Chapter 17 Electron Microscopy of Collagen Fibril Structure In Vitro and In Vivo Including Three-Dimensional Reconstruction

Methods in Cell Biology

Volumn 88, Issue , 2008, Pages 319-345

  Starborg, Tobias ^a   Lu, Yinhui ^a   Kadler, Karl E ^a   Holmes, David F ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRILLAR COLLAGEN; PROCOLLAGEN;

ANIMAL; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; CYTOLOGY; ELECTRON MICROSCOPY; FIBROBLAST; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; METHODOLOGY; PHYSIOLOGY; REVIEW; SURFACE PROPERTY; TENDON; THREE DIMENSIONAL IMAGING; ULTRASTRUCTURE;

ANIMALS; COMPUTER SIMULATION; FIBRILLAR COLLAGENS; FIBROBLASTS; HUMANS; IMAGING, THREE-DIMENSIONAL; MICROSCOPY, ELECTRON; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROCOLLAGEN; SURFACE PROPERTIES; TENDONS;

EID: 46249124038     PISSN: 0091679X     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0091-679X(08)00417-2     Document Type: Review

References (75)

1. Baldock C., Gilpin C.J., Koster A.J., Ziese U., Kadler K.E., Kielty C.M., and Holmes D.F. Three-dimensional reconstructions of extracellular matrix polymers using automated electron tomography. J. Struct. Biol. 138 (2002) 130-136
2. Baldock C., Koster A.J., Ziese U., Rock M.J., Sherratt M.J., Kadler K.E., Shuttleworth C.A., and Kielty C.M. The supramolecular organization of fibrillin-rich microfibrils. J. Cell Biol. 152 (2001) 1045-1056
3. Barge A., Ruggiero F., and Garrone R. Structure of the basement membrane of corneal epithelium: Quick-freeze, deep-etch comparative study of networks deposited in culture and during development. Biol. Cell 72 (1991) 141-147
4. Baumeister W., and Steven A.C. Macromolecular electron microscopy in the era of structural genomics. Trends Biochem. Sci. 25 (2000) 624-631
5. Bergmanson J.P., Horne J., Doughty M.J., Garcia M., and Gondo M. Assessment of the number of lamellae in the central region of the normal human corneal stroma at the resolution of the transmission electron microscope. Eye Contact Lens 31 (2005) 281-287
6. Birk D.E. Type V collagen: Heterotypic type I/V collagen interactions in the regulation of fibril assembly. Micron 32 (2001) 223-237
7. Birk D.E., Fitch J.M., Babiarz J.P., and Linsenmayer T.F. Collagen type I and type V are present in the same fibril in the avian corneal stroma. J. Cell Biol. 106 (1988) 999-1008
8. Birk D.E., Nurminskaya M.V., and Zycband E.I. Collagen fibrillogenesis in situ: Fibril segments undergo post-depositional modifications resulting in linear and lateral growth during matrix development. Dev. Dyn. 202 (1995) 229-243
9. Birk D.E., Southern J.F., Zycband E.I., Fallon J.T., and Trelstad R.L. Collagen fibril bundles: A branching assembly unit in tendon morphogenesis. Development 107 (1989) 437-443 (Cambridge, England)
10. Birk D.E., and Trelstad R.L. Extracellular compartments in tendon morphogenesis: Collagen fibril, bundle, and macroaggregate formation. J. Cell Biol. 103 (1986) 231-240
11. Birk D.E., Zycband E.I., Winkelmann D.A., and Trelstad R.L. Collagen fibrillogenesis in situ: Fibril segments are intermediates in matrix assembly. Proc. Natl. Acad. Sci. USA 86 (1989) 4549-4553
12. Bos K.J., Holmes D.F., Meadows R.S., Kadler K.E., McLeod D., and Bishop P.N. Collagen fibril organisation in mammalian vitreous by freeze etch/rotary shadowing electron microscopy. Micron 32 (2001) 301-306
13. Canty E.G., and Kadler K.E. Procollagen trafficking, processing and fibrillogenesis. J Cell Sci. 118 (2005) 1341-1353
14. Canty E.G., Lu Y., Meadows R.S., Shaw M.K., Holmes D.F., and Kadler K.E. Coalignment of plasma membrane channels and protrusions (fibripositors) specifies the parallelism of tendon. J. Cell Biol. 165 (2004) 553-563
15. Canty E.G., Starborg T., Lu Y., Humphries S.M., Holmes D.F., Meadows R.S., Huffman A., O'Toole E.T., and Kadler K.E. Actin filaments are required for fibripositor-mediated collagen fibril alignment in tendon. J. Biol. Chem. 281 (2006) 38592-38598
16. Capaldi M.J., and Chapman J.A. The C-terminal extrahelical peptide of type I collagen and its role in fibrillogenesis in vitro. Biopolymers 21 (1982) 2291-2313
17. Chapman J.A., Tzaphlidou M., Meek K.M., and Kadler K.E. The collagen fibril-A model system for studying the staining and fixation of a protein. Electron Microsc. Rev. 3 (1990) 143-182
18. Colige A., Sieron A.L., Li S.W., Schwarze U., Petty E., Wertelecki W., Wilcox W., Krakow D., Cohn D.H., Reardon W., Byers P.H., and Lapière C.M. 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 (1999) 308-317
19. Eikenberry E.F., Childs B., Sheren S.B., Parry D.A., Craig A.S., and Brodsky B. Crystalline fibril structure of type II collagen in lamprey notochord sheath. J. Mol. Biol. 176 (1984) 261-277
20. Gelman R.A., Williams B.R., and Piez K.A. Collagen fibril formation. Evidence for a multistep process. J. Biol. Chem. 254 (1979) 180-186
21. Goh K.L., Meakin J.R., Aspden R.M., and Hukins D.W. Stress transfer in collagen fibrils reinforcing connective tissues: Effects of collagen fibril slenderness and relative stiffness. J. Theor. Biol. 245 (2007) 305-311
22. Graham H.K., Holmes D.F., Watson R.B., and 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 (2000) 891-902
23. Gross J., and Kirk D. The heat precipitation of collagen from neutral salt solutions: Some rate-regulating factors. J. Biol. Chem. 233 (1958) 355-360
24. Hirsch M., Noske W., Prenant G., and Renard G. Fine structure of the developing avian corneal stroma as revealed by quick-freeze, deep-etch electron microscopy. Exp. Eye Res. 69 (1999) 267-277
25. Hodge A.J. Molecular models illustrating the possible distributions of "holes" in simple systematically staggered arrays of type I collagen molecules in native-type fibrils. Connect Tissue Res. 21 (1989) 137-147
26. Hoffpauir B.K., Pope B.A., and Spirou G.A. Serial sectioning and electron microscopy of large tissue volumes for 3D analysis and reconstruction: A case study of the calyx of Held. Nat. Protocols 2 (2007) 9-22
27. Holmes D.F., Capaldi M.J., and Chapman J.A. Reconstitution of collagen fibrils in vitro; the assembly process depends on the initiating procedure. Int. J. Biol. Macromol. 8 (1986) 161-166
28. Holmes D.F., Gilpin C.J., Baldock C., Ziese U., Koster A.J., and Kadler K.E. Corneal collagen fibril structure in three dimensions: Structural insights into fibril assembly, mechanical properties, and tissue organization. Proc. Natl. Acad. Sci. USA 98 (2001) 7307-7312
29. Holmes D.F., Graham H.K., and Kadler K.E. Collagen fibrils forming in developing tendon show an early and abrupt limitation in diameter at the growing tips. J. Mol. Biol. 283 (1998) 1049-1058
30. Holmes D.F., Graham H.K., Trotter J.A., and Kadler K.E. STEM/TEM studies of collagen fibril assembly. Micron 32 (2001) 273-285
31. Holmes D., and Kadler K. Protocol 6.44 Collagen fibril assembly in vitro. In: Harris J.R., Graham J.M., and Rickwood D. (Eds). Cell Biology Protocols (2006), Wiley, Chichester, UK 375-378
32. Holmes D.F., and Kadler K.E. The 10 + 4 microfibril structure of thin cartilage fibrils. Proc. Natl. Acad. Sci. USA 103 (2006) 17249-17254
33. Holmes D.F., Lowe M.P., and Chapman J.A. Vertebrate (chick) collagen fibrils formed in vivo can exhibit a reversal in molecular polarity. J. Mol. Biol. 235 (1994) 80-83
34. Hulmes D.J., Bruns R.R., and Gross J. On the state of aggregation of newly secreted procollagen. Proc. Natl. Acad. Sci. USA 80 (1983) 388-392
35. Hulmes D.J., and Miller A. Quasi-hexagonal molecular packing in collagen fibrils. Nature 282 (1979) 878-880
36. Huxley-Jones J., Robertson D.L., and Boot-Handford R.P. On the origins of the extracellular matrix in vertebrates. Matrix Biol. 26 (2007) 2-11
37. Kadler K.E., Baldock C., Bella J., and Boot-Handford R.P. Collagens at a glance. J. Cell. Sci. 120 (2007) 1955-1958
38. Kadler K.E., Hojima Y., and Prockop D.J. Assembly of collagen fibrils de novo by cleavage of the type I pC-collagen with procollagen C-proteinase. Assay of critical concentration demonstrates that collagen self-assembly is a classical example of an entropy-driven process. J. Biol. Chem. 262 (1987) 15696-15701
39. Kannus P. Structure of the tendon connective tissue. Scand. J. Med. Sci. Sports 10 (2000) 312-320
40. Keene D.R., Oxford J.T., and Morris N.P. Ultrastructural localization of collagen types II, IX, and XI in the growth plate of human rib and fetal bovine epiphyseal cartilage: Type XI collagen is restricted to thin fibrils. J. Histochem. Cytochem. 43 (1995) 967-979
41. Koster A.J., Chen H., Sedat J.W., and Agard D.A. Automated microscopy for electron tomography. Ultramicroscopy 46 (1992) 207-227
42. Kremer J.R., Mastronarde D.N., and McIntosh J.R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116 (1996) 71-76
43. Lawrence A., Bouwer J.C., Perkins G., and Ellisman M.H. Transform-based backprojection for volume reconstruction of large format electron microscope tilt series. J. Struct. Biol. 154 (2006) 144-167
44. Leighton M., and Kadler K.E. Paired basic/Furin-like proprotein convertase cleavage of Pro-BMP-1 in the trans-Golgi network. J. Biol. Chem. 278 (2003) 18478-18484
45. Linsenmayer T.F., Gibney E., Igoe F., Gordon M.K., Fitch J.M., Fessler L.I., and Birk D.E. Type V collagen: Molecular structure and fibrillar organization of the chicken alpha 1(V) NH2-terminal domain, a putative regulator of corneal fibrillogenesis. J. Cell Biol. 121 (1993) 1181-1189
46. Ma B., Zimmermann T., Rohde M., Winkelbach S., He F., Lindenmaier W., and Dittmar K.E. Use of autostitch for automatic stitching of microscope images. Micron 38 (2007) 492-499
47. Mastronarde D.N. Dual-axis tomography: An approach with alignment methods that preserve resolution. J. Struct. Biol. 120 (1997) 343-352
48. Mastronarde D.N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152 (2005) 36-51
49. McDonald K.L., and Auer M. High-pressure freezing, cellular tomography, and structural cell biology. Biotechniques 41 (2006) 137 139, 141 passim
50. McIntosh R., Nicastro D., and Mastronarde D. New views of cells in 3D: An introduction to electron tomography. Trends Cell Biol. 15 (2005) 43-51
51. Morphew M.K. 3D immunolocalization with plastic sections. Methods Cell Biol. 79 (2007) 493-513
52. Mosser G., Anglo A., Helary C., Bouligand Y., and Giraud-Guille M.M. Dense tissue-like collagen matrices formed in cell-free conditions. Matrix Biol. 25 (2006) 3-13
53. Mould A.P., Holmes D.F., Kadler K.E., and Chapman J.A. Mica sandwich technique for preparing macromolecules for rotary shadowing. J. Ultrastruct. Res. 91 (1985) 66-76
54. Myllyharju J., and Kivirikko K.I. Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet. 20 (2004) 33-43
55. Nickell S., Kofler C., Leis A.P., and Baumeister W. A visual approach to proteomics. Nat. Rev. Mol. Cell Biol. 7 (2006) 225-230
56. O'Toole E.T., Giddings Jr. T.H., and Dutcher S.K. Understanding microtubule organizing centers by comparing mutant and wild-type structures with electron tomography. Methods Cell Biol. 79 (2007) 125-143
57. Orgel J.P., Irving T.C., Miller A., and Wess T.J. Microfibrillar structure of type I collagen in situ. Proc. Natl. Acad. Sci. USA 103 (2006) 9001-9005
58. Parry D.A., Barnes G.R., and 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 203 (1978) 305-321
59. Provenzano P.P., and Vanderby Jr. R. Collagen fibril morphology and organization: Implications for force transmission in ligament and tendon. Matrix Biol. 25 (2006) 71-84
60. Raspanti M., Viola M., Sonaggere M., Tira M.E., and Tenni R. Collagen fibril structure is affected by collagen concentration and decorin. Biomacromolecules 8 (2007) 2087-2091
61. Richardson S.H., Starborg T., Lu Y., Humphries S.M., Meadows R.S., and Kadler K.E. Tendon development requires regulation of cell condensation and cell shape via cadherin-11-mediated cell-cell junctions. Mol. Cell Biol 27 (2007) 6218-6228
62. Sandberg K. Methods for image segmentation in cellular tomography. Methods Cell Biol. 79 (2007) 769-798
63. Starborg T., and Kadler K.E. The power behind the electron microscopist. Biol. Sci. Rev. 18 (2005) 16-20
64. Suzuki N., Labosky P.A., Furuta Y., Hargett L., Dunn R., Fogo A.B., Takahara K., Peters D.M., Greenspan D.S., and Hogan B.L. Failure of ventral body wall closure in mouse embryos lacking a procollagen C-proteinase encoded by Bmp1, a mammalian gene related to Drosophila tolloid. Development 122 (1996) 3587-3595 (Cambridge, England)
65. Thurmond F.A., and Trotter J.A. Native collagen fibrils from echinoderms are molecularly bipolar. J. Mol. Biol. 235 (1994) 73-79
66. Tong J., Arslan I., and Midgley P. A novel dual-axis iterative algorithm for electron tomography. J. Struct. Biol. 153 (2006) 55-63
67. Trotter J.A., Chapman J.A., Kadler K.E., and Holmes D.F. Growth of sea cucumber collagen fibrils occurs at the tips and centers in a coordinated manner. J. Mol. Biol. 284 (1998) 1417-1424
68. Trotter J.A., Tipper J., Lyons-Levy G., Chino K., Heuer A.H., Liu Z., Mrksich M., Hodneland C., Dillmore W.S., Koob T.J., Koob-Emunds M.M., Kadler K., and Holmes D. Towards a fibrous composite with dynamically controlled stiffness: Lessons from echinoderms. Biochem. Soc. Trans. 28 (2000) 357-362
69. Trotter J.A., Kadler K.E., and Holmes D.F. Echinoderm collagen fibrils grow by surface-nucleation-and-propagation from both centers and ends. J. Mol. Biol. 300 (2000) 531-540
70. Wang W.M., Lee S., Steiglitz B.M., Scott I.C., Lebares C.C., Allen M.L., Brenner M.C., Takahara K., and Greenspan D.S. Transforming growth factor-beta induces secretion of activated ADAMTS-2. A procollagen III N-proteinase. J. Biol. Chem. 278 (2003) 19549-19557
71. Weinstock M., and Leblond C.P. Synthesis, migration, and release of precursor collagen by odontoblasts as visualized by radioautography after (3H) proline administration. J. Cell Biol. 60 (1974) 92-127
72. Wess T.J. Collagen fibril form and function. Adv. Protein Chem. 70 (2005) 341-374
73. Wood G.C., and Keech M.K. The formation of fibrils from collagen solutions. I. The effect of experimental conditions: Kinetic and electron-microscope studies. Biochem. J. 75 (1960) 588-598
74. Zheng S.Q., Keszthelyi B., Branlund E., Lyle J.M., Braunfeld M.B., Sedat J.W., and Agard D.A. UCSF tomography: An integrated software suite for real-time electron microscopic tomographic data collection, alignment, and reconstruction. J. Struct. Biol. 157 (2007) 138-147
75. Ziese U., Janssen A.H., Murk J.L., Geerts W.J., Van der Krift T., Verkleij A.J., and Koster A.J. Automated high-throughput electron tomography by pre-calibration of image shifts. J. Microsc. 205 (2002) 187-200