Extracellular matrix macroassembly dynamics in early vertebrate embryos.
This chapter focuses on the in vivo macroassembly dynamics of fibronectin and fibrillin-2--two prominent extracellular matrix (ECM) components, present in vertebrate embryos at the earliest stages of development. The ECM is an inherently dynamic structure with a well-defined position fate: ECM filaments are not only anchored to and move with established tissue boundaries, but are repositioned prior to the formation of new anatomical features. We distinguish two ECM filament relocation processes-each operating on different length scales. First, ECM filaments are moved by large-scale tissue motion, which rearranges major organ primordia within the embryo. The second type of motion, on the scale of the individual ECM filaments, is driven by local motility and protrusive activity of nearby cells. The motion decomposition is made practically possible by recent advances in microscopy and high-resolution particle image velocimetry algorithms. We demonstrate that both kinds of motion contribute substantially to the establishment of normal ECM structure, and both must be taken into account when attempting to understand ECM macroassembly during embryonic morphogenesis. The tissue-scale motion changes the local amount (density) and the tissue-level structure (e.g., orientation) of ECM fibers. Local reorganization includes filament assembly and the segregation of ECM into specific patterns. Local reorganization takes place most actively at Hensen's node and around the primitive streak. These regions are also sites of active cell migration, where fibrillin-2 and fibronectin are often colocalized in ECM globules, and new fibrillin-2 foci are deposited. During filament assembly, the globular patches of ECM are joined into larger linear structures in a hierarchical process: increasingly larger structures are created by the aggregation of smaller units. A future understanding of ECM assembly thus requires the study of the complex interactions between biochemical assembly steps, local cell action, and tissue motion.
Czirok
Andras
A
Department of Anatomy and Cell Biology, University of Kansas Medical Center, Kansas City, 66160, USA.
Zamir
Evan A
EA
Filla
Michael B
MB
Little
Charles D
CD
Rongish
Brenda J
BJ
D000818:Animals; D002465:Cell Movement / Q000502:physiology; D004622:Embryo, Mammalian / Q000033:anatomy & histology / Q000502:physiology; D004625:Embryo, Nonmammalian; D005109:Extracellular Matrix / Q000737:chemistry / Q000502:physiology*; D000071837:Fibrillins; D005353:Fibronectins / Q000378:metabolism; D008840:Microfilament Proteins / Q000378:metabolism; D009024:Morphogenesis
D000071837:Fibrillins; D005353:Fibronectins; D008840:Microfilament Proteins