![]() |
|
|
Vol. 11, Issue 3, 1047-1060, March 2000




§
*Craniofacial Developmental Biology and Regeneration Branch,
National Institute of Craniofacial and Dental Research, National
Institutes of Health, Bethesda, Maryland; and This study establishes that the physical state of the extracellular
matrix can regulate integrin-mediated cytoskeletal
assembly and tyrosine phosphorylation to generate two distinct types of cell-matrix adhesions. In primary fibroblasts,
Department
of Molecular Cell Biology, The Weizmann Institute of Science, Rehovot,
Israel
5
1 integrin associates mainly
with fibronectin fibrils and forms adhesions structurally distinct from
focal contacts, independent of actomyosin-mediated cell contractility.
These "fibrillar adhesions" are enriched in tensin, but contain low
levels of the typical focal contact components paxillin, vinculin, and
tyrosine-phosphorylated proteins. However, when the fibronectin is
covalently linked to the substrate,
5
1 integrin forms highly tyrosine-phosphorylated, "classical"
focal contacts containing high levels of paxillin and vinculin. These experiments indicate that the physical state of the matrix, not just
its molecular composition, is a critical factor in defining cytoskeletal organization and phosphorylation at adhesion sites. We
propose that molecular organization of adhesion sites is controlled by
at least two mechanisms: 1) specific integrins associate with their ligands in transmembrane complexes with appropriate cytoplasmic anchor proteins (e.g., fibronectin-
5
1
integrin-tensin complexes), and 2) physical properties (e.g.,
rigidity) of the extracellular matrix regulate local tension at
adhesion sites and activate local tyrosine phosphorylation, recruiting
a variety of plaque molecules to these sites. These mechanisms generate
structurally and functionally distinct types of matrix adhesions in fibroblasts.
Present address: The Hematology Institute,
Tel-Aviv Medical Center, Tel-Aviv, Israel.
§
Corresponding author. E-mail address:
benny.geiger{at}weizmann.ac.il.
This article has been cited by other articles:
![]() |
I. Delon and N. H. Brown The integrin adhesion complex changes its composition and function during morphogenesis of an epithelium J. Cell Sci., December 1, 2009; 122(23): 4363 - 4374. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Estrada-Bernal, J. C. Gatlin, S. Sunpaweravong, and K. H. Pfenninger Dynamic adhesions and MARCKS in melanoma cells J. Cell Sci., July 1, 2009; 122(13): 2300 - 2310. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Kuriyama, M. Bettencourt-Dias, I. Hoffmann, M. Arnold, and L. Sandvig {gamma}-Tubulin-containing abnormal centrioles are induced by insufficient Plk4 in human HCT116 colorectal cancer cells J. Cell Sci., June 15, 2009; 122(12): 2014 - 2023. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. T. T. Bach, S. Creed, J. Zhong, M. Mahmassani, G. Schevzov, J. Stehn, L. N. Cowell, P. Naumanen, P. Lappalainen, P. W. Gunning, et al. Tropomyosin Isoform Expression Regulates the Transition of Adhesions To Determine Cell Speed and Direction Mol. Cell. Biol., March 15, 2009; 29(6): 1506 - 1514. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. C Burghardt, J. R Burghardt, J. D Taylor II, A. T Reeder, B. T Nguen, T. E Spencer, K. J Bayless, and G. A Johnson Enhanced focal adhesion assembly reflects increased mechanosensation and mechanotransduction at maternal-conceptus interface and uterine wall during ovine pregnancy Reproduction, March 1, 2009; 137(3): 567 - 582. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Puklin-Faucher and M. P. Sheetz The mechanical integrin cycle J. Cell Sci., January 15, 2009; 122(2): 179 - 186. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. R. Legate and R. Fassler Mechanisms that regulate adaptor binding to {beta}-integrin cytoplasmic tails J. Cell Sci., January 15, 2009; 122(2): 187 - 198. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. Hirata, H. Tatsumi, and M. Sokabe Mechanical forces facilitate actin polymerization at focal adhesions in a zyxin-dependent manner J. Cell Sci., September 1, 2008; 121(17): 2795 - 2804. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. Pouthas, P. Girard, V. Lecaudey, T. B. N. Ly, D. Gilmour, C. Boulin, R. Pepperkok, and E. G. Reynaud In migrating cells, the Golgi complex and the position of the centrosome depend on geometrical constraints of the substratum J. Cell Sci., July 15, 2008; 121(14): 2406 - 2414. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. J. Pendegrass, D. Gordon, C. A. Middleton, S. Ng. M. Sun, and G. W. Blunn Sealing the skin barrier around transcutaneous implants: IN VITRO STUDY OF KERATINOCYTE PROLIFERATION AND ADHESION IN RESPONSE TO SURFACE MODIFICATIONS OF TITANIUM ALLOY J Bone Joint Surg Br, January 1, 2008; 90-B(1): 114 - 121. [Abstract] [Full Text] [PDF] |
||||
![]() |
W.-H. Su, H.-i. Chen, and C. J. Jen Polymorphonuclear leukocyte transverse migration induces rapid alterations in endothelial focal contacts J. Leukoc. Biol., September 1, 2007; 82(3): 542 - 550. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. S. Wallace, S. A. Strike, and G. A. Truskey Smooth muscle cell rigidity and extracellular matrix organization influence endothelial cell spreading and adhesion formation in coculture Am J Physiol Heart Circ Physiol, September 1, 2007; 293(3): H1978 - H1986. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Papp, M. P. Fadel, H. Kim, C. A. McCulloch, and M. Opas Calreticulin Affects Fibronectin-based Cell-Substratum Adhesion via the Regulation of c-Src Activity J. Biol. Chem., June 1, 2007; 282(22): 16585 - 16598. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Yoneda, D. Ushakov, H. A.B. Multhaupt, and J. R. Couchman Fibronectin Matrix Assembly Requires Distinct Contributions from Rho Kinases I and -II Mol. Biol. Cell, January 1, 2007; 18(1): 66 - 75. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. H. Romer, K. G. Birukov, and J. G.N. Garcia Focal Adhesions: Paradigm for a Signaling Nexus Circ. Res., March 17, 2006; 98(5): 606 - 616. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. M. Hoffman, C. C. Jensen, S. Kloeker, C.-L. A. Wang, M. Yoshigi, and M. C. Beckerle Genetic ablation of zyxin causes Mena/VASP mislocalization, increased motility, and deficits in actin remodeling J. Cell Biol., February 27, 2006; 172(5): 771 - 782. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. D. Matthews, D. R. Overby, R. Mannix, and D. E. Ingber Cellular adaptation to mechanical stress: role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels J. Cell Sci., February 1, 2006; 119(3): 508 - 518. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. M. Pizzo, K. Kokini, L. C. Vaughn, B. Z. Waisner, and S. L. Voytik-Harbin Extracellular matrix (ECM) microstructural composition regulates local cell-ECM biomechanics and fundamental fibroblast behavior: a multidimensional perspective J Appl Physiol, May 1, 2005; 98(5): 1909 - 1921. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. J. Kong, T. R. Polte, E. Alsberg, and D. J. Mooney FRET measurements of cell-traction forces and nano-scale clustering of adhesion ligands varied by substrate stiffness PNAS, March 22, 2005; 102(12): 4300 - 4305. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Wang, J. Fan, C. Laschinger, P. D. Arora, A. Kapus, A. Seth, and C. A. McCulloch Smooth Muscle Actin Determines Mechanical Force-induced p38 Activation J. Biol. Chem., February 25, 2005; 280(8): 7273 - 7284. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Bae, T. Sakai, and D. F. Mosher Assembly of Exogenous Fibronectin by Fibronectin-null Cells Is Dependent on the Adhesive Substrate J. Biol. Chem., August 20, 2004; 279(34): 35749 - 35759. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. Takahara, I. Shirato, K. Asanuma, M. Yamashita, Y. Takeda, and Y. Tomino Tensin Is Expressed in Glomerular Mesangial Cells and Is Related to Their Attachment to Surrounding Extracellular Matrix J. Histochem. Cytochem., May 1, 2004; 52(5): 683 - 692. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. J. Kempiak and J. E. Segall Stimulation of Cells Using EGF-Coated Magnetic Beads Sci. Signal., February 3, 2004; 2004(218): pl1 - pl1. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Ilic, B. Kovacic, K. Johkura, D. D. Schlaepfer, N. Tomasevic, Q. Han, J.-B. Kim, K. Howerton, C. Baumbusch, N. Ogiwara, et al. FAK promotes organization of fibronectin matrix and fibrillar adhesions J. Cell Sci., January 15, 2004; 117(2): 177 - 187. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. Baluska, J. Samaj, P. Wojtaszek, D. Volkmann, and D. Menzel Cytoskeleton-Plasma Membrane-Cell Wall Continuum in Plants. Emerging Links Revisited Plant Physiology, October 1, 2003; 133(2): 482 - 491. [Full Text] [PDF] |
||||
![]() |
B. Hinz, V. Dugina, C. Ballestrem, B. Wehrle-Haller, and C. Chaponnier {alpha}-Smooth Muscle Actin Is Crucial for Focal Adhesion Maturation in Myofibroblasts Mol. Biol. Cell, June 1, 2003; 14(6): 2508 - 2519. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Kabir-Salmani, S. Shiokawa, Y. Akimoto, K. Sakai, S. Nagamatsu, K. Sakai, Y. Nakamura, A. Lotfi, H. Kawakami, and M. Iwashita {alpha}v{beta}3 Integrin Signaling Pathway Is Involved in Insulin-Like Growth Factor I-Stimulated Human Extravillous Trophoblast Cell Migration Endocrinology, April 1, 2003; 144(4): 1620 - 1630. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Sottile and D. C. Hocking Fibronectin Polymerization Regulates the Composition and Stability of Extracellular Matrix Fibrils and Cell-Matrix Adhesions Mol. Biol. Cell, October 1, 2002; 13(10): 3546 - 3559. [Abstract] [Full Text] [PDF] |
||||
![]() |
A.-M. C. Yvon, J. W. Walker, B. Danowski, C. Fagerstrom, A. Khodjakov, and P. Wadsworth Centrosome Reorientation in Wound-Edge Cells Is Cell Type Specific Mol. Biol. Cell, June 1, 2002; 13(6): 1871 - 1880. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Nadav, A. Eldor, O. Yacoby-Zeevi, E. Zamir, I. Pecker, N. Ilan, B. Geiger, I. Vlodavsky, and B.-Z. Katz Activation, processing and trafficking of extracellular heparanase by primary human fibroblasts J. Cell Sci., May 15, 2002; 115(10): 2179 - 2187. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. A. Esteban-Barragan, P. Avila, M. Alvarez-Tejado, M. D. Gutierrez, A. Garcia-Pardo, F. Sanchez-Madrid, and M. O. Landazuri Role of the von Hippel-Lindau Tumor Suppressor Gene in the Formation of {beta}1-Integrin Fibrillar Adhesions Cancer Res., May 1, 2002; 62(10): 2929 - 2936. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Zamir and B. Geiger Molecular complexity and dynamics of cell-matrix adhesions J. Cell Sci., March 12, 2002; 114(20): 3583 - 3590. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. Dugina, L. Fontao, C. Chaponnier, J. Vasiliev, and G. Gabbiani Focal adhesion features during myofibroblastic differentiation are controlled by intracellular and extracellular factors J. Cell Sci., March 11, 2002; 114(18): 3285 - 3296. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Werner, F. Kheradmand, R. R. Isberg, and Z. Werb Phagocytosis mediated by Yersinia invasin induces collagenase-1 expression in rabbit synovial fibroblasts through a proinflammatory cascade J. Cell Sci., March 11, 2002; 114(18): 3333 - 3343. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Bhatt, I. Kaverina, C. Otey, and A. Huttenlocher Regulation of focal complex composition and disassembly by the calcium-dependent protease calpain J. Cell Sci., January 9, 2002; 115(17): 3415 - 3425. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Y. Koo, D. J. Irvine, A. M. Mayes, D. A. Lauffenburger, and L. G. Griffith Co-regulation of cell adhesion by nanoscale RGD organization and mechanical stimulus J. Cell Sci., January 4, 2002; 115(7): 1423 - 1433. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. Paulhe, C. Racaud-Sultan, A. Ragab, C. Albiges-Rizo, H. Chap, N. Iberg, O. Morand, and B. Perret Differential Regulation of Phosphoinositide Metabolism by alpha Vbeta 3 and alpha Vbeta 5 Integrins upon Smooth Muscle Cell Migration J. Biol. Chem., November 2, 2001; 276(45): 41832 - 41840. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Guo, P. W. Sanders, A. Woods, and C. Wu The Distribution and Regulation of Integrin-Linked Kinase in Normal and Diabetic Kidneys Am. J. Pathol., November 1, 2001; 159(5): 1735 - 1742. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. M. Suter and P. Forscher Transmission of growth cone traction force through apCAM-cytoskeletal linkages is regulated by Src family tyrosine kinase activity J. Cell Biol., October 29, 2001; 155(3): 427 - 438. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. M. Laukaitis, D. J. Webb, K. Donais, and A. F. Horwitz Differential Dynamics of {alpha}5 Integrin, Paxillin, and {alpha}-Actinin during Formation and Disassembly of Adhesions in Migrating Cells J. Cell Biol., June 25, 2001; 153(7): 1427 - 1440. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Riveline, E. Zamir, N. Q. Balaban, U. S. Schwarz, T. Ishizaki, S. Narumiya, Z. Kam, B. Geiger, and A. D. Bershadsky 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., June 11, 2001; 153(6): 1175 - 1186. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. A. Beningo, M. Dembo, I. Kaverina, J. V. Small, and Y.-l. Wang Nascent Focal Adhesions Are Responsible for the Generation of Strong Propulsive Forces in Migrating Fibroblasts J. Cell Biol., May 14, 2001; 153(4): 881 - 888. [Abstract] [Full Text] [PDF] |
||||
![]() |
R Massoumi and A Sjolander Leukotriene D(4) affects localisation of vinculin in intestinal epithelial cells via distinct tyrosine kinase and protein kinase C controlled events J. Cell Sci., January 5, 2001; 114(10): 1925 - 1934. [Abstract] [PDF] |
||||
![]() |
T. Olski, A. Noegel, and E Korenbaum Parvin, a 42 kDa focal adhesion protein, related to the alpha-actinin superfamily J. Cell Sci., January 2, 2001; 114(3): 525 - 538. [Abstract] [PDF] |
||||
![]() |
G Segal, W Lee, P. Arora, M McKee, G Downey, and C. McCulloch Involvement of actin filaments and integrins in the binding step in collagen phagocytosis by human fibroblasts J. Cell Sci., January 1, 2001; 114(1): 119 - 129. [Abstract] [PDF] |
||||
![]() |
M. Gonzales, B. Weksler, D. Tsuruta, R. D. Goldman, K. J. Yoon, S. B. Hopkinson, F. W. Flitney, and J. C. R. Jones Structure and Function of a Vimentin-associated Matrix Adhesion in Endothelial Cells Mol. Biol. Cell, January 1, 2001; 12(1): 85 - 100. [Abstract] [Full Text] |
||||
![]() |
P. Le, N Benlimame, A Lagana, A Raz, and I. Nabi Clathrin-mediated endocytosis and recycling of autocrine motility factor receptor to fibronectin fibrils is a limiting factor for NIH-3T3 cell motility J. Cell Sci., January 9, 2000; 113(18): 3227 - 3240. [Abstract] [PDF] |
||||
![]() |
J. M. Larios, R. Budhiraja, B. L. Fanburg, and V. J. Thannickal Oxidative Protein Cross-linking Reactions Involving L-Tyrosine in Transforming Growth Factor-beta 1-stimulated Fibroblasts J. Biol. Chem., May 11, 2001; 276(20): 17437 - 17441. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Benzing, P. Gerke, K. Hopker, F. Hildebrandt, E. Kim, and G. Walz Nephrocystin interacts with Pyk2, p130Cas, and tensin and triggers phosphorylation of Pyk2 PNAS, August 14, 2001; 98(17): 9784 - 9789. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Ballestrem, B. Hinz, B. A. Imhof, and B. Wehrle-Haller Marching at the front and dragging behind: differential {alpha}V{beta}3-integrin turnover regulates focal adhesion behavior J. Cell Biol., December 24, 2001; 155(7): 1319 - 1332. [Abstract] [Full Text] [PDF] |
||||