Transitions in cell organization and in expression of contractile andextracellular matrix proteins during development of chicken aortic smoothmuscle: evidence for a complex spatial and temporaldifferentiation program

摘要

Whereas the understanding of the mechanisms underlying skeletal and cardiac muscle development has been increased dramatically in recent years, the understanding of smooth muscle development is still in its infancy. This paper summarizes studies on the ontogeny of chicken smooth muscle cells in the wall of the aorta and aortic arch-derived arteries. Employing immunocyto-chemistry with antibodies against smooth muscle contractile and extracellular matrix proteins we trace smooth muscle cell patterning from early development throughout adulthood. Comparing late stage embryos to young and adult chickens we demonstrate, for all the stages analyzed, that the cells in the media of aortic arch-derived arteries and of the thoracic aorta are organized in alternating lamellae. The lamellar cells, but not the interlamellar cells, express smooth muscle specific contractile proteins and are surrounded by basement membrane proteins. This smooth muscle cell organization of lamellar and interlamellar cells is fully acquired by embryonic day 11 (ED11). We further show that, during earlier stages of embryogenesis (ED3 through ED7), cells expressing smooth muscle proteins appear only in the peri-endothelial region of the aortic and aortic arch wall and are organized as a narrow band of cells that does notdemonstrate the lamellar-interlamellar pattern. On ED9, infrequent cellsorganized in lamellar-interlamellar organization can be detected and theirfrequency increases by ED10. In addition to changes in cell organization, weshow that there is a characteristic sequence of contractile and extracellularmatrix protein expression during development of the aortic wall. At ED3 theperi-endothelial band of differentiated smooth muscle cells is already positivefor smooth muscle alpha actin (αSM-actin) and fibronectin. By the nextembryonic day the peri-endothelial cell layer is also positive for smooth musclemyosin light chain kinase (SM-MLCK). Subsequently, by ED5 this peri-endothelialband of differentiated smooth muscle cells is positive for αSM-actin,SM-MLCK, SM-calponin, fibronectin, and collagen type IV. However, laminin anddesmin (characteristic basement membrane and contractile proteins of smoothmuscle) are first seen only at the onset of the lamellar-interlamellar cellorganization (ED9 to ED10). We conclude that the development of chicken aorticsmooth muscle involves transitions in cell organization and in expression ofsmooth muscle proteins until the adult-like phenotype is achieved bymid-embryogenesis. This detailed analysis of the ontogeny of chick aortic smoothmuscle should provide a sound basis for future studies on the regulatorymechanisms underlying vascular smooth muscle development.