title: Light and hydrogen peroxide inhibit C. elegans Feeding through gustatory receptor orthologs and pharyngeal neurons.
abstract: While gustatory sensing of the five primary flavors (sweet, salty, sour, bitter, and savory) has been extensively studied, pathways that detect non-canonical taste stimuli remain relatively unexplored. In particular, while reactive oxygen species cause generalized damage to biological systems, no gustatory mechanism to prevent ingestion of such material has been identified in any organism. We observed that light inhibits C. elegans feeding and used light as a tool to uncover molecular and neural mechanisms for gustation. Light can generate hydrogen peroxide, and we discovered that hydrogen peroxide similarly inhibits feeding. The gustatory receptor family members LITE-1 and GUR-3 are required for the inhibition of feeding by light and hydrogen peroxide. The I2 pharyngeal neurons increase calcium in response to light and hydrogen peroxide, and these responses require GUR-3 and a conserved antioxidant enzyme peroxiredoxin PRDX-2. Our results demonstrate a gustatory mechanism that mediates the detection and blocks ingestion of a non-canonical taste stimulus, hydrogen peroxide.
authors: Howard Hughes Medical Institute, Department of Biology, McGovern Institute for Brain Research, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA; Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA.
authors: Nikhil
authors: N
authors: Bhatla
authors: Howard Hughes Medical Institute, Department of Biology, McGovern Institute for Brain Research, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA. Electronic address: horvitz@mit.edu.
authors: H Robert
authors: HR
authors: Horvitz
mesh_terms: D000818:Animals; D030801:Animals, Genetically Modified; D017173:Caenorhabditis elegans; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism; D002118:Calcium / Q000378:metabolism; D004307:Dose-Response Relationship, Radiation; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism*; D005247:Feeding Behavior / Q000187:drug effects / Q000502:physiology / Q000528:radiation effects; D006861:Hydrogen Peroxide / Q000494:pharmacology*; D053685:Laser Therapy; D008027:Light; D008124:Locomotion / Q000187:drug effects / Q000528:radiation effects; D008565:Membrane Proteins / Q000235:genetics / Q000378:metabolism; D009154:Mutation / Q000235:genetics; D009474:Neurons / Q000187:drug effects / Q000502:physiology / Q000528:radiation effects; D062308:Optogenetics; D016877:Oxidants / Q000494:pharmacology*; D054464:Peroxiredoxins / Q000235:genetics / Q000378:metabolism; D010614:Pharynx / Q000166:cytology*; D011930:Reaction Time / Q000187:drug effects; D011956:Receptors, Cell Surface / Q000235:genetics / Q000378:metabolism*
chemical_list: D029742:Caenorhabditis elegans Proteins; D029721:Drosophila Proteins; D008565:Membrane Proteins; D016877:Oxidants; D011956:Receptors, Cell Surface; C405956:gustatory receptor, Drosophila; C532483:lite-1 protein, C elegans; D006861:Hydrogen Peroxide; C534226:PRDX-2 protein, C elegans; D054464:Peroxiredoxins; D002118:Calcium
references: PLoS One. 2013;8(3):e58190
references: 23483992
references: PLoS Genet. 2013;9(3):e1003341
references: 23505386
references: PLoS Genet. 2013;9(9):e1003710
references: 24068941
references: J Histochem Cytochem. 2014 Jan;62(1):85-96
references: 24152995
references: BMC Neurosci. 2014;15:14
references: 24433322
references: Neuron. 2014 Mar 5;81(5):984-1000
references: 24607224
references: Redox Biol. 2014;2:535-62
references: 24634836
references: Nature. 2001 Sep 13;413(6852):219-25
references: 11557991
references: Science. 2001 Oct 5;294(5540):158-60
references: 11588261
references: Infect Immun. 2002 Sep;70(9):5202-7
references: 12183571
references: Cell. 2002 Nov 15;111(4):471-81
references: 12437921
references: J Neurosci. 2003 Jan 1;23(1):269-76
references: 12514224
references: Proc Natl Acad Sci U S A. 2003 Nov 25;100 Suppl 2:14526-30
references: 14523229
references: Proc Natl Acad Sci U S A. 2003 Nov 25;100 Suppl 2:14537-42
references: 14608037
references: Infect Immun. 2004 Feb;72(2):1192-4
references: 14742574
references: J Mol Biol. 2004 May 7;338(4):745-55
references: 15099742
references: J Comp Neurol. 2004 Aug 2;475(4):540-50
references: 15236235
references: Infect Immun. 2004 Aug;72(8):4512-20
references: 15271910
references: Science. 1976 Feb 6;191(4226):468-9
references: 1108203
references: In Vitro. 1978 Aug;14(8):715-22
references: 689707
references: J Dairy Sci. 1980 Mar;63(3):353-7
references: 6768778
references: Science. 1982 May 28;216(4549):1012-4
references: 6805073
references: Science. 1990 Apr 13;248(4952):189-94
references: 2183352
references: J Opt Soc Am A Opt Image Sci Vis. 1997 Nov;14(11):2884-92
references: 9379246
references: Nature. 1998 Oct 29;395(6705):854
references: 9804418
references: Nat Neurosci. 2005 Sep;8(9):1263-8
references: 16116447
references: Curr Biol. 2006 Sep 19;16(18):R792-4
references: 16979544
references: Mol Cell. 2007 Apr 13;26(1):1-14
references: 17434122
references: Neuron. 2007 Apr 19;54(2):205-18
references: 17442243
references: Nature. 2007 Aug 30;448(7157):1054-7
references: 17728758
references: Exp Eye Res. 2008 Feb;86(2):452-5
references: 18078932
references: Nat Neurosci. 2008 Aug;11(8):916-22
references: 18604203
references: PLoS Biol. 2008 Aug 5;6(8):e198
references: 18687026
references: Nat Neurosci. 2008 Oct;11(10):1168-76
references: 18806786
references: J Biol Chem. 2009 Feb 13;284(7):4464-72
references: 19106090
references: Cell. 2009 Sep 18;138(6):1209-21
references: 19766572
references: Science. 2009 Oct 16;326(5951):443-5
references: 19833970
references: Nat Methods. 2009 Dec;6(12):875-81
references: 19898485
references: J Neurosci. 2010 May 5;30(18):6247-52
references: 20445050
references: Nature. 2010 May 6;465(7294):91-5
references: 20364123
references: Nat Neurosci. 2010 Jun;13(6):715-22
references: 20436480
references: J Neurosci. 2010 Jun 23;30(25):8376-82
references: 20573884
references: J Cell Biol. 2010 Aug 9;190(3):285-96
references: 20696704
references: Nature. 2010 Dec 16;468(7326):921-6
references: 21068723
references: Genetics. 1993 Oct;135(2):385-404
references: 8244003
references: Am J Forensic Med Pathol. 1994 Mar;15(1):44-50
references: 8166115
references: Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3384-7
references: 9096403
references: Cell. 2014 Jun 19;157(7):1535-51
references: 24949967
references: Proc Natl Acad Sci U S A. 2011 Jul 12;108(28):11680-5
references: 21709218
references: Nat Neurosci. 2011 Dec;14(12):1534-41
references: 22057190
references: J Biol Chem. 2012 Feb 10;287(7):4403-10
references: 22147704
references: Nat Commun. 2012;3:776
references: 22491324
references: Free Radic Biol Med. 2012 Oct 1;53(7):1522-30
references: 22902630
references: PLoS One. 2013;8(1):e53419
references: 23301069