Kupffer cell receptor CLEC4F is important for the destruction of desialylated platelets in mice.

Animals Asialoglycoprotein Receptor / metabolism Blood Platelets / metabolism Disease Models, Animal Lectins, C-Type / metabolism Mice Receptors, Immunologic / metabolism

Journal

Cell death and differentiation
ISSN: 1476-5403
Titre abrégé: Cell Death Differ
Pays: England
ID NLM: 9437445

Informations de publication

Date de publication:
11 2021
Historique:
received: 30 09 2020
accepted: 26 04 2021
revised: 21 04 2021
pubmed: 17 5 2021
medline: 24 3 2022
entrez: 16 5 2021
Statut: ppublish

Résumé

The liver has recently been identified as a major organ for destruction of desialylated platelets. However, the underlying mechanism remains unclear. Kupffer cells, which are professional phagocytic cells in the liver, comprise the largest population of resident tissue macrophages in the body. Kupffer cells express a C-type lectin receptor, CLEC4F, that recognizes desialylated glycans with an unclear in vivo role in mediating platelet destruction. In this study, we generated a CLEC4F-deficient mouse model (Clec4f

Identifiants

DOI: 10.1038/s41418-021-00797-w PMID: 33993195 PMC: PMC8564511
pubmed: 33993195
doi: 10.1038/s41418-021-00797-w
pii: 10.1038/s41418-021-00797-w
pmc: PMC8564511
doi:

Substances chimiques

Asialoglycoprotein Receptor 0
CLEC4F protein, mouse 0
Kupffer cell receptor 0
Lectins, C-Type 0
Receptors, Immunologic 0

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

3009-3021

Subventions

Organisme : NHLBI NIH HHS
ID : P01 HL131474
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI151371
Pays : United States
Organisme : Oklahoma Medical Research Foundation (OMRF)
ID : 9000

Informations de copyright

© 2021. The Author(s).

Références

Morrell CN, Aggrey AA, Chapman LM, Modjeski KL. Emerging roles for platelets as immune and inflammatory cells. Blood 2014;123:2759–67.
doi: 10.1182/blood-2013-11-462432
Grewal PK. The Ashwell-Morell receptor. Methods Enzymol. 2010;479:223–41.
doi: 10.1016/S0076-6879(10)79013-3
Grewal PK, Aziz PV, Uchiyama S, Rubio GR, Lardone RD, Le D, et al. Inducing host protection in pneumococcal sepsis by preactivation of the Ashwell-Morell receptor. Proc Natl Acad Sci USA. 2013;110:20218–23.
doi: 10.1073/pnas.1313905110
Grewal PK, Uchiyama S, Ditto D, Varki N, Le DT, Nizet V, et al. The Ashwell receptor mitigates the lethal coagulopathy of sepsis. Nat Med. 2008;14:648–55.
doi: 10.1038/nm1760
Herzog BH, Fu J, Wilson SJ, Hess PR, Sen A, McDaniel JM, et al. Podoplanin maintains high endothelial venule integrity by interacting with platelet CLEC-2. Nature. 2013;502:105–9.
doi: 10.1038/nature12501
Boulaftali Y, Hess PR, Getz TM, Cholka A, Stolla M, Mackman N, et al. Platelet ITAM signaling is critical for vascular integrity in inflammation. J Clin Invest. 2013;123:908–16.
Rumjantseva V, Grewal PK, Wandall HH, Josefsson EC, Sorensen AL, Larson G, et al. Dual roles for hepatic lectin receptors in the clearance of chilled platelets. Nat Med. 2009;15:1273–80.
doi: 10.1038/nm.2030
Li J, van der Wal DE, Zhu G, Xu M, Yougbare I, Ma L, et al. Desialylation is a mechanism of Fc-independent platelet clearance and a therapeutic target in immune thrombocytopenia. Nat Commun. 2015;6:7737.
doi: 10.1038/ncomms8737
Li Y, Fu J, Ling Y, Yago T, McDaniel JM, Song J, et al. Sialylation on O-glycans protects platelets from clearance by liver Kupffer cells. Proc Natl Acad Sci USA. 2017;114:8360–5.
doi: 10.1073/pnas.1707662114
Xiang B, Zhang G, Guo L, Li XA, Morris AJ, Daugherty A, et al. Platelets protect from septic shock by inhibiting macrophage-dependent inflammation via the cyclooxygenase 1 signalling pathway. Nat Commun. 2013;4:2657.
doi: 10.1038/ncomms3657
Li R, Hoffmeister KM, Falet H. Glycans and the platelet life cycle. Platelets. 2016;27:505–11.
doi: 10.3109/09537104.2016.1171304
McArthur K, Chappaz S, Kile BT. Apoptosis in megakaryocytes and platelets: the life and death of a lineage. Blood. 2018;131:605–10.
doi: 10.1182/blood-2017-11-742684
Marini I, Zlamal J, Faul C, Holzer U, Hammer S, Pelzl L, et al. Autoantibody-mediated desialylation impairs human thrombopoiesis and platelet life span. Haematologica. 2021;106:196–207.
Monti E, Bonten E, D’Azzo A, Bresciani R, Venerando B, Borsani G, et al. Sialidases in vertebrates: a family of enzymes tailored for several cell functions. Adv Carbohydr Chem Biochem. 2010;64:403–79.
doi: 10.1016/S0065-2318(10)64007-3
Grozovsky R, Giannini S, Falet H, Hoffmeister KM. Novel mechanisms of platelet clearance and thrombopoietin regulation. Curr Opin Hematol. 2015;22:445–51.
doi: 10.1097/MOH.0000000000000170
Sorensen AL, Rumjantseva V, Nayeb-Hashemi S, Clausen H, Hartwig JH, Wandall HH, et al. Role of sialic acid for platelet life span: exposure of beta-galactose results in the rapid clearance of platelets from the circulation by asialoglycoprotein receptor-expressing liver macrophages and hepatocytes. Blood. 2009;114:1645–54.
doi: 10.1182/blood-2009-01-199414
Guillot A, Tacke F. Liver macrophages: old dogmas and new insights. Hepatol Commun. 2019;3:730–43.
doi: 10.1002/hep4.1356
Epelman S, Lavine KJ, Randolph GJ. Origin and functions of tissue macrophages. Immunity. 2014;41:21–35.
doi: 10.1016/j.immuni.2014.06.013
Fadden AJ, Holt OJ, Drickamer K. Molecular characterization of the rat Kupffer cell glycoprotein receptor. Glycobiology 2003;13:529–37.
doi: 10.1093/glycob/cwg068
Yang CY, Chen JB, Tsai TF, Tsai YC, Tsai CY, Liang PH, et al. CLEC4F is an inducible C-type lectin in F4/80-positive cells and is involved in alpha-galactosylceramide presentation in liver. PLoS ONE. 2013;8:e65070.
doi: 10.1371/journal.pone.0065070
Haltiwanger RS, Lehrman MA, Eckhardt AE, Hill RL. The distribution and localization of the fucose-binding lectin in rat tissues and the identification of a high affinity form of the mannose/N-acetylglucosamine-binding lectin in rat liver. J Biol Chem. 1986;261:7433–9.
doi: 10.1016/S0021-9258(17)38410-7
Hoyle GW, Hill RL. Molecular cloning and sequencing of a cDNA for a carbohydrate binding receptor unique to rat Kupffer cells. J Biol Chem. 1988;263:7487–92.
doi: 10.1016/S0021-9258(18)68524-2
Taylor ME, Snelling T, Smith DF, Drickamer K. Absence of a human ortholog of rodent Kupffer cell galactose-binding receptor encoded by the CLEC4f gene. Glycobiology. 2019;29:332–45.
doi: 10.1093/glycob/cwy113
Grozovsky R, Begonja AJ, Liu K, Visner G, Hartwig JH, Falet H, et al. The Ashwell-Morell receptor regulates hepatic thrombopoietin production via JAK2-STAT3 signaling. Nat Med. 2015;21:47–54.
doi: 10.1038/nm.3770
Deppermann C, Kratofil RM, Peiseler M, David BA, Zindel J, Castanheira F, et al. Macrophage galactose lectin is critical for Kupffer cells to clear aged platelets. J Exp Med. 2020;217:e20190723.
Wong CH, Jenne CN, Petri B, Chrobok NL, Kubes P. Nucleation of platelets with blood-borne pathogens on Kupffer cells precedes other innate immunity and contributes to bacterial clearance. Nat Immunol. 2013;14:785–92.
doi: 10.1038/ni.2631
Huo Y, Schober A, Forlow SB, Smith DF, Hyman MC, Jung S, et al. Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat Med. 2003;9:61–7.
doi: 10.1038/nm810
Xia L, Ramachandran V, McDaniel JM, Nguyen KN, Cummings RD, McEver RP. N-terminal residues in murine P-selectin glycoprotein ligand-1 required for binding to murine P-selectin. Blood. 2003;101:552–9.
doi: 10.1182/blood-2001-11-0036
Hoffmeister KM, Falet H. Platelet clearance by the hepatic Ashwell-Morrell receptor: mechanisms and biological significance. Thromb Res. 2016;141:S68–72. Suppl 2
doi: 10.1016/S0049-3848(16)30370-X
Ward SE, O’Sullivan JM, Drakeford C, Aguila S, Jondle CN, Sharma J, et al. A novel role for the macrophage galactose-type lectin receptor in mediating von Willebrand factor clearance. Blood. 2018;131:911–6.
doi: 10.1182/blood-2017-06-787853
McEver RP, Moore KL, Cummings RD. Leukocyte trafficking mediated by selectin-carbohydrate interactions. J Biol Chem. 1995;270:11025–8.
doi: 10.1074/jbc.270.19.11025
Ma X, Li Y, Kondo Y, Shi H, Han J, Jiang Y, et al. Slc35a1 deficiency causes thrombocytopenia due to impaired megakaryocytopoiesis and excessive platelet clearance in the liver. Haematologica. 2021;106:759–69.
pubmed: 32303557
Hoover CM, Kondo Y, Shao B, McDaniel M, Lee R, McGee S, et al. Heightened activation of embryonic megakaryocytes causes aneurysms in the developing brain of mice lacking podoplanin. 2021;blood.2020010310. https://doi.org/10.1182/blood.2020010310 . Online ahead of print.

Auteurs

Yizhi Jiang (Y)

Jiangsu Institute of Hematology, National Clinical Research Center for Hematologic Diseases, NHC Key Laboratory of Thrombosis and Hemostasis, The First Affiliated Hospital of Soochow University, Suzhou, 215006, China.
Department of Hematology, The First Affiliated Hospital of Wannan Medical College, Wuhu, 241001, China.
Cardiovascular Biology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK, 73104, USA.
Collaborative Innovation Center of Hematology, Soochow University, Suzhou, 215006, China.

Yaqiong Tang (Y)

Jiangsu Institute of Hematology, National Clinical Research Center for Hematologic Diseases, NHC Key Laboratory of Thrombosis and Hemostasis, The First Affiliated Hospital of Soochow University, Suzhou, 215006, China.
Cardiovascular Biology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK, 73104, USA.
Collaborative Innovation Center of Hematology, Soochow University, Suzhou, 215006, China.

Christopher Hoover (C)

Cardiovascular Biology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK, 73104, USA.
ORCID: 0000-0002-7846-2438

Yuji Kondo (Y)

Cardiovascular Biology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK, 73104, USA.

Dongping Huang (D)

Department of Hematology, The First Affiliated Hospital of Wannan Medical College, Wuhu, 241001, China.

Damien Restagno (D)

State Key Laboratory of Radiation Medicine and Protection, Soochow University, Suzhou, 215123, China.
ORCID: 0000-0002-5120-7787

Bojing Shao (B)

Cardiovascular Biology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK, 73104, USA.

Liang Gao (L)

Cardiovascular Biology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK, 73104, USA.

J Michael McDaniel (J)

Cardiovascular Biology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK, 73104, USA.

Meixiang Zhou (M)

Cardiovascular Biology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK, 73104, USA.

Robert Silasi-Mansat (R)

Cardiovascular Biology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK, 73104, USA.
ORCID: 0000-0001-9590-6160

Samuel McGee (S)

Cardiovascular Biology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK, 73104, USA.

Miao Jiang (M)

Jiangsu Institute of Hematology, National Clinical Research Center for Hematologic Diseases, NHC Key Laboratory of Thrombosis and Hemostasis, The First Affiliated Hospital of Soochow University, Suzhou, 215006, China.
Collaborative Innovation Center of Hematology, Soochow University, Suzhou, 215006, China.

Xia Bai (X)

Jiangsu Institute of Hematology, National Clinical Research Center for Hematologic Diseases, NHC Key Laboratory of Thrombosis and Hemostasis, The First Affiliated Hospital of Soochow University, Suzhou, 215006, China.
Collaborative Innovation Center of Hematology, Soochow University, Suzhou, 215006, China.
State Key Laboratory of Radiation Medicine and Protection, Soochow University, Suzhou, 215123, China.

Florea Lupu (F)

Cardiovascular Biology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK, 73104, USA.

Changgeng Ruan (C)

Jiangsu Institute of Hematology, National Clinical Research Center for Hematologic Diseases, NHC Key Laboratory of Thrombosis and Hemostasis, The First Affiliated Hospital of Soochow University, Suzhou, 215006, China.
Collaborative Innovation Center of Hematology, Soochow University, Suzhou, 215006, China.
State Key Laboratory of Radiation Medicine and Protection, Soochow University, Suzhou, 215123, China.

Jamey D Marth (JD)

Center for Nanomedicine, SBP Medical Discovery Institute, and Department of Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, CA, 93106, USA.

Depei Wu (D)

Jiangsu Institute of Hematology, National Clinical Research Center for Hematologic Diseases, NHC Key Laboratory of Thrombosis and Hemostasis, The First Affiliated Hospital of Soochow University, Suzhou, 215006, China. wudepei@suda.edu.cn.
Collaborative Innovation Center of Hematology, Soochow University, Suzhou, 215006, China. wudepei@suda.edu.cn.

Yue Han (Y)

Jiangsu Institute of Hematology, National Clinical Research Center for Hematologic Diseases, NHC Key Laboratory of Thrombosis and Hemostasis, The First Affiliated Hospital of Soochow University, Suzhou, 215006, China. hanyue@suda.edu.cn.
Collaborative Innovation Center of Hematology, Soochow University, Suzhou, 215006, China. hanyue@suda.edu.cn.

Lijun Xia (L)

Jiangsu Institute of Hematology, National Clinical Research Center for Hematologic Diseases, NHC Key Laboratory of Thrombosis and Hemostasis, The First Affiliated Hospital of Soochow University, Suzhou, 215006, China. Lijun-Xia@omrf.org.
Cardiovascular Biology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK, 73104, USA. Lijun-Xia@omrf.org.
Collaborative Innovation Center of Hematology, Soochow University, Suzhou, 215006, China. Lijun-Xia@omrf.org.
ORCID: 0000-0002-9586-7971

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Kupffer cell receptor CLEC4F is important for...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Récepteurs de surface cellulaire › Récepteurs des asialoglycoprotéines › Kupffer cell receptor CLEC4F is important for...
questionsmedicales.fr › Systèmes sanguin et immunitaire › Sang › Cellules sanguines › Plaquettes › Kupffer cell receptor CLEC4F is important for...
questionsmedicales.fr › Techniques d'investigation › Modèles théoriques › Modèles biologiques › Modèles animaux de maladie humaine › Kupffer cell receptor CLEC4F is important for...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Lectines › Lectines de type C › Kupffer cell receptor CLEC4F is important for...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Kupffer cell receptor CLEC4F is important for...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Récepteurs de surface cellulaire › Récepteurs immunologiques › Kupffer cell receptor CLEC4F is important for...