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Collagen Fibrillar Structure and Hierarchies

  • Chapter
Collagen

Abstract

Collagen is most commonly found in animals as long, slender generally cylindrical fibrillar structures with tapered ends that are most easily recognized by a 65–67 nm axial periodicity. Collagen fibrils are substantial constituents of skin, tendon, bone, ligament, cornea, and cartilage, where the fundamental tensile properties of the fibril are finely tuned to serve bespoke biomechanical, and less well understood structural signaling roles.

Many of these properties derive from the structural organization within a fibril, where the axial and lateral organization and topology of the collagen molecules ensure strong intermolecular interactions and cross-linkage. The presence of different collagen types within a single fibril is a structural prerequisite in many tissues. However, the necessity for heterotypic fibrillar structures may point to fine tuning of the structural properties in a composite, such as fibril size regulation, dispersion of crystallinity, and interfibrillar communication. Furthermore the specific properties of an individual tissue also rely on the suprafibrillar architecture at the mesoscopic level.

The chapter will discuss current information about fibrillar structure from both homo- and heterotypic fibrils from a structural and biochemical viewpoint. Fibrils rich in collagen I, II and III will be considered as will the contribution of minor fibrillar and FACIT collagens. The molecular organization in both axial and lateral senses will be reviewed for both helicoidal and quasi crystalline fibrillar structures. Current models that account for the dynamic behavior of collagen segments within the fibril will be reviewed and the basis for order and disorder within the fibril discussed. The discrete size and polydispersity of fibrils will be discussed in terms of tissue properties and characteristics. The surface features of fibrils will be considered which conveniently leads to the possible features of interfibrillar interactions.

The overall properties and morphology of a fibril are as important as its internal organization. For example, the fibril surface is a complex area that contains collagen molecules and a variety of proteoglycans. These dictate the interaction between fibrils and specify the environment of partner macromolecules. They are also important in restricting fibril growth and permitting fusion to occur. The defined diameter (or distribution of fibril diameters) and overall slender tapering of collagen fibrils has significance in determining the macroscopic mechanical properties of the tissues. The variety of local suprafibrillar and resultant architectures such as bundles, felt work, lamellae and fibers that are evidenced in tissues will be discussed.

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References

  • Adachi, E. and Hayashi, T. (1986). In vitro formation of hybrid fibrils of type-V collagen and type-I collagen – Limited growth of type-I collagen into thick fibrils by type-V collagen. Connect. Tissue Res. 14, 257–266.

    Article  Google Scholar 

  • Bailey, A. J. (2001). Molecular mechanisms of ageing in connective tissues. Mech. Ageing Dev. 122, 735–755.

    Article  Google Scholar 

  • Baselt, D. R., Revel, J. P., and Baldeschwieler, J. D. (1993). Subfibrillar structure of type-I collagen observed by atomic-force microscopy. Biophys. J. 65, 2644–2655.

    Google Scholar 

  • Birk, D. E. (2001). Type V collagen: Heterotypic type I/V collagen interactions in the regulation of fibril assembly. Micron 32, 223–237.

    Article  Google Scholar 

  • Birk, D. E. and Trelstad, R. L. (1996). Extracellular compartments in tendon morphogenesis: collagen fibril, bundle, and macroaggregate formation. J. Cell Biol. 103, 231–240.

    Article  Google Scholar 

  • Birk, D. E., Zychband, E. I., Woodruff, S., Winkelmann, D. A., and Trelstad, R. L. (1997). Collagen fibrillogenesis in situ: Fibril segments become long fibrils as the developing tendon matures. Dev. Dyn. 208, 291–298.

    Article  Google Scholar 

  • Bishop, P. N. (2000). Structural macromolecules and supramolecular organisation of the vitreous gel. Prog. Retin. Eye Res. 19, 323–344.

    Article  MathSciNet  Google Scholar 

  • Blaschke, U. K., Eikenberry, E. F., Hulmes, D. J. S., Galla, H. J., and Bruckner, P. (2000). Collagen XI nucleates self-assembly and limits lateral growth of cartilage fibrils. J. Biol. Chem. 275, 10370–10378.

    Article  Google Scholar 

  • Bos, K. J., Holmes, D. F. Meadows, R. S., Kadler, K. E., McLeod, D., and Bishop, P. N. (2001). Collagen fibril organisation in mammalian vitreous by freeze etch/rotary shadowing electron microscopy. Micron 32, 301–306.

    Article  Google Scholar 

  • Bozec L, van der Heijden G, and Horton, M. (2007). Collagen fibrils: nanoscale ropes. Biophys J. 92, 70–75.

    Article  Google Scholar 

  • Brodsky, B., Eikenberry, E. F., and Cassidy, K. (1980). An unusual collagen periodicity in skins. Biochim. Biophys. Acta. 621, 162–166.

    Google Scholar 

  • Brown, E. M., King, G., and Chen, J. M. (1997). Model of the helical portion of a type I collagen microfibril. J. Am. Leather Chem. As. 92, 1–7.

    Google Scholar 

  • Buehler, M. K. (2006). Nature designs tough collagen: Explaining the nanostructure of collagen fibrils. PNAS 103, 12285–12290.

    Article  Google Scholar 

  • Burgeson, R. E. (1988). New collagens, new concepts. Ann. Rev. Cell Biol. 4, 551–577.

    Google Scholar 

  • Cameron, G. J., Alberts, I. L., Laing, J. H., and Wess, T. J. (2002). Structure of type I and type III heterotypic collagen fibrils: An X-ray diffraction study. J. Struct. Biol. 137, 15–22.

    Article  Google Scholar 

  • Cameron, G. J, Cairns, D. E, and Wess, T. J. (2007). The variability in type I collagen helical pitch is reflected in the D periodic fibrillar structure. J Mol Biol. 28;372(4),1097–1107.

    Article  Google Scholar 

  • Chakravarti, S., Magnuson, T., Lass, J. H., Jepsen, K. J., LaMantia, C., and Carroll, H. (1998). Lumican regulates collagen fibril assembly: Skin fragility and corneal opacity in the absence of lumican. J. Cell Biol. 141, 1277–1286.

    Article  Google Scholar 

  • Chanut-Delalande, H., Fichard, A., Bernocco, S., Garrone, R., Hulmes, D. J. S., and Ruggiero, F. (2001). Control of heterotypic fibril formation by collagen V is determined by chain stoichiometry. J. Biol. Chem. 276, 24352–24359.

    Google Scholar 

  • Chapman, J. A. (1989). The regulation of size and form in the assembly of collagen fibrils in vivo. Biopolymers 28, 1367–1382.

    Article  Google Scholar 

  • Christiansen, D. L., Huang, E. K., Silver, F. H., and Christiansen, U. (2000). Assembly of type I collagen: fusion of fibril subunits and the influence of fibril diameter on mechanical properties. Matrix Biol. 19, 409–420.

    Article  Google Scholar 

  • Craig, A. S., Birtles, M. J., Conway, J. F., and Parry, D. A. D. (1989). An estimate of the mean length of collagen fibrils in rat tail tendon as a function of age. Connect. Tissue Res.19, 51–62.

    Article  Google Scholar 

  • Danielson, K. G., Siracusa, L. D., Donovan, P. J., and Iozzo, R. V. (1999). Decorin, epiphycan, and lumican genes are closely linked on murine chromosome 10 and are deleted in lethal steel mutants. Mamm. Genome 10, 201–203.

    Article  Google Scholar 

  • Derwin, K. A., Soslowsky, L. J., Kimura, J. H., and Plaas, A. H. (2001). Proteoglycans and glycosaminoglycan fine structure in the mouse tail tendon fascicle. J. Orthop. Res. 19, 269–277.

    Article  Google Scholar 

  • Eikenberry, E. F., Childs, B., Sheren, S. B., Parry, D. A. D., Craig, A. S., and Brodsky, B. (1984). Crystalline fibril structure of type-II collagen in lamprey notochord sheath. J. Mol. Biol. 176, 261–277.

    Article  Google Scholar 

  • Eyre, D. R. (2002). Collagen of articular cartilage. Arthritis Res. 4, 30–35.

    Article  Google Scholar 

  • Eyre, D. R., Pietka, T., Weis, M. A., and Wu, J. J. (2004). Covalent cross-linking of the NC1 domain of collagen type IX to collagen type II in cartilage. J. Biol. Chem. 279, 2568–2574.

    Article  Google Scholar 

  • Folkhard, W., Christmann, D., Geercken, W., Knorzer, E., Koch, M. H., Mosler, E., Nemetschek-Gansler, H., and Nemetschek, T. (1987a). Twisted fibrils are a structural principle in the assembly of interstitial collagens, chordae tendinae included. Z. Naturforsch. [C] 42, 1303–1306.

    Google Scholar 

  • Folkhard, W., Mosler, E., Geercken, E., Knorzer, H., Nemetschek-Gansler, H., and Nemetschek, T. (1987b). Quantitative analysis of the molecular sliding mechanism in native tendon collagen – Time resolved dynamic studies using synchrotron radiation. Int. J. Biol. Macromol.9, 169–175.

    Google Scholar 

  • Franc, S. (1993). Ultrastructural evidences of a distinct axial domain within native rat tail tendon collagen fibrils. J. Submicrosc. Cytol. Pathol. 25, 85–91.

    Google Scholar 

  • Fraser, R. D. B., MacRae, T. P., Miller, A., and Suzuki, E. (1983). Molecular conformation and packing in collagen fibrils. J. Mol. Biol. 167, 497–521.

    Article  Google Scholar 

  • Fraser, R. D. B., MacRae, T. P., and Miller, A. (1987). Molecular packing in type I collagen fibrils. J. Mol. Biol. 193, 115–125.

    Article  Google Scholar 

  • Fratzl, P. (2003). Cellulose and collagen: from fibres to tissues. Curr. Opin. Colloid Interface Sci. 8, 32–39.

    Article  Google Scholar 

  • Fratzl, P., Fratzl-Zelman, N., and Klaushofer, K. (1993). Collagen packing and mineralization. An X-ray scattering investigation of turkey leg tendon. Biophys. J. 64, 260–266.

    Google Scholar 

  • Fratzl, P., Gupta, H. S., Paschalisb, E. P., and Roschgerb, P. (2004). Structure and mechanical quality of the collagen–mineral nano-composite in bone. J. Mater. Chem. 14, 2115–2123.

    Article  Google Scholar 

  • Fratzl, P., Misof, K., Zizak, I., Rapp, G., Amenitsch, H., and Bernstorff, S. (1998). Fibrillar structure and mechanical properties of collagen. J. Struct. Biol. 122, 119–122.

    Article  Google Scholar 

  • Giraud-Guille, M.-M. (1996). Twisted liquid crystalline supramolecular arrangements in morphogenesis. Int. Rev. Cytol. 166, 59–101.

    Google Scholar 

  • Goh, K. L., Hiller, J., Haston, J. L., Holmes, D. F., Kadler, K. E., Murdoch, A., Meakin, J. R., and Wess, T. J. (2005). Analysis of collagen fibril diameter distribution in connective tissues using small-angle X-ray scattering. Biochim. Biophys. Acta. 1722, 183–188.

    Google Scholar 

  • Graham, H. K., Holmes, D. F., Watson, R. B., and Kadler, K. E. (2000), 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.

    Article  Google Scholar 

  • Gutsmann, T., Fantner, G. E., Venturoni, M., Ekani-Nkodo, A., Thompson, J. B., Kindt, J. H., Morse, D. E., Fygenson, D. K., and Hansma, P. K. (2003). Evidence that collagen fibrils in tendons are inhomogeneously structured in a tubelike manner. Biophys. J. 84, 2593–2598.

    Google Scholar 

  • Hansen, U., and Bruckner, P. (2003). Macromolecular specificity of collagen fibrillogenesis. Fibrils of collagens I and XI contain a heterotypic alloyed core and a collagen I sheath. J. Biol. Chem. 278, 37352–37359.

    Article  Google Scholar 

  • Hedlund, H., Hedbom, E., Heinegard, D., Mengarelli-Widholm, S., Reinholt, F. P., and Svensson, O. (1999). Association of the aggrecan keratan sulfate-rich region with collagen in bovine articular cartilage. J. Biol. Chem. 274, 5777–5781.

    Article  Google Scholar 

  • Hedlund, H., Mengarelli-Widholm, S., Heinegard, D., Reinholt, F. P., and Svensson, O. (1994). Fibromodulin distribution and association with collagen. Matrix Biol. 14, 227–232.

    Article  Google Scholar 

  • Henkel, W. (1996). Cross-link analysis of the C-telopeptide domain from type III collagen. Biochem. J. 318, 497–503.

    Google Scholar 

  • Henkel, W., and Glanville, R. W. (1982). Covalent crosslinking between molecules of type I and type III collagen. The involvement of the N-terminal, nonhelical regions of the alpha 1 (I) and alpha 1 (III) chains in the formation of intermolecular crosslinks. Eur. J. Biochem. 122, 205–213.

    Article  Google Scholar 

  • Hodge, A. J., and Petruska, J. A. (1963). Recent studies with the electron microscope on ordered aggregates of the tropocollagen molecule. In “Aspects of Protein Chemistry” (G. N. Ramachandran, Ed.), pp. 289–300. Academic Press, London.

    Google Scholar 

  • Hofmann, H., Fietzek, P. P., and Kuhn, K. (1980). Comparative analysis of the sequences of the three collagen chains a1(I), a2 and a1(III); Function and genetic aspects. J. Mol. Biol. 141, 293–314.

    Article  Google Scholar 

  • Holmes, D. F., Gilpin, C. J., Baldock, C., Ziese, U., Koster, A. J., and Kadler, K. E. (2001). Corneal collagen fibril structure in three dimensions: Structural insights into fibril assembly, mechanical properties, and tissue organization. PNAS 98, 7307–7312.

    Article  Google Scholar 

  • Holmes, D. F. and Kadler, K. E. (2006). The 10+4 microfibril structure of thin cartilage fibrils. PNAS 103, 17249–17254.

    Article  Google Scholar 

  • Hoshi, K., Kemmotsu, S., Takeuchi, Y., Amizuka, N., and Ozawa, H. (1999). The primary calcification in bones follows removal of decorin and fusion of collagen fibrils. J. Bone Miner. Res. 14, 273–280.

    Article  Google Scholar 

  • Hulmes, D. J. S. (2002). Building collagen molecules, fibrils, and suprafibrillar structures. J. Struct. Biol. 137, 2–10.

    Article  Google Scholar 

  • Hulmes, D. J. S., Holmes, D. F., and Cummings, C. (1985). Crystalline regions in collagen fibrils. J. Mol. Biol. 184, 473–477.

    Article  Google Scholar 

  • Hulmes, D. J. S., Miller, A., Parry, D. A. D., Piez, K. A., and Woodhead-Galloway, J. (1973). Analysis of the primary structure of collagen for the origins of molecular packing. J. Mol. Biol. 79, 137–148.

    Article  Google Scholar 

  • Hulmes, D. J. S., Miller, A., White, S. W., and Brodsky-Doyle, B. (1977). Interpretation of the meridional diffraction pattern from collagen fibres in terms of the known amino acid sequence. J. Mol. Biol. 110, 643–666.

    Article  Google Scholar 

  • Hulmes, D. J. S., Miller, A., White, S. W., Timmins, P. A., and Berthet-Colominas, C. (1980). Interpretation of the low angle meridional neutron diffraction patterns from collagen fibres in terms of the amino acid sequence. Int. J. Biol. Macromol. 2, 338–345.

    Article  Google Scholar 

  • Hulmes, D. J. S., Wess, T. J., Prockop, D. J., and Fratzl, P. (1995). Radial packing, order and disorder in collagen fibrils. Biophys. J. 68, 1661–1670.

    Article  Google Scholar 

  • Hwang, W. S., Li, B., Jin, L. H., Ngo, K., Schachar, N. S., and Hughes, G. N. F. (1992). Collagen fibril structure of normal, aging, and osteoarthritic cartilage. J. Pathol. 167, 425–433.

    Article  Google Scholar 

  • Itoh, T., Kobayashi, M., and Hashimoto, M. (1998). The role of intermolecular electrostatic interaction on appearance of the periodic band structure in type I collagen fibril. Jpn. J. Appl. Phys. 37, L190–L192.

    Google Scholar 

  • Jeffery, A. K., Blunn, G. W., Archer, C. W. and Bentley, G. (1991). Three-dimensional collagen architecture in bovine articular cartilage. J. Bone Joint Surg. Br. 73-B, 795–801.

    Google Scholar 

  • Jesoir, J. C., Miller, A., and Berthet-Colominas, C. (1981). Crystalline three dimensional packing is a general feature of type I collagen fibrils. FEBS Lett. 13, 238–240.

    Google Scholar 

  • Jokinen, J., Dadu, E., Nykvist, P., Köpylö, J., White, D. J., Ivaska, J., Vehvilöinen, P., Reunanen, H., Larjava, H., Hökkinen, L., and Heino, J. (2004). Integrin-mediated cell adhesion to type I collagen fibrils. J. Biol. Chem. 279, 31956-31963.

    Article  Google Scholar 

  • Jones, E. Y., and Miller, A. (1991). Analysis of structural design features in collagen. J. Mol. Biol. 218, 209–219.

    Article  Google Scholar 

  • Kadler, K. (1994). Extracellular matrix. 1: fibril-forming collagens. Protein Profile 1, 519–638.

    Google Scholar 

  • Kannus, P. (2000). Structure of the tendon connective tissue. Scand. J. Med. Sci. Spor. 10, 312–320.

    Article  Google Scholar 

  • Kassner, A., Tiedemann, K., Notbohm, M., Ludwig, T., Morgelin, M., Reinhardt, D. P., Chu, M. L., Bruckner, P., and Grassel, S. (2004). Molecular structure and interaction of recombinant human type XVI collagen. J. Mol. Biol. 339, 835–853.

    Article  Google Scholar 

  • Kastelic, J., Galeski, A., and Baer, E. (1978). Multicomposite structure of tendon. Connect. Tissue Res. 6, 11–23.

    Google Scholar 

  • Knight, D. P., and Vollrath, F. (2002). Biological liquid crystal elastomers. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 357, 155–163.

    Article  Google Scholar 

  • Koch, M., Laub, F., Zhou, P., Hahn, R. A., Tanaka, S., Burgeson, R. E., Gerecke, D. R., Ramirez, F., and Gordon, M. K. (2003). Collagen XXIV, a vertebrate fibrillar collagen with structural features of invertebrate collagens selective expression in developing cornea and bone. J. Biol. Chem. 278(44), 43236–43244.

    Article  Google Scholar 

  • Landis, W. J., Hodgens, K. J., Song, M. J., Arena, J., Kiyonaga, S., Marko, M., Owen, C., and McEwen, B. F. (1996). Mineralization of collagen may occur on fibril surfaces: Evidence from conventional and high-voltage electron microscopy and three dimensional imaging. J. Struct. Biol. 117, 24–35.

    Article  Google Scholar 

  • Linsenmayer, T. F., Gibney, E., Igoe, F., Gordon, M. K., Fitch, J. M., Fessler, L. I., and Birk, D. E. (1993). 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, 1181–1189.

    Article  Google Scholar 

  • Liu, X. H., Otter, A., Scott, P. G., Cann, J. R., and Kotovych, G. (1993). Conformational analysis of the type-II and type-III collagen alpha-1 chain C-telopeptides by H- 1–nmr and circular-dichroism spectroscopy. J. Biomol. Struct. Dyn. 11, 541–555.

    Google Scholar 

  • Lucic, D., Mollenhauer, J., Kilpatrick, K. E., and Cole, A. A. (2003). N-telopeptide of type II collagen interacts with annexin V on human chondrocytes. Connect. Tissue Res.44, 225–239.

    Article  Google Scholar 

  • MacBeath, J. R., Shackleton, D. R., and Hulmes, D. J. S. (1993). Tyrosine-rich acidic matrix protein (TRAMP) accelerates collagen fibril formation in vitro. J. Biol. Chem. 268, 19826–19832.

    Google Scholar 

  • McBride, D. J., Choe, V., Shapiro, J. R., and Brodsky, B. (1997). Altered collagen structure in mouse tail tendon lacking the alpha 2(I) chain. J. Mol. Biol. 270, 275–284.

    Article  Google Scholar 

  • Malone, J. P., George, A., and Veis, A. (2004). Type I collagen N-telopeptides adopt an ordered structure when docked to their helix receptor during fibrillogenesis. Proteins 54, 206–215.

    Article  Google Scholar 

  • Marchant, J. K., Hahn, R. A., Linsenmayer, T. F., and Birk, D. E. (1996). Reduction of type V collagen using a dominant-negative strategy alters the regulation of fibrillogenesis and results in the loss of corneal-specific fibril morphology. J. Cell Biol. 135, 1415–1426.

    Article  Google Scholar 

  • Marchini, M., Morocutti, M., Ruggeri, A., Koch, M. H. J., Bigi, A., and Roveri, N. (1986). Differences in the fibril structure of corneal and tendon collagen. An electron microscopy and X-ray diffraction investigation. Connect. Tissue Res. 15, 269–281.

    Article  Google Scholar 

  • Martin, R., Farjanel, J., Eichenberger, D., Colige, A., Kessler, E., Hulmes, D. J. S., and Giraud-Guille, M. M. (2000). Liquid crystalline ordering of procollagen as a determinant of three-dimensional extracellular matrix architecture. J. Mol. Biol. 301, 11–17.

    Article  Google Scholar 

  • Meek, K. M., Chapman, J. A., and Hardcastle, R. A. (1979). The staining pattern of collagen fibrils. Improved correlation with sequence data. J. Biol. Chem. 254, 10710–10714.

    Google Scholar 

  • Meek, K. M., and Fullwood, N. J. (2001). Corneal and scleral collagens – A microscopist’s perspective. Micron 32, 261–272.

    Article  Google Scholar 

  • Mendler, M., Eich-Bender, S. G., Vaughan, L., Winterhalter, K. H. and Bruckner, P. (1989). Cartilage contains mixed fibrils of collagen types II, IX, and XI. J. Cell Biol., 108, 191–197.

    Article  Google Scholar 

  • Michna, H. (1984). Morphometric analysis of loading-induced changes in collagen fibril populations in young tendons. Cell Tissue Res. 236, 465–470.

    Article  Google Scholar 

  • Miles, C. A, Sims, T. J, Camacho, N. P, and Bailey, A. J. (2002). The role of the alpha2 chain in the stabilization of the collagen type I heterotrimer: a study of the type I homotrimer in oim mouse tissues. J. Mol. Biol. 321, 797–805.

    Article  Google Scholar 

  • Miller, A., and Tochetti, D. (1981). Calculated X-ray diffraction pattern from a quasihexagonal model for the molecular arrangement in collagen. Int. J. Macromol. 3, 9–18.

    Article  Google Scholar 

  • Mizuno, K., Adachi, E., Imamura, Y., Katsumata, O., and Hayashi, T. (2001). The fibril structure of type V collagen triple-helical domain. Micron 32, 317–323.

    Article  Google Scholar 

  • Niyibizi, C. and Eyre, D. R. (1994). Structural characteristics of cross-linking sites in type V collagen of bone. Chain specificities and heterotypic links to type I collagen. Eur. J. Biochem. 224, 943–950.

    Article  Google Scholar 

  • North, A. C. T., Cowan, P. M., and Randall, J. T. (1954). Structural units in collagen fibrils. Nature 174, 1142–1143.

    Article  Google Scholar 

  • Olsen, B. R. (1997). Collagen IX. Int. J. Biochem. Cell Biol. 29, 555–558.

    Article  Google Scholar 

  • Orgel, J. P. R. O., Irving, T. C., Miller, A., and Wess, T. J. (2006). Microfibrillar structure of type I collagen in situ. PNAS 103, 9001–9005.

    Article  Google Scholar 

  • Orgel, J. P. R. O., Miller, A., Irving, T. C., Fischetti, R. F., Hammersley, A. P., and Wess, T. J. (2001). The in situ supermolecular structure of type I collagen. Structure 9, 1061–1069.

    Article  Google Scholar 

  • Orgel, J. P., Wess, T. J., and Miller, A. (2000). The in situ conformation and axial location of the intermolecular cross-linked non-helical telopeptides of type I collagen. Struct. Fold. Des. 8, 137–142.

    Article  Google Scholar 

  • Ortolani, F., Giordano, M., and Marchini, M. (2000). A model for type II collagen fibrils: Distinctive D-band patterns in native and reconstituted fibrils compared with sequence data for helix and telopeptide domains. Biopolymers 54, 448–463.

    Article  Google Scholar 

  • Ottani, V., Raspanti, M., and Ruggeri, A. (2001). Collagen structure and functional implications. Micron 32, 251–260.

    Article  Google Scholar 

  • Parry, D. A. (1988). The molecular and fibrillar structure of collagen and its relationship to the mechanical properties of connective tissue. Biophys. Chem. 29, 195–209.

    Article  Google Scholar 

  • Parry, D. A. D., Barnes, G. R. G., and Craig, A. S. (1978). A comparison of the size distribution of collagen fibrils in connective tissues as a function of age and a possible relationship between fibril size distribution and mechanical properties. Proc. R. Soc. Lond. B. 203, 305–321.

    Google Scholar 

  • Parry, D. A. D., and Craig, A. S. (1979). Electron microscope evidence for an 80 Angstrom unit in collagen fibrils. Nature 282, 213–225.

    Article  Google Scholar 

  • Parry, D. A. D., and Craig, A. S. (1984). Growth and Development of Collagen Fibrils in Connective Tissues. In “Ultrastructure of the Connective Tissue Matrix” (A. Ruggeri and P. M. Motta, Eds.), pp. 34–64. Martinus Nijhoff, Netherlands.

    Google Scholar 

  • Paterlini, M. G., Nemethy, G., and Scheraga, H. A. (1995). The energy of formation of internal loops in triple-helical collagen polypeptides. Biopolymers 35, 607–619.

    Article  Google Scholar 

  • Patterson-Kane, J. C., Wilson, A. M., Firth, E. C., Parry, D. A. D., and Goodship, A. E. (1997). Comparison of collagen fibril populations in the superficial digital flexor tendons of exercised and non-exercised thoroughbreds. Equine Vet. J. 29, 121–125.

    Article  Google Scholar 

  • Pihlajamaa, T., Lankinen, H., Ylostalo, J., Valmu, L., Jaalinoja, J., Zaucke, F., Spitznagel, L., Gosling, S., Puustinen, A., Morgelin, M., Peranen, J., Maurer, P., Ala-Kokko, L., and Kilpelainen, I. (2004). Characterization of recombinant amino-terminal NC4 domain of human collagen IX: Interaction with glycosaminoglycans and cartilage oligomeric matrix protein. J. Biol. Chem. 279, 24265–24273.

    Article  Google Scholar 

  • Pope, F. M., Martin, G. R., Lichtenstein, J. R., Penttinen, R., Gerson, B., Rowe, D. W., and McKusick, V. A.. (1975). Patients with Ehlers-Danlos syndrome type IV lack type III collagen. PNAS 72, 1314–1316.

    Article  Google Scholar 

  • Prockop, D. J., and Fertala, A. (1998). The collagen fibril: the almost crystalline structure. J. Struct. Biol.122, 111–118.

    Article  Google Scholar 

  • Redaelli, A., Vesentini, S., Soncini, M., Vena, P., Mantero, S., and Montevecchi, F. M. (2003). Possible role of decorin glycosaminoglycans in fibril to fibril force transfer in relative mature tendons: A computational study from molecular to microstructural level. J. Biomech. 36,1555–1569.

    Article  Google Scholar 

  • Sanders, J. E., and Goldstein, B. S. (2001). Collagen fibril diameters increase and fibril densities decrease in skin subjected to repetitive compressive and shear stresses. J. Biomech. 34,1581–1587.

    Article  Google Scholar 

  • Sasaki, N., and Odajima, S. (1996). Elongation mechanism of collagen fibrils and forcestrain relations of tendon at each level of structural hierarchy. J. Biomech. 29, 1131–1136.

    Article  Google Scholar 

  • Sasaki, N., Shukunami, N., Matsushima, N., and Izumi, Y. (1999). Time resolved X-ray diffraction from tendon collagen during creep using synchrotron radiation. J. Biomech. 32, 285–292.

    Article  Google Scholar 

  • Scott, J. E., and Thomlinson, A. M. (1998). The structure of interfibrillar proteoglycan bridges (‘shape modules’) in extracellular matrix of fibrous connective tissues and their stability in various chemical environments. J. Anat. 192, 391–405.

    Article  Google Scholar 

  • Shaw, L. M., Olsen, B. R. (1991). FACIT collagens: diverse molecular bridges in extracellular matrices. Trends Biochem. Sci. 1, 191–194.

    Article  Google Scholar 

  • Silver, F. H., Christiansen, D. L., Snowhill, P. B., and Chen, Y. (2001). Transition from viscous to elastic-based dependency of mechanical properties of self-assembled type I collagen fibers. J. Appl. Polymer Sci. 79, 134–142.

    Article  Google Scholar 

  • Silver, F. H., Kato, Y. P., Ohno, M., Wasserman, A. J. (1992). Analysis of mammalian connective tissue: relationship between hierarchical structures and mechanical properties. J. Long Term Eff. Med. Implants. 2(2–3),165–98.

    Google Scholar 

  • Smith, J. W. (1968). Molecular pattern in native collagen. Nature 219, 157–158.

    Article  Google Scholar 

  • Svensson, L., Aszodi, A., Reinholt, F. P., Fassler, R., Heinegard, D., and Oldberg, A. (1999). Fibromodulin-null mice have abnormal collagen fibrils, tissue organization, and altered Lumican deposition in tendon. J. Biol. Chem. 274, 9636–9647.

    Article  Google Scholar 

  • Thomas, E. K., Nakamura, M., Wienke, D., Isacke, C. M., Pozzi, A., and Liang, P.. (2005). Endo180 binds to the C-terminal region of type I collagen. J. Biol. Chem. 280, 22596–22605.

    Article  Google Scholar 

  • Trus, B. L., and Piez, K. A. (1980). Compressed microfibril models of the nativecollagen fibril. Nature 286, 300–301.

    Article  Google Scholar 

  • van der Rest, M,, and Garrone, R. (1991). Collagen family of proteins. FASEB J 51, 2814-2823.

    Google Scholar 

  • Vaughan, L., Mendler, M., Huber, S., Bruckner, P., Winterhalter, K. H., Irwin, M. I., and Mayne, R. (1988). D-periodic Distribution of collagen type IX along cartilage fibrils. J. Cell Biol. 106, 991–997.

    Article  Google Scholar 

  • Vitagliano, L., Nemethy, G., Zagari, A., and Scheraga, H. A. (1995). Structure of the type-I collagen molecule based on conformational energy computations: The triple-stranded helix and the n-terminal telopeptide. J. Mol. Biol. 247, 69–80.

    Article  Google Scholar 

  • Watanabe, M., Kobayashi, M., Fujita, Y., Senga, K., Mizutani, H., Ueda, M., and Hoshino, T. (1997). Association of type VI collagen with D-periodic collagen fibrils in developing tail tendons of mice. Arch. Histol. Cytol. 60, 427–434.

    Article  Google Scholar 

  • Weiner, S., Traub, W., and Wagner, H. D. (1999). Lamellar bone: structure-function relations. J. Struct. Biol. 126, 241–255.

    Article  Google Scholar 

  • Wen, C. K., and Goh, M. C. (2004). AFM nanodissection reveals internal structural details of single collagen fibrils. Nano. Lett. 4, 129–132.

    Article  Google Scholar 

  • Wenstrup, R. J., Florer, J. B., Brunskill, E. W., Bell, S. B., Chervoneva, I., and Birk, D. E. (2004). Type V collagen controls the initiation of collagen fibril assembly. J. Biol. Chem. 279,53331–53337.

    Article  Google Scholar 

  • Wess, T. J., Hammersley, A., Wess, L., and Miller, A. (1995). Type I collagen packing conformation of the triclinic unit cell. J. Mol. Biol. 248, 487–493.

    Google Scholar 

  • Wess, T. J., Hammersley, A. P., Wess, L., and Miller, A. (1998). A consensus model for molecular packing of type I collagen. J. Struct. Biol. 122, 92–100.

    Article  Google Scholar 

  • White, J., Werkmeister, J. A., Ramshaw, J. A. M., and Birk, D. E. (1997). Organization of fibrillar collagen in the human and bovine cornea: Collagen types V and III. Connect. Tissue Res. 36, 165–174.

    Article  Google Scholar 

  • Wu JJ, Murray J, Eyre DR (1996). Evidence for copolymeric crosslinking between types II and III collagens in human articular cartilage. Trans. Orthop. Res. Soc. 21, 42.

    Google Scholar 

  • Yamamoto, T., Domon, T., Takahashi, S., Islam, N., and Suzuki, R. (2000b). Twisted plywood structure of an alternating lamellar pattern in cellular cementum of human teeth. Anat. Embryol. 202, 25–30.

    Article  Google Scholar 

  • Yamamoto, S., Hashizume, H., Hitomi, J., Shigeno, M., Sawaguchi, S., Abe, H., and Ushiki, T. (2000a). The subfibrillar arrangement of corneal and scleral collagen fibrils as revealed by scanning electron and atomic force microscopy. Arch. Histol. Cytol. 63, 127–135.

    Article  Google Scholar 

  • Yamamoto, T. and Wakita, M. (1992). Bundle formation of principal fibers in rat molars. J. Periodont. Res. 27, 20–27.

    Article  Google Scholar 

  • Yamamoto K, and Yamamoto, M. (1994). Cell adhesion receptors for native and denatured type I collagens and fibronectin in rabbit arterial smooth muscle cells in culture. Exp. Cell Res. 214, 258–263.

    Article  Google Scholar 

  • Yamazaki, M., Majeska, R. J., Yoshioka, T. H., Moriya, H., Thomas, A., and Einhorn, T. A. (2005). Spatial and temporal expression of fibril-forming minor collagen genes (types V and XI) during fracture healing. J. Orthop. Res. 15, 757–764.

    Article  Google Scholar 

  • Young, R. D., Lawrence, P. A., Duance, V. C., Aigner, T., and Monaghan, P. (2000a). Immunolocalization of collagen types II and III in single fibrils of human articular cartilage. J. Histochem. Cytochem. 48, 423–432.

    Google Scholar 

  • Zhang, G., Young, B. B., Ezura, Y., Favata, M., Soslowsky, L. J., Chakravarti, S., and Birk, D. E. (2005). Development of tendon structure and function: Regulation of collagen fibrillogenesis. J. Musculoskelet. Neuronal. Interact. 5, 5–21.

    Google Scholar 

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  1. T.J. Wess
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  1. Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, 14424 Potsdam, Germany

    Peter Fratzl

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Wess, T. (2008). Collagen Fibrillar Structure and Hierarchies. In: Fratzl, P. (eds) Collagen. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-73906-9_3

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