High density and ligand affinity confer ultrasensitive signal detection by a guanylyl cyclase chemoreceptor

J Cell Biol. 2014 Aug 18;206(4):541-57. doi: 10.1083/jcb.201402027.

Abstract

Guanylyl cyclases (GCs), which synthesize the messenger cyclic guanosine 3',5'-monophosphate, control several sensory functions, such as phototransduction, chemosensation, and thermosensation, in many species from worms to mammals. The GC chemoreceptor in sea urchin sperm can decode chemoattractant concentrations with single-molecule sensitivity. The molecular and cellular underpinnings of such ultrasensitivity are not known for any eukaryotic chemoreceptor. In this paper, we show that an exquisitely high density of 3 × 10(5) GC chemoreceptors and subnanomolar ligand affinity provide a high ligand-capture efficacy and render sperm perfect absorbers. The GC activity is terminated within 150 ms by dephosphorylation steps of the receptor, which provides a means for precise control of the GC lifetime and which reduces "molecule noise." Compared with other ultrasensitive sensory systems, the 10-fold signal amplification by the GC receptor is surprisingly low. The hallmarks of this signaling mechanism provide a blueprint for chemical sensing in small compartments, such as olfactory cilia, insect antennae, or even synaptic boutons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arbacia / metabolism*
  • Chemoreceptor Cells / metabolism
  • Chemotactic Factors / physiology
  • Cyclic GMP / biosynthesis*
  • Guanylate Cyclase / metabolism*
  • HEK293 Cells
  • Humans
  • Male
  • Phosphorylation
  • Protein Binding
  • Receptors, Guanylate Cyclase-Coupled / metabolism*
  • Signal Transduction
  • Spermatozoa / metabolism*

Substances

  • Chemotactic Factors
  • Guanylate Cyclase
  • Receptors, Guanylate Cyclase-Coupled
  • Cyclic GMP