A 12-lipoxygenase-Gpr31 signaling axis is required for pancreatic organogenesis in the zebrafish.


Journal

FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484

Informations de publication

Date de publication:
11 2020
Historique:
received: 11 09 2019
revised: 21 08 2020
accepted: 25 08 2020
pubmed: 13 9 2020
medline: 1 5 2021
entrez: 12 9 2020
Statut: ppublish

Résumé

12-Lipoxygenase (12-LOX) is a key enzyme in arachidonic acid metabolism, and alongside its major product, 12-HETE, plays a key role in promoting inflammatory signaling during diabetes pathogenesis. Although 12-LOX is a proposed therapeutic target to protect pancreatic islets in the setting of diabetes, little is known about the consequences of blocking its enzymatic activity during embryonic development. Here, we have leveraged the strengths of the zebrafish-genetic manipulation and pharmacologic inhibition-to interrogate the role of 12-LOX in pancreatic development. Lipidomics analysis during zebrafish development demonstrated that 12-LOX-generated metabolites of arachidonic acid increase sharply during organogenesis stages, and that this increase is blocked by morpholino-directed depletion of 12-LOX. Furthermore, we found that either depletion or inhibition of 12-LOX impairs both exocrine pancreas growth and unexpectedly, the generation of insulin-producing β cells. We demonstrate that morpholino-mediated knockdown of GPR31, a purported G-protein-coupled receptor for 12-HETE, largely phenocopies both the depletion and the inhibition of 12-LOX. Moreover, we show that loss of GPR31 impairs pancreatic bud fusion and pancreatic duct morphogenesis. Together, these data provide new insight into the requirement of 12-LOX in pancreatic organogenesis and islet formation, and additionally provide evidence that its effects are mediated via a signaling axis that includes the 12-HETE receptor GPR31.

Identifiants

pubmed: 32918516
doi: 10.1096/fj.201902308RR
pmc: PMC7606739
mid: NIHMS1634728
doi:

Substances chimiques

Receptors, G-Protein-Coupled 0
Zebrafish Proteins 0
Arachidonic Acid 27YG812J1I
Lipoxygenases EC 1.13.11.-

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

14850-14862

Subventions

Organisme : NIDDK NIH HHS
ID : R01 DK060581
Pays : United States
Organisme : NIDDK NIH HHS
ID : T32 DK064466
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK097512
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK105588
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK020579
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK020595
Pays : United States
Organisme : NCATS NIH HHS
ID : R03 TR003381
Pays : United States

Informations de copyright

© 2020 Federation of American Societies for Experimental Biology.

Références

Prostaglandins Other Lipid Mediat. 2014 Oct;113-115:52-61
pubmed: 25175316
Mediators Inflamm. 2012;2012:851798
pubmed: 23326022
J Biol Chem. 2011 Sep 30;286(39):33832-40
pubmed: 21712392
Prostaglandins Other Lipid Mediat. 2018 May;136:23-32
pubmed: 29605541
Proc Natl Acad Sci U S A. 2004 Nov 2;101(44):15579-84
pubmed: 15496467
Adv Exp Med Biol. 1999;469:83-9
pubmed: 10667314
Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):3100-5
pubmed: 9501222
Curr Biol. 2011 Apr 26;21(8):712-7
pubmed: 21497092
J Med Chem. 2011 Aug 11;54(15):5485-97
pubmed: 21739938
Biochim Biophys Acta. 2015 Apr;1851(4):308-30
pubmed: 25316652
PLoS One. 2011;6(4):e18556
pubmed: 21602908
Development. 2015 Apr 15;142(8):1407-17
pubmed: 25852199
Dev Biol. 2007 Apr 15;304(2):875-90
pubmed: 17335795
Curr Top Dev Biol. 2017;124:235-276
pubmed: 28335861
J Biol Chem. 2019 Apr 19;294(16):6612-6620
pubmed: 30792307
Development. 2005 Nov;132(22):5069-79
pubmed: 16258076
J Neurosci. 2015 Apr 15;35(15):6079-92
pubmed: 25878281
Diabetes. 2008 Jan;57(1):199-208
pubmed: 17940120
BMC Mol Biol. 2008 Nov 12;9:102
pubmed: 19014500
J Biol Chem. 1996 Sep 27;271(39):24055-62
pubmed: 8798642
Diabetologia. 2015 Mar;58(3):549-57
pubmed: 25417214
Rapid Commun Mass Spectrom. 2008;22(2):75-83
pubmed: 18059001
Proc Natl Acad Sci U S A. 2011 Dec 20;108(51):20479-84
pubmed: 22143766
Nat Med. 2018 Jan;24(1):73-83
pubmed: 29227475
Acta Biochim Biophys Sin (Shanghai). 2007 May;39(5):384-90
pubmed: 17492136
Brain Res. 2008 Oct 27;1237:35-43
pubmed: 18789910
Diabetes. 2017 Nov;66(11):2875-2887
pubmed: 28842399
Proc Natl Acad Sci U S A. 2009 Sep 1;106(35):14896-901
pubmed: 19706417
J Clin Invest. 1999 May 15;103(10):1431-6
pubmed: 10330425
FASEB J. 2016 Jun;30(6):2360-9
pubmed: 26965684
Biochemistry. 2019 Feb 12;58(6):848-857
pubmed: 30565457
Nat Protoc. 2008;3(1):59-69
pubmed: 18193022
Dev Biol. 2016 Jan 15;409(2):354-69
pubmed: 26658317
Sci Rep. 2015 Aug 24;5:13269
pubmed: 26299433
Mol Cell Biol. 2014 Oct 1;34(19):3735-45
pubmed: 25071151
Redox Biol. 2013 Dec 17;2:105-13
pubmed: 24416717
J Cell Biol. 2017 Aug 7;216(8):2329-2338
pubmed: 28619714
J Biol Chem. 2011 Oct 28;286(43):37804-12
pubmed: 21880725
Dev Biol. 2008 May 15;317(2):467-79
pubmed: 18394596
J Nat Prod. 2003 Feb;66(2):230-5
pubmed: 12608855
Diabet Med. 2017 Feb;34(2):292-294
pubmed: 27353008
J Clin Endocrinol Metab. 2015 Mar;100(3):E387-95
pubmed: 25532042

Auteurs

Marimar Hernandez-Perez (M)

Department of Pediatrics, Center for Diabetes and Metabolic Diseases, Indiana University School of Medicine, Indianapolis, IN, USA.

Abhishek Kulkarni (A)

Department of Biochemistry and Molecular Biology, Indiana University School of Medicine, Indianapolis, IN, USA.

Niharika Samala (N)

Department of Medicine, Indiana University School of Medicine, Indianapolis, IN, USA.

Cody Sorrell (C)

Department of Pediatrics, Center for Diabetes and Metabolic Diseases, Indiana University School of Medicine, Indianapolis, IN, USA.

Kimberly El (K)

Department of Pediatrics, Center for Diabetes and Metabolic Diseases, Indiana University School of Medicine, Indianapolis, IN, USA.

Isra Haider (I)

Department of Pediatrics, Center for Diabetes and Metabolic Diseases, Indiana University School of Medicine, Indianapolis, IN, USA.

Ansari Mukhtar Aleem (A)

Department of Chemistry and Biochemistry, University of California Santa Cruz, Santa Cruz, CA, USA.

Theodore R Holman (TR)

Department of Chemistry and Biochemistry, University of California Santa Cruz, Santa Cruz, CA, USA.

Ganesha Rai (G)

National Center for Advancing Translational Sciences, National Institutes of Health, Rockville, MD, USA.

Sarah A Tersey (SA)

Department of Pediatrics, Center for Diabetes and Metabolic Diseases, Indiana University School of Medicine, Indianapolis, IN, USA.

Raghavendra G Mirmira (RG)

Department of Pediatrics, Center for Diabetes and Metabolic Diseases, Indiana University School of Medicine, Indianapolis, IN, USA.
Department of Biochemistry and Molecular Biology, Indiana University School of Medicine, Indianapolis, IN, USA.
Department of Medicine, Indiana University School of Medicine, Indianapolis, IN, USA.
Department of Medicine, Kovler Diabetes Center, The University of Chicago, Chicago, IL, USA.

Ryan M Anderson (RM)

Department of Pediatrics, Center for Diabetes and Metabolic Diseases, Indiana University School of Medicine, Indianapolis, IN, USA.
Department of Medicine, Kovler Diabetes Center, The University of Chicago, Chicago, IL, USA.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH