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

Pichlo, Magdalena; Bungert-Plumke, S.; Weyand, I.; Seifert, Reinhard; Bönigk, Wolfgang; Strünker, Timo; Kashikar, Nachiket Dilip; Goodwin, Norman; Müller, Astrid; Pelzer, P.; Van, Q.; Enderlein, J.; Klemm, C.; Krause, E.; Trotschel, C.; Poetsch, A.; Kremmer, E.; Kaupp, Ulrich Benjamin

doi:10.1083/jcb.201402027

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

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Pichlo, Magdalena
Department of Molecular Sensory Systems, Center of Advanced European Studies and Research (caesar), Max Planck Society;

/persons/resource/persons182767

Seifert, Reinhard
Department of Molecular Sensory Systems, Center of Advanced European Studies and Research (caesar), Max Planck Society;

/persons/resource/persons182720

Bönigk, Wolfgang
Department of Molecular Sensory Systems, Center of Advanced European Studies and Research (caesar), Max Planck Society;

/persons/resource/persons182770

Strünker, Timo
Department of Molecular Sensory Systems, Center of Advanced European Studies and Research (caesar), Max Planck Society;

/persons/resource/persons182742

Kashikar, Nachiket Dilip
Department of Molecular Sensory Systems, Center of Advanced European Studies and Research (caesar), Max Planck Society;

/persons/resource/persons182734

Goodwin, Norman
Department of Molecular Sensory Systems, Center of Advanced European Studies and Research (caesar), Max Planck Society;

/persons/resource/persons182751

Müller, Astrid
Department of Molecular Sensory Systems, Center of Advanced European Studies and Research (caesar), Max Planck Society;

/persons/resource/persons182743

Kaupp, Ulrich Benjamin
Department of Molecular Sensory Systems, Center of Advanced European Studies and Research (caesar), Max Planck Society;

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http://www.ncbi.nlm.nih.gov/pubmed/25135936
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http://jcb.rupress.org/content/206/4/541.full.pdf
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Citation

Pichlo, M., Bungert-Plumke, S., Weyand, I., Seifert, R., Bönigk, W., Strünker, T., et al. (2014). High density and ligand affinity confer ultrasensitive signal detection by a guanylyl cyclase chemoreceptor. The Journal of cell biology, 206(4), 541-557. doi:10.1083/jcb.201402027.

Cite as: https://hdl.handle.net/11858/00-001M-0000-0028-619B-E

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 x 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.