hoh, J. H. (2005). Micromechanical architecture of the endothelial cell cortex. Biophysical Journal, 88(1), 670–679.PubMed Pesen, D., & Hoh, J. H. (2005). Micromechanical architecture of the endothelial cell cortex. Biophysical Journal, 88(1), 670–679.PubMed
96.
go back to reference Oberhauser, A. F., Badilla-Fernandez, C., Carrion-Vasquez, M., & Fernandez, J. M. (2002). The mechanical hierarchies of fibronectin observed with single-molecule AFM. Journal of Molecular Biology, 319, 433–447.PubMed Oberhauser, A. F., Badilla-Fernandez, C., Carrion-Vasquez, M., & Fernandez, J. M. (2002). The mechanical hierarchies of fibronectin observed with single-molecule AFM. Journal of Molecular Biology, 319, 433–447.PubMed
97.
go back to reference Carl, P., Kwok, C. H., Manderson, G., Speicher, D. W., & Discher, D. E. (2001). Forced unfolding modulated by disulfide bonds in the Ig domains of a cell adhesion molecule. Proceedings of the National Academy of Sciences of the United States of America, 98, 1565–1570.PubMed Carl, P., Kwok, C. H., Manderson, G., Speicher, D. W., & Discher, D. E. (2001). Forced unfolding modulated by disulfide bonds in the Ig domains of a cell adhesion molecule. Proceedings of the National Academy of Sciences of the United States of America, 98, 1565–1570.PubMed
98.
go back to reference Rotsch, C., Jacobson, K., & Radmacher, M. (1999). Dimensional and mechanical dynamics of active and stable edges in motile fibroblasts investigated by using atomic force microscopy. Proceedings of the National Academy of Sciences of the United States of America, 96(3), 921–926.PubMed Rotsch, C., Jacobson, K., & Radmacher, M. (1999). Dimensional and mechanical dynamics of active and stable edges in motile fibroblasts investigated by using atomic force microscopy. Proceedings of the National Academy of Sciences of the United States of America, 96(3), 921–926.PubMed
99.
go back to reference A-Hassan, E., Heinz, W. F., Antonik, M. D., D’Costa, N. P., Nageswaran, S., Schoenenberger, C. A., et al. (1998). Relative microelastic mapping of living cells by atomic force microscopy. Biophysical Journal, 74(3), 1564–1578.PubMed A-Hassan, E., Heinz, W. F., Antonik, M. D., D’Costa, N. P., Nageswaran, S., Schoenenberger, C. A., et al. (1998). Relative microelastic mapping of living cells by atomic force microscopy. Biophysical Journal, 74(3), 1564–1578.PubMed
100.
go back to reference Charras, G. T., & Horton, M. A. (2002). Single cell mechanotransduction and its modulation analyzed by atomic force microscope indentation. Biophysical Journal, 82(6), 2970–2981.PubMed Charras, G. T., & Horton, M. A. (2002). Single cell mechanotransduction and its modulation analyzed by atomic force microscope indentation. Biophysical Journal, 82(6), 2970–2981.PubMed
101.
go back to reference Parekh, S. H., Chaudhuri, O., Theriot, J. A., & Fletcher, D. A. (2005). Loading history determines the velocity of actin-network growth. Nature Cell Biology, 7(12), 1219–1223.PubMed Parekh, S. H., Chaudhuri, O., Theriot, J. A., & Fletcher, D. A. (2005). Loading history determines the velocity of actin-network growth. Nature Cell Biology, 7(12), 1219–1223.PubMed
102.
go back to reference Chaudhuri, O., Parekh, S. H., & Fletcher, D. A. (2007). Reversible stress softening of actin networks. Nature, 445(7125), 295–298.PubMed Chaudhuri, O., Parekh, S. H., & Fletcher, D. A. (2007). Reversible stress softening of actin networks. Nature, 445(7125), 295–298.PubMed
103.
go back to reference Prass, M., Jacobson, K., Mogilner, A., & Radmacher, M. (2006). Direct measurement of the lamellipodial protrusive force in a migrating cell. Journal of Cell Biology, 174(6), 767–772.PubMed Prass, M., Jacobson, K., Mogilner, A., & Radmacher, M. (2006). Direct measurement of the lamellipodial protrusive force in a migrating cell. Journal of Cell Biology, 174(6), 767–772.PubMed
104.
go back to reference Lam, W. A., Rosenbluth, M. J., & Fletcher, D. A. (2008). Increased leukaemia cell stiffness is associated with symptoms of leucostasis in paediatric acute lymphoblastic leukaemia. British Journal of Haematology, 142(3), 497–501.PubMed Lam, W. A., Rosenbluth, M. J., & Fletcher, D. A. (2008). Increased leukaemia cell stiffness is associated with symptoms of leucostasis in paediatric acute lymphoblastic leukaemia. British Journal of Haematology, 142(3), 497–501.PubMed
105.
go back to reference Lam, W. A., Rosenbluth, M. J., & Fletcher, D. A. (2007). Chemotherapy exposure increases leukemia cell stiffness. Blood, 109(8), 3505–3508.PubMed Lam, W. A., Rosenbluth, M. J., & Fletcher, D. A. (2007). Chemotherapy exposure increases leukemia cell stiffness. Blood, 109(8), 3505–3508.PubMed
106.
go back to reference Rosenbluth, M. J., Lam, W. A., & Fletcher, D. A. (2006). Force microscopy of nonadherent cells: A comparison of leukemia cell deformability. Biophysical Journal, 90(8), 2994–3003.PubMed Rosenbluth, M. J., Lam, W. A., & Fletcher, D. A. (2006). Force microscopy of nonadherent cells: A comparison of leukemia cell deformability. Biophysical Journal, 90(8), 2994–3003.PubMed
107.
go back to reference Strahs, K. R., Burt, J. M., & Berns, M. W. (1978). Contractility changes in cultured cardiac cells following laser microirradiation of myofibrils and the cell surface. Experimental Cell Research, 113(1), 75–83.PubMed Strahs, K. R., Burt, J. M., & Berns, M. W. (1978). Contractility changes in cultured cardiac cells following laser microirradiation of myofibrils and the cell surface. Experimental Cell Research, 113(1), 75–83.PubMed
108.
go back to reference Strahs, K. R., & Berns, M. W. (1979). Laser microirradiation of stress fibers and intermediate filaments in non-muscle cells from cultured rat heart. Experimental Cell Research, 119(1), 31–45.PubMed Strahs, K. R., & Berns, M. W. (1979). Laser microirradiation of stress fibers and intermediate filaments in non-muscle cells from cultured rat heart. Experimental Cell Research, 119(1), 31–45.PubMed
109.
go back to reference Koonce, M. P., Strahs, K. R., & Berns, M. W. (1982). Repair of laser-severed stress fibers in myocardial non-muscle cells. Experimental Cell Research, 141(2), 375–384.PubMed Koonce, M. P., Strahs, K. R., & Berns, M. W. (1982). Repair of laser-severed stress fibers in myocardial non-muscle cells. Experimental Cell Research, 141(2), 375–384.PubMed
110.
go back to reference Burt, J. M., Strahs, K. R., & Berns, M. W. (1979). Correlation of cell surface alterations with contractile response in laser microbeam irradiated myocardial cells. A scanning electron microscope study. Experimental Cell Research, 118(2), 341–351.PubMed Burt, J. M., Strahs, K. R., & Berns, M. W. (1979). Correlation of cell surface alterations with contractile response in laser microbeam irradiated myocardial cells. A scanning electron microscope study. Experimental Cell Research, 118(2), 341–351.PubMed
111.
go back to reference Botvinick, E. L., Venugopalan, V., Shah, J. V., Liaw, L. H., & Berns, M. W. (2004). Controlled ablation of microtubules using a picosecond laser. Biophysical Journal, 87(6), 4203–4212.PubMed Botvinick, E. L., Venugopalan, V., Shah, J. V., Liaw, L. H., & Berns, M. W. (2004). Controlled ablation of microtubules using a picosecond laser. Biophysical Journal, 87(6), 4203–4212.PubMed
112.
go back to reference Ingber, D. E. (2002). Mechanical signalling and the cellular response to extracellular matrix in angiogenesis and cardiovascular physiology. Circulation Research, 91(10), 877–887.PubMed Ingber, D. E. (2002). Mechanical signalling and the cellular response to extracellular matrix in angiogenesis and cardiovascular physiology. Circulation Research, 91(10), 877–887.PubMed
113.
go back to reference Assoian, R. K., & Klein, E. A. (2008). Growth control by intracellular tension and extracellular stiffness. Trends in Cell Biology, 18(7), 347–352.PubMed Assoian, R. K., & Klein, E. A. (2008). Growth control by intracellular tension and extracellular stiffness. Trends in Cell Biology, 18(7), 347–352.PubMed
114.
go back to reference Burridge, K., & ChrzanowskaWodnicka, M. (1996). Focal adhesions, contractility, and signaling. Annual Review of Cell and Developmental Biology, 12, 463–518.PubMed Burridge, K., & ChrzanowskaWodnicka, M. (1996). Focal adhesions, contractility, and signaling. Annual Review of Cell and Developmental Biology, 12, 463–518.PubMed
115.
go back to reference Etienne-Manneville, S., & Hall, A. (2002). Rho GTPases in cell biology. Nature, 420(6916), 629–635.PubMed Etienne-Manneville, S., & Hall, A. (2002). Rho GTPases in cell biology. Nature, 420(6916), 629–635.PubMed
116.
go back to reference Hotulainen, P., & Lappalainen, P. (2006). Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. Journal of Cell Biology, 173(3), 383–394.PubMed Hotulainen, P., & Lappalainen, P. (2006). Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. Journal of Cell Biology, 173(3), 383–394.PubMed
117.
go back to reference Sipkema, P., van der Linden, P. J. W., Westerhof, N., & Yin, F. C. P. (2003). Effect of cyclic axial stretch of rat arteries on endothelial cytoskeletal morphology and vascular reactivity. Journal of Biomechanics, 36(5), 653–659.PubMed Sipkema, P., van der Linden, P. J. W., Westerhof, N., & Yin, F. C. P. (2003). Effect of cyclic axial stretch of rat arteries on endothelial cytoskeletal morphology and vascular reactivity. Journal of Biomechanics, 36(5), 653–659.PubMed
118.
go back to reference Hayes, A. J., Benjamin, M., & Ralphs, J. R. (1999). Role of actin stress fibres in the development of the intervertebral disc: Cytoskeletal control of extracellular matrix assembly. Developmental Dynamics, 215(3), 179–189.PubMed Hayes, A. J., Benjamin, M., & Ralphs, J. R. (1999). Role of actin stress fibres in the development of the intervertebral disc: Cytoskeletal control of extracellular matrix assembly. Developmental Dynamics, 215(3), 179–189.PubMed
119.
go back to reference Elkin, B. S., Azeloglu, E. U., Costa, K. D., & Morrison, B. (2007). Mechanical heterogeneity of the rat hippocampus measured by atomic force microscope indentation. Journal of Neurotrauma, 24(5), 812–822.PubMed Elkin, B. S., Azeloglu, E. U., Costa, K. D., & Morrison, B. (2007). Mechanical heterogeneity of the rat hippocampus measured by atomic force microscope indentation. Journal of Neurotrauma, 24(5), 812–822.PubMed
120.
go back to reference Cavey, M., Rauzi, M., Lenne, P. F., & Lecuit, T. (2008). A two-tiered mechanism for stabilization and immobilization of E-cadherin. Nature, 453(7196), 751–U2.PubMed Cavey, M., Rauzi, M., Lenne, P. F., & Lecuit, T. (2008). A two-tiered mechanism for stabilization and immobilization of E-cadherin. Nature, 453(7196), 751–U2.PubMed
121.
go back to reference Daniels, B. R., Masi, B. C., & Wirtz, D. (2006). Probing single-cell micromechanics in vivo: The microrheology of C-elegans developing embryos. Biophysical Journal, 90(12), 4712–4719.PubMed Daniels, B. R., Masi, B. C., & Wirtz, D. (2006). Probing single-cell micromechanics in vivo: The microrheology of C-elegans developing embryos. Biophysical Journal, 90(12), 4712–4719.PubMed
122.
go back to reference Panorchan, P., Lee, J. S. H., Kole, T. P., Tseng, Y., & Wirtz, D. (2006). Microrheology and ROCK signaling of human endothelial cells embedded in a 3D matrix. Biophysical Journal, 91(9), 3499–3507.PubMed Panorchan, P., Lee, J. S. H., Kole, T. P., Tseng, Y., & Wirtz, D. (2006). Microrheology and ROCK signaling of human endothelial cells embedded in a 3D matrix. Biophysical Journal, 91(9), 3499–3507.PubMed
123.
go back to reference Bloom, R. J., George, J. P., Celedon, A., Sun, S. X., & Wirtz, D. (2008). Mapping local matrix remodeling induced by a migrating tumor cell using 3-D multiple-particle tracking. Biophysical Journal, 95(8), 4077–4088. Bloom, R. J., George, J. P., Celedon, A., Sun, S. X., & Wirtz, D. (2008). Mapping local matrix remodeling induced by a migrating tumor cell using 3-D multiple-particle tracking. Biophysical Journal, 95(8), 4077–4088.
124.
go back to reference Roy, P., Petroll, W. M., Cavanagh, H. D., & Jester, J. V. (1999). Exertion of tractional force requires the coordinated up-regulation of cell contractility and adhesion. Cell Motility and the Cytoskeleton, 43(1), 23–34.PubMed Roy, P., Petroll, W. M., Cavanagh, H. D., & Jester, J. V. (1999). Exertion of tractional force requires the coordinated up-regulation of cell contractility and adhesion. Cell Motility and the Cytoskeleton, 43(1), 23–34.PubMed
125.
go back to reference Petroll, W. M., Ma, L., & Jester, J. V. (2003). Direct correlation of collagen matrix deformation with focal adhesion dynamics in living corneal fibroblasts. Journal of Cell Science, 116(8), 1481–1491.PubMed Petroll, W. M., Ma, L., & Jester, J. V. (2003). Direct correlation of collagen matrix deformation with focal adhesion dynamics in living corneal fibroblasts. Journal of Cell Science, 116(8), 1481–1491.PubMed
126.
go back to reference Vanni, S., Lagerholm, B. C., Otey, C., Taylor, D. L., & Lanni, F. (2003). Internet-Based image analysis quantifies contractile behavior of individual fibroblasts inside model tissue. Biophysical Journal, 84(4), 2715–2727.PubMed Vanni, S., Lagerholm, B. C., Otey, C., Taylor, D. L., & Lanni, F. (2003). Internet-Based image analysis quantifies contractile behavior of individual fibroblasts inside model tissue. Biophysical Journal, 84(4), 2715–2727.PubMed
127.
go back to reference Vega, F. M., & Ridley, A. J. (2008). Rho GTPases in cancer cell biology. FEBS Letters, 582(14), 2093–2101.PubMed Vega, F. M., & Ridley, A. J. (2008). Rho GTPases in cancer cell biology. FEBS Letters, 582(14), 2093–2101.PubMed
128.
go back to reference Raftopoulou, M., & Hall, A. (2004). Cell migration: Rho GTPases lead the way. Developmental Biology, 265(1), 23–32.PubMed Raftopoulou, M., & Hall, A. (2004). Cell migration: Rho GTPases lead the way. Developmental Biology, 265(1), 23–32.PubMed
129.
go back to reference Friedl, P., & Wolf, K. (2003). Tumour-cell invasion and migration: Diversity and escape mechanisms. Nature Reviews Cancer, 3(5), 362–374.PubMed Friedl, P., & Wolf, K. (2003). Tumour-cell invasion and migration: Diversity and escape mechanisms. Nature Reviews Cancer, 3(5), 362–374.PubMed
130.
go back to reference Lozano, E., Betson, M., & Braga, V. M. M. (2003). Tumor progression: small GTPases and loss of cell-cell adhesion. Bioessays, 25(5), 452–463.PubMed Lozano, E., Betson, M., & Braga, V. M. M. (2003). Tumor progression: small GTPases and loss of cell-cell adhesion. Bioessays, 25(5), 452–463.PubMed
131.
go back to reference Ying, H., Biroc, S. L., Li, W. W., Alicke, B., Xuan, J. A., Pagila, R., et al. (2006). The Rho kinase inhibitor fasudil inhibits tumor progression in human and rat tumor models. Molecular Cancer Therapeutics, 5(9), 2158–2164.PubMed Ying, H., Biroc, S. L., Li, W. W., Alicke, B., Xuan, J. A., Pagila, R., et al. (2006). The Rho kinase inhibitor fasudil inhibits tumor progression in human and rat tumor models. Molecular Cancer Therapeutics, 5(9), 2158–2164.PubMed
132.
go back to reference Bershadsky, A., Kozlov, M., & Geiger, B. (2006). Adhesion-mediated mechanosensitivity: a time to experiment, and a time to theorize. Current Opinion in Cell Biology, 18(5), 472–481.PubMed Bershadsky, A., Kozlov, M., & Geiger, B. (2006). Adhesion-mediated mechanosensitivity: a time to experiment, and a time to theorize. Current Opinion in Cell Biology, 18(5), 472–481.PubMed
133.
go back to reference Schlaepfer, D. D., Hanks, S. K., Hunter, T., & Vandergeer, P. (1994). Integrin-Mediated Signal-Transduction Linked to Ras Pathway by Grb2 Binding to Focal Adhesion Kinase. Nature, 372(6508), 786–791.PubMed Schlaepfer, D. D., Hanks, S. K., Hunter, T., & Vandergeer, P. (1994). Integrin-Mediated Signal-Transduction Linked to Ras Pathway by Grb2 Binding to Focal Adhesion Kinase. Nature, 372(6508), 786–791.PubMed
134.
go back to reference Ridley, A. J., & Hall, A. (1992). The Small Gtp-Binding Protein Rho Regulates the Assembly of Focal Adhesions and Actin Stress Fibers in Response to Growth-Factors. Cell, 70(3), 389–399.PubMed Ridley, A. J., & Hall, A. (1992). The Small Gtp-Binding Protein Rho Regulates the Assembly of Focal Adhesions and Actin Stress Fibers in Response to Growth-Factors. Cell, 70(3), 389–399.PubMed
135.
go back to reference Sechi, A. S., & Wehland, J. (2000). The actin cytoskeleton and plasma membrane connection: PtdIns(4,5)P-2 influences cytoskeletal protein activity at the plasma membrane. Journal of Cell Science, 113(21), 3685–3695.PubMed Sechi, A. S., & Wehland, J. (2000). The actin cytoskeleton and plasma membrane connection: PtdIns(4,5)P-2 influences cytoskeletal protein activity at the plasma membrane. Journal of Cell Science, 113(21), 3685–3695.PubMed
136.
go back to reference Gilmore, A. P., & Burridge, K. (1996). Regulation of vinculin binding to talin and actin by phosphatidyl-inositol-4-5-bisphosphate. Nature, 381(6582), 531–535.PubMed Gilmore, A. P., & Burridge, K. (1996). Regulation of vinculin binding to talin and actin by phosphatidyl-inositol-4-5-bisphosphate. Nature, 381(6582), 531–535.PubMed
137.
go back to reference Schwartz, M. A., Schaller, M. D., & Ginsberg, M. H. (1995). Integrins: Emerging paradigms of signal transduction. Annual Review of Cell and Developmental Biology, 11, 549–599.PubMed Schwartz, M. A., Schaller, M. D., & Ginsberg, M. H. (1995). Integrins: Emerging paradigms of signal transduction. Annual Review of Cell and Developmental Biology, 11, 549–599.PubMed
138.
go back to reference Tilghman, R. W., & Parsons, J. T. (2008). Focal adhesion kinase as a regulator of cell tension in the progression of cancer. Seminars in Cancer Biology, 18(1), 45–52.PubMed Tilghman, R. W., & Parsons, J. T. (2008). Focal adhesion kinase as a regulator of cell tension in the progression of cancer. Seminars in Cancer Biology, 18(1), 45–52.PubMed
139.
go back to reference Gabarra-Niecko, V., Schaller, M. D., & Dunty, J. M. (2003). FAK regulates biological processes important for the pathogenesis of cancer. Cancer and Metastasis Reviews, 22(4), 359–374.PubMed Gabarra-Niecko, V., Schaller, M. D., & Dunty, J. M. (2003). FAK regulates biological processes important for the pathogenesis of cancer. Cancer and Metastasis Reviews, 22(4), 359–374.PubMed
140.
go back to reference Mitra, S. K., Hanson, D. A., & Schlaepfer, D. D. (2005). Focal adhesion kinase: In command and control of cell motility. Nature Reviews Molecular Cell Biology, 6(1), 56–68.PubMed Mitra, S. K., Hanson, D. A., & Schlaepfer, D. D. (2005). Focal adhesion kinase: In command and control of cell motility. Nature Reviews Molecular Cell Biology, 6(1), 56–68.PubMed
141.
go back to reference Parsons, J. T. (2003). Focal adhesion kinase: the first ten years. Journal of Cell Science, 116(8), 1409–1416.PubMed Parsons, J. T. (2003). Focal adhesion kinase: the first ten years. Journal of Cell Science, 116(8), 1409–1416.PubMed
142.
go back to reference Schlaepfer, D. D., Mitra, S. K., & Ilic, D. (2004). Control of motile and invasive cell phenotypes by focal adhesion kinase. Biochimica et Biophysica Acta-Molecular Cell Research, 1692(2–3), 77–102. Schlaepfer, D. D., Mitra, S. K., & Ilic, D. (2004). Control of motile and invasive cell phenotypes by focal adhesion kinase. Biochimica et Biophysica Acta-Molecular Cell Research, 1692(2–3), 77–102.
143.
go back to reference Liu, T. J., LaFortune, T., Honda, T., Ohmori, O., Hatakeyama, S., Meyer, T., et al. (2007). Inhibition of both focal adhesion kinase and insulin-like growth factor-I receptor kinase suppresses glioma proliferation in vitro and in vivo. Molecular Cancer Therapeutics, 6(4), 1357–1367.PubMed Liu, T. J., LaFortune, T., Honda, T., Ohmori, O., Hatakeyama, S., Meyer, T., et al. (2007). Inhibition of both focal adhesion kinase and insulin-like growth factor-I receptor kinase suppresses glioma proliferation in vitro and in vivo. Molecular Cancer Therapeutics, 6(4), 1357–1367.PubMed
144.
go back to reference Shen, T. L., & Guan, J. L. (2001). Differential regulation of cell migration and cell cycle progression by FAK complexes with Src, PI3K, Grb7 and Grb2 in focal contacts. FEBS Letters, 499(1–2), 176–181.PubMed Shen, T. L., & Guan, J. L. (2001). Differential regulation of cell migration and cell cycle progression by FAK complexes with Src, PI3K, Grb7 and Grb2 in focal contacts. FEBS Letters, 499(1–2), 176–181.PubMed
145.
go back to reference Izaguirre, G., Aguirre, L., Hu, Y. P., Lee, H. Y., Schlaepfer, D. D., Aneskievich, B. J., et al. (2001). The cytoskeletal/non-muscle isoform of alpha-actinin is phosphorylated on its actin-binding domain by the focal adhesion kinase. Journal of Biological Chemistry, 276(31), 28676–28685.PubMed Izaguirre, G., Aguirre, L., Hu, Y. P., Lee, H. Y., Schlaepfer, D. D., Aneskievich, B. J., et al. (2001). The cytoskeletal/non-muscle isoform of alpha-actinin is phosphorylated on its actin-binding domain by the focal adhesion kinase. Journal of Biological Chemistry, 276(31), 28676–28685.PubMed
146.
go back to reference Wang, H. B., Dembo, M., Hanks, S. K., & Wang, Y. L. (2001). Focal adhesion kinase is involved in mechanosensing during fibroblast migration. Proceedings of the National Academy of Sciences of the United States of America, 98(20), 11295–11300.PubMed Wang, H. B., Dembo, M., Hanks, S. K., & Wang, Y. L. (2001). Focal adhesion kinase is involved in mechanosensing during fibroblast migration. Proceedings of the National Academy of Sciences of the United States of America, 98(20), 11295–11300.PubMed
147.
go back to reference Hamasaki, K., Mimura, T., Furuya, H., Morino, N., Yamazaki, T., Komuro, I., et al. (1995). Stretching Mesangial Cells Stimulates Tyrosine Phosphorylation of Focal Adhesion Kinase Pp125(Fak). Biochemical and Biophysical Research Communications, 212(2), 544–549.PubMed Hamasaki, K., Mimura, T., Furuya, H., Morino, N., Yamazaki, T., Komuro, I., et al. (1995). Stretching Mesangial Cells Stimulates Tyrosine Phosphorylation of Focal Adhesion Kinase Pp125(Fak). Biochemical and Biophysical Research Communications, 212(2), 544–549.PubMed
148.
go back to reference Mofrad, M. R., Golji, J., Abdul Rahim, N. A., & Kamm, R. D. (2004). Force-induced unfolding of the focal adhesion targeting domain and the influence of paxillin binding. Mechanics and Chemistry of Biosystems, 1(4), 253–65.PubMed Mofrad, M. R., Golji, J., Abdul Rahim, N. A., & Kamm, R. D. (2004). Force-induced unfolding of the focal adhesion targeting domain and the influence of paxillin binding. Mechanics and Chemistry of Biosystems, 1(4), 253–65.PubMed
149.
go back to reference Johnson, K. R., Leight, J. L., & Weaver, V. M. (2007). Demystifying the effects of a three-dimensional microenvironment in tissue morphogenesis. Methods in Cell Biology, 83(1), 547–583.PubMed Johnson, K. R., Leight, J. L., & Weaver, V. M. (2007). Demystifying the effects of a three-dimensional microenvironment in tissue morphogenesis. Methods in Cell Biology, 83(1), 547–583.PubMed
Metadata
Title
Mechanics, malignancy, and metastasis: The force journey of a tumor cell
Authors
Sanjay Kumar
Valerie M. Weaver
Publication date
01-06-2009
Publisher
Springer US
Published in
Cancer and Metastasis Reviews / Issue 1-2/2009
Print ISSN: 0167-7659
Electronic ISSN: 1573-7233
DOI
https://doi.org/10.1007/s10555-008-9173-4

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