Studying early stages of fibronectin fibrillogenesis in living cells by atomic force microscopy

Time-lapse atomic force microscopy imaging is used to visualize the initial stages of fibronectin fibrillogenesis directly in living cells with high resolution. This approach provides new structural and mechanistic details, such as a stepwise extension mechanism and an accelerating effect of extracellular Mn2+ on early FN fibrillogenesis.

[1]  R. Clark,et al.  In vivo co-distribution of fibronectin and actin fibers in granulation tissue: immunofluorescence and electron microscope studies of the fibronexus at the myofibroblast surface , 1984, The Journal of cell biology.

[2]  M. Humphries,et al.  Regulation of integrin alpha 5 beta 1-fibronectin interactions by divalent cations. Evidence for distinct classes of binding sites for Mn2+, Mg2+, and Ca2+. , 1995, The Journal of biological chemistry.

[3]  D. M. Peters,et al.  Arrangement of cellular fibronectin in noncollagenous fibrils in human fibroblast cultures. , 1991, Journal of cell science.

[4]  B. Geiger,et al.  Force-induced fibronectin fibrillogenesis in vitro , 2008 .

[5]  S. Aota,et al.  Requirement for the synergy site for cell adhesion to fibronectin depends on the activation state of integrin alpha 5 beta 1. , 1995, The Journal of biological chemistry.

[6]  R. Keller,et al.  Live imaging of cell protrusive activity, and extracellular matrix assembly and remodeling during morphogenesis in the frog, Xenopus laevis , 2008, Developmental dynamics : an official publication of the American Association of Anatomists.

[7]  T. Ando,et al.  Development of High-Speed AFM and Its Biological Applications , 2014 .

[8]  Ravi A. Desai,et al.  Activation of beta 1 but not beta 3 integrin increases cell traction forces , 2013, FEBS letters.

[9]  Daniel J Müller,et al.  Analyzing focal adhesion structure by atomic force microscopy , 2005, Journal of Cell Science.

[10]  V. Vogel,et al.  Coexisting conformations of fibronectin in cell culture imaged using fluorescence resonance energy transfer , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Daniel J. Muller,et al.  Multiparametric high-resolution imaging of native proteins by force-distance curve–based AFM , 2014, Nature Protocols.

[12]  Cheng Zhu,et al.  JCB_200810002 1275..1284 , 2009 .

[13]  J. Schwarzbauer,et al.  Fibronectins, their fibrillogenesis, and in vivo functions. , 2011, Cold Spring Harbor perspectives in biology.

[14]  D. Mosher,et al.  Formation of Sodium Dodecyl Sulfate-stable Fibronectin Multimers , 1996, The Journal of Biological Chemistry.

[15]  H. Erickson,et al.  Dynamics and elasticity of the fibronectin matrix in living cell culture visualized by fibronectin-green fluorescent protein. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Jens Friedrichs,et al.  Cellular remodelling of individual collagen fibrils visualized by time-lapse AFM. , 2007, Journal of molecular biology.

[17]  J. Schwarzbauer,et al.  Modulatory roles for integrin activation and the synergy site of fibronectin during matrix assembly. , 1997, Molecular biology of the cell.

[18]  R. Keller,et al.  Fibronectin, mesoderm migration, and gastrulation in Xenopus. , 1996, Developmental biology.

[19]  Daniel J. Ehrlich,et al.  Using Molecular Mechanics to Predict Bulk Material Properties of Fibronectin Fibers , 2012, PLoS Comput. Biol..

[20]  Mark J. Bradshaw,et al.  Contribution of unfolding and intermolecular architecture to fibronectin fiber extensibility. , 2011, Biophysical journal.

[21]  H. Erickson,et al.  Dual labeling of the fibronectin matrix and actin cytoskeleton with green fluorescent protein variants. , 2002, Journal of cell science.

[22]  J. Schwarzbauer,et al.  Regulation of fibronectin matrix assembly by activated Ras in transformed cells , 2000, Oncogene.

[23]  Viola Vogel,et al.  Molecular architecture of native fibronectin fibrils , 2015, Nature Communications.

[24]  Viola Vogel,et al.  Fibronectin extension and unfolding within cell matrix fibrils controlled by cytoskeletal tension , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Peters,et al.  Conformation of Fibronectin Fibrils Varies: Discrete Globular Domains of Type III Repeats Detected , 1998, Microscopy and Microanalysis.

[26]  Viola Vogel,et al.  Force-Induced Unfolding of Fibronectin in the Extracellular Matrix of Living Cells , 2007, PLoS biology.

[27]  L. Zardi,et al.  High-resolution cryo-scanning electron microscopy study of the macromolecular structure of fibronectin fibrils. , 1997, Scanning.

[28]  J. Schwarzbauer,et al.  Fibronectin fibrillogenesis, a cell-mediated matrix assembly process. , 2005, Matrix biology : journal of the International Society for Matrix Biology.

[29]  R. Hynes,et al.  Molecular biology of fibronectin. , 1985, Annual review of cell biology.

[30]  I. Singer.  The fibronexus: a transmembrane association of fibronectin-containing fibers and bundles of 5 nm microfilaments in hamster and human fibroblasts , 1979, Cell.

[31]  M. Marsden,et al.  Regulation of cell polarity, radial intercalation and epiboly in Xenopus: novel roles for integrin and fibronectin. , 2001, Development.

[32]  Andrés J. García,et al.  Cyclic mechanical reinforcement of integrin-ligand interactions. , 2013, Molecular cell.

[33]  Melinda Larsen,et al.  Fibronectin requirement in branching morphogenesis , 2003, Nature.

[34]  Emilios Tahinci,et al.  Guidance of mesoderm cell migration in the Xenopus gastrula requires PDGF signaling , 2004, Development.

[35]  P. Norton,et al.  Fibronectin organization under and near cells , 2006, European Biophysics Journal.

[36]  R. Keller,et al.  Assembly and remodeling of the fibrillar fibronectin extracellular matrix during gastrulation and neurulation in Xenopus laevis , 2004, Developmental dynamics : an official publication of the American Association of Anatomists.

[37]  J. Schwarzbauer,et al.  Assembly of fibronectin extracellular matrix. , 2010, Annual review of cell and developmental biology.

[38]  H. Erickson,et al.  Fibronectin molecule visualized in electron microscopy: a long, thin, flexible strand , 1981, The Journal of cell biology.

[39]  Mariano Carrion-Vazquez,et al.  The mechanical hierarchies of fibronectin observed with single-molecule AFM. , 2002, Journal of molecular biology.

[40]  C. Franz,et al.  Inverting adherent cells for visualizing ECM interactions at the basal cell side. , 2013, Ultramicroscopy.

[41]  D. M. Peters,et al.  Substrate-specific binding of the amino terminus of fibronectin to an integrin complex in focal adhesions. , 1994, The Journal of biological chemistry.

[42]  D. Mosher,et al.  Co-assembly of plasma and cellular fibronectins into fibrils in human fibroblast cultures , 1990, The Journal of cell biology.

[43]  P. McKeown-Longo,et al.  Localization of fibronectin matrix assembly sites on fibroblasts and endothelial cells. , 1997, Journal of cell science.

[44]  Yong Chen,et al.  Atomic force microscopic investigation on the potential early intermediate stages of fibrillogenesis of fibronectin within fibrils. , 2007, Biochemical and biophysical research communications.

[45]  F. Grinnell.  Manganese-dependent cell-substratum adhesion. , 1984, Journal of cell science.

[46]  V. Nelea,et al.  Periodic beaded-filament assembly of fibronectin on negatively charged surface. , 2010, Journal of structural biology.

[47]  Klaus Schulten,et al.  Identifying unfolding intermediates of FN-III(10) by steered molecular dynamics. , 2002, Journal of molecular biology.

[48]  K Schulten,et al.  Comparison of the early stages of forced unfolding for fibronectin type III modules , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[49]  F. Grinnell.  Fibronectin and wound healing. , 1982, The American Journal of dermatopathology.

[50]  R. Winklbauer,et al.  Fibronectin fibril growth in the extracellular matrix of the Xenopus embryo. , 1995, Journal of cell science.

[51]  Melinda Larsen,et al.  Cell and fibronectin dynamics during branching morphogenesis , 2006, Journal of Cell Science.

[52]  M. Sheetz,et al.  Periodic Lamellipodial Contractions Correlate with Rearward Actin Waves , 2004, Cell.

[53]  E. Ruoslahti,et al.  Regulation of the fibronectin receptor affinity by divalent cations. , 1988, The Journal of biological chemistry.

[54]  B. Geiger,et al.  The removal of extracellular fibronectin from areas of cell-substrate contact , 1981, Cell.

[55]  J Engel,et al.  Shapes, domain organizations and flexibility of laminin and fibronectin, two multifunctional proteins of the extracellular matrix. , 1981, Journal of molecular biology.

[56]  Harold P. Erickson,et al.  2.0 Å Crystal Structure of a Four-Domain Segment of Human Fibronectin Encompassing the RGD Loop and Synergy Region , 1996, Cell.

[57]  R. Segal,et al.  Studies on intercellular LETS glycoprotein matrices , 1978, Cell.

[58]  H. Erickson,et al.  Probing the Folded State of Fibronectin Type III Domains in Stretched Fibrils by Measuring Buried Cysteine Accessibility* , 2011, The Journal of Biological Chemistry.