A neural circuit linking two sugar sensors regulates satiety-dependent fructose drive in


Journal

Science advances
ISSN: 2375-2548
Titre abrégé: Sci Adv
Pays: United States
ID NLM: 101653440

Informations de publication

Date de publication:
03 Dec 2021
Historique:
entrez: 1 12 2021
pubmed: 2 12 2021
medline: 2 12 2021
Statut: ppublish

Résumé

In flies, neuronal sensors detect prandial changes in circulating fructose levels and either sustain or terminate feeding, depending on internal state. Here, we describe a three-part neural circuit that imparts satiety-dependent modulation of fructose sensing. We show that dorsal fan-shaped body neurons display oscillatory calcium activity when hemolymph glucose is high and that these oscillations require glutamatergic input from SLP-AB or “Janus” neurons projecting from the protocerebrum to the asymmetric body. Suppression of activity in this circuit, either by starvation or by genetic silencing, promotes specific drive for fructose ingestion. This is achieved through neuropeptidergic signaling by tachykinin, which is released from the fan-shaped body when glycemia is high. Tachykinin, in turn, signals to Gr43a-positive fructose sensors to modulate their response to fructose. Together, our results demonstrate how a three-layer neural circuit links the detection of two sugars to produce precise satiety-dependent control of feeding behavior.

Identifiants

pubmed: 34851668
doi: 10.1126/sciadv.abj0186
pmc: PMC8635442
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

eabj0186

Références

Nature. 2004 Feb 12;427(6975):605-6
pubmed: 14961111
Learn Mem. 2008 Feb 28;15(3):133-42
pubmed: 18310460
Phys Rev Lett. 2009 Oct 9;103(15):158102
pubmed: 19905668
Cell. 2015 Jun 18;161(7):1656-67
pubmed: 26073942
PLoS Genet. 2020 Oct 26;16(10):e1009064
pubmed: 33104728
Nature. 2006 Feb 2;439(7076):551-6
pubmed: 16452971
Neuron. 2013 Oct 2;80(1):171-83
pubmed: 24094110
PLoS Genet. 2021 Mar 8;17(3):e1009425
pubmed: 33684132
Cell Rep. 2012 Oct 25;2(4):991-1001
pubmed: 23063364
Neurosci Biobehav Rev. 2018 Feb;85:1-20
pubmed: 28887225
Peptides. 2009 Mar;30(3):545-56
pubmed: 19022310
Neurosci Biobehav Rev. 2010 Jun;34(7):1023-35
pubmed: 20060015
J Nutr Sci Vitaminol (Tokyo). 2009 Jun;55(3):201-7
pubmed: 19602827
Cell Res. 2021 May;31(5):580-588
pubmed: 33273704
Biol Cybern. 1988;60(2):121-30
pubmed: 3228555
Cell Rep. 2015 Feb 24;10(7):1023-31
pubmed: 25704807
Neuron. 2009 Feb 12;61(3):373-84
pubmed: 19217375
J Comp Neurol. 2015 May 1;523(7):997-1037
pubmed: 25380328
Curr Biol. 2014 Sep 8;24(17):1978-84
pubmed: 25131672
Neuron. 2018 Apr 18;98(2):350-365.e5
pubmed: 29673482
Eur J Neurosci. 1997 Dec;9(12):2702-11
pubmed: 9517475
Nature. 1996 Nov 14;384(6605):162-6
pubmed: 8906790
Metabolism. 2012 May;61(5):641-51
pubmed: 22152650
Nutrients. 2019 Dec 29;12(1):
pubmed: 31905727
Neuroscience. 2012 Apr 19;208:11-26
pubmed: 22361394
Curr Opin Neurobiol. 2002 Dec;12(6):633-8
pubmed: 12490252
J Exp Biol. 2019 Feb 6;222(Pt Suppl 1):
pubmed: 30728235
Neuropharmacology. 2010 Jan;58(1):248-58
pubmed: 19576913
Proc Natl Acad Sci U S A. 2015 Oct 6;112(40):E5523-32
pubmed: 26324910
J Neurobiol. 2006 Jan;66(1):33-46
pubmed: 16193493
Hereditas. 1999;130(2):95-103
pubmed: 10479996
J Exp Biol. 2011 Dec 15;214(Pt 24):4201-8
pubmed: 22116763
Nature. 2019 Oct;574(7779):559-564
pubmed: 31645735
Cell Rep. 2018 Aug 7;24(6):1573-1584
pubmed: 30089267
Nat Methods. 2014 Mar;11(3):338-46
pubmed: 24509633
Nature. 2004 Apr 1;428(6982):569-74
pubmed: 15058305
Neurobiol Learn Mem. 2008 Nov;90(4):589-95
pubmed: 18755283
Elife. 2020 Dec 30;9:
pubmed: 33377868
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Am J Physiol Endocrinol Metab. 2013 Apr 1;304(7):E677-85
pubmed: 23341495
Genetics. 2004 May;167(1):311-23
pubmed: 15166157
Physiology (Bethesda). 2020 Jan 1;35(1):4-15
pubmed: 31799908
Cell Tissue Res. 2004 May;316(2):281-93
pubmed: 14999560
Nature. 2013 Jul 18;499(7458):295-300
pubmed: 23868258
Front Neuroinform. 2022 Jul 20;16:896292
pubmed: 35935535
Annu Rev Entomol. 2014;59:165-84
pubmed: 24160424
J Biol Chem. 1980 May 25;255(10):4673-9
pubmed: 6768723
J Neurosci. 2012 Oct 17;32(42):14767-74
pubmed: 23077061
J Comp Neurol. 2018 Nov 1;526(16):2585-2611
pubmed: 30084503
Proc Natl Acad Sci U S A. 2009 Aug 4;106(31):13070-5
pubmed: 19625621
Front Neural Circuits. 2015 Mar 10;9:8
pubmed: 25805973
Nat Commun. 2014 Aug 04;5:4560
pubmed: 25087594
EMBO J. 1991 Nov;10(11):3221-9
pubmed: 1717263
Neurosci Biobehav Rev. 2021 Sep;128:346-357
pubmed: 34182019
Nat Neurosci. 2012 Nov;15(11):1516-23
pubmed: 23064381
Clin Neurophysiol. 1999 Nov;110(11):1842-57
pubmed: 10576479
Nat Commun. 2017 Jun 05;8:15510
pubmed: 28580949
Cell Mol Life Sci. 2012 Dec;69(23):4051-66
pubmed: 22828865
Curr Biol. 2019 Nov 4;29(21):3611-3621.e3
pubmed: 31630955
J Comp Neurol. 2011 Feb 1;519(2):290-315
pubmed: 21165976
Curr Biol. 2011 May 10;21(9):746-50
pubmed: 21514159
Elife. 2020 Jun 26;9:
pubmed: 32589143
Cell. 2012 Nov 21;151(5):1113-25
pubmed: 23178127
Proc Natl Acad Sci U S A. 2009 Feb 17;106(7):2383-8
pubmed: 19179284
Science. 2011 Jun 24;332(6037):1571-6
pubmed: 21700877
Curr Biol. 2015 Mar 2;25(5):621-627
pubmed: 25702577
Cell. 2004 Jun 25;117(7):981-91
pubmed: 15210117
Elife. 2021 Oct 26;10:
pubmed: 34696823
Nat Commun. 2021 Jul 5;12(1):4131
pubmed: 34226544
Elife. 2019 Jul 19;8:
pubmed: 31322499
Cell. 2014 Jan 16;156(1-2):221-35
pubmed: 24439378
Neuron. 2015 Jul 1;87(1):139-51
pubmed: 26074004
Elife. 2019 Sep 19;8:
pubmed: 31535971
Proc Natl Acad Sci U S A. 2008 Nov 4;105(44):16871-5
pubmed: 18971329
Nature. 2019 Dec;576(7785):121-125
pubmed: 31748749
J Exp Biol. 1988 Sep;139:169-79
pubmed: 2905379
Neuron. 2017 Nov 15;96(4):783-795.e4
pubmed: 29107518
Nat Commun. 2015 Mar 25;6:6667
pubmed: 25807033
Proc Natl Acad Sci U S A. 2011 Jul 12;108(28):11644-9
pubmed: 21709242
J Comp Neurol. 2003 Sep 15;464(2):180-96
pubmed: 12898611
Fly (Austin). 2014;8(1):19-25
pubmed: 24406333
Curr Opin Neurobiol. 2011 Jun;21(3):475-85
pubmed: 21429736
Neuron. 2016 Dec 7;92(5):1036-1048
pubmed: 27889096
PLoS One. 2019 Jul 11;14(7):e0219719
pubmed: 31295329
Cell Tissue Res. 2009 Jun;336(3):509-19
pubmed: 19357870
Nat Neurosci. 2012 Feb 26;15(4):592-9
pubmed: 22366756
J Neurobiol. 2006 Jul;66(8):821-34
pubmed: 16673386
Appetite. 2001 Feb;36(1):79-83
pubmed: 11161347
Neuron. 2008 Mar 27;57(6):930-41
pubmed: 18367093

Auteurs

Pierre-Yves Musso (PY)

Department of Zoology and Life Sciences Institute, University of British Columbia, Vancouver, Canada.

Pierre Junca (P)

Department of Zoology and Life Sciences Institute, University of British Columbia, Vancouver, Canada.

Michael D Gordon (MD)

Department of Zoology and Life Sciences Institute, University of British Columbia, Vancouver, Canada.

Classifications MeSH