High density and ligand affinity confer ultrasensitive signal detection by a guanylyl cyclase chemoreceptor.
| Title: | High density and ligand affinity confer ultrasensitive signal detection by a guanylyl cyclase chemoreceptor. |
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| Authors: | Pichlo M; Center of Advanced European Studies and Research, 53175 Bonn, Germany Marine Biological Laboratory, Woods Hole, MA 02543.; Bungert-Plümke S; Marine Biological Laboratory, Woods Hole, MA 02543 Institute of Complex Systems (ICS-4), Forschungszentrum Jülich, 52425 Jülich, Germany.; Weyand I; Marine Biological Laboratory, Woods Hole, MA 02543 Institute of Complex Systems (ICS-4), Forschungszentrum Jülich, 52425 Jülich, Germany.; Seifert R; Center of Advanced European Studies and Research, 53175 Bonn, Germany Marine Biological Laboratory, Woods Hole, MA 02543.; Bönigk W; Center of Advanced European Studies and Research, 53175 Bonn, Germany.; Strünker T; Center of Advanced European Studies and Research, 53175 Bonn, Germany Marine Biological Laboratory, Woods Hole, MA 02543.; Kashikar ND; Center of Advanced European Studies and Research, 53175 Bonn, Germany Marine Biological Laboratory, Woods Hole, MA 02543 Sussex Neuroscience, School of Life Sciences, University of Sussex, Brighton BN1 9QG, England, UK.; Goodwin N; Center of Advanced European Studies and Research, 53175 Bonn, Germany Marine Biological Laboratory, Woods Hole, MA 02543 Babraham Institute, Cambridge CB22 3AT, England, UK.; Müller A; Center of Advanced European Studies and Research, 53175 Bonn, Germany.; Pelzer P; Marine Biological Laboratory, Woods Hole, MA 02543 Department of Functional Neuroanatomy, Institute of Anatomy and Cell Biology, Heidelberg University, 69120 Heidelberg, Germany.; Van Q; III. Physikalisches Institut, Universität Göttingen, 37077 Göttingen, Germany.; Enderlein J; III. Physikalisches Institut, Universität Göttingen, 37077 Göttingen, Germany.; Klemm C; Leibniz-Institut für Molekulare Pharmakologie, 13125 Berlin, Germany.; Krause E; Leibniz-Institut für Molekulare Pharmakologie, 13125 Berlin, Germany.; Trötschel C; Plant Biochemistry, Ruhr University Bochum. 44801 Bochum, Germany.; Poetsch A; Plant Biochemistry, Ruhr University Bochum. 44801 Bochum, Germany.; Kremmer E; Institut für Molekulare Immunologie, Helmholtz-Zentrum München, 81377 München, Germany.; Kaupp UB; Center of Advanced European Studies and Research, 53175 Bonn, Germany Marine Biological Laboratory, Woods Hole, MA 02543 u.b.kaupp@caesar.de.; Körschen HG; Collienne U |
| Source: | The Journal of cell biology [J Cell Biol] 2014 Aug 18; Vol. 206 (4), pp. 541-57. |
| Publication Type: | Journal Article; Research Support, Non-U.S. Gov't |
| Language: | English |
| Journal Info: | Publisher: Rockefeller University Press Country of Publication: United States NLM ID: 0375356 Publication Model: Print Cited Medium: Internet ISSN: 1540-8140 (Electronic) Linking ISSN: 00219525 NLM ISO Abbreviation: J Cell Biol Subsets: MEDLINE |
| Imprint Name(s): | Original Publication: New York : Rockefeller University Press |
| MeSH Terms: | Arbacia/*metabolism ; Cyclic GMP/*biosynthesis ; Guanylate Cyclase/*metabolism ; Receptors, Guanylate Cyclase-Coupled/*metabolism ; Spermatozoa/*metabolism; Chemoreceptor Cells/metabolism ; Chemotactic Factors/physiology ; Animals ; HEK293 Cells ; Humans ; Male ; Phosphorylation ; Protein Binding ; Signal Transduction |
| 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.; (© 2014 Pichlo et al.) |
| Comments: | Erratum in: J Cell Biol. 2014 Dec 8;207(5):675. Körschen, Heinz G [Added] and Collienne, Ursel [Added]. |
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| Substance Nomenclature: | 0 (Chemotactic Factors); EC 4.6.1.2 (Guanylate Cyclase); EC 4.6.1.2 (Receptors, Guanylate Cyclase-Coupled); H2D2X058MU (Cyclic GMP) |
| Entry Date(s): | Date Created: 20140820 Date Completed: 20141118 Latest Revision: 20240321 |
| Update Code: | 20260130 |
| PubMed Central ID: | PMC4137060 |
| DOI: | 10.1083/jcb.201402027 |
| PMID: | 25135936 |
| Database: | MEDLINE |
Journal Article; Research Support, Non-U.S. Gov't