Biofilm propensity of Staphylococcus aureus skin isolates is associated with increased atopic dermatitis severity and barrier dysfunction in the MPAACH pediatric cohort.
Staphylococcus aureus
S100A8/S100A9
atopic dermatitis
biofilm
filaggrin
Journal
Allergy
ISSN: 1398-9995
Titre abrégé: Allergy
Pays: Denmark
ID NLM: 7804028
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
14
12
2019
revised:
30
04
2020
accepted:
24
05
2020
pubmed:
9
7
2020
medline:
15
5
2021
entrez:
9
7
2020
Statut:
ppublish
Résumé
Atopic dermatitis (AD) patients are often colonized with Staphylococcus aureus, and staphylococcal biofilms have been reported on adult AD skin lesions. The commensal S epidermidis can antagonize S aureus, although its role in AD is unclear. We sought to characterize S aureus and S epidermidis colonization and biofilm propensity and determine their associations with AD severity, barrier function, and epidermal gene expression in the first US early-life cohort of children with AD, the Mechanisms of Progression of Atopic Dermatitis to Asthma in Children (MPAACH). The biofilm propensity of staphylococcal isolates was assessed by crystal violet assays. Gene expression of filaggrin and antimicrobial alarmins S100A8 and S100A9 was measured in keratinocyte RNA extracted from skin tape strips. Staphylococcal biofilms sampled from MPAACH skin were visualized using scanning electron microscopy. Sixty-two percent of staphylococcal isolates (sampled from 400 subjects) formed moderate/strong biofilms. Sixty-eight percent of subjects co-colonized with both staphylococcal species exhibited strains that formed cooperative mixed-species biofilms. Scanning electron microscopy verified the presence of staphylococcal biofilms on the skin of MPAACH children. Staphylococcus aureus strains showing higher relative biofilm propensity compared with S epidermidis were associated with increased AD severity (P = .03) and increased lesional and nonlesional transepidermal water loss (P = .01, P = .03). Our data suggest a pathogenic role for S aureus biofilms in AD. We found that strain-level variation in staphylococcal isolates governs the interactions between S epidermidis and S aureus and that the balance between these two species, and their biofilm propensity, has important implications for AD.
Sections du résumé
BACKGROUND
Atopic dermatitis (AD) patients are often colonized with Staphylococcus aureus, and staphylococcal biofilms have been reported on adult AD skin lesions. The commensal S epidermidis can antagonize S aureus, although its role in AD is unclear. We sought to characterize S aureus and S epidermidis colonization and biofilm propensity and determine their associations with AD severity, barrier function, and epidermal gene expression in the first US early-life cohort of children with AD, the Mechanisms of Progression of Atopic Dermatitis to Asthma in Children (MPAACH).
METHODS
The biofilm propensity of staphylococcal isolates was assessed by crystal violet assays. Gene expression of filaggrin and antimicrobial alarmins S100A8 and S100A9 was measured in keratinocyte RNA extracted from skin tape strips. Staphylococcal biofilms sampled from MPAACH skin were visualized using scanning electron microscopy.
RESULTS
Sixty-two percent of staphylococcal isolates (sampled from 400 subjects) formed moderate/strong biofilms. Sixty-eight percent of subjects co-colonized with both staphylococcal species exhibited strains that formed cooperative mixed-species biofilms. Scanning electron microscopy verified the presence of staphylococcal biofilms on the skin of MPAACH children. Staphylococcus aureus strains showing higher relative biofilm propensity compared with S epidermidis were associated with increased AD severity (P = .03) and increased lesional and nonlesional transepidermal water loss (P = .01, P = .03).
CONCLUSIONS
Our data suggest a pathogenic role for S aureus biofilms in AD. We found that strain-level variation in staphylococcal isolates governs the interactions between S epidermidis and S aureus and that the balance between these two species, and their biofilm propensity, has important implications for AD.
Identifiants
pubmed: 32640045
doi: 10.1111/all.14489
pmc: PMC8561741
mid: NIHMS1746471
doi:
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
302-313Subventions
Organisme : NIAID NIH HHS
ID : R01 AI127392
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM063483
Pays : United States
Organisme : NIAID NIH HHS
ID : U19 AI070235
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR001425
Pays : United States
Informations de copyright
© 2020 EAACI and John Wiley and Sons A/S. Published by John Wiley and Sons Ltd.
Références
Lancet. 2001 Jul 14;358(9276):135-8
pubmed: 11463434
J Clin Microbiol. 1985 Dec;22(6):996-1006
pubmed: 3905855
J Allergy Clin Immunol. 2018 Nov;142(5):1643-1647.e12
pubmed: 30048670
J Allergy Clin Immunol. 2008 Mar;121(3):725-730.e2
pubmed: 18249438
J Biol Chem. 2015 Jul 31;290(31):18991-8
pubmed: 26055713
Proc Natl Acad Sci U S A. 2013 Jan 15;110(3):E202-11
pubmed: 23277549
Cell Microbiol. 2004 Mar;6(3):269-75
pubmed: 14764110
Br J Dermatol. 2003 Mar;148(3):526-32
pubmed: 12653745
J Biomed Inform. 2009 Apr;42(2):377-81
pubmed: 18929686
J Dermatol Sci. 2005 Jun;38(3):207-13
pubmed: 15927814
J Invest Dermatol. 1993 Mar;100(3):225-8
pubmed: 8440891
Cell Host Microbe. 2017 Dec 13;22(6):746-756.e5
pubmed: 29199097
J Allergy Clin Immunol. 2007 Jul;120(1):150-5
pubmed: 17512043
Protein Sci. 2017 Oct;26(10):1964-1973
pubmed: 28707417
Science. 2019 Jan 4;363(6422):
pubmed: 30523076
Acta Derm Venereol. 1990;70(5):400-4
pubmed: 1980973
Curr Allergy Asthma Rep. 2015 Nov;15(11):65
pubmed: 26404536
J Immunol. 2011 Jun 1;186(11):6585-96
pubmed: 21525381
Br J Dermatol. 2017 Nov;177(5):1394-1400
pubmed: 28317091
J Bacteriol. 2014 Oct;196(19):3482-93
pubmed: 25070736
JAMA Dermatol. 2014 Mar;150(3):260-5
pubmed: 24452476
Nat Med. 2000 Nov;6(11):1275-7
pubmed: 11062541
Nat Rev Immunol. 2016 May 27;16(6):353-66
pubmed: 27231051
Nat Microbiol. 2018 Aug;3(8):881-890
pubmed: 30013237
Nature. 2015 Apr 2;520(7545):104-8
pubmed: 25539086
J Allergy Clin Immunol. 2012 Jun;129(6):1538-46.e6
pubmed: 22409988
J Microbiol Methods. 2000 Apr;40(2):175-9
pubmed: 10699673
Sci Rep. 2018 Jun 28;8(1):9573
pubmed: 29955077
J Invest Dermatol. 2017 Feb;137(2):377-384
pubmed: 27765722
Clin Rev Allergy Immunol. 2016 Dec;51(3):329-337
pubmed: 27377298
Int J Dermatol. 2011 Aug;50(8):992-3
pubmed: 21781075
J Dermatol Sci. 2005 Jun;38(3):197-205
pubmed: 15927813
Biochem J. 2017 Feb 1;474(3):427-443
pubmed: 27872164
Curr Allergy Asthma Rep. 2014 May;14(5):433
pubmed: 24633617
Dermatology. 2013;226(3):222-6
pubmed: 23796755
Sci Rep. 2017 Aug 18;7(1):8689
pubmed: 28821865
Science. 2014 Nov 21;346(6212):954-9
pubmed: 25414304
J Allergy Clin Immunol. 2009 Sep;124(3):485-93, 493.e1
pubmed: 19665780
Immunity. 2015 Apr 21;42(4):756-66
pubmed: 25902485
Science. 2019 Jan 18;363(6424):227-228
pubmed: 30655428
Curr Opin Pediatr. 2003 Aug;15(4):399-404
pubmed: 12891053
Eur J Clin Microbiol Infect Dis. 2002 Apr;21(4):269-76
pubmed: 12072937
J Allergy Clin Immunol. 2017 Jan;139(1):166-172
pubmed: 27609659
Nat Rev Microbiol. 2004 Feb;2(2):95-108
pubmed: 15040259
Proc Natl Acad Sci U S A. 2016 Jan 12;113(2):410-5
pubmed: 26715750
Proc Natl Acad Sci U S A. 2013 Mar 5;110(10):3841-6
pubmed: 23431180
J Clin Invest. 2003 Nov;112(10):1466-77
pubmed: 14617746
J Korean Med Sci. 2003 Feb;18(1):93-6
pubmed: 12589094
J Clin Cell Immunol. 2014 Apr;5(2):
pubmed: 25419479
Proc Natl Acad Sci U S A. 2012 Jan 24;109(4):1281-6
pubmed: 22232686
J Invest Dermatol. 2014 Aug;134(8):2114-2121
pubmed: 24468745
Toxins (Basel). 2016 Dec 23;9(1):
pubmed: 28025545
Sci Transl Med. 2019 Feb 20;11(480):
pubmed: 30787169
J Allergy Clin Immunol. 2010 Dec;126(6):1184-90.e3
pubmed: 21036388
J Allergy Clin Immunol. 2015 Apr;135(4):930-935.e1
pubmed: 25618747
J Invest Dermatol. 2017 Dec;137(12):2497-2504
pubmed: 28842320
J Allergy Clin Immunol Pract. 2020 Jul - Aug;8(7):2285-2293.e6
pubmed: 32302785
J Invest Dermatol. 2018 Oct;138(10):2224-2233
pubmed: 29604251
Dermatology. 1997;195(1):10-9
pubmed: 9267730
Proc Natl Acad Sci U S A. 2008 Dec 9;105(49):19456-61
pubmed: 19047636
PLoS Pathog. 2008 Apr 25;4(4):e1000052
pubmed: 18437240
J Bacteriol. 2010 Nov;192(21):5663-73
pubmed: 20817770
Trends Mol Med. 2014 Mar;20(3):166-78
pubmed: 24380647
J Immunol. 2016 Jan 1;196(1):336-44
pubmed: 26582948
N Engl J Med. 2008 Apr 3;358(14):1483-94
pubmed: 18385500
Infect Immun. 2015 Sep;83(9):3428-37
pubmed: 26077761
J Allergy Clin Immunol. 2020 Dec;146(6):1442-1445
pubmed: 32320735
Nature. 2010 May 20;465(7296):346-9
pubmed: 20485435
J Invest Dermatol. 2002 May;118(5):845-50
pubmed: 11982763
Clin Orthop Relat Res. 2005 Aug;(437):41-7
pubmed: 16056024
Front Immunol. 2014 Feb 05;5:37
pubmed: 24550921
Genome Res. 2012 May;22(5):850-9
pubmed: 22310478
J Biol Chem. 2004 Feb 13;279(7):5268-77
pubmed: 14630910
Br J Dermatol. 2009 Aug;161(2):300-5
pubmed: 19438853
Sci Transl Med. 2017 Feb 22;9(378):
pubmed: 28228596
Nature. 2013 Nov 21;503(7476):397-401
pubmed: 24172897
mBio. 2015 Aug 25;6(4):
pubmed: 26307164
Clin Exp Allergy. 2014 Dec;44(12):1515-24
pubmed: 25352374
J Dermatol Sci. 1997 Nov;16(1):23-30
pubmed: 9438904
J Invest Dermatol. 2010 Jan;130(1):192-200
pubmed: 19710683
Science. 1999 May 21;284(5418):1318-22
pubmed: 10334980
Clin Microbiol Rev. 2002 Apr;15(2):167-93
pubmed: 11932229
Science. 2008 Feb 15;319(5865):962-5
pubmed: 18276893
Clin Rev Allergy Immunol. 2007 Dec;33(3):167-77
pubmed: 18163223
J Dermatol. 2004 Feb;31(2):78-85
pubmed: 15160859
Curr Allergy Asthma Rep. 2017 Oct 23;17(12):81
pubmed: 29063212
Dermatology. 1993;186(1):23-31
pubmed: 8435513
Clin Exp Allergy. 2019 Jun;49(6):829-837
pubmed: 30830718
Infect Immun. 2001 Mar;69(3):1957-60
pubmed: 11179383