Two-way regulation between cells and aligned collagen fibrils: Local 3D matrix formation and accelerated neural differentiation of human decidua parietalis placental stem cells

[Display omitted] •We examined the two-way regulation between cells and aligned collagen fibrils.•Aligned collagen fibrils prompted cell polarization.•Dynamic cell growth prompted the construction of a local 3D matrix.•The local 3D matrix induced upregulation of β-1 integrin around the cell body.•The concerted changes supported fast and efficient neural differentiation. It has been well established that an aligned matrix provides structural and signaling cues to guide cell polarization and cell fate decision. However, the modulation role of cells in matrix remodeling and the feedforward effect on stem cell differentiation have not been studied extensively. In this study, we report on the concerted changes of human decidua parietalis placental stem cells (hdpPSCs) and the highly ordered collagen fibril matrix in response to cell–matrix interaction. With high-resolution imaging, we found the hdpPSCs interacted with the matrix by deforming the cell shape, harvesting the nearby collagen fibrils, and reorganizing the fibrils around the cell body to transform a 2D matrix to a localized 3D matrix. Such a unique 3D matrix prompted high expression of β-1 integrin around the cell body that mediates and facilitates the stem cell differentiation toward neural cells. The study offers insights into the coordinated, dynamic changes at the cell–matrix interface and elucidates cell modulation of its matrix to establish structural and biochemical cues for effective cell growth and differentiation.