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1 Department of Physics and Chemistry, Universidade Estadual do Ceara, Fortaleza, Ceara, Brazil; Biomedical Engineering, Boston University, Boston, MA, USA; Department of Physics, Universidade Federal do Ceara, Fortaleza, Ceara, Brazil
2 Biomedical Engineering, Boston University, Boston, MA, USA
3 Department of Physics, Universidade Federal do Ceara, Fortaleza, Ceara, Brazil
4 Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
* To whom correspondence should be addressed. E-mail: bsuki{at}bu.edu.
Collagen and elastin are thought to dominate the elasticity of the connective tissue including lung parenchyma. The glycosaminoglycans (GAGs) on the proteoglycans may also play a role since osmolarity of interstitial fluid can alter the repulsive forces on the negatively charged GAGs 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 (Ar) 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 Ar 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.
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