Human Semaphorin 3 Variants Link Melanocortin Circuit Development and Energy Balance.


Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
07 02 2019
Historique:
received: 04 12 2017
revised: 28 08 2018
accepted: 05 12 2018
pubmed: 22 1 2019
medline: 4 12 2019
entrez: 22 1 2019
Statut: ppublish

Résumé

Hypothalamic melanocortin neurons play a pivotal role in weight regulation. Here, we examined the contribution of Semaphorin 3 (SEMA3) signaling to the development of these circuits. In genetic studies, we found 40 rare variants in SEMA3A-G and their receptors (PLXNA1-4; NRP1-2) in 573 severely obese individuals; variants disrupted secretion and/or signaling through multiple molecular mechanisms. Rare variants in this set of genes were significantly enriched in 982 severely obese cases compared to 4,449 controls. In a zebrafish mutagenesis screen, deletion of 7 genes in this pathway led to increased somatic growth and/or adiposity demonstrating that disruption of Semaphorin 3 signaling perturbs energy homeostasis. In mice, deletion of the Neuropilin-2 receptor in Pro-opiomelanocortin neurons disrupted their projections from the arcuate to the paraventricular nucleus, reduced energy expenditure, and caused weight gain. Cumulatively, these studies demonstrate that SEMA3-mediated signaling drives the development of hypothalamic melanocortin circuits involved in energy homeostasis.

Identifiants

pubmed: 30661757
pii: S0092-8674(18)31623-4
doi: 10.1016/j.cell.2018.12.009
pmc: PMC6370916
pii:
doi:

Substances chimiques

Leptin 0
Melanocortins 0
Nerve Tissue Proteins 0
Receptors, Cell Surface 0
Semaphorins 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

729-742.e18

Subventions

Organisme : Medical Research Council
ID : MR/L003120/1
Pays : United Kingdom
Organisme : British Heart Foundation
ID : RG/13/13/30194
Pays : United Kingdom
Organisme : Department of Health
ID : BTRU-2014-10024
Pays : United Kingdom
Organisme : NIDDK NIH HHS
ID : R01 DK118401
Pays : United States
Organisme : Medical Research Council
ID : MR/S025685/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 098497/Z/12/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 100574/Z/12/Z
Pays : United Kingdom
Organisme : NIDDK NIH HHS
ID : R01 DK084142
Pays : United States
Organisme : Medical Research Council
ID : MC_UU_12012/1
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Medical Research Council
ID : G0900554
Pays : United Kingdom
Organisme : Wellcome Trust
ID : WT098051
Pays : United Kingdom
Organisme : Cancer Research UK
ID : C375/A17721
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 099038/Z/12/Z
Pays : United Kingdom
Organisme : British Heart Foundation
ID : RG/10/17/28553
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 203141/Z/16/Z
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_00014/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M000141/1
Pays : United Kingdom
Organisme : British Heart Foundation
ID : RG/18/13/33946
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_12012/5
Pays : United Kingdom
Organisme : NIDDK NIH HHS
ID : R01 DK102780
Pays : United States

Commentaires et corrections

Type : CommentIn
Type : CommentIn

Informations de copyright

Copyright © 2018 The Authors. Published by Elsevier Inc. All rights reserved.

Références

Nucleic Acids Res. 2014 Dec 16;42(22):e168
pubmed: 25300484
Stem Cells Int. 2018 Feb 25;2018:1075156
pubmed: 29535768
Nat Neurosci. 2016 Apr;19(4):571-7
pubmed: 26974950
Cell. 1997 Jan 10;88(1):131-41
pubmed: 9019399
J Neurosci. 2002 May 15;22(10):4025-35
pubmed: 12019322
Nat Med. 1999 Sep;5(9):1066-70
pubmed: 10470087
J Clin Invest. 2015 Jun;125(6):2413-28
pubmed: 25985275
Nat Struct Mol Biol. 2012 Dec;19(12):1293-9
pubmed: 23104057
Hum Reprod. 2012 May;27(5):1460-5
pubmed: 22416012
PLoS One. 2015 Mar 23;10(3):e0120776
pubmed: 25799180
Nat Rev Neurosci. 2012 Sep;13(9):605-18
pubmed: 22895477
Bioinformatics. 2014 Oct 15;30(20):2843-51
pubmed: 24974202
Mol Syst Biol. 2011 Oct 11;7:539
pubmed: 21988835
Nature. 2010 Oct 28;467(7319):1061-73
pubmed: 20981092
Nat Neurosci. 2010 Jan;13(1):133-40
pubmed: 20023653
Proc Natl Acad Sci U S A. 2014 Jan 28;111(4):E455-64
pubmed: 24443550
Annu Rev Cell Dev Biol. 2007;23:263-92
pubmed: 17539753
Nature. 2015 Oct 1;526(7571):82-90
pubmed: 26367797
Cell Metab. 2012 Feb 8;15(2):256-64
pubmed: 22245570
Nat Neurosci. 1998 Oct;1(6):445-50
pubmed: 10196541
Eur J Endocrinol. 2018 Apr;178(4):377-388
pubmed: 29419413
N Engl J Med. 2003 Mar 20;348(12):1085-95
pubmed: 12646665
Genome Res. 2015 Jul;25(7):1030-42
pubmed: 26048245
Nat Genet. 1998 Oct;20(2):113-4
pubmed: 9771699
Dev Dyn. 2009 Dec;238(12):2975-3015
pubmed: 19891001
Nature. 2014 Feb 13;506(7487):185-90
pubmed: 24463508
Science. 2004 Apr 2;304(5667):108-10
pubmed: 15064420
Neuron. 2004 Jun 24;42(6):983-91
pubmed: 15207242
J Neurosci. 2012 Jun 20;32(25):8554-9
pubmed: 22723695
Neuron. 1997 Sep;19(3):519-30
pubmed: 9331345
Nat Genet. 2011 May;43(5):491-8
pubmed: 21478889
Sci Rep. 2017 Jun 29;7(1):4394
pubmed: 28663568
Proc Natl Acad Sci U S A. 2015 Apr 7;112(14):4363-8
pubmed: 25831505
J Cell Sci. 2014 Dec 15;127(Pt 24):5240-52
pubmed: 25335892
Am J Hum Genet. 2012 Nov 2;91(5):839-48
pubmed: 23103226
Am J Hum Genet. 2007 Sep;81(3):559-75
pubmed: 17701901
Science. 2013 Jul 19;341(6143):278-81
pubmed: 23869017
J Clin Invest. 2012 Mar;122(3):1000-9
pubmed: 22326958
Am J Hum Genet. 2015 Apr 2;96(4):581-96
pubmed: 25839327
Trials. 2014 Sep 17;15:363
pubmed: 25230735
Nat Genet. 2006 Aug;38(8):904-9
pubmed: 16862161
Nat Med. 2010 Apr;16(4):403-5
pubmed: 20348924
Curr Protoc Bioinformatics. 2013;43:11.10.1-11.10.33
pubmed: 25431634
Neuron. 2001 Oct 25;32(2):249-63
pubmed: 11683995
Neuron. 2016 Aug 3;91(3):548-60
pubmed: 27397516
Nature. 2017 Oct 5;550(7674):109-113
pubmed: 28953869
Nat Genet. 1998 Jun;19(2):155-7
pubmed: 9620771
PLoS Genet. 2012 Aug;8(8):e1002896
pubmed: 22927827
Nat Genet. 2013 Dec;45(12):1418-27
pubmed: 24141362
Nat Genet. 1998 Oct;20(2):111-2
pubmed: 9771698
Nature. 2001 May 24;411(6836):480-4
pubmed: 11373681
Nat Genet. 2013 May;45(5):513-7
pubmed: 23563609
Dis Model Mech. 2017 Jun 1;10(6):797-809
pubmed: 28348140

Auteurs

Agatha A van der Klaauw (AA)

University of Cambridge Metabolic Research Laboratories and NIHR Cambridge Biomedical Research Centre, Wellcome-MRC Institute of Metabolic Science, Addenbrooke's Hospital, Cambridge, UK.

Sophie Croizier (S)

The Saban Research Institute, Developmental Neuroscience Program, Center for Endocrinology, Diabetes and Metabolism, Children's Hospital Los Angeles, University of Southern California, Los Angeles, CA 90027, USA; Center for Integrative Genomics, University of Lausanne, Lausanne, Switzerland.

Edson Mendes de Oliveira (E)

University of Cambridge Metabolic Research Laboratories and NIHR Cambridge Biomedical Research Centre, Wellcome-MRC Institute of Metabolic Science, Addenbrooke's Hospital, Cambridge, UK.

Lukas K J Stadler (LKJ)

University of Cambridge Metabolic Research Laboratories and NIHR Cambridge Biomedical Research Centre, Wellcome-MRC Institute of Metabolic Science, Addenbrooke's Hospital, Cambridge, UK.

Soyoung Park (S)

The Saban Research Institute, Developmental Neuroscience Program, Center for Endocrinology, Diabetes and Metabolism, Children's Hospital Los Angeles, University of Southern California, Los Angeles, CA 90027, USA.

Youxin Kong (Y)

Division of Structural Biology, Wellcome Centre for Human Genetics, University of Oxford, Oxford, UK; Pathogenesis of Vascular Infections Unit, INSERM, Institut Pasteur, Paris, France.

Matthew C Banton (MC)

University of Cambridge Metabolic Research Laboratories and NIHR Cambridge Biomedical Research Centre, Wellcome-MRC Institute of Metabolic Science, Addenbrooke's Hospital, Cambridge, UK; School of Biological and Marine Sciences, University of Plymouth, Plymouth, UK.

Panna Tandon (P)

Centre for Cardiovascular Science, The Queen's Medical Research Institute, University of Edinburgh, UK.

Audrey E Hendricks (AE)

Wellcome Sanger Institute, Cambridge, UK; Department of Mathematical and Statistical Sciences, University of Colorado-Denver, Denver, CO 80204, USA.

Julia M Keogh (JM)

University of Cambridge Metabolic Research Laboratories and NIHR Cambridge Biomedical Research Centre, Wellcome-MRC Institute of Metabolic Science, Addenbrooke's Hospital, Cambridge, UK.

Susanna E Riley (SE)

Centre for Cardiovascular Science, The Queen's Medical Research Institute, University of Edinburgh, UK.

Sofia Papadia (S)

University of Cambridge Metabolic Research Laboratories and NIHR Cambridge Biomedical Research Centre, Wellcome-MRC Institute of Metabolic Science, Addenbrooke's Hospital, Cambridge, UK.

Elana Henning (E)

University of Cambridge Metabolic Research Laboratories and NIHR Cambridge Biomedical Research Centre, Wellcome-MRC Institute of Metabolic Science, Addenbrooke's Hospital, Cambridge, UK.

Rebecca Bounds (R)

University of Cambridge Metabolic Research Laboratories and NIHR Cambridge Biomedical Research Centre, Wellcome-MRC Institute of Metabolic Science, Addenbrooke's Hospital, Cambridge, UK.

Elena G Bochukova (EG)

University of Cambridge Metabolic Research Laboratories and NIHR Cambridge Biomedical Research Centre, Wellcome-MRC Institute of Metabolic Science, Addenbrooke's Hospital, Cambridge, UK; The Blizard Institute, Barts and The London School of Medicine and Dentistry, Queen Mary University of London, London, UK.

Vanisha Mistry (V)

University of Cambridge Metabolic Research Laboratories and NIHR Cambridge Biomedical Research Centre, Wellcome-MRC Institute of Metabolic Science, Addenbrooke's Hospital, Cambridge, UK.

Stephen O'Rahilly (S)

University of Cambridge Metabolic Research Laboratories and NIHR Cambridge Biomedical Research Centre, Wellcome-MRC Institute of Metabolic Science, Addenbrooke's Hospital, Cambridge, UK.

Richard B Simerly (RB)

The Saban Research Institute, Developmental Neuroscience Program, Center for Endocrinology, Diabetes and Metabolism, Children's Hospital Los Angeles, University of Southern California, Los Angeles, CA 90027, USA; Department of Molecular Physiology and Biophysics, Vanderbilt University, Nashville, Tennessee, TN 37232-0615, USA.

James E N Minchin (JEN)

Centre for Cardiovascular Science, The Queen's Medical Research Institute, University of Edinburgh, UK.

Inês Barroso (I)

University of Cambridge Metabolic Research Laboratories and NIHR Cambridge Biomedical Research Centre, Wellcome-MRC Institute of Metabolic Science, Addenbrooke's Hospital, Cambridge, UK; Wellcome Sanger Institute, Cambridge, UK.

E Yvonne Jones (EY)

Division of Structural Biology, Wellcome Centre for Human Genetics, University of Oxford, Oxford, UK.

Sebastien G Bouret (SG)

The Saban Research Institute, Developmental Neuroscience Program, Center for Endocrinology, Diabetes and Metabolism, Children's Hospital Los Angeles, University of Southern California, Los Angeles, CA 90027, USA; INSERM U1172, Jean-Pierre Aubert Research Center, Lille, France. Electronic address: sbouret@chla.usc.edu.

I Sadaf Farooqi (IS)

University of Cambridge Metabolic Research Laboratories and NIHR Cambridge Biomedical Research Centre, Wellcome-MRC Institute of Metabolic Science, Addenbrooke's Hospital, Cambridge, UK. Electronic address: isf20@cam.ac.uk.

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Classifications MeSH