Dynamics of the lens basement membrane capsule and its interaction with connective tissue-like extracapsular matrix proteins

• Published in: Matrix biology Vol. 96; pp. 18 - 46
• Main Authors: DeDreu, JodiRae, Walker, Janice L., Menko, A. Sue
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 01.02.2021; Elsevier Science Ltd
• Subjects: Animals; Basement Membrane - metabolism; Basement membranes; Chick Embryo; Collagen (type IV); Collagen IV; Collagen Type I - metabolism; Collagen Type I - ultrastructure; Connective tissue; Connective Tissue - metabolism; Connective Tissue - ultrastructure; Connective tissues; Extracellular Matrix - metabolism; Extracellular Matrix - ultrastructure; Extracellular Matrix Proteins - metabolism; Extracellular Matrix Proteins - ultrastructure; Fibrillin; Fibrillins - metabolism; Fibrillins - ultrastructure; Fibrils; Fibronectin; Fibronectins - metabolism; Fibronectins - ultrastructure; Heparan Sulfate Proteoglycans - chemistry; Heparan Sulfate Proteoglycans - metabolism; Lamellae; Laminin; Laminin - metabolism; Laminin - ultrastructure; Lens capsule; Lens, Crystalline - physiology; Matrix protein; Membrane Glycoproteins - metabolism; Membrane Glycoproteins - ultrastructure; Membrane proteins; Mice; Microscopy, Confocal; Perlecan; Proteins; Tenascin; Tenascin - chemistry; Tenascin - metabolism; Tenascin C; Lens capsule; Laminin; Collagen IV; Fibrillin; Perlecan; Tenascin-C
• ISSN: 0945-053X; 1569-1802; 1569-1802
• DOI: 10.1016/j.matbio.2020.12.005

•Discovery of a unique basement membrane structure in the lens equatorial zone consisting of two distinct laminin/perlecan lamellae spanning a central domain rich in collagen IV and nidogen.•The first demonstration of an extracapsular matrix zone consisting of the connective tissue proteins fibrillin-2, tenascin-C and fibronectin closely linked to the superficial surface of the lens basement membrane capsule.•Region-specific features of the matrix components of both the lens capsule and the extracapsular zone define distinct functional roles related to the different compartments of the visual system with which the lens interfaces. The lens, suspended in the middle of the eye by tendon-like ciliary zonule fibers and facing three different compartments of the eye, is enclosed in what has been described as the thickest basement membrane in the body. While the protein components of the capsule have been a subject of study for many years, the dynamics of capsule formation, and the region-specific relationship of its basement membrane components to one another as well as to other matrix molecules remains to be explored. Through high resolution confocal and super-resolution imaging of the lens capsule and 3D surface renderings of acquired z-stacks, our studies revealed that each of its basement membrane proteins, laminin, collagen IV, nidogen and perlecan, has unique structure, organization, and distribution specific both to the region of the lens that the capsule is located in and the position of the capsule within the eye. We provide evidence of basal membrane gradients across the depth of the capsule as well as the synthesis of distinct basement membrane lamella within the capsule. These distinctions are most prominent in the equatorial capsule zone where collagen IV and nidogen span the capsule depth, while laminin and perlecan are located in two separate lamellae located at the innermost and outermost capsule domains. We discovered that an extracapsular matrix compartment rich in the connective tissue-like matrix molecules fibronectin, tenascin-C, and fibrillin is integrated with the superficial surface of the lens capsule. Each matrix protein in this extracapsular zone also exhibits region-specific distribution with fibrils of fibrillin, the matrix protein that forms the backbone of the ciliary zonules, inserting within the laminin/perlecan lamella at the surface of the equatorial lens capsule.