Light and Hydrogen Peroxide Inhibit C. elegans Feeding through Gustatory Receptor Orthologs and Pharyngeal Neurons

被引:89
作者
Bhatla, Nikhil [1 ,2 ]
Horvitz, H. Robert [1 ]
机构
[1] MIT, Howard Hughes Med Inst, Dept Biol, McGovern Inst Brain Res, Cambridge, MA 02139 USA
[2] MIT, Dept Brain & Cognit Sci, Cambridge, MA 02139 USA
基金
美国国家科学基金会;
关键词
CAENORHABDITIS-ELEGANS; NEURAL ACTIVITY; TASTE; DROSOPHILA; PEROXIREDOXIN; ACTIVATION; EXPRESSION; CARBONATION; PREFERENCE; REGULATOR;
D O I
10.1016/j.neuron.2014.12.061
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
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.
引用
收藏
页码:804 / 818
页数:15
相关论文
共 57 条
[1]   In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2 [J].
Arenkiel, Benjamin R. ;
Peca, Joao ;
Davison, Ian G. ;
Feliciano, Catia ;
Deisseroth, Karl ;
Augustine, George J. ;
Ehlers, Michael D. ;
Feng, Guoping .
NEURON, 2007, 54 (02) :205-218
[2]  
Bedford THB, 1927, BRIT J EXP PATHOL, V8, P437
[3]   Identification and Functional Characterization of the Caenorhabditis elegans Riboflavin Transporters rft-1 and rft-2 [J].
Biswas, Arundhati ;
Elmatari, Daniel ;
Rothman, Jason ;
LaMunyon, Craig W. ;
Said, Hamid M. .
PLOS ONE, 2013, 8 (03)
[4]  
Blum HF, 1932, PHYSIOL REV, V12, P0023, DOI 10.1152/physrev.1932.12.1.23
[5]   Hydrogen peroxide-mediated killing of Caenorhabditis elegans:: a common feature of different streptococcal species [J].
Bolm, M ;
Jansen, WTM ;
Schnabel, R ;
Chhatwal, GS .
INFECTION AND IMMUNITY, 2004, 72 (02) :1192-1194
[6]   Millisecond-timescale, genetically targeted optical control of neural activity [J].
Boyden, ES ;
Zhang, F ;
Bamberg, E ;
Nagel, G ;
Deisseroth, K .
NATURE NEUROSCIENCE, 2005, 8 (09) :1263-1268
[7]   The molecular basis for water taste in Drosophila [J].
Cameron, Peter ;
Hiroi, Makoto ;
Ngai, John ;
Scott, Kristin .
NATURE, 2010, 465 (7294) :91-U101
[8]   Taste Preference for Fatty Acids Is Mediated by GPR40 and GPR120 [J].
Cartoni, Cristina ;
Yasumatsu, Keiko ;
Ohkuri, Tadahiro ;
Shigemura, Noriatsu ;
Yoshida, Ryusuke ;
Godinot, Nicolas ;
le Coutre, Johannes ;
Ninomiya, Yuzo ;
Damak, Sami .
JOURNAL OF NEUROSCIENCE, 2010, 30 (25) :8376-8382
[9]   The Taste of Carbonation [J].
Chandrashekar, Jayaram ;
Yarmolinsky, David ;
von Buchholtz, Lars ;
Oka, Yuki ;
Sly, William ;
Ryba, Nicholas J. P. ;
Zuker, Charles S. .
SCIENCE, 2009, 326 (5951) :443-445
[10]   The Amiloride-Sensitive Epithelial Na+ Channel PPK28 Is Essential for Drosophila Gustatory Water Reception [J].
Chen, Zijing ;
Wang, Qingxiu ;
Wang, Zuoren .
JOURNAL OF NEUROSCIENCE, 2010, 30 (18) :6247-6252