Huntington's disease is a deadly neurodegenerative disease caused by the fibrilization of huntingtin (HTT) exon-1 protein mutants. Despite extensive efforts over the past decade, much remains unknown about the structures of (mutant) HTT exon-1 and their enigmatic roles in aggregation. Particularly, whether the first 17 residues in the N-terminal (HTT-N17) adopt a helical or a coiled structure remains unclear. Here, with the rigorous study of molecular dynamics simulations, we explored the most possible structures of HTT-N17 in both dodecylphosphocholine (DPC) micelles and aqueous solution, using three commonly applied force fields (OPLS-AA/L, CHARMM36, and AMBER99sb∗-ILDNP) to examine the underlying molecular mechanisms and rule out potential artifacts. We show that local environments are essential for determining the secondary structure of HTT-N17. This is evidenced by the insertion of five hydrophobic residues of HTT-N17 into the DPC micelle, which promotes the formation of an amphipathic helix, whereas such amphipathic helices unfold quickly in aqueous solution. A relatively low free-energy barrier (∼3 kcal/mol) for the secondary structure transformation was also observed for all three force fields from their respective folding-free-energy landscapes, which accounts for possible HTT-N17 conformational changes upon environmental shifts such as membrane binding and protein complex aggregation.