Neurons Detect Increases and Decreases in Oxygen Levels Using Distinct Guanylate Cyclases

Manuel Zimmer, Jesse M. Gray, Navin Pokala, Andy J. Chang, David S. Karow, Michael A. Marletta, Martin L. Hudson, David Morton, Nikos Chronis, Cornelia I. Bargmann

Research output: Contribution to journalArticle

148 Citations (Scopus)

Abstract

Homeostatic sensory systems detect small deviations in temperature, water balance, pH, and energy needs to regulate adaptive behavior and physiology. In C. elegans, a homeostatic preference for intermediate oxygen (O2) levels requires cGMP signaling through soluble guanylate cyclases (sGCs), proteins that bind gases through an associated heme group. Here we use behavioral analysis, functional imaging, and genetics to show that reciprocal changes in O2 levels are encoded by sensory neurons that express alternative sets of sGCs. URX sensory neurons are activated by increases in O2 levels, and require the sGCs gcy-35 and gcy-36. BAG sensory neurons are activated by decreases in O2 levels, and require the sGCs gcy-31 and gcy-33. The sGCs are instructive O2 sensors, as forced expression of URX sGC genes causes BAG neurons to detect O2 increases. Both sGC expression and cell-intrinsic dynamics contribute to the differential roles of URX and BAG in O2-dependent behaviors.

Original languageEnglish (US)
Pages (from-to)865-879
Number of pages15
JournalNeuron
Volume61
Issue number6
DOIs
StatePublished - Mar 26 2009

Fingerprint

Guanylate Cyclase
Oxygen
Neurons
Sensory Receptor Cells
Psychological Adaptation
Heme
Gases
Soluble Guanylyl Cyclase
Temperature
Water
Genes
Proteins

Keywords

  • DEVBIO
  • MOLNEURO
  • SIGNALING

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Zimmer, M., Gray, J. M., Pokala, N., Chang, A. J., Karow, D. S., Marletta, M. A., ... Bargmann, C. I. (2009). Neurons Detect Increases and Decreases in Oxygen Levels Using Distinct Guanylate Cyclases. Neuron, 61(6), 865-879. https://doi.org/10.1016/j.neuron.2009.02.013

Neurons Detect Increases and Decreases in Oxygen Levels Using Distinct Guanylate Cyclases. / Zimmer, Manuel; Gray, Jesse M.; Pokala, Navin; Chang, Andy J.; Karow, David S.; Marletta, Michael A.; Hudson, Martin L.; Morton, David; Chronis, Nikos; Bargmann, Cornelia I.

In: Neuron, Vol. 61, No. 6, 26.03.2009, p. 865-879.

Research output: Contribution to journalArticle

Zimmer, M, Gray, JM, Pokala, N, Chang, AJ, Karow, DS, Marletta, MA, Hudson, ML, Morton, D, Chronis, N & Bargmann, CI 2009, 'Neurons Detect Increases and Decreases in Oxygen Levels Using Distinct Guanylate Cyclases', Neuron, vol. 61, no. 6, pp. 865-879. https://doi.org/10.1016/j.neuron.2009.02.013
Zimmer M, Gray JM, Pokala N, Chang AJ, Karow DS, Marletta MA et al. Neurons Detect Increases and Decreases in Oxygen Levels Using Distinct Guanylate Cyclases. Neuron. 2009 Mar 26;61(6):865-879. https://doi.org/10.1016/j.neuron.2009.02.013
Zimmer, Manuel ; Gray, Jesse M. ; Pokala, Navin ; Chang, Andy J. ; Karow, David S. ; Marletta, Michael A. ; Hudson, Martin L. ; Morton, David ; Chronis, Nikos ; Bargmann, Cornelia I. / Neurons Detect Increases and Decreases in Oxygen Levels Using Distinct Guanylate Cyclases. In: Neuron. 2009 ; Vol. 61, No. 6. pp. 865-879.
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