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Biological Hydrogels As Selective Diffusion Barriers

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Biological Hydrogels As Selective Diffusion Barriers Review Biological hydrogels as selective diffusion barriers Oliver Lieleg and Katharina Ribbeck Department of Biological Engineering, Massachusetts Institute of Technology (MIT), 77 Massachusetts Avenue, Cambridge, MA 02139, USA The controlled exchange of molecules between orga- between different cells (Figure 2a). Similarly, the basal nelles, cells, or organisms and their environment is lamina creates an envelope around blood vessels, controls crucial for life. Biological gels such as mucus, the extra- the exchange of material between the bloodstream and the cellular matrix (ECM), and the biopolymer barrier within tissue, and governs angiogenesis [11]. the nuclear pore are well suited to achieve such a selec- The mucus layer of wet epithelia (Figure 2b) not only tive exchange, allowing passage of particular molecules serves as a lubricant but also acts as the first line of defense while rejecting many others. Although hydrogel-based of the body against pathogens, aids in the adsorption of filters are integral parts of biology, clear concepts of how nutrients to facilitate their uptake by the epithelium, and their barrier function is controlled at a microscopic level changes its properties to enable sperm migration through are still missing. We summarize here our current under- the gel during ovulation [12,13]. The selective permeability standing of how selective filtering is established by properties of mucus have a crucial role in health and different biopolymer-based hydrogels. We ask if the disease. Alterations in mucus permeability can result in modulation of microscopic particle transport in biologi- severe problems ranging from viral and parasitic infec- cal hydrogels is based on a generic filtering principle tions, and cystic fibrosis [14,15], to some forms of infertility which employs biochemical/biophysical interactions due to failure of the sperm to migrate through the female with the filtered molecules rather than size-exclusion genital tract. effects. The nuclear membrane in eukaryotic cells constitutes a major barrier that regulates the exchange of macromole- Biological hydrogels cules between the nucleus and cytoplasmic compartments Biological hydrogels are networks of protein–polysaccha- [16]. The exchange of material takes place through nuclear ride chains that typically contain 90–99% water. They pore complexes [17], large macromolecular assemblies that surround biological functional entities such as cells, tis- are filled with polymers and permit passage of specific sues, organs, or entire organisms. Past research has prin- transporter molecules (nuclear transport receptors), but cipally focused on the mechanical characteristics of reject the majority of cytoplasmic proteins (Figure 2c). biological gels. These gels can cover a wide spectrum of ECM, mucus and nuclear pore complexes can seem very material properties, ranging from relatively soft and vis- different with respect to their composition and function. cous-like to highly elastic. Indeed, biological hydrogels Even so, all three systems are based on hydrogels that act establish and regulate the mechanical properties of cells as diffusion barriers by allowing the passage of some types and tissues [1,2] and serve as lubricants in joints or on of macromolecules, while rejecting many others. epithelial surfaces [3–5]. We highlight below the mechanisms that govern selec- However, the physiological role of biological gels is not tive filtering in these three hydrogel-based filters. We point limited to their mechanical performance. They can also out similarities and differences in their filtering mecha- form selective barriers that control the exchange of mole- nisms, and relate them to structural key components of cules between different compartments. In environments these biological hydrogels. Our intention is not to provide a where biological hydrogels serve as diffusion barriers, they detailed review of each gel system, for this we refer the are often associated with a lipid bilayer (Figure 1). The reader to excellent reviews of the respective subjects. selective permeability properties of lipid bilayers have Instead, we will discuss selected gel features that contrib- been extensively studied in the last century [6,7]. However, ute to our understanding of the mechanisms governing little is known about the structure and dynamics of the selective filtering. associated hydrogels and how their properties allow them to act as selective barriers that permit passage of particu- Design strategies for a biopolymer-based permeability lar objects but reject others. filter The ECM in the connective tissue of mammalian species A permeability barrier could discriminate molecules either mediates cell adhesion and proliferation [8] and regulates by size or by surface properties. In the first case, the mesh the distribution of proteins, growth factors, ions and drugs size of the hydrogel (Box 1) defines a molecular size cut-off: [9,10], which is necessary for successful communication objects with dimensions larger than the mesh size will be rejected, whereas smaller objects are allowed to pass Corresponding author: Ribbeck, K. ([email protected]). (Box 2, Figure Ia). One drawback of size exclusion is its 0962-8924/$ – see front matter ß 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.tcb.2011.06.002 Trends in Cell Biology, September 2011, Vol. 21, No. 9 543 [(Figure_1)TD$IG]Review Trends in Cell Biology September 2011, Vol. 21, No. 9 Extracellular matrix Mucus Growth factors/ drugs/pathogens Hydrogel layer Cell membrane with selective channels Cytoskeleton TRENDS in Cell Biology Figure 1. The cell membrane/hydrogel barrier. Eukaryotic cells are surrounded by a plasma membrane which mediates both compartmentation and the exchange of material with the extracellular space. This plasma membrane is typically externally coated with a hydrogel such as the ECM or mucus which provides an additional permeability barrier. For example, extracellular hydrogels can prevent molecules or microscopic particles such as viruses or bacteria from reaching the plasma membrane. The detailed microscopic mechanisms by which macromolecules or pathogens are retained by biological hydrogels are still poorly understood. [(Figure_2)TD$IG] (a) Epithelium CConnectiveon tissue (b) (c) Entering/rejected particles Mucus Epithelium Nuclear pore with Hydrogel barrier nucleoporin polymers (d) (e) Extracellular polymers Aqueous and vitreous humor In bacterial biofilm in the mammalian eye TRENDS in Cell Biology Figure 2. Biopolymer-based hydrogels control the translocation of microscopic objects and act as selective permeability filters. They allow the passage of particular molecules (green) while rejecting others (orange). (a) ECM systems such as the basal lamina or the connective tissue regulate the passage of molecules to and from the blood stream or between cells. (b) All wet epithelia in our body are lined with a layer of mucin polymers, which form a hydrogel that shields the underlying cells from infectious agents such as viruses or bacteria. (c) Nuclear pores are filled with nucleoporin polymers which regulate the import and export of proteins into or out of the nucleus. (d) In bacterial biofilms, extracellular polymers effectively shield the bacteria from some antibiotics while allowing nutrients to enter the biofilm. (e) The vitreous humor in the mammalian eye allows the penetration of particular antibiotics while blocking others. 544 Review Trends in Cell Biology September 2011, Vol. 21, No. 9 Box 1. Probing the local microenvironment in hydrogels Hydrogels are predominantly composed of water, which fills the geometrical constraints and, in the case of non-inert particles, binding space between the hydrogel polymers. The average distance between events with the biopolymers, can retard the diffusion of molecules distinct polymer strands is referred to as the hydrogel mesh size. In (Figure Ib,c). Ideally, rigid and completely inert tracer particles are cases where the total polymer concentration and the length of used for mesh size measurements (i.e. particles that show no binding individual polymer strands are known, this mesh size can be interactions with the hydrogel components). Only such inert particles estimated mathematically. An exact measurement of hydrogel mesh are able to explore fully the microenvironment inside the hydrogel sizes is, however, difficult to achieve. Hydrogel pore sizes as obtained and thus report the correct mesh size. from the analysis of electron micrographs are prone to artifacts that Inside a hydrogel mesh the local viscosity that an inert diffusing arise both from the need to stain hydrogel biopolymers with contrast- particle encounters is typically close to that of water or buffer, enhancing heavy metals and from structural collapse of the hydrogel depending on what liquid is used to hydrate the biopolymers. This during the processing required for electron microscopy. Therefore, microviscosity of a hydrogel should not be confused with the viscous particle-tracking techniques [74,75] are commonly used to probe the modulus that is, for example, obtained from diffusion measurements local microenvironment of hydrogels [3,76] and a size cut-off is with particles that are larger than the hydrogel mesh size (Figure Ic), determined from the abrupt change in the transport behavior of tracer or from macroscopic shear rheometry. These techniques report a particles of different sizes [36] (compare Figure Ia and c). However, the meso- or macromechanical material property of the hydrogel
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