Differential expressions of collagen types IV, III, and I during the development of invasive trophoblasts in rats

Abstract

We examined the differential expressions of collagen types IV, III, and I in the developing feto-maternal placental tissue of pregnant rats by a combination of in situ hybridization and immunohistochemistry. At day 9.5 of gestation, polygonal invasive cytotrophoblasts from the ectoplacental cone, which was modifying the maternal central artery, revealed intensely expressed α1(IV) and α1(III) collagen mRNAs. The localization patterns of these translated products, collagen type IV and procollagen type III, were slightly different in the invasive cytotrophoblasts. Collagen type IV densely deposited intracellularly and intercellularly in the maternal central artery and in the thickened basement membranes of the cytotrophoblasts. However, expression of α1(I) collagen mRNA and procollagen type I was hardly detectable in the cytotrophoblasts. At day 13 of gestation, a high level of α1(IV) collagen mRNA was expressed in the cytotrophoblastic cell layer (trophospongium) and in the invasive large cytotrophoblasts. A moderate level of α1(III) collagen mRNA was also expressed mainly in the cytotrophoblasts, while α1(I) collagen mRNA was expressed at very low levels. Interestingly, procollagen type III failed to show linear immunoreactivity in the subepithelial extracellular matrix beneath the maternal artery with the invasive cytotrophoblasts. Additional quantitative analyses of these type IV, III, and I collagen mRNA levels in in situ hybridization experiments between several cell types also revealed significant differences individually. Electron-microscopic study detected no cross-striated collagen fibers in the thickened basement membrane-like structures adjacent to the invasive cytotrophoblasts. Fibrillar and basement membrane collagen gene expressions, their protein syntheses, and the processing of these procollagens seem to be developmentally regulated in the invasive cytotrophoblasts during the organization of feto-maternal placental tissue. The remodeling of the maternal central artery by the invasive cytotrophoblasts is important for ensuring the adequate blood supply to the developing placenta and fetus.