S100A8/A9 drives the formation of procoagulant platelets through GPIbα.


Journal

Blood
ISSN: 1528-0020
Titre abrégé: Blood
Pays: United States
ID NLM: 7603509

Informations de publication

Date de publication:
15 12 2022
Historique:
accepted: 09 08 2022
received: 29 11 2021
pubmed: 27 8 2022
medline: 20 12 2022
entrez: 26 8 2022
Statut: ppublish

Résumé

S100A8/A9, also known as "calprotectin" or "MRP8/14," is an alarmin primarily secreted by activated myeloid cells with antimicrobial, proinflammatory, and prothrombotic properties. Increased plasma levels of S100A8/A9 in thrombo-inflammatory diseases are associated with thrombotic complications. We assessed the presence of S100A8/A9 in the plasma and lung autopsies from patients with COVID-19 and investigated the molecular mechanism by which S100A8/A9 affects platelet function and thrombosis. S100A8/A9 plasma levels were increased in patients with COVID-19 and sustained high levels during hospitalization correlated with poor outcomes. Heterodimeric S100A8/A9 was mainly detected in neutrophils and deposited on the vessel wall in COVID-19 lung autopsies. Immobilization of S100A8/A9 with collagen accelerated the formation of a fibrin-rich network after perfusion of recalcified blood at venous shear. In vitro, platelets adhered and partially spread on S100A8/A9, leading to the formation of distinct populations of either P-selectin or phosphatidylserine (PS)-positive platelets. By using washed platelets, soluble S100A8/A9 induced PS exposure but failed to induce platelet aggregation, despite GPIIb/IIIa activation and alpha-granule secretion. We identified GPIbα as the receptor for S100A8/A9 on platelets inducing the formation of procoagulant platelets with a supporting role for CD36. The effect of S100A8/A9 on platelets was abolished by recombinant GPIbα ectodomain, platelets from a patient with Bernard-Soulier syndrome with GPIb-IX-V deficiency, and platelets from mice deficient in the extracellular domain of GPIbα. We identified the S100A8/A9-GPIbα axis as a novel targetable prothrombotic pathway inducing procoagulant platelets and fibrin formation, in particular in diseases associated with high levels of S100A8/A9, such as COVID-19.

Identifiants

pubmed: 36026606
pii: S0006-4971(22)01113-2
doi: 10.1182/blood.2021014966
pmc: PMC10653093
doi:

Substances chimiques

Calgranulin A 0
Fibrin 9001-31-4
Phosphatidylserines 0
S100A9 protein, human 0
Calgranulin B 0
adhesion receptor 0
Platelet Glycoprotein GPIb-IX Complex 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2626-2643

Subventions

Organisme : British Heart Foundation
ID : PG/21/10737
Pays : United Kingdom
Organisme : British Heart Foundation
ID : AA/18/2/34218
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 204951
Pays : United Kingdom
Organisme : British Heart Foundation
ID : FS/IBSRF/20/25039
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : British Heart Foundation
ID : CH03/003
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_PC_19029
Pays : United Kingdom
Organisme : British Heart Foundation
ID : CH/03/003/15571
Pays : United Kingdom

Informations de copyright

© 2022 by The American Society of Hematology.

Références

Front Cell Infect Microbiol. 2021 Oct 21;11:751232
pubmed: 34746027
Transl Res. 2011 Jul;158(1):71-5
pubmed: 21708357
J Leukoc Biol. 1993 Feb;53(2):197-204
pubmed: 8445331
Biochem Biophys Rep. 2016 Mar 19;6:94-100
pubmed: 28955868
Blood. 2011 Jun 9;117(23):6355-66
pubmed: 21478428
Blood. 2000 Feb 1;95(3):903-10
pubmed: 10648402
J Biol Chem. 1991 Apr 25;266(12):7706-13
pubmed: 2019594
Thromb J. 2005 Oct 11;3:15
pubmed: 16219103
FASEB J. 2020 Jul;34(7):9337-9357
pubmed: 32463151
Dev Cell. 2013 Feb 25;24(4):372-83
pubmed: 23395392
Blood Adv. 2022 Jun 28;6(12):3593-3605
pubmed: 35443030
J Cereb Blood Flow Metab. 2013 Feb;33(2):287-92
pubmed: 23149559
Blood. 2009 Nov 26;114(23):4883-5
pubmed: 19726719
Platelets. 2013;24(1):63-70
pubmed: 22372532
J Biol Chem. 2002 Feb 1;277(5):3658-65
pubmed: 11723110
Atherosclerosis. 2020 Aug;307:109-120
pubmed: 32439204
J Gerontol A Biol Sci Med Sci. 2015 Feb;70(2):225-31
pubmed: 24917177
Cells. 2022 Jan 11;11(2):
pubmed: 35053354
Sci Rep. 2019 Oct 30;9(1):15660
pubmed: 31666644
Blood. 2021 Feb 25;137(8):1061-1071
pubmed: 33512415
Curr Opin Hematol. 2020 Jan;27(1):34-40
pubmed: 31688457
Blood. 2017 May 25;129(21):2917-2927
pubmed: 28336528
Blood. 2017 Nov 16;130(20):2171-2179
pubmed: 28972013
J Thromb Haemost. 2021 Dec;19(12):3062-3072
pubmed: 34538029
Cerebrovasc Dis. 2009;28(3):276-82
pubmed: 19609079
Cell Mol Immunol. 2020 Sep;17(9):992-994
pubmed: 32620787
Proc Natl Acad Sci U S A. 2019 Aug 27;116(35):17444-17449
pubmed: 31405966
Arterioscler Thromb Vasc Biol. 2012 Oct;32(10):2475-83
pubmed: 22837472
Front Cardiovasc Med. 2022 Jan 24;8:802566
pubmed: 35141292
Shock. 2002 Apr;17(4):263-8
pubmed: 11954824
Biochemistry. 2001 Jan 9;40(1):241-8
pubmed: 11141076
Front Cardiovasc Med. 2021 Dec 10;8:795624
pubmed: 34957266
Blood Transfus. 2011 May;9 Suppl 2:s3-8
pubmed: 21839029
ESC Heart Fail. 2020 Aug;7(4):1442-1451
pubmed: 32462801
JCI Insight. 2017 Jun 2;2(11):
pubmed: 28570273
Arterioscler Thromb Vasc Biol. 2017 Sep;37(9):1596-1597
pubmed: 28835486
J Investig Med. 2020 Apr;68(4):813-820
pubmed: 31843956
Mediators Inflamm. 2013;2013:828354
pubmed: 24453429
Clin Chem Lab Med. 2019 Apr 24;57(5):707-715
pubmed: 30471216
Nat Commun. 2017 May 30;8:15559
pubmed: 28555620
Eur J Clin Invest. 1995 Nov;25(11):843-51
pubmed: 8582450
Cell Host Microbe. 2021 Feb 10;29(2):222-235.e4
pubmed: 33388094
JACC Basic Transl Sci. 2021 Mar;6(3):202-218
pubmed: 33649738
Geroscience. 2021 Aug;43(4):2055-2065
pubmed: 34109507
Blood. 2010 Apr 8;115(14):2947-55
pubmed: 20154219
Res Pract Thromb Haemost. 2020 Dec 20;5(1):27-37
pubmed: 33537527
Mol Med Rep. 2020 Dec;22(6):5293-5303
pubmed: 33174028
J Thromb Thrombolysis. 2021 Feb;51(2):446-453
pubmed: 33151461
Blood. 2020 Sep 10;136(11):1330-1341
pubmed: 32678428
Thromb Res. 2018 Oct;170:87-96
pubmed: 30138777
Pathobiology. 2021;88(1):15-27
pubmed: 33049751
Expert Rev Clin Immunol. 2021 May;17(5):431-443
pubmed: 33750254
Heart. 2015 Jul;101(14):1126-32
pubmed: 25999588
Eur J Immunol. 1989 Jun;19(6):1053-61
pubmed: 2666142
Arterioscler Thromb Vasc Biol. 2012 Dec;32(12):2946-55
pubmed: 23087357
J Thromb Haemost. 2013 Jun;11 Suppl 1:330-9
pubmed: 23809136
Haematologica. 2018 Dec;103(12):2097-2108
pubmed: 30026342
Arthritis Res Ther. 2016 Oct 24;18(1):247
pubmed: 27776554
Eur Heart J. 2019 Aug 21;40(32):2724-2726
pubmed: 31334753
Front Immunol. 2018 Mar 13;9:447
pubmed: 29593718
Nat Commun. 2019 Apr 16;10(1):1780
pubmed: 30992428
Blood. 2010 Nov 18;116(20):4317-27
pubmed: 20705757
Thromb Haemost. 2015 Nov;114(5):994-1003
pubmed: 26202300
Cytokine Growth Factor Rev. 2022 Feb;63:90-97
pubmed: 34728150
J Clin Invest. 2014 May;124(5):2160-71
pubmed: 24691441
Arterioscler Thromb Vasc Biol. 2022 Jan;42(1):49-62
pubmed: 34809447
Cell. 2020 Sep 17;182(6):1401-1418.e18
pubmed: 32810439
Thromb Res. 2014 Mar;133(3):308-14
pubmed: 24296115
Sci Adv. 2021 Sep 10;7(37):eabh2434
pubmed: 34516880
Front Immunol. 2019 Dec 17;10:2884
pubmed: 31921147
PLoS One. 2017 Dec 8;12(12):e0188921
pubmed: 29220362
Cardiovasc Res. 2022 Dec 9;118(15):3085-3096
pubmed: 35709328
PLoS One. 2015 Feb 23;10(2):e0115828
pubmed: 25706559
Front Immunol. 2018 Jun 11;9:1298
pubmed: 29942307
J Thromb Haemost. 2015 Jun;13 Suppl 1:S82-91
pubmed: 26149054
Biochemistry. 1996 Apr 16;35(15):4929-38
pubmed: 8664285
Ann Intensive Care. 2021 Jul 17;11(1):113
pubmed: 34273008
Circ Cardiovasc Genet. 2014 Oct;7(5):615-24
pubmed: 25049041
Blood. 2013 Mar 7;121(10):1850-7
pubmed: 23303820
Front Immunol. 2019 Jul 17;10:1687
pubmed: 31379873
Lab Med. 2019 Oct 10;50(4):370-380
pubmed: 30994906
Am J Med Sci. 2016 Sep;352(3):261-6
pubmed: 27650230

Auteurs

Martina Colicchia (M)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.

Waltraud C Schrottmaier (WC)

Center for Physiology and Pharmacology, Medical University of Vienna, Vienna, Austria.

Gina Perrella (G)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.
Department of Biochemistry, CARIM, Maastricht University, Maastricht, The Netherlands.

Jasmeet S Reyat (JS)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.

Jenefa Begum (J)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.

Alexandre Slater (A)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.

Joshua Price (J)

Institute of Inflammation and Ageing, University of Birmingham, Birmingham, United Kingdom.

Joanne C Clark (JC)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.

Zhaogong Zhi (Z)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.

Megan J Simpson (MJ)

Aberdeen Cardiovascular & Diabetes Centre, Institute of Medical Sciences, School of Medicine, Medical Sciences and Nutrition, University of Aberdeen, Aberdeen, United Kingdom.

Joshua H Bourne (JH)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.

Natalie S Poulter (NS)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.
Centre of Membrane Proteins and Receptors (COMPARE), Universities of Birmingham and Nottingham, The Midlands, United Kingdom.

Abdullah O Khan (AO)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.

Phillip L R Nicolson (PLR)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.
Department of Haematology, Queen Elizabeth Hospital, Birmingham, United Kingdom.

Matthew Pugh (M)

Institute of Immunology and Immunotherapy, University of Birmingham, Birmingham, United Kingdom.

Paul Harrison (P)

Institute of Inflammation and Ageing, University of Birmingham, Birmingham, United Kingdom.

Asif J Iqbal (AJ)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.

George E Rainger (GE)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.

Steve P Watson (SP)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.
Centre of Membrane Proteins and Receptors (COMPARE), Universities of Birmingham and Nottingham, The Midlands, United Kingdom.

Mark R Thomas (MR)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.

Nicola J Mutch (NJ)

Aberdeen Cardiovascular & Diabetes Centre, Institute of Medical Sciences, School of Medicine, Medical Sciences and Nutrition, University of Aberdeen, Aberdeen, United Kingdom.

Alice Assinger (A)

Center for Physiology and Pharmacology, Medical University of Vienna, Vienna, Austria.

Julie Rayes (J)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.
Centre of Membrane Proteins and Receptors (COMPARE), Universities of Birmingham and Nottingham, The Midlands, United Kingdom.

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