Morphogenetic fields in embryogenesis, regeneration, and cancer: Non-local control of complex patterning

Establishment of shape during embryonic development, and the maintenance of shape against injury or tumorigenesis, requires constant coordination of cell behaviors toward the patterning needs of the host organism. Molecular cell biology and genetics have made great strides in understanding the mechanisms that regulate cell function. However, generalized rational control of shape is still largely beyond our current capabilities. Significant instructive signals function at long range to provide positional information and other cues to regulate organism-wide systems properties like anatomical polarity and size control. Is complex morphogenesis best understood as the emergent property of local cell interactions, or as the outcome of a computational process that is guided by a physically encoded map or template of the final goal state? Here I review recent data and molecular mechanisms relevant to morphogenetic fields: large-scale systems of physical properties that have been proposed to store patterning information during embryogenesis, regenerative repair, and cancer suppression that ultimately controls anatomy. Placing special emphasis on the role of endogenous bioelectric signals as an important component of the morphogenetic field, I speculate on novel approaches for the computational modeling and control of these fields with applications to synthetic biology, regenerative medicine, and evolutionary developmental biology.

This image is a representation of a regenerating planarian flatworm. The tail portion, which has been amputated, will regrow perfectly. This illustrates the concept of morphostasis—the ability of some living systems to dynamically restore their pattern. The image shows neoblast stem cells (light red dots), blastema (orange tissue at the wound site), and the bioelectrical gradients that are crucial for maintaining long-range anatomical polarity (yellow “field” lines). The morphogenetic field of patterning information (the target morphology) which will guide the rebuilding of the tail is schematized as a wire framework (white)—a scaffold of force and information underlying the subsequent gene expression and anatomy.Figure optionsDownload as PowerPoint slide