Mechanisms of Disease:The Biophysical Interpretation of the ECM Affects Physiological and Pathophysiological Cellular Behavior

Zusammenfassung

Physiologische und pathophysiologische Migration während der Organentwicklung oder der systemischen Dissemination von Tumorzellen bedarf einer hochkomplexen Regulation der Interaktion mit der extrazellulären Matrix. Sowohl die Wahrnehmung der physikalischen Eigenschaften der Matrix als auch der Kräfte, die auf die individuelle Zelle einwirken, sind Grundvoraussetzung für produktive Migration. Dieser Übersichtsartikel fasst aktuelle Konzepte der Transmission physikalischer Reize in biochemische Signale in nichtneuronalen Zellen zusammen und analysiert die Bedeutung der Regulation von Affinitätsmodulation und Umsatzraten für die Formation und Funktionalität von Matrixinteraktionen unter besonderer Berücksichtigung onkogener Signalwege wie Src-Familien-Kinasen und der „focal adhesion kinase”.

Abstract

Physiological and pathophysiological migration during the development and systemic spread of tumor cells requires a highly regulated interaction with the extracellular matrix. Sensing of the physical properties of the matrix as well as of forces exerted by the cell or acting on a cell is a prerequisite for productive migration. This review focuses on current concepts of the transmission of a physical stimulus into a biochemical signal in non-neuronal cells. Moreover, we summarize the current concepts on the regulation of affinity-modulation and regulation of protein-turnover for the formation and functionality of adhesion sites with special emphasis on the role of oncogenic signal transduction pathways such as Src family kinases and focal adhesion kinase.

Schlüsselwörter

Migration - Metastasierung - Mechanotransduktion

Key words

Migration - metastatic disease - mechanotransduction

References

• 1 Bissell M J, Labarge M A. Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment?.  Cancer Cell. 2005;  43 17-23
• 2 Illmensee K, Mintz B. Totipotency and normal differentiation of single teratocarcinoma cells cloned by injection into blastocysts.  Proc Natl Acad Sci USA. 1976;  43 549-553
• 3 Mintz B, Illmensee K. Normal genetically mosaic mice produced from malignant teratocarcinoma cells.  Proc Natl Acad Sci USA. 1975;  43 3585-3589
• 4 Hochedlinger K, Blelloch R, Brennan C. et al . Reprogramming of a melanoma genome by nuclear transplantation.  Genes Dev. 2004;  43 1875-1885
• 5 Blelloch R H, Hochedlinger K, Yamada Y. et al . Nuclear cloning of embryonal carcinoma cells.  Proc Natl Acad Sci USA. 2004;  43 13 985-13 990
• 6 Giancotti F G, Ruoslahti E. Integrin signaling.  Science. 1999;  43 1028-1032
• 7 Thiery J P, Chopin D. Epithelial cell plasticity in development and tumor progression.  Cancer Metastasis Rev. 1999;  43 31-42
• 8 Kassis J, Lauffenburger D A, Turner T. et al . Tumor invasion as dysregulated cell motility.  Semin Cancer Biol. 2001;  43 105-117
• 9 Geiger B, Bershadsky A. Exploring the neighborhood: adhesion-coupled cell mechanosensors.  Cell. 2002;  43 139-142
• 10 Geiger B, Bershadsky A, Pankov R. et al . Transmembrane crosstalk between the extracellular matrix - cytoskeleton crosstalk.  Nat Rev Mol Cell Biol. 2001;  43 793-805
• 11 Katz B Z, Zamir E, Bershadsky A. et al . Physical state of the extracellular matrix regulates the structure and molecular composition of cell-matrix adhesions.  Mol Biol Cell. 2000;  43 1047-1060
• 12 Sheetz M P, Felsenfeld D, Galbraith C G. et al . Cell migration as a five-step cycle.  Biochem Soc Symp. 1999;  43 233-243
• 13 Pelham R J Jr, Wang Y L. Cell locomotion and focal adhesions are regulated by the mechanical properties of the substrate.  Biol Bull. 1998;  43 348-349, discussion 349 - 350
• 14 Lo C M, Wang H B, Dembo M. et al . Cell movement is guided by the rigidity of the substrate.  Biophys J. 2000;  43 144-152
• 15 Choquet D, Felsenfeld D P, Sheetz M P. Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages.  Cell. 1997;  43 39-48
• 16 Tamada M, Sheetz M P, Sawada Y. Activation of a signaling cascade by cytoskeleton stretch.  Dev Cell. 2004;  43 709-718
• 17 Varmus H, Hirai H, Morgan D. et al . Function, location, and regulation of the src protein-tyrosine kinase.  Princess Takamatsu Symp. 1989;  43 63-70
• 18 Han B, Bai X H, Lodyga M. et al . Conversion of mechanical force into biochemical signaling.  J Biol Chem. 2004;  43 54 793-54 801
• 19 von Wichert G, Jiang G, Kostic A. et al . RPTP-alpha acts as a transducer of mechanical force on alphav/beta3-integrin-cytoskeleton linkages.  J Cell Biol. 2003;  43 143-153
• 20 Hall A. Rho GTPases and the actin cytoskeleton.  Science. 1998;  43 509-514
• 21 Hotchin N A, Hall A. The assembly of integrin adhesion complexes requires both extracellular matrix and intracellular rho/rac GTPases.  J Cell Biol. 1995;  43 1857-1865
• 22 Clark E A, King W G, Brugge J S. et al . Integrin-mediated signals regulated by members of the rho family of GTPases.  J Cell Biol. 1998;  43 573-586
• 23 Ridley A J, Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors.  Cell. 1992;  43 389-399
• 24 Chrzanowska-Wodnicka M, Burridge K. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions.  J Cell Biol. 1996;  43 1403-1415
• 25 Amano M, Chihara K, Kimura K. et al . Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase.  Science. 1997;  43 1308-1311
• 26 Amano M, Ito M, Kimura K. et al . Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase).  J Biol Chem. 1996;  43 20 246-20 249
• 27 Kawano Y, Fukata Y, Oshiro N. et al . Phosphorylation of myosin-binding subunit (MBS) of myosin phosphatase by Rho-kinase in vivo.  J Cell Biol. 1999;  43 1023-1038
• 28 Burridge K, Chrzanowska-Wodnicka M. Focal adhesions, contractility, and signaling.  Annu Rev Cell Dev Biol. 1996;  43 463-518
• 29 Helfman D M, Levy E T, Berthier C. et al . Caldesmon inhibits nonmuscle cell contractility and interferes with the formation of focal adhesions.  Mol Biol Cell. 1999;  43 3097-3112
• 30 Coussen F, Choquet D, Sheetz M P. et al . Trimers of the fibronectin cell adhesion domain localize to actin filament bundles and undergo rearward translocation.  J Cell Sci. 2002;  43 2581-2590
• 31 Felsenfeld D P, Choquet D, Sheetz M P. Ligand binding regulates the directed movement of beta1 integrins on fibroblasts.  Nature. 1996;  43 438-440
• 32 Jiang G, Giannone G, Critchley D R. et al . Two-piconewton slip bond between fibronectin and the cytoskeleton depends on talin.  Nature. 2003;  43 334-337
• 33 Giannone G, Jiang G, Sutton D H. et al . Talin1 is critical for force-dependent reinforcement of initial integrin-cytoskeleton bonds but not tyrosine kinase activation.  J Cell Biol. 2003;  43 409-419
• 34 Zeng L, Si X, Yu W P. et al . PTP alpha regulates integrin-stimulated FAK autophosphorylation and cytoskeletal rearrangement in cell spreading and migration.  J Cell Biol. 2003;  43 137-146
• 35 Volberg T, Romer L, Zamir E. et al . pp60 (c-src) and related tyrosine kinases: a role in the assembly and reorganization of matrix adhesions.  J Cell Sci. 2001;  43 2279-2289
• 36 Wang Y, Botvinick E L, Zhao Y. et al . Visualizing the mechanical activation of Src.  Nature. 2005;  43 1040-1045
• 37 Bokel C, Brown N H. Integrins in development: moving on, responding to, and sticking to the extracellular matrix.  Dev Cell. 2002;  43 311-321
• 38 Pantaloni D, Le Clainche C, Carlier M F. Mechanism of actin-based motility.  Science. 2001;  43 1502-1506
• 39 Pollard T D, Borisy G G. Cellular motility driven by assembly and disassembly of actin filaments.  Cell. 2003;  43 453-465
• 40 Small J V, Stradal T, Vignal E. et al . The lamellipodium: where motility begins.  Trends Cell Biol. 2002;  43 112-120
• 41 Mitchison T J, Cramer L P. Actin-based cell motility and cell locomotion.  Cell. 1996;  43 371-379
• 42 Dembo M, Wang Y L. Stresses at the cell-to-substrate interface during locomotion of fibroblasts.  Biophys J. 1999;  43 2307-2316
• 43 Pelham R J Jr, Wang Y. High resolution detection of mechanical forces exerted by locomoting fibroblasts on the substrate.  Mol Biol Cell. 1999;  43 935-945
• 44 Giannone G, Dubin-Thaler B J, Dobereiner H G. et al . Periodic lamellipodial contractions correlate with rearward actin waves.  Cell. 2004;  43 431-443
• 45 Riveline D, Zamir E, Balaban N Q. et al . Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism.  J Cell Biol. 2001;  43 1175-1186
• 46 Totsukawa G, Yamakita Y, Yamashiro S. et al . Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts.  J Cell Biol. 2000;  43 797-806
• 47 Totsukawa G, Wu Y, Sasaki Y. et al . Distinct roles of MLCK and ROCK in the regulation of membrane protrusions and focal adhesion dynamics during cell migration of fibroblasts.  J Cell Biol. 2004;  43 427-439
• 48 Poperechnaya A, Varlamova O, Lin P J. et al . Localization and activity of myosin light chain kinase isoforms during the cell cycle.  J Cell Biol. 2000;  43 697-708
• 49 Beningo K A, Dembo M, Kaverina I. et al . Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts.  J Cell Biol. 2001;  43 881-888
• 50 Sawada Y, Nakamura K, Doi K. et al . Rap1 is involved in cell stretching modulation of p38 but not ERK or JNK MAP kinase.  J Cell Sci. 2001;  43 1221-1227
• 51 Sawada Y, Sheetz M P. Force transduction by Triton cytoskeletons.  J Cell Biol. 2002;  43 609-615
• 52 Oberhauser A F, Hansma P K, Carrion-Vazquez M. et al . Stepwise unfolding of titin under force-clamp atomic force microscopy.  Proc Natl Acad Sci USA. 2001;  43 468-472
• 53 Oberhauser A F, Marszalek P E, Erickson H P. et al . The molecular elasticity of the extracellular matrix protein tenascin.  Nature. 1998;  43 181-185
• 54 Oberhauser A F, Badilla-Fernandez C, Carrion-Vazquez M. et al . The mechanical hierarchies of fibronectin observed with single-molecule AFM.  J Mol Biol. 2002;  43 433-447
• 55 Webb D J, Parsons J T, Horwitz A F. Adhesion assembly, disassembly and turnover in migrating cells - over and over and over again.  Nat Cell Biol. 2002;  43 E97-E100
• 56 Wiseman P W, Brown C M, Webb D J. et al . Spatial mapping of integrin interactions and dynamics during cell migration by image correlation microscopy.  J Cell Sci. 2004;  43 5521-5534
• 57 Webb D J, Zhang H, Horwitz A F. Cell migration: an overview.  Methods Mol Biol. 2005;  43 3-11
• 58 Laukaitis C M, Webb D J, Donais K. et al . Differential dynamics of alpha 5 integrin, paxillin, and alpha-actinin during formation and disassembly of adhesions in migrating cells.  J Cell Biol. 2001;  43 1427-1440
• 59 Miyamoto S, Teramoto H, Coso O A. et al . Integrin function: molecular hierarchies of cytoskeletal and signaling molecules.  J Cell Biol. 1995;  43 791-805
• 60 Yamada K M, Miyamoto S. Integrin transmembrane signaling and cytoskeletal control.  Curr Opin Cell Biol. 1995;  43 681-689
• 61 Miyamoto S, Akiyama S K, Yamada K M. Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function.  Science. 1995;  43 883-885
• 62 Webb D J, Donais K, Whitmore L A. et al . FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly.  Nat Cell Biol. 2004;  43 154-161
• 63 von Wichert G, Feng G S, Haimovich B. et al . Force dependent establishment of integrin-cytoskeleton linkages requires downregulation of focal contact dynamics by Shp2.  EMBO J. 2003;  43 5023-5035
• 64 Ilic D, Furuta Y, Kanazawa S. et al . Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice.  Nature. 1995;  43 539-544
• 65 Sieg D J, Hauck C R, Schlaepfer D D. Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration.  J Cell Sci. 1999;  43 2677-2691
• 66 Owen J D, Ruest P J, Fry D W. et al . Induced focal adhesion kinase (FAK) expression in FAK-null cells enhances cell spreading and migration requiring both auto- and activation loop phosphorylation sites and inhibits adhesion-dependent tyrosine phosphorylation of Pyk2.  Mol Cell Biol. 1999;  43 4806-4818
• 67 Iyer V V, Ballestrem C, Kirchner J. et al . Measurement of protein tyrosine phosphorylation in cell adhesion.  Methods Mol Biol. 2005;  43 289-302
• 68 Zaidel-Bar R, Ballestrem C, Kam Z. et al . Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells.  J Cell Sci. 2003;  43 4605-4613
• 69 Katz B Z, Romer L, Miyamoto S. et al . Targeting membrane-localized focal adhesion kinase to focal adhesions: roles of tyrosine phosphorylation and SRC family kinases.  J Biol Chem. 2003;  43 29 115-29 120
• 70 Klinghoffer R A, Sachsenmaier C, Cooper J A. et al . Src family kinases are required for integrin but not PDGFR signal transduction.  Embo J. 1999;  43 2459-2471
• 71 Fincham V J, Frame M C. The catalytic activity of Src is dispensable for translocation to focal adhesions but controls the turnover of these structures during cell motility.  Embo J. 1998;  43 81-92
• 72 Felsenfeld D P, Schwartzberg P L, Venegas A. et al . Selective regulation of integrin-cytoskeleton interactions by the tyrosine kinase Src.  Nat Cell Biol. 1999;  43 200-206
• 73 Smilenov L B, Mikhailov A, Pelham R J. et al . Focal adhesion motility revealed in stationary fibroblasts.  Science. 1999;  43 1172-1174
• 74 Zamir E, Katz M, Posen Y. et al . Dynamics and segregation of cell-matrix adhesions in cultured fibroblasts.  Nat Cell Biol. 2000;  43 191-196
• 75 Ballestrem C, Hinz B, Imhof B A. et al . Marching at the front and dragging behind: differential alphaVbeta3-integrin turnover regulates focal adhesion behavior.  J Cell Biol. 2001;  43 1319-1332
• 76 Ren X D, Kiosses W B, Sieg D J. et al . Focal adhesion kinase suppresses Rho activity to promote focal adhesion turnover.  J Cell Sci. 2000;  43 3673-3678
• 77 Giannone G, Ronde P, Gaire M. et al . Calcium oscillations trigger focal adhesion disassembly in human U87 astrocytoma cells.  J Biol Chem. 2002;  43 26 364-26 371
• 78 Edlund M, Lotano M A, Otey C A. Dynamics of alpha-actinin in focal adhesions and stress fibers visualized with alpha-actinin-green fluorescent protein.  Cell Motil Cytoskeleton. 2001;  43 190-200
• 79 Tsuruta D, Gonzales M, Hopkinson S B. et al . Microfilament-dependent movement of the beta3 integrin subunit within focal contacts of endothelial cells.  Faseb J. 2002;  43 866-868
• 80 Critchley D R. Focal adhesions - the cytoskeletal connection.  Curr Opin Cell Biol. 2000;  43 133-139
• 81 Schaller M D. Paxillin: a focal adhesion-associated adaptor protein.  Oncogene. 2001;  43 6459-6472
• 82 Balaban N Q, Schwarz U S, Riveline D. et al . Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates.  Nat Cell Biol. 2001;  43 466-472
• 83 Galbraith C G, Yamada K M, Sheetz M P. The relationship between force and focal complex development.  J Cell Biol. 2002;  43 1-13
• 84 Izaguirre G, Aguirre L, Hu Y P. et al . The cytoskeletal/non-muscle isoform of alpha-actinin is phosphorylated on its actin-binding domain by the focal adhesion kinase.  J Biol Chem. 2001;  43 28 676-28 685
• 85 Otey C A, Pavalko F M, Burridge K. An interaction between alpha-actinin and the beta 1 integrin subunit in vitro.  J Cell Biol. 1990;  43 721-729
• 86 Pavalko F M, Otey C A, Simon K O. et al . Alpha-actinin: a direct link between actin and integrins.  Biochem Soc Trans. 1991;  43 1065-1069
• 87 Xu J, Tseng Y, Wirtz D. Strain hardening of actin filament networks. Regulation by the dynamic cross-linking protein alpha-actinin.  J Biol Chem. 2000;  43 35 886-35 892
• 88 Xu J, Wirtz D, Pollard T D. Dynamic cross-linking by alpha-actinin determines the mechanical properties of actin filament networks.  J Biol Chem. 1998;  43 9570-9576
• 89 Wachsstock D H, Schwarz W H, Pollard T D. Cross-linker dynamics determine the mechanical properties of actin gels.  Biophys J. 1994;  43 801-809
• 90 Wachsstock D H, Schwartz W H, Pollard T D. Affinity of alpha-actinin for actin determines the structure and mechanical properties of actin filament gels.  Biophys J. 1993;  43 205-214
• 91 Cukierman E, Pankov R, Stevens D R. et al . Taking cell-matrix adhesions to the third dimension.  Science. 2001;  43 1708-1712
• 92 Meshel A S, Wei Q, Adelstein R S. et al . Basic mechanism of three-dimensional collagen fibre transport by fibroblasts.  Nat Cell Biol. 2005;  43 157-164
• 93 Wolf K, Mazo I, Leung H. et al . Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis.  J Cell Biol. 2003;  43 267-277
• 94 Wei L, Yang Y, Zhang X. et al . Altered regulation of Src upon cell detachment protects human lung adenocarcinoma cells from anoikis.  Oncogene. 2004;  43 9052-9061
• 95 Frisch S M, Vuori K, Ruoslahti E. et al . Control of adhesion-dependent cell survival by focal adhesion kinase.  J Cell Biol. 1996;  43 793-799
• 96 Wang H B, Dembo M, Hanks S K. et al . Focal adhesion kinase is involved in mechanosensing during fibroblast migration.  Proc Natl Acad Sci USA. 2001;  43 11 295-11 300
• 97 Owens L V, Xu L, Craven R J. et al . Overexpression of the focal adhesion kinase (p125FAK) in invasive human tumors.  Cancer Res. 1995;  43 2752-2755
• 98 Frame M C, Fincham V J, Carragher N O. et al . v-Src’s hold over actin and cell adhesions.  Nat Rev Mol Cell Biol. 2002;  43 233-245
• 99 Talamonti M S, Roh M S, Curley S A. et al . Increase in activity and level of pp60c-src in progressive stages of human colorectal cancer.  J Clin Invest. 1993;  43 53-60
• 100 Hsia D A, Mitra S K, Hauck C R. et al . Differential regulation of cell motility and invasion by FAK.  J Cell Biol. 2003;  43 753-767
• 101 McLean G W, Komiyama N H, Serrels B. et al . Specific deletion of focal adhesion kinase suppresses tumor formation and blocks malignant progression.  Genes Dev. 2004;  43 2998-3003
• 102 Hernandez-Alcoceba R, del P eso L, Lacal J C. The Ras family of GTPases in cancer cell invasion.  Cell Mol Life Sci. 2000;  43 65-76