Molecular architecture of native fibronectin fibrils

Nature Communications

Volumn 6, Issue , 2015, Pages

  Früh, Susanna Maria ^a   Schoen, Ingmar ^a   Ries, Jonas ^b   Vogel, Viola ^a  

^a ETH ZURICH   (Switzerland)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; EPITOPE; FIBRONECTIN;

ANTIBODY; BLEACHING; HIERARCHICAL SYSTEM; MICROSCOPY; MOLECULAR ANALYSIS; PROTEIN; SAMPLING;

AMINO TERMINAL SEQUENCE; ARTICLE; BLEACHING; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DIRECT STOCHASTIC OPTICAL RECONSTRUCTION MICROSCOPY; EXTRACELLULAR MATRIX; EXTRACELLULAR SPACE; HUMAN; HUMAN CELL; MICROSCOPY; PHOTOPERIODICITY; PROTEIN ASSEMBLY; PROTEIN STRUCTURE; SKIN FIBROBLAST; CHEMISTRY; FLUORESCENCE IMAGING; PROTEIN CONFORMATION; ULTRASTRUCTURE;

EXTRACELLULAR MATRIX; FIBRONECTINS; HUMANS; OPTICAL IMAGING; PHOTOBLEACHING; PROTEIN CONFORMATION;

EID: 84930622055     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8275     Document Type: Article

References (70)

1. Mecham R. The Extracellular Matrix: an Overview (Springer Science & Business Media, 2011
2. Hynes R. O. & Yamada K. M. Extracellular Matrix Biology (Cold Spring Habor Laboratory Press, 2012
3. Stoffels J. M. J., Zhao C. & Baron,W. Fibronectin in tissue regeneration: timely disassembly of the scaffold is necessary to complete the build. Cell. Mol. Life Sci. 70, 4243-4253 (2013
4. Rozario T., Dzamba B., Weber G. F., Davidson L. A. & DeSimone D. W. The physical state of fibronectin matrix differentially regulates morphogenetic movements in vivo. Dev. Biol. 327, 386-398 (2009
5. Hynes R. O. The extracellular matrix: not just pretty fibrils. Science 326, 1216-1219 (2009
6. Kadler K. E., Hill A. & Canty-Laird E. G. Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators. Curr. Opin. Cell Biol. 20, 495-501 (2008
7. Wight T. N. & Potter-Perigo S. The extracellular matrix: an active or passive player in fibrosis?. Am. J. Physiol. Gastrointest. Liver Physiol. 301, G950-G955 (2011
8. Miles F. L. & Sikes R. A. Insidious changes in stromal matrix fuel cancer progression. Mol. Cancer Res. 12, 297-312 (2014
9. Park J. & Schwarzbauer J. E. Mammary epithelial cell interactions with fibronectin stimulate epithelial-mesenchymal transition. Oncogene 33, 1649-1657 (2014
10. Vogel V. Mechanotransduction involving multimodular proteins: converting force into biochemical signals. Annu. Rev. Biophys. Biomol. Struct. 35, 459-488 (2006
11. Vakonakis L. & Campbell L. D. Extracellular matrix: from atomic resolution to ultrastructure. Curr. Opin. Cell Biol. 19, 578-583 (2007
12. Schwarzbauer J. E. & DeSimone D. W. Fibronectins, their fibrillogenesis, and in vivo functions. Cold Spring Harb. Perspect. Biol. 3, a005041 (2011
13. Baron M., Norman D.,Willis A. & Campbell I. D. Structure of the fibronectin type 1 module. Nature 345, 642-646 (1990
14. Main A. L., Harvey T. S., Baron M., Boyd J. & Campbell I. D. The threedimensional structure of the tenth type III module of fibronectin: an insight into RGD-mediated interactions. Cell 71, 671-678 (1992
15. Pickford A. R., Potts J. R., Bright J. R., Phan I. & Campbell D. Solution structure of a type 2 module from fibronectin: Implications for the structure and function of the gelatin-binding domain. Structure 5, 359-370 (1997
16. Erickson H. P., Carrell N. & McDonagh J. Fibronectin molecule visualized in electron-microscopy-a long, thin, flexible strand. J. Cell Biol. 91, 673-678 (1981
17. Schwarzbauer J. E. Identification of the fibronectin sequences required for assembly of a fibrillar matrix. J. Cell Biol. 113, 1463-1473 (1991
18. McDonald J. A., Kelley D. G. & Broekelmann T. J. Role of fibronectin in collagen deposition-fab to the gelatin-binding domain of fibronectin inhibits both fibronectin and collagen organization in fibroblast extracellular-matrix. J. Cell Biol. 92, 485-492 (1982
19. McDonald J. A., et al. Fibronectin's cell-adhesive domain and an aminoterminal matrix assembly domain participate in its assembly into fibroblast pericellular matrix. J. Biol. Chem. 262, 2957-2967 (1987
20. Sottile J., Schwarzbauer J., Selegue J. & Mosher D. F. Five type I modules of fibronectin form a functional unit that binds to fibroblasts and Staphylococcus aureus. J. Biol. Chem. 266, 12840-12843 (1991
21. Aguirre K. M., McCormick R. J. & Schwarzbauer J. E. Fibronectin selfassociation is mediated by complementary sites within the amino-terminal onethird of the molecule. J. Biol. Chem. 269, 27863-27868 (1994
22. Chernousov M. A., Fogerty F. J., Koteliansky V. E. & Mosher D. F. Role of the I-9 and III-1 modules of fibronectin in formation of an extracellular fibronectin matrix. J. Biol. Chem. 266, 10851-10858 (1991
23. Morla A. & Ruoslahti E. A fibronectin self-assembly site involved in fibronectin matrix assembly: reconstruction in a synthetic peptide. J. Cell Biol. 118, 421-429 (1992
24. Hocking D. C., Sottile J. & McKeown-Longo P. J. Fibronectin's III-1 module contains a conformation-dependent binding site for the amino-terminal region of fibronectin. J. Biol. Chem. 269, 19183-19187 (1994
25. Sechler J. L., et al. A novel fibronectin binding site required for fibronectin fibril growth during matrix assembly. J. Cell Biol. 154, 1081-1088 (2001
26. Chen Y., Zardi L. & Peters D. M. High-resolution cryo-scanning electron microscopy study of the macromolecular structure of fibronectin fibrils. Scanning 19, 349-355 (1997
27. Peters D. M. P., Chen Y., Zardi L. & Brummel S. Conformation of Fibronectin Fibrils Varies: Discrete Globular Domains of Type III Repeats Detected. Microsc. Microanal. 4, 385-396 (1998
28. Dzamba B. J. & Peters D. M. Arrangement of cellular fibronectin in noncollagenous fibrils in human fibroblast cultures. J. Cell Sci. 100, 605-612 (1991
29. Vakonakis I., Staunton D., Rooney L. M. & Campbell I. D. Interdomain association in fibronectin: insight into cryptic sites and fibrillogenesis. EMBO J. 26, 2575-2583 (2007
30. Maqueda A., Moyano J. V., del Cerro M. H., Peters D. M. & Garcia-Pardo A. The heparin III-binding domain of fibronectin (III4-5 repeats) binds to fibronectin and inhibits fibronectin matrix assembly. Matrix Biol. 26, 642-651 (2007
31. Singh P., Carraher C. & Schwarzbauer J. E. Assembly of fibronectin extracellular matrix. Annu. Rev. Cell Dev. Biol. 26, 397-419 (2010
32. Graille M., Pagano M., Rose T., Ravaux M. R. & van Tilbeurgh H. Zinc induces structural reorganization of gelatin binding domain from human fibronectin and affects collagen binding. Structure 18, 710-718 (2010
33. Atkin K. E., et al. The streptococcal binding site in the gelatin-binding domain of fibronectin is consistent with a non-linear arrangement of modules. J. Biol. Chem. 285, 36977-36983 (2010
34. Fürstenberg A. & Heilemann M. Single-molecule localization microscopynear- molecular spatial resolution in light microscopy with photoswitchable fluorophores. Phys. Chem. Chem. Phys. 15, 14919-14930 (2013
35. Betzig E., et al. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313, 1642-1645 (2006
36. Rust M. J., Bates M. & Zhuang X. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 3, 793-795 (2006
37. Heilemann M., et al. Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes. Angew. Chem. Int. Ed. 47, 6172-6176 (2008
38. Qu X., Wu D., Mets L. & Scherer N. F. Nanometer-localized multiple singlemolecule fluorescence microscopy. Proc. Natl Acad. Sci. USA 101, 11298-11303 (2004
39. Gordon M. P., Ha T. & Selvin P. R. Single-molecule high-resolution imaging with photobleaching. Proc. Natl Acad. Sci. USA 101, 6462-6465 (2004
40. Kanchanawong P., et al. Nanoscale architecture of integrin-based cell adhesions. Nature 468, 580-584 (2010
41. Pertsinidis A., Zhang Y. & Chu S. Subnanometre single-molecule localization, registration and distance measurements. Nature 466, 647-651 (2010
42. Xu K., Zhong G. & Zhuang X. Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science 339, 452-456 (2013
43. Löschberger A., et al. Super-resolution imaging visualizes the eightfold symmetry of gp210 proteins around the nuclear pore complex and resolves the central channel with nanometer resolution. J. Cell Sci. 125, 570-575 (2012
44. Szymborska A., et al. Nuclear pore scaffold structure analyzed by superresolution microscopy and particle averaging. Science 341, 655-658 (2013
45. Früh, S. M., et al. Functional modification of fibronectin by N-terminal FXIIIamediated transamidation. Chembiochem. 15, 1481-1486 (2014
46. Mao Y. & Schwarzbauer J. E. Fibronectin fibrillogenesis, a cell-mediated matrix assembly process. Matrix Biol. 24, 389-399 (2005
47. Smith M. L., et al. Force-induced unfolding of fibronectin in the extracellular matrix of living cells. PLoS Biol. 5, e268-2254 (2007
48. Ohashi T., Kiehart D. P. & Erickson H. P. Dynamics and elasticity of the fibronectin matrix in living cell culture visualized by fibronectin-green fluorescent protein. Proc. Natl Acad. Sci. USA 96, 2153-2158 (1999
49. Baneyx G., Baugh L. & Vogel V. Coexisting conformations of fibronectin in cell culture imaged using fluorescence resonance energy transfer. Proc. Natl Acad. Sci. USA 98, 14464-14468 (2001
50. Vakonakis I., et al. Motogenic sites in human fibronectin are masked by long range interactions. J. Biol. Chem. 284, 15668-15675 (2009
51. Chen L. B., Murray A., Segal R. A., Bushnell A. & Walsh M. L. Studies on intercellular LETS glycoprotein matrices. Cell 14, 377-391 (1978
52. Johnson K. J., Sage H., Briscoe G. & Erickson H. P. The compact conformation of fibronectin is determined by intramolecular ionic interactions. J. Biol. Chem. 274, 15473-15479 (1999
53. Litvinovich S. V., et al. Formation of amyloid-like fibrils by self-association of a partially unfolded fibronectin type III module. J. Mol. Biol. 280, 245-258 (1998
54. Lu H., Isralewitz B., Krammer A., Vogel V. & Schulten K. Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation. Biophys. J. 75, 662-671 (1998
55. Kufer S. K., Puchner E. M., Gumpp H., Liedl T. & Gaub H. E. Singlemolecule cut-and-paste surface assembly. Science 319, 594-596 (2008
56. Klotzsch E., et al. Fibronectin forms the most extensible biological fibers displaying switchable force-exposed cryptic binding sites. Proc. Natl Acad. Sci. USA 106, 18267-18272 (2009
57. McKeown-Longo P. J. & Mosher D. F. Binding of plasma fibronectin to celllayers of human-skin fibroblasts. J. Cell Biol. 97, 466-472 (1983
58. Peleg O., et al. Fibers with integrated mechanochemical switches: minimalistic design principles derived from fibronectin. Biophys. J. 103, 1909-1918 (2012
59. Geiger B., Spatz J. P. & Bershadsky A. D. Environmental sensing through focal adhesions. Nat. Rev. Mol. Cell Biol. 10, 21-33 (2009
60. Schoen I., Pruitt B. L. & Vogel V. The Yin-Yang of rigidity sensing: how forces and mechanical properties regulate the cellular response to materials. Annu. Rev. Mater. Res. 43, 589-618 (2013
61. Chabria M., Hertig S., Smith M. L. & Vogel V. Stretching fibronectin fibres disrupts binding of bacterial adhesins by physically destroying an epitope. Nat. Commun. 1, 135 (2010
62. Little W. C., Schwartlander R., Smith M. L., Gourdon D. & Vogel V. Stretched extracellular matrix proteins turn fouling and are functionally rescued by the chaperones albumin and casein. Nano Lett. 9, 4158-4167 (2009
63. Castellani P., et al. Transformed human-cells release different fibronectin variants than do normal-cells. J. Cell Biol. 103, 1671-1677 (1986
64. Dempsey G. T., Vaughan J. C., Chen K. H., Bates M. & Zhuang X. Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging. Nat. Methods 8, 1027-1036 (2011
65. Vogelsang J., et al. A reducing and oxidizing system minimizes photobleaching and blinking of fluorescent dyes. Angew. Chem. Int. Ed. Engl. 47, 5465-5469 (2008
66. Ries J., Kaplan C., Platonova E., Eghlidi H. & Ewers H. A simple, versatile method for GFP-based super-resolution microscopy via nanobodies. Nat. Methods 9, 582-584 (2012
67. Smith C. S., Joseph N., Rieger B. & Lidke K. A. Fast, single-molecule localization that achieves theoretically minimum uncertainty. Nat. Methods 7, 373-375 (2010
68. Lampe A., Haucke V., Sigrist S. J., Heilemann M. & Schmoranzer J. Multicolour direct STORM with red emitting carbocyanines. Biol. Cell 104, 229-237 (2012
69. Kerssemakers J. W. J., et al. Assembly dynamics of microtubules at molecular resolution. Nature 442, 709-712 (2006
70. Schoen I. Localization precision in stepwise photobleaching experiments. Biophys. J. 107, 2122-2129 (2014