Literature DB >> 28536200

Modulation of sensory information processing by a neuroglobin in Caenorhabditis elegans.

Shigekazu Oda1, Yu Toyoshima2, Mario de Bono1.   

Abstract

Sensory receptor neurons match their dynamic range to ecologically relevant stimulus intensities. How this tuning is achieved is poorly understood in most receptors. The roundworm Caenorhabditis elegans avoids 21% O2 and hypoxia and prefers intermediate O2 concentrations. We show how this O2 preference is sculpted by the antagonistic action of a neuroglobin and an O2-binding soluble guanylate cyclase. These putative molecular O2 sensors confer a sigmoidal O2 response curve in the URX neurons that has highest slope between 15 and 19% O2 and approaches saturation when O2 reaches 21%. In the absence of the neuroglobin, the response curve is shifted to lower O2 values and approaches saturation at 14% O2 In behavioral terms, neuroglobin signaling broadens the O2 preference of Caenorhabditis elegans while maintaining avoidance of 21% O2 A computational model of aerotaxis suggests the relationship between GLB-5-modulated URX responses and reversal behavior is sufficient to broaden O2 preference. In summary, we show that a neuroglobin can shift neural information coding leading to altered behavior. Antagonistically acting molecular sensors may represent a common mechanism to sharpen tuning of sensory neurons.

Entities:  

Keywords:  computational model; neural coding; neuroglobin; oxygen sensing; sensory neuron tuning

Mesh:

Substances:

Year:  2017        PMID: 28536200      PMCID: PMC5468664          DOI: 10.1073/pnas.1614596114

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  30 in total

Review 1.  Function and evolution of vertebrate globins.

Authors:  T Burmester; T Hankeln
Journal:  Acta Physiol (Oxf)       Date:  2014-05-28       Impact factor: 6.311

2.  Biochemical characterization and ligand binding properties of neuroglobin, a novel member of the globin family.

Authors:  S Dewilde; L Kiger; T Burmester; T Hankeln; V Baudin-Creuza; T Aerts; M C Marden; R Caubergs; L Moens
Journal:  J Biol Chem       Date:  2001-07-25       Impact factor: 5.157

3.  The neural circuit for touch sensitivity in Caenorhabditis elegans.

Authors:  M Chalfie; J E Sulston; J G White; E Southgate; J N Thomson; S Brenner
Journal:  J Neurosci       Date:  1985-04       Impact factor: 6.167

4.  The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis.

Authors:  J T Pierce-Shimomura; T M Morse; S R Lockery
Journal:  J Neurosci       Date:  1999-11-01       Impact factor: 6.167

5.  Experience-dependent modulation of C. elegans behavior by ambient oxygen.

Authors:  Benny H H Cheung; Merav Cohen; Candida Rogers; Onder Albayram; Mario de Bono
Journal:  Curr Biol       Date:  2005-05-24       Impact factor: 10.834

Review 6.  Oxygen sensors in context.

Authors:  Jeremy P T Ward
Journal:  Biochim Biophys Acta       Date:  2007-11-01

Review 7.  Oxygen sensing by the carotid body: mechanisms and role in adaptation to hypoxia.

Authors:  José López-Barneo; Patricia González-Rodríguez; Lin Gao; M Carmen Fernández-Agüera; Ricardo Pardal; Patricia Ortega-Sáenz
Journal:  Am J Physiol Cell Physiol       Date:  2016-01-13       Impact factor: 4.249

8.  What is the function of neuroglobin?

Authors:  Thorsten Burmester; Thomas Hankeln
Journal:  J Exp Biol       Date:  2009-05       Impact factor: 3.312

Review 9.  Redefining the components of central CO2 chemosensitivity--towards a better understanding of mechanism.

Authors:  Robert T R Huckstepp; Nicholas Dale
Journal:  J Physiol       Date:  2011-10-17       Impact factor: 5.182

10.  Decoding a neural circuit controlling global animal state in C. elegans.

Authors:  Patrick Laurent; Zoltan Soltesz; Geoffrey M Nelson; Changchun Chen; Fausto Arellano-Carbajal; Emmanuel Levy; Mario de Bono
Journal:  Elife       Date:  2015-03-11       Impact factor: 8.140

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1.  Social and sexual behaviors in C. elegans: the first fifty years.

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Journal:  J Neurogenet       Date:  2020-11-04       Impact factor: 1.250

2.  A Single-Neuron Chemosensory Switch Determines the Valence of a Sexually Dimorphic Sensory Behavior.

Authors:  Kelli A Fagan; Jintao Luo; Ross C Lagoy; Frank C Schroeder; Dirk R Albrecht; Douglas S Portman
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3.  Aerotaxis Assay in Caenorhabditis elegans to Study Behavioral Plasticity.

Authors:  Qiaochu Li; Daniel-Cosmin Marcu; Paul H Dear; Karl Emanuel Busch
Journal:  Bio Protoc       Date:  2022-08-20

4.  Correlation between convection requirement and carotid body responses to hypoxia and hemoglobin affinity: comparison between two rat strains.

Authors:  Dona F Boggs; Delbert L Kilgore; Scott Lacefield
Journal:  J Comp Physiol B       Date:  2021-05-10       Impact factor: 2.200

5.  Changes to social feeding behaviors are not sufficient for fitness gains of the Caenorhabditis elegans N2 reference strain.

Authors:  Yuehui Zhao; Lijiang Long; Wen Xu; Richard F Campbell; Edward E Large; Joshua S Greene; Patrick T McGrath
Journal:  Elife       Date:  2018-10-17       Impact factor: 8.140

6.  Dynamics of pattern formation and emergence of swarming in Caenorhabditis elegans.

Authors:  Esin Demir; Y Ilker Yaman; Mustafa Basaran; Askin Kocabas
Journal:  Elife       Date:  2020-04-06       Impact factor: 8.140

  6 in total

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