The structures of the mammalian water transport protein Aqp1 and of its bacterial homologue GlpF enables us to test whether homology models can be used to explore relationships between structure, dynamics and function in mammalian transport proteins. Molecular dynamics simulations (totalling almost 40 ns) were performed starting from: the X-ray structure of Aqp1; a homology model of Aqp1 based on the GlpF structure; and intermediate resolution structures of Aqp1 derived from electron microscopy. Comparisons of protein RMSDs vs. time suggest that the homology models are of comparable conformational stability to the X-ray structure, whereas the intermediate resolution structures exhibit significant conformation drift. For simulations based on the X-ray structure and on homology models, the flexibility profile vs. residue number correlates well with the crystallographic B-values for each residue. In the simulations based on intermediate resolution structures, mobility of the highly conserved NPA loops is substantially higher than in the simulations based on the X-ray structure or the homology models. Pore radius profiles remained relatively constant in the X-ray and homology model simulations but showed substantial fluctuations (reflecting the higher NPA loop mobility) in the intermediate resolution simulations. The orientation of the dipoles of water molecules within the pore is of key importance in maintaining low proton permeability through Aqp1. This property seems to be quite robust to the starting model used in the simulation. These simulations suggest that homology models based on bacterial homologues may be used to derive functionally relevant information on the structural dynamics of mammalian transport proteins.