Clumping Factor B Promotes Adherence of Staphylococcus Aureus to Corneocytes in Atopic Dermatitis

Overview

Journal Infect Immun

Publisher American Society for Microbiology

Specialty Allergy & Immunology

Date 2017 Apr 5

PMID 28373353

Citations 51

Authors

Orla M Fleury

Maeve A McAleer

Cecile Feuillie

Cecile Formosa-Dague

Emily Sansevere

Desiree E Bennett

Aisling M Towell

W H Irwin McLean

Sanja Kezic

D Ashley Robinson

Padraic G Fallon

Timothy J Foster

Yves F Dufrene

Alan D Irvine

Joan A Geoghegan

Affiliations

Soon will be listed here.

Abstract

skin infection is a frequent and recurrent problem in children with the common inflammatory skin disease atopic dermatitis (AD). colonizes the skin of the majority of children with AD and exacerbates the disease. The first step during colonization and infection is bacterial adhesion to the cornified envelope of corneocytes in the outer layer, the stratum corneum. Corneocytes from AD skin are structurally different from corneocytes from normal healthy skin. The objective of this study was to identify bacterial proteins that promote the adherence of to AD corneocytes. strains from clonal complexes 1 and 8 were more frequently isolated from infected AD skin than from the nasal cavity of healthy children. AD strains had increased ClfB ligand binding activity compared to normal nasal carriage strains. Adherence of single bacteria to corneocytes from AD patients was studied using atomic force microscopy. Bacteria expressing ClfB recognized ligands distributed over the entire corneocyte surface. The ability of an isogenic ClfB-deficient mutant to adhere to AD corneocytes compared to that of its parent clonal complex 1 clinical strain was greatly reduced. ClfB from clonal complex 1 strains had a slightly higher binding affinity for its ligand than ClfB from strains from other clonal complexes. Our results provide new insights into the first step in the establishment of colonization in AD patients. ClfB is a key adhesion molecule for the interaction of with AD corneocytes and represents a target for intervention.

Citing Articles

Single-cell sequencing of human Langerhans cells identifies altered gene expression profiles in patients with atopic dermatitis.

Tamminga S, Van Der Wal M, Saager E, van der Gang L, Boesjes C, Hendriks A Immunohorizons. 2025; 9(2).

PMID: 39849992 PMC: 11841975. DOI: 10.1093/immhor/vlae009.

Understanding the role of in atopic dermatitis: strain diversity, microevolution, and prophage influences.

Wang Z, Hulpusch C, Traidl-Hoffmann C, Reiger M, Schloter M Front Med (Lausanne). 2024; 11:1480257.

PMID: 39624034 PMC: 11608963. DOI: 10.3389/fmed.2024.1480257.

Investigating genomic diversity of associated with pediatric atopic dermatitis in South Africa.

Ndhlovu G, Javkar K, Matuvhunye T, Ngondoh F, Jamrozy D, Bentley S Front Microbiol. 2024; 15:1422902.

PMID: 39224215 PMC: 11366657. DOI: 10.3389/fmicb.2024.1422902.

Distinct T cell signatures are associated with Staphylococcus aureus skin infection in pediatric atopic dermatitis.

Clowry J, Dempsey D, Claxton T, Towell A, Turley M, Sutton M JCI Insight. 2024; 9(9).

PMID: 38716729 PMC: 11141913. DOI: 10.1172/jci.insight.178789.

Staphylococcus aureus skin colonization is mediated by SasG lectin variation.

Mills K, Maciag J, Wang C, Crawford J, Enroth T, Keim K Cell Rep. 2024; 43(4):114022.

PMID: 38568806 PMC: 11866565. DOI: 10.1016/j.celrep.2024.114022.

References

OBrien L, Walsh E, Massey R, Peacock S, Foster T . Staphylococcus aureus clumping factor B (ClfB) promotes adherence to human type I cytokeratin 10: implications for nasal colonization. Cell Microbiol. 2002; 4(11):759-70. DOI: 10.1046/j.1462-5822.2002.00231.x. View

Sandilands A, Smith F, Irvine A, McLean W . Filaggrin's fuller figure: a glimpse into the genetic architecture of atopic dermatitis. J Invest Dermatol. 2007; 127(6):1282-4. DOI: 10.1038/sj.jid.5700876. View

Ganesh V, Liang X, Geoghegan J, Cohen A, Venugopalan N, Foster T . Lessons from the Crystal Structure of the S. aureus Surface Protein Clumping Factor A in Complex With Tefibazumab, an Inhibiting Monoclonal Antibody. EBioMedicine. 2016; 13:328-338. PMC: 5264652. DOI: 10.1016/j.ebiom.2016.09.027. View

Beaussart A, El-Kirat-Chatel S, Herman P, Alsteens D, Mahillon J, Hols P . Single-cell force spectroscopy of probiotic bacteria. Biophys J. 2013; 104(9):1886-92. PMC: 3647156. DOI: 10.1016/j.bpj.2013.03.046. View

Zollner T, Wichelhaus T, Hartung A, von Mallinckrodt C, Wagner T, Brade V . Colonization with superantigen-producing Staphylococcus aureus is associated with increased severity of atopic dermatitis. Clin Exp Allergy. 2000; 30(7):994-1000. DOI: 10.1046/j.1365-2222.2000.00848.x. View

Yeung M, Balma-Mena A, Shear N, Simor A, Pope E, Walsh S . Identification of major clonal complexes and toxin producing strains among Staphylococcus aureus associated with atopic dermatitis. Microbes Infect. 2010; 13(2):189-97. DOI: 10.1016/j.micinf.2010.10.023. View

Ponnuraj K, Bowden M, Davis S, Gurusiddappa S, Moore D, Choe D . A "dock, lock, and latch" structural model for a staphylococcal adhesin binding to fibrinogen. Cell. 2003; 115(2):217-28. DOI: 10.1016/s0092-8674(03)00809-2. View

Horsburgh M, Aish J, White I, Shaw L, Lithgow J, Foster S . sigmaB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J Bacteriol. 2002; 184(19):5457-67. PMC: 135357. DOI: 10.1128/JB.184.19.5457-5467.2002. View

Lofblom J, Kronqvist N, Uhlen M, Stahl S, Wernerus H . Optimization of electroporation-mediated transformation: Staphylococcus carnosus as model organism. J Appl Microbiol. 2007; 102(3):736-47. DOI: 10.1111/j.1365-2672.2006.03127.x. View

10.

Rojo A, Aguinaga A, Monecke S, Yuste J, Gastaminza G, Espana A . Staphylococcus aureus genomic pattern and atopic dermatitis: may factors other than superantigens be involved?. Eur J Clin Microbiol Infect Dis. 2013; 33(4):651-8. DOI: 10.1007/s10096-013-2000-z. View

11.

Lower S, Lamlertthon S, Casillas-Ituarte N, Lins R, Yongsunthon R, Taylor E . Polymorphisms in fibronectin binding protein A of Staphylococcus aureus are associated with infection of cardiovascular devices. Proc Natl Acad Sci U S A. 2011; 108(45):18372-7. PMC: 3215016. DOI: 10.1073/pnas.1109071108. View

12.

Mulcahy M, Geoghegan J, Monk I, OKeeffe K, Walsh E, Foster T . Nasal colonisation by Staphylococcus aureus depends upon clumping factor B binding to the squamous epithelial cell envelope protein loricrin. PLoS Pathog. 2013; 8(12):e1003092. PMC: 3531522. DOI: 10.1371/journal.ppat.1003092. View

13.

Kobayashi T, Glatz M, Horiuchi K, Kawasaki H, Akiyama H, Kaplan D . Dysbiosis and Staphylococcus aureus Colonization Drives Inflammation in Atopic Dermatitis. Immunity. 2015; 42(4):756-66. PMC: 4407815. DOI: 10.1016/j.immuni.2015.03.014. View

14.

van Belkum A, Verkaik N, de Vogel C, Boelens H, Verveer J, Nouwen J . Reclassification of Staphylococcus aureus nasal carriage types. J Infect Dis. 2009; 199(12):1820-6. DOI: 10.1086/599119. View

15.

Harris S, Cartwright E, Torok M, Holden M, Brown N, Ogilvy-Stuart A . Whole-genome sequencing for analysis of an outbreak of meticillin-resistant Staphylococcus aureus: a descriptive study. Lancet Infect Dis. 2012; 13(2):130-6. PMC: 3556525. DOI: 10.1016/S1473-3099(12)70268-2. View

16.

Kennedy E, Connolly J, OB Hourihane J, Fallon P, McLean W, Murray D . Skin microbiome before development of atopic dermatitis: Early colonization with commensal staphylococci at 2 months is associated with a lower risk of atopic dermatitis at 1 year. J Allergy Clin Immunol. 2016; 139(1):166-172. PMC: 5207796. DOI: 10.1016/j.jaci.2016.07.029. View

17.

Kezic S, ORegan G, Yau N, Sandilands A, Chen H, Campbell L . Levels of filaggrin degradation products are influenced by both filaggrin genotype and atopic dermatitis severity. Allergy. 2011; 66(7):934-40. PMC: 3586662. DOI: 10.1111/j.1398-9995.2010.02540.x. View

18.

Formosa-Dague C, Speziale P, Foster T, Geoghegan J, Dufrene Y . Zinc-dependent mechanical properties of Staphylococcus aureus biofilm-forming surface protein SasG. Proc Natl Acad Sci U S A. 2015; 113(2):410-5. PMC: 4720321. DOI: 10.1073/pnas.1519265113. View

19.

Tauber M, Balica S, Hsu C, Jean-Decoster C, Lauze C, Redoules D . Staphylococcus aureus density on lesional and nonlesional skin is strongly associated with disease severity in atopic dermatitis. J Allergy Clin Immunol. 2015; 137(4):1272-1274.e3. DOI: 10.1016/j.jaci.2015.07.052. View

20.

Formosa-Dague C, Fu Z, Feuillie C, Derclaye S, Foster T, Geoghegan J . Forces between Staphylococcus aureus and human skin. Nanoscale Horiz. 2020; 1(4):298-303. DOI: 10.1039/c6nh00057f. View