Topographies of extracytoplasmic compartments in developing chick tendon fibroblasts

The complex topography of the fibroblast leading to the formation of extracellular compartments is demonstrated in the native three-dimensional state in cryofractured chick embryo tendon at different stages of development. Tendon collagen fibrils, fibril bundles, and macroaggregates are intimately associated with these extracytoplasmic domains. The localization of fibrils within narrow channels, bundles within peripheral compartments, and the coalescence of bundles into macroaggregates within larger extracytoplasmic compartments is illustrated at different stages of development. Changing patterns of matrix organization are apparent as morphogenesis proceeds. Our interpretation is that collagen fibrils, oriented along the tendon axis, appear in extracytoplasmic channels defined by the fibroblast which are added at the periphery of the cell until a row of fibrils outlines the cellular border at Day 10. By Day 14, cytoplasmic processes have partitioned the fibrils into groups and then into round bundles. New fibrils are continually added to the fibril bundles through fusion of the extracytoplasmic channels. As the bundles grow larger, the cell boundaries between the bundles retract and bundles begin to coalesce into macroaggregates. The fibroblast becomes attenuated, bundle-forming compartments disappear as processes retract, bundles coalesce, and macroaggregates predominate by Day 17. This work is consistent with the model proposed for the compartmentalization of the extracellular space by the fibroblast, providing distinct microenvironments where collagen fibrillogenesis and matrix morphogenesis occur under close cellular regulation.