Using transmission electron microscopy and 3View to determine collagen fibril size and three-dimensional organization

Nature Protocols

Volumn 8, Issue 7, 2013, Pages 1433-1448

  Starborg, Tobias ^a   Kalson, Nicholas S ^a   Lu, Yinhui ^a   Mironov, Aleksandr ^a   Cootes, Timothy F ^b   Holmes, David F ^a   Kadler, Karl E ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN FIBRIL; COLLAGEN; FIBRILLAR COLLAGEN;

ARTICLE; CELL SIZE; CLINICAL PROTOCOL; CONTROLLED STUDY; EXPERIMENTAL DESIGN; HUMAN; IMAGE ANALYSIS; IMAGE PROCESSING; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DYNAMICS; MOLECULAR IMAGING; MOLECULAR SIZE; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; THREE DIMENSIONAL IMAGING; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; CHICK EMBRYO; CYTOLOGY; METABOLISM; PROCEDURES; SCANNING ELECTRON MICROSCOPY; TENDON; ULTRASTRUCTURE;

ANIMALS; CHICK EMBRYO; COLLAGEN; FIBRILLAR COLLAGENS; IMAGING, THREE-DIMENSIONAL; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; TENDONS;

EID: 84889681551     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2013.086     Document Type: Article

References (45)

1. Kadler, K.E., Baldock, C., Bella, J. & Boot-Handford, R.P. Collagens at a glance. J. Cell Sci. 120, 1955-1958 (2007).
2. Kadler, K.E., Holmes, D.F., Trotter, J.A. & Chapman, J.A. Collagen fibril formation. Biochem. J. 316 (Part 1), 1-11 (1996).
3. Parry, D.A., Barnes, G.R. & Craig, A.S. A comparison of the size distribution of collagen fibrils in connective tissues as a function of age and a possible relation between fibril size distribution and mechanical properties. Proc. R. Soc. Lond. B Biol. Sci. 203, 305-321 (1978).
4. Graham, H.K. et al. Tissue section AFM: in situ ultrastructural imaging of native biomolecules. Matrix Biol. 29, 254-260 (2010).
5. Trelstad, R.L. & Hayashi, K. Tendon collagen fibrillogenesis: intracellular subassemblies and cell surface changes associated with fibril growth. Dev. Biol. 71, 228-242 (1979).
6. Birk, D.E. & Trelstad, R.L. Extracellular compartments in tendon morphogenesis: collagen fibril, bundle, and macroaggregate formation. J. Cell Biol. 103, 231-240 (1986).
7. Canty, E.G. et al. Coalignment of plasma membrane channels and protrusions (fibripositors) specifies the parallelism of tendon. J. Cell Biol. 165, 553-563 (2004).
8. Canty, E.G. et al. Actin filaments are required for fibripositor-mediated collagen fibril alignment in tendon. J. Biol. Chem. 281, 38592-38598 (2006).
9. Leighton, S.B. SEM images of block faces, cut by a miniature microtome within the SEM - a technical note. Scan. Electron Microsc. 73-76 (1981).
10. Tapia, J.C. et al. High-contrast en bloc staining of neuronal tissue for field emission scanning electron microscopy. Nat. Protoc. 7, 193-206 (2012).
11. Andres, B. et al. 3D segmentation of SBFSEM images of neuropil by a graphical model over supervoxel boundaries. Med. Image Anal. 16, 796-805 (2012).
12. Briggman, K.L. & Bock, D.D. Volume electron microscopy for neuronal circuit reconstruction. Curr. Opin. Neurobiol. 22, 154-161 (2012).
13. Rouquette, J. et al. Revealing the high-resolution three-dimensional network of chromatin and interchromatin space: a novel electron-microscopic approach to reconstructing nuclear architecture. Chromosome Res. 17, 801-810 (2009).
14. Rezakhaniha, R., Fonck, E., Genoud, C. & Stergiopulos, N. Role of elastin anisotropy in structural strain energy functions of arterial tissue. Biomech. Model Mechanobiol. 10, 599-611 (2011).
15. Denk, W. & Horstmann, H. Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol. 2, e329 (2004).
16. Saalfeld, S., Cardona, A., Hartenstein, V. & Tomancak, P. As-rigid-as-possible mosaicking and serial section registration of large ssTEM datasets. Bioinformatics 26, i57-63 (2010).
17. Saalfeld, S., Fetter, R., Cardona, A. & Tomancak, P. Elastic volume reconstruction from series of ultra-thin microscopy sections. Nat. Methods 9, 717-720 (2012).
18. Kaynig, V., Fuchs, T.J. & Buhmann, J.M. Geometrical consistent 3D tracing of neuronal processes in ssTEM data. Med. Image Comput. Comput. Assist Interv. 13, 209-216 (2010).
19. Briggman, K.L., Helmstaedter, M. & Denk, W. Wiring specificity in the direction-selectivity circuit of the retina. Nature 471, 183-188 (2011).
20. Williams, M.E. et al. Cadherin-9 regulates synapse-specific differentiation in the developing hippocampus. Neuron 71, 640-655 (2011).
21. Graham, H.K., Holmes, D.F., Watson, R.B. & Kadler, K.E. Identification of collagen fibril fusion during vertebrate tendon morphogenesis. The process relies on unipolar fibrils and is regulated by collagen- proteoglycan interaction. J. Mol. Biol. 295, 891-902 (2000).
22. Holmes, D.F., Tait, A., Hodson, N.W., Sherratt, M.J. & Kadler, K.E. Growth of collagen fibril seeds from embryonic tendon: fractured fibril ends nucleate new tip growth. J. Mol. Biol. 399, 9-16 (2010).
23. Kalson, N.S. et al. Slow stretching that mimics embryonic growth rate stimulates structural and mechanical development of tendon-like tissue in vitro. Develop. Dynam. 240, 2520-2528 (2011).
24. Trotter, J.A., Kadler, K.E. & Holmes, D.F. Echinoderm collagen fibrils grow by surface-nucleation-and-propagation from both centers and ends. J. Mol. Biol. 300, 531-540 (2000).
25. Vogel, A., Holbrook, K.A., Steinmann, B., Gitzelmann, R. & Byers, P.H. Abnormal collagen fibril structure in the gravis form (type I) of Ehlers-Danlos syndrome. Lab. Invest. 40, 201-206 (1979).
26. Michalickova, K., Susic, M., Willing, M.C., Wenstrup, R.J. & Cole, W.G. Mutations of the α2(V) chain of type V collagen impair matrix assembly and produce Ehlers-Danlos syndrome type I. Hum. Mol. Genet. 7, 249-255 (1998).
27. Burrows, N.P. et al. A point mutation in an intronic branch site results in aberrant splicing of COL5A1 and in Ehlers-Danlos syndrome type II in two British families. Am. J. Hum. Genet. 63, 390-398 (1998).
28. Richards, A.J. et al. A single base mutation in COL5A2 causes Ehlers-Danlos syndrome type II. J. Med. Genet. 35, 846-848 (1998).
29. Watson, R.B. et al. Ehlers-Danlos syndrome type VIIB. Incomplete cleavage of abnormal type I procollagen by N-proteinase in vitro results in the formation of copolymers of collagen and partially cleaved pNcollagen that are near circular in cross-section. J. Biol. Chem. 267, 9093-9100 (1992).
30. Colige, A. et al. Human Ehlers-Danlos syndrome type VII C and bovine dermatosparaxis are caused by mutations in the procollagen I N-proteinase gene. Am. J. Hum. Genet. 65, 308-317 (1999).
31. Danielson, K.G. et al. Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J. Cell Biol. 136, 729-743 (1997).
32. Myllyharju, J. & Kivirikko, K.I. Collagens and collagen-related diseases. Ann. Med. 33, 7-21 (2001).
33. Schneider, C.A., Rasband, W.S. & Eliceiri, K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675 (2012).
34. Craig, A.S., Birtles, M.J., Conway, J.F. & Parry, D.A. An estimate of the mean length of collagen fibrils in rat tail-tendon as a function of age. Connect. Tissue Res. 19, 51-62 (1989).
35. Starborg, T., Lu, Y., Huffman, A., Holmes, D.F. & Kadler, K.E. Electron microscope 3D reconstruction of branched collagen fibrils in vivo. Scand. J. Med. Sci. Sports 19, 547-552 (2009).
36. Trotter, J.A., Chapman, J.A., Kadler, K.E. & Holmes, D.F. Growth of sea cucumber collagen fibrils occurs at the tips and centers in a coordinated manner. J. Mol. Biol. 284, 1417-1424 (1998).
37. Holmes, D.F., Lowe, M.P. & Chapman, J.A. Vertebrate (chick) collagen fibrils formed in vivo can exhibit a reversal in molecular polarity. J. Mol. Biol. 235, 80-83 (1994).
38. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682 (2012).
39. Kremer, J.R., Mastronarde, D.N. & McIntosh, J.R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76 (1996).
40. Chapman, J.A., Tzaphlidou, M., Meek, K.M. & Kadler, K.E. The collagen fibril - a model system for studying the staining and fixation of a protein. Electron Microsc. Rev. 3, 143-182 (1990).
41. Knott, G., Marchman, H., Wall, D. & Lich, B. Serial section scanning electron microscopy of adult brain tissue using focused ion beam milling. J. Neurosci. 28, 2959-2964 (2008).
42. Kapacee, Z. et al. Tension is required for fibripositor formation. Matrix Biol. 27, 371-375 (2008).
43. Herchenhan, A. et al. Tenocyte contraction induces crimp formation in tendon-like tissue. Biomech. Model Mechanobiol. 11, 449-459 (2012).
44. Kadler, K.E., Hojima, Y. & Prockop, D.J. Collagen fibrils in vitro grow from pointed tips in the C- to N-terminal direction. Biochem. J. 268, 339-343 (1990).
45. Wong, J.K. et al. The cellular biology of flexor tendon adhesion formation: an old problem in a new paradigm. Am. J. Pathol. 175, 1938-1951 (2009).