TY - JOUR
T1 - Ultrafast hydration dynamics in melittin folding and aggregation
T2 - Helix formation and tetramer self-assembly
AU - Qiu, Weihong
AU - Zhang, Luyuan
AU - Kao, Ya-Ting
AU - Lu, Wenyun
AU - Li, Tanping
AU - Kim, Jongjoo
AU - Sollenberger, Gregory M.
AU - Wang, Lijuan
AU - Zhong, Dongping
PY - 2005/9/8
Y1 - 2005/9/8
N2 - Melittin, an amphipathic peptide from honeybee venom, consists of 26 amino acid residues and adopts different conformations from a random coil, to an α-helix, and to a self-assembled tetramer under certain aqueous environments. We report here our systematic studies of the hydration dynamics in these conformations using single intrinsic tryptophan (W19) as a molecular probe. With femtosecond resolution, we observed the solvation dynamics occurring in 0.62 and 14.7 ps in a random-coiled primary structure. The former represents bulklike water motion, and the latter reflects surface-type hydration dynamics of proteins. As a comparison, a model tripeptide (KWK) was also studied. At a membrane-water interface, melittin folds into a secondary α-helical structure, and the interfacial water motion was found to take as long as 114 ps, indicating a well-ordered water structure along the membrane surface. In high-salt aqueous solution, the dielectric screening and ionic solvation promote the hydrophobic core collapse in melittin aggregation and facilitate the tetramer formation. This self-assembled tertiary structure is also stabilized by the strong hydrophilic interactions of charged C-terminal residues and associated ions with water molecules in the two assembled regions. The hydration dynamics was observed to occur in 87 ps, significantly slower than typical water relaxation at protein surfaces but similar to water motion at membrane interfaces. Thus, the observed time scale of ∼100 ps probably implies appropriate water mobility for mediating the formation of high-order structures of melittin in an α-helix and a self-assembled tetramer. These results elucidate the critical role of hydration dynamics in peptide conformational transitions and protein structural stability and integrity.
AB - Melittin, an amphipathic peptide from honeybee venom, consists of 26 amino acid residues and adopts different conformations from a random coil, to an α-helix, and to a self-assembled tetramer under certain aqueous environments. We report here our systematic studies of the hydration dynamics in these conformations using single intrinsic tryptophan (W19) as a molecular probe. With femtosecond resolution, we observed the solvation dynamics occurring in 0.62 and 14.7 ps in a random-coiled primary structure. The former represents bulklike water motion, and the latter reflects surface-type hydration dynamics of proteins. As a comparison, a model tripeptide (KWK) was also studied. At a membrane-water interface, melittin folds into a secondary α-helical structure, and the interfacial water motion was found to take as long as 114 ps, indicating a well-ordered water structure along the membrane surface. In high-salt aqueous solution, the dielectric screening and ionic solvation promote the hydrophobic core collapse in melittin aggregation and facilitate the tetramer formation. This self-assembled tertiary structure is also stabilized by the strong hydrophilic interactions of charged C-terminal residues and associated ions with water molecules in the two assembled regions. The hydration dynamics was observed to occur in 87 ps, significantly slower than typical water relaxation at protein surfaces but similar to water motion at membrane interfaces. Thus, the observed time scale of ∼100 ps probably implies appropriate water mobility for mediating the formation of high-order structures of melittin in an α-helix and a self-assembled tetramer. These results elucidate the critical role of hydration dynamics in peptide conformational transitions and protein structural stability and integrity.
UR - http://www.scopus.com/inward/record.url?scp=25444458922&partnerID=8YFLogxK
U2 - 10.1021/jp0511754
DO - 10.1021/jp0511754
M3 - Article
C2 - 16853151
AN - SCOPUS:25444458922
VL - 109
SP - 16901
EP - 16910
JO - Journal of Physical Chemistry B
JF - Journal of Physical Chemistry B
SN - 1520-6106
IS - 35
ER -