Co-option of neurotransmitter signaling for inter-organismal communication in C. elegans.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
18 07 2019
18 07 2019
Historique:
received:
27
09
2018
accepted:
28
06
2019
entrez:
20
7
2019
pubmed:
20
7
2019
medline:
18
12
2019
Statut:
epublish
Résumé
Biogenic amine neurotransmitters play a central role in metazoan biology, and both their chemical structures and cognate receptors are evolutionarily conserved. Their primary roles are in cell-to-cell signaling, as biogenic amines are not normally recruited for communication between separate individuals. Here, we show that in the nematode C. elegans, a neurotransmitter-sensing G protein-coupled receptor, TYRA-2, is required for avoidance responses to osas#9, an ascaroside pheromone that incorporates the neurotransmitter, octopamine. Neuronal ablation, cell-specific genetic rescue, and calcium imaging show that tyra-2 expression in the nociceptive neuron, ASH, is necessary and sufficient to induce osas#9 avoidance. Ectopic expression in the AWA neuron, which is generally associated with attractive responses, reverses the response to osas#9, resulting in attraction instead of avoidance behavior, confirming that TYRA-2 partakes in the sensing of osas#9. The TYRA-2/osas#9 signaling system represents an inter-organismal communication channel that evolved via co-option of a neurotransmitter and its cognate receptor.
Identifiants
pubmed: 31320626
doi: 10.1038/s41467-019-11240-7
pii: 10.1038/s41467-019-11240-7
pmc: PMC6639374
doi:
Substances chimiques
Caenorhabditis elegans Proteins
0
Receptors, Biogenic Amine
0
TYRA-2 protein, C elegans
0
norsynephrine receptor
0
Octopamine
14O50WS8JD
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
3186Subventions
Organisme : NIDCD NIH HHS
ID : R01 DC016058
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS107475
Pays : United States
Références
Curr Biol. 2002 Apr 30;12(9):730-4
pubmed: 12007416
Cell. 1997 Oct 17;91(2):161-9
pubmed: 9346234
Nature. 2005 Feb 3;433(7025):541-5
pubmed: 15690045
Nature. 2006 Aug 10;442(7103):645-50
pubmed: 16878137
Methods Cell Biol. 2012;107:177-206
pubmed: 22226524
Sci Adv. 2016 May 06;2(5):e1501372
pubmed: 27386520
Pharmacol Rev. 2018 Jul;70(3):549-620
pubmed: 29941461
Genome Biol Evol. 2014 Mar;6(3):606-19
pubmed: 24567306
J Neurosci. 2006 Oct 4;26(40):10082-90
pubmed: 17021164
Dev Biol. 1999 Nov 15;215(2):314-31
pubmed: 10545240
Science. 2009 Nov 13;326(5955):994-8
pubmed: 19797623
J Neurosci Res. 2014 May;92(5):671-8
pubmed: 24446241
J Neurosci. 2011 Aug 10;31(32):11718-27
pubmed: 21832201
PLoS One. 2011 Mar 15;6(3):e17804
pubmed: 21423575
Nat Commun. 2012 Mar 13;3:739
pubmed: 22415830
Cell Rep. 2015 Sep 22;12(11):1748-60
pubmed: 26365196
Cell. 1996 Mar 22;84(6):899-909
pubmed: 8601313
Nat Rev Neurosci. 2010 Mar;11(3):212-7
pubmed: 20029439
Proc Natl Acad Sci U S A. 2007 Jan 16;104(3):834-9
pubmed: 17213328
Sci Signal. 2014 Apr 29;7(323):ra39
pubmed: 24782565
Elife. 2015 Sep 22;4:e10181
pubmed: 26394000
Nature. 2008 Aug 28;454(7208):1115-8
pubmed: 18650807
Nat Methods. 2007 Sep;4(9):727-31
pubmed: 17704783
Nat Methods. 2010 Jul;7(7):554-9
pubmed: 20512143
Nat Prod Rep. 2015 Jul;32(7):994-1006
pubmed: 26059053
Mol Cell Neurosci. 2001 Mar;17(3):589-99
pubmed: 11273652
Neurobiol Learn Mem. 2017 May;141:189-198
pubmed: 28450080
WormBook. 2006 Apr 05;:1-23
pubmed: 18050449
Proc Natl Acad Sci U S A. 2016 Mar 8;113(10):E1392-401
pubmed: 26903633
Semin Cell Dev Biol. 2014 Sep;33:18-24
pubmed: 24977334
J Neurosci. 2007 Dec 5;27(49):13402-12
pubmed: 18057198
Nat Commun. 2015 Jan 13;6:5655
pubmed: 25585042
EMBO J. 2012 Feb 1;31(3):667-78
pubmed: 22124329
Methods Mol Biol. 2016;1454:107-22
pubmed: 27514919
Curr Biol. 2010 Nov 23;20(22):R965-9
pubmed: 21093785
J Biol Chem. 2013 Jun 28;288(26):18778-83
pubmed: 23689506
Annu Rev Entomol. 2005;50:447-77
pubmed: 15355245
Science. 1998 Dec 11;282(5396):2028-33
pubmed: 9851919
Biophys Rep. 2018;4(1):17-24
pubmed: 29577066
Proc Natl Acad Sci U S A. 2009 May 12;106(19):7708-13
pubmed: 19346493
Nature. 2009 May 28;459(7246):574-7
pubmed: 19387439
PLoS Genet. 2011 Jun;7(6):e1002109
pubmed: 21698137
J Neurochem. 2005 Jul;94(1):181-91
pubmed: 15953361
WormBook. 2006 Oct 13;:1-25
pubmed: 18050432
Nat Chem Biol. 2007 Jul;3(7):420-2
pubmed: 17558398
MethodsX. 2015 Feb 07;2:59-63
pubmed: 26150972
Proc Natl Acad Sci U S A. 2012 Jun 19;109(25):9917-22
pubmed: 22665789
J Vis Exp. 2017 Sep 7;(127):
pubmed: 28930991
J Neurochem. 2002 Sep;82(6):1352-9
pubmed: 12354282
Front Syst Neurosci. 2017 Aug 22;11:60
pubmed: 28878633
Proc Natl Acad Sci U S A. 2004 Oct 26;101(43):15512-7
pubmed: 15492222
J Exp Biol. 2015 Feb 15;218(Pt 4):562-71
pubmed: 25696819
Cell. 1993 Aug 13;74(3):515-27
pubmed: 8348618
PLoS Biol. 2012 Jan;10(1):e1001237
pubmed: 22253572
J Neurosci. 2017 Aug 16;37(33):7811-7823
pubmed: 28698386
Sci Rep. 2016 Oct 19;6:35359
pubmed: 27759117
WormBook. 2007 Feb 20;:1-15
pubmed: 18050501
Genetics. 2004 Aug;167(4):1677-87
pubmed: 15342507
Elife. 2016 Nov 28;5:
pubmed: 27893361
Genome Res. 2004 Oct;14(10B):2162-8
pubmed: 15489339
Neuron. 2016 Dec 7;92(5):1049-1062
pubmed: 27866800
Development. 2003 Apr;130(7):1215-24
pubmed: 12588839
Nature. 2011 Aug 17;477(7364):321-5
pubmed: 21849976
BMC Genomics. 2006 Dec 08;7:309
pubmed: 17156446
J Neurosci. 2007 Jun 6;27(23):6150-62
pubmed: 17553987
Annu Rev Med. 2009;60:355-66
pubmed: 19630576
Nat Neurosci. 1999 Nov;2(11):959-64
pubmed: 10526333
Neuron. 2005 Apr 21;46(2):247-60
pubmed: 15848803
Genes Cells. 2017 Feb;22(2):210-219
pubmed: 28105749