Molecular Biology of the Cell by Bruce Alberts, Alexander Johnson, Julian Lewis, David Morgan, Martin Raff, Keith Roberts, Peter Walter by by Bruce Alberts, Alexander Johnson, Julian Lewis, David Morg

1064 Chapter 19: Cell Junctions and the Extracellular Matrix
(B)
100 nm
(A)
type IX collagen
molecule
fibril of
type II collagen
(C)
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 MBoC6 m19.68/19.43 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.
1 mm
Figure 19–43 The shaping of the
extracellular matrix by cells. This
micrograph shows a region between two
pieces of embryonic chick heart (rich in
fibroblasts as well as heart muscle cells)
that were cultured
MBoC6
on
m19.69/19.44
a collagen gel for
4 days. A dense tract of aligned collagen
fibers has formed between the explants,
presumably as a result of the fibroblasts
in the explants tugging on the collagen.
(From D. Stopak and A.K. Harris, Dev. Biol.
90:383–398, 1982. With permission from
Academic Press.)