Mechanical interactions between collagen and proteoglycans: implications
for the stability of lung tissue
JOURNAL OF APPLIED PHYSIOLOGY, 98 (2):
672-679 (2005)DOI: 10.1152/japplphysiol.00619.2004
Abstract
Collagen and elastin are thought to dominate the elasticity of the
connective tissue including lung parenchyma. The glycosaminoglycans on
the proteoglycans may also play a role because osmolarity of
interstitial fluid can alter the repulsive forces on the negatively
charged glycosaminoglycans, allowing them to collapse or inflate, which
can affect the stretching and folding pattern of the fibers. Hence, we
hypothesized that the elasticity of lung tissue arises primarily from 1)
the topology of the collagen-elastin network and 2) the mechanical
interaction between proteoglycans and fibers. We measured the
quasi-static, uniaxial stress-strain curves of lung tissue sheets in
hypotonic, normal, and hypertonic solutions. We found that the
stress-strain curve was sensitive to osmolarity, but this sensitivity
decreased after proteoglycan digestion. Images of immunofluorescently
labeled collagen networks showed that the fibers follow the alveolar
walls that form a hexagonal-like structure. Despite the large
heterogeneity, the aspect ratio of the hexagons at 30% uniaxial strain
increased linearly with osmolarity. We developed a two-dimensional
hexagonal network model of the alveolar structure incorporating the
mechanical properties of the collagen-elastin fibers and their
interaction with proteoglycans. The model accounted for the
stress-strain curves observed under all experimental conditions. The
model also predicted how aspect ratio changed with osmolarity and
strain, which allowed us to estimate the Young's modulus of a single
alveolar wall and a collagen fiber. We therefore identify a novel and
important role for the proteoglycans: they stabilize the
collagen-elastin network of connective tissues and contribute to lung
elasticity and alveolar stability at low to medium lung volumes.