Maternal ω3 docosapentaenoic acid inhibits infant allergic dermatitis through TRAIL-expressing plasmacytoid dendritic cells in mice.
14-lipoxygenation
TRAIL
breast milk
infant allergy
ω3 DPA
Journal
Allergy
ISSN: 1398-9995
Titre abrégé: Allergy
Pays: Denmark
ID NLM: 7804028
Informations de publication
Date de publication:
08 2020
08 2020
Historique:
received:
11
07
2019
revised:
26
12
2019
accepted:
09
01
2020
pubmed:
7
2
2020
medline:
15
5
2021
entrez:
7
2
2020
Statut:
ppublish
Résumé
Maternal dietary exposures are considered to influence the development of infant allergies through changes in the composition of breast milk. Cohort studies have shown that ω3 polyunsaturated fatty acids (PUFAs) in breast milk may have a beneficial effect on the preventing of allergies in infants; however, the underlying mechanisms remain to be investigated. We investigated how the maternal intake of dietary ω3 PUFAs affects fatty acid profiles in the breast milk and their pups and reduced the incidence of allergic diseases in the pups. Contact hypersensitivity (CHS) induced by 2,4-dinitrofluorobenzene (DNFB) and fluorescein isothiocyanate was applied to the skin in pups reared by mother maintained with diets mainly containing ω3 or ω6 PUFAs. Skin inflammation, immune cell populations, and expression levels of immunomodulatory molecules in pups and/or human cell line were investigated by using flow cytometric, immunohistologic, and quantitative RT-PCR analyses. ω3 PUFA metabolites in breast milk and infant's serum were evaluated by lipidomics analysis using LC-MS/MS. We show that maternal intake of linseed oil, containing abundant ω3 α-linolenic acid, resulted in the increased levels of ω3 docosapentaenoic acid (DPA) and its 14-lipoxygenation products in the breast milk of mouse dams; these metabolites increased the expression of TNF-related apoptosis-inducing ligand (TRAIL) on plasmacytoid dendritic cells (pDCs) in their pups and thus inhibited infant CHS. Indeed, the administration of DPA-derived 14-lipoxygenation products to mouse pups ameliorated their DNFB CHS. These findings suggest that an inhibitory mechanism in infant skin allergy is induced through maternal metabolism of dietary ω3 PUFAs in mice.
Sections du résumé
BACKGROUND
Maternal dietary exposures are considered to influence the development of infant allergies through changes in the composition of breast milk. Cohort studies have shown that ω3 polyunsaturated fatty acids (PUFAs) in breast milk may have a beneficial effect on the preventing of allergies in infants; however, the underlying mechanisms remain to be investigated. We investigated how the maternal intake of dietary ω3 PUFAs affects fatty acid profiles in the breast milk and their pups and reduced the incidence of allergic diseases in the pups.
METHODS
Contact hypersensitivity (CHS) induced by 2,4-dinitrofluorobenzene (DNFB) and fluorescein isothiocyanate was applied to the skin in pups reared by mother maintained with diets mainly containing ω3 or ω6 PUFAs. Skin inflammation, immune cell populations, and expression levels of immunomodulatory molecules in pups and/or human cell line were investigated by using flow cytometric, immunohistologic, and quantitative RT-PCR analyses. ω3 PUFA metabolites in breast milk and infant's serum were evaluated by lipidomics analysis using LC-MS/MS.
RESULTS
We show that maternal intake of linseed oil, containing abundant ω3 α-linolenic acid, resulted in the increased levels of ω3 docosapentaenoic acid (DPA) and its 14-lipoxygenation products in the breast milk of mouse dams; these metabolites increased the expression of TNF-related apoptosis-inducing ligand (TRAIL) on plasmacytoid dendritic cells (pDCs) in their pups and thus inhibited infant CHS. Indeed, the administration of DPA-derived 14-lipoxygenation products to mouse pups ameliorated their DNFB CHS.
CONCLUSION
These findings suggest that an inhibitory mechanism in infant skin allergy is induced through maternal metabolism of dietary ω3 PUFAs in mice.
Identifiants
pubmed: 32027039
doi: 10.1111/all.14217
pmc: PMC7496639
doi:
Substances chimiques
Fatty Acids, Omega-3
0
Fatty Acids, Unsaturated
0
TNF-Related Apoptosis-Inducing Ligand
0
docosapentaenoic acid
NS3OZT14QT
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1939-1955Informations de copyright
© 2020 The Authors. Allergy published by John Wiley & Sons Ltd.
Références
J Invest Dermatol. 1995 Sep;105(3):334-8
pubmed: 7665908
Proc Natl Acad Sci U S A. 2017 Apr 11;114(15):3963-3968
pubmed: 28356517
Nat Immunol. 2014 Nov;15(11):1064-9
pubmed: 25240383
Sci Rep. 2013;3:1940
pubmed: 23736886
Nat Rev Immunol. 2009 May;9(5):353-63
pubmed: 19365408
Lipids. 2000 Jan;35(1):61-9
pubmed: 10695925
Nature. 2012 Apr 25;484(7395):524-8
pubmed: 22538616
J Allergy Clin Immunol. 2010 Apr;125(4):866-71
pubmed: 20236698
J Immunol. 2014 Apr 1;192(7):2975-83
pubmed: 24600030
Hepatology. 2007 Feb;45(2):445-54
pubmed: 17256750
Leuk Res. 2009 Sep;33(9):1224-32
pubmed: 19443030
J Invest Dermatol. 2013 Feb;133(2):303-15
pubmed: 22931926
J Invest Dermatol. 2018 Oct;138(10):2174-2184
pubmed: 29577920
Am J Clin Nutr. 2003 Jan;77(1):226-33
pubmed: 12499346
Medicine (Baltimore). 2016 Apr;95(15):e3391
pubmed: 27082611
Prostaglandins Leukot Essent Fatty Acids. 2017 Jun;121:1-6
pubmed: 28651692
Am J Physiol Endocrinol Metab. 2013 Sep 15;305(6):E700-16
pubmed: 23880316
Front Immunol. 2013 Nov 12;4:372
pubmed: 24282405
Allergol Select. 2017 Aug 4;1(1):71-76
pubmed: 30402605
Lipids Health Dis. 2013 Jun 15;12:89
pubmed: 23767972
Nutrients. 2015 Oct 22;7(10):8802-17
pubmed: 26506385
J Pediatr. 2007 Oct;151(4):347-51, 351.e1-2
pubmed: 17889066
Endocr Metab Immune Disord Drug Targets. 2014 Mar;14(1):9-15
pubmed: 24450452
Sci Rep. 2018 Apr 27;8(1):6639
pubmed: 29703903
Redox Biol. 2015 Dec;6:297-310
pubmed: 26298204
Allergy. 2018 Feb;73(2):295-312
pubmed: 28869762
Allergy. 2020 Aug;75(8):1939-1955
pubmed: 32027039
J Biochem. 2012 Oct;152(4):313-9
pubmed: 22923733
FASEB J. 2017 Apr;31(4):1273-1288
pubmed: 28087575
J Allergy Clin Immunol. 2018 Aug;142(2):470-484.e12
pubmed: 29288079
PLoS One. 2011;6(12):e29662
pubmed: 22216341
Blood. 2004 Oct 15;104(8):2418-24
pubmed: 15205263
Immunol Lett. 2013 Mar;151(1-2):61-7
pubmed: 23416169
Cell Rep. 2018 Oct 2;25(1):47-56.e3
pubmed: 30282037
J Invest Dermatol. 2005 Oct;125(4):746-52
pubmed: 16185275
Allergol Int. 2017 Jul;66(3):392-397
pubmed: 28320580
Exp Ther Med. 2011 Mar;2(2):317-323
pubmed: 22977504
J Lipid Res. 2013 Oct;54(10):2851-7
pubmed: 23873268
J Immunol. 2007 Sep 1;179(5):2690-4
pubmed: 17709480
Eur J Immunol. 2012 Nov;42(11):3019-27
pubmed: 22806638
Curr Allergy Asthma Rep. 2015 Feb;15(2):501
pubmed: 25612797
J Mammary Gland Biol Neoplasia. 2009 Dec;14(4):397-400
pubmed: 19936987
J Nutr. 2011 Feb;141(2):214-22
pubmed: 21178083
Eur J Immunol. 2006 Nov;36(11):2981-92
pubmed: 17048272
Proc Natl Acad Sci U S A. 2007 Oct 30;104(44):17453-8
pubmed: 17956986
Am J Clin Nutr. 2016 Sep;104(3):646-62
pubmed: 27534637
Clin Exp Allergy. 2015 Mar;45(3):583-601
pubmed: 25077553
Nutrients. 2016 Feb 17;8(2):99
pubmed: 26901223
Development. 2016 Nov 15;143(22):4236-4248
pubmed: 27729410
Epilepsy Behav. 2014 Apr;33:138-43
pubmed: 24662925
J Immunol. 2013 Mar 1;190(5):2199-207
pubmed: 23359502
J Exp Med. 2015 Oct 19;212(11):1921-30
pubmed: 26438363
Allergol Int. 2017 Oct;66(4):523-528
pubmed: 28693971
Immunity. 2010 Dec 14;33(6):905-16
pubmed: 21145760
Mucosal Immunol. 2016 May;9(3):757-766
pubmed: 26462421
J Immunol. 2014 Oct 15;193(8):4021-31
pubmed: 25217163
Nat Med. 2006 Feb;12(2):214-9
pubmed: 16444265
APMIS. 2012 Jan;120(1):1-27
pubmed: 22151305
Blood. 2010 Feb 11;115(6):1156-65
pubmed: 19965634
Cell. 2008 Oct 3;135(1):37-48
pubmed: 18854153
Prog Lipid Res. 2016 Oct;64:30-56
pubmed: 27496755
Pediatr Allergy Immunol. 2011 Aug;22(5):505-14
pubmed: 21332799
J Invest Dermatol. 2000 Aug;115(2):141-8
pubmed: 10951228
Immunity. 2008 Sep 19;29(3):464-75
pubmed: 18789731
J Allergy Clin Immunol. 2003 Dec;112(6):1178-84
pubmed: 14657879
J Invest Dermatol. 2009 Jun;129(6):1412-20
pubmed: 19122650
Adv Pharmacol. 2013;66:129-55
pubmed: 23433457
Sci Rep. 2015 Jun 11;5:9750
pubmed: 26065911
J Mol Med (Berl). 2017 Jun;95(6):575-588
pubmed: 28528513
Adv Nutr. 2012 May 01;3(3):370-6
pubmed: 22585914
Int J Biochem Cell Biol. 2007;39(7-8):1462-75
pubmed: 17403612
Clin Dev Immunol. 2012;2012:730568
pubmed: 23049602
J Lipid Res. 2005 Apr;46(4):706-15
pubmed: 15654130
Front Immunol. 2018 May 23;9:1119
pubmed: 29875774
Allergo J Int. 2015;24:170-179
pubmed: 27069837