Absolute proteomic quantification reveals design principles of sperm flagellar 
chemosensation.

Trötschel, Christian; Hamzeh, Hussein; Alvarez, Luis; Pascal, René; Lavryk, Fedir; Bönigk, Wolfgang; Körschen, Heinz Gerd; Müller, Astrid; Poetsch, Ansgar; Rennhack, Andreas; Gui, Long; Nicastro, Daniela; Strünker, Timo; Seifert, Reinhard; Kaupp, Ulrich Benjamin

doi:10.15252/embj.2019102723

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Absolute proteomic quantification reveals design principles of sperm flagellar chemosensation.

MPS-Authors

Hamzeh, Hussein
Department of Molecular Sensory Systems, Center of Advanced European Studies and Research (caesar), Max Planck Society;
External Organizations;

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

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

Lavryk, Fedir
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/persons182745

Körschen, Heinz Gerd
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/persons182759

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

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

/persons/resource/persons182767

Seifert, Reinhard
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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Citation

Trötschel, C., Hamzeh, H., Alvarez, L., Pascal, R., Lavryk, F., Bönigk, W., et al. (2020). Absolute proteomic quantification reveals design principles of sperm flagellar chemosensation. EMBO Journal, 39(4): e102723. doi:10.15252/embj.2019102723.

Cite as: https://hdl.handle.net/21.11116/0000-0005-6FBB-D

Abstract

Cilia serve as cellular antennae that translate sensory information into physiological responses. In the sperm flagellum, a single chemoattractant molecule can trigger a Ca2+ rise that controls motility. The mechanisms underlying such ultra-sensitivity are ill-defined. Here, we determine by mass spectrometry the copy number of nineteen chemosensory signaling proteins in sperm flagella from the sea urchin Arbacia punctulata. Proteins are up to 1,000-fold more abundant than the free cellular messengers cAMP, cGMP, H+ , and Ca2+ . Opto-chemical techniques show that high protein concentrations kinetically compartmentalize the flagellum: Within milliseconds, cGMP is relayed from the receptor guanylate cyclase to a cGMP-gated channel that serves as a perfect chemo-electrical transducer. cGMP is rapidly hydrolyzed, possibly via "substrate channeling" from the channel to the phosphodiesterase PDE5. The channel/PDE5 tandem encodes cGMP turnover rates rather than concentrations. The rate-detection mechanism allows continuous stimulus sampling over a wide dynamic range. The textbook notion of signal amplification-few enzyme molecules process many messenger molecules-does not hold for sperm flagella. Instead, high protein concentrations ascertain messenger detection. Similar mechanisms may occur in other small compartments like primary cilia or dendritic spines.