NMR Structure of Navel Orangeworm Moth Pheromone-Binding Protein (AtraPBP1): Implications for pH-Sensitive Pheromone Detection,
- 20 January 2010
- journal article
- research article
- Published by American Chemical Society (ACS) in Biochemistry
- Vol. 49 (7), 1469-1476
- https://doi.org/10.1021/bi9020132
Abstract
The navel orangeworm, Amyelois transitella (Walker), is an agricultural insect pest that can be controlled by disrupting male−female communication with sex pheromones, a technique known as mating disruption. Insect pheromone-binding proteins (PBPs) provide fast transport of hydrophobic pheromones through the aqueous sensillar lymph and promote sensitive delivery of pheromones to receptors. Here we present the three-dimensional structure of a PBP from A. transitella (AtraPBP1) in solution at pH 4.5 determined by nuclear magnetic resonance (NMR) spectroscopy. Pulsed-field gradient NMR diffusion experiments, multiangle light scattering, and 15N NMR relaxation analysis indicate that AtraPBP1 forms a stable monomer in solution at pH 4.5 in contrast to forming mostly dimers at pH 7. The NMR structure of AtraPBP1 at pH 4.5 contains seven α-helices (α1, L8−L23; α2, D27−F36; α3, R46−V62; α4, A73−M78; α5, D84−S100; α6, R107−L125; α7, M131−E141) that adopt an overall main-chain fold similar to that of PBPs found in Antheraea polyphemus and Bombyx mori. The AtraPBP1 structure is stabilized by three disulfide bonds formed by C19/C54, C50/C108, and C97/C117 and salt bridges formed by H69/E60, H70/E57, H80/E132, H95/E141, and H123/D40. All five His residues are cationic at pH 4.5, whereas H80 and H95 become neutral at pH 7.0. The C-terminal helix (α7) contains hydrophobic residues (M131, V133, V134, V135, V138, L139, and A140) that contact conserved residues (W37, L59, A73, F76, A77, I94, V111, and V115) suggested to interact with bound pheromone. Our NMR studies reveal that acid-induced formation of the C-terminal helix at pH 4.5 is triggered by a histidine protonation switch that promotes rapid release of bound pheromone under acidic conditions.Keywords
This publication has 41 references indexed in Scilit:
- Ligand Binding Turns Moth Pheromone-binding Protein into a pH SensorJournal of Biological Chemistry, 2009
- Olfactory Proteins Mediating Chemical Communication in the Navel Orangeworm Moth, Amyelois transitellaPLOS ONE, 2009
- Molecular switches for pheromone release from a moth pheromone-binding proteinBiochemical and Biophysical Research Communications, 2008
- Structural Basis of Ligand Binding and Release in Insect Pheromone-binding Proteins: NMR Structure of Antheraea polyphemus PBP1 at pH 4.5Journal of Molecular Biology, 2007
- Bombyx mori Pheromone-Binding Protein Binding Nonpheromone Ligands: Implications for Pheromone RecognitionStructure, 2007
- Pheromone reception in fruit flies expressing a moth's odorant receptorProceedings of the National Academy of Sciences, 2006
- Coil-to-helix transition and ligand release of Bombyx mori pheromone-binding proteinBiochemical and Biophysical Research Communications, 2005
- Duality Monomer–Dimer of the Pheromone-Binding Protein from Bombyx moriBiochemical and Biophysical Research Communications, 2000
- Relationship between nuclear magnetic resonance chemical shift and protein secondary structureJournal of Molecular Biology, 1991
- Isolation, identification, and synthesis of a female sex pheromone of the navel orangeworm,Amyelois transitella (Lepidoptera: Pyralidae)Journal of Chemical Ecology, 1979