Amyloid β (Aβ) peptides are considered the major causative agents of Alzheimer's disease (AD). In a widely accepted mechanism for AD pathogenesis, Aβ peptides are proposed to play multiple roles in damaging brain cells and their synaptic communications. Due to the heterogeneous nature of Aβ oligomers, their in vivo structures have not been understood. Most experimental and computational studies favored β-rich structures of Aβ as observed in Aβ fibrils. In this in silico study, we investigated an alternative perspective on the structures and function of Aβ oligomers in the cell membrane. Transmembrane α-helix bundles of the Aβ17-42 tetramer and trimer were observed in extensive temperature replica exchange molecular dynamics (REMD) simulations. We observed three minima on the free-energy landscape of each oligomer, namely, A, B, and C for the tetramer and D, E, and F for the trimer. Except for F, the minima consist of 4 or 3 parallel helices spanning across the membrane model dipalmitoylphosphatidylcholine. Replica exchange molecular dynamics-umbrella sampling (REMD-US) simulation was applied to study the process of a Ca2+ crossing the pore formed by the α-helix bundles in A-E in comparison to that in a calcium channel and a proton channel. REMD-US reveals that A, C, and D allow Ca2+ to cross their pore with a free-energy barrier comparable to that found for the calcium channel. In contrast, the free-energy barrier of a Ca2+ ion crossing B, E, and the proton channel is significantly higher. This result suggests that Aβ peptide oligomers could form transmembrane α-helix bundles that provide feasible pathways for Ca2+ transport. This is an intriguing observation that will stimulate further studies.