Morphogenetic rearrangement of injected collagen in developing chicken limb buds.

A fundamental question concerning the development of the extracellular matrix is what factors control the arrangement of collagen fibrils within a tissue and at the same time allow for the great diversity of geometric forms exhibited by collagen. In this report, we test the possibility that physical forces within the embryo serve to organize collagen fibers into regular patterns. In particular, we test the prediction that patterns of stress having this morphogenetic function are generated by cell traction, the contractile force exerted by cells to propel themselves. To study the effects of these mechanical forces on the extracellular matrix, type I collagen was fluorescently labeled and injected into developing chicken wing buds. When the injected limbs were allowed to develop and then examined histologically, the exogenous collagen was found incorporated within normal connective tissues of the wing. The labeled collagen became arranged according to its site of injection, forming parts of tendons, perichondria, cartilages, perineuria, and blood vessels. Since the injected collagen formed a gel within minutes of its injection, the subsequent incorporation of this performed collagen within organized structures cannot be explained in terms of molecular self-assembly or other mechanisms occurring during collagen deposition. These results demonstrate that, within developing tissues, patterns of forces exist that are capable of physically rearranging collagen and determining its long-range order.