Figure 19–41 Collagen fibrils in the tadpole skin. this electron micrograph shows the plywoodlike arrangement of the fibrils: successive layers of fibrils are laid down nearly at right angles to each other. this organization is also found in mature bone and in the cornea. (Courtesy of Jerome Gross.) 5 µm (A) type IX collagen molecule fbril of type II collagen (B) (C) 100 nm Figure 19–42 Type IX collagen. (a) type IX collagen molecules binding  in a periodic pattern to the surface of a fibril containing type II collagen.  (B) Electron micrograph of a rotary-shadowed type-II-collagen-containing fibril in cartilage, decorated by type IX collagen molecules. (C) an individual type IX collagen molecule. (B and C, from L. Vaughan et al., J. Cell Biol. 106:991–997, 1988. With permission from the rockefeller University press.) molecules after secretion by guiding collagen fibril formation near the plasma membrane. In addition, cells can influence this organization by secreting, along with their fibrillar collagens, different kinds and amounts of other matrix macromolecules. In particular, they secrete the fibrous protein fibronectin, as we discuss later, and this precedes the formation of collagen fibrils and helps guide their organization.
Fibril-associated collagens, such as types IX and XII collagens, are thought to be especially important in organizing collagen fibrils. They differ from fibrillar collagens in the following ways. First, their triple-stranded helical structure is interrupted by one or two short nonhelical domains, which makes the molecules more flexible than fibrillar collagen molecules. Second, they do not aggregate with one another to form fibrils in the extracellular space. Instead, they bind in a periodic manner to the surface of fibrils formed by the fibrillar collagens. Type IX molecules bind to type-II-collagen-containing fibrils in cartilage, the cornea, and the vitreous of the eye (Figure 19–42), whereas type XII molecules bind to type-I-collagen-containing fibrils in tendons and various other tissues.
Fibril-associated collagens are thought to mediate the interactions of collagen fibrils with one another and with other matrix macromolecules to help determine the organization of the fibrils in the matrix.
Cells help Organize the Collagen Fibrils they Secrete by Exerting tension on the Matrix
Cells interact with the extracellular matrix mechanically as well as chemically, and studies in culture suggest that the mechanical interaction can have dramatic effects on the architecture of connective tissue. Thus, when fibroblasts are mixed with a meshwork of randomly oriented collagen fibrils that form a gel in a culture dish, the fibroblasts tug on the meshwork, drawing in collagen from their surroundings and thereby causing the gel to contract to a small fraction of its initial volume. By similar activities, a cluster of fibroblasts surrounds itself with a capsule of densely packed and circumferentially oriented collagen fibers.
If two small pieces of embryonic tissue containing fibroblasts are placed far apart on a collagen gel, the intervening collagen becomes organized into a compact band of aligned fibers that connect the two explants (Figure 19–43). The fibroblasts subsequently migrate out from the explants along the aligned collagen fibers. Thus, the fibroblasts influence the alignment of the collagen fibers, and the collagen fibers in turn affect the distribution of the fibroblasts.
Fibroblasts may have a similar role in organizing the extracellular matrix inside the body. First they synthesize the collagen fibrils and deposit them in the correct orientation. Then they work on the matrix they have secreted, crawling over it and tugging on it so as to create tendons and ligaments and the tough, dense layers of connective tissue that surround and bind together most organs.