Literature DB >> 27660389

The Signaling Pathway of Caenorhabditis elegans Mediates Chemotaxis Response to the Attractant 2-Heptanone in a Trojan Horse-like Pathogenesis.

Chunmei Zhang1, Ninghui Zhao2, Yao Chen1, Donghua Zhang1, Jinyuan Yan3, Wei Zou1, Keqin Zhang1, Xiaowei Huang4.   

Abstract

The nematode Caenorhabditis elegans exhibits behavioral responses to a wide range of odorants associated with food and pathogens. A previous study described a Trojan Horse-like strategy of pathogenesis whereby the bacterium Bacillus nematocida B16 emits the volatile organic compound 2-heptanone to trap C. elegans for successful infection. Here, we further explored the receptor for 2-heptanone as well as the pathway involved in signal transduction in C. elegans Our experiments showed that 2-heptanone sensing depended on the function of AWC neurons and a GPCR encoded by str-2 Consistent with the above observation, the HEK293 cells expressing STR-2 on their surfaces showed a transient elevation in intracellular Ca2+ levels after 2-heptanone applications. After combining the assays of RNA interference and gene mutants, we also identified the Gα subunits and their downstream components in the olfactory signal cascade that are necessary for responding to 2-heptanone, including Gα subunits of egl-30 and gpa-3, phospholipase C of plc-1and egl-8, and the calcium channel of cmk-1 and cal-1. Our work demonstrates for the first time that an integrated signaling pathway for 2-heptanone response in C. elegans involves recognition by GPCR STR-2, activation by Gα subunits of egl-30/gpa-3 and transfer to the PLC pathway, indicating that a potentially novel olfactory pathway exists in AWC neurons. Meanwhile, since 2-heptanone, a metabolite from the pathogenic bacterium B. nematocida B16, can be sensed by C. elegans and thus strongly attract its host, our current work also suggested coevolution between the pathogenic microorganism and the chemosensory system in C. elegans.
© 2016 by The American Society for Biochemistry and Molecular Biology, Inc.

Entities:  

Keywords:  2-heptanone; Caenorhabditis elegans (C. elegans); G protein-coupled receptor (GPCR); bacterial pathogenesis; chemotaxis; chemotaxis response; co-evolution; microbial pathogens; olfactory pathway; signal transduction

Mesh:

Substances:

Year:  2016        PMID: 27660389      PMCID: PMC5095415          DOI: 10.1074/jbc.M116.741132

Source DB:  PubMed          Journal:  J Biol Chem        ISSN: 0021-9258            Impact factor:   5.157


  32 in total

1.  Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans.

Authors:  C I Bargmann; H R Horvitz
Journal:  Neuron       Date:  1991-11       Impact factor: 17.173

Review 2.  The olfactory signal transduction for attractive odorants in Caenorhabditis elegans.

Authors:  Chunmei Zhang; Jinyuan Yan; Yao Chen; Chunyan Chen; Keqin Zhang; Xiaowei Huang
Journal:  Biotechnol Adv       Date:  2013-11-02       Impact factor: 14.227

3.  Guanylyl cyclase expression in specific sensory neurons: a new family of chemosensory receptors.

Authors:  S Yu; L Avery; E Baude; D L Garbers
Journal:  Proc Natl Acad Sci U S A       Date:  1997-04-01       Impact factor: 11.205

4.  Caenorhabditis elegans senses bacterial autoinducers.

Authors:  Elmus Beale; Guigen Li; Man-Wah Tan; Kendra P Rumbaugh
Journal:  Appl Environ Microbiol       Date:  2006-07       Impact factor: 4.792

Review 5.  Genetic and cellular analysis of behavior in C. elegans.

Authors:  C I Bargmann
Journal:  Annu Rev Neurosci       Date:  1993       Impact factor: 12.449

6.  A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in caenorhabditis elegans.

Authors:  D A Birnby; E M Link; J J Vowels; H Tian; P L Colacurcio; J H Thomas
Journal:  Genetics       Date:  2000-05       Impact factor: 4.562

Review 7.  Molecular neurogenetics of chemotaxis and thermotaxis in the nematode Caenorhabditis elegans.

Authors:  I Mori; Y Ohshima
Journal:  Bioessays       Date:  1997-12       Impact factor: 4.345

Review 8.  Neurobiology of the Caenorhabditis elegans genome.

Authors:  C I Bargmann
Journal:  Science       Date:  1998-12-11       Impact factor: 47.728

Review 9.  Invertebrates yield a plethora of atypical guanylyl cyclases.

Authors:  David B Morton
Journal:  Mol Neurobiol       Date:  2004-04       Impact factor: 5.590

10.  A cyclic nucleotide-gated channel inhibits sensory axon outgrowth in larval and adult Caenorhabditis elegans: a distinct pathway for maintenance of sensory axon structure.

Authors:  C M Coburn; I Mori; Y Ohshima; C I Bargmann
Journal:  Development       Date:  1998-01       Impact factor: 6.868

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  16 in total

Review 1.  Multisensory integration in C. elegans.

Authors:  D Dipon Ghosh; Michael N Nitabach; Yun Zhang; Gareth Harris
Journal:  Curr Opin Neurobiol       Date:  2017-03-06       Impact factor: 6.627

2.  Chemosensory signal transduction in Caenorhabditis elegans.

Authors:  Denise M Ferkey; Piali Sengupta; Noelle D L'Etoile
Journal:  Genetics       Date:  2021-03-31       Impact factor: 4.562

3.  Genetic and functional diversification of chemosensory pathway receptors in mosquito-borne filarial nematodes.

Authors:  Nicolas J Wheeler; Zachary W Heimark; Paul M Airs; Alexis Mann; Lyric C Bartholomay; Mostafa Zamanian
Journal:  PLoS Biol       Date:  2020-06-08       Impact factor: 8.029

Review 4.  Lipid and Carbohydrate Metabolism in Caenorhabditis elegans.

Authors:  Jennifer L Watts; Michael Ristow
Journal:  Genetics       Date:  2017-10       Impact factor: 4.562

5.  Dauer Formation in C. elegans Is Modulated through AWC and ASI-Dependent Chemosensation.

Authors:  Pratima Pandey; Umer S Bhat; Anuradha Singh; Aiswarya Joy; Varun Birari; Nagesh Y Kadam; Kavita Babu
Journal:  eNeuro       Date:  2021-04-14

6.  An atlas of Caenorhabditis elegans chemoreceptor expression.

Authors:  Berta Vidal; Ulkar Aghayeva; Haosheng Sun; Chen Wang; Lori Glenwinkel; Emily A Bayer; Oliver Hobert
Journal:  PLoS Biol       Date:  2018-01-02       Impact factor: 8.029

Review 7.  The Natural Biotic Environment of Caenorhabditis elegans.

Authors:  Hinrich Schulenburg; Marie-Anne Félix
Journal:  Genetics       Date:  2017-05       Impact factor: 4.562

8.  Odor-dependent temporal dynamics in Caenorhabitis elegans adaptation and aversive learning behavior.

Authors:  Jae Im Choi; Hee Kyung Lee; Hae Su Kim; So Young Park; Tong Young Lee; Kyoung-Hye Yoon; Jin I Lee
Journal:  PeerJ       Date:  2018-06-12       Impact factor: 2.984

9.  Deficiency of Innate Immunity against Pseudomonas aeruginosa Enhances Behavioral Avoidance via the HECW-1/NPR-1 Module in Caenorhabditis elegans.

Authors:  Hua Bai; Wei Zou; Wenhui Zhou; Keqin Zhang; Xiaowei Huang
Journal:  Infect Immun       Date:  2021-07-26       Impact factor: 3.441

10.  Identification of attractive odorants released by preferred bacterial food found in the natural habitats of C. elegans.

Authors:  Soleil E Worthy; Lillian Haynes; Melissa Chambers; Danika Bethune; Emily Kan; Kevin Chung; Ryan Ota; Charles J Taylor; Elizabeth E Glater
Journal:  PLoS One       Date:  2018-07-23       Impact factor: 3.240

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