Origins of glycan selectivity in streptococcal Siglec-like adhesins suggest mechanisms of receptor adaptation.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
18 05 2022
Historique:
received: 10 04 2021
accepted: 26 04 2022
entrez: 18 5 2022
pubmed: 19 5 2022
medline: 21 5 2022
Statut: epublish

Résumé

Bacterial binding to host receptors underlies both commensalism and pathogenesis. Many streptococci adhere to protein-attached carbohydrates expressed on cell surfaces using Siglec-like binding regions (SLBRs). The precise glycan repertoire recognized may dictate whether the organism is a strict commensal versus a pathogen. However, it is currently not clear what drives receptor selectivity. Here, we use five representative SLBRs and identify regions of the receptor binding site that are hypervariable in sequence and structure. We show that these regions control the identity of the preferred carbohydrate ligand using chimeragenesis and single amino acid substitutions. We further evaluate how the identity of the preferred ligand affects the interaction with glycoprotein receptors in human saliva and plasma samples. As point mutations can change the preferred human receptor, these studies suggest how streptococci may adapt to changes in the environmental glycan repertoire.

Identifiants

pubmed: 35585145
doi: 10.1038/s41467-022-30509-y
pii: 10.1038/s41467-022-30509-y
pmc: PMC9117288
doi:

Substances chimiques

Adhesins, Bacterial 0
Ligands 0
Polysaccharides 0
Sialic Acid Binding Immunoglobulin-like Lectins 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

2753

Subventions

Organisme : NIAID NIH HHS
ID : R01 AI106987
Pays : United States
Organisme : NIGMS NIH HHS
ID : P41 GM103393
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI130684
Pays : United States
Organisme : NIGMS NIH HHS
ID : P41 GM103694
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM137458
Pays : United States
Organisme : NIGMS NIH HHS
ID : R24 GM098791
Pays : United States
Organisme : NIDCR NIH HHS
ID : R03 DE029516
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA221244
Pays : United States

Informations de copyright

© 2022. The Author(s).

Références

Glycobiology. 2017 Aug 1;27(8):743-754
pubmed: 28549117
J Biol Chem. 2016 Apr 1;291(14):7230-40
pubmed: 26833566
Mol Cell. 1998 Apr;1(5):719-28
pubmed: 9660955
J Biochem. 2011 Nov;150(5):545-52
pubmed: 21813503
Syst Biol. 2012 May;61(3):539-42
pubmed: 22357727
Biochem J. 2013 Jul 15;453(2):261-70
pubmed: 23611418
J Appl Crystallogr. 2007 Aug 1;40(Pt 4):658-674
pubmed: 19461840
Glycobiology. 2018 Aug 1;28(8):601-611
pubmed: 29796594
J Comput Chem. 2005 Dec;26(16):1668-88
pubmed: 16200636
Cell Rep. 2015 Jun 30;11(12):1966-78
pubmed: 26095364
Nat Commun. 2021 Jul 1;12(1):4070
pubmed: 34210959
Proc Natl Acad Sci U S A. 2016 Jul 19;113(29):E4170-9
pubmed: 27357658
Protein Cell. 2013 Aug;4(8):569-72
pubmed: 23842991
J Biol Chem. 2003 Jan 31;278(5):3372-7
pubmed: 12438315
J Chem Theory Comput. 2015 Aug 11;11(8):3696-713
pubmed: 26574453
J Biol Chem. 2012 Jun 8;287(24):20313-20
pubmed: 22493425
PLoS Pathog. 2021 Jan 19;17(1):e1009222
pubmed: 33465168
RSC Chem Biol. 2021 Oct 18;2(6):1618-1630
pubmed: 34977577
Infect Immun. 2004 Nov;72(11):6528-37
pubmed: 15501784
J Biol Chem. 2020 Oct 23;295(43):14737-14749
pubmed: 32820052
Mol Oral Microbiol. 2016 Apr;31(2):175-88
pubmed: 26172471
J Biochem. 2007 Mar;141(3):389-99
pubmed: 17234683
Microb Pathog. 2008 Oct;45(4):297-301
pubmed: 18656529
Bioinformatics. 2005 May 1;21(9):2104-5
pubmed: 15647292
J Biochem. 2015 Apr;157(4):197-200
pubmed: 25762728
Glycobiology. 2014 Dec;24(12):1312-22
pubmed: 25049238
Infect Immun. 2006 Jan;74(1):740-3
pubmed: 16369032
Infect Immun. 2006 Mar;74(3):1933-40
pubmed: 16495569
Biochemistry. 1998 Apr 7;37(14):4916-27
pubmed: 9538010
J Chem Theory Comput. 2013 Jul 9;9(7):3084-95
pubmed: 26583988
Bioinformatics. 2012 Jun 15;28(12):1647-9
pubmed: 22543367
Mol Oral Microbiol. 2012 Aug;27(4):257-69
pubmed: 22759311
PLoS Pathog. 2019 Jun 24;15(6):e1007896
pubmed: 31233555
Annu Rev Pathol. 2011;6:365-93
pubmed: 21073341
J Biol Chem. 2010 Nov 5;285(45):35079-91
pubmed: 20807768
Cell. 2006 Sep 8;126(5):841-5
pubmed: 16959563
Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32
pubmed: 15572765
PLoS One. 2015 Dec 29;10(12):e0145834
pubmed: 26714191
Annu Rev Microbiol. 2000;54:413-37
pubmed: 11018133
Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21
pubmed: 20124702
PLoS Pathog. 2017 Nov 14;13(11):e1006707
pubmed: 29136651
Glycobiology. 2016 Nov;26(11):1222-1234
pubmed: 27037304
F1000 Biol Rep. 2011;3:19
pubmed: 21941598
J Biol Chem. 1996 Apr 19;271(16):9267-72
pubmed: 8621587
Biochem J. 2020 Oct 16;477(19):3695-3707
pubmed: 32910185
Infect Immun. 2019 Sep 19;87(10):
pubmed: 31308084
Proc Natl Acad Sci U S A. 1998 Sep 29;95(20):11751-6
pubmed: 9751737
Mol Microbiol. 2005 Oct;58(2):380-92
pubmed: 16194227
PLoS Pathog. 2014 Dec 04;10(12):e1004540
pubmed: 25474103
Biochemistry. 2016 Oct 25;55(42):5927-5937
pubmed: 27685666
PLoS One. 2016 Apr 21;11(4):e0154098
pubmed: 27101147
PLoS Pathog. 2011 Jul;7(7):e1002112
pubmed: 21765814
mBio. 2020 Jul 28;11(4):
pubmed: 32723915
Br J Haematol. 2005 Apr;129(1):101-9
pubmed: 15801962
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
pubmed: 15034147
J Biol Chem. 2008 Sep 26;283(39):26297-301
pubmed: 18544537
Glycobiology. 2009 Mar;19(3):288-300
pubmed: 19043084
Glycobiology. 2017 Jan;27(1):3-49
pubmed: 27558841
Curr Probl Cardiol. 2006 Apr;31(4):274-352
pubmed: 16546554

Auteurs

Barbara A Bensing (BA)

Division of Infectious Diseases, Veterans Affairs Medical Center, Department of Medicine, University of California, San Francisco, CA, USA.
the Northern California Institute for Research and Education, San Francisco, CA, 94121, USA.

Haley E Stubbs (HE)

Graduate Program in Chemical and Physical Biology, Vanderbilt University, Nashville, TN, 37232, USA.

Rupesh Agarwal (R)

University of Tennessee/Oak Ridge National Laboratory, Center for Molecular Biophysics, Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831-6309, USA.
Department of Biochemistry and Cellular and Molecular Biology, University of Tennessee, Knoxville, TN, 37996, USA.

Izumi Yamakawa (I)

Department of Pharmacology, Vanderbilt University, Nashville, TN, 37232, USA.
School of Nursing, Belmont University, Nashville, TN, 37212, USA.

Kelvin Luong (K)

Department of Pharmacology, Vanderbilt University, Nashville, TN, 37232, USA.

Kemal Solakyildirim (K)

Department of Chemistry, Erzincan Binali Yildirim University, Erzincan, 24100, Turkey.
Department of Chemistry, University of California, Davis, CA, 95616, USA.

Hai Yu (H)

Department of Chemistry, University of California, Davis, CA, 95616, USA.

Azadeh Hadadianpour (A)

Department of Microbiology, Pathology, and Immunology, Vanderbilt University, Nashville, TN, 37232, USA.

Manuel A Castro (MA)

Department of Biochemistry, Vanderbilt University, Nashville, TN, 37232, USA.

Kevin P Fialkowski (KP)

Department of Pharmacology, Vanderbilt University, Nashville, TN, 37232, USA.
College of Medicine, University of Arkansas for Medical Sciences, Little Rock, AR, 72205, USA.

KeAndreya M Morrison (KM)

Department of Pharmacology, School of Graduate Studies and Research, Meharry Medical College, Nashville, TN, 37208, USA.

Zdzislaw Wawrzak (Z)

LS-CAT Synchrotron Research Center, Northwestern University, Argonne, IL, 60439, USA.

Xi Chen (X)

Department of Chemistry, University of California, Davis, CA, 95616, USA.

Carlito B Lebrilla (CB)

Department of Chemistry, University of California, Davis, CA, 95616, USA.

Jerome Baudry (J)

Department of Biological Sciences, The University of Alabama in Huntsville, Huntsville, AL, 35899, USA.

Jeremy C Smith (JC)

University of Tennessee/Oak Ridge National Laboratory, Center for Molecular Biophysics, Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831-6309, USA.
Department of Biochemistry and Cellular and Molecular Biology, University of Tennessee, Knoxville, TN, 37996, USA.

Paul M Sullam (PM)

Division of Infectious Diseases, Veterans Affairs Medical Center, Department of Medicine, University of California, San Francisco, CA, USA.
the Northern California Institute for Research and Education, San Francisco, CA, 94121, USA.

T M Iverson (TM)

Department of Pharmacology, Vanderbilt University, Nashville, TN, 37232, USA. tina.iverson@vanderbilt.edu.
Department of Biochemistry, Vanderbilt University, Nashville, TN, 37232, USA. tina.iverson@vanderbilt.edu.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH